Calcineurin: A poorly understood regulator of muscle mass

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 10, 2013, Pages 2173-2178

  Hudson, Matthew B ^a   Price, S Russ ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Atrophy; Calcineurin; Cell signaling; Hypertrophy; Skeletal muscle

Indexed keywords

CALCINEURIN; CALCINEURIN INHIBITOR; CALCIUM ION; CYCLOSPORIN A; INSULIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; SOMATOMEDIN; TACROLIMUS;

ARTICLE; GENETIC MODEL; HUMAN; INTRACELLULAR SIGNALING; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE GROWTH; MUSCLE HYPERTROPHY; MUSCLE MASS; NONHUMAN; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; SKELETAL MUSCLE;

ATROPHY; CALCINEURIN; CELL SIGNALING; CNA; CNAΑ; CNAΒΒ; CSA; CYCLOSPORINE; FORKHEAD BOX O; FOXO; HYPERTROPHY; IGF-1; INSULIN-LIKE GROWTH FACTOR-1; ISOFORM OF THE CNA CATALYTIC SUBUNIT; MCK; MEF2; MLC; MUSCLE CREATINE KINASE; MYOCYTE ENHANCING FACTOR 2; MYOSIN LIGHT CHAIN; NFAT; NUCLEAR FACTOR OF ACTIVATED T CELLS; PHOSPHATIDYLINOSITOL 3-KINASE; PI3K; SKELETAL MUSCLE; Α ISOFORM OF THE CNA CATALYTIC SUBUNIT;

ANIMALS; CALCINEURIN; HUMANS; HYPERTROPHY; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR ATROPHY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84885189457     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.06.029     Document Type: Review

References (86)

