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. 2024 Sep 11;35(4):497–523. doi: 10.1007/s00335-024-10063-2

Mammalian genome research resources available from the National BioResource Project in Japan

Saori Mizuno-Iijima 1,✉, Shoko Kawamoto 2, Masahide Asano 3, Tomoji Mashimo 4, Shigeharu Wakana 5, Katsuki Nakamura 6, Ken-ichi Nishijima 7, Hitoshi Okamoto 8, Kuniaki Saito 9, Sawako Yoshina 10, Yoshihiro Miwa 11, Yukio Nakamura 12, Moriya Ohkuma 13, Atsushi Yoshiki 1,✉
PMCID: PMC11522087  PMID: 39261329

Abstract

Mammalian genome research has conventionally involved mice and rats as model organisms for humans. Given the recent advances in life science research, to understand complex and higher-order biological phenomena and to elucidate pathologies and develop therapies to promote human health and overcome diseases, it is necessary to utilize not only mice and rats but also other bioresources such as standardized genetic materials and appropriate cell lines in order to gain deeper molecular and cellular insights. The Japanese bioresource infrastructure program called the National BioResource Project (NBRP) systematically collects, preserves, controls the quality, and provides bioresources for use in life science research worldwide. In this review, based on information from a database of papers related to NBRP bioresources, we present the bioresources that have proved useful for mammalian genome research, including mice, rats, other animal resources; DNA-related materials; and human/animal cells and microbes.

Introduction

Bioresources represent a fundamental component of the research infrastructure that supports the life sciences. The development of bioresources is a lengthy and meticulous process, and they serve as the foundation for discoveries and future research endeavors. The sharing of these resources among researchers is crucial for the advancement of research and development. In response to this need, the Ministry of Education, Culture, Sports, Science and Technology (MEXT) established the National BioResource Project (NBRP) in FY2002. This initiative aims to create a systematic framework for the collection, preservation, and distribution of bioresources, with a particular emphasis on those requiring strategic development at the national level. This review synthesizes information on bioresources that have proven valuable for mammalian genome research. These resources include mice, rats, other animal resources, DNA-related materials, and human/animal cells and microbes. This review draws upon data extracted from a comprehensive database of publications related to NBRP bioresources, offering insights into the current landscape and potential future directions of bioresource utilization in genomic research.

Mice

The Core Center of NBRP-Mice is the Experimental Animal Division of the RIKEN BioResource Research Center (RIKEN BRC) (Mizuno-Iijima et al. 2022), which has collected mouse strains developed mainly in Japan that have been reported in academic publications (Fig. 1) in order to preserve unique and cutting-edge mouse models (Table 1). NBRP-Mice performs rigorous quality control, including microbial and genetic testing to ensure the reproducibility of animal experiments. As one of the international hubs for mouse resources, we continuously participate in global mouse resource networks such as International Mouse Strain Resource (IMSR), International Mouse Phenotyping Consortium (IMPC), Asian Mouse Mutagenesis & Resource Association (AMMRA) and Asian Network of Research Resource Centers (ANRRC). NBRP-Mice has archived approximately 10,000 mouse strains, most of which are genetically modified mice, as tools for gene functional analysis tools, including Cre/Flp drivers, fluorescent and luminescent reporters, and human disease models such as the third-generation Alzheimer’s disease model with genetic mutations of Alzheimer’s disease patients (Sasaguri et al. 2018; Sato et al. 2021) as well as a novel Down syndrome mouse model using a mouse artificial chromosome-based chromosome engineering technique (Kazuki et al. 2020). Information on the available mouse strains is disseminated through the NBRP-Mice website (https://mus.brc.riken.jp/) and the IMSR (https://www.findmice.org/), an all-encompassing database of the major international mouse repositories. NBRP-Mice receives requests from research communities worldwide (Fig. 2) and distributes live mice, frozen embryos/sperm, recovered litters from frozen embryos/sperm, and organ/tissue/genomic DNA. To date, NBRP-Mice has distributed mouse resources to researchers at 712 domestic and 1003 overseas academic and industry organizations in 44 countries. Outstanding research results from studies using NBRP-Mice have been published in 1300 papers so far (Fig. 3) and registered in our database.

Fig. 1.

Fig. 1

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Breakdown of collected mouse strains in NBRP-Mice (FY2017-FY2023)

Table 1.

Representative mouse resources for mammalian genomic research

Research application Strain name RBRC# Publications by developer scientists Latest publications by user scientists
Journal Journal Title
Gene function analysis tools Cre driver Tg B6.Cg-Tg(CAG-Cre)CZ-MO2Osb RBRC01828 Biochem Biophys Res Commun. 2004 Aug 20;321(2):275–9 Hum Mol Genet. 2024 May 13:ddae080 Lymphatic endothelial cell-specific NRAS p.Q61R mutant embryos show abnormal lymphatic vessel morphogenesis
Nat Commun. 2023 Dec 13;14(1):8095 Niacin restriction with NAMPT-inhibition is synthetic lethal to neuroendocrine carcinoma
Sci Signal. 2022 Nov;15(758):eabl5304 Semaphorin 4D induces articular cartilage destruction and inflammation in joints by transcriptionally reprogramming chondrocytes
Cre driver KI ICR.Cg-Mesp1 < tm2(cre)Ysa > /YsaRbrc RBRC01145 Development. 1999 Aug;126(15):3437–47 Am J Hum Genet. 2024 May 2;111(5):939–953 A regulatory variant impacting TBX1 expression contributes to basicranial morphology in Homo sapiens
J Dent Res. 2020 Sep;99(10):1182–1191 TBX1 Regulates chondrocyte maturation in the Spheno-occipital synchondrosis
Cre driver Tg B6;FVB-Tg(ACTA1-cre)AMcle/Rbrc RBRC01386 Int J Biol Sci. 2010 Sep 20;6(6):546–55 Biochem Biophys Res Commun. 2024 Jun 30:715:150001 Prolyl isomerase Pin1 in skeletal muscles contributes to systemic energy metabolism and exercise capacity through regulating SERCA activity
J Vet Med Sci. 2022 Apr 13;84(4):507–510 Application of the colorimetric loop-mediated isothermal amplification (LAMP) technique for genotyping Cre-driver mice
Cre driver Tg C57BL/6Cr-Tg(Pcdh21-cre)BYoko RBRC02189 Genesis. 2005 Sep;43(1):12–6 Dev Cell. 2023 Jul 24;58(14):1221–1236.e7 Activity-dependent local protection and lateral inhibition control synaptic competition in developing mitral cells in mice
Front Neurosci. 2023 Aug 23:17:1247375 Learning-dependent structural plasticity of intracortical and sensory connections to functional domains of the olfactory tubercle
Cre driver KI B6.129P2-Lyzs < tm1(cre)Ifo >  RBRC02302 Transgenic Res. 1999 Aug;8(4):265–77 J Neuroinflammation. 2023 May 2;20(1):102 Role of macrophage autophagy in postoperative pain and inflammation in mice
Cell Rep. 2020 May 5;31(5):107579 Secreted phospholipase PLA2G2D contributes to metabolic health by mobilizing ω3 polyunsaturated fatty acids in WAT
FLPe driver Tg C57BL/6-Tg(CAG-flpe)36Ito/ItoRbrc RBRC01834 Exp Anim. 2006 Apr;55(2):137–41 Proc Natl Acad Sci U S A. 2023 Aug 8;120(32):e2206860120 MBTD1 preserves adult hematopoietic stem cell pool size and function
Cell Rep. 2023 May 30;42(5):112530 FOXK1 promotes nonalcoholic fatty liver disease by mediating mTORC1-dependent inhibition of hepatic fatty acid oxidation
Blood. 2021 Feb 18;137(7):908–922 UTX maintains the functional integrity of the murine hematopoietic system by globally regulating aging-associated genes
EGFP reporter Tg C57BL/6-Tg(CAG-EGFP)C14-Y01-FM131Osb RBRC00267 FEBS Lett. 1997 May 5;407(3):313–9 Cell Rep Methods. 2023 Jul 5;3(7):100519 Stimulated Raman scattering microscopy reveals a unique and steady nature of brain water dynamics
EMBO Mol Med. 2018 Jul;10(7):e8643 Hepato-entrained B220+CD11c+NK1.1+ cells regulate pre-metastatic niche formation in the lung
EGFP reporter Tg B6;B6C3-Tg(Acro3-EGFP)01Osb RBRC00886 FEBS Lett. 1999 Apr 23;449(2–3):277–83 Sci Rep. 2023 Jul 31;13(1):12354 Culture-space control is effective in promoting haploid cell formation and spermiogenesis in vitro in neonatal mice
Commun Biol. 2022 May 26;5(1):504 Temperature sensitivity of DNA double-strand break repair underpins heat-induced meiotic failure in mouse spermatogenesis
Nrf2 KO B6.129P2-Nfe2l2 < tm1Mym > /MymRbrc RBRC01390 Biochem Biophys Res Commun. 1997 Jul 18;236(2):313–22 Int J Biol Sci. 2024 Apr 22;20(7):2592–2606 TAZ deficiency impairs the autophagy-lysosomal pathway through NRF2 dysregulation and lysosomal dysfunction
Theranostics. 2024 Feb 24;14(5):1841–1859 Dual regulation of NEMO by Nrf2 and miR-125a inhibits ferroptosis and protects liver from endoplasmic reticulum stress-induced injury
Trp53 KO B6.Cg-Trp53 < tm1Sia > /Rbrc RBRC01361 Oncogene. 1993 Dec;8(12):3313–22 Sci Rep. 2024 Jan 11;14(1):1069 Transcription factor FoxO1 regulates myoepithelial cell diversity and growth
EMBO Mol Med. 2023 Jan 11;15(1):e15631 IMPDH inhibition activates TLR-VCAM1 pathway and suppresses the development of MLL-fusion leukemia
Atg5 flox B6.129S-Atg5 < tm1Myok >  RBRC02975 Nature. 2006 Jun 15;441(7095):885–9 mBio. 2023 Nov 1;14(6):e0148023 The nonstructural protein 1 of respiratory syncytial virus hijacks host mitophagy as a novel mitophagy receptor to evade the type I IFN response in HEp-2 cells
Nat Commun. 2023 Jul 13;14(1):4084 Liver lipophagy ameliorates nonalcoholic steatohepatitis through extracellular lipid secretion
J Neuroinflammation. 2023 May 2;20(1):102 Role of macrophage autophagy in postoperative pain and inflammation in mice
Atg7 flox B6.Cg-Atg7 < tm1Tchi >  RBRC02759 J Cell Biol. 2005 May 9;169(3):425–34 Nat Commun. 2024 May 14;15(1):4052 Dysfunctional adipocytes promote tumor progression through YAP/TAZ-dependent cancer-associated adipocyte transformation
Cell Mol Gastroenterol Hepatol. 2024 Mar 5;18(1):15–40 Autophagy contributes to homeostasis in esophageal epithelium where high autophagic vesicle level marks basal cells with limited proliferation and enhanced self-renewal potential
Cell Death Discov. 2023 Dec 15;9(1):456 Pharmacological inhibition of MALT1 (mucosa-associated lymphoid tissue lymphoma translocation protein 1) induces ferroptosis in vascular smooth muscle cells
Human disease models Alzheimer’s disease C57BL/6-App < tm3(NL-G-F)Tcs >  RBRC06344 Nat Neurosci. 2014 May;17(5):661–3 Nutrients. 2024 Feb 15;16(4):538 Potential therapeutic effects of Bifidobacterium breve MCC1274 on Alzheimer’s disease pathologies in AppNL-G-F Mice
Sci Rep. 2024 Jan 2;14(1):227 The long-term effects of heated tobacco product exposure on the central nervous system in a mouse model of prodromal Alzheimer’s disease
PLoS One. 2024 May 10;19(5):e0303375 Disturbance in the protein landscape of cochlear perilymph in an Alzheimer’s disease mouse model
PLoS One. 2024 Feb 5;19(2):e0297289 Perinatal choline supplementation prevents learning and memory deficits and reduces brain amyloid Aβ42 deposition in AppNL-G-F Alzheimer’s disease model mice
Biochem Biophys Res Commun. 2023 Nov 26:683:149106 Apolipoprotein E genotype-dependent accumulation of amyloid β in APP-knock-in mouse model of Alzheimer’s disease
Wild derived-inbred strains Mus musculus molossium MSM/Ms RBRC00209 Exp Anim. 2009 Apr;58(2):123–34 Exp Anim. 2024 Mar 6. 2024 Mar 6 Inter-subspecies mouse F1 hybrid embryonic stem cell lines newly established for studies of allelic imbalance in gene expression
Biol Reprod. 2021 Jan 4;104(1):234–243 Development of assisted reproductive technologies for Mus spretus
Nat Commun. 2020 Jun 24;11(1):3199 Identification of distinct loci for de novo DNA methylation by DNMT3A and DNMT3B during mammalian development
Stem Cell Reports. 2019 May 14;12(5):1113–1128 De Novo DNA Methylation at Imprinted Loci during reprogramming into naive and primed pluripotency
Nature. 2017 Aug 10;548(7666):224–227 Derivation of ground-state female ES cells maintaining gamete-derived DNA methylation
Mus musculus molossium JF1/Ms RBRC00639 Genome Res. 2013 Aug;23(8):1329–38 Epigenetics Chromatin. 2024 Jun 5;17(1):20 Imprinted DNA methylation of the H19 ICR is established and maintained in vivo in the absence of Kaiso
Genes Dev. 2022 Jan 1;36(1–2):84–102 Highly rigid H3.1/H3.2-H3K9me3 domains set a barrier for cell fate reprogramming in trophoblast stem cells
Commun Biol. 2021 Dec 17;4(1):1410 Orientation of mouse H19 ICR affects imprinted H19 gene expression through promoter methylation-dependent and -independent mechanisms
Sci Rep. 2020 Feb 5;10(1):1884 Role of the imprinted allele of the Cdkn1c gene in mouse neocortical development
Epigenetics chromatin. 2020 Jan 14;13(1):2 Recapitulation of gametic DNA methylation and its post-fertilization maintenance with reassembled DNA elements at the mouse Igf2/H19 locus
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Fig. 2.

