Melatonin prevents cell death and mitochondrial dysfunction via a SIRT1-dependent mechanism during ischemic-stroke in mice

Journal of Pineal Research

Volumn 58, Issue 1, 2015, Pages 61-70

  Yang, Yang ^a,b   Jiang, Shuai ^a   Dong, Yushu ^c,d   Fan, Chongxi ^e   Zhao, Lei ^a   Yang, Xiangmin ^a   Li, Juan ^a   Di, Shouyin ^e   Yue, Liang ^a   Liang, Guobiao ^c   Reiter, Russel J ^f   Qu, Yan ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c GENERAL HOSPITAL OF NORTHERN THEATER COMMAND   (China)

^d The 463 Hospital of Chinese PLA   (China)

^e FOURTH MILITARY MEDICAL UNIVERSITY   (China)

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

Author keywords

cerebral protection; ischemia reperfusion; melatonin; mitochondrial dysfunction; SIRT1 signaling

Indexed keywords

CYTOCHROME C; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MELATONIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P53; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SELISISTAT; SIRTUIN 1; 6-CHLORO-2,3,4,9-TETRAHYDRO-1H-CARBAZOLE-1-CARBOXAMIDE; ANTIOXIDANTS; CARBAZOLES; SIRT1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN EDEMA; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN PROTECTION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NEUROLOGICAL SCORE; NONHUMAN; REPERFUSION INJURY; SCORING SYSTEM; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMALS; ANTAGONISTS AND INHIBITORS; CELL DEATH; DRUG EFFECTS; METABOLISM; MICE; MITOCHONDRIA; PATHOLOGY; RATS; STROKE;

ANIMALS; ANTIOXIDANTS; BRAIN ISCHEMIA; CARBAZOLES; CELL DEATH; MALE; MELATONIN; MICE; MITOCHONDRIA; RATS; SIGNAL TRANSDUCTION; SIRTUIN 1; STROKE;

EID: 84919621569     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/jpi.12193     Document Type: Article

References (57)

