Abstract
We identified a novel gene, Ks-1, which is expressed preferentially in the small-type Kenyon cells of the honeybee brain. This gene is also expressed in some of the large soma neurons in the brain and in the suboesophageal ganglion. Reverse transcription-polymerase chain reaction experiments indicated that Ks-1 transcripts are enriched in the honeybee brain. cDNA cloning revealed that the consensus Ks-1 cDNA is over 17 kbp and contains no significant open reading frames. Furthermore, fluorescent in situ hybridization revealed that Ks-1 transcripts are located in the nuclei of the neural cells, accumulating in some scattered spots. These findings demonstrate that Ks-1 encodes a novel class of noncoding nuclear RNA and is possibly involved in the regulation of neural functions.
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- Akhtar A., Becker P. B. Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol Cell. 2000 Feb;5(2):367–375. doi: 10.1016/s1097-2765(00)80431-1. [DOI] [PubMed] [Google Scholar]
- Amrein H., Axel R. Genes expressed in neurons of adult male Drosophila. Cell. 1997 Feb 21;88(4):459–469. doi: 10.1016/s0092-8674(00)81886-3. [DOI] [PubMed] [Google Scholar]
- Bohmann K., Ferreira J., Santama N., Weis K., Lamond A. I. Molecular analysis of the coiled body. J Cell Sci Suppl. 1995;19:107–113. doi: 10.1242/jcs.1995.supplement_19.16. [DOI] [PubMed] [Google Scholar]
- Brown C. J., Hendrich B. D., Rupert J. L., Lafrenière R. G., Xing Y., Lawrence J., Willard H. F. The human XIST gene: analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell. 1992 Oct 30;71(3):527–542. doi: 10.1016/0092-8674(92)90520-m. [DOI] [PubMed] [Google Scholar]
- Carmo-Fonseca M., Pepperkok R., Carvalho M. T., Lamond A. I. Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J Cell Biol. 1992 Apr;117(1):1–14. doi: 10.1083/jcb.117.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis R. L. Physiology and biochemistry of Drosophila learning mutants. Physiol Rev. 1996 Apr;76(2):299–317. doi: 10.1152/physrev.1996.76.2.299. [DOI] [PubMed] [Google Scholar]
- Doucas V. The promyelocytic (PML) nuclear compartment and transcription control. Biochem Pharmacol. 2000 Oct 15;60(8):1197–1201. doi: 10.1016/s0006-2952(00)00413-5. [DOI] [PubMed] [Google Scholar]
- Eddy S. R. Noncoding RNA genes. Curr Opin Genet Dev. 1999 Dec;9(6):695–699. doi: 10.1016/s0959-437x(99)00022-2. [DOI] [PubMed] [Google Scholar]
- Eichmüller S., Hammer M., Schäfer S. Neurosecretory cells in the honeybee brain and suboesophageal ganglion show FMRFamide-like immunoreactivity. J Comp Neurol. 1991 Oct 1;312(1):164–174. doi: 10.1002/cne.903120112. [DOI] [PubMed] [Google Scholar]
- Gilbert S. L., Sharp P. A. Promoter-specific hypoacetylation of X-inactivated genes. Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13825–13830. doi: 10.1073/pnas.96.24.13825. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heard E., Clerc P., Avner P. X-chromosome inactivation in mammals. Annu Rev Genet. 1997;31:571–610. doi: 10.1146/annurev.genet.31.1.571. [DOI] [PubMed] [Google Scholar]
- Heisenberg M., Borst A., Wagner S., Byers D. Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet. 1985 Feb;2(1):1–30. doi: 10.3109/01677068509100140. [DOI] [PubMed] [Google Scholar]
- Heisenberg M. What do the mushroom bodies do for the insect brain? an introduction. Learn Mem. 1998 May-Jun;5(1-2):1–10. [PMC free article] [PubMed] [Google Scholar]
- Hong Y. K., Ontiveros S. D., Strauss W. M. A revision of the human XIST gene organization and structural comparison with mouse Xist. Mamm Genome. 2000 Mar;11(3):220–224. doi: 10.1007/s003350010040. [DOI] [PubMed] [Google Scholar]
- Kamikouchi A., Takeuchi H., Sawata M., Natori S., Kubo T. Concentrated expression of Ca2+/ calmodulin-dependent protein kinase II and protein kinase C in the mushroom bodies of the brain of the honeybee Apis mellifera L. J Comp Neurol. 2000 Feb 21;417(4):501–510. doi: 10.1002/(sici)1096-9861(20000221)417:4<501::aid-cne8>3.0.co;2-4. [DOI] [PubMed] [Google Scholar]
- Kamikouchi A., Takeuchi H., Sawata M., Ohashi K., Natori S., Kubo T. Preferential expression of the gene for a putative inositol 1,4,5-trisphosphate receptor homologue in the mushroom bodies of the brain of the worker honeybee Apis mellifera L. Biochem Biophys Res Commun. 1998 Jan 6;242(1):181–186. doi: 10.1006/bbrc.1997.7870. [DOI] [PubMed] [Google Scholar]