Fig. 2

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Breakdown of distributed mouse strains from NBRP-Mice (FY2017-FY2023)

Fig. 3.

Fig. 3

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Number of publications using NBRP-Mice mouse resources

In addition to genetically modified strains, NBRP-Mice also preserves wild-derived inbred strains such as the Japanese subspecies MSM/MsRbrc (MSM, RBRC00209) and JF1/MsRbrc (JF1, RBRC00639). The enormous number of genomic polymorphisms present between these subspecies and classical inbred strains is useful for understanding the genomic function and diverse biological phenotypes in mice and other mammals including humans as well. MoG+ (https://molossinus.brc.riken.jp/mogplus/) (Takada et al. 2022) is a mouse genome database designed to support research using Mus musculus subspecies, with a focus on comparisons between mouse subspecies and classical inbred strains. MoG+ provides access to more than 40 million polymorphisms found by comparative genomic analysis of 10 Asian wild-derived strains, including Mus musculus molossinus-derived MSM and JF1; Mus musculus musculus-derived KJR/Ms (RBRC00655), SWN/Ms (RBRC00654), CHD/Ms (RBRC00738), NJL/Ms (RBRC00207), and BLG2/Ms (RBRC00653); Mus musculus domesticus-derived BFM/2Ms (RBRC00659) and PGN2/Ms (RBRC00667); and Mus musculus castaneus-derived HMI/Ms (RBRC00657), all of which are available from NBRP-Mice, while linking to mouse resource catalog information, human genome variations, and so on. In addition, public genome polymorphism information on 36 classical inbred strains is stored. MoG+ has been utilized for disease and phenotypic analysis (Takeishi et al. 2022; Yasuda et al. 2020). Reproductive engineering techniques are being developed to support research involving subspecies mouse strains (Hasegawa et al. 2021; Hirose et al. 2017; Mochida et al. 2014). An example of the use of subspecies strains is gene expression analysis based on single nucleotide polymorphisms (SNPs) in F1 hybrid mice (Saito et al. 2024; Yagi et al. 2017, 2020). Genomic DNA derived from these multiple subspecies strains has also been used (Bamunusinghe et al. 2013, 2016, 2018).

Rats

The Core Center of NBRP-Rats is the Institute of Laboratory Animals, Graduate School of Medicine, Kyoto University. Scientists conducting research involving rats have conventionally accumulated physiological and pharmacological data. Compared with mice, rats have typically been used for experiments involving drug administration and surgery because of their larger body size and for behavioral studies because of their higher intelligence. NBRP-Rats collects rat strains that have been maintained by individual scientists or laboratories in Japan and overseas, making over 800 strains available, including inbred and genetically modified strains, and has provided about 1500 strains so far (Table 2). NBRP-Rats has common inbred strains, spontaneous mutants, congenic strains, recombinant inbred strains, transgenic and newly genetically modified strains, and so on. Recently, genome-edited rats have also been collected. Available strains can be accessed via the NBRP-Rats website (https://www.anim.med.kyoto-u.ac.jp/nbr/Default.aspx). NBRP-Rats provides reference information for strain selection, including the results of approximately 200 strains on 109 phenotypic measurements for physiological and behavioral parameters such as body weight at various ages, blood pressure, spontaneous locomotor activity, and the passive avoidance test (https://www.anim.med.kyoto-u.ac.jp/nbr/phenome.aspx); the phylogenetic tree of 132 rat strains based on genomic profile data (https://www.anim.med.kyoto-u.ac.jp/nbr/phylo.aspx); and a pedigree-like charting tool showing 357 simple sequence length polymorphism (SSLP) marker differences for 179 genotyped rat strains (https://www.anim.med.kyoto-u.ac.jp/nbr/pedigree/sb.aspx). NBRP-Rats has also worked to develop reproductive technology and has established optimal freezing and thawing methods for sperm, stable in vitro fertilization (IVF) technology (Honda et al. 2019; Mochida et al. 2024; Morita et al. 2023) and is making progress in the cryopreservation of rat strains.

Table 2.

