Myofibrillar instability exacerbated by acute exercise in filaminopathy

Human Molecular Genetics

Volumn 24, Issue 25, 2015, Pages 7207-7220

  Chevessier, Frédéric ^a   Schuld, Julia ^b   Orfanos, Zacharias ^b   Plank, Anne C ^a   Wolf, Lucie ^a   Maerkens, Alexandra ^c,d   Unger, Andreas ^d   Schlötzer Schrehardt, Ursula ^a   Kley, Rudolf A ^c   Von Hörsten, Stephan ^a   Marcus, Katrin ^d   Linke, Wolfgang A ^d   Vorgerd, Matthias ^c   Van der Ven, Peter F M ^b   Fürst, Dieter O ^b   Schröder, Rolf ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FILAMIN; PROTEIN AGGREGATE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOPSY; CONTROLLED STUDY; DISEASE EXACERBATION; EXERCISE; GENE MUTATION; HUMAN; HUMAN TISSUE; MORPHOLOGY; MUSCLE DISEASE; MUSCLE WEAKNESS; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ELECTRON MICROSCOPY; GENETICS; GENOTYPE; MOUSE; MUSCLE FIBRIL; MUSCULAR DYSTROPHY; PATHOLOGY; PHENOTYPE; SKELETAL MUSCLE;

ANIMALS; FILAMINS; GENOTYPE; MICE; MICROSCOPY, ELECTRON; MUSCLE, SKELETAL; MUSCULAR DISEASES; MUSCULAR DYSTROPHIES; MYOFIBRILS; PHENOTYPE;

EID: 84959226839     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv421     Document Type: Article

References (61)

