Novel pathogenic variants and genes for myopathies identified by whole exome sequencing

Molecular Genetics and Genomic Medicine

Volumn 3, Issue 4, 2015, Pages 283-301

  Hunter, Jesse M ^a   Ahearn, Mary Ellen ^a   Balak, Christopher D ^a   Liang, Winnie S ^a   Kurdoglu, Ahmet ^a   Corneveaux, Jason J ^a   Russell, Megan ^a   Huentelman, Matthew J ^a   Craig, David W ^a   Carpten, John ^a   Coons, Stephen W ^b   Demello, Daphne E ^c   Hall, Judith G ^d   Bernes, Saunder M ^c   Baumbach Reardon, Lisa ^a  

^a TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^b BARROW NEUROLOGICAL INSTITUTE   (United States)

^c PHOENIX CHILDREN'S HOSPITAL   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Arthrogryposis; CACNA1S; Central core disease; COL6A3; COL6A6; EMD; Exome; Muscular dystrophy; Myopathy; RYR1

Indexed keywords

EID: 84946051097     PISSN: None     EISSN: 23249269     Source Type: Journal    
DOI: 10.1002/mgg3.142     Document Type: Article

References (55)

1. Adzhubei, I. A., S. Schmidt, L. Peshkin, V. E. Ramensky, A. Gerasimova, P. Bork, et al. 2010. A method and server for predicting damaging missense mutations. Nat. Methods 7:248–249.
2. Baker, K. E., and R. Parker. 2004. Nonsense-mediated mRNA decay: terminating erroneous gene expression. Curr. Opin. Cell Biol. 16:293–299.
3. Bharucha-Goebel, D. X., M. Santi, L. Medne, K. Zukosky, J. Dastgir, P. B. Shieh, et al. 2013. Severe congenital RYR1-associated myopathy: the expanding clinicopathologic and genetic spectrum. Neurology 80:1584–1589.
4. Bonaldo, P., P. Braghetta, M. Zanetti, S. Piccolo, D. Volpin, and G. M. Bressan. 1998. Collagen VI deficiency induces early onset myopathy in the mouse: an animal model for Bethlem myopathy. Hum. Mol. Genet. 7:2135–2140.
5. Bonne, G., F. Leturcq, and R. Ben Yaou. 1993. Emery-Dreifuss muscular dystrophy. In R. A. Pagon, M. P. Adam, and H. H. Ardinger, T. D. Bird, C. R. Dolan, C. T. Fong, R. J. H. Smith, K. Stephens, eds. GeneReviews®. University of Washington, Seattle, WA.
6. Bonnemann, C. G. 2011. The collagen VI-related myopathies: muscle meets its matrix. Nat. Rev. Neurol. 7:379–390.
7. Brinas, L., P. Richard, S. Quijano-Roy, C. Gartioux, C. Ledeuil, E. Lacene, et al. 2010. Early onset collagen VI myopathies: genetic and clinical correlations. Ann. Neurol. 68:511–520.
8. Brown, C. A., J. Scharner, K. Felice, M. N. Meriggioli, M. Tarnopolsky, M. Bower, et al. 2011. Novel and recurrent EMD mutations in patients with Emery-Dreifuss muscular dystrophy, identify exon 2 as a mutation hot spot. J. Hum. Genet. 56:589–594.
9. Burge, J. A., and M. G. Hanna. 2012. Novel insights into the pathomechanisms of skeletal muscle channelopathies. Curr. Neurol. Neurosci. Rep. 12:62–69.
10. Bushby, K. M., J. Collins, and D. Hicks. 2014. Collagen type VI myopathies. Adv. Exp. Med. Biol. 802:185–199.
11. Butterfield, R. J., A. R. Foley, J. Dastgir, S. Asman, D. M. Dunn, Y. Zou, et al. 2013. Position of glycine substitutions in the triple helix of COL6A1, COL6A2, and COL6A3 is correlated with severity and mode of inheritance in collagen VI myopathies. Hum. Mutat. 34:1558–1567.
12. Chu, M. L., D. Conway, T. C. Pan, C. Baldwin, K. Mann, R. Deutzmann, et al. 1988. Amino acid sequence of the triple-helical domain of human collagen type VI. J. Biol. Chem. 263:18601–18606.
13. Cingolani, P., A. Platts, L. Wang le, M. Coon, T. Nguyen, L. Wang, et al. 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6:80–92.
14. De Palma, S., D. Capitanio, M. Vasso, P. Braghetta, C. Scotton, P. Bonaldo, et al. 2014. Muscle proteomics reveals novel insights into the pathophysiological mechanisms of collagen VI myopathies. J. Proteome Res. 13:5022–5030.
15. Deymeer, F., A. E. Oge, C. Bayindir, C. Kaymaz, Y. Nisanci, K. Adalet, et al. 1993. Emery-Dreifuss muscular dystrophy with unusual features. Muscle Nerve 16:1359–1365.
