Reciprocal co-regulation of EGR2 and MECP2 is disrupted in Rett syndrome and autism

Human Molecular Genetics

Volumn 18, Issue 3, 2009, Pages 525-534

  Swanberg, Susan E ^a   Nagarajan, Raman P ^a   Peddada, Sailaja ^a   Yasui, Dag H ^a   Lasalle, Janine M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 2; METHYL CPG BINDING PROTEIN 2;

ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN CORTEX; BRAIN DEVELOPMENT; CELL CULTURE; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE FUNCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; INTRON; MOUSE; NONHUMAN; PATHOGENESIS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; RETT SYNDROME; RNA INTERFERENCE;

ADOLESCENT; ADULT; ANIMALS; AUTISTIC DISORDER; CELL LINE, TUMOR; CEREBRAL CORTEX; CHILD; CHILD, PRESCHOOL; EARLY GROWTH RESPONSE PROTEIN 2; FEMALE; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; INFANT; INFANT, NEWBORN; MALE; METHYL-CPG-BINDING PROTEIN 2; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; RETT SYNDROME;

EID: 58749104036     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn380     Document Type: Article

References (85)

1. American Psychiatric Association and Task Force on DSM-IV (1994) Diagnostic and Statistical Manual of Mental Disorders: DSM-IV., 4th edn. American Psychiatric Association, Washington, DC.
2. Nomura, Y. (2005) Early behavior characteristics and sleep disturbance in Rett syndrome. Brain. Dev., 27 (Suppl. 1), S35-S42.
3. Nomura, Y. and Segawa, M. (2005) Natural history of Rett syndrome. J. Child. Neurol., 20, 764-778.
4. Hagberg, B. (2005) Rett syndrome: Long-term clinical follow-up experiences over four decades. J. Child Neurol., 20, 722-727.
5. Kerr, A.M. and Julu, P.O. (1999) Recent insights into hyperventilation from the study of Rett syndrome. Arch. Dis. Child, 80, 384-387.
6. Motil, K.J., Schultz, R.J., Browning, K., Trautwein, L. and Glaze, D.G. (1999) Oropharyngeal dysfunction and gastroesophageal dysmotility are present in girls and women with Rett syndrome. J. Pediatr. Gastroenterol. Nutr., 29, 31-37.
7. 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.
8. Kumar, A., Kamboj, S., Malone, B.M., Kudo, S., Twiss, J.L., Czymmek, K.J., LaSalle, J.M. and Schanen, N.C. (2008) Analysis of protein domains and Rett syndrome mutations indicate that multiple regions influence chromatin-binding dynamics of the chromatin-associated protein MECP2 in vivo. J. Cell. Sci., 121, 1128-1137.
9. Yasui, D.H., Peddada, S., Bieda, M.C., Vallero, R.O., Hogart, A., Nagarajan, R.P., Thatcher, K.N., Farnham, P.J. and Lasalle, J.M. (2007) Integrated epigenomic analyses of neuronal MeCP2 reveal a role for long-range interaction with active genes. Proc. Natl Acad. Sci. USA 104, 19416-19421.
10. Chahrour, M., Jung, S.Y., Shaw, C., Zhou, X., Wong, S.T., Qin, J. and Zoghbi, H.Y. (2008) MeCP2, a key contributor to neurological disease, activates and represses transcription. Science, 320, 1224-1229.
11. Shahbazian, M.D. and Zoghbi, H.Y. (2001) Molecular genetics of Rett syndrome and clinical spectrum of MECP2 mutations. Curr. Opin. Neurol., 14, 171-176.
12. 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.
13. 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.
14. Villard, L. (2007) MECP2 mutations in males. J. Med. Genet., 44 417-423.
15. Smyk, M., Obersztyn, E., Nowakowska, B., Nawara, M., Cheung, S.W., Mazurczak, T., Stankiewicz, P. and Bocian, E. (2007) Different-sized duplications of Xq28, including MECP2, in three males with mental retardation, absent or delayed speech, and recurrent infections. Am. J. Med. Genet. B. Neuropsychiatr. Genet., 6, 799-806.
