Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3

Human Molecular Genetics

Volumn 14, Issue 4, 2005, Pages 483-492

  Samaco, Rodney C ^a   Hogart, Amber ^a   LaSalle, Janine M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; DNA; METHYL CPG BINDING PROTEIN 2; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3A; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ALLELE; ANIMAL TISSUE; ARTICLE; AUTISM; AUTOMATION; BRAIN DEVELOPMENT; CHILD; CHROMOSOME 15Q; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOMETRY; DEVELOPMENTAL DISORDER; DNA MICROARRAY; EPIGENETICS; GENE CONSTRUCT; GENE EXPRESSION REGULATION; GENETIC SUSCEPTIBILITY; HAPPY PUPPET SYNDROME; HUMAN; HUMAN TISSUE; HYPOTHESIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEFICIENCY; QUANTITATIVE ANALYSIS; RETT SYNDROME; TRANSCRIPTION REGULATION; X CHROMOSOME LINKED DISORDER;

ANGELMAN SYNDROME; ANIMALS; AUTISTIC DISORDER; BRAIN; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOMES, HUMAN, PAIR 15; DNA-BINDING PROTEINS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOMIC IMPRINTING; HUMANS; IN SITU HYBRIDIZATION; LASER SCANNING CYTOMETRY; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; RECEPTORS, GABA-A; REPRESSOR PROTEINS; RETT SYNDROME; UBIQUITIN-PROTEIN LIGASES;

EID: 14044252235     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddi045     Document Type: Article

References (70)

1. Volkmar, F.R. and Pauls, D. (2003) Autism. Lancet, 362, 1133-1141.
2. Amir, R.E., Van den Veyver, I.B., Wan, M., Tran, C.Q., Francke, U. and Zoghbi, H.Y. (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl- CpG-binding protein 2. Nat. Genet., 23, 185-188.
3. Lalande, M. (1996) Parental imprinting and human disease. Annu. Rev. Genet., 30, 173-195.
4. Zoghbi, H.Y. (2003) Postnatal neurodevelopmental disorders: meeting at the synapse? Science, 302, 826-830.
5. Mount, R.H., Charman, T., Hastings, R.P., Reilly, S. and Cass, H. (2003) Features of autism in Rett syndrome and severe mental retardation. J. Autism Dev. Disord., 33, 435-442.
6. Peters, S.U., Beaudet, A.L., Madduri, N. and Bacino, C.A. (2004) Autism in Angelman syndrome: implications for autism research. Clin. Genet., 66, 530-536.
7. Moretti, P., Bouwknecht, J.A., Teague, R., Paylor, R. and Zoghbi, H.Y. (2005) Abnormalities of social interactions and home cage behavior in a mouse model of Rett syndrome. Hum. Mol. Genet., 14 205-220.
8. Watson, P., Black, G., Ramsden, S., Barrow, M., Super, M., Kerr, B. and Clayton-Smith, J. (2001) Angelman syndrome phenotype associated with mutations in MECP2, a gene encoding a methyl CpG binding protein. J. Med. Genet., 38, 224-228.
9. Lam, C., Yeung, W., Ko, C., Poon, P., Tong, S., Chan, K., Lo, I., Chan, L., Hui, J., Wong, V. et al. (2000) Spectrum of mutations in the MECP2 gene in patients with infantile autism and Rett syndrome. J. Med. Genet., 37, E41.
10. Beyer, K.S., Blasi, F., Bacchelli, E., Klauck, S.M., Maestrini, E., Poustka, A. and International Molecular Genetic Study of Autism (2002) Mutation analysis of the coding sequence of the MECP2 gene in infantile autism. Hum. Genet., 111, 305-309.
11. Schroer, R.J., Phelan, M.C., Michaelis, R.C., Crawford, E.C., Skinner, S.A., Cuccaro, M., Simensen, R.J., Bishop, J., Skinner, C., Fender, D. et al. (1998) Autism and maternally derived aberrations of chromosome 15q. Am. J. Med. Genet., 76, 327-336.
