Neutrophil-induced skeletal muscle damage: A calculated and controlled response following hindlimb unloading and reloading

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 6, 2008, Pages

  Dumont, Nicolas ^a   Bouchard, Patrice ^a   Frenette, Jérôme ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Contractile properties; Hindlimb suspension; Inflammation; Neutrophils

Indexed keywords

DYE; LIPOPOLYSACCHARIDE; PROCION ORANGE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HINDLIMB; IMMUNOHISTOLOGY; IN VITRO STUDY; LEUKOCYTE; LEUKOCYTE ACTIVATION; MALE; MEMBRANE DAMAGE; MOUSE; MUSCLE ATROPHY; MUSCLE CONTRACTILITY; MUSCLE FIBER MEMBRANE; MUSCLE FORCE; MUSCLE FUNCTION; MUSCLE INJURY; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PRIORITY JOURNAL; SOLEUS MUSCLE; WEIGHT BEARING;

ANIMALS; HINDLIMB SUSPENSION; INFLAMMATION; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR ATROPHY; NEUTROPHIL INFILTRATION; NEUTROPHILS; PEROXIDASE; RECOVERY OF FUNCTION; TIME FACTORS;

EID: 57749116202     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90318.2008     Document Type: Article

References (65)

1. Armstrong R. The physiological role and pharmacological potential of nitric oxide in neutrophil activation. Int Immunopharmacol 1: 1501-1512, 2001.
2. Arnold L, Henry A, Poron F, Baba-Amer Y, van Rooijen N, Plonquet A, Gherardi RK, Chazaud B. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J Exp Med 204: 1057-1069, 2007.
3. Auger MJ. Mononuclear phagocytes. BMJ 298: 546-548, 1989.
4. Barton GM. A calculated response: control of inflammation by the innate immune system. J Clin Invest 118: 413-420, 2008.
5. Brown CR, Blaho VA, Loiacono CM. Treatment of mice with the neutrophil-depleting antibody RB6-8C5 results in early development of experimental lyme arthritis via the recruitment of Gr-1- polymorphonuclear leukocyte-like cells. Infect Immun 72: 4956-4965, 2004.
6. Cantini M, Giurisato E, Radu C, Tiozzo S, Pampinella F, Senigaglia D, Zaniolo G, Mazzoleni F, Vitiello L. Macrophage-secreted myogenic factors: a promising tool for greatly enhancing the proliferative capacity of myoblasts in vitro and in vivo. Neurol Sci 23: 189-194, 2002.
7. Cario E, Rosenberg IM, Brandwein SL, Beck PL, Reinecker HC, Podolsky DK. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. J Immunol 164: 966-972, 2000.
8. Cassatella MA. Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol 73: 369-509, 1999.
9. Chazaud B, Sonnet C, Lafuste P, Bassez G, Rimaniol AC, Poron F, Authier FJ, Dreyfus PA, Gherardi RK. Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J Cell Biol 163: 1133-1143, 2003.
10. Conlan JW, North RJ. Neutrophils are essential for early anti-Listeria defense in the liver, but not in the spleen or peritoneal cavity, as revealed by a granulocyte-depleting monoclonal antibody. J Exp Med 179: 259-268, 1994.
11. Cote CH, Perreault G, Frenette J. Carbohydrate utilization in rat soleus muscle is influenced by carbonic anhydrase III activity. Am J Physiol Regul Integr Comp Physiol 273: R1211-R1218, 1997.
12. Daley JM, Thomay AA, Connolly MD, Reichner JS, Albina JE. Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice. J Leukoc Biol 83: 64-70, 2008.
13. Dovi JV, He LK, DiPietro LA. Accelerated wound closure in neutrophil-depleted mice. J Leukoc Biol 73: 448-455, 2003.
14. Dumont N, Lepage K, Cote CH, Frenette J. Mast cells can modulate leukocyte accumulation and skeletal muscle function following hindlimb unloading. J Appl Physiol 103: 97-104, 2007.
15. Elbim C, Bailly S, Chollet-Martin S, Hakim J, Gougerot-Pocidalo MA. Differential priming effects of proinflammatory cytokines on human neutrophil oxidative burst in response to bacterial N-formyl peptides. Infect Immun 62: 2195-2201, 1994.
16. Fantone JC, Ward PA. Polymorphonuclear leukocyte-mediated cell and tissue injury: oxygen metabolites and their relations to human disease. Hum Pathol 16: 973-978, 1985.
17. Ford-Hutchinson AW, Bray MA, Doig MV, Shipley ME, Smith MJ. Leukotriene B, a potent chemokinetic and aggregating substance released from polymorphonuclear leukocytes. Nature 286: 264-265, 1980.
18. Frenette J, Cai B, Tidball JG. Complement activation promotes muscle inflammation during modified muscle use. Am J Pathol 156: 2103-2110, 2000.
