Imprinted expression of UBE3A in non-neuronal cells from a Prader-willi syndrome patient with an atypical deletion

Human Molecular Genetics

Volumn 23, Issue 9, 2014, Pages 2364-2373

  Martins Taylor, Kristen ^a   Hsiao, Jack S ^a   Chen, Pin Fang ^a   Glatt Deeley, Heather ^a   De Smith, Adam J ^b   Blakemore, Alexandra I F ^b   Lalande, Marc ^a   Chamberlain, Stormy J ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL NUCLEOLAR RNA; UBIQUITIN LIGASE E3A; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; UNTRANSLATED RNA; UBE3A PROTEIN, HUMAN;

ARTICLE; CELL LINE; CHROMOSOME 15Q; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; FIBROBLAST; GENE; GENE DELETION; GENE EXPRESSION; GENETIC DISORDER; GENOME IMPRINTING; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; NERVE CELL; NEUROLOGIC DISEASE; PLURIPOTENT STEM CELL; PRADER WILLI SYNDROME; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SNORD116 GENE; UBE3A ATS GENE; UBE3A GENE; GENETICS; HAPPY PUPPET SYNDROME; IMMUNOHISTOCHEMISTRY; METABOLISM;

ANGELMAN SYNDROME; CELL LINE; HUMANS; IMMUNOHISTOCHEMISTRY; INDUCED PLURIPOTENT STEM CELLS; PRADER-WILLI SYNDROME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE DELETION; UBIQUITIN-PROTEIN LIGASES;

EID: 84897476311     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt628     Document Type: Article

References (34)