16. Nagarajan, R.P., Hogart, A.R., Gwye, Y., Martin, M.R. and LaSalle, J.M. (2006) Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation. Epigenetics, 1, 1-11.
17. Loat, C., Curran, S., Lewis, C., Abrahams, B., Duvall, J., Geschwind, D., Bolton, P. and Craig, I. (2008) Methyl-CpG-binding protein (MECP2) polymorphisms and vulnerability to autism. Genes Brain Behav., 7, 754-760.
18. Samaco, R.C., Fryer, J.D., Ren, J., Fyffe, S., Chao, H.T., Sun, Y., Greer, J.J., Zoghbi, H.Y. and Neul, J.L. (2008) A partial loss of function allele of methyl-CpG-binding protein 2 predicts a human neurodevelopmental syndrome. Hum. Mol. Genet., 17, 1718-1727.
19. Kerr, B., Alvarez-Saavedra, M., Saez, M.A., Saona, A. and Young, J.I. (2008) Defective body-weight regulation, motor control and abnormal social interactions in Mecp2 hypomorphic mice. Hum. Mol. Genet., 17, 1707-1717.
20. Katz, L.C. and Shatz, C.J. (1996) Synaptic activity and the construction of cortical circuits. Science, 274, 1133-1138.
21. 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.
22. Zhou, Z., Hong, E.J., Cohen, S., Zhao, W.N., Ho, H.Y., Schmidt, L., Chen, W.G., Lin, Y., Savner, E., Griffith, E.C. et al. (2006) Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269.
23. Herdegen, T. and Leah, J.D. (1998) Inducible and constitutive transcription factors in the mammalian nervous system: Control of gene expression by Jun, Fos and Krox, and CREB/ATF proteins. Brain Res. Brain Res. Rev., 28, 370-490.
24. Dragunow, M. (1996) A role for immediate-early transcription factors in learning and memory. Behav. Genet., 26, 293-299.
25. Sng, J.C., Taniura, H. and Yoneda, Y. (2004) A tale of early response genes. Biol. Pharm. Bull., 27, 606-612.
26. Shaulian, E. and Karin, M. (2002) AP-1 as a regulator of cell life and death. Nat. Cell Biol., 4, E131-E136.
27. Davis, S., Bozon, B. and Laroche, S. (2003) How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? Behav. Brain Res., 142, 17-30.
28. 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.
29. 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.
30. Chang, Q., Khare, G., Dani, V., Nelson, S. and Jaenisch, R. (2006) The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron, 49, 341-348.
31. Glorioso, C., Sabatini, M., Unger, T., Hashimoto, T., Monteggia, L.M., Lewis, D.A. and Mirnics, K. (2006) Specificity and timing of neocortical transcriptome changes in response to BDNF gene ablation during embryogenesis or adulthood. Mol. Psychiatry, 11, 633-648.
32. De, S., Shuler, C.F. and Turman, J.E. Jr (2003) The ontogeny of Krox-20 expression in brainstem and cerebellar neurons. J. Chem. Neuroanat. 25, 213-226.
33. Williams, J., Dragunow, M., Lawlor, P., Mason, S., Abraham, W.C., Leah, J., Bravo, R., Demmer, J. and Tate, W. (1995) Krox20 may play a key role in the stabilization of long-term potentiation. Brain Res. Mol. Brain Res., 28, 87-93.
34. Inokuchi, K., Murayama, A. and Ozawa, F. (1996) mRNA differential display reveals Krox-20 as a neural plasticity-regulated gene in the rat hippocampus. Biochem. Biophys. Res. Commun., 221, 430-436.
35. Lumsden, A. and Krumlauf, R. (1996) Patterning the vertebrate neuraxis. Science, 274, 1109-1115.
36. Borday, C., Chatonnet, F., Thoby-Brisson, M., Champagnat, J. and Fortin, G. (2005) Neural tube patterning by Krox20 and emergence of a respiratory control. Respir. Physiol. Neurobiol., 149, 63-72.