- Kelley R. L., Kuroda M. I. Noncoding RNA genes in dosage compensation and imprinting. Cell. 2000 Sep 29;103(1):9–12. doi: 10.1016/s0092-8674(00)00099-4. [DOI] [PubMed] [Google Scholar]
- Koken M. H., Puvion-Dutilleul F., Guillemin M. C., Viron A., Linares-Cruz G., Stuurman N., de Jong L., Szostecki C., Calvo F., Chomienne C. The t(15;17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 1994 Mar 1;13(5):1073–1083. doi: 10.1002/j.1460-2075.1994.tb06356.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kozak M. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 1987 Oct 26;15(20):8125–8148. doi: 10.1093/nar/15.20.8125. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kucharski R., Maleszka R., Hayward D. C., Ball E. E. A royal jelly protein is expressed in a subset of Kenyon cells in the mushroom bodies of the honey bee brain. Naturwissenschaften. 1998 Jul;85(7):343–346. doi: 10.1007/s001140050512. [DOI] [PubMed] [Google Scholar]
- Lamond A. I., Earnshaw W. C. Structure and function in the nucleus. Science. 1998 Apr 24;280(5363):547–553. doi: 10.1126/science.280.5363.547. [DOI] [PubMed] [Google Scholar]
- Li Y., Strausfeld N. J. Morphology and sensory modality of mushroom body extrinsic neurons in the brain of the cockroach, Periplaneta americana. J Comp Neurol. 1997 Nov 3;387(4):631–650. [PubMed] [Google Scholar]
- Matera A. G. Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends Cell Biol. 1999 Aug;9(8):302–309. doi: 10.1016/s0962-8924(99)01606-2. [DOI] [PubMed] [Google Scholar]
- Meller V. H. Dosage compensation: making 1X equal 2X. Trends Cell Biol. 2000 Feb;10(2):54–59. doi: 10.1016/s0962-8924(99)01693-1. [DOI] [PubMed] [Google Scholar]
- Meller V. H., Gordadze P. R., Park Y., Chu X., Stuckenholz C., Kelley R. L., Kuroda M. I. Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila. Curr Biol. 2000 Feb 10;10(3):136–143. doi: 10.1016/s0960-9822(00)00311-0. [DOI] [PubMed] [Google Scholar]
- Meller V. H., Wu K. H., Roman G., Kuroda M. I., Davis R. L. roX1 RNA paints the X chromosome of male Drosophila and is regulated by the dosage compensation system. Cell. 1997 Feb 21;88(4):445–457. doi: 10.1016/s0092-8674(00)81885-1. [DOI] [PubMed] [Google Scholar]
- Miura T., Kamikouchi A., Sawata M., Takeuchi H., Natori S., Kubo T., Matsumoto T. Soldier caste-specific gene expression in the mandibular glands of Hodotermopsis japonica (Isoptera: termopsidae). Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13874–13879. doi: 10.1073/pnas.96.24.13874. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mizunami M., Iwasaki M., Okada R., Nishikawa M. Topography of four classes of Kenyon cells in the mushroom bodies of the cockroach. J Comp Neurol. 1998 Sep 21;399(2):162–175. doi: 10.1002/(sici)1096-9861(19980921)399:2<162::aid-cne2>3.0.co;2-z. [DOI] [PubMed] [Google Scholar]
- Mizunami M., Okada R., Li Y., Strausfeld N. J. Mushroom bodies of the cockroach: activity and identities of neurons recorded in freely moving animals. J Comp Neurol. 1998 Dec 28;402(4):501–519. [PubMed] [Google Scholar]
- Mizunami M., Weibrecht J. M., Strausfeld N. J. Mushroom bodies of the cockroach: their participation in place memory. J Comp Neurol. 1998 Dec 28;402(4):520–537. [PubMed] [Google Scholar]
- Mutsuddi M., Lakhotia S. C. Spatial expression of the hsr-omega (93D) gene in different tissues of Drosophila melanogaster and identification of promoter elements controlling its developmental expression. Dev Genet. 1995;17(4):303–311. doi: 10.1002/dvg.1020170403. [DOI] [PubMed] [Google Scholar]
- Ohashi K., Sawata M., Takeuchi H., Natori S., Kubo T. Molecular cloning of cDNA and analysis of expression of the gene for alpha-glucosidase from the hypopharyngeal gland of the honeybee Apis mellifera L. Biochem Biophys Res Commun. 1996 Apr 16;221(2):380–385. doi: 10.1006/bbrc.1996.0604. [DOI] [PubMed] [Google Scholar]
