Identification of Potential Stroke Targets by Lentiviral Vector Mediated Overexpression of HIF-1α and HIF-2α in a Primary Neuronal Model of Hypoxia

Journal of Cerebral Blood Flow and Metabolism

Volumn 24, Issue 2, 2004, Pages 245-258

  Ralph, G S ^a   Parham, S ^a   Lee, S R ^a   Beard, G L ^a   Craigon, M H ^a   Ward, N ^a   White, J R ^a   Barber, R D ^a   Rayner, W ^a   Kingsman, S M ^a   Mundy, C R ^a   Mazarakis, N D ^a   Krige, D ^a  

^a OXFORD BIOMEDICA UK LTD   (United Kingdom)

Author keywords

HIF; Hypoxia; Lentiviral vectors; Stroke therapeutics

Indexed keywords

LENTIVIRUS VECTOR; VIRUS VECTOR;

ANIMAL CELL; ARTICLE; BRAIN HYPOXIA; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EXPRESSED SEQUENCE TAG; GENE; GENE EXPRESSION; GENE IDENTIFICATION; GENE INDUCTION; GENE OVEREXPRESSION; HIF2A GENE; HIFA GENE; HYPOXIA; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STROKE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE;

EID: 10744226140     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.WCB.0000110532.48786.46     Document Type: Article

References (90)

