Delayed fusion and altered gene expression contribute to semicircular canal defects in Chd7 deficient mice

Mechanisms of Development

Volumn 129, Issue 9-12, 2012, Pages 308-323

  Hurd, Elizabeth A ^a   Micucci, Joseph A ^a   Reamer, Elyse N ^a   Martin, Donna M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

CHD7; Chromatin remodeling; Cristae; Gene regulation; Inner ear morphogenesis; Semicircular canal

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; DNA BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 10; JAGGED1; NETRIN 1; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR OTX; TRANSCRIPTION FACTOR OTX1; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BMP2 GENE; BMP4 GENE; CHROMODOMAIN HELICASE DNA BINDING PROTEIN 7 GENE; CONTROLLED STUDY; DEVELOPMENTAL GENE; EMBRYO; FEMALE; FGF10 GENE; GENE; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE FUNCTION; HETEROZYGOSITY LOSS; HMX3 GENE; INTERNAL AUDITORY CANAL; LMO4 GENE; MORPHOGENESIS; MOUSE; MSX1 GENE; NETRIN 1 GENE; NONHUMAN; PRIORITY JOURNAL; SEMICIRCULAR CANAL;

ANIMALS; CELL PROLIFERATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROZYGOTE; MESODERM; MICE; MORPHOGENESIS; MUTATION; NERVE GROWTH FACTORS; SEMICIRCULAR CANALS; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 84867901153     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2012.06.002     Document Type: Article

References (46)

