Epigenetic regulation in neural crest development

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 91, Issue 8, 2011, Pages 788-796

  Liu, Yifei ^a   Xiao, Andrew ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromatin; Chromatin remodeling; Epigenetic regulation; Neural crest; Neural crest cell

Indexed keywords

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONGENITAL HEART MALFORMATION; EAR DISEASE; EMBRYO DEVELOPMENT; EPIGENETICS; HISTONE MODIFICATION; HUMAN; MANDIBULOFACIAL DYSOSTOSIS; NEURAL CREST; NEURAL CREST CELL; NEUROBLASTOMA; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; NEURAL CREST;

VERTEBRATA;

EID: 79961164002     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.20797     Document Type: Review

References (121)

1. Adams ME, Hurd EA, Beyer LA, et al. 2007. Defects in vestibular sensory epithelia and innervation in mice with loss of Chd7 function: implications for human CHARGE syndrome. J Comp Neurol 504: 519-532.
2. Agger K, Cloos PA, Christensen J, et al. 2007. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449: 731-734.
3. Albert M, Helin K. 2010. Histone methyltransferases in cancer. Semin Cell Dev Biol 21: 209-220.
4. Alsdorf R, Wyszynski DF. 2005. Teratogenicity of sodium valproate. Expert Opin Drug Saf 4: 345-353.
5. Ashe A, Morgan DK, Whitelaw NC, et al. 2008. A genome-wide screen for modifiers of transgene variegation identifies genes with critical roles in development. Genome Biol 9: R182.
6. Aybar MJ, Mayor R. 2002. Early induction of neural crest cells: lessons learned from frog, fish and chick. Curr Opin Genet Dev 12: 452-458.
7. Bajpai R, Chen DA, Rada-Iglesias A, et al. 2010. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 463: 958-962.
8. Barski A, Cuddapah S, Cui K, et al. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
9. Berger SL. 2007. The complex language of chromatin regulation during transcription. Nature 447: 407-412.
10. Bernstein BE, Meissner A, Lander ES. 2007. The mammalian epigenome. Cell 128: 669-681.
11. Betancur P, Bronner-Fraser M, Sauka-Spengler T. 2010. Assembling neural crest regulatory circuits into a gene regulatory network. Annu Rev Cell Dev Biol 26: 581-603.
12. Beuren AJ, Apitz J, Harmjanz D. 1962. Supravalvular aortic stenosis in association with mental retardation and a certain facial appearance. Circulation 26: 1235-1240.
13. Biacsi R, Kumari D, Usdin K. 2008. SIRT1 inhibition alleviates gene silencing in Fragile X mental retardation syndrome. PLoS Genet 4: e1000017.
14. Bird A. 2007. Perceptions of epigenetics. Nature 447: 396-398.
15. Bolande RP. 1974. The neurocristopathies: a unifying concept of disease arising in neural crest maldevelopment. Human Pathology 5: 409-429.
16. Bondurand N, Kuhlbrodt K, Pingault V, et al. 1999. A molecular analysis of the yemenite deaf-blind hypopigmentation syndrome: SOX10 dysfunction causes different neurocristopathies. Hum Mol Genet 8: 1785-1789.
17. Bosman EA, Penn AC, Ambrose JC, et al. 2005. Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum Mol Genet 14: 3463-3476.
18. Bracken AP, Helin K. 2009. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer 9: 773-784.
19. Briscoe J, Wilkinson DG. 2004. Establishing neuronal circuitry: Hox genes make the connection. Genes Dev 18: 1643-1648.
20. Carpenter EM, Goddard JM, Chisaka O, et al. 1993. Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118: 1063-1075.
21. Carrozza MJ, Utley RT, Workman JL, Cǒté J. 2003. The diverse functions of histone acetyltransferase complexes. Trends Genet 19: 321-329.
22. Cavellán E, Asp P, Percipalle P, Farrants AK. 2006. The WSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription. J Biol Chem 281: 16264-16271.
23. Cheung I, Shulha HP, Jiang Y, et al. 2010. Developmental regulation and individual differences of neuronal H3K4me3 epigenomes in the prefrontal cortex. Proc Natl Acad Sci U S A 107: 8824-8829.
24. Chopra VS, Hong JW, Levine M. 2009. Regulation of Hox gene activity by transcriptional elongation in Drosophila. Curr Biol 19: 688-693.
25. Couly G, Creuzet S, Bennaceur S, et al. 2002. Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129: 1061-1073.
26. Couly G, Grapin-Botton A, Coltey P, et al. 1998. Determination of the identity of the derivatives of the cephalic neural crest: incompatibility between Hox gene expression and lower jaw development. Development 125: 3445-3459.
