Melatonin inhibits free radical-mediated mitochondrial-dependent hepatocyte apoptosis and liver damage induced during malarial infection

Journal of Pineal Research

Volumn 43, Issue 4, 2007, Pages 372-381

  Guha, Mithu ^a   Maity, Pallab ^a   Choubey, Vinay ^b   Mitra, Kalyan ^b   Reiter, Russel J ^c   Bandyopadhyay, Uday ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b CENTRAL DRUG RESEARCH INSTITUTE   (India)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Apoptosis; Liver; Malaria; Melatonin; Oxidative stress

Indexed keywords

ALPHA TOCOPHEROL; ASCORBIC ACID; CASPASE 3; DNA FRAGMENT; FREE RADICAL; GLUTATHIONE; HYDROXYL RADICAL; MELATONIN; MEMBRANE PROTEIN; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FLUOROMETRY; LIPID PEROXIDATION; LIVER FUNCTION; LIVER FUNCTION TEST; LIVER INJURY; LIVER MITOCHONDRION; MALARIA; MOUSE; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; DNA FRAGMENTATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FREE RADICALS; GENE EXPRESSION; HEPATOCYTES; HYDROXYL RADICAL; LIPID PEROXIDATION; LIVER; LIVER FUNCTION TESTS; MALARIA; MELATONIN; MICE; MICROSCOPY, ELECTRON; MITOCHONDRIA; OXIDATIVE STRESS; PLASMODIUM YOELII; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 34848826062     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2007.00488.x     Document Type: Article

References (72)

