Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 5 , Pages 617-625 , May 2007

Recovery of Function in Skeletal Muscle Following 2 Different Contraction-Induced Injuries

  • Richard M. Lovering, PT, PhD

      Affiliations

    • Department of Physiology, University of Maryland, School of Medicine, Baltimore, MD
    • Corresponding Author InformationReprint requests to Richard M. Lovering, PT, PhD, Dept of Physiology, University of Maryland, School of Medicine, 685 W Baltimore St, Baltimore, MD 21201
    • ,
  • Joseph A. Roche, PT

      Affiliations

    • Department of Physical Therapy & Rehabilitation Science, University of Maryland, School of Medicine, Baltimore, MD
    • ,
  • Robert J. Bloch, PhD

      Affiliations

    • Department of Physiology, University of Maryland, School of Medicine, Baltimore, MD
    • ,
  • Patrick G. De Deyne, MPT, PhD

      Affiliations

    • DePuy Biologics/Cell Biology and Preclinical Evaluation, Raynham, MA.

References 

  1. Rathbone CR, Wenke JC, Warren GL, Armstrong RB. Importance of satellite cells in the strength recovery after eccentric contraction-induced muscle injury. Am J Physiol Regul Integr Comp Physiol. 2003;285:R1490–R1495
  2. Lefaucheur JP, Sebille A. The cellular events of injured muscle regeneration depend on the nature of the injury. Neuromuscul Disord. 1995;5:501–509
  3. Aarimaa V, Rantanen J, Best T, Schultz E, Corr D, Kalimo H. Mild eccentric stretch injury in skeletal muscle causes transient effects on tensile load and cell proliferation. Scand J Med Sci Sports. 2004;14:367–372
  4. Hameed M, Orrell RW, Cobbold M, Goldspink G, Harridge SD. Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J Physiol. 2003;547:247–254
  5. Linderman JK, Gosselink KL, Booth FW, Mukku VR, Grindeland RE. Resistance exercise and growth hormone as countermeasures for skeletal muscle atrophy in hindlimb-suspended rats. Am J Physiol. 1994;267:R365–R371
  6. Yan Z, Biggs RB, Booth FW. Insulin-like growth factor immunoreactivity increases in muscle after acute eccentric contractions. J Appl Physiol. 1993;74:410–414
  7. Hill M, Wernig A, Goldspink G. Muscle satellite (stem) cell activation during local tissue injury and repair. J Anat. 2003;203:89–99
  8. Lieber RL, Thornell LE, Friden J. Muscle cytoskeletal disruption occurs within the first 15 min of cyclic eccentric contraction. J Appl Physiol. 1996;80:278–284
  9. Nosaka K, Sakamoto K, Newton M, Sacco P. The repeated bout effect of reduced-load eccentric exercise on elbow flexor muscle damage. Eur J Appl Physiol. 2001;85:34–40
  10. Pizza FX, Peterson JM, Baas JH, Koh TJ. Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice. J Physiol. 2005;562:899–913
  11. Lovering RM, De Deyne PG. Contractile function, sarcolemma integrity, and the loss of dystrophin after skeletal muscle eccentric contraction-induced injury. Am J Physiol Cell Physiol. 2004;286:C230–C238
  12. Lovering RM, Hakim M, Moorman CT, De Deyne PG. The contribution of contractile pre-activation to loss of function after a single lengthening contraction. J Biomech. 2005;38:1501–1507
  13. Hakim M, Hage W, Lovering RM, Moorman CT, Curl LA, De Deyne PG. Dexamethasone and recovery of contractile tension after a muscle injury. Clin Orthop Relat Res. 2005;439:235–242Oct
  14. MacIntyre DL, Reid WD, Lyster DM, McKenzie DC. Different effects of strenuous eccentric exercise on the accumulation of neutrophils in muscle in women and men. Eur J Appl Physiol. 2000;81:47–53
  15. MacIntyre DL, Reid WD, Lyster DM, Szasz IJ, McKenzie DC. Presence of WBC, decreased strength, and delayed soreness in muscle after eccentric exercise. J Appl Physiol. 1996;80:1006–1013
