The functional role of calcineurin in hypertrophy, regeneration, and disorders of skeletal muscle

Journal of Biomedicine and Biotechnology

Volumn 2010, Issue , 2010, Pages

  Sakuma, Kunihiro ^a   Yamaguchi, Akihiko ^b  

^a TOYOHASHI UNIVERSITY OF TECHNOLOGY   (Japan)

^b HEALTH SCIENCES UNIVERSITY OF HOKKAIDO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CYCLOSPORIN A; MYOGENIN; MYOSTATIN; TACROLIMUS; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR NFAT;

COMPETITIVE INHIBITION; DIFFERENTIATION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME STRUCTURE; HUMAN; LIMB GIRDLE MUSCULAR DYSTROPHY; MUSCLE HYPERTROPHY; MUSCLE REGENERATION; MUSCLE TWITCH; MUSCULAR DYSTROPHY; MYOPATHY; NONHUMAN; PLANTARIS MUSCLE; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; ULLRICH CONGENITAL MUSCULAR DYSTROPHY; UPREGULATION; ANIMAL; CHEMISTRY; ENZYMOLOGY; HYPERTROPHY; METABOLISM; MUSCLE DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REGENERATION;

ANIMALS; CALCINEURIN; HUMANS; HYPERTROPHY; MUSCLE, SKELETAL; MUSCULAR DISEASES; REGENERATION;

EID: 77951698006     PISSN: 11107243     EISSN: 11107251     Source Type: Journal    
DOI: 10.1155/2010/721219     Document Type: Review

References (84)