37. DeSteno, D.A. and Schmauss, C. (2008) Induction of early growth response gene 2 expression in the forebrain of mice performing an attention-set-shifting task. Neuroscience, 152, 417-428.
38. Hu, V.W., Frank, B.C., Heine, S., Lee, N.H. and Quackenbush, J. (2006) Gene expression profiling of lymphoblastoid cell lines from monozygotic twins discordant in severity of autism reveals differential regulation of neurologically relevant genes. BMC Genomics, 7, 118.
39. Unoki, M. and Nakamura, Y. (2003) Methylation at CpG islands in intron 1 of EGR2 confers enhancer-like activity. FEBS Lett., 554, 67-72.
40. Horike, S., Cai, S., Miyano, M., Cheng, J.F. and Kohwi-Shigematsu, T. (2005) Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat. Genet., 37, 31-40.
41. Namciu, S.J., Friedman, R.D., Marsden, M.D., Sarausad, L.M., Jasoni, C.L. and Fournier, R.E. (2004) Sequence organization and matrix attachment regions of the human serine protease inhibitor gene cluster at 14q32.1. Mamm. Genome, 15, 162-178.
42. Jung, B.P., Jugloff, D.G., Zhang, G., Logan, R., Brown, S. and Eubanks, J.H. (2003) The expression of methyl CpG binding factor MeCP2 correlates with cellular differentiation in the developing rat brain and in cultured cells. J. Neurobiol., 55, 86-96.
43. Schug, J. (2008) Using TESS to predict transcription factor binding sites in DNA sequence. Curr. Protoc. Bioinformatics, Chapter 2, Supplement 21, Unit 2.6.
44. Liu, J. and Francke, U. (2006) Identification of cis-regulatory elements for MECP2 expression. Hum. Mol. Genet., 15, 1769-1782.
45. Thatcher, K.N., Peddada, S., Yasui, D.H. and Lasalle, J.M. (2005) Homologous pairing of 15q11-13 imprinted domains in brain is developmentally regulated but deficient in Rett and autism samples. Hum. Mol. Genet., 14, 785-797.
46. Jang, S.W., LeBlanc, S.E., Roopra, A., Wrabetz, L. and Svaren, J. (2006) In vivo detection of Egr2 binding to target genes during peripheral nerve myelination. J. Neurochem., 98, 1678-1687.
47. 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.
48. Yamada, K., Gerber, D.J., Iwayama, Y., Ohnishi, T., Ohba, H., Toyota, T., Aruga, J., Minabe, Y., Tonegawa, S. and Yoshikawa, T. (2007) Genetic analysis of the calcineurin pathway identifies members of the EGR gene family, specifically EGR3, as potential susceptibility candidates in schizophrenia. Proc. Natl Acad. Sci. USA, 104, 2815-2820.
49. Gallitano-Mendel, A., Wozniak, D.F., Pehek, E.A. and Milbrandt, J. (2008) Mice lacking the immediate early gene Egr3 respond to the anti-aggressive effects of clozapine yet are relatively resistant to its sedating effects. Neuropsychopharmacology, 33, 1266-1275.
50. Orsetti, M., Di Brisco, F., Canonico, P.L., Genazzani, A.A. and Ghi, P. (2008) Gene regulation in the frontal cortex of rats exposed to the chronic mild stress paradigm, an animal model of human depression. Eur. J. Neurosci., 27, 2156-2164.
51. Gallitano-Mendel, A., Izumi, Y., Tokuda, K., Zorumski, C.F., Howell, M.P., Muglia, L.J., Wozniak, D.F. and Milbrandt, J. (2007) The immediate early gene early growth response gene 3 mediates adaptation to stress and novelty. Neuroscience, 148, 633-643.
52. Rinehart, N.J., Bradshaw, J.L., Moss, S.A., Brereton, A.V. and Tonge, B.J. (2001) A deficit in shifting attention present in high-functioning autism but not Asperger's disorder. Autism, 5, 67-80.
53. Shafritz, K.M., Dichter, G.S., Baranek, G.T. and Belger, A. (2008) The neural circuitry mediating shifts in behavioral response and cognitive set in autism. Biol. Psychiatry, 63, 974-980.