12. Wagstaff, J., Chaillet, J.R. and Lalande, M. (1991) The GABAA receptor beta 3 subunit gene: characterization of a human cDNA from chromosome 15q11q13 and mapping to a region of conserved synteny on mouse chromosome 7. Genomics, 11, 1071-1078.
13. Cook, E.H., Courchesne, R.Y., Cox, N.J., Lord, C., Gonen, D., Guter, S.J., Lincoln, A., Nix, K., Haas, R., Leventhal, B.L. et al. (1998) Linkage-disequilibrium mapping of autistic disorder, with 15q11-q13 markers. Am. J. Hum. Genet., 62, 1077-1083.
14. Buxbaum, J.D., Silverman, J.M., Smith, C.J., Greenberg, D.A., Kilifarski, M., Reichert, J., Cook, E.H., Fang, Y., Song, C.Y. and Vitale, R. (2002) Association between a GABRB3 polymorphism and autism. Mol. Psychiat., 7, 311-316.
15. Nicholls, R.D., Gottlieb, W., Russell, L.B., Davda, M., Horsthemke, B. and Rinchik, E.M. (1993) Evaluation of potential models for imprinted and nonimprinted components of human chromosome 15q11-q13 syndromes by fine-structure homology mapping in the mouse. Proc. Natl Acad. Sci. USA, 90, 2050-2054.
16. Samaco, R.C., Nagarajan, R.P., Braunschweig, D. and LaSalle, J.M. (2004) Multiple pathways regulate MeCP2 expression in normal brain development and exhibit defects in autism-spectrum disorders. Hum. Mol. Genet., 13, 629-639.
17. Lewis, J.D., Meehan, R.R., Henzel, W.J., Maurer-Fogy, I., Jeppesen, P., Klein, F. and Bird, A. (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell, 69, 905-914.
18. Nan, X., Campoy, F.J. and Bird, A. (1997) MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell, 88, 471-481.
19. Nan, X., Ng, H.H., Johnson, C.A., Laherty, C.D., Turner, B.M., Eisenman, R.N. and Bird, A. (1998) Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature, 393, 386-389.
20. Jones, P.L., Veenstra, G.J., Wade, P.A., Vermaak, D., Kass, S.U., Landsberger, N., Strouboulis, J. and Wolffe, A.P. (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat. Genet., 19, 187-191.
21. Fuks, F., Hurd, P.J., Wolf, D., Nan, X., Bird, A.P. and Kouzarides, T. (2003) The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem., 278, 4035-4040.
22. Kimura, H. and Shiota, K. (2003) Methyl-CpG-binding protein, MeCP2, is a target molecule for maintenance DNA methyltransferase, Dnmt1. J. Biol. Chem., 278, 4806-4812.
23. Guy, J., Hendrich, B., Holmes, M., Martin, J.E. and Bird, A. (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet., 27, 322-326.
24. Chen, R.Z., Akbarian, S., Tudor, M. and Jaenisch, R. (2001) Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet., 27, 327-331.
25. Shahbazian, M., Young, J., Yuva-Paylor, L., Spencer, C., Antalffy, B., Noebels, J., Armstrong, D., Paylor, R. and Zoghbi, H. (2002) Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron, 35, 243-254.
26. Tudor, M., Akbarian, S., Chen, R.Z. and Jaenisch, R. (2002) Transcriptional profiling of a mouse model for Rett syndrome reveals subtle transcriptional changes in the brain. Proc. Natl Acad. Sci. USA 99, 15536-15541.
27. Colantuoni, C., Jeon, O.H., Hyder, K., Chenchik, A., Khimani, A.H., Narayanan, V., Hoffman, E.P., Kaufmann, W.E., Naidu, S. and Pevsner, J. (2001) Gene expression profiling in postmortem Rett syndrome brain: differential gene expression and patient classification. Neurobiol. Dis., 8, 847-865.
