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. 2020 Apr 10;96(4):131–158. doi: 10.2183/pjab.96.012

Table 2.

Examples of the direct reprogramming with various methods

Source cells Target cells Transgenes and/or Treatment Species Cell transplantation Published year PMID
Integration-free transduction
Fibroblasts (BJ and MRC-5 cells) Hepatocytes HNF1A and Any two of the three factors: FOXA1, FOXA3, and HNF4A (mRNA transfection) Human   2014 2496371559)
Non-sensory cochlear epithelial cells Neuronal cells Ascl1; Ascl1 and Neurod (plasmid electroporation) Mouse   2014 2492835139)
Cardiac fibroblasts Cardiomyocytes Gata4, Mef2c, and Tbx5 (peptide-enhanced mRNA transfection) Mouse   2015 25834424116)
Astrocytes Neural stem cells Sox2 (Leu3p-αIPM system) Mouse   2016 27148066121)
Fetal and embryonic fibroblasts and Brain cells in vivo Neuronal cells Ascl1, Brn2, and Myt1l (mRNA transfection with a GO-PEI-based reagent in vitro and in vivo) Mouse & Human   2016 2814563140)
Peripheral blood mononuclear cells Photoreceptor cells CRX, RAX1, and NEUROD1 (SeV infection) Human   2016 27170256112)
Gingival fibroblasts and Adult dermal fibroblasts Osteoblasts OCT4, OSTERIX, and L-MYC (plasmid transfection) Human YES 2016 2699086081)
Fibroblasts Hepatocytes OCT4, FOXA2, HNF1A, and GATA3 (protein transduction with HVJ-E) Human   2017 2858733162)
Fibroblasts Neurocytes SOX2, GATA3, and NEUROD1 (protein transduction with HVJ-E) Human   2017 2858733162)
Fibroblasts (3T6 cells) Neuronal cells Ascl1, Brn2, and Foxa1 (plasmid transfection with a polysaccharide-based reagent) Mouse   2017 28855426119)
Mesenchymal stem cells Hepatocytes Hnf4a and Foxa3 (PiggyBac transposon) Mouse   2017 28295042114)
Dermal fibroblasts Endothelial progenitor cells ETV2 (mRNA transfection) Human YES 2017 27778229117)
Fibroblasts (3T6 cells) Neuronal cells Ascl1, Brn4, and Tcf3 (plasmid transfection with a polysaccharide-based reagent) Mouse   2017 29137640120)
Mesenchymal stem cells and Dermal fibroblasts Neural stem cells SOX2 (mRNA transfection) Human   2018 29909688118)
Adult fibroblasts Neural precursor cells SOX2; SOX2 and PAX6; SOX2 and LMX1A; SOX2, LMX1A, and FOXA2 (plasmid transfection) Human   2018 3001847136)
Dermal fibroblasts Neural precursor cells SOX2 and PAX6 (chemically modified mRNA or plasmid transfection) Human   2018 3045044034)
Embryonic fibroblasts Hepatocytes Hnf4a and Foxa3 (modified mRNA transfection) Mouse YES 2018 30327781115)
Foreskin fibroblasts Neuronal cells ASCL1 + miR-124 + P53 knockdown (episomal plasmid transfection) Human   2019 30539819122)
Bone marrow-derived cells, Fibroblasts, and Keratinocytes Neural precursor cells MSI1, NGN2, and MBD2 (plasmid transfection) Human YES 2019 3119617337)
Renal proximal tubular epithelial (HK2) cells Nephron progenitor cells SNAI2, EYA1, and SIX1 (PiggyBac transposon) Human   2019 30827514103)
Chemical compounds (with or without transcription factors)
Fibroblasts (IMR90 or MRC5 cells) Cholinergic neurons NGN2 + Forskolin and dorsomorphin treatment Human   2013 23873306130)
