Melatonin as an antioxidant for stroke neuroprotection

Cell Transplantation

Volumn 25, Issue 5, 2016, Pages 883-891

  Watson, Nate ^a   Diamandis, Theo ^a   Gonzales Portillo, Chiara ^a   Reyes, Stephanny ^a   Borlongan, Cesar V ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Antioxidant; Dementia; Melatonin; Melatonin receptors; Neuroprotection; Pineal gland

Indexed keywords

EPIGALLOCATECHIN GALLATE; LAVENDER OIL; MELATONIN; MELATONIN RECEPTOR; NATURAL PRODUCT; ANTIOXIDANT; CATECHIN; NEUROPROTECTIVE AGENT;

ANTIOXIDANT ACTIVITY; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CHINESE MEDICINE; DEMENTIA; NEUROPROTECTION; NONHUMAN; PINEAL BODY; PRIORITY JOURNAL; REVIEW; STEM CELL TRANSPLANTATION; ANALOGS AND DERIVATIVES; ANIMAL; BIOLOGICAL THERAPY; CYTOLOGY; DRUG EFFECTS; HUMAN; METABOLISM; STEM CELL; STROKE; TRANSPLANTATION;

ANIMALS; ANTIOXIDANTS; CATECHIN; CELL- AND TISSUE-BASED THERAPY; HUMANS; MELATONIN; NEUROPROTECTION; NEUROPROTECTIVE AGENTS; PINEAL GLAND; RECEPTORS, MELATONIN; STEM CELL TRANSPLANTATION; STEM CELLS; STROKE;

EID: 84964273506     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368915X689749     Document Type: Review

References (78)

