Molecular and cellular basis of calpainopathy (limb girdle muscular dystrophy type 2A)

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1772, Issue 2, 2007, Pages 128-144

  Kramerova, Irina ^a   Beckmann, Jacques S ^b   Spencer, Melissa J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

Calpain; Dysferlin; Dystrophy; Muscle; Titin

Indexed keywords

CALPAIN; CALPAIN 3; CYTOSKELETON PROTEIN; DYSFERLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MUSCLE PROTEIN; PROTEASOME; PROTEINASE; UBIQUITIN;

AUTOSOMAL RECESSIVE INHERITANCE; CALPAINOPATHY; CAPN3 GENE; CONGENITAL HEART MALFORMATION; CYTOSKELETON; GENE; GENE MUTATION; HISTOPATHOLOGY; HUMAN; LIMB GIRDLE MUSCULAR DYSTROPHY; LIMB GIRDLE MUSCULAR DYSTROPHY TYPE 2A; MUSCLE ATROPHY; MUSCLE FIBRIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SARCOMERE;

ANIMALS; CALPAIN; HUMANS; MUSCLE PROTEINS; MUSCULAR DYSTROPHIES, LIMB-GIRDLE; MUTATION, MISSENSE;

EID: 33846372980     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2006.07.002     Document Type: Review

References (125)

1. Bushby K. Report on the 12th ENMC sponsored international workshop-The "limb-girdle" muscular dystrophies. Neuromuscul. Disord. 2 (1992) 3-5
2. Richard I., Broux O., Allamand V., Fougerousse F., Chiannilkulchai N., Bourg N., Brenguier L., Devaud C., Pasturaud P., Roudaut C., et al. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81 (1995) 27-40
3. Guyon J.R., Kudryashova E., Potts A., Dalkilic I., Brosius M.A., Thompson T.G., Beckmann J.S., Kunkel L.M., and Spencer M.J. Calpain 3 cleaves filamin C and regulates its ability to interact with gamma- and delta-sarcoglycans. Muscle Nerve 28 (2003) 472-483
4. Kramerova I., Kudryashova E., Venkatraman G., and Spencer M.J. Calpain 3 participates in muscle remodeling by acting upstream of the ubiquitin-proteasome pathway. Hum. Mol. Genet. 14 (2005) 2125-2134
5. Taveau M., Bourg N., Sillon G., Roudaut C., Bartoli M., and Richard I. Calpain 3 is activated through autolysis within the active site and lyses sarcomeric and sarcolemmal components. Mol. Cell. Biol. 23 (2003) 9127-9135
6. Erb W.H. Ueber die "juvenile Form" der progressiven Muskelatrophie und ihre Beziehungen zur sogehannten Pseudohypertrophie der Muskeln. Deutsch. Archiv. Klin. Med. 34 (1884) 467-519
7. Walton J.N., and Nattrass F.J. On the classification, natural history and treatment of the myopathies. Brain 77 (1954) 169-231
8. Beckmann J.S., Richard I., Hillaire D., Broux O., Antignac C., Bois E., Cann H., Cottingham Jr. R.W., Feingold N., Feingold J., et al. A gene for limb-girdle muscular dystrophy maps to chromosome 15 by linkage. C. R. Acad. Sci. III 312 (1991) 141-148
9. Brooke M.H. Clinical examination of patients with neuromuscular disease. Adv. Neurol. 17 (1977) 25-39
10. Bradley W.G., and Kelemen J. Genetic counseling in Duchenne muscular dystrophy. Muscle Nerve 2 (1979) 325-328
11. Fougerousse F., Broux O., Richard I., Allamand V., de S.A., Bourg N., Brenguier L., Devaud C., Pasturaud P., Roudaut C., et al. Mapping of a chromosome 15 region involved in limb girdle muscular dystrophy. Hum. Mol. Genet. 3 (1994) 285-293
12. Chiannilkulchai N., Pasturaud P., Richard I., Auffray C., and Beckmann J.S. A primary expression map of the chromosome 15q15 region containing the recessive form of limb-girdle muscular dystrophy (LGMD2A) gene. Hum. Mol. Genet. 4 (1995) 717-725