19. Frenette J, St-Pierre M, Cote CH, Mylona E, Pizza FX. Muscle impairment occurs rapidly and precedes inflammatory cell accumulation after mechanical loading. Am J Physiol Regul Integr Comp Physiol 282: R351-R357, 2002.
20. Frost RA, Nystrom GJ, Lang CH. Lipopolysaccharide and proinflammatory cytokines stimulate interleukin-6 expression in C2C12 myoblasts: role of the Jun NH2-terminal kinase. Am J Physiol Regul Integr Comp Physiol 285: R1153-R1164, 2003.
21. Frost RA, Nystrom GJ, Lang CH. Lipopolysaccharide regulates proinflammatory cytokine expression in mouse myoblasts and skeletal muscle. Am J Physiol Regul Integr Comp Physiol 283: R698-R709, 2002.
22. Galli SJ, Nakae S, Tsai M. Mast cells in the development of adaptive immune responses. Nat Immunol 6: 135-142, 2005.
23. Garcia-Ramallo E, Marques T, Prats N, Beleta J, Kunkel SL, Godessart N. Resident cell chemokine expression serves as the major mechanism for leukocyte recruitment during local inflammation. J Immunol 169: 6467-6473, 2002.
24. Gillitzer R. Inflammation in human skin: a model to study chemokine-mediated leukocyte migration in vivo. J Pathol 194: 393-394, 2001.
25. Heit B, Colarusso P, Kubes P. Fundamentally different roles for LFA-1, Mac-1 and alpha4-integrin in neutrophil chemotaxis. J Cell Sci 118: 5205-5220, 2005.
26. Hestdal K, Ruscetti FW, Ihle JN, Jacobsen SE, Dubois CM, Kopp WC, Longo DL, Keller JR. Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J Immunol 147: 22-28, 1991.
27. Iizawa O, Akamatsu H, Niwa Y. Neutrophil chemotaxis, phagocytosis, and generation of reaction oxygen species show a hierarchy of responsiveness to increasing concentrations of N-formyl-Met-Leu-Phe. Biol Signals 4: 14-18, 1995.
28. Iwahori Y, Ishiguro N, Shimizu T, Kondo S, Yabe Y, Oshima T, Iwata H, Sendo F. Selective neutrophil depletion with monoclonal antibodies attenuates ischemia/reperfusion injury in skeletal muscle. J Reconstr Microsurg 14: 109-116, 1998.
29. Jaeschke H, Farhood A, Bautista AP, Spolarics Z, Spitzer JJ, Smith CW. Functional inactivation of neutrophils with a Mac-1 (CD11b/CD18) monoclonal antibody protects against ischemia-reperfusion injury in rat liver. Hepatology 17: 915-923, 1993.
30. Kalff JC, Schwarz NT, Walgenbach KJ, Schraut WH, Bauer AJ. Leukocytes of the intestinal muscularis: their phenotype and isolation. J Leukoc Biol 63: 683-691, 1998.
31. Kasama T, Miwa Y, Isozaki T, Odai T, Adachi M, Kunkel SL. Neutrophil-derived cytokines: potential therapeutic targets in inflammation. Curr Drug Targets Inflamm Allergy 4: 273-279, 2005.
32. Lapointe BM, Cote CH. Anesthetics can alter subsequent in vitro assessment of contractility in slow and fast skeletal muscles of rat. Am J Physiol Regul Integr Comp Physiol 277: R917-R921, 1999.
33. Lapointe BM, Fremont P, Cote CH. Adaptation to lengthening contractions is independent of voluntary muscle recruitment but relies on inflammation. Am J Physiol Regul Integr Comp Physiol 282: R323-R329, 2002.
34. Lapointe BM, Frenette J, Cote CH. Lengthening contraction-induced inflammation is linked to secondary damage but devoid of neutrophil invasion. J Appl Physiol 92: 1995-2004, 2002.
35. Lewinsohn DM, Bargatze RF, Butcher EC. Leukocyte-endothelial cell recognition: evidence of a common molecular mechanism shared by neutrophils, lymphocytes, and other leukocytes. J Immunol 138: 4313-4321, 1987.
36. Lu H, Ballantyne C, Smith CW. LFA-1 (CD11a/CD18) triggers hydrogen peroxide production by canine neutrophils. J Leukoc Biol 68: 73-80, 2000.
37. Malm C, Sjodin TL, Sjoberg B, Lenkei R, Renstrom P, Lundberg IE, Ekblom B. Leukocytes, cytokines, growth factors and hormones in human skeletal muscle and blood after uphill or downhill running. J Physiol 556: 983-1000, 2004.
38. McDonald PP, Bald A, Cassatella MA. Activation of the NF-κB pathway by inflammatory stimuli in human neutrophils. Blood 89: 3421-3433, 1997.
39. Merchant SH, Gurule DM, Larson RS. Amelioration of ischemia-reperfusion injury with cyclic peptide blockade of ICAM-1. Am J Physiol Heart Circ Physiol 284: H1260-H1268, 2003.
40. Moraes TJ, Zurawska JH, Downey GP. Neutrophil granule contents in the pathogenesis of lung injury. Curr Opin Hematol 13: 21-27, 2006.
41. Morey-Holton ER, Globus RK. Hindlimb unloading rodent model: technical aspects. J Appl Physiol 92: 1367-1377, 2002.
