Muscle oxidative capacity during IL-6-dependent cancer cachexia

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 2, 2011, Pages

  White, James P ^a   Baltgalvis, Kristen A ^a   Puppa, Melissa J ^a   Sato, Shuichi ^a   Baynes, John W ^a   Carson, James A ^a  

^a UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Fission 1 protein; Mitochondria; Mitofusin 2 protein; Wasting

Indexed keywords

CELL NUCLEUS DNA; CYTOCHROME C; CYTOCHROME C OXIDASE; INTERLEUKIN 6; MESSENGER RNA; MITOCHONDRIAL DNA; MITOFUSIN 1; MITOFUSIN 2; MYOSIN HEAVY CHAIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CACHEXIA; CONTROLLED STUDY; EPIDIDYMIS FAT; GASTROCNEMIUS MUSCLE; MOUSE; MUSCLE MASS; MUSCLE METABOLISM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SOLEUS MUSCLE; WEIGHT CHANGE;

ADIPOSE TISSUE; ALDEHYDES; ANIMALS; BODY WEIGHT; CACHEXIA; CATALASE; COLONIC NEOPLASMS; CYTOCHROMES C; DNA, MITOCHONDRIAL; ELECTRON TRANSPORT COMPLEX IV; GENE EXPRESSION; GENES, APC; GTP PHOSPHOHYDROLASES; HINDLIMB; INTERLEUKIN-6; ION CHANNELS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; SIRTUIN 1; STAT3 TRANSCRIPTION FACTOR; SUCCINATE DEHYDROGENASE; SUPEROXIDE DISMUTASE; TRANS-ACTIVATORS;

EID: 79551514029     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00300.2010     Document Type: Article

References (61)