1. 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.
2. Hankey GJ,. Anticoagulant therapy for patients with ischaemic stroke. Nat Rev Neurol 2012; 8: 319-328.
3. Blanco M, Castillo J,. Stroke in 2012: major advances in the treatment of stroke. Nat Rev Neurol 2013; 9: 68-70.
4. Mattiasson G, Shamloo M, Gido G, et al. Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat Med 2003; 9: 1062-1068.
5. Reiter RJ, Tan DX, Manchester LC, et al. Melatonin defeats neurally-derived free radicals and reduces the associated neuromorphological and neurobehavioral damage. J Physiol Pharmacol 2007; 58 (Suppl. 6): 5-22.
6. Thompson JW, Narayanan SV, Koronowski KB, et al. Signaling pathways leading to ischemic mitochondrial neuroprotection. J Bioenerg Biomembr 2014; [Epub ahead of print].
7. Duan W, Yang Y, Yan J, et al. The effects of curcumin post-treatment against myocardial ischemia and reperfusion by activation of the JAK2/STAT3 signaling pathway. Basic Res Cardiol 2012; 107: 263.
8. Xie R, Wang P, Ji X, et al. Ischemic post-conditioning facilitates brain recovery after stroke by promoting Akt/mTOR activity in nude rats. J Neurochem 2013; 127: 723-732.
9. Hasseldam H, Hansen-Schwartz J, Munkholm N, et al. Remote post-conditioning reduces hypoxic damage early after experimental stroke. Neurol Res 2013; 35: 336-343.
10. Kilic U, Kilic E, Reiter RJ, et al. Signal transduction pathways involved in melatonin-induced neuroprotection after focal cerebral ischemia in mice. J Pineal Res 2005; 38: 67-71.
11. Kilic U, Yilmaz B, Reiter RJ, et al. Effects of memantine and melatonin on signal transduction pathways vascular leakage and brain injury after focal cerebral ischemia in mice. Neuroscience 2013; 237: 268-276.
12. Yang Y, Sun Y, Yi W, et al. A review of melatonin as a suitable antioxidant against myocardial ischemia-reperfusion injury and clinical heart diseases. J Pineal Res 2014; 57: 357-366.
13. 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.
14. Agil A, Reiter RJ, Jimenez-Aranda A, et al. Melatonin ameliorates low-grade inflammation and oxidative stress in young Zucker diabetic fatty rats. J Pineal Res 2013; 54: 381-388.
15. Garcia JJ, Lopez-Pingarron L, Almeida-Souza P, et al. Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: a review. J Pineal Res 2014; 56: 225-237.
16. Zhang HM, Zhang Y,. Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. J Pineal Res 2014; 57: 131-146.
17. Hung MW, Tipoe GL, Poon AM, et al. Protective effect of melatonin against hippocampal injury of rats with intermittent hypoxia. J Pineal Res 2008; 44: 214-221.
18. Coto-Montes A, Boga JA, Rosales-Corral S, et al. Role of melatonin in the regulation of autophagy and mitophagy: a review. Mol Cell Endocrinol 2012; 361: 12-23.
19. 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.
20. Rosales-Corral SA, Acuna-Castroviejo D, Coto-Montes A, et al. Alzheimer's disease: pathological mechanisms and the beneficial role of melatonin. J Pineal Res 2012; 52: 167-202.
21. Mayo JC, Sainz RM, Tan DX, et al. Melatonin and Parkinson's disease. Endocrine 2005; 27: 169-178.
22. Song TY, Lin HC, Chen CL, et al. Ergothioneine and melatonin attenuate oxidative stress and protect against learning and memory deficits in C57BL/6J mice treated with d -galactose. Free Radic Res 2014; 48: 1049-1060.
23. de Berardis D, Marini S, Fornaro M, et al. The melatonergic system in mood and anxiety disorders and the role of agomelatine: implications for clinical practice. Int J Mol Sci 2013; 14: 12458-12483.
24. He P, Ouyang X, Zhou S, et al. A novel melatonin agonist Neu-P11 facilitates memory performance and improves cognitive impairment in a rat model of Alzheimer' disease. Horm Behav 2013; 64: 1-7.
25. Cazzola R, Rondanelli M, Faliva M, et al. Effects of DHA-phospholipids, melatonin and tryptophan supplementation on erythrocyte membrane physico-chemical properties in elderly patients suffering from mild cognitive impairment. Exp Gerontol 2012; 47: 974-978.
26. Reiter RJ, Tan DX, Paredes SD, et al. Beneficial effects of melatonin in cardiovascular disease. Ann Med 2010; 42: 276-285.
27. 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.
28. Parada E, Buendia I, Leon R, et al. Neuroprotective effect of melatonin against ischemia is partially mediated by alpha-7 nicotinic receptor modulation and HO-1 overexpression. J Pineal Res 2014; 56: 204-212.
29. 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.
30. Alonso-Alconada D, Alvarez A, Arteaga O, et al. Neuroprotective effect of melatonin: a novel therapy against perinatal hypoxia-ischemia. Int J Mol Sci 2013; 14: 9379-9395.
31. Yang Y, Duan W, Li Y, et al. Novel role of silent information regulator 1 in myocardial ischemia. Circulation 2013; 128: 2232-2240.
32. Yang Y, Duan W, Li Y, et al. New role of silent information regulator 1 in cerebral ischemia. Neurobiol Aging 2013; 34: 2879-2888.