  16. Warren GL, Ingalls CP, Lowe DA, Armstrong RB. What mechanisms contribute to the strength loss that occurs during and in the recovery from skeletal muscle injury?. J Orthop Sports Phys Ther. 2002;32:58–64
  17. Faulkner JA, Brooks SV, Opiteck JA. Injury to skeletal muscle fibers during contractions: conditions of occurrence and prevention. Phys Ther. 1993;73:911–921
  18. Warren GL, Lowe DA, Armstrong RB. Measurement tools used in the study of eccentric contraction-induced injury. Sports Med. 1999;27:43–59
  19. Adams GR, Caiozzo VJ, Haddad F, Baldwin KM. Cellular and molecular responses to increased skeletal muscle loading after irradiation. Am J Physiol Cell Physiol. 2002;283:C1182–C1195
  20. Martins KJ, Gordon T, Pette D, et al. Effect of satellite cell ablation on low-frequency stimulated fast-to-slow fibre type transitions in rat skeletal muscle. J Physiol. 2006;572(Pt 1):281–294
  21. Yan Z, Choi S, Liu X, et al. Highly coordinated gene regulation in mouse skeletal muscle regeneration. J Biol Chem. 2003;278:8826–8836
  22. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156–159
  23. Brooks SV, Zerba E, Faulkner JA. Injury to muscle fibres after single stretches of passive and maximally stimulated muscles in mice. J Physiol. 1995;488(Pt 2):459–469
  24. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol. 2001;91:534–551
  25. Garry DJ, Yang Q, Bassel-Duby R, Williams RS. Persistent expression of MNF identifies myogenic stem cells in postnatal muscles. Dev Biol. 1997;188:280–294
  26. Hamer PW, McGeachie JM, Davies MJ, Grounds MD. Evans Blue Dye as an in vivo marker of myofibre damage: optimising parameters for detecting initial myofibre membrane permeability. J Anat. 2002;200:69–79
  27. Irintchev A, Langer M, Zweyer M, Theisen R, Wernig A. Functional improvement of damaged adult mouse muscle by implantation of primary myoblasts. J Physiol. 1997;500(Pt 3):775–785
  28. Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84:209–238
  29. Fisher BD, Baracos VE, Shnitka TK, Mendryk SW, Reid DC. Ultrastructural events following acute muscle trauma. Med Sci Sports Exerc. 1990;22:185–193
  30. Rosenblatt JD, Yong D, Parry DJ. Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve. 1994;17:608–613
  31. Rosenblatt JD, Parry DJ. Adaptation of rat extensor digitorum longus muscle to gamma irradiation and overload. Pflugers Arch. 1993;423:255–264
  32. Best TM, Hunter KD. Muscle injury and repair. Phys Med Rehabil Clin N Am. 2000;11:251–266
  33. Tidball JG. Inflammatory processes in muscle injury and repair. Am J Physiol Regul Integr Comp Physiol. 2005;288:R345–R353
  34. Heslop L, Morgan JE, Partridge TA. Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci. 2000;113(Pt 12):2299–2308
  35. McNeil PL, Terasaki M. Coping with the inevitable: how cells repair a torn surface membrane. Nat Cell Biol. 2001;3:E124–E129
  36. Papadimitriou JM, Robertson TA, Mitchell CA, Grounds MD. The process of new plasmalemma formation in focally injured skeletal muscle fibers. J Struct Biol. 1990;103:124–134
  37. Bansal D, Miyake K, Vogel SS, et al. Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature. 2003;423:168–172
  38. Lennon NJ, Kho A, Bacskai BJ, Perlmutter SL, Hyman BT, Brown RH. Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing. J Biol Chem. 2003;278:50466–50473
  39. Doherty KR, McNally EM. Repairing the tears: dysferlin in muscle membrane repair. Trends Mol Med. 2003;9:327–330
  40. Mozdziak PE, Schultz E, Cassens RG. The effect of in vivo and in vitro irradiation (25 Gy) on the subsequent in vitro growth of satellite cells. Cell Tissue Res. 1996;283:203–208