28. Traynor, J., Agarwal, P., Lazzeroni, L. and Francke, U. (2002) Gene expression patterns vary in clonal cell cultures from Rett syndrome females with eight different MECP2 mutations. BMC Med. Genet. 3, 12.
29. Chen, W.G., Chang, Q., Lin, Y., Meissner, A., West, A.E., Griffith, E.C., Jaenisch, R. and Greenberg, M.E. (2003) Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science, 302, 885-889.
30. Martinowich, K., Hattori, D., Wu, H., Fouse, S., He, F., Hu, Y., Fan, G. and Sun, Y.E. (2003) DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science, 302, 890-893.
31. Balmer, D., Arredondo, J., Samaco, R.C. and LaSalle, J.M. (2002) MECP2 mutations in Rett syndrome adversely affect lymphocyte growth, but do not affect imprinted gene expression in blood or brain. Hum. Genet., 110, 545-552.
32. Braunschweig, D., Simcox, T., Samaco, R.C. and LaSalle, J.M. (2004) X-chromosome inactivation ratios affect wild-type MeCP2 expression within mosaic Rett syndrome and Mecp2-/+ mouse brain. Hum. Mol. Genet. 13, 1275-1286.
33. 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 nucleolar RNA species and as an antisense RNA for UBE3A. Hum. Mol. Genet., 10, 2687-2700.
34. Gregory, R.I., Randall, T.E., Johnson, C.A., Khosla, S., Hatada, I., O'Neill, L.P., Turner, B.M. and Feil, R. (2001) DNA methylation is linked to deacetylation of histone H3, but not H4, on the imprinted genes Snrpn and U2afl-rsl. Mol. Cell. Biol., 21, 5426-5436.
35. Balmer, D., Goldstine, J., Rao, Y.M. and LaSalle, J.M. (2003) Elevated methyl-CpG-binding protein 2 expression is acquired during postnatal human brain development and is correlated with alternative polyadenylation, J. Mol. Med., 81, 61-68.
36. Rougeulle, C., Glatt, H. and Lalande, M. (1997) The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brain (letter). Nat. Genet., 17, 14-15.
37. Jiang, Y.H., Sahoo, T., Michaelis, R.C., Bercovich, D., Bressler, J., Kashork, C.D., Liu, Q., Shaffer, L.G., Schroer, R.J., Stockton, D.W. et al. (2004) A mixed epigenetic/genetic model for oligogenic inheritance of autism with a limited role for UBE3A. Am. J. Med. Genet., 131A, 1-10.
38. Cook, E.H., Jr, Courchesne, R.Y., Cox, N.J., Lord, C., Gonen, D., Guter, S.J., Lincoln, A., Nix, K., Haas, R., Leventhal, B.L. et al. (1998) Linkage-disequilibrium mapping of autistic disorder, with 15q11-q13 markers. Am. J. Hum. Genet., 62, 1077-1083.
39. McCauley, J.L., Olson, L.M., Delahanty, R., Amin, T., Nurmi, E.L., Organ, E.L., Jacobs, M.M., Folstein, S.E., Haines, J.L. and Sutcliffe, J.S. (2004) A linkage disequilibrium map of the 1-Mb 15q12 GABA(A) receptor subunit cluster and association to autism. Am. J. Med. Genet., 131B, 51-59.
40. IMGSoA Consortium (1998) A full genome screen for autism with evidence for linkage to a region on chromosome 7q. Hum. Mol. Genet. 7, 571-578.
41. Philippe, A., Martinez, M., Guilloud-Bataille, M., Gillberg, C., Rastam, M., Sponheim, E., Coleman, M., Zappella, M., Aschauer, H., Van Maldergem, L. et al. (1999) Genome-wide scan for autism susceptibility genes. Paris Autism Research International Sibpair Study. Hum. Mol. Genet., 8, 805-812.