Representative rat resources for mammalian genomic research

Research application Strain name NBRP Rat No Publications by developer scientists Latest publications by user scientists
Journal Journal Title
Gene function analysis tools GFP reporter Tg W-Tg(CAG-GFP)184Ys 0273 Biochem Biophys Res Commun. 2001 Aug 31;286(4):779–85 Pediatr Res. 2023 Dec;94(6):1921–1928 Therapeutic efficacy of intravenous infusion of mesenchymal stem cells in rat perinatal brain injury
Sci Rep. 2022 Oct 10;12(1):16986 Intravenous infusion of bone marrow-derived mesenchymal stem cells improves tissue perfusion in a rat hindlimb ischemia model
BMC Urol. 2021 Nov 13;21(1):156 Possible role of intravenous administration of mesenchymal stem cells to alleviate interstitial cystitis/bladder pain syndrome in a Toll-like receptor-7 agonist-induced experimental animal model in rat
EGFP reporter Tg LEW-Tg(CAG-EGFP)1Ys 0297 Biochem Biophys Res Commun. 2005 Apr 1;329(1):288–95 Life Sci. 2022 Jul 15:301:120604 Early effects of adipose-derived stem cell sheets against detrusor underactivity in a rat cryo-injury model
Cell Mol Life Sci. 2022 May 10;79(6):289 IL4 stimulated macrophages promote axon regeneration after peripheral nerve injury by secreting uPA to stimulate uPAR upregulated in injured axons
Radiat Environ Biophys. 2020 Nov;59(4):711–721 The effect of radiation on the ability of rat mammary cells to form mammospheres
Optogenetic reporetr Tg W-Tg(Thy1-COP4/YFP*)4Jfhy 0685 PLoS One. 2009 Nov 5;4(11):e7679 J Pharmacol Sci. 2024 Apr;154(4):312–315 Laminar-selective spinal astrocyte population capable of converting tactile information into nociceptive in rats
Front Mol Neurosci. 2022 Jun 23:15:911122 Selective involvement of a subset of spinal dorsal horn neurons operated by a prodynorphin promoter in Aβ fiber-mediated neuropathic allodynia-like behavioral responses in rats
Proc Natl Acad Sci USA. 2021 Jan 19;118(3):e2021220118 A subset of spinal dorsal horn interneurons crucial for gating touch-evoked pain-like behavior
Cre fluorescent reporter Tg LE-Tg(Gt(ROSA)26Sor-CAG-tdTomato)24Jfhy 0734 PLoS One. 2016 May 19;11(5):e0155687 Endocrinology. 2024 Feb 20;165(4):bqae028 neonatal aromatase inhibition blocked defeminization of avpv kiss1 neurons and lh surge-generating system in male rats
Sci Rep. 2023 Nov 22;13(1):20495 Conditional Oprk1-dependent Kiss1 deletion in kisspeptin neurons caused estrogen-dependent LH pulse disruption and LH surge attenuation in female rats
J Reprod Dev. 2023 Oct 20;69(5):227–238 Sex difference in developmental changes in visualized Kiss1 neurons in newly generated Kiss1-Cre rats
Luciferase reporter Tg LEW-Tg(Gt(ROSA)26Sor-luc)11Jmsk 0299 Transplantation. 2006 Apr 27;81(8):1179–84 Mol Imaging Biol. 2021 Oct;23(5):639–649 Bioluminescence imaging in vivo confirms the viability of pancreatic islets transplanted into the greater omentum
Mol Imaging Biol. 2019 Jun;21(3):454–464 A trimodal imaging platform for tracking viable transplanted pancreatic islets in vivo: F-19 MR, fluorescence, and bioluminescence imaging
ChemistryOpen. 2019 Jan 23;8(2):155–165 Manganese-zinc ferrites: safe and efficient nanolabels for cell imaging and tracking in vivo
Human disease models SCID (CRISPR) F344-Il2rgem1Iexas 0883 PLoS One. 2010 Jan 25;5(1):e8870 Regen Ther. 2024 Jan 6:25:229–237 Host-to-graft propagation of inoculated α-synuclein into transplanted human induced pluripotent stem cell-derived midbrain dopaminergic neurons
Tissue Eng Part A. 2024 Feb;30(3–4):144–153 Comparative study of immunodeficient rat strains in engraftment of human-induced pluripotent stem cell-derived airway epithelia
Regen Ther. 2022 Jan 14:19:77–87 Transplantation of a human induced pluripotent stem cell-derived airway epithelial cell sheet into the middle ear of rats
SCID (TALEN) F344-Il2rgem7Kyo 0694 Sci Rep. 2013 Nov 29:3:3379 JACC Basic Transl Sci. 2021 Feb 19;6(3):239–254 Intramyocardial transplantation of human iPS cell-derived cardiac spheroids improves cardiac function in heart failure animals
mSphere. 2016 Dec 21;1(6):e00334-16 J Vet Med Sci. 2018 Sep 13;80(9):1400–1406 Rat polyomavirus 2 infection in a colony of X-linked severe combined immunodeficiency rats in Japan
PLoS One. 2017 Dec 28;12(12):e0190150 Creating a stem cell niche in the inner ear using self-assembling peptide amphiphiles
SCID (ZFN) F344-Il2rgem2Kyo 0586 PLoS One. 2010 Jan 25;5(1):e8870 J Neurosci Res. 2020 Aug;98(8):1575–1587 Zonisamide promotes survival of human-induced pluripotent stem cell-derived dopaminergic neurons in the striatum of female rats
Parasitol Int. 2018 Aug;67(4):357–361 Intestinal immunity suppresses carrying capacity of rats for the model tapeworm, Hymenolepis diminuta
Stem Cells Dev. 2016 Jun 1;25(11):815–25 Fail-safe therapy by gamma-ray irradiation against tumor formation by human-induced pluripotent stem cell-derived neural progenitors
Epilepsy (Inbred) NER/Kyo 0010 Epilepsia. 1998 Jan;39(1):99–107 Exp Anim. 2021 Feb 6;70(1):137–143 PHF24 is expressed in the inhibitory interneurons in rats
Mamm Genome. 2020 Apr;31(3–4):86–94 Comparative genomic analysis of inbred rat strains reveals the existence of ancestral polymorphisms
Epilepsy Res. 2019 Sep:155:106159 Anti-seizure effect and neuronal activity change in the genetic-epileptic model rat with acute and chronic vagus nerve stimulation
Neuronal degeneration (Inbred) GRY/Idr 0368 Experientia. 1991 Dec 1;47(11–12):1215–8 Neurochem Int. 2020 Dec:141:104859 Scn1a and Cacna1a mutations mutually alter their original phenotypes in rats
Exp Anim. 2020 Apr 24;69(2):153–160 Poor mother–offspring relationships in rats with Cacna1a mutation
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At the Institute of Medical Science, The University of Tokyo, which is an NBRP-Rats Sub-Core Center, the development of novel genome-edited rat models is underway. Three severely immunodeficient (SCID) rat strains generated using the CRISPR/Cas9 system [F344-Il2rgem1Iexas (NBRP Rat No: 0883), F344-Rag2em1Iexas (NBRP Rat No: 0894), and F344-Il2rg/Rag2em1Iexas (NBRP Rat No: 0895)] (Mashimo et al. 2010) have already been made available to researchers (https://www.ims.u-tokyo.ac.jp/animal-genetics/scid/index_en.html). SCID rats can be transplanted with human induced pluripotent stem cells (iPS cells), cancer cells, liver cells, and so on. Therefore, SCID rats are useful for analyzing human physiological functions in vivo (Eguchi et al. 2022; Lahr et al. 2021; Miyasaka et al. 2022). In fact, the demand from translational research and regenerative medicine is increasing every year. In addition, NBRP-Rats has been collecting and developing new Cre driver rats, and 22 Cre driver strains are available for conditional studies. In the near future, a database of Cre driver rats will be made available on the website, and the results of comprehensive expression analysis, local expression analysis using adeno-associated virus (AAV), behavioral analysis, and magnetic resonance imaging (MRI) analysis will be published as phenotype information.

The other animal resources

In addition to laboratory mice and rats, the NBRP provides Aged mice and Japanese macaques as mammalian resources for researchers in Japan. NBRP-Aged mice provides three standard mouse strains [C57BL/6J, C57BL/6N (B6N), BALB/cA] that are bred for about 2 years in a uniform environment under strict microbiological control. Aged mice are expected to be used for various aging research, such as elucidating the mechanisms of the aging process, aging control, and aging-related diseases. The Japanese macaque is a species of macaque monkey. Due to their close relationship with humans, Japanese macaques are used mainly in the field of neuroscience but also in the fields of infectious diseases, immunology, and regenerative medicine. Compared with other Southeast Asian macaque species such as rhesus and cynomolgus macaques, Japanese macaques have a curious and calm temperament as well as highly developed cognitive and learning abilities, making them suitable for research on higher brain functions and fine motor functions that require complex task acquisition (Kubota et al. 2024; Kumano and Uka 2024; Sasaki et al. 2024). In fact, Japanese macaques have contributed to the elucidation of the pathogenesis and pathology of neurological disorders such as dementia and Parkinson's disease as well as to the development of treatments to restore neurological functions (Chiken et al. 2021; Darbin et al. 2022; Oyama et al. 2023).

The NBRP supports life science research by providing a total of 12 animal bioresources for which whole-genome sequencing has been performed, which is necessary for analyzing orthologs of human genes (Table 3). For example, chickens and quails have been used in a variety of fields, particularly in embryology. In vitro culture of primordial germ cells (PGCs) is now possible in 20 chicken strains, and gene transfer and genome editing of chickens using such cells are under development. To meet the demand for fluorescent live imaging of developmental processes, NBRP-Chickens & Quails provides a transgenic chicken strain (pLSi/ΔAeGFP-TG) that expresses enhanced green fluorescent protein (eGFP) almost systemically under the control of the chicken β-actin promoter (Motono et al. 2010; Tsujino et al. 2019) and a PRDM14-eGFP knock-in chicken strain that express eGFP under the control of the chicken endogenous PRDM14 promoter (Hagihara et al. 2020). As a tool for generating new models, Cas9-T2A-mCherry transgenic chickens that expresses Cas9 under the control of the homeostatic human EF1α promoter are also available. NBRP-Chickens & Quails releases the results of quail genome analysis as the Quail Genome Browser (http://viewer.shigen.info/uzura/index.php). A PGK:H2B-chFP-TG quail strain that expresses mCherry throughout the body (Huss et al. 2015) is used for live imaging of developmental processes, with the advantage of easy microsurgery in embryos (Haneda et al. 2024; Yoshihi et al. 2020).

Table 3.

Animal resources available from the NBRP

Bioresource category Core center Resource website
Mice Experimental Animal Division, RIKEN BioResource Research Center https://mus.brc.riken.jp/
Aged mice Department of Animal Experimentation, Foundation for Biomedical Research and Innovation at Kobe https://www.fbri-kobe.org/laboratory/animal_experimentation/nbrp/
Rats Institute of Laboratory Animals, Graduate School of Medicine, Kyoto University http://www.anim.med.kyoto-u.ac.jp/NBR/default.aspx
Japanese macaques Center for the Evolutionary Origins of Human Behavior, Kyoto University https://nihonzaru.jp/aboutus_2_e.html
Chicken/Quail Avian Bioscience Research Center, Graduate School of Bioagricultural Sciences, Nagoya University, Tokai National Higher Education and Research System https://www.agr.nagoya-u.ac.jp/~nbrp/en/index.html
Clawed frogs/Newts Amphibian Research Center, Hiroshima University https://xenopus.nbrp.jp/NBRP_Xenopus/NBRP_Clawed_frogs_Newts_Top_EN.html
Zebrafish RIKEN Center for Brain Science https://shigen.nig.ac.jp/zebra/index_en.html
Medaka Lab of Bioresources, National Institute for Basic Biology, National Institutes of Natural Sciences https://shigen.nig.ac.jp/medaka/
Ciona intestinalis Shimoda Marine Research Center, University of Tsukuba https://marinebio.nbrp.jp/ciona/
Drosophila Department of Chromosome Science, National Institute of Genetics, Research Organization of Information and Systems https://fruitfly.jp/flystock/index_e.html
Silkworms Institute of Genetic Resources, Graduate School of Bioresources and Bioenvironmental Science, Kyushu University https://silkworm.nbrp.jp/index_en.html
C.elegans Tokyo Women’ s Medical University School of Medicine https://shigen.nig.ac.jp/c.elegans/
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Zebrafish are transparent throughout embryogenesis, are easy to breed, have a short life cycle, and are amenable to mutation and genetic modification. NBRP-Zebrafish has about 400 mutant lines and about 1800 transgenic lines. The neuronal composition and neural mechanisms of the zebrafish brain are highly conserved with those of humans, making zebrafish particularly useful in the field of neuroscience. Tg(CM-isl1:GFP), which expresses green fluorescent protein (GFP) in hindbrain motor neurons (Higashijima et al. 2020), is useful for imaging neural circuit networks (Derrick et al. 2024; Zhao et al. 2024). Tg(vglut2a:loxP-DsRed-loxP-GFP), which expresses DsRed in glutamatergic neurons prior to Cre recombinase exposure and GFP in the Cre-recombined cells (Satou et al. 2012), has been used to elucidate the mechanisms of neural circuit construction processes (Itoh et al. 2024; Schmidt et al. 2024) and the relationship between behavior/movement and neuronal activity (Berg et al. 2023; Carbo-Tano et al. 2023).