  41. d’Albis A, Couteaux R, Janmot C, Roulet A, Mira JC. Regeneration after cardiotoxin injury of innervated and denervated slow and fast muscles of mammals (Myosin isoform analysis). Eur J Biochem. 1988;174:103–110
  42. Harris JB, Johnson MA. Further observations on the pathological responses of rat skeletal muscle to toxins isolated from the venom of the Australian tiger snake, Notechis scutatus scutatus. Clin Exp Pharmacol Physiol. 1978;5:587–600
  43. Hall-Craggs EC, Seyan HS. Histochemical changes in innervated and denervated skeletal muscle fibers following treatment with bupivacaine (marcain). Exp Neurol. 1975;46:345–354
  44. Fukushima K, Badlani N, Usas A, Riano F, Fu F, Huard J. The use of an antifibrosis agent to improve muscle recovery after laceration. Am J Sports Med. 2001;29:394–402
  45. Schultz E, Jaryszak DL, Valliere CR. Response of satellite cells to focal skeletal muscle injury. Muscle Nerve. 1985;8:217–222
  46. Hurme T, Kalimo H. Activation of myogenic precursor cells after muscle injury. Med Sci Sports Exerc. 1992;24:197–205
  47. Irintchev A, Wernig A. Muscle damage and repair in voluntarily running mice: strain and muscle differences. Cell Tissue Res. 1987;249:509–521
  48. McCully KK, Faulkner JA. Injury to skeletal muscle fibers of mice following lengthening contractions. J Appl Physiol. 1985;59:119–126
  49. Appell HJ, Forsberg S, Hollmann W. Satellite cell activation in human skeletal muscle after training: evidence for muscle fiber neoformation. Int J Sports Med. 1988;9:297–299
  50. Vierck J, O’Reilly B, Hossner K, et al. Satellite cell regulation following myotrauma caused by resistance exercise. Cell Biol Int. 2000;24:263–272
  51. Garry DJ, Meeson A, Elterman J, et al. Myogenic stem cell function is impaired in mice lacking the forkhead/winged helix protein MNF. Proc Natl Acad Sci U S A. 2000;97:5416–5421
  52. Creuzet S, Lescaudron L, Li Z, Fontaine-Perus J. MyoD, myogenin, and desmin-nls-lacZ transgene emphasize the distinct patterns of satellite cell activation in growth and regeneration. Exp Cell Res. 1998;243:241–253
  53. Kurek JB, Bower JJ, Romanella M, Koentgen F, Murphy M, Austin L. The role of leukemia inhibitory factor in skeletal muscle regeneration. Muscle Nerve. 1997;20:815–822
  54. Pavlath GK, Thaloor D, Rando TA, Cheong M, English AW, Zheng B. Heterogeneity among muscle precursor cells in adult skeletal muscles with differing regenerative capacities. Dev Dyn. 1998;212:495–508
  55. Mitchell CA, McGeachie JK, Grounds MD. Cellular differences in the regeneration of murine skeletal muscle: a quantitative histological study in SJL/J and BALB/c mice. Cell Tissue Res. 1992;269:159–166
  56. Tidball JG, Wehling-Henricks M. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J Physiol. 2007;578:327–336
  57. Bondesen BA, Mills ST, Kegley KM, Pavlath GK. The COX-2 pathway is essential during early stages of skeletal muscle regeneration. Am J Physiol Cell Physiol. 2004;287:C475–C483
  58. Mendias CL, Tatsumi R, Allen RE. Role of cyclooxygenase-1 and -2 in satellite cell proliferation, differentiation, and fusion. Muscle Nerve. 2004;30:497–500
  59. Toumi H, Best TM. The inflammatory response: friend or enemy for muscle injury?. Br J Sports Med. 2003;37:284–286

 Supported in part by the University of Maryland Muscle Biology Training Program, National Institutes of Health (grant nos. T32 AR07592, F32 HD047099-02, K01 HD 01165), the Muscular Dystrophy Association, and the National Football League Charities.

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated.

PII: S0003-9993(07)00107-4

doi: 10.1016/j.apmr.2007.02.010

Archives of Physical Medicine and Rehabilitation
Volume 88, Issue 5 , Pages 617-625 , May 2007

Article Tools

* Image Usage & Resolution