A novel classification system to predict the pathogenic effects of CHD7 missense variants in CHARGE syndrome

Human Mutation

Volumn 33, Issue 8, 2012, Pages 1251-1260

  Bergman, Jorieke E H ^a,g   Janssen, Nicole ^a,g   van der Sloot, Almer M ^b   de Walle, Hermien E K ^a   Schoots, Jeroen ^c   Rendtorff, Nanna D ^d   Tranebjærg, Lisbeth ^d,e   Hoefsloot, Lies H ^c   van Ravenswaaij Arts, Conny M A ^a   Hofstra, Robert M W ^f  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

^f BISPEBJERG HOSPITAL   (Denmark)

^g ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

CHARGE syndrome; CHD7, missense mutation; Classification system; Genotype phenotype correlation; Prediction pathogenicity

Indexed keywords

PROTEIN; PROTEIN CHD7; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; CLASSIFICATION ALGORITHM; GENE SEGREGATION; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; HUMAN; MISSENSE MUTATION; PATHOGENICITY; PREDICTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; SYNDROME CHARGE;

CHARGE SYNDROME; DNA HELICASES; DNA-BINDING PROTEINS; GENOTYPE; HUMANS; MUTATION, MISSENSE; PHENOTYPE;

EID: 84863875415     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22106     Document Type: Article

References (69)

1. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. 2010. A method and server for predicting damaging missense mutations. Nat Methods 7:248-249.
2. Alibes A, Nadra AD, De Masi F, Bulyk ML, Serrano L, Stricher F. 2010. Using protein design algorithms to understand the molecular basis of disease caused by protein-DNA interactions: the Pax6 example. Nucleic Acids Res 38:7422-7431.
3. Armougom F, Moretti S, Poirot O, Audic S, Dumas P, Schaeli B, Keduas V, Notredame C. 2006. Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-coffee. Nucleic Acids Res 34:W604-W608.
4. Asakura Y, Toyota Y, Muroya K, Kurosawa K, Fujita K, Aida N, Kawame H, Kosaki K, Adachi M. 2008. Endocrine and radiological studies in patients with molecularly confirmed CHARGE syndrome. J Clin Endocrinol Metab 93:920-924.
5. Bartels CF, Scacheri C, White L, Scacheri PC, Bale S. 2010. Mutations in the CHD7 gene: the experience of a commercial laboratory. Genet Test Mol Biomarkers 14:881-891.
6. Bell J, Bodmer D, Sistermans E, Ramsden SC. 2007. Practice guidelines for the interpretation and reporting of unclassified variants (UVs) in clinical molecular genetics. CMGS/VKGL 6 p.
7. Bergman JE, de Wijs I, Jongmans MC, Admiraal RJ, Hoefsloot LH, Ravenswaaij-Arts CM. 2008. Exon copy number alterations of the CHD7 gene are not a major cause of CHARGE and CHARGE-like syndrome. Eur J Med Genet 51:417-425.
8. Bergman JE, Bocca G, Hoefsloot LH, Meiners LC, Ravenswaaij-Arts CM. 2011a. Anosmia predicts hypogonadotropic hypogonadism in CHARGE syndrome. J Pediatr 158:474-479.
9. Bergman JE, Janssen N, Hoefsloot LH, Jongmans MC, Hofstra RM, van Ravenswaaij-Arts CM. 2011b. CHD7 mutations and CHARGE syndrome: the clinical implications of an expanding phenotype. J Med Genet 48:334-342.
10. Blake KD, Davenport SL, Hall BD, Hefner MA, Pagon RA, Williams MS, Lin AE, Graham Jr JM. 1998. CHARGE association: an update and review for the primary pediatrician. Clin Pediatr (Phila) 37:159-173.
11. Bosman EA, Penn AC, Ambrose JC, Kettleborough R, Stemple DL, Steel KP. 2005. Multiple mutations in mouse Chd7 provide models for CHARGE syndrome. Hum Mol Genet 14:3463-3476.
12. Chan PA, Duraisamy S, Miller PJ, Newell JA, McBride C, Bond JP, Raevaara T, Ollila S, Nystrom M, Grimm AJ, Christodoulou J, Oetting WS, Greenblatt MS. 2007. Interpreting missense variants: comparing computational methods in human disease genes CDKN2A, MLH1, MSH2, MECP2, and tyrosinase (TYR). Hum Mutat 28:683-693.
13. Cheadle JP, Gill H, Fleming N, Maynard J, Kerr A, Leonard H, Krawczak M, Cooper DN, Lynch S, Thomas N, Hughes H, Hulten M, Ravine D, Sampson JR, Clarke A. 2000. Long-read sequence analysis of the MECP2 gene in Rett syndrome patients: correlation of disease severity with mutation type and location. Hum Mol Genet 9:1119-1129.
14. Dauber A, Hirschhorn JN, Picker J, Maher TA, Milunsky A. 2010. Delayed puberty due to a novel mutation in CHD7 causing CHARGE syndrome. Pediatrics 126:e1594-e1598.
15. De Arriba Munoz A, Monge Galindo L, Lopez Pison J, Lafuente Hidalgo M, Perez Delgado R, Dominguez Cajal M, Rebage V. 2011. CHARGE syndrome and CHD7 gene mutation. Neurologia 26:255.
16. Delahaye A, Sznajer Y, Lyonnet S, Elmaleh-Berges M, Delpierre I, Audollent S, Wiener-Vacher S, Mansbach AL, Amiel J, Baumann C, Bremond-Gignac D, Attie-Bitach T, Verloes A, Sanlaville D. 2007. Familial CHARGE syndrome because of CHD7 mutation: clinical intra- and interfamilial variability. Clin Genet 72:112-121.
17. Durr H, Korner C, Muller M, Hickmann V, Hopfner KP. 2005. X-ray structures of the sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121:363-373.
18. Felix TM, Hanshaw BC, Mueller R, Bitoun P, Murray JC. 2006. CHD7 gene and non-syndromic cleft lip and palate. Am J Med Genet A 140:2110-2114.
19. Feret H, McDonald-McGinn DM, Santani A, Zackai EH. 2010. Expanding the phenotypic overlap between CHARGE and Kallmann syndromes due to CHD7 mutations. No. 1671. Abstract of poster presented at 60th Annual ASHG Meeting, Washington DC, 2-6 Nov. 2010. www.ashg.org/2010meeting/abstracts/fulltext/f22415.htm.
20. Flanagan JF, Blus BJ, Kim D, Clines KL, Rastinejad F, Khorasanizadeh S. 2007. Molecular implications of evolutionary differences in CHD double chromodomains. J Mol Biol 369:334-342.
21. Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y, Minor W, Rastinejad F, Khorasanizadeh S. 2005. Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438:1181-1185.
22. Frederic MY, Lalande M, Boileau C, Hamroun D, Claustres M, Beroud C, Collod-Beroud G. 2009. UMD-predictor, a new prediction tool for nucleotide substitution pathogenicity-application to four genes: FBN1, FBN2, TGFBR1, and TGFBR2. Hum Mutat 30:952-959.