1. Schröder, R. and Schoser, B. (2009) Myofibrillar myopathies: a clinical and myopathological guide. Brain Pathol., 19, 483-492.
2. Selcen, D. (2011) Myofibrillar myopathies. Neuromuscul. Disord., 21, 161-171.
3. Feng, Y. and Walsh, C.A. (2004) The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nat. Cell Biol., 6, 1034-1038.
4. Popowicz, G.M., Schleicher, M., Noegel, A.A. and Holak, T.A. (2006) Filamins: promiscuous organizers of the cytoskeleton. Trends Biochem. Sci., 31, 411-419.
5. Stossel, T.P., Condeelis, J., Cooley, L., Hartwig, J.H., Noegel, A., Schleicher, M. and Shapiro, S.S. (2001) Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol., 2, 138-145.
6. van der Flier, A. and Sonnenberg, A. (2001) Structural and functional aspects of filamins. Biochim. Biophys. Acta, 1538, 99-117.
7. Robertson, S.P. (2005) Filamin A: phenotypic diversity. Curr. Opin. Genet. Dev., 15, 301-307.
8. Farrington-Rock, C., Firestein, M.H., Bicknell, L.S., Superti-Furga, A., Bacino, C.A., Cormier-Daire, V., Le Merrer, M., Baumann, C., Roume, J., Rump, P. et al. (2006) Mutations in two regions of FLNB result in atelosteogenesis I and III. Hum. Mutat., 27, 705-710.
9. Bicknell, L.S., Farrington-Rock, C., Shafeghati, Y., Rump, P., Alanay, Y., Alembik, Y., Al-Madani, N., Firth, H., Karimi-Nejad, M.H., Kim, C.A. et al. (2007) A molecular and clinical study of Larsen syndrome caused by mutations in FLNB. J. Med. Genet., 44, 89-98.
10. Vorgerd, M., van der Ven, P.F.M., Bruchertseifer, V., Löwe, T., Kley, R.A., Schröder, R., Lochmüller, H., Himmel, M., Koehler, K., Fürst, D.O. et al. (2005) A mutation in the dimerization domain of filamin c causes a novel type of autosomal dominant myofibrillar myopathy. Am. J. Hum. Genet., 77, 297-304.
11. Fürst, D.O., Goldfarb, L.G., Kley, R.A., Vorgerd, M., Olivé, M. and van der Ven, P.F.M. (2013) Filamin C-related myopathies: pathology and mechanisms. Acta Neuropathol., 125, 33-46.
12. Shatunov, A., Olivé, M., Odgerel, Z., Stadelmann-Nessler, C., Irlbacher, K., van Landeghem, F., Bayarsaikhan, M., Lee, H.S., Goudeau, B., Chinnery, P.F. et al. (2009) In-frame deletion in the seventh immunoglobulin-like repeat of filamin C in a family with myofibrillar myopathy. Eur. J. Hum. Genet., 17, 656-663.
13. Kley, R.A., Hellenbroich, Y., van der Ven, P.F.M., Fürst, D.O., Huebner, A., Bruchertseifer, V., Peters, S.A., Heyer, C.M., Kirschner, J., Schröder, R. et al. (2007) Clinical and morphological phenotype of the filamin myopathy: a study of 31 German patients. Brain, 130, 3250-3264.
14. Guergueltcheva, V., Peeters, K., Baets, J., Ceuterick-de Groote, C., Martin, J.J., Suls, A., de Vriendt, E., Mihaylova, V., Chamova, T., Almeida-Souza, L. et al. (2011) Distal myopathy with upper limb predominance caused by filamin C haploinsufficiency. Neurology, 77, 2105-2114.
15. Duff, R.M., Tay, V., Hackman, P., Ravenscroft, G., McLean, C., Kennedy, P., Steinbach, A., Schöffler, W., van der Ven, P.F.M., Fürst, D.O. et al. (2011) Mutations in the N-terminal actinbinding domain of filamin C cause a distal myopathy. Am. J. Hum. Genet., 88, 729-740.
16. Valdés-Mas, R., Gutiérrez-Fernández, A., Gómez, J., Coto, E., Astudillo, A., Puente, D.A., Reguero, J.R., Alvarez, V., Morís, C., León, D. et al. (2014) Mutations in filamin C cause a new form of familial hypertrophic cardiomyopathy. Nat. Commun., 5, 5326.
17. Kley, R.A., Serdaroglu-Oflazer, P., Leber, Y., Odgerel, Z., van der Ven, P.F.M., Olive, M., Ferrer, I., Onipe, A., Mihaylov, M., Bilbao, J.M. et al. (2012) Pathophysiology of protein aggregation and extended phenotyping in filaminopathy. Brain, 135, 2642-2660.
18. Löwe, T., Kley, R.A., van der Ven, P.F.M., Himmel, M., Huebner, A., Vorgerd, M. and Fürst, D.O. (2007) The pathomechanism of filaminopathy: altered biochemical properties explain the cellular phenotype of a protein aggregation myopathy. Hum. Mol. Genet., 16, 1351-1358.
19. Fridén, J., Sjöström, M. and Ekblom, B. (1981) A morphological study of delayed muscle soreness. Experientia, 37, 506-507.
20. Newham, D.J., McPhail, G., Mills, K.R. and Edwards, R.H. (1983) Ultrastructural changes after concentric and eccentric contractions of human muscle. J. Neurol. Sci., 61, 109-122.
21. Agbulut, O., Destombes, J., Thiesson, D. and Butler-Browne, G. (2000) Age-related appearance of tubular aggregates in the skeletal muscle of almost all male inbred mice. Histochem. Cell Biol., 114, 477-481.