1. Pette D., Staron R. S., Cellular and molecular diversities of mammalian skeletal muscle fibers Reviews of Physiology Biochemistry and Pharmacology 1990 116 1 76
2. Berchtold M. W., Brinkmeier H., Muntener M., Calcium ion in skeletal muscle: Its crucial role for muscle function, plasticity, and disease Physiological Reviews 2000 80 3 1215 1265 (Pubitemid 30452014)
3. Swindells M. B., Ikura M., Pre-formation of the semi-open conformation by the apo-calmodulin C-terminal domain and implications for binding IQ-motifs Nature Structural Biology 1996 3 6 501 504 (Pubitemid 26174697)
4. Schulz R. A., Yutzey K. E., Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development Developmental Biology 2004 266 1 1 16 (Pubitemid 38083191)
5. Molkentin J. D., Lu J.-R., Antos C. L., A calcineurin-dependent transcriptional pathway for cardiac hypertrophy Cell 1998 93 2 215 228 (Pubitemid 28180855)
6. Bueno O. F., Wilkins B. J., Tymitz K. M., Impaired cardiac hypertrophic response in calcineurin A -deficient mice Proceedings of the National Academy of Sciences of the United States of America 2002 99 7 4586 4591 (Pubitemid 34286028)
7. Bourajjaj M., Armand A.-S., da Costa Martins P. A., NFATc2 is a necessary mediator of calcineurin-dependent cardiac hypertrophy and heart failure Journal of Biological Chemistry 2008 283 32 22295 22303
8. Mallinson J., Meissner J., Chang K. C., Chapter 2. Calcineurin signaling and the slow oxidative skeletal muscle fiber type International Review of Cell and Molecular Biology 2009 277 67 101
9. Schiaffino S., Sandri M., Murgia M., Activity-dependent signaling pathways controlling muscle diversity and plasticity Physiology 2007 22 4 269 278
10. Guerini D., Klee C. B., Cloning of human calcineurin A: evidence for two isozymes and identification of a polyproline structural domain Proceedings of the National Academy of Sciences of the United States of America 1989 86 23 9183 9187 (Pubitemid 20010389)
11. Lara-Pezzi E., Winn N., Paul A., A naturally occurring calcineurin variant inhibits FoxO activity and enhances skeletal muscle regeneration Journal of Cell Biology 2007 179 6 1205 1218 (Pubitemid 350277739)
12. Crabtree G. R., Olson E. N., NFAT signaling: choreographing the social lives of cells Cell 2002 109 2, supplement 1 S67 S79
13. Crabtree G. R., Generic signals and specific outcomes: signaling through Ca 2 +, calcineurin, and NF-AT Cell 1999 96 5 611 614 (Pubitemid 129746807)
14. Rusnak F., Mertz P., Calcineurin: form and function Physiological Reviews 2000 80 4 1483 1521
15. Vega R. B., Rothermel B. A., Weinheimer C. J., Dual roles of modulatory calcineurin-interacting protein 1 in cardiac hypertrophy Proceedings of the National Academy of Sciences of the United States of America 2003 100 2 669 674
16. Yang J., Rothermel B., Vega R. B., Independent signals control expression of the calcineurin inhibitory proteins MCIP1 and MCIP2 in striated muscles Circulation Research 2000 87 12 E61 E68
17. Frey N., Frank D., Lippl S., Calsarcin-2 deficiency increases exercise capacity in mice through calcineurin/NFAT activation Journal of Clinical Investigation 2008 118 11 3598 3608
18. Bischoff R., Engel A. G., Armstrong F., The satellite cell and muscle regeneration Myology 1994 New York, NY, USA McGraw-Hill 97 118
19. Hawke T. J., Garry D. J., Myoegnic satellite cells: physiology to molecular biology Journal of Applied Physiology 2001 91 2 534 551
20. Jennische E., Matejka G. L., IGF-I binding and IGF-I expression in regenerating muscle of normal and hypophysectomized rats Acta Physiologica Scandinavica 1992 146 1 79 86
21. Semsarian C., Wu M.-J., Ju Y.-K., Skeletal muscle hypertrophy is mediated by a Ca 2 + -dependent calcineurin signalling pathway Nature 1999 400 6744 576 581
22. Dobrowolny G., Giacinti C., Pelosi L., Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model Journal of Cell Biology 2005 168 2 193 199
23. Delling U., Tureckova J., Lim H. W., De Windt L. J., Rotwein P., Molkentin J. D., A calcineurin-NFATc3-dependent pathway regulates skeletal muscle differentiation and slow myosin heavy-chain expression Molecular and Cellular Biology 2000 20 17 6600 6611
24. Friday B. B., Horsley V., Pavlath G. K., Calcineurin activity is required for the initiation of skeletal muscle differentiation Journal of Cell Biology 2000 149 3 657 666
25. Friday B. B., Mitchell P. O., Kegley K. M., Pavlath G. K., Calcineurin initiates skeletal muscle differentiation by activating MEF2 and MyoD Differentiation 2003 71 3 217 227
26. Sakuma K., Nishikawa J., Nakao R., Calcineurin is a potent regulator for skeletal muscle regeneration by association with NFATc1 and GATA-2 Acta Neuropathologica 2003 105 3 271 280
27. Abbott K. L., Friday B. B., Thaloor D., Murphy T. J., Pavlath G. K., Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells Molecular Biology of the Cell 1998 9 10 2905 2916
28. Koulmann N., Sanchez H., NGuessan B., The responsiveness of regenerated soleus muscle to pharmacological calcineurin inhibition Journal of Cellular Physiology 2006 208 1 116 122
29. Stupka N., Schertzer J. D., Bassel-Duby R., Olson E. N., Lynch G. S., Calcineurin-A activation enhances the structure and function of regenerating muscles after myotoxic injury American Journal of Physiology 2007 293 2 R686 R694
