Statin-associated myopathy and its exacerbation with exercise

Muscle and Nerve

Volumn 42, Issue 4, 2010, Pages 469-479

  Meador, Benjamin M ^a   Huey, Kimberly A ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b DRAKE UNIVERSITY   (United States)

Author keywords

Exercise; Myopathy; Physical activity; Skeletal muscle; Statins

Indexed keywords

3 HYDROXY 3 METHYLGLUTARYL COENZYME A; ATORVASTATIN; CASPASE 3; CASPASE 9; CERIVASTATIN; CHOLESTEROL; CREATINE KINASE; GLYCOGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MEVALONIC ACID; PROTEASOME; REACTIVE OXYGEN METABOLITE; SIMVASTATIN; SQUALENE SYNTHASE; TERPENOID; TUMOR NECROSIS FACTOR ALPHA; UBIQUINONE; UBIQUITIN;

APOPTOSIS; CELL MEMBRANE FLUIDITY; CHOLESTEROL SYNTHESIS; CREATINE KINASE BLOOD LEVEL; DISEASE EXACERBATION; DISEASE SEVERITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EXERCISE; EXERCISE INTENSITY; GLYCOGEN MUSCLE LEVEL; HUMAN; HYPERCHOLESTEROLEMIA; LOAD CARRYING CAPACITY; MUSCLE FIBER MEMBRANE; MUSCLE HYPERTROPHY; MUSCLE INJURY; MYOPATHY; NONHUMAN; PRENYLATION; PRIORITY JOURNAL; REVIEW; RHABDOMYOLYSIS; SIDE EFFECT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; BLOOD; METABOLISM; MUSCULAR DISEASES; PATHOPHYSIOLOGY; PHYSICAL EDUCATION; RISK ASSESSMENT; RISK FACTOR;

CREATINE KINASE; EXERCISE; GLYCOGEN; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; HYPERCHOLESTEROLEMIA; MUSCLE, SKELETAL; MUSCULAR DISEASES; PHYSICAL EDUCATION AND TRAINING; RISK ASSESSMENT; RISK FACTORS;

EID: 77957681638     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.21817     Document Type: Review

References (126)

1. Dirks AJ, Jones KM. Statin-induced apoptosis and skeletal myopathy. Am J Physiol 2006;291:C1208-1212.
2. Ford ES, Mokdad AH, Giles WH, Mensah GA. Serum total cholesterol concentrations and awareness, treatment, and control of hypercholesterolemia among US adults: findings from the National Health and Nutrition Examination Survey, 1999 to 2000. Circulation 2003;107:2185-2189.
3. Friday KE. Aggressive lipid management for cardiovascular prevention: evidence from clinical trials. Exp Biol Med 2003;228:769-778.
4. Mantel-Teeuwisse AK, Klungel OH, Schalekamp T, Verschuren WM, Porsius AJ, de Boer A. Suboptimal choices and dosing of statins at start of therapy. Br J Clin Pharmacol 2005;60:83-89. (Pubitemid 40942785)
5. Vaughan CJ, Gotto AM Jr. Update on statins: 2003. Circulation 2004;110:886-892.
6. Kashani A, Phillips CO, Foody JM, Wang Y, Mangalmurti S, Ko DT, et al. Risks associated with statin therapy: a systematic overview of randomized clinical trials. Circulation 2006;114:2788-2797.
