Eccentric exercise induces chronic alterations in musculoskeletal nociception in the rat

European Journal of Neuroscience

Volumn 32, Issue 5, 2010, Pages 819-825

  Alvarez, Pedro ^a   Levine, Jon D ^a   Green, Paul G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

hyperalgesia; interleukin 6; muscle; prostaglandin E2; protein kinase C ; tumor necrosis factor

Indexed keywords

INTERLEUKIN 6; OLIGODEOXYNUCLEOTIDE; PROSTAGLANDIN E2; PROTEIN KINASE C EPSILON;

ANIMAL EXPERIMENT; ARTICLE; CHRONIC PAIN; ECCENTRIC MUSCLE CONTRACTION; EXERCISE; GASTROCNEMIUS MUSCLE; HYPERALGESIA; INFLAMMATION; MALE; MYALGIA; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; DINOPROSTONE; DISEASE MODELS, ANIMAL; HINDLIMB; HYPERALGESIA; INTERLEUKIN-6; MALE; MUSCLE, SKELETAL; MUSCULOSKELETAL DISEASES; OLIGODEOXYRIBONUCLEOTIDES, ANTISENSE; PAIN; PHYSICAL CONDITIONING, ANIMAL; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 77956417515     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07359.x     Document Type: Article

References (63)