42. Morland CM, Morland BJ, Darbyshire PJ, Stockley RA. Migration of CD18-deficient neutrophils in vitro: evidence for a CD18-independent pathway induced by IL-8. Biochim Biophys Acta 1500: 70-76, 2000.
43. Nash GB, Buckley CD, Ed Rainger G. The local physicochemical environment conditions the proinflammatory response of endothelial cells and thus modulates leukocyte recruitment. FEBS Lett 569: 13-17, 2004.
44. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6: 173-182, 2006.
45. Nguyen HX, Lusis AJ, Tidball JG. Null mutation of myeloperoxidase in mice prevents mechanical activation of neutrophil lysis of muscle cell membranes in vitro and in vivo. J Physiol 565: 403-413, 2005.
46. Orimo S, Hiyamuta E, Arahata K, Sugita H. Analysis of inflammatory cells and complement C3 in bupivacaine-induced myonecrosis. Muscle Nerve 14: 515-520, 1991.
47. Parsonage G, Falciani F, Burman A, Filer A, Ross E, Bofill M, Martin S, Salmon M, Buckley CD. Global gene expression profiles in fibroblasts from synovial, skin and lymphoid tissue reveals distinct cytokine and chemokine expression patterns. Thromb Haemost 90: 688-697, 2003.
48. Pedrosa J, Saunders BM, Appelberg R, Orme IM, Silva MT, Cooper AM. Neutrophils play a protective nonphagocytic role in systemic Mycobacterium tuberculosis infection of mice. Infect Immun 68: 577-583, 2000.
49. Pillinger MH, Abramson SB. The neutrophil in rheumatoid arthritis. Rheum Dis Clin North Am 21: 691-714, 1995.
50. Pizza FX, Baylies H, Mitchell JB. Adaptation to eccentric exercise: neutrophils and E-selectin during early recovery. Can J Appl Physiol 26: 245-253, 2001.
51. Pizza FX, Koh TJ, McGregor SJ, Brooks SV. Muscle inflammatory cells after passive stretches, isometric contractions, and lengthening contractions. J Appl Physiol 92: 1873-1878, 2002.
52. Pizza FX, Peterson JM, Baas JH, Koh TJ. Neutrophils contribute to muscle injury and impair its resolution after lengthening contractions in mice. J Physiol 562: 899-913, 2005.
53. Pouliot M, Gilbert C, Borgeat P, Poubelle PE, Bourgoin S, Creminon C, Maclouf J, McColl SR, Naccache PH. Expression and activity of prostaglandin endoperoxide synthase-2 in agonist-activated human neutrophils. FASEB J 12: 1109-1123, 1998.
54. Rogers HW, Unanue ER. Neutrophils are involved in acute, nonspecific resistance to Listeria monocytogenes in mice. Infect Immun 61: 5090-5096, 1993.
55. Sabroe I, Dower SK, Whyte MK. The role of Toll-like receptors in the regulation of neutrophil migration, activation, and apoptosis. Clin Infect Dis 41 Suppl 7: S421-S426, 2005.
56. Sawyer DW, Donowitz GR, Mandell GL. Polymorphonuclear neutrophils: an effective antimicrobial force. Rev Infect Dis 11 Suppl 7: S1532-S1544, 1989.
57. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA. The neutrophil as a cellular source of chemokines. Immunol Rev 177: 195-203, 2000.
58. Scapini P, Laudanna C, Pinardi C, Allavena P, Mantovani A, Sozzani S, Cassatella MA. Neutrophils produce biologically active macrophage inflammatory protein-3α (MIP-3α)/CCL20 and MIP-3β/CCL19. Eur J Immunol 31: 1981-1988, 2001.
59. Shappell SB, Toman C, Anderson DC, Taylor AA, Entman ML, Smith CW. Mac-1 (CD11b/CD18) mediates adherence-dependent hydrogen peroxide production by human and canine neutrophils. J Immunol 144: 2702-2711, 1990.
60. Sonnet C, Lafuste P, Arnold L, Brigitte M, Poron F, Authier FJ, Chretien F, Gherardi RK, Chazaud B. Human macrophages rescue myoblasts and myotubes from apoptosis through a set of adhesion molecular systems. J Cell Sci 119: 2497-2507, 2006.
61. Tidball JG, Berchenko E, Frenette J. Macrophage invasion does not contribute to muscle membrane injury during inflammation. J Leukoc Biol 65: 492-498, 1999.
62. 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 578: 327-336, 2007.
63. Tsivitse SK, Mylona E, Peterson JM, Gunning WT, Pizza FX. Mechanical loading and injury induce human myotubes to release neutrophil chemoattractants. Am J Physiol Cell Physiol 288: C721-C729, 2005.
64. Tyagi S, Klickstein LB, Nicholson-Weller A. C5a-stimulated human neutrophils use a subset of 2 integrins to support the adhesion-dependent phase of superoxide production. J Leukoc Biol 68: 679-686, 2000.
65. von Stebut E, Metz M, Milon G, Knop J, Maurer M. Early macrophage influx to sites of cutaneous granuloma formation is dependent on MIP-1α/β released from neutrophils recruited by mast cell-derived TNFα. Blood 101: 210-215, 2003.