16. Emery, A. E. 1989. Emery-Dreifuss syndrome. J. Med. Genet. 26:637–641.
17. Engvall, E., H. Hessle, and G. Klier. 1986. Molecular assembly, secretion, and matrix deposition of type VI collagen. J. Cell Biol. 102:703–710.
18. ESP. 2013. NHLBI GO Exome Sequencing Project (ESP), Seattle, WA. Available at http://evs.gs.washington.edu/EVS/.
19. Exome_Aggregation_Consortium. 2014. Exome Aggregation Consortium (ExAC). Cambridge, MA.
20. Fitzgerald, J., C. Rich, F. H. Zhou, and U. Hansen. 2008. Three novel collagen VI chains, alpha4(VI), alpha5(VI), and alpha6(VI). J. Biol. Chem. 283:20170–20180.
21. Gara, S. K., P. Grumati, A. Urciuolo, P. Bonaldo, B. Kobbe, M. Koch, et al. 2008. Three novel collagen VI chains with high homology to the alpha3 chain. J. Biol. Chem. 283:10658–10670.
22. Gara, S. K., P. Grumati, S. Squarzoni, P. Sabatelli, A. Urciuolo, P. Bonaldo, et al. 2011. Differential and restricted expression of novel collagen VI chains in mouse. Matrix Biol. 30:248– 257.
23. Hanchard, N. A., D. R. Murdock, P. L. Magoulas, M. Bainbridge, D. Muzny, Y. Q. Wu, et al. 2013. Exploring the utility of whole-exome sequencing as a diagnostic tool in a child with atypical episodic muscle weakness. Clin. Genet. 83:457–461.
24. Kim, J. H., G. P. Jarvik, B. L. Browning, R. Rajagopalan, A. S. Gordon, M. J. Rieder, et al. 2013. Exome sequencing reveals novel rare variants in the ryanodine receptor and calcium channel genes in malignant hyperthermia families. Anesthesiology 119:1054–1065.
25. Kircher, M., D. M. Witten, P. Jain, B. J. O’Roak, G. M. Cooper, and J. Shendure. 2014. A general framework for estimating the relative pathogenicity of human genetic variants. Nat. Genet. 46:310–315.
26. Knupp, C., and J. M. Squire. 2001. A new twist in the collagen story–the type VI segmented supercoil. EMBO J. 20:372– 376.
27. Kumar, P., S. Henikoff, and P. C. Ng. 2009. Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4:1073– 1081.
28. Lampe, A. K., Y. Zou, D. Sudano, K. K. O’Brien, D. Hicks, S. H. Laval, et al. 2008. Exon skipping mutations in collagen VI are common and are predictive for severity and inheritance. Hum. Mutat. 29:809–822.
29. Li, H., and R. Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760.
30. Li, H., B. Handsaker, A. Wysoker, J. Fennell, N. Ruan, G. Homer, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079.
31. Maclennan, D. H., and E. Zvaritch. 2011. Mechanistic models for muscle diseases and disorders originating in the sarcoplasmic reticulum. Biochim. Biophys. Acta 1813:948– 964.
32. Manojlovic, Z., and B. Stefanovic. 2012. A novel role of RNA helicase A in regulation of translation of type I collagen mRNAs. RNA 18:321–334.
33. McKenna, A., M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis, A. Kernytsky, et al. 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20:1297–1303.
34. Monnier, N., V. Procaccio, P. Stieglitz, and J. Lunardi. 1997. Malignant-hyperthermia susceptibility is associated with a mutation of the alpha 1-subunit of the human dihydropyridine-sensitive L-type voltage-dependent calcium-channel receptor in skeletal muscle. Am. J. Hum. Genet. 60:1316–1325.
35. Ng, S. B., E. H. Turner, P. D. Robertson, S. D. Flygare, A. W. Bigham, C. Lee, et al. 2009. Targeted capture and massively parallel sequencing of 12 human exomes. Nature 461:272– 276.
36. Ng, S. B., D. A. Nickerson, M. J. Bamshad, and J. Shendure. 2010. Massively parallel sequencing and rare disease. Hum. Mol. Genet. 19:R119–R124.
37. Pan, T. C., R. Z. Zhang, M. A. Pericak-Vance, R. Tandan, T. Fries, J. M. Stajich, et al. 1998. Missense mutation in a von Willebrand factor type A domain of the alpha 3(VI) collagen gene (COL6A3) in a family with Bethlem myopathy. Hum. Mol. Genet. 7:807–812.
38. Paolini, C., J. D. Fessenden, I. N. Pessah, and C. Franzini-Armstrong. 2004. Evidence for conformational coupling between two calcium channels. Proc. Natl. Acad. Sci. USA 101:12748–12752.