13. Allamand V., Broux O., Richard I., Fougerousse F., Chiannilkulchai N., Bourg N., Brenguier L., Devaud C., Pasturaud P., Pereira de Souza A., et al. Preferential localization of the limb-girdle muscular dystrophy type 2A gene in the proximal part of a 1-cM 15q15.1-q15.3 interval. Am. J. Hum. Genet. 56 (1995) 1417-1430 (see comments)
14. Allamand V., and Beckmann J.S. Mapping using linkage disequilibrium estimates: a comparative study. Hum. Hered. 47 (1997) 237-240
15. Sorimachi H., Imajoh O.S., Emori Y., Kawasaki H., Ohno S., Minami Y., and Suzuki K. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types. Specific expression of the mRNA in skeletal muscle. J. Biol. Chem. 264 (1989) 20106-20111
16. Sorimachi H., Forsberg N.E., Lee H.J., Joeng S.Y., Richard I., Beckmann J.S., Ishiura S., and Suzuki K. Highly conserved structure in the promoter region of the gene for muscle-specific calpain, p94. Biol. Chem. 377 (1996) 859-864
17. Herasse M., Ono Y., Fougerousse F., Kimura E., Stockholm D., Beley C., Montarras D., Pinset C., Sorimachi H., Suzuki K., et al. Expression and functional characteristics of calpain 3 isoforms generated through tissue-specific transcriptional and posttranscriptional events. Mol.Cell. Biol. 19 (1999) 4047-4055
18. Bushby K.M. Diagnostic criteria for the limb-girdle muscular dystrophies: report of the ENMC Consortium on Limb-Girdle Dystrophies. Neuromuscul. Disord. 5 (1995) 71-74
19. Bushby K.M., and Beckmann J.S. The limb-girdle muscular dystrophies-proposal for a new nomenclature. Neuromuscul. Disord. 5 (1995) 337-343
20. Fanin M., Nascimbeni A.C., Fulizio L., Trevisan C.P., Meznaric-Petrusa M., and Angelini C. Loss of calpain-3 autocatalytic activity in LGMD2A patients with normal protein expression. Am. J. Pathol. 163 (2003) 1929-1936
21. Allamand V., Broux O., Bourg N., Richard I., Tischfield J.A., Hodes M.E., Conneally P.M., Fardeau M., Jackson C.E., and Beckmann J.S. Genetic heterogeneity of autosomal recessive limb-girdle muscular dystrophy in a genetic isolate (Amish) and evidence for a new locus. Hum. Mol. Genet. 4 (1995) 459-463
22. Lim L.E., Duclos F., Broux O., Bourg N., Sunada Y., Allamand V., Meyer J., Richard I., Moomaw C., Slaughter C., et al. Beta-sarcoglycan: characterization and role in limb-girdle muscular dystrophy linked to 4q12. Nat. Genet. 11 (1995) 257-265
23. Fokkema I.F., den Dunnen J.T., and Taschner P.E. LOVD: easy creation of a locus-specific sequence variation database using an "LSDB-in-a-box" approach. Hum. Mutat. 26 (2005) 63-68
24. Ono Y., Shimada H., Sorimachi H., Richard I., Saido T.C., Beckmann J.S., Ishiura S., and Suzuki K. Functional defects of a muscle-specific calpain, p94, caused by mutations associated with limb-girdle muscular dystrophy type 2A. J. Biol. Chem. 273 (1998) 17073-17078
25. Kramerova I., Kudryashova E., Tidball J.G., and Spencer M.J. Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum. Mol. Genet. 13 (2004) 1373-1388
26. Saenz A., Leturcq F., Cobo A.M., Poza J.J., Ferrer X., Otaegui D., Camano P., Urtasun M., Vilchez J., Gutierrez-Rivas E., et al. LGMD2A: genotype-phenotype correlations based on a large mutational survey on the calpain 3 gene. Brain 128 (2005) 732-742
27. Richard I., Roudaut C., Saenz A., Pogue R., Grimbergen J.E., Anderson L.V., Beley C., Cobo A.M., de Diego C., Eymard B., et al. Calpainopathy-a survey of mutations and polymorphisms. Am. J. Hum. Genet. 64 (1999) 1524-1540
28. Fanin M., Nascimbeni A.C., Fulizio L., and Angelini C. The frequency of limb girdle muscular dystrophy 2A in northeastern Italy. Neuromuscul. Disord. 15 (2005) 218-224
