Statin-induced myopathy is associated with mitochondrial complex III inhibition

Cell Metabolism

Volumn 22, Issue 3, 2015, Pages 399-407

  Schirris, Tom J J ^a   Renkema, G Herma ^a   Ritschel, Tina ^a   Voermans, Nicol C ^a   Bilos, Albert ^a   Van Engelen, Baziel G M ^a   Brandt, Ulrich ^a   Koopman, Werner J H ^a   Beyrath, Julien D ^a   Rodenburg, Richard J ^a   Willems, Peter H G M ^a   Smeitink, Jan A M ^a   Russel, Frans G M ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ATORVASTATIN; CERIVASTATIN; CYTOCHROME C; CYTOCHROME C1; FLUINDOSTATIN; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LACTONE; MEVINOLIN; PITAVASTATIN; SIMVASTATIN; UBIQUINOL CYTOCHROME C REDUCTASE; UBIQUINONE;

ANIMAL CELL; APOPTOSIS; ARTICLE; BASAL METABOLIC RATE; CELL RESPIRATION; CLINICAL ARTICLE; CONCENTRATION AT STEADY-STATE; CONTROLLED STUDY; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; FATTY ACID TRANSPORT; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LIPOPHILICITY; LONG TERM EXPOSURE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MUSCLE BIOPSY; MUSCLE TISSUE; MUSCLE WEAKNESS; MYOBLAST; MYOPATHY; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN PRENYLATION; RESPIRATION DEPRESSION; RHABDOMYOLYSIS; SKIN FIBROBLAST; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CELL LINE; CHEMICAL STRUCTURE; CHEMICALLY INDUCED; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; METABOLISM; MITOCHONDRION; MOUSE; MUSCLE; MUSCLE DISEASE; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL LINE; CELL RESPIRATION; CELLS, CULTURED; ELECTRON TRANSPORT COMPLEX III; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; LACTONES; MICE; MITOCHONDRIA; MODELS, MOLECULAR; MUSCLES; MUSCULAR DISEASES; MYOBLASTS;

EID: 84940667098     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2015.08.002     Document Type: Article

References (41)

