Evidence for FHL1 as a novel disease gene for isolated hypertrophic cardiomyopathy

Human Molecular Genetics

Volumn 21, Issue 14, 2012, Pages 3237-3254

  Friedrich, Felix W ^a   Wilding, Brendan R ^b   Reischmann, Silke ^a   Crocini, Claudia ^a   Lang, Patrick ^c   Charron, Philippe ^d,e,h   Müller, Oliver J ⁱ   Mcgrath, Meagan J ^b   Vollert, Ingra ^a   Hansen, Arne ^a   Linke, Wolfgang A ^c   Hengstenberg, Christian ^j   Bonne, Gisèle ^e,f,g   Morner, Stellan ^k   Wichter, Thomas ^l,o   Madeira, Hugo ^m   Arbustini, Eloisa ⁿ   Eschenhagen, Thomas ^a   Mitchell, Christina A ^b   Isnard, Richard ^d,h   Carrier, Lucie ^a,e,f   more..

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b MONASH UNIVERSITY   (Australia)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d INSERM   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f Sorbonne Université   (France)

^g ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^h PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

ⁱ UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^j UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^k UMEÅ UNIVERSITY   (Sweden)

^l UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^m HOSPITAL DE SANTA MARIA   (Portugal)

ⁿ FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

^o MarienHospital Osnabruck   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

FOUR AND A HALF LIM DOMAINS 1 PROTEIN; PROTEASOME; PROTEIN; UNCLASSIFIED DRUG;

ADENO ASSOCIATED VIRUS; ANIMAL TISSUE; ARTICLE; BINDING ASSAY; CONTROLLED STUDY; FEMALE; GENE DELETION; GENE MUTATION; GENE TRANSFER; GENETIC VARIABILITY; HEART CONTRACTION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HEART MUSCLE RELAXATION; HUMAN; HUMAN CELL; HYPERTROPHIC CARDIOMYOPATHY; MAJOR CLINICAL STUDY; MALE; MUSCLE FIBRIL; MUSCLE WEAKNESS; MUTANT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; RAT; TISSUE ENGINEERING; VIRAL GENE DELIVERY SYSTEM;

ADOLESCENT; ADULT; AGED; ANIMALS; CARDIOMYOPATHY, HYPERTROPHIC; CASE-CONTROL STUDIES; CELLS, CULTURED; CHILD; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIM DOMAIN PROTEINS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MUSCLE PROTEINS; MUTATION; MYOCYTES, CARDIAC; PEDIGREE; YOUNG ADULT;

ADENO-ASSOCIATED VIRUS; RATTUS;

EID: 84864004251     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds157     Document Type: Article

References (63)