1. Albers, G. W.; Goldstein L. B.; Hess, D. C.; Wechsler, L. R.; Fuire, K. L.; Gorelick, P. B.; Hurn, P.; Liebskind, D. S.; Nogueira, R. G.; Saver, J. L. Stroke Treatment Academic Industry Roundtable (STAIR) recommendations for maximizing the use of intravenous thrombolytics and expanding treatment options with intra-arterial and neuroprotective therapies. Stroke 42:2645-2650; 2011
2. Axelrod, J.; Wurtman, R. J.; Snyder, S. H. Control of hydroxyindole-O-methyltransferase activity in the rat pineal gland by environmental light. J. Biol. Chem. 240:949-954; 1965
3. Bega, D.; Gonzalez-Latapi, P.; Zadikoff, C.; Simuni, T. A review of the clinical evidence for complementary and alternative therapies in Parkinson’s disease. Curr. Treat. Options Neurol. 16:314; 2014
4. Ben-Nathan, D.; Maestroni, G. J. M.; Conti, A. The protective effect of melatonin in viral and bacterial infections. In: Maestroni, G. J. M.; Conti, A.; Reiter, R. J., eds. Therapeutic potential of melatonin. Karger, Basel; 1997:72-80
5. Ben-Nathan, D.; Maestroni G. J. M.; Lustig, S.; Conti, S. Protective effects of melatonin in mice infected with encephalitis virus. Arch. Virol. 140:223-230; 1995
6. Beni, S. M.; Kohen, R.; Reiter, R. J.; Tan, D. X.; Shohami, E. Melatonin-induced neuroprotection after closed head injury is associated with increased brain antioxidants and attenuated late-phase activation of NF-kb and AP-1. FASEB J. 18:149-151; 2004
7. Borlongan, C. V.; Sanberg, P. R. Neural transplantation for treatment of Parkinson’s disease. Drug Discov. Today 7:674-682; 2002
8. Borlongan, C. V.; Sumaya, I.; Moss, D.; Kumazaki, M.; Sakurai, T.; Hida, H.; Nishino, H. Melatonin-secreting pineal gland: A novel tissue source for neural transplantation therapy in stroke. Cell Transplant. 12:225-234; 2003
9. Cagnoli, C. M.; Atabay, C.; Kharlamova, E.; Manev, H. Melatonin protects neurons from singlet oxygen-induced apoptosis. J. Pineal Res. 18:222-226; 1995
10. Carillo-Vico, A.; Guerrero, J. M.; Lardone, P. J; Reiter, R. J. A review of the multiple actions of melatonin on the immune system. Endocrine 27:189-200; 2005
11. Chacko, S. M.; Thambi, T. P.; Kuttan, R.; Nishigaki, I. Beneficial effects of green tea: A literature review. Chin. Med. 5:13; 2010
12. Chen, G.; Huo, Y.; Tan, D.-X.; Liang, Z.; Zhang, W.; Zhang, Y. Melatonin in Chinese medicinal herbs. Life Sci. 73:19-26; 2003
13. Chen, L.; Qiu, R.; Li, L.; He, D.; Lv, H.; Wu, X.; Gu, N. The role of exogenous neural stem cells transplantation in cerebral ischemic stroke. J. Biomed. Nanotechnol. 10:3219-3230; 2014
14. Chen, T. Y.; Lee, M. Y.; Chen, H. Y.; Kuo, Y. L.; Lin, S. C.; Wu, T. S.; Lee, E. J. Melatonin attenuates the postischemic increase in blood-brain barrier permeability and decreases hemorrhagic transformation of tissue-plasminogen activator therapy following ischemic stroke in mice. J. Pineal Res. 40:242-250; 2006
15. Cutler, R. G. Oxidative stress: Its potential relevance to human disease and longevity determinants. Age 18:91-96; 1995
16. Currier, N. L.; Sun, L. Z.; Miller, S. C. Exogenous melatonin: Quantitative enhancement in vivo of cells mediating nonspecific immunity. J. Neuroimmunol. 104:101-108; 2000
17. Cuzzocrea, S.; Costantino, G.; Caputi, A. P. Protective effect of melatonin on cellular energy depletion mediated by peroxynitrite and poly (ADP-ribose) synthetase activation in a non-septic shock model induced by zymosan in the rat. J. Pineal Res. 25:78-85; 1998
18. Ellis, L. C. Melatonin reduces mortality from Aleutian disease in mink (Mustela vison). J. Pineal Res. 21:214-217; 1996
19. Gasparova, Z.; Stara, V.; Stolc, S. Effect of antioxidants on functional recovery after in vitro-induced ischemia and long-term potentiation recorded in the pyramidal layer of the CA1 area of rat hippocampus. Gen. Physiol. Biophys. 33:43-52; 2014
20. Giordano, M.; Palermo, M. S. Melatonin-induced enhancement of antibody-dependent cellular cytotoxicity. J. Pineal Res. 10:117-121; 1991
