Inflammation induced by Bothrops asper venom (DOI:10.1016/j.toxicon.2009.03.019);Inflammation induced by Bothrops asper venom

Toxicon

Volumn 54, Issue 1, 2009, Pages 67-76

  Teixeira, Catarina ^a   Cury, Yara ^a   Moreira, Vanessa ^a   Picolo, Gisele ^a   Chaves, Fernando ^b  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

Bothrops asper; Inflammation; Pain; Toxins; Venom

Indexed keywords

BOTHROPS ASPER VENOM; METALLOPROTEINASE; PHOSPHOLIPASE A2; SERINE PROTEINASE; SNAKE VENOM; UNCLASSIFIED DRUG;

ARTICLE; CELL INFILTRATION; EDEMA; ENVENOMATION; EXPERIMENTAL STUDY; HUMAN; INFLAMMATION; INFLAMMATORY CELL; NOCICEPTION; NONHUMAN; PAIN; PRIORITY JOURNAL;

ANIMALIA; BOTHROPS ASPER; SERPENTES;

EID: 67349216771     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2009.05.026     Document Type: Erratum

References (87)

1. Abrahamsen B., Zhao J., Asante C.O., Cendan C.M., Marsh S., Martinez-Barbera J.P., Nassar M.A., Dickenson A.H., and Wood J.N. Cell and molecular basis of mechanical, cold, and inflammatory pain. Science 321 (2008) 702-705
2. Alape-Girón A., Sanz L., Escolano J., Flores-Díaz M., Madrigal M., Sasa M., and Calvete J.J. Snake venomics of the lancehead pitviper Bothrops asper: geographic, individual, and ontogenetic variations. J. Proteome Res. 7 (2008) 3556-3571
3. Arroyo O., Rojas G., and Gutiérrez J.M. Envenenamiento por mordedura de serpiente en Costa Rica en 1996: epidemiología y consideraciones clínicas. Acta Méd. Costarric. 41 (1999) 23-29
4. Avila-Agüero M.L., París M.M., Hu S., Peterson P.K., Gutiérrez J.M., Lomonte B., Faingezicht I., and Snakebite Study Group. Systemic cytokine response in children bitten by snakes in Costa Rica. Pediatr. Emerg. Care 17 (2001) 425-429
5. Bjarnason J.B., and Fox J.W. Hemorrhagic metalloproteinases from snake venoms. Pharmacol. Ther. 62 (1994) 325-372
6. Bolaños R. Serpientes, Venenos y Ofidismo en Centroamérica (1984), Editorial Universidad de Costa Rica, San José pp. 136
7. Carlos T.M., and Harlan J.M. Leukocyte-endothelial adhesion molecules. Blood 84 (1994) 2068-2101
8. Chacur M., Picolo G., Gutiérrez J.M., Teixeira C.F.P., and Cury Y. Pharmacological modulation of hyperalgesia induced by Bothrops asper (terciopelo) snake venom. Toxicon 39 (2001) 1173-1181
9. Chacur M., Longo I., Picolo G., Gutierrez J.M., Lomonte B., Guerra J.L., Teixeira C.F.P., and Cury Y. Hyperalgesia induced by Asp49 and Lys49 phospholipases A2 from Bothrops asper snake venom: pharmacological mediation and molecular determinants. Toxicon 41 (2003) 667-678
10. Chacur M., Gutierrez J.M., Milligan E.D., Wieseler-Frank J., Britto L.R.G., Maier S.F., Watkins L.R., and Cury Y. Snake venom components enhance pain upon subcutaneous injection: an initial examination of spinal cord mediators. Pain 111 (2004) 65-76
11. Chacur M., Milligan E.D., Sloan E.M., Wieseler-Frank J., Barrientos R., Martin D., Poole S., Gutierrez J.M., Maier S.F., Cury Y., and Watkins L.R. Snake venom phospholipase A2s (Asp49 and Lys49) induce mechanical allodynia upon peri-sciatic administration: involvement of spinal cord proinflammatory cytokines and nitric oxide. Pain 108 (2004) 180-191
12. Chaves F., Gutiérrez J.M., and Brenes F. Pathological and biochemical changes induced in mice after intramuscular injection of venom from newborn specimens of the snake Bothrops asper (Terciopelo). Toxicon 30 (1992) 1099-1109