1. 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.
2. Bach, I. (2000) The LIM domain: regulation by association. Mech. Dev., 91, 5-17.
3. 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 muscle LIM protein 1, SLIM1. Localization of SLIM1 at 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.
4. Robinson, P.A., Brown, S., McGrath, M.J., Coghill, I.D., Gurung, R. and Mitchell, C.A. (2003) Skeletal muscle LIM protein 1 regulates integrin-mediated myoblast adhesion, spreading, and migration. Am. J. Physiol. Cell Physiol., 284, C681-C695.
5. Muller, J.M., Metzger, E., Greschik, H., Bosserhoff, A.K., Mercep, L., Buettner, R. and Schule, R. (2002) The transcriptional coactivator FHL2 transmits Rho signals from the cell membrane into the nucleus. EMBO J., 21, 736-748.
6. 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.
7. 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.
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 protein C and regulates myosin filament formation and sarcomere assembly. J. Biol. Chem., 281, 7666-7683.
9. Yang, Z., Browning, C.F., Hallaq, H., Yermalitskaya, L., Esker, J., Hall, M.R., Link, A.J., Ham, A.J., McGrath, M.J., Mitchell, C.A. et al. (2008) Four and a half LIM protein 1: a partner for KCNA5 in human atrium. Cardiovasc. Res., 78, 449-457.
10. 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.
11. Taniguchi, Y., Furukawa, T., Tun, T., Han, H. and Honjo, T. (1998) LIM protein KyoT2 negatively regulates transcription by association with the RBP-J DNA-binding protein. Mol. Cell. Biol., 18, 644-654.
12. Ng, E.K., Lee, S.M., Li, H.Y., Ngai, S.M., Tsui, S.K., Waye, M.M., Lee, C.Y. and Fung, K.P. (2001) Characterization of tissue-specific LIM domain protein (FHL1C) which is an alternatively spliced isoform of a human LIM-only protein (FHL1). J. Cell. Biochem., 82, 1-10.
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, termed XMPMA, is caused by mutations in FHL1. Am. J. Hum. Genet., 82, 88-99.
14. 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.
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. Knoblauch, H., Geier, C., Adams, S., Budde, B., Rudolph, A., Zacharias, U., Schulz-Menger, J., Spuler, A., Yaou, R.B., Nurnberg, P. et al. (2010) Contractures and hypertrophic cardiomyopathy in a novel FHL1 mutation. Ann. Neurol., 67, 136-140.
19. Hwang, D.M., Dempsey, A.A., Wang, R.X., Rezvani, M., Barrans, J.D., Dai, K.S., Wang, H.Y., Ma, H., Cukerman, E., Liu, Y.Q. et al. (1997) A genome-based resource for molecular cardiovascular medicine: toward a compendium of cardiovascular genes. Circulation, 96, 4146-4203.
20. Lim, D.S., Roberts, R. and Marian, A.J. (2001) Expression profiling of cardiac genes in human hypertrophic cardiomyopathy: insight into the pathogenesis of phenotypes. J. Am. Coll. Cardiol., 38, 1175-1180.
21. Gaussin, V., Tomlinson, J.E., Depre, C., Engelhardt, S., Antos, C.L., Takagi, G., Hein, L., Topper, J.N., Liggett, S.B., Olson, E.N. et al. (2003) Common genomic response in different mouse models of beta-adrenergic-induced cardiomyopathy. Circulation, 108, 2926-2933.
22. Gersh, B.J., Maron, B.J., Bonow, R.O., Dearani, J.A., Fifer, M.A., Link, M.S., Naidu, S.S., Nishimura, R.A., Ommen, S.R., Rakowski, H. et al. (2011) 2011 ACCF/AHA guideline for the diagnosis and treatment of hypertrophic cardiomyopathy: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J. Thorac. Cardiovasc. Surg., 142, e153-e203.
23. Elliott, P., Andersson, B., Arbustini, E., Bilinska, Z., Cecchi, F., Charron, P., Dubourg, O., Kuhl, U., Maisch, B., McKenna, W.J. et al. (2008) Classification of the cardiomyopathies: a position statement from the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases. Eur. Heart J., 29, 270-276.
24. Schlossarek, S., Mearini, G. and Carrier, L. (2011) Cardiac myosin-binding protein C in hypertrophic cardiomyopathy: mechanisms and therapeutic opportunities. J. Mol. Cell. Cardiol., 50, 613-620.
25. Seidman, C. (2002) Genetic causes of inherited cardiac hypertrophy: Robert L. Frye Lecture. Mayo Clin. Proc., 77, 1315-1319.
