FHL1 mutants that cause clinically distinct human myopathies form protein aggregates and impair myoblast differentiation

Journal of Cell Science

Volumn 127, Issue 10, 2014, Pages 2269-2281

  Wilding, Brendan R ^a   McGrath, Meagan J ^a   Bonne, Gisèle ^b,c,d   Mitchell, Christina A ^a  

^a MONASH UNIVERSITY   (Australia)

^b Sorbonne Université   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

FHL1; Myopathy; RBM; SPM; XMPMA

Indexed keywords

FOUR AND A HALF LIM DOMAIN PROTEIN 1; MUTANT PROTEIN; NUCLEIC ACID BINDING PROTEIN; UNCLASSIFIED DRUG; FHL1 PROTEIN, HUMAN; LIM PROTEIN; MUSCLE PROTEIN; PROTEIN AGGREGATE; SIGNAL PEPTIDE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELLULAR DISTRIBUTION; CLINICAL FEATURE; CONTROLLED STUDY; DELETION MUTANT; DISEASE SEVERITY; EMERY DREIFUSS MUSCULAR DYSTROPHY; HEREDITARY SPINAL MUSCULAR ATROPHY; HUMAN; HUMAN CELL; HYPERTROPHIC CARDIOMYOPATHY; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; MISSENSE MUTATION; MOUSE; MUSCLE ATROPHY; MYOBLAST; MYOPATHY; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SKELETAL MUSCLE; STOP CODON; VECTOR CONTROL; GENETICS; METABOLISM; MUSCLE DISEASE; MUTATION; PATHOLOGY; PHYSIOLOGY;

CELL DIFFERENTIATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIM DOMAIN PROTEINS; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCULAR DISEASES; MUTATION; MYOBLASTS; PROTEIN AGGREGATES;

EID: 84900796161     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.140905     Document Type: Article

References (57)

