Doxorubicin acts through tumor necrosis factor receptor subtype 1 to cause dysfunction of murine skeletal muscle

Journal of Applied Physiology

Volumn 107, Issue 6, 2009, Pages 1935-1942

  Gilliam, Laura A A ^a   Ferreira, Leonardo F ^a   Bruton, Joseph D ^b   Moylan, Jennifer S ^a   Westerblad, Håkan ^b   St Clair, Daret K ^c   Reid, Michael B ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cachexia; Cancer; Chemotherapy; Fatigue; Weakness

Indexed keywords

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CALCIUM; DOXORUBICIN; ENZYME-LINKED IMMUNOSORBENT ASSAY; MALE; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE FATIGUE; MUSCLE STRENGTH; MUSCLE WEAKNESS; MUSCLE, SKELETAL; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 73449104584     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00776.2009     Document Type: Article

References (51)

1. Adams V, Mangner N, Gasch A, Krohne C, Gielen S, Hirner S, Thierse HJ, Witt CC, Linke A, Schuler G, Labeit S. Induction of MuRF1 is essential for TNF-alpha-induced loss of muscle function in mice. J Mol Biol 384: 48-59, 2008.
2. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88: 287-332, 2008.
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 Online 509: 565-575, 1998.
4. Andrade FH, Reid MB, Westerblad H. Contractile response of skeletal muscle to low peroxide concentrations: myofibrillar calcium sensitivity as a likely target for redox-modulation. FASEB J 15: 309-311, 2001.
5. Bonifati DM, Ori C, Rossi CR, Caira S, Fanin M, Angelini C. Neuromuscular damage after hyperthermic isolated limb perfusion in patients with melanoma or sarcoma treated with chemotherapeutic agents. Cancer Chemother Pharmacol 46: 517-522, 2000.
6. Bower JE, Ganz PA, Aziz N, Fahey JL. Fatigue and proinflammatory cytokine activity in breast cancer survivors. Psychosom Med 64: 604-611, 2002.
7. 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.
8. Close RI. Dynamic properties of mammalian skeletal muscles. Physiol Rev 52: 129-197, 1972.
9. De Beer EL, Finkle H, Voest EE, Van Heijst BGV, Schiereck P. Doxorubicin interacts directly with skinned single skeletal muscle fibres. Eur J Pharmacol 214: 97-100, 1992.
10. Delgado G, Potkul RK, Treat JA, Lewandowski GS, Barter JF, Forst D, Rahman A. A phase I/II study of intraperitoneally administered doxorubicin entrapped in cardiolipin liposomes in patients with ovarian cancer. Am J Obstet Gynecol 160: 812-819, 1989.
11. Donovan KA, Jacobsen PB, Andrykowski MA, Winters EM, Balducci L, Malik U, Kenady D, McGrath P. Course of fatigue in women receiving chemotherapy and/or radiotherapy for early stage breast cancer. J Pain Symptom Manage 28: 373-380, 2004.
12. Doroshow JH, Tallent C, Schechter JE. Ultrastructural features of Adriamycin-induced skeletal and cardiac muscle toxicity. Am J Pathol 118: 288-297, 1985.
13. Dudnakova TV, Lakomkin VL, Tsyplenkova VG, Shekhonin BV, Shirinsky VP, Kapelko VI. Alterations in myocardial cytoskeletal and regulatory protein expression following a single Doxorubicin injection. J Cardiovasc Pharmacol 41: 788-794, 2003.
14. Elbl L, Vasova I, Tomaskova I, Jedlicka F, Kral Z, Navratil M, Smardova L, Wagnerova B, Vorlicek J. Cardiopulmonary exercise testing in the evaluation of functional capacity after treatment of lymphomas in adults. Leuk Lymphoma 47: 843-851, 2006.
15. Evans WK, Nixon DW, Daly JM, Ellenberg SS, Gardner L, Wolfe E, Shepherd FA, Feld R, Gralla R, Fine S. A randomized study of oral nutritional support versus ad lib nutritional intake during chemotherapy for advanced colorectal and non-small-cell lung cancer. J Clin Oncol 5: 113-124, 1987.
16. Freireich EJ, Gehan EA, Rall DP, Schmidt LH, Skipper HE. Quantitative comparison of toxicity of anticancer agents in mouse, rat, hamster, dog, monkey, and man. Cancer Chemother Rep 50: 219-244, 1966.
17. Garcia-Martinez C, Lopez-Soriano FJ, Argiles JM. Acute treatment with tumour necrosis factor-alpha induces changes in protein metabolism in rat skeletal muscle. Mol Cell Biochem 125: 11-18, 1993.
18. Gielen S, Adams V, Mobius-Winkler S, Linke A, Erbs S, Yu J, Kempf W, Schubert A, Schuler G, Hambrecht R. Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J Am Coll Cardiol 42: 861-868, 2003.
19. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods 25: 386-401, 2001.
20. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
21. Hardin BJ, Campbell KS, Smith JD, Arbogast S, Smith J, Moylan JS, Reid MB. TNF-α acts via TNFR1 and muscle-derived oxidants to depress myofibrillar force in murine skeletal muscle. J Appl Physiol 104: 694- 699, 2008.
22. Johansen PB. Doxorubicin pharmacokinetics after intravenous and intraperitoneal administration in the nude mouse. Cancer Chemother Pharmacol 5: 267-270, 1981.
23. Kang YJ, Sun X, Chen Y, Zhou Z. Inhibition of doxorubicin chronic toxicity in catalase-overexpressing transgenic mouse hearts. Chem Res Toxicol 15: 1-6, 2002.
24. 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.