1. An S, Zheng Y, Bleu T (2000) Sphingosine 1-phosphate-induced cell proliferation, survival, and related signaling events mediated by G protein-coupled receptors Edg3 and Edg5. J Biol Chem 275: 288-296
2. Azzouz M, Martin-Rendon E, Barber RD, Mitrophanous KA, Carter EE, Rohll JB, Kingsman SM, Kingsman AJ, Mazarakis ND (2002) Multicistronic lentiviral vector-mediated striatal gene transfer of aromatic L-amino acid decarboxylase tyrosine hydroxylase and GTP cyclohydrolase 1 induces sustained transgene expression dopamine production and functional improvement in a rat model of Parkinson's disease. J Neurosci 22:10302-10312
3. Bates S, Read SJ, Harrison DC, Topp S, Morrow R, Gale D, Murdock P, Barone FC, Parsons AA, Gloger IS (2001) Characterization of gene expression changes following permanent MCAO in the rat using subtractive hybridization. Brain Res Mol Brain Res 93:70-80
4. Bernaudin M, Nedelec AS, Divoux D, MacKenzie ET, Petit E, Schumann-Bard P (2002a) Normobaric hypoxia induces tolerance to focal permanent cerebral ischemia in association with an increased expression of hypoxia-inducible factor-1 and its target genes erythropoietin and VEGF in the adult mouse brain. J Cereb Blood Flow Metab 22:393-403
5. Bernaudin M, Tang Y, Reilly M, Petit E, Sharp FR (2002b) 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 277:39728-39738
6. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal a new serum-free medium combination. J Neurosci Res 35:567-576
7. Brugg B, Michel PP, Agid Y, Ruberg M (1996) Ceramide induces apoptosis in cultured mesencephalic neurons. J Neurochem 66:733-739
8. Brusselmans K, Bono F, Maxwell P, Dor Y, Dewerchin M, Collen D, Herbert JM, Carmeliet P (2001) Hypoxia-inducible factor-2alpha (HIF-2alpha) is involved in the apoptotic response to hypoglycemia but not to hypoxia. J Biol Chem 276:39192-39196
9. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain, RK Collen, D Keshert, E Keshet E (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis cell proliferation and tumour angiogenesis. Nature 394:485-490
10. Chakravarty P, Suthar TP, Coppock HA, Nicholl CG, Bloom SR, Legon S, Smith DM (2000) CGRP and adrenomedullin binding correlates with transcript levels for calcitonin receptor-like receptor (CRLR) and receptor activity modifying proteins (RAMPs) in rat tissues. Br J Pharmacol 130:189-195
11. Cheng B, Christakos S, Mattson MP (1994) Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron 12:139-153
12. Clark WM, Raps EC, Tong DC, Kelly RE (2000) Cervene (Nalmefene) in acute ischemic stroke: final results of a phase III efficacy study The Cervene Stroke Study Investigators. Stroke 31:1234-1239
13. Cockman ME, Masson N, Mole DR, Jaakkola P, Chang GW, Clifford SC, Maher ER, Pugh CW, Ratcliffe PJ, Maxwell PH (2000) Hypoxia inducible factor-alpha-bibding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem 275: 25733-25741
14. Crews ST, Fan CM (1999) Remembrance of things PAS: regulation of development by bHLH-PAS proteins. Curr Opin Genet Dev 9:580-587
15. Culmsee C, Monnig J, Kemp BE, Mattson MP (2001) AMP-activated protein kinase is highly expressed in neurons in the developing rat brain and promotes neuronal survival following glucose deprivation. J Mol Neurosci 17:45-58
16. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J, Cong R, Franzoso G (2001) Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signaling. Nature 414:308-313
17. Devireddy LR, Teodoro JG, Richard FA, Green MR (2001) Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation. Science 293:829-834
18. Edsall LC, Cuvillier O, Twitty S, Spiegel S, Milstien S (2001) Sphingosine kinase expression regulates apoptosis and caspase activation in PC 12 cells. J Neurochem 76:1573-1584
19. Favier J, Kempf H, Corvol P, Gasc JM (2001) Coexpression of endothelial PAS protein 1 with essential angiogenic factors suggests its involvement in human vascular development. Dev Dyn 222: 377-388
20. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL (1999) Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res 16:3915-3918
21. Flower DR (1996) The lipocalin protein family: structure and function. Biochem J 318:1-14
