The effects of hypoxic preconditioning on white matter damage following hypoxic-ischaemic injury in the neonatal rat brain

International Journal of Developmental Neuroscience

Volumn 37, Issue , 2014, Pages 69-75

  Suryana, Eurwin ^a   Jones, Nicole M ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Hypoxia ischaemia; Hypoxic preconditioning; Myelination; Neonatal; Oligodendrocytes

Indexed keywords

MYELIN; MYELIN BASIC PROTEIN; OXYGEN; ANTIGEN; CHONDROITIN SULFATE PROTEOGLYCAN 4; O ANTIGEN; PROTEOGLYCAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HYPOXIA; BRAIN SIZE; BRAIN TISSUE; CAROTID ARTERY OBSTRUCTION; CELL DENSITY; CELL LINEAGE; CELL MATURATION; CONTROLLED STUDY; CORPUS CALLOSUM; FEMALE; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOHISTOCHEMISTRY; MALE; MYELINATION; NEUROPROTECTION; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SHAM PROCEDURE; STEM CELL; WHITE MATTER INJURY; ANIMAL; COMPLICATION; ISCHEMIC PRECONDITIONING; LEUKOENCEPHALOPATHIES; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS; CORPUS CALLOSUM; FEMALE; HYPOXIA, BRAIN; ISCHEMIC PRECONDITIONING; LEUKOENCEPHALOPATHIES; MYELIN BASIC PROTEIN; O ANTIGENS; OLIGODENDROGLIA; PROTEOGLYCANS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84904599704     PISSN: 07365748     EISSN: 1873474X     Source Type: Journal    
DOI: 10.1016/j.ijdevneu.2014.06.007     Document Type: Article

References (47)

1. Aktivitelerine A.E. Effects of hypoxic preconditioning in antioxidant enzyme activities in hypoxic-ischemic brain damage in immature rats. Turk. Neurosurg. 2008, 18:165-171.
2. Back S.A., Gan X., Li Y., Rosenberg P.A., Volpe J.J. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J. Neurosci. 1998, 18:6241-6253.
3. Back S.A., Han B.H., Luo N.L., Chricton C.A., Xanthoudakis S., Tam J., et al. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci. 2002, 22:455-463.
4. Back S.A., Luo N.L., Borenstein N.S., Levine J.M., Volpe J.J., Kinney H.C. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J. Neurosci. 2001, 21:1302-1312.
5. Back S.A., Luo N.L., Mallinson R.A., O'Malley J.P., Wallen L.D., Frei B., et al. Selective vulnerability of preterm white matter to oxidative damage defined by F2-isoprostanes. Ann. Neurol. 2005, 58:108-120.
6. Biran V., Joly L.M., Heron A., Vernet A., Vega C., Mariani J., et al. Glial activation in white matter following ischemia in the neonatal P7 rat brain. Exp. Neurol. 2006, 199:103-112.
7. Bradl M., Lassmann H. Oligodendrocytes: biology and pathology. Acta Neuropathol. 2010, 119:37-53.
8. Buser J.R., Maire J., Riddle A., Gong X., Nguyen T., Nelson K., et al. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 2012, 71:93-109.
9. Buser J.R., Segovia K.N., Dean J.M., Nelson K., Beardsley D., Gong X., et al. Timing of appearance of late oligodendrocyte progenitors coincides with enhanced susceptibility of preterm rabbit cerebral white matter to hypoxia-ischemia. J. Cereb. Blood Flow Metab. 2010, 30:1053-1065.
10. Carty M.L., Wixey J.A., Colditz P.B., Buller K.M. Post-insult minocycline treatment attenuates hypoxia-ischemia-induced neuroinflammation and white matter injury in the neonatal rat: a comparison of two different dose regimens. Int. J. Dev. Neurosci. 2008, 26:477-485.
11. Carty M.L., Wixet J.A., Reinebrant H.E., Gobe G., Colditz P.B., Buller K.M. Ibuprofen inhibits neuroinflammaion and attenuates white matter damage following hypoxia-ischemia in the immature rodent brain. Brain Res. 2011, 1402:9-19.
12. Cimarosti H., Jones N.M., O'Shea R.D., Pow D.V., Salbego C., Beart P.M. Hypoxic preconditioning in neonatal rat brain involves regulation of excitatory amino acid transporter 2 and estrogen receptor alpha. Neurosci. Lett. 2005, 385:52-57.
13. Connor J.R., Menzies S.L. Relationship of iron to oligodendrocytes and myelination. Glia 1996, 17:83-93.
14. Craig A., Ling Luo N., Beardsley D.J., Wingate-Pearse N., Walker D.W., Hohimer A.R., et al. Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. Exp. Neurol. 2003, 181:231-240.
15. Dawson M.R., Polito A., Levine J.M., Reynolds R. NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol. Cell. Neurosci. 2003, 24:476-488.
16. Deng W., Rosenberg P.A., Volpe J.J., Jensen F.E. Calcium-permeable AMPA/kainate receptors mediate toxicity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:6801-6806.
17. Dineen R.A., Vilisaar J., Hlinka J., Bradshaw C.M., Morgan P.S., Constantinescu C.S., et al. Disconnection as a mechanism for cognitive dysfunction in multiple sclerosis. Brain 2009, 132:239-249.
18. Folkerth R.D., Haynes R.L., Borenstein N.S., Belliveau R.A., Trachtenberg F., Rosenberg P.A., et al. Developmental lag in superoxide dismutases relative to other antioxidant enzymes in premyelinated human telencephalic white matter. J. Neuropathol. Exp. Neurol. 2004, 63:990-999.
19. French H.M., Reid M., Mamontov P., Simmons R.A., Grinspan J.B. Oxidative stress disrupts oligodendrocyte maturation. J. Neurosci. Res. 2009, 87:3076-3087.
20. Gidday J.M. Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 2006, 7:437-448.
21. Gidday J.M., Fitzgibbons J.C., Shah A.R., Park T. Neuroprotection from ischemic brain injury by hypoxic preconditioning in the neonatal rat. Neurosci. Lett. 1994, 168:221-224.
22. Huang Z., Liu J., Cheung P.Y., Chen C. Long-term cognitive impairment and myelination deficiency in a rat model of perinatal hypoxic-ischemic brain injury. Brain Res. 2009, 1301:100-109.
23. Jakovcevski I., Filipovic R., Mo Z., Rakic S., Zecevic N. Oligodendrocyte development and the onset of myelination in the human fetal brain. Front. Neuroanat. 2009, 3:1-15.
24. Jones N.M., Bergeron M. Hypoxia-induced ischemic tolerance in neonatal rat brain involves enhanced ERK1/2 signaling. J. Neurochem. 2004, 89:157-167.
25. Jones N.M., Bergeron M. Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J. Cereb. Blood Flow Metab. 2001, 21:1105-1114.
26. Jones N.M., Kardashyan L., Callaway J.K., Lee E.M., Beart P.M. Long-term functional and protective actions of preconditioning with hypoxia, cobalt chloride, and desferrioxamine against hypoxic-ischemic injury in neonatal rats. Pediatr. Res. 2008, 63:620-624.
27. Juurlink B.H., Thorburne S.K., Hertz L. Peroxide-scavenging deficit underlies oligodendrocyte susceptibility to oxidative stress. Glia 1998, 22:371-378.
28. Liu Y., Silverstein F.S., Skoff R., Barks J.D. Hypoxic-ischemic oligodendroglial injury in neonatal rat brain. Pediatr. Res. 2002, 51:25-33.
29. Lyons S.A., Kettenmann H. Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J. Cereb. Blood Flow Metab. 1998, 18:521-530.
30. Miki K., Ishibashi S., Sun L., Xu H., Ohashi W., Kuroiwa T., et al. Intensity of chronic cerebral hypoperfusion determines white/gray matter injury and cognitive/motor dysfunction in mice. J. Neurosci. Res. 2009, 87:1270-1281.
31. Miyamoto O., Auer R. Hypoxia, hyperoxia, ischemia, and brain necrosis. Neurology 2000, 54:362-371.
32. Nishiyama A., Lin X.H., Giese N., Heldin C.H., Stallcup W.B. Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J. Neurosci. Res. 1996, 43:299-314.
33. Patneau D.K., Wright P.W., Winters C., Mayer M.L., Gallo V. Glial cells of the oligodendrocyte lineage express both kainate- and AMPA-preferring subtypes of glutamate receptor. Neuron 1994, 12:357-371.
34. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2009, Elsevier, UK. Compact 6th edn.
35. Rice J., Vannucci R., Brierly J. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Annals of Neurology 1981, 9:131-141.
36. Rosenberg P.A., Dai W., Gan X.D., Ali S., Fu J., Back S.A., et al. Mature myelin basic protein-expressing oligodendrocytes are insensitive to kainate toxicity. J. Neurosci. Res. 2003, 71:237-245.
37. Scolding N., Franklin R., Stevens S., Heldin C.H., Compston A., Newcombe J. Oligodendrocyte progenitors are present in the normal adult human CNS and in the lesions of multiple sclerosis. Brain 1998, 121:2221-2228.
38. Segovia K.N., McClure M., Moravec M., Luo N.L., Wan Y., Gong X., et al. Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury. Ann. Neurol. 2008, 63:520-530.
39. Sizonenko S.V., Camm E.J., Dayer A., Kiss J.Z. Glial responses to neonatal hypoxic-ischemic injury in the rat cerebral cortex. Int. J. Dev. Neurosci. 2008, 26:37-45.
40. Sommer I., Schachner M. Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev. Biol. 1981, 83:311-327.
41. Talos D.M., Fishman R.E., Park H., Folkerth R.D., Follett P.L., Volpe J.J., et al. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. J. Comp. Neurol. 2006, 497:42-60.
42. Tanaka K., Nogawa S., Suzuki S., Dembo T., Kosakai A. Upregulation of oligodendrocyte progenitor cells associated with restoration of mature oligodendrocytes and myelination in peri-infarct area in the rat brain. Brain Res. 2003, 989:172-179.
43. Vannucci R.C., Towfighi J., Vannucci S.J. Hypoxic preconditioning and hypoxic-ischemic brain damage in the immature rat: pathologic and metabolic correlates. J. Neurochem. 1998, 71:1215-1220.
44. Vannucci S.J., Hagberg H. Hypoxia-ischemia in the immature brain. J. Exp. Biol. 2004, 208:3149-3154.
45. Volpe J.J., Kinney H.C., Jensen F.E., Rosenberg P.A. The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int. J. Dev. Neurosci. 2011, 29:423-440.
46. Yu S., Zhao T., Guo M., Fang H., Ma J., Ding A., et al. Hypoxic preconditioning up-regulates glucose transport activity and glucose transporter (GLUT1 and GLUT3) gene expression after acute anoxic exposure in the cultured rat hippocampal neurons and astrocytes. Brain Res. 2008, 1211:22-29.
47. Zeis T., Graumann U., Reynolds R., Schaeren-Wiemers N. Normal-appearing white matter in multiple sclerosis is in a subtle balance between inflammation and neuroprotection. Brain 2007, 131:288-303.