Embryonic fibroblasts and Neonatal tail-tip fibroblasts Cardiomyocytes CHIR99021, RepSox, Forskolin, Valproic acid, Parnate, and TTNPB treatment Mouse   2015 26292833123)
Embryonic fibroblasts and Adult tail-tip fibroblasts Neural stem cells Valproic acid, Bix01294, RG108, PD0325901, CHIR99021, Vitamin C, and A83-01 treatment Mouse YES 2015 26788068124)
Fibroblasts Neuronal cells Valproic acid, CHIR99021, RepSox, Forskolin, SP600125, GO6983, and Y-27632 treatment Human   2015 26253202125)
Fibroblasts Neuronal cells ISX9, SB431542, Forskolin, CHIR99021, and I-BET151 treatment Mouse   2015 26253201126)
Embryonic fibroblasts Neural stem cells A83-01, Purmorphamine, Valproic acid, and Thiazovivin treatment Mouse   2017 27207831131)
Urine-derived cells Hepatocytes FOXA3 and HNF1A or HNF4A + CHIR99021, RepSox, Valproic acid, Parnate, TTNPB, and Dznep treatment Human   2018 30315254127)
Embryonic and adult fibroblasts Skeletal muscle progenitor cells Myod + CHIR99021, RepSox, and Forskolin treatment Mouse YES 2018 29742392128)
Adult dermal fibroblasts, Fetal pancreas fibroblasts, and Peripheral blood mononuclear cells Neural plate border stem cells BRN2, KLF4, SOX2, and ZIC3 + CHIR99021, ALK5 inhibitor, Purmorphamine, Tranylcypromine treatment Human YES 2018 30581079132)
Striatal neurons Dopaminergic neurons Sox2, Nurr1, Lmx1a, and Foxa2 + Valproic acid treatment (in vivo infection) Mouse   2018 3031829242)
Glioblastoma cells (U87MG cells) Neuronal cells Forskolin, ISX9, CHIR99021, I-BET151, and DAPT treatment Human   2018 30091580129)
Dermal fibroblasts Neuronal cells NGN2 and ASCL1 + Pyrintegrin, ZM336372, AZ960, and KC7F2 treatment Human   2019 31099332133)
Culture condition and soluble factors (with transcription factors)
Liver cells in vivo β cells PDX1 + EGF and nicotinamide treatment Human YES 2005 15899968134)
Adult dermal fibroblasts and Neonatal foreskin fibroblasts Multilineage blood progenitor cells OCT4 + hematopoietic cytokines treatment Human YES 2010 21057492135)
Embryonic fibroblasts Cardiomyocytes OSKM + cytokines (including Bmp4) treatment Mouse   2011 21278734136)
Adult skin fibroblasts Neural stem cells OSKM + neurosphere culture Mouse YES 2012 22467474137)
Amniocytes Vascular endothelial cells ETV2, FLI1, and ERG1 + TGFβ inhibitor treatment Human YES 2012 23084400139)
Embryonic stem cells-derived fibroblasts Neural crest cells SOX10 + Environmental cues including WNT activation Human YES 2014 25158936140)
Newborn fibroblasts Hepatocytes OSK + Soluble factors Human YES 2014 24572354226)
Dermal fibroblasts Oligodendrocyte progenitor cells Oct4 + OPC induction medium Mouse YES 2015 26497893141)
Embryonic fibroblasts Keratinocytes OSK + Bmp4 and RA treatment Mouse YES 2016 27473056142)
Skin fibroblasts Neural stem cells OCT3/4, SOX2, KLF4, L-MYC, and LIN28 + P53 knockdown + Neurotrophins treatment Human   2016 27822179138)
miRNAs (with or without transcription factors)
Cardiac fibroblasts Cardiomyocytes miR-1, miR-133, miR-208, and miR-499 Mouse   2012 22539765147)
Embryonic fibroblasts Neuronal cells Ptb knockdown Mouse   2013 23313552143)