22. Chevessier, F., Marty, I., Paturneau-Jouas, M., Hantaï, D. and Verdière-Sahuqué, M. (2004) Tubular aggregates are from whole sarcoplasmic reticulum origin: alterations in calcium binding protein expression in mouse skeletal muscle during aging. Neuromuscul. Disord., 14, 208-216.
23. Yu, J.G., Fürst, D.O. and Thornell, L.E. (2003) The mode ofmyofibril remodelling in human skeletal muscle affected by DOMS induced by eccentric contractions. Histochem. Cell Biol., 119, 383-393.
24. Kley, R.A., Maerkens, A., Leber, Y., Theis, V., Schreiner, A., van der Ven, P.F.M., Uszkoreit, J., Stephan, C., Eulitz, S., Euler, N. et al. (2013) A combined laser microdissection and mass spectrometry approach reveals new disease relevant proteins accumulating in aggregates of filaminopathy patients. Mol. Cell Proteomics, 12, 215-227.
25. Luan, X., Hong, D., Zhang, W., Wang, Z. and Yuan, Y. (2010) A novel heterozygous deletion-insertion mutation (2695-2712 del/GTTTGT ins) in exon 18 of the filamin C gene causes filaminopathy in a large Chinese family. Neuromuscul. Disord., 20, 390-396.
26. Dalkilic, I., Schienda, J., Thompson, T.G. and Kunkel, L.M. (2006) Loss of FilaminC (FLNc) results in severe defects in myogenesis and myotube structure. Mol. Cell Biol., 26, 6522-6534.
27. Fujita, M., Mitsuhashi, H., Isogai, S., Nakata, T., Kawakami, A., Nonaka, I., Noguchi, S., Hayashi, Y.K., Nishino, I. and Kudo, A. (2012) Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro. Dev. Biol., 361, 79-89.
28. Ruparelia, A.A., Zhao, M., Currie, P.D. and Bryson-Richardson, R.J. (2012) Characterization and investigation of zebrafish models of filamin-related myofibrillar myopathy. Hum. Mol. Genet., 21, 4073-4083.
29. Yu, J.G., Carlsson, L. and Thornell, L.E. (2004) Evidence for myofibril remodeling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem. Cell Biol., 121, 219-227.
30. Carlsson, L., Yu, J.G., Moza, M., Carpén, O. and Thornell, L.E. (2007) Myotilin-a prominent marker of myofibrillar remodelling. Neuromuscul. Disord., 17, 61-68.
31. Fridén, J., Sjöström, M. and Ekblom, B. (1983) Myofibrillar damage following intense eccentric exercise in man. Int. J. Sports Med., 4, 170-176.
32. Yu, J.G. and Thornell, L.E. (2002) Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study. Histochem. Cell Biol., 118, 171-179.
33. Eulitz, S., Sauer, F., Pelissier, M.C., Boisguerin, P., Molt, S., Schuld, J., Orfanos, Z., Kley, R.A., Volkmer, R., Wilmanns, M. et al. (2013) Identification of Xin-repeat proteins as novel ligands of the SH3 domains of nebulin and nebulette and analysis of their interaction during myofibril formation and remodeling. Mol. Biol. Cell, 24, 3215-3226.
34. Molt, S., Bührdel, J.B., Yakovlev, S., Schein, P., Orfanos, Z., Kirfel, G., Winter, L., Wiche, G., van der Ven, P.F.M., Rottbauer, W. et al. (2014) Aciculin interacts with filamin C and Xin and is essential for myofibril assembly, remodeling and maintenance. J. Cell Sci., 127, 3578-3592.
35. Meltzer, H.Y., Kuncl, R.W. and Yang, V. (1976) Incidence of Z band streaming and myofibrillar disruptions in skeletal muscle from healthy young people. Neurology, 26, 853-857.
36. Armstrong, R.B., Ogilvie, R.W. and Schwane, J.A. (1983) Eccentric exercise-induced injury to rat skeletal muscle. J. Appl. Physiol. Respir. Environ. Exerc. Physiol., 54, 80-93.
37. Gibala, M.J., MacDougall, J.D., Tarnopolsky, M.A., Stauber, W.T. and Elorriaga, A. (1995) Changes in human skeletal muscle ultrastructure and force production after acute resistance exercise. J. Appl. Physiol. (1985), 78, 702-708.
38. Ogilvie, R.W., Armstrong, R.B., Baird, K.E. and Bottoms, C.L. (1988) Lesions in the rat soleus muscle following eccentrically biased exercise. Am. J. Anat., 182, 335-346.
39. Fridén, J. (1984) Muscle soreness after exercise: implications of morphological changes. Int. J. Sports Med., 5, 57-66.
40. Claeys, K.G., van der Ven, P.F.M., Behin, A., Stojkovic, T., Eymard, B., Dubourg, O., Laforêt, P., Faulkner, G., Richard, P., Vicart, P. et al. (2009) Differential involvement of sarcomeric proteins in myofibrillarmyopathies: a morphological and immunohistochemical study. Acta Neuropathol., 117, 293-307.
41. Olivé, M., Odgerel, Z., Martínez, A., Poza, J.J., Bragado, F.G., Zabalza, R.J., Jericó, I., Gonzalez-Mera, L., Shatunov, A., Lee, H.S. et al. (2011) Clinical and myopathological evaluation of earlyand late-onset subtypes of myofibrillar myopathy. Neuromuscul. Disord., 21, 533-542.
