Mature middle and inner ears express Chd7 and exhibit distinctive pathologies in a mouse model of CHARGE syndrome

Hearing Research

Volumn 282, Issue 1-2, 2011, Pages 184-195

  Hurd, Elizabeth A ^a   Adams, Meredith E ^a   Layman, Wanda S ^a   Swiderski, Donald L ^b   Beyer, Lisa A ^b   Halsey, Karin E ^b   Benson, Jennifer M ^b   Gong, Tzy Wen ^b   Dolan, David F ^b   Raphael, Yehoash ^b   Martin, Donna M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PRESTIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY OSSICLE; AUDITORY THRESHOLD; CELL LOSS; CHD7 GENE; COCHLEAR INNERVATION; CONDUCTION DEAFNESS; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; EVOKED BRAIN STEM AUDITORY RESPONSE; GENE EXPRESSION; GENE FREQUENCY; GENE LOCATION; GENETIC CORRELATION; HAIR CELL; IMMUNOHISTOCHEMISTRY; INNER EAR; INNERVATION; MARKER GENE; MIDDLE EAR; MOUSE; NEUROEPITHELIUM; NOISE; NONHUMAN; PATHOPHYSIOLOGY; PERCEPTION DEAFNESS; PHENOTYPE; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; SPIRAL GANGLION; SYNDROME CHARGE; WILD TYPE;

ACOUSTIC STIMULATION; AGE FACTORS; ANIMALS; AUDITORY THRESHOLD; BETA-GALACTOSIDASE; CHARGE SYNDROME; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; EAR, INNER; EAR, MIDDLE; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FEMALE; GENES, REPORTER; HEARING LOSS, CONDUCTIVE; HEARING LOSS, SENSORINEURAL; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, 129 STRAIN; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, SCANNING; MOLECULAR MOTOR PROTEINS; MUTATION; NOISE; OTOACOUSTIC EMISSIONS, SPONTANEOUS; PROMOTER REGIONS, GENETIC;

EID: 82755189504     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2011.08.005     Document Type: Article

References (58)