21. Gumuslu, E.; Mutlu, O.; Sunnetci, D.; Ulak, G.; Celikyurt, I. K.; Cine, N.; Akar, F.; Savli, H.; Erden, F. The antidepressant agomelatine improves memory deterioration and upregulates CREB and BDNF gene expression levels in unpredictable chronic mild stress (UCMS)-exposed mice. Drug Target Insights 8:11-21; 2014
22. Gupta, Y. K.; Chaudhary, G.; Sinha, K. Enhanced protection by melatonin and meloxicam combination in a middle cerebral artery occlusion model of acute ischemic stroke in rat. Can. J. Physiol. Pharmacol. 80:210-217; 2002
23. Hardeland, R., Poeggeler, B., Srinivasan, V., Trakht, I.; Pandi-Perumal, S. R.; Cardinali, D. P. Melatonergic drugs in clinical practice. Arzneimittelforschung 58:1-10; 2008
24. Imbesi, M.; Uz, T.; Manev, H. Role of melatonin receptors in the effects of melatonin on BDNF and neuroprotection in mouse cerebellar neurons. J. Neural Transm. 115:1495-1499; 2008
25. Jeong, H. C.; Kim, M. S.; Lim, Y. J.; Ryu, C. H.; Jun, J. A.; Jeun, S. S. Mesenchymal stem cells expressing brainderived neurotrophic factor enhance endogenous neurogenesis in an ischemic stroke model. Biomed. Res. Int. 2014:129-145; 2014
26. Juranek, I.; Horakova, L.; Rackova, L.; Stefek, M. Antioxidants in treating pathologies involving oxidative damage: An update on medicinal chemistry and biological activity of stobadine and related pyridoindoles. Curr. Med. Chem. 17:552-570; 2010
27. Kahan, B. D.; Gholerial, R. Immunosuppressive agents. Surg. Clin. North Am. 74:1029-1054; 1994
28. Kalaria, R. N. Risk factors and neurodegenerative mechanisms in stroke related dementia. Panminerva Med. 54:139-148; 2012
29. Kaneko, N.; Kako, E.; Sawamoto, K. Enhancement of ventricular-subventricular zone-derived neurogenesis and oligodendrogenesis by erythropoietin and its derivatives. Front. Cell Neurosci. 7:235; 2013
30. Kaneko, Y.; Hayashi, T.; Yu, S.; Tajiri, N.; Solomita, M. A.; Chheda, S. H.; Weinbren, N. L.; Parolini, O.; Borlongan, C. V. Human amniotic epithelial cells express melatonin receptor MT1, but not melatonin receptor MT2: A new perspective to neuroprotection. J. Pineal Res. 50:272-280; 2011
31. Kilic, E.; Kilic, U.; Bacigaluppi, M.; Guo, A.; Abdallah, N. B.; Wolfer, D. P.; Reiter, R. J.; Hermann, D. M.; Bassetti, C. L. 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. 45:142-148; 2008
32. Kilic, E.; Ozdemir, Y. G.; Bolay, H.; Kelestimur, H.; Dalkara, T. Pinealectomy aggravates and melatonin administration attenuates brain damage in focal ischemia. J. Cereb. Blood Flow Metab. 19:511-516; 1999
33. Kondoh, T.; Uneyama, H.; Nishino, H.; Torii, K. Melatonin reduces cerebral edema formation caused by transient forebrain ischemia in rats. Life Sci. 72:583-590; 2002
34. Kondziolka, D.; Wechsler, L.; Goldstein, S.; Meltzer, C.; Thulborn, K. R.; Gebel, J.; Jannetta, P.; DeCesare, S.; Elder, E. M.; McGrogan, M.; Reitman, M. A.; Bynum, L. Transplantation of cultured human neuronal cells for patients with stroke. Neurology 55:565-569; 2000
35. Kong, X.; Li, X.; Cai, Z.; Yang, N.; Liu, Y.; Shu, J.; Pan, L.; Zuo, P. Melatonin regulates the viability and differentiation of rat midbrain neural stem cells. Cell Mol. Neurobiol. 28:569-579; 2008
36. Lee, C. H.; Yoo, K. Y.; Choi, J. H.; Park, O. K.; Hwang, I. K.; Kwon, Y. G.; Kim, Y. M.; Won, M. H. Melatonin’s protective action against ischemic neuronal damage is associated with up-regulation of the MT2 melatonin receptor. J. Neurosci. Res. 88:2630-2640; 2010
37. Lee, E. J.; Lee, M. Y.; Chen, H. Y.; Hsu, Y. S.; Wu, T. S.; Chen, S. T.; Chang, G. L. Melatonin attenuates gray and white matter damage in a mouse model of transient focal cerebral ischemia. J. Pineal Res. 38:42-52; 2005
38. Lee, J. M.; Zipfel, G. J.; Choi, D. W. The changing landscape of ischaemic brain injury mechanisms. Nature 399:A7-14; 1999
39. Lee, M. Y.; Kuan, Y. H.; Chen, H. Y.; Chen T. Y.; Chen, S. T.; Huang, C. C.; Yang, I. P.; Hsu, Y. S.; Wu, T. S.; Lee, E. J. Intravenous administration of melatonin reduces the intracerebral cellular inflammatory response following transient focal cerebral ischemia in rats. J. Pineal Res. 42:297-309; 2007
