Mitochondrial dysfunction-associated OPA1 cleavage contributes to muscle degeneration: Preventative effect of hydroxytyrosol acetate

Cell Death and Disease

Volumn 5, Issue 11, 2014, Pages

  Wang, X ^a   Li, H ^a   Zheng, A ^a   Yang, L ^a   Liu, J ^a,b   Chen, C ^a   Tang, Y ^a   Zou, X ^a   Li, Y ^a   Long, J ^a   Zhang, Y ^b   Feng, Z ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b TIANJIN UNIVERSITY OF SPORT   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; HYDROXYTYROSOL; MESSENGER RNA; MITOCHONDRIAL COMPLEX II; MITOCHONDRIAL COMPLEX V; MYOSIN HEAVY CHAIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; CATECHOL DERIVATIVE; GUANOSINE TRIPHOSPHATASE; HYDROXYTYROSYL ACETATE; OLIVE OIL; OPA1 PROTEIN (GTPASE), MOUSE; SUCCINATE DEHYDROGENASE (UBIQUINONE); VEGETABLE OIL;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CELL VIABILITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; MULTIGENE FAMILY; MUSCLE ATROPHY; MYOBLAST; MYOTUBE; NONHUMAN; OPTIC ATROPHY 1; OPTIC NERVE ATROPHY; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN CONTENT; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL DIFFERENTIATION; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MITOCHONDRION; PATHOLOGY; PROTEIN DEGRADATION; SKELETAL MUSCLE;

ACETATES; ACETYLCYSTEINE; ANIMALS; CARBONYL CYANIDE P-TRIFLUOROMETHOXYPHENYLHYDRAZONE; CATECHOLS; CELL DIFFERENTIATION; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; GENE EXPRESSION REGULATION; GTP PHOSPHOHYDROLASES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MITOCHONDRIA; MUSCLE FIBERS, SKELETAL; MYOBLASTS; MYOSIN HEAVY CHAINS; OLIVE OIL; OXIDATIVE STRESS; PLANT OILS; PROTEOLYSIS; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; TERT-BUTYLHYDROPEROXIDE;

EID: 84927945734     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.473     Document Type: Article

References (47)

