The inhibition of apoptosis by melatonin in VSC4.1 motoneurons exposed to oxidative stress, glutamate excitotoxicity, or TNF-α toxicity involves membrane melatonin receptors

Journal of Pineal Research

Volumn 48, Issue 2, 2010, Pages 157-169

  Das, Arabinda ^a   McDowell, Misty ^a   Pava, Matthew J ^a   Smith, Joshua A ^a   Reiter, Russel J ^b   Woodward, John J ^a   Varma, Abhay K ^a   Ray, Swapan K ^c   Banik, Naren L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^c UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cytoprotective; Glutamate; H2O2; Melatonin; Motoneurons; Tumor necrosis factor alpha

Indexed keywords

CALPAIN; CYSTEINE PROTEINASE; MELATONIN; MELATONIN 1 RECEPTOR; MELATONIN 2 RECEPTOR; MELATONIN RECEPTOR; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; REACTIVE OXYGEN METABOLITE; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; CELL MEMBRANE POTENTIAL; CONTROLLED STUDY; ENZYME ACTIVITY; EXCITOTOXICITY; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MOTONEURON; MOTOR PERFORMANCE; NEUROPROTECTION; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CALCIUM; CASPASE 8; CELLS, CULTURED; GLUTAMIC ACID; HYDROGEN PEROXIDE; MELATONIN; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MOTOR NEURONS; OXIDATIVE STRESS; RECEPTOR, MELATONIN, MT1; RECEPTOR, MELATONIN, MT2; RECEPTORS, MELATONIN; TRYPTAMINES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 75149124310     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2009.00739.x     Document Type: Article

References (49)