26. Richard, P., Villard, E., Charron, P. and Isnard, R. (2006) The genetic bases of cardiomyopathies. J. Am. Coll. Cardiol., 48, A79-A89.
27. Friedrich, F.W. and Carrier, L. (2012) Genetics of hypertrophic and dilated cardiomyopathy. Curr. Pharm. Biotechnol. [Epub ahead of print].
28. Dougu, N., Joho, S., Shan, L., Shida, T., Matsuki, A., Uese, K., Hirono, K., Ichida, F., Tanaka, K., Nishino, I. et al. (2009) Novel LAMP-2 mutation in a family with Danon disease presenting with hypertrophic cardiomyopathy. Circ. J., 73, 376-380.
29. Yang, Z., McMahon, C.J., Smith, L.R., Bersola, J., Adesina, A.M., Breinholt, J.P., Kearney, D.L., Dreyer, W.J., Denfield, S.W., Price, J.F. et al. (2005) Danon disease as an underrecognized cause of hypertrophic cardiomyopathy in children. Circulation, 112, 1612-1617.
30. Schoser, B., Goebel, H.H., Janisch, I., Quasthoff, S., Rother, J., Bergmann, M., Muller-Felber, W. and Windpassinger, C. (2009) Consequences of mutations within the C terminus of the FHL1 gene. Neurology, 73, 543-551.
31. Mearini, G., Schlossarek, S., Willis, M.S. and Carrier, L. (2008) The ubiquitin-proteasome system in cardiac dysfunction. Biochim. Biophys. Acta, 1782, 749-763.
32. Schlossarek, S. and Carrier, L. (2011) The ubiquitin-proteasome system in cardiomyopathies. Curr. Opin. Cardiol., 26, 190-195.
33. Ferrans, V.J. and Rodriguez, E.R. (1983) Specificity of light and electron microscopic features of hypertrophic obstructive and nonobstructive cardiomyopathy. Qualitative, quantitative and etiologic aspects. Eur. Heart J., 4 (Suppl. F), 9-22.
34. Bahrudin, U., Morisaki, H., Morisaki, T., Ninomiya, H., Higaki, K., Nanba, E., Igawa, O., Takashima, S., Mizuta, E., Miake, J. et al. (2008) Ubiquitin-proteasome system impairment caused by a missense cardiac myosin-binding protein C mutation and associated with cardiac dysfunction in hypertrophic cardiomyopathy. J. Mol. Biol., 384, 896-907.
35. Sarikas, A., Carrier, L., Schenke, C., Doll, D., Flavigny, J., Lindenberg, K.S., Eschenhagen, T. and Zolk, O. (2005) Impairment of the ubiquitin-proteasome system by truncated cardiac myosin binding protein C mutants. Cardiovasc. Res., 66, 33-44.
36. Mearini, G., Gedicke, C., Schlossarek, S., Witt, C.C., Kramer, E., Cao, P., Gomes, M.D., Lecker, S.H., Labeit, S., Willis, M.S. et al. (2010) Atrogin-1 and MuRF1 regulate cardiac MyBP-C levels via different mechanisms. Cardiovasc. Res., 85, 357-366.
37. Vignier, N., Schlossarek, S., Fraysse, B., Mearini, G., Kramer, E., Pointu, H., Mougenot, N., Guiard, J., Reimer, R., Hohenberg, H. et al. (2009) Nonsense-mediated mRNA decay and ubiquitin-proteasome system regulate cardiac myosin-binding protein C mutant levels in cardiomyopathic mice. Circ. Res., 105, 239-248.
38. Michelsen, J.W., Sewell, A.K., Louis, H.A., Olsen, J.I., Davis, D.R., Winge, D.R. and Beckerle, M.C. (1994) Mutational analysis of the metal sites in an LIM domain. J. Biol. Chem., 269, 11108-11113.
39. Schessl, J., Columbus, A., Hu, Y., Zou, Y., Voit, T., Goebel, H.H. and Bonnemann, 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.
40. 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.
41. Muchir, A., Massart, C., van Engelen, B.G., Lammens, M., Bonne, G. and Worman, H.J. (2006) Proteasome-mediated degradation of integral inner nuclear membrane protein emerin in fibroblasts lacking A-type lamins. Biochem. Biophys. Res. Commun., 351, 1011-1017.
42. Gong, Q., Zhang, L., Vincent, G.M., Horne, B.D. and Zhou, Z. (2007) Nonsense mutations in hERG cause a decrease in mutant mRNA transcripts by nonsense-mediated mRNA decay in human long-QT syndrome. Circulation, 116, 17-24.
43. van Dijk, S.J., Dooijes, D., Dos Remedios, C., Michels, M., Lamers, J.M., Winegrad, S., Schlossarek, S., Carrier, L., Ten Cate, F.J., Stienen, G.J. et al. (2009) Cardiac myosin-binding protein C mutations and hypertrophic cardiomyopathy. Haploinsufficiency, deranged phosphorylation, and cardiomyocyte dysfunction. Circulation, 119, 1473-1483.
