Exome sequencing identifies titin mutations causing hereditary myopathy with early respiratory failure (HMERF) in families of diverse ethnic origins

BMC Neurology

Volumn 13, Issue , 2013, Pages

  Toro, Camilo ^a   Olivé, Montse ^b   Dalakas, Marinos C ^c   Sivakumar, Kumaraswami ^d   Bilbao, Juan M ^e   Tyndel, Felix ^e   Vidal, Noemí ^b   Farrero, Eva ^b   Sambuughin, Nyamkhishig ^f   Goldfarb, Lev G ^g  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^c UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^d BARROW NEUROLOGICAL INSTITUTE   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

^f UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^g NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Fibronectin type III; HMERF; Myopathy; Respiratory failure; Titin; Titin A band mutation

Indexed keywords

ARGININE; CONNECTIN; FIBRONECTIN; TAR DNA BINDING PROTEIN;

ADULT; ARTICLE; CLINICAL ARTICLE; CLINICAL FEATURE; ELECTROMYOGRAM; ETHNICITY; EXOME; FEMALE; GENE IDENTIFICATION; GENE MUTATION; GENE SEQUENCE; GENETIC SCREENING; GENETIC VARIABILITY; HEREDITARY MYOPATHY WITH EARLY RESPIRATORY FAILURE; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; LUNG FUNCTION TEST; MALE; MISSENSE MUTATION; MUSCLE BIOPSY; MUSCLE STRENGTH; MUSCLE WEAKNESS; MYOPATHY; NERVE CONDUCTION; PHENOTYPE; RESPIRATORY FAILURE; SINGLE NUCLEOTIDE POLYMORPHISM;

ADOLESCENT; ADULT; DISABILITY EVALUATION; DNA MUTATIONAL ANALYSIS; ELECTROMYOGRAPHY; EXOME; FAMILY HEALTH; FEMALE; GENETIC DISEASES, INBORN; HUMANS; MALE; MUSCLE PROTEINS; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DISEASES; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN KINASES; RESPIRATORY INSUFFICIENCY; TOMOGRAPHY, X-RAY COMPUTED; UNITED STATES; YOUNG ADULT;

EID: 84875063943     PISSN: None     EISSN: 14712377     Source Type: Journal    
DOI: 10.1186/1471-2377-13-29     Document Type: Article

References (51)

