Evolution of the coordinate regulation of glycolytic enzyme genes by hypoxia

Journal of Experimental Biology

Volumn 206, Issue 17, 2003, Pages 2911-2922

  Webster, Keith A ^a  

^a UNIVERSITY OF MIAMI   (United States)

Author keywords

Anaerobic; Evolution; Gene expression; Glycolysis; HIF 1; Hypoxia

Indexed keywords

ARCA PROTEIN, E COLI; ARCB PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; FNR PROTEIN, E COLI; IRON SULFUR PROTEIN; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN KINASE; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; ANOXIA; ENERGY METABOLISM; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; GLYCOLYSIS; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SOUTHERN BLOTTING;

ANIMALS; ANOXIA; BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, SOUTHERN; ENERGY METABOLISM; ESCHERICHIA COLI PROTEINS; EVOLUTION; GENE EXPRESSION REGULATION; GLYCOLYSIS; IRON-SULFUR PROTEINS; MEMBRANE PROTEINS; PROTEIN KINASES; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

ANIMALIA; ESCHERICHIA COLI; EUKARYOTA; MAMMALIA;

EID: 0042761742     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.00516     Document Type: Review

References (100)

1. Alefounder, P. R. and Perham, R. N. (1989). Identification, molecular cloning and sequence analysis of a gene cluster encoding the class II fructose1,6-bisphosphate aldolase, 3-phosphoglycerate kinase and a putative second glyceraldehyde 3-phosphate dehydrogenase of Escherichia coli. Mol. Microbiol. 3, 723-732.
2. Bacon, N. C., Wappner, P., O'Rourke, J. F., Bartlett, S. M., Shilo, B., Pugh, C. W. and Ratcliffe, P. J. (1998). Regulation of the Drosophila bHLH-PAS protein Sima by hypoxia: functional evidence for homology with mammalian HIF-1 alpha. Biochem. Biophys. Res. Commun. 249, 811-816.
3. Barnabas, J., Schwartz, R. M. and Dayhoff, M. O. (1982). Evolution of major metabolic innovations in the precambrian. Orig. Life 12, 81-91.
4. Barnell, W. O., Yi, K. C. and Conway, T. (1990). Nucleotide sequence and genetic organization of a Zymomonas mobilis gene cluster that encodes several enzymes of glucose metabolism. J. Bacteriol. 172, 7227-7240.
5. Belouski, E., Watson, D. E. and Bennett, G. N. (1998). Cloning, sequence, and expression of the phosphofructokinase gene of Clostridium acetobutylicum ATCC 824 in Escherichia coli. Curr. Microbiol. 37, 17-22.
6. Birnbaum, M. J., van Wijnen, A. J., Odgren, P. R., Last, T. J., Suske, G., Stein, G. S. and Stein, J. L. (1995). Sp1 trans-activation of cell cycle regulated promoters is selectively repressed by Sp3. Biochemistry 34, 16503-16508.
7. Bledig, S. A., Ramseier, T. M. and Saier, M. H., Jr (1996). Frur mediates catabolite activation of pyruvate kinase (pykF) gene expression in Escherichia coli. J. Bacteriol. 178, 280-283.
8. Bruick, R. K. and McKnight, S. L. (2001). A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340.
9. +-dependent glyceraldehyde-3-phosphate dehydrogenase from Thermoproteus tenax. The first identified archaeal member of the aldehyde dehydrogenase superfamily is a glycolytic enzyme with unusual regulatory properties. J. Biol. Chem. 273, 6149-6156.
10. Bunn, H. F. and Poyton, R. O. (1996). Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76, 839-885.
11. Cannio, R., Fiorentino, G., Morana, A., Rossi, M. and Bartolucci, S. (2000). Oxygen: friend or foe? Archaeal superoxide dismutases in the protection of intra-and extracellular oxidative stress. Front. Biosci. 5, D768-D779.