1. Cassidy, S.B., Dykens, E. and Williams, C.A. (2000) Prader-Willi and Angelman syndromes: sister imprinted disorders. Am. J. Med. Genet., 97, 136-146.
2. Williams, C.A., Beaudet, A.L., Clayton-Smith, J., Knoll, J.H., Kyllerman, M., Laan, L.A., Magenis, R.E., Moncla, A., Schinzel, A.A., Summers, J.A. et al. (2006) Angelman syndrome 2005: updated consensus for diagnostic criteria. Am. J. Med. Genet. A, 140, 413-418.
3. Miller, J.L., Lynn, C.H., Driscoll, D.C., Goldstone, A.P., Gold, J.A., Kimonis, V., Dykens, E., Butler, M.G., Shuster, J.J., Driscoll, D.J. (2011) Nutritional phases in Prader-Willi syndrome. Am. J. Med. Genet. Part A., 155A, 1040-1049.
4. Cassidy, S.B. and Driscoll, D.J. (2009) Prader-Willi syndrome. Eur. J. Hum. Genet., 17, 3-13.
5. Reis, A., Dittrich, B., Greger, V., Buiting, K., Lalande, M., Gillessen-Kaesbach, G., Anvret, M. and Horsthemke, B. (1994) Imprinting mutations suggested by abnormal DNA methylation patterns in familial Angelman and Prader-Willi syndromes. Am. J. Hum. Genet., 54, 741-747.
6. Saitoh, S., Buiting, K., Rogan, P.K., Buxton, J.L., Driscoll, D.J., Arnemann, J., Konig, R., Malcolm, S., Horsthemke, B. and Nicholls, R.D. (1996) Minimal definition of the imprinting center and fixation of chromosome 15q11-q13 epigenotype by imprinting mutations. Proc. Natl. Acad. Sci. USA., 93, 7811-7815.
7. Jong, M.T., Carey, A.H., Caldwell, K.A., Lau, M.H., Handel, M.A., Driscoll, D.J., Stewart, C.L., Rinchik, E.M. and Nicholls, R.D. (1999) Imprinting of a RINGzinc-finger encoding gene in themouse chromosomeregion homologous to the Prader-Willi syndrome genetic region. Hum. Mol. Genet., 8, 795-803.
8. Boccaccio, I., Glatt-Deeley, H., Watrin, F., Roeckel, N., Lalande, M. and Muscatelli, F. (1999) The human MAGEL2 gene and its mouse homologue are paternally expressed and mapped to the Prader-Willi region. Hum. Mol. Genet., 8, 2497-2505.
9. Jay, P., Rougeulle, C., Massacrier, A., Moncla, A., Mattei, M.G., Malzac, P., Roeckel, N., Taviaux, S., Lefranc, J.L., Cau, P. et al. (1997) The human necdin gene, NDN, is maternally imprinted and located in the Prader-Willi syndrome chromosomal region. Nat. Genet., 17, 357-361.
10. Buiting, K., Nazlican, H., Galetzka, D., Wawrzik, M., Gross, S. and Horsthemke, B. (2007) C15orf2 and a novel noncoding transcript from the Prader-Willi/Angelman syndrome region show monoallelic expression in fetal brain. Genomics., 89, 588-595.
11. Cattanach, B.M., Barr, J.A., Evans, E.P., Burtenshaw, M., Beechey, C.V., Leff, S.E., Brannan, C.I., Copeland, N.G., Jenkins, N.A. and Jones, J. (1992) A candidate mouse model for Prader-Willi syndrome which shows an absence of Snrpn expression. Nat. Genet., 2, 270-274.
12. Glenn, C.C., Porter, K.A., Jong, M.T., Nicholls, R.D. and Driscoll, D.J. (1993) Functional imprinting and epigenetic modification of the human SNRPN gene. Hum. Mol. Genet., 2, 2001-2005.
13. Runte, M., Huttenhofer, A., Gross, S., Kiefmann, M., Horsthemke, B. and Buiting, K. (2001) The IC-SNURF-SNRPN transcript serves as a host for multiple small nucleolarRNAspecies and as an antisenseRNAfor UBE3A. Hum. Mol. Genet., 10, 2687-2700.
14. Cavaille, J., Buiting, K., Kiefmann, M., Lalande, M., Brannan, C.I., Horsthemke, B., Bachellerie, J.P., Brosius, J. and Huttenhofer, A. (2000) Identification of brain-specific and imprinted small nucleolar RNA genes exhibiting an unusual genomic organization. Proc. Natl. Acad. Sci. USA., 97, 14311-14316.
15. Wevrick, R., Kerns, J.A. and Francke, U. (1994) Identification of a Novel Paternally Expressed Gene in the Prader-Willi-Syndrome Region. Hum. Mol. Genet., 3, 1877-1882.
16. 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.
17. Chamberlain, S.J., Chen, P.F., Ng, K.Y., Bourgois-Rocha, F., Lemtiri-Chlieh, F., Levine, E.S. and Lalande, M. (2010) Induced pluripotent stem cell models of the genomic imprinting disorders Angelman and Prader-Willi syndromes. Proc. Natl. Acad. Sci. USA., 107, 17668-17673.
18. Rougeulle, C., Glatt, H. and Lalande, M. (1997) The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brain. Nat. Genet., 17, 14-15.
19. Meng, L., Person, R.E. and Beaudet, A.L. (2012) Ube3a-ATS is an atypical RNA polymerase II transcript that represses the paternal expression of Ube3a. Hum. Mol. Genet., 21, 3001-3012.
20. Kishino, T., Lalande, M. and Wagstaff, J. (1997) UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet., 15, 70-73.
21. de Smith, A.J., Purmann, C., Walters, R.G., Ellis, R.J., Holder, S.E., Van Haelst, M.M., Brady, A.F., Fairbrother, U.L., Dattani, M., Keogh, J.M. et al. (2009)A deletion of the HBII-85 class of small nucleolar RNAs (snoRNAs) is associated with hyperphagia, obesity and hypogonadism. Hum. Mol. Genet., 18, 3257-3265.
22. Sahoo, T., del Gaudio, D., German, J.R., Shinawi, M., Peters, S.U., Person, R.E., Garnica, A., Cheung, S.W. and Beaudet, A.L. (2008) Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nat. Genet., 40, 719-721.
23. Duker, A.L., Ballif, B.C., Bawle, E.V., Person, R.E., Mahadevan, S., Alliman, S., Thompson, R., Traylor, R., Bejjani, B.A., Shaffer, L.G. et al. (2010) Paternally inherited microdeletion at 15q11.2 confirms a significant role for theSNORD116C/DboxsnoRNAcluster in Prader-Willi syndrome. Eur. J. Hum. Genet., 18, 1196-1201.
24. Somers, A., Jean, J.C., Sommer, C.A., Omari, A., Ford, C.C., Mills, J.A., Ying, L., Sommer, A.G., Jean, J.M., Smith, B.W. et al. (2010) Generation of transgene-free lung disease-specific human induced pluripotent stem cells using a single excisable lentiviral stem cell cassette. Stem Cells., 28, 1728-1740.
25. Bock, C., Kiskinis, E., Verstappen, G., Gu, H., Boulting, G., Smith, Z.D., Ziller, M., Croft, G.F., Amoroso, M.W., Oakley, D.H. et al. (2011) Reference Maps of human ES and iPS cell variation enable high-throughput characterization of pluripotent cell lines. Cell., 144, 439-452.
26. Landers, M., Bancescu, D.L., Le Meur, E., Rougeulle, C., Glatt-Deeley, H., Brannan, C., Muscatelli, F. and Lalande, M. (2004) Regulation of the large (approximately 1000 kb) imprinted murine Ube3a antisense transcript by alternative exons upstream of Snurf/Snrpn. Nuc. Acids Res., 32, 3480-3492.
27. Huang, H.S., Allen, J.A., Mabb, A.M., King, I.F., Miriyala, J., Taylor-Blake, B., Sciaky, N., Dutton, J.W. Jr, Lee, H.M., Chen, X. et al. (2012) Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons. Nature., 481, 185-189.
28. King, I.F., Yandava, C.N., Mabb, A.M., Hsiao, J.S., Huang, H.S., Pearson, B.L., Calabrese, J.M., Starmer, J., Parker, J.S., Magnuson, T. et al. (2013) Topoisomerases facilitate transcription of long genes linked to autism. Nature., 501, 58-62.
29. 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. Genomics., 73, 316-322.
30. Rougeulle, C., Navarro, P. and Avner, P. (2003) Promoter-restricted H3 Lys 4 di-methylation is an epigenetic mark for monoallelic expression. Hum. Mol. Genet., 12, 3343-3348.
31. Zeng, H., Guo, M., Martins-Taylor, K., Wang, X., Zhang, Z., Park, J.W., Zhan, S., Kronenberg, M.S., Lichtler, A., Liu, H.X. et al. (2010) Specification of region-specific neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells. PLoS One., 5, e11853.
32. Kishino, T. and Wagstaff, J. (1998) Genomic organization of the UBE3A/E6-AP gene and related pseudogenes. Genomics., 47, 101-107.
33. Germain, N.D., Banda, E.C., Becker, S., Naegele, J.R. and Grabel, L.B. (2013) Derivation and Isolation of NKX2.1-Positive Basal Forebrain Progenitors from Human Embryonic Stem Cells. Stem Cells Dev., 22, 1477-1489.
34. Farber, C., Dittrich, B., Buiting, K. and Horsthemke, B. (1999) The chromosome 15 imprinting centre (IC) region has undergone multiple duplication events and contains an upstream exon of SNRPN that is deleted in all Angelman syndrome patients with an IC microdeletion. Hum. Mol. Genet., 8, 337-343.