Structural and functional characterization of simvastatin-induced myotoxicity in different skeletal muscles

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 1, 2014, Pages 406-415

  Simsek Ozek, Nihal ^a,b   Bal, I Burak ^c   Sara, Yildirim ^c   Onur, Rustu ^c   Severcan, Feride ^a  

^a MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^b ATATÜRK UNIVERSITY   (Turkey)

^c HACETTEPE UNIVERSITY   (Turkey)

Author keywords

Contractility; Diaphragm; Extensor digitorum longus; Fourier Transform Infrared spectroscopy; Soleus; Statin

Indexed keywords

GLYCOGEN; ION CHANNEL; LIPID; MUSCLE PROTEIN; NUCLEIC ACID; SIMVASTATIN;

ALPHA HELIX; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENUATED TOTAL REFLECTANCE FOURIER TRANSFORM INFRARED SPECTROSCOPY; BETA SHEET; CELL MEMBRANE; CHEMICAL STRUCTURE; CONTROLLED STUDY; DIAPHRAGM; EXTENSOR DIGITORUM LONGUS MUSCLE; FAST MUSCLE; INFRARED SPECTROSCOPY; MALE; MEASUREMENT; MEMBRANE CHANNEL; MIXED TWITCH MUSCLE; MUSCLE; MUSCLE CONTRACTILITY; MUSCLE CONTRACTION; MUSCLE FUNCTION; MUSCLE STRENGTH; MUSCLE STRUCTURE; MUSCLE TISSUE; MYOTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DENATURATION; RAT; SKELETAL MUSCLE; SLOW MUSCLE; SOLEUS MUSCLE; SPECTROMETER; SPECTROSCOPY; TOXICITY;

RATTUS;

ATR-FTIR; ATTENUATED TOTAL REFLECTANCE FOURIER TRANSFORM INFRARED SPECTROSCOPY; CONTRACTILITY; DIA; DIAPHRAGM; EDL; EXTENSOR DIGITORUM LONGUS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; FTIR; SOL; SOLEUS; STATIN;

ANIMALS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; ION CHANNELS; MALE; MUSCLE CONTRACTION; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MUSCULAR DISEASES; RATS; RATS, WISTAR; SIMVASTATIN; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84885333598     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.09.010     Document Type: Article

References (63)