1. Allen, D. L., Roy, R. R. and Edgerton, V. R. (1999). Myonuclear domains in muscle adaptation and disease. Muscle Nerve 22, 1350-1360.
2. Bader, D., Masaki, T. and Fischman, D. A. (1982). Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 95, 763-770.
3. Brais, B., Bouchard, J. P., Xie, Y. G., Rochefort, D. L., Chrétien, N., Tomé, F. M., Lafrenière, R. G., Rommens, J. M., Uyama, E., Nohira, O. et al. (1998). Short GCG expansions in the PABP2 gene cause oculopharyngeal muscular dystrophy. Nat. Genet. 18, 164-167.
4. Brooke, M. H. and Neville, H. E. (1972). Reducing body myopathy. Neurology 22, 829-840.
5. Brown, S., Biben, C., Ooms, L. M., Maimone, M., McGrath, M. J., Gurung, R., Harvey, R. P. and Mitchell, C. A. (1999). The cardiac expression of striated muscle LIM protein 1 (SLIM1) is restricted to the outflow tract of the developing heart. J. Mol. Cell. Cardiol. 31, 837-843.
6. Chen, D. H., Raskind, W. H., Parson, W. W., Sonnen, J. A., Vu, T., Zheng, Y., Matsushita, M., Wolff, J., Lipe, H. and Bird, T. D. (2010). A novel mutation in FHL1 in a family with X-linked scapuloperoneal myopathy: phenotypic spectrum and structural study of FHL1 mutations. J. Neurol. Sci. 296, 22-29.
7. Chu, P. H., Ruiz-Lozano, P., Zhou, Q., Cai, C. and Chen, J. (2000). Expression patterns of FHL/SLIM family members suggest important functional roles in skeletal muscle and cardiovascular system. Mech. Dev. 95, 259-265.
8. Cowling, B. S., McGrath, M. J., Nguyen, M. A., Cottle, D. L., Kee, A. J., Brown, S., Schessl, J., Zou, Y., Joya, J., Bönnemann, C. G. et al. (2008). Identification of FHL1 as a regulator of skeletal muscle mass: implications for human myopathy. J. Cell Biol. 183, 1033-1048.
9. Cowling, B. S., Cottle, D. L., Wilding, B. R., D'Arcy, C. E., Mitchell, C. A. and McGrath, M. J. (2011). Four and a half LIM protein 1 gene mutations cause four distinct human myopathies: a comprehensive review of the clinical, histological and pathological features. Neuromuscul. Disord. 21, 237-251.
10. Dalakas, M. C. (2006). Sporadic inclusion body myositis - diagnosis, pathogenesis and therapeutic strategies. Nat. Clin. Pract. Neurol. 2, 437-447.
11. de Luna, N., Gallardo, E., Soriano, M., Dominguez-Perles, R., de la Torre, C., Rojas-García, R., Garclá-Verdugo, J. M. and Illa, I. (2006). Absence of dysferlin alters myogenin expression and delays human muscle differentiation "in vitro". J. Biol. Chem. 281, 17092-17098.
12. Domenighetti, A. A., Chu, P. H., Wu, T., Sheikh, F., Gokhin, D. S., Guo, L. T., Cui, Z., Peter, A. K., Christodoulou, D. C., Parfenov, M. G. et al. (2014). Loss of FHL1 induces an age-dependent skeletal muscle myopathy associated with myofibrillar and intermyofibrillar disorganization in mice. Hum. Mol. Genet. 23, 209-225.
13. Feldkirchner, S., Walter, M. C., Kubny, C., Mueller, S., Kress, W., Hanisch, F. G., Schoser, B. and Schessl, J. (2011). P5.53 The C224W FHL1 mutation is causing a protein aggregation disorder of muscle: Two brothers revisited. Neuromuscul. Disord. 21, 740.
14. Feldkirchner, S., Walter, M. C., Müller, S., Kubny, C., Krause, S., Kress, W., Hanisch, F. G., Schoser, B. and Schessl, J. (2013). Proteomic characterization of aggregate components in an intrafamilial variable FHL1-associated myopathy. by a novel mutation in four-and-a-half LIM domain 1 gene (FHL1). Neuromuscul. Disord. 23, 418-426.
15. Friedrich, F. W., Wilding, B. R., Reischmann, S., Crocini, C., Lang, P., Charron, P., Müller, O. J., McGrath, M. J., Vollert, I., Hansen, A. et al. (2012). Evidence for FHL1 as a novel disease gene for isolated hypertrophic cardiomyopathy. Hum. Mol. Genet. 21, 3237-3254.
16. Greene, W. K., Baker, E., Rabbitts, T. H. and Kees, U. R. (1999). Genomic structure, tissue expression and chromosomal location of the LIM-only gene, SLIM1. Gene 232, 203-207.
17. Gueneau, L., Bertrand, A. T., Jais, J. P., Salih, M. A., Stojkovic, T., Wehnert, M., Hoeltzenbein, M., Spuler, S., Saitoh, S., Verschueren, A. et al. (2009). Mutations of the FHL1 gene cause Emery-Dreifuss muscular dystrophy. Am. J. Hum. Genet. 85, 338-353.