7. Ucar M, Mjorndal T, Dahlqvist R. HMG-CoA reductase inhibitors and myotoxicity. Drug Safety 2000;22:441-457.
8. Omar MA, Wilson JP. FDA adverse event reports on statin-associated rhabdomyolysis. Ann Pharmacother 2002;36:288-295.
9. Bruckert E, Hayem G, Dejager S, Yau C, Begaud B. Mild to moderate muscular symptoms with high-dosage statin therapy in hyperlipidemic patients - the PRIMO study. Cardiovasc Drugs Ther 2005;19:403-414. (Pubitemid 43228152)
10. Cannon CP, Braunwald E, McCabe CH, Rader DJ, Rouleau JL, Belder R, et al. Intensive versus moderate lipid lowering with statins after acute coronary syndromes. N Engl J Med 2004;350:1495-1504. (Pubitemid 38477774)
11. Pasternak RC, Smith SC Jr, Bairey-Merz CN, Grundy SM, Cleeman JI, Lenfant C. ACC/AHA/NHLBI clinical advisory on the use and safety of statins. Stroke 2002;33:2337-2341. (Pubitemid 35014654)
12. Mascitelli L, Pezzetta F. Physical activity in statin-treated patients. Int J Cardiol 2009;134;136-137.
13. Tomlinson SS, Mangione KK. Potential adverse effects of statins on muscle. Phys Ther 2005;85:459-465.
14. Sinzinger H, Wolfram R, Peskar BA. Muscular side effects of statins. J Cardiovasc Pharmacol 2002;40:163-171.
15. Sinzinger H, O'Grady J. Professional athletes suffering from familial hypercholesterolaemia rarely tolerate statin treatment because of muscular problems. Br J Clin Pharmacol 2004;57:525-528.
16. Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults - the evidence report. Obesity Res 1998;6(suppl 2):51S-209S.
17. Hu FB, Willett WC, Li T, Stampfer MJ, Colditz GA, Manson JE. Adiposity as compared with physical activity in predicting mortality among women. N Engl J Med 2004;351:2694-2703. (Pubitemid 39665323)
18. Hu G, Tuomilehto J, Silventoinen K, Barengo NC, Peltonen M, Jousilahti P. The effects of physical activity and body mass index on cardiovascular, cancer and all-cause mortality among 47 212 middle-aged Finnish men and women. Int J Obesity 2005;29:894-902. (Pubitemid 41076228)
19. Meyer HE, Sogaard AJ, Tverdal A, Selmer RM. Body mass index and mortality: the influence of physical activity and smoking. Med Sci Sports Exerc 2002;34:1065-1070. (Pubitemid 34747404)
20. Sui X, LaMonte MJ, Laditka JN, Hardin JW, Chase N, Hooker SP, et al. Cardiorespiratory fitness and adiposity as mortality predictors in older adults. JAMA 2007;298:2507-2516. (Pubitemid 350223537)
21. Wei M, Kampert JB, Barlow CE, Nichaman MZ, Gibbons LW, Paffenbarger RS Jr, et al. Relationship between low cardiorespiratory fitness and mortality in normal-weight, overweight, and obese men. JAMA 1999;282:1547-1553.
22. Sewright KA, Clarkson PM, Thompson PD. Statin myopathy: incidence, risk factors, and pathophysiology. Curr Atheroscler Rep 2007;9:389-396.
23. Thompson PD, Clarkson P, Karas RH. Statin-associated myopathy. JAMA 2003;289:1681-1690.
24. Blanco-Colio LM, Villa A, Ortego M, Hernandez-Presa MA, Pascual A, Plaza JJ, et al. 3-Hydroxy-3-methyl-glutaryl coenzyme A reductase inhibitors, atorvastatin and simvastatin, induce apoptosis of vascular smooth muscle cells by downregulation of Bcl-2 expression and Rho A prenylation. Atherosclerosis 2002;161:17-26. (Pubitemid 34214817)
25. Boucher K, Siegel CS, Sharma P, Hauschka PV, Solomon KR. HMG-CoA reductase inhibitors induce apoptosis in pericytes. Microvasc Res 2006;71:91-102.
26. Cafforio P, Dammacco F, Gernone A, Silvestris F. Statins activate the mitochondrial pathway of apoptosis in human lymphoblasts and myeloma cells. Carcinogenesis 2005;26:883-891.
