Molecular mechanisms underlying skeletal muscle weakness in human cancer: Reduced myosin-actin cross-bridge formation and kinetics

Journal of Applied Physiology

Volumn 114, Issue 7, 2013, Pages 858-868

  Toth, Michael J ^a,b   Miller, Mark S ^b   Callahan, Damien M ^a   Sweeny, Andrew P ^a   Nunez, Ivette ^a   Grunberg, Steven M ^a   Der Torossian, Hirak ^b   Couch, Marion E ^b   Dittus, Kim ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VERMONT   (United States)

Author keywords

Disability; Lung cancer; Ultrastructure

Indexed keywords

ACTIN; MYOSIN HEAVY CHAIN;

AGED; ARTICLE; FEMALE; HUMAN; KINETICS; MALE; METABOLISM; MIDDLE AGED; MUSCLE ISOMETRIC CONTRACTION; MUSCLE WEAKNESS; NEOPLASM; PATHOPHYSIOLOGY; SKELETAL MUSCLE;

ACTINS; AGED; FEMALE; HUMANS; ISOMETRIC CONTRACTION; KINETICS; MALE; MIDDLE AGED; MUSCLE WEAKNESS; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; NEOPLASMS;

EID: 84878618215     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01474.2012     Document Type: Article

References (64)

