Abstract
Genomic imprinting is an epigenetic phenomenon that results in differential expression of both alleles, depending on their parent of origin. We have recently identified many imprinted small non-coding RNA genes belonging to the C/D RNA and microRNA gene families, both of which are usually known to play key roles in post-transcriptional metabolism of specific genes (e.g. C/D RNAs guide ribose methylation of target RNAs while microRNAs elicit either translational repression or RNA interference). Although the functional and evolutionary significance of this association between C/D RNA genes, microRNA genes and genomic imprinting is still highly elusive, these observations provide a framework for further analysis of the potential role of small non-coding RNAs in epigenetic control.
References
Bachellerie, J. P., Cavaille, J., and Hüttenhofer, A. (2002). The expanding snoRNA world. Biochimie84, 775–790.10.1016/S0300-9084(02)01402-5Search in Google Scholar
Barlow, D. P. (1993). Methylation and imprinting: from host defense to gene regulation? Science260, 309–310.10.1126/science.8469984Search in Google Scholar
Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell116, 281–297.10.1016/S0092-8674(04)00045-5Search in Google Scholar
Bird, A. (1997). Does DNA methylation control transposition of selfish elements in the germline? Trends Genet.13, 469–472.Search in Google Scholar
Burns, C. M., Chu, H., Rueter, S. M., Hutchinson, L. K., Canton, H., Sanders-Bush, E., and Emeson, R. B. (1997). Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature387, 303–308.10.1038/387303a0Search in Google Scholar PubMed
Cavaille, J., and Bachellerie, J. P. (1998). SnoRNA-guided ribose methylation of rRNA: structural features of the guide RNA duplex influencing the extent of the reaction. Nucleic Acids Res.26, 1576–1587.10.1093/nar/26.7.1576Search in Google Scholar PubMed PubMed Central
Cavaille, J., Buiting, K., Kiefmann, M., Lalande, M., Brannan, C. I., Horsthemke, B., Bachellerie, J. P., Brosius, J., and Hüttenhofer, A. (2000). Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. Proc. Natl. Acad. Sci. USA97, 14311–14316.10.1073/pnas.250426397Search in Google Scholar PubMed PubMed Central
Cavaille, J., Vitali, P., Basyuk, E., Hüttenhofer, A., and Bachellerie, J. P. (2001). A novel brain-specific box C/D small nucleolar RNA processed from tandemly repeated introns of a noncoding RNA gene in rats. J. Biol. Chem.276, 26374–26383.10.1074/jbc.M103544200Search in Google Scholar PubMed
Cavaille, J., Seitz, H., Paulsen, M., Ferguson-Smith, A. C., and Bachellerie, J. P. (2002). Identification of tandemly-repeated C/D snoRNA genes at the imprinted human 14q32 domain reminiscent of those at the Prader-Willi/Angelman syndrome region. Hum. Mol. Genet.11, 1527–1538.10.1093/hmg/11.13.1527Search in Google Scholar PubMed
Chai, J. H., Locke, D. P., Ohta, T., Greally, J. M., and Nicholls, R. D. (2001). Retrotransposed genes such as Frat3 in the mouse chromosome 7C Prader-Willi syndrome region acquire the imprinted status of their insertion site. Mamm. Genome12, 813–821.10.1007/s00335-001-2083-1Search in Google Scholar PubMed
Chamberlain, S. J., and Brannan, C. I. (2001). The Prader-Willi syndrome imprinting center activates the paternally expressed murine Ube3a antisense transcript but represses paternal Ube3a. Genomics73, 316–322.10.1006/geno.2001.6543Search in Google Scholar PubMed