1. Allen DL, Loh AS Posttranscriptional mechanisms involving microRNA-27a and b contribute to fast-specific and glucocorticoid-mediated myostatin expression in skeletal muscle. American Journal of Physiology Cell Physiology 2011; 300:C124-37.
2. Arany Z. PGC-1 coactivators and skeletal muscle adaptations in health and disease. Current Opinion in Genetics & Development 2008; 18:426-34.
3. Banzet S, Sanchez H, Chapot R., Peinnequin A, Bigard X, Koulmann N. Basal peroxisome proliferator activated receptor gamma coactivator 1alpha expression is independent of calcineurin in skeletal muscle. Metabolism: Clinical and Experimental 2012; 61:389-94.
4. Bodine SC, Stitt TN, Gonzalez M, Kline W.O., Stover GL, Bauerlein R, et al Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nature Cell Biology 2001; 3:1014-9.
5. Breil M, Chariot P. Muscle disorders associated with cyclosporine treatment. Muscle Nerve 1999; 22:1631-6.
6. Chhabra R, Dubey R, Saini N. Gene expression profiling indicate role of ER stress in miR-23a-27a-24-2 cluster induced apoptosis in HEK293T cells. RNA Biology 2011; 8:648-64.
7. 2+, calcineurin, and NF-AT. Cell 1999; 96:611-4.
8. Davies KJ, Ermak G, Rothermel BA, Pritchard M, Heitman J, Ahnn J, et al. Renaming the DSCR1/Adapt78 gene family as RCAN: regulators of calcineurin. FASEB Journal 2007; 21:3023-8.
9. Dunn SE, Burns JL, Michel RN Calcineurin is required for skeletal muscle hypertrophy. Journal of Biological Chemistry 1999; 274:21908-12.
10. Dunn SE, Chin ER, Michel RN Matching of calcineurin activity to upstream effectors is critical for skeletal muscle fiber growth. Journal of Cell Biology 2000; 151:663-72.
11. Eley HL, Tisdale MJ Skeletal muscle atrophy, a link between depression of protein synthesis and increase in degradation. Journal of Biological Chemistry 2007; 282:7087-97.
12. English RF, Pophal SA, Bacanu S.A., Fricker J., Boyle GJ, Ellis D, et al Long-term comparison of tacrolimus- and cyclosporine-induced nephrotoxicity in pediatric heart-transplant recipients. American Journal of Transplantation 2002; 2:769-73.
13. Fiedler B, Wollert KC Targeting calcineurin and associated pathways in cardiac hypertrophy and failure. Expert Opinionon Therapeutic Targets 2005; 9:963-73.
14. Franch HA, Price SR Molecular signaling pathways regulating muscle proteolysis during atrophy. Current Opinion in Clinical Nutrition & Metabolic Care 2005; 8:271-5.
15. Friday BB, Horsley V, Pavlath GK. Calcineurin activity is required for the initiation of skeletal muscle differentiation. Journal of Cell Biology 2000; 149:657-66.
16. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. International Journal of Biochemistry & Cell Biology 2005; 37:1974-84.
17. Guerfali I, Manissolle C, Durieux A.C., Bonnefoy R., Bartegi A, Freyssenet D, et al CaMKIV transactivate PGC-1alpha promoter, but differentially regulate cytochrome c promoter in rat skeletal muscle. Pflugers Archiv 2007; 454:297-305.
18. Heisel O, Heisel R, Balshaw R., Keown P. New onset diabetes mellitus in patients receiving calcineurin inhibitors: a systematic review and meta-analysis. American Journal of Transplantation 2004; 4:583-95.
19. Horsley V, Friday BB, Matteson S, Kegley K.M., Gephart J., Pavlath GK Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. Journal of Cell Biology 2001; 153:329-38.
20. Horsley V, Jansen KM, Mills S.T., Pavlath GK IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 2003; 113:483-94.
21. 2+ control calcineurin-NFAT signaling and pathological hypertrophy in cardiac myocytes? Science Signaling 2008; 1:pe31.
22. Hudson MB, Smuder AJ, Nelson W.B., Bruells CS, Levine S, Powers SK Both high level pressure support ventilation and controlled mechanical ventilation induce diaphragm dysfunction and atrophy. Critical Care Medicine 2012; 40:1254-60.
23. Jackman RW, Kandarian SC The molecular basis of skeletal muscle atrophy. American Journal of Physiology Cell Physiology 2004; 287:C834-43.
24. Jiang LQ, Garcia-Roves PM, de Castro Barbosa T, Zierath JR. Constitutively active calcineurin in skeletal muscle increases endurance performance and mitochondrial respiratory capacity. American Journal of Physiology Endocrinology and Metabolism 2010; 298:E8-16.
25. Kegley KM, Gephart J, Warren G.L., Pavlath GK Altered primary myogenesis in NFATC3(-/-) mice leads to decreased muscle size in the adult. Developmental Biology 2001; 232:115-26.
26. Klee CB, Ren H, Wang X. Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. Journal of Biological Chemistry 1998; 273:13367-70.
27. Lara-Pezzi E., Winn N, Paul A., McCullagh K, Slominsky E, Santini M.P., et al A naturally occurring calcineurin variant inhibits FoxO activity and enhances skeletal muscle regeneration. Journal of Cell Biology 2007; 179:1205-18.
28. Lecker SH, Goldberg AL, Mitch WE Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. Journal of the American Society of Nephrology 2006; 17:1807-19.
29. Lecker SH, Jagoe RT, Gilbert A, Gomes M., Baracos V, Bailey J, et al Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEBJournal 2004; 18:39-51.