29. Chou F.L., Angelini C., Daentl D., Garcia C., Greco C., Hausmanowa-Petrusewicz I., Fidzianska A., Wessel H., and Hoffman E.P. Calpain III mutation analysis of a heterogeneous limb-girdle muscular dystrophy population. Neurology 52 (1999) 1015-1020
30. Richard I., Roudaut C., Fougerousse F., Chiannilkulchai N., and Beckmann J.S. An STS map of the limb girdle muscular dystrophy type 2A region. Mamm. Genome 6 (1995) 754-756
31. Richard I., and Beckmann J.S. How neutral are synonymous codon mutations?. Nat. Genet. 10 (1995) 259 (letter)
32. Urtasun M., Sáenz A., Roudaut C., Poza J.J., Urtizberea J.A., Cobo A.M., Richard I., García Bragado F., Leturcq F., Kaplan J.C., et al. Limb-girdle muscular dystrophy in Guipúzcoa (Basque Country, Spain). Brain 121 (1998) 1735-1747
33. Beckmann J.S. Disease taxonomy-monogenic muscular dystrophy. Br. Med. Bull 55 (1999) 340-357
34. Zajdel R.W., Sanger J.M., Denz C.R., Lee S., Dube S., Poiesz B.J., Sanger J.W., and Dube D.K. A novel striated tropomyosin incorporated into organized myofibrils of cardiomyocytes in cell and organ culture. FEBS Lett. 520 (2002) 35-39
35. Zlotogora J., Gieselmann V., and Bach G. Multiple mutations in a specific gene in a small geographic area: a common phenomenon?. Am. J. Hum. Genet. 58 (1996) 241-243
36. Jia Z., Petrounevitch V., Wong A., Moldoveanu T., Davies P.L., Elce J.S., and Beckmann J.S. Mutations in calpain 3 associated with limb girdle muscular dystrophy: analysis by molecular modeling and by mutation in m-calpain. Biophys. J. 80 (2001) 2590-2596
37. Zatz M., Vainzof M., and Passos-Bueno M.R. Limb-girdle muscular dystrophy: one gene with different phenotypes, one phenotype with different genes. Curr. Opin. Neurol. 13 (2000) 511-517
38. Pénisson-Besnier I., Richard I., Dubas F., Beckmann J.S., and Fardeau M. Pseudometabolic expression and phenotypic variability of calpain deficiency in two siblings. Muscle Nerve 21 (1998) 1078-1080
39. Richard I., Brenguier L., Dincer P., Roudat C., Bady B., Burgunder J.-M., Chamaly R., Garcia C.A., Halaby G., Jackson C.E., et al. Multiple independent molecular etiology for Limb-Girdle Muscular Dystrophy Type 2A patients from various geographical origins. Am. J. Hum. Genet. 60 (1997) 1128-1138
40. Kawai H., Akaike M., Kunishige M., Inui T., Adachi K., Kimura C., Kawajiri M., Nishida Y., Endo I., Kashiwagi S., et al. Clinical, pathological, and genetic features of limb-girdle muscular dystrophy type 2A with new calpain 3 gene mutations in seven patients from three Japanese families. Muscle Nerve 21 (1998) 1493-1501
41. Chae J., Minami N., Jin Y., Nakagawa M., Murayama K., Igarashi F., and Nonaka I. Calpain 3 gene mutations: genetic and clinico-pathologic findings in limb-girdle muscular dystrophy. Neuromuscul. Dis. 11 (2001) 547-555
42. Mercuri E., Bushby K., Ricci E., Birchall D., Pane M., Kinali M., Allsop J., Nigro V., Saenz A., Nascimbeni A., et al. Muscle MRI findings in patients with limb girdle muscular dystrophy with calpain 3 deficiency (LGMD2A) and early contractures. Neuromuscul. Disord. 15 (2005) 164-171
43. Fougerousse G., Durand M., Suel L., Pourquie O., Delezoide A., Romero N.B., Abitbol M., and Beckmann J.S. Expression of Genes (CAPN3, SGCA, SGCB, AND TTN) involved in progressive muscular dystrophies during early human development. Genomics 48 (1998) 145-156
44. Hermanova M., Zapletalova E., Sedlackova J., Chrobakova T., Letocha O., Kroupova I., Zamecnik J., Vondracek P., Mazanec R., Marikova T., et al. Analysis of histopathologic and molecular pathologic findings in Czech LGMD2A patients. Muscle Nerve 33 (2006) 424-432
