De Novo Mutations in CHD4, an ATP-Dependent Chromatin Remodeler Gene, Cause an Intellectual Disability Syndrome with Distinctive Dysmorphisms

American Journal of Human Genetics

Volumn 99, Issue 4, 2016, Pages 934-941

  Weiss, Karin ^a   Terhal, Paulien A ^b   Cohen, Lior ^c,d   Bruccoleri, Michael ^e   Irving, Melita ^f   Martinez, Ariel F ^a   Rosenfeld, Jill A ^g   Machol, Keren ^g   Yang, Yaping ^g   Liu, Pengfei ^g   Walkiewicz, Magdalena ^g   Beuten, Joke ^g   Gomez Ospina, Natalia ^h   Haude, Katrina ⁱ   Fong, Chin To ⁱ   Enns, Gregory M ^h   Bernstein, Jonathan A ^h   Fan, Judith ^j   Gotway, Garrett ^j   Ghorbani, Mohammad ^e   van Gassen, Koen ^b   Monroe, Glen R ^b   van Haaften, Gijs ^b   Basel Vanagaite, Lina ^c,d,k   Yang, Xiang Jiao ^e   Campeau, Philippe M ^l   Muenke, Maximilian ^a   more..

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^d TEL AVIV UNIVERSITY   (Israel)

^e MCGILL UNIVERSITY   (Canada)

^f GUY S HOSPITAL   (United Kingdom)

^g BAYLOR COLLEGE OF MEDICINE   (United States)

^h STANFORD UNIVERSITY   (United States)

ⁱ UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^j UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^k RABIN MEDICAL CENTER   (Israel)

^l UNIVERSITY OF MONTREAL   (Canada)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; AMINO ACID SUBSTITUTION; ARTICLE; CASE REPORT; CHD4 GENE; CHILD; EXOME; FACE DYSMORPHIA; FEMALE; GENE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HEARING IMPAIRMENT; HUMAN; INTELLECTUAL IMPAIRMENT; MACROCEPHALY; MALE; MISSENSE MUTATION; PRIORITY JOURNAL; SCHOOL CHILD; ABNORMALITIES; ALEXANDER DISEASE; ANIMAL; CELL NUCLEUS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEVELOPMENTAL DISORDER; FACE; GENETICS; HAND MALFORMATION; METABOLISM; MICROGNATHIA; MOUSE; MULTIPLE MALFORMATION SYNDROME; NECK; PRESCHOOL CHILD; SYNDROME;

ADENOSINE TRIPHOSPHATE; AUTOANTIGEN; CHD4 PROTEIN, HUMAN; DNA HELICASE; HDAC1 PROTEIN, HUMAN; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; MI-2BETA PROTEIN, MOUSE; NUCLEAR PROTEIN; SMARCA4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ABNORMALITIES, MULTIPLE; ADENOSINE TRIPHOSPHATE; ADOLESCENT; ANIMALS; AUTOANTIGENS; CELL NUCLEUS; CHILD; CHILD, PRESCHOOL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DEVELOPMENTAL DISABILITIES; DNA HELICASES; EXOME; FACE; FEMALE; HAND DEFORMITIES, CONGENITAL; HEARING LOSS; HISTONE DEACETYLASE 1; HUMANS; INTELLECTUAL DISABILITY; MALE; MEGALENCEPHALY; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; MICROGNATHISM; MUTATION, MISSENSE; NECK; NUCLEAR PROTEINS; SYNDROME; TRANSCRIPTION FACTORS;

EID: 84991730430     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.08.001     Document Type: Article

References (50)

