Neuroprotective effect of melatonin against ischemia is partially mediated by alpha-7 nicotinic receptor modulation and HO-1 overexpression

Journal of Pineal Research

Volumn 56, Issue 2, 2014, Pages 204-212

  Parada, Esther ^a   Buendia, Izaskun ^a   León, Rafael ^a,b   Negredo, Pilar ^c   Romero, Alejandro ^a,e   Cuadrado, Antonio ^a,d   López, Manuela G ^a,b   Egea, Javier ^a,b  

^a INSTITUTO TEÓFILO HERNANDO   (Spain)

^b HOSPITAL UNIVERSITARIO DE LA PRINCESA   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d CSIC   (Spain)

^e UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

HO 1; ischemia; melatonin; neuroprotection; nicotinic receptors

Indexed keywords

ALPHA BUNGAROTOXIN; ANTIOXIDANT; BUNGAROTOXIN RECEPTOR; HEME OXYGENASE 1; LUZINDOLE; MELATONIN; METHYLLYCACONITINE; NICOTINIC RECEPTOR; OXYGEN; PROPIDIUM IODIDE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2; GLUCOSE; NEUROPROTECTIVE AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BINDING SITE; BRAIN INFARCTION; BRAIN ISCHEMIA; CELL DEATH; CELL STIMULATION; CELL VIABILITY; FLUORESCENCE ANALYSIS; GENE OVEREXPRESSION; IN VIVO STUDY; KNOCKOUT MOUSE; LUCIFERASE ASSAY; MOTOR COORDINATION; MOUSE; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; ORGANOTYPIC HIPPOCAMPAL CULTURE; OXIDATIVE STRESS; RAT; REOXYGENATION; REPORTER GENE; SLICE CULTURE; THERAPY EFFECT; WESTERN BLOTTING; WILD TYPE; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; HIPPOCAMPAL CA1 REGION; HUMAN; ISCHEMIA; METABOLISM; THROMBOSIS; TUMOR CELL LINE;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CELL LINE, TUMOR; CELLS, CULTURED; GLUCOSE; HEME OXYGENASE-1; HUMANS; ISCHEMIA; MELATONIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPROTECTIVE AGENTS; OXYGEN; RECEPTORS, NICOTINIC; THROMBOSIS;

EID: 84893752602     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12113     Document Type: Article

References (50)

