Targeted overexpression of mitochondrial catalase protects against cancer chemotherapy-induced skeletal muscle dysfunction

American Journal of Physiology - Endocrinology and Metabolism

Volumn 311, Issue 2, 2016, Pages E293-E301

  Gilliam, Laura A A ^a,b   Lark, Daniel S ^a   Reese, Lauren R ^a,b   Torres, Maria J ^a   Ryan, Terence E ^a,b   Lin, Chien Te ^a,b   Cathey, Brook L ^a,b   Darrell Neufer, P ^a,b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

Author keywords

Cancer; Chemotherapy; Mitochondria; Reactive oxygen species; Skeletal muscle

Indexed keywords

CATALASE; DOXORUBICIN; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); ANTINEOPLASTIC AGENT; HYDROGEN PEROXIDE; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY COMPOSITION; BREAST CANCER; CANCER CHEMOTHERAPY; CONTROLLED STUDY; FATTY ACID OXIDATION; FEMALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; MUSCLE FUNCTION; MYOPATHY; NONHUMAN; OXIDATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIRATORY FUNCTION; SOLEUS MUSCLE; WESTERN BLOTTING; ANIMAL; BREAST NEOPLASMS; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; MUSCLE CONTRACTION; MUSCLE MITOCHONDRION; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; SKELETAL MUSCLE; TRANSGENIC MOUSE;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CATALASE; DISEASE MODELS, ANIMAL; DOXORUBICIN; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX II; FEMALE; HYDROGEN PEROXIDE; MICE; MICE, TRANSGENIC; MITOCHONDRIA, MUSCLE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; OXIDATION-REDUCTION; PROTEINS;

EID: 84983802402     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00540.2015     Document Type: Article

References (39)

