Neutrophils do not contribute to local tissue damage, but play a key role in skeletal muscle regeneration, in mice injected with Bothrops asper snake venom

Muscle and Nerve

Volumn 28, Issue 4, 2003, Pages 449-459

  Teixeira, C F P ^a   Zamuner S R ^a   Zuliani, J P ^a   Fernandes, C M ^a   Cruz Hofling, M A ^b   Fernandes, I ^a   Chaves, F ^c   Gutierrez J M ^c  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

Bothrops asper snake venom; Muscle regeneration; Myonecrosis; Myotoxic phospholipase A2; Neutrophil leukocytes

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN G ANTIBODY; MONOCLONAL ANTIBODY; PHOSPHOLIPASE A2; SNAKE VENOM; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEEDING; BOTHROPS ASPER VENOM; CONTROLLED STUDY; EDEMA; GASTROCNEMIUS MUSCLE; GRANULOCYTE; HISTOLOGY; INFLAMMATORY INFILTRATE; MALE; MUSCLE NECROSIS; MUSCLE REGENERATION; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SKELETAL MUSCLE;

ANIMALS; ANTIBODIES, MONOCLONAL; BOTHROPS; CROTALID VENOMS; EXUDATES AND TRANSUDATES; GRANULOCYTES; IMMUNOGLOBULIN G; INJECTIONS, INTRAMUSCULAR; LEUKOCYTE COUNT; MALE; MICE; MUSCLE, SKELETAL; MYOSITIS; NECROSIS; NEUROTOXINS; NEUTROPHILS; PHOSPHOLIPASES A; REGENERATION;

EID: 0141592399     PISSN: 0148639X     EISSN: None     Source Type: Journal    
DOI: 10.1002/mus.10453     Document Type: Article

References (54)