27. Erl W. Statin-induced vascular smooth muscle cell apoptosis: a possible role in the prevention of restenosis? Curr Drug Targets 2005; 5:135-144.
28. Fromigue O, Hay E, Modrowski D, Bouvet S, Jacquel A, Auberger P, et al. RhoA GTPase inactivation by statins induces osteosarcoma cell apoptosis by inhibiting p42/p44-MAPKs-Bcl-2 signaling independently of BMP-2 and cell differentiation. Cell Death Diff 2006; 13:1845-1856. (Pubitemid 44542398)
29. Graaf MR, Richel DJ, van Noorden CJ, Guchelaar HJ. Effects of statins and farnesyltransferase inhibitors on the development and progression of cancer. Cancer Treatment Rev 2004;30:609-641.
30. Guijarro C, Blanco-Colio LM, Ortego M, Alonso C, Ortiz A, Plaza JJ, et al. 3-Hydroxy-3-methylglutaryl coenzyme a reductase and isoprenylation inhibitors induce apoptosis of vascular smooth muscle cells in culture. Circ Res 1998;83:490-500. (Pubitemid 28411050)
31. Li X, Liu L, Tupper JC, Bannerman DD, Winn RK, Sebti SM, et al. Inhibition of protein geranylgeranylation and RhoA/RhoA kinase pathway induces apoptosis in human endothelial cells. J Biol Chem 2002;277:15309-15316. (Pubitemid 34967792)
32. Nagashima T, Okazaki H, Yudoh K, Matsuno H, Minota S. Apoptosis of rheumatoid synovial cells by statins through the blocking of protein geranylgeranylation: a potential therapeutic approach to rheumatoid arthritis. Arthritis Rheum 2006;54:579-586. (Pubitemid 43228634)
33. Zhong WB, Wang CY, Chang TC, Lee WS. Lovastatin induces apoptosis of anaplastic thyroid cancer cells via inhibition of protein geranylgeranylation and de novo protein synthesis. Endocrinology 2003;144:3852-3859.
34. Demyanets S, Kaun C, Pfaffenberger S, Hohensinner PJ, Rega G, Pammer J, et al. Hydroxymethylglutaryl-coenzyme A reductase inhibitors induce apoptosis in human cardiac myocytes in vitro. Biochem Pharmacol 2006;71:1324-1330.
35. Johnson TE, Zhang X, Bleicher KB, Dysart G, Loughlin AF, Schaefer WH, et al. Statins induce apoptosis in rat and human myotube cultures by inhibiting protein geranylgeranylation but not ubiquinone. Toxicol Appl Pharmacol 2004;200:237-250.
36. Matzno S, Yasuda S, Juman S, Yamamoto Y, Nagareya-Ishida N, Tazuya-Murayama K, et al. Statin-induced apoptosis linked with membrane farnesylated Ras small G protein depletion, rather than geranylated Rho protein. J Pharm Pharmacol 2005;57:1475-1484.
37. Mutoh T, Kumano T, Nakagawa H, Kuriyama M. Involvement of tyrosine phosphorylation in HMG-CoA reductase inhibitor-induced cell death in L6 myoblasts. FEBS Lett 1999;444:85-89.
38. Sacher J, Weigl L, Werner M, Szegedi C, Hohenegger M. Delineation of myotoxicity induced by 3-hydroxy-3-methylglutaryl CoA reductase inhibitors in human skeletal muscle cells. J Pharmacol Exp Ther 2005;314:1032-1041. (Pubitemid 41205966)
39. Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, et al. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 2004;113: 115-123. (Pubitemid 38541638)
40. McClung JM, Kavazis AN, DeRuisseau KC, Falk DJ, Deering MA, Lee Y, et al. Caspase-3 regulation of diaphragm myonuclear domain during mechanical ventilation-induced atrophy. Am J Respir Crit Care Med 2007;175:150-159.