1. Timmons JA, Norrbom J, Scheele C, Thonberg H, Wahlestedt C, Tesch P. Expression profiling following local muscle inactivity in humans provides new perspective on diabetes-related genes. Genomics 2006; 87: 165-172.
2. Kang C, Ji LL. Muscle immobilization and remobilization downregulates PGC-1alpha signaling and the mitochondrial biogenesis pathway. J Appl Physiol (1985) 2013; 115: 1618-1625.
3. Mecocci P, Fano G, Fulle S, MacGarvey U, Shinobu L, Polidori MC et al. Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. Free Radic Biol Med 1999; 26: 303-308.
4. Dewys WD, Begg C, Lavin PT, Band PR, Bennett JM, Bertino JR et al. Prognostic effect of weight loss prior to chemotherapy in cancer patients. Eastern Cooperative Oncology Group. Am J Med 1980; 69: 491-497.
5. O'Gorman P, McMillan DC, McArdle CS. Longitudinal study of weight, appetite, performance status, and inflammation in advanced gastrointestinal cancer. Nutr Cancer 1999; 35: 127-129.
6. Feng Z, Bai L, Yan J, Li Y, Shen W, Wang Y et al. Mitochondrial dynamic remodeling in strenuous exercise-induced muscle and mitochondrial dysfunction: regulatory effects of hydroxytyrosol. Free Radic Biol Med 2011; 50: 1437-1446.
7. Casanova E, Baselga-Escudero L, Ribas-Latre A, Arola-Arnal A, Blade C, Arola L et al. Epigallocatechin gallate counteracts oxidative stress in docosahexaenoic acid-treated myocytes. Biochim Biophys Acta 2014; 1837: 783-791.
8. Kim B, Kim JS, Yoon Y, Santiago MC, Brown MD, Park JY. Inhibition of Drp1-dependent mitochondrial division impairs myogenic differentiation. Am J Physiol Regul Integr Comp Physiol 2013; 305: R927-R938.
9. Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y et al. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 2010; 29: 1774-1785.
10. Cao K, Xu J, Zou X, Li Y, Chen C, Zheng A et al. Hydroxytyrosol prevents diet-induced metabolic syndrome and attenuates mitochondrial abnormalities in obese mice. Free Radic Biol Med 2014; 67: 396-407.
11. Olichon A, Emorine LJ, Descoins E, Pelloquin L, Brichese L, Gas N et al. The human dynamin-related protein OPA1 is anchored to the mitochondrial inner membrane facing the inter-membrane space. FEBS Lett 2002; 523: 171-176.
12. Suen DF, Norris KL, Youle RJ. Mitochondrial dynamics and apoptosis. Genes Dev 2008; 22: 1577-1590.
13. Delettre C, Griffoin JM, Kaplan J, Dollfus H, Lorenz B, Faivre L et al. Mutation spectrum and splicing variants in the OPA1 gene. Hum Genet 2001; 109: 584-591.
14. Merkwirth C, Dargazanli S, Tatsuta T, Geimer S, Lower B, Wunderlich FT et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 2008; 22: 476-488.
15. Ishihara N, Fujita Y, Oka T, Mihara K. Regulation of mitochondrial morphology through proteolytic cleavage of OPA1. EMBO J 2006; 25: 2966-2977.
16. Baricault L, Segui B, Guegand L, Olichon A, Valette A, Larminat F et al. OPA1 cleavage depends on decreased mitochondrial ATP level and bivalent metals. Exp Cell Res 2007; 313: 3800-3808.
17. Griparic L, Kanazawa T, van der Bliek AM. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J Cell Biol 2007; 178: 757-764.
18. Macvicar TD, Lane JD. Impaired OMA1 dependent OPA1 cleavage and reduced DRP1 fission activity combine to prevent mitophagy in OXPHOS dependent cells. J Cell Sci 2014; 127(Pt 10): 2313-2325.
19. Kieper N, Holmstrom KM, Ciceri D, Fiesel FC, Wolburg H, Ziviani E et al. Modulation of mitochondrial function and morphology by interaction of Omi/HtrA2 with the mitochondrial fusion factor OPA1. Exp Cell Res 2010; 316: 1213-1224.
20. Maltecca F, Aghaie A, Schroeder DG, Cassina L, Taylor BA, Phillips SJ et al. The mitochondrial protease AFG3L2 is essential for axonal development. J Neurosci 2008; 28: 2827-2836.
21. Maltecca F, Magnoni R, Cerri F, Cox GA, Quattrini A, Casari G. Haploinsufficiency of AFG3L2, the gene responsible for spinocerebellar ataxia type 28, causes mitochondria-mediated Purkinje cell dark degeneration. J Neurosci 2009; 29: 9244-9254.
22. Dorn GW 2nd, Clark CF, Eschenbacher WH, Kang MY, Engelhard JT, Warner SJ et al. MARF and Opa1 control mitochondrial and cardiac function in Drosophila. Circ Res 2011; 108: 12-17.
23. Parra V, Verdejo HE, Iglewski M, Del Campo A, Troncoso R, Jones D et al. Insulin stimulates mitochondrial fusion and function in cardiomyocytes via the Akt-mTOR-NFkappaB-Opa-1 signaling pathway. Diabetes 2014; 63: 75-88.
24. Pelucchi C, Bosetti C, Negri E, Lipworth L, La Vecchia C. Olive oil and cancer risk: an update of epidemiological findings through 2010. Curr Pharm Des 2011; 17: 805-812.