1. M. Evans, and A. Rees Effects of HMG-CoA reductase inhibitors on skeletal muscle - are all statins the same? Drug Saf. 25 2002 649 663
2. M. Fukami, N. Maeda, J. Fukushige, Y. Kogure, Y. Shimada, T. Ogawa, and Y. Tsujita Effects of HMG-CoA reductase inhibitors on skeletal muscles of rabbits Res. Exp. Med. (Berl) 193 1993 263 273 (Pubitemid 23319581)
3. S. Guis, D. Figarella-Branger, J.P. Mattei, F. Nicoli, Y. Le Fur, G. Kozak-Ribbens, J.F. Pellissier, P.J. Cozzone, N. Amabile, and D. Bendahan In vivo and in vitro characterization of skeletal muscle metabolism in patients with statin-induced adverse effects Arthritis Rheum. 55 2006 551 557 (Pubitemid 44289873)
4. P. Kaufmann, M. Torok, A. Zahno, K.M. Waldhauser, K. Brecht, and S. Krahenbuhl Toxicity of statins on rat skeletal muscle mitochondria Cell. Mol. Life Sci. 63 2006 2415 2425 (Pubitemid 44653050)
5. B.A. Hamelin, and J. Turgeon Hydrophilicity/lipophilicity: relevance for the pharmacology and clinical effects of HMG-CoA reductase inhibitors Trends Pharmacol. Sci. 19 1998 26 37 (Pubitemid 28094090)
6. Y. Levy, R. Leibowitz, M. Aviram, J.G. Brook, and U. Cogan Reduction of plasma cholesterol by lovastatin normalizes erythrocyte membrane fluidity in patients with severe hypercholesterolemia Br. J. Clin. Pharmacol. 34 1992 427 430
7. I. Morita, I. Sato, L. Ma, and S. Murota Enhancement of membrane fluidity in cholesterol-poor endothelial cells pre-treated with simvastatin Endothelium 5 1997 107 113 (Pubitemid 27273679)
8. S. Pierno, A. De Luca, D. Tricarico, A. Roselli, F. Natuzzi, E. Ferrannini, M. Laico, and D.C. Camerino Potential risk of myopathy by HMG-CoA reductase inhibitors: a comparison of pravastatin and simvastatin effects on membrane electrical properties of rat skeletal muscle fibers J. Pharmacol. Exp. Ther. 275 1995 1490 1496 (Pubitemid 26129941)
9. E.G. Bliznakov, and D.J. Wilkins Biochemical and clinical consequences of inhibiting coenzyme Q(10) biosynthesis by lipid-lowering HMG-CoA reductase inhibitors (statins): a critical overview Adv. Ther. 15 1998 218 228 (Pubitemid 28454901)
10. C. Guijarro, L.M. Blanco-Colio, M. Ortego, C. Alonso, A. Ortiz, J.J. Plaza, C. Diaz, G. Hernandez, and J. Egido 3-Hydroxy-3-methylglutaryl coenzyme a reductase and isoprenylation inhibitors induce apoptosis of vascular smooth muscle cells in culture Circ. Res. 83 1998 490 500 (Pubitemid 28411050)
11. N.S. Ozek, Y. Sara, R. Onur, and F. Severcan Low dose simvastatin induces compositional, structural and dynamic changes in rat skeletal extensor digitorum longus muscle tissue Biosci. Rep. 30 2010 41 50
12. F.R. Westwood, A. Bigley, K. Randall, A.M. Marsden, and R.C. Scott Statin-induced muscle necrosis in the rat: distribution, development, and fibre selectivity Toxicol. Pathol. 33 2005 246 257 (Pubitemid 40381453)
13. H. Obayashi, Y. Nezu, H. Yokota, N. Kiyosawa, K. Mori, N. Maeda, Y. Tani, S. Manabe, and A. Sanbuissho Cerivastatin induces type-I fiber-, not type-II fiber-, predominant muscular toxicity in the young male F344 rats J. Toxicol. Sci. 36 2011 445 452
14. F. Severcan, and P. Haris Vibrational Spectroscopy in Diagnosis and Screening First edition 2012 IOS Press UK
15. G. Cakmak, F. Zorlu, M. Severcan, and F. Severcan Screening of protective effect of amifostine on radiation-induced structural and functional variations in rat liver microsomal membranes by FT-IR spectroscopy Anal. Chem. 83 2011 2438 2444
