Hypoxia-inducible factor 1 protects hypoxic astrocytes against glutamate toxicity

ASN Neuro

Volumn 4, Issue 4, 2012, Pages 231-241

  Badawi, Yomna ^a   Ramamoorthy, Prabhu ^a   Shi, Honglian ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Brain ischaemia; Cell viability; Glutamate; Glutathione; Hypoxia inducible factor 1; Stroke

Indexed keywords

2 METHOXYESTRADIOL; BUTHIONINE SULFOXIMINE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; GLUTATHIONE; HYPOXIA INDUCIBLE FACTOR 1; LIFICIGUAT;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL HYPOXIA; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; EXCITOTOXICITY; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN STABILITY; RAT; UPREGULATION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELL HYPOXIA; CEREBRAL CORTEX; CYTOTOXICITY TESTS, IMMUNOLOGIC; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATORS; ESTRADIOL; EXCITATORY AMINO ACIDS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; GLUTATHIONE; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INDAZOLES; L-LACTATE DEHYDROGENASE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84862699673     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1042/AN20120006     Document Type: Article

References (56)

1. Baird NA, Turnbull DW, Johnson EA (2006) Induction of the heat shock pathway during hypoxia requires regulation of heat shock factor by hypoxia-inducible factor-1. J Biol Chem 281:38675-38681.
2. Baranova O, Miranda LF, Pichiule P, Dragatsis I, Johnson RS, Chavez JC (2007) Neuron-specific inactivation of the hypoxia inducible factor 1 increases brain injury in a mouse model of transient focal cerebral ischemia. J Neurosci 27:6320.
3. Batti L, Taylor C, O'Connor J (2010) Hydroxylase inhibition reduces synaptic transmission and protects against a glutamate-induced ischemia in the CA1 region of the rat hippocampus. Neuroscience 167:1014-1024.
4. Bjorklund O, Shang M, Tonazzini I, Dare E, Fredholm BB (2008) Adenosine A1 and A3 receptors protect astrocytes from hypoxic damage. Eur J Pharmacol 596:6-13.
5. Bolanos JP, Heales SJ, Land JM, Clark JB (1995) Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurons and astrocytes in primary culture. J Neurochem 64:1965-1972.
6. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA (1995) Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92:7162.
7. Brennan AM, Suh SW, Won SJ, Narasimhan P, Kauppinen TM, Lee H, Edling Y, Chan PH, Swanson RA (2009) NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat Neurosci 12:857-863.
8. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100.
9. Chatterjee S, Noack H, Possel H, Keilhoff G, Wolf G (1999) Glutathione levels in primary glial cultures: monochlorobimane provides evidence of cell type-specific distribution. Glia 27:152-161.
10. Chen CJ, Liao SL, Kuo JS (2000) Gliotoxic action of glutamate on cultured astrocytes. J Neurochem 75:1557-1565.
11. Chen Y, Swanson RA (2003) Astrocytes and brain injury. J Cereb Blood Flow Metab 23:137-149.
12. Chu PWY, Beart PM, Jones NM (2010) Preconditioning protects against oxidative injury involving hypoxia-inducible factor-1 and vascular endothelial growth factor in cultured astrocytes. Eur J Pharmacol 633:24-32.
13. Diaz Z, Assaraf MI, Miller WH Jr, Schipper HM (2005) Astroglial cytoprotection by erythropoietin pre conditioning: implications for ischemic and degenerative CNS disorders. J Neurochem 93:392-402.
14. Eltzschig HK, Abdulla P, Hoffman E, Hamilton KE, Daniels D, Schonfeld C, Loffler M, Reyes G, Duszenko M, Karhausen J, Robinson A, Westerman KA, Coe IR, Colgan SP (2005) HIF-1-dependent repression of equilibrative nucleoside transporter (ENT) in hypoxia. J Exp Med 202:1493-1505.