40. Lee, S.; Shin, J.; Hong, Y.; Lee, M.; Kim, K.; Lee, S. R.; Chang, K. T.; Hong, Y. Beneficial effects of melatonin on stroke-induced muscle atrophy in focal cerebral ischemic rats. Lab. Anim. Res. 28:47-54; 2012
41. Leker, R.; Teichner, A.; Lavie, G.; Shohami, E.; Lamensorf, I.; Ovadia, H. The nitroxide antioxidant tempol is cerebroprotective against focal cerebral ischemia in spontaneously hypertensive rats. Exp. Neurol. 176:355-363; 2002
42. Lekic, T.; Hartman, R.; Rojas, H.; Manaenko, A.; Chen, W.; Ayer, R.; Tang, J.; Zhang, J. H. Protective effect of melatonin upon neuropathology, striatal function, and memory ability after intracerebral hemorrhage in rats. J. Neurotrauma 27:627-637; 2010
43. Lin, H. W.; Lee, E. J. Effects of melatonin in experimental stroke models in acute, sub-acute, and chronic stages. Neuropsychiatr. Dis. Treat. 5:157-162; 2009
44. Luo, Z. G.; Zou, F. X.; Zhou, W. Q. The review of Chinese medicine on VD. Zhongguo Zhongyi Jichu Yixue Zazhi 7:76-77; 2001
45. Luscher, C.; Malenka, R. C.; Nicoll, R. A. Monitoring glutamate release during LTP with glial transporter currents. Neuron 21:435-441; 1998
46. Maestroni, G. J. The immunoendocrine role of melatonin. J. Pineal Res. 14:1-10; 1993
47. Manev, H.; Uz, T.; Kharlamov, A.; Joo, J. Y. Increased brain damage after stroke or excitotoxic seizures in melatonindeficient rats. FASEB J. 10:1546-1551; 1996
48. Mao, L. L.; Cheng, Q.; Guardiola-Lemaitre, B.; SchusterKlein, C.; Dong, C.; Lai, L.; Hill, S. M. In vitro and in vivo antitumor activity of melatonin receptor agonists. J. Pineal Res. 49:210-221; 2010
49. Melchiorri, D.; Reiter, R. J.; Sewerynek, E.; Chen, L. D.; Nistico, G. Melatonin reduces kainate-induced lipidperoxidation in homogenates of different brain-regions. FASEB J. 9:1205-1210; 1995
50. Mor, M.; Rivara, S.; Pala, D.; Bedini, A.; Spadoni, G.; Tarzia, G. Recent advances in the development of melatonin MT1 and MT2 receptor agonists. Expert Opin. Ther. Pat. 20:1059-1077; 2010
51. Moriya, T.; Horie, N.; Mitome, M.; Shinohara, K. Melatonin influences the proliferative and differentiative activity of neural stem cells. J. Pineal Res. 42:411-418; 2007
52. Nelson, P. T.; Kondziolka, D.; Wechsler, L.; Goldstein, S.; Gebel, J.; DeCesare, S.; Elder, E. M.; Zhang, P. J.; Jacobs, A.; McGrogan, M.; Lee, V. M.; Trojanowski, J. Q. Clonal human (hNT) neuron grafts for stroke therapy: Neuropathology in a patient 27 months after implantation. Am. J. Pathol. 160:1201-1206; 2002
53. Niles, L. P.; Armstrong, K. J.; Castro, L. M.; Dao, C. V.; Sharma, R.; McMillan, C. R.; Doering, L. C.; Kirkham, D. L. Neural stem cells express melatonin receptors and neurotrophic factors: Colocalization of the MT1 receptor with neuronal and glial markers. BMC Neurosci. 5:41; 2004
54. Pei, Z.; Pang, S. F.; Cheung, R. T. Pretreatment with melatonin reduces volume of cerebral infarction in a rat middle cerebral artery occlusion stroke model. J. Pineal Res. 32:168-172; 2002
55. Quin, X.; Liu, Y.; Wu, Y.; Wang, S.; Wang, D.; Zhu, J.; Ye, Q.; Mou, W.; Kang, L. A meta-analysis of Chinese herbal medicines for vascular dementia. Neural Regen. Res. 8: 1685-1692; 2013
56. Ramirez-Rodriguez, G.; Klempin, F.; Babu, H.; BenitezKing, G.; Kempermann, G. Melatonin modulates cell survival of new neurons in the hippocampus of adult mice. Neuropsychopharmacology 34:2180-2191; 2009
57. Redmond, D. E. Cellular replacement therapy for Parkinson’s disease-Where we are today? Neuroscientist 8:457-488; 2002
58. Reifler, A. N.; Chervenak, A. P.; Dolikian, M. E.; Benenati, B. A.; Meyers, B. S.; Demertzis, Z. D.; Lynch, A. M.; Li, B. Y.; Wachter, R. D.; Abufarha, F. S.; Dulka, E. A.; Pack, W.; Zhao, X.; Wong, K. Y. The rat retina has five types of ganglion-cell photoreceptors. Exp. Eye Res. 130:17-28; 2015
59. Reiter, R. J. Oxidative damage in the central nervous system: Protection by melatonin. Prog. Neurobiol. 56:359-384; 1998
60. Reiter, R. J.; Tan, D.; Fuentes-Broto, L. Melatonin: A multitasking molecule. Prog. Brain Res. 181:127-151; 2010