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. Adams GR, Caiozzo VI, Baldwin KM. Skeletal muscle unweighting: spaceflight and ground-based models. J Appl Physiol 95:2185-2201, 2003. (Pubitemid 37444955)
3. Baker F, Denniston M, Haffer SC, Liberatos P. Change in health-related quality of life of newly diagnosed cancer patients, cancer survivors, and controls. Cancer 115:3024-3033, 2009.
4. Bamman MM, Clarke MS, Talmadge RJ, Feeback DL. Enhanced protein electrophoresis technique for separating human skeletal muscle myosin heavy chain isoforms. Electrophoresis 20:466-468, 1999. (Pubitemid 29183406)
5. Banduseela V, Ochala J, Lamberg K, Kalimo H, Larsson L. Muscle paralysis and myosin loss in a patient with cancer cachexia. Acta Myol 26:136-144, 2007. (Pubitemid 351668921)
6. Barreiro E, De La Puente B, Busquets S, López-Soriano FJ, Gea J, Argilés JM. Both oxidative and nitrosative stress are associated with muscle wasting in tumour-bearing rats. FEBS Lett 579:1646-1652, 2005. (Pubitemid 40341537)
7. Barreiro E, Peinado VI, Galdiz JB, Ferrer E, Marin-Corral J, Sánchez F, Gea J, Barberà JA, ENIGMA in COPD Project. Cigarette smoke-induced oxidative stress: a role in chronic obstructive pulmonary disease skeletal muscle dysfunction. Am J Respir Crit Care Med 182:477-488, 2010.
8. Bean JF, Kiely DK, La Rose S, Leveille SG. Which impairments are most associated with high mobility performance in older adults? Implications for a rehabilitation prescription. Arch Phys Med Rehabil 89:2278-2284, 2008.
9. Bean JF, Kiely DK, Leveille SG, Herman S, Huynh C, Fielding R, Frontera WR. The 6-minute walk test in mobility-limited elders: what is being measured? J Gerontol 57 A: M751-M756, 2002. (Pubitemid 35340557)
10. Bottinelli R. Functional heterogeneity of mammalian single muscle fibres: do myosin isoforms tell the whole story? Pflugers Arch 443:6-17, 2001. (Pubitemid 33070885)
11. Brenner B. Effect of Ca2. on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contrac tion. Proc Natl Acad Sci USA 85:3265-3269, 1988.
12. Brunelli A, Pompili C, Berardi R, Mazzanti P, Onofri A, Salati M, Cascinu S, Sabbatini A. Performance at preoperative stair-climbing test is associated with prognosis after pulmonary resection in Stage Inon-small cell lung cancers. Ann Thorac Surg 93:1796-1800, 2012.
13. Butt Z, Rosenbloom SK, Abernethy AP, Beaumont JL, Paul D, Hamptom D, Jacobsen PB, Syrjala KL, Von Roenn JH, Cella D. Do Fatigue is the most important symptom for advanced cancer patients who w have had chemotherapy. J Natl Compr Canc Netw 6:448-455, 2008. (Pubitemid 351754243)
14. Cosper PF, Leinwand LA. Myosin heavy chain is not selectively de-ad creased in murine cancer cachexia. Int J Cancer 130:2722-2727, 2012.
15. D'Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, Saltin B, Bottinelli R. The effect of ageing and immobilization o on structure and function of human skeletal muscle fibres. J Physiol 552:499-511, 2003. (Pubitemid 37321847)
16. Dagda RK, Cherra SJ, Kulich SM, Tandon A, Park D, Chu CT. Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J Biol Chem 284:13843-13855, 2009.
17. Debigaré R, Côté CH, Hould FS, Le Blanc P, Maltais F. In vitro and in vivo contractile properties of the vastus lateralis muscle in males with ysi COPD. Eur Resp J 21:273-278, 2003. (Pubitemid 36204542)
18. Dewys WD, Begg C, Lavin PT, Band PR, Bennett JM, Bertino JR, Og Cohen MH, Douglass HO Jr, Engstrom PF, Ezdinli EZ, Horton J, Johnson GJ, Moertel CG, Oken MM, Perlia C, Rosenbaum C, Silverrg Stein MN, Skeel RT, Sponzo RW, Tormey DC. Prognostic effect of weight loss prior to chemotherapy in cancer patients. Am J Med 69:491-497, 1980. (Pubitemid 10018703)
19. Eley HL, Skipworth RJ, Deans DA, Fearon KC, Tisdale MJ. Increased expression of phosphorylated forms of RNA-dependent protein kinase and ie eukaryotic initiation factor 2. may signal skeletal muscle atrophy in r B weight-losing cancer patients. Br J Cancer 98:443-449, 2007. (Pubitemid 351161247)
20. Fearon KC, Glass DJ, Guttridge DC. Cancer cachexia: mediators, and signaling and metabolic pathways. Cell Metabolism 16:1-14, 2012.
21. Fitts RH, Romatowski JG, Peters JR, Paddon-Jones D, Wolfe RR, Un Ferrando AA. The deleterious effects of bed rest on human skeletal muscle fibers are exacerbated by hypercortisolemia and ameliorated by dietary supplementation. Am J Physiol Cell Physiol 293:C313-C320, 4, 2013 2007. (Pubitemid 47105022)