16. L.N. Johnson-Anuna, G.P. Eckert, J.H. Keller, U. Igbavboa, C. Franke, T. Fechner, M. Schubert-Zsilavecz, M. Karas, W.E. Muller, and W.G. Wood Chronic administration of statins alters multiple gene expression patterns in mouse cerebral cortex J. Pharmacol. Exp. Ther. 312 2005 786 793 (Pubitemid 40189580)
17. Ö. Yilmaz, S. Keser, M. Tuzcu, and B. Çetintas Resveratrol (trans-3,4′,5-trihydroxystilbene) decreases lipid peroxidation level and protects antioxidant capacity in sera and erythrocytes of old female Wistar rats induced by the kidney carcinogen potassium bromate Environ. Toxicol. Pharmacol. 24 2007 79 85 (Pubitemid 47088334)
18. M. Nara, M. Okazaki, and H. Kagi Infrared study of human serum very-low-density and low-density lipoproteins. Implication of esterified lipid CO stretching bands for characterizing lipoproteins Chem. Phys. Lipids 117 2002 1 6 (Pubitemid 35007263)
19. P. Lasch, W. Haensch, D. Naumann, and M. Diem Imaging of colorectal adenocarcinoma using FT-IR microspectroscopy and cluster analysis Biochim. Biophys. Acta 1688 2004 176 186 (Pubitemid 38264412)
20. F. Severcan, O. Bozkurt, R. Gurbanov, and G. Gorgulu FT-IR spectroscopy in diagnosis of diabetes in rat animal model J. Biophotonics 3 2010 621 631
21. F. Draux, P. Jeannesson, C. Gobinet, J. Sule-Suso, J. Pijanka, C. Sandt, P. Dumas, M. Manfait, and G.D. Sockalingum IR spectroscopy reveals effect of non-cytotoxic doses of anti-tumour drug on cancer cells Anal. Bioanal. Chem. 395 2009 293 301
22. T.N. Patel, M.H. Shishehbor, and D.L. Bhatt A review of high-dose statin therapy: targeting cholesterol and inflammation in atherosclerosis Eur. Heart J. 28 2007 664 672 (Pubitemid 46439226)
23. T. Prueksaritanont, R. Subramanian, X. Fang, B. Ma, Y. Lin, J.H. Qiu, P.G. Pearson, and T.A. Baillie Glucuronidation of statins in animals and humans: a novel mechanism of statin lactonization Drug Metab. Dispos. 30 2002 505 512 (Pubitemid 34456970)
24. M. Boberg, R. Angerbauer, W.K. Kanhai, W. Karl, A. Kern, M. Radtke, and W. Steinke Biotransformation of cerivastatin in mice, rats, and dogs in vivo Drug Metab. Dispos. 26 1998 640 652 (Pubitemid 28345847)
25. T. Komai, K. Kawai, T. Tokui, Y. Tokui, C. Kuroiwa, E. Shigehara, and M. Tanaka Disposition and metabolism of pravastatin sodium in rats, dogs and monkeys Eur. J. Drug Metab. Pharmacokinet. 17 1992 103 113
26. W.E. Stehbens An appraisal of cholesterol feeding in experimental atherogenesis Prog. Cardiovasc. Dis. 29 1986 107 128 (Pubitemid 16003136)
27. N. Cartier, S. Guidoux, F. Rocchiccioli, and P. Aubourg Simvastatin does not normalize very long chain fatty acids in adrenoleukodystrophy mice FEBS Lett. 478 2000 205 208 (Pubitemid 30621618)
28. S. Youssef, O. Stuve, J.C. Patarroyo, P.J. Ruiz, J.L. Radosevich, E.M. Hur, M. Bravo, D.J. Mitchell, R.A. Sobel, L. Steinman, and S.S. Zamvil The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease Nature 420 2002 78 84 (Pubitemid 35291443)
29. R.E. Keesey, and T.L. Powley The regulation of body weight Annu. Rev. Psychol. 37 1986 109 133
30. G.A. Nader Molecular determinants of skeletal muscle mass: getting the "AKT" together Int. J. Biochem. Cell Biol. 37 2005 1985 1996 (Pubitemid 41206816)
31. M.D. Gomes, S.H. Lecker, R.T. Jagoe, A. Navon, and A.L. Goldberg Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy Proc. Natl. Acad. Sci. U. S. A. 98 2001 14440 14445 (Pubitemid 33121410)