12. Chang, C. and Meyerowitz, E. M. (1994). Eukaryotes have 'two-component' signal transducers. Res. Microbiol. 145, 481-486.
13. Chistoserdova, L., Vorholt, J. A., Thauer, R. K. and Lidstrom, M. E. (1998). Cl transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. Science 281, 99-102.
14. Conway, T. (1992). The Entner-Doudoroff pathway: history, physiology and molecular biology. FEMS Microbiol. Rev. 9, 1-27.
15. D'Angio, C. T. and Finkelstein, J. N. (2000). Oxygen regulation of gene expression: a study in opposites. Mol. Genet. Metab. 71, 371-380.
16. DeLong, E. F., Wu, K. Y., Prezelin, B. B. and Jovine, R. V. (1994). High abundance of Archaea in Antarctic marine picoplankton. Nature 371, 695-697.
17. Dennis, E. S., Gerlach, W. L., Walker, J. C., Lavin, M. and Peacock, W. J. (1988). Anaerobically regulated aldolase gene of maize. Mol. Biol. 202, 759-767.
18. Discher, D. J., Bishopric, N. H., Wu, X., Peterson, C. A. and Webster, K. A. (1998). Hypoxia regulates β-enolase and pyruvate kinase-M promoters by modulating Sp1/Sp3 binding to a conserved GC element. J. Biol. Chem. 273, 26087-26093.
19. Dolferus, R., Jacobs, M., Peacock, W. J. and Dennis, E. S. (1994). Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiol. 105, 1075-1087.
20. Fardeau, M. L., Faudon, C., Cayol, J. L., Magot, M., Patel, B. K. and Ollivier, B. (1996). Effect of thiosulphate as electron acceptor on glucose and xylose oxidation by Thermoanaerobacter finnii and a Thermoanaerobacter sp. isolated from oil field water. Res. Microbiol. 147, 159-165.
21. Ferguson, L. R. and von Borstel, R. C. (1992). Induction of the cytoplasmic 'petite' mutation by chemical and physical agents in Saccharomyces cerevisiae. Mutat. Res. 265, 103-148.
22. Firth, J. D., Ebert, B. L., Pugh, C. W. and Ratcliffe, P. J. (1994). Oxygen- regulated control elements in the phosphoglycerate kinase and lactate dehydrogenase A genes: similarities with the erythropoietin 3′ enhancer. Proc. Natl. Acad. Sci. USA 91, 6496-6500.
23. Fothergill-Gilmore, L. (1986). The evolution of the glycolytic pathway. Trends Biochem. Sci. 11, 47-51.
24. Fothergill-Gilmore, L. A. and Michels, P. A. (1993). Evolution of glycolysis. Prog. Biophys. Mol. Biol. 59, 105-235.
25. Fothergill-Gilmore, L. A. and Watson, H. C. (1989). The phosphoglycerate mutases. Adv. Enzymol. Rel. Areas Mol. Biol. 62, 227-313.
26. Friedrich, C. G. (1998). Physiology and genetics of sulfur-oxidizing bacteria. Adv. Microb. Physiol. 39, 235-289.
27. Gebbia, J. A., Backenson, P. B., Coleman, J. L., Anda, P. and Benach, J. L. (1997). Glycolytic enzyme operon of Borrelia burgdorferi: characterization and evolutionary implications. Gene 188, 221-228.
28. Hagen, G., Muller, S., Beato, M. and Suske, G. (1994). Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 13, 3843-3851.
29. Hannaert, V., Brinkmann, H., Nowitzki, U., Lee, J. A., Albert, M. A., Sensen, C. W., Gaasterland, T., Muller, M., Michels, P. and Martin, W. (2000). Enolase from Trypanosoma brucei, from the amitochondriate protist Mastigamoeba balamuthi, and from the chloroplast and cytosol of Euglena gracilis: pieces in the evolutionary puzzle of the eukaryotic glycolytic pathway. Mol. Biol. Evol. 17, 989-1000.
30. Hardie, D. G. (2000). Metabolic control: a new solution to an old problem. Curr. Biol. 10, R757-R759.
31. Hochachka, P. W. (1999). The metabolic implications of intracellular circulation. Proc. Natl. Acad. Sci. USA 96, 12233-12239.