1. Abadie V., Wiener-Vacher S., Morisseau-Durand M.P., Poree C., Amiel J., Amanou L., Peigne C., Lyonnet S., Manac'h Y. Vestibular anomalies in CHARGE syndrome: investigations on and consequences for postural development. Eur. J. Pediatr. 2000, 159:569-574.
2. Adams M.E., Hurd E.A., Beyer L.A., Swiderski D.L., Raphael Y., Martin D.M. 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.
3. Admiraal R.J., Huygen P.L. Vestibular areflexia as a cause of delayed motor skill development in children with the CHARGE association. Int. J. Pediatr. Otorhinolaryngol. 1997, 39:205-222.
4. Amiel J., Attiee-Bitach T., Marianowski R., Cormier-Daire V., Abadie V., Bonnet D., Gonzales M., Chemouny S., Brunelle F., Munnich A., Manach Y., Lyonnet S. Temporal bone anomaly proposed as a major criteria for diagnosis of CHARGE syndrome. Am. J. Med. Genet. A 2001, 99:124-127.
5. Arnold J.S., Braunstein E.M., Ohyama T., Groves A.K., Adams J.C., Brown M.C., Morrow B.E. Tissue-specific roles of Tbx1 in the development of the outer, middle and inner ear, defective in 22q11DS patients. Hum. Mol. Genet. 2006, 15:1629-1639.
6. Bergman J.E., Bosman E.A., van Ravenswaaij-Arts C.M., Steel K.P. Study of smell and reproductive organs in a mouse model for CHARGE syndrome. Eur. J. Hum. Genet. 2010, 18:171-177.
7. Beyer L.A., Odeh H., Probst F.J., Lambert E.H., Dolan D.F., Camper S.A., Kohrman D.C., Raphael Y. Hair cells in the inner ear of the pirouette and shaker 2 mutant mice. J. Neurocytol. 2000, 29:227-240.
8. Bosman E.A., Penn A.C., Ambrose J.C., Kettleborough R., Stemple D.L., Steel K.P. Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum. Mol. Genet. 2005, 14:3463-3476.
9. Calvert J.A., Dedos S.G., Hawker K., Fleming M., Lewis M.A., Steel K.P. A missense mutation in Fgfr1 causes ear and skull defects in hush puppy mice. Mamm. Genome 2011, 22:290-305.
10. Dallos P. Cochlear amplification, outer hair cells and prestin. Curr. Opin. Neurobiol. 2008, 18:370-376.
11. Desai U., Rosen H., Mulliken J.B., Gopen Q., Meara J.G., Rogers G.F. Audiologic findings in Pfeiffer syndrome. J. Craniofac. Surg. 2010, 21:1411-1418.
12. Dhooge I., Lemmerling M., Lagache M., Standaert L., Govaert P., Mortier G. Otological manifestations of CHARGE association. Ann. Otol. Rhinol. Laryngol. 1998, 107:935-941.
13. Edwards B.M., Van Riper L.A., Kileny P.R. Clinical manifestations of CHARGE Association. Int. J. Pediatr. Otorhinolaryngol. 1995, 33:23-42.
14. Edwards B.M., Kileny P.R., Van Riper L.A. CHARGE syndrome: a window of opportunity for audiologic intervention. Pediatrics 2002, 110:119-126.
15. Fekete D.M. Development of the vertebrate ear: insights from knockouts and mutants. Trends Neurosci. 1999, 22:263-269.
16. Funke B., Epstein J.A., Kochilas L.K., Lu M.M., Pandita R.K., Liao J., Bauerndistel R., Schuler T., Schorle H., Brown M.C., Adams J., Morrow B.E. Mice overexpressing genes from the 22q11 region deleted in velo-cardio-facial syndrome/DiGeorge syndrome have middle and inner ear defects. Hum. Mol. Genet. 2001, 10:2549-2556.
17. Gao X., Gordon D., Zhang D., Browne R., Helms C., Gillum J., Weber S., Devroy S., Swaney S., Dobbs M., Morcuende J., Sheffield V., Lovett M., Bowcock A., Herring J., Wise C. CHD7 gene polymorphisms are associated with susceptibility to idiopathic scoliosis. Am. J. Hum. Genet. 2007, 80:957-965.
18. Gehr D.D., Janssen T., Michaelis C.E., Deingruber K., Lamm K. Middle ear and cochlear disorders result in different DPOAE growth behaviour: implications for the differentiation of sound conductive and cochlear hearing loss. Hear Res. 2004, 193:9-19.
19. Glueckert R., Rask-Andersen H., Sergi C., Schmutzhard J., Mueller B., Beckmann F., Rittinger O., Hoefsloot L.H., Schrott-Fischer A., Janecke A.R. 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.
20. Guyot J.P., Gacek R.R., DiRaddo P. The temporal bone anomaly in CHARGE association. Arch. Otolaryngol. Head Neck Surg. 1987, 113:321-324.
