Identification of FHL1 as a therapeutic target for duchenne muscular dystrophy deficits

Human Molecular Genetics

Volumn 23, Issue 3, 2014, Pages 618-636

  D'Arcy, Colleen E ^a   Feeney, Sandra J ^a   McLean, Catriona A ^b,c   Gehrig, Stefan M ^d   Lynch, Gordon S ^d   Smith, Jaclyn E ^a   Cowling, Belinda S ^e   Mitchell, Christina A ^a   McGrath, Meagan J ^a  

^a MONASH UNIVERSITY   (Australia)

^b ALFRED HOSPITAL   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FOUR AND A HALF LIM DOMAIN PROTEIN 1; GLYCOPROTEIN; LIM PROTEIN; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR NFATC1; UNCLASSIFIED DRUG; UTROPHIN;

ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DIAPHRAGM DISEASE; DUCHENNE MUSCULAR DYSTROPHY; MOUSE; MUSCLE ATROPHY; MUSCLE CONTRACTION; MUSCLE INJURY; MYOFIBROSIS; MYOSITIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INDUCTION; SARCOLEMMA; SIGNAL TRANSDUCTION; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALS; DIAPHRAGM; DYSTROPHIN; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIM DOMAIN PROTEINS; MICE; MICE, INBRED MDX; MICE, TRANSGENIC; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; NFATC TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; SARCOLEMMA; SIGNAL TRANSDUCTION; UTROPHIN;

EID: 84892454097     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt449     Document Type: Article

References (61)