54. Massa, V., Gaudenzi, G., Sangiorgio, L., Cotelli, F. and Giavini, E. (2007) Krox20 is down-regulated following triazole in vitro embryonic exposure: A polycompetitor-based assay. Toxicol. Lett., 169, 196-204.
55. Guennoun, R., Benmessahel, Y., Delespierre, B., Gouezou, M., Rajkowski, K.M., Baulieu, E.E. and Schumacher, M. (2001) Progesterone stimulates Krox-20 gene expression in Schwann cells. Brain Res. Mol. Brain Res. 90, 75-82.
56. Honkaniemi, J., Zhang, J.S., Longo, F.M. and Sharp, F.R. (2000) Stress induces zinc finger immediate early genes in the rat adrenal gland. Brain Res., 877, 203-208.
57. Honkaniemi, J. and Sharp, F.R. (1999) Prolonged expression of zinc finger immediate-early gene mRNAs and decreased protein synthesis following kainic acid induced seizures. Eur. J. Neurosci., 11 10-17.
58. Okada, A., Kushima, K., Aoki, Y., Bialer, M. and Fujiwara, M. (2005) Identification of early-responsive genes correlated to valproic acid-induced neural tube defects in mice. Birth Defects Res. A. Clin. Mol. Teratol., 73, 229-238.
59. Wagner, G.C., Reuhl, K.R., Cheh, M., McRae, P. and Halladay, A.K. (2006) A new neurobehavioral model of autism in mice: Pre- and postnatal exposure to sodium valproate. J. Autism Dev. Disord., 36, 779-793.
60. Alsdorf, R. and Wyszynski, D.F. (2005) Teratogenicity of sodium valproate. Expert Opin. Drug Saf., 4, 345-353.
61. Arndt, T.L., Stodgell, C.J. and Rodier, P.M. (2005) The teratology of autism. Int. J. Dev. Neurosci., 23, 189-199.
62. Williams, G., King, J., Cunningham, M., Stephan, M., Kerr, B. and Hersh, J.H. (2001) Fetal valproate syndrome and autism: Additional evidence of an association. Dev. Med. Child Neurol., 43, 202-216.
63. Helmbacher, F., Pujades, C., Desmarquet, C., Frain, M., Rijli, F.M., Chambon, P. and Charnay, P. (1998) Hoxa1 and Krox-20 synergize to control the development of rhombomere 3. Development, 125, 4739-4748.
64. Chatonnet, F., Thoby-Brisson, M., Abadie, V., Dominguez del Toro, E., Champagnat, J. and Fortin, G. (2002) Early development of respiratory rhythm generation in mouse and chick. Respir. Physiol. Neurobiol., 131, 5-13.
65. Kubik, S., Miyashita, T. and Guzowski, J.F. (2007) Using immediate-early genes to map hippocampal subregional functions. Learn Mem., 14 758-770.
66. Kamholz, J., Awatramani, R., Menichella, D., Jiang, H., Xu, W. and Shy, M. (1999) Regulation of myelin-specific gene expression. Relevance to CMT1. Ann. NY Acad. Sci., 883, 91-108.
67. LeBlanc, S.E., Jang, S.W., Ward, R.M., Wrabetz, L. and Svaren, J. (2006) Direct regulation of myelin protein zero expression by the Egr2 transactivator. J. Biol. Chem., 281, 5453-5460.
68. Mechta-Grigoriou, F., Garel, S. and Charnay, P. (2000) Nab proteins mediate a negative feedback loop controlling Krox-20 activity in the developing hindbrain. Development, 127, 119-128.
69. Maconochie, M.K., Nonchev, S., Manzanares, M., Marshall, H. and Krumlauf, R. (2001) Differences in Krox20-dependent regulation of Hoxa2 and Hoxb2 during hindbrain development. Dev. Biol., 233, 468-481.
70. Ghislain, J., Desmarquet-Trin-Dinh, C., Gilardi-Hebenstreit, P., Charnay, P. and Frain, M. (2003) Neural crest patterning: Autoregulatory and crest-specific elements co-operate for Krox20 transcriptional control. Development, 130, 941-953.