42. IMGSoA Consortium (2001) A genomewide screen for autism: strong evidence for linkage to chromosomes 2q, 7q, and 16p. Am. J. Hum. Genet., 69, 570-581.
43. Yonan, A.L., Alarcon, M., Cheng, R., Magnusson, P.K., Spence, S.J., Palmer, A.A., Grunn, A., Juo, S.H., Terwilliger, J.D., Liu, J. et al. (2003) A genomewide screen of 345 families for autism-susceptibility loci. Am. J. Hum. Genet., 73, 886-897.
44. Salmon, B., Hallmayer, J., Rogers, T., Kalaydjieva, L., Petersen, P.B., Nicholas, P., Pingree, C., McMahon, W., Spiker, D., Lotspeich, L. et al. (1999) Absence of linkage and linkage disequilibrium to chromosome 15q11-q13 markers in 139 multiplex families with autism. Am. J. Med. Genet., 88, 551-556.
45. Shao, Y., Cuccaro, M.L., Hauser, E.R., Raiford, K.L., Menold, M.M., Wolpert, C.M., Ravan, S.A., Elston, L., Decena, K., Donnelly, S.L. et al. (2003) Fine mapping of autistic disorder to chromosome 15q11-q13 by use of phenotypic subtypes. Am. J. Hum. Genet., 72 539-548.
46. Nurmi, E.L., Amin, T., Olson, L.M., Jacobs, M.M., McCauley, J.L., Lam, A.Y., Organ, E.L., Folstein, S.E., Haines, J.L. and Sutcliffe, J.S. (2003) Dense linkage disequilibrium mapping in the 15q11-q13 maternal expression domain yields evidence for association in autism. Mol. Psychiat., 8, 624-634, 570.
47. Veenstra-VanderWeele, J., Gonen, D., Leventhal, B.L. and Cook, E.H., Jr (1999) Mutation screening of the UBE3A/E6-AP gene in autistic disorder. Mol. Psychiat., 4, 64-67.
48. Nurmi, E.L., Bradford, Y., Chen, Y.-h., Hall, J., Arnone, B., Gardiner, M.B., Hutcheson, H.B., Gilbert, J.R., Pericak-Vance, M.A., Copeland-Yates, S.A. et al. (2001) Linkage disequilibrium at the Angelman syndrome gene UBE3A in autism families. Genomics, 77 105-113.
49. Sinkkonen, S.T., Homanics, G.E. and Korpi, E.R. (2003) Mouse models of Angelman syndrome, a neurodevelopmental disorder, display different brain regional GABA(A) receptor alterations. Neurosci. Lett. 340, 205-208.
50. Buettner, V.L., Longmate, J.A., Barish, M.E., Mann, J.R. and Singer-Sam, J. (2004) Analysis of imprinting in mice with uniparental duplication of proximal chromosomes 7 and 15 by use of a custom oligonucleotide microarray. Mamm. Genome, 15, 199-209.
51. Blatt, G.J., Fitzgerald, C.M., Guptill, J.T., Booker, A.B., Kemper, T.L. and Bauman, M.L. (2001) Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study. J. Autism Dev. Disord., 31, 537-543.
52. Moreno-Fuenmayor, H., Borjas, L., Arrieta, A., Valera, V. and Socorro-Candanoza, L. (1996) Plasma excitatory amino acids in autism. Invest. Clin., 37, 113-128.
53. Dhossche, D., Applegate, H., Abraham, A., Maertens, P., Bland, L., Bencsath, A. and Martinez, J. (2002) Elevated plasma gamma-aminobutyric acid (GABA) levels in autistic youngsters: stimulus for a GABA hypothesis of autism. Med. Sci. Monit., 8, PR1-6.
54. Aldred, S., Moore, K.M., Fitzgerald, M. and Waring, R.H. (2003) Plasma amino acid levels in children with autism and their families. J. Autism Dev. Disord., 33, 93-97.
