Hypoxic damage to the periventricular white matter in neonatal brain: Role of vascular endothelial growth factor, nitric oxide and excitotoxicity

Journal of Neurochemistry

Volumn 98, Issue 4, 2006, Pages 1200-1216

  Kaur, Charanjit ^a   Sivakumar, Viswanathan ^a   Ang, Lin Stella ^a   Sundaresan, Alamelu ^b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b TEXAS SOUTHERN UNIVERSITY   (United States)

Author keywords

Excitotoxicity; Hypoxia; Neonatal brain; Nitric oxide; Periventricular white matter damage; Vascular endothelial growth factor

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN DAMAGE; BRAIN HYPOXIA; BRAIN LEVEL; CELLULAR DISTRIBUTION; COLORIMETRY; CONTROLLED STUDY; CORPUS CALLOSUM; ELECTRON MICROSCOPY; ENZYME ACTIVATION; ENZYME IMMUNOASSAY; EXCITOTOXICITY; EXPOSURE; IMMUNOHISTOCHEMISTRY; MICROGLIA; NERVE FIBER; NERVE FIBER DEGENERATION; NEWBORN; NEWBORN HYPOXIA; NONHUMAN; PERIVENTRICULAR WHITE MATTER DAMAGE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA ANALYSIS; UPREGULATION; WESTERN BLOTTING; WHITE MATTER;

ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN; COLORIMETRY; CORPUS CALLOSUM; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLIAL FIBRILLARY ACIDIC PROTEIN; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-ISCHEMIA, BRAIN; IMMUNOENZYME TECHNIQUES; IMMUNOHISTOCHEMISTRY; LATERAL VENTRICLES; MICROSCOPY, ELECTRON; MYELIN BASIC PROTEINS; MYELIN SHEATH; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

RATTUS NORVEGICUS;

EID: 33746388438     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03964.x     Document Type: Article

References (51)

1. Back S. A. and Rivkees S. A. (2004) Emerging concepts in periventricular white matter injury. Semin. Perinatol. 28, 405-414.
2. Ballabh P., Braun A. and Nedergaard M. (2004) Anatomic analysis of blood vessels in germinal matrix, cerebral cortex, and white matter in developing infants. Pediatr. Res. 56, 117-124.
3. Baud O., Daire J. L., Dalmaz Y., Fontaine R. H., Krueger R. C., Sebag G., Evrard P., Gressens P. and Verney C. (2004) Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol. 14, 1-10.
4. Bolanos J. P. and Almeida A. (1999) Roles of nitric oxide in brain hypoxia-ischemia. Biochim. Biophys. Acta 1411, 415-436.
5. Bradford M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
6. Croll S. D., Goodman J. H. and Scharfman H. E. (2004) Vascular endothelial growth factor (VEGF) in seizures: a double-edged sword. Adv. Exp. Med. Biol. 548, 57-68.
7. Dammann O., Hagberg H. and Leviton A. (2001) Is periventricular leukomalacia an axonopathy as well as an oligopathy? Pediatr. Res. 49, 453-457.
8. Farkas E., Donka G., de Vos R. A., Mihaly A., Bari F. and Luiten P. G. (2004) Experimental cerebral hypoperfusion induces white matter injury and microglial activation in the rat brain. Acta Neuropathol. 108, 57-64.
9. Follett P. L., Deng W., Dai W., Talos D. M., Massillon L. J., Rosenberg P. A., Volpe J. J. and Jensen F. E. (2004) Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J. Neurosci. 24, 4412-4420.
10. Grimm C., Wenzel A., Groszer M., Mayser H., Seeliger M., Samardzija M., Bauer C., Gassmann M. and Reme C. E. (2002) HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat. Med. 8, 718-724.
11. Hagberg H., Peebles D. and Mallard C. (2002) Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment. Retard. Dev. Disabil. Res. Rev. 8, 30-38.
12. Haynes R. L., Baud O., Li J., Kinney H. C., Volpe J. J. and Folkerth D. R. (2005) Oxidative and nitrative injury in periventricular leukomalacia: a review. Brain Pathol. 15, 225-233.
13. Iadecola C., Zhang F. and Xu X. (1995) Inhibition of inducible nitric oxide synthase ameliorate cerebral ischemic damage. Am. J. Physiol. 268, R286-R292.
14. Iwata O., Iwata S., Tamura M., Nakamura T., Hirabayashi S., Fueki N., Kondou Y., Hizume E. and Kihara H. (2004) Periventricular low intensities on fluid attenuated inversion recovery imaging in the newborn infant: relationships to the clinical data and long-term outcome. Pediatr. Int. 46, 150-157.
15. Iyer N. V., Kotch L. E., Agani F. et al. (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 12, 149-162.
16. Janigro D., West G. A., Nguyen T. S. and Winn H. R. (1994) Regulation of blood-brain barrier endothelial cells by nitric oxide. Circ. Res. 75, 528-538.
17. Johnston M. V. (2001) Excitotoxicity in neonatal hypoxia. Ment. Retard. Dev. Disabil. Res. Rev. 1, 229-234.
18. Kaur C. and You Y. (2000) Ultrastructure and function of the amoeboid microglial cells in the periventricular white matter in postnatal rat brain following a hypoxic exposure. Neurosci. Lett. 290, 17-20.
19. Kaur C., Hao A. J., Wu C. H. and Ling E. A. (2001) Origin of microglia. Microsc. Res. Tech. 54, 2-9.
20. Kirn W. K. and Ko K. H. (1998) Potentiation of N-methyl-D-aspartate- mediated neurotoxicity by immunostimulated murine microglia. J. Neurosci. Res. 54, 17-26.
21. Kimura R., Nakase H., Tamaki R. and Sakaki T. (2005) Vascular endothelial growth factor antagonist reduces brain edema formation and venous infarction. Stroke 36, 1259-1263.
22. Leviton A. and Gilles F. H. (1984) Acquired perinatal leukoencephalopathy. Ann. Neurol. 16, 1-8.
23. Ling E. A., Kaur C., Yick T. Y. and Wong W. C. (1990) Immunocytochemical localization of CR3 complement receptors with OX-42 in amoeboid microglia in postnatal rats. Anat. Embryol. 182, 481-486.
24. Livak K. J. and Schmittgen T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T) Method. Methods 24, 402-408.
25. Mayhan W. G. (1999) VEGF increases permeability of the blood-brain barrier via a nitric oxide synthase/cGMP-dependent pathway. Am. J. Physiol 276, C1148-C1153.
26. Meng S. Z., Arai Y., Deguchi K. and Takashima S. (1997) Early detection of axonal and neuronal lesions in prenatal-onset periventricular leukomalacia. Brain Dev. 19, 480-484.
27. Merrill J. E., Ignarro L. J., Sherman M. P., Melinek J. and Lane T. E. (1993) Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151, 2132-2141.
28. Min J. K., Lee Y. M., Kim J. H., Kim Y. M., Kim S. W., Lee S. Y., Gho Y. S., Oh G. T. and Kwon Y. G. (2005) Hepatocyte growth factor suppresses vascular endothelial growth factor-induced expression of endothelial ICAM-1 and VCAM-1 by inhibiting the nuclear 1 factor-kappaB pathway. Circ. Res. 96, 300-307.
29. Morimoto K., Murasugi T. and Oda T. (2002) Acute Neuroinflammation Exacerbates Excitotoxicity in Rat Hippocampus in Vivo. Exp. Neurol. 177, 95-104.
30. Nosarti C., Rushe T. M., Woodruff P. W., Stewart A. L., Rifkin L. and Murray R. M. (2004) Corpus callosum size and very preterm birth: relationship to neuropsychological outcome. Brain 127, 2080-2089.
31. Ohyu J., Marumo G., Ozawa H. et al. (1999) Early axonal and glial pathology in fetal sheep brains with leukomalacia induced by repeated umbilical cord occlusion. Brain Dev. 21, 248-252.
32. Piani D., Spranger M., Frei K., Schaffner A. and Fontana A., (1992) Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur. J. Immunol. 22, 2429-2436.
33. Saunders N. R., Habgood M. D. and Dziegielewska K. M. (1999) Barrier mechanisms in the brain, II. Immature brain. Clin. Exp. Pharmacol. Physiol. 26, 85-91.
34. Schoch H. J., Fischer S. and Marti H. H. (2002) Hypoxia-induced vascular endothelial growth factor expression causes vascular leakage in the brain. Brain 125, 2549-2557.
35. Semenza G. L. (1998) Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr. Opin. Genet. Dev. 8, 588-594.
36. Semenza G. L. (2000) Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem. Pharmacol. 59, 47-53.
37. Semenza G. L. (2004) Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19, 176-182.
38. Senger D. R., Galli S. J., Dvorak A. M., Pernizzi C. A., Harvey V. S. and Dvorak H. F. (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219, 983-985.
39. Sheldon R. A., Chuai J. and Ferriero D. M. (1996) A rat model for hypoxic-ischemic brain damage in very premature infants. Biol. Neonate. 69, 327-341.
40. Shuxin Li and Stys P. K. (2000) Mechanisms of Ionotropic Glutamate Receptor-Mediated Excitotoxicity in Isolated Spinal Cord White Matter. J. Neorusci. 20, 1190-1198.
41. Skoff R. P., Bessert D. A., Barks J. D., Song D., Cerghet M. and Silverstein F. S. (2001) Hypoxic-ischemic injury results in acute disruption of myelin gene expression and death of oligodendroglial precursors in neonatal mice. Int. J. Dev. Neurosci. 19, 197-208.
42. Sondell M., Lundborg G. and Kanje M. (1999) Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J. Neurosci. 19, 5731-5540.
43. Svedin P., Kjellmer I., Welin A. K., Blad S. and Mallard C. (2005) Maturational effects of lipopolysaccharide on white-matter injury in fetal sheep. J. Child Neurol. 20, 960-967.
44. Tahraoui S. L., Marret S., Bodenant C., Leroux P., Dommergues M. A., Evrard P. and Gressens P. (2001) Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol. 11, 56-71.
45. Thiel V. E. and Audus K. L. (2001) Nitric oxide and blood-brain barrier integrity. Antiox. Redox Signal. 3, 273-278.
46. Tsuji M., Saul J. P., du Plessis A., Eichenwald E., Sobh J., Crocker R. and Volpe J. J. (2000) Cerebral intravascular oxygenation correlates with mean arterial pressure in critically ill premature infants. Pediatrics 106, 625-632.
47. Vannucci R. C. and Vannucci S. J. (2005) Perinatal hypoxic-ischemic brain damage: evolution of an animal model. Dev. Neurosci. 27, 81-86.
48. Vannucci R. C., Lyons D. T. and Vasta F. (1988) Regional cerebral blood flow during hypoxia-ischemia in immature rats. Stroke 19, 245-250.
49. Volpe J. J. (2001) Neurobiology of periventricular leukomalacia in the premature infant. Pediatr. Res. 50, 553-562.
50. You Y. and Kaur C. (2000) Expression of induced nitric oxide synthase in amoeboid microglia in postnatal rats following an exposure to hypoxia. Neurosci. Lett. 279, 101-104.
51. Young P. P., Fantz C. R. and Sands M. S. (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.