Targeting interleukin-1β reduces intense acute swimming-induced muscle mechanical hyperalgesia in mice

Journal of Pharmacy and Pharmacology

Volumn 66, Issue 7, 2014, Pages 1009-1020

  Borghi, Sergio M ^a   Zarpelon, Ana C ^a   Pinho Ribeiro, Felipe A ^a   Cardoso, Renato D R ^a   Cunha, Thiago M ^b   Alves Filho, José C ^b   Ferreira, Sergio H ^b   Cunha, Fernando Q ^b   Casagrande, Rubia ^a   Verri, Waldiceu A ^a  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

cytokine; DOMS; mice; muscle mechanical hyperalgesia; oxidative stress; pain

Indexed keywords

CREATINE KINASE; GLUCOSE; GLUTATHIONE; HYDROCORTISONE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1BETA; LACTIC ACID; PEROXIDASE;

ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; ENZYME ACTIVITY; GASTROCNEMIUS MUSCLE; HYPERALGESIA; MALE; MOUSE; MUSCLE CELL; NOCICEPTION; NONHUMAN; OXIDATIVE STRESS; PROTEIN FUNCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; SPINAL CORD; SWIMMING; ANIMAL; BLOOD; DRUG EFFECTS; METABOLISM; MUSCULOSKELETAL PAIN; PATHOLOGY;

ANIMALS; CREATINE KINASE; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; HYPERALGESIA; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1BETA; MALE; MICE; MUSCLE CELLS; MUSCLE, SKELETAL; MUSCULOSKELETAL PAIN; PEROXIDASE; SPINAL CORD; SWIMMING;

EID: 84902546361     PISSN: 00223573     EISSN: 20427158     Source Type: Journal    
DOI: 10.1111/jphp.12226     Document Type: Article

References (68)

