Role of nitric oxide in the local and systemic pathophysiological effects induced by Bothrops asper snake venom in mice

Inflammation Research

Volumn 55, Issue 6, 2006, Pages 245-253

  Chaves, F ^a   Teixeira, C F P ^b   Gutierrez J M ^a  

^a UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^b INSTITUTO BUTANTAN   (Brazil)

Author keywords

Bothrops asper venom; Hemorrhage; L NAME; Lethality; Myonecrosis; NO; NO synthase

Indexed keywords

AMINOGUANIDINE; BATROXOBIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; SNAKE VENOM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLEEDING; CELL INFILTRATION; CONTROLLED STUDY; ENVENOMATION; FOOT EDEMA; LEUKOCYTE COUNT; MOUSE; MUSCLE NECROSIS; MUSCLE TISSUE; NONHUMAN; PATHOPHYSIOLOGY; SNAKE; THROMBOCYTE COUNT; TISSUE INJURY;

ANIMALS; BOTHROPS; CROTALID VENOMS; EDEMA; ENZYME INHIBITORS; GUANIDINES; HEMORRHAGE; MICE; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; SNAKE BITES;

EID: 33748492712     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-006-0078-9     Document Type: Article

References (52)

1. Warrell DA. Clinical toxicology of snakebite in Asia. In: Meier J, White J (eds.), Handbook of Clinical Toxicology of Animal Venoms and Poisons. CRC Press, Florida, 1995; pp 493-594.
2. Warrell DA. Snakebites in Central and South America: epidemiology, clinical features, and clinical management. In: Campbell JA, Lamar WW (eds.), The Venomous Reptiles of the Western Hemisphere, vol II. Comstock, Ithaca, 2004; pp 709-61.
3. Gutiérrez JM. Clinical toxicology of snakebites in Central America. In: Meier J, White J (eds.), Handbook of Clinical Toxicology of Animal Venoms and Poisons. CRC Press, Florida, 1995; pp 645-65.
4. Savage JW. The Amphibians and Reptiles of Costa Rica. The University of Chicago Press, Chicago, 2002; 934 p.
5. 2 myotoxins from Bothrops snake venoms. Toxicon 1995; 33: 1405-24.
6. Gutiérrez JM, Rucavado A. Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage. Biochimie 2000; 82: 841-50.
7. 2: insights into the mechanisms of local and systemic myotoxicity. Toxicon 2003; 42: 915-31.
8. Aragón-Ortiz F, Gubensek F. Characterization of thrombin-like proteinase from Bothrops asper venom. In: Rosenberg P (ed.), Toxins: Animal, Plant and Microbial. Pergamon Press, Oxford, 1978; pp 107-11.
9. Franceschi, A, Rucavado A, Mora N, Gutiérrez JM. Purification and characterization of BaH4, a hemorrhagic metalloproteinase from the venom of the snake Bothrops asper. Toxicon 2000; 38: 63-77.
10. Rucavado A, Soto M, Kamiguti AS, Theakston RDG, Fox JW, Escalante T, Gutiérrez JM. Characterization of aspercetin, a platelet aggregating component from the venom of the snake Bothrops asper which induces thrombocytopenia and potentiates metalloproteinase-induced hemorrhage. Thromb Haemost 2001; 85: 710-5.
11. Rucavado A, Soto M, Escalante T, Loría GD, Arni R, Gutiérrez JM. Thrombocytopenia and platelet hypoaggregation induced by Bothrops asper snake venom: toxins involved and their contribution to metalloproteinase-induced pulmonary hemorrhage. Thromb Haemost 2005; 94: 123-31.
12. Loría GD, Rucavado A, Kamiguti AS, Theakston RDG, Fox JW, Alape A, Gutiérrez JM. Characterization of 'basparin A', a prothrombin-activating metalloproteinase, from the venom of the snake Bothrops asper that inhibits platelet aggregation and induces defibrination and thrombosis. Arch Biochem Biophys 2003; 418: 13-24.