41. Supinski GS, Callahan LA. Caspase activation contributes to endotoxin- induced diaphragm weakness. J Appl Physiol 2006;100: 1770-1777.
42. Lamperti C, Naini AB, Lucchini V, Prelle A, Bresolin N, Moggio M, et al. Muscle coenzyme Q10 level in statin-related myopathy. Arch Neurol 2005;62:1709-1712.
43. Seachrist JL, Loi CM, Evans MG, Criswell KA, Rothwell CE. Roles of exercise and pharmacokinetics in cerivastatin-induced skeletal muscle toxicity. Toxicol Sci 2005;88:551-561.
44. Schaefer WH, Lawrence JW, Loughlin AF, Stoffregen DA, Mixson LA, Dean DC, et al. Evaluation of ubiquinone concentration and mitochondrial function relative to cerivastatin-induced skeletal myopathy in rats. Toxicol Appl Pharmacol 2004;194:10-23.
45. Gharavi AG, Diamond JA, Smith DA, Phillips RA. Niacin-induced myopathy. Am J Cardiol 1994;74:841-842.
46. Langer T, Levy RI. Acute muscular syndrome associated with administration of clofibrate. N Engl J Med 1968;279:856-858.
47. Flint OP, Masters BA, Gregg RE, Durham SK. HMG CoA reductase inhibitor-induced myotoxicity: pravastatin and lovastatin inhibit the geranylgeranylation of low-molecular-weight proteins in neonatal rat muscle cell culture. Toxicol Appl Pharmacol 1997;145:99-110.
48. Matzno S, Yamauchi T, Gohda M, Ishida N, Katsuura K, Hanasaki Y, et al. Inhibition of cholesterol biosynthesis by squalene epoxidase inhibitor avoids apoptotic cell death in L6 myoblasts. J Lipid Res 1997;38:1639-1648.
49. Casey PJ, Seabra MC. Protein prenyltransferases. J Biol Chem 1996; 271:5289-5292.
50. Glomset JA, Farnsworth CC. Role of protein modification reactions in programming interactions between ras-related GTPases and cell membranes. Ann Rev Cell Biol 1994;10:181-205.
51. Hancock JF, Magee AI, Childs JE, Marshall CJ. All ras proteins are polyisoprenylated but only some are palmitoylated. Cell 1989;57: 1167-1177.
52. Willumsen BM, Christensen A, Hubbert NL, Papageorge AG, Lowy DR. The p21 ras C-terminus is required for transformation and membrane association. Nature 1984;310:583-586.
53. Kramer HF, Goodyear LJ. Exercise, MAPK, and NF-kappaB signaling in skeletal muscle. J Appl Physiol 2007;103:388-395.
54. Yamazaki H, Suzuki M, Aoki T, Morikawa S, Maejima T, Sato F, et al. Influence of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors on ubiquinone levels in rat skeletal muscle and heart: relationship to cytotoxicity and inhibitory activity for cholesterol synthesis in human skeletal muscle cells. J Atheroscler Thromb 2006;13:295-307.
55. Marcoff L, Thompson PD. The role of coenzyme Q10 in statin-associated myopathy: a systematic review. J Am Coll Cardiol 2007;49: 2231-2237. (Pubitemid 46856819)
56. Laaksonen R, Jokelainen K, Laakso J, Sahi T, Harkonen M, Tikkanen MJ, et al. The effect of simvastatin treatment on natural antioxidants in low-density lipoproteins and high-energy phosphates and ubiquinone in skeletal muscle. Am J Cardiol 1996;77:851-854. (Pubitemid 26143495)
57. Shimomura Y, Suzuki M, Sugiyama S, Hanaki Y, Ozawa T. Protective effect of coenzyme Q10 on exercise-induced muscular injury. Biochem Biophys Res Commun 1991;176:349-355.
58. Thompson PD, Clarkson PM, Rosenson RS. An assessment of statin safety by muscle experts. Am J Cardiol 2006;97:69C-76.
