DLX5 and DLX6 expression is biallelic and not modulated by MeCP2 deficiency

American Journal of Human Genetics

Volumn 81, Issue 3, 2007, Pages 492-506

  Schüle, Birgitt ^a   Hong, Hua Li ^a   Fisch Kohl, Claudia ^a   Purmann, Carolin ^a   Francke, Uta ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHYL CPG BINDING PROTEIN 2; TRANSCRIPTION FACTOR DLX5; TRANSCRIPTION FACTOR DLX6; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; AUTISM; CHROMOSOME 7; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GENE EXPRESSION; GENE MUTATION; GENE OVEREXPRESSION; GENOME IMPRINTING; HUMAN; HUMAN TISSUE; HYBRID CELL; LYMPHOBLASTOID CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RETT SYNDROME; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM;

MUS;

EID: 34548268591     PISSN: 00029297     EISSN: None     Source Type: Journal    
DOI: 10.1086/520063     Document Type: Article

References (72)

1. dbSNP, http://www.ncbi.nlm.nih.gov/projects/SNP/
2. GenBank, http://www.ncbi.nlm.nih.gov/Genbank/ (for DLX5 [accession number NM_005221.5], DLX6 [accession number NM_005222.2], and Dlx6 [accession number BC114342.1] reference sequences)
3. HGVS Nomenclature for the Description of Sequence Variants, http://www.hgvs.org/mutnomen/
4. Online Mendelian Inheritance in Man (OMIM), http://www.ncbi.nlm.nih.gov/ Omim/ (for RTT and MECP2)
5. Rett A (1966) Uber ein eigenartiges hirnatrophisches Syndrom bei Hyperammonamie im Kindesalter. Wien Med Wochenschr 116:723-738
6. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185-188
7. Francke U (2006) Neurogenetics of MeCP2 deficiency. Nat Clin Pract Neurol 2:212-221
8. Wan M, Lee SS, Zhang X, Houwink-Manville I, Song HR, Amir RE, Budden S, Naidu S, Pereira JL, Lo IF, et al (1999) Rett syndrome and beyond: recurrent spontaneous and familial MECP2 mutations at CpG hotpots. Am J Hum Genet 65:1520-1529
9. Carney RM, Wolpert CM, Ravan SA, Shahbazian M, Ashley-Koch A, Cuccaro ML, Vance JM, Pericak-Vance MA (2003) Identification of MeCP2 mutations in a series of females with autistic disorder. Pediatr Neurol 28:205-211
10. Kankirawatana P, Leonard H, Ellaway C, Scurlock J, Mansour A, Makris CM, Dure LS, Friez M, Lane J, Kiraly-Borri C, et al (2006) Early progressive encephalopathy in boys and MECP2 mutations. Neurology 67:164-166
11. Giacometti E, Luikenhuis S, Beard C, Jaenisch R (2007) Partial rescue of MeCP2 deficiency by postnatal activation of MeCP2. Proc Natl Acad Sci USA 104:1931-1936
12. Guy J, Gan J, Selfridge J, Cobb S, Bird A (2007) Reversal of neurological defects in a mouse model of Rett syndrome. Science 315:1143-1147
13. Nan X, Campoy FJ, Bird A (1997) MeCP2 is a transcriptional repressor with abundant binding sites in genomic chromatin. Cell 88:471-481
14. Colantuoni C, Jeon OH, Hyder K, Chenchik A, Khimani AH, Narayanan V, Hoffman EP, Kaufmann WE, Naidu S, Pevsner J (2001) Gene expression profiling in postmortem Rett syndrome brain: differential gene expression and patient classification. Neurobiol Dis 8:847-865
15. Tudor M, Akbarian S, Chen RZ, 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
16. Traynor J, Agarwal P, Lazzeroni L, 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
17. Ballestar E, Ropero S, Alaminos M, Armstrong J, Setien F, Agrelo R, Fraga MF, Herranz M, Avila S, Pineda M, et al (2005) The impact of MECP2 mutations in the expression patterns of Rett syndrome patients. Hum Genet 116:91-104
