Melatonin protects periventricular white matter from damage due to hypoxia

Journal of Pineal Research

Volumn 48, Issue 3, 2010, Pages 185-193

  Kaur, C ^a   Sivakumar, V ^a   Ling, E A ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Glutathione; Hypoxia; Lipid peroxidation; Melatonin; Neonatal brain; Periventricular white matter; Vascular permeability

Indexed keywords

GLUTATHIONE; MALONALDEHYDE; MELATONIN; NITRIC OXIDE; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD VESSEL PERMEABILITY; BRAIN DAMAGE; CELL VACUOLE; CHOROID PLEXUS; CONTROLLED STUDY; EPENDYMA CELL; HYPOXIA; MICROGLIA; NERVE CELL NECROSIS; NERVE FIBER DEGENERATION; NONHUMAN; OLIGODENDROGLIA; RAT; WHITE MATTER;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; ASTROCYTES; CELL LINE; CEREBRAL VENTRICLES; GLUTATHIONE; HYPOXIA, BRAIN; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; MALONDIALDEHYDE; MELATONIN; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NITRIC OXIDE; OLIGODENDROGLIA; RATS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77749336553     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2009.00740.x     Document Type: Article

References (58)

1. Takashima S, Armstrong DL, Becker LE. Subcortical leukomalacia. Relationship to development of the cerebral sulcus and its vascular supply. Arch Neurol 1978 35: 470 472.
2. Inder TE, Huppi PS, Warfield S et al. Periventricular white matter injury in the premature infant is followed by reduced cerebral cortical gray matter volume at term. Ann Neurol 1999 46: 755 760.
3. Volpe JJ. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 2001 50: 553 562.
4. Kaur C, Sivakumar V, Ang LS, Sundaresan A. Hypoxic damage to the periventricular white matter in neonatal brain: role of vascular endothelial growth factor, nitric oxide and excitotoxicity. J Neurochem 2006 98: 1200 1216.
5. Meister A, Anderson ME Glutathione. Annu Rev Biochem 1983 52: 711 760.
6. Mizui T, Kinouchi H, Chan PH. Depletion of brain glutathione by buthionine sulfoximine enhances cerebral ischemic injury in rats. Am J Physiol 1992 262: H313 H317.
7. Bobyn PJ, Franklin JL, Wall CM, Thornhill JA, Juurlink BH, Paterson PG. The effects of dietary sulfur amino acid deficiency on rat brain glutathione concentration and neural damage in global hemispheric hypoxia-ischemia. Nutr Neurosci 2002 5: 407 416.
8. Back SA, Gan X, Li Y, Rosenberg PA, Volpe JJ. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 1998 18: 6241 6253.
9. Back SA, Han BH, Luo NL et al. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 2002 22: 455 463.
10. Sivakumar V, Lu J, Ling EA, Kaur C. Vascular endothelial growth factor and nitric oxide production in response to hypoxia in the choroid plexus in neonatal brain. Brain Pathol 2008 18: 71 85.
11. Kondoh T, Uneyama H, Nishino H, Torii K. Melatonin reduces cerebral edema formation caused by transient forebrain ischemia in rats. Life Sci 2002 72: 583 590.
12. Kaur C, Sivakumar V, Zhang Y, Ling EA. Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia 2006 54: 826 839.
13. Kaur C, Ling EA. Antioxidants and neuroprotection in the adult and developing central nervous system. Curr Med Chem 2008 15: 3068 3080.
14. Pei Z, Cheung RT. Pretreatment with melatonin exerts anti-inflammatory effects against ischemia/reperfusion injury in a rat middle cerebral artery occlusion stroke model. J Pineal Res 2004 37: 85 91.
15. Lee MY, Kuan YH, Chen HY et al. Intravenous administration of melatonin reduces the intracerebral cellular inflammatory response following transient focal cerebral ischemia in rats. J Pineal Res 2007 42: 297 309.
16. Cuzzocrea S, Costantino G, Gitto E et al. Protective effects of melatonin in ischemic brain injury. J Pineal Res 2000 29: 217 227. (Pubitemid 30786397)
17. Erşahin M, Sehirli O, Toklu HZ et al. Melatonin improves cardiovascular function and ameliorates renal, cardiac and cerebral damage in rats with renovascular hypertension. J Pineal Res 2009 47: 97 106.
18. Caballero B, Vega-Naredo I, Sierra V et al. Melatonin alters cell death processes in response to age-related oxidative stress in the brain of senescence-accelerated mice. J Pineal Res 2009 46: 106 114.
19. Luchetti F, Betti M, Canonico B et al. ERK MAPK activation mediates the antiapoptotic signaling of melatonin in UVB-stressed U937 cells. Free Radic Biol Med 2009 46: 339 351.
20. Maity P, Bindu S, Dey S et al. Melatonin reduces indomethacin-induced gastric mucosal cell apoptosis by preventing mitochondrial oxidative stress and the activation of mitochondrial pathway of apoptosis. J Pineal Res 2009 46: 314 323.
21. Kaur C, Sivakumar V, Ling EA. Expression of tranferrin receptors in the pineal gland of postnatal and adult rats and its alteration in hypoxia and melatonin treatment. Glia 2007 55: 263 273.
22. Richter-Landsberg C, Heinrich M. OLN-93: a new permanent oligodendroglia cell line derived from primary rat brain glial cultures. J Neurosci Res 1996 45: 161 173.
23. Kaur C, Sivakumar V, Lu J, Ling EA. Melatonin attenuates hypoxia-induced ultrastructural changes and increased vascular permeability in the developing hippocampus. Brain Pathol 2008 18: 533 547.
24. Deng Y, Lu J, Sivakumar V, Ling EA, Kaur C. Amoeboid microglia in the periventricular white matter induces oligodendrocyte damage through expression of proinflammatory cytokines via MAP kinase signalling pathway in hypoxic neonatal rats. Brain Pathol 2008 18: 387 400.
25. Johnston MV. Hypoxic and ischemic disorders of infants and children. Lecture for 38th meeting of Japanese Society of Child Neurology, Tokyo, Japan, July 1996. Brain Dev 1997 19: 235 239.
26. Mcquillen PS, Ferriero DM. Selective vulnerability in the developing central nervous system. Pediatr Neurol 2004 30: 227 235.
27. Rezaie P, Dean A. Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system. Neuropathology 2002 22: 106 132.
28. Follett PL, Deng W, Dai W et al. Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci 2004 24: 4412 4420.
29. Folkerth RD. Periventricular leukomalacia: overview and recent findings. Pediatr Dev Pathol 2006 9: 3 13.
30. Dammann O, Hagberg H, Leviton A. Is periventricular leukomalacia an axonopathy as well as an oligopathy? Pediatr Res 2001 49: 453 457.
31. Ness JK, Romanko MJ, Rothstein RP, Wood TL, Levison SW. Perinatal hypoxia-ischemia induces apoptotic and excitotoxic death of periventricular white matter oligodendrocyte progenitors. Dev Neurosci 2001 23: 203 208.
32. Tan DX, Chen LD, Poeggler B, Manchester LC, Reiter RJ. Melatonin: a potent endogenous hydroxyl radical scavenger. Endocrine J 1993 1: 57 60.
33. 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.
34. Manda K, Ueno M, Anzai K. Space radiation-induced inhibition of neurogenesis in the hippocampal dentate gyrus and memory impairment in mice: ameliorative potential of the melatonin metabolite, AFMK. J Pineal Res 2008 45 : 430 438.
35. Reiter RJ, Tan DX, Manchester LC, Qi W. Biochemical reactivity of melatonin with reactive oxygen and nitrogen species: a review of the evidence. Cell Biochem Biophys 2001 34 : 237 256.
36. Reiter RJ, Paredes SD, Manchester LC, Tan DX. Reducing oxidative/nitrosative stress: a newly-discovered gene for melatonin. Crit Rev Biochem Mol Biol 2009 44 : 175 200.
37. Pablos MI, Agapito MT, Gutierrez R et al. Melatonin stimulates the activity of the detoxifying enzyme glutathione peroxidase in several tissues of chicks. J Pineal Res 1995 19 : 111 115.
38. Ozturk G, Coskun S, Erbas D, Hasanoglu E. The effect of melatonin on liver superoxide dismutase activity, serum nitrate and thyroid hormone levels. Jpn J Physiol 2000 50 : 149 153.
39. Rodriguez C, Mayo JC, Sainz RM et al. Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004 36 : 1 9.
40. Reiter RJ, Tan DX, Gitto E et al. Pharmacological utility of melatonin in reducing oxidative cellular and molecular damage. Pol J Pharmacol 2004 56 : 159 170.
41. Subramanian P, Mirunalini S, Pandi-Perumal SR, Trakht I, Cardinali DP. Melatonin treatment improves the antioxidant status and decreases lipid content in brain and liver of rats. Eur J Pharmacol 2007 571 : 116 119.
42. Fe particle irradiation. J Pineal Res 2008 44 : 189 196.
43. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991 11 : 81 128.
44. Lin S, Rhodes PG, Lei M, Zhang F, Cai Z. alpha-Phenyl-n-tert-butyl- nitrone attenuates hypoxic-ischemic white matter injury in the neonatal rat brain. Brain Res 2004 1007 : 132 141.
45. Mccracken E, Valeriani V, Simpson C, Jover T, McCulloch J, Dewar D. The lipid peroxidation by-product 4-hydroxynonenal is toxic to axons and oligodendrocytes. J Cereb Blood Flow Metab 2000 20 : 1529 1536.
46. Li J, Baud O, Vartanian T, Volpe JJ, Rosenberg PA. Peroxynitrite generated by inducible nitric oxide synthase and NADPH oxidase mediates microglial toxicity to oligodendrocytes. Proc Natl Acad Sci USA 2005 102 : 9936 9941.
47. JanaKy R, Cruz-Aguado R, Oja SS, Shaw CA. Glutathione in the nervous system: roles in neural function in health and implicationsfor neurological disease. In : Handbook of Neurochemistry and Molecular Neurolobiology, Oja SS, Schousboe A, Saransaari P, eds., 3rd edn, vol 6. Springer, New York, pp. 347 399.
48. Tan S, Sagara Y, Liu Y, Maher P, Schubert D. The regulation of reactive oxygen species production during programmed cell death. J Cell Biol 1998 141 : 1423 1432.
49. Oka A, Belliveau MJ, Rosenberg PA, Volpe JJ. Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J Neurosci 1993 13 : 1441 1453.
50. Yonezawa M, Back SA, Gan X, Rosenberg PA, Volpe JJ. Cystine deprivation induces oligodendroglial death: rescue by free radical scavengers and by a diffusible glial factor. J Neurochem 1996 67 : 566 573.
51. Sivakumar V, Ling EA, Lu J, Kaur C. Role of glutamate and its receptors and insulin-like growth factors in hypoxia induced periventricular white matter injury. Glia 2009 Doi :.
52. Mayo JC, Sainz RM, Antolin I, Herrera F, Martin V, Rodriguez C. Melatonin regulation of antioxidant enzyme gene expression. Cell Mol Life Sci 2002 59 : 1706 1713.
53. Ergenekon E, Gücüyener K, Erbas D, Aral S, Koç E, Atalay Y. Cerebrospinal fluid and serum vascular endothelial growth factor and nitric oxide levels in newborns with hypoxic ischemic encephalopathy. Brain Dev 2004 26 : 283 286.
54. Mayhan WG. VEGF increases permeability of the blood-brain barrier via a nitric oxide synthase/cGMP-dependent pathway. Am J Physiol 1999 76 : C1148 C1153.
55. Fukumura D, Gohongi T, Kadambi A et al. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci USA 2001 98 : 2604 2609.
56. Hoog N, Darley-Usmar VN, Wilson MT, Moncada S. Production of hydroxyl radicals from the simultaneous generation of superoxide and nitric oxide. Biochemistry 1992 281 : 419.
57. Radi R, Beckmann JS, Bush KM, Freeman BA. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 1991 266 : 4244 4250.
58. Reiter RJ, Garcia JJ, Pie J. Oxidative toxicity in models of neurodegeneration: responses to melatonin. Restor Neurol Neurosci 1998 12 : 135 142.