59. De Pinieux G, Chariot P, Ammi-Said M, Louarn F, Lejonc JL, Astier A, et al. Lipid-lowering drugs and mitochondrial function: effects of HMG-CoA reductase inhibitors on serum ubiquinone and blood lactate/pyruvate ratio. Br J Clin Pharmacol 1996;42:333-337.
60. Phillips PS, Haas RH, Bannykh S, Hathaway S, Gray NL, Kimura BJ, et al. Statin-associated myopathy with normal creatine kinase levels. Ann Intern Med 2002;137:581-585.
61. Kaufmann P, Torok M, Zahno A, Waldhauser KM, Brecht K, Krahenbuhl S. Toxicity of statins on rat skeletal muscle mitochondria. Cell Mol Life Sci 2006;63:2415-2425. (Pubitemid 44653050)
62. Smit JWA, Amelink GJ, de Bruin TWA, Bar DW, Erkelens DW. Increased human myoglobin and creatine kinase serum levels after standardized exercise during simvastatin treatment. Eur J Clin Invest 1990;A31.
63. Jaweed M, Glennon T, Dean M. Serum creatine kinase levels in response to combined lovastatin administration and exercise. Clin Res 1993;41:600A.
64. Reust CS, Curry SC, Guidry JR. Lovastatin use and muscle damage in healthy volunteers undergoing eccentric muscle exercise. West J Med 1991;154:198-200.
65. Thompson PD, Gadaleta PA, Yurgalevitch S, Cullinane E, Herbert PN. Effects of exercise and lovastatin on serum creatine kinase activity. Metab Clin Exp 1991;40:1333-1336.
66. Thompson PD, Zmuda JM, Domalik LJ, Zimet RJ, Staggers J, Guyton JR. Lovastatin increases exercise-induced skeletal muscle injury. Metab Clin Exp 1997;46:1206-1210. (Pubitemid 27418513)
67. Friden J, Sjostrom M, Ekblom B. Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 1983;4:170-176. (Pubitemid 13017794)
68. McCully KK, Faulkner JA. Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol 1985;59:119-126. (Pubitemid 15230302)
69. Kearns AK, Bilbie CL, Clarkson PM, White CM, Sewright KA, O'Fallon KS, et al. The creatine kinase response to eccentric exercise with atorvastatin 10 mg or 80 mg. Atherosclerosis 2008;200:121-125.
70. LaRosa JC, Grundy SM, Waters DD, Shear C, Barter P, Fruchart JC, et al. Intensive lipid lowering with atorvastatin in patients with stable coronary disease. N Engl J Med 2005;352:1425-1435.
71. Newman C, Tsai J, Szarek M, Luo D, Gibson E. Comparative safety of atorvastatin 80 mg versus 10 mg derived from analysis of 49 completed trials in 14,236 patients. Am J Cardiol 2006;97:61-67.
72. Kuipers H, Janssen E, Keizer H, Verstappen S. Serum CPK and amount of muscle damage in rats. Med Sci Sports Exerc 1985;17: 195.
73. Manfredi TG, Fielding RA, O'Reilly KP, Meredith CN, Lee HY, Evans WJ. Plasma creatine kinase activity and exercise-induced muscle damage in older men. Med Sci Sports Exerc 1991;23:1028-1034.
74. Newham DJ, McPhail G, Mills KR, Edwards RH. Ultrastructural changes after concentric and eccentric contractions of human muscle. J Neurol Sci 1983;61:109-122.
75. England JD, Walsh JC, Stewart P, Boyd I, Rohan A, Halmagyi GM. Mitochondrial myopathy developing on treatment with the HMG CoA reductase inhibitors - simvastatin and pravastatin. Austral NZ J Med 1995;25:374-375.