30. Lecker SH, Mitch WE Proteolysis by the ubiquitin-proteasome system and kidney disease. Journal of the American Society of Nephrology 2011; 22:821-4.
31. Li HH, Kedar V, Zhang C., McDonough H, Arya R, Wang D.Z., et al Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. Journal of Clinical Investigation 2004; 114:1058-71.
32. Lin J, Wu H, Tarr P.T., Zhang CY, Wu Z, Boss O, et al Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002; 418:797-801.
33. Lin Z, Murtaza I, Wang K., Jiao J, Gao J, Li PF miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proceedings of the National Academy of Sciences of the United States of America 2009; 106:12103-8.
34. Liu HB, Yang BF, Dong DL Calcineurin and electrical remodeling in pathologic cardiac hypertrophy. Trends in Cardiovascular Medicine 2010; 20:148-53.
35. Long YC, Glund S, Garcia-Roves PM, Zierath JR Calcineurin regulates skeletal muscle metabolism via coordinated changes in gene expression. Journal of Biological Chemistry 2007; 282:1607-14.
36. Mallinson J, Meissner J, Chang KC Calcineurin signaling and the slow oxidative skeletal muscle fiber type. International Review of Cell & Molecular Biology 2009; 277:67-101 [chapter 2].
37. Mammucari C, Milan G, Romanello V., Masiero E, Rudolf R, Del Piccolo P, et al FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metabolism 2007; 6:458-71.
38. Mancini M, Toker A. NFAT proteins: emerging roles in cancer progression. Nature Reviews Cancer 2009; 9:810-20.
39. Masuda S, Inui K. An up-date review on individualized dosage adjustment of calcineurin inhibitors in organ transplant patients. Pharmacology & Therapeutics 2006; 112:184-98.
40. McCarthy JJ, Esser KA, Peterson C.A., Dupont-Versteegden EE. Evidence of MyomiR network regulation of beta-myosin heavy chain gene expression during skeletal muscle atrophy. Physiological Genomics 2009; 39:219-26.
41. Mitchell PO, Mills ST, Pavlath GK Calcineurin differentially regulates maintenance and growth of phenotypically distinct muscles. American Journal of Physiology Cell Physiology 2002; 282:C984-92.
42. Mitchell PO, Pavlath GK Multiple roles of calcineurin in skeletal muscle growth. Clinical Orthopaedics and Related Research 2002(403 Suppl):S197-202.
43. Miyazaki M, Hitomi Y, Kizaki T., Ohno H, Katsumura T, Haga S., et al Calcineurin-mediated slow-type fiber expression and growth in reloading condition. Medicine & Science in Sports & Exercise 2006; 38:1065-72.
44. Molkentin JD. Calcineurin-NFAT signaling regulates the cardiac hypertrophic response in coordination with the MAPKs. Cardiovascular Research 2004; 63:467-75.
45. Mootha VK, Lindgren CM, Eriksson K.F., Subramanian A., Sihag S, Lehar J, et al PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nature Genetics 2003; 34:267-73.
46. Musaro A, McCullagh KJ, Naya F.J., Olson EN, Rosenthal N. IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 1999; 400:581-5.
47. Naya FJ, Mercer B, Shelton J., Richardson JA, Williams RS, Olson EN Stimulation of slow skeletal muscle fiber gene expression by calcineurin in vivo. Journal of Biological Chemistry 2000; 275:4545-8.
48. Ni YG, Berenji K, Wang N., Oh M, Sachan N, Dey A., et al Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation 2006; 114:1159-68.
49. Ni YG, Wang N, Cao D.J., Sachan N., Morris DJ, Gerard RD, et al FoxO transcription factors activate Akt and attenuate insulin signaling in heart by inhibiting protein phosphatases. Proceedings of the National Academy of Sciences of the United States of America 2007; 104:20517-22.
50. Oh M, Rybkin II, Copeland V, Czubryt MP, Shelton JM, van Rooij E, et al. Calcineurin is necessary forthe maintenance but not embryonic development of slow muscle fibers. Molecular and Cellular Biology 2005; 25:6629-38.
51. Oishi Y, Ogata T, Yamamoto K.I., Terada M, Ohira T, Ohira Y, et al. Cellular adaptations in soleus muscle during recovery after hindlimb unloading. Acta Physiologica (Oxford, England) 2008; 192:381-95.
52. Parsons SA, Millay DP, Wilkins B.J., Bueno OF, Tsika GL, Neilson JR, et al Genetic loss of calcineurin blocks mechanical overload-induced skeletal muscle fiber type switching but not hypertrophy. Journal of Biological Chemistry 2004; 279:26192-200.
53. Parsons SA, Wilkins BJ, Bueno O.F., Molkentin JD Altered skeletal muscle phenotypes in calcineurin Aalpha and Abeta gene-targeted mice. Molecular and Cellular Biology 2003; 23:4331-43.
54. Patti ME, Butte AJ, Crunkhorn S, Cusi K., Berria R, Kashyap S, et al Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proceedings of the National Academy of Sciences of the United States of America 2003; 100:8466-71.
55. Powers SK, Kavazis AN, DeRuisseau KC Mechanisms of disuse muscle atrophy: role of oxidative stress. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 2005; 288:R337-44.
56. Powers SK, Kavazis AN, McClung JM Oxidative stress and disuse muscle atrophy. Journal of Applied Physiology 2007; 102:2389-97.