45. Tagawa K., Taya C., Hayashi Y., Nakagawa M., Ono Y., Fukuda R., Karasuyama H., Toyama-Sorimachi N., Katsui Y., Hata S., et al. Myopathy phenotype of transgenic mice expressing active site-mutated inactive p94 skeletal muscle-specific calpain, the gene product responsible for limb girdle muscular dystrophy type 2A. Hum. Mol. Genet. 9 (2000) 1393-1402
46. Vainzof M., de Paula F., Tsanaclis A.M., and Zatz M. The effect of calpain 3 deficiency on the pattern of muscle degeneration in the earliest stages of LGMD2A. J. Clin. Pathol. 56 (2003) 624-626
47. Goll D.E., Thompson V.F., Li H., Wei W., and Cong J. The calpain system. Physiol. Rev. 83 (2003) 731-801
48. Sorimachi H., and Suzuki K. The structure of calpain. J. Biochem. 129 (2001) 653-664
49. Moldoveanu T., Hosfield C.M., Lim D., Elce J.S., Jia Z., and Davies P.L. A Ca(2+) switch aligns the active site of calpain. Cell 108 (2002) 649-660
50. Kinbara K., Ishiura S., Tomioka S., Sorimachi H., Jeong S.Y., Amano S., Kawasaki H., Kolmerer B., Kimura S., Labeit S., et al. Purification of native p94, a muscle-specific calpain, and characterization of its autolysis. Biochem. J. 335 (1998) 589-596
51. Ravulapalli R., Diaz B.G., Campbell R.L., and Davies P.L. Homodimerization of calpain 3 penta-EF-hand domain. Biochem. J. 388 (2005) 585-591
52. Sorimachi H., Kimura S., Kinbara K., Kazama J., Takahashi M., Yajima H., Ishiura S., Sasagawa N., Nonaka I., Sugita H., et al. Structure and physiological functions of ubiquitous and tissue-specific calpain species. Muscle-specific calpain, p94, interacts with connectin/titin. Adv. Biophys. 33 (1996) 101-122
53. Sorimachi H., Kinbara K., Kimura S., Takahashi M., Ishiura S., Sasagawa N., Sorimachi N., Shimada H., Tagawa K., Maruyama K., et al. Muscle-specific calpain, p94, responsible for limb girdle muscular dystrophy type 2A, associates with connectin through IS2, a p94-specific sequence. J. Biol. Chem. 270 (1995) 31158-31162
54. Diaz B.G., Moldoveanu T., Kuiper M.J., Campbell R.L., and Davies P.L. Insertion sequence 1 of muscle-specific calpain, p94, acts as an internal propeptide. J. Biol. Chem. (2004) 27656-27666
55. Ma H., Shih M., Fukiage C., Azuma M., Duncan M.K., Reed N.A., Richard I., Beckmann J.S., and Shearer T.R. Influence of specific regions in Lp82 calpain on protein stability, activity, and localization within the lens. Invest. Ophthalmol. Visual Sci. 41 (2000) 4232-4239
56. Azuma M., Fukiage C., Higashine M., Nakajima T., Ma H., and Shearer T.R. Identification and characterization of a retina-specific calpain (Rt88) from rat. Curr. Eye Res. 21 (2000) 710-720
57. Nakajima T., Fukiage C., Azuma M., Ma H., and Shearer T.R. Different expression patterns for ubiquitous calpains and Capn3 splice variants in monkey ocular tissues. Biochim. Biophys. Acta 1519 (2001) 55-64
58. Spencer M.J., Guyon J.R., Sorimachi H., Potts A., Richard I., Herasse M., Chamberlain J., Dalkilic I., Kunkel L.M., and Beckmann J.S. Stable expression of calpain 3 from a muscle transgene in vivo: immature muscle in transgenic mice suggests a role for calpain 3 in muscle maturation. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 8874-8879
59. Ono Y., Kakinuma K., Torii F., Irie A., Nakagawa K., Labeit S., Abe K., Suzuki K., and Sorimachi H. Possible regulation of the conventional calpain system by skeletal muscle-specific calpain, p94/calpain 3. J. Biol. Chem. 279 (2004) 2761-2771
60. Fukiage C., Nakajima E., Ma H., Azuma M., and Shearer T.R. Characterization and regulation of lens-specific calpain Lp82. J. Biol. Chem. 277 (2002) 20678-20685