1. Alessandri-Haber, N., Yeh, J.J., Boyd, A.E., Parada, C.A., Chen, X., Reichling, D.B. Levine, J.D. (2003) Hypotonicity induces TRPV4-mediated nociception in rat. Neuron, 39, 497 511.
2. Alessandri-Haber, N., Dina, O.A., Yeh, J.J., Parada, C.A., Reichling, D.B. Levine, J.D. (2004) Transient receptor potential vanilloid 4 is essential in chemotherapy-induced neuropathic pain in the rat. J. Neurosci., 24, 4444 4452.
3. Aley, K.O. Levine, J.D. (1997) Multiple receptors involved in peripheral alpha 2, mu, and A1 antinociception, tolerance, and withdrawal. J. Neurosci., 17, 735 744.
4. Aley, K.O., Messing, R.O., Mochly-Rosen, D. Levine, J.D. (2000) Chronic hypersensitivity for inflammatory nociceptor sensitization mediated by the epsilon isozyme of protein kinase C. J. Neurosci., 20, 4680 4685.
5. Al-Shatti, T., Barr, A.E., Safadi, F.F., Amin, M. Barbe, M.F. (2005) Increase in inflammatory cytokines in median nerves in a rat model of repetitive motion injury. J. Neuroimmunol., 167, 13 22.
6. Alund, M., Larsson, S.E. Lewin, T. (1992) Work-related chronic neck impairment. Neck motion analysis in female traverse crane operators. Scand. J. Rehabil. Med., 24, 133 139.
7. Barbe, M.F., Barr, A.E., Gorzelany, I., Amin, M., Gaughan, J.P. Safadi, F.F. (2003) Chronic repetitive reaching and grasping results in decreased motor performance and widespread tissue responses in a rat model of MSD. J. Orthop. Res., 21, 167 176.
8. Barr, A.E. Barbe, M.F. (2002) Pathophysiological tissue changes associated with repetitive movement: a review of the evidence. Phys. Ther., 82, 173 187.
9. Betts, J.A., Toone, R.J., Stokes, K.A. Thompson, D. (2009) Systemic indices of skeletal muscle damage and recovery of muscle function after exercise: effect of combined carbohydrate-protein ingestion. Appl. Physiol. Nutr. Metab., 34, 773 784.
10. Beyreuther, B.K., Geis, C., Stohr, T. Sommer, C. (2007) Antihyperalgesic efficacy of lacosamide in a rat model for muscle pain induced by TNF. Neuropharmacology, 52, 1312 1317.
11. Buford, T.W., Cooke, M.B., Shelmadine, B.D., Hudson, G.M., Redd, L. Willoughby, D.S. (2009) Effects of eccentric treadmill exercise on inflammatory gene expression in human skeletal muscle. Appl. Physiol. Nutr. Metab., 34, 745 753.
12. Croft, L., Bartlett, J.D., Maclaren, D.P., Reilly, T., Evans, L., Mattey, D.L., Nixon, N.B., Drust, B. Morton, J.P. (2009) High-intensity interval training attenuates the exercise-induced increase in plasma IL-6 in response to acute exercise. Appl. Physiol. Nutr. Metab., 34, 1098 1107.
13. Dalsgaard, M.K., Ott, P., Dela, F., Juul, A., Pedersen, B.K., Warberg, J., Fahrenkrug, J. Secher, N.H. (2004) The CSF and arterial to internal jugular venous hormonal differences during exercise in humans. Exp. Physiol., 89, 271 277.
14. Diehl, B., Hoheisel, U. Mense, S. (1993) The influence of mechanical stimuli and of acetylsalicylic acid on the discharges of slowly conducting afferent units from normal and inflamed muscle in the rat. Exp. Brain Res., 92, 431 440.
15. Dina, O.A., Parada, C.A., Yeh, J., Chen, X., McCarter, G.C. Levine, J.D. (2004) Integrin signaling in inflammatory and neuropathic pain in the rat. Eur. J. Neurosci., 19, 634 642.
16. Dina, O.A., Hucho, T., Yeh, J., Malik-Hall, M., Reichling, D.B. Levine, J.D. (2005) Primary afferent second messenger cascades interact with specific integrin subunits in producing inflammatory hyperalgesia. Pain, 115, 191 203.
17. Dina, O.A., Green, P.G. Levine, J.D. (2008a) Role of interleukin-6 in chronic muscle hyperalgesic priming. Neuroscience, 152, 521 525.
18. Dina, O.A., Levine, J.D. Green, P.G. (2008b) Muscle inflammation induces a protein kinase c epsilon-dependent chronic-latent muscle pain. J. Pain, 9, 457 462.
19. Dina, O.A., Joseph, E.K., Levine, J.D. Green, P.G. (2010) Mechanisms mediating vibration-induced chronic musculoskeletal pain analyzed in the rat. J. Pain, 11, 369 377.
20. Gerdle, B., Lemming, D., Kristiansen, J., Larsson, B., Peolsson, M. Rosendal, L. (2007) Biochemical alterations in the trapezius muscle of patients with chronic whiplash associated disorders (WAD) - A microdialysis study. Eur. J. Pain, 12, 82 93.
21. Hamada, K., Vannier, E., Sacheck, J.M., Witsell, A.L. Roubenoff, R. (2005) Senescence of human skeletal muscle impairs the local inflammatory cytokine response to acute eccentric exercise. FASEB J., 19, 264 266.