Charlier, C., Segers, K., Karim, L., Shay, T., Gyapay, G., Cockett, N., and Georges, M. (2001a). The callipyge mutation enhances the expression of coregulated imprinted genes in cis without affecting their imprinting status. Nat. Genet.27, 367–369.10.1038/86856Search in Google Scholar
Charlier, C., Segers, K., Wagenaar, D., Karim, L., Berghmans, S., Jaillon, O., Shay, T., Weissenbach, J., Cockett, N., Gyapay, G., and Georges, M. (2001b). Human-ovine comparative sequencing of a 250–kb imprinted domain encompassing the callipyge (clpg) locus and identification of six imprinted transcripts: DLK1, DAT, GTL2, PEG11, antiPEG11, and MEG8. Genome Res.11, 850–862.10.1101/gr.172701Search in Google Scholar
de los Santos, T., Schweizer, J., Rees, C. A., and Francke, U. (2000). Small evolutionarily conserved RNA, resembling C/D box small nucleolar RNA, is transcribed from PWCR1, a novel imprinted gene in the Prader-Willi deletion region, which Is highly expressed in brain. Am. J. Hum. Genet.67, 1067–1082.10.1086/303106Search in Google Scholar
Freking, B. A., Murphy, S. K., Wylie, A. A., Rhodes, S. J., Keele, J. W., Leymaster, K. A., Jirtle, R. L., and Smith, T. P. (2002). Identification of the single base change causing the callipyge muscle hypertrophy phenotype, the only known example of polar overdominance in mammals. Genome Res.12, 1496–1506.10.1101/gr.571002Search in Google Scholar
Gallagher, R. C., Pils, B., Albalwi, M., and Francke, U. (2002). Evidence for the role of PWCR1/HBII-85 C/D box small nucleolar RNAs in Prader-Willi syndrome. Am. J. Hum. Genet.71, 669–678.10.1086/342408Search in Google Scholar
Georges, M., Charlier, C., and Cockett, N. (2003). The callipyge locus: evidence for the trans interaction of reciprocally imprinted genes. Trends Genet.19, 248–252.10.1016/S0168-9525(03)00082-9Search in Google Scholar
Georgiades, P., Watkins, M., Surani, M. A., and Ferguson-Smith, A. C. (2000). Parental origin-specific developmental defects in mice with uniparental disomy for chromosome 12. Development127, 4719–4728.10.1242/dev.127.21.4719Search in Google Scholar
Grewal, S. I., and Rice, J. C. (2004). Regulation of heterochromatin by histone methylation and small RNAs. Curr. Opin. Cell Biol.16, 230–238.10.1016/j.ceb.2004.04.002Search in Google Scholar
Gribnau, J., Diderich, K., Pruzina, S., Calzolari, R., and Fraser, P. (2000). Intergenic transcription and developmental remodeling of chromatin subdomains in the human b-globin locus. Mol. Cell5, 377–386.10.1016/S1097-2765(00)80432-3Search in Google Scholar
Hüttenhofer, A., Kiefmann, M., Meier-Ewert, S., O’Brien, J., Lehrach, H., Bachellerie, J. P., and Brosius, J. (2001). RNomics: an experimental approach that identifies 201 candidates for novel, small, non-messenger RNAs in mouse. EMBO J.20, 2943–2953.10.1093/emboj/20.11.2943Search in Google Scholar PubMed PubMed Central
Johnson, D. K., Stubbs, L. J., Culiat, C. T., Montgomery, C. S., Russell, L. B., and Rinchik, E. M. (1995). Molecular analysis of 36 mutations at the mouse pink-eyed dilution (p) locus. Genetics141, 1563–1571.10.1093/genetics/141.4.1563Search in Google Scholar