1. Acharyya S, Ladner KJ, Nelsen LL, Damrauer J, Reiser PJ, Swoap S, Guttridge DC. Cancer cachexia is regulated by selective targeting of skeletal muscle gene products. J Clin Invest 114: 370-378, 2004. (Pubitemid 39071609)
2. Adhihetty PJ, Uguccioni G, Leick L, Hidalgo J, Pilegaard H, Hood DA. The role of PGC-1α on mitochondrial function and apoptotic susceptibility in muscle. Am J Physiol Cell Physiol 297: C217-C225, 2009.
3. al-Majid S, McCarthy DO. Cancer-induced fatigue and skeletal muscle wasting: the role of exercise. Biol Res Nurs 2: 186-197, 2001.
4. 2 generation. Am J Physiol Cell Physiol 290: C844-C851, 2006.
5. Bach D, Naon D, Pich S, Soriano FX, Vega N, Rieusset J, Laville M, Guillet C, Boirie Y, Wallberg-Henriksson H, Manco M, Calvani M, Castagneto M, Palacin M, Mingrone G, Zierath JR, Vidal H, Zorzano A. Expression of Mfn2, the Charcot-Marie-Tooth neuropathy type 2A gene, in human skeletal muscle: effects of type 2 diabetes, obesity, weight loss, and the regulatory role of tumor necrosis factor-α and interleukin-6. Diabetes 54: 2685-2693, 2005.
6. Min/+ mice. Am J Physiol Regul Integr Comp Physiol 294: R393-R401, 2008.
7. Min/+ mice. J Appl Physiol 109:1155-1161, 2010.
8. Min/+ mouse. Pflügers Arch 457: 989-1001, 2009.
9. 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.
10. Belizario JE, Lorite MJ, Tisdale MJ. Cleavage of caspases-1, -3, -6, -8, and -9 substrates by proteases in skeletal muscles from mice undergoing cancer cachexia. Br J Cancer 84: 1135-1140, 2001.
11. Biesecker G, Karimi S, Desjardins J, Meyer D, Abbott B, Bendele R, Richardson F. Evaluation of mitochondrial DNA content and enzyme levels in tenofovir DF-treated rats, rhesus monkeys, and woodchucks. Antiviral Res 58: 217-225, 2003.
12. Booth FW, Criswell DS. Molecular events underlying skeletal muscle atrophy and the development of effective countermeasures. Int J Sports Med 18, Suppl 4: S265-S269, 1997.
13. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
14. Carson JA, Baltgalvis KA. Interleukin 6 as a key regulator of muscle mass during cachexia. Exerc Sport Sci Rev 38: 168-176, 2010.
15. Chen CN, Ferrington DA, Thompson LV. Carbonic anhydrase III and four-and-a-half LIM protein 1 are preferentially oxidized with muscle unloading. J Appl Physiol 105: 1554-1561, 2008.
16. Crunkhorn S, Dearie F, Mantzoros C, Gami H, da Silva WS, Espinoza D, Faucette R, Barry K, Bianco AC, Patti ME. Peroxisome proliferator activator receptor gamma coactivator-1 expression is reduced in obesity: potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J Biol Chem 282: 15439-15450, 2007. (Pubitemid 47093279)
17. Cunningham JT, Rodgers JT, Arlow DH, Vazquez F, Mootha VK, Puigserver P. mTOR controls mitochondrial oxidative function through a YY1-PGC-1α transcriptional complex. Nature 450: 736-740, 2007.
18. De Sousa E, Veksler V, Bigard X, Mateo P, Ventura-Clapier R. Heart failure affects mitochondrial but not myofibrillar intrinsic properties of skeletal muscle. Circulation 102: 1847-1853, 2000.
19. Deschenes MR. Effects of aging on muscle fibre type and size. Sports Med 34: 809-824, 2004.
20. Ding H, Jiang N, Liu H, Liu X, Liu D, Zhao F, Wen L, Liu S, Ji LL, Zhang Y. Response of mitochondrial fusion and fission protein gene expression to exercise in rat skeletal muscle. Biochim Biophys Acta 1800: 250-256, 2010.
21. Fattori E, Cappelletti M, Zampaglione I, Mennuni C, Calvaruso F, Arcuri M, Rizzuto G, Costa P, Perretta G, Ciliberto G, La Monica N. Gene electro-transfer of an improved erythropoietin plasmid in mice and non-human primates. J Gene Med 7: 228-236, 2005.
22. Figueras M, Busquets S, Carbo N, Barreiro E, Almendro V, Argiles JM, Lopez-Soriano FJ. Interleukin-15 is able to suppress the increased DNA fragmentation associated with muscle wasting in tumour-bearing rats. FEBS Lett 569: 201-206, 2004.
23. Garnier A, Fortin D, Zoll J, N'Guessan B, Mettauer B, Lampert E, Veksler V, Ventura-Clapier R. Coordinated changes in mitochondrial function and biogenesis in healthy and diseased human skeletal muscle. FASEB J 19: 43-52, 2005.
24. Gosker HR, Hesselink MK, Duimel H, Ward KA, Schols AM. Reduced mitochondrial density in the vastus lateralis muscle of patients with COPD. Eur Respir J 30: 73-79, 2007.
25. Hernandez-Alvarez MI, Thabit H, Burns N, Shah S, Brema I, Hatunic M, Finucane F, Liesa M, Chiellini C, Naon D, Zorzano A, Nolan JJ. Subjects with early-onset type 2 diabetes show defective activation of the skeletal muscle PGC-1α/mitofusin-2 regulatory pathway in response to physical activity. Diabetes Care 33: 645-651, 2010.
26. Hood DA, Irrcher I, Ljubicic V, Joseph AM. Coordination of metabolic plasticity in skeletal muscle. J Exp Biol 209: 2265-2275, 2006.
27. Hoppeler H, Fluck M. Plasticity of skeletal muscle mitochondria: structure and function. Med Sci Sports Exerc 35: 95-104, 2003. (Pubitemid 36084147)
28. Jakobsson P, Jorfeldt L, Henriksson J. Metabolic enzyme activity in the quadriceps femoris muscle in patients with severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 151: 374-377, 1995.
29. James DI, Parone PA, Mattenberger Y, Martinou JC. hFis1, a novel component of the mammalian mitochondrial fission machinery. J Biol Chem 278: 36373-36379, 2003.
30. Kandarian SC, Jackman RW. Intracellular signaling during skeletal muscle atrophy. Muscle Nerve 33: 155-165, 2006.