61. De Tullio R., Stifanese R., Salamino F., Pontremoli S., and Melloni E. Characterization of a new p94-like calpain form in human lymphocytes. Biochem. J. 375 (2003) 689-696
62. Konig N., Raynaud F., Feane H., Durand M., Mestre-Frances N., Rossel M., Ouali A., and Benyamin Y. Calpain 3 is expressed in astrocytes of rat and Microcebus brain. J. Chem. Neuroanat. 25 (2003) 129-136
63. Welm A.L., Timchenko N.A., Ono Y., Sorimachi H., Radomska H.S., Tenen D.G., Lekstrom-Himes J., and Darlington G.J. C/EBPalpha is required for proteolytic cleavage of cyclin A by calpain 3 in myeloid precursor cells. J. Biol. Chem. 277 (2002) 33848-33856
64. Hosfield C.M., Elce J.S., Davies P.L., and Jia Z. Crystal structure of calpain reveals the structural basis for Ca(2+)-dependent protease activity and a novel mode of enzyme activation. EMBO J. 18 (1999) 6880-6889
65. Ohno S., Emori Y., Imajoh S., Kawasaki H., Kisaragi M., and Suzuki K. Evolutionary origin of a calcium-dependent protease by fusion of genes for a thiol protease and a calcium-binding protein?. Nature 312 (1984) 566-570
66. Sorimachi H., Ishiura S., and Suzuki K. Structure and physiological function of calpains. Biochem. J. 328 (1997) 721-732
67. Strobl S., Fernandez-Catalan C., Braun M., Huber R., Masumoto H., Nakagawa K., Irie A., Sorimachi H., Bourenkow G., Bartunik H., et al. The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 588-592
68. Hosfield C.M., Moldoveanu T., Davies P.L., Elce J.S., and Jia Z. Calpain mutants with increased Ca2+ sensitivity and implications for the role of the C(2)-like domain. J. Biol. Chem. 276 (2001) 7404-7407
69. Moldoveanu T., Jia Z., and Davies P.L. Calpain activation by cooperative Ca2+ binding at two non-EF-hand sites. J. Biol. Chem. 279 (2004) 6106-6114
70. Garcia Diaz B.E., Gauthier S., and Davies P.L. Ca2+ dependency of calpain 3 (p94) activation. Biochemistry 45 (2006) 3714-3722
71. Sorimachi H., Toyama-Sorimachi N., Saido T.C., Kawasaki H., Sugita H., Miyasaka M., Arahata K., Ishiura S., and Suzuki K. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268 (1993) 10593-10605
72. Branca D., Gugliucci A., Bano D., Brini M., and Carafoli E. Expression, partial purification and functional properties of themuscle-specific calpain isoform p94. Eur. J. Biochem. 265 (1999) 839-846
73. Rey M.A., and Davies P.L. The protease core of the muscle-specific calpain, p94, undergoes Ca2+-dependent intramolecular autolysis. FEBS Lett. 532 (2002) 401-406
74. Baghdiguian S., Martin M., Richard I., Pons F., Astier C., Bourg N., Hay R.T., Chemaly R., Halaby G., Loiselet J., et al. Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IkappaB alpha/NF-kappaB pathway in limb-girdle muscular dystrophy type 2A. Nat. Med. 5 (1999) 503-511 (published erratum appears in Nat Med 1999 Jul;5(7):849)
75. Cai D., Frantz J.D., Tawa N.E., Jr. P.A., Melendez B.C., Oh H.G., Lidov P.O., Hasselgren W.R., Frontera J., Lee D.J., et al. IKKbeta/NF-kappaB activation causes severe muscle wasting in mice. Cell 119 (2004) 285-298
76. Richard I., Roudaut C., Marchand S., Baghdiguian S., Herasse M., Stockholm D., Ono Y., Suel L., Bourg N., Sorimachi H., et al. Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IKBa/Nuclear Factor KB pathway perturbation in mice. J. Cell Biol. 151 (2000) 1-9
77. Thompson T.G., Chan Y.M., Hack A.A., Brosius M., Rajala M., Lidov H.G., McNally E.M., Watkins S., and Kunkel L.M. Filamin 2 (FLN2): a muscle-specific sarcoglycan interacting protein. J. Cell Biol. 148 (2000) 115-126