Killian, J. K., Byrd, J. C., Jirtle, J. V., Munday, B. L., Stoskopf, M. K., MacDonald, R. G., and Jirtle, R. L. (2000). M6P/IGF2R imprinting evolution in mammals. Mol.Cell5, 707–716.10.1016/S1097-2765(00)80249-XSearch in Google Scholar
Kiss, T. (2001). Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs. EMBO J.20, 3617–3622.10.1093/emboj/20.14.3617Search in Google Scholar
Komine, Y., Tanaka, N. K., Yano, R., Takai, S., Yuasa, S., Shiroishi, T., Tsuchiya, K., and Yamamori, T. (1999). A novel type of non-coding RNA expressed in the rat brain. Brain Res. Mol. Brain Res.66, 1–13.10.1016/S0169-328X(98)00343-XSearch in Google Scholar
Lai, E. C. (2003). microRNAs: runts of the genome assert themselves. Curr. Biol.13, R925–936.10.1016/j.cub.2003.11.017Search in Google Scholar
Lin, S. P., Youngson, N., Takada, S., Seitz, H., Reik, W., Paulsen, M., Cavaille, J., and Ferguson-Smith, A. C. (2003). Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1–Gtl2 imprinted cluster on mouse chromosome 12. Nat. Genet.35, 97–102.10.1038/ng1233Search in Google Scholar
Lynch, C., and Tristem, M. (2003). A co-opted gypsy-type LTR-retrotransposon is conserved in the genomes of humans, sheep, mice, and rats. Curr. Biol.13, 1518–1523.10.1016/S0960-9822(03)00618-3Search in Google Scholar
Martens, J. A., Laprade, L., and Winston, F. (2004). Intergenic transcription is required to repress the Saccharomyces cerevisiae SER3 gene. Nature429, 571–574.10.1038/nature02538Search in Google Scholar
Martienssen, R. (1998). Transposons, DNA methylation and gene control. Trends Genet.14, 263–264.10.1016/S0168-9525(98)01518-2Search in Google Scholar
Matzke, M., Aufsatz, W., Kanno, T., Daxinger, L., Papp, I., Mette, M. F., and Matzke, A. J. (2004). Genetic analysis of RNA-mediated transcriptional gene silencing. Biochim. Biophys. Acta1677, 129–141.10.1016/j.bbaexp.2003.10.015Search in Google Scholar PubMed
Meguro, M., Mitsuya, K., Nomura, N., Kohda, M., Kashiwagi, A., Nishigaki, R., Yoshioka, H., Nakao, M., Oishi, M., and Oshimura, M. (2001). Large-scale evaluation of imprinting status in the Prader-Willi syndrome region: an imprinted direct repeat cluster resembling small nucleolar RNA genes. Hum. Mol. Genet.10, 383–394.10.1093/hmg/10.4.383Search in Google Scholar
Mette, M. F., van der Winden, J., Matzke, M., and Matzke, A. J. (2002). Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiol.130, 6–9.10.1104/pp.007047Search in Google Scholar
Nicholls, R. D., and Knepper, J. L. (2001). Genome organization, function, and imprinting in Prader-Willi and Angelman syndromes. Annu. Rev. Genomics Hum. Genet.2, 153–175.10.1146/annurev.genom.2.1.153Search in Google Scholar
Reik, W., and Walter, J. (2001). Genomic imprinting: parental influence on the genome. Nat. Rev. Genet.2, 21–32.10.1038/35047554Search in Google Scholar
Rougeulle, C., Cardoso, C., Fontes, M., Colleaux, L., and Lalande, M. (1998). An imprinted antisense RNA overlaps UBE3A and a second maternally expressed transcript. Nat. Genet.19, 15–16.10.1038/ng0598-15Search in Google Scholar
Runte, M., Hüttenhofer, A., Gross, S., Kiefmann, M., Horsthemke, B., and Buiting, K. (2001). The IC-SNURF-SNRPN transcript serves as a host for multiple small nucleolar RNA species and as an antisense RNA for UBE3A. Hum. Mol. Genet.10, 2687–2700.10.1093/hmg/10.23.2687Search in Google Scholar