Drosophila is used to study life phenomena and in disease research because of its many similarities to humans, including gene homology and basic biological mechanisms. The NBRP-Drosophila conserves many useful mutants for life science research, including about 14,000 RNAi strains and about 30 FlyCas9 strains. CAS-001 (Kondo and Ueda 2013), a transgenic line expressing the Cas9 protein, can be crossed with various guide RNA strains to generate gene knock-out mutant flies with high efficiency. The generation of mutant strains with CAS-001 is versatile and has been reported in the development of novel models for metabolic disease research (Martelli et al. 2024) and biochemical research (Banreti et al. 2022). GAL4 enhancer trap insertion strains (Hayashi et al. 2002) are useful for tissue-specific expression and knock-down using the GAL4/UAS system, and approximately 4200 such lines have been conserved. A traffic jam-GAL4 driver strain (DGRC#104055), which is expressed in all stages of ovarian follicle cells at every developmental stage, has been used by many scientists in various fields as well as for the elucidation of reproductive mechanisms (Mallart et al. 2024; Taniguchi and Igaki 2023).

Caenorhabditis elegans is useful for understanding gene function because C.elegans has only about 1000 somatic cells, the cell lineage of which has been extensively described, and detailed descriptions of its morphology have been made through serial electron microscopy images. NBRP-C. elegans has about half the number of deletion mutants as there are genes in wild-type C. elegans. The drp-1 deletion mutant (tm1108), an ortholog of the human DMNL1 gene that functions in mitochondrial division, has been used to study mitochondria-related diseases (Chen et al. 2024) and aging (Sharifi et al. 2024). The brc-1 deletion mutant (tm1145), an ortholog of the human BRCA1 gene that is involved in DNA repair and has been reported to be associated with several diseases including cancer, is used to elucidate DNA repair mechanisms (Bujarrabal-Dueso et al. 2023; Wang et al. 2023).

DNA-related materials

The Gene Engineering Division, RIKEN BRC provides genetic materials such as plasmids, expression and reporter vectors, and comprehensive clone sets of cDNAs and genomic DNAs. To date, NBRP-DNA-related materials have conserved about 3.8 million resources including about 3400 research tools for imaging and genome editing, about 600,000 human cDNA/genomic DNA clones, about 350,000 mouse cDNA/genomic DNA clones, and 1.3 million animal cDNA/genomic DNA clones (Table 4). Mammalian expression vectors for protein production and gene expression, mouse and rat BAC clones, and fluorescent and luminescent protein expression vectors for imaging are used to generate genetically modified mice, rats, and mammalian cells. BAC clones can be searched with the BAC browser, using gene symbols as keywords, and the physical location of BAC clones on the genome can be confirmed. The BAC browsers for B6N and MSM mouse strains (http://analysis2.nig.ac.jp/mouseBrowser/cgi-bin/index.cgi?org=mm), for F344/Stm and LE/Stm rat strains (http://analysis2.nig.ac.jp/ratBrowser/cgi-bin/index.cgi?org=rn), and for Japanese macaque (http://analysis2.nig.ac.jp/jmonkeyBrowser/cgi-bin/index.cgi?org=jm) are published on the website. The B6N BAC library consists of 128,000 clones representing 90.2% of the actual coverage of the haploid genome. The MSM BAC library consists of 200,000 BAC clones.

Table 4.

Representative DNA materials for mammalian genomic research

Category Resource name RDB# Publications by developer or user scientists
Journal Title
Genomic clone C57BL/6N BAC B6N Mouse BAC clone RDB07573 Life Sci Alliance. 2023 May 16;6(8):e202301897 Identification of a novel enhancer essential for Satb1 expression in TH2 cells and activated ILC2s
Methods Mol Biol. 2023:2637:161–180 VCre/VloxP and SCre/SloxP as reliable site-specific recombination systems for genome engineering
BMC Biol. 2022 Mar 9;20(1):64 BET proteins are essential for the specification and maintenance of the epiblast lineage in mouse preimplantation embryos
PLoS One. 2022 Aug 25;17(8):e0273279 Evidence for a functional role of Start, a long noncoding RNA, in mouse spermatocytes
iScience. 2021 May 29;24(6):102660 Suv4-20h2 protects against influenza virus infection by suppression of chromatin loop formation
MSM/Ms BAC MSM Mouse BAC clone RDB04214 J Mol Biol. 2022 Apr 15;434(7):167509 Enhancer Dependent repositioning of TCRb locus with respect to the chromosome territory
Nat Commun. 2019 Feb 27;10(1):947 Hepatic Sdf2l1 controls feeding-induced ER stress and regulates metabolism
Sci Rep. 2018 Aug 14;8(1):12125 Tmc2 expression partially restores auditory function in a mouse model of DFNB7/B11 deafness caused by loss of Tmc1 function
Biochem Biophys Res Commun. 2018 Jan 29;496(1):231–237 Pde6brd1 mutation modifies cataractogenesis in Foxe3rct mice
Sci Rep. 2017 Sep 11;7(1):11208 The parathyroid hormone regulates skin tumour susceptibility in mice
F344/Stm BAC Rat BAC RNB1 RDB06273 Nat Commun. 2019 Feb 5;10(1):451 Generation of pluripotent stem cell-derived mouse kidneys in Sall1-targeted anephric rats
LE/Stm BAC Rat BAC RNB2 RDB06274 Nat Genet. 2013 Jul;45(7):767–75 Combined sequence-based and genetic mapping analysis of complex traits in outbred rats
cDNA clone NIA/NIH mouse cDNA Clone NIA 15K Mouse cDNA Clone RDB05723 Dev Cell. 2023 Aug 21;58(16):1447–1461.e6 Nodal flow transfers polycystin to determine mouse left–right asymmetry
J Virol. 2019 Jun 14;93(13):e00269-19 Reduced folate carrier: an entry receptor for a novel feline leukemia virus variant
Genome Network Project Human cDNA GNP Clone RDB07566 J Biol Chem. 2024 Mar;300(3):105679 Methyl vinyl ketone and its analogs covalently modify PI3K and alter physiological functions by inhibiting PI3K signaling
Sci Rep. 2023 Dec 27;13(1):22991 Protein N-myristoylation plays a critical role in the mitochondrial localization of human mitochondrial complex I accessory subunit NDUFB7
Sci Transl Med. 2023 Jun 14;15(700):eadd1531 Fusobacterium infection facilitates the development of endometriosis through the phenotypic transition of endometrial fibroblasts
Biochemistry. 2023 Jun 6;62(11):1679–1688 Identification of the most impactful asparagine residues for γS-crystallin aggregation by deamidation
BMC Cancer. 2023 May 10;23(1):424 MALAT1 functions as a transcriptional promoter of MALAT1::GLI1 fusion for truncated GLI1 protein expression in cancer
NRCD Human cDNA NRCD human cDNA clones RDB06607 Commun Biol. 2020 May 22;3(1):253 Phosphoproteomics identifies dual-site phosphorylation in an extended basophilic motif regulating FILIP1-mediated degradation of filamin-C
Br J Cancer. 2019 Apr;120(8):819–826 High filamin-C expression predicts enhanced invasiveness and poor outcome in glioblastoma multiforme
Mammalian expression vector Mammalian expression vector with CAG promoter pCAGGS RDB08938 Exp Anim. 2022 May 20;71(2):184–192 Tracing location by applying emerald luciferase in an early phase of murine endometriotic lesion formation
EMBO J. 2021 Feb 15;40(4):e105375 Thalidomide and its metabolite 5-hydroxythalidomide induce teratogenicity via the cereblon neosubstrate PLZF
Expressing FLAG-tagged fusion protein pCMV_S-FLAG RDB05956 Sci Rep. 2020 Mar 18;10(1):4933 Jdp2-deficient granule cell progenitors in the cerebellum are resistant to ROS-mediated apoptosis through xCT/Slc7a11 activation
Conditional gene expression A cassette to introduce cDNA into mammalian chromosome pCALNL5 RDB01862 Lab Anim (NY). 2023 Oct;52(10):247–257 Development of two mouse strains conditionally expressing bright luciferases with distinct emission spectra as new tools for in vivo imaging
J Biol Chem. 2023 Jul;299(7):104905 O-GalNAc glycosylation determines intracellular trafficking of APP and Aβ production
J Biol Chem. 2022 Jun;298(6):101880 Endothelial expression of human amyloid precursor protein leads to amyloid β in the blood and induces cerebral amyloid angiopathy in knock-in mice
Expression clone of Cre recombinase pCAGGS-Cre RDB08998 Development. 2019 Nov 4;146(21):dev174938 Developmental analyses of mouse embryos and adults using a non-overlapping tracing system for all three germ layers
Recombinant adenovirus expressing recombinase Cre AxCANCre RDB01748 Development. 2023 Oct 15;150(20):dev201157 Glutamine protects mouse spermatogonial stem cells against NOX1-derived ROS for sustaining self-renewal division in vitro
J Reprod Dev. 2022 Dec 19;68(6):369–376 Adenovirus-mediated gene delivery restores fertility in congenitally infertile female mice
Life Sci Alliance. 2019 Apr 2;2(2):e201900374 ROS amplification drives mouse spermatogonial stem cell self-renewal
Recombinant adenovirus expressing humanized FLPe AxEFhFLPe RDB08123 J Mol Biol. 2009 Jul 10;390(2):221–30 Activities of various FLP recombinases expressed by adenovirus vectors in mammalian cells
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NBRP-DNA-related materials collects useful tools that are expected to be requested by researchers in the future using artificial intelligence technology. Regarding genome-editing tools, Cas9-poly(A) expressing improved plasmid [T7-NLS hCas9-pA (RDB13130)] (Yoshimi et al. 2016) and the expression vector of sgRNA with hSpCas9-Cdt1(mouse) fusion protein [px330-mC (RDB14406)] (Mizuno-Iijima et al. 2021) are available. In addition to conventionally used fluorescent and luminescent proteins, NBRP-DNA-related materials also provides the highly photostable and bright GFP StayGold [e.g., (n1)StayGold/pRSET (RDB19605) (Hirano et al. 2022) and pRSETB/mStayGold (RDB20214) (Ando et al. 2023)], and the novel yellow fluorescent protein Achilles [Achilles/pRSETB (RDB15982)] (Yoshioka-Kobayashi et al. 2020) to meet the needs of researchers. The highly luminescent luciferases Akaluc [pcDNA3 Venus-Akaluc (RDB15781)] (Iwano et al. 2018) and oFluc [pPmat Luc1 (RDB14359)] (Ogoh et al. 2020) are also provided. Reporter mice expressing Akaluc or oFluc are available from NBRP-Mice [C57BL/6J-Gt(ROSA)26Sorem13(CAG-luc)Rbrc/#77 (RBRC10451), C57BL/6J-Gt(ROSA)26Sorem14(CAG-Venus/Akaluc)Rbrc/#87 (RBRC10858), C57BL/6J-Gt(ROSA)26Sorem13.1(CAG-luc)Rbrc/#77 (RBRC10919), and C57BL/6J-Gt(ROSA)26Sorem17.1(CAG-Venus/Akaluc)Rbrc/#11 (RBRC10921)] (Nakashiba et al. 2023).

