HIF-1α-deficient mice have increased brain injury after neonatal hypoxia-ischemia

Developmental Neuroscience

Volumn 31, Issue 5, 2009, Pages 452-458

  Sheldon, R Ann ^a   Osredkar, Damjan ^a   Lee, Christina L ^a   Jiang, Xiangning ^a   Mu, Dezhi ^a,b   Ferriero, Donna M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SICHUAN UNIVERSITY   (China)

Author keywords

Brain injury; Hypoxia inducible factor 1 ; Neonatal hypoxia ischemia; Transcription factor

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CRE RECOMBINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN HYPOXIA; BRAIN ISCHEMIA; CONTROLLED STUDY; GENE DELETION; GENE INACTIVATION; HISTOLOGY; IMMUNOFLUORESCENCE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANOXIA; BLOTTING, WESTERN; CEREBRAL CORTEX; CYTOPROTECTION; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-ISCHEMIA, BRAIN; MALE; MICE; MICE, TRANSGENIC; NEURONS; STATISTICS, NONPARAMETRIC; UP-REGULATION;

EID: 68349101972     PISSN: 03785866     EISSN: None     Source Type: Journal    
DOI: 10.1159/000232563     Document Type: Article

References (38)

1. Bernaudin M, Tang Y, Reilly M, Petit E, Sharp FR: Brain genomic response following hypoxia and re-oxygenation in the neonatal rat. Identification of genes that might contribute to hypoxia-induced ischemic tolerance. J Biol Chem 2002; 277: 39728-39738.
2. Ran R, Xu H, Lu A, Bernaudin M, Sharp FR: Hypoxia preconditioning in the brain. Dev Neurosci 2005; 27: 87-92.
3. Weidemann A, Johnson RS: Biology of HIF-1-alpha. Cell Death Differ 2008; 15: 621-627.
4. Semenza GL: HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000; 88: 1474-1480.
5. Jones NM, Bergeron M: Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J Cereb Blood Flow Metab 2001; 21: 1105-1114.
6. Jones NM, Lee EM, Brown TG, Jarrott B, Beart PM: Hypoxic preconditioning produces differential expression of hypoxia-inducible factor-1-alpha (HIF-1-alpha) and its regulatory enzyme HIF prolyl hydroxylase 2 in neonatal rat brain. Neurosci Lett 2006; 404: 72-77.
7. Bergeron M, Gidday JM, Yu AY, Semenza GL, Ferriero DM, Sharp FR: Role of hypoxia-inducible factor-1 (HIF-1) in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann Neurol 2000; 48: 285-296.
8. Hayashi T, Abe K, Suzuki H, Itoyama Y: Rapid induction of vascular endothelial growth factor gene expression after transient middle cerebral artery occlusion in rats. Stroke 1997; 28: 2039-2044.
9. Mu D, Chang YS, Vexler ZS, Ferriero DM: Hypoxia-inducible factor 1 alpha and Erythropoietin upregulation with deferoxamine salvage after neonatal stroke. Exp Neurol 2005; 195: 407-415.
10. Bergeron M, Yu AY, Solway KE, Semenza GL, Sharp FR: Induction of hypoxia-inducible factor-1 (HIF-1) and its target genes following focal ischaemia in rat brain. Eur J Neurosci 1999; 11: 4159-4170.
11. Kumral A, Uysal N, Tugyan K, Sonmez A, Yilmaz O, Gokmen N, Kiray M, Genc S, Du-man N, Koroglu TF, Ozkan H, Genc K: Erythropoietin improves long-term spatial memory deficits and brain injury following neonatal hypoxia-ischemia in rats. Behav Brain Res 2004; 153: 77-86.
12. Matsushita H, Johnston MV, Lange MS, Wilson MA: Protective effect of erythropoietin in neonatal hypoxic ischemia in mice. Neuroreport 2003; 14: 1757-1761.
13. Chang YS, Mu D, Wendland M, Sheldon RA, Vexler ZS, McQuillen PS, Ferriero DM: Erythropoietin improves functional and histological outcome in neonatal stroke. Pe-diatr Res 2005; 58: 106-111.
14. Gonzalez FF, McQuillen P, Mu D, Chang Y, Wendland M, Vexler Z, Ferriero DM: Erythropoietin enhances long-term neuroprotection and neurogenesis in neonatal stroke. Dev Neurosci 2007; 29: 321-330.
15. Semenza GL: Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr Opin Genet Dev 1998; 8: 588-594.
16. Sharp FR, Bernaudin M: HIF-1 and oxygen sensing in the brain. Nat Rev Neurosci 2004; 5: 437-448.
