Melatonin alleviates Echis carinatus venom-induced toxicities by modulating inflammatory mediators and oxidative stress

Journal of Pineal Research

Volumn 56, Issue 3, 2014, Pages 295-312

  Katkar, G D ^a   Shanmuga Sundaram, M ^a   Hemshekhar, M ^a   Sharma, D Rachana ^a   Sebastin Santhosh, M ^a   Sunitha, K ^a   Rangappa, K S ^a   Girish, K S ^a,b   Kemparaju, K ^a  

^a UNIVERSITY OF MYSORE   (India)

^b TUMKUR UNIVERSITY   (India)

Author keywords

Echis carinatus; hemorrhage; melatonin; oxidative damage; snake venom metalloproteases; viper venom

Indexed keywords

BIOLOGICAL MARKER; MELATONIN; VIPER VENOM; AUTACOID; FREE RADICAL;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD COMPONENT; CONTROLLED STUDY; DRUG EFFICACY; ECHIS CARINATUS; HISTOPATHOLOGY; INFLAMMATION; KIDNEY PARENCHYMA; LIVER; LIVER PROTECTION; MEDIATOR; MOUSE; MUSCLE; MUSCLE NECROSIS; NONHUMAN; OXIDATIVE STRESS; RAT; RENAL PROTECTION; SKIN; SNAKEBITE; TISSUE NECROSIS; TOXICITY; ANIMAL; BLOOD; DRUG EFFECTS; HEMORRHAGE; KIDNEY; METABOLISM; NECROSIS; PATHOLOGY; SKELETAL MUSCLE; SNAKE BITES; WISTAR RAT;

ANIMALS; FREE RADICALS; HEMORRHAGE; INFLAMMATION MEDIATORS; KIDNEY; LIVER; MELATONIN; MICE; MUSCLE, SKELETAL; NECROSIS; OXIDATIVE STRESS; RATS, WISTAR; SNAKE BITES; VIPER VENOMS;

EID: 84896134975     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12123     Document Type: Article

References (66)