1. Menezes, M.P. and North, K.N. (2011) Inherited neuromuscular disorders: pathway to diagnosis. J. Paediatr. Child Health, 48, 458-465.
2. Malik, V., Rodino-Klapac, L.R. and Mendell, J.R. (2012) Emerging drugs for Duchenne muscular dystrophy. Expert. Opin. Emerg. Drugs, 17, 261-277.
3. Hoffman, E.P., Brown, R.H. Jr. and Kunkel, L.M. (1987) Dystrophin: the protein product of the duchenne muscular dystrophy locus. Cell, 51, 919-928.
4. Lapidos, K.A., Kakkar, R. and McNally, E.M. (2004) The dystrophin glycoprotein complex. Circ. Res., 94, 1023-1031.
5. Deconinck, N. and Dan, B. (2007) Pathophysiology of Duchenne muscular dystrophy: current hypotheses. Pediatr. Neurol., 36, 1-7.
6. Miura, P. and Jasmin, B.J. (2006) Utrophin upregulation for treating Duchenne or Becker muscular dystrophy: how close are we?. Trends Mol. Med., 12, 122-129.
7. Blake, D.J., Weir, A., Newey, S.E. and Davies, K.E. (2002) Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev., 82, 291-329.
8. Tinsley, J.M., Potter, A.C., Phelps, S.R., Fisher, R., Trickett, J.I. and Davies, K.E. (1996) Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature, 384, 349-353.
9. Tinsley, J., Deconinck, N., Fisher, R., Kahn, D., Phelps, S., Gillis, J.M. and Davies, K.E. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med., 4, 1441-1444.
10. Cerletti, M., Negri, T., Cozzi, F., Colpo, R. Andreetta, F., Croci, D., Davies, K.E., Cornelio, F., Pozza, O., Karpati, G. et al. (2003) Dystrophic phenotype of canine X-linked muscular dystrophy is mitigated by adenovirus-mediated utrophin gene transfer. Gene Ther., 10, 750-757.
11. Khurana, T.S., Watkins, S.C., Chafey, P., Chelly, J., Tome, F.M.S., Fardeau, M., Kaplan, J.-C. and Kunkel, L.M. (1991) Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromuscul. Disord., 1, 185-194.
12. Olson, E.N. and Williams, R.S. (2000) Remodeling muscles with calcineurin. Bioessays, 22, 510-519.
13. Chakkalakal, J.V., Stocksley, M.A., Harrison, M.A., Angus, L.M., Deschenes-Furry, J., St-Pierre, S., Megeney, L.A., Chin, E.R., Michel, R.N. and Jasmin, B.J. (2003) Expression of utrophinAmRNAcorrelates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc. Natl Acad. Sci. USA, 100, 7791-7796.
14. Stupka, N., Schertzer, J.D., Bassel-Duby, R., Olson, E.N. and Lynch, G.S. (2008) Stimulation of calcineurin A{alpha} activity attenuates muscle pathophysiology in mdx dystrophic mice. Am. J. Physiol. Regul. Integr. Comp. Physiol., 294, R983-R992.
15. Chakkalakal, J.V., Harrison, M.A., Carbonetto, S., Chin, E., Michel, R.N. and Jasmin, B.J. (2004) Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice. Hum. Mol. Genet., 13, 379-388.
16. Stupka, N., Plant, D.R., Schertzer, J.D., Emerson, T.M., Bassel-Duby, R., Olson, E.N. and Lynch, G.S. (2006) Activated calcineurin ameliorates contraction-induced injury to skeletal muscles of mdx dystrophic mice. J. Physiol., 575, 645-656.
17. Chakkalakal, J.V., Michel, S.A., Chin, E.R., Michel, R.N. and Jasmin, B.J. (2006) Targeted inhibition of Ca2+ /calmodulin signaling exacerbates the dystrophic phenotype in mdx mouse muscle. Hum. Mol. Genet., 15, 1423-1435.
18. Chin, E.R., Olson, E.N., Richardson, J.A., Yang, Q., Humphries, C., Shelton, J.M., Wu, H., Zhu, W., Bassel-Duby, R. and Williams, R.S. (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev., 12, 2499-2509.
19. Serrano, A.L., Murgia, M., Pallafacchina, G., Calabria, E., Coniglio, P., Lomo, T. and Schiaffino, S. (2001) Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc. Natl Acad. Sci. USA, 98, 13108-13113.
20. Gramolini, A.O., Belanger, G., Thompson, J.M., Chakkalakal, J.V. and Jasmin, B.J. (2001) Increased expression of utrophin in a slow versus a fast muscle involves posttranscriptional events. Am. J. Physiol. Cell Physiol., 281, C1300-C1309.
21. Webster, C., Silberstein, L., Hays, A.P. and Blau, H.M. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell, 52, 503-513.
22. Moens, P., Baatsen, P.H. and Marechal, G. (1993) Increased susceptibility of EDL muscles from mdx mice to damage induced by contractions with stretch. J. Muscle Res. Cell Motil., 14, 446-451.
23. 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.
24. Friedrich, F.W., Wilding, B.R., Reischmann, S., Crocini, C., Lang, P., Charron, P., Muller, 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.