1. Hardeland R. Melatonin: signaling mechanisms of a pleiotropic agent. Biofactors 2009 35 : 183 192.
2. Reiter RJ, Tan DX, Manchester LC, Pilar Terron M, Flores LJ, Koppisepi S. Medical implications of melatonin: receptor-mediated and receptor-independent actions. Adv Med Sci 2007 52 : 11 28.
3. Martín M, Macías M, Escames G, León J, Acuña-Castroviejo D. Melatonin but not vitamins C and E maintains glutathione homeostasis in t-butyl hydroperoxide-induced mitochondrial oxidative stress. FASEB J 2000 14 : 1677 1679. (Pubitemid 30688616)
4. Jou MJ, Peng TI, Yu PZ et al. Melatonin protects against common deletion of mitochondrial DNA-augmented mitochondrial oxidative stress and apoptosis. J Pineal Res 2007 43 : 389 403.
5. Reiter RJ, Paredes SD, Korkmaz A, Jou MJ, Tan DX. Melatonin combats molecular terrorism at the mitochondrial level. Interdisc Toxicol 2008 1 : 137 149.
6. Tan DX, Chen LD, Poeggeler B, Manchester LC, Reiter RJ. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr J 1993 1 : 57 60.
7. Carrillo-Vico A, García-Mauriño S, Calvo JR, Guerrero JM. Melatonin counteracts the inhibitory effect of PGE2 on IL-2 production in human lymphocytes via its mt1 membrane receptor. FASEB J 2003 17 : 755 757.
8. Tamura EK, Cecon E, Monteiro AW, Silva CL, Markus RP. Melatonin inhibits LPS-induced NO production in rat endothelial cells. J Pineal Res 2009 46 : 268 274.
9. Hill SM, Blask DE. Effects of the pineal hormone melatonin on the proliferation and morphological characteristics of human breast cancer cells (MCF-7) in culture. Cancer Res 1988 48 : 6121 6126.
10. Joo SS, Yoo YM. Melatonin induces apoptotic death in LNCaP cells via p38 and JNK pathways: therapeutic implications for prostate cancer. J Pineal Res 2009 47 : 8 14.
11. Sainz RM, Mayo JC, Uría H et al. The pineal neurohormone melatonin prevents in vivo and in vitro apoptosis in thymocytes. J Pineal Res 1995 19 : 178 188.
12. Martín V, Sainz RM, Antolín I, Mayo JC, Herrera F, Rodríguez C. Several antioxidant pathways are involved in astrocyte protection by melatonin. J Pineal Res 2002 33 : 204 212.
13. Manda K, Ueno M, Anzai K. Cranial irradiation-induced inhibition of neurogenesis in hippocampal dentate gyrus of adult mice: attenuation by melatonin pretreatment. J Pineal Res 2009 46 : 71 78.
14. Mayo JC, Sainz RM, Uría H, Antolín I, Esteban MM, Rodríguez C. Inhibition of cell proliferation: a mechanism likely to mediate the prevention of neuronal cell death by melatonin. J Pineal Res 1998 25 : 12 18.
15. Herrera F, Sainz RM, Mayo JC, Martín V, Antolín I, Rodríguez C. Glutamate induces oxidative stress not mediated by glutamate receptors or cystine transporters: protective effect of melatonin and other antioxidants. J Pineal Res 2001 31 : 356 362.
16. Beni SM, Kohen R, Reiter RJ, Tan DX, Shohami E. Melatonin-induced neuroprotection after closed head injury is associated with increased brain antioxidants and attenuated late-phase activation of NF-kappaB and AP-1. FASEB J 2004 18 : 149 151.
17. Jahnke G, Marr M, Myers C, Wilson R, Travlos G, Price C. Maternal and developmental toxicity evaluation of melatonin administered orally to pregnant Sprague-Dawley rats. Toxicol Sci 1999 50 : 271 279.
18. Costa EJ, Lopes RH, Lamy-Freund MT. Permeability of pure lipid bilayers to melatonin. J Pineal Res 1995 19 : 123 126.
19. Reiter RJ, Tan DX, Pappolla MA. Melatonin relieves the neural oxidative burden that contributes to dementias. Ann N Y Acad Sci 2004 1035 : 179 196.
20. Lissoni P, Bucovec R, Bonfanti A et al. Thrombopoietic properties of 5-methoxytryptamine plus melatonin versus melatonin alone in the treatment of cancer-related thrombocytopenia. J Pineal Res 2001 30 : 123 126.
21. León J, Macías M, Escames G et al. Structure-related inhibition of calmodulin-dependent neuronal nitric-oxide synthase activity by melatonin and synthetic kynurenines. Mol Pharmacol 2000 58 : 967 975.
22. Peyrot F, Ducrocq C. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res 2008 45 : 235 246.
23. Natarajasi M, Sadeghi K, Reiter RJ, Meltz ML. The neurohormone melatonin inhibits cytokine, mitogen and ionizing radiation induced NF-κB. Biochem Mol Biol Int 1995 37 : 1063 1070.
24. Chuang JI, Mohan N, Meltz ML, Reiter RJ. Effect of melatonin on NF-kappa-B DNA-binding activity in the rat spleen. Cell Biol Int 1996 20 : 687 692.
25. Becker-André M, Wiesenberg I, Schaeren-Wiemers N et al. Pineal gland hormone melatonin binds and activates an orphan of the nuclear receptor superfamily. J Biol Chem 1994 269 : 28531 28534.