- Platero J. S., Hartnett T., Eissenberg J. C. Functional analysis of the chromo domain of HP1. EMBO J. 1995 Aug 15;14(16):3977–3986. doi: 10.1002/j.1460-2075.1995.tb00069.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prasanth K. V., Rajendra T. K., Lal A. K., Lakhotia S. C. Omega speckles - a novel class of nuclear speckles containing hnRNPs associated with noncoding hsr-omega RNA in Drosophila. J Cell Sci. 2000 Oct;113(Pt 19):3485–3497. doi: 10.1242/jcs.113.19.3485. [DOI] [PubMed] [Google Scholar]
- Redies C. Cadherins in the central nervous system. Prog Neurobiol. 2000 Aug;61(6):611–648. doi: 10.1016/s0301-0082(99)00070-2. [DOI] [PubMed] [Google Scholar]
- Robinson G. E., Strambi A., Strambi C., Paulino-Simões Z. L., Tozeto S. O., Barbosa J. M. Juvenile hormone titers in European and Africanized honey bees in Brazil. Gen Comp Endocrinol. 1987 Jun;66(3):457–459. doi: 10.1016/0016-6480(87)90258-9. [DOI] [PubMed] [Google Scholar]
- Robinson K. O., Ferguson H. J., Cobey S., Vaessin H., Smith B. H. Sperm-mediated transformation of the honey bee, Apis mellifera. Insect Mol Biol. 2000 Dec;9(6):625–634. doi: 10.1046/j.1365-2583.2000.00225.x. [DOI] [PubMed] [Google Scholar]
- Rybak J., Menzel R. Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol. 1993 Aug 15;334(3):444–465. doi: 10.1002/cne.903340309. [DOI] [PubMed] [Google Scholar]
- Satijn D. P., Gunster M. J., van der Vlag J., Hamer K. M., Schul W., Alkema M. J., Saurin A. J., Freemont P. S., van Driel R., Otte A. P. RING1 is associated with the polycomb group protein complex and acts as a transcriptional repressor. Mol Cell Biol. 1997 Jul;17(7):4105–4113. doi: 10.1128/mcb.17.7.4105. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schürmann F. W., Ottersen O. P., Honegger H. W. Glutamate-like immunoreactivity marks compartments of the mushroom bodies in the brain of the cricket. J Comp Neurol. 2000 Mar 6;418(2):227–239. [PubMed] [Google Scholar]
- Smith E. R., Pannuti A., Gu W., Steurnagel A., Cook R. G., Allis C. D., Lucchesi J. C. The drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol Cell Biol. 2000 Jan;20(1):312–318. doi: 10.1128/mcb.20.1.312-318.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Spector D. L. Macromolecular domains within the cell nucleus. Annu Rev Cell Biol. 1993;9:265–315. doi: 10.1146/annurev.cb.09.110193.001405. [DOI] [PubMed] [Google Scholar]
- Spector D. L. Nuclear organization and gene expression. Exp Cell Res. 1996 Dec 15;229(2):189–197. doi: 10.1006/excr.1996.0358. [DOI] [PubMed] [Google Scholar]
- Strausfeld N. J., Hansen L., Li Y., Gomez R. S., Ito K. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem. 1998 May-Jun;5(1-2):11–37. [PMC free article] [PubMed] [Google Scholar]
- Strausfeld N. J., Homberg U., Kloppenburg P., Homburg U., Kloppenberg P. Parallel organization in honey bee mushroom bodies by peptidergic Kenyon cells. J Comp Neurol. 2000 Aug 14;424(1):179–195. [PubMed] [Google Scholar]
- Takeuchi H., Kage E., Sawata M., Kamikouchi A., Ohashi K., Ohara M., Fujiyuki T., Kunieda T., Sekimizu K., Natori S. Identification of a novel gene, Mblk-1, that encodes a putative transcription factor expressed preferentially in the large-type Kenyon cells of the honeybee brain. Insect Mol Biol. 2001 Oct;10(5):487–494. doi: 10.1046/j.0962-1075.2001.00288.x. [DOI] [PubMed] [Google Scholar]
- Wang Y., Zhang W., Jin Y., Johansen J., Johansen K. M. The JIL-1 tandem kinase mediates histone H3 phosphorylation and is required for maintenance of chromatin structure in Drosophila. Cell. 2001 May 18;105(4):433–443. doi: 10.1016/s0092-8674(01)00325-7. [DOI] [PubMed] [Google Scholar]
- Withers G. S., Fahrbach S. E., Robinson G. E. Selective neuroanatomical plasticity and division of labour in the honeybee. Nature. 1993 Jul 15;364(6434):238–240. doi: 10.1038/364238a0. [DOI] [PubMed] [Google Scholar]
- Yang M. Y., Armstrong J. D., Vilinsky I., Strausfeld N. J., Kaiser K. Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron. 1995 Jul;15(1):45–54. doi: 10.1016/0896-6273(95)90063-2. [DOI] [PubMed] [Google Scholar]
- Zeng C., Kim E., Warren S. L., Berget S. M. Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J. 1997 Mar 17;16(6):1401–1412. doi: 10.1093/emboj/16.6.1401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Belle J. S., Heisenberg M. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science. 1994 Feb 4;263(5147):692–695. doi: 10.1126/science.8303280. [DOI] [PubMed] [Google Scholar]