55. Jiang, Y.H., Armstrong, D., Albrecht, U., Atkins, C.M., Noebels, J.L., Eichele, G., Sweatt, J.D. and Beaudet, A.L. (1998) Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron, 21, 799-811.
56. DeLorey, T.M., Handforth, A., Anagnostaras, S.G., Homanics, G.E., Minassian, B.A., Asatourian, A., Fanselow, M.S., Delgado-Escueta, A., Ellison, G.D. and Olsen, R.W. (1998) Mice lacking the beta3 subunit of the GABAA receptor have the epilepsy phenotype and many of the behavioral characteristics of Angelman syndrome. J. Neurosci., 18, 8505-8514.
57. Murrell, A., Heeson, S. and Reik, W. (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat. Genet., 36, 889-893.
58. Weitzel, J.M., Buhrmester, H. and Stratling, W.H. (1997) Chicken MAR-binding protein ARBP is homologous to rat methyl-CpG- binding protein MeCP2. Mol. Cell. Biol., 17, 5656-5666.
59. 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.
60. 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.
61. Meguro, M., Kashiwagi, A., Mitsuya, K., Nakao, M., Kondo, I., Saitoh, S. and Oshimura, M. (2001) A novel maternally expressed gene, ATP10C, encodes a putative aminophospholipid translocase associated with Angelman syndrome. Nat. Genet., 28, 19-20.
62. Herzing, L.B.K., Kim, S.-J., Cook, E.H. and Ledbetter, D.H. (2001) The human aminophospholipid-transporting ATPase gene ATP10C maps adjacent to UBE3A and exhibits similar imprinted expression. Am. J. Hum. Genet., 68, 1501-1505.
63. Sinnett, D., Wagstaff, J., Glatt, K., Woolf, E., Kirkness, E.J. and Lalande, M. (1993) High-resolution mapping of the gamma-aminobutyric acid receptor subunit beta 3 and alpha 5 gene cluster on chromosome 15q11-q13, and localization of breakpoints in two Angelman syndrome patients. Am. J. Hum. Genet., 52, 1216-1229.
64. LaSalle, J. and Lalande, M. (1996) Homologous association of oppositely imprinted chromosomal domains. Science, 272, 725-728.
65. Tsai, T.F., Bressler, J., Jiang, Y.H. and Beaudet, A.L. (2003) Disruption of the genomic imprint in trans with homologous recombination at Snrpn in ES cells. Genesis, 37, 151-161.
66. LaSalle, J., Goldstine, J., Balmer, D. and Greco, C. (2001) Quantitative localization of heterologous methyl-CpG-binding protein 2 (MeCP2) expression phenotypes in normal and Rett syndrome brain by laser scanning cytometry. Hum. Mol. Genet., 10, 1729-1740.
67. Yamasaki, K., Joh, K., Ohta, T., Masuzaki, H., Ishimam, T., Mukai, T., Niikawa, N., Ogawa, M., Wagstaff, J. and Kishino, T. (2003) Neurons but not glial cells show reciprocal imprinting of sense and antisense transcripts of Ube3a. Hum. Mol. Genet., 12, 837-847.
68. Yoon, B.J., Herman, H., Sikora, A., Smith, L.T., Plass, C. and Soloway, P.D. (2002) Regulation of DNA methylation of Rasgrfl. Nat. Genet., 30, 92-96.
69. Yasui, D., Miyano, M., Cai, S., Varga-Weisz, P. and Kohwi-Shigematsu, T. (2002) SATB1 targets chromatin remodelling to regulate genes over long distances. Nature, 419, 641-645.
70. Yang, Y., Hu, J.F., Ulaner, G.A., Li, T., Yao, X., Vu, T.H. and Hoffman, A.R. (2003) Epigenetic regulation of Igf2/H19 imprinting at CTCF insulator binding sites. J. Cell. Biochem., 90, 1038-1055.