39. Petrovski, S., Q. Wang, E. L. Heinzen, A. S. Allen, and D. B. Goldstein. 2013. Genic intolerance to functional variation and the interpretation of personal genomes. PLoS Genet. 9: e1003709.
40. Polster, A., J. D. Ohrtman, K. G. Beam, and S. Papadopoulos. 2012. Fluorescence resonance energy transfer (FRET) indicates that association with the type I ryanodine receptor (RyR1) causes reorientation of multiple cytoplasmic domains of the dihydropyridine receptor (DHPR) alpha(1S) subunit. J. Biol. Chem. 287:41560–41568.
41. Rebbeck, R. T., Y. Karunasekara, P. G. Board, N. A. Beard, M. G. Casarotto, and A. F. Dulhunty. 2014. Skeletal muscle excitation-contraction coupling: who are the dancing partners? Int. J. Biochem. Cell Biol. 48:28–38.
42. Reva, B., Y. Antipin, and C. Sander. 2007. Determinants of protein function revealed by combinatorial entropy optimization. Genome Biol. 8:R232.
43. Reva, B., Y. Antipin, and C. Sander. 2011. Predicting the functional impact of protein mutations: application to cancer genomics. Nucleic Acids Res. 39:e118.
44. Richards, C. S., S. Bale, D. B. Bellissimo, S. Das, W. W. Grody, M. R. Hegde, et al. 2008. ACMG recommendations for standards for interpretation and reporting of sequence variations: Revisions 2007. Genet. Med. 10:294–300.
45. Sabatelli, P., S. K. Gara, P. Grumati, A. Urciuolo, F. Gualandi, R. Curci, et al. 2011. Expression of the collagen VI alpha5 and alpha6 chains in normal human skin and in skin of patients with collagen VI-related myopathies. J. Invest Dermatol. 131:99–107.
46. Sabatelli, P., F. Gualandi, S. K. Gara, P. Grumati, A. Zamparelli, E. Martoni, et al. 2012. Expression of collagen VI alpha5 and alpha6 chains in human muscle and in Duchenne muscular dystrophy-related muscle fibrosis. Matrix Biol. 31:187–196.
47. Sherry, S. T., M. H. Ward, M. Kholodov, J. Baker, L. Phan, E. M. Smigielski, et al. 2001. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res. 29:308– 311.
48. Shihab, H. A., J. Gough, D. N. Cooper, P. D. Stenson, G. L. Barker, K. J. Edwards, et al. 2013. Predicting the functional, molecular, and phenotypic consequences of amino acid substitutions using hidden Markov models. Hum. Mutat. 34:57–65.
49. Solomon, B. D., A. D. Nguyen, K. A. Bear, and T. G. Wolfsberg. 2013. Clinical genomic database. Proc. Natl. Acad. Sci. USA 110:9851–9855.
50. Sorato, E., S. Menazza, A. Zulian, P. Sabatelli, F. Gualandi, L. Merlini, et al. 2014. Monoamine oxidase inhibition prevents mitochondrial dysfunction and apoptosis in myoblasts from patients with collagen VI myopathies. Free Radic. Biol. Med. 75C:40–47.
51. Tagliavini, F., F. Sardone, S. Squarzoni, N. M. Maraldi, L. Merlini, C. Faldini, et al. 2013. Ultrastructural changes in muscle cells of patients with collagen VI-related myopathies. Muscles Ligaments Tendons J. 3:281–286.
52. Tagliavini, F., C. Pellegrini, F. Sardone, S. Squarzoni, M. Paulsson, R. Wagener, et al. 2014. Defective collagen VI alpha6 chain expression in the skeletal muscle of patients with collagen VI-related myopathies. Biochim. Biophys. Acta 1842:1604–1612.
53. Wu, S., M. C. Ibarra, M. C. Malicdan, K. Murayama, Y. Ichihara, H. Kikuchi, et al. 2006. Central core disease is due to RYR1 mutations in more than 90% of patients. Brain 129:1470–1480.
54. Yates, J. R., J. P. Warner, J. A. Smith, F. Deymeer, J. P. Azulay, I. Hausmanowa-Petrusewicz, et al. 1993. Emery-Dreifuss muscular dystrophy: linkage to markers in distal Xq28. J. Med. Genet. 30:108–111.
55. Yates, J. R., J. Bagshaw, V. M. Aksmanovic, E. Coomber, R. McMahon, J. L. Whittaker, et al. 1999. Genotype-phenotype analysis in X-linked Emery-Dreifuss muscular dystrophy and identification of a missense mutation associated with a milder phenotype. Neuromuscul. Disord. 9:159–165.