Human and animal cells

The Cell Engineering Division, RIKEN BRC has collected many cultured cell lines, including about 4600 human cell lines and about 3800 animal cell lines. Mouse embryonic stem (ES) cell lines with germline-transmission [e.g., B6J-S1UTR (AES0140), B6NJ-22UTR (AES0141) (Tanimoto et al. 2008), and EGR-G101 (AES0182) (Fujihara et al. 2013)] are used to generate genetically engineered mice, using both conventional gene targeting and genome-editing technologies (Hasan et al. 2021; Noda et al. 2017, 2019; Serizawa et al. 2019). As mentioned above, because SCID rat strains are transplantable with human cells, human iPS cells and cancer cells have been transplanted and used for in vivo functional analysis. Some users have reported research results in combination with human iPS cells derived from healthy volunteers provided by NBRP-Human and animal cells (Gima et al. 2024; Hayashi et al. 2024; Tada et al. 2022). NBRP-Human and animal cells also provides human iPS cell lines derived from patients with various diseases (Table 5). These disease-specific iPS cell lines are expected to be further used for research with a view toward clinical application.

Table 5.

Disease-specific iPS cells available from the NBRP

Disease-specific iPS cells Publications by developer or user scientists
Disease group Diseases Patients Cell line Name of diseases Cell No Journal Title
Neuromuscular diseases 62 305 1201 Amyotrophic lateral sclerosis (ALS) HPS0292, HPS0293, HPS0290, HPS0291 Front Neurosci. 2023 Oct 2:17:1251228. 37849894 Loss of TDP-43 function contributes to genomic instability in amyotrophic lateral sclerosis
Spinal muscular atrophy type 1 HPS0158 Stem Cell Reports. 2015 Apr 14;4(4):561–8 Modeling the early phenotype at the neuromuscular junction of spinal muscular atrophy using patient-derived iPSCs
Muscular dystrophy, Duchenne type HPS0164 Mol Ther Nucleic Acids. 2023 Apr 19:32:522–535 Single-swap editing for the correction of common Duchenne muscular dystrophy mutations
Alexander disease HPS3529 J Cell Mol Med. 2024 Apr;28(7):e18214 Induced pluripotent stem cell-based assays recapture multiple properties of human astrocytes
Rett syndrome HPS3049 Cell Rep Methods. 2022 Nov 29;2(12):100352 De-erosion of X chromosome dosage compensation by the editing of XIST regulatory regions restores the differentiation potential in hPSCs
Metabolic diseases 9 40 168 Lysosomal storage disease (Mucopolysaccharidosis (MPS)) HPS0660 Stem Cell Res. 2019 Apr:36:101406 Generation of a human induced pluripotent stem cell line, BRCi001-A, derived from a patient with mucopolysaccharidosis type I
Adrenoleukodystrophy (ALD) HPS1090, HPS1096 Stem Cell Res. 2021 May:53:102337 Generation of two human induced pluripotent stem cell lines derived from two X-linked adrenoleukodystrophy patients with ABCD1 mutations
Mitochondrial diseases HPS0070, HPS0458, HPS0461, HPS2864 Int J Mol Sci. 2023 Dec 6;24(24):17186 MELAS-Derived Neurons Functionally Improve by Mitochondrial Transfer from Highly Purified Mesenchymal Stem Cells (REC)
Wilson’s disease HPS0049, HPS0053, HPS0045 Hum Mol Genet. 2022 Oct 28;31(21):3652–3671 Retinoids rescue ceruloplasmin secretion and alleviate oxidative stress in Wilson's disease-specific hepatocytes
Pompe’s disease HPS0175 Stem Cells Transl Med. 2017 Jan;6(1):31–39 Metabolomic Profiling of Pompe Disease-Induced Pluripotent Stem Cell-Derived Cardiomyocytes Reveals That Oxidative Stress Is Associated with Cardiac and Skeletal Muscle Pathology
Skin and connective tissue diseases 8 23 126  − 
Immune diseases 23 53 25 Chronic infantile neurological cutaneous and articular (CINCA) syndrome (somatic mosaicism) HPS0117, HPS0119, HPS0120 Blood. 2012 Aug 9;120(6):1299–308 Induced pluripotent stem cells from CINCA syndrome patients as a model for dissecting somatic mosaicism and drug discovery
Circulatory system diseases 3 28 60  − 
Hematologic diseases 8 26 128 X-linked Chronic granulomatous disease (X-CGD, gp91phox-deficiency) HPS0337, HPS0338, HPS0339 Mol Ther Methods Clin Dev. 2015 Dec 9:2:15046 An assessment of the effects of ectopic gp91phox expression in XCGD iPSC-derived neutrophils
Chédiak-Higashi syndrome HPS0515 Pediatr Int. 2022 Jan;64(1):e15390 iPS cells from Chediak-Higashi syndrome patients recapitulate the giant granules in myeloid cells
Kidney and urologic diseases 7 17 67  − 
Bone, cartilage, and articular diseases 11 41 126 Fibrodysplasia ossificans progressiva (FOP) HPS0376 Nat Biomed Eng. 2023 May;7(5):672–691 Optimization of Cas9 activity through the addition of cytosine extensions to single-guide RNAs
Fibrodysplasia ossificans progressiva (FOP) HPS0376, HPS0377, HPS0378 Orphanet J Rare Dis. 2013 Dec 9:8:190. 2013 Dec 9:8:190 Induced pluripotent stem cells from patients with human fibrodysplasia ossificans progressiva show increased mineralization and cartilage formation
Endocrine diseases 9 25 130 Familial central diabetes insipidus HPS1011 Sci Rep. 2022 Oct 17;12(1):17381 Differentiation of human induced pluripotent stem cells into hypothalamic vasopressin neurons with minimal exogenous signals and partial conversion to the naive state
Respiratory tract diseases 9 19 106  − 
Eye diseases 4 15 26 Age related Macular degeneration HPS1072 Stem Cell Res. 2020 May:45:101787 Generation of a human induced pluripotent stem cell line, BRCi004-A, derived from a patient with age-related macular degeneration
Best disease HPS1012 Stem Cell Res. 2020 May:45:101782 Generation of a human induced pluripotent stem cell line, BRCi005-A, derived from a Best disease patient with BEST1 mutations
Otorhinolaryngologic diseases 1 1 3  − 
Digestive system diseases 8 19 114  − 
Diseases due to chromosomal aberrations and gene mutations 18 25 118 Prader Willi syndrome HPS0082 Stem Cell Res. 2021 May:53:102351 Abnormal DNA methylation in pluripotent stem cells from a patient with Prader-Willi syndrome results in neuronal differentiation defects
Prader–Willi Syndrome, abnormal methylation of Ch15 HPS2846 Sci Rep. 2023 Jul 25;13(1):12053 Defects in early synaptic formation and neuronal function in Prader-Willi syndrome
22q11.2 deletion syndrome HPS1627, HPS2296 Stem Cell Res. 2022 May:61:102744 Generation of human induced pluripotent stem cell lines derived from four DiGeorge syndrome patients with 22q11.2 deletion
Other diseases 51 116 476 Juvenile nephronophthisis HPS0447, HPS0450 Stem Cell Res. 2020 May:45:101815 Generation of two human induced pluripotent stem cell lines derived from two juvenile nephronophthisis patients with NPHP1 deletion
Alzheimer disease HPS0255, HPS0256, HPS0257, HPS0258, HPS0854, HPS1745, HPS1747 Stem Cell Reports. 2023 Mar 14;18(3):688–705 BMP4-SMAD1/5/9-RUNX2 pathway activation inhibits neurogenesis and oligodendrogenesis in Alzheimer’s patients' iPSCs in senescence-related conditions
HPS0258, HPS1745, HPS1747 Cell Stem Cell. 2013 Apr 4;12(4):487–96 Modeling Alzheimer’s disease with iPSCs reveals stress phenotypes associated with intracellular Aβ and differential drug responsiveness
Epilepsy HPS1732 Stem Cell Res. 2017 Oct:24:12–15 Induced pluripotent stem cells derived from an autosomal dominant lateral temporal epilepsy (ADLTE) patient carrying S473L mutation in leucine-rich glioma inactivated 1 (LGI1)
Total 231 753 3110
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NBRP-Human and animal cells performs genetic analysis of some disease-specific iPS cells to promote their use. For example, for iPS cells derived from amyotrophic lateral sclerosis, commonly referred to as ALS, the results of target sequence analysis for the casual genes (SOD1/ TARDBP/ ALS10/ TDP-43 genes) have been published on the RIKEN BRC website (https://cell.brc.riken.jp/en/ga-als). As for iPS cells derived from spinocerebellar degeneration, the results of the number of repeated sequences in related 8-gene regions have been published (https://cell.brc.riken.jp/en/ga-scd). In addition to the cell material itself, human iPS cell lines (disease-specific iPS cells and healthy human iPS cells) provide clinical information such as sex, age and the names of diseases, and researchers can use these data upon appropriate application and review.