13. Chaves F., Barboza M., and Gutiérrez J.M. Pharmacological study of edema induced by venom of the snake Bothrops asper (terciopelo). Toxicon 33 (1995) 31-39
14. 2 isolated from the venom of snake Bothrops asper (terciopelo). Toxicon 36 (1998) 1861-1869
15. Chaves F., Teixeira C.F., and Gutiérrez J.M. Role of nitric oxide in the local and systemic pathophysiological effects induced by Bothrops asper snake venom in mice. Inflamm. Res. 55 (2006) 245-253
16. Cheng J.K., and Ji R.R. Intracellular signaling in primary sensory neurons and persistent pain. Neurochem. Res. 33 (2008) 1970-1978
17. Cummins T.R., Sheets P.L., and Waxman S.G. The roles of sodium channels in nociception: implications for mechanisms of pain. Pain 131 (2007) 243-257
18. Farsky S.H., Gonçalves L.R., Gutiérrez J.M., Correa A.P., Rucavado A., Gasque P., and Tambourgi D.V. Bothrops asper snake venom and its metalloproteinase BaP-1 activate the complement system. Role in leucocyte recruitment. Mediators Inflamm. 9 (2000) 213-221
19. Fernandes C.M., Zamuner S.R., Zuliani J.P., Rucavado A., Gutiérrez J.M., and Teixeira C.F.P. Inflammatory effects of BaP1 a metalloproteinase isolated from Bothrops asper snake venom: leukocyte recruitment and release of cytokines. Toxicon 47 (2006) 549-559
20. Fernandes C.M., Pereira Teixeira C.F., Leite A.C., Gutiérrez J.M., and Rocha F.A. The snake venom metalloproteinase BaP1 induces joint hypernociception through TNF-alpha and PGE2-dependent mechanisms. Br. J. Pharmacol. 151 (2007) 1254-1261
21. Garcia-Leme J., Hammamura L., Leite M.P., and Rocha e Silva M. Pharmacological analysis of the acute inflammatory process induced in the rat's paw by local injection of carrageenin and by heating. Br. J. Pharmacol. 48 (1973) 88-96
22. Giordano J. The neurobiology of nociceptive and anti-nociceptive systems. Pain Physician 8 (2005) 277-290
23. Granger D.N., and Kubes P. The microcirculation and inflammation: modulation of leukocyte-endothelial cell adhesion. J. Leukoc. Biol. 55 (1994) 662-675
24. Gutiérrez J.M. Clinical toxicology of snake bite in Central America. In: Meier J., and White J. (Eds). Handbook of Clinical Toxicology of Animal Venoms and Poisons (1995), CRC Press, Boca Raton, FL 645-665
25. 2 myotoxins from Bothrops snake venoms. Toxicon 33 (1995) 1405-1424
26. Gutiérrez J.M., and Lomonte B. Phospholipase A2 myotoxins from Bothrops snake venoms. In: Kini R.M. (Ed). Venom Phospholipases A2 Enzymes. Structure, Function and Mechanism (1997), Wiley, United Kingdom 321-352
27. Gutiérrez J.M., Arroyo O., and Bolaños R. Myonecrosis, hemorrhage and edema induced by Bothrops asper venom in white mice. Toxicon 18 (1980) 603-610
28. Gutiérrez J.M., Chaves F., Bolaños R., Cerdas L., Rojas E., Arroyo O., and Portilla E. Neutralization de los efectos locales de1 veneno de Bothrops asper por un antiveneno polivalente. Toxicon 19 (1981) 493-500
29. Gutiérrez J.M., Chaves F., and Cerdas L. Inflammatory infiltrate in skeletal muscle injected with Bothrops asper venom. Rev. Biol. Trop 34 (1986) 209-214
30. Gutiérrez J.M., Rojas G., Lomonte B., Gené J.A., and Cerdas L. Comparative study of the edema-forming activity of Costa Rican snake venoms and its neutralization by polyvalent antivenom. Comp. Biochem. Physiol. C 85 (1986) 171-175