22. Halterman MW, Federoff HJ (1999) HIF-1alpha and p53 promote hypoxia-induced delayed neuronal death in models of CNS ischemia. Exp Neurol 159:65-72
23. Hartfield PJ, Mayne GC, Murray AW (1997) Ceramide induces apoptosis in PC 12 cells. FEBS Lett 401:148-152
24. Hartmann U, Maurer P (2001) Proteoglycans in the nervous system-the quest for functional roles in vivo. Matrix Biol 20:23-35
25. Hayashi T, Sasaki C, Iwai M, Sato K, Zhang WR, Warita H, Abe K (2001) Induction of PML immunoreactivity in rat brain neurons after transient middle cerebral artery occlusion. Neurol Res 23:772-776
26. He KL, Ting AT (2002) A20 inhibits tumor necrosis factor (TNF) alpha-induced apoptosis by disrupting recruitment of TRADD and RIP to the TNF receptor 1 complex in Jurkat T cells. Mol Cell Biol 22:6034-6045
27. Heiss WD, Graf R (1994) The ischemic penumbra. Curr Opin Neurol 7:11-19
28. Hofmann K, Tschopp J (1995) The death domain motif found in Fas (Apo-1) and TNF receptor is present in proteins involved in apoptosis and axonal guidance. FEBS Lett 371:321-323
29. Huang LE, Arany Z, Livingston DM, Bunn HF (1996) Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 271:32253-32259
30. Hudson CC, Liu M, Chiang GG, Otterness DM, Loomis DC, Kaper F, Giaccia AJ, Abraham RT (2002) Regulation of hypoxia-inducible factor 1alpha expression and function by the mammalian target of rapamycin. Mol Cell Biol 20:7004-7014
31. Jiang BH, Zheng JZ, Leung SW, Roe R, Semenza GL (1997) Transactivation and inhibitory domains of hypoxia-inducible factor 1alpha Modulation of transcriptional activity by oxygen tension. J Biol Chem 272:19253-19260
32. Jin R, De Smaele E, Zazzeroni F, Nguyen DU, Papa S, Jones J, Cox C, Gelinas C, Franzoso G (2002) Regulation of the gadd45beta promoter by NF-kappaB. DNA Cell Biol 21:491-503
33. Jung Y, Isaacs JS, Lee S, Trepel J, Liu ZG, Neckers L (2003) Hypoxia-inducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent nuclear factor kappa B activation. Biochem J 370:1011-1017
34. Kapas S, Clark AJ (1995) Identification of an orphan receptor gene as a type 1 calcitonin gene-related peptide receptor. Biochem Biophys Res Commun 217:832-8
35. Kappel A, Ronicke V, Damert A, Flamme I, Risau W, Breier G (1999) Identification of vascular endothelial growth factor (VEGF) receptor-2 (Flk-1) promoter/enhancer sequences sufficient for angioblast and endothelial cell-specific transcription in transgenic mice. Blood 93:4284-4292
36. Karakesisoglou I, Yang Y, Fuchs E (2000) An epidermal plakin that integrates actin and microtubule networks at cellular junctions. J Cell Biol 149:195-208
37. Kemp BE, Mitchelhill KI, Stapleton D, Michell BJ, Chen ZP, Witters LA (1999) Dealing with energy demand: the AMP-activated protein kinase. Trends Biochem Sci 24:22-25
38. Kennedy SP, Sun D, Oleynek JJ, Hoth CF, Kong J, Hill RJ (1998) Expression of the rat adrenomedullin receptor or a putative human adrenomedullin receptor does not correlate with adrenomedullin binding or functional response. Biochem Biophys Res Commun 244:832-837
39. Kobayashi H, Matsukawa S, Kobayashi S, Kubota T (2000) Changes in expression of mRNAs in the gerbil hippocampus following transient forebrain ischemia. Neurol Res 22:825-831
40. Ladoux A, Frelin C (2000) Coordinated Up-regulation by hypoxia of adrenomedullin and one of its putative receptors (RDC-1) in cells of the rat blood-brain barrier. J Biol Chem 275:39914-39919
41. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL (2001) HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 12:3995-4004
42. Lee EG, Boone DL, Chai S, Libby SL, Chien M, Lodolce JP, Ma A (2000) Failure to regulate TNF-induced NF-kappaB and cell death responses in A20-deficient mice. Science 289:2350-2354
43. Leonardo ED, Hinck L, Masu M, Keino-Masu K, Fazeli A, Stoeckli ET, Ackerman SL, Weinberg RA, Tessier-Lavigne M (1997) Guidance of developing axons by netrin-1 and its receptors. Cold Spring Harb Symp Quant Biol 62:467-478
44. Li Q, Stephenson D (2002) Postischemic administration of basic fibroblast growth factor improves sensorimotor function and reduces infarct size following permanent focal cerebral ischemia in the rat. Exp Neurol 177:531-537