76. Masters BA, Palmoski MJ, Flint OP, Gregg RE, Wang-Iverson D, Durham SK. In vitro myotoxicity of the 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors, pravastatin, lovastatin, and simvastatin, using neonatal rat skeletal myocytes. Toxicol Appl Pharmacol 1995;131:163-174.
77. Sinzinger H, Schmid P, O'Grady J. Two different types of exercise-induced muscle pain without myopathy and CK-elevation during HMG-Co-enzyme-A-reductase inhibitor treatment. Atherosclerosis 1999;143:459-460. (Pubitemid 29166930)
78. Urso ML, Clarkson PM, Hittel D, Hoffman EP, Thompson PD. Changes in ubiquitin proteasome pathway gene expression in skeletal muscle with exercise and statins. Arterioscler Thromb Vasc Biol 2005;25:2560-2566. (Pubitemid 43732279)
79. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin- 1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 2001;98:14440-14445. (Pubitemid 33121410)
80. Hasselgren PO, Fischer JE. Muscle cachexia: current concepts of intracellular mechanisms and molecular regulation. Ann Surg 2001; 233:9-17. (Pubitemid 32042769)
81. Hunter RB, Stevenson E, Koncarevic A, Mitchell-Felton H, Essig DA, Kandarian SC. Activation of an alternative NF-kappaB pathway in skeletal muscle during disuse atrophy. FASEB J 2002;16:529-538.
82. Taillandier D, Aurousseau E, Meynial-Denis D, Bechet D, Ferrara M, Cottin P, et al. Coordinate activation of lysosomal, Ca2+-activated and ATP-ubiquitin-dependent proteinases in the unweighted rat soleus muscle. Biochem J 1996;316:65-72.
83. Waclawik AJ, Lindal S, Engel AG. Experimental lovastatin myopathy. J Neuropathol Exper Neurol 1993;52:542-549.
84. Westwood FR, Bigley A, Randall K, Marsden AM, Scott RC. Statin-induced muscle necrosis in the rat: distribution, development, and fibre selectivity. Toxicol Pathol 2005;33:246-257.
85. Smit JW, Bar PR, Geerdink RA, Erkelens DW. Heterozygous familial hypercholesterolaemia is associated with pathological exercise-induced leakage of muscle proteins, which is not aggravated by simvastatin therapy. Eur J Clin Invest 1995;25:79-84.
86. Smith PF, Eydelloth RS, Grossman SJ, Stubbs RJ, Schwartz MS, Germershausen JI, et al. HMG-CoA reductase inhibitor-induced myopathy in the rat: cyclosporine A interaction and mechanism studies. J Pharmacol Exper Ther 1991;257:1225-1235.
87. Gollnick PD, Piehl K, Saltin B. Selective glycogen depletion pattern in human muscle fibres after exercise of varying intensity and at varying pedalling rates. J Physiol 1974;241:45-57.
88. Perseghin G, Price TB, Petersen KF, Roden M, Cline GW, Gerow K, et al. Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N Engl J Med 1996;335:1357-1362.
89. Thorburn AW, Gumbiner B, Bulacan F, Brechtel G, Henry RR. Multiple defects in muscle glycogen synthase activity contribute to reduced glycogen synthesis in non-insulin dependent diabetes mellitus. J Clin Invest 1991;87:489-495.
90. Shek A, Ferrill MJ. Statin - fibrate combination therapy. Ann Pharmacother 2001;35:908-917.
91. Price TB, Perseghin G, Duleba A, Chen W, Chase J, Rothman DL, et al. NMR studies of muscle glycogen synthesis in insulin-resistant offspring of parents with non-insulin-dependent diabetes mellitus immediately after glycogen-depleting exercise. Proc Natl Acad Sci USA 1996;93:5329-5334.
92. Balnave CD, Thompson MW. Effect of training on eccentric exercise- induced muscle damage. J Appl Physiol 1993;75:1545-1551.