25. 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. (2013) Loss of FHL1 induces an age-dependent skeletal muscle myopathy associated with myofibrillar and intermyofibrillar disorganization in mice. Hum. Mol. Genet., 23, 209-225.
26. Cowling, B.S., McGrath, M.J., Nguyen, M.A., Cottle, D.L., Kee, A.J., Brown, S., Schessl, J., Zou, Y., Joya, J., Bonnemann, 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.
27. Sicinski, P., Geng, Y., Ryder-Cook, A.S., Barnard, E.A., Darlinson, M.G. and Barnard, P.J. (1989) The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science, 244, 1578-1580.
28. Augusto, V., Padovani, C.R., Eduardo, G. and Campos, R. (2004) Skeletal muscle fibre types in C57BL6J mice. Braz. J. Morphol. Sci., 21, 89-94.
29. Corbett, M.A., Robinson, C.S., Dunglison, G.F., Yang, N., Joya, J.E., Stewart, A.W., Schnell, C., Gunning, P.W., North, K.N. and Hardeman, E.C. (2001) A mutation in alpha-tropomyosin slow affects muscle strength, maturation and hypertrophy in a mouse model for nemaline myopathy.Hum. Mol. Genet., 10, 317-328.
30. Grounds, M.D., Radley, H.G., Lynch, G.S., Nagaraju, K. and De Luca, A. (2009) Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol. Dis., 31, 1-19.
31. Radley, H.G., Davies, M.J. and Grounds, M.D. (2008) Reduced muscle necrosis and long-term benefits in dystrophicmdx mice after cV1q (blockade of TNF) treatment. Neuromuscul. Disord., 18, 227-238.
32. Radley, H.G. and Grounds, M.D. (2006) Cromolyn administration (to block mast cell degranulation) reduces necrosis of dystrophic muscle in mdx mice. Neurobiol. Dis., 23, 387-397.
33. Gehrig, S.M., van der Poel, C., Sayer, T.A., Schertzer, J.D., Henstridge, D.C., Church, J.E., Lamon, S., Russell, A.P., Davies, K.E., Febbraio, M.A. et al. (2012) Hsp72 preserves muscle function and slows progression of severe muscular dystrophy. Nature, 484, 394-398.
34. Villalta, S.A., Rinaldi, C., Deng, B., Liu, G., Fedor, B. and Tidball, J.G. (2011) Interleukin-10 reduces the pathology of mdx muscular dystrophy by deactivating M1 macrophages and modulating macrophage phenotype. Hum. Mol. Genet., 20, 790-805.
35. Villalta, S.A., Nguyen, H.X., Deng, B., Gotoh, T. and Tidball, J.G. (2009) Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum. Mol. Genet., 18, 482-496.
36. Loh, K.C., Leong, W.-I., Carlson, M.E., Oskouian, B., Kumar, A., Fyrst, H., Zhang, M., Proia, R.L., Hoffman, E.P. and Saba, J.D. (2012) Sphingosine-1-Phosphate enhances satellite cell activation in dystrophic muscles through a S1PR2/STAT3 signaling pathway.PLoSONE, 7, e37218.
37. Galvagni, F., Cantini, M. and Oliviero, S. (2002) The utrophin gene is transcriptionally up-regulated in regenerating muscle. J. Biol. Chem., 277, 19106-19113.
38. Aramburu, J., Yaffe, M.B., Lopez-Rodriguez, C., Cantley, L.C., Hogan, P.G. and Rao, A. (1999) Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science, 285, 2129-2133.
39. Chakkalakal, J.V., Miura, P., Belanger, G., Michel, R.N. and Jasmin, B.J. (2008) Modulation of utrophinAmRNAstability in fast versus slow muscles via an AU-rich element and calcineurin signaling. Nucleic Acids Res., 36, 826-838.
40. Amirouche, A., Tadesse, H., Lunde, J.A., Belanger, G., Cote, J. and Jasmin, B.J. (2013) Activation of p38 signaling increases utrophin A expression in skeletal muscle via the RNA-binding protein KSRP and inhibition of AU-rich element-mediated mRNA decay: implications for novel DMD therapeutics. Hum. Mol. Genet., 22, 3093-3111.
41. Amenta, A.R., Yilmaz, A., Bogdanovich, S., McKechnie, B.A., Abedi, M., Khurana, T.S. and Fallon, J.R. (2011) Biglycan recruits utrophin to the sarcolemma and counters dystrophic pathology in mdx mice. Proc. Natl Acad. Sci. USA, 108, 762-767.
42. Pardo, J.V., Siliciano, J.D. and Craig, S.W. (1983) A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements ('costameres') mark sites of attachment between myofibrils and sarcolemma. Proc. Natl Acad. Sci. USA, 80, 1008-1012.
43. Krag, T.O.B., Bogdanovich, S., Jensen, C.J., Fischer, M.D., Hansen-Schwartz, J., Javazon, E.H., Flake, A.W., Edvinsson, L. and Khurana, T.S. (2004) Heregulin ameliorates the dystrophic phenotype in mdx mice. Proc. Natl Acad. Sci. USA, 101, 13856-13860.
44. 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 proteinCand regulates myosin filament formation and sarcomere assembly. J. Biol. Chem., 281, 7666-7683.