57. Powers SK, Smuder AJ, Judge AR Oxidative stress and disuse muscle atrophy: cause or consequence. Current Opinion in Clinical Nutrition & Metabolic Care 2012; 15:240-5.
58. Price SR, Gooch JL, Donaldson S.K., Roberts-Wilson TK. Muscle atrophy in chronic kidney disease results from abnormalities in insulin signaling. Journal of Renal Nutrition 2010; 20:S24-8.
59. Quiat D, Olson EN MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment. Journal of Clinical Investigation 2013; 123:11-8.
60. Reed SA, Sandesara PB, Senf S.M., Judge AR Inhibition of FoxO transcriptional activity prevents muscle fiber atrophy during cachexia and induces hypertrophy. FASEB Journal 2012; 26:987-1000.
61. Roberts-Wilson T.K., Reddy RN, Bailey JL, Zheng B, Ordas R, Gooch JL, et al. Calcineurin signaling and PGC-1alpha expression are suppressed during muscle atrophy due to diabetes. Biochimicaet Biophysica Acta 2010; 1803:960-7.
62. Rusnak F, Mertz P. Calcineurin: form and function. Physiological Reviews 2000; 80:1483-521.
63. Sacheck JM, Hyatt JP, Raffaello A, Jagoe R.T., Roy RR, Edgerton VR, et al Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB Journal 2007; 21:140-55.
64. Sacheck JM, Ohtsuka A, McLary S.C., Goldberg AL IGF-I stimulates muscle growth by suppressing protein breakdown and expression of atrophy-related ubiquitin ligases,atrogin-1 and MuRF1. Endocrinology and Metabolism: American Journal of Physiology 2004; 287:E591-601.
65. Sakuma K, Akiho M, Nakashima H, Nakao R, Hirata M, Inashima S, et al. Cyclosporin A modulates cellular localization of MEF2C protein and blocks fiber hypertrophy in the overloaded soleus muscle of mice. Acta Neuropathologica 2008; 115:663-74.
66. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 2008; 23:160-70.
67. Sandri M, Lin J, Handschin C., Yang W, Arany ZP, Lecker SH, et al. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proceedings of the National Academy of Sciences of the United States of America 2006; 103:16260-5.
68. Sandri M, Sandri C, Gilbert A., Skurk C, Calabria E, Picard A., et al Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004; 117:399-412.
69. Schiaffino S, Dyar KA, Ciciliot S, Blaauw B., Sandri M. Mechanisms regulating skeletal muscle growth and atrophy. FEBS Journal 2013., http://dx.doi.org/10.1111/febs.12253 [Epub ahead of print].
70. Schiaffino S, Mammucari C. Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skeletal Muscle 2011; 1:4.
71. Schiaffino S, Sandri M, Murgia M. Activity-dependent signaling pathways controlling muscle diversity and plasticity. Physiology (Bethesda) 2007; 22:269-78.
72. Schiaffino S, Serrano A. Calcineurin signaling and neural control of skeletal muscle fiber type and size. Trends in Pharmacological Sciences 2002; 23:569-75.
73. 2+-dependent calcineurin signalling pathway. Nature 1999; 400:576-81.
74. *. Critical Care Medicine 2012; 40:927-34.
75. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. Journal of Physiology 2003; 551:33-48.
76. Stupka N, Plant DR, Schertzer J.D., Emerson TM, Bassel-Duby R, Olson EN, et al Activated calcineurin ameliorates contraction-induced injury to skeletal muscles of mdx dystrophic mice. Journal of Physiology 2006; 575:645-56.
77. Talmadge RJ, Otis JS, Rittler M.R., Garcia ND, Spencer SR, Lees SJ, et al Calcineurin activation influences muscle phenotype in a muscle-specific fashion. BMC Cell Biology 2004; 5:28.
78. Ventadour S, Attaix D. Mechanisms of skeletal muscle atrophy. Current Opinion in Rheumatology 2006; 18:631-5.
79. Wada S, Kato Y, Okutsu M., Miyaki S, Suzuki K, Yan Z., et al Translational suppression of atrophic regulators by microRNA-23a integrates resistance to skeletal muscle atrophy. Journal of Biological Chemistry 2011; 286:38456-65.
80. Wenz T, Rossi SG, Rotundo R.L., Spiegelman BM, Moraes CT Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proceedings of the National Academy of Sciences 2009; 106: 20405-10.
81. Whidden MA, Smuder AJ, Wu M, Hudson M.B., Nelson WB, Powers SK Oxidative stress is required for mechanical ventilation-induced protease activation in the diaphragm. Journal of Applied Physiology 2010; 108:1376-82.
82. Wilkins BJ, Molkentin JD Calcium-calcineurin signaling in the regulation of cardiac hypertrophy. Biochemical and Biophysical Research Communications 2004; 322:1178-91.
83. Williams CR, Gooch JL. Calcineurin inhibitors and immunosuppression - a tale of two isoforms. Expert Reviews in Molecular Medicine 2012; 14:e14.
84. Workeneh BT, Mitch WE Review of muscle wasting associated with chronic kidney disease. American Journal of Clinical Nutrition 2010; 91:1128S-32S.
85. Zhao J, Brault JJ, Schild A, Cao P., Sandri M, Schiaffino S, et al FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metabolism 2007; 6: 472-83.
86. Zheng B, Ohkawa S, Li H., Roberts-Wilson TK, Price SR FOXO3a mediates signaling crosstalk that coordinates ubiquitin and atrogin-1/MAFbx expression during glucocorticoid-induced skeletal muscle atrophy. FASEB Journal 2010; 24:2660-9. Kidney Diseases Kidney Diseases