22. Hoheisel, U., Unger, T. Mense, S. (2005) Excitatory and modulatory effects of inflammatory cytokines and neurotrophins on mechanosensitive group IV muscle afferents in the rat. Pain, 114, 168 176.
23. Jones, D.A., Newham, D.J., Round, J.M. Tolfree, S.E. (1986) Experimental human muscle damage: morphological changes in relation to other indices of damage. J. Physiol., 375, 435 448.
24. Jonsdottir, I.H., Schjerling, P., Ostrowski, K., Asp, S., Richter, E.A. Pedersen, B.K. (2000) Muscle contractions induce interleukin-6 mRNA production in rat skeletal muscles. J. Physiol., 528 (Pt 1 157 163.
25. Joseph, E.K., Parada, C.A. Levine, J.D. (2003) Hyperalgesic priming in the rat demonstrates marked sexual dimorphism. Pain, 105, 143 150.
26. Joseph, E.K., Bogen, O., Alessandri-Haber, N. Levine, J.D. (2007) PLC-beta 3 signals upstream of PKC epsilon in acute and chronic inflammatory hyperalgesia. Pain, 132, 67 73.
27. Kano, Y., Sampei, K. Matsudo, H. (2004) Time course of capillary structure changes in rat skeletal muscle following strenuous eccentric exercise. Acta Physiol. Scand., 180, 291 299.
28. Kano, Y., Masuda, K., Furukawa, H., Sudo, M., Mito, K. Sakamoto, K. (2008) Histological skeletal muscle damage and surface EMG relationships following eccentric contractions. J. Physiol. Sci., 58, 349 355.
29. Keller, C., Steensberg, A., Hansen, A.K., Fischer, C.P., Plomgaard, P. Pedersen, B.K. (2005a) Effect of exercise, training, and glycogen availability on IL-6 receptor expression in human skeletal muscle. J. Appl. Physiol., 99, 2075 2079.
30. Keller, P., Penkowa, M., Keller, C., Steensberg, A., Fischer, C.P., Giralt, M., Hidalgo, J. Pedersen, B.K. (2005b) Interleukin-6 receptor expression in contracting human skeletal muscle: regulating role of IL-6. FASEB J., 19, 1181 1183.
31. Khasar, S.G., Gold, M.S., Dastmalchi, S. Levine, J.D. (1996) Selective attenuation of mu-opioid receptor-mediated effects in rat sensory neurons by intrathecal administration of antisense oligodeoxynucleotides. Neurosci. Lett., 218, 17 20.
32. Khasar, S.G., Gold, M.S. Levine, J.D. (1998) A tetrodotoxin-resistant sodium current mediates inflammatory pain in the rat. Neurosci. Lett., 256, 17 20.
33. Koltzenburg, M., Wall, P.D. McMahon, S.B. (1999) Does the right side know what the left is doing? Trends Neurosci., 22, 122 127.
34. Levine, J.D., Dardick, S.J., Basbaum, A.I. Scipio, E. (1985) Reflex neurogenic inflammation. I. Contribution of the peripheral nervous system to spatially remote inflammatory responses that follow injury. J. Neurosci., 5, 1380 1386.
35. Liao, P., Zhou, J., Ji, L.L. Zhang, Y. (2010) Eccentric contraction induces inflammatory responses in rat skeletal muscle: role of tumor necrosis factor [alpha]. Am. J. Physiol. Regul. Integr. Comp. Physiol., 298, R599 R607.
36. Meckel, Y., Eliakim, A., Seraev, M., Zaldivar, F., Cooper, D.M., Sagiv, M. Nemet, D. (2009) The effect of a brief sprint interval exercise on growth factors and inflammatory mediators. J. Strength Cond. Res., 23, 225 230.
37. Mortensen, O.H., Andersen, K., Fischer, C., Nielsen, A.R., Nielsen, S., Akerstrom, T., Aastrom, M.B., Borup, R. Pedersen, B.K. (2008) Calprotectin is released from human skeletal muscle tissue during exercise. J. Physiol., 586, 3551 3562.
38. Muller-Newen, G. (2003) The cytokine receptor gp130: faithfully promiscuous. Sci. STKE, 2003, PE40.
39. Murase, S., Terazawa, E., Queme, F., Ota, H., Matsuda, T., Hirate, K., Kozaki, Y., Katanosaka, K., Taguchi, T., Urai, H. Mizumura, K. (2010) Bradykinin and nerve growth factor play pivotal roles in muscular mechanical hyperalgesia after exercise (delayed-onset muscle soreness). J. Neurosci., 30, 3752 3761.
40. Ochi, E., Nakazato, K. Ishii, N. (2007) Effects of eccentric exercise on joint stiffness and muscle connectin (titin) isoform in the rat hindlimb. J. Physiol. Sci., 57, 1 6.
41. Parada, C.A., Yeh, J.J., Joseph, E.K. Levine, J.D. (2003a) Tumor necrosis factor receptor type-1 in sensory neurons contributes to induction of chronic enhancement of inflammatory hyperalgesia in rat. Eur. J. Neurosci., 17, 1847 1852.
42. Parada, C.A., Yeh, J.J., Reichling, D.B. Levine, J.D. (2003b) Transient attenuation of protein kinase C epsilon can terminate a chronic hyperalgesic state in the rat. Neuroscience, 120, 219 226.