13. Lomonte B, Tarkowski A, Hanson LÅ. Host response to Bothrops asper snake venom. Analysis of edema formation, inflammatory cells, and cytokine release in a mouse model. Inflammation 1993; 17: 93-105.
14. Chaves F, Barboza M, Gutiérrez JM. Pharmacological study of edema induced by venom of the snake Bothrops asper (terciopelo) in mice. Toxicon 1995; 33: 31-9.
15. Petricevich VL, Teixeira CFP, Tambourgi DV, Gutiérrez JM. Increments in serum cytokine and nitric oxide levels in mice injected with Bothrops asper and Bothrops jararaca snake venoms. Toxicon 2000; 38: 1253-66.
16. Chacur M, Picolo G, Gutiérrez JM, Teixeira CFP Cury Y. Pharmacological modulation of hyperalgesia induced by Bothrops asper (terciopelo) snake venom. Toxicon 2001; 39: 1173-81.
17. Avila-Aguero ML, París MM, Hu S, Peterson PK, Gutiérrez JM, Lomonte B, Faingezicht I. Systemic cytokine response in children bitten by snakes in Costa Rica. Pediat Emerg Care 2001; 17: 425-9.
18. Rucavado A, Escalante T, Teixeira CFP, Femandes CM, Díaz C, Gutiérrez JM. Increments in cytokines and matrix metalloproteinases in skeletal muscle after injection of tissue damaging toxins from the venom of the snake Bothrops asper. Med Inflamm 2002; 11: 121-8.
19. Moilanen E, Whittle B, Moncada S. Nitric oxide as a factor in inflammation. In: Gallin JI, Snyderman R (Eds), Inflammation. Basic Principles and Correlates. Philadelphia, Lippincot, 1999; pp 787-800.
20. Zamunér SR, 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: 1505-13.
21. Miyabara EH, Tostes RC, Selistre-de-Araújo HS, Aoki MS, Moriscot AS. Role of nitric oxide in myotoxic activity induced by crotoxin in vivo. Toxicon 2004; 43: 425-32.
22. Muscará M, Wallace JL. Nitric oxide. V. Therapeutic potential of nitric oxide donors and inhibitors. Am. J. Physiol 1999; 276: G1313-G1316.
23. Wu CC, Yen MH. Higher levels of plasma nitric oxide in spontaneously hypertensive rats. Am. J. Hypert. 1999; 12: 476-82.
24. Gutiérrez JM, Gené JA, Rojas G, Cerdas L. Neutralization of proteolytic and hemorrhagic activities of Costa Rican snake venoms by a polyvalent antivenom. Toxicon 1985; 23: 887-93.
25. Ownby CL, Colberg TR, Odell GV. A new method for quantitating hemorrhage induced by rattlesnake venoms: ability of polyvalent antivenom to neutralize hemorrhagic activity. Toxicon 1984; 22: 227-33.
26. Teixeira CFP, Zamunér SR, Zuliani JP, Fernandes CM, Cruz-Hofling MA, Fernandes I et al. 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 Nerve 2003; 28: 449-59.
27. Bolaños R. Toxicity of Costa Rican snake venoms for the white mouse. Am J Trop Med Hyg 1972; 21: 360-3.
28. Gutiérrez JM, Ownby CL, Odell GV. Pahogenesis of myonecrosis induced by crude venom and a myotoxin of Bothrops asper. Exp Molec Pathol 1984; 40: 367-79.
29. Gutiérrez JM, Chaves F, Cerdas L. Inflammatory infiltrate in skeletal muscle injected with Bothrops asper venom. Rev Biol Trop 1986; 34: 209-19.
30. Gené JA, Roy A, Rojas G, Gutiérrez JM, Cerdas L. Comparative study on coagulant, defibrinating, fibrinolytic and fibrinogenolytic activities of Costa Rican crotaline snake venoms and their neutralization by a polyvalent antivenom. Toxicon 1989; 27: 841-8.
31. Nakane M, Schmidt HHHW, Pollock JS, Forstermann U, Murad F. Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett 1993; 316: 175-80.
32. Nguyen HX, Tidball JG. Interactions between neutrophils and macrophages promote macrophage killing of muscle cells in vitro. J Physiol 2003; 547: 125-32.