31. Gutiérrez J.M., Lomonte B., Chaves F., Moreno E., and Cerdas L. Pharmacological activities of a toxic phospholipase A isolated from the venom of the snake Bothrops asper. Comp. Biochem. Physiol. 84 (1986) 159-164
32. Gutiérrez J.M., Romero M., Díaz C., Borkow G., and Ovadia M. Isolation and characterization of a metalloproteinase with weak hemorrhagic activity from the venom of the snake Bothrops asper (terciopelo). Toxicon 33 (1995) 19-29
33. Haddad J.J. On the enigma of pain and hyperalgesia: a molecular perspective. Biochem. Biophys. Res. Comm. 353 (2007) 217-224
34. Harvey V.L., and Dickenson A.H. Mechanisms of pain in nonmalignant disease. Curr. Opin. Support. Palliat. Care 2 (2008) 133-139
35. Hopkins S.J. The pathophysiological role of cytokines. Leg. Med. 5 (2003) S45-S57
36. Hubbard A., and Rothlein R. Intercellular adhesion molecule-1 (ICAM-1) expression and cell signaling cascades. Free Radic. Biol. Med. 28 (2000) 1379-1386
37. Jorge M.T., Ribeiro L.A., and O'Connell J.L. Prognostic factors for amputation in the case of envenoming by snakes of the Bothrops genus (Viperidae). Ann. Trop. Med. Parasitol. 93 (1999) 401-408
38. Kaplanski G., Marin V., Montero-Julian F., Mantovani A., and Farnarier C. IL-6: a regulator of the transition from neutrophil to monocyte recruitment during inflammation. Trends Immunol. 24 (2003) 25-29
39. Kim D., Park D., Choi S., Lee S., Sun M., Kim C., and Shin H.S. Thalamic control of visceral nociception mediated by T-Type Ca2+ channels. Science 302 (2003) 117-119
40. Lomonte B., and Carmona E. Individual expression patterns of myotoxin isoforms in the venom of the snake. Bothrops asper. Comp. Biochem. Physiol. B 102 (1992) 325-329
41. Lomonte B., Tarkowski A., and Hanson L.A. Host response to Bothrops asper snake venom. Analysis of edema formation, inflammatory cells, and cytokine release in a mouse model. Inflammation 17 (1993) 93-105
42. Lomonte B., Lundgren J., Johansson B., and Bagge U. The dynamics of local tissue damage induced by Bothrops asper snake venom and myotoxin II on the mouse cremaster muscle: an intravital and electron microscopic study. Toxicon 32 (1994) 41-55
43. 2 myotoxins from crotalid snake venoms and their structural determinants of myotoxic action. Toxicon 42 (2003) 885-901
44. Luvisetto S., Marinelli S., Panasiti M.S., D'Amato F.R., Fletcher C.F., Pavone F., and Pietrobon D. Pain sensitivity in mice lacking the Ca(v)2.1alpha1 subunit of P/Q-type Ca2+ channels. Neuroscience 142 (2006) 823-832
45. McMahon S.B., Cafferty W.B., and Marchand F. Immune and glial cell factors as pain mediators and modulators. Exp. Neurol. 192 (2005) 444-462
46. Medzhitov R. Origin and physiological roles of inflammation. Nature 454 (2008) 428-435
47. Mora J., Mora R., Lomonte B., and Gutiérrez J.M. Effects of Bothrops asper snake venom on lymphatic vessels: insights into a hidden aspect of envenomation. PLoS Negl. Trop. Dis. 2 (2008) e318
48. Moreira V., Gutiérrez J.M., Soares A.M., Zamunér S.R., Purgatto E., and Teixeira C.F.P. Secretory phospholipases A2 isolated from Bothrops asper and from Crotalus durissus terrificus snake venoms induce distinct mechanisms for biosynthesis of prostaglandins E(2) and D(2) and expression of cyclooxygenases. Toxicon 52 (2008) 428-439