32. M.L. Urso, P.M. Clarkson, D. Hittel, E.P. Hoffman, and P.D. Thompson Changes in ubiquitin proteasome pathway gene expression in skeletal muscle with exercise and statins Arterioscler. Thromb. Vasc. Biol. 25 2005 2560 2566 (Pubitemid 43732279)
33. J.I. Hanai, P. Cao, P. Tanksale, S. Imamura, E. Koshimizu, J. Zhao, S. Kishi, M. Yamashita, P.S. Phillips, V.P. Sukhatme, and S.H. Lecker The muscle-specific ubiquitin ligase atrogin-1/MAFbx mediates statin-induced muscle toxicity J. Clin. Invest. 117 2007 3940 3951 (Pubitemid 350224103)
34. C. Franzini-Armstrong, and F. Protasi Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions Physiol. Rev. 77 1997 699 729 (Pubitemid 27328738)
35. 2 + J. Membr. Biol. 159 1997 179 185 (Pubitemid 27438105)
36. K. Motojima, P. Passilly, J.M. Peters, F.J. Gonzalez, and N. Latruffe Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor alpha and gamma activators in a tissue- and inducer-specific manner J. Biol. Chem. 273 1998 16710 16714 (Pubitemid 28311694)
37. G.M. Camerino, M.A. Pellegrino, L. Brocca, C. Digennaro, D.C. Camerino, S. Pierno, and R. Bottinelli Statin or fibrate chronic treatment modifies the proteomic profile of rat skeletal muscle Biochem. Pharmacol. 81 2011 1054 1064
38. V. Barone, F. Bertocchini, R. Bottinelli, F. Protasi, P.D. Allen, C. Franzini Armstrong, C. Reggiani, and V. Sorrentino Contractile impairment and structural alterations of skeletal muscles from knockout mice lacking type 1 and type 3 ryanodine receptors FEBS Lett. 422 1998 160 164 (Pubitemid 28064533)
39. B.A. Schick, R. Laaksonen, J.J. Frohlich, H. Paiva, T. Lehtimaki, K.H. Humphries, and H.C. Cote Decreased skeletal muscle mitochondrial DNA in patients treated with high-dose simvastatin Clin. Pharmacol. Ther. 81 2007 650 653 (Pubitemid 46625111)
40. P.I. Haris, and F. Severcan FTIR spectroscopic characterization of protein structure in aqueous and non-aqueous media J. Mol. Catal. B. Enzym. 7 1999 207 221 (Pubitemid 29408531)
41. H. Yamazaki, M. Suzuki, T. Aoki, S. Morikawa, T. Maejima, F. Sato, K. Sawanobori, M. Kitahara, T. Kodama, and Y. Saito 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. 13 2006 295 307
42. S.K. Baker, and M.A. Tarnopolsky Statin myopathies: pathophysiologic and clinical perspectives Clin. Invest. Med. 24 2001 258 272 (Pubitemid 33097304)
43. R.H. Sills, D.J. Moore, and R. Mendelsoh Erythrocyte peroxidation: quantitation by Fourier transform infrared spectroscopy Anal. Biochem. 218 1994 118 123 (Pubitemid 24124755)
44. F. Severcan, I. Sahin, and N. Kazanci Melatonin strongly interacts with zwitterionic model membranes - evidence from Fourier transform infrared spectroscopy and differential scanning calorimetry Biochim. Biophys. Acta 668 2005 215 222 (Pubitemid 40298925)
45. F. Severcan, and S. Cannistraro Model membrane partition ESR study in the presence of α-tocopherol by a new spin probe Biosci. Rep. 9 1989 489 495
46. M. Kocak, and F. Severcan Interactions of cholesterol reducing agent simvastatin with neutral DPPC and DMPC multilamellar liposomes Biophysical Society Meeting Abstracts Supplement Biophys. J. 2007 59a
47. B. Szalontai, Y. Nishiyama, Z. Gombos, and N. Murata Membrane dynamics as seen by Fourier transform infrared spectroscopy in a cyanobacterium, Synechocystis PCC 6803. The effects of lipid unsaturation and the protein-to-lipid ratio Biochim. Biophys. Acta 1509 2000 409 419