61. Romeu, L. R.; da Motta, E. L.; Maganhin, C. C.; Oshima, C. T.; Fonseca, M. C.; Barrueco, K. F.; Simoes, R. S.; Pellegrino, R.; Baracat, E. C.; Soares-Junior, J. M. Effects of melatonin on histomorphology and on the expression of steroid receptors, VEGF, and PCNA in ovaries of pinealectomized female rats. Fertil. Steril. 95:1379-1384; 2011
62. Sharma, R.; McMillan, C. R.; Niles, L. P. Neural stem cell transplantation and melatonin treatment in a 6-hydroxydopamine model of Parkinson’s disease. J. Pineal Res. 43:245-254; 2007
63. Shinozuka, K.; Staples, M.; Borlongan, C. V. Melatoninbased therapeutics for neuroprotection in stroke. Int. J. Mol. Sci. 14:8924-8947; 2013
64. Simpson, D.; Curran, M. P. Ramelteon-A review of its use in insomnia. Drugs 68:1901-1919; 2008
65. Skinner, D. C.; Malpaux, B. High melatonin concentrations in third ventricular cerebrospinal fluid are not due to galen vein blood recirculating through the choroid plexus. Endocrinology 140:4399-4405; 1999
66. Stem Cell Therapies as an Emerging Paradigm in Stroke Participants. Stem Cell Therapies as an Emerging Paradigm in Stroke (STEPS): Bridging basic and clinical science for cellular and neurogenic factor therapy in treating stroke. Stroke 40:510-515; 2009
67. Suzuki, A.; Fukushima, H.; Mukawa, T.; Toyoda, H.; Wu, L. J.; Zhao, M. G.; Xu, H.; Shang, Y.; Endoh, K.; Iwamoto, T.; Mamiya, N.; Okano, E.; Hasegawa, S.; Mercaldo, V.; Zhang, Y.; Maeda, R.; Ohta, M.; Josselyn, S. A.; Zhuo, M.; Kida, S. Upregulation of CREB-mediated transcription enhances both shortand long-term memory. J. Neurosci. 31:8786-8802; 2011
68. Suzuki, M.; Tabuchi, M.; Ikeda, M.; Tomita, T. Concurrent formation of peroxynitrite with the expression of inducible nitric oxide synthase in the brain during middle cerebral artery occlusion and reperfusion in rats. Brain Res. 951:113-120; 2002
69. Tan, D. X.; Manchester, L. C.; Reiter, R. J.; Qi, W.; Hanes, M. A.; Farley, N. J. High physiological levels of melatonin in the bile of mammals. Life Sci. 65:2523-2529; 1999
70. Tan, S.; Zhi, P. K.; Luo, Z. K.; Shi, J. Severe instead of mild hyperglycemia inhibits neurogenesis in the subventricular zone of adult rats after transient focal cerebral ischemia. Neuroscience 303:138-148; 2015
71. Vakili, A.; Sharifat, S.; Akhavan, M. M.; Bandegi, R. A. Effect of lavender oil (Lavandula angustifolia) on cerebral edema and its possible mechanisms in an experimental model of stroke. Brain Res. 1548:56-62; 2014
72. Wang, D.; Yuan, X.; Liu, T.; Liu, L.; Hu, Y.; Wang, Z.; Zheng, Q. Neuroprotective activity of lavender oil on transient focal cerebral ischemia in mice. Molecules 17:9803-9817; 2012
73. Wang, Y.; Lin, S. Z.; Chiou, A. L.; Williams, L. R.; Hoffer, B. J. Glial cell line-derived neurotrophic factor protects against ischemia-induced injury in the cerebral cortex. J. Neurosci. 17:4341-4348; 1997
74. Xu, S. C.; He, M. D.; Zhong, M.; Zhang, Y. W.; Wang, Y.; Yang, J.; Yu, Z. P.; Zhou, Z. Melatonin protects against Nickel-induced neurotoxicity in vitro by reducing oxidative stress and maintaining mitochondrial function. J. Pineal Res. 49:86-94; 2010
75. Yang, C. L.; Guo, H.; Zhou, H.; Suo, D. Q.; Li, W. J.; Zhou, Y.; Zhao, Y.; Yang, W. S.; Jin, X. Chronic oleoylethanolamide treatment improves spatial cognitive deficits through enhancing hippocampal neurogenesis after transient focal cerebral ischemia. Biochem. Pharmacol. 94:270-281; 2015
76. Yao, C.; Zhang, J.; Liu, G.; Chen, F.; Lin, Y. Neuroprotection by (−)-epigallocatechin-3-gallate in a rat model of stroke is mediated through inhibition of endoplasmic reticulum stress. Mol. Med. Rep. 9:69-72; 2014
77. Yu, H. S.; Yee, R. W.; Hawes, K. A.; Reiter, R. J. Diurnal rhythms of immunoreactive melatonin in the aqueous humor and serum of male pigmented rabbits. Neurosci. Lett. 116:309-314; 1990
78. Zhao, Y.; Xiao, M.; He, W.; Cai, Z. Minocycline upregulates cyclic AMP response element binding protein and brain-derived neurotrophic factor in the hippocampus of cerebral ischemia rats and improves behavioral deficits. Neuropsychiatr. Dis. Treat. 11:507-516; 2015.