Microbes

The NBRP also manages general microbes (bacteria, archaea, yeast, and filamentous fungi), prokaryotes (Escherichia coli and Bacillus subtilis), pathogenic eukaryotic microbes, pathogenic bacteria, and human pathogenic viruses). The most popular paper among NBRP-Mice users’ results sorted by Citation Index is one that identified and isolated 11 gut bacterial strains that strongly induce IFNγ-producing CD8T cells and showed that administration of these strains inhibited infection and tumor growth in mouse strains (Tanoue et al. 2019). The influence of the gut microbiota and skin microbiota on phenotype is a topic of great interest, and more results are expected in the future.

Research Resource Circulation

All the article information discussed in this paper, which is based on studies using NBRP resources, is registered and accessible in the Research Resource Circulation (RRC) database (https://rrc.nbrp.jp/) (Fig. 4). RRC is an integrated database that connects published research outcomes to the specific bioresources used in those studies. Its primary objective is to aggregate and organize information on published papers and patents that have utilized these resources and to make this information publicly available along with statistical data, thereby enhancing the information content of each resource and promoting their utilization.

Fig. 4.

Fig. 4

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Research Resource Circulation (RRC) Database: a system for tracking and analyzing the utilization of NBRP bioresources and research outcomes

A key feature of the RRC is assigning a unique RRC ID to each paper corresponding PubMed information, strain names, citation metrics, and other relevant data. Development of the RRC began in 2007, and it presently contains entries for approximately 55,000 papers and 1300 patents. Users can easily register papers using PubMed IDs or DOIs. Moreover, the RRC is linked with NCBI’s LinkOut service, enabling resource links to be added to corresponding papers in PubMed.

Conclusion

The NBRP provides useful biological resources, technologies, and information for mammalian genome research both in Japan and overseas, and many users’ research results have been reported. Not only the use of individual bioresources but also the combination of bioresources has been reported by many users. We encourage global scientists to conduct a comprehensive search with biological resources of high quality available from NBRP. In addition, we are constantly updating the information on each bioresource to meet the needs of increasingly sophisticated and complex research while reviewing the latest research trends and increasing the number of stored resources. We hope you will make effective use of the NBRP to advance mammalian genome research.

Acknowledgements

We sincerely thank Dr. Yuji Kohara, Program Director of NBRP; Dr. Yuichi Obata, Program Officer of NBRP; and Dr. Toshihiko Shiroishi, Director of RIKEN BRC for their thoughtful leadership and guidance. We are grateful to Drs. Ayumi Koso and Asuka Mukai, NBRP Public Relations Team for providing accurate information and advice. The NBRP is supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan.

Author contributions

S.M.-I. made a conceptualization and wrote the main manuscript text. S.K. prepared Fig. 4. M.A., T.M., S.W., K.N., K.-I.N., H.O., K.S., S.Y., Y.M., Y.N., and M.O. provided accurate information and data. A.Y. supervised the manuscripts. All authors reviewed and revised the manuscript.

Data availability

No datasets were generated or analysed during the current study.

Declarations

Conflict of interest

The authors declare no competing interests.

Footnotes

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Contributor Information

Saori Mizuno-Iijima, Email: saori.mizuno@riken.jp.

Atsushi Yoshiki, Email: atsushi.yoshiki@riken.jp.