25. Perez-Martinez P, Garcia-Rios A, Delgado-Lista J, Perez-Jimenez F, Lopez-Miranda J. Mediterranean diet rich in olive oil and obesity, metabolic syndrome and diabetes mellitus. Curr Pharm Des 2011; 17: 769-777.
26. Fito M, Cladellas M, de la Torre R, Marti J, Alcantara M, Pujadas-Bastardes M et al. Antioxidant effect of virgin olive oil in patients with stable coronary heart disease: a randomized, crossover, controlled, clinical trial. Atherosclerosis 2005; 181: 149-158.
27. Pierno S, Tricarico D, Liantonio A, Mele A, Digennaro C, Rolland JF et al. An olive oil-derived antioxidant mixture ameliorates the age-related decline of skeletal muscle function. Age (Dordr) 2014; 36: 73-88.
28. Lisete-Torres P, Losada-Barreiro S, Albuquerque H, Sanchez-Paz V, Paiva-Martins F, Bravo-Diaz C. Distribution of hydroxytyrosol and hydroxytyrosol acetate in olive oil emulsions and their antioxidant efficiency. J Agric Food Chem 2012; 60: 7318-7325.
29. del Campo A, Parra V, Vasquez-Trincado C, Gutierrez T, Morales PE, Lopez-Crisosto C et al. Mitochondrial fragmentation impairs insulin-dependent glucose uptake by modulating Akt activity through mitochondrial Ca2+ uptake. Am J Physiol Endocrinol Metabol 2014; 306: E1-E13.
30. Spinazzi M, Cazzola S, Bortolozzi M, Baracca A, Loro E, Casarin A et al. A novel deletion in the GTPase domain of OPA1 causes defects in mitochondrial morphology and distribution, but not in function. Hum Mol Genet 2008; 17: 3291-3302.
31. Duvezin-Caubet S, Jagasia R, Wagener J, Hofmann S, Trifunovic A, Hansson A et al. Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J Biol Chem 2006; 281: 37972-37979.
32. Zhang Q, Seltmann H, Zouboulis CC, Konger RL. Involvement of PPARgamma in oxidative stress-mediated prostaglandin E(2) production in SZ95 human sebaceous gland cells. J Invest Dermatol 2006; 126: 42-48.
33. Marchetti M, Resnick L, Gamliel E, Kesaraju S, Weissbach H, Binninger D. Sulindac enhances the killing of cancer cells exposed to oxidative stress. PLoS One 2009; 4: e5804.
34. Krishnan N, Dickman MB, Becker DF. Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress. Free Radic Biol Med 2008; 44: 671-681.
35. Maechler P, Jornot L, Wollheim CB. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J Biol Chem 1999; 274: 27905-27913.
36. Ballinger SW, Patterson C, Yan CN, Doan R, Burow DL, Young CG et al. Hydrogen peroxideand peroxynitrite-induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells. Circ Res 2000; 86: 960-966.
37. Tyska MJ, Warshaw DM. The myosin power stroke. Cell Motil Cytoskeleton 2002; 51: 1-15.
38. Pandorf CE, Caiozzo VJ, Haddad F, Baldwin KM. A rationale for SDS-PAGE of MHC isoforms as a gold standard for determining contractile phenotype. J Appl Physiol (1985) 2010; 108: 222-222. author reply 226.
39. Li YP, Schwartz RJ, Waddell ID, Holloway BR, Reid MB. Skeletal muscle myocytes undergo protein loss and reactive oxygen-mediated NF-kappaB activation in response to tumor necrosis factor alpha. FASEB J 1998; 12: 871-880.
40. Sarzi E, Angebault C, Seveno M, Gueguen N, Chaix B, Bielicki G et al. The human OPA1delTTAG mutation induces premature age-related systemic neurodegeneration in mouse. Brain 2012; 135(Pt 12): 3599-3613.
41. Lodi R, Tonon C, Valentino ML, Manners D, Testa C, Malucelli E et al. Defective mitochondrial adenosine triphosphate production in skeletal muscle from patients with dominant optic atrophy due to OPA1 mutations. Arch Neurol 2011; 68: 67-73.
42. Joseph AM, Adhihetty PJ, Buford TW, Wohlgemuth SE, Lees HA, Nguyen LM et al. The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high-and low-functioning elderly individuals. Aging Cell 2012; 11: 801-809.
43. Frezza C, Cipolat S, Martins de Brito O, Micaroni M, Beznoussenko GV, Rudka T et al. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell 2006; 126: 177-189.
44. Cipolat S, Rudka T, Hartmann D, Costa V, Serneels L, Craessaerts K et al. Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling. Cell 2006; 126: 163-175.
45. Liu J, Peng Y, Feng Z, Shi W, Qu L, Li Y et al. Reloading functionally ameliorates disuse-induced muscle atrophy by reversing mitochondrial dysfunction, and similar benefits are gained by administering a combination of mitochondrial nutrients. Free Radic Biol Med 2014; 69: 116-128.
46. Li X, Liu Z, Luo C, Jia H, Sun L, Hou B et al. Lipoamide protects retinal pigment epithelial cells from oxidative stress and mitochondrial dysfunction. Free Radic Biol Med 2008; 44: 1465-1474.
47. Sun L, Luo C, Long J, Wei D, Liu J. Acrolein is a mitochondrial toxin: effects on respiratory function and enzyme activities in isolated rat liver mitochondria. Mitochondrion 2006; 6: 136-142.