25. Kotler DP. Cachexia. Ann Intern Med 133: 622-634, 2000.
26. 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.
27. Lännergren J, Westerblad H. The temperature dependence of isometric contractions of single, intact fibres dissected from a mouse foot muscle. J Physiol 390: 285-293, 1987.
28. Li X, Moody MR, Engel D, Walker S, Clubb FJ Jr, Sivasubramanian N, Mann DL, and Reid MB. Cardiac-specific overexpression of tumor necrosis factor-alpha causes oxidative stress and contractile dysfunction in mouse diaphragm. Circulation 102: 1690-1696, 2000.
29. Lien YC, Lin SM, Nithipongvanitch R, Oberley TD, Noel T, Zhao Q, Daosukho C, St Clair DK. Tumor necrosis factor receptor deficiency exacerbated Adriamycin-induced cardiomyocytes apoptosis: an insight into the Fas connection. Mol Cancer Ther 5: 261-269, 2006.
30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25: 402-408, 2001.
31. Llovera M, Garcia-Martinez C, Lopez-Soriano J, Carbo N, Agell N, Lopez-Soriano FJ, Argiles JM. Role of TNF receptor 1 in protein turnover during cancer cachexia using gene knockout mice. Mol Cell Endocrinol 142: 183-189, 1998.
32. Mariappan N, Soorappan RN, Haque M, Sriramula S, Francis J. TNF-α-induced mitochondrial oxidative stress and cardiac dysfunction: restoration by superoxide dismutase mimetic Tempol. Am J Physiol Heart Circ Physiol 293: H2726-H2737, 2007.
33. McLoon LK, Falkenberg JH, Dykstra D, Iaizzo PA. Doxorubicin chemomyectomy as a treatment for cervical dystonia: histological assessment after direct injection into the sternocleidomastoid muscle. Muscle Nerve 21: 1457-1464, 1998.
34. McMullen CA, Andrade FH. Contractile dysfunction and altered metabolic profile of the aging rat thyroarytenoid muscle. J Appl Physiol 100: 602-608, 2006.
35. Miller M, Maguire R, Kearney N. Patterns of fatigue during a course of chemotherapy: results from a multi-centre study. Eur J Oncol Nurs 11: 126-132, 2007.
36. Mukherjee S, Banerjee SK, Maulik M, Dinda AK, Talwar KK, Maulik SK. Protection against acute adriamycin-induced cardiotoxicity by garlic: role of endogenous antioxidants and inhibition of TNF-alpha expression. BMC Pharmacol 3: 16, 2003.
37. Piscitelli SC, Rodvold KA, Rushing DA, Tewksbury DA. Pharmacokinetics and pharmacodynamics of doxorubicin in patients with small cell lung cancer. Clin Pharmacol Ther 53: 555-561, 1993.
38. Reid MB, Lannergren J, Westerblad H. Respiratory and limb muscle weakness induced by tumor necrosis factor-alpha: involvement of muscle myofilaments. Am J Respir Crit Care Med 166: 479-484, 2002.
39. Reid MB, Li YP. Tumor necrosis factor-alpha and muscle wasting: a cellular perspective. Respir Res 2: 269-272, 2001.
40. 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.
41. Salles G, Bienvenu J, Bastion Y, Barbier Y, Doche C, Warzocha K, Gutowski MC, Rieux C, Coiffier B. Elevated circulating levels of TNFα and its p55 soluble receptor are associated with an adverse prognosis in lymphoma patients. Br J Haematol 93: 352-359, 1996.
42. Stone P, Hardy J, Broadley K, Tookman AJ, Kurowska A, A'Hern R. Fatigue in advanced cancer: a prospective controlled cross-sectional study. Br J Cancer 79: 1479-1486, 1999.
43. Tangpong J, Cole MP, Sultana R, Estus S, Vore M, St CW, Ratanachaiyavong S, St Clair DK, Butterfield DA. Adriamycin-mediated nitration of manganese superoxide dismutase in the central nervous system: insight into the mechanism of chemobrain. J Neurochem 100: 191-201, 2007.
44. Tangpong J, Cole MP, Sultana R, Joshi G, Estus S, Vore M, St CW, Ratanachaiyavong S, St Clair DK, Butterfield DA. Adriamycin-induced, TNF-alpha-mediated central nervous system toxicity. Neurobiol Dis 23: 127-139, 2006.
45. 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.
46. 2+ pump function in rats. J Appl Physiol 103: 1921-1928, 2007.
47. Usta Y, Ismailoglu UB, Bakkaloglu A, Orhan D, Besbas N, Sahin-Erdemli I, Ozen S. Effects of pentoxifylline in adriamycin-induced renal disease in rats. Pediatr Nephrol 19: 840-843, 2004.
48. van Norren K, van Helvoort A, Argiles JM, van Tuijl S, Arts K, Gorselink M, Laviano A, Kegler D, Haagsman HP, van der Beek EM. Direct effects of doxorubicin on skeletal muscle contribute to fatigue. Br J Cancer 100: 311-314, 2009.
49. Viner RI, Williams TD, Schoneich C. Peroxynitrite modification of protein thiols: oxidation, nitrosylation, and S-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum Ca-ATPase. Biochemistry 38: 12408-12415, 1999.
50. Zhi G, Ryder JW, Huang J, Ding P, Chen Y, Zhao Y, Kamm KE, Stull JT. Myosin light chain kinase and myosin phosphorylation effect frequency-dependent potentiation of skeletal muscle contraction. Proc Natl Acad Sci USA 102: 17519-17524, 2005.
51. Zorzato F, Salviati G, Facchinetti T, Volpe P. Doxorubicin induces calcium release from terminal cisternae of skeletal muscle. A study on isolated sarcoplasmic reticulum and chemically skinned fibers. J Biol Chem 260: 7349-7355, 1985.