33. Herskovits AZ, Guarente L,. SIRT1 in neurodevelopment and brain senescence. Neuron 2014; 81: 471-483.
34. Thompson JW, Dave KR, Saul I, et al. Epsilon PKC increases brain mitochondrial SIRT1 protein levels via heat shock protein 90 following ischemic preconditioning in rats. PLoS One 2013; 8: e75753.
35. Chen HZ, Guo S, Li ZZ, et al. A critical role for interferon regulatory factor 9 in cerebral ischemic stroke. J Neurosci 2014; 34: 11897-11912.
36. Wang LM, Wang YJ, Cui M, et al. A dietary polyphenol resveratrol acts to provide neuroprotection in recurrent stroke models by regulating AMPK and SIRT1 signaling, thereby reducing energy requirements during ischemia. Eur J Neurosci 2013; 37: 1669-1681.
37. Hernandez-Jimenez M, Hurtado O, Cuartero MI, et al. Silent information regulator 1 protects the brain against cerebral ischemic damage. Stroke 2013; 44: 2333-2337.
38. Carloni S, Albertini MC, Galluzzi L, et al. Melatonin reduces endoplasmic reticulum stress and preserves sirtuin 1 expression in neuronal cells of newborn rats after hypoxia-ischemia. J Pineal Res 2014; 57: 192-199.
39. Kilic E, Kilic U, Bacigaluppi M, et al. Delayed melatonin administration promotes neuronal survival, neurogenesis and motor recovery, and attenuates hyperactivity and anxiety after mild focal cerebral ischemia in mice. J Pineal Res 2008; 45: 142-148.
40. Kilic U, Yilmaz B, Ugur M, et al. Evidence that membrane-bound G protein-coupled melatonin receptors MT1 and MT2 are not involved in the neuroprotective effects of melatonin in focal cerebral ischemia. J Pineal Res 2012; 52: 228-235.
41. 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.
42. Swanson RA, Morton MT, Tsao-Wu G, et al. A semiautomated method for measuring brain infarct volume. J Cereb Blood Flow Metab 1990; 10: 290-293.
43. Lin TN, He YY, Wu G, et al. Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 1993; 24: 117-121.
44. Guo Z, Cao G, Yang H, et al. A combination of four active compounds alleviates cerebral ischemia-reperfusion injury in correlation with inhibition of autophagy and modulation of AMPK/mTOR and JNK pathways. J Neurosci Res 2014; 92: 1295-1306.
45. Cui Y, Zhang H, Ji M, et al. Hydrogen-rich saline attenuates neuronal ischemia-reperfusion injury by protecting mitochondrial function in rats. J Surg Res 2014; [Epub ahead of print].
46. Ye R, Kong X, Yang Q, et al. Ginsenoside Rd attenuates redox imbalance and improves stroke outcome after focal cerebral ischemia in aged mice. Neuropharmacology 2011; 61: 815-824.
47. Gaur V, Aggarwal A, Kumar A,. Protective effect of naringin against ischemic reperfusion cerebral injury: possible neurobehavioral, biochemical and cellular alterations in rat brain. Eur J Pharmacol 2009; 616: 147-154.
48. Reiter RJ, Cabrera J, Sainz RM, et al. Melatonin as a pharmacological agent against neuronal loss in experimental models of Huntington's disease, Alzheimer's disease and Parkinsonism. Ann N Y Acad Sci 1999; 890: 471-485.
49. Reiter RJ, Paredes SD, Manchester LC, et al. Reducing oxidative/nitrosative stress: a newly-discovered genre for melatonin. Crit Rev Biochem Mol Biol 2009; 44: 175-200.
50. Morris KC, Lin HW, Thompson JW, et al. Pathways for ischemic cytoprotection: role of sirtuins in caloric restriction, resveratrol, and ischemic preconditioning. J Cereb Blood Flow Metab 2011; 31: 1003-1019.
51. Yang Y, Duan W, Lin Y, et al. SIRT1 activation by curcumin pretreatment attenuates mitochondrial oxidative damage induced by myocardial ischemia reperfusion injury. Free Radic Biol Med 2013; 65: 667-679.
52. Khan RS, Dine K, Das Sarma J, et al. SIRT1 activating compounds reduce oxidative stress mediated neuronal loss in viral induced CNS demyelinating disease. Acta Neuropathol Commun 2014; 2: 3.
53. Khader A, Yang WL, Kuncewitch M, et al. Sirtuin 1 activation stimulates mitochondrial biogenesis and attenuates renal injury after ischemia-reperfusion. Transplantation 2014; 98: 148-156.
54. Govender J, Loos B, Marais E, et al. Mitochondrial catastrophe during doxorubicin-induced cardiotoxicity: a review of the protective role of melatonin. J Pineal Res 2014; 57: 367-380.
55. Galley HF, Lowes DA, Allen L, et al. Melatonin as a potential therapy for sepsis: a phase I dose escalation study and an ex vivo whole blood model under conditions of sepsis. J Pineal Res 2014; 56: 427-438.
56. Patki G, Lau YS,. Melatonin protects against neurobehavioral and mitochondrial deficits in a chronic mouse model of Parkinson's disease. Pharmacol Biochem Behav 2011; 99: 704-711.
57. Garcia-Macia M, Vega-Naredo I, De Gonzalo-Calvo D, et al. Melatonin induces neural SOD2 expression independent of the NF-kappaB pathway and improves the mitochondrial population and function in old mice. J Pineal Res 2011; 50: 54-63.