References

  1. Ando R, Shimozono S, Ago H, Takagi M, Sugiyama M, Kurokawa H, Hirano M, Niino Y, Ueno G, Ishidate F, Fujiwara T, Okada Y, Yamamoto M, Miyawaki A (2023) StayGold variants for molecular fusion and membrane-targeting applications. Nat Methods 21(4):648–656. 10.1038/s41592-023-02085-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bamunusinghe D, Liu Q, Lu X, Oler A, Kozak CA (2013) Endogenous gammaretrovirus acquisition in Mus musculus subspecies carrying functional variants of the XPR1 virus receptor. J Virol 87(17):9845–9855. 10.1128/jvi.01264-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bamunusinghe D, Naghashfar Z, Buckler-White A, Plishka R, Baliji S, Liu Q, Kassner J, Oler AJ, Hartley J, Kozak CA (2016) Sequence diversity, intersubgroup relationships, and origins of the mouse Leukemia gammaretroviruses of laboratory and wild mice. J Virol 90(23):10682–10692. 10.1128/jvi.03186-15 [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bamunusinghe D, Skorski M, Buckler-White A, Kozak CA (2018) Xenotropic mouse gammaretroviruses isolated from pre-leukemic tissues include a recombinant. Viruses 10(8):418. 10.3390/v10080418 [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Banreti A, Bhattacharya S, Wien F, Matsuo K, Réfrégiers M, Meinert C, Meierhenrich U, Hudry B, Thompson D, Noselli S (2022) Biological effects of the loss of homochirality in a multicellular organism. Nat Commun 13(1):7059. 10.1038/s41467-022-34516-x [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berg EM, Mrowka L, Bertuzzi M, Madrid D, Picton LD, El Manira A (2023) Brainstem circuits encoding start, speed, and duration of swimming in adult zebrafish. Neuron 111(3):372-386.e4. 10.1016/j.neuron.2022.10.034 [DOI] [PubMed] [Google Scholar]
  7. Bujarrabal-Dueso A, Sendtner G, Meyer DH, Chatzinikolaou G, Stratigi K, Garinis GA, Schumacher B (2023) The DREAM complex functions as conserved master regulator of somatic DNA-repair capacities. Nat Struct Mol Biol 30(4):475–488. 10.1038/s41594-023-00942-8 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carbo-Tano M, Lapoix M, Jia X, Thouvenin O, Pascucci M, Auclair F, Quan FB, Albadri S, Aguda V, Farouj Y, Hillman EMC, Portugues R, Del Bene F, Thiele TR, Dubuc R, Wyart C (2023) The mesencephalic locomotor region recruits V2a reticulospinal neurons to drive forward locomotion in larval zebrafish. Nat Neurosci. 10.1038/s41593-023-01418-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chen TY, Wang FY, Lee PJ, Hsu AL, Ching TT (2024) Mitochondrial S-adenosylmethionine deficiency induces mitochondrial unfolded protein response and extends lifespan in Caenorhabditis elegans. Aging Cell 23(4):e14103. 10.1111/acel.14103 [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chiken S, Takada M, Nambu A (2021) Altered dynamic information flow through the cortico-basal ganglia pathways mediates Parkinson’s disease symptoms. Cereb Cortex 31(12):5363–5380. 10.1093/cercor/bhab164 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Darbin O, Hatanaka N, Takara S, Kaneko N, Chiken S, Naritoku D, Martino A, Nambu A (2022) Subthalamic nucleus deep brain stimulation driven by primary motor cortex γ2 activity in parkinsonian monkeys. Sci Rep 12(1):6493. 10.1038/s41598-022-10130-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Derrick CJ, Szenker-Ravi E, Santos-Ledo A, Alqahtani A, Yusof A, Eley L, Coleman AHL, Tohari S, Ng AY, Venkatesh B, Alharby E, Mansard L, Bonnet-Dupeyron MN, Roux AF, Vaché C, Roume J, Bouvagnet P, Almontashiri NAM, Henderson DJ, Reversade B, Chaudhry B (2024) Functional analysis of germline VANGL2 variants using rescue assays of VANGL2 knockout zebrafish. Hum Mol Genet 33(2):150–169. 10.1093/hmg/ddad171 [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eguchi S, Kimura K, Kageyama K, Tani N, Tanaka R, Nishio K, Shinkawa H, Ohira GO, Amano R, Tanaka S, Yamamoto A, Takemura S, Yashiro M, Kubo S (2022) Optimal organ for patient-derived Xenograft model in pancreatic cancer and microenvironment that contributes to success. Anticancer Res 42(5):2395–2404. 10.21873/anticanres.15718 [DOI] [PubMed] [Google Scholar]
  14. Fujihara Y, Kaseda K, Inoue N, Ikawa M, Okabe M (2013) Production of mouse pups from germline transmission-failed knockout chimeras. Transgenic Res 22(1):195–200. 10.1007/s11248-012-9635-x [DOI] [PubMed] [Google Scholar]
  15. Gima S, Oe K, Nishimura K, Ohgita T, Ito H, Kimura H, Saito H, Takata K (2024) Host-to-graft propagation of inoculated α-synuclein into transplanted human induced pluripotent stem cell-derived midbrain dopaminergic neurons. Regen Ther 25:229–237. 10.1016/j.reth.2023.12.019 [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hagihara Y, Okuzaki Y, Matsubayashi K, Kaneoka H, Suzuki T, Iijima S, Nishijima KI (2020) Primordial germ cell-specific expression of eGFP in transgenic chickens. Genesis 58(8):e23388. 10.1002/dvg.23388 [DOI] [PubMed] [Google Scholar]
  17. Haneda Y, Miyagawa-Tomita S, Uchijima Y, Iwase A, Asai R, Kohro T, Wada Y, Kurihara H (2024) Diverse contribution of amniogenic somatopleural cells to cardiovascular development: with special reference to thyroid vasculature. Dev Dyn 253(1):59–77. 10.1002/dvdy.532 [DOI] [PubMed] [Google Scholar]
  18. Hasan ASH, Dinh TTH, Le HT, Mizuno-Iijima S, Daitoku Y, Ishida M, Tanimoto Y, Kato K, Yoshiki A, Murata K, Mizuno S, Sugiyama F (2021) Characterization of a bicistronic knock-in reporter mouse model for investigating the role of CABLES2 in vivo. Exp Anim 70(1):22–30. 10.1538/expanim.20-0063 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hasegawa A, Mochida K, Matoba S, Inoue K, Hama D, Kadota M, Hiraiwa N, Yoshiki A, Ogura A (2021) Development of assisted reproductive technologies for Mus spretus. Biol Reprod 104(1):234–243. 10.1093/biolre/ioaa177 [DOI] [PubMed] [Google Scholar]
  20. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, Takeuchi H, Aigaki T, Matsuzaki F, Nakagoshi H, Tanimura T, Ueda R, Uemura T, Yoshihara M, Goto S (2002) GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34(1–2):58–61. 10.1002/gene.10137 [DOI] [PubMed] [Google Scholar]
  21. Hayashi Y, Ohnishi H, Kitano M, Kishimoto Y, Takezawa T, Okuyama H, Yoshimatsu M, Kuwata F, Tada T, Mizuno K, Omori K (2024) Comparative study of immunodeficient rat strains in engraftment of human-induced pluripotent stem cell-derived airway epithelia. Tissue Eng Part A 30(3–4):144–153. 10.1089/ten.tea.2023.0214 [DOI] [PubMed] [Google Scholar]
  22. Higashijima S, Hotta Y, Okamoto H (2020) Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J Neurosci 20(1):206–218. 10.1523/jneurosci.20-01-00206.2000 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hirano M, Ando R, Shimozono S, Sugiyama M, Takeda N, Kurokawa H, Deguchi R, Endo K, Haga K, Takai-Todaka R, Inaura S, Matsumura Y, Hama H, Okada Y, Fujiwara T, Morimoto T, Katayama K, Miyawaki A (2022) A highly photostable and bright green fluorescent protein. Nat Biotechnol 40(7):1132–1142. 10.1038/s41587-022-01278-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hirose M, Hasegawa A, Mochida K, Matoba S, Hatanaka Y, Inoue K, Goto T, Kaneda H, Yamada I, Furuse T, Abe K, Uenoyama Y, Tsukamura H, Wakana S, Honda A, Ogura A (2017) CRISPR/Cas9-mediated genome editing in wild-derived mice: generation of tamed wild-derived strains by mutation of the a (nonagouti) gene. Sci Rep 14(7):42476. 10.1038/srep42476 [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Honda A, Tachibana R, Hamada K, Morita K, Mizuno N, Morita K, Asano M (2019) Efficient derivation of knock-out and knock-in rats using embryos obtained by in vitro fertilization. Sci Rep 9(1):11571. 10.1038/s41598-019-47964-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Huss D, Benazeraf B, Wallingford A, Filla M, Yang J, Fraser SE, Lansford R (2015) A transgenic quail model that enables dynamic imaging of amniote embryogenesis. Development 142(16):2850–2859. 10.1242/dev.121392 [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Itoh T, Uehara M, Yura S, Wang JC, Fujii Y, Nakanishi A, Shimizu T, Hibi M (2024) Foxp and Skor family proteins control differentiation of Purkinje cells from Ptf1a- and Neurog1-expressing progenitors in zebrafish. Development 151(7):202546. 10.1242/dev.202546 [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Iwano S, Sugiyama M, Hama H, Watakabe A, Hasegawa N, Kuchimaru T, Tanaka KZ, Takahashi M, Ishida Y, Hata J, Shimozono S, Namiki K, Fukano T, Kiyama M, Okano H, Kizaka-Kondoh S, McHugh TJ, Yamamori T, Hioki H, Maki S, Miyawaki A (2018) Single-cell bioluminescence imaging of deep tissue in freely moving animals. Science 359(6378):935–939. 10.1126/science.aaq1067 [DOI] [PubMed] [Google Scholar]
  29. Kazuki Y, Gao FJ, Li Y, Moyer AJ, Devenney B, Hiramatsu K, Miyagawa-Tomita S, Abe S, Kazuki K, Kajitani N, Uno N, Takehara S, Takiguchi M, Yamakawa M, Hasegawa A, Shimizu R, Matsukura S, Noda N, Ogonuki N, Inoue K, Matoba S, Ogura A, Florea LD, Savonenko A, Xiao M, Wu D, Batista DA, Yang J, Qiu Z, Singh N, Richtsmeier JT, Takeuchi T, Oshimura M, Reeves RH (2020) A non-mosaic transchromosomic mouse model of down syndrome carrying the long arm of human chromosome 21. Elife 9:e56223. 10.7554/elife.56223 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kondo S, Ueda R (2013) Highly improved gene targeting by germline-specific Cas9 expression in Drosophila. Genetics 195(3):715–721. 10.1534/genetics.113.156737 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kubota S, Sasaki C, Kikuta S, Yoshida J, Ito S, Gomi H, Oya T, Seki K (2024) Modulation of somatosensory signal transmission in the primate cuneate nucleus during voluntary hand movement. Cell Rep 43(3):113884. 10.1016/j.celrep.2024.113884 [DOI] [PubMed] [Google Scholar]
  32. Kumano H, Uka T (2024) Employment of time-varying sensory evidence to test the mechanisms underlying flexible decision-making. NeuroReport 35(2):107–114. 10.1097/wnr.0000000000001980 [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lahr CA, Landgraf M, Wagner F, Cipitria A, Moreno-Jiménez I, Bas O, Schmutz B, Meinert C, Mashimo T, Miyasaka Y, Holzapfel BM, Shafiee A, McGovern JA, Hutmacher DW (2021) A humanised rat model reveals ultrastructural differences between bone and mineralised tumour tissue. Bone 158:116018. 10.1016/j.bone.2021.116018 [DOI] [PubMed] [Google Scholar]
  34. Mallart C, Netter S, Chalvet F, Claret S, Guichet A, Montagne J, Pret AM, Malartre M (2024) JAK-STAT-dependent contact between follicle cells and the oocyte controls Drosophila anterior–posterior polarity and germline development. Nat Commun 15(1):1627. 10.1038/s41467-024-45963-z [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Martelli F, Lin J, Mele S, Imlach W, Kanca O, Barlow CK, Paril J, Schittenhelm RB, Christodoulou J, Bellen HJ, Piper MDW, Johnson TK (2024) Identifying potential dietary treatments for inherited metabolic disorders using Drosophila nutrigenomics. Cell Rep 43(3):113861. 10.1016/j.celrep.2024.113861 [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Mashimo T, Takizawa A, Voigt B, Yoshimi K, Hiai H, Kuramoto T, Serikawa T (2010) Generation of knockout rats with X-linked severe combined immunodeficiency (X-SCID) using zinc-finger nucleases. PLoS ONE 5(1):e8870. 10.1371/journal.pone.0008870 [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Miyasaka Y, Wang J, Hattori K, Yamauchi Y, Hoshi M, Yoshimi K, Ishida S, Mashimo T (2022) A high-quality severe combined immunodeficiency (SCID) rat bioresource. PLoS ONE 17(8):e0272950. 10.1371/journal.pone.0272950 [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Mizuno-Iijima S, Ayabe S, Kato K, Matoba S, Ikeda Y, Dinh TTH, Le HT, Suzuki H, Nakashima K, Hasegawa Y, Hamada Y, Tanimoto Y, Daitoku Y, Iki N, Ishida M, Ibrahim EAE, Nakashiba T, Hamada M, Murata K, Miwa Y, Okada-Iwabu M, Iwabu M, Yagami KI, Ogura A, Obata Y, Takahashi S, Mizuno S, Yoshiki A, Sugiyama F (2021) Efficient production of large deletion and gene fragment knock-in mice mediated by genome editing with Cas9-mouse Cdt1 in mouse zygotes. Methods 191:23–31. 10.1016/j.ymeth.2020.04.007 [DOI] [PubMed] [Google Scholar]