45. Libert F, Parmentier M, Lefort A, Dumont JE, Vassart G (1990) Complete nucleotide sequence of a putative G protein coupled receptor: RDC1. Nucleic Acids Res 18:1917
46. Liu X, Zhu XZ (1999) Increased expression and nuclear accumulation of basic fibroblast growth factor in primary cultured astrocytes following ischemic-like insults. Brain Res Mol Brain Res 71:171-7
47. Llambi F, Causeret F, Bloch-Gallego E, Mehlen P (2001) Netrin-1 acts as a survival factor via its receptors UNC5H and DCC. Embo J 20:2715-2722
48. Maceyka M, Payne SG, Milstien S, Spiegel S (2002) Sphingosine kinase sphingosine-1-phosphate and apoptosis. Biochim Biophys Acta 1585:193-201
49. Marti HJ, Bernaudin M, Bellail A, Schoch H, Euler M, Petit E, Risau W (2000) Hypoxia-induced vascular endothelial growth factor expression precedes neovascularization after cerebral ischemia. Am J Pathol 156:965-976
50. Martin-Rendon E, White LJ, Olsen A, Mitrophanous KA, Mazarakis ND (2002) New Methods to Titrate EIAV-Based Lentiviral Vectors. Mol Ther 5:566-570
51. Masumura M, Murayama N, Inoue T, Ohno T (1996) Selective induction of fibroblast growth factor receptor-1 mRNA after transient focal ischemia in the cerebral cortex of rats. Neurosci Lett 213:119-122
52. Mattson MP, Culmsee C, Yu Z, Camandola S (2000) Roles of nuclear factor kappaB in neuronal survival and plasticity. J Neurochem 74:443-456
53. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ (1999) The tumor suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399:271-275
54. Mazarakis ND, Azzouz M, Rohll JB, Ellard FM, Wilkes FJ, Olsen AL, Carter EE, Barber RD, Baban DF, Kingsman SM, Kingsman AJ, O'Malley K, Mitrophanous KA (2001) Rabies virus glycoprotein pseudotyping of lentiviral vectors enables retrograde axonal transport and access to the nervous system after peripheral delivery. Hum Mol Genet 10:2109-2121
55. Miller BA, Perez RS, Shah AR, Gonzales ER, Park TS, Gidday JM (2001) Cerebral protection by hypoxic preconditioning in a murine model of focal ischemia-reperfusion. Neuroreport 12:1663-1669
56. Mitoma J, Ito M, Furuya S, Hirabayashi Y (1998) Bipotential roles of ceramide in the growth of hippocampal neurons: promotion of cell survival and dendritic outgrowth in dose- and developmental stage-dependent manners. J Neurosci Res 51:712-722
57. Mitrophanous K, Yoon S, Rohll J, Patil D, Wilkes F, Kim V, Kingsman S, Kingsman A, Mazarakis N (1999) Stable gene transfer to the nervous system using a non-primate lentiviral vector. Gene Ther 6:1808-1818
58. O'Dowd BF, Nguyen T, Lynch KR, Kolakowski LF Jr, Thompson M, Cheng R, Marchese A, Ng G, Heng HH, George SR (1996) A novel gene codes for a putative G protein-coupled receptor with an abundant expression in brain. FEBS Lett 394:325-329
59. O'Dwyer PJ, Yao KS, Ford P, Godwin AK, Clayton M (1994) Effects of hypoxia on detoxicating enzyme activity and expression in HT29 colon adenocarcinoma cells. Cancer Res 54:3082-3087
60. Peng J, Zhang L, Drysdale L, Fong GH (2000) The transcription factor EPAS-1/hypoxia-inducible factor 2alpha plays an important role in vascular remodeling. Proc Natl Acad Sci U S A 97:8386-8391
61. Rapraeger AC (1995) In the clutches of proteoglycans: how does heparan sulfate regulate FGF binding? Chem Biol 2:645-649
62. Rapraeger AC (2000) Syndecan-regulated receptor signaling. J Cell Biol 149:995-998
63. Read SJ, Parsons AA, Harrison DC, Philpott K, Kabnick K, O'Brien S, Clark S, Brawner M, Bates S, Gloger I, Legos JJ, Barone FC (2001) Stroke genomics: approaches to identify validate and understand ischemic stroke gene expression. J Cereb Blood Flow Metab 21:755-778
64. Richard DE, Berra E, Pouyssegur J (2000) Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J Biol Chem 35:26765-26771
65. Rohll JB, Mitrophanous KA, Martin-Rendon E, Ellard FM, Radcliffe PA, Mazarakis ND, Kingsman SM (2002) Design production safety evaluation and clinical applications of nonprimate lentiviral vectors. Methods Enzymol 346:466-500
66. Salomoni P, Pandolfi PP (2002) The role of PML in tumor suppression. Cell 108:165-170
67. Sandau KB, Zhou J, Kietzmann T, Brune B (2001) Regulation of the hypoxia-inducible factor 1alpha by the inflammatory mediators nitric oxide and tumor necrosis factor-alpha in contrast to desferroxamine and phenylarsine oxide. J Biol Chem 43:39805-39811
