Chronic exposure to stretch-shortening contractions results in skeletal muscle adaptation in young rats and maladaptation in old rats

Applied Physiology, Nutrition and Metabolism

Volumn 31, Issue 5, 2006, Pages 573-587

  Cutlip, Robert G ^a   Baker, Brent A ^a   Geronilla, Kenneth B ^a   Mercer, Robert R ^a   Kashon, Michael L ^a   Miller, Gerald R ^a   Murlasits, Zsolt ^b   Alway, Stephen E ^b  

^a NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cellular interstitium; Dorsiflexor muscles; Repetitive exposure; Stretch shortening cycles

Indexed keywords

ADAPTATION; AGING; ANIMAL; ARTICLE; BROWN NORWAY RAT; FISCHER 344 RAT; HISTOLOGY; MALE; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE ISOMETRIC CONTRACTION; PHYSIOLOGY; RAT; SKELETAL MUSCLE; TIME; ULTRASTRUCTURE;

ADAPTATION, PHYSIOLOGICAL; AGING; ANIMALS; ISOMETRIC CONTRACTION; MALE; MUSCLE CONTRACTION; MUSCLE FIBERS; MUSCLE, SKELETAL; RATS; RATS, INBRED BN; RATS, INBRED F344; TIME FACTORS;

EID: 33846116523     PISSN: 17155312     EISSN: None     Source Type: Journal    
DOI: 10.1139/H06-033     Document Type: Article

References (54)