93. Brown SJ, Child RB, Day SH, Donnelly AE. Exercise-induced skeletal muscle damage and adaptation following repeated bouts of eccentric muscle contractions. J Sports Sci 1997;15:215-222.
94. Mair J, Mayr M, Muller E, Koller A, Haid C, Artner-Dworzak E, et al. Rapid adaptation to eccentric exercise - induced muscle damage. Int J Sports Med 1995;16:352-356.
95. Davies KJ, Packer L, Brooks GA. Biochemical adaptation of mitochondria, muscle, and whole-animal respiration to endurance training. Arch Biochem Biophys 1981;209:539-554.
96. Brooks GA. Exercise physiology: human bioenergetics and its applications. Mountain View, CA: Mayfield; 2000. 851 p.
97. Nishimura RN, Sharp FR. Heat shock proteins and neuromuscular disease. Muscle Nerve 2005;32:693-709. (Pubitemid 41746258)
98. Escobedo J, Pucci AM, Koh TJ. HSP25 protects skeletal muscle cells against oxidative stress. Free Rad Biol Med 2004;37:1455-1462. (Pubitemid 39349246)
99. Jiang B, Xiao W, Shi Y, Liu M, Xiao X. Heat shock pretreatment inhibited the release of Smac/DIABLO from mitochondria and apoptosis induced by hydrogen peroxide in cardiomyocytes and C2C12 myogenic cells. Cell Stress Chaperones 2005;10:252-262. (Pubitemid 41813372)
100. Koh TJ. Do small heat shock proteins protect skeletal muscle from injury? Exerc Sport Sci Rev 2002;30:117-121.
101. Koh TJ, Escobedo J. Cytoskeletal disruption and small heat shock protein translocation immediately after lengthening contractions. Am J Physiol Cell Physiol 2004;286:C713-722. (Pubitemid 38292678)
102. Liu Y, Steinacker JM. Changes in skeletal muscle heat shock proteins: pathological significance. Front Biosci 2001;6:D12-25.
103. Paulsen G, Vissing K, Kalhovde JM, Ugelstad I, Bayer ML, Kadi F, et al. Maximal eccentric exercise induces a rapid accumulation of small heat shock proteins on myofibrils and a delayed HSP70 response in humans. Am J Physiol Regul Integr Comp Physiol 2007; 293:R844-853. (Pubitemid 47205071)
104. Paulsen G, Lauritzen F, Bayer ML, Kalhovde JM, Ugelstad I, Owe SG, et al. Subcellular movement and expression of HSP27, alphaB-crystallin, and HSP70 after two bouts of eccentric exercise in humans. J Appl Physiol 2009;107:570-582.
105. Golenhofen N, Perng MD, Quinlan RA, Drenckhahn D. Comparison of the small heat shock proteins alphaB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle. Histochem Cell Biol 2004;122:415-425.
106. Huey KA, Thresher JS, Brophy CM, Roy RR. Inactivity-induced modulation of Hsp20 and Hsp25 content in rat hindlimb muscles. Muscle Nerve 2004;30:95-101.
107. Inaguma Y, Goto S, Shinohara H, Hasegawa K, Ohshima K, Kato K. Physiological and pathological changes in levels of the two small stress proteins, HSP27 and alpha B crystallin, in rat hindlimb muscles. J Biochem (Tokyo) 1993;114:378-384.
108. Locke M, Noble EG, Atkinson BG. Inducible isoform of HSP70 is constitutively expressed in a muscle fiber type specific pattern. Am J Physiol 1991;261:C774-779.