44. van Dijk, S.J., Paalberends, E.R., Najafi, A., Michels, M., Sadayappan, S., Carrier, L., Boontje, N.M., Kuster, D.W., van Slegtenhorst, M., Dooijes, D. et al. (2012) Contractile dysfunction irrespective of the mutant protein in human hypertrophic cardiomyopathy with normal systolic function. Circ. Heart Fail., 5, 36-46.
45. Linke, W.A., Rudy, D.E., Centner, T., Gautel, M., Witt, C., Labeit, S. and Gregorio, C.C. (1999) I-band titin in cardiac muscles is a three-element molecular spring and is critical for maintaining thin filament structure. J. Cell Biol., 146, 631-644.
46. LeWinter, M.M., Wu, Y., Labeit, S. and Granzier, H. (2007) Cardiac titin: structure, functions and role in disease. Clin. Chim. Acta, 375, 1-9.
47. Kwapiszewska, G., Wygrecka, M., Marsh, L.M., Schmitt, S., Trosser, R., Wilhelm, J., Helmus, K., Eul, B., Zakrzewicz, A., Ghofrani, H.A. et al. (2008) Fhl-1, a new key protein in pulmonary hypertension. Circulation, 118, 1183-1194.
48. 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.
49. 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.
50. 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.
51. Su, H. and Wang, X. (2010) The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc. Res., 85, 253-262.
52. Schlossarek, S., Schuermann, F., Geertz, B., Mearini, G., Eschenhagen, T. and Carrier, L. (2011) Adrenergic stress reveals septal hypertrophy and proteasome impairment in heterozygous Mybpc3-targeted knock-in mice. J. Muscle Res. Cell Motil. [Epub ahead of print].
53. Schlossarek, S., Englmann, D.R., Sultan, K.R., Sauer, M., Eschenhagen, T. and Carrier, L. (2012) Defective proteolytic systems in Mybpc3-targeted mice with cardiac hypertrophy. Basic Res. Cardiol., 107, 1-13.
54. Predmore, J.M., Wang, P., Davis, F., Bartolone, S., Westfall, M.V., Dyke, D.B., Pagani, F., Powell, S.R. and Day, S.M. (2010) Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation, 121, 997-1004.
55. Tang, M., Li, J., Huang, W., Su, H., Liang, Q., Tian, Z., Horak, K.M., Molkentin, J.D. and Wang, X. (2010) Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc. Res., 88, 424-433.
56. Friedrich, F.W., Bausero, P., Sun, Y., Treszl, A., Kramer, E., Juhr, D., Richard, P., Wegscheider, K., Schwartz, K., Brito, D. et al. (2009) A new polymorphism in human calmodulin III gene promoter is a potential modifier gene for familial hypertrophic cardiomyopathy. Eur. Heart J., 30, 1648-1655.
57. Charron, P., Dubourg, O., Desnos, M., Bouhour, J.B., Isnard, R., Hagège, A., Carrier, L., Bonne, G., Tesson, F., Richard, P. et al. (1998) Diagnostic value of electrocardiography and echocardiography for familial hypertrophic cardiomyopathy in genotyped children. Eur. Heart J., 19, 1377-1382.
58. Muller, O.J., Schinkel, S., Kleinschmidt, J.A., Katus, H.A. and Bekeredjian, R. (2008) Augmentation of AAV-mediated cardiac gene transfer after systemic administration in adult rats. Gene. Ther., 15, 1558-1565.
59. Neagoe, C., Kulke, M., del Monte, F., Gwathmey, J.K., de Tombe, P.P., Hajjar, R.J. and Linke, W.A. (2002) Titin isoform switch in ischemic human heart disease. Circulation, 106, 1333-1341.
60. Pohlmann, L., Kroger, I., Vignier, N., Schlossarek, S., Kramer, E., Coirault, C., Sultan, K.R., El-Armouche, A., Winegrad, S., Eschenhagen, T. et al. (2007) Cardiac myosin-binding protein C is required for complete relaxation in intact myocytes. Circ. Res., 101, 928-938.
61. Bardswell, S.C., Cuello, F., Rowland, A.J., Sadayappan, S., Robbins, J., Gautel, M., Walker, J.W., Kentish, J.C. and Avkiran, M. (2010) Distinct sarcomeric substrates are responsible for protein kinase D-mediated regulation of cardiac myofilament Ca2+ sensitivity and cross-bridge cycling. J. Biol. Chem., 285, 5674-5682.
62. Hansen, A., Eder, A., Bonstrup, M., Flato, M., Mewe, M., Schaaf, S., Aksehirlioglu, B., Schworer, A., Uebeler, J. and Eschenhagen, T. (2010) Development of a drug screening platform based on engineered heart tissue. Circ. Res., 107, 35-44.
63. Schaaf, S., Shibamiya, A., Mewe, M., Eder, A., Stohr, A., Hirt, M.N., Rau, T., Zimmermann, W.H., Conradi, L., Eschenhagen, T. et al. (2011) Human engineered heart tissue as a versatile tool in basic research and preclinical toxicology. PLoS One, 6, e26397.