23. Fujita K, Aida N, Asakura Y, Kurosawa K, Niwa T, Muroya K, Adachi M, Nishimura G, Inoue T. 2009. Abnormal basiocciput development in CHARGE syndrome. Am J Neuroradiol 30:629-634.
24. 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. 2007. CHD7 gene polymorphisms are associated with susceptibility to idiopathic scoliosis. Am J Hum Genet 80:957-965.
25. Guerois R, Nielsen JE, Serrano L. 2002. Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320:369-387.
26. Hauk G, McKnight JN, Nodelman IM, Bowman GD. 2010. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol Cell 39:711-723.
27. Holak HM, Kohlhase J, Holak SA, Holak NH. 2008. New recognized ophthalmic morphologic anomalies in CHARGE syndrome caused by the R2319C mutation in the CHD7 gene. Ophthalmic Genet 29:79-84.
28. Janssen N, Bergman JE, Swertz MA, Tranebjaerg L, Lodahl M, Schoots J, Hofstra RM, van Ravenswaaij-Arts CM, Hoefsloot LH. 2012. Mutation update on the CHD7 gene involved in CHARGE syndrome. Hum Mutat doi: 10.1002/humu.22086.
29. Jongmans MC, Admiraal RJ, van der Donk KP, Vissers LE, Baas AF, Kapusta L, van Hagen JM, Donnai D, de Ravel TJ, Veltman JA, Geurts van Kessel A, De Vries BB, Brunner HG, Hoefsloot LH, van Ravenswaaij CM. 2006. CHARGE syndrome: the phenotypic spectrum of mutations in the CHD7 gene. J Med Genet 43:306-314.
30. Jongmans MC, Hoefsloot LH, van der Donk KP, Admiraal RJ, Magee A, van de Laar I, Hendriks Y, Verheij JB, Walpole I, Brunner HG, van Ravenswaaij CM. 2008. Familial CHARGE syndrome and the CHD7 gene: a recurrent missense mutation, intrafamilial recurrence and variability. Am J Med Genet A 146:43-50.
31. Jongmans MC, Ravenswaaij-Arts CM, Pitteloud N, Ogata T, Sato N, Claahsen-van der Grinten, van der Donk K, Seminara S, Bergman JE, Brunner HG, Crowley Jr WF, Hoefsloot LH. 2009. CHD7 mutations in patients initially diagnosed with Kallmann syndrome-the clinical overlap with CHARGE syndrome. Clin Genet 75:65-71.
32. Kim HG, Kurth I, Lan F, Meliciani I, Wenzel W, Eom SH, Kang GB, Rosenberger G, Tekin M, Ozata M, Bick DP, Sherins RJ, Walker SL, Shi Y, Gusella JF, Layman LC. 2008. Mutations in CHD7, encoding a chromatin-remodeling protein, cause idiopathic hypogonadotropic hypogonadism and Kallmann syndrome. Am J Hum Genet 83:511-519.
33. Krieger E, Darden T, Nabuurs SB, Finkelstein A, Vriend G. 2004. Making optimal use of empirical energy functions: force-field parameterization in crystal space. Proteins 57:678-683.
34. Krieger E, Joo K, Lee J, Lee J, Raman S, Thompson J, Tyka M, Baker D, Karplus K. 2009. Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins 77(Suppl 9):114-122.
35. Krieger E, Koraimann G, Vriend G. 2002. Increasing the precision of comparative models with YASARA NOVA-a self-parameterizing force field. Proteins 47:393-402.
36. Kumar P, Henikoff S, Ng PC. 2009. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4:1073-1081.
37. Lalani SR, Safiullah AM, Fernbach SD, Harutyunyan KG, Thaller C, Peterson LE, McPherson JD, Gibbs RA, White LD, Hefner M, Davenport SL, Graham JM, Bacino CA, Glass NL, Towbin JA, Craigen WJ, Neish SR, Lin AE, Belmont JW. 2006. Spectrum of CHD7 mutations in 110 individuals with CHARGE syndrome and genotype-phenotype correlation. Am J Hum Genet 78:303-314.
38. Levy CM, Knudtzon J. 1993. Kallmann syndrome in two sisters with other developmental anomalies also affecting their father. Clin Genet 43:51-53.
39. Mathe E, Olivier M, Kato S, Ishioka C, Hainaut P, Tavtigian SV. 2006. Computational approaches for predicting the biological effect of p53 missense mutations: a comparison of three sequence analysis based methods. Nucleic Acids Res 34:1317-1325.
40. McGee TL, Seyedahmadi BJ, Sweeney MO, Dryja TP, Berson EL. 2010. Novel mutations in the long isoform of the USH2A gene in patients with Usher syndrome type II or non-syndromic retinitis pigmentosa. J Med Genet 47:499-506.
41. Ng PC, Henikoff S. 2006. Predicting the effects of amino acid substitutions on protein function. Annu Rev Genomics Hum Genet 7:61-80.
42. Notredame C, Higgins DG, Heringa J. 2000. T-coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205-217.
43. Okuda M, Horikoshi M, Nishimura Y. 2007. Structural polymorphism of chromodomains in Chd1. J Mol Biol 365:1047-1062.
44. Pagon RA, Graham Jr JM, Zonana J, Yong SL. 1981. Coloboma, congenital heart disease, and choanal atresia with multiple anomalies: CHARGE association. J Pediatr 99:223-227.
45. Pauli S, von Velsen N, Burfeind P, Steckel M, Manz J, Buchholz A, Borozdin W, Kohlhase J. 2012. CHD7 mutations causing CHARGE syndrome are predominantly of paternal origin. Clin Genet 81:234-239.
46. Pertea M, Lin X, Salzberg SL. 2001. GeneSplicer: a new computational method for splice site prediction. Nucleic Acids Res 29:1185-1190.