27. Creuzet S, Couly G, Vincent C, Le Douarin NM. 2002. Negative effect of Hox gene expression on the development of the neural crest-derived facial skeleton. Development 129: 4301-4313.
28. Crews D, McLachlan JA. 2006. Epigenetics, evolution, endocrine disruption, health, and disease. Endocrinology 147(6 Suppl): S4-10.
29. Cus R, Maurus D, Kühl M. 2006. Cloning and developmental expression of WSTF during Xenopus laevis embryogenesis. Gene Expr Patterns 6: 340-346.
30. Dasen JS, Jessell TM. 2009. Hox networks and the origins of motor neuron diversity. Curr Top Dev Biol 88: 169-200.
31. Dollé P, Lufkin T, Krumlauf R, et al. 1993. Local alterations of Krox-20 and Hox gene expression in the hindbrain suggest lack of rhombomeres 4 and 5 in homozygote null Hoxa-1 (Hox-1.6) mutant embryos. Proc Natl Acad Sci U S A 90: 7666-7670.
32. Duboule D, Dollé P. 1989. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J 8: 1497-1505.
33. Dupin E, Creuzet S, Le Douarin NM. 2006. The contribution of the neural crest to the vertebrate body. Adv Exp Med Biol 589: 96-119.
34. Duvic M, Vu J. 2007. Vorinostat: a new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs 16: 1111-1120.
35. Echelard Y, Vassileva G, McMahon AP. 1994. Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development 120: 2213-2224.
36. Ekwall K. 2005. Genome-wide analysis of HDAC function. Trends Genet 21: 608-615.
37. Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT. 2004. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 18: 170-183.
38. Gammill LS, Bronner-Fraser M. 2003. Neural crest specification: migrating into genomics. Nat Rev Neurosci 4: 795-805.
39. Garcia-Fernàndez J. 2005. The genesis and evolution of homeobox gene clusters. Nat Rev Genet 6: 881-892.
40. Gaufo GO, Wu S, Capecchi MR. 2004. Contribution of Hox genes to the diversity of the hindbrain sensory system. Development 131: 1259-1266.
41. Gavalas A, Davenne M, Lumsden A, et al. 1997. Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124: 3693-3702.
42. Gendron-Maguire M, Mallo M, Zhang M, Gridley T. 1993. Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell 75: 1317-1331.
43. Gibney ER, Nolan CM. 2010. Epigenetics and gene expression. Heredity 105: 4-13.
44. Goddard JM, Rossel M, Manley NR, Capecchi MR. 1996. Mice with targeted disruption of Hoxb-1 fail to form the motor nucleus of the VIIth nerve. Development 122: 3217-3228.
45. Goldberg AD, Allis CD, Bernstein E. 2007. Epigenetics: a landscape takes shape. Cell 128: 635-638.
46. Grammatopoulos GA, Bell E, Toole L, et al. 2000. Homeotic transformation of branchial arch identity after Hoxa2 overexpression. Development 127: 5355-5365.
47. Haberland M, Mokalled MH, Montgomery RL, Olson EN. 2009. Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes Dev 23: 1625-1630.
48. Hall BK. 2009. The neural crest and neural crest cells in vertebrate development and evolution. 2nd ed. New York: Springer.
49. Hanson RD, Hess JL, Yu BD, et al. 1999. Mammalian Trithorax and polycomb-group homologues are antagonistic regulators of homeotic development. Proc Natl Acad Sci U S A 96: 14372-14377.
50. Harris J, Robert E, Källéen B, et al. 1997. Epidemiology of choanal atresia with special reference to the CHARGE association. Pediatrics 99: 363-367.
51. Herz HM, Shilatifard A. 2010. The JARID2-PRC2 duality. Genes Dev 24(9): 857-861.
52. Hirabayashi Y, Gotoh Y. 2010. Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 11: 377-388.
53. Ho L, Crabtree GR. 2010. Chromatin remodelling during development. Nature 463: 474-484.
54. Hrzenjak A, Moinfar F, Kremser ML, et al. 2010. Histone deacetylase inhibitor vorinostat suppresses the growth of uterine sarcomas in vitro and in vivo. Mol Cancer 9: 49.
55. Hsieh J, Nakashima K, Kuwabara T, et al. 2004. Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 101: 16659-16664.
56. Hurd EA, Capers PL, Blauwkamp MN, et al. 2007. Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues. Mamm Genome 18: 94-104.
57. Hurd EA, Poucher HK, Cheng K, et al. 2010. The ATP-dependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear. Development 137: 3139-3150.
58. Inoue K, Shilo K, Boerkoel CF, et al. 2002. Congenital hypomyelinating neuropathy, central dysmyelination, and Waardenburg-Hirschsprung disease: phenotypes linked by SOX10 mutation. Ann Neurol 52: 836-842.
59. Issekutz KA, Graham JMJr, Prasad C, et al. 2005. An epidemiological analysis of CHARGE syndrome: preliminary results from a Canadian study. Am J Med Genet A 133A: 309-317.
60. Källéen K, Robert E, Mastroiacovo P, et al. 1999. CHARGE Association in newborns: a registry-based study. Teratology 60: 334-343.
61. Kaplan P, Wang PP, Francke U. 2001. Williams (Williams Beuren) syndrome: a distinct neurobehavioral disorder. J Child Neurol 16: 177-190.
62. Kavanaugh SM, White LA, Kolesar JM. 2010. Vorinostat: a novel therapy for the treatment of cutaneous T-cell lymphoma. Am J Health Syst Pharm 67: 793-797.
63. Kmita M, Duboule D. 2003. Organizing axes in time and space; 25 years of colinear tinkering. Science 301: 331-333.
64. Knutson SK, Chyla BJ, Amann JM, et al. 2008. Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks. EMBO J 27: 1017-1028.
65. Kouzarides T. 2007. Chromatin modifications and their function. Cell 128: 693-705.
66. Krumlauf R. 1994. Hox genes in vertebrate development. Cell 78: 191-201.
67. Lagger G, O'Carroll D, Rembold M, et al. 2002. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J 21: 2672-2681.
68. Layman WS, McEwen DP, Beyer LA, et al. 2009. Defects in neural stem cell proliferation and olfaction in Chd7 deficient mice indicate a mechanism for hyposmia in human CHARGE syndrome. Hum Mol Genet 18: 1909-1923.
69. Lu X, Meng X, Morris CA, Keating MT. 1998. A novel human gene, WSTF, is deleted in Williams syndrome. Genomics 54: 241-249.
70. Luger K, Mader AW, Richmond RK, et al. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
71. Mahalingam D, Medina EC, Esquivel JA2nd, et al. 2010. Vorinostat enhances the activity of temsirolimus in renal cell carcinoma through suppression of survivin levels. Clin Cancer Res 16: 141-153.
72. Mark M, Lufkin T, Vonesch JL, et al. 1993. Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119: 319-338.
73. Martin DM. 2010. Chromatin remodeling in development and disease: focus on CHD7. PLoS Genet 6: e1001010.
74. Mayor R, Young R, Vargas A. 1999. Development of neural crest in Xenopus. Curr Top Dev Biol 43: 85-113.
75. Meulemans D, Bronner-Fraser M. 2004. Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7: 291-299.
76. Mikkelsen TS, Ku M, Jaffe DB, et al. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560.
77. Mills AA. 2010. Throwing the cancer switch: reciprocal roles of polycomb and trithorax proteins. Nat Rev Cancer 10: 669-682.
78. Minoux M, Rijli FM. 2010. Molecular mechanisms of cranial neural crest cell migration and patterning in craniofacial development. Development 137: 2605-2621.
79. Montgomery RL, Davis CA, Potthoff MJ, et al. 2007. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 21: 1790-1802.
80. Montgomery RL, Potthoff MJ, Haberland M, et al. 2008. Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J Clin Invest 118: 3588-3597.
81. Nihal M, Roelke CT, Wood GS. 2010. Anti-melanoma effects of vorinostat in combination with polyphenolic antioxidant (-)-epigallocatechin-3-gallate (EGCG). Pharm Res 27: 1103-1114.
82. Ordovás JM, Smith CE. 2010. Epigenetics and cardiovascular disease. Nat Rev Cardiol 7: 510-519.
83. Osborne LR. 2010. Animal models of Williams syndrome. Am J Med Genet C Semin Med Genet 154C: 209-219.
84. Pan G, Tian S, Nie J, et al. 2007. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1: 299-312.
85. Papp B, Müller J. 2006. Histone trimethylation and the maintenance of transcriptional ON and OFF states by trxG and PcG proteins. Genes Dev 20: 2041-2054.
86. Pasqualetti M, Ori M, Nardi I, Rijli FM. 2000. Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus. Development 127: 5367-5378.
87. Pearson JC, Lemons D, McGinnis W. 2005. Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6: 893-904.
88. Pingault V, Bondurand N, Kuhlbrodt K, et al. 1998. SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet 18: 171-173.
89. Pober BR. 2010. Williams-Beuren syndrome. N Engl J Med 362: 239-252.
90. Poot RA, Bozhenok L, van den Berg DL, et al. 2004. The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol 6: 1236-1244.
91. Portela A, Esteller M. 2010. Epigenetic modifications and human disease. Nat Biotechnol 28: 1057-1068.
92. Ree AH, Dueland S, Folkvord S, et al. 2010. Vorinostat, a histone deacetylase inhibitor, combined with pelvic palliative radiotherapy for gastrointestinal carcinoma: the Pelvic Radiation and Vorinostat (PRAVO) phase 1 study. Lancet Oncol 11: 459-464.
93. Rijli FM, Mark M, Lakkaraju S, et al. 1993. A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell 75: 1333-1349.
94. Sampson ER, Amin V, Schwarz EM, et al. 2011. The histone deacetylase inhibitor vorinostat selectively sensitizes fibrosarcoma cells to chemotherapy. J Orthop Res 29: 623-632.
95. Santagati F, Minoux M, Ren SY, Rijli FM. 2005. Temporal requirement of Hoxa2 in cranial neural crest skeletal morphogenesis. Development 132: 4927-4936.
96. Santagati F, Rijli FM. 2003. Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci 4: 806-818.
97. Sauka-Spengler T, Bronner-Fraser M. 2008. A gene regulatory networkorchestrates neural crest formation. Nat Rev Mol Cell Biol 9: 557-568.
98. Schnetz MP, Bartels CF, Shastri K, et al. 2009. Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res 19: 590-601.
99. Schnetz MP, Handoko L, Akhtar-Zaidi B, et al. 2010. CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression. PLoS Genet 6: e1001023.
100. Schwartz YB, Kahn TG, Nix DA, et al. 2006. Genome-wide analysis of Polycomb targets in Drosophila melanogaster. Nat Genet 38: 700-705.
101. Siebert JR, Graham JMJr, MacDonald C. 1985. Pathologic features of the charge association: support for involvement of the neural crest. Teratology 31: 331-336.
102. Soshnikova N, Duboule D. 2009. Epigenetic temporal control of mouse Hox genes in vivo. Science 324: 1320-1323.
103. Steventon B, Carmona-Fontaine C, Mayor R. 2005. Genetic network during neural crest induction: from cell specification to cell survival. Semin Cell Dev Biol 16: 647-654.
104. Strahl BD, Allis CD. 2000. The language of covalent histone modifications. Nature 403: 41-45.
105. Strobl-Mazzulla PH, Sauka-Spengler T, Bronner-Fraser M. 2010. Histone demethylase JmjD2A regulates neural crest specification. Dev Cell 19: 460-468.
106. Studer M, Lumsden A, Ariza-McNaughton L, et al. 1996. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384: 630-634.
107. Swigut T, Wysocka J. 2007. H3K27 demethylases, at long last. Cell 131(1): 29-32.
108. Terranova R, Agherbi H, Boned A, et al. 2006. Histone and DNA methylation defects at Hox genes in mice expressing a SET domain-truncated form of Mll. Proc Natl Acad Sci U S A 103: 6629-6634.
109. Thiagalingam S, Cheng KH, Lee HJ, et al. 2003. Histone deacetylases: unique players in shaping the epigenetic histone code. Ann N Y Acad Sci 983: 84-100.
110. Tolhuis B, de Wit E, Muijrers I, et al. 2006. Genome-wide profiling of PRC1 and PRC2 Polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38: 694-699.
111. Trainor PA. 2003. Making headway: the roles of Hox genes and neural crest cells in craniofacial development. ScientificWorldJournal 3: 240-264.
112. Vermeulen M, Eberl HC, Matarese F, et al. 2010. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142: 967-980.
113. Vissers LE, van Ravenswaaij CM, Admiraal R, et al. 2004. Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet 36: 955-957.
114. Wang Z, Zang C, Cui K, et al. 2009. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138: 1019-1031.
115. Williams JC, Barratt-Boyes BG, Lowe JB. 1961. Supravalvular aortic stenosis. Circulation 24: 1311-1318.
116. Wyszynski DF, Nambisan M, Surve T, et al. 2005. Increased rate of major malformations in offspring exposed to valproate during pregnancy. Neurology 64: 961-965.
117. Xiao A, Li H, Shechter D, et al. 2009. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457: 57-62.
118. Yang XJ, Seto E. 2008. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9: 206-218.
119. Yoshimura K, Kitagawa H, Fujiki R, et al. 2009. Distinct function of 2 chromatin remodeling complexes that share a common subunit, Williams syndrome transcription factor (WSTF). Proc Natl Acad Sci U S A 106: 9280-9285.
120. Yu BD, Hess JL, Horning SE, et al. 1995. Altered Hox expression and segmental identity in Mll-mutant mice. Nature 378: 505-508.
121. Zentner GE, Layman WS, Martin DM, Scacheri PC. 2010. Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A 152A: 674-686.