Loss of FHL1 induces an age-dependent skeletal muscle myopathy associated with myofibrillar and intermyofibrillar disorganization in mice

Human Molecular Genetics

Volumn 23, Issue 1, 2014, Pages 209-225

  Domenighetti, Andrea A ^a   Chu, Pao Hsien ^d,e   Wu, Tongbin ^a   Sheikh, Farah ^a   Gokhin, David S ^b,c,f   Guo, Ling T ^c   Cui, Ziyou ^g   Peter, Angela K ^a   Christodoulou, Danos C ^h   Parfenov, Michael G ^h   Gorham, Joshua M ^h   Li, Daniel Y ^a   Banerjee, Indroneal ^a   Lai, Xianyin ⁱ   Witzmann, Frank A ⁱ   Seidman, Christine E ^h   Seidman, Jonathan G ^h   Gomes, Aldrin V ^g   Shelton, G Diane ^c   Lieber, Richard L ^b,c   Chen, Ju ^a   more..

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^e CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h HARVARD MEDICAL SCHOOL   (United States)

ⁱ INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIM DOMAIN PROTEIN 1; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; DISORIENTATION; EMERY DREIFUSS MUSCULAR DYSTROPHY; LONGITUDINAL STUDY; MATURATION; MISSENSE MUTATION; MUSCLE CELL; MUSCULAR DYSTROPHY; MYOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKELETAL MUSCLE; SURVIVAL RATE;

AGE FACTORS; ANIMALS; CELL DIFFERENTIATION; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIM DOMAIN PROTEINS; MALE; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; MUSCULAR DYSTROPHY, EMERY-DREIFUSS; MYOBLASTS, SKELETAL; MYOFIBRILS;

EID: 84890327624     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt412     Document Type: Article

References (44)