22. Gallagher IJ, Stephens NA, MacDonald AJ, Skipworth RJ, Husi H, Greig CA, Ross JA, Timmons JA, Fearon KC. Suppression of skeletal muscle turnover in cancer cachexia: evidence from the transcriptome in sequential human muscle biopsies. Clin Canc Res 18:2817-2827, 2012.
23. Gilliam LA, St. Clair DK. Chemotherapy-induced weakness and fatigue in skeletal muscle: the role of oxidative stress. Antioxid Redox Signal 15:2543-2563, 2011.
24. Harridge SD, Bottinelli R, Canepari M, Pellegrino MA, Reggiani C, Esbjörnsson M, Saltin B. Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflugers Arch 432:913-920, 1996. (Pubitemid 26281590)
25. 2+ activation and slows cross-bridge cycling kinetics in skeletal muscle. J Appl Physiol 91:2233-2239, 2001. (Pubitemid 33015078)
26. Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN. Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr 52:214-218, 1990.
27. Huxley AF. Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255-318, 1957.
28. Ivy JL, Costill DL, Maxwell BD. Skeletal muscle determinants of maximum aerobic power in man. Eur J Appl Physiol Occup Physiol 44:1-8, 1980. (Pubitemid 10066784)
29. Isokinetic contractile properties of the quadriceps with relation to fiber type. Eur J Appl Physiol Occup Physiol 47:247-255, 1981.
30. Jatoi A, Hillman S, Stella P, Mailliard J, Sloan J, Vanone S, Cannon M, Kutteh L, Kanard A, Jett J. Daily activities: exploring their spectrum and prognostic impact in older, chemotherapy-treated lung cancer patients. Support Care Cancer 11:460-464, 2003. (Pubitemid 36869952)
31. Jendrach M, Mai S, Pohl S, Vöth M, Bereiter-Hahn J. Short-and long-term alterations of mitochondrial morphology, dynamics and mtDNA after transient oxidative stress. Mitochondrion 8:293-304, 2008.
32. Jones LW, Eves ND, Haykowsky M, Freedland SJ, Mackey JR. Exercise intolerance in cancer and the role of exercise therapy to reverse dysfunction. Lancet Oncol 10:598-605, 2009.
33. Jones LW, Hornsby WE, Goetzinger A, Forbes LM, Sherrard EL, Quist M, Lane AT, West M, Eves ND, Gradison M, Coan A, Herndon JE, Abernethy AP. Prognostic significance of functional capacity and exercise behavior in patients with metastatic non-small cell lung cancer. Lung Cancer 76:248-252, 2012.
34. Jones LW, Watson D, Herndon JE, Eves ND, Haithcock BE, Loewen G, Kohman L. Peak oxygen consumption and long-term all-cause mortality in non-small cell lung cancer. Cancer 116:4825-4832, 2010.
35. Kawai M, Saeki Y, Zhao Y. Crossbridge scheme and the kinetic constants of elementary steps deduced from chemically skinned papillary and trabecular muscles of the ferret. Circ Res 73:35-50, 1993. (Pubitemid 23173054)
36. Li M, Larsson L. Force-generating capacity of human myosin isoforms extracted from single muscle fibre segments. J Physiol 588:5105-5114, 2010.
37. Massey R, Jedlicka D. The Massey bedside swallowing screen. J Neurosci Nurs 34:7-60, 2002.
38. Maughan RJ, Watson JS, Weir J. Strength and cross-sectional area of human skeletal muscle. J Physiol 338:37-49, 1983. (Pubitemid 13099474)
39. Miller KL, Kocak Z, Kahn D, Zhou SM, Baydush A, Hollis D, Folz RJ, Tisch A, Clough R, Yu X, Light K, Marks LB. Preliminary report of the 6-minute walk test as a predictor of radiation-induced pulmonary toxicity. Int J Radiat Oncol Biol Phys 62:1009-1013, 2005. (Pubitemid 40884411)
40. Miller MS, Van Buren P, Le Winter MM, Braddock JM, Ades PA, Maughan DW, Palmer BM, Toth MJ. Chronic heart failure decreases cross-bridge kinetics in single skeletal muscle fibers from humans. J Physiol 588:4039-4053, 2010.
41. Miller MS, Van Buren P, Le Winter MM, Lecker SH, Selby DE, Palmer BM, Maughan DW, Ades PA, Toth MJ. Mechanisms underlying skeletal muscle weakness in human heart failure: alterations in single fiber myosin protein content and function. Circ Heart Fail 2:700-706, 2009.
42. Mulieri LA, Barnes W, Leavitt B, Ittleman F, Le Winter MM, Maughan DW. Alterations of myocardial dynamic stiffness implicating abnormal cross-bridge function in human mitral regurgitation heart failure. Circ Res 90:66-72, 2002. (Pubitemid 34074610)
43. Palmer BM, Fishbaugher DE, Schmitt JP, Wang Y, Alpert NR, Seidman CE, Seidman JG, Van Buren P, Maughan DW. Differential cross-bridge kinetics of FHC myosin mutations R403Q and R453C in heterzygous mouse myocardium. Am J Physiol Heart Circ Physiol 287:H91-H99, 2004. (Pubitemid 38802340)