78. Stossel T.P., Condeelis J., Cooley L., Hartwig J.H., Noegel A., Schleicher M., and Shapiro S.S. Filamins as integrators of cell mechanics and signalling. Nat. Rev., Mol. Cell Biol. 2 (2001) 138-145
79. van der Ven P.F., Wiesner S., Salmikangas P., Auerbach D., Himmel M., Kempa S., Hayess K., Pacholsky D., Taivainen A., Schröder R., et al. Indications for a novel muscular dystrophy pathway. gamma-filamin, the muscle-specific filamin isoform, interacts with myotilin. J. Cell Biol. 151 (2000) 235-248
80. Vorgerd M., van der Ven P.F., Bruchertseifer V., Lowe T., Kley R.A., Schroder R., Lochmuller H., Himmel M., Koehler K., Furst D.O., et al. A mutation in the dimerization domain of filamin c causes a novel type of autosomal dominant myofibrillar myopathy. Am. J. Hum. Genet. 77 (2005) 297-304
81. Bansal D., and Campbell K.P. Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol. 14 (2004) 206-213
82. Bashir R., Britton S., Strachan T., Keers S., Vafiadaki E., Lako M., Richard I., Marchand S., Bourg N., Argov Z., et al. A gene related to Caenorhabditis elegans spermatogenesis factor fer-1 is mutated in limb-girdle muscular dystrophy type 2B. Nat. Genet. 20 (1998) 37-42
83. Liu J., Aoki M., Illa I., Wu C., Fardeau M., Angelini C., Serrano C., Urtizberea J.A., Hentati F., Hamida M.B., et al. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat. Genet. 20 (1998) 31-36
84. Illa I., Serrano-Munuera C., Gallardo E., Lasa A., Rojas-Garcia R., Palmer J., Gallano P., Baiget M., Matsuda C., and Brown R.H. Distal anterior compartment myopathy: a dysferlin mutation causing a new muscular dystrophy phenotype. Ann. Neurol. 49 (2001) 130-134
85. Bansal D., Miyake K., Vogel S.S., Groh S., Chen C.C., Williamson R., McNeil P.L., and Campbell K.P. Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423 (2003) 168-172
86. Anderson L.V.B., Harrison R.M., Pogue R., Vafiadaki E., Pollitt C., Davison K., Moss J.A., Keers S., Pyle A., Shaw P.J., et al. Secondary reduction in calpain 3 expression in patients with limb girdle muscular dystrophy type 2B and Miyoshi myopathy (primary dysferlinopathies). Neuromuscul. Dis. 10 (2000) 553-559
87. Chrobakova T., Hermanova M., Kroupova I., Vondracek P., Marikova T., Mazanec R., Zamecnik J., Stanek J., Havlova M., and Fajkusova L. Mutations in Czech LGMD2A patients revealed by analysis of calpain3 mRNA and their phenotypic outcome. Neuromuscul. Disord. 14 (2004) 659-665
88. Huang Y., Verheesen P., Roussis A., Frankhuizen W., Ginjaar I., Haldane F., Laval S., Anderson L.V., Verrips T., Frants R.R., et al. Protein studies in dysferlinopathy patients using llama-derived antibody fragments selected by phage display. Eur. J. Hum. Genet. 13 (2005) 721-730
89. Lennon N.J., Kho A., Bacskai B.J., Perlmutter S.L., Hyman B.T., and Brown Jr. R.H. Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing. J. Biol. Chem. 278 (2003) 50466-50473
90. Fougerousse F., Gonin P., Durand M., Richard I., and Raymackers J.M. Force impairment in calpain 3-deficient mice is not correlated with mechanical disruption. Muscle Nerve 27 (2003) 616-623
91. Keira Y., Noguchi S., Minami N., Hayashi Y.K., and Nishino I. Localization of calpain 3 in human skeletal muscle and its alteration in limb-girdle muscular dystrophy 2A muscle. J. Biochem. (Tokyo) 133 (2003) 659-664
92. Kinbara K., Sorimachi H., Ishiura S., and Suzuki K. Muscle-specific calpain, p94, interacts with the extreme C-terminal region of connectin, a unique region flanked by two immunoglobulin C2 motifs. Arch. Biochem. Biophys. 342 (1997) 99-107
