Statins interfere with the attachment of S. cerevisiae mtDNA to the inner mitochondrial membrane

References

• Buhaescu I, Izzedine H. Mevalonate pathway: a review of clinical and therapeutical implications. Clin Biochem 2007;40:575–84.
   PubMed Web of Science ®Google Scholar
• Friesen JA, Rodwell VW. The 3-hydroxy-3-methylglutaryl coenzyme-A (HMG-CoA) reductases. Genome Biol 2004;5:248.
   PubMed Web of Science ®Google Scholar
• Burg JS, Espenshade PJ. Regulation of HMG-CoA reductase in mammals and yeast. Prog Lipid Res 2011;50:403–10.
   PubMed Web of Science ®Google Scholar
• Istvan ES. Structural mechanism for statin inhibition of 3-hydroxy-3-methylglutaryl coenzyme A reductase. Am Heart J 2002;144:S27–S32.
   PubMed Web of Science ®Google Scholar
• Golomb BA, Evans MA. Statin adverse effects. Am J Cardiovasc Drugs 2008;8:373–418.
   PubMed Web of Science ®Google Scholar
• Tomaszewski M, Stępień KM, Tomaszewska J, Czuczwar SJ. Statin-induced myopathies. Pharmacol Rep 2011;63:859–66.
   PubMed Web of Science ®Google Scholar
• du Souich P, Roederer G, Dufour R. Myotoxicity of statins: mechanism of action. Pharmacol Ther 2017;175:1–16.
   PubMed Web of Science ®Google Scholar
• Matsubara A, Oda S, Akai S, et al. Establishment of a drug-induced rhabdomyolysis mouse model by co-administration of ciprofloxacin and atorvastatin. Toxicol Lett 2018;291:184–93.
   PubMed Web of Science ®Google Scholar
• Knauer MJ, Urquhart BL, Meyer zu Schwabedissen HE, et al. Human skeletal muscle drug transporters determine local exposure and toxicity of statins. Circ Res 2010;106:297–306.
   PubMed Web of Science ®Google Scholar
• Tournadre A. Statins, myalgia, and rhabdomyolysis. Joint Bone Spine 2019;1–6.
   Web of Science ®Google Scholar
• Kaufmann P, Török M, Zahno A, et al. Toxicity of statins on rat skeletal muscle mitochondria. Cell Mol Life Sci 2006;63:2415–25.
   PubMed Web of Science ®Google Scholar
• Apostolopoulou M, Corsini A, Roden M. The role of mitochondria in statin‐induced myopathy. Eur J Clin Invest 2015;45:745–54.
   PubMed Web of Science ®Google Scholar
• Bolotin‐Fukuhara M, Fairhead C. Candida glabrata: a deadly companion? Yeast 2014;31:279–88.
   PubMed Web of Science ®Google Scholar
• Lorenz RT, Parks LW. Effects of lovastatin (mevinolin) on sterol levels and on activity of azoles in Saccharomyces cerevisiae. Antimicrob Agents Chemother 1990;34:1660–5.
   PubMed Web of Science ®Google Scholar
• Westermeyer C, Macreadie IG. Simvastatin reduces ergosterol levels, inhibits growth and causes loss of mtDNA in Candida glabrata. FEMS Yeast Res 2007;7:436–41.
   PubMed Web of Science ®Google Scholar
• Barrientos A. Yeast models of human mitochondrial diseases. IUBMB Life 2008;55:83–95.
   Google Scholar
• Rinaldi T, Dallabona C, Ferrero I, et al. Mitochondrial diseases and the role of the yeast models. FEMS Yeast Res 2010;10:1006–22.
   PubMed Web of Science ®Google Scholar
• Francisci S, Montanari A. Mitochondrial diseases: yeast as a model for the study of suppressors. Biochim Biophys Acta Mol Cell Res 2017;1864:666–73.
   PubMed Web of Science ®Google Scholar
• Cirigliano A, Macone A, Bianchi MM, et al. Ergosterol reduction impairs mitochondrial DNA maintenance in S. cerevisiae. Biochim Biophys Acta Mol Cell Res 2019;1864:290–303.
   Google Scholar
• Ottaviano D, Montanari A, De Angelis L, et al. Unsaturated fatty acids-dependent linkage between respiration and fermentation revealed by deletion of hypoxic regulatory KlMGA2 gene in the facultative anaerobe-respiratory yeast Kluyveromyces lactis. FEMS Yeast Res 2015; 15:fov028.