1. Alway, S.E. 1995. Slowing of contractile properties in quail skeletal muscle with aging. J. Gerontol. A. Biol. Sci. Med. Sci. 50A: B26-B33. PMID:7814776.
2. Alway, S.E., Degens, H., Krishnamurthy, G., and Smith, C.A. 2002. Potential role for Id myogenic repressors in apoptosis and attenuation of hypertrophy in muscles of aged rats. Am. J. Physiol. Cell Physiol. 283: C66-C76. PMID:12055074.
3. Avela, J., and Komi, P.V. 1998. Reduced stretch reflex sensitivity and muscle stiffness after long-lasting stretch-shortening cycle exercise in humans. Eur. J. Appl. Physiol. Occup. Physiol. 78: 403-410. doi:10.1007/ s004210050438. PMID:9809840.
4. Baker, B.A., Mercer, R.R., Geronilla, K.B., Kashon, M.L., Miller, G.R., and Cutlip, R.G. 2006. Stereological analysis of muscle morphology following exposure to repetitive stretch-shortening cycles in a rat model. Appl. Physiol. Nutr. Metab. 31: 167-179. PMID:16604135.
5. Benz, R.J., Friden, J., and Lieber, R.L. 1998. Simultaneous stiffness and force measurements reveal subtle injury to rabbit soleus muscles. Mol. Cell. Biochem. 179: 147-158. doi:10.1023/ A:1006824324509. PMID:9543357.
6. Bernard, B.P., Putz-Anderson, V., Burt, S.E., Cole, L.L., Fairfield-Estill, C., Fine, L.J., et al. 1997. Musculoskeletal disorders and workplace factors. A critical review of epidemiologic evidence for work-related musculoskeletal disorders of the neck, upper extremity, and low back. Cincinnati, NIOSH.
7. Booth, F.W.. Weeden, S.H., and Tseng, B.S. 1994. Effect of aging on human skeletal muscle and motor function. Med. Sci. Sports Exerc. 26: 556-560. PMID:8007802.
8. Brooks, S.V., and Faulkner, J.A. 1988. Contractile properties of skeletal muscles from young, adult and aged mice. J. Physiol. 404: 71-82. PMID:3253447.
9. Brooks, S.V., and Faulkner, J.A. 1990. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am. J. Physiol. 258: C436-C442. PMID:2316632.
10. Brooks, S.V., and Faulkner, J.A. 1994. Isometric, shortening, and lengthening contractions of muscle fiber segments from adult and old mice. Am. J. Physiol. 267: C507-C513. PMID:8074185.
11. Brooks, S.V., and Faulkner, J.A. 1996. The magnitude of the initial injury induced by stretches of maximally activated muscle fibres of mice and rats increases in old age. J. Physiol. 497: 573-580. PMID:8961197.
12. Brooks, S.V., Zerba, E., and Faulkner, J.A. 1995. Injury to muscle fibres after single stretches of passive and maximally stimulated muscles in mice. J. Physiol. 488: 459-469. PMID:8568684.
13. Brooks, S.V., Opiteck, J.A., and Faulkner, J.A. 2001. Conditioning of skeletal muscles in adult and old mice for protection from contraction-induced injury. J. Gerontol. A Biol. Sci. Med. Sci. 56: B163-B171. PMID:11283187.
14. Carson, J.A., Alway, S.E., and Yamaguchi, M. 1995. Time course of hypertrophic adaptations of the anterior latissimus dorsi muscle to stretch overload in aged Japanese quail. J. Gerontol. A. Biol. Sci. Med. Sci. 50: B391-B398. PMID:7583796.
15. Conboy, I.M., Conboy, M.J., Wagers, A.J., Girma, E.R., Weissman, I.L., and Rando, T.A. 2005. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature (London). 433: 760-764. doi:10.1038/nature03260. PMID:15716955.
16. Cutlip, R.G., Stauber, W.T., Willison, R.H., McIntosh, T.A., and Means, K.H. 1997. Dynamometer for rat plantar flexor muscles in vivo. Med. Biol. Eng. Comput. 35: 540-543. PMID:9374061.
17. Cutlip, R.G., Geronilla, K.B., Baker, B.A., Kashon, M.L., Miller, G.R., and Schopper, A.W. 2004. Impact of muscle length during stretch-shortening contractions on real-time and temporal muscle performance measures in rats in vivo. J. Appl. Physiol. 96: 507-516. doi:10.1152/japplphysiol.00046. 2003. PMID:14555680.
18. Davis, J., Kaufman, K.R., and Lieber, R.L. 2003. Correlation between active and passive isometric force and intramuscular pressure in the isolated rabbit tibialis anterior muscle. J. Biomech. 36: 505-512. doi:10.1016/S0021-9290(02)00430-X. PMID:12600341.
19. Degens, H., and Alway, S.E. 2003. Skeletal muscle function and hypertrophy are diminished in old age. Muscle Nerve. 27: 339-347. doi:10.1002/mus.10314. PMID:12635121.
20. Devor, S.T., and Faulkner, J.A. 1999. Regeneration of new fibers in muscles of old rats reduces contraction-induced injury. J. Appl. Physiol. 87: 750-756. PMID:10444636.
21. Eddinger, T.J., Cassens, R.G., and Moss, R.L. 1986. Mechanical and histochemical characterization of skeletal muscles from senescent rats. Am. J. Physiol. 251: C421-C430. PMID:2944390.
22. Ettema, G.J. 1996. Mechanical efficiency and efficiency of storage and release of series elastic energy in skeletal muscle during stretch-shorten cycles. J. Exp. Biol. 199: 1983-1997. PMID:8831144.
23. Evans, W.J., and Campbell, W.W. 1993. Sarcopenia and age-related changes in body composition and functional capacity. J. Nutr. 123: 465-468. PMID:8429405.
24. Faulkner, J.A., Jones, D.A., and Round, J.M. 1989. Injury to skeletal muscles of mice by forced lengthening during contractions. Q. J. Exp. Physiol. 74: 661-670. PMID:2594927.
25. Faulkner, J.A., Opiteck, J.A., and Brooks, S.V. 1992. Injury to skeletal muscle during altitude training: induction and prevention. Int. J. Sports Med. 13(Suppl. 1): S160-S162. PMID:1483761.
26. Geronilla, K.B., Miller, G.R., Mowrey, K.F., Wu, J.Z., Kashon, M.L., Brumbaugh, K., et al. 2003. Dynamic force responses of skeletal muscle during stretch-shortening cycles. Eur. J. Appl. Physiol. 90: 144-153. doi:10.1007/s00421-003-0849-8. PMID:14504946.