71. Mager, G.M., Ward, R.M., Srinivasan, R., Jang, S.W., Wrabetz, L. and Svaren, J. (2008) Active gene repression by the Egr2.NAB Complex during peripheral nerve myelination. J. Biol. Chem., 283, 18187-18197.
72. Peddada, S., Yasui, D.H. and LaSalle, J.M. (2006) Inhibitors of differentiation (ID1, ID2, ID3 and ID4) genes are neuronal targets of MeCP2 that are elevated in Rett syndrome. Hum. Mol. Genet., 15 2003-2014.
73. Tischfield, M.A., Bosley, T.M., Salih, M.A., Alorainy, I.A., Sener, E.C., Nester, M.J., Oystreck, D.T., Chan, W.M., Andrews, C., Erickson, R.P. et al. (2005) Homozygous HOXA1 mutations disrupt human brainstem, inner ear, cardiovascular and cognitive development. Nat. Genet., 37, 1035-1047.
74. Morrow, E.M., Yoo, S.Y., Flavell, S.W., Kim, T.K., Lin, Y., Hill, R.S., Mukaddes, N.M., Balkhy, S., Gascon, G., Hashmi, A. et al. (2008) Identifying autism loci and genes by tracing recent shared ancestry. Science, 321, 218-223.
75. Hogart, A., Nagarajan, R.P., Patzel, K.A., Yasui, D.H. and Lasalle, J.M. (2007) 15q11-13 GABAA receptor genes are normally biallelically expressed in brain yet are subject to epigenetic dysregulation in autism-spectrum disorders. Hum. Mol. Genet., 16, 691-703.
76. Courchesne, E. (2004) Brain development in autism: Early overgrowth followed by premature arrest of growth. Ment. Retard. Dev. Disabil. Res. Rev., 10, 106-111.
77. Zoghbi, H.Y. (2003) Postnatal neurodevelopmental disorders: Meeting at the synapse? Science, 302, 826-830.
78. Kondo, M., Gray, L.J., Pelka, G., Christodoulou, J., Tam, P.P.L. and Hannan, A.J. (2008) Environmental enrichment ameliorates a motor coordination deficit in a mouse model of Rett syndrome-Mecp2 gene dosage effects and BDNF expression. Eur. J. Neurosci., 12, 3342-3350.
79. Nag, N., Moriuchi, J.M., Peitzman, C.G., Ward, B.C., Klodny, N.H. and Berger-Sweeney, J.E. (2008) Environmental enrichment alters locomotor behaviour and ventricular volume in Mecp2(1lox) mice. Behav. Brain. Res., epub ahead of print.
80. Rogers, S.J. and Vismara, L.A. (2008) Evidence-based comprehensive treatments for early autism. J. Clin. Child Adolesc. Psychol., 37, 8-38.
81. Cheng, M.C., Liao, D.L., Hsiung, C.A., Chen, C.Y., Liao, Y.C. and Chen, C.H. (2008) Chronic treatment with aripiprazole induces differential gene expression in the rat frontal cortex. Int. J. Neuropsychopharmacol., 11, 207-216.
82. Koch, C. and Stratling, W.H. (2004) DNA binding of methyl-CpG-binding protein MeCP2 in human MCF7 cells. Biochemistry, 43, 5011-5021.
83. Klose, R.J., Sarraf, S.A., Schmiedeberg, L., McDermott, S.M., Stancheva, I. and Bird, A.P. (2005) DNA binding selectivity of MeCP2 due to a requirement for A/T sequences adjacent to methyl-CpG. Mol. Cell, 19, 667-678.
84. Nardelli, J., Gibson, T. and Charnay, P. (1992) Zinc finger-DNA recognition: Analysis of base specificity by site-directed mutagenesis. Nucleic Acids Res., 20, 4137-4144.
85. Swirnoff, A.H. and Milbrandt, J. (1995) DNA-binding specificity of NGFI-A and related zinc finger transcription factors. Mol. Cell. Biol., 15, 2275-2287.