21. Haginomori S., Sando I., Miura M., Casselbrant M.L. Temporal bone histopathology in CHARGE association. Ann. Otol. Rhinol. Laryngol. 2002, 111:397-401.
22. Harding G.W., Bohne B.A., Vos J.D. The effect of an age-related hearing loss gene (Ahl) on noise-induced hearing loss and cochlear damage from low-frequency noise. Hear Res. 2005, 204:90-100.
23. Hawker K., Fuchs H., Angelis M.H., Steel K.P. Two new mouse mutants with vestibular defects that map to the highly mutable locus on chromosome 4. Int. J. Audiol. 2005, 44:171-177.
24. Hurd E.A., Poucher H.K., Cheng K., Raphael Y., Martin D.M. The ATP-dependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear. Development 2010, 137:3139-3150.
25. Hurd E.A., Capers P.L., Blauwkamp M.N., Adams M.E., Raphael Y., Poucher H.K., Martin D.M. 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.
26. Jongmans M.C., Admiraal R.J., van der Donk K.P., Vissers L.E., Baas A.F., Kapusta L., van Hagen J.M., Donnai D., de Ravel T.J., Veltman J.A., Geurts van Kessel A., De Vries B.B., Brunner H.G., Hoefsloot L.H., van Ravenswaaij C.M. CHARGE syndrome: the phenotypic spectrum of mutations in the CHD7 gene. J. Med. Genet. 2006, 43:306-314.
27. Karolyi I.J., Dootz G.A., Halsey K., Beyer L., Probst F.J., Johnson K.R., Parlow A.F., Raphael Y., Dolan D.F., Camper S.A. Dietary thyroid hormone replacement ameliorates hearing deficits in hypothyroid mice. Mamm. Genome 2007, 18:596-608.
28. Kiernan A.E., Erven A., Voegeling S., Peters J., Nolan P., Hunter J., Bacon Y., Steel K.P., Brown S.D., Guenet J.L. ENU mutagenesis reveals a highly mutable locus on mouse chromosome 4 that affects ear morphogenesis. Mamm. Genome 2002, 13:142-148.
29. Lalani S.R., Safiullah A.M., Fernbach S.D., Harutyunyan K.G., Thaller C., Peterson L.E., McPherson J.D., Gibbs R.A., White L.D., Hefner M., Davenport S.L., Graham J.M., Bacino C.A., Glass N.L., Towbin J.A., Craigen W.J., Neish S.R., Lin A.E., Belmont J.W. Spectrum of CHD7 mutations in 110 individuals with CHARGE syndrome and genotype-phenotype Correlation. Am. J. Hum. Genet. 2006, 78:303-314.
30. Lanson B.G., Green J.E., Roland J.T., Lalwani A.K., Waltzman S.B. Cochlear implantation in Children with CHARGE syndrome: therapeutic decisions and outcomes. Laryngoscope 2007, 117:1260-1266.
31. Layman W.S., Hurd E.A., Martin D.M. Reproductive dysfunction and decreased GnRH neurogenesis in a mouse model of CHARGE syndrome. Hum. Mol. Genet. 2011, 20:3138-3150.
32. Layman W.S., McEwen D.P., Beyer L.A., Lalani S.R., Fernbach S.D., Oh E., Swaroop A., Hegg C.C., Raphael Y., Martens J.R., Martin D.M. 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.
33. Lemmerling M., Dhooge I., Mollet P., Mortier G., Van Cauwenberge P., Kunnen M. CT of the temporal bone in the CHARGE association. Neuroradiology 1998, 40:462-465.
34. Lenz D.R., Dror A.A., Wekselman G., Fuchs H., Hrabe de Angelis M., Avrahamn K.B. The inner ear phenotype pf Volchok (Vlk): an ENU-induced mouse model for CHARGE syndrome. Audiol. Med. 2010, 1-10.
35. Martin D.M. Chromatin remodeling in development and disease: focus on CHD7. PLoS Genet. 2010, 6:e1001010.
36. Matsuo I., Kuratani S., Kimura C., Takeda N., Aizawa S. Mouse Otx2 functions in the formation and patterning of rostral head. Genes. Dev. 1995, 9:2646-2658.
37. Moraes F., Novoa A., Jerome-Majewska L.A., Papaioannou V.E., Mallo M. Tbx1 is required for proper neural crest migration and to stabilize spatial patterns during middle and inner ear development. Mech. Dev. 2005, 122:199-212.
38. Morgan D., Bailey M., Phelps P., Bellman S., Grace A., Wyse R. Ear-nose-throat abnormalities in the CHARGE association. Arch. Otolaryngol. Head Neck Surg. 1993, 119:49-54.
39. Morimoto A.K., Wiggins R.H., Hudgins P.A., Hedlund G.L., Hamilton B., Mukherji S.K., Telian S.A., Harnsberger H.R. Absent semicircular canals in CHARGE syndrome: radiologic spectrum of findings. AJNR Am. J. Neuroradiol. 2006, 27:1663-1671.
40. Morsli H., Tuorto F., Choo D., Postiglione M.P., Simeone A., Wu D.K. Otx1 and Otx2 activities are required for the normal development of the mouse inner ear. Development 1999, 126:2335-2343.
