The mutation in Chd7 causes misexpression of Bmp4 and developmental defects in telencephalic midline

American Journal of Pathology

Volumn 181, Issue 2, 2012, Pages 626-641

  Jiang, Xuan ^a   Zhou, Yue ^a   Xian, Li ^a   Chen, Weiqian ^a   Wu, Hanwei ^a   Gao, Xiang ^a,b  

^a NANJING UNIVERSITY   (China)

^b WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; DNA BINDING PROTEIN; DNA BINDING PROTEIN 7; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL DEATH; CELL FATE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DOWN REGULATION; EMBRYO; EXON; FEMALE; FOREBRAIN; GENE LOCUS; IN VITRO STUDY; LATERAL BRAIN VENTRICLE; MOUSE; NONHUMAN; NONSENSE MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNDROME CHARGE; TELENCEPHALON;

ANIMALS; APOPTOSIS; BEHAVIOR, ANIMAL; BONE MORPHOGENETIC PROTEIN 4; CELL LINE, TUMOR; CELL LINEAGE; CELL PROLIFERATION; CROSSES, GENETIC; DNA-BINDING PROTEINS; DOWN-REGULATION; EMBRYO, MAMMALIAN; ENHANCER ELEMENTS, GENETIC; EYE ABNORMALITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HUMANS; MALE; MICE; MICE, INBRED C57BL; MUTATION; NEUROGLIA; PROTEIN BINDING; SIGNAL TRANSDUCTION; TELENCEPHALON;

EID: 84864131784     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.05.006     Document Type: Article

References (67)

1. K. Kallen, E. Robert, P. Mastroiacovo, E.E. Castilla, B. Kallen CHARGE association in newborns: a registry-based study Teratology 60 1999 334 343
2. K.A. Issekutz, J.M. Graham Jr, C. Prasad, I.M. Smith, K.D. Blake An epidemiological analysis of CHARGE syndrome: preliminary results from a Canadian study Am J Med Genet A 133 2005 309 317
3. D. Sanlaville, A. Verloes CHARGE syndrome: an update Eur J Hum Genet 15 2007 389 399
4. J. Harris, E. Robert, B. Kallen Epidemiology of choanal atresia with special reference to the CHARGE association Pediatrics 99 1997 363 367
5. W.S. Layman, E.A. Hurd, D.M. Martin Chromodomain proteins in development: lessons from CHARGE syndrome Clin Genet 78 2010 11 20
6. A.E. Lin, J.r. Siebert, J.M. Graham Jr Central nervous system malformations in the CHARGE association Am J Med Genet 37 1990 304 310
7. G. Pinto, V. Abadie, R. Mesnage, J. Blustajn, S. Cabrol, J. Amiel, L. Hertz-Pannier, A.M. Bertrand, S. Lyonnet, R. Rappaport, I. Netchine CHARGE syndrome includes hypogonadotropic hypogonadism and abnormal olfactory bulb development J Clin Endocrinol Metab 90 2005 5621 5626
8. L.E. Vissers, C.M. van Ravenswaaij, R. Admiraal, J.A. Hurst, B.B. de Vries, I.M. Janssen, W.A. van der Vliet, E.H. Huys, P.J. de Jong, B.C. Hamel, E.F. Schoenmakers, H.G. Brunner, J.A. Veltman, A.G. van Kessel Mutations in a new member of the chromodomain gene family cause CHARGE syndrome Nat Genet 36 2004 955 957
9. D. Sanlaville, H.C. Etchevers, M. Gonzales, J. Martinovic, M. Clement-Ziza, A.L. Delezoide, M.C. Aubry, A. Pelet, S. Chemouny, C. Cruaud, S. Audollent, C. Esculpavit, G. Goudefroye, C. Ozilou, C. Fredouille, N. Joye, N. Morichon-Delvallez, Y. Dumez, J. Weissenbach, A. Munnich, J. Amiel, F. Encha-Razavi, S. Lyonnet, M. Vekemans, T. Attie-Bitach Phenotypic spectrum of CHARGE syndrome in fetuses with CHD7 truncating mutations correlates with expression during human development J Med Genet 43 2006 211 217
10. T. Woodage, M.A. Basrai, A.D. Baxevanis, P. Hieter, F.S. Collins Characterization of the CHD family of proteins Proc Natl Acad Sci U S A 94 1997 11472 11477
11. V. Delmas, D.G. Stokes, R.P. Perry A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain Proc Natl Acad Sci U S A 90 1993 2414 2418
12. C.G. Marfella, A.N. Imbalzano The Chd family of chromatin remodelers Mutat Res 618 2007 30 40
13. M.E. Adams, E.A. Hurd, L.A. Beyer, D.L. Swiderski, Y. Raphael, D.M. Martin Defects in vestibular sensory epithelia and innervation in mice with loss of Chd7 function: implications for human CHARGE syndrome J Comp Neurol 504 2007 519 532
14. E.A. Bosman, A.C. Penn, J.C. Ambrose, R. Kettleborough, D.L. Stemple, K.P. Steel Multiple mutations in mouse Chd7 provide models for CHARGE syndrome Hum Mol Genet 14 2005 3463 3476
15. E.A. Hurd, P.L. Capers, M.N. Blauwkamp, M.E. Adams, Y. Raphael, H.K. Poucher, D.M. Martin Loss of Chd7 function in gene-trapped reporter mice is embryonic lethal and associated with severe defects in multiple developing tissues Mamm Genome 18 2007 94 104
16. M.P. Schnetz, C.F. Bartels, K. Shastri, D. Balasubramanian, G.E. Zentner, R. Balaji, X. Zhang, L. Song, Z. Wang, T. Laframboise, G.E. Crawford, P.C. Scacheri Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns Genome Res 19 2009 590 601
17. M.P. Schnetz, L. Handoko, B. Akhtar-Zaidi, C.F. Bartels, C.F. Pereira, A.G. Fisher, D.J. Adams, P. Flicek, G.E. Crawford, T. Laframboise, P. Tesar, C.L. Wei, P.C. Scacheri CHD7 targets active gene enhancer elements to modulate ES cell-specific gene expression PLoS Genet 6 2010 e1001023
18. E.A. Hurd, H.K. Poucher, K. Cheng, Y. Raphael, D.M. Martin The ATP-dependent chromatin remodeling enzyme CHD7 regulates pro-neural gene expression and neurogenesis in the inner ear Development 137 2010 3139 3150
19. W.S. Layman, D.P. McEwen, L.A. Beyer, S.R. Lalani, S.D. Fernbach, E. Oh, A. Swaroop, C.C. Hegg, Y. Raphael, J.R. Martens, D.M. Martin 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 2009 1909 1923
20. W.S. Layman, E.A. Hurd, D.M. Martin Reproductive dysfunction and decreased GnRH neurogenesis in a mouse model of CHARGE syndrome Hum Mol Genet 20 2011 3138 3150
21. R. Bajpai, D.A. Chen, A. Rada-Iglesias, J. Zhang, Y. Xiong, J. Helms, C.P. Chang, Y. Zhao, T. Swigut, J. Wysocka CHD7 cooperates with PBAF to control multipotent neural crest formation Nature 463 2010 958 962
22. D.J. Melicharek, L.C. Ramirez, S. Singh, R. Thompson, D.R. Marenda Kismet/CHD7 regulates axon morphology, memory and locomotion in a Drosophila model of CHARGE syndrome Hum Mol Genet 19 2010 4253 4264
23. E. Engelen, U. Akinci, J.C. Bryne, J. Hou, C. Gontan, M. Moen, D. Szumska, C. Kockx, W. van Ijcken, D.H. Dekkers, J. Demmers, E.J. Rijkers, S. Bhattacharya, S. Philipsen, L.H. Pevny, F.G. Grosveld, R.J. Rottier, B. Lenhard, R.A. Poot Sox2 cooperates with Chd7 to regulate genes that are mutated in human syndromes Nat Genet 43 2011 607 611
24. T. Batsukh, L. Pieper, A.M. Koszucka, N. von Velsen, S. Hoyer-Fender, M. Elbracht, J.E. Bergman, L.H. Hoefsloot, S. Pauli CHD8 interacts with CHD7, a protein which is mutated in CHARGE syndrome Hum Mol Genet 19 2010 2858 2866
25. Y. Ohkubo, C. Chiang, J.L. Rubenstein Coordinate regulation and synergistic actions of BMP4 SHH and FGF8 in the rostral prosencephalon regulate morphogenesis of the telencephalic and optic vesicles Neuroscience 111 2002 1 17
26. E.S. Monuki The morphogen signaling network in forebrain development and holoprosencephaly J Neuropathol Exp Neurol 66 2007 566 575
27. M. Bachler, A. Neubuser Expression of members of the Fgf family and their receptors during midfacial development Mech Dev 100 2001 313 316
28. L. Gimeno, P. Brulet, S. Martinez Study of Fgf15 gene expression in developing mouse brain Gene Expr Patterns 3 2003 473 481
29. S. Garel, K.J. Huffman, J.L. Rubenstein Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants Development 130 2003 1903 1914
30. E.E. Storm, J.L. Rubenstein, G.R. Martin Dosage of Fgf8 determines whether cell survival is positively or negatively regulated in the developing forebrain Proc Natl Acad Sci U S A 100 2003 1757 1762
31. P.H. Crossley, S. Martinez, Y. Ohkubo, J.L. Rubenstein Coordinate expression of Fgf8 Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles Neuroscience 108 2001 183 206
32. J. Briscoe, J. Ericson The specification of neuronal identity by graded Sonic Hedgehog signalling Semin Cell Dev Biol 10 1999 353 362
33. Y. Furuta, D.W. Piston, B.L. Hogan Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development Development 124 1997 2203 2212
34. D.S. Currle, X. Cheng, C.M. Hsu, E.S. Monuki Direct and indirect roles of CNS dorsal midline cells in choroid plexus epithelia formation Development 132 2005 3549 3559
35. M. Fernandes, G. Gutin, H. Alcorn, S.K. McConnell, J.M. Hebert Mutations in the BMP pathway in mice support the existence of two molecular classes of holoprosencephaly Development 134 2007 3789 3794
36. J.M. Hebert, Y. Mishina, S.K. McConnell BMP signaling is required locally to pattern the dorsal telencephalic midline Neuron 35 2002 1029 1041
37. R.M. Anderson, A.R. Lawrence, R.W. Stottmann, D. Bachiller, J. Klingensmith Chordin and noggin promote organizing centers of forebrain development in the mouse Development 129 2002 4975 4987
38. F. He, Z. Wang, J. Zhao, J. Bao, J. Ding, H. Ruan, Q. Xie, Z. Zhang, X. Gao Large-scale screening of disease model through ENU mutagenesis in mice Chin Sci Bull 24 2003 2665 2671
39. B. Birren, E.D. Green Genome Analysis: A Laboratory Manual 1997 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY 71 134
40. B.D. Hall Choanal atresia and associated multiple anomalies J Pediatr 95 1979 395 398
41. Y. Asakura, Y. Toyota, K. Muroya, K. Kurosawa, K. Fujita, N. Aida, H. Kawame, K. Kosaki, M. Adachi Endocrine and radiological studies in patients with molecularly confirmed CHARGE syndrome J Clin Endocrinol Metab 93 2008 920 924
42. K.R. Jessen, R. Mirsky Glial cells in the enteric nervous system contain glial fibrillary acidic protein Nature 286 1980 736 737
43. D.C. Lu, Z. Zador, J. Yao, F. Fazlollahi, G.T. Manley Aquaporin-4 reduces post-traumatic seizure susceptibility by promoting astrocytic glial scar formation in mice J Neurotrauma 2011
44. L.T. Evans, R. Morse, D.W. Roberts Epilepsy surgery in tuberous sclerosis: a review Neurosurg Focus 32 2012 E5
45. E.A. Grove, S. Tole, J. Limon, L. Yip, C.W. Ragsdale The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice Development 125 1998 2315 2325
46. E.S. Monuki, F.D. Porter, C.A. Walsh Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway Neuron 32 2001 591 604
47. A. Bach, Y. Lallemand, M.A. Nicola, C. Ramos, L. Mathis, M. Maufras, B. Robert Msx1 is required for dorsal diencephalon patterning Development 130 2003 4025 4036
48. V.S. Caviness Jr, T. Takahashi, R.S. Nowakowski Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model Trends Neurosci 18 1995 379 383
49. K. Hentges, K. Thompson, A. Peterson The flat-top gene is required for the expansion and regionalization of the telencephalic primordium Development 126 1999 1601 1609
50. X. Geng, C. Speirs, O. Lagutin, A. Inbal, W. Liu, L. Solnica-Krezel, Y. Jeong, D.J. Epstein, G. Oliver Haploinsufficiency of Six3 fails to activate Sonic hedgehog expression in the ventral forebrain and causes holoprosencephaly Dev Cell 15 2008 236 247
51. S. Shanmugalingam, C. Houart, A. Picker, F. Reifers, R. Macdonald, A. Barth, K. Griffin, M. Brand, S.W. Wilson Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon Development 127 2000 2549 2561
52. S. Xuan, C.A. Baptista, G. Balas, W. Tao, V.C. Soares, E. Lai Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres Neuron 14 1995 1141 1152
53. D.O. Jones, I.G. Cowell, P.B. Singh Mammalian chromodomain proteins: their role in genome organisation and expression Bioessays 22 2000 124 137
54. Y. Alvarez, M.T. Alonso, V. Vendrell, L.C. Zelarayan, P. Chamero, T. Theil, M.R. Bosl, S. Kato, M. Maconochie, D. Riethmacher, T. Schimmang Requirements for FGF3 and FGF10 during inner ear formation Development 130 2003 6329 6338
55. S. Rinkwitz, E. Bober, R. Baker Development of the vertebrate inner ear Ann N Y Acad Sci 942 2001 1 14
56. B.T. Phillips, K. Bolding, B.B. Riley Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction Dev Biol 235 2001 351 365
57. R.K. Ladher, T.J. Wright, A.M. Moon, S.L. Mansour, G.C. Schoenwolf FGF8 initiates inner ear induction in chick and mouse Genes Dev 19 2005 603 613
58. W. Liu, S.H. Oh, Y. Kang Yk, G. Li, T.M. Doan, M. Little, L. Li, K. Ahn, E.B. Crenshaw 3rd, D.A. Frenz Bone morphogenetic protein 4 (BMP4): a regulator of capsule chondrogenesis in the developing mouse inner ear Dev Dyn 226 2003 427 438
59. W. Liu, S. Butts, H. Kim, D.A. Frenz Negative regulation of otic capsule chondrogenesis: it can make you Smad Ann N Y Acad Sci 1116 2007 141 148
60. L.M. Gerlach, M.R. Hutson, J.A. Germiller, D. Nguyen-Luu, J.C. Victor, K.F. Barald Addition of the BMP4 antagonist, noggin, disrupts avian inner ear development Development 127 2000 45 54
61. X. Cheng, C.M. Hsu, D.S. Currle, J.S. Hu, A.J. Barkovich, E.S. Monuki Central roles of the roof plate in telencephalic development and holoprosencephaly J Neurosci 26 2006 7640 7649
62. E.E. Storm, S. Garel, U. Borello, J.M. Hebert, S. Martinez, S.K. McConnell, G.R. Martin, J.L. Rubenstein Dose-dependent functions of Fgf8 in regulating telencephalic patterning centers Development 133 2006 1831 1844
63. D. Cordero, R. Marcucio, D. Hu, W. Gaffield, M. Tapadia, J.A. Helms Temporal perturbations in sonic hedgehog signaling elicit the spectrum of holoprosencephaly phenotypes J Clin Invest 114 2004 485 494
64. C.L. Dou, S. Li, E. Lai Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres Cereb Cortex 9 1999 543 550
65. H.B. Wood, V. Episkopou Comparative expression of the mouse Sox1 Sox2 and Sox3 genes from pre-gastrulation to early somite stages Mech Dev 86 1999 197 201
66. V. Graham, J. Khudyakov, P. Ellis, L. Pevny SOX2 functions to maintain neural progenitor identity Neuron 39 2003 749 765
67. I. Takada, M. Mihara, M. Suzawa, F. Ohtake, S. Kobayashi, M. Igarashi, M.Y. Youn, K. Takeyama, T. Nakamura, Y. Mezaki, S. Takezawa, Y. Yogiashi, H. Kitagawa, G. Yamada, S. Takada, Y. Minami, H. Shibuya, K. Matsumoto, S. Kato A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation Nat Cell Biol 9 2007 1273 1285