93. Gregorio C.C., Granzier H., Sorimachi H., and Labeit S. Muscle assembly: a titanic achievement?. Curr. Opin. Cell Biol. 11 (1999) 18-25
94. Granzier H.L., and Labeit S. Titin and its associated proteins: the third myofilament system of the sarcomere. Adv. Protein Chem. 71 (2005) 89-119
95. Labeit S., and Kolmerer B. Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270 (1995) 293-296 (see comments)
96. Wang K., Forbes J.G., and Jin A.J. Single molecule measurements of titin elasticity. Prog. Biophys. Mol. Biol. 77 (2001) 1-44
97. Lange S., Xiang F., Yakovenko A., Vihola A., Hackman P., Rostkova E., Kristensen J., Brandmeier B., Franzen G., Hedberg B., et al. The kinase domain of titin controls muscle gene expression and protein turnover. Science 308 (2005) 1599-1603
98. Garvey S.M., Rajan C., Lerner A.P., Frankel W.N., and Cox G.A. The muscular dystrophy with myositis (mdm) mouse mutation disrupts a skeletal muscle-specific domain of titin. Genomics 79 (2002) 146-149
99. Haravuori H., Vihola A., Straub V., Auranen M., Richard I., Marchand S., Voit T., Labeit S., Somer H., Peltonen L., et al. Secondary calpain3 deficiency in 2q-linked muscular dystrophy: titin is the candidate gene. Neurology 56 (2001) 869-877
100. Witt C.C., Ono Y., Puschmann E., McNabb M., Wu Y., Gotthardt M., Witt S.H., Haak M., Labeit D., Gregorio C.C., et al. Induction and myofibrillar targeting of CARP, and suppression of the Nkx2.5 pathway in the MDM mouse with impaired titin-based signaling. J. Mol. Biol. 336 (2004) 145-154
101. Jenne D.E., Kley R.A., Vorgerd M., Schroder J.M., Weis J., Reimann H., Albrecht B., Nurnberg P., Thiele H., Muller C.R., et al. Limb girdle muscular dystrophy in a sibling pair with a homozygous Ser606Leu mutation in the alternatively spliced IS2 region of calpain 3. Biol. Chem. 386 (2005) 61-67
102. Huebsch K.A., Kudryashova E., Wooley C.M., Sher R.B., Seburn K.L., Spencer M.J., and Cox G.A. Mdm muscular dystrophy: interactions with calpain 3 and a novel functional role for titin's N2A domain. Hum. Mol. Genet. 14 (2005) 2801-2811
103. Selcen D., and Engel A.G. Mutations in ZASP define a novel form of muscular dystrophy in humans. Ann. Neurol. 57 (2005) 269-276
104. Moreira E.S., Wiltshire T.J., Faulkner G., Nilforoushan A., Vainzof M., Suzuki O.T., Valle G., Reeves R., Zatz M., Passos-Bueno M.R., et al. Limb-girdle muscular dystrophy type 2G is caused by mutations in the gene encoding the sarcomeric protein telethonin. Nat. Genet. 24 (2000) 163-166
105. Udd B., Haravuori H., Kalimo H., Partanen J., Pulkkinen L., Paetau A., Peltonen L., and Somer H. Tibial muscular dystrophy-from clinical description to linkage on chromosome 2q31. Neuromuscul. Dis. 8 (1998) 327-332
106. Hackman P., Vihola A., Haravuori H., Marchand S., Sarparanta J., De Seze J., Labeit S., Witt C., Peltonen L., Richard I., et al. Tibial muscular dystrophy is a titinopathy caused by mutations in TTN, the gene encoding the giant skeletal-muscle protein titin. Am. J. Hum. Genet. 71 (2002) 492-500
107. Hauser M.A., Horrigan S.K., Salmikangas P., Torian U.M., Viles K.D., Dancel R., Tim R.W., Taivainen A., Bartoloni L., Gilchrist J.M., et al. Myotilin is mutated in limb girdle muscular dystrophy 1A. Hum. Mol. Genet. 9 (2000) 2141-2147
108. Beckmann J.S., Richard I., Broux O., Fougerousse F., Allamand V., Chiannilkulchai N., Lim L.E., Duclos F., Bourg N., Brenguier L., et al. Identification of muscle-specific calpain and beta-sarcoglycan genes in progressive autosomal recessive muscular dystrophies. Neuromuscul. Disord. 6 (1996) 455-462