44. Palmer BM, Suzuki T, Wang Y, Barnes W, Miller MS, Maughan D. Two-state model of acto-myosin attachment-detachment predicts C-process of sinusoidal analysis. Biophys J 93:760-769, 2007. (Pubitemid 47219771)
45. Perkins WJ, Han YS, Sieck GC. Skeletal muscle foce and actomyosin ATPase activity reduced by nitric oxide donor. J Appl Physiol 83:1326-1332, 1997. (Pubitemid 27433102)
46. Piazzesi G, Reconditi M, Linari M, Lucii L, Bianco P, Brunello E, Decostre V, Stewart A, Gore DB, Irving TC, Irving M, Lombardi V. Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size. Cell 131:784-795, 2007. (Pubitemid 350103598)
47. Ramamoorthy S, Donohue M, Buck M. Decreased Jun-D and myogenin expression in muscle wasting of human cachexia. Am J Physiol Endocrinol Metab 297:E392-E401, 2009.
48. Reeve BB, Potosky AL, Smith AW, Han PK, Hays RD, Davis WW, Arora NK, Haffer SC, Clauser SB. Impact of cancer on health-related quality of life of older Americans. J Natl Compr Canc Netw 101:860-868, 2009.
49. Reid KF, Fielding RA. Skeletal muscle power: a critical determinant of physical functioning in older adults. Exerc Sport Sci Rev 40:4-12, 2012.
50. Reid MB, Moylan JS. Beyond atrophy: redox mechanisms of muscle dysfunction in chronic inflammatory disease. J Physiol 589:2171-2179, 2011.
51. Savage PD, Shaw AO, Miller MS, Van Buren P, Le Winter MM, Ades PA, Toth MJ. Effect of resistance training on physical disability in chronic heart failure. Med Sci Sports Exer 43:1379-1386, 2011.
52. Schmitt T, Martignoni M, Bachmann J, Fechtner K, Friess H, Kinscherf R, Hildebrandt W. Activity of the Akt-dependent anabolic and catabolic pathways in muscle and liver samples in cancer-related cachexia. J Mol Med 85:647-654, 2007. (Pubitemid 46870894)
53. Sjöström M, Angquist KA, Bylund AC, Fridén J, Gustavsson L, Scherstén T. Morphometric analysis of human muscle fiber types. Muscle Nerve 5:538-553, 1982.
54. Stephens NA, Gray C, MacDonald AJ, Tan BH, Gallagher IJ, Skipworth RJ, Ross JA, Fearon KC, Greig CA. Sexual dimorphism modulates the impact of cancer cachexia on lower limb muscle mass and function. Clin Nutr 31:499-505, 2012.
55. Toth MJ, Matthews DE, Tracy RP, Previs MJ. Age-related differences in skeletal muscle protein synthesis: relation to markers of immune activation. Am J Physiol Endocrinol Metab 288:E883-E891, 2005. (Pubitemid 40547881)
56. Toth MJ, Miller MS, Van Buren P, Bedrin NG, Le Winter MM, Ades PA, Palmer BM. Resistance training alters skeletal muscle structure and function in human heart failure: effects at the tissue, cellular and molecular levels. J Physiol 590:1243-1259, 2012.
57. Toth MJ, Miller MS, Ward KA, Ades PA. Skeletal muscle mitochondrial density, gene expression, and enzyme activities in human heart failure: minimal effects of the disease and resistance training. J Appl Physiol 112:1864-1874, 2012.
58. Toth MJ, Shaw AO, Miller MS, Van Buren P, Le Winter MM, Maughan D, Ades PA. Reduced knee extensor function in heart failure is not explained by inactivity. Int J Cardiol 143:276-282, 2010.
59. Van Den Borst B, Slot IG, Hellwig VA, Vosse BA, Kelders MC, Barreiro E, Schols AM, Gosker HR. Loss of quadriceps muscle oxidative phenotype and decreased endurance in patients with mild-to-moderate COPD. J Appl Physiol First published July 19, 2012; doi:10.1152/japplphysiol.00508.2012.
60. Vogelzang NJ, Breibart W, Cella D, Curt GA, Groopman JE, Horning SJ, Itri LM, Johnson DH, Scherr SL, Portenoy RK. Patient, caregiver, and oncologist perceptions of cancer-related fatigue: results of a tripart assessment survey. Fatigue Coalition Semin Hematol 34:4-12, 1997. (Pubitemid 27319139)
61. Weber MA, Krakowski-Roosen H, Schröder L, Kinscherf R, Krix M, Kopp-Schneider A, Essig M, Bachert P, Kauczor HU, Hildebrandt W. Morphology, metabolism, microcirculation, and strength of skeletal muscles in cancer-related cachexia. Acta Oncol 48:116-124, 2009.
62. White JP, Baltgalvis KA, Puppa MJ, Sato S, Baynes JW, Carson JA. Muscle oxidative capacity during IL-6-dependent cancer cachexia. Am J Physiol Regul Integr Comp Physiol 300:R201-R211, 2011.
63. Wüst R, Morse C, De Haan A, Rittweger J, Jones D, Degens H. Skeletal muscle properties and fatigue resistance in relation to smoking history. Eur J Appl Physiol 104:103-110, 2008.
64. Zhao Y, Kawai M. The effect of lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. II Elementary steps affected by the spacing change. Biophys J 64:197-210, 1993. (Pubitemid 23063942)