109. Ogata T, Oishi Y, Roy RR, Ohmori H. Endogenous expression and developmental changes of HSP72 in rat skeletal muscles. J Appl Physiol 2003;95:1279-1286. (Pubitemid 37034026)
110. Kretz A, Schmeer C, Tausch S, Isenmann S. Simvastatin promotes heat shock protein 27 expression and Akt activation in the rat retina and protects axotomized retinal ganglion cells in vivo. Neurobiol Dis 2006;21:421-430. (Pubitemid 43099865)
111. Wang X, Tokuda H, Hatakeyama D, Hirade K, Niwa M, Ito H, et al. Mechanism of simvastatin on induction of heat shock protein in osteoblasts. Arch Biochem Biophys 2003;415:6-13. (Pubitemid 36687911)
112. Ghayour-Mobarhan M, Lamb DJ, Vaidya N, Livingstone C, Wang T, Ferns GA. Heat shock protein antibody titers are reduced by statin therapy in dyslipidemic subjects: a pilot study. Angiology 2005;56:61-68.
113. Pirillo A, Jacoviello C, Longoni C, Radaelli A, Catapano AL. Simvastatin modulates the heat shock response and cytotoxicity mediated by oxidized LDL in cultured human endothelial smooth muscle cells. Biochem Biophys Res Commun 1997;231:437-441.
114. Shin YO, Bae JS, Lee JB, Kim JK, Kim YJ, Kim C, et al. Effect of cardiac rehabilitation and statin treatment on anti-HSP antibody titers in patients with coronary artery disease after percutaneous coronary intervention. Int Heart J 2006;47:671-682. (Pubitemid 44773221)
115. Arya R, Mallik M, Lakhotia SC. Heat shock genes - integrating cell survival and death. J Biosci 2007;32:595-610. (Pubitemid 46708710)
116. Beere HM. Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J Clin Invest 2005;115:2633-2639.
117. Garrido C, Brunet M, Didelot C, Zermati Y, Schmitt E, Kroemer G. Heat shock proteins 27 and 70: anti-apoptotic proteins with tumorigenic properties. Cell Cycle 2006;5:2592-2601. (Pubitemid 44785803)
118. Akbar MT, Lundberg AM, Liu K, Vidyadaran S, Wells KE, Dolatshad H, et al. The neuroprotective effects of heat shock protein 27 overexpression in transgenic animals against kainate-induced seizures and hippocampal cell death. J Biol Chem 2003;278:19956-19965.
119. Huey KA, Roy RR, Zhong H, Lullo C. Time-dependent changes in caspase-3 activity and heat shock protein 25 after spinal cord transection in adult rats. Exp Physiol 2008;93:415-425.
120. Lee HJ, Lee YJ, Kwon HC, Bae S, Kim SH, Min JJ, et al. Radioprotective effect of heat shock protein 25 on submandibular glands of rats. Am J Pathol 2006;169:1601-1611. (Pubitemid 351181992)
121. Huey KA. Regulation of Hsp25 expression and phosphorylation in functionally overloaded rat plantaris and soleus muscles. J Appl Physiol 2006;100:451-456.
122. Huey KA, McCall GE, Zhong H, Roy RR. Modulation of HSP25 and TNF-α during the early stages of functional overload of a rat slow and fast muscle. J Appl Physiol 2007;102:2307-2314. (Pubitemid 47080765)
123. Huey KA, Meador BM. Contribution of IL-6 to the Hsp72, Hsp25, and alphaB-crystallin [corrected] responses to inflammation and exercise training in mouse skeletal and cardiac muscle. J Appl Physiol 2008;105:1830-1836.
124. Beyer RE, Morales-Corral PG, Ramp BJ, Kreitman KR, Falzon MJ, Rhee SY, et al. Elevation of tissue coenzyme Q (ubiquinone) and cytochrome c concentrations by endurance exercise in the rat. Arch Biochem Biophys 1984;234:323-329.
125. Gohil K, Rothfuss L, Lang J, Packer L. Effect of exercise training on tissue vitamin E and ubiquinone content. J Appl Physiol 1987; 63:1638-1641. (Pubitemid 18024208)
126. Karlsson J, Lin L, Sylven C, Jansson E. Muscle ubiquinone in healthy physically active males. Mol Cell Biochem 1996;156:169-172. (Pubitemid 26108899)