1. Allbrook D. Skeletal muscle regeneration. Muscle Nerve 1981;4:234-245.
2. Arce V, Brenes F, Gutiérrez JM. Degenerative and regenerative changes in murine skeletal muscle after injection of venom from the snake Bothrops asper: a histochemical and immunocytochemical study. Int J Exp Pathol 1991;72:211-226.
3. Bjarnason JB, Fox JW. Hemorrhagic metalloproteinases from snake venoms. Pharmacol Ther 1994;62:325-372.
4. Cassatella MA. The production of cytokines by polymorphonuclear neutrophils. Immunol Today 1995;16:21-26.
5. Chacur M, Picolo G, Gutiérrez JM, Teixeira CFP, Cury Y. Pharmacological modulation of hyperalgesia induced by Bothrops asper (terciopelo) snake venom. Toxicon 2001;39:1173-1181.
6. Chaves F, Barboza M, Gutiérrez JM. Pharmacological study of edema induced by venom of the snake Bothrops asper (terciopelo). Toxicon 1995;33:31-39.
7. 2, anticoagulant and myotoxic activities. Biochim Biophys Acta 1991;1070:455-460.
8. Fahey TJ, Tracey KJ, Tekamp-Olson P, Cousens LS, Jones WG, Shires GT, Cerami A, Sherry B. Macrophage inflammatory protein 1 modulates macrophage function. J Immunol 1992;148:2764-2769.
9. Fan HW, Cardoso JL. Clinical toxicology of snake bites in South America. In: Meier J, White J, editors. Handbook of clinical toxicology of animal venoms and poisons. Florida: CRC Press; 1995. p 667-688.
10. Farsky SHP, Costa-Cruz JWM, Cury Y, Teixeira CFP. Leukocyte response induced by Bothrops jararaca crude venom. In vivo and in vitro studies. Toxicon 1997;35:185-193.
11. Fernandes I, Cormont F, Latinne D, Bazin H, Takehara HA, Mota I. A rapid efficient purification method for horse IgG(T) using a rat monoclonal antibody. Braz J Med Biol Res 1994;27:2599-2606.
12. Flores CA, Zappellini A, Prado-Franceschi J. Lypoxygenase-derived mediators may be involved in in vivo neutrophil migration induced by Bothrops erythromelas and Bothrops alternatus venoms. Toxicon 1993;31:1551-1559.
13. Gillitzer R, Goebeler M. Chemokines in cutaneous wound healing. J Leukoc Biol 2001;69:513-521.
14. Grounds M. Towards understanding skeletal muscle regeneration. Pathol Res Pract 1991;187:1-22.
15. Gutiérrez JM. Clinical toxicology of snakebite in Central America. In: Meier J, White J, editors. Handbook of clinical toxicology of animal venoms and poisons. Florida: CRC Press; 1995. p 645-665.
16. Gutiérrez JM, Lomonte B. Local tissue damage induced by Bothrops snake venoms: a review. Memorias Instituto Butantan 1989;51:211-223.
17. 2 enzymes. Structure, function and mechanism. Chichester: Wiley; 1997. p 321-352.
18. Gutiérrez JM, Rucavado A. Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage. Biochimie 2000;82:841-850.
19. Gutiérrez JM, Ownby CL, Odell GV. Isolation of a myotoxin from Bothrops asper venom: partial characterization and action on skeletal muscle. Toxicon 1984;22:115-128.
20. Gutiérrez JM, Ownby CL, Odell GV. Pathogenesis of myonecrosis induced by crude venom and a myotoxin of Bothrops asper. Exp Molec Pathol 1984;40:367-379.
21. Gutiérrez JM, Ownby CL, Odell GV. Skeletal muscle regeneration after myonecrosis induced by crude venom and a myotoxin from the snake Bothrops asper (Fer-de-Lance). Toxicon 1984;22:719-731.
22. Gutiérrez JM, Chaves F, Cerdas L. Inflammatory infiltrate in skeletal muscle injected with Bothrops asper venom. Rev Biol Trop 1986;34:209-219.
23. Gutiérrez JM, Chaves F, Mata E, Cerdas L. Skeletal muscle regeneration after myonecrosis induced by Bothrops asper (terciopelo) venom. Toxicon 1986;24:223-231.
24. Gutiérrez JM, Arce V, Brenes F, Chaves F. Changes in myofibrillar components after skeletal muscle necrosis induced by a myotoxin isolated from the venom of the snake Bothrops asper. Exp Mol Pathol 1990;52:25-36.
25. 2 isolated from the venom of Bothrops jararacussu. Exp Mol Pathol 1991;55:217-229.
26. Gutiérrez JM, Romero M, Núñez J, Chaves F, Borkow G, Ovadia M. Skeletal muscle necrosis and regeneration after injection of BAH1, a hemorrhagic metalloproteinase isolated from the venom of the snake Bothrops asper (terciopelo). Exp Mol Pathol 1995;62:28-41.
27. Gutiérrez JM, León G, Rojas G, Lomonte B, Rucavado A, Chaves F. Neutralization of local tissue damage induced by Bothrops asper (terciopelo) snake venom. Toxicon 1998;36:1529-1538.
28. 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 1991;147:22-28.
29. Hunt TK, Knighton DR, Thakral KK, Goodson WH, Andrews WS. Studies on inflammation and wound healing: angiogenesis and collagen synthesis stimulated in vivo by resident and activated wound macrophages. Surgery 1984;96:48-54.