30. Grobet L., Pirottin D., Farnir F., Modulating skeletal muscle mass by postnatal, muscle-specific inactivation of the myostatin gene Genesis 2003 35 4 227 238
31. McPherron A. C., Lawler A. M., Lee S.-J., Regulation of skeletal muscle mass in mice by a new TGF- superfamily member Nature 1997 387 6628 83 90
32. Sakuma K., Nakao R., Aoi W., Cyclosporin A treatment upregulates Id1 and Smad3 expression and delays skeletal muscle regeneration Acta Neuropathologica 2005 110 3 269 280
33. Al-Shanti N., Stewart C. E., Ca 2 + /calmodulin-dependent transcriptional pathways: potential mediators of skeletal muscle growth and development Biological Reviews 2009 84 4 637 652
34. Michel R. N., Dunn S. E., Chin E. R., Calcineurin and skeletal muscle growth Proceedings of the Nutrition Society 2004 63 2 341 349
35. Michel R. N., Chin E. R., Chakkalakal J. V., Eibl J. K., Jasmin B. J., Ca 2 + /calmodulin-based signalling in the regulation of the muscle fibre phenotype and its therapeutic potential via modulation of utrophin A and myostatin expression Applied Physiology, Nutrition and Metabolism 2007 32 5 921 929
36. Sakuma K., Watanabe K., Sano M., Uramoto I., Totsuka T., Differential adaptation of growth and differentiation factor 8/myostatin, fibroblast growth factor 6 and leukemia inhibitory factor in overloaded, regenerating and denervated rat muscles Biochimica et Biophysica Acta 2000 1497 1 77 88 (Pubitemid 30330892)
37. Sakuma K., Watanabe K., Hotta N., The adaptive responses in several mediators linked with hypertrophy and atrophy of skeletal muscle after lower limb unloading in humans Acta Physiologica 2009 197 2 151 159
38. Wehling M., Cai B., Tidball J. G., Modulation of myostatin expression during modified muscle use FASEB Journal 2000 14 1 103 110 (Pubitemid 30051528)
39. Gonzalez-Cadavid N. F., Taylor W. E., Yarasheski K., Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting Proceedings of the National Academy of Sciences of the United States of America 1998 95 25 14938 14943 (Pubitemid 29003735)
40. Allen D. L., Unterman T. G., Regulation of myostatin expression and myoblast differentiation by FoxO and SMAD transcription factors American Journal of Physiology 2007 292 1 C188 C199
41. Langley B., Thomas M., Bishop A., Sharma M., Gilmour S., Kambadur R., Myostatin inhibits myoblast differentiation by down-regulating MyoD expression Journal of Biological Chemistry 2002 277 51 49831 49840 (Pubitemid 36014431)
42. Muthuri S. K., Chin E. R., Michel R. N., Myostatin as a putative downstream gene target of calcineurin signaling associated with muscle growth remodeling FASEB Journal 2007 21 895.14
43. Li H.-H., Kedar V., Zhang C., Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex Journal of Clinical Investigation 2004 114 8 1058 1071 (Pubitemid 39578695)
44. Ni Y. G., Berenji K., Wang N., Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling Circulation 2006 114 11 1159 1168
45. Sandri M., Sandri C., Gilbert A., Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy Cell 2004 117 3 399 412
46. Stitt T. N., Drujan D., Clarke B. A., The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors Molecular Cell 2004 14 3 395 403
47. Frost R. A., Lang C. H., Protein kinase B/Akt: a nexus of growth factor and cytokine signaling in determining muscle mass Journal of Applied Physiology 2007 103 1 378 387
48. Glass D. J., Skeletal muscle hypertrophy and atrophy signaling pathways International Journal of Biochemistry and Cell Biology 2005 37 10 1974 1984
49. Rommel C., Bodine S. C., Clarke B. A., Mediation of IGF-1-induced skeletal myotube hypertrophy by Pl(3)K/Akt/mTOR and Pl(3)K/Akt/GSK3 pathways Nature Cell Biology 2001 3 11 1009 1013
50. Musar A., McCullagh K. J. A., Naya F. J., Olson E. N., Rosenthal N., IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1 Nature 1999 400 6744 581 585
51. Dunn S. E., Burns J. L., Michel R. N., Calcineurin is required for skeletal muscle hypertrophy Journal of Biological Chemistry 1999 274 31 21908 21912
52. Naya F. J., Mercer B., Shelton J., Richardson J. A., Williams R. S., Olson E. N., Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo Journal of Biological Chemistry 2000 275 7 4545 4548
53. Bodine S. C., Stitt T. N., Gonzalez M., Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo Nature Cell Biology 2001 3 11 1014 1019
54. Parsons S. A., Wilkins B. J., Bueno O. F., Molkentin J. D., Altered skeletal muscle phenotypes in calcineurin A and A gene-targeted mice Molecular and Cellular Biology 2003 23 12 4331 4343
55. Parsons S. A., Millay D. P., Wilkins B. J., Genetic loss of calcineurin blocks mechanical overload-induced skeletal muscle fiber type switching but not hypertrophy Journal of Biological Chemistry 2004 279 25 26192 26200
56. Talmadge R. J., Otis J. S., Rittler M. R., Calcineurin activation influences muscle phenotype in a muscle-specific fashion BMC Cell Biology 2004 5, article 28
57. Lai K.-M. V., Gonzalez M., Poueymirou W. T., Conditional activation of Akt in adult skeletal muscle induces rapid hypertrophy Molecular and Cellular Biology 2004 24 21 9295 9304
58. Oh M., Rybkin I. I., Copeland V., Calcineurin is necessary for the maintenance but not embryonic development of slow muscle fibers Molecular and Cellular Biology 2005 25 15 6629 6638