49. Moreira V., Gutiérrez J.M., Amaral R.B., Zamuner S.R., and Teixeira C.F.P. Effects of Bothrops asper snake venom on the expression of cyclooxygenases and production of prostaglandins by peritoneal leukocytes in vivo, and by isolated neutrophils and macrophages in vitro. Prostaglandins Leukot. Essent. Fatty Acids 8 (2009) 107-114
50. Ohsaka A. Hemorrhagic, necrotizing and edema-forming effects of snake venoms. In: Lee C.Y. (Ed). Handbook of Experimental Pharmacology. Snake Venoms vol. 52 (1979), Springer-Verlag, Berlin 480-546
51. Olivo R.A., Teixeira C.F.P., Wallace J.L., Gutiérrez J.M., and Zamunér S.R. Role of cyclooxygenases in oedema-forming activity of bothropic venoms. Toxicon 49 (2007) 670-677
52. Otero R., Gutiérrez J., Mesa M.B., Duque E., Rodríguez O., Luis Arango J., Gómez F., Toro A., Cano F., Rodríguez L.M., Caro E., Martínez J., Cornejo W., Gómez L.M., Uribe F.L., Cárdenas S., Núñez V., and Díaz A. Complications of Bothrops, Porthidium, and Bothriechis snakebites in Colombia. A clinical and epidemiological study of 39 cases attended in a university hospital. Toxicon 40 (2002) 1107-1114
53. Pérez A.V., Saravia P., Rucavado A., Sant'Ana C.D., Soares A.M., and Gutiérrez J.M. Local and systemic pathophysiological alterations induced by a serine proteinase from the venom of the snake Bothrops jararacussu. Toxicon 49 (2007) 1063-1069
54. Picolo G., Chacur M., Gutiérrez J.M., Teixeira C.F.P., and Cury Y. Evaluation of antivenoms in the neutralization of hyperalgesia and edema induced by Bothrops jararaca and Bothrops asper snake venoms. Braz. J. Med. Biol. Res. 35 (2002) 1221-1228
55. Rabinovitch M., and De Stefano M.J. Macrophage spreading in vitro. I. Inducers of spreading. Exp. Cell. Res. 77 (1973) 323-334
56. Ribeiro L.A., and Jorge M.T. Acidentes por serpentes do gênero Bothrops: série de 3139 casos. Rev. Soc. Bras. Med. Trop. 30 (1997) 475-480
57. Rittner H.L., Brack A., and Stein C. Pain and the immune system. Br. J. Anaesth. 101 (2008) 40-44
58. Rittner H.L., Brack A., and Stein C. The other side of the medal: how chemokines promote analgesia. Neurosci. Lett. 437 (2008) 203-208
59. Robertson T.A., Maley M.A.L., Grounds M.D., and Papadimitriou J.M. The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp. Cell Res. 207 (1993) 321-331
60. Rohn T.T., Nelson L.K., Sipes K.M., Swain S.D., Jutila K.L., and Quinn M.T. Priming of human neutrophils by peroxynitrite: potential role in enhancement of the local inflammatory response. J. Leukoc. Biol. 65 (1999) 59-70
61. Rosenfeld G. Symptomatology, pathology and treatment of snake bites in South America. In: Bucherl W., and Buckley E.E. (Eds). Venomous Animals and Their Venoms (1971), Academic Press, New York 345-403
62. Rucavado A., Lomonte B., Ovadia M., and Gutiérrez J.M. Local tissue damage induced by BaP1, a metalloproteinase isolated from Bothrops asper (Terciopelo) snake venom. Exp. Mol. Pathol. 63 (1995) 186-199
63. Rucavado A., Núñez J., and Gutiérrez J.M. Blister formation and skin damage induced by BaP1, a haemorrhagic metalloproteinase from the venom of the snake Bothrops asper. Int. J. Exp. Pathol. 79 (1998) 245-254
64. Rucavado A., Escalante T., Teixeira C.F.P., Fernandes C.M., Diaz C., and Gutiérrez J.M. Increments in cytokines and matrix metalloproteinases in skeletal muscle after injection of tissue-damaging toxins from the venom of the snake Bothrops asper. Mediators Inflamm. 11 (2002) 121-128
65. Ryan G.B., and Majno G. Antiinflammation. A review. Am. J. Pathol. 86 (1977) 183-276