68. Semenza GL (2001a) HIF-1 and mechanisms of hypoxia sensing. Curr Opin Cell Biol 13:167-171
69. Semenza GL (2001b) Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 7:345-350
70. Sharp FR, Lu A, Tang Y, Millhorn DE (2000) Multiple molecular penumbras after focal cerebral ischemia. J Cereb Blood Flow Metab 20:1011-1032
71. Soneoka Y, Cannon PM, Ramsdale EE, Griffiths JC, Romano G, Kingsman SM, Kingsman AJ (1995) A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res 23:628-633
72. Song BW, Vinters HV, Wu D, Pardridge WM (2002) Enhanced neuroprotective effects of basic fibroblast growth factor in regional brain ischemia after conjugation to a blood-brain barrier delivery vector. J Pharmacol Exp Ther 301:605-610
73. Song HY, Rothe M, Goeddel DV (1996) The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-kappaB activation. Proc Natl Acad Sci USA 93:6721-6725
74. Sreedharan SP, Robichon A, Peterson KE, Goetzl EJ (1991) Cloning and expression of the human vasoactive intestinal peptide receptor. Proc Natl Acad Sci USA 88:4986-4990
75. Takekawa M, Saito H (1998) A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTKI/MEKK4 MAPKKK. Cell 95:521-530
76. Tang Y, Lu A, Aronow BJ, Wagner KR, Sharp FR (2002) Genomic responses of the brain to ischemic stroke intracerebral haemorrhage kainate seizures hypoglycemia and hypoxia. Eur J Neurosci 15:1937-1952
77. Tanimoto K, Makino Y, Pereira T, Poellinger L (2000) Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. Embo J 19:4298-4309
78. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133
79. Tian H, Hammer RE, Matsumoto AM, Russell DW, McKnight SL (1998) The hypoxia-responsive transcription factor EPAS1 is essential for catecholamine homeostasis and protection against heart failure during embryonic development. Genes Dev 12:3320-3324
80. Thornton RD, Lane P, Borghaei RC, Pease EA, Caro J, Mochan E (2000) Interleukin 1 induces hypoxia-inducible factor 1 in human gingival and synovial fibroblasts. Biochem J 350:307-312
81. Wang X, Yue TL, Barone FC, White RF, Clark RK, Willette RN, Sulpizio AC, Aiyar NV, Ruffolo RR Jr, Feuerstein GZ (1995) Discovery of adrenomedullin in rat ischemic cortex and evidence for its role in exacerbating focal brain ischemic damage. Proc Natl Acad Sci USA 92:11480-11484
82. Wang ZG, Ruggero D, Ronchetti S, Zhong S, Gaboli M, Rivi R, Pandolfi PP (1998) PML is essential for multiple apoptotic pathways. Nat Genet 20:266-272
83. White JR, Harris RA, Lee SR, Craigon MH, Binley K, Price T, Beard GL, Mundy CR, Naylor S (2003) Genetic amplification of the transcriptional response to hypoxia as a novel means of identifying regulators of angiogenesis. Genomics 83:1-8
84. Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, Talks KL, Wood SM, Gatter KC, Harris AL, Pugh CW, Ratcliffe PJ, Maxwell PH (1998) Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 92:2260-2268
85. Wu WS, Xu ZX, Hittelman WN, Salomoni P, Pandolfi PP, Chang KS (2003) Promyelocytic leukemia protein sensitizes tumor necrosis factor alpha- induced apoptosis by inhibiting the NF-kappaB survival pathway. J Biol Chem 278:12294-12304
86. Xia P, Wang L, Moretti PA, Albanese N, Chai F, Pitson SM, D'Andrea RJ, Gamble JR, Vadas MA (2002) Sphingosine kinase interacts with TRAF2 and dissects tumor necrosis factor-alpha signaling. J Biol Chem 277:7996-8003
87. Xu DG, Crocker SJ, Doucet JP, St-Jean M, Tamai K, Hakim AM, Ikeda JE, Liston P, Thompson CS, Korneluk RG, MacKenzie A, Robertson GS (1997) Elevation of neuronal expression of NAIP reduces ischemic damage in the rat hippocampus. Nat Med 3:997-1004
88. Yu Z, Zhou D, Bruce-Keller AJ, Kindy MS, Mattson MP (1999) Lack of the p50 subunit of nuclear factor-kappaB increases the vulnerability of hippocampal neurons to excitotoxic injury. J Neurosci 19:8856-8865
89. Zelzer E, Levy Y, Kahana C, Shilo BZ, Rubinstein M, Cohen B (1998) Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT EMBO J 17:5085-5094
90. Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, Georgescu MM, Simons JW, Semenza GL (2000) Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res 6:1541-1545