33. Pizza FX, Hernandez IJ, Tidball JG. Nitric oxide synthase inhibition reduces muscle inflammation and necrosis in modified muscle use. J Leuk Biol 1998; 64: 427-33.
34. Rubinstein I, Abassi Z, Coleman R, Milman F, Winaver J, Better OS. Involvement of nitric oxide system in experimental muscle crush injury. J Clin Invest 1998; 101: 1325-33.
35. Qi WN, Chen LE, Zhang L, Eu JP, Seaber AV, Urbaniak JR. Reperfusion injury in skeletal muscle is reduced in inducible nitric oxide synthase knockout mice. J Appl Physiol 2004; 97: 1323-8.
36. Azevedo-Marques MM, Hering SE, Cupo P. Evidence that Crotalus durissus terrificus (South American rattlesnake) envenomation in humans causes myolysis rather than hemolysis. Toxicon 1987; 25: 1163-8.
37. Salvini TF, Amaral AC, Miyabara EH, Turri JAO, Danella PM, Selistre de Araujo HS. Systemic skeletal muscle necrosis induced by crotoxin. Toxicon 2001; 39: 1141-9.
38. 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 Molec Pathol 1995; 62: 28-41.
39. Rucavado A, Lomonte B, Ovadia M, Gutiérrez JM. Local tissue damage induced by BaP1, a metalloproteinase isolated from Bothrops asper (terciopelo) snake venom. Exp Molec Pathol 1995; 63: 186-99.
40. Greenblatt EP, Loeb AL, Longnecker DE. Marked regional heterogeneity in the magnitude of EDRF/NO-mediated vascular tone in awake rats. J Cardiovasc Res 1993; 21: 235-40.
41. Gutiérrez JM, Rucavado A, Escalante T, Díaz C. Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage. Toxicon 2005; 45: 997-1011.
42. Laing GD, Clissa PB, Theakston RDG, Moura-da-Silva AM, Taylor MJ. Inflammatory pathogenesis of snake venom metalloproteinase-induced skin necrosis. Eur J Immunol 2003; 33: 3458-63.
43. Trebien HA, Calixto JB. Pharmacological evaluation of rat paw edema induced by Bothrops jararaca venom. Agents Actions 1989; 26: 292-300.
44. Medeiros MV, Binhara IM, Moreno H, Zatz R, De Nucci G, Antunes E. Effect of chronic nitric oxide synthesis inhibition on the inflammatory responses induced by carrageenin in rats. Eur. J. Pharmacol. 1995; 285: 109-114.
45. Chacur M, Gutiérrez JM, Milligan ED, Wieseler-Frank J, Britto LRG, Maier SF et al. Snake venom components enhance pain upon subcutaneous injection: an initial examination of spinal cord mediators. Pain 2004; 111: 65-76.
46. Farsky SHP, Borelli P, Fock RA, Proto SZ, Ferreira JMC, Mello SBV. Chronic blockade of nitric oxide biosynthesis in rats: effect on leukocyte endothelial interaction and on leukocyte recruitment. Inflamm Res 2004; 53: 442-52.
47. Lefer DJ, Jones SP, Girod WG, Baines A, Grisham MB, Cockrell AS et al. Leukocyte-endothelial cell interactions in nitric oxide synthase-deficient mice. Am. J. Physiol. 1999; 276: H1943-H1950.
48. Rocha JCS, Peixoto MEB, Jancar S, Cunha FQ, Ribeiro RA, Rocha FAC. Dual effect of nitric oxide in articular inflammatory pain in zymosan-induced arthritis in rats. Br. J. Pharmacol. 2002; 136: 588-96.
49. Endres M, Laufs U, Liao JK, Moskowitz MA. Targeting eNOS for stroke protection. Trends Neurosci. 2004; 27: 283-9.
50. Walford G, Loscalzo J. Nitric oxide in vascular biology. J Thromb Haemost 2003; 1: 2112-8.
51. Carlson RW, Schaeffer RC, Whigham H, Michaelis S, Russell FE, Weil MH. Rattlesnake venom shock in the rat: development of a method. Am J Physiol 1975; 229: 1668-74.
52. Iadecola C. Bright and dark sides of nitric oxide in ischaemic brain injury. Trends Neurosci 1997; 20: 132-9.