109. Hoffman E.P., Brown Jr. R.H., and Kunkel L.M. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51 (1987) 919-928
110. Bönnemann C.G., Modi R., Noguchi S., Mizuno Y., Yoshida M., Gussoni E., McNally E.M., Duggan D.J., Angelini C., and Hoffman E.P. Beta-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nat. Genet. 11 (1995) 266-273 (published erratum appears in Nat Genet 1996 Jan;12(1):110)
111. Hack A.A., Ly C.T., Jiang F., Clendenin C.J., Sigrist K.S., Wollmann R.L., and McNally E.M. Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J. Cell Biol. 142 (1998) 1279-1287
112. Jung D., Leturcq F., Sunada Y., Duclos F., Tomé F.M., Moomaw C., Merlini L., Azibi K., Chaouch M., Slaughter C., et al. Absence of gamma-sarcoglycan (35 DAG) in autosomal recessive muscular dystrophy linked to chromosome 13q12. FEBS. Lett. 381 (1996) 15-20
113. Jung D., Duclos F., Apostol B., Straub V., Lee J.C., Allamand V., Venzke D.P., Sunada Y., Moomaw C.R., Leveille C.J., et al. Characterization of delta-sarcoglycan, a novel component of the oligomeric sarcoglycan complex involved in limb-girdle muscular dystrophy. J. Biol. Chem. 271 (1996) 32321-32329
114. McNally E.M., Duggan D., Gorospe J.R., Bönnemann C.G., Fanin M., Pegoraro E., Lidov H.G., Noguchi S., Ozawa E., Finkel R.S., et al. Mutations that disrupt the carboxyl-terminus of gamma-sarcoglycan cause muscular dystrophy. Hum. Mol. Genet. 5 (1996) 1841-1847
115. Fardeau M., Matsumura K., Tome F.M., Collin H., Leturcq F., Kaplan J.C., and Campbell K.P. Deficiency of the 50 kDa dystrophin associated glycoprotein (adhalin) in severe autosomal recessive muscular dystrophies in children native from European countries. C. R. Acad. Sci. III 316 (1993) 799-804
116. Sotgia F., Woodman S.E., Bonuccelli G., Capozza F., Minetti C., Scherer P.E., and Lisanti M.P. Phenotypic behavior of caveolin-3 R26Q, a mutant associated with hyperCKemia, distal myopathy, and rippling muscle disease. Am. J. Physiol.: Cell Physiol. 285 (2003) C1150-C1160
117. Ervasti J.M., and Campbell K.P. Membrane organization of the dystrophin-glycoprotein complex. Cell 66 (1991) 1121-1131
118. Bushby K. The limb-girdle muscular dystrophies-multiple genes, multiple mechanisms. Hum. Mol. Genet. 8 (1999) 1875-1882
119. McNally E.M., Duggan D., Gorospe J.R., Bonnemann C.G., Fanin M., Pegoraro E., Lidov H.G., Noguchi S., Ozawa E., Finkel R.S., et al. Mutations that disrupt the carboxyl-terminus of gamma-sarcoglycan cause muscular dystrophy. Hum. Mol. Genet. 5 (1996) 1841-1847
120. Fox J.E. Identification of actin-binding protein as the protein linking the membrane skeleton to glycoproteins on platelet plasma membranes. J. Biol. Chem. 260 (1985) 11970-11977
121. Tidball J.G., and Spencer M.J. Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J. Physiol. 545 (2002) 819-828
122. Solomon V., Lecker S.H., and Goldberg A.L. The N-end rule pathway catalyzes a major fraction of the protein degradation in skeletal muscle. J. Biol. Chem. 273 (1998) 25216-25222
123. Solomon V., and Goldberg A.L. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J. Biol. Chem. 271 (1996) 26690-26697
124. Jiang Y.H., and Beaudet A.L. Human disorders of ubiquitination and proteasomal degradation. Curr. Opin. Pediatr. 16 (2004) 419-426
125. Garcia-Mata R., Gao Y.S., and Sztul E. Hassles with taking out the garbage: aggravating aggresomes. Traffic 3 (2002) 388-396