66. Saegusa H., Kurihara T., Zong S., Kazuno A., Matsuda Y., Nonaka T., Han W., Toriyama H., and Tanabe T. Suppression of inflammatory and neuropathic pain symptoms in mice lacking the N-type Ca2+ channel. EMBO J. 20 (2001) 2349-2356
67. Saegusa H., Matsuda Y., and Tanabe T. Effects of ablation of N- and R-type Ca(2+) channels on pain transmission. Neurosci. Res. 43 (2002) 1-7
68. Saravia-Otten P., Frisan T., Thelestam M., and Gutiérrez J.M. Membrane independent activation of fibroblast proMMP-2 by snake venom: novel roles for venom proteinases. Toxicon 44 (2004) 749-764
69. Sawai Y. Studies on snakebites in the Asian areas. In: Eaker D., and Wadstrom T. (Eds). Natural Toxins (1980), Pergamon Press, Oxford 25-32
70. Schaible H.G., and Richter F. Pathophysiology of pain. Langenbecks Arch. Surg. 389 (2004) 237-243
71. Serhan C.N., and Savill J. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6 (2005) 1191-1197
72. Sherwood E.R., and Toliver-Kinsky T. Mechanisms of the inflammatory response. Best Pract. Res. Clin. Anaesthesiol. 18 (2004) 385-405
73. Sternlicht M.D., and Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Biol. 17 (2001) 463-516
74. Streuli C. Extracellular matrix remodeling and cellular differentiation. Curr. Opin. Cell Biol. 11 (1999) 634-640
75. Suwa T., Hogg J.C., Quinlan K.B., and Van Eeden S.F. The effect of interleukin-6 on l-selectin levels on polymorphonuclear leukocytes. Am. J. Physiol. Heart Circ. Physiol. 283 (2002) H879-H884
76. Teixeira C.F.P., Zamunér S.R., Zuliani J.P., Fernandes C.M., Cruz-Hofling M.A., Fernandes I., Chaves F., and Gutiérrez J.M. 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 28 (2003) 449-459
77. Till G.O. Chemotatic factors. In: Rother K., and Till G.O. (Eds). The Complement System (1998), Springer, Berlin 374-367
78. Tortora G.J., and Grabowski S.R. Principles of Anatomy and Physiology. tenth ed. (2002), John Wiley, Hoboken
79. Vanegas H., and Schaible H. Effects of antagonists to high-threshold calcium channels upon spinal mechanisms of pain, hyperalgesia and allodynia. Pain 85 (2000) 9-18
80. Watkins L.R., Wieseler-Frank J., Milligan E.D., Johnston I., and Maier S.F. Contribution of glia to pain processing in health and disease. In: Cervero F., and Jensen T.S. (Eds). Handbook of Clinical Neurology. Pain Vol. 81 (2006), Elsevier BV, London, UK 309-323
81. Wieseler-Frank J., Maier S.F., and Watkins L.R. Glial activation and pathological pain. Neurochem. Int. 45 (2004) 389-395
82. Woolf C.J. Pain: moving from symptom control toward mechanism-specific pharmacologic management. Ann. Intern. Med. 140 (2004) 441-451
83. Woolf C.J., and Salter M.W. Neuronal plasticity: increasing the gain in pain. Science 288 (2000) 1765-1769
84. Zamuner S.R., Gutiérrez J.M., Muscará M.N., Teixeira S.A., and Teixeira C.F.P. Bothrops asper and Bothrops jararaca snake venoms trigger microbicidal functions of peritoneal leukocytes in vivo. Toxicon 39 (2001) 1505-1513
85. Zamuner S.R., Zuliani J.P., Fernandes C.M., Gutiérrez J.M., and Teixeira C.F.P. Inflammation induced by Bothrops asper venom: release of proinflammatory cytokines and eicosanoids, and role of adhesion molecules in leukocyte infiltration. Toxicon 46 (2005) 806-813
86. 2 isolated from Bothrops asper snake venom: role of catalytic activity. Toxicon 45 (2005) 335-346
87. 2. Toxicon 46 (2005) 523-532