18. Nuber UA, Kriaucionis S, Roloff TC, Guy J, Selfridge J, Steinhoff C, Schulz R, Lipkowitz B, Ropers HH, Holmes MC, et al (2005) Up-regulation of glucocorticoid-regulated genes in a mouse model of Rett syndrome. Hum Mol Genet 14:2247-2256
19. Delgado IJ, Kim DS, Thatcher KN, LaSalle JM, Van den Veyver IB (2006) Expression profiling of clonal lymphocyte cell cultures from Rett syndrome patients. BMC Med Genet 7:61
20. Deng V, Matagne V, Banine F, Frerking M, Ohliger P, Budden S, Pevsner J, Dissen GA, Sherman LS, Ojeda SR (2007) FXYD1 is a MeCP2 target gene overexpressed in the brains of Rett syndrome patients and Mecp2-null mice. Hum Mol Genet 16:640-650
21. Jordan C, Li H-H, Kwan H, Francke U (2007) Cerebellar gene expression profiles of mouse models for Rett syndrome reveal novel MeCP2 targets. BMC Med Genet 8:36
22. Reik W, Walter J (1998) Imprinting mechanisms in mammals. Curr Opin Genet Dev 8:154-164
23. Morison IM, Ramsay JP, Spencer HG (2005) A census of mammalian imprinting. Trends Genet 21:457-465
24. Balmer D, Arredondo J, Samaco RC, LaSalle JM (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
25. Samaco RC, Hogart A, LaSalle JM (2005) Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. Hum Mol Genet 14:483-492
26. Makedonski K, Abuhatzira L, Kaufman Y, Razin A, Shemer R (2005) MeCP2 deficiency in Rett syndrome causes epigenetic aberrations at the PWS/AS imprinting center that affects UBE3A expression. Hum Mol Genet 14:1049-1058
27. Jordan C, Francke U (2006) Ube3a expression is not altered in Mecp2 mutant mice. Hum Mol Genet 15:2210-2215
28. Horike S, Cai S, Miyano M, Cheng JF, Kohwi-Shigematsu T (2005) Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat Genet 37:31-40
29. Guy J, Hendrich B, Holmes M, Martin JE, Bird A (2001) A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat Genet 27:322-326
30. Kimura MI, Kazuki Y, Kashiwagi A, Kai Y, Abe S, Barbieri O, Levi G, Oshimura M (2004) Dlx5, the mouse homologue of the human-imprinted DLX5 gene, is biallelically expressed in the mouse brain. J Hum Genet 49:273-277
31. Stuhmer T, Anderson SA, Ekker M, Rubenstein JL (2002) Ectopic expression of the Dlx genes induces glutamic acid decarboxylase and Dlx expression. Development 129:245-252
32. Okita C, Meguro M, Hoshiya H, Haruta M, Sakamoto YK, Oshimura M (2003) A new imprinted cluster on the human chromosome 7q21-q31, identified by human-mouse monochromosomal hybrids. Genomics 81:556-559
33. Panganiban G, Rubenstein JL (2002) Developmental functions of the Distal-less/Dlx homeobox genes. Development 129:4371-4386
34. Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, Mantero S, Bober E, Barbieri O, Simeone A, Levi G (1999) Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126:3795-3809
35. Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, Pedersen RA, Rubenstein JL (1999) Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126:3831-3846
36. Perera M, Merlo GR, Verardo S, Paleari L, Corte G, Levi G (2004) Defective neuronogenesis in the absence of Dlx5. Mol Cell Neurosci 25:153-161
37. Yan H, Papadopoulos N, Marra G, Perrera C, Jiricny J, Boland CR, Lynch HT, Chadwick RB, de la Chapelle A, Berg K, et al (2000) Conversion of diploidy to haploidy. Nature 403:723-724