18. Knoblauch, H., Geier, C., Adams, S., Budde, B., Rudolph, A., Zacharias, U., Schulz-Menger, J., Spuler, A., Yaou, R. B., Nürnberg, P. et al. (2010). Contractures and hypertrophic cardiomyopathy in a novel FHL1 mutation. Ann. Neurol. 67, 136-140.
19. Kopito, R. R. (2000). Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524-530.
20. Kudo, L. C., Karsten, S. L., Chen, J., Levitt, P. and Geschwind, D. H. (2007). Genetic analysis of anterior posterior expression gradients in the developing mammalian forebrain. Cereb. Cortex 17, 2108-2122.
21. Lee, S. M., Tsui, S. K., Chan, K. K., Garcia-Barcelo, M., Waye, M. M., Fung, K. P., Liew, C. C. and Lee, C. Y. (1998). Chromosomal mapping, tissue distribution and cDNA sequence of four-and-a-half LIM domain protein 1 (FHL1). Gene 216, 163-170.
22. Lee, J. Y., Chien, I. C., Lin, W. Y., Wu, S. M., Wei, B. H., Lee, Y. E. and Lee, H. H. (2012). Fhl1 as a downstream target of Wnt signaling to promote myogenesis of C2C12 cells. Mol. Cell. Biochem. 365, 251-262.
23. Liewluck, T., Hayashi, Y. K., Ohsawa, M., Kurokawa, R., Fujita, M., Noguchi, S., Nonaka, I. and Nishino, I. (2007). Unfolded protein response and aggresome formation in hereditary reducing-body myopathy. Muscle Nerve 35, 322-326.
24. Liu, Y., Cseresnyés, Z., Randall, W. R. and Schneider, M. F. (2001). Activity- dependent nuclear translocation and intranuclear distribution of NFATc in adult skeletal muscle fibers. J. Cell Biol. 155, 27-40.
25. Loughna, P. T., Mason, P., Bayol, S. and Brownson, C. (2000). The LIM-domain protein FHL1 (SLIM 1) exhibits functional regulation in skeletal muscle. Mol. Cell Biol. Res. Commun. 3, 136-140.
26. McGrath, M. J., Mitchell, C. A., Coghill, I. D., Robinson, P. A. and Brown, S. (2003). Skeletal muscle LIM protein 1 (SLIM1/FHL1) induces alpha 5 beta 1- integrin-dependent myocyte elongation. Am.J.Physiol.285, C1513-C1526.
27. McGrath, M. J., Cottle, D. L., Nguyen, M. A., Dyson, J. M., Coghill, I. D., Robinson, P. A., Holdsworth, M., Cowling, B. S., Hardeman, E. C., Mitchell, C. A. et al. (2006). Four and a half LIM protein 1 binds myosin-binding protein C and regulates myosin filament formation and sarcomere assembly. J. Biol. Chem. 281, 7666-7683.
28. Merrick, D., Stadler, L. K., Larner, D. and Smith, J. (2009). Muscular dystrophy begins early in embryonic development deriving from stem cell loss and disrupted skeletal muscle formation. Dis. Model. Mech. 2, 374-388.
29. Monticelli, S. and Rao, A. (2002). NFAT1 and NFAT2 are positive regulators of IL- 4 gene transcription. Eur. J. Immunol. 32, 2971-2978.
30. Moreno, J. A., Radford, H., Peretti, D., Steinert, J. R., Verity, N., Martin, M. G., Halliday, M., Morgan, J., Dinsdale, D., Ortori, C. A. et al. (2012). Sustained translational repression by eIF2a-P mediates prion neurodegeneration. Nature 485, 507-511.
31. Morgan, M. J. and Madgwick, A. J. (1999). The LIM proteins FHL1 and FHL3 are expressed differently in skeletal muscle. Biochem. Biophys. Res. Commun. 255, 245-250.
32. Oh, S. J., Meyers, G. J., Wilson, E. R., Jr and Alexander, C. B. (1983). A benign form of reducing body myopathy. Muscle Nerve 6, 278-282.
33. Pavlath, G. K. and Horsley, V. (2003). Cell fusion in skeletal muscle-central role of NFATC2 in regulating muscle cell size. Cell Cycle 2, 419-422.
34. Quinzii, C. M., Vu, T. H., Min, K. C., Tanji, K., Barral, S., Grewal, R. P., Kattah, A., Camaño, P., Otaegui, D., Kunimatsu, T. et al. (2008). X-linked dominant scapuloperoneal myopathy is due to a mutation in the gene encoding four-and- a-half-LIM protein 1. Am. J. Hum. Genet. 82, 208-213.
35. Ross, C. A. and Poirier, M. A. (2004). Protein aggregation and neurodegenerative disease. Nat. Med. 10 Suppl., S10-S17.
36. Schessl, J., Zou, Y., McGrath, M. J., Cowling, B. S., Maiti, B., Chin, S. S., Sewry, C., Battini, R., Hu, Y., Cottle, D. L. et al. (2008). Proteomic identification of FHL1 as the protein mutated in human reducing body myopathy. J. Clin. Invest. 118, 904-912.