1. WHO. Expert Committee on Malaria. World Health Organ Tech Rep Ser 2000 892 : 1 74.
2. Sachs J, Malaney P. The economic and social burden of malaria. Nature 2002 415 : 680 685.
3. Kochar DK, Agarwal P, Kochar SK et al. Hepatocyte dysfunction and hepatic encephalopathy in Plasmodium falciparum malaria. QJM 2003 96 : 505 512.
4. Guha M, Kumar S, Choubey V et al. Apoptosis in liver during malaria: role of oxidative stress and implication of mitochondrial pathway. FASEB J 2006 20 : 1224 1226.
5. Ehrich JH, Eke FU. Malaria-induced renal damage: facts and myths. Pediatr Nephrol 2007 22 : 626 637.
6. Herrera JM. [Cardiac lesions in vivax malaria. Study of a case with coronary and myocardial damage]. Arch Inst Cardiol Mex 1960 30 : 26 36.
7. Grobusch MP, Kremsner PG. Uncomplicated malaria. Curr Top Microbiol Immunol 2005 295 : 83 104.
8. Vuong PN, Richard F, Snounou G et al. Development of irreversible lesions in the brain, heart and kidney following acute and chronic murine malaria infection. Parasitology 1999 6 : 543 553.
9. Verma S, Aggarwal A. Hyper-reactive malarial splenomegaly: rare cause of pyrexia of unknown origin. Ind J Pediatr 2007 74 : 409 411.
10. Anstey NM, Handojo T, Pain MC et al. Lung injury in vivax malaria: pathophysiological evidence for pulmonary vascular sequestration and posttreatment alveolar-capillary inflammation. J Infect Dis 2007 195 : 589 596.
11. Schofield L. Intravascular infiltrates and organ-specific inflammation in malaria pathogenesis. Immunol Cell Biol 2007 85 : 130 137.
12. Pabon A, Carmona J, Burgos LC et al. Oxidative stress in patients with non-complicated malaria. Clin Biochem 2003 36 : 71 78.
13. Clark IA, Chaudhri G, Cowden WB. Some roles of free radicals in malaria. Free Radic Biol Med 1989 6 : 315 321.
14. Siddiqi NJ, Pandey VC. Studies on hepatic oxidative stress and antioxidant defence systems during arteether treatment of Plasmodium yoelii nigeriensis infected mice. Mol Cell Biochem 1999 196 : 169 173.
15. Rodriguez-Acosta A, Finol HJ, Pulido-Mendez M et al. Liver ultrastructural pathology in mice infected with Plasmodium berghei. J Submicrosc Cytol Pathol 1998 30 : 299 307.
16. Reiter RJ, Tan DX, Maldonado MD. Melatonin as an antioxidant: physiology versus pharmacology. J Pineal Res 2005 39 : 215 216.
17. Ozdemir D, Uysal N, Gonenc S et al. Effect of melatonin on brain oxidative damage induced by traumatic brain injury in immature rats. Physiol Res 2005 54 : 631 637.
18. Cuzzocrea S, Reiter RJ. Pharmacological action of melatonin in shock, inflammation and ischemia/reperfusion injury. Eur J Pharmacol 2001 426 : 1 10.
19. Allegra M, Reiter RJ, Tan DX et al. The chemistry of melatonin's interaction with reactive species. J Pineal Res 2003 34 : 1 10.
20. Rosen J, Than NN, Koch D et al. Interactions of melatonin and its metabolites with the ABTS cation radical: extension of the radical scavenger cascade and formation of a novel class of oxidation products, C2-substituted 3-indolinones. J Pineal Res 2006 41 : 374 381.
21. Manda K, Ueno M, Anzai K. AFMK, a melatonin metabolite, attenuates X-ray-induced oxidative damage to DNA, proteins and lipids in mice. J Pineal Res 2007 42 : 386 393.
22. Tan DX, Manchester LC, Terron MP et al. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007 42 : 28 42.
23. Reiter RJ, Tan DX, Osuna C et al. Actions of melatonin in the reduction of oxidative stress. A review. J Biomed Sci 2000 7 : 444 458.
24. Natarajan M, Reiter RJ, Meltz ML et al. Effect of melatonin on cell growth, metabolic activity, and cell cycle distribution. J Pineal Res 2001 31 : 228 233.
25. Dobsak P, Siegelova J, Eicher JC et al. Melatonin protects against ischemia-reperfusion injury and inhibits apoptosis in isolated working rat heart. Pathophysiology 2003 9 : 179 187.
26. Kaneko S, Okumura K, Numaguchi Y et al. Melatonin scavenges hydroxyl radical and protects isolated rat hearts from ischemic reperfusion injury. Life Sci 2000 67 : 101 112.
27. Lagneux C, Joyeux M, Demenge P et al. Protective effects of melatonin against ischemia-reperfusion injury in the isolated rat heart. Life Sci 2000 66 : 503 509.
28. Leon J, Acuna-Castroviejo D, Escames G et al. Melatonin mitigates mitochondrial malfunction. J Pineal Res 2005 38 : 1 9.
29. Maldonado MD, Murillo-Cabezas F, Terron MP et al. The potential of melatonin in reducing morbidity-mortality after craniocerebral trauma. J Pineal Res 2007 42 : 1 11.
30. Catala A, Zvara A, Puskas LG et al. Melatonin-induced gene expression changes and its preventive effects on adriamycin-induced lipid peroxidation in rat liver. J Pineal Res 2007 42 : 43 49.
31. Xu J, Sun S, Wei W et al. Melatonin reduces mortality and oxidatively mediated hepatic and renal damage due to diquat treatment. J Pineal Res 2007 42 : 166 171.
32. Rodriguez C, Mayo JC, Sainz RM et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004 36 : 1 9.
33. Sewerynek E, Abe M, Reiter RJ et al. Melatonin administration prevents lipopolysaccharide-induced oxidative damage in phenobarbital-treated animals. J Cell Biochem 1995 58 : 436 444.
34. Sewerynek E, Melchiorri D, Chen L et al. Melatonin reduces both basal and bacterial lipopolysaccharide-induced lipid peroxidation in vitro. Free Radic Biol Med 1995 19 : 903 909.
35. Adlam VJ, Harrison JC, Porteous CM et al. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J 2005 19 : 1088 1095.
36. Martin M, Macias M, Escames G et al. Melatonin but not vitamins C and E maintains glutathione homeostasis in t-butyl hydroperoxide-induced mitochondrial oxidative stress. FASEB J 2000 14 : 1677 1679.