38. Gallagher RC, Pils B, Albalwi M, 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
39. den Dunnen JT, Antonarakis SE (2000) Mutation nomenclature extensions and suggestions to describe complex mutations: a discussion. Hum Mutat 15:7-12
40. Hamilton SP, Woo JM, Carlson EJ, Ghanem N, Ekker M, Rubenstein JL (2005) Analysis of four DLX homeobox genes in autistic probands. BMC Genet 6:52
41. Schanen NC (2006) Epigenetics of autism spectrum disorders. Hum Mol Genet Spec 2 15:R138-R150
42. Badcock C, Crespi B (2006) Imbalanced genomic imprinting in brain development: an evolutionary basis for the aetiology of autism. J Evol Biol 19:1007-1032
43. Itaba-Matsumoto N, Maegawa S, Yamagata H, Kondo I, Oshimura M, Nanba E (2007) Imprinting status of paternally imprinted DLX5 gene in Japanese patients with Rett syndrome. Brain Dev (electronically published March 17, 2007) (accessed May 19, 2007)
44. Chadwick LH, Wade PA (2007) MeCP2 in Rett syndrome: transcriptional repressor or chromatin architectural protein? Curr Opin Genet Dev 17:121-125
45. Itoh M, Ide S, Takashima S, Kudo S, Nomura Y, Segawa M, Kubota T, Mori H, Tanaka S, Horie H, et al (2007) Methyl CpG-binding protein 2 (a mutation of which causes Rett syndrome) directly regulates insulin-like growth factor binding protein 3 in mouse and human brains. J Neuropathol Exp Neurol 66:117-123
46. Kuwajima T, Nishimura I, Yoshikawa K (2006) Necdin promotes GABAergic neuron differentiation in cooperation with Dlx homeodomain proteins. J Neurosci 26:5383-5392
47. Bienvenu T, Chelly J (2006) Molecular genetics of Rett syndrome: when DNA methylation goes unrecognized. Nat Rev Genet 7:415-426
48. Zhou QP, Le TN, Qiu X, Spencer V, de Melo J, Du G, Plews M, Fonseca M, Sun JM, Davie JR, et al (2004) Identification of a direct Dlx homeodomain target in the developing mouse forebrain and retina by optimization of chromatin immunoprecipitation. Nucleic Acids Res 32:884-892
49. Yasui D, Miyano M, Cai S, Varga-Weisz P, Kohwi-Shigematsu T (2002) SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419:641-645
50. Georgel FT, Horowitz-Scherer RA, Adkins N, Woodcock CL, Wade PA, Hansen JC (2003) Chromatin compaction by human MeCP2: assembly of novel secondary chromatin structures in the absence of DNA methylation. J Biol Chem 278:32181-32188
51. Nikitina T, Shi X, Ghosh RP, Horowitz-Scherer RA, Hansen JC, Woodcock CL (2007) Multiple modes of interaction between the methylated DNA binding protein MeCP2 and chromatin. Mol Cell Biol 27:864-877
52. Francke U, Pellegrino MA (1977) Assignment of the major histocompatibility complex to a region of the short arm of human chromosome 6. Proc Natl Acad Sci USA 74:1147-1151
53. Francke U, Busby N, Shaw D, Hansen S, Brown MG (1976) Intrachromosomal gene mapping in man: assignment of nucleoside phosphorylase to region 14cen leads to 14q21 by interspecific hybridization of cells with a t(X;14)(p22;q21) translocation. Somatic Cell Genet 2:27-40
54. Meguro M, Mitsuya K, Sui H, Shigenami K, Kugoh H, Nakao M, Oshimura M (1997) Evidence for uniparental, paternal expression of the human GABAA receptor subunit genes, using microcell-mediated chromosome transfer. Hum Mol Genet 6:2127-2133
55. Gabriel JM, Higgins MJ, Gebuhr TC, Shows TB, Saitoh S, Nicholls RD (1998) A model system to study genomic imprinting of human genes. Proc Natl Acad Sci USA 95:14857-14862