1. American Cancer Society. Cancer Facts & Figures 2015. Atlanta, GA: American Cancer Society, 2015.
2. 2 emission and cellular redox state link excess fat intake to insulin resistance in both rodents and humans. J Clin Invest 119: 573–581, 2009.
3. Andrade FH, Reid MB, Allen DG, Westerblad H. Effect of hydrogen peroxide and dithiothreitol on contractile function of single skeletal muscle fibres from the mouse. J Physiol 509: 565–575, 1998.
4. Barreiro E, de la Puente B, Busquets S, Lopez-Soriano FJ, Gea J, Argiles JM. Both oxidative and nitrosative stress are associated with muscle wasting in tumour-bearing rats. FEBS Lett 579: 1646–1652, 2005.
5. Bower JE, Ganz PA, Desmond KA, Bernaards C, Rowland JH, Meyerowitz BE, Belin TR. Fatigue in long-term breast carcinoma survivors: a longitudinal investigation. Cancer 106: 751–758, 2006.
6. Chabner BA, Ryan DP, Paz-Ares L, Garcia-Carbonero R, Calabresi P, Hardman JG, Limbird LE, Gilman AG. Goodman & Gilman’s The Pharmacologic Basis of Therapeutics. New York: McGraw-Hill, Medical Publishing Division, 2001, p. 1389–1459.
7. Cummings J, Willmott N, Calman KC. Effect of a subcutaneously growing Walker 256 carcinosarcoma on host tissue mitochondrial function and magnesium content. Cancer Res 44: 1333–1336, 1984.
8. Dickey JS, Gonzalez Y, Aryal B, Mog S, Nakamura AJ, Redon CE, Baxa U, Rosen E, Cheng G, Zielonka J, Parekh P, Mason KP, Joseph J, Kalyanaraman B, Bonner W, Herman E, Shacter E, Rao VA. Mito-tempol and dexrazoxane exhibit cardioprotective and chemotherapeutic effects through specific protein oxidation and autophagy in a syngeneic breast tumor preclinical model. PLoS One 8: e70575, 2013.
9. Fermoselle C, García-Arumí E, Puig-Vilanova E, Andreu AL, Urtreger AJ, de Kier Joffé ED, Tejedor A, Puente-Maestu L, Barreiro E. Mitochondrial dysfunction and therapeutic approaches in respiratory and limb muscles of cancer cachectic mice. Exp Physiol 98: 1349–1365, 2013.
10. Fisher-Wellman KH, Lin CT, Ryan TE, Reese LR, Gilliam LA, Cathey BL, Lark DS, Smith CD, Muoio DM, Neufer PD. Pyruvate dehydrogenase complex and nicotinamide nucleotide transhydrogenase constitute an energy-consuming redox circuit. Biochem J 467: 271–280, 2015.
11. Gilliam LA, Ferreira LF, Bruton JD, Moylan JS, Westerblad H, St Clair DK, Reid MB. Doxorubicin acts through tumor necrosis factor receptor subtype 1 to cause dysfunction of murine skeletal muscle. J Appl Physiol 107: 1935–1942, 2009.
12. Gilliam LA, Fisher-Wellman KH, Lin CT, Maples JM, Cathey BL, Neufer PD. The anticancer agent doxorubicin disrupts mitochondrial energy metabolism and redox balance in skeletal muscle. Free Radic Biol Med 65: 988–996, 2013.
13. Gilliam LA, Moylan JS, Callahan LA, Sumandea MP, Reid MB. Doxorubicin causes diaphragm weakness in murine models of cancer chemotherapy. Muscle Nerve 43: 94–102, 2011.
14. Gilliam LA, Moylan JS, Ferreira LF, Reid MB. TNF/TNFR1 signaling mediates doxorubicin-induced diaphragm weakness. Am J Physiol Lung Cell Mol Physiol 300: L225–L231, 2011.
15. Gilliam LA, Moylan JS, Patterson EW, Smith JD, Wilson AS, Rabbani Z, Reid MB. Doxorubicin acts via mitochondrial ROS to stimulate catabolism in C2C12 myotubes. Am J Physiol Cell Physiol 302: C195–C202, 2012.
16. Gonzalez Y, Pokrzywinski KL, Rosen ET, Mog S, Aryal B, Chehab LM, Vijay V, Moland CL, Desai VG, Dickey JS, Rao VA. Reproductive hormone levels and differential mitochondria-related oxidative gene expression as potential mechanisms for gender differences in cardiosensitivity to Doxorubicin in tumor-bearing spontaneously hypertensive rats. Cancer Chemother Pharmacol 76: 447–459, 2015.
17. Gouspillou G, Scheede-Bergdahl C, Spendiff S, Vuda M, Meehan B, Mlynarski H, Archer-Lahlou E, Sgarioto N, Purves-Smith FM, Konokhova Y, Rak J, Chevalier S, Taivassalo T, Hepple RT, Jagoe RT. Anthracycline-containing chemotherapy causes long-term impairment of mitochondrial respiration and increased reactive oxygen species release in skeletal muscle. Sci Rep 5: 8717, 2015.
18. Jacobsen PB, Hann DM, Azzarello LM, Horton J, Balducci L, Lyman GH. Fatigue in women receiving adjuvant chemotherapy for breast cancer: characteristics, course, and correlates. J Pain Symptom Manage 18: 233–242, 1999.