   PubMed Web of Science ®Google Scholar
• De Luca C, Zhou Y, Montanari A, et al. Can yeast be used to study mitochondrial diseases? Biolistic tRNA mutants for the analysis of mechanisms and suppressors. Mitochondrion 2009;9:408–17.
   PubMed Web of Science ®Google Scholar
• De Angelis L, Rinaldi T, Cirigliano A, et al. Functional roles of the fatty acid desaturases encoded by KlOLE1, FAD2 and FAD3 in the yeast Kluyveromyces lactis. Microbiology 2016;162:1435–45.
   PubMed Web of Science ®Google Scholar
• Kang C, Goodman CA, Hornberger TA, Ji LL. PGC-1a overexpression by in vivo transfection attenuates mitochondrial deterioration of skeletal muscle caused by immobilization. FASEB J. 2015;29(10):4092–106.
   Google Scholar
• Bard M, Lees ND, Burnett AS, Parker RA. Isolation and characterization of mevinolin resistant mutants of Saccharomyces cerevisiae. Microbiology 1988;134:1071–8.
   Web of Science ®Google Scholar
• Fowler DM, Cooper SJ, Stephany JJ, et al. Suppression of statin effectiveness by copper and zinc in yeast and human cells. Mol BioSyst 2011;7:533–44.
   PubMedGoogle Scholar
• Maciejak A, Leszczynska A, Warchol I, et al. The effects of statins on the mevalonic acid pathway in recombinant yeast strains expressing human HMG-CoA reductase. BMC Biotechnol 2013;13:68.
   PubMed Web of Science ®Google Scholar
• Davies BS, Rine J. A role for sterol levels in oxygen sensing in Saccharomyces cerevisiae. Genetics 2006;174:191–201.
   PubMed Web of Science ®Google Scholar
• Serratore ND, Baker KM, Macadlo LA, et al. A novel sterol-signaling pathway governs azole antifungal drug resistance and hypoxic gene repression in Saccharomyces cerevisiae. Genetics 2018;208:1037–55.
   PubMed Web of Science ®Google Scholar
• Dimmer KS, Fritz S, Fuchs F, et al. Genetic basis of mitochondrial function and morphology in Saccharomyces cerevisiae. Mol Biol Cell 2002;13:847–53.
   PubMed Web of Science ®Google Scholar
• Altmann K, Westermann B. Role of essential genes in mitochondrial morphogenesis in Saccharomyces cerevisiae. Mol Biol Cell 2005;16:5410–7.
   PubMed Web of Science ®Google Scholar
• Chen XJ, Clark-Walker GD. Mutations in MGI genes convert Kluyveromyces lactis into a petite-positive yeast. Genetics 1993;133:517–25.
   PubMed Web of Science ®Google Scholar
• Bianchi MM, Brambilla L, Protani F, et al. Efficient homolactic fermentation by Kluyveromyces lactis strains defective in pyruvate utilization and transformed with the heterologous LDH gene. Appl Environ Microbiol 2001;67:5621–5.
   PubMed Web of Science ®Google Scholar
• Ramachandran R, Wierzbicki A. Statins, muscle disease and mitochondria. J Clin Med 2017;6:75.
   Web of Science ®Google Scholar
• Tay SK, DiMauro S, Pang AY, et al. Myotoxicity of lipid-lowering agents in a teenager with MELAS mutation. Pediatr Neurol 2008;39:426–8.
   PubMed Web of Science ®Google Scholar
• Vladutiu GD, Simmons Z, Isackson PJ, et al. Genetic risk factors associated with lipid‐lowering drug‐induced myopathies. Muscle Nerve 2006;34:153–62.
   PubMed Web of Science ®Google Scholar
• Feuermann M, Francisci S, Rinaldi T, et al. The yeast counterparts of human ‘MELAS’mutations cause mitochondrial dysfunction that can be rescued by overexpression of the mitochondrial translation factor EF‐Tu. EMBO Rep 2003;4:53–8.
   PubMed Web of Science ®Google Scholar
• Montanari A, Besagni C, De Luca C, et al. Yeast as a model of human mitochondrial tRNA base substitutions: investigation of the molecular basis of respiratory defects. RNA 2007;14:275–83.
   PubMed Web of Science ®Google Scholar
• Blau HM, Pavlath GK, Hardeman EC, et al. Plasticity of the differentiated state. Science 1985;230:758–66.