  39. Mizuno-Iijima S, Nakashiba T, Ayabe S, Nakata H, Ike F, Hiraiwa N, Mochida K, Ogura A, Masuya H, Kawamoto S, Tamura M, Obata Y, Shiroishi T, Yoshiki A (2022) Mouse resources at the RIKEN bioresource research center and the national bioresource project core facility in Japan. Mamm Genome 33(1):181–191. 10.1007/s00335-021-09916-x [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Mochida K, Hasegawa A, Otaka N, Hama D, Furuya T, Yamaguchi M, Ichikawa E, Ijuin M, Taguma K, Hashimoto M, Takashima R, Kadota M, Hiraiwa N, Mekada K, Yoshiki A, Ogura A (2014) Devising assisted reproductive technologies for wild-derived strains of mice: 37 strains from five subspecies of Mus musculus. PLoS ONE 9(12):e114305. 10.1371/journal.pone.0114305 [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Mochida K, Morita K, Sasaoka Y, Morita K, Endo H, Hasegawa A, Asano M, Ogura A (2024) Superovulation with an anti-inhibin monoclonal antibody improves the reproductive performance of rat strains by increasing the pregnancy rate and the litter size. Sci Rep 14(1):8294. 10.1038/s41598-024-58611-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Morita K, Honda A, Asano M (2023) A Simple and efficient method for generating KO rats using in vitro fertilized oocytes. Methods Mol Biol 2637:233–246. 10.1007/978-1-0716-3016-7_18 [DOI] [PubMed] [Google Scholar]
  43. Motono M, Yamada Y, Hattori Y, Nakagawa R, Nishijima K, Iijima S (2010) Production of transgenic chickens from purified primordial germ cells infected with a lentiviral vector. J Biosci Bioeng 109(4):315–321. 10.1016/j.jbiosc.2009.10.007 [DOI] [PubMed] [Google Scholar]
  44. Nakashiba T, Ogoh K, Iwano S, Sugiyama T, Mizuno-Iijima S, Nakashima K, Mizuno S, Sugiyama F, Yoshiki A, Miyawaki A, Abe K (2023) Development of two mouse strains conditionally expressing bright luciferases with distinct emission spectra as new tools for in vivo imaging. Lab Anim (NY) 52(10):247–257 [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Noda T, Oji A, Ikawa M (2017) Genome editing in mouse zygotes and embryonic stem cells by introducing SgRNA/Cas9 expressing plasmids. Methods Mol Biol 1630:67–80. 10.1007/978-1-4939-7128-2_6 [DOI] [PubMed] [Google Scholar]
  46. Noda T, Fujihara Y, Matsumura T, Oura S, Kobayashi S, Ikawa M (2019) Seminal vesicle secretory protein 7, PATE4, is not required for sperm function but for copulatory plug formation to ensure fecundity. Biol Reprod 100(4):1035–1045. 10.1093/biolre/ioy247 [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Ogoh K, Akiyoshi R, Suzuki H (2020) Cloning and mutagenetic modification of the firefly luciferase gene and its use for bioluminescence microscopy of engrailed expression during Drosophila metamorphosis. Biochem Biophys Rep 23:100771. 10.1016/j.bbrep.2020.100771 [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Oyama K, Nagai Y, Minamimoto T (2023) Targeted delivery of chemogenetic adeno-associated viral vectors to cortical sulcus regions in macaque monkeys by handheld injections. Bio Protoc 13(23):e4897. 10.21769/bioprotoc.4897 [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Saito A, Tahara R, Hirose M, Kadota M, Hasegawa A, Kondo S, Kato H, Amano T, Yoshiki A, Ogura A, Kiyosawa H (2024) Inter-subspecies mouse F1 hybrid embryonic stem cell lines newly established for studies of allelic imbalance in gene expression. Exp Anim. 10.1538/expanim.24-0002 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Sasaguri H, Nagata K, Sekiguchi M, Fujioka R, Matsuba Y, Hashimoto S, Sato K, Kurup D, Yokota T, Saido TC (2018) Introduction of pathogenic mutations into the mouse Psen1 gene by Base Editor and Target-AID. Nat Commun 9(1):2892. 10.1038/s41467-018-05262-w [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Sasaki R, Ohta Y, Onoe H, Yamaguchi R, Miyamoto T, Tokuda T, Tamaki Y, Isa K, Takahashi J, Kobayashi K, Ohta J, Isa T (2024) Balancing risk-return decisions by manipulating the mesofrontal circuits in primates. Science 383(6678):55–61. 10.1126/science.adj6645 [DOI] [PubMed] [Google Scholar]
  52. Sato K, Watamura N, Fujioka R, Mihira N, Sekiguchi M, Nagata K, Ohshima T, Saito T, Saido TC, Sasaguri H (2021) A third-generation mouse model of Alzheimer’s disease shows early and increased cored plaque pathology composed of wild-type human amyloid β peptide. J Biol Chem 297(3):101004. 10.1016/j.jbc.2021.101004 [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Satou C, Kimura Y, Higashijima S (2012) Generation of multiple classes of V0 neurons in zebrafish spinal cord: progenitor heterogeneity and temporal control of neuronal diversity. J Neurosci 32(5):1771–1783. 10.1523/jneurosci.5500-11.2012 [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Schmidt AR, Placer HJ, Muhammad IM, Shephard R, Patrick RL, Saurborn T, Horstick EJ, Bergeron SA (2024) Transcriptional control of visual neural circuit development by GS homeobox 1. PLoS Genet 20(4):e1011139. 10.1371/journal.pgen.1011139 [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Serizawa T, Isotani A, Matsumura T, Nakanishi K, Nonaka S, Shibata S, Ikawa M, Okano H (2019) Developmental analyses of mouse embryos and adults using a non-overlapping tracing system for all three germ layers. Development 146(21):174938. 10.1242/dev.174938 [DOI] [PubMed] [Google Scholar]
  56. Sharifi S, Chaudhari P, Martirosyan A, Eberhardt AO, Witt F, Gollowitzer A, Lange L, Woitzat Y, Okoli EM, Li H, Rahnis N, Kirkpatrick J, Werz O, Ori A, Koeberle A, Bierhoff H, Ermolaeva M (2024) Reducing the metabolic burden of rRNA synthesis promotes healthy longevity in Caenorhabditis elegans. Nat Commun 15(1):1702. 10.1038/s41467-024-46037-w [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Tada T, Ohnishi H, Yamamoto N, Kuwata F, Hayashi Y, Okuyama H, Morino T, Kasai Y, Kojima H, Omori K (2022) Transplantation of a human induced pluripotent stem cell-derived airway epithelial cell sheet into the middle ear of rats. Regen Ther 19:77–87. 10.1016/j.reth.2022.01.001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Takada T, Fukuta K, Usuda D, Kushida T, Kondo S, Kawamoto S, Yoshiki A, Obata Y, Fujiyama A, Toyoda A, Noguchi H, Shiroishi T, Masuya H (2022) MoG+: a database of genomic variations across three mouse subspecies for biomedical research. Mamm Genome 33(1):31–43. 10.1007/s00335-021-09933-w [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Takeishi T, Fujiwara K, Osada N, Mita A, Takada T, Shiroishi T, Suzuki H (2022) Phylogeographic study using nuclear genome sequences of Asip to infer the origins of ventral fur color variation in the house mouse Mus musculus. Genes Genet Syst 96(6):271–284. 10.1266/ggs.21-00075 [DOI] [PubMed] [Google Scholar]
  60. Taniguchi K, Igaki T (2023) Sas-Ptp10D shapes germ-line stem cell niche by facilitating JNK-mediated apoptosis. PLoS Genet 19(3):e1010684. 10.1371/journal.pgen.1010684 [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Tanimoto Y, Iijima S, Hasegawa Y, Suzuki Y, Daitoku Y, Mizuno S, Ishige T, Kudo T, Takahashi S, Kunita S, Sugiyama F, Yagami K (2008) Embryonic stem cells derived from C57BL/6J and C57BL/6N mice. Comp Med 58(4):347–352 [PMC free article] [PubMed] [Google Scholar]
  62. Tanoue T, Morita S, Plichta DR, Skelly AN, Suda W, Sugiura Y, Narushima S, Vlamakis H, Motoo I, Sugita K, Shiota A, Takeshita K, Yasuma-Mitobe K, Riethmacher D, Kaisho T, Norman JM, Mucida D, Suematsu M, Yaguchi T, Bucci V, Inoue T, Kawakami Y, Olle B, Roberts B, Hattori M, Xavier RJ, Atarashi K, Honda K (2019) A defined commensal consortium elicits CD8 T cells and anti-cancer immunity. Nature 565(7741):600–605. 10.1038/s41586-019-0878-z [DOI] [PubMed] [Google Scholar]
  63. Tsujino K, Okuzaki Y, Hibino N, Kawamura K, Saito S, Ozaki Y, Ishishita S, Kuroiwa A, Iijima S, Matsuda Y, Nishijima K, Suzuki T (2019) Identification of transgene integration site and anatomical properties of fluorescence intensity in a EGFP transgenic chicken line. Dev Growth Diffe 61(7–8):393–401 [DOI] [PubMed] [Google Scholar]
  64. Wang S, Meyer DH, Schumacher B (2023) Inheritance of paternal DNA damage by histone-mediated repair restriction. Nature 613(7943):365–374. 10.1038/s41586-022-05544-w [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Yagi M, Kishigami S, Tanaka A, Semi K, Mizutani E, Wakayama S, Wakayama T, Yamamoto T, Yamada Y (2017) Derivation of ground-state female ES cells maintaining gamete-derived DNA methylation. Nature 548(7666):224–227. 10.1038/nature23286 [DOI] [PubMed] [Google Scholar]
  66. Yagi M, Kabata M, Tanaka A, Ukai T, Ohta S, Nakabayashi K, Shimizu M, Hata K, Meissner A, Yamamoto T, Yamada Y (2020) Identification of distinct loci for de novo DNA methylation by DNMT3A and DNMT3B during mammalian development. Nat Commun 11(1):3199. 10.1038/s41467-020-16989-w [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Yasuda SP, Miyasaka Y, Hou X, Obara Y, Shitara H, Seki Y, Matsuoka K, Takahashi A, Wakai E, Hibino H, Takada T, Shiroishi T, Kominami R, Kikkawa Y (2020) Two loci contribute to age-related hearing loss resistance in the Japanese wild-derived inbred MSM/Ms mice. Biomedicines 10(9):2221. 10.3390/biomedicines10092221 [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Yoshihi K, Kato K, Iida H, Teramoto M, Kawamura A, Watanabe Y, Nunome M, Nakano M, Matsuda Y, Sato Y, Mizuno H, Iwasato T, Ishii Y, Kondoh H (2020) Live imaging of avian epiblast and anterior mesendoderm grafting reveals the complexity of cell dynamics during early brain development. Development 149(6):199999. 10.1242/dev.199999 [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Yoshimi K, Kunihiro Y, Kaneko T, Nagahora H, Voigt B, Mashimo T (2016) ssODN-mediated knock-in with CRISPR-cas for large genomic regions in zygotes. Nat Commun 20(7):10431. 10.1038/ncomms10431 [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Yoshioka-Kobayashi K, Matsumiya M, Niino Y, Isomura A, Kori H, Miyawaki A, Kageyama R (2020) Coupling delay controls synchronized oscillation in the segmentation clock. Nature 580(7801):119–123. 10.1038/s41586-019-1882-z [DOI] [PubMed] [Google Scholar]
  71. Zhao S, Wang C, Luo H, Li F, Wang Q, Xu J, Huang Z, Liu W, Zhang W (2024) A role for retinoblastoma 1 in hindbrain morphogenesis by regulating GBX family. J Genet Genomics. 10.1016/j.jgg.2024.03.008 [DOI] [PubMed] [Google Scholar]

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Data Availability Statement

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