45. Schertzer, J.D., Ryall, J.G. and Lynch, G.S. (2006) Systemic administration of IGF-I enhances oxidative status and reduces contraction-induced injury in skeletal muscles of mdx dystrophic mice. Am. J. Physiol. Endocrinol. Metab., 291, E499-E505.
46. Schertzer, J.D., Gehrig, S.M., Ryall, J.G. and Lynch, G.S. (2007) Modulation of Insulin-like Growth Factor (IGF)-I and IGF-binding protein interactions enhances skeletal muscle regeneration and ameliorates the dystrophic pathology in mdx mice. Am. J. Pathol., 171, 1180-1188.
47. Gehrig, S.M., Koopman, R., Naim, T., Tjoakarfa, C. and Lynch, G.S. (2010) Making fast-twitch dystrophic muscles bigger protects them from contraction injury and attenuates the dystrophic pathology. Am. J. Pathol., 176, 29-33.
48. Kim, M.H., Kay, D.I., Rudra, R.T., Chen, B.M., Hsu, N., Izumiya, Y., Martinez, L., Spencer, M.J., Walsh, K., Grinnell, A.D. et al. (2011) Myogenic Akt signaling attenuates muscular degeneration, promotes myofiber regeneration and improves muscle function in dystrophin-deficient mdx mice. Hum. Mol. Genet., 20, 1324-1338.
49. Blaauw, B., Mammucari, C., Toniolo, L., Agatea, L., Abraham, R., Sandri, M., Reggiani, C. and Schiaffino, S. (2008) Akt activation prevents the force drop induced by eccentric contractions in dystrophin-deficient skeletal muscle. Hum. Mol. Genet., 17, 3686-3696.
50. Gramolini, A.O., Angus, L.M., Schaeffer, L., Burton, E.A., Tinsley, J.M., Davies, K.E., Changeux, J.-P. and Jasmin, B.J. (1999) Induction of utrophin gene expression by heregulin in skeletal muscle cells: role of the N-box motif and GA binding protein. Proc. Natl Acad. Sci. USA, 96, 3223-3227.
51. Khurana, T.S., Rosmarin, A.G., Shang, J., Krag, T.O.B., Das, S. and Gammeltoft, S. (1999) Activation of utrophin promoter by heregulin via the ets-related transcription factor complex GA-binding protein alpha/beta. Mol. Biol. Cell, 10, 2075-2086.
52. Miura, P., Thompson, J., Chakkalakal, J.V., Holcik, M. and Jasmin, B.J. (2005) The utrophin A 5' -untranslated region confers internal ribosome entry site-mediated translational control during regeneration of skeletal muscle fibers. J. Biol. Chem., 280, 32997-33005.
53. Angus, L.M., Chakkalakal, J.V., Mejat, A., Eibl, J.K., Belanger, G., Megeney, L.A., Chin, E.R., Schaeffer, L., Michel, R.N. and Jasmin, B.J. (2005) Calcineurin-NFAT signaling, together with GABP and peroxisome PGC-1alpha, drives utrophin gene expression at the neuromuscular junction. Am. J. Physiol. Cell Physiol., 289, C908-C917.
54. 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.
55. Gramolini, A.O., Karpati, G. and Jasmin, B.J. (1999) Discordant expression of utrophin and its transcript in human and mouse skeletal muscles. J. Neuropathol. Exp. Neurol., 58, 235-244.
56. Weir, A.P., Morgan, J.E. and Davies, K.E. (2004) A-utrophin up-regulation in mdx skeletal muscle is independent of regeneration. Neuromuscul. Disord., 14, 19-23.
57. Peter, A.K., Marshall, J.L. and Crosbie, R.H. (2008) Sarcospan reduces dystrophic pathology: stabilization of the utrophin-glycoprotein complex. J. Cell Biol., 183, 419-127.
58. Kleopa, K.A., Drousiotou, A., Mavrikiou, E., Ormiston, A. and Kyriakides, T. (2006) Naturally occurring utrophin correlates with disease severity in Duchenne muscular dystrophy. Hum. Mol. Genet., 15, 1623-1628.
59. Jorgensen, L.H., Jensen, C.H., Wewer, U.M. and Schroder, H.D. (2007) Transgenic overexpression of ADAM12 suppresses muscle regeneration and aggravates dystrophy in aged mdx mice. Am. J. Pathol., 171, 1599-1607.
60. Brown, S., McGrath, M.J., Ooms, L.M., Gurung, R., Maimone, M.M. and Mitchell, C.A. (1999) Characterization of two isoforms of the skeletal muscleLIMprotein 1, SLIM1. Localization of SLIM1at focal adhesions and the isoform slimmer in the nucleus of myoblasts and cytoplasm of myotubes suggests distinct roles in the cytoskeleton and in nuclear-cytoplasmic communication. J. Biol. Chem., 274, 27083-27091.
61. Valdés, J.A., Flores, S., Fuentes, E.N., Osorio-Fuentealba, C., Jaimovich, E. and Molina, A. (2013)IGF-1 induces IP3-dependent calcium signal involved in the regulation of myostatin gene expression mediated by NFAT during myoblast differentiation. J. Cell. Physiol., 228, 1452-1463.