59. Sakuma K., Akiho M., Nakashima H., Cyclosporin A modulates cellular localization of MEF2C protein and blocks fiber hypertrophy in the overloaded soleus muscle of mice Acta Neuropathologica 2008 115 6 663 674
60. Mitchell P. O., Mills S. T., Pavlath G. K., Calcineurin differentially regulates maintenance and growth of phenotypically distinct muscles American Journal of Physiology 2002 282 5 C984 C992
61. Miyazaki M., Hitomi Y., Kizaki T., Calcineurin-mediated slow-type fiber expression and growth in reloading condition Medicine and Science in Sports and Exercise 2006 38 6 1065 1072
62. Oishi Y., Ogata T., Yamamoto K.-I., Cellular adaptations in soleus muscle during recovery after hindlimb unloading Acta Physiologica 2008 192 3 381 395
63. Molkentin J. D., Lu J.-R., Antos C. L., A calcineurin-dependent transcriptional pathway for cardiac hypertrophy Cell 1998 93 2 215 228
64. Wilkins B. J., Molkentin J. D., Calcineurin and cardiac hypertrophy: where have we been? Where are we going? The Journal of Physiology 2002 541 1 1 8 (Pubitemid 35203232)
65. Dunn S. E., Chin E. R., Michel R. N., Matching of calcineurin activity to upstream effectors is critical for skeletal muscle fiber growth Journal of Cell Biology 2000 151 3 663 672
66. Horsley V., Friday B. B., Matteson S., Kegley K. M., Gephart J., Pavlath G. K., Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway Journal of Cell Biology 2001 153 2 329 338 (Pubitemid 34280219)
67. Kegley K. M., Gephart J., Warren G. L., Pavlath G. K., Altered primary myogenesis in NFATC3 -/- mice leads to decreased muscle size in the adult Developmental Biology 2001 232 1 115 126 (Pubitemid 32250949)
68. Hinits Y., Hughes S. M., Mef2s are required for thick filament formation in nascent muscle fibres Development 2007 134 13 2511 2519
69. Potthoff M. J., Arnold M. A., McAnally J., Richardson J. A., Bassel-Duby R., Olson E. N., Regulation of skeletal muscle sarcomere integrity and postnatal muscle function by Mef2c Molecular and Cellular Biology 2007 27 23 8143 8151
70. Dunn S. E., Simard A. R., Bassel-Duby R., Williams R. S., Michel R. N., Nerve activity-dependent modulation of calcineurin signaling in adult fast and slow skeletal muscle fibers Journal of Biological Chemistry 2001 276 48 45243 45254
71. Alfieri C. M., Evans-Anderson H. J., Yutzey K. E., Developmental regulation of the mouse IGF-I exon 1 promoter region by calcineurin activation of NFAT in skeletal muscle American Journal of Physiology 2007 292 5 C1887 C1894
72. Allen D. L., Uyenishi J. J., Cleary A. S., Mehan R. S., Lindsay S. F., Reed J. M., Calcineurin activates interleukin-6 transcription in mouse skeletal muscle in vivo and in C2C12 myotubes in vitro American Journal of Physiology 2010 298 1 R198 R210
73. Paul A. C., Rosenthal N., Different modes of hypertrophy in skeletal muscle fibers Journal of Cell Biology 2002 156 4 751 760
74. Chakkalakal J. V., Stocksley M. A., Harrison M.-A., Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling Proceedings of the National Academy of Sciences of the United States of America 2003 100 13 7791 7796
75. Chakkalakal J. V., Harrison M.-A., Carbonetto S., Chin E., Michel R. N., Jasmin B. J., Stimulation of calcineurin signaling attenuates the dystrophic pathology in mdx mice Human Molecular Genetics 2004 13 4 379 388
76. Stupka N., Gregorevic P., Plant D. R., Lynch G. S., The calcineurin signal transduction pathway is essential for successful muscle regeneration in mdx dystrophic mice Acta Neuropathologica 2004 107 4 299 310
77. Angus L. M., Chakkalakal J. V., Mejat A., Calcineurin-NFAT signaling, together with GABP and PGC-1, drives utrophin gene expression at the neuromuscular junction American Journal of Physiology 2005 289 4 C908 C917
78. Chakkalakal J. V., Michel S. A., Chin E. R., Michel R. N., Jasmin B. J., Targeted inhibition of Ca 2 + /calmodulin signaling exacerbates the dystrophic phenotype in mdx mouse muscle Human Molecular Genetics 2006 15 9 1423 1435
79. Stupka N., Michell B. J., Kemp B. E., Lynch G. S., Differential calcineurin signalling activity and regeneration efficacy in diaphragm and limb muscles of dystrophic mdx mice Neuromuscular Disorders 2006 16 5 337 346
80. Stupka N., Plant D. R., Schertzer J. D., Activated calcineurin ameliorates contraction-induced injury to skeletal muscles of mdx dystrophic mice Journal of Physiology 2006 575 2 645 656
81. Angelin A., Tiepolo T., Sabatelli P., Mitochondrial dysfunction in the pathogenesis of Ullrich congenital muscular dystrophy and prospective therapy with cyclosporins Proceedings of the National Academy of Sciences of the United States of America 2007 104 3 991 996
82. Parsons S. A., Millay D. P., Sargent M. A., Genetic disruption of calcineurin improves skeletal muscle pathology and cardiac disease in a mouse model of limb-girdle muscular dystrophy Journal of Biological Chemistry 2007 282 13 10068 10078
83. Stupka N., Schertzer J. D., Bassel-Duby R., Olson E. N., Lynch G. S., Stimulation of calcineurin Aalpha activity attenuates muscle pathophysiology in mdx dystrophic mice American Journal of Physiology 2008 294 3 R983 R992
84. Merlini L., Angelin A., Tiepolo T., Cyclosporin A corrects mitochondrial dysfunction and muscle apoptosis in patients with collagen VI myopathies Proceedings of the National Academy of Sciences of the United States of America 2008 105 13 5225 5229