1. T.T. Abd, and T.A. Jacobson Statin-induced myopathy: a review and update Expert Opin. Drug Saf. 10 2011 373 387
2. A. Alfirevic, D. Neely, J. Armitage, H. Chinoy, R.G. Cooper, R. Laaksonen, D.F. Carr, K.M. Bloch, J. Fahy, A. Hanson, and et al. Phenotype standardization for statin-induced myotoxicity Clin. Pharmacol. Ther. 96 2014 470 476
3. A. Arduini, A. Peschechera, F. Giannessi, and P. Carminati Improvement of statin-associated myotoxicity by L-carnitine J. Thromb. Haemost. 2 2004 2270 2271
4. J. Armitage The safety of statins in clinical practice Lancet 370 2007 1781 1790
5. K.D. Ballard, and P.D. Thompson Does reduced creatine synthesis protect against statin myopathy? Cell Metab. 18 2013 773 774
6. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The Protein Data Bank Nucleic Acids Res. 28 2000 235 242
7. U. Brandt, and B. Trumpower The protonmotive Q cycle in mitochondria and bacteria Crit. Rev. Biochem. Mol. Biol. 29 1994 165 197
8. U. Brandt, H. Schägger, and G. von Jagow Characterisation of binding of the methoxyacrylate inhibitors to mitochondrial cytochrome c reductase Eur. J. Biochem. 173 1988 499 506
9. P.J. Crowley, E.A. Berry, T. Cromartie, F. Daldal, C.R. Godfrey, D.W. Lee, J.E. Phillips, A. Taylor, and R. Viner The role of molecular modeling in the design of analogues of the fungicidal natural products crocacins A and D Bioorg. Med. Chem. 16 2008 10345 10355
10. J.J. DiNicolantonio CoQ10 and L-carnitine for statin myalgia? Expert Rev. Cardiovasc. Ther. 10 2012 1329 1333
11. J.S. Floyd, J.C. Bis, J.A. Brody, S.R. Heckbert, K. Rice, and B.M. Psaty GATM locus does not replicate in rhabdomyolysis study Nature 513 2014 E1 E3
12. C.D. Furberg, and B. Pitt Withdrawal of cerivastatin from the world market Curr. Control. Trials Cardiovasc. Med. 2 2001 205 207
13. E. Gnaiger Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology Int. J. Biochem. Cell Biol. 41 2009 1837 1845
14. J. 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
15. K.B. Hoffman, C. Kraus, M. Dimbil, and B.A. Golomb A survey of the FDA's AERS database regarding muscle and tendon adverse events linked to the statin drug class PLoS ONE 7 2012 e42866
16. J. Hur, Z. Liu, W. Tong, R. Laaksonen, and J.P. Bai Drug-induced rhabdomyolysis: from systems pharmacology analysis to biochemical flux Chem. Res. Toxicol. 27 2014 421 432
17. A.J. Janssen, F.J. Trijbels, R.C. Sengers, L.T. Wintjes, W. Ruitenbeek, J.A. Smeitink, E. Morava, B.G. van Engelen, L.P. van den Heuvel, and R.J. Rodenburg Measurement of the energy-generating capacity of human muscle mitochondria: diagnostic procedure and application to human pathology Clin. Chem. 52 2006 860 871
18. A.J. Janssen, F.J. Trijbels, R.C. Sengers, J.A. Smeitink, L.P. van den Heuvel, L.T. Wintjes, B.J. Stoltenborg-Hogenkamp, and R.J. Rodenburg Spectrophotometric assay for complex I of the respiratory chain in tissue samples and cultured fibroblasts Clin. Chem. 53 2007 729 734
19. A.V. Kuznetsov, V. Veksler, F.N. Gellerich, V. Saks, R. Margreiter, and W.S. Kunz Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells Nat. Protoc. 3 2008 965 976
20. E. Link, S. Parish, J. Armitage, L. Bowman, S. Heath, F. Matsuda, I. Gut, M. Lathrop, R. Collins SEARCH Collaborative Group SLCO1B1 variants and statin-induced myopathy - a genomewide study N. Engl. J. Med. 359 2008 789 799
21. J.A. Luzum, J.P. Kitzmiller, P.J. Isackson, C. Ma, M.W. Medina, A.M. Dauki, E.B. Mikulik, H.M. Ochs-Balcom, and G.D. Vladutiu GATM polymorphism associated with the risk for statin-induced myopathy does not replicate in case-control analysis of 715 dyslipidemic individuals Cell Metab. 21 2015 622 627
22. L.M. Mangravite, B.E. Engelhardt, M.W. Medina, J.D. Smith, C.D. Brown, D.I. Chasman, B.H. Mecham, B. Howie, H. Shim, D. Naidoo, and et al. A statin-dependent QTL for GATM expression is associated with statin-induced myopathy Nature 502 2013 377 380