19. Jones LW, Watson D, Herndon JE 2nd, Eves ND, Haithcock BE, Loewen G, Kohman L. Peak oxygen consumption and long-term allcause mortality in nonsmall cell lung cancer. Cancer 116: 4825–4832, 2010.
20. Kluza J, Marchetti P, Gallego MA, Lancel S, Fournier C, Loyens A, Beauvillain JC, Bailly C. Mitochondrial proliferation during apoptosis induced by anticancer agents: effects of doxorubicin and mitoxantrone on cancer and cardiac cells. Oncogene 23: 7018–7030, 2004.
21. Koskelo EK, Saarinen UM, Siimes MA. Skeletal muscle wasting and protein-energy malnutrition in children with a newly diagnosed acute leukemia. Cancer 66: 373–376, 1990.
22. Lamb GD, Posterino GS. Effects of oxidation and reduction on contractile function in skeletal muscle fibres of the rat. J Physiol 546: 149–163, 2003.
23. Leuthauser SW, Oberley LW, Oberley TD, Loven DP. Lowered superoxide dismutase activity in distant organs of tumor-bearing mice. J Natl Cancer Inst 72: 1065–1074, 1984.
24. Li T, Danelisen I, Singal PK. Early changes in myocardial antioxidant enzymes in rats treated with adriamycin. Mol Cell Biochem 232: 19–26, 2002.
25. Mattarollo SR, Loi S, Duret H, Ma Y, Zitvogel L, Smyth MJ. Pivotal role of innate and adaptive immunity in anthracycline chemotherapy of established tumors. Cancer Res 71: 4809–4820, 2011.
26. Min K, Kwon OS, Smuder AJ, Wiggs MP, Sollanek KJ, Christou DD, Yoo JK, Hwang MH, Szeto HH, Kavazis AN, Powers SK. Increased mitochondrial emission of reactive oxygen species and calpain activation are required for doxorubicin-induced cardiac and skeletal muscle myopathy. J Physiol 593: 2017–2036, 2015.
27. Mohamed HE, Asker ME, Ali SI, el-Fattah TM. Protection against doxorubicin cardiomyopathy in rats: role of phosphodiesterase inhibitors type 4. J Pharm Pharmacol 56: 757–768, 2004.
28. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 417: 1–13, 2009.
29. Myers C, Bonow R, Palmeri S, Jenkins J, Corden B, Locker G, Doroshow J, Epstein S. A randomized controlled trial assessing the prevention of doxorubicin cardiomyopathy by N-acetylcysteine. Semin Oncol 10: 53–55, 1983.
30. Perry CG, Kane DA, Lin CT, Kozy R, Cathey BL, Lark DS, Kane CL, Brophy PM, Gavin TP, Anderson EJ, Neufer PD. Inhibiting myosin-ATPase reveals a dynamic range of mitochondrial respiratory control in skeletal muscle. Biochem J 437: 215–222, 2011.
31. Quinlan CL, Orr AL, Perevoshchikova IV, Treberg JR, Ackrell BA, Brand MD. Mitochondrial complex II can generate reactive oxygen species at high rates in both the forward and reverse reactions. J Biol Chem 287: 27255–27264, 2012.
32. Rephaeli A, Waks-Yona S, Nudelman A, Tarasenko I, Tarasenko N, Phillips DR, Cutts SM, Kessler-Icekson G. Anticancer prodrugs of butyric acid and formaldehyde protect against doxorubicin-induced cardiotoxicity. Br J Cancer 96: 1667–1674, 2007.
33. Saeed MF, Premecz S, Goyal V, Singal PK, Jassal DS. Catching broken hearts: pre-clinical detection of doxorubicin and trastuzumab mediated cardiac dysfunction in the breast cancer setting. Can J Physiol Pharmacol 92: 546–550, 2014.
34. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabinovitch PS. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science 308: 1909–1911, 2005.
35. Schwartz AL. Daily fatigue patterns and effect of exercise in women with breast cancer. Cancer Pract 8: 16–24, 2000.
36. Smuder AJ, Kavazis AN, Min K, Powers SK. Exercise protects against doxorubicin-induced oxidative stress and proteolysis in skeletal muscle. J Appl Physiol 110: 935–942, 2011.
37. Szeto HH. Development of mitochondria-targeted aromatic-cationic peptides for neurodegenerative diseases. Ann NY Acad Sci 1147: 112–121, 2008.
38. Tozer RG, Tai P, Falconer W, Ducruet T, Karabadjian A, Bounous G, Molson JH, Droge W. Cysteine-rich protein reverses weight loss in lung cancer patients receiving chemotherapy or radiotherapy. Antioxid Redox Signal 10: 395–402, 2008.
39. Unverferth DV, Jagadeesh JM, Unverferth BJ, Magorien RD, Leier CV, Balcerzak SP. Attempt to prevent doxorubicin-induced acute human myocardial morphologic damage with acetylcysteine. J Natl Cancer Inst 71: 917–920, 1983.