41. Noben-Trauth K., Zheng Q.Y., Johnson K.R. Association of cadherin 23 with polygenic inheritance and genetic modification of sensorineural hearing loss. Nat. Genet. 2003, 35:21-23.
42. Nolen L.D., Amor D., Haywood A., St Heaps L., Willcock C., Mihelec M., Tam P., Billson F., Grigg J., Peters G., Jamieson R.V. Deletion at 14q22-23 indicates a contiguous gene syndrome comprising anophthalmia, pituitary hypoplasia, and ear anomalies. Am J Med Genet A 2006, 140:1711-1718.
43. Osborne M.P., Comis S.D. Preparation of inner ear sensory hair bundles for high resolution scanning electron microscopy. Scanning Microsc. 1991, 5:555-564.
44. Park K., Ueno K., Lim D.J. Developmental anatomy of the eustachian tube and middle ear in mice. Am. J. Otol. 1992, 13:93-100.
45. Pau H., Hawker K., Fuchs H., De Angelis M.H., Steel K.P. Characterization of a new mouse mutant, flouncer, with a balance defect and inner ear malformation. Otol. Neurotol. 2004, 25:707-713.
46. Qin Z., Wood M., Rosowski J.J. Measurement of conductive hearing loss in mice. Hear Res. 2010, 263:93-103.
47. Randall V., McCue K., Roberts C., Kyriakopoulou V., Beddow S., Barrett A.N., Vitelli F., Prescott K., Shaw-Smith C., Devriendt K., Bosman E., Steffes G., Steel K.P., Simrick S., Basson M.A., Illingworth E., Scambler P.J. Great vessel development requires biallelic expression of Chd7 and Tbx1 in pharyngeal ectoderm in mice. J. Clin. Invest. 2009, 119:3301-3310.
48. Reyes M.R., LeBlanc E.M., Bassila M.K. Hearing loss and otitis media in velo-cardio-facial syndrome. Int. J. Pediatr. Otorhinolaryngol. 1999, 47:227-233.
49. Sanlaville D., Etchevers H.C., Gonzales M., Martinovic J., Clement-Ziza M., Delezoide A.L., Aubry M.C., Pelet A., Chemouny S., Cruaud C., Audollent S., Esculpavit C., Goudefroye G., Ozilou C., Fredouille C., Joye N., Morichon-Delvallez N., Dumez Y., Weissenbach J., Munnich A., Amiel J., Encha-Razavi F., Lyonnet S., Vekemans M., Attie-Bitach T. Phenotypic spectrum of CHARGE syndrome in fetuses with CHD7 truncating mutations correlates with expression during human development. J. Med. Genet. 2006, 43:211-217.
50. Shah U.K., Ohlms L.A., Neault M.W., Willson K.D., McGuirt W.F., Hobbs N., Jones D.T., McGill T.J., Healy G.B. Otologic management in children with the CHARGE association. Int. J. Pediatr. Otorhinolaryngol. 1998, 44:139-147.
51. Takada I., Mihara M., Suzawa M., Ohtake F., Kobayashi S., Igarashi M., Youn M.Y., Takeyama K., Nakamura T., Mezaki Y., Takezawa S., Yogiashi Y., Kitagawa H., Yamada G., Takada S., Minami Y., Shibuya H., Matsumoto K., Kato S. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat. Cell Biol. 2007, 9:1273-1285.
52. Tellier A.L., Cormier-Daire V., Abadie V., Amiel J., Sigaudy S., Bonnet D., de Lonlay-Debeney P., Morrisseau-Durand M.P., Hubert P., Michel J.L., Jan D., Dollfus H., Baumann C., Labrune P., Lacombe D., Philip N., LeMerrer M., Briard M.L., Munnich A., Lyonnet S. CHARGE syndrome: report of 47 cases and review. Am. J. Med. Genet. 1998, 76:402-409.
53. Thelin J.W., Mitchell J.A., Hefner M.A., Davenport S.L. CHARGE syndrome. Part II. Hearing loss. Int. J. Pediatr. Otorhinolaryngol. 1986, 12:145-163.
54. Vissers L.E., van Ravenswaaij C.M., Admiraal R., Hurst J.A., de Vries B.B., Janssen I.M., van der Vliet W.A., Huys E.H., de Jong P.J., Hamel B.C., Schoenmakers E.F., Brunner H.G., Veltman J.A., van Kessel A.G. Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat. Genet. 2004, 36:955-957.
55. Wiener-Vacher S.R., 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.
56. Wright C.G., Brown O.E., Meyerhoff W.L., Rutledge J.C. Auditory and temporal bone abnormalities in CHARGE association. Ann. Otol. Rhinol. Laryngol. 1986, 95:480-486.
57. Wright E.M., O'Connor R., Kerr B.A. Radial aplasia in CHARGE syndrome: a new association. Eur. J. Med. Genet. 2009, 52:239-241.
58. Zentner G.E., Layman W.S., Martin D.M., Scacheri P.C. Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A 2010, 152A:674-686.