47. Pey AL, Stricher F, Serrano L, Martinez A. 2007. Predicted effects of missense mutations on native-state stability account for phenotypic outcome in phenylketonuria, a paradigm of misfolding diseases. Am J Hum Genet 81:1006-1024.
48. Rakoczy EP, Kiel C, McKeone R, Stricher F, Serrano L. 2011. Analysis of disease-linked rhodopsin mutations based on structure, function, and protein stability calculations. J Mol Biol 405:584-606.
49. Ramensky V, Bork P, Sunyaev S. 2002. Human non-synonymous SNPs: server and survey. Nucleic Acids Res 30:3894-3900.
50. Reese MG, Eeckman FH, Kulp D, Haussler D. 1997. Improved splice site detection in genie. J Comput Biol 4:311-323.
51. Reis CR, van der Sloot AM, Natoni A, Szegezdi E, Setroikromo R, Meijer M, Sjollema K, Stricher F, Cool RH, Samali A, Serrano L, Quax WJ. 2010. Rapid and efficient cancer cell killing mediated by high-affinity death receptor homotrimerizing TRAIL variants. Cell Death Dis 1:e83.
52. Sanlaville D, Etchevers HC, Gonzales M, Martinovic J, Clement-Ziza M, Delezoide AL, Aubry MC, 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. 2006. Phenotypic spectrum of CHARGE syndrome in fetuses with CHD7 truncating mutations correlates with expression during human development. J Med Genet 43:211-217.
53. Sanlaville D, Verloes A. 2007. CHARGE syndrome: an update. Eur J Hum Genet 15:389-399.
54. Schymkowitz JW, Rousseau F, Martins IC, Ferkinghoff-Borg J, Stricher F, Serrano L. 2005. Prediction of water and metal binding sites and their affinities by using the fold-X force field. Proc Natl Acad Sci USA 102:10147-10152.
55. Swertz MA, Dijkstra M, Adamusiak T, van der Velde JK, Kanterakis A, Roos ET, Lops J, Thorisson GA, Arends D, Byelas G, Muilu J, Brookes AJ, de Brock EO, Jansen RC, Parkinson H. 2010. The MOLGENIS toolkit: rapid prototyping of biosoftware at the push of a button. BMC Bioinformatics 11(SUPPL 12):S12.
56. Tavtigian SV, Deffenbaugh AM, Yin L, Judkins T, Scholl T, Samollow PB, de Silva D, Zharkikh A, Thomas A. 2006. Comprehensive statistical study of 452 BRCA1 missense substitutions with classification of eight recurrent substitutions as neutral. J Med Genet 43:295-305.
57. Tavtigian SV, Greenblatt MS, Lesueur F, Byrnes GB, IARC Unclassified Genetic Variants Working Group. 2008. In silico analysis of missense substitutions using sequence-alignment based methods. Hum Mutat 29:1327-1336.
58. Thoma NH, Czyzewski BK, Alexeev AA, Mazin AV, Kowalczykowski SC, Pavletich NP. 2005. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat Struct Mol Biol 12:350-356.
59. Van der Sloot AM, Tur V, Szegezdi E, Mullally MM, Cool RH, Samali A, Serrano L, Quax WJ. 2006. Designed tumor necrosis factor-related apoptosis-inducing ligand variants initiating apoptosis exclusively via the DR5 receptor. Proc Natl Acad Sci USA 103:8634-8639.
60. Verloes A. 2005. Updated diagnostic criteria for CHARGE syndrome: a proposal. Am J Med Genet A 133:306-308.
61. Vissers LE, van Ravenswaaij CM, Admiraal R, Hurst JA, De Vries BB, Janssen IM, van der Vliet WA, Huys EH, de Jong PJ, Hamel BC, Schoenmakers EF, Brunner HG, Veltman JA, van Kessel AG. 2004. Mutations in a new member of the chromodomain gene family cause CHARGE syndrome. Nat Genet 36:955-957.
62. Vuorela P, la-Mello S, Saloranta C, Penttinen M, Poyhonen M, Huoponen K, Borozdin W, Bausch B, Botzenhart EM, Wilhelm C, Kaariainen H, Kohlhase J. 2007. 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 9:690-694.
63. Vuorela PE, Penttinen MT, Hietala MH, Laine JO, Huoponen KA, Kaariainen HA. 2008. A familial CHARGE syndrome with a CHD7 nonsense mutation and new clinical features. Clin Dysmorphol 17:249-253.
64. Wessels K, Bohnhorst B, Luhmer I, Morlot S, Bohring A, Jonasson J, Epplen JT, Gadzicki D, Glaser S, Gohring G, Malzer M, Hein A, Arslan-Kirchner M, Stuhrmann M, Schmidtke J, Pabst B. 2010. Novel CHD7 mutations contributing to the mutation spectrum in patients with CHARGE syndrome. Eur J Med Genet 53:280-285.
65. Wincent J, Holmberg E, Stromland K, Soller M, Mirzaei L, Djureinovic T, Robinson KL, Anderlid BM, Schoumans J. 2008. CHD7 mutation spectrum in 28 Swedish patients diagnosed with CHARGE syndrome. Clin Genet 74:31-38.
66. Yeo G, Burge CB. 2004. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 11:377-394.
67. Zanetti A, Ferraresi E, Picci L, Filocamo M, Parini R, Rosano C, Tomanin R, Scarpa M. 2009. Segregation analysis in a family at risk for the Maroteaux-Lamy syndrome conclusively reveals c.1151G>A (p.S384N) as to be a polymorphism. Eur J Hum Genet 17:1160-1164.
68. Zentner GE, Layman WS, Martin DM, Scacheri PC. 2010. Molecular and phenotypic aspects of CHD7 mutation in CHARGE syndrome. Am J Med Genet A 152A:674-686.
69. Zhang MQ. 1998. Statistical features of human exons and their flanking regions. Hum Mol Genet 7:919-932.