31. Lee YJ, Jeong SY, Karbowski M, Smith CL, Youle RJ. Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis. Mol Biol Cell 15: 5001-5011, 2004.
32. Li P, Waters RE, Redfern SI, Zhang M, Mao L, Annex BH, Yan Z. Oxidative phenotype protects myofibers from pathological insults induced by chronic heart failure in mice. Am J Pathol 170: 599-608, 2007.
33. Liesa M, Borda-d'Agua B, Medina-Gomez G, Lelliott CJ, Paz JC, Rojo M, Palacin M, Vidal-Puig A, Zorzano A. Mitochondrial fusion is increased by the nuclear coactivator PGC-1α. PLoS One 3: e3613, 2008.
34. -ΔΔCT Method. Methods (San Diego, Calif) 25: 402-408, 2001.
35. Lustgarten MS, Jang YC, Liu Y, Muller FL, Qi W, Steinhelper M, Brooks SV, Larkin L, Shimizu T, Shirasawa T, McManus LM, Bhattacharya A, Richardson A, Van Remmen H. Conditional knockout of Mn-SOD targeted to type IIB skeletal muscle fibers increases oxidative stress and is sufficient to alter aerobic exercise capacity. Am J Physiol Cell Physiol 297: C1520-C1532, 2009.
36. McCarthy DO. Rethinking nutritional support for persons with cancer cachexia. Biol Res Nurs 5: 3-17, 2003.
37. McClung JM, Judge AR, Powers SK, Yan Z. p38 MAPK links oxidative stress to autophagy-related gene expression in cachectic muscle wasting. Am J Physiol Cell Physiol 298: C542-C549, 2010.
38. Min/+ mouse. J Appl Physiol 99: 2379-2387, 2005.
39. Min/+ mice. J Appl Physiol 98: 2219-2225, 2005.
40. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, Puigserver P, Carlsson E, Ridderstrale M, Laurila E, Houstis N, Daly MJ, Patterson N, Mesirov JP, Golub TR, Tamayo P, Spiegelman B, Lander ES, Hirschhorn JN, Altshuler D, Groop LC. PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273, 2003.
41. Moylan JS, Reid MB. Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35: 411-429, 2007.
42. Nachlas MM, Tsou KC, De Souza E, Cheng CS, Seligman AM. Cytochemical demonstration of succinic dehydrogenase by the use of a new p-nitrophenyl substituted ditetrazole. J Histochem Cytochem 5: 420-436, 1957.
43. Parra V, Eisner V, Chiong M, Criollo A, Moraga F, Garcia A, Hartel S, Jaimovich E, Zorzano A, Hidalgo C, Lavandero S. Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc Res 77: 387-397, 2008.
44. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, DeFronzo R, Finlayson J, Kahn CR, Mandarino LJ. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100: 8466-8471, 2003.
45. Pich S, Bach D, Briones P, Liesa M, Camps M, Testar X, Palacin M, Zorzano A. The Charcot-Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum Mol Genet 14: 1405-1415, 2005.
46. Puente-Maestu L, Perez-Parra J, Godoy R, Moreno N, Tejedor A, Gonzalez-Aragoneses F, Bravo JL, Alvarez FV, Camano S, Agusti A. Abnormal mitochondrial function in locomotor and respiratory muscles of COPD patients. Eur Respir J 33: 1045-1052, 2009.
47. Puigserver P, Spiegelman BM. Peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr Rev 24: 78-90, 2003.
48. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM. PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103: 16260-16265, 2006.
49. Scarpulla RC. Transcriptional activators and coactivators in the nuclear control of mitochondrial function in mammalian cells. Gene 286: 81-89, 2002.
50. Skov V, Glintborg D, Knudsen S, Jensen T, Kruse TA, Tan Q, Brusgaard K, Beck-Nielsen H, Hojlund K. Reduced expression of nuclear-encoded genes involved in mitochondrial oxidative metabolism in skeletal muscle of insulin-resistant women with polycystic ovary syndrome. Diabetes 56: 2349-2355, 2007.
51. Soriano FX, Liesa M, Bach D, Chan DC, Palacin M, Zorzano A. Evidence for a mitochondrial regulatory pathway defined by peroxisome proliferator-activated receptor-γ coactivator-1α, estrogen-related receptor-α, and mitofusin 2. Diabetes 55: 1783-1791, 2006.
52. Sparks LM, Xie H, Koza RA, Mynatt R, Hulver MW, Bray GA, Smith SR. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 54: 1926-1933, 2005.
53. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127: 397-408, 2006.
54. Sugioka R, Shimizu S, Tsujimoto Y. Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis. J Biol Chem 279: 52726-52734, 2004.
55. Tisdale MJ. Cachexia in cancer patients. Nat Rev Cancer 2: 862-871, 2002.
56. Tisdale MJ. Cancer cachexia. Curr Opin Gastroenterol 26: 146-151, 2010.
57. Vescovo G, Ravara B, Gobbo V, Angelini A, Dalla Libera L. Skeletal muscle fibres synthesis in heart failure: role of PGC-1α, calcineurin and GH. Int J Cardiol 104: 298-306, 2005.
58. Yokota T, Kinugawa S, Hirabayashi K, Matsushima S, Inoue N, Ohta Y, Hamaguchi S, Sobirin MA, Ono T, Suga T, Kuroda S, Tanaka S, Terasaki F, Okita K, Tsutsui H. Oxidative stress in skeletal muscle impairs mitochondrial respiration and limits exercise capacity in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 297: H1069-H1077, 2009.
59. Yu Z, Li P, Zhang M, Hannink M, Stamler JS, Yan Z. Fiber type-specific nitric oxide protects oxidative myofibers against cachectic stimuli. PLoS One 3: e2086, 2008.
60. Zorzano A, Hernandez-Alvarez MI, Palacin M, Mingrone G. Alterations in the mitochondrial regulatory pathways constituted by the nuclear co-factors PGC-1α or PGC-1β and mitofusin 2 in skeletal muscle in type 2 diabetes. Biochim Biophys Acta 2010.
61. Zorzano A, Liesa M, Palacin M. Role of mitochondrial dynamics proteins in the pathophysiology of obesity and type 2 diabetes. Int J Biochem Cell Biol 41: 1846-1854, 2009.