1. Acampora D., Mazan S., Avantaggiato V., Barone P., Tuorto F., Lallemand Y., Brulet P., Simeone A. Epilepsy and brain abnormalities in mice lacking the Otx1 gene. Nat. Genet. 1996, 14:218-222.
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. Alsina B., Giraldez F., Pujades C. Patterning and cell fate in ear development. Int. J. Dev. Biol. 2009, 53:1503-1513.
4. 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.
5. Bok J., Chang W., Wu D.K. Patterning and morphogenesis of the vertebrate inner ear. Int. J. Dev. Biol. 2007, 51:521-533.
6. 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.
7. Chang W., Brigande J.V., Fekete D.M., Wu D.K. The development of semicircular canals in the inner ear: role of FGFs in sensory cristae. Development 2004, 131:4201-4211.
8. Chang W., Lin Z., Kulessa H., Hebert J., Hogan B.L., Wu D.K. Bmp4 is essential for the formation of the vestibular apparatus that detects angular head movements. PLoS Genet. 2008, 4:e1000050.
9. Chang W., Nunes F.D., De Jesus-Escobar J.M., Harland R., Wu D.K. Ectopic noggin blocks sensory and nonsensory organ morphogenesis in the chicken inner ear. Dev. Biol. 1999, 216:369-381.
10. Chang W., ten Dijke P., Wu D.K. BMP pathways are involved in otic capsule formation and epithelial-mesenchymal signaling in the developing chicken inner ear. Dev. Biol. 2002, 251:380-394.
11. Chatterjee S., Kraus P., Lufkin T. A symphony of inner ear developmental control genes. BMC Genet. 2010, 11:68.
12. Crickmore M.A., Mann R.S. The control of size in animals: insights from selector genes. Bioessays 2008, 30:843-853.
13. Deng M., Pan L., Xie X.L., Gan L. Requirement for Lmo4 in the vestibular morphogenesis of mouse inner ear. Dev. Biol. 2010, 338:38-49.
14. Engelen E., Akinci U., Bryne J.C., Hou J., Gontan C., Moen M., Szumska D., Kockx C., van Ijcken W., Dekkers D.H., Demmers J., Rijkers E.J., Bhattacharya S., Philipsen S., Pevny L.H., Grosveld F.G., Rottier R.J., Lenhard B., Poot R.A. Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes. Nat. Genet. 2011, 43:607-611.
15. Fekete D.M. Development of the vertebrate ear: insights from knockouts and mutants. Trends Neurosci. 1999, 22:263-269.
16. Fekete D.M., Campero A.M. Axon guidance in the inner ear. Int. J. Dev. Biol. 2007, 51:549-556.
17. Fekete D.M., Wu D.K. Revisiting cell fate specification in the inner ear. Curr. Opin. Neurobiol. 2002, 12:35-42.
18. Haddon C.M., Lewis J.H. Hyaluronan as a propellant for epithelial movement: the development of semicircular canals in the inner ear of Xenopus. Development 1991, 112:541-550.
19. Hebert J.M., McConnell S.K. Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 2000, 222:296-306.
20. 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.
21. 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.
22. Kelley M.W. Regulation of cell fate in the sensory epithelia of the inner ear. Nat. Rev. Neurosci. 2006, 7:837-849.
23. Kiernan A.E., Ahituv N., Fuchs H., Balling R., Avraham K.B., Steel K.P., Hrabe de Angelis M. The Notch ligand Jagged1 is required for inner ear sensory development. Proc. Natl. Acad. Sci. USA 2001, 98:3873-3878.
24. 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.
25. Kiernan A.E., Pelling A.L., Leung K.K., Tang A.S., Bell D.M., Tease C., Lovell-Badge R., Steel K.P., Cheah K.S. Sox2 is required for sensory organ development in the mammalian inner ear. Nature 2005, 434:1031-1035.
26. Lang H., Bever M.M., Fekete D.M. Cell proliferation and cell death in the developing chick inner ear: spatial and temporal patterns. J. Comp. Neurol. 2000, 417:205-220.
27. Lillevali K., Matilainen T., Karis A., Salminen M. Partially overlapping expression of Gata2 and Gata3 during inner ear development. Dev. Dyn. 2004, 231:775-781.
28. Mann R.S., Carroll S.B. Molecular mechanisms of selector gene function and evolution. Curr. Opin. Genet. Dev. 2002, 12:592-600.
29. Martin D.M., Skidmore J.M., Fox S.E., Gage P.J., Camper S.A. Pitx2 distinguishes subtypes of terminally differentiated neurons in the developing mouse neuroepithelium. Dev. Biol. 2002, 252:84-99.
30. Martin P., Swanson G.J. 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.
31. 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.
32. Morsli H., Choo D., Ryan A., Johnson R., Wu D.K. Development of the mouse inner ear and origin of its sensory organs. J. Neurosci. 1998, 18:3327-3335.
33. 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.
34. Pauley S., Wright T.J., Pirvola U., Ornitz D., Beisel K., Fritzsch B. Expression and function of FGF10 in mammalian inner ear development. Dev. Dyn. 2003, 227:203-215.
35. Raft S., Nowotschin S., Liao J., Morrow B.E. Suppression of neural fate and control of inner ear morphogenesis by Tbx1. Development 2004, 131:1801-1812.
36. 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.
37. Salminen M., Meyer B.I., Bober E., Gruss P. Netrin 1 is required for semicircular canal formation in the mouse inner ear. Development 2000, 127:13-22.
38. Sanchez-Calderon H., Milo M., Leon Y., Varela-Nieto I. A network of growth and transcription factors controls neuronal differentiation and survival in the developing ear. Int. J. Dev. Biol. 2007, 51:557-570.
39. Schnetz M.P., Bartels C.F., Shastri K., Balasubramanian D., Zentner G.E., Balaji R., Zhang X., Song L., Wang Z., Laframboise T., Crawford G.E., Scacheri P.C. Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res. 2009, 19:590-601.
40. 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.
41. Tsai H., Hardisty R.E., Rhodes C., Kiernan A.E., Roby P., Tymowska-Lalanne Z., Mburu P., Rastan S., Hunter A.J., Brown S.D., Steel K.P. The mouse slalom mutant demonstrates a role for Jagged1 in neuroepithelial patterning in the organ of Corti. Hum. Mol. Genet. 2001, 10:507-512.
42. 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.
43. Wang W., Van De Water T., Lufkin T. Inner ear and maternal reproductive defects in mice lacking the Hmx3 homeobox gene. Development 1998, 125:621-634.
44. 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.
45. Winnier G., Blessing M., Labosky P.A., Hogan B.L. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 1995, 9:2105-2116.
46. Woodage T., Basrai M.A., Baxevanis A.D., Hieter P., Collins F.S. Characterization of the CHD family of proteins. Proc. Natl. Acad. Sci. USA 1997, 94:11472-11477.