1. Morgan, M.J., Madgwick, A.J., Charleston, B., Pell, J.M. and Loughna, P.T. (1995) The developmental regulation of a novel muscle LIM-protein. Biochem. Biophys. Res. Commun., 212, 840-846.
2. Morgan, M.J. and Madgwick, A.J. (1996) Slim defines a novel family of LIM-proteins expressed in skeletal muscle. Biochem. Biophys. Res. Commun., 225, 632-638.
3. Taniguchi, Y., Furukawa, T., Tun, T., Han, H. and Honjo, T. (1998) LIM protein KyoT2 negatively regulates transcription by association with the RBPJ DNA binding protein. Mol. Cell. Biol., 18, 644-654.
4. 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 ofSLIM1at 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.
5. Chu, P.H., Ruiz-Lozano, P., Zhou, Q., Cai, C. and Chen, J. (2000) Expression patterns ofFHL/SLIMfamily members suggest important functional roles in skeletal muscle and cardiovascular system. Mech. Dev., 95, 259-265.
6. Shathasivam, T., Kislinger, T. and Gramolini, A.O. (2010) Genes, proteins and complexes: the multifaceted nature of FHL family proteins in diverse tissues. J. Cell. Mol. Med., 14, 2702-2720.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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, termedXMPMA,is caused by mutations in FHL1. Am. J. Hum. Genet., 82, 88-99.
14. Schoser, B., Goebel, H.H., Janisch, I., Quasthoff, S., Rother, J., Bergmann, M., Müller-Felber, W. and Windpassinger, C. (2009) Consequences of mutations within theCterminus of theFHL1gene. Neurology, 73, 543-551.
15. 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.
16. Quinzii, C.M., Vu, T.H., Min, K.C., Tanji, K., Barral, S., Grewal, R.P., Kattah, A., Camano, 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.
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. Tiffin, H.R., Jenkins, Z.A., Gray, M.J., Cameron-Christie, S.R., Eaton, J., Aftimos, S., Markie, D. and Robertson, S.P. (2013) Dysregulation of FHL1 spliceforms due to an indel mutation produces an Emery-Dreifuss muscular dystrophy plus phenotype. Neurogenetics, 14, 113-121.
19. 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. Neuromuscul. Disord., 23, 418-426.
20. 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.
21. 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.
22. Tirrell, T.F., Cook, M.S., Carr, J.A., Lin, E., Ward, S.R. and Lieber, R.L. (2012) Human skeletal muscle biochemical diversity. J. Exp. Biol., 215, 2551-2559.
23. Greene, E. (1935) Anatomy of the Rat. Hafner Publishing Co., New York 1955.
24. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) Tophat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
25. Ramaswamy, K.S., Palmer, M.L., van der Meulen, J.H., Renoux, A., Kostrominova, T.Y., Michele, D.E. and Faulkner, J.A. (2011) Lateral transmission of force is impaired in skeletal muscles of dystrophic mice and very old rats. J. Physiol., 589, 1195-1208.
26. Scott, W., Stevens, J. and Binder-Macleod, S.A. (2001) Human skeletal muscle fiber type classifications. Phys. Ther., 81, 1810-1816.
27. McGuire, M., Dumbleton, M., MacDermott, M. and Bradford, A. (2001) Contractile and electrical properties of sternohyoid muscle in streptozotocin diabetic rats. Clin. Exp. Pharmacol. Physiol., 28, 184-187.
28. Remmers, J.E., deGroot, W.J., Sauerland, E.K. and Anch, A.M. (1978) Pathogenesis of upper airway occlusion during sleep. J. Appl. Physiol., 44, 931-938.
29. Khan, Y. and Heckmatt, J.Z. (1994) Obstructive apnoeas in Duchenne muscular dystrophy. Thorax, 49, 157-161. 30. Dedrick, D.L. and Brown, L.K. (2004) Obstructive sleep apnea syndrome complicating oculopharyngeal muscular dystrophy. Chest, 125, 334-336.
30. Dedrick, D.L. and Brown, L.K. (2004) Obstructive sleep apnea syndrome complicating oculopharyngeal muscular dystrophy. Chest, 125, 334-336.
31. Attal, P., Lambert, F., Marchand-Adam, S., Bobin, S., Pourny, J.C., Chemla, D., Lecarpentier, Y. and Coirault, C. (2000) Severe mechanical dysfunction in pharyngeal muscle from adult mdx mice. Am. J. Respir. Crit. Care Med., 162, 278-281.
32. van Lunteren, E. and Moyer, M. (2003) Sternohyoid muscle fatigue properties of dy/dy dystrophic mice, an animal model of merosin-deficient congenital muscular dystrophy. Pediatr. Res., 54, 547-553.
33. 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.
34. 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.
35. Lalonde, R. and Strazielle, C. (2011) Brain regions and genes affecting limb-clasping responses. Brain Res. Rev., 67, 252-259.
36. Christodoulou, D.C., Gorham, J.M., Herman, D.S. and Seidman, J.G. (2011) Construction of normalized RNA-seq libraries for next-generation sequencing using the crab duplex-specific nuclease. Curr. Protoc. Mol. Biol., Chapter 4, Unit 4.12.
37. Lai, X., Bacallao, R.L., Blazer-Yost, B.L., Hong, D., Mason, S.B. and Witzmann, F.A. (2008) Characterization of the renal cyst fluid proteome in autosomal dominant polycystic kidney disease (ADPKD) patients. Proteomics Clin. Appl., 2, 1140-1152.
38. Lai, X., Wang, L., Tang, H. and Witzmann, F.A. (2011) A novel alignment method and multiple filters for exclusion of unqualified peptides to enhance label-free quantification using peptide intensity in LC-MS/MS. J. Proteome Res., 10, 4799-4812.
39. Talmadge, R.J. and Roy, R.R. (1993) Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol., 75, 2337- 2340.
40. Dubowitz, V. and Sewry, C.A. (2007) Muscle Biopsy:APractical Approach. 3rd edn. Saunders Elsevier, London, pp. 21-39.
41. ørtenblad, N., Nielsen, J., Saltin, B. and Holmberg, H.C. (2011) Role of glycogen availability in sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J. Physiol., 589, 711-725.
42. Chleboun, G.S., Patel, T.J. and Lieber, R.L. (1997) Skeletal muscle architecture and fiber-type distribution with the multiple bellies of the mouse extensor digitorum longus muscle. Acta Anat. (Basel), 159, 147-155.
43. Sam, M., Shah, S., Fridén, J., Milner, D.J., Capetanaki, Y. and Lieber, R.L. (2000) Desmin knockout muscles generate lower stress and are less vulnerable to injury compared with wild type muscles. Am. J. Physiol. Cell. Physiol., 279, C1116-C1122.
44. Rando, T.A. and Blau, H.M. (1994) Primary mouse myoblast purification, characterization, and transplantation for cell-mediated gene therapy. J. Cell. Biol., 125, 1275-1287.