1. 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.
2. Zha L, Fan L, Sun G, et al. Melatonin sensitizes human hepatoma cells to endoplasmic reticulum stress-induced apoptosis. J Pineal Res 2012; 52: 322-331.
3. Gitto E, Aversa S, Salpietro CD, et al. Pain in neonatal intensive care: role of melatonin as an analgesic antioxidant. J Pineal Res 2012; 52: 291-295.
4. Dominguez-Alonso A, Ramirez-Rodriguez G, Benitez-King G,. Melatonin increases dendritogenesis in the hilus of hippocampal organotypic cultures. J Pineal Res 2012; 52: 427-436.
5. 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 2012. doi: 10.1111/j.1600-079X.2012.01014.x.
6. Galano A, Tan DX, Reiter RJ,. Melatonin as a natural ally against oxidative stress: a physicochemical examination. J Pineal Res 2011; 51: 1-16.
7. 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.
8. Tan DX, Chen LD, Poeggeler B, et al. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr J 1993; 1: 57-60.
9. 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. (Pubitemid 23253014)
10. 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. (Pubitemid 34833071)
11. Tan DX, Manchester LC, Reiter RJ, et al. Melatonin directly scavenges hydrogen peroxide: a potentially new metabolic pathway of melatonin biotransformation. Free Radic Biol Med 2000; 29: 1177-1185.
12. Reiter RJ, Tan DX, Manchester LC, et al. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem Biophys 2001; 34: 237-256. (Pubitemid 33615836)
13. Ximenes VF, Silva SO, Rodrigues MR, et al. Superoxide-dependent oxidation of melatonin by myeloperoxidase. J Biol Chem 2005; 280: 38160-38169. (Pubitemid 43853710)
14. Rodriguez C, Mayo JC, Sainz RM, et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9. (Pubitemid 38130283)
15. Tomas-Zapico C, Coto-Montes A,. A proposed mechanism to explain the stimulatory effect of melatonin on antioxidative enzymes. J Pineal Res 2005; 39: 99-104. (Pubitemid 41140746)
16. Lopez-Burillo S, Tan DX, Mayo JC, et al. Melatonin, xanthurenic acid, resveratrol, EGCG, vitamin C and alpha-lipoic acid differentially reduce oxidative DNA damage induced by Fenton reagents: a study of their individual and synergistic actions. J Pineal Res 2003; 34: 269-277. (Pubitemid 36469773)
17. Romero A, Egea J, Garcia AG, et al. Synergistic neuroprotective effect of combined low concentrations of galantamine and melatonin against oxidative stress in SH-SY5Y neuroblastoma cells. J Pineal Res 2010; 49: 141-148.
18. Reiter RJ, Tan DX, Sainz RM, et al. Melatonin: reducing the toxicity and increasing the efficacy of drugs. J Pharm Pharmacol 2002; 54: 1299-1321. (Pubitemid 35174175)
19. Balami JS, Chen RL, Grunwald IQ, et al. Neurological complications of acute ischaemic stroke. Lancet Neurol 2011; 10: 357-371.
20. Lakhan SE, Kirchgessner A, Hofer M,. Inflammatory mechanisms in ischemic stroke: therapeutic approaches. J Transl Med 2009; 7: 97.
21. Jung JE, Kim GS, Chen H, et al. Reperfusion and neurovascular dysfunction in stroke: from basic mechanisms to potential strategies for neuroprotection. Mol Neurobiol 2010; 41: 172-179.
22. Manev H, Uz T, Kharlamov A, et al. Increased brain damage after stroke or excitotoxic seizures in melatonin-deficient rats. FASEB J 1996; 10: 1546-1551. (Pubitemid 26384452)
23. Kensler TW, Wakabayashi N, Biswal S,. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu Rev Pharmacol Toxicol 2007; 47: 89-116.
24. Kaspar JW, Niture SK, Jaiswal AK,. Nrf 2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 2009; 47: 1304-1309.
25. Shah ZA, Li RC, Thimmulappa RK, et al. Role of reactive oxygen species in modulation of Nrf2 following ischemic reperfusion injury. Neuroscience 2007; 147: 53-59. (Pubitemid 46881103)
26. Innamorato NG, Rojo AI, Garcia-Yague AJ, et al. The transcription factor Nrf2 is a therapeutic target against brain inflammation. J Immunol 2008; 181: 680-689.
27. Kim YS, Zhuang H, Koehler RC, et al. Distinct protective mechanisms of HO-1 and HO-2 against hydroperoxide-induced cytotoxicity. Free Radic Biol Med 2005; 38: 85-92. (Pubitemid 39626912)
28. Yang C, Zhang X, Fan H, et al. Curcumin upregulates transcription factor Nrf2, HO-1 expression and protects rat brains against focal ischemia. Brain Res 2009; 1282: 133-141.