1. Girish KS, Kemparaju K,. Overlooked issues of snakebite management: time for strategic approach. Curr Top Med Chem 2011; 11: 2494-2508.
2. Gutiérrez JM, Warrell DA, Williams DJ, et al. Global Snakebite Initiative. The need for full integration of snakebite envenoming within a global strategy to combat the neglected tropical diseases: the way forward. PLoS Negl Trop Dis 2013; 7: e2162.
3. Warrell DA,. Snake bite. Lancet 2010; 375: 77-88.
4. Simpson ID, Norris RL,. Snakes of medical importance in India: is the concept of the "Big 4" still relevant and useful? Wilderness Environ Med 2007; 18: 2-9.
5. Mahadeswaraswamy YH, Nagaraju S, Girish KS, et al. Local tissue destruction and procoagulation properties of Echis carinatus venom: inhibition by Vitis vinifera seed methanol extract. Phytother Res 2008; 22: 963-969.
6. Sebastin Santhosh M, Hemshekhar M, Thushara RM, et al. Vipera russelli venom-induced oxidative stress and hematological alterations: Amelioration by crocin a dietary colorant. Cell Biochem Funct 2013; 31: 41-50.
7. Santhosh MS, Sundaram MS, Sunitha K, et al. Viper venom-induced oxidative stress and activation of inflammatory cytokines: a therapeutic approach for overlooked issues of snakebite management. Inflamm Res 2013; 62: 721-731.
8. Rother RP, Bell L, Hillmen P, et al. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA 2005; 293: 1653-1662.
9. Barraviera B, Coelho KY, Curi PR, et al. Liver dysfunction in patients bitten by Crotalus Durissus terrificus (Laurenti, 1768) snakes in Botucatu (State of São Paulo, Brazil). Rev Inst Med Trop Sao Paulo 1995; 37: 63-69.
10. Yamasaki SC, Villarroel JS, Barone JM, et al. Aminopeptidase activities, oxidative stress and renal function in Crotalus durissus terrificus envenomation in mice. Toxicon 2008; 52: 445-454.
11. Kanjanabuch T, Sitprija V,. Snakebite nephrotoxicity in Asia. Semin Nephrol 2008; 28: 363-372.
12. Da Silva JG, Da Silva Soley B, Gris V, et al. Effects of the Crotalus durissus terrificus snake venom on hepatic metabolism and oxidative stress. J Biochem Mol Toxicol 2011; 25: 195-203.
13. Sajevic T, Leonardi A, Križaj I,. Haemostatically active proteins in snake venoms. Toxicon 2011; 57: 627-645.
14. de Morais IC, Torres AF, Pereira GJ, et al. Bothrops leucurus venom induces nephrotoxicity in the isolated perfused kidney and cultured renal tubular epithelia. Toxicon 2013; 61: 38-46.
15. Girish KS, Paul M, Thushara RM, et al. Melatonin elevates apoptosis in human platelets via ROS mediated mitochondrial damage. Biochem Biophys Res Commun 2013; 438: 198-204.
16. Mercolini L, Mandrioli R, Raggi MA,. Content of melatonin and other antioxidants in grape-related foodstuffs: measurement using a MEPS-HPLC-F method. J Pineal Res 2012; 53: 21-28.
17. Roopin M, Yacobi YZ, Levy O,. Occurrence, diel patterns, and the influence of melatonin on the photosynthetic performance of cultured Symbiodinium. J Pineal Res 2013; 55: 89-100.
18. Hardeland R, Madrid JA, Tan DX, et al. Melatonin, the circadian multioscillator system and health: the need for detailed analyses of peripheral melatonin signaling. J Pineal Res 2012; 52: 139-166.
19. Barrett P, Bolborea M,. Molecular pathways involved in seasonal body weight and reproductive responses governed by melatonin. J Pineal Res 2012; 52: 376-388.
20. Reiter RJ, Tan DX, Rosales-Corral S, et al. The universal nature, unequal distribution and antioxidant functions of melatonin and its derivatives. Mini Rev Med Chem 2013; 13: 373-384.
21. Favero G, Rodella LF, Reiter RJ, et al. Melatonin and its atheroprotective effects: a review. Mol Cell Endocrinol 2013; 382: 926-937.
22. Mareš J, Stopka P, Nohejlová K, et al. Oxidative stress induced by epileptic seizure and its attenuation by melatonin. Physiol Res 2013; 62: 67-74.
23. Mauriz JL, Collado PS, Veneroso C, et al. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J Pineal Res 2013; 54: 1-14.
24. Gitto E, Marseglia L, Manti S, et al. Protective role of melatonin in neonatal diseases. Oxid Med Cell Longev 2013; 0: 980374.
25. Bizzarri M, Proietti S, Cucina A, et al. Molecular mechanisms of the pro-apoptotic actions of melatonin in cancer: a review. Expert Opin Ther Targets 2013; 17: 1483-1496.
26. Aydogan MS, Erdogan MA, Polat A, et al. Protective effects of melatonin and β-d-glucan against liver injury in rats-a comparative study. Adv Clin Exp Med 2013; 22: 621-627.
27. Hardeland R,. Melatonin and the theories of aging: a critical appraisal of melatonin's role in antiaging mechanisms. J Pineal Res 2013; 55: 325-356.
28. Espino J, Pariente JA, Rodríguez AB,. Oxidative stress and immunosenescence: therapeutic effects of melatonin. Oxid Med Cell Longev 2012; 2012: 670294.
29. Tan DX, Chen LD, Poeggeler B, et al. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr J 1993; 1: 57-60.
30. Galano A, Tan DX, Reiter RJ,. On the free radical scavenging activities of melatonin's metabolites, AFMK and AMK. J Pineal Res 2013; 54: 245-257.
31. Kondo H, Kondo S, Ikezawa H, et al. Studies on the quantitative method for determination of hemorrhagic activity of Habu snake venom. Jpn J Med Sci Biol 1960; 13: 43-52.
32. Heussen C, Dowdle EB,. Electrophoretic analysis of plasminogen activators in polyacrylamide gels containing sodium dodecyl sulphate and copolymerized substrates. Anal Biochem 1980; 102: 196-202.
33. Mahadeswaraswamy YH, Kumar MS, Gowtham YJ, et al. The polyphenol 3, 4, 5-tri-hydroxy benzoic acid inhibits Indian Daboia russelli venom and its hemorrhagic complex induced local toxicity. Curr Top Med Chem 2011; 11: 2520-2530.