Seitz, H., Youngson, N., Lin, S. P., Dalbert, S., Paulsen, M., Bachellerie, J. P., Ferguson-Smith, A. C., and Cavaille, J. (2003). Imprinted microRNA genes transcribed antisense to a reciprocally imprinted retrotransposon-like gene. Nat. Genet.34, 261–262.10.1038/ng1171Search in Google Scholar
Seitz, H., Royo, H., Bortolin, M. L., Lin, S. P., Ferguson-Smith, A. C., and Cavaille, J. (2004). A large imprinted microRNA gene cluster at the mouse Dlk1–Gtl2 domain. Genome Res.14, 1741–1748.10.1101/gr.2743304Search in Google Scholar
Sleutels, F., and Barlow, D. P. (2002). The origins of genomic imprinting in mammals. Adv. Genet.46, 119–163.10.1016/S0065-2660(02)46006-3Search in Google Scholar
Sleutels, F., Zwart, R., and Barlow, D. P. (2002). The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature415, 810–813.10.1038/415810aSearch in Google Scholar PubMed
Smit, M., Segers, K., Carrascosa, L. G., Shay, T., Baraldi, F., Gyapay, G., Snowder, G., Georges, M., Cockett, N., and Charlier, C. (2003). Mosaicism of Solid Gold supports the causality of a noncoding A-to-G transition in the determinism of the callipyge phenotype. Genetics163, 453–456.10.1093/genetics/163.1.453Search in Google Scholar
Takada, S., Paulsen, M., Tevendale, M., Tsai, C. E., Kelsey, G., Cattanach, B. M., and Ferguson-Smith, A. C. (2002). Epigenetic analysis of the Dlk1–Gtl2 imprinted domain on mouse chromosome 12: implications for imprinting control from comparison with Igf2–H19. Hum. Mol. Genet.11, 77–86.10.1093/hmg/11.1.77Search in Google Scholar
Tsai, T. F., Jiang, Y. H., Bressler, J., Armstrong, D., and Beaudet, A. L. (1999). Paternal deletion from Snrpn to Ube3a in the mouse causes hypotonia, growth retardation and partial lethality and provides evidence for a gene contributing to Prader-Willi syndrome. Hum. Mol. Genet.8, 1357–1364.10.1093/hmg/8.8.1357Search in Google Scholar
Verona, R. I., Mann, M. R., and Bartolomei, M. S. (2003). Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu. Rev. Cell. Dev. Biol.19, 237–259.10.1146/annurev.cellbio.19.111401.092717Search in Google Scholar
Whitelaw, E., and Martin, D. I. (2001). Retrotransposons as epigenetic mediators of phenotypic variation in mammals. Nat. Genet.27, 361–365.10.1038/86850Search in Google Scholar
Wilkins, J. F., and Haig, D. (2003). What good is genomic imprinting: the function of parent-specific gene expression. Nat. Rev. Genet.4, 359–368.10.1038/nrg1062Search in Google Scholar
Wirth, J., Back, E., Huttenhofer, A., Nothwang, H. G., Lich, C., Gross, S., Menzel, C., Schinzel, A., Kioschis, P., Tommerup, N. et al. (2001). A translocation breakpoint cluster disrupts the newly defined 3′ end of the SNURF-SNRPN transcription unit on chromosome 15. Hum. Mol. Genet.10, 201–210.10.1093/hmg/10.3.201Search in Google Scholar
Yekta, S., Shih, I. H., and Bartel, D. P. (2004). MicroRNA-directed cleavage of HOXB8 mRNA. Science304, 594–596.10.1126/science.1097434Search in Google Scholar
Yi-Brunozzi, H. Y., Easterwood, L. M., Kamilar, G. M., and Beal, P. A. (1999). Synthetic substrate analogs for the RNA-editing adenosine deaminase ADAR-2. Nucleic Acids Res.27, 2912–2917.10.1093/nar/27.14.2912Search in Google Scholar
Yoder, J. A., Walsh, C. P., and Bestor, T. H. (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet.13, 335–340.10.1016/S0168-9525(97)01181-5Search in Google Scholar
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