26. 125I-iodomelatonin binding sites in the chicken brain. J Pineal Res 1990 9 : 179 191.
27. 125I-iodomelatonin binding sites in spleens of guinea pigs. Life Sci 1992 50 : 1719 1726.
28. Andrabi SA, Sayeed I, Siemen D, Wolf G, Horn TF. Direct inhibition of the mitochondrial permeability transition pore: a possible mechanism responsible for anti-apoptotic effects of melatonin. FASEB J 2004 18 : 869 871.
29. Tan DX, Manchester LC, Terron MP, Flores LJ, Tamura H, Reiter RJ. Melatonin as a naturally occurring co-substrate of quinone reductase-2, the putative MT3 melatonin membrane receptor: hypothesis and significance. J Pineal Res 2007 43 : 317 320.
30. Kilic U, Kilic E, Reiter RJ, Bassetti CL, Hermann DM. Signal transduction pathways involved in melatonin-induced neuroprotection after focal cerebral ischemia in mice. J Pineal Res 2005 38 : 67 71.
31. Koh PO. Melatonin attenuates the focal cerebral ischemic injury by inhibiting the dissociation of pBad from 14-3-3. J Pineal Res 2008 44 : 101 106.
32. Koh PO. Melatonin prevents the injury-induced decline of Akt/forkhead transcription factors phosphorylation. J Pineal Res 2008 45 : 199 203.
33. Coyle JT, Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science 1993 262 : 689 695.
34. Das A, Sribnick EA, Wingrave JM et al. Calpain activation in apoptosis of ventral spinal cord 4.1 (VSC4.1) motoneurons exposed to glutamate: calpain inhibition provides functional neuroprotection. J Neurosci Res 2005 81 : 551 562.
35. Das A, Banik NL, Ray SK. Differentiation decreased telomerase activity in rat glioblastoma C6 cells and increased sensitivity to IFN-γ and taxol for apoptosis. Neurochem Res 2007 32 : 2167 2183.
36. Das A, Banik NL, Ray SK. Garlic compounds generate reactive oxygen species leading to activation of stress kinases and cysteine proteases for apoptosis in human glioblastoma T98G and U87MG cells. Cancer 2007 110 : 1083 1095.
37. Brunner P, Sözer-Topcular N, Jockers R et al. Pineal and cortical melatonin receptors MT1 and MT2 are decreased in Alzheimer's disease. Eur J Histochem 2006 50 : 311 316.
38. Jimenez-Jorge S, Jimenez-Caliani AJ, Guerrero JM et al. Melatonin synthesis and melatonin-membrane receptor (MT1) expression during rat thymus development: role of the pineal gland. J Pineal Res 2005 391 : 77 83.
39. Savaskan E, Ayoub MA, Ravid R et al. Reduced hippocampal MT2 melatonin receptor expression in Alzheimer's disease. J Pineal Res 2005 38 : 10 16.
40. 125I]iodomelatonin binding and MT1 gene expression. J Pineal Res 2002 33 : 218 224.
41. Samantaray S, Das A, Thakore NP et al. Therapeutic potential of melatonin in traumatic central nervous system injury. J Pineal Res 2009 47 : 134 142.
42. Das A, Belagodu A, Reiter RJ, Ray SK, Banik NL. Cytoprotective effects of melatonin on C6 astroglial cells exposed to glutamate excitotoxicity and oxidative stress. J Pineal Res 2008 45 : 117 124.
43. Dubocovich ML, Rivera-Bermudez MA, Gerdin MJ, Masana MI. Molecular pharmacology, regulation and function of mammalian melatonin receptors. Front Biosci 2003 8 : 1093 1108.
44. Witt-Enderby PA, Radio NM, Doctor JS, Davis VL. Therapeutic treatments potentially mediated by melatonin receptors: potential clinical uses in the prevention of osteoporosis, cancer and as an adjuvant therapy. J Pineal Res 2006 41 : 297 305.
45. Chan AS, Lai FP, Lo RK, Voyno-Yasenetskaya TA, Stanbridge EJ, Wong YH. Melatonin mt1 and MT2 receptors stimulate c-Jun N-terminal kinase via pertussis toxin-sensitive and -insensitive G proteins. Cell Signal 2002 14 : 249 257.
46. Puig B, Gomez-Isla T, Ribe E et al. Expression of stress-activated kinases c-Jun N-terminal kinase (SAPK/JNK-P) and p38 kinase (p38-P), and tau hyperphosphorylation in neurites surrounding Aβ plaques in APP Tg2576 mice. Neuropathol Appl Neurobiol 2004 30 : 491 502.
47. Lin CF, Chen CL, Chang WT et al. Sequential caspase-2 and caspase-8 activation upstream of mitochondria during ceramide and etoposide-induced apoptosis. J Biol Chem 2004 279 : 40755 40761.
48. Lin AM, Fang SF, Chao PL, Yang CH. Melatonin attenuates arsenite-induced apoptosis in rat brain: involvement of mitochondrial and endoplasmic reticulum pathways and aggregation of alpha-synuclein. J Pineal Res 2007 43 : 163 171.
49. Macías M, Escames G, Leon J et al. Calreticulin-melatonin. An unexpected relationship. Eur J Biochem 2003 270 : 832 840.