34. Tung JS, Mark GE, Hollis GF,. A microplate assay for hyaluronidase and hyaluronidase inhibitors. Anal Biochem 1994; 223: 149-152.
35. Gutiérrez JM, Arce V, Brenes F, et al. 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.
36. Yamakawa M, Nozaki M, Hokama Z,. Fractionation of Sakishima habu (Trimeresurus elegans) venom and lethal hemorrhagic and edema forming activities of the fractions. In: Animal, Plant and Microbial Toxins., Ohsaka A, Hayashi K, Sawai Y, eds., Plenum Press, New York, NY, USA, 1976; pp. 97-109.
37. 2. Thromb Haemost 1983; 49: 151.
38. Ouyang C, Teng CM,. Fibrinogenolytic enzymes of Trimeresurus mucrosquamatus venom. Biochim Biophys Acta 1976; 420: 298-308.
39. Kumar MS, Devaraj VR, Vishwanath BS, et al. Anti-coagulant activity of a metalloprotease: further characterization from the Indian cobra (Naja naja) venom. J Thromb Thrombolysis 2010; 29: 340-348.
40. Driver AS, Kodavanti PS, Mundy WR,. Age related changes in reactive oxygen species production in rat brain homogenates. Neurotoxicol Teratol 2000; 22: 175-181.
41. Botsoglou N, Taitzoglou I, Zervos I, et al. Potential of long-term dietary administration of rosemary in improving the antioxidant status of rat tissues following carbon tetrachloride intoxication. Food Chem Toxicol 2010; 48: 944-950.
42. Ohkawa H, Ohishi N, Yagi K,. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351-358.
43. Levine RL, Garland D, Oliver CN, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 1990; 186: 464-478.
44. Kostyuk VA, Potapovich AI,. Superoxide driven oxidation of quercetin under simple sensitive assay for determination of superoxide dismutase. Biochem Int 1989; 19: 1117-1124.
45. Aebi H,. Catalase. Methods Enzymol 1059; 1984: 1211-1225.
46. Guthenberg C, Alin P, Mannervik B,. Glutathione transferase from rat testis. Methods Enzymol 1985; 113: 507-510.
47. Wendel A,. Glutathione peroxidase. Methods Enzymol 1981; 77: 325-333.
48. Carlberg I, Mannervik B,. Glutathione reductase. Methods Enzymol 1985; 113: 484-490.
49. Lowry OH, Rosebrough NJ, Farr AL, et al. Protein measurement using folin-phenol reagent. J Biol Chem 1951; 193: 265-275.
50. Hernández R, Cabalceta C, Saravia-Otten P, et al. Poor regenerative outcome after skeletal muscle necrosis induced by Bothrops asper venom: alterations in microvasculature and nerves. PLoS ONE 2011; 6: e19834.
51. Anai K, Sugiki M, Yoshida E, et al. Neutralization of a snake venom hemorrhagic metalloproteinase prevents coagulopathy after subcutaneous injection of Bothrops jararaca venom in rats. Toxicon 2002; 40: 63-68.
52. Girish KS, Jagadeesha DK, Rajeev KB, et al. Snake venom hyaluronidase: an evidence for isoforms and extracellular matrix degradation. Mol Cell Biochem 2002; 240: 105-110.
53. Girish KS, Shashidharamurthy R, Nagaraju S, et al. Isolation and characterization of hyaluronidase a "spreading factor" from Indian cobra (Naja naja) venom. Biochimie 2004; 86: 193-202.
54. Girish KS, Kemparaju K, Nagaraju S, et al. Hyaluronidase inhibitors: a biological and therapeutic perspective. Curr Med Chem 2009; 16: 2261-2288.
55. Santhosh MS, Hemshekhar M, Sunitha K, et al. Snake venom induced local toxicities: plant secondary metabolites as an auxiliary therapy. Mini Rev Med Chem 2013; 13: 106-123.
56. Sunitha K, Hemshekhar M, Santhosh MS, et al. Inhibition of hemorrhagic activity of viper venoms by N-acetyl cysteine: involvement of N-acetyl and thiol groups. Curr Top Med Chem 2011; 11: 2589-2600.
57. Sunitha K, Hemshekhar M, Gaonkar SL, et al. Neutralization of haemorrhagic activity of viper venoms by 1-(3-dimethylaminopropyl)-1-(4- fluorophenyl)-3-oxo-1,3-dihydroisobenzofuran-5-carbonitrile. Basic Clin Pharmacol Toxicol 2011; 109: 292-299.
58. Pereañez JA, Patiño AC, Rey-Suarez P, et al. Glycolic acid inhibits enzymatic, hemorrhagic and edema-inducing activities of BaP1, a P-I metalloproteinase from Bothrops asper snake venom: insights from docking and molecular modeling. Toxicon 2013; 71: 41-48.
59. Fox JW, Serrano SM,. Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon 2005; 45: 969-985.
60. Albuquerque PL, Jacinto CN, Silva Junior GB, et al. Acute kidney injury caused by Crotalus and Bothrops snake venom: a review of epidemiology, clinical manifestations and treatment. Rev Inst Med Trop Sao Paulo 2013; 55: 295-301.
61. Marcussi S, Santos PR, Menaldo DL, et al. Evaluation of the genotoxicity of Crotalus durissus terrificus snake venom and its isolated toxins on human lymphocytes. Mutat Res 2011; 724: 59-63.
62. Zamuner SR, Zuliani JP, Fernandes CM, et al. Inflammation induced by Bothrops asper venom: release of proinflammatory cytokines and eicosanoids, and role of adhesion molecules in leukocyte infiltration. Toxicon 2005; 46: 806-813.
63. Fernandes CM, Zamuner SR, Zuliani JP, et al. Inflammatory effects of BaP1 a metalloproteinase isolated from Bothrops asper snake venom: leukocyte recruitment and release of cytokines. Toxicon 2006; 47: 549-559.
64. Loscalzo J,. Membrane redox state and apoptosis: death by peroxide. Cell Metab 2008; 8: 182-183.
65. Giustarini D, Dalle-Donne I, Milzani A, et al. Low molecular mass thiols, disulfides and protein mixed disulfides in rat tissues: influence of sample manipulation, oxidative stress and ageing. Mech Ageing Dev 2011; 132: 141-148.
66. Rodriguez C, Mayo JC, Sainz RM, et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9.