37. Schessl, J., Taratuto, A. L., Sewry, C., Battini, R., Chin, S. S., Maiti, B., Dubrovsky, A. L., Erro, M. G., Espada, G., Robertella, M. et al. (2009). Clinical, histological and genetic characterization of reducing body myopathy caused by mutations in FHL1. Brain 132, 452-464.
38. Schessl, J., Columbus, A., Hu, Y., Zou, Y., Voit, T., Goebel, H. H. and Bönnemann, C. G. (2010). Familial reducing body myopathy with cytoplasmic bodies and rigid spine revisited: identification of a second LIM domain mutation in FHL1. Neuropediatrics 41, 43-46.
39. Schmeichel, K. L. and Beckerle, M. C. (1997). Molecular dissection of a LIM domain. Mol. Biol. Cell 8, 219-230.
40. Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675.
41. Schoser, B., Goebel, H. H., Janisch, I., Quasthoff, S., Rother, J., Bergmann, M., Müller-Felber, W. and Windpassinger, C. (2009). Consequences of mutations within the C terminus of the FHL1 gene. Neurology 73, 543-551.
42. Schreckenbach, T., Henn, W., Kress, W., Roos, A., Maschke, M., Feiden, W., Dillmann, U., Schulz, J. B., Weis, J. and Claeys, K. G. (2013). Novel FHL1 mutation in a family with reducing body myopathy. Muscle Nerve 47, 127-134.
43. Schröder, R. and Schoser, B. (2009). Myofibrillar myopathies: a clinical and myopathological guide. Brain Pathol. 19, 483-492.
44. Selcen, D., Bromberg, M. B., Chin, S. S. and Engel, A. G. (2011). Reducing bodies and myofibrillar myopathy features in FHL1 muscular dystrophy. Neurology 77, 1951-1959.
45. Semsarian, C., Wu, M. J., Ju, Y. K., Marciniec, T., Yeoh, T., Allen, D. G., Harvey, R. P. and Graham, R. M. (1999). Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway. Nature 400, 576-581.
46. Shalaby, S., Hayashi, Y. K., Goto, K., Ogawa, M., Nonaka, I., Noguchi, S. and Nishino, I. (2008). Rigid spine syndrome caused by a novel mutation in four- and-a-half LIM domain 1 gene (FHL1). Neuromuscul. Disord. 18, 959-961.
47. Shalaby, S., Hayashi, Y. K., Nonaka, I., Noguchi, S. and Nishino, I. (2009). Novel FHL1 mutations in fatal and benign reducing body myopathy. Neurology 72, 375-376.
48. Sheikh, F., Raskin, A., Chu, P. H., Lange, S., Domenighetti, A. A., Zheng, M., Liang, X., Zhang, T., Yajima, T., Gu, Y. et al. (2008). An FHL1-containing complex within the cardiomyocyte sarcomere mediates hypertrophic biomechanical stress responses in mice. J. Clin. Invest. 118, 3870-3880.
49. Stefani, M. and Dobson, C. M. (2003). Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J Mol Med (Berl) 81, 678-699.
50. Tanaka, M., Kim, Y. M., Lee, G., Junn, E., Iwatsubo, T. and Mouradian, M. M. (2004). Aggresomes formed by alpha-synuclein and synphilin-1 are cytoprotective. J. Biol. Chem. 279, 4625-4631.
51. Taylor, J. P., Tanaka, F., Robitschek, J., Sandoval, C. M., Taye, A., Markovic-Plese, S. and Fischbeck, K. H. (2003). Aggresomes protect cells by enhancing the degradation of toxic polyglutamine-containing protein. Hum. Mol. Genet. 12, 749-757.
52. Thomas, M., Yu, Z., Dadgar, N., Varambally, S., Yu, J., Chinnaiyan, A. M. and Lieberman, A. P. (2005). The unfolded protein response modulates toxicity of the expanded glutamine androgen receptor. J. Biol. Chem. 280, 21264-21271.
53. Tomé, F. M. and Fardeau, M. (1975). Congenital myopathy with "reducing bodies" in muscle fibres. Acta Neuropathol. 31, 207-217.
54. van Bebber, F., Paquet, D., Hruscha, A., Schmid, B. and Haass, C. (2010). Methylene blue fails to inhibit Tau and polyglutamine protein dependent toxicity in zebrafish. Neurobiol. Dis. 39, 265-271.
55. Vesa, J., Su, H., Watts, G. D., Krause, S., Walter, M. C., Martin, B., Smith, C., Wallace, D. C. and Kimonis, V. E. (2009). Valosin containing protein associated inclusion body myopathy: abnormal vacuolization, autophagy and cell fusion in myoblasts. Neuromuscul. Disord. 19, 766-772.
56. Wang, S. and Kaufman, R. J. (2012). The impact of the unfolded protein response on human disease. J. Cell Biol. 197, 857-867.
57. Windpassinger, C., Schoser, B., Straub, V., Hochmeister, S., Noor, A., Lohberger, B., Farra, N., Petek, E., Schwarzbraun, T., Ofner, L. et al. (2008). An X-linked myopathy with postural muscle atrophy and generalized hypertrophy, termed XMPMA, is caused by mutations in FHL1. Am. J. Hum. Genet. 82, 88-99.