Melatonin attenuates hypoxia-induced ultrastructural changes and increased vascular permeability in the developing hippocampus

Brain Pathology

Volumn 18, Issue 4, 2008, Pages 533-547

  Kaur, Charanjit ^a   Sivakumar, Viswanathan ^a   Lu, Jia ^b   Tang, Feng Ru ^c   Ling, Eng Ang ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b DSO NATIONAL LABORATORIES   (Singapore)

^c NATIONAL NEUROSCIENCE INSTITUTE   (Singapore)

Author keywords

Developing hippocampus; Hypoxia; Nitric oxide; Vascular endothelial growth factor; Vascular leakage

Indexed keywords

COMPLEMENTARY DNA; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HORSERADISH PEROXIDASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN G; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOTHIOCYANIC ACID DERIVATIVE; MELATONIN; MESSENGER RNA; MONOCLONAL ANTIBODY; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; POLYCLONAL ANTIBODY; RHODAMINE; VASCULOTROPIN;

ANALYTICAL EQUIPMENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BRAIN DAMAGE; BRAIN DEVELOPMENT; CELL ULTRASTRUCTURE; COLORIMETRY; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; ENZYME IMMUNOASSAY; HIPPOCAMPUS; HYPOXIA; IMMUNOHISTOCHEMISTRY; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ANTIOXIDANTS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN EDEMA; DENDRITES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HIPPOCAMPUS; HORSERADISH PEROXIDASE; HYPOXIA, BRAIN; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MELATONIN; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROPROTECTIVE AGENTS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; RATS; RATS, WISTAR; RHODAMINES; TREATMENT OUTCOME; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 51249118951     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2008.00156.x     Document Type: Article

References (43)

1. Almli CR, Levy TJ, Han BH, Shah AR, Gidday JM, Holtzman DM (2000) BDNF protects against spatial memory deficits following neonatal hypoxia-ischemia. Exp Neurol 166 : 99 114.
2. Balduini W, De Angelis V, Mazzoni E, Cimino M (2000) Long-lasting behavioral alterations following a hypoxic/ischemic brain injury in neonatal rats. Brain Res 859 : 318 325.
3. Bates DO, Harper SJ (2002) Regulation of vascular permeability by vascular endothelial growth factors. Vascul Pharmacol 39 : 225 237.
4. Battegay EJ (1995) Angiogenesis: mechanistic insights, neovascular diseases, and therapeutic prospects. J Mol Med 73 : 333 346.
5. Bergamasco B, Benna P, Ferrero P, Gavinelli R (1984) Neonatal hypoxia and epileptic risk: a clinical prospective study. Epilepsia 25 : 131 136.
6. Black SM, Bedolli MA, Martinez S, Bristow JD, Ferriero DM, Soifer SJ (1995) Expression of neuronal nitric oxide synthase corresponds to regions of selective vulnerability to hypoxia-ischaemia in the developing rat brain. Neurobiol Dis 2 : 145 155.
7. Bolanos JP, Almeida A (1999) Roles of nitric oxide in brain hypoxia-ischemia. Biochim Biophys Acta 1411 : 415 436.
8. Breier G, Albrecht U, Sterrer S, Risau W (1992) Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114 : 521 532.
9. Brown GC, Bolaños JP, Heales SJ, Clark JB (1995) Nitric oxide produced by activated astrocytes rapidly and reversibly inhibits cellular respiration. Neurosci Lett 193 : 201 214.
10. Colbourne F, Sutherland GR, Auer RN (1999) Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J Neurosci 19 : 4200 4210.
11. Connolly DT (1991) Vascular permeability factor: a unique regulator of blood vessel function. J Cell Biochem 47 : 219 223.
12. Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun CO, et al (2001) Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci USA 98 : 2604 2609.
13. Iadecola C, Zhang F, Casey R, Nagayama M, Ross ME (1997) Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 17 : 9157 9164.
14. Janigro D, West GA, Nguyen TS, Winn HR (1994) Regulation of blood-brain barrier endothelial cells by nitric oxide. Circ Res 75 : 528 538.
15. Jensen FE, Wang C, Stafstrom CE, Liu Z, Geary C, Stevens MC (1998) Acute and chronic increases in excitability in rat hippocampal slices after perinatal hypoxia in vivo. J Neurophysiol 79 : 73 81.
16. Kaur C, Sivakumar V, Singh G, Singh J, Ling EA (2005) Response of Purkinje neurons to hypobaric hypoxic exposure as shown by alteration in expression of glutamate receptors, nitric oxide synthases and calcium binding proteins. Neuroscience 135 : 1217 1229.
17. Kaur C, Sivakumar V, Zhang Y, Ling EA (2006) Hypoxia-induced astrocytic reaction and increased vascular permeability in the rat cerebellum. Glia 54 : 826 839.
18. Kaur C, Sivakumar V, Ang LS, Sunderasan L (2006) Hypoxic damage to the periventricular white matter in neonatal brain: role of vascular endothelial growth factor, nitric oxide and excitotoxicity. J Neurochem 98 : 1200 1216.
19. Kroll J, Waltenberger J (1998) VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR). Biochem Biophys Res Commun 252 : 743 746.
20. Levick JR, Smaje LH (1987) An analysis of the permeability of a fenestra. Microvasc Res 33 : 233 256.
21. Lissoni P, Rovelli F, Malugani F, Bucovec R, Conti A, Maestroni GJ (2001) Anti-angiogenic activity of melatonin in advanced cancer patients. Neuro Endocrinol Lett 22 : 45 47.
22. Livak KJ, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 24 : 402 408.
23. Lu J, Kaur C, Ling EA (1993) Uptake of tracer by the epiplexus cells via the choroid plexus epithelium following an intravenous or intraperitoneal injection of horseradish peroxidase in rats. J Anat 183 : 609 617.
24. Marinos RS, Zhang W, Wu G, Kelly KA, Meininger CJ (2001) Tetrahydrobiopterin levels regulate endothelial cell proliferation. Am J Physiol Heart Circ Physiol 281 : H482 H489.
25. Matsuoka Y, Kitamura Y, Fukunaga R, Shimohama S, Nabeshima T, Tooyama I, et al (1997) In vivo hypoxia-induced neuronal damage in dentate gyrus of rat hippocampus: changes in NMDA receptors and the effect of MK-801. Neurochem Int 30 : 533 542.
26. Mayhan WG (1999) VEGF increases permeability of the blood-brain barrier via a nitric oxide synthase/cGMP-dependent pathway. Am J Physiol 276 : C1148 1153.
27. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L (1995) A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 182 : 1683 1693.
28. Milkiewicz M, Ispanovic E, Doyle JL, Haas TL (2006) Regulators of angiogenesis and strategies for their therapeutic manipulation. Int J Biochem Cell Biol 38 : 333 357.
29. Mishra OP, Mishra R, Ashraf QM, Delivoria-Papadopoulos M (2006) Nitric oxide-mediated mechanism of neuronal nitric oxide synthase and inducible nitric oxide synthase expression during hypoxia in the cerebral cortex of newborn piglets. Neuroscience 140 : 857 863.
30. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z (1999) Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13 : 9 22.
31. Nyakas C, Buwalda B, Luiten PG (1996) Hypoxia and brain development. Prog Neurobiol 49 : 1 51.
32. Owens J Jr., Robbins CA, Wenzel HJ, Schwartzkroin PA (1997) Acute and chronic effects of hypoxia on the developing hippocampus. Ann Neurol 41 : 187 199.
33. Raman L, Tkac I, Ennis K, Georgieff MK, Gruetter R, Rao R (2005) In vivo effect of chronic hypoxia on the neurochemical profile of the developing rat hippocampus. Brain Res Dev Brain Res 156 : 202 209.
34. Reiter RJ (1997) Antioxidant actions of melatonin. Adv Pharmacol 38 : 103 117.
35. Roberts WG, Palade GE (1995) Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci 108 : 2369 2379.
36. Schoch HJ, Fischer S, Marti HH (2002) Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 125 : 2549 2557.
37. Semenza GL (1998) Hypoxia-inducible factor 1: master regulator of O2homeostasis. Curr Opin Genet Dev 8 : 588 594.
38. Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219 : 983 985.
39. Shweiki D, Itin A, Soffer D, Keshet E (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359 : 843 845.
40. Tutunculer F, Eskiocak S, Basaran UN, Ekuklu G, Ayvaz S, Vatansever U (2005) The protective role of melatonin in experimental hypoxic brain damage. Pediatr Int 47 : 434 439.
41. Wei G, Dawson VL, Zweier JL (1999) Role of neuronal and endothelial nitric oxide synthase in nitric oxide generation in the brain following cerebral ischemia. Biochim Biophys Acta 1455 : 23 34.
42. Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wiegand SJ, Holash J (2000) Vascular-specific growth factors and blood vessel formation. Nature 407 : 242 248.
43. Young PP, Fantz CR, Sands MS (2004) VEGF disrupts the neonatal blood brain barrier and increases life span after non-ablative BMT in a murine model of congenital neurodegeneration caused by a lysosomal enzyme deficiency. Exp Neurol 188 : 104 114.