43. Parada, C.A., Reichling, D.B. Levine, J.D. (2005) Chronic hyperalgesic priming in the rat involves a novel interaction between cAMP and PKCepsilon second messenger pathways. Pain, 113, 185 190.
44. Pedersen, B.K. (2009) Edward F. Adolph distinguished lecture: muscle as an endocrine organ: IL-6 and other myokines. J. Appl. Physiol., 107, 1006 1014.
45. Pedersen, B.K. Febbraio, M.A. (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol. Rev., 88, 1379 1406.
46. Rice, T.L., Chantler, I. Loram, L.C. (2008) Neutralisation of muscle tumour necrosis factor alpha does not attenuate exercise-induced muscle pain but does improve muscle strength in healthy male volunteers. Br. J. Sports Med., 42, 758 762.
47. Rosa Neto, J.C., Lira, F.S., Oyama, L.M., Zanchi, N.E., Yamashita, A.S., Batista, M.L.J., Oller do Nascimento, C.M. Seelaender, M. (2009) Exhaustive exercise causes an anti-inflammatory effect in skeletal muscle and a pro-inflammatory effect in adipose tissue in rats. Eur. J. Appl. Physiol., 106, 697 704.
48. Rosendal, L., Kristiansen, J., Gerdle, B., Sogaard, K., Peolsson, M., Kjaer, M., Sorensen, J. Larsson, B. (2005a) Increased levels of interstitial potassium but normal levels of muscle IL-6 and LDH in patients with trapezius myalgia. Pain, 119, 201 209.
49. Rosendal, L., Sogaard, K., Kjaer, M., Sjogaard, G., Langberg, H. Kristiansen, J. (2005b) Increase in interstitial interleukin-6 of human skeletal muscle with repetitive low-force exercise. J. Appl. Physiol., 98, 477 481.
50. Schafers, M., Sorkin, L.S. Sommer, C. (2003) Intramuscular injection of tumor necrosis factor-alpha induces muscle hyperalgesia in rats. Pain, 104, 579 588.
51. Shah, J.P., Phillips, T.M., Danoff, J.V. Gerber, L.H. (2005) An in vivo microanalytical technique for measuring the local biochemical milieu of human skeletal muscle. J. Appl. Physiol., 99, 1977 1984.
52. Shah, J.P., Danoff, J.V., Desai, M.J., Parikh, S., Nakamura, L.Y., Phillips, T.M. Gerber, L.H. (2008) Biochemicals associated with pain and inflammation are elevated in sites near to and remote from active myofascial trigger points. Arch. Phys. Med. Rehabil., 89, 16 23.
53. Sluka, K.A. Rasmussen, L.A. (2010) Fatiguing exercise enhances hyperalgesia to muscle inflammation. Pain, 148, 188 197.
54. Sluka, K.A., Radhakrishnan, R., Benson, C.J., Eshcol, J.O., Price, M.P., Babinski, K., Audette, K.M., Yeomans, D.C. Wilson, S.P. (2007) ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain, 129, 102 112.
55. Smith, L.L., McKune, A.J., Semple, S.J., Sibanda, E., Steel, H. Anderson, R. (2007) Changes in serum cytokines after repeated bouts of downhill running. Appl. Physiol. Nutr. Metab., 32, 233 240.
56. Stauber, W.T. (2004) Factors involved in strain-induced injury in skeletal muscles and outcomes of prolonged exposures. J. Electromyogr. Kinesiol., 14, 61 70.
57. Steensberg, A., van Hall, G., Osada, T., Sacchetti, M., Saltin, B. Klarlund Pedersen, B. (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J. Physiol., 529 (Pt 1 237 242.
58. Steensberg, A., Dalsgaard, M.K., Secher, N.H. Pedersen, B.K. (2006) Cerebrospinal fluid IL-6, HSP72, and TNF-alpha in exercising humans. Brain Behav. Immun., 20, 585 589.
59. Summer, G.J., Romero-Sandoval, E.A., Bogen, O., Dina, O.A., Khasar, S.G. Levine, J.D. (2008) Proinflammatory cytokines mediating burn-injury pain. Pain, 135, 98 107.
60. Taguchi, T., Matsuda, T., Tamura, R., Sato, J. Mizumura, K. (2005) Muscular mechanical hyperalgesia revealed by behavioural pain test and c-Fos expression in the spinal dorsal horn after eccentric contraction in rats. J. Physiol., 564, 259 268.
61. Toft, A.D., Jensen, L.B., Bruunsgaard, H., Ibfelt, T., Halkjaer-Kristensen, J., Febbraio, M. Pedersen, B.K. (2002) Cytokine response to eccentric exercise in young and elderly humans. Am. J. Physiol. Cell Physiol., 283, C289 C295.
62. Tomiya, A., Aizawa, T., Nagatomi, R., Sensui, H. Kokubun, S. (2004) Myofibers express IL-6 after eccentric exercise. Am. J. Sports Med., 32, 503 508.
63. Wang, Y., Nesbitt, J.E., Fuentes, N.L. Fuller, G.M. (1992) Molecular cloning and characterization of the rat liver IL-6 signal transducing molecule, gp130. Genomics, 14, 666 672.