1. Ebbeling CB, Clarkson PM,. Exercise-induced muscle damage and adaption. Sports Med 1989; 7: 207-234.
2. Armstrong RB,. Mechanisms of exercise-induced delayed onset muscle soreness: a brief review. Med Sci Sports Exerc 1984; 16: 1864-1868.
3. McIntyre DL, et al. Delayed muscle soreness. The inflammatory response to muscle injury and its clinical implications. Sports Med 1995; 20: 24-40.
4. Cheung K, et al. Delayed onset muscle soreness: treatment strategies and performance factors. Sports Med 2003; 33: 145-164.
5. Munehiro T, et al. Establishment of an animal model for delayed-onset muscle soreness after high-intensity eccentric exercise and its application for investigating the efficacy of low-load eccentric training. J Orthop Sci 2012; 17: 244-252.
6. Graven-Nielsen T, Arendt-Nielsen L,. Induction and assessment of muscle pain, referred pain, and muscular hyperalgesia. Curr Pain Headache Rep 2003; 7: 443-451.
7. Alvarez P, et al. Eccentric exercise induces chronic alterations in musculoskeletal nociception in the rat. Eur J Neurosci 2010; 32: 819-825.
8. Verri WA Jr, et al. Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 2006; 112: 116-138.
9. Ferreira SH, et al. Interleukin-1 beta as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature 1988; 334: 698-700.
10. Loram LC, et al. Cytokine profiles during carrageenan-induced inflammatory hyperalgesia in rat muscle and hind paw. J Pain 2007; 8: 127-136.
11. Liburt NR, et al. Exercise-induced increases in inflammatory cytokines in muscle and blood of horses. Equine Vet J Suppl 2010; 38: 280-288.
12. Pedersen BK, et al. The cytokine response to strenuous exercise. Can J Physiol Pharmacol 1998; 76: 505-511.
13. Meier B, et al. Human fibroblasts release reactive oxygen species in response to interleukin-1 or tumour necrosis factor-alpha. Biochem J 1989; 263: 539-545.
14. Jiménez-Altayõ F, et al. Increased superoxide anion production by interleukin-1beta impairs nitric oxide-mediated relaxation in resistance arteries. J Pharmacol Exp Ther 2006; 316: 42-52.
15. Powers SK, Jackson MJ,. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 2008; 88: 1243-1276.
16. Izquierdo M, et al. Cytokine and hormone responses to resistance training. Eur J Appl Physiol 2009; 107: 397-409.
17. Smith LL,. Acute inflammation: the underlying mechanism in delayed onset muscle soreness? Med Sci Sports Exerc 1991; 23: 542-551.
18. Friden J, et al. Myofibrillar damage following eccentric exercise in man. Int J Sports Med 1983; 4: 170-176.
19. Armstrong RB, et al. Eccentric exercise-induced injury to rat skeletal muscle. J Appl Physiol 1983; 54: 80-93.
20. Carlson BM, Faulkner JA,. The regeneration of skeletal muscle fibres following Injury: a review. Med Sci Sports Exerc 1983; 15: 187-198.
21. Cannon JG, et al. Increased interleukin 1 beta in human skeletal muscle after exercise. Am J Physiol 1989; 257 (2 Pt 2): R451-R455.
22. Lewis PB, et al. Muscle soreness and delayed-onset muscle soreness. Clin Sports Med 2012; 31: 255-262.
23. Martins-Pinge MC, et al. Attenuated pressor responses to amino acids in the rostral ventrolateral medulla after swimming training in conscious rats. Auton Neurosci 2005; 112: 21-28.
24. Kuphal KE, et al. Extended swimming exercise reduces inflammatory and peripheral neuropathic pain in rodents. J Pain 2007; 8: 989-997.
25. Cunha TM, et al. An electronic pressure-meter nociception paw test for mice. Braz J Med Biol Res 2004; 37: 401-407.
26. Guerrero AT, et al. Hypernociception elicited by tibio-tarsal joint flexion in mice: a novel experimental arthritis model for pharmacological screening. Pharmacol Biochem Behav 2006; 84: 244-251.
27. Verri WA Jr, et al. IL-33 mediates antigen-induced cutaneous and articular hypernociception in mice. Proc Natl Acad Sci U S A 2008; 105: 2723-2728.
28. Casagrande R, et al. Protective effect of topical formulations containing quercetin against UVB-induced oxidative stress in hairless mice. J Photochem Photobiol B 2006; 84: 21-27.
29. Navarro SA, et al. Analgesic activity of piracetam: effect on cytokine production and oxidative stress. Pharmacol Biochem Behav 2013; 13: 64-66.
30. Borghi SM, et al. Vitexin inhibits inflammatory pain in mice by targeting TRPV1, oxidative stress, and cytokines. J Nat Prod 2013; 76: 1141-1149.
31. Zarpelon AC, et al. IL-33/ST2 signalling contributes to carrageenin-induced innate inflammation and inflammatory pain: role of cytokines, endothelin-1 and prostaglandin E2. Br J Pharmacol 2013; 169: 90-101.
32. Zarpelon AC, et al. The nitroxyl donor, Angeli's salt, inhibits inflammatory hyperalgesia in rats. Neuropharmacology 2013; 71: 1-9.
33. Verri WA Jr, et al. IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy. Ann Rheum Dis 2010; 69: 1697-1703.
34. Imbe H, et al. Stress-induced hyperalgesia: animal models and putative mechanisms. Front Biosci 2006; 11: 2179-2192.
35. Oka T, et al. Intracerebroventricular injection of interleukin-1 beta induced hyperalgesia in rats. Brain Res 1993; 624: 61-68.
36. 2 in the brain. Ann N Y Acad Sci 1998; 840: 269-281.
37. Cunha JM, et al. Cytokine-mediated inflammatory hyperalgesia limited by interleukin-1 receptor antagonist. Br J Pharmacol 2000; 130: 1418-1424.