27. Gosselin, L.E. 2000. Attenuation of force deficit after lengthening contractions in soleus muscle from trained rats. J. Appl. Physiol. 88: 1254-1258. PMID:10749815.
28. Horita, T., Komi, P.V., Nicol, C., and Kyrolainen, H. 1999. Effect of exhausting stretch-shortening cycle exercise on the time course of mechanical behaviour in the drop jump: possible role of muscle damage. Eur. J. Appl. Physiol. Occup. Physiol. 79: 160-167. doi:10.1007/s004210050490. PMID:10029337.
29. Ingalls, C.P., Warren, G.L., Lowe, D.A., Boorstein, D.B., and Armstrong, R.B. 1996. Differential effects of anesthetics on in vivo skeletal muscle contractile function in the mouse. J. Appl. Physiol. 80: 332-340. PMID:8847324.
30. Ingalls, C.P., Warren, G.L., Williams, J.H., Ward, C.W., and Armstrong, R.B. 1998. E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions. J. Appl. Physiol. 85: 58-67. PMID:9655756.
31. Klitgaard, H., Brunet, A., Maton, B., Lamaziere, C., Lesty, C., and Monod, H. 1989a. Morphological and biochemical changes in old rat muscles: effect of increased use. J. Appl. Physiol. 67: 1409-1417. PMID:2793742.
32. Klitgaard, H., Marc, R., Brunet, A., Vandewalle, H., and Monod, H. 1989b. Contractile properties of old rat muscles: effect of increased use. J. Appl. Physiol. 67: 1401-1408. PMID:2529239.
33. Koh, T.J., Peterson, J.M., Pizza, F.X., and Brooks, S.V. 2003. Passive stretches protect skeletal muscle of adult and old mice from lengthening contraction-induced injury. J. Gerontol. A. Biol. Sci. Med. Sci. 58: 592-597. PMID:12865474.
34. Komi, P.V. 2000. stretch-shortening cycle: a powerful model to study normal and fatigued muscle. J. Biomech. 33: 1197-1206. doi:10.1016/S0021-9290(00)00064-6. PMID:10899328.
35. Lieber, R.L., and Friden, J. 1993. Muscle damage is not a function of muscle force but active muscle strain. J. Appl. Physiol. 74: 520-526. PMID:8458765.
36. Lowe, D.A., and Alway, S.E. 1999. Stretch-induced myogenin, MyoD, and MRF4 expression and acute hypertrophy in quail slow-tonic muscle are not dependent upon satellite cell proliferation. Cell Tissue Res. 296: 531-539. doi:10.1007/ S004410051314. PMID:10370140.
37. Lowe, D.A., Lund, T., and Alway, S.E. 1998. Hypertrophy-stimulated myogenic regulatory factor mRNA increases are attenuated in fast muscle of aged quails. Am. J. Physiol. 275: C155-C162. PMID:9688846.
38. Lynch, G.S., and Faulkner, J.A. 1998. Contraction-induced injury to single muscle fibers: velocity of stretch does not influence the force deficit. Am. J. Physiol. 275: C1548-C1554. PMID:9843716.
39. Macpherson, P.C., Schork, M.A., and Faulkner, J.A. 1996. Contraction-induced injury to single fiber segments from fast and slow muscles of rats by single stretches. Am. J. Physiol. 271: C1438-C1446. PMID:8944625.
40. Manfredi, T.G., Fielding, R.A., O'Reilly, K.P., Meredith, C.N., Lee, H.Y., and Evans, W.J. 1991. Plasma creatine kinase activity and exercise-induced muscle damage in older men. Med. Sci. Sports Exerc. 23: 1028-1034. PMID:1943622.
41. McBride, T.A., Gorin, F.A., and Carlsen, R.C. 1995. Prolonged recovery and reduced adaptation in aged rat muscle following eccentric exercise. Mech. Ageing Dev. 83: 185-200. doi:10.1016/ 0047-6374(95)01629-E. PMID:8583836.
42. Sacco, P., and Jones, D.A. 1992. The protective effect of damaging eccentric exercise against repeated bouts of exercise in the mouse tibialis anterior muscle. Exp. Physiol. 77: 757-760. PMID:1418957.
43. Stevens, E.D. 1996. Effect of phase of stimulation on acute damage caused by eccentric contractions in mouse soleus muscle. J. Appl. Physiol. 80: 1958-1962. PMID:8806900.
44. Stevens, E.D., and Faulkner, J.A. 2000. The capacity of mdx mouse diaphragm muscle to do oscillatory work. J. Physiol. 522: 457-466. doi:10.1111/j.1469-7793.2000.t01-3-00457.x. PMID:10713969.
45. Underwood, E.E. 1970. Quantatative stereology. Addison-Wesley Publishing Co., Reading, Mass.
46. Van Der Meulen, J.H., McArdle, A., Jackson, M.J., and Faulkner, J.A. 1997. Contraction-induced injury to the extensor digitorum longus muscles of rats: the role of vitamin E. J. Appl. Physiol. 83: 817-823. PMID:9292468.
47. Warren III, G.L., Williams, J.H., Ward, C.W., Matoba, H., Ingalls, C.P., Hermann, K.M., and Armstrong, R.B. 1996. Decreased contraction economy in mouse EDL muscle injured by eccentric contractions. J. Appl. Physiol. 81: 2555-2564. PMID:9018506.
48. Weibel, E.R. 1972. The value of stereology in analysing structure and function of cells and organs. J. Microsc. 95: 3-13. PMID:5067270.
49. Weibel, E.R. 1974. Selection of the best method in stereology. J. Microsc. 100: 261-269. PMID:4599320.
50. Weibel, E.R. 1975. Quantitation in morphology: possibilities and limits. Beitr. Pathol. 155: 1-17. PMID:1098647.
51. Willems, M.E., and Stauber, W.T. 2001. Force deficits after repeated stretches of activated skeletal muscles in female and male rats. Acta Physiol. Scand. 172: 63-67. doi:10.1046/j.1365-201X.2001.00808.x. PMID:11437740.
52. Wong, T.S., and Booth, F.W. 1990. Protein metabolism in rat tibialis anterior muscle after stimulated chronic eccentric exercise. J. Appl. Physiol. 69: 1718-1724. PMID:1703146.
53. Zerba, E., and Faulkner, J.A. 1990. A single lengthening contraction can induce injury to skeletal muscle fibers. Physiologist, 33: A122.
54. Zerba, E., Komorowski, T.E., and Faulkner, J.A. 1990. Free radical injury to skeletal muscles of young, adult, and old mice. Am. J. Physiol. 258: C429-C435. PMID:2316631.