48. M.S. Awayda, W. Shao, F. Guo, M. Zeidel, and W.G. Hill ENaC-membrane interactions: regulation of channel activity by membrane order J. Gen. Physiol. 123 2004 709 727 (Pubitemid 38781376)
49. R. Kinder, C. Ziegler, and J.M. Wessels Gamma-irradiation and UV-C light-induced lipid peroxidation: a Fourier transform-infrared absorption spectroscopic study Int. J. Radiat. Biol. 71 1997 561 571 (Pubitemid 27229753)
50. P. Sirvent, J. Mercier, and A. Lacampagne New insights into mechanisms of statin-associated myotoxicity Curr. Opin. Pharmacol. 8 2008 333 338
51. S. Pierno, A. De Luca, A. Liantonio, C. Camerino, and D. Conte Camerin Effects of HMG-CoA reductase inhibitors on excitation-contraction coupling of rat skeletal muscle Eur. J. Pharmacol. 364 1999 43 48 (Pubitemid 29015785)
52. S. Pierno, M.P. Didonna, V. Cippone, A. De Luca, M. Pisoni, A. Frigeri, G.P. Nicchia, M. Svelto, G. Chiesa, C. Sirtori, E. Scanziani, C. Rizzo, D. De Vito, and D. Conte Camerino Effects of chronic treatment with statins and fenofibrate on rat skeletal muscle: a biochemical, histological and electrophysiological study Br. J. Pharmacol. 149 2006 909 919 (Pubitemid 44851715)
53. A.G. Lee Lipids and their effects on membrane proteins: evidence against a role for fluidity Prog. Lipid Res. 30 1991 323 348 (Pubitemid 121003881)
54. A. Carruthers, and D.L. Melchior How bilayer lipids affect membrane protein activity Trends Biochem. Sci. 11 1986 331 335
55. K. Turnheim, J. Gruber, C. Wachter, and V. Ruiz-Gutierrez Membrane phospholipid composition affects function of potassium channels from rabbit colon epithelium Am. J. Physiol. 277 1999 C83 C90
56. A.M. Kleinfeld Current views of membrane structure Curr. Top. Membr. Transp. 29 1987 1 27
57. P.S. Phillips, and R.H. Haas Statin myopathy as a metabolic muscle disease Expert. Rev. Cardiovasc. Ther. 6 2008 971 978
58. D.E. Goll, M.H. Stromer, and R.M. Robson Skeletal muscle, nervous system, temperature regulation and special senses M.J. Swenson, Duke's Physiology of Domestic Animals 1977 Cornell University Press New York 504 530
59. M.R. Bonfim, J.C.S. Camargo Filho, L.C.M. Vanderlei, Padulla, M.F. Accioly, R.S.D. Souza, and R. Azoubel Muscle response to the association of statin and physical exercise in rats Int. J. Morphol. 27 2009 1155 1161
60. S. Larsen, N. Stride, M. Hey-Mogensen, C.N. Hansen, L.E. Bang, H. Bundgaard, L.B. Nielsen, J.W. Helge, and F. Dela Simvastatin effects on skeletal muscle: relation to decreased mitochondrial function and glucose intolerance J. Am. Coll. Cardiol. 61 2013 44 53
61. E. Ponsot, J. Zoll, B. N'Guessan, F. Ribera, E. Lampert, R. Richard, V. Veksler, R. Ventura-Clapier, and B. Mettauer J. Cell. Physiol. 203 2005 479 486
62. J. Lin, H. Wu, P.T. Tarr, C. Zhang, Z. Wu, O. Boss, L.F. Michael, P. Puigserver, E. Isotani, E.N. Olson, B.B. Lowell, R. Bassel-Duby, and B.M. Spiegelman Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres Nature 418 2002 797 801
63. K. Nakahara, M. Kuriyama, Y. Sonoda, H. Yoshidome, H. Nakagawa, J. Fujiyama, I. Higuchi, M. Osame,Myopathy induced by HMG-CoA reductase inhibitors in rabbits: a pathological, electrophysiological, and biochemical study, Toxicol. Appl. Pharmacol. 152 (1998) 99106. (Pubitemid 28498678)