1. Edström L, Thornell LE, Albo J, Landin S, Samuelsson M. Myopathy with respiratory failure and typical myofibrillar lesions. J Neurol Sci 1990, 96:211-228. 10.1016/0022-510X(90)90134-9, 2376753.
2. Chinnery PF, Johnson MA, Walls TJ, Gibson GJ, Fawcett PR, Jamieson S. A novel autosomal dominant distal myopathy with early respiratory failure: clinico-pathologic characteristics and exclusion of linkage to candidate genetic loci. Ann Neurol 2001, 49:443-452. 10.1002/ana.93, 11310621.
3. Birchall D, von der Hagen M, Bates D, Bushby KM, Chinnery PF. Subclinical semitendinosus and obturator externus involvement defines an autosomal dominant myopathy with early respiratory failure. Neuromuscul Disord 2005, 15:595-600. 10.1016/j.nmd.2005.05.002, 16084088.
4. Tasca G, Mirabella M, Broccolini A, Monforte M, Sabatelli M, Biscione GL. An Italian case of hereditary myopathy with early respiratory failure (HMERF) not associated with the titin kinase domain R279W mutation. Neuromuscul Disord 2010, 20:730-734. 10.1016/j.nmd.2010.07.269, 20708934.
5. Lange S, Xiang F, Yakovenko A, Vihola A, Hackman P, Rostkova E. The kinase domain of titin controls muscle gene expression and protein turnover. Science 2005, 308:1599-1603. 10.1126/science.1110463, 15802564.
6. Mayans O, van der Ven PF, Wilm M, Mues A, Young P, Fürst DO. Structural basis for activation of the titin kinase domain during myofibrillogenesis. Nature 1998, 395:863-869. 10.1038/27603, 9804419.
7. Pfeffer G, Elliott HR, Griffin H, Barresi R, Miller J, Marsh J. Titin mutation segregates with hereditary myopathy with early respiratory failure. Brain 2012, 135:1695-1713. 10.1093/brain/aws102, 22577215.
8. Ohlsson M, Hedberg C, Brådvik B, Lindberg C, Tajsharghi H, Danielsson O, Melberg A. Hereditary myopathy with early respiratory failure associated with a mutation in a-band titin. Brain 2012, 135:1682-1694. 10.1093/brain/aws103, 22577218.
9. Gerull B, Gramlich M, Atherton J, McNabb M, Trombitas K, Sasse-Klaassen S, Seidman JG. Mutations of TTN, encoding the giant muscle filament titin, cause familial dilated cardiomyopathy. Nat Genet 2002, 30:201-204. 10.1038/ng815, 11788824.
10. Hackman P, Vihola A, Haravuori H, Marchand S, Sarparanta J, De Seze J. Tibial muscular dystrophy is a titinopathy caused by mutations in TTN, the gene encoding the giant skeletal-muscle protein titin. Am J Hum Genet 2002, 71:492-500. 10.1086/342380, 379188, 12145747.
11. Haravuori H, Vihola A, Straub V, Auranen M, Richard I, Marchand S. Secondary calpain3 deficiency in 2q-linked muscular dystrophy: titin is the candidate gene. Neurology 2001, 56:869-877. 10.1212/WNL.56.7.869, 11294923.
12. Pénisson-Besnier I, Hackman P, Suominen T, Sarparanta J, Huovinen S, Richard-Crémieux I, Udd B. Myopathies caused by homozygous titin mutations: limb-girdle muscular dystrophy 2J and variations of phenotype. J Neurol Neurosurg Psychiatry 2010, 81:1200-1202. 10.1136/jnnp.2009.178434, 20571043.
13. Carmignac V, Salih MAM, Quijano-Roy S, Marchand S, Al Rayess MM, Mukhtar MM. C-terminal titin deletions cause a novel early-onset myopathy with fatal cardiomyopathy. Ann Neurol 2007, 61:340-351. 10.1002/ana.21089, 17444505.
14. Herman DS, Lam L, Taylor MRG, Wang L, Teekakirikul P, Christodoulou D, Conner L. Truncations of titin causing dilated cardiomyopathy. New Engl J Med 2012, 366:619-628. 10.1056/NEJMoa1110186, 22335739.
15. Fürst DO, Osborn M, Nave R, Weber K. The organization of titin filaments in the half-sarcomere revealed by monoclonal antibodies in immunoelectron microscopy: a map of ten nonrepetitive epitopes starting at the Z line extends close to M line. J Cell Biol 1988, 106:1563-1572. 10.1083/jcb.106.5.1563, 2115059, 2453516.