38. Schafers M, et al. Combined epineurial therapy with neutralizing antibodies to tumor necrosis factor-alpha and interleukin-1 receptor has an additive effect in reducing neuropathic pain in mice. Neurosci Lett 2001; 310: 113-116.
39. Zelenka M, et al. Intraneural injection of interleukin-1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 2005; 116: 257-263.
40. Bonyadi M, et al. The effect of regular training on plasma cytokine response in healthy and diabetic rats. Saudi Med J 2009; 30: 1390-1394.
41. Shah JP, et al. Biochemicals associated with pain and inflammation are elevated in sites near to and remote from active myofascial trigger points. Arch Phys Med Rehabil 2008; 89: 16-23.
42. Chen YW, et al. Molecular responses of human muscle to eccentric exercise. J Appl Physiol 2003; 95: 2485-2494.
43. Konrad M, et al. The acute effect of ingesting a quercetin-based supplement on exercise-induced inflammation and immune changes in runners. Int J Sport Nutr Exerc Metab 2011; 21: 338-346.
44. Przybyla B, et al. Aging alters macrophage properties in human skeletal muscle both at rest and in response to acute resistance exercise. Exp Gerontol 2006; 41: 320-327.
45. Gao YJ, Ji RR,. Chemokines, neuronal-glial interactions, and central processing of neuropathic pain. Pharmacol Ther 2010; 126: 56-68.
46. Faccioli LH, et al. Recombinant interleukin-1 and tumor necrosis factor induce neutrophil migration 'in vivo' by indirect mechanisms. Agents Actions 1990; 30: 344-349.
47. Cunha TM, et al. Crucial role of neutrophils in the development of mechanical inflammatory hypernociception. J Leukoc Biol 2008; 83: 824-832.
48. Guerrero AT, et al. Involvement of LTB4 in zymosan-induced joint nociception in mice: participation of neutrophils and PGE2. J Leukoc Biol 2008; 83: 122-130.
49. Malm C, et al. Immunological changes in human skeletal muscle and blood after eccentric exercise and multiple biopsies. J Physiol 2000; 529 (Pt 1): 243-262.
50. Morozov VI, et al. The effects of high-intensity exercise on skeletal muscle neutrophil myeloperoxidase in untrained and trained rats. Eur J Appl Physiol 2006; 97: 716-722.
51. Henrique de Araujo T, et al. Intracellular localization of myeloperoxidase in murine peritoneal B-lymphocytes and macrophages. Cell Immunol 2013; 281: 27-30.
52. Criswell D, et al. High intensity training-induced changes in skeletal muscle antioxidant enzyme activity. Med Sci Sports Exerc 1993; 25: 1135-1140.
53. Augusto V, et al. Skeletal muscle fiber types in C57BL6J mice. Braz J Morphol Sci 2004; 21: 89-94.
54. Sale DG,. Influence of exercise and training on motor unit activation. Exerc Sport Sci Rev 1987; 15: 95-151.
55. Huang KF, et al. Interleukin-1 receptor antagonist inhibits the release of glutamate, hydroxyl radicals, and prostaglandin E(2) in the hypothalamus during pyrogen-induced fever in rabbits. Eur J Pharmacol 2010; 629: 125-131.
56. Wang ZQ, et al. A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 2004; 309: 869-878.
57. Verri WA Jr, et al. eds. Flavonoids as anti-inflammatory and analgesic drugs: mechanisms of action and perspectives in the development of pharmaceutical forms. In:, Atta-ur-Hahman FRS, ed. Studies in Natural Products Chemistry, Vol. 36. Amsterdam: Elsevier, 2012: 297-322.
58. Wittmack EK, et al. Voltage-gated sodium channel Nav1.6 is modulated by p38 mitogen-activated protein kinase. J Neurosci 2005; 25: 6621-6630.
59. Hudmon A, et al. Phosphorylation of sodium channel Na(v)1.8 by p38 mitogen-activated protein kinase increases current density in dorsal root ganglion neurons. J Neurosci 2008; 28: 3190-3201.
60. Diaz-Ruiz A, et al. Differential time-course of the increase of antioxidant thiol-defenses in the acute phase after spinal cord injury in rats. Neurosci Lett 2009; 452: 56-59.
61. Guedes RP, et al. Sciatic nerve transection increases gluthatione antioxidant system activity and neuronal nitric oxide synthase expression in the spinal cord. Brain Res Bull 2009; 80: 422-427.
62. Quintero L, et al. Long-lasting delayed hyperalgesia after subchronic swim stress. Pharmacol Biochem Behav 2000; 67: 449-458.
63. Quintero L, et al. Repeated swim stress increases pain-induced expression of c-Fos in the rat lumbar cord. Brain Res 2003; 965: 259-268.
64. Suarez-Roca H, et al. Stress-induced muscle and cutaneous hyperalgesia: differential effect of milnacipran. Physiol Behav 2006; 88: 82-87.
65. Mazzardo-Martins L, et al. High-intensity extended swimming exercise reduces pain-related behavior in mice: involvement of endogenous opioids and the serotonergic system. J Pain 2010; 11: 1384-1393.
66. Authier FJ, et al. Differential expression of the IL-1 system components during in vitro myogenesis: implication of IL-1beta in induction of myogenic cell apoptosis. Cell Death Differ 1999; 6: 1012-1021.
67. Di Matteo MA, et al. Superoxide, nitric oxide, peroxynitrite and cytokine combinations all cause functional impairment and morphological changes in rat islets of Langerhans and insulin secreting cell lines, but dictate cell death by different mechanisms. Apoptosis 1997; 2: 164-177.
68. Mizumura K, Taguchi T,. Facilitated response of muscle thin-fiber receptors in mechanical hyperalgesia after exercise. In:, Graven-Nielsen T, et al., eds. Fundamentals of Musculoskeletal Pain, 1st edn. Seattle, WA: IASP Press, 2008: 47-59. Nível Superior