1. 1 Bjornsson, H.T., The Mendelian disorders of the epigenetic machinery. Genome Res. 25 (2015), 1473–1481.
2. 2 López, A.J., Wood, M.A., Role of nucleosome remodeling in neurodevelopmental and intellectual disability disorders. Front. Behav. Neurosci., 9, 2015, 100.
3. 3 Santen, G.W., Kriek, M., van Attikum, H., SWI/SNF complex in disorder: SWItching from malignancies to intellectual disability. Epigenetics 7 (2012), 1219–1224.
4. 4 Hargreaves, D.C., Crabtree, G.R., ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21 (2011), 396–420.
5. 5 Seelig, H.P., Moosbrugger, I., Ehrfeld, H., Fink, T., Renz, M., Genth, E., The major dermatomyositis-specific Mi-2 autoantigen is a presumed helicase involved in transcriptional activation. Arthritis Rheum. 38 (1995), 1389–1399.
6. 6 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 94 (1997), 11472–11477.
7. 7 Hall, J.A., Georgel, P.T., CHD proteins: a diverse family with strong ties. Biochem. Cell Biol. 85 (2007), 463–476.
8. 8 Xue, Y., Wong, J., Moreno, G.T., Young, M.K., Côté, J., Wang, W., NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol. Cell 2 (1998), 851–861.
9. 9 Lai, A.Y., Wade, P.A., Cancer biology and NuRD: a multifaceted chromatin remodelling complex. Nat. Rev. Cancer 11 (2011), 588–596.
10. 10 Zhang, Y., LeRoy, G., Seelig, H.P., Lane, W.S., Reinberg, D., The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95 (1998), 279–289.
11. 11 Wade, P.A., Jones, P.L., Vermaak, D., Wolffe, A.P., A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr. Biol. 8 (1998), 843–846.
12. 12 Basta, J., Rauchman, M., The nucleosome remodeling and deacetylase complex in development and disease. Transl. Res. 165 (2015), 36–47.
13. 13 Yamada, T., Yang, Y., Hemberg, M., Yoshida, T., Cho, H.Y., Murphy, J.P., Fioravante, D., Regehr, W.G., Gygi, S.P., Georgopoulos, K., Bonni, A., Promoter decommissioning by the NuRD chromatin remodeling complex triggers synaptic connectivity in the mammalian brain. Neuron 83 (2014), 122–134.
14. 14 Denner, D.R., Rauchman, M., Mi-2/NuRD is required in renal progenitor cells during embryonic kidney development. Dev. Biol. 375 (2013), 105–116.
15. 15 Linder, B., Mentele, E., Mansperger, K., Straub, T., Kremmer, E., Rupp, R.A., CHD4/Mi-2beta activity is required for the positioning of the mesoderm/neuroectoderm boundary in Xenopus. Genes Dev. 21 (2007), 973–983.
16. 16 Ingram, K.G., Curtis, C.D., Silasi-Mansat, R., Lupu, F., Griffin, C.T., The NuRD chromatin-remodeling enzyme CHD4 promotes embryonic vascular integrity by transcriptionally regulating extracellular matrix proteolysis. PLoS Genet., 9, 2013, e1004031.
17. 17 Sparmann, A., Xie, Y., Verhoeven, E., Vermeulen, M., Lancini, C., Gargiulo, G., Hulsman, D., Mann, M., Knoblich, J.A., van Lohuizen, M., The chromodomain helicase Chd4 is required for Polycomb-mediated inhibition of astroglial differentiation. EMBO J. 32 (2013), 1598–1612.
18. 18 Le Gallo, M., O'Hara, A.J., Rudd, M.L., Urick, M.E., Hansen, N.F., O'Neil, N.J., Price, J.C., Zhang, S., England, B.M., Godwin, A.K., et al., NIH Intramural Sequencing Center (NISC) Comparative Sequencing Program. Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat. Genet. 44 (2012), 1310–1315.