16. Bang ML, Centner T, Fornoff F, Geach AJ, Gotthardt M, McNabb M. The complete gene sequence of titin, expression of an unusual approximately 700-kDa titin isoform, and its interaction with obscurin identify a novel Z-disc to I-band linking system. Circ Res 2001, 89:1065-1072. 10.1161/hh2301.100981, 11717165.
17. Gregorio CC, Granzier H, Sorimachi H, Labeit S. Muscle assembly: a titanic achievement?. Curr Opin Cell Biol 1999, 11:18-25. 10.1016/S0955-0674(99)80003-9, 10047523.
18. Labeit S, Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 1995, 270:293-296. 10.1126/science.270.5234.293, 7569978.
19. Puchner EM, Alexandrovich A, Kho AL, Hensen U, Schafer LV, Brandmeier B. Mechanoenzymatics of titin kinase. Proc Natl Acad Sci USA 2008, 105:13385-13390. 10.1073/pnas.0805034105, 2527993, 18765796.
20. Muhle-Goll C, Habeck M, Cazorla O, Nilges M, Labeit S, Granzier H. Structural and functional studies of titin's fn3 modules reveal conserved surface patterns and binding to myosin S1-a possible role in the frank-starling mechanism of the heart. J Mol Biol 2001, 313:431-447. 10.1006/jmbi.2001.5017, 11800567.
21. Tskhovrebova L, Trinick J. Titin: properties and family relationships. Nat Rev Mol Cell Biol 2003, 4:679-689.
22. Gautel M, Goulding D, Bullard B, Weber K, Fürst DO. The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J Cell Sci 1996, 109:2747-2754.
23. Labeit S, Barlow DP, Gautel M, Gibson T, Holt J, Hsieh CL. A regular pattern of two types of 100-residue motif in the sequence of titin. Nature 1990, 345:273-276. 10.1038/345273a0, 2129545.
24. Labeit S, Gautel M, Lakey A, Trinick J. Towards a molecular understanding of titin. EMBO J 1992, 11:1711-1716. 556628, 1582406.
25. Trinick J. Titin and nebulin: protein rulers in muscle?. Trends Biochem Sci 1994, 19:405-409. 10.1016/0968-0004(94)90088-4, 7817397.
26. Shatunov A, Olivé M, Odgerel Z, Stadelmann-Nessler C, Irlbacher K, van Landeghem F. In-frame deletion in the seventh immunoglobulin-like repeat of filamin C in a family with myofibrillar myopathy. Eur J Hum Genet 2009, 17:656-663. 10.1038/ejhg.2008.226, 2672961,2672961, 19050726.
27. Olivé M, Odgerel Z, Martínez A, Poza JJ, Bragado FG, Zabalza RJ. Clinical and myopathological evaluation of early- and late-onset subtypes of myofibrillar myopathy. Neuromuscul Disord 2011, 21:533-542. 10.1016/j.nmd.2011.05.002, 21676617.
28. Adams DR, Sincan M, Fuentes Fajardo K, Mullikin JC, Pierson TM. Analysis of DNA sequence variants detected by high-throughput sequencing. Hum Mutat 2012, 33:599-608. 10.1002/humu.22035, 22290882.
29. Teer JK, Bonnycastle LL, Chines PS, Hansen NF, Aoyama N, Swift AJ. Systematic comparison of three genomic enrichment methods for massively parallel DNA sequencing. Genome Res 2010, 20:1420-1431. 10.1101/gr.106716.110, 2945191, 20810667.
30. Johnston JJ, Teer JK, Cherukuri PF, Hansen NF, Loftus SK, . NIH Intramural Sequencing Center Massively parallel sequencing of exons on the X chromosome identifies RBM10 as the gene that causes a syndromic form of cleft palate. Am J Hum Genet 2010, 86:743-748. 10.1016/j.ajhg.2010.04.007, 2868995, 20451169, NIH Intramural Sequencing Center.
31. Jahn L, Sadoshima J, Izumo S. Cyclins and cyclin-dependent kinases are differentially regulated during terminal differentiation of C2C12 muscle cells. Exp Cell Res 1994, 212:297-307. 10.1006/excr.1994.1147, 8187822.
32. Nakano S, Engel AG, Akiguchi I, Kimura J. Myofibrillar myopathy. III. Abnormal expression of cyclin-dependent kinases and nuclear proteins. J Neuropathol Exp Neurol 1997, 56:850-856. 10.1097/00005072-199708000-00002, 9258254.
33. Bucher RM, Svergun DI, Muhle-Goll C, Mayans O. The structure of the FnIII tandem A77-A78 points to a periodically conserved architecture in the myosin-binding region of titin. J Mol Biol 2010, 401:843-853. 10.1016/j.jmb.2010.06.011, 20542041.