15. Gabryel B, Malecki A (2006) Ebselen attenuates oxidative stress in ischemic astrocytes depleted of glutathione. Comparison with glutathione precursors. Pharmacol Rep 58:381-392.
16. Giffard RG, Swanson RA (2005) Ischemia-induced programmed cell death in astrocytes. Glia 50:299-306.
17. Guo S, Bragina O, Xu Y, Cao Z, Chen H, Zhou B, Morgan M, Lin Y, Jiang BH, Liu KJ (2008) Glucose upregulates HIF-1a expression in primary cortical neurons in response to hypoxia through maintaining cellular redox status. J Neurochem 105:1849-1860.
18. Haddad JJE, Land SC (2000) O2-evoked regulation of HIF-1a and NF-kB in perinatal lung epithelium requires glutathione biosynthesis. Am J Physiol Lung Cell Mol Physiol 278:L492-L503.
19. Haddad JJE, Olver RE, Land SC (2000) Antioxidant/pro-oxidant equilibrium regulates HIF-1 and NF-kB redox sensitivity. J Biol Chem 275:21130.
20. Haralick RM, Shanmugam K, Dinstein I (1973) Textural features for image classification. IEEE Trans Syst Man Cyber 3:610-621.
21. Heurteaux C, Lauritzen I, Widmann C, Lazdunski M (1995) Essential role of adenosine, adenosine A1 receptors, and ATP-sensitive K+ channels in cerebral ischemic preconditioning. Proc Natl Acad Sci USA 92:4666-4670.
22. Im JY, Paik SG, Han PL (2006) Cadmium-induced astroglial death proceeds via glutathione depletion. J Neurosci Res 83:301-308.
23. Jin KL, Mao XO, Nagayama T, Goldsmith PC, Greenberg DA (2000) Induction of vascular endothelial growth factor receptors and phosphatidylinositol 39-kinase/Akt signaling by global cerebral ischemia in the rat. Neuroscience 100:713-717.
24. Jin W, Kong Z, Shen Z, Jin Y, Zhang W, Chen G (2011) Regulation of hypoxia inducible factor-1a expression by the alteration of redox status in HepG2 cells. J Exp Clin Cancer Res 30:61.
25. Lehmann C, Bette S, Engele J (2009) High extracellular glutamate modulates expression of glutamate transporters and glutamine synthetase in cultured astrocytes. Brain Res 1297:1-8.
26. Li SH, Shin DH, Chun YS, Lee MK, Kim MS, Park JW. 2008. A novel mode of action of YC-1 in HIF inhibition: stimulation of FIH-dependent p300 dissociation from HIF-1. Mol Cancer Ther 7:3729.
27. Lin JH, Lou N, Kang N, Takano T, Hu F, Han X, Xu Q, Lovatt D, Torres A, Willecke K, Yang J, Kang J, Nedergaard M (2008) A central role of connexin 43 in hypoxic preconditioning. J Neurosci 28:681-695.
28. Liu J, Narasimhan P, Song YS, Nishi T, Yu F, Lee YS, Chan PH (2006) Epo protects SOD2 deficient mouse astrocytes from damage by oxidative stress. Glia 53:360-365.
29. Liu Q, Berchner-Pfannschmidt U, Moller U, Brecht M, Wotzlaw C, Acker H, Jungermann K, Kietzmann T (2004) A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc Natl Acad Sci USA 101:4302.
30. Lukaszevicz AC, Sampaio N, Guegan C, Benchoua A, Couriaud C, Chevalier E, Sola B, Lacombe P, Onteniente B (2002) High sensitivity of protoplasmic cortical astroglia to focal ischemia. J Cereb Blood Flow Metab 22:289-298.
31. Mabjeesh NJ, Escuin D, LaVallee TM, Pribluda VS, Swartz GM, Johnson MS, Willard MT, Zhong H, Simons JW, Giannakakou P (2003) 2ME2 inhibits tumor growth and angiogenesis by disrupting microtubules and dysregulating HIF. Cancer Cell 3:363-375.
32. Makar TK, Nedergaard M, Preuss A, Gelbard AS, Perumal AS, Cooper AJL (1994) Vitamin E, ascorbate, glutathione, glutathicne disulfide, and enzymes of glutathione metabolism in cultures of chick astrocytes and neurons: evidence that astrocytes play an important role in antioxidative processes in the brain. J Neurochem 62:45-53.
33. Mani N, Khaibullina A, Krum JM, Rosenstein JM (2005) Astrocyte growth effects of vascular endothelial growth factor (VEGF) application to perinatal neocortical explants: receptor mediation and signal transduction pathways. Exp Neurol 192:394-406.
34. Martin LJ, Brambrink AM, Lehmann C, Portera-Cailliau C, Koehler R, Rothstein J, Traystman RJ (1997) Hypoxia-ischemia causes abnormalities in glutamate transporters and death of astroglia and neurons in newborn striatum. Ann Neurol 42:335-348.