37. Petrosillo G, Di Venosa N, Pistolese M et al. Protective effect of melatonin against mitochondrial dysfunction associated with cardiac ischemia-reperfusion: role of cardiolipin. FASEB J 2006 20 : 269 276.
38. Pandi-Perumal SR, Srinivasan V, Maestroni GJ et al. Melatonin: nature's most versatile biological signal? FEBS J 2006 273 : 2813 2838.
39. Jou MJ, Peng TI, Reiter RJ et al. Visualization of the antioxidative effects of melatonin at the mitochondrial level during oxidative stress-induced apoptosis of rat brain astrocytes. J Pineal Res 2004 37 : 55 70.
40. Andrabi SA, Sayeed I, Siemen D et al. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti-apoptotic effects of melatonin. FASEB J 2004 18 : 869 871.
41. Montilla P, Cruz A, Padillo FJ et al. Melatonin versus vitamin E as protective treatment against oxidative stress after extra-hepatic bile duct ligation in rats. J Pineal Res 2001 31 : 138 144.
42. Lopez PM, Finana IT, De Agueda MC et al. Protective effect of melatonin against oxidative stress induced by ligature of extra-hepatic biliary duct in rats: comparison with the effect of S-adenosyl-L-methionine. J Pineal Res 2000 28 : 143 149.
43. Poeggeler B, Reiter RJ, Tan DX et al. Melatonin, hydroxyl radical-mediated oxidative damage, and aging: a hypothesis. J Pineal Res 1993 14 : 151 168.
44. Wissing D, Mouritzen H, Jaattela M. TNF-induced mitochondrial changes and activation of apoptotic proteases are inhibited by A20. Free Radic Biol Med 1998 25 : 57 65.
45. Lowry OH, Rosebrough NJ, Farr AL et al. Protein measurement with the Folin phenol reagent. J Biol Chem 1951 193 : 265 275.
46. Cossarizza A, Baccarani-Contri M, Kalashnikova G et al. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5′,6,6′-tetrachloro-1,1',3, 3'-tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 1993 197 : 40 45.
47. Sedlak J, Lindsay RH. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 1968 25 : 192 205.
48. Buege JA, Aust SD. Microsomal lipid peroxidation. Meth Enzymol 1978 52 : 302 310.
49. Biswas K, Bandyopadhyay U, Chattopadhyay I et al. A novel antioxidant and antiapoptotic role of omeprazole to block gastric ulcer through scavenging of hydroxyl radical. J Biol Chem 2003 278 : 10993 11001.
50. Levine RL, Garland D, Oliver CN et al. Determination of carbonyl content in oxidatively modified proteins. Meth Enzymol 1990 186 : 464 478.
51. Babbs CF, Steiner MG. Detection and quantitation of hydroxyl radical using dimethyl sulfoxide as molecular probe. Methods Enzymol 1990 186 : 137 147.
52. Kacmaz A, User EY, Sehirli AO et al. Protective effect of melatonin against ischemia/reperfusion-induced oxidative remote organ injury in the rat. Surg Today 2005 35 : 744 750.
53. Bao Q, Shi Y. Apoptosome: a platform for the activation of initiator caspases. Cell Death Differ 2007 14 : 56 65.
54. Steller H. Mechanisms and genes of cellular suicide. Science 1995 267 : 1445 1449.
55. Pagliara P, Carla EC, Caforio S et al. Kupffer cells promote lead nitrate-induced hepatocyte apoptosis via oxidative stress. Comp Hepatol 2003 2 : 8.
56. Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2002 2 : 647 656.
57. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007 87 : 99 163.
58. Zimmermann KC, Bonzon C, Green DR. The machinery of programmed cell death. Pharmacol Ther 2001 92 : 57 70.
59. Gulbins E, Dreschers S, Bock J. Role of mitochondria in apoptosis. Exp Physiol 2003 88 : 85 90.
60. Li P, Nijhawan D, Budihardjo I et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997 91 : 479 489.
61. Jiang X, Wang X. Cytochrome c-mediated apoptosis. Annu Rev Biochem 2004 73 : 87 106.
62. Feng Z, Qin C, Chang Y et al. Early melatonin supplementation alleviates oxidative stress in a transgenic mouse model of Alzheimer's disease. Free Radic Biol Med 2006 40 : 101 109.
63. Farber JL, Kyle ME, Coleman JB. Mechanisms of cell injury by activated oxygen species. Lab Invest 1990 62 : 670 679.
64. Pieri C, Moroni F, Marra M et al. Melatonin is an efficient antioxidant. Arch Gerontol Geriatr 1995 20 : 159 165.
65. Poeggeler B, Thuermann S, Dose A et al. Melatonin's unique radical scavenging properties - roles of its functional substituents as revealed by a comparison with its structural analogs. J Pineal Res 2002 33 : 20 30.
66. Budu A, Peres R, Bueno VB et al. N1-acetyl-N2-formyl-5-methoxykynuramine modulates the cell cycle of malaria parasites. J Pineal Res 2007 42 : 261 266.
67. Toure-Balde A, Sarthou JL, Aribot G et al. Plasmodium falciparum induces apoptosis in human mononuclear cells. Infect Immun 1996 64 : 744 750.
68. Dockrell DH. Apoptotic cell death in the pathogenesis of infectious diseases. J Infect 2001 42 : 227 234.
69. Mcvicker BL, Tuma DJ, Kubik JL et al. Ethanol-induced apoptosis in polarized hepatic cells possibly through regulation of the Fas pathway. Alcohol Clin Exp Res 2006 30 : 1906 1915.
70. Lee HJ, Oh YK, Rhee M et al. The role of STAT1/IRF-1 on synergistic ROS production and loss of mitochondrial transmembrane potential during hepatic cell death induced by LPS/d-GalN. J Mol Biol 2007 369 : 967 984.
71. Kim WH, Hong F, Radaeva S et al. STAT1 plays an essential role in LPS/D-galactosamine-induced liver apoptosis and injury. Am J Physiol Gastrointest Liver Physiol 2003 285 : G761 G768.
72. Liu D, Liu XY, Robinson D et al. Suppression of Staphylococcal enterotoxin B-induced toxicity by a nuclear import inhibitor. J Biol Chem 2004 279 : 19239 19246.