56. Kugoh H, Mitsuya K, Meguro M, Shigenami K, Schulz TC, Oshimura M (1999) Mouse A9 cells containing single human chromosomes for analysis of genomic imprinting. DNA Res 6:165-172
57. Inoue J, Mitsuya K, Maegawa S, Kugoh H, Kadota M, Okamura D, Shinohara T, Nishihara S, Takehara S, Yamauchi K, et al (2001) Construction of 700 human/mouse A9 monochromosomal hybrids and analysis of imprinted genes on human chromosome 6. J Hum Genet 46:137-145
58. Piras G, El Kharroubi A, Kozlov S, Escalante-Alcalde D, Hernandez L, Copeland NG, Gilbert DJ, Jenkins NA, Stewart CL (2000) Zac1 (Lot1), a potential tumor suppressor gene, and the gene for ε-sarcoglycan are maternally imprinted genes: identification by a subtractive screen of novel uniparental fibroblast lines. Mol Cell Biol 20:3308-3315
59. Ono R, Kobayashi S, Wagatsuma H, Aisaka K, Kohda T, Kaneko-Ishino T, Ishino F (2001) A retrotransposon-derived gene, PEG10, is a novel imprinted gene located on human chromosome 7q21. Genomics 73:232-237
60. Müller B, Hedrich K, Kock N, Dragasevic N, Svetel M, Garrels J, Landt O, Nitschke M, Pramstaller PP, Reik W, et al (2002) Evidence that paternal expression of the ε-sarcoglycan gene accounts for reduced penetrance in myoclonus-dystonia. Am J Hum Genet 71:1303-1311
61. Grabowski M, Zimprich A, Lorenz-Depiereux B, Kalscheuer V, Asmus F, Gasser T, Meitinger T, Strom TM (2003) The epsilon-sarcoglycan gene (SGCE), mutated in myoclonus-dystonia syndrome, is maternally imprinted. Eur J Hum Genet 11:138-144
62. Ono R, Shiura H, Aburatani H, Kohda T, Kaneko-Ishino T, Ishino F (2003) Identification of a large novel imprinted gene cluster on mouse proximal chromosome 6. Genome Res 13:1696-1705
63. Neitzel H (1986) A routine method for the establishment of permanent growing lymphoblastoid cell lines. Hum Genet 73:320-326
64. Hannula K, Lipsanen-Nyman M, Scherer SW, Holmberg C, Hoglund P, Kere J (2001) Maternal and paternal chromosomes 7 show differential methylation of many genes in lymphoblast DNA. Genomics 73:1-9
65. McRae AF, Matigian NA, Vadlamudi L, Mulley JC, Mowry B, Martin NG, Berkovic SF, Hayward NK, Visscher PM (2007) Replicated effects of sex and genotype on gene expression in human lymphoblastoid cell lines. Hum Mol Genet 16:364-373
66. Cowles CR, Hirschhorn JN, Altshuler D, Lander ES (2002) Detection of regulatory variation in mouse genes. Nat Genet 32:432-437
67. Yan H, Yuan W, Velculescu VE, Vogelstein B, Kinzler KW (2002) Allelic variation in human gene expression. Science 297:1143
68. Lo HS, Wang Z, Hu Y, Yang HH, Gere S, Buetow KH, Lee MP (2003) Allelic variation in gene expression is common in the human genome. Genome Res 13:1855-1862
69. Bray NJ, Buckland PR, Owen MJ, O'Donovan MC (2003) Cis-acting variation in the expression of a high proportion of genes in human brain. Hum Genet 113:149-153
70. Pastinen T, Sladek R, Gurd S, Sammak A, Ge B, Lepage P, Lavergne K, Villeneuve A, Gaudin T, Brandstrom H, et al (2004) A survey of genetic and epigenetic variation affecting human gene expression. Physiol Genomics 16:184-193
71. Doss S, Schadt EE, Drake TA, Lusis AJ (2005) Cis-acting expression quantitative trait loci in mice. Genome Res 15:681-691
72. Heard E, Disteche CM (2006) Dosage compensation in mammals: fine-tuning the expression of the X chromosome. Genes Dev 20:1848-1867