35. Masuda S, Okano M, Yamagishi K, Nagao M, Ueda M, Sasaki R (1994) A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes. J Biol Chem 269:19488.
36. Monopoli A, Lozza G, Forlani A, Mattavelli A, Ongini E (1998) Blockade of adenosine A2A receptors by SCH 58261 results in neuroprotective effects in cerebral ischemia in rats. Neuroreport 9:3955.
37. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63.
38. Noda T, Iwakirir R, Fujimoto K, Aw TY (2001) Induction of mild intracellular redox imbalance inhibits proliferation of CaCo-2 cells. FASEB J 15:2131-2139.
39. Phelps CH (1972) Barbiturate-induced glycogen accumulation in brain: an electron microscopic study. Brain Res 39:225-234.
40. Schubert D, Soucek T, Blouw B (2009) The induction of HIF-1 reduces astrocyte activation by amyloid beta peptide. Eur J Neurosci 29:1323.
41. Semenza GL, Agani F, Booth G, Forsythe J, Iyer N, Jiang BH, Leung S, Roe R, Wiener C, Yu A (1997) Structural and functional analysis of hypoxiainducible factor 1. Kidney Int 51:553-555.
42. Shin CY, Jang ES, Choi JW, Ryu JR, Kim WK, Kim HC, Choi CR, Ko KH (2002) Adenosine and purine nucleosides protect rat primary astrocytes from peroxynitrite-potentiated, glucose deprivation-induced death: preservation of intracellular ATP level. Exp Neurol 176:175-182.
43. Shrivastava K, Shukla D, Bansal A, Sairam M, Banerjee P, Ilavazhagan G (2008) Neuroprotective effect of cobalt chloride on hypobaric hypoxiainduced oxidative stress. Neurochem Int 52:368-375.
44. Siddiq A, Aminova LR, Ratan RR (2007) Hypoxia inducible factor prolyl 4-hydroxylase enzymes: center stage in the battle against hypoxia, metabolic compromise and oxidative stress. Neurochem Res 32:931-946.
45. Silver IA, Deas J, Erecińska M (1997) Ion homeostasis in brain cells: differences in intracellular ion responses to energy limitation between cultured neurons and glial cells. J Neurosci 78:589-602.
46. Sinor AD, Irvin SM, Cobbs CS, Chen J, Graham SH, Greenberg DA (1998) Hypoxic induction of vascular endothelial growth factor (VEGF) protein in astroglial cultures. Brain Res 812:289-291.
47. Sommani P, Yamashita K, Miyoshi T, Tsunemine H, Kodaki T, Mori H, Hirota K, Arai T, Sasada M, Makino K (2007) Inhibitory effect of 6-formylpterin on HIF-1a protein accumulation. Biol Pharm Bull 30:2181-2184.
48. Swanson RA, Choi DW (1993) Glial glycogen stores affect neuronal survival during glucose deprivation in vitro. J Cereb Blood Flow Metab 13:162-169.
49. Synnestvedt K, Furuta GT, Comerford KM, Louis N, Karhausen J, Eltzschig HK, Hansen KR, Thompson LF, Colgan SP (2002) Ecto-59-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J Clin Invest 110:993-1002.
50. Tajima M, Kurashima Y, Sugiyama K, Ogura T, Sakagami H (2009) The redox state of glutathione regulates the hypoxic induction of HIF-1. Eur J Pharmacol 606:45-49.
51. Takano T, Oberheim N, Cotrina ML, Nedergaard M (2009) Astrocytes and ischemic injury. Stroke 40(3 Suppl),:S8-S12.
52. Vangeison G, Rempe DA (2009) The Janus-faced effects of hypoxia on astrocyte function. Neuroscientist 15:579.
53. Wardas J (2002) Neuroprotective role of adenosine in the CNS. Polish J Pharmacol 54:313-326.
54. Wellman TL, Jenkins J, Penar PL, Tranmer B, Zahr R, Lounsbury KM (2004) Nitric oxide and reactive oxygen species exert opposing effects on the stability of hypoxia-inducible factor-1a (HIF-1a) in explants of human pial arteries. FASEB J 18:379-381.
55. Wick A, Wick W, Waltenberger J, Weller M, Dichgans J, Schulz JB (2002) Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J Neurosci 22:6401-6407.
56. Yu ACH, Wong HK, Yung HW, Lau LT (2001) Ischemia-induced apoptosis in primary cultures of astrocytes. Glia 35:121-130.