Cardiac fibroblasts and Embryonic fibroblasts Cardiomyocytes Gata4, Mef2c, and Tbx5 + miR-133; Gata4, Mef2c, Tbx5, Mesp1, and Myocd + miR-133 Mouse & Human   2014 24920580148)
Adult dermal fibroblasts, Umbilical cord blood cells, and Senescent somatic cells Neural stem cells SOX2 + HMGA2 expression or LET-7B inhibition Human YES 2015 25600877144)
Fibroblasts Cardiomyocytes GATA4, MEF2C, TBX5, ESRRG, MESP1, MYOCARDIN, ZFPM2, and HAND2 + miR-1 Human   2017 28796841149)
Adult fibroblasts Neuronal cells miR-9/9* and miR-124 Human   2017 28886366145)
Adult fibroblasts Spinal cord motor neurons ISL1 and LHX3 + miR-9/9* and miR-124 Human   2017 28886366145)
Brain vascular pericytes Cholinergic neuronal cells ASCL1, MYT1L, BRN2, and TLX3 + miR-124 Human YES 2018 29453933146)
Physical stimulation (with or without transcription factors)
Embryonic fibroblasts Neuronal cells Ascl1, Brn2, and Myt1l + Substrate topography Mouse   2014 24709523153)
Fibroblasts Cardiomyocytes Myocardin, Tbx5, and Mef2c + Microgroove Mouse   2015 26302234154)
Embryonic fibroblasts Dopaminergic neurons Ascl1, Pitx3, Nurr1, and Lmx1a + Nanogroove Mouse   2015 25662493155)
Dermal fibroblasts Endothelial progenitor cells ETV2 + Hypoxia Human   2016 27488544151)
Neonatal tail-tip fibroblasts Cardiomyocytes Gata4, Mef2c, and Tbx5 + Microgroove Mouse   2016 27376554156)
Fibroblasts Cardiomyocytes Gata4, Mef2c, and Tbx5 + Hypoxia Mouse   2016 26757100152)
Dermal fibroblasts Chondrocytes Electrical stimulation Human   2019 31005261157)
CRISPR/Cas9-based methods
Embryonic fibroblasts Neuronal cells CRISPR/Cas9-based transcriptional activators + gRNAs for Brn2, Ascl1, and Myt1l Mouse   2016 27524438158)
Liver cells in vivo β cells CRISPR/Cas9-based transcriptional activators + gRNA for Pdx1 (in vivo infection) Mouse YES 2017 2922478371)
Protein engineering (with transcription factors)
Embryonic fibroblasts Cardiomyocytes Gata4, Tbx5, and Hand2 + Mef2c fused with M3 domain of Myod Mouse   2013 23794713159)
Astrocytes Neuronal cells Ascl1, Creb-VP16, and Icer Mouse   2017 28321434160)
Other methods
Bone marrow stromal cells Renal proximal tubular epithelial cells HK2 cell-extracts treatment + streptolysin O Human YES 2015 25754206161)
Embryonic fibroblasts Cardiomyocytes Gata4, Hand2, Mef2c, and Tbx5 + miR-1 and miR-133 + TGFβ inhibitors or ROCK inhibitors Mouse   2015 26354680162)
Pancreatic exocrine cells β cells Pdx1, Ngn3, and Mafa (synthetic mRNA transfection) + 5-Aza treatment Mouse   2016 27187823163)
Neonatal cardiac and tail-tip fibroblasts Cardiomyocytes miR-1, miR-133, miR-208, and miR-499 + three-dimensional culture Mouse   2016 27941896164)
Neonatal cardiac and tail-tip fibroblasts Cardiomyocytes miR-1, miR-133, miR-208, and miR-499 + Reprogramming medium Mouse   2016 26975336165)
Adipose-derived stem cells and Neonatal foreskin fibroblasts Neural stem cells iPSC induction followed by TRA-1-60–/SSEA4–selection Human YES 2016 27569063166)
Fibroblasts Adipocytes OCT4 and C/EBPB (protein transduction with HVJ-E) + Adipogenic differentiation medium Human   2017 2858733162)