29. Carneiro RC, Markus RP,. Presynaptic nicotinic receptors involved in release of noradrenaline and ATP from the prostatic portion of the rat vas deferens. J Pharmacol Exp Ther 1990; 255: 95-100. (Pubitemid 20361488)
30. Carneiro RC, Cipolla-Neto J, Markus RP,. Diurnal variation of the rat vas deferens contraction induced by stimulation of presynaptic nicotinic receptors and pineal function. J Pharmacol Exp Ther 1991; 259: 614-619.
31. Markus RP, Zago WM, Carneiro RC,. Melatonin modulation of presynaptic nicotinic acetylcholine receptors in the rat vas deferens. J Pharmacol Exp Ther 1996; 279: 18-22. (Pubitemid 27166888)
32. Markus RP, Santos JM, Zago W, et al. Melatonin nocturnal surge modulates nicotinic receptors and nicotine-induced [3H]glutamate release in rat cerebellum slices. J Pharmacol Exp Ther 2003; 305: 525-530. (Pubitemid 36459166)
33. Stoppini L, Buchs PA, Muller D,. A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 1991; 37: 173-182.
34. Parada E, Egea J, Buendia I, et al. The microglial alpha7-acetylcholine nicotinic receptor is a key element in promoting neuroprotection by inducing heme oxygenase-1 via nuclear factor erythroid-2-related factor 2. Antioxid Redox Signal 2013; 19: 1135-1148.
35. Zou LY, Cheung RT, Liu S, et al. Melatonin reduces infarction volume in a photothrombotic stroke model in the wild-type but not cyclooxygenase-1-gene knockout mice. J Pineal Res 2006; 41: 150-156. (Pubitemid 44141750)
36. Avendano C, Roda JM, Carceller F, et al. Morphometric study of focal cerebral ischemia in rats: a stereological evaluation. Brain Res 1995; 673: 83-92.
37. Quinn LP, Perren MJ, Brackenborough KT, et al. A beam-walking apparatus to assess behavioural impairments in MPTP-treated mice: pharmacological validation with R-(-)-deprenyl. J Neurosci Methods 2007; 164: 43-49. (Pubitemid 46938674)
38. de Ryck M, van Reempts J, Borgers M, et al. Photochemical stroke model: flunarizine prevents sensorimotor deficits after neocortical infarcts in rats. Stroke 1989; 20: 1383-1390. (Pubitemid 19254555)
39. Reiter RJ, Tan DX,. Melatonin: a novel protective agent against oxidative injury of the ischemic/reperfused heart. Cardiovasc Res 2003; 58: 10-19. (Pubitemid 36351618)
40. Okatani Y, Wakatsuki A, Reiter RJ, et al. Protective effect of melatonin against mitochondrial injury induced by ischemia and reperfusion of rat liver. Eur J Pharmacol 2003; 469: 145-152. (Pubitemid 36629560)
41. Sener G, Sehirli AO, Keyer-Uysal M, et al. The protective effect of melatonin on renal ischemia-reperfusion injury in the rat. J Pineal Res 2002; 32: 120-126. (Pubitemid 34289590)
42. Reiter RJ, Tan DX, Leon J, et al. When melatonin gets on your nerves: its beneficial actions in experimental models of stroke. Exp Biol Med (Maywood) 2005; 230: 104-117.
43. Nair SM, Rahman RM, Clarkson AN, et al. Melatonin treatment following stroke induction modulates L-arginine metabolism. J Pineal Res 2011; 51: 313-323.
44. Chern CM, Liao JF, Wang YH, et al. Melatonin ameliorates neural function by promoting endogenous neurogenesis through the MT2 melatonin receptor in ischemic-stroke mice. Free Radic Biol Med 2012; 52: 1634-1647.
45. Sezabra ML, Bignotto M, Pinto LR Jr, et al. Randomized, double-blind clinical trial, controlled with placebo, of the toxicology of chronic melatonin treatment. J Pineal Res 2000; 29: 193-200.
46. Feng Z, Chang Y, Cheng Y, et al. Melatonin alleviates behavioral deficits associated with apoptosis and cholinergic system dysfunction in the APP 695 transgenic mouse model of Alzheimer's disease. J Pineal Res 2004; 37: 129-136. (Pubitemid 39120217)
47. Sommansson A, Nylander O, Sjoblom M,. Melatonin decreases duodenal epithelial paracellular permeability via a nicotinic receptor-dependent pathway in rats in vivo. J Pineal Res 2013; 54: 282-291.
48. Vile GF, Basu-Modak S, Waltner C, et al. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc Natl Acad Sci U S A 1994; 91: 2607-2610. (Pubitemid 24139396)
49. Gozzelino R, Jeney V, Soares MP,. Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 2010; 50: 323-354.
50. Poss KD, Tonegawa S,. Reduced stress defense in heme oxygenase 1-deficient cells. Proc Natl Acad Sci U S A 1997; 94: 10925-10930. (Pubitemid 27430837)