   PubMed Web of Science ®Google Scholar
• Katz DH, Intwala SS, Stone NJ. Addressing statin adverse effects in the clinic: the 5 Ms. J Cardiovasc Pharmacol Ther 2014;19:533–42.
   PubMed Web of Science ®Google Scholar
• Sirvent P, Fabre O, Bordenave S, et al. Muscle mitochondrial metabolism and calcium signaling impairment in patients treated with statins. Toxicol Appl Pharmacol 2012;259:263–8.
   PubMed Web of Science ®Google Scholar
• Shakoury-Elizeh M, Protchenko O, Berger A, et al. Metabolic response to iron deficiency in Saccharomyces cerevisiae. J Biol Chem 2010;285:14823–33.
   PubMed Web of Science ®Google Scholar
• Chariot P, Abadia R, Agnus D, et al. Simvastatin-induced rhabdomyolysis followed by a MELAS syndrome. Am J Med 1993;94:109.
   PubMed Web of Science ®Google Scholar
• Ferguson LR, Von Borstel RC. Induction of the cytoplasmic ‘petite’mutation by chemical and physical agents in Saccharomyces cerevisiae. Mutat Res 1992;265:103–48.
   PubMedGoogle Scholar
• Sezgin E, Levental I, Mayor S, Eggeling C. The mystery of membrane organization: composition, regulation and roles of lipid rafts. Nat Rev Mol Cell Biol 2017;18:361.
   PubMed Web of Science ®Google Scholar
• Gerhold JM, Cansiz-Arda Ş, Lõhmus M, et al. Human mitochondrial DNA-protein complexes attach to a cholesterol-rich membrane structure. Sci Rep 2015;5:15292.
   PubMed Web of Science ®Google Scholar
• Murley A, Lackner LL, Osman C, et al. ER-associated mitochondrial division links the distribution of mitochondria and mitochondrial DNA in yeast. Elife 2013;2:e00422.
   PubMed Web of Science ®Google Scholar
• He J, Cooper HM, Reyes A, et al. Mitochondrial nucleoid interacting proteins support mitochondrial protein synthesis. Nucleic Acids Res 2012;40:6109–21.
   PubMed Web of Science ®Google Scholar
• Gilkerson R, Bravo L, Garcia I, et al. The mitochondrial nucleoid: integrating mitochondrial DNA into cellular homeostasis. Cold Spring Harb Perspect Biol 2013;5:a011080.
   PubMed Web of Science ®Google Scholar
• Peralta S, Goffart S, Williams SL, et al. ATAD3 controls mitochondrial cristae structure in mouse muscle, influencing mtDNA replication and cholesterol levels. J Cell Sci 2018;131:jcs217075.
   PubMed Web of Science ®Google Scholar
• De Pinieux G, Chariot P, Ammi‐Said M, 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 2003;42:333–7.
   Google Scholar
• Nadanaciva S, Dykens JA, Bernal A, et al. Mitochondrial impairment by PPAR agonists and statins identified via immunocaptured OXPHOS complex activities and respiration. Toxicol Appl Pharmacol 2007;223:277–87.
   PubMed Web of Science ®Google Scholar
• Sirvent P, Bordenave S, Vermaelen M, et al. Simvastatin induces impairment in skeletal muscle while heart is protected. Biochem Biophys Res Commun 2005;338:1426–34.
   PubMed Web of Science ®Google Scholar
• Larsen S, Stride N, Hey-Mogensen M, et al. Simvastatin effects on skeletal muscle: relation to decreased mitochondrial function and glucose intolerance. J Am Coll Cardiol 2013;61:44–53.
   PubMed Web of Science ®Google Scholar
• Schick BA, Laaksonen R, Frohlich JJ, et al. Decreased skeletal muscle mitochondrial DNA in patients treated with high‐dose simvastatin. Clin Pharmacol Ther 2007;81:650–3.
   PubMed Web of Science ®Google Scholar
• Stringer HA, Sohi GK, Maguire JA, Côté HC. Decreased skeletal muscle mitochondrial DNA in patients with statin-induced myopathy. J Neurol Sci 2013;325:142–7.
   PubMed Web of Science ®Google Scholar
• Sin J, Andres AM, Taylor DJ, et al. Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts. Autophagy 2016;12:369–80.
   PubMed Web of Science ®Google Scholar