34. Nicolao P, Xiang F, Gunnarsson LG, Giometto B, Edström L, Anvret M, Zhang Z. Autosomal dominant myopathy with proximal weakness and early respiratory muscle involvement maps to chromosome 2q. Am J Hum Genet 1999, 64:788-792. 10.1086/302281, 1377796, 10053013.
35. Neumann M, Kwong LK, Sampathu DM, Trojanowski JQ, Lee VM. TDP-43 proteinopathy in frontotemporal lobar degeneration and amyotrophic lateral sclerosis: protein misfolding diseases without amyloidosis. Arch Neurol 2007, 64:1388-1394. 10.1001/archneur.64.10.1388, 17923623.
36. Weihl CC, Temiz P, Miller SE, Watts G, Smith C, Forman M. TDP-43 accumulation in inclusion body myopathy muscle suggests a common pathogenic mechanism with frontotemporal dementia. J Neurol Neurosurg Psychiatry 2008, 79:1186-1189. 10.1136/jnnp.2007.131334, 2586594, 18796596.
37. Olivé M, Janué A, Moreno D, Gámez J, Torrejón-Escribano B, Ferrer I. TAR DNA-binding protein 43 accumulation in protein aggregate myopathies. J Neuropathol Exp Neurol 2009, 68:262-273. 10.1097/NEN.0b013e3181996d8f, 19225410.
38. Küsters B, van Hoeve BJ, Schelhaas HJ, Ter Laak H, van Engelen BG, Lammens M. TDP-43 accumulation is common in myopathies with rimmed vacuoles. Acta Neuropathol 2009, 117:209-211. 10.1007/s00401-008-0471-2, 19066918.
39. Goebel HH. Protein aggregate myopathies. Introduction. Brain Pathol 2009, 19:480-482.
40. Tsuburaya RS, Monma K, Oya Y, Nakayama T, Fukuda T, Sugie H. Acid phosphatase-positive globular inclusions is a good diagnostic marker for two patients with adult-onset pompe disease lacking disease specific pathology. Neuromuscul Disorders 2012, 22:389-393.
41. van der Ploeg AT, Reuser AJ. Pompe's Disease. Lancet 2008, 372:1342-1353. 10.1016/S0140-6736(08)61555-X, 18929906.
42. Pénisson-Besnier I, Talvinen K, Dumez C, Vihola A, Dubas F, Fardeau M. Myotilinopathy in a family with late onset myopathy. Neuromuscul Disord 2006, 16:427-431. 10.1016/j.nmd.2006.04.009, 16793270.
43. Fischer D, Clemen CS, Olive' M, Ferrer I, Goudeau B, Roth U. Different early pathogenesis in myotilinopathy compared to primary desminopathy. Neuromuscul Disord 2006, 16:361-367. 10.1016/j.nmd.2006.03.007, 16684602.
44. Claeys KG, Fardeau M, Schröder R, Suominen T, Tolksdorf K, Behin A. Electron microscopy in myofibrillar myopathies reveal clues to the mutated gene. Neuromuscul Disord 2008, 18:656-666. 10.1016/j.nmd.2008.06.367, 18653338.
45. Kley RA, Hellenbroich Y, van der Ven PF, Fürst DO, Huebner A, Bruchertseifer V. Clinical and morphological phenotype of the filamin myopathy: a study of 31 german patients. Brain 2007, 130:3250-3264. 10.1093/brain/awm271, 18055494.
46. Tasca G, Odgerel Z, Monforte M, Aurino S, Clarke NF, Waddell LB, Udd B, Ricci E, Goldfarb LG. Novel FLNC mutation in a patient with myofibrillar myopathy in combination with late-onset cerebellar ataxia. Muscle Nerve 2012, 46:275-282. 10.1002/mus.23349, 22806379.
47. Goldfarb LG, Dalakas MC. Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. J Clin Invest 2009, 119:1806-1813. 10.1172/JCI38027, 2701871, 19587455.
48. Selcen D. Myofibrillar myopathies. Neuromuscul Disord 2011, 21:161-171. 10.1016/j.nmd.2010.12.007, 3052736, 21256014.
49. Taylor M, Graw S, Sinagra G, Barnes C, Slavov D, Brun F. Genetic variation in titin in arrhythmogenic right ventricular cardiomyopathy-overlap syndromes. Circulation 2011, 124:876-885. 10.1161/CIRCULATIONAHA.110.005405, 3167235, 21810661.
50. Steward A, Adhya S, Clarke J. Sequence conservation in Ig-like domains: the role of highly conserved proline residues in the fibronectin type III superfamily. J Mol Biol 2002, 318:935-940. 10.1016/S0022-2836(02)00184-5, 12054791.
51. Gautel M. Cytoskeletal protein kinases: titin and its relations in mechanosensing. Pflugers Arch 2011, 462:119-134. 10.1007/s00424-011-0946-1, 3114093, 21416260.