30. Kasama T, Strieter RM, Lukacs NW, Burdick MD, Kunkel SL. Regulation of neutrophil-derivated chemokine expression by IL-10. J Immunol 1994;152:3559-3569.
31. Kasama T, Strieter RM, Standford TJ, Burdick MD, Kunkel SL. Expression and regulation of human neutrophil-derivated macrophage inflammatory protein 1 alpha. J Exp Med 1993;178:63-72.
32. Korthuis RJ, Grisham MB, Granger DN. Leukocyte depletion attenuates vascular injury in postischemic skeletal muscle. Am J Physiol 1988;254:H823-H827.
33. Krippendorf BB, Riley DA. Distinguishing unloading- versus reloading-induced changes in rat soleus muscle. Muscle Nerve 1993;16:99-108.
34. Lescaudron L, Peltékian E, Fontaine-Pérus J, Paulin D, Zampieri M, García L, Parrish E. Blood borne macrophages are essential for the triggering of muscle regeneration following muscle transplant. Neuromuscul Disord 1999;9:72-80.
35. Lomonte B, Tarkowski A, Hanson LÅ. Host response to Bothrops asper snake venom. Analysis of oedema formation, inflammatory cells, and cytokine release in a mouse model. Inflammation 1993;17:93-105.
36. McLennan IS. Resident macrophages (ED2- and ED3-positive) do not phagocytose degenerating rat skeletal muscle fibers. Cell Tissue Res 1993;272:193-196.
37. Moreira L, Gutiérrez JM, Borkow G, Ovadia M. Ultrastructural alterations in mouse capillary blood vessels after experimental injection of venom from the snake Bothrops asper (terciopelo). Exp Mol Pathol 1992;57:124-133.
38. Oppenheim JJ, Zachariae CO, Mukaida M, Matsushima K. Properties of the novel pro-inflammatory supergene "intercrine" cytokine family. Annu Rev Immunol 1991;9:617-648.
39. Ownby CL. Pathology of rattlesnake envenomation. In: Tu, AT, editor. Rattlesnake venoms. Their actions and treatment. New York: Marcel Dekker; 1982. p 163-209.
40. Pizza FX, McLoughlin TJ, McGregor SJ, Calomeni EP, Gunning WT. Neutrophils injure cultured skeletal myotubes. Am J Physiol Cell Physiol 2001;281:C335-C341.
41. Roberts P, McGeachie JK, Grounds MD. The host environment determines strain-specific differences in the timing of skeletal muscle regeneration: cross-transplantation studies between SJL/J and BALB/c mice. J Anat 1997;191:585-594.
42. Robertson TA, Maley MAL, Grounds MD, Papadimitriou JM. The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp Cell Res 1993;207:321-331.
43. Sandri M, Sandri C, Brun B, Giurisato E, Cantini M, Rossini K, Destro C, Arslan P, Carraro U. Inhibition of FasL sustains phagocytic cells and delays myogenesis in regenerating muscle fibers. J Leukoc Biol 2001;69:482-489.
44. Schratzberger P, Dunzendorfer S, Reinisch N, Kahler CM, Harold M, Wiedermann CJ. Release of chemoattractants for human monocytes from endothelial cells by interaction with neutrophils. Cardiovasc Res 1998;38:516-521.
45. Smith JK, Grisham MB, Granger DN, Korthuis RJ. Free radical defense mechanisms and neutrophil infiltration in postischemic skeletal muscle. Am J Physiol 1989;256:H789-H793.
46. St. Pierre BA, Tidball JG. Differential response of macrophage subpopulation to soleus reloading after rat hindlimb suspension. J Appl Physiol 1994;77:290-297.
47. Taub DD, Conlon K, Lloyd AR, Oppenheim JJ, Kelvin DJ. Preferential migration of activated CD4+ and CD8+ T cells in response to MIP-1 alpha and MIP-1 beta. Science 1993;260:355-358.
48. Teixeira CFP, Cury Y, Oga S, Jancar S. Hyperalgesia induced by Bothrops jararaca venom in rats: role of eicosanoids and platelet-activating factor (PAF). Toxicon 1994;32:419-426.
49. Tidball JG. Inflammatory cell response to acute muscle injury. Med Sci Sports Exerc 1995;27:1022-1032.
50. Trebien HA, Calixto JB. Pharmacological evaluation of rat paw oedema induced by Bothrops jararaca venom. Agents Actions 1989;26:292-300.
51. Vassiloyanakopoulos AP, Okamoto S, Fierer J. The crucial role of polymorphonuclear leukocytes in resistance to Salmonella dublin infections in genetically susceptible and resistant mice. Proc Natl Acad Sci USA 1998;95:7676-7681.
52. Warrell DA. The global problem of snake bite: its prevention and treatment. In: Gopalakrishnakone P, Tan CK, editors. Recent advances in toxinology research, vol 1. Singapore: National University of Singapore; 1992. p 121-153.
53. Winter CA, Risley EA, Nuss GW. Carrageenan-induced edema in the hindpaw of the rat as an assay for anti-inflammatory drugs. Proc Soc Exp Biol Med 1962;15:706-711.
54. Zamunér S, Gutiérrez JM, Muscará MN, Teixeira SA, Teixeira CFP. Bothrops asper and Bothrops jararaca snake venoms trigger microbicidal functions of peritoneal leukocytes in vivo. Toxicon 2001;39:1505-1513.