23. L. Marcoff, and P.D. Thompson The role of coenzyme Q10 in statin-associated myopathy: a systematic review J. Am. Coll. Cardiol. 49 2007 2231 2237
24. J. Mourmans, U. Wendel, H.A. Bentlage, J.M. Trijbels, J.A. Smeitink, I.F. de Coo, F.J. Gabreëls, R.C. Sengers, and W. Ruitenbeek Clinical heterogeneity in respiratory chain complex III deficiency in childhood J. Neurol. Sci. 149 1997 111 117
25. P.J. Mullen, B. Lüscher, H. Scharnagl, S. Krähenbühl, and K. Brecht Effect of simvastatin on cholesterol metabolism in C2C12 myotubes and HepG2 cells, and consequences for statin-induced myopathy Biochem. Pharmacol. 79 2010 1200 1209
26. P.J. Mullen, A. Zahno, P. Lindinger, S. Maseneni, A. Felser, S. Krähenbühl, and K. Brecht Susceptibility to simvastatin-induced toxicity is partly determined by mitochondrial respiration and phosphorylation state of Akt Biochim. Biophys. Acta 1813 2011 2079 2087
27. M. Needham, and F.L. Mastaglia Statin myotoxicity: a review of genetic susceptibility factors Neuromuscul. Disord. 24 2014 4 15
28. B.A. Parker, J.A. Capizzi, A.S. Grimaldi, P.M. Clarkson, S.M. Cole, J. Keadle, S. Chipkin, L.S. Pescatello, K. Simpson, C.M. White, and P.D. Thompson Effect of statins on skeletal muscle function Circulation 127 2013 96 103
29. T. Prueksaritanont, R. Subramanian, X. Fang, B. Ma, Y. Qiu, J.H. Lin, 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
30. G.H. Renkema, S.B. Wortmann, R.J. Smeets, H. Venselaar, M. Antoine, G. Visser, T. Ben-Omran, L.P. van den Heuvel, H.J. Timmers, J.A. Smeitink, and R.J. Rodenburg SDHA mutations causing a multisystem mitochondrial disease: novel mutations and genetic overlap with hereditary tumors Eur. J. Hum. Genet. 23 2015 202 209
31. R.J. Rodenburg Biochemical diagnosis of mitochondrial disorders J. Inherit. Metab. Dis. 34 2011 283 292
32. P. Sirvent, J. Mercier, and A. Lacampagne New insights into mechanisms of statin-associated myotoxicity Curr. Opin. Pharmacol. 8 2008 333 338
33. P. Sirvent, O. Fabre, S. Bordenave, D. Hillaire-Buys, E. Raynaud De Mauverger, A. Lacampagne, and J. Mercier Muscle mitochondrial metabolism and calcium signaling impairment in patients treated with statins Toxicol. Appl. Pharmacol. 259 2012 263 268
34. I.B. Skottheim, A. Gedde-Dahl, S. Hejazifar, K. Hoel, and A. Asberg Statin induced myotoxicity: the lactone forms are more potent than the acid forms in human skeletal muscle cells in vitro Eur. J. Pharm. Sci. 33 2008 317 325
35. C. Stormo, M.P. Bogsrud, M. Hermann, A. Åsberg, A.P. Piehler, K. Retterstøl, and M.K. Kringen UGT1A1 28 is associated with decreased systemic exposure of atorvastatin lactone Mol. Diagn. Ther. 17 2013 233 237
36. D.A. Taha, C.H. De Moor, D.A. Barrett, and P. Gershkovich Translational insight into statin-induced muscle toxicity: from cell culture to clinical studies Transl. Res. 164 2014 85 109
37. G.D. Vladutiu, Z. Simmons, P.J. Isackson, M. Tarnopolsky, W.L. Peltier, A.C. Barboi, N. Sripathi, R.L. Wortmann, and P.S. Phillips Genetic risk factors associated with lipid-lowering drug-induced myopathies Muscle Nerve 34 2006 153 162
38. C.M. White A review of the pharmacologic and pharmacokinetic aspects of rosuvastatin J. Clin. Pharmacol. 42 2002 963 970
39. D.J. Wood, J. de Vlieg, M. Wagener, and T. Ritschel Pharmacophore fingerprint-based approach to binding site subpocket similarity and its application to bioisostere replacement J. Chem. Inf. Model. 52 2012 2031 2043
40. A. Zeharia, A. Shaag, R.H. Houtkooper, T. Hindi, P. de Lonlay, G. Erez, L. Hubert, A. Saada, Y. de Keyzer, G. Eshel, and et al. Mutations in LPIN1 cause recurrent acute myoglobinuria in childhood Am. J. Hum. Genet. 83 2008 489 494
41. P. Zhang, M.A. Verity, and K. Reue Lipin-1 regulates autophagy clearance and intersects with statin drug effects in skeletal muscle Cell Metab. 20 2014 267 279