32. Hochachka, P. W. and Lutz, P. L. (2001). Mechanism, origin, and evolution of anoxia tolerance in animals. Comp. Biochem. Physiol. 130B, 435-459.
33. Hofer, H. W. (1996). Conservation, evolution, and specificity in cellular control by protein phosphorylation. Experientia 52, 449-454.
34. Hu, J., Discher, D. J., Bishopric, N. H. and Webster, K. A. (1998). Hypoxia regulates expression of the endothelin-1 gene through a proximal hypoxia-inducible factor-1 binding site on the antisense strand. Biochem. Biophys. Res. Comm. 245, 894-899.
35. Iwasaki, T., Wakagi, T. and Oshima, T. (1995). Ferredoxin-dependent redox system of a thermoacidophilic archaeon, Sulfolobus sp. strain 7. Purification and characterization of a novel reduced ferredoxin-reoxidizing iron-sulfur flavoprotein. J. Biol. Chem. 270, 17878-17883.
36. 2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev. 12, 149-162.
37. 2-regulated prolyl hydroxylation. Science 292, 468-472.
38. Janssen, P. H. and Morgan, H. W. (1992). Heterotrophic sulfur reduction by Thermotoga sp. strain FjSS3.B1. FEMS Microbiol. Lett. 75, 213-217.
39. Jiang, H., Guo, R. and Powell-Coffman, J. A. (2001). The Caenorhabditis elegans hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc. Natl. Acad. Sci. USA 98, 7916-7921.
40. Jiang, Y., Vasconcelles, M. J., Wretzel, S., Light, A., Martin, C. E. and Goldberg, M. A. (2001). MGA2 is involved in the low-oxygen response element-dependent hypoxic induction of genes in Saccharomyces cerevisiae. Mol. Cell Biol. 21, 6161-6169.
41. Kasting, J. F. (1993). Earth's early atmosphere. Science 259, 920-926.
42. Kelly, R. M. and Adams, M. W. (1994). Metabolism in hyperthermophilic microorganisms. Antonie Van Leeuwenhoek 66, 247-270.
43. Kiley, P. J. and Reznikoff, W. S. (1991). Fnr mutants that activate gene expression in the presence of oxygen. J. Bacteriol. 173, 16-22.
44. Koch, A. L. (1998). How did bacteria come to be? Adv. Microb. Physiol. 40, 353-399.
45. Kumar, A. P. and Butler, A. P. (1997). Transcription factor Sp3 antagonizes activation of the ornithine decarboxylase domains. Nucl. Acids Res. 25, 2012-2019.
46. Kumari, S., Beatty, C. M., Browning, D. F., Busby, S. J., Simel, E. J., Hovel-Miner, G. and Wolfe, A. J. (2000). Regulation of acetyl coenzyme A synthetase in Escherichia coli. J. Bacteriol. 182, 4173-4179.
47. Leyva-Vazquez, M. A. and Setlow, P. (1994). Cloning and nucleotide sequences of the genes encoding triose phosphate isomerase, phosphoglycerate mutase, and enolase from Bacillus subtilis. J. Bacteriol. 176, 3903-3910.
48. Li, C. W., Chen, J. Y. and Hua, T. E. (1998). Precambrian sponges with cellular structures. Science 279, 879-882.
49. Liaud, M. F., Lichtle, C., Apt, K., Martin, W. and Cerff, R. (2000). Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol. Biol. Evol. 17, 213-223.
50. Lonberg, N. and Gilbert, W. (1985). Intron/exon structure of the chicken pyruvate kinase gene. Cell 40, 81-90.
51. Luca, P. D., Majello, B. and Lania, L. (1996). Sp3 represses transcription when tethered to promoter DNA or targeted to promoter proximal RNA. J. Biol. Chem. 271, 8533-8536.
52. Luesink, E. J., van Herpen, R. E., Grossiord, B. P., Kuipers, O. P. and de Vos, W. M. (1998). Transcriptional activation of the glycolytic las operon and catabolite repression of the gal operon in Lactococcus lactis are mediated by the catabolite control protein CcpA. Mol. Microbiol. 30, 789-798.
53. Ma, K., Loessner, H., Heider, J., Johnson, M. K. and Adams, M. W. (1995). Effects of elemental sulfur on the metabolism of the deep-sea hyperthermophilic archaeon Thermococcus strain ES-1: characterization of a sulfur-regulated, non-heme iron alcohol dehydrogenase. J. Bacteriol. 177, 4748-4756.
54. Majello, B., Luca, P. D. and Lania, L. (1997). Sp3 is a bifunctional transcription regulator with modular independent activation and repression domains. J. Biol. Chem. 272, 4021-4026.
55. McClelland, G. B., Hochachka, P. W. and Weber, J. M. (1998). Carbohydrate utilization during exercise after high-altitude acclimation: a new perspective. Proc. Natl. Acad. Sci. USA 95, 10288-10293.
56. Mehrani, H. and Storey, K. B. (1995). Enzymatic control of glycogenolysis during anoxic submergence in the freshwater turtle Trachemys scripta. Int. J. Biochem. Cell. Biol. 27, 821-830.
57. Mertens, E. (1991). Pyrophosphate-dependent phosphofructokinase, an anaerobic glycolytic enzyme? FEBS Lett. 285, 1-5.
58. Millhorn, D. E., Raymond, R., Conforti, L., Zhu, W., Beltner-Johnson, D., Filisko, T., Genter, M. B., Kobayashi, S. and Peng, M. (1997). Regulation of gene expression for tyrosine hydroxylase in oxygen sensitive cells by hypoxia. Kidney Int. 51, 527-535.
59. Murphy, B. J., Andrews, G. K., Bittel, D., Discher, D. J., McCue, J., Green, C. J., Yanovsky, M., Giaccia, A., Sutherland, R. M., Laderoute, K. R. and Webster, K. A. (1999). Activation of metallithionein gene expression by hypoxia involves metal response elements and metal transcription factor-1. Cancer Res. 59, 1315-1322.
60. Nishi, K., Park, C. S., Pepper, A. E., Eichinger, G., Innis, M. A. and Holland, M. J. (1995). The GCR1 requirement for yeast glycolytic gene expression is suppressed by dominant mutations in the SGC1 gene, which encodes a novel basic-helix-loop-helix protein. Mol. Cell Biol. 15, 2646-2653.
61. O'Callaghan, J. and Conrad, M. (1992). Symbiotic interactions in the EVOLVE III ecosystem model. Biosystems 26, 199-209.
62. Olive, M. R., Peacock, W. J. and Dennis, E. S. (1991). The anaerobic response element contains two GC-rich sequences essential for binding a nuclear protein and hypoxic activation of the maize Adh1 promoter. Nucl. Acids. Res. 19, 7053-7060.
63. Papagiannis, M. D. (1984). Life-related aspects of stellar evolution. Orig. Life. 14, 43-50.
64. Parkinson, J. S. and Kofoid, E. C. (1992). Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26, 71-112.
65. Parolin, M. L., Spriet, L. L., Hultman, E., Hollidge-Horvat, M. G., Jones, N. L. and Heigenhauser, G. J. (2000). Regulation of glycogen phosphorylase and PDH during exercise in human skeletal muscle during hypoxia. Am. J. Physiol. Endocrinol. Metab. 278, E522-E534.
66. Pasteur, L. (1861). Expériences et vues nouvelles sur la nature des fermentations. Comp. Rend. Acad. Sci. 52, 1260-1264.
67. Peak, M. J., Peak, J. G., Stevens, F. J., Blamey, J., Mai, X., Zhou, Z. H. and Adams, M. W. (1994). The hyperthermophilic glycolytic enzyme enolase in the archaeon, Pyrococcus furiosus: comparison with mesophilic enolases. Arch. Biochem. Biophys. 313, 280-286.
68. Piechaczyk, M., Blanchard, J. M., Riaad-El, Sabouty, S., Dani, C., Marty, L. and Jeanteur, P. (1984). Unusual abundance of vertebrate 3-phosphate dehydrogenase pseudogenes. Nature 312, 469-471.
69. Poorman, R. A., Randolph, A., Kemp, R. G. and Heinrikson, R. L. (1984). Evolution of phosphofructokinase-gene duplication and creation of new effector sites. Nature 309, 467-469.
70. Prabhakar, N. R. (2001). Oxygen sensing during intermittent hypoxia: cellular and molecular mechanisms. J. Appl. Physiol. 90, 1986-1994.
71. Rasmussen, B., Bengtson, S., Fletcher, I. R. and McNaughton, N. J. (2002). Discoidal impressions and trace-like fossils more than 1200 million years old. Science 296, 1112-1115.
72. Reeve, J. N. (1992). Molecular biology of methanogens. Annu. Rev. Microbiol. 46, 165-191.
73. Reid, R. P., Visscher, P. T., Decho, A. W., Stolz, J. F., Bebout, B. M., Dupraz, C., Macintyre, I. G., Paerl, H. W., Pinckney, J. L., Prufert-Bebout, L. et al. (2000). The role of microbes in accretion, lamination and early lithification of modern marine stromatolites. Nature 406, 989-992.
74. Riddle, S. R., Ahmad, A., Ahmad, S., Deeb, S. S., Malkki, M., Schneider, B. K., Allen, C. B. and White, C. W. (2000). Hypoxia induces hexokinase II gene expression in human lung cell line A549. Am. J. Physiol. Lung. Cel. Mol. Physiol. 278, L407-L416.
75. Romano, A. H. and Conway, T. (1996). Evolution of carbohydrate metabolic pathways. Res. Microbiol. 147, 448-455.
76. Rossman, M. G. (1981). Evolution of glycolytic enzymes. Phil. Trans. R. Soc. Lond. B 293, 191-203.
77. Schlapfer, B. S. and Zuber, H. (1992). Cloning and sequencing of the genes encoding glyceraldehyde-3-phosphate dehydrogenase, phosphoglycerate kinase and triosephosphate isomerase (gap operon) from mesophilic Bacillus megaterium: comparison with corresponding sequences from thermophilic Bacillus stearothermophilus. Gene 122, 53-62.
78. Segerer, A., Stetter, K. O. and Klink, F. (1985). Two contrary modes of chemolithotrophy in the same archaebacterium. Nature 313, 787-789.
79. Seilacher, A., Bose, P. K. and Pflüger, F. (1998). Triploblastic Animals More Than 1 Billion Years Ago: Trace Fossil Evidence from India. Science 282, 80-83.
80. Selig, M., Xavier, K. B., Santos, H. and Schonheit, P. (1997). Comparative analysis of Embden-Meyerhof and Entner-Doudoroff glycolytic pathways in hyperthermophilic archaea and the bacterium Thermotoga. Arch. Microbiol. 167, 217-232.
81. Semenza, G. L., Jiang, B., Leung, S. W., Passantino, R., Concordet, J., Maire, P. and Giallongo, A. (1996). 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.
82. Semenza, G. L. (2001). Hypoxia-inducible factor 1: control of oxygen homeostasis in health and disease. Pediatr. Res. 49, 614-617.
83. Siebers, B., Klenk, H.-P. and Hensel, R. (1998). PPi-Dependent Phosphofructokinase from Thermoproteus tenax, an Archaeal Descendant of an Ancient Line in Phosphofructokinase Evolution. J. Bacteriol 180, 2137-2143.
84. Soitamo, A. J., Rabergh, C. M., Gassmann, M., Sistonen, L. and Nikinmaa, M. (2001). Characterization of a hypoxia-inducible factor (HIF-1alpha) from rainbow trout. Accumulation of protein occurs at normal venous oxygen tension. J. Biol. Chem. 276, 19699-19705.
85. Spiro, S. and Guest, J. R. (1991). Adaptive responses to oxygen limitation in Escherichia coli. Trends Biochem. Sci. 16, 310-314.
86. Tobisch, S., Zuhlke, D., Bernhardt, J., Stulke, J. and Hecker, M. (1999). Role of CcpA in regulation of the central pathways of carbon catabolism in Bacillus subtilis. J. Bacteriol. 181, 6996-7004.
87. Unkles, S. E., Logsdon, J. M., Jr, Robison, K., Kinghorn, J. R. and Duncan, J. M. (1997). The tigA gene is a transcriptional fusion of glycolytic genes encoding triose-phosphate isomerase and glyceraldehyde-3-phosphate dehydrogenase in oomycota. J. Bacteriol. 179, 6816-6823.
88. van der Oost, J., