Functional genomics approach to hypoxia signaling

Journal of Applied Physiology

Volumn 96, Issue 2, 2004, Pages 765-773

  Seta, Karen A ^a   Millhorn, David E ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

Author keywords

Microarray; Real time polymerase chain reaction; RNA interference; Subtractive suppression hybridization

Indexed keywords

GENE PRODUCT; HEXOKINASE; PHOSPHOGLYCERATE KINASE; PLASMINOGEN ACTIVATOR INHIBITOR; PYRUVATE KINASE; TRANSCRIPTION FACTOR JUNB; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; VASCULOTROPIN;

APOPTOSIS; CANCER THERAPY; CARDIOVASCULAR DISEASE; CELL KINETICS; CELL SURVIVAL; CLONOGENESIS; DNA LIBRARY; DNA MICROARRAY; DRUG DESIGN; ENERGY BALANCE; EXPRESSED SEQUENCE TAG; GENE CONTROL; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GENOMICS; HYPOXIA; NONHUMAN; NORTHERN BLOTTING; OXYGEN SUPPLY; PHENOTYPE; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SIGNAL TRANSDUCTION; STROKE; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; UPREGULATION;

ANIMALS; ANOXIA; GENOMICS; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

EID: 0942265977     PISSN: 87507587     EISSN: None     Source Type: Journal    
DOI: 10.1152/japplphysiol.00836.2003     Document Type: Review

References (90)

1. An WG, Kanekal M, Simon MC, Maltepe E, Blagosklonny MV, and Neckers LM. Stabilization of wild-type p53 by hypoxia-inducible factor 1α. Nature 392: 405-408, 1998.
2. Bae MK, Ahn MY, Jeong JW, Bae MH, Lee YM, Bae SK, Park JW, Kim KR, and Kim KW. Jab1 interacts directly with HIF-1α and regulates its stability. J Biol Chem 277: 9-12, 2002.
3. 2+/calmodulin signaling systems in PC12 cells. Biochem Biophys Res Commun 241: 61-66, 1998.
4. Beitner-Johnson D and Millhorn DE. Hypoxia induces phosphorylation of the cyclic AMP response element-binding protein by a novel signaling mechanism. J Biol Chem 273: 19834-19839, 1998.
5. Beitner-Johnson D, Rust RT, Hsieh T, and Millhorn DE. Regulation of CREB by moderate hypoxia in PC12 cells. Adv Exp Med Biol 475: 143-152, 2000.
6. Beitner-Johnson D, Rust RT, Hsieh TC, and Millhorn DE. Hypoxia activates Akt and induces phosphorylation of GSK-3 in PC12 cells. Cell Signal 13: 23-27, 2001.
7. Beitner-Johnson D, Seta K, Yuan Y, Kim HW, Rust R, Conrad PW, Kobayashi S, and Millhorn DE. Identification of hypoxia-responsive genes in a dopaminergic cell line by subtractive cDNA libraries and microarray analysis. Parkinsonism Related Disorders 7: 273-281, 2001.
8. Beitner-Johnson D, Shull GE, Dedman JR, and Millhorn DE. Regulation of gene expression by hypoxia: a molecular approach. Respir Physiol 110: 87-97, 1997.
9. Brusselmans K, Bono F, Maxwell P, Dor Y, Dewerchin M, Collen D, Herbert JM, and Carmeliet P. Hypoxia-inducible factor-2α (HIF-2α) is involved in the apoptotic response to hypoglycemia but not to hypoxia. J Biol Chem 276: 39192-39196, 2001.
10. Bustin SA. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J Mol Endocrinol 25: 169-196, 2000.
11. Chandel NS, Vander Heiden MG, Thompson CB, and Schumacker PT. Redox regulation of p53 during hypoxia. Oncogene 19: 3840-3848, 2000.
12. + role of the Kv1.2-subunit in mediating the hypoxic response. J Physiol 524:783-793, 2000.
13. + channel in rat PC12 cells by hypoxia. J Physiol 502: 293-305, 1997.
14. 2-sensing and hypoxia tolerance in pheochromocytoma cells. Comp Biochem Physiol B 128: 187-204, 2001.
15. Conrad PW, Freeman TL, Beitner-Johnson D, and Millhorn DE. EPAS1 trans-activation during hypoxia requires p42/p44 MAPK. J Biol Chem 274:33709-33713, 1999.
16. Conrad PW, Rust RT, Han J, Millhorn DE, and Beitner-Johnson D. Selective activation of p38α and p38γ by hypoxia. Role in regulation of cyclin D1 by hypoxia in PC12 cells. J Biol Chem 274: 23570-23576, 1999.
17. Czyzyk-Krzeska MF, Bayliss DA, Lawson EE, and Millhorn DE. Regulation of tyrosine hydroxylase gene expression in the rat carotid body by hypoxia. J Neurochem 58: 1538-1546, 1992.
18. Czyzyk-Krzeska MF, Furnari BA, Lawson EE, and Millhorn DE. Hypoxia increases rate of transcription and stability of tyrosine hydroxylase mRNA in pheochromocytoma (PC12) cells. J Biol Chem 269: 760-764, 1994.
19. + channel in the type-I cell of the rabbit carotid body. FEBS Lett 249: 195-198, 1989.
20. Diatchenko L, Chenchik A, and Siebert P. Suppression subtractive hybridization: a method for generating subtracted cDNA libraries starting from poly(A+) or total RNA. In: RT-PCR Methods for Gene Cloning and Analysis, edited by Siebert P and Larrick J. Boston, MA: BioTechniques Books, 1998, p. 213-239.
21. Diatchenko L, Lau YFC, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, and Siebert PD. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93: 6025-6030, 1996.
22. DiDonato J, Mercurio F, Rosette C, Wu-Li J, Suyang H, Ghosh S, and Karin M. Mapping of the inducible IκB phosphorylation sites that, signal its ubiquitination and degradation. Mol Cell Biol 16: 1295-1304, 1996.
23. Evinger MJ, Cikos S, Nwafor-Anene V, Powers JF, and Tischler AS. Hypoxia activates multiple transcriptional pathways in mouse pheochromocytoma cells. Ann NY Acad Sci 971: 61-65, 2002.
24. Fishman M, Greene WL, and Platika D. Oxygen chemoreception by carotid body cells in culture. Proc Natl Acad Sci USA 82: 1448-1450, 1985.
25. Fitzpatrick TE and Graham CH. Stimulation of plasminogen activator inhibitor-1 expression in immortalized human trophoblast cells cultured under low levels of oxygen. Exp Cell Res 245: 155-162, 1998.
26. Ghafar MA, Anastasiadis AG, Chen MW, Burchardt M, Olsson LE, Xie H, Benson MC, and Buttyan R. Acute hypoxia increases the aggressive characteristics and survival properties of prostate cancer cells. Prostate 54: 58-67, 2003.
27. Gonzales CY, Kwok Y, Gibb J, and Fidone S. Effects of hypoxia on tyrosine hydroxylase activity in rat carotid body. J Neurochem 33: 713-719, 1979.
28. Graeber TG, Peterson JF, Tsai M, Monica K, Fornace AJ Jr, and Giaccia AJ. Hypoxia induces accumulation of p53 protein, but activation of a G1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol Cell Biol 14: 6264-6277, 1994.
29. Green LA and Tischler AS. PC12 pheochromocytoma cultures in neurobiological research. Adv Cell Neurobiol 3: 373-414, 1982.
30. Gu YZ, Moran SM, Hogenesch JB, Wartman L, and Bradfield CA. Molecular characterization and chromosomal localization of a third alpha-class hypoxia inducible factor subunit, HIF3α. Gene Expr 7: 205-213, 1998.
31. Gurskaya NG, Diatchenko L, Chenchik A, Siebert PD, Khaspekov GL, Lukyanov KA, Vagner LL, Ermolaeva OD, Lukyanov SA, and Sverdlov ED. Equalizing cDNA subtraction based on selective suppression of polymerase chain reaction: cloning of Jurkay cell transcripts induced by phytohemaglutinin and phorbol 12-myristate 13-acitate. Anal Biochem 240: 90-97, 1996.
32. Hara S, Hamada J, Kobayashi C, Kondo Y, and Imura N. Expression and characterization of hypoxia-inducible factor (HIF)-3α in human kidney: suppression of HIF-mediated gene expression by HIF-3α. Biochem Biophys Res Commun 287: 808-813, 2001.
33. Hegde P, Qi R, Abernathy K, Gay C, Dharap S, Gaspard R, Hughes JE, Snesrud E, Lee N, and Quackenbush J. A concise guide to cDNA microarray analysis. Biotechniques 29: 548-562, 2000.
34. Hochachka PW, Buck LT, Doll CJ, and Land SC. Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci USA 93: 9493-9498, 1996.
35. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95: 7987-7992, 1998.
36. Imbert V, Rupec RA, Livolsi A, Pahl HL, Traenckner EB, Mueller-Dieckmann C, Farahifar D, Rossi B, Auberger P, Baeuerle PA, and Peyron JF. Tyrosine phosphorylation of IκB-α activates NF-κB without proteolytic degradation of IκB-α. Cell 86: 787-798, 1996.
37. Kerr MK and Churchill GA. Experimental design for gene expression microarrays. Biostatistics 2: 183-201, 2001.
38. Kerr MK and Churchill GA. Statistical design and the analysis of gene expression microarray data. Genet Res 77: 123-128, 2001.
39. Kilbourne EJ, Nankova BB, Lewis EJ, McMahon A, Osaka H, Sabban DB, and Sabban EL. Regulated expression of the tyrosine hydroxylase gene by membrane depolarization. Identification of the responsive element and possible second messengers. J Biol Chem 267: 7563-7569, 1992.
40. 2A receptor-mediated inhibition of calcium current in rat PC12 cells via downregulation of protein kinase A. J Physiol 512.2: 351-363, 1998.
41. 2A receptor. J Physiol 508.1: 95-107, 1998.
42. Kobayashi S and Millhorn DE. Regulation of N-methyl-D-aspartate receptor expression and N-methyl-D-aspartate-induced cellular response during chronic hypoxia in differentiated rat PC12 cells. Neuroscience 101: 1153-1162, 2000.
43. 2A receptor gene by hypoxia in PC12 cells. A potential role in cell protection. J Biol Chem 274: 20358-20365, 1999.
44. Koong A, Chen EY, and Giaccia AJ. Hypoxia causes the activation of nuclear factor κB through the phosphorylation of IκBα on tyrosine residues. Cancer Res 54: 1425-1430, 1994.
45. Liang P and Pardee AB. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257: 967-971, 1992.
46. Lopez-Barneo J. Oxygen-sensing ion channels and the regulation of cellular functions. Trends Neurosci 19: 435-440, 1996.
47. 2 in the type I chemoreceptor cells. Science 241: 580-582, 1988.
48. Michiels C, Minet E, Michel G, Mottet D, Piret JP, and Raes M. HIF-1 and AP-1 cooperate to increase gene expression in hypoxia: role of MAP kinases. IUBMB Life 52: 49-53, 2001.
49. Millhorn DE, Norris M, and Raymond R. Stimulation of tyrosine hydroxylase gene transcription during hypoxia: Regulation by cis-trans interactions. In: Stress: Molecular Genetic and Neurobiological Advances, edited by McCarty R, Aguilera G, Sabban E, and Kvetnansky R. New York: Gordon and Breach Science, 1996, p. 629-645.
50. Millhorn DE, Raymond R, Conforti L, Zhu W, Beitner-Johnson D, Filisko T, Genter MB, Kobayashi S, and Peng M. Regulation of gene expression for tyrosine hydroxylase in oxygen sensitive cells by hypoxia. Kidney Int 51: 527-535, 1997.
51. Minet E, Michel G, Mottet D, Piret JP, Barbieux A, Raes M, and Michiels C. c-JUN gene induction and AP-1 activity is regulated by a JNK-dependent pathway in hypoxic HepG2 cells. Exp Cell Res 265: 114-124, 2001.
52. Mishra RR, Adhikary G, Simonson MS, Cherniack NS, and Prabhakar NR. Role of c-fos in hypoxia-induced AP-1 cis-element activity and tyrosine hydroxylase gene expression. Brain Res Mol Brain Res 59: 74-83, 1998.
53. Niitsu Y, Hori O, Yamaguchi A, Bando Y, Ozawa K, Tamatani M, Ogawa S, and Tohyama M. Exposure of cultured primary rat astrocytes to hypoxia results in intracellular glucose depletion and induction of glycolytic enzymes. Brain Res Mol Brain Res 74: 26-34, 1999.
54. 2-responsive sequences on the tyrosine hydroxylase gene. J Biol Chem 270:23774-23779, 1995.
55. Park SK, Dadak AM, Haase VH, Fontana L, Giaccia AJ, and Johnson RS. Hypoxia-induced gene expression occurs solely through the action of hypoxia-inducible factor 1α (HIF-1α): role of cytoplasmic trapping of HIF-2α. Mol Cell Biol 23: 4959-4971, 2003.
56. Prabhakar NR, Shenoy BC, Simonson MS, and Cherniack NS. Cell selective induction and transcriptional activation of immediate early genes by hypoxia. Brain Res 697: 266-270, 1995.
57. Quackenbush J. Computational analysis of microarray data. Nature Rev Genetics 2: 418-427, 2001.
58. Ravi R, Mookerjee B, Bhujwalla ZM, Sutter CH, Artemov D, Zeng Q, Dillehay LE, Madan A, Semenza GL, and Bedi A. Regulation of tumor angiogenesis by p53-induced degradation of hypoxia-inducible factor 1α. Genes Dev 14: 34-44, 2000.
59. Renton A, Llanos S, and Lu X. Hypoxia induces p53 through a pathway distinct from most DNA-damaging and stress-inducing agents. Carcinogenesis 24: 1177-1182, 2003.
60. Royds JA, Dower SK, Qwarnstrom EE, and Lewis CE. Response of tumour cells to hypoxia: role of p53 and NFκB. Mol Pathol 51: 55-61, 1998.
61. Sansome C, Zaika A, Marchenko ND, and Moll UM. Hypoxia death stimulus induces translocation of p53 protein to mitochondria. Detection by immunofluorescence on whole cells. FEBS Lett 488: 110-115, 2001.
62. Schena M, Shalon D, Davis RW, and Brown PO. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270: 467-470, 1995.
63. Scortegagna M, Morris MA, Oktay Y, Bennett M, and Garcia JA. The HIF family member EPAS1/HIF-2α is required for normal hematopoiesis in mice. Blood 102: 1634-1640, 2003.
64. Semenza GL. HIF-1 and human disease: one highly involved factor. Genes Dev 14: 1983-1981, 2000.
65. 2, and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107: 1-3, 2001.
66. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet JP, Maire P, and Giallongo A. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 271: 32529-32537, 1996.
67. Semenza GL, Roth PH, Fang HM, and Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 269: 23757-23763, 1994.
68. Semenza GL and Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 12: 5447-5454, 1992.
69. Seta KA, Ferguson TK, and Millhorn DE. Discovery of oxygen responsive genes in pheochromocytoma cells. In: Methods in Enzymology. In press.
70. Seta KA, Kim R, Kim HW, Millhorn DE, and Beitner-Johnson D. Hypoxia-induced regulation of MAPK phosphatase-1 as identified by subtractive suppression hybridization and cDNA microarray analysis. J Biol Chem 276: 44405-44412, 2001.
71. Seta KA, Spicer Z, Yuan Y, Lu G, and Millhorn DE. Responding to hypoxia: lessons from a model cell line. Science's STKE; http://www.stke.org/cgi/content/full/sigtrans;2002/146/rell, 2002.
72. Shalon D, Smith SJ, and Brown PO. A DNA microarray system for analyzing complex DNA samples using two-color fluorescent probe hybridization. Genome Res 6: 639-645, 1996.
73. Shaw K, Montague W, and Yoshizaki K. Biochemical studies on the release of dopamine from the rat carotid body. In Vitro 1013: 42-46, 1989.
74. Shi Q, Le X, Abbruzzese JL, Wang B, Mujaida N, Matsushima K, Huang S, Xiong Q, and Xie K. Cooperation between transcription factor AP-1 and NF-κB in the induction of interleukin-8 in human pancreatic adenocarcinoma cells by hypoxia. J Interferon Cytokine Res 19: 1363-1371, 1999.
75. Shweiki D, Itin A, Soffer D, and Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359: 843-845, 1992.
76. Singh S, Darnay BG, and Aggarwal BB. Site-specific tyrosine phosphorylation of IκBα negatively regulates its inducible phosphorylation and degradation. J Biol Chem 271: 31049-31054, 1996.
77. Sowter HM, Ratcliffe PJ, Watson P, Greenberg AH, and Harris AL. HIF-1-dependent regulation of hypoxic induction of the cell death factors BNIP3 and NIX in human tumors. Cancer Res 61: 6669-6673, 2001.
78. Srinivas V, Zhang LP, Zhu XH, and Caro J. Characterization of an oxygen/redox-dependent degradation domain of hypoxia-inducible factor α (HIF-α) proteins. Biochem Biophys Res Commun 260: 557-561, 1999.
79. Tabata M, Tarumoto T, Ohmine K, Furukawa Y, Hatake K, Ozawa K, Hasegawa Y, Mukai H, Yamamoto M, and Imagawa S. Stimulation of GATA-2 as a mechanism of hydrogen peroxide suppression in hypoxia-induced erythropoietin gene expression. J Cell Physiol 186: 260-267, 2001.
80. Tang TTL and Lasky LA. The forkhead transcription factor FOXO4 induces the down-regulation of hypoxia-inducible factor 1 α by a von Hippel-Lindau protein-independent mechanism. J Biol Chem 278: 30125-30135, 2003.
81. Velculescu VE, Zhang L, Vogelstein B, and Kinzler KW. Serial analysis of gene expression. Science 270: 484-487, 1995.
82. Weir EK and Archer SL. The mechanism of acute hypoxic pulmonary vasoconsctiction, the tale of two channels. FASEB J 9: 183-189, 1995.
83. Wisdom R. AP-1: one switch for many signals. Exp Cell Res 253: 180-185, 1999.
84. Wu H and Lozano G. NFκB activation of p53. A potential mechanism for suppressing cell growth in response to stress. J Biol Chem 269: 20067-20074, 1994.
85. Xu L, Xie K, Mukaida N, Matsushima K, and Fidler IJ. Hypoxia-induced elevation in interleukin-8 expression by human ovarian carcinoma cells. Cancer Res 59: 5822-5829, 1999.
86. Yamashita K, Discher DJ, Hu J, Bishopric NH, and Webster KA. Molecular regulation of the endothelin-1 gene by hypoxia. Contributions of hypoxia-inducible factor-1, activator protein-1, GATA-2, AND p300/CBP. J Biol Chem 276: 12645-12653, 2001.
87. Zhang HM, Cheung P, Yanagawa B, McManus BM, and Yang DC. BNips: a group of pro-apoptotic proteins in the Bcl-2 family. Apoptosis 8: 229-236, 2003.
88. Zhu H and Bunn F. Oxygen sensing and signaling: impact on the regulation of physiologically important genes. Respir Physiol 115: 239-247, 1999.
89. + current. Am J Physiol Cell Physiol 271: C658-C665, 1996.
90. Zon LI, Youssoufian H, Mather C, Lodish HF, and Orkin SH. Activation of the erythropoietin receptor promoter by transcription factor GATA-1. Proc Natl Acad Sci USA 88: 10638-10641, 1991.