42. Proske, U. and Morgan, D.L. (2001) Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J. Physiol., 537, 333-345.
43. Thompson, J.L., Balog, E.M., Fitts, R.H. and Riley, D.A. (1999) Five myofibrillar lesion types in eccentrically challenged, unloaded rat adductor longus muscle-a test model. Anat. Rec., 254, 39-52.
44. Arndt, V., Dick, N., Tawo, R., Dreiseidler, M., Wenzel, D., Hesse, M., Fürst, D.O., Saftig, P., Saint, R., Fleischmann, B.K. et al. (2010) Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr. Biol., 20, 143-148.
45. Ulbricht, A., Eppler, F.J., Tapia, V.E., van der Ven, P.F.M., Hampe, N., Hersch, N., Vakeel, P., Stadel, D., Haas, A., Saftig, P. et al. (2013) Cellular mechanotransduction relies on tension-induced and chaperone-assisted autophagy. Curr. Biol., 23, 430-435.
46. Cuervo, A.M., Bergamini, E., Brunk, U.T., Dröge, W., Ffrench, M. and Terman, A. (2005) Autophagy and aging: the importance of maintaining clean" cells. Autophagy, 1, 131-140.
47. Martinez-Vicente, M., Sovak, G. and Cuervo, A.M. (2005) Protein degradation and aging. Exp. Gerontol., 40, 622-633.
48. van der Ven, P.F.M., Wiesner, S., Salmikangas, P., Auerbach, D., Himmel, M., Kempa, S., Hayeß, K., Pacholsky, D., Taivainen, A., Schröder, R. et al. (2000) Indications for a novel muscular dystrophy pathway. γ-filamin, the musclespecific filamin isoform, interacts with myotilin. J. Cell Biol., 151, 235-248.
49. Faulkner, G., Pallavicini, A., Comelli, A., Salamon, M., Bortoletto, G., Ievolella, C., Trevisan, S., Kojic, S., Dalla, V.F., Laveder, P. et al. (2000) FATZ: a filamin-, actinin-, and telethoninbinding protein of the Z-disk of skeletal muscle. J. Biol. Chem., 275, 41234-41242.
50. Takada, F., Vander Woude, D.L., Tong, H.Q., Thompson, T.G., Watkins, S.C., Kunkel, L.M. and Beggs, A.H. (2001) Myozenin: an α-actinin-and γ-filamin-binding protein of skeletal muscle Z lines. Proc. Natl. Acad. Sci. USA., 98, 1595-1600.
51. Frey, N. and Olson, E.N. (2002) Calsarcin-3, a novel skeletal muscle-specific member of the calsarcin family, interacts with multiple Z-disc proteins. J. Biol. Chem., 277, 13998-14004.
52. Gontier, Y., Taivainen, A., Fontao, L., Sonnenberg, A., van der Flier, A., Carpén, O., Faulkner, G. and Borradori, L. (2005) The Z-disc proteins myotilin and FATZ-1 interact with each other and are connected to the sarcolemma via muscle-specific filamins. J. Cell Sci., 118, 3739-3749.
53. Linnemann, A., van der Ven, P.F.M., Vakeel, P., Albinus, B., Simonis, D., Bendas, G., Schenk, J.A., Micheel, B., Kley, R.A. and Fürst, D.O. (2010) The sarcomeric Z-disc component myopodin is a multiadapter protein that interacts with filamin and α-actinin. Eur. J. Cell Biol., 89, 681-692.
54. 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. (2000) Filamin 2 (FLN2). A muscle-specific sarcoglycan interacting protein. J. Cell. Biol., 148, 115-126.
55. Himmel, M., van der Ven, P.F.M., Stöcklein, W. and Fürst, D.O. (2003) The limits of promiscuity: isoform-specific dimerization of filamins. Biochemistry, 42, 430-439.
56. Zhang, M., Liu, J., Cheng, A., Deyoung, S.M. and Saltiel, A.R. (2007) Identification of CAP as a costameric protein that interacts with filamin C. Mol. Biol. Cell, 18, 4731-4740.
57. Maiweilidan, Y., Klauza, I. and Kordeli, E. (2011) Novel interactions of ankyrins-G at the costameres: the muscle-specific obscurin/titin-binding-related domain (OTBD) binds plectin and filamin C. Exp. Cell Res., 317, 724-736.
58. Clemen, C.S., Stöckigt, F., Strucksberg, K.-H., Chevessier, F., Winter, L., Schütz, J., Bauer, R., Thorweihe, J.-M., Wenzel, D., Schlötzer-Schrehardt, U. et al. (2015) The toxic effect of R350P mutant desmin in striated muscle of man and mouse. Acta Neuropathol., 129, 297-315.
59. Alexandru, A., Jagla, W., Graubner, S., Becker, A., Bäuscher, C., Kohlmann, S., Sedlmeier, R., Raber, K.A., Cynis, H., Rönicke, R. et al. (2011) Selective hippocampal neurodegeneration in transgenic mice expressing small amounts of truncated Aβ is induced by pyroglutamate-Aβ formation. J. Neurosci., 31, 12790-12801.
60. Urbach, Y.K., Raber, K.A., Canneva, F., Plank, A.-C., Andreasson, T., Ponten, H., Kullingsjö, J., Nguyen, H.P., Riess, O. and von Hörsten, S. (2014) Automated phenotyping and advanced data mining exemplified in rats transgenic for Huntington's disease. J. Neurosci. Methods, 234, 38-53.
61. Engel, W.K. and Cunningham, G.G. (1963) Rapid examination of muscle tissue. An improved trichrome method for freshfrozen biopsy sections. Neurology, 13, 919-923.