19. 19 Zhao, S., Choi, M., Overton, J.D., Bellone, S., Roque, D.M., Cocco, E., Guzzo, F., English, D.P., Varughese, J., Gasparrini, S., et al. Landscape of somatic single-nucleotide and copy-number mutations in uterine serous carcinoma. Proc. Natl. Acad. Sci. USA 110 (2013), 2916–2921.
20. 20 Monroe, G.R., Frederix, G.W., Savelberg, S.M., de Vries, T.I., Duran, K.J., van der Smagt, J.J., Terhal, P.A., van Hasselt, P.M., Kroes, H.Y., Verhoeven-Duif, N.M., et al. Effectiveness of whole-exome sequencing and costs of the traditional diagnostic trajectory in children with intellectual disability. Genet. Med., 9, 2016, 999.
21. 21 Deciphering Developmental Disorders Study. Large-scale discovery of novel genetic causes of developmental disorders. Nature 519 (2015), 223–228.
22. 22 Sobreira, N., Schiettecatte, F., Valle, D., Hamosh, A., GeneMatcher: a matching tool for connecting investigators with an interest in the same gene. Hum. Mutat. 36 (2015), 928–930.
23. 23 Teer, J.K., Green, E.D., Mullikin, J.C., Biesecker, L.G., VarSifter: visualizing and analyzing exome-scale sequence variation data on a desktop computer. Bioinformatics 28 (2012), 599–600.
24. 24 Firth, H.V., Wright, C.F., DDD Study. The Deciphering Developmental Disorders (DDD) study. Dev. Med. Child Neurol. 53 (2011), 702–703.
25. 25 Yang, Y., Muzny, D.M., Xia, F., Niu, Z., Person, R., Ding, Y., Ward, P., Braxton, A., Wang, M., Buhay, C., et al. Molecular findings among patients referred for clinical whole-exome sequencing. JAMA 312 (2014), 1870–1879.
26. 26 Morra, R., Lee, B.M., Shaw, H., Tuma, R., Mancini, E.J., Concerted action of the PHD, chromo and motor domains regulates the human chromatin remodelling ATPase CHD4. FEBS Lett. 586 (2012), 2513–2521.
27. 27 Watson, A.A., Mahajan, P., Mertens, H.D., Deery, M.J., Zhang, W., Pham, P., Du, X., Bartke, T., Zhang, W., Edlich, C., et al. The PHD and chromo domains regulate the ATPase activity of the human chromatin remodeler CHD4. J. Mol. Biol. 422 (2012), 3–17.
28. 28 Richmond, E., Peterson, C.L., Functional analysis of the DNA-stimulated ATPase domain of yeast SWI2/SNF2. Nucleic Acids Res. 24 (1996), 3685–3692.
29. 29 Bouazoune, K., Kingston, R.E., Chromatin remodeling by the CHD7 protein is impaired by mutations that cause human developmental disorders. Proc. Natl. Acad. Sci. USA 109 (2012), 19238–19243.
30. 30 Kircher, M., Witten, D.M., Jain, P., O'Roak, B.J., Cooper, G.M., Shendure, J., A general framework for estimating the relative pathogenicity of human genetic variants. Nat. Genet. 46 (2014), 310–315.
31. 31 Choi, Y., Chan, A.P., PROVEAN web server: a tool to predict the functional effect of amino acid substitutions and indels. Bioinformatics 31 (2015), 2745–2747.
32. 32 Kumar, P., Henikoff, S., Ng, P.C., Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4 (2009), 1073–1081.
33. 33 Samocha, K.E., Robinson, E.B., Sanders, S.J., Stevens, C., Sabo, A., McGrath, L.M., Kosmicki, J.A., Rehnström, K., Mallick, S., Kirby, A., et al. A framework for the interpretation of de novo mutation in human disease. Nat. Genet. 46 (2014), 944–950.
34. 34 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., et al. Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat. Genet. 36 (2004), 955–957.
35. 35 Chénier, S., Yoon, G., Argiropoulos, B., Lauzon, J., Laframboise, R., Ahn, J.W., Ogilvie, C.M., Lionel, A.C., Marshall, C.R., Vaags, A.K., et al. CHD2 haploinsufficiency is associated with developmental delay, intellectual disability, epilepsy and neurobehavioural problems. J. Neurodev. Disord., 6, 2014, 9.
36. 36 Bernier, R., Golzio, C., Xiong, B., Stessman, H.A., Coe, B.P., Penn, O., Witherspoon, K., Gerdts, J., Baker, C., Vulto-van Silfhout, A.T., et al. Disruptive CHD8 mutations define a subtype of autism early in development. Cell 158 (2014), 263–276.
37. 37 Polo, S.E., Kaidi, A., Baskcomb, L., Galanty, Y., Jackson, S.P., Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 29 (2010), 3130–3139.
38. 38 Van Nostrand, J.L., Brady, C.A., Jung, H., Fuentes, D.R., Kozak, M.M., Johnson, T.M., Lin, C.Y., Lin, C.J., Swiderski, D.L., Vogel, H., et al. Inappropriate p53 activation during development induces features of CHARGE syndrome. Nature 514 (2014), 228–232.
39. 39 Tsurusaki, Y., Okamoto, N., Ohashi, H., Kosho, T., Imai, Y., Hibi-Ko, Y., Kaname, T., Naritomi, K., Kawame, H., Wakui, K., et al. Mutations affecting components of the SWI/SNF complex cause Coffin-Siris syndrome. Nat. Genet. 44 (2012), 376–378.
40. 40 Tsurusaki, Y., Okamoto, N., Ohashi, H., Mizuno, S., Matsumoto, N., Makita, Y., Fukuda, M., Isidor, B., Perrier, J., Aggarwal, S., et al. Coffin-Siris syndrome is a SWI/SNF complex disorder. Clin. Genet. 85 (2014), 548–554.
41. 41 Van Houdt, J.K., Nowakowska, B.A., Sousa, S.B., van Schaik, B.D., Seuntjens, E., Avonce, N., Sifrim, A., Abdul-Rahman, O.A., van den Boogaard, M.J., Bottani, A., et al. Heterozygous missense mutations in SMARCA2 cause Nicolaides-Baraitser syndrome. Nat. Genet. 44 (2012), 445–449, S1.
42. 42 Picketts, D.J., Higgs, D.R., Bachoo, S., Blake, D.J., Quarrell, O.W., Gibbons, R.J., ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome. Hum. Mol. Genet. 5 (1996), 1899–1907.
43. 43 O'Shaughnessy-Kirwan, A., Signolet, J., Costello, I., Gharbi, S., Hendrich, B., Constraint of gene expression by the chromatin remodelling protein CHD4 facilitates lineage specification. Development 142 (2015), 2586–2597.
44. 44 Sousa, S.B., Hennekam, R.C., Nicolaides-Baraitser Syndrome International Consortium. Phenotype and genotype in Nicolaides-Baraitser syndrome. Am. J. Med. Genet. C. Semin. Med. Genet. 166C (2014), 302–314.
45. 45 Reynolds, N., O'Shaughnessy, A., Hendrich, B., Transcriptional repressors: multifaceted regulators of gene expression. Development 140 (2013), 505–512.
46. 46 Smeenk, G., Wiegant, W.W., Vrolijk, H., Solari, A.P., Pastink, A., van Attikum, H., The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J. Cell Biol. 190 (2010), 741–749.
47. 47 Hodges, C., Kirkland, J.G., Crabtree, G.R., The many roles of BAF (mSWI/SNF) and PBAF complexes in cancer. Cold Spring Harb. Perspect. Med., 6, 2016, a026930.
48. 48 Kosho, T., Miyake, N., Carey, J.C., Coffin-Siris syndrome and related disorders involving components of the BAF (mSWI/SNF) complex: historical review and recent advances using next generation sequencing. Am. J. Med. Genet. C. Semin. Med. Genet. 166C (2014), 241–251.
49. 49 David, G., Neptune, M.A., DePinho, R.A., SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activities. J. Biol. Chem. 277 (2002), 23658–23663.
50. 50 Walkinshaw, D.R., Weist, R., Kim, G.W., You, L., Xiao, L., Nie, J., Li, C.S., Zhao, S., Xu, M., Yang, X.J., The tumor suppressor kinase LKB1 activates the downstream kinases SIK2 and SIK3 to stimulate nuclear export of class IIa histone deacetylases. J. Biol. Chem. 288 (2013), 9345–9362.