Chromodomain proteins in development: Lessons from CHARGE syndrome

Clinical Genetics

Volumn 78, Issue 1, 2010, Pages 11-20

  Layman, W S ^a   Hurd, E A ^b   Martin, D M ^a,b  

^a Department of Human Genetics ^*  (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

CHARGE syndrome; CHD7; Chromodomain helicase DNA binding gene 7

Indexed keywords

ARTICLE; BINDING SITE; CELL FREE SYSTEM; CHD7 GENE; DNA FLANKING REGION; EXPERIMENTAL MOUSE; GENE; GENE FUNCTION; GENE MUTATION; HUMAN; INNER EAR MALFORMATION; KALLMANN SYNDROME; MULTIPLE MALFORMATION SYNDROME; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; SMELLING DISORDER; SOFT TISSUE DEFECT; SYNDROME CHARGE; ANIMAL; DEAFBLINDNESS; DEFICIENCY; GROWTH, DEVELOPMENT AND AGING; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNDROME;

CHD7 PROTEIN, HUMAN; CHD7 PROTEIN, MOUSE; DNA BINDING PROTEIN; DNA HELICASE;

ABNORMALITIES, MULTIPLE; ANIMALS; DEAF-BLIND DISORDERS; DNA HELICASES; DNA-BINDING PROTEINS; GROWTH AND DEVELOPMENT; HUMANS; MICE; SYNDROME;

EID: 77954587234     PISSN: 00099163     EISSN: 13990004     Source Type: Journal    
DOI: 10.1111/j.1399-0004.2010.01446.x     Document Type: Article

References (86)

1. Hall BD. Choanal atresia and associated multiple anomalies. J Pediatr 1979, 95:395-398.
2. Aramaki M, Udaka T, Kosaki R. Phenotypic spectrum of CHARGE syndrome with CHD7 mutations. J Pediatr 2006, 148:410-414.
3. Jongmans MC, Admiraal RJ, van der Donk KP. CHARGE syndrome: the phenotypic spectrum of mutations in the CHD7 gene. J Med Genet 2006, 43:306-314.
4. Lalani SR, Safiullah AM, Fernbach SD. Spectrum of CHD7 mutations in 110 individuals with CHARGE syndrome and genotype-phenotype correlation. Am J Hum Genet 2006, 78:303-314.
5. Sanlaville D, Etchevers HC, Gonzales M. Phenotypic spectrum of CHARGE syndrome in fetuses with CHD7 truncating mutations correlates with expression during human development. J Med Genet 2006, 43:211-217.
6. Vissers LE, van Ravenswaaij CM, Admiraal R. Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet 2004, 36:955-957.
7. Harris J, Robert E, Kallen B. Epidemiology of choanal atresia with special reference to the CHARGE association. Pediatrics 1997, 99:363-367.
8. Issekutz KA, Graham JM, Prasad C, Smith IM, Blake KD. An epidemiological analysis of CHARGE syndrome: preliminary results from a Canadian study. Am J Med Genet A 2005, 133:309-317.
9. Kallen K, Robert E, Mastroiacovo P, Castilla EE, Kallen B. CHARGE Association in newborns: a registry-based study. Teratology 1999, 60:334-343.
10. Sanlaville D, Verloes A. CHARGE syndrome: an update. Eur J Hum Genet 2007, 15:389-399.
11. Vuorela P, Ala-Mello S, Saloranta C. Molecular analysis of the CHD7 gene in CHARGE syndrome: identification of 22 novel mutations and evidence for a low contribution of large CHD7 deletions. Genet Med 2007, 9:690-694.
12. Delahaye A, Sznajer Y, Lyonnet S. Familial CHARGE syndrome because of CHD7 mutation: clinical intra- and interfamilial variability. Clin Genet 2007, 72:112-121.
13. Jongmans MC, Hoefsloot LH, van der Donk KP. Familial CHARGE syndrome and the CHD7 gene: a recurrent missense mutation, intrafamilial recurrence and variability. Am J Med Genet A 2008, 146:43-50.
14. Pauli S, Pieper L, Haberle J. Proven germline mosaicism in a father of two children with CHARGE syndrome. Clin Genet 2009, 75:473-479.
15. Alazami AM, Alzahrani F, Alkuraya FS. Expanding the " E" in CHARGE. Am J Med Genet A 2008, 146A:1890-1892.
16. Asakura Y, Toyota Y, Muroya K. Endocrine and radiological studies in patients with molecularly confirmed CHARGE syndrome. J Clin Endocrinol Metab 2008, 93:920-924.
17. Bergman JE, de Wijs I, Jongmans MC, Admiraal RJ, Hoefsloot LH, van Ravenswaaij-Arts CM. Exon copy number alterations of the CHD7 gene are not a major cause of CHARGE and CHARGE-like syndrome. Eur J Med Genet 2008, 51:417-425.
18. Chopra C, Baretto R, Duddridge M, Browning MJ. T-cell immunodeficiency in CHARGE syndrome. Acta Paediatr 2009, 98:408-410.
19. Felix TM, Hanshaw BC, Mueller R, Bitoun P, Murray JC. CHD7 gene and non-syndromic cleft lip and palate. Am J Med Genet A 2006, 140:2110-2114.
20. Fujita K, Aida N, Asakura Y. Abnormal basiocciput development in CHARGE syndrome. AJNR Am J Neuroradiol 2009, 30:629-634.
21. Gennery AR, Slatter MA, Rice J. Mutations in CHD7 in patients with CHARGE syndrome cause T-B + natural killer cell + severe combined immune deficiency and may cause Omenn-like syndrome. Clin Exp Immunol 2008, 153:75-80.
22. Hoover-Fong J, Savage WJ, Lisi E, Winkelstein J, Thomas GH, Hoefsloot LH, Loeb DM. Congenital T cell deficiency in a patient with CHARGE syndrome. J Pediatr 2009, 154:140-142.
23. Johnson D, Morrison N, Grant L. Confirmation of CHD7 as a cause of CHARGE association identified by mapping a balanced chromosome translocation in affected monozygotic twins. J Med Genet 2006, 43:280-284.
24. Jongmans MC, van Ravenswaaij-Arts CM, Pitteloud N. CHD7 mutations in patients initially diagnosed with Kallmann syndrome-the clinical overlap with CHARGE syndrome. Clin Genet 2009, 75:65-71.
25. Jyonouchi S, McDonald-McGinn DM, Bale S, Zackai EH, Sullivan KE. CHARGE (coloboma, heart defect, atresia choanae, retarded growth and development, genital hypoplasia, ear anomalies/deafness) syndrome and chromosome 22q11.2 deletion syndrome: a comparison of immunologic and nonimmunologic phenotypic features. Pediatrics 2009, 123:e871-e877.
26. Kim HG, Kurth I, Lan F. Mutations in CHD7, encoding a chromatin-remodeling protein, cause idiopathic hypogonadotropic hypogonadism and Kallmann syndrome. Am J Hum Genet 2008, 83:511-519.
27. Lee YW, Kim SC, Shin YL. Clinical and genetic analysis of the CHD7 gene in Korean patients with CHARGE syndrome. Clin Genet 2009, 75:290-293.
28. Ogata T, Fujiwara I, Ogawa E, Sato N, Udaka T, Kosaki K. Kallmann syndrome phenotype in a female patient with CHARGE syndrome and CHD7 mutation. Endocr J 2006, 53:741-743.
29. Sanka M, Tangsinmankong N, Loscalzo M, Sleasman JW, Dorsey MJ. Complete DiGeorge syndrome associated with CHD7 mutation. J Allergy Clin Immunol 2007, 120:952-954.
30. Udaka T, Okamoto N, Aramaki M. An Alu retrotransposition-mediated deletion of CHD7 in a patient with CHARGE syndrome. Am J Med Genet A 2007, 143:721-726.
31. Van de Laar I, Dooijes D, Hoefsloot L, Simon M, Hoogeboom J, Devriendt K. Limb anomalies in patients with CHARGE syndrome: an expansion of the phenotype. Am J Med Genet A 2007, 143A:2712-2715.
32. Wincent J, Holmberg E, Stromland K. CHD7 mutation spectrum in 28 Swedish patients diagnosed with CHARGE syndrome. Clin Genet 2008, 74:31-38.
33. Wright EM, O'Connor R, Kerr BA. Radial aplasia in CHARGE syndrome: a new association. Eur J Med Genet 2009, 52:239-241.
34. Writzl K, Cale CM, Pierce CM, Wilson LC, Hennekam RC. Immunological abnormalities in CHARGE syndrome. Eur J Med Genet 2007, 50:338-345.
35. Zentner GE, Layman WS, Martin DM, Scacheri PC. Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A 2010, 152A:674-686.
36. Azoulay R, Fallet-Bianco C, Garel C, Grabar S, Kalifa G, Adamsbaum C. MRI of the olfactory bulbs and sulci in human fetuses. Pediatr Radiol 2006, 36:97-107.
37. Blustajn J, Kirsch CF, Panigrahy A, Netchine I. Olfactory anomalies in CHARGE syndrome: imaging findings of a potential major diagnostic criterion. AJNR Am J Neuroradiol 2008, 29:1266-1269.
38. Chalouhi C, Faulcon P, Le Bihan C, Hertz-Pannier L, Bonfils P, Abadie V. Olfactory evaluation in children: application to the CHARGE syndrome. Pediatrics 2005, 116:e81-e88.
39. Layman WS, McEwen DP, Beyer LA. Defects in neural stem cell proliferation and olfaction in Chd7 deficient mice indicate a mechanism for hyposmia in human CHARGE syndrome. Hum Mol Genet 2009, 18:1909-1923.
40. Pinto G, Abadie V, Mesnage R. CHARGE syndrome includes hypogonadotropic hypogonadism and abnormal olfactory bulb development. J Clin Endocrinol Metab 2005, 90:5621-5626.
41. Bosman EA, Penn AC, Ambrose JC, Kettleborough R, Stemple DL, Steel KP. Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum Mol Genet 2005, 14:3463-3476.
42. Hurd EA, Capers PL, Blauwkamp MN. Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues. Mamm Genome 2007, 18:94-104.
43. Glueckert R, Rask-Andersen H, Sergi C. Histology and synchrotron radiation-based microtomography of the inner ear in a molecularly confirmed case of CHARGE syndrome. Am J Med Genet A 2010, 152A:665-673.
44. Morimoto AK, Wiggins RH. Absent semicircular canals in CHARGE syndrome: radiologic spectrum of findings. AJNR Am J Neuroradiol 2006, 27:1663-1671.
45. Satar B, Mukherji SK, Telian SA. Congenital aplasia of the semicircular canals. Otol Neurotol 2003, 24:437-446.
46. Arndt S, Laszig R, Beck R. Spectrum of hearing disorders and their management in children with CHARGE syndrome. Otol Neurotol 2010, 31:67-73.
47. Abadie V, Wiener-Vacher S, Morisseau-Durand MP. Vestibular anomalies in CHARGE syndrome: investigations on and consequences for postural development. Eur J Pediatr 2000, 159:569-574.
48. Wiener-Vacher SR, Amanou L, Denise P, Narcy P, Manach Y. Vestibular function in children with the CHARGE association. Arch Otolaryngol Head Neck Surg 1999, 125:342-347.
49. Adams ME, Hurd EA, Beyer LA, Swiderski DL, Raphael Y, Martin DM. Defects in vestibular sensory epithelia and innervation in mice with loss of Chd7 function: implications for human CHARGE syndrome. J Comp Neurol 2007, 504:519-532.
50. Hawker K, Fuchs H, Angelis MH, Steel KP. Two new mouse mutants with vestibular defects that map to the highly mutable locus on chromosome 4. Int J Audiol 2005, 44:171-177.
51. Kiernan AE, Erven A, Voegeling S. ENU mutagenesis reveals a highly mutable locus on mouse Chromosome 4 that affects ear morphogenesis. Mamm Genome 2002, 13:142-148.
52. Pau H, Hawker K, Fuchs H, De Angelis MH, Steel KP. Characterization of a new mouse mutant, flouncer, with a balance defect and inner ear malformation. Otol Neurotol 2004, 25:707-713.
53. Martin P, Swanson GJ. Descriptive and experimental analysis of the epithelial remodellings that control semicircular canal formation in the developing mouse inner ear. Dev Biol 1993, 159:549-558.
54. Salminen M, Meyer BI, Bober E, Gruss P. Netrin 1 is required for semicircular canal formation in the mouse inner ear. Development 2000, 127:13-22.
55. Bhagavath B, Podolsky RH, Ozata M. Clinical and molecular characterization of a large sample of patients with hypogonadotropic hypogonadism. Fertil Steril 2006, 85:706-713.
56. Kim HG, Bhagavath B, Layman LC. Clinical manifestations of impaired GnRH neuron development and function. Neurosignals 2008, 16:165-182.
57. Chung WC, Moyle SS, Tsai PS. Fibroblast growth factor 8 signaling through fibroblast growth factor receptor 1 is required for the emergence of gonadotropin-releasing hormone neurons. Endocrinology 2008, 149:4997-5003.
58. Falardeau J, Chung WC, Beenken A. Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest 2008, 118:2822-2831.
59. Hardelin JP, Dode C. The complex genetics of Kallmann syndrome: KAL1, FGFR1, FGF8, PROKR2, PROK2, et al. Sex Dev 2008, 2:181-193.
60. Bergman JE, Bosman EA, van Ravenswaaij-Arts CM, Steel KP. Study of smell and reproductive organs in a mouse model for CHARGE syndrome. Eur J Hum Genet 2009, 18(2):171-177.
61. Ho L, Crabtree GR. Chromatin remodelling during development. Nature 2010, 463:474-484.
62. Hall JA, Georgel PT. CHD proteins: a diverse family with strong ties. Biochem Cell Biol 2007, 85:463-476.
63. Marfella CG, Imbalzano AN. The Chd family of chromatin remodelers. Mutat Res 2007, 618:30-40.
64. Boyer LA, Latek RR, Peterson CL. The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol 2004, 5:158-163.
65. Schnetz MP, Bartels CF, Shastri K. Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res 2009, 19(4):590-601.
66. Bajpai R, Chen DA, Rada-Iglesias A. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 2010, 463:958-962.
67. Takada I, Mihara M, Suzawa M. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol 2007, 9:1273-1285.
68. Srinivasan S, Dorighi KM, Tamkun JW. Drosophila Kismet regulates histone H3 lysine 27 methylation and early elongation by RNA polymerase II. PLoS Genet 2008, 4:1-15.
69. Phippard D, Lu L, Lee D, Saunders JC, Crenshaw EB. Targeted mutagenesis of the POU-domain gene Brn4/Pou3f4 causes developmental defects in the inner ear. J Neurosci 1999, 19:5980-5989.
70. Vore AP, Chang EH, Hoppe JE. Deletion of and novel missense mutation in POU3F4 in 2 families segregating X-linked nonsyndromic deafness. Arch Otolaryngol Head Neck Surg 2005, 131:1057-1063.
71. Abdelhak S, Kalatzis V, Heilig R. A human homologue of the Drosophila eyes absent gene underlies branchio-oto-renal (BOR) syndrome and identifies a novel gene family. Nat Genet 1997, 15:157-164.
72. Xu PX, Adams J, Peters H, Brown MC, Heaney S, Maas R. Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nat Genet 1999, 23:113-117.
73. Hatch EP, Noyes CA, Wang X, Wright TJ, Mansour SL. Fgf3 is required for dorsal patterning and morphogenesis of the inner ear epithelium. Development 2007, 134:3615-3625.
74. Mansour SL. Targeted disruption of int-2 (fgf-3) causes developmental defects in the tail and inner ear. Mol Reprod Dev 1994, 39:62-67. discussion 67-68.
75. Tekin M, Hismi BO, Fitoz S. Homozygous mutations in fibroblast growth factor 3 are associated with a new form of syndromic deafness characterized by inner ear agenesis, microtia, and microdontia. Am J Hum Genet 2007, 80:338-344.
76. Milunsky JM, Zhao G, Maher TA, Colby R, Everman DB. LADD syndrome is caused by FGF10 mutations. Clin Genet 2006, 69:349-354.
77. Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel K, Fritzsch B. Expression and function of FGF10 in mammalian inner ear development. Dev Dyn 2003, 227:203-215.
78. Koch B, Goold A, Egelhoff J, Benton C. Partial absence of the posterior semicircular canal in Alagille syndrome: CT findings. Pediatr Radiol 2006, 36:977-979.
79. Laclef C, Souil E, Demignon J, Maire P. Thymus, kidney and craniofacial abnormalities in Six 1 deficient mice. Mech Dev 2003, 120:669-679.
80. Ruf RG, Xu PX, Silvius D. SIX1 mutations cause branchio-oto-renal syndrome by disruption of EYA1-SIX1-DNA complexes. Proc Natl Acad Sci U S A 2004, 101:8090-8095.
81. Zheng W, Huang L, Wei ZB, Silvius D, Tang B, Xu PX. The role of Six1 in mammalian auditory system development. Development 2003, 130:3989-4000.
82. Kawauchi S, Shou J, Santos R. Fgf8 expression defines a morphogenetic center required for olfactory neurogenesis and nasal cavity development in the mouse. Development 2005, 132:5211-5223.
83. Meyers EN, Lewandoski M, Martin GR. An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 1998, 18:136-141.
84. Ng KL, Li JD, Cheng MY, Leslie FM, Lee AG, Zhou QY. Dependence of olfactory bulb neurogenesis on prokineticin 2 signaling. Science 2005, 308:1923-1927.
85. Zhang C, Ng KL, Li JD. Prokineticin 2 is a target gene of proneural basic helix-loop-helix factors for olfactory bulb neurogenesis. J Biol Chem 2007, 282:6917-6921.
86. Matsumoto S, Yamazaki C, Masumoto KH. Abnormal development of the olfactory bulb and reproductive system in mice lacking prokineticin receptor PKR2. Proc Natl Acad Sci U S A 2006, 103:4140-4145.