17. Chang S, Jiang X, Zhao C, Lee C, Ferriero DM: Exogenous low dose hydrogen peroxide increases hypoxia-inducible factor-1-alpha protein expression and induces preconditioning protection against ischemia in primary cortical neurons. Neurosci Lett 2008; 441: 134-138.
18. Mu D, Jiang X, Sheldon RA, Fox CK, Ham-rick SE, Vexler ZS, Ferriero DM: Regulation of hypoxia-inducible factor 1-alpha and induction of vascular endothelial growth factor in a rat neonatal stroke model. Neurobiol Dis 2003; 14: 524-534.
19. Hamrick SEG, McQuillen PS, Madan A, Fer-riero DM: Mechanisms of desferoxamine neuroprotection: a role for HIF-1-alpha. Pediatr Res 2003; 53: 25A.
20. Baranova O, Miranda LF, Pichiule P, Dragatsis I, Johnson RS, Chavez JC: Neuron-specific inactivation of the hypoxia inducible factor 1 alpha increases brain injury in a mouse model of transient focal cerebral ischemia. J Neurosci 2007; 27: 6320-6332.
21. Helton R, Cui J, Scheel JR, Ellison JA, Ames C, Gibson C, Blouw B, Ouyang L, Dragatsis I, Zeitlin S, Johnson RS, Lipton SA, Barlowe C: Brain-specific knock-out of hypoxia-inducible factor-1-alpha reduces rather than increases hypoxic-ischemic damage. J Neurosci 2005; 25: 4099-4107.
22. Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, Johnson RS: Hypoxia-inducible factor-1-alpha is a positive factor in solid tumor growth. Cancer Res 2000; 60: 4010-4015.
23. Dragatsis I, Zeitlin S: CaMKII-alpha-Cre transgene expression and recombination patterns in the mouse brain. Genesis 2000; 26: 133-135.
24. Rice JE 3rd, Vannucci RC, Brierley JB: The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 1981; 9: 131-141.
25. Ditelberg JS, Sheldon RA, Epstein CJ, Ferriero DM: Brain injury after perinatal hypoxia-ischemia is exacerbated in copper/zinc su-peroxide dismutase transgenic mice. Pediatr Res 1996; 39: 204-208.
26. Sheldon RA, Sedik C, Ferriero DM: Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res 1998; 810: 114-122.
27. Ferriero DM: Neonatal brain injury. N Engl J Med 2004; 351: 1985-1995.
28. McQuillen PS, Ferriero DM: Selective vulnerability in the developing central nervous system. Ped Neurol 2004; 30: 227-235.
29. Roitbak T, Li L, Cunningham LA: Neural stem/progenitor cells promote endothelial cell morphogenesis and protect endothelial cells against ischemia via HIF-1-alpha-regulated VEGF signaling. J Cereb Blood Flow Metab 2008; 28: 1530-1542.
30. Feng Y, Rhodes PG, Bhatt AJ: Neuroprotective effects of vascular endothelial growth factor following hypoxic-ischemic brain injury in neonatal rats. Pediatr Res 2008;64: 370-374.
31. Zhao T, Zhang CP, Liu ZH, Wu LY, Huang X, Wu HT, Xiong L, Wang X, Wang XM, Zhu LL, Fan M: Hypoxia-driven proliferation of embryonic neural stem/progenitor cells - Role of hypoxia-inducible transcription factor-1-alpha. FEBS J 2008; 275: 1824-1834.
32. Tomita S, Ueno M, Sakamoto M, Kitahama Y, Ueki M, Maekawa N, Sakamoto H, Gassmann M, Kageyama R, Ueda N, Gonzalez FJ, Takahama Y: Defective brain development in mice lacking the HIF-1-alpha gene in neural cells. Mol Cell Biol 2003; 23: 6739-6749.
33. Chen W, Jadhav V, Tang J, Zhang JH: HIF-1-alpha inhibition ameliorates neonatal brain injury in a rat pup hypoxic-ischemic model. Neurobiol Dis 2008; 31: 433-1431
34. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nico-tera P: Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995; 15: 961-973.
35. Portera-Cailliau C, Price DL, Martin LJ: Ex-citotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 1997; 378: 70-87.
36. Petralia RS, Sans N, Wang YX, Wenthold RJ: Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 2005; 29: 436-452.
37. Mojsilovic-Petrovic J, Callaghan D, Cui H, Dean C, Stanimirovic DB, Zhang W: Hypoxia-inducible factor-1 (HIF-1) is involved in the regulation of hypoxia-stimulated expression of monocyte chemoattractant protein-1 (MCP-1/CCL2) and MCP-5 (CCL12) in as-trocytes. J Neuroinflammation 2007; 4: 12.
38. Vangeison G, Carr D, Federoff HJ, Rempe DA: The good, the bad, and the cell type-specific roles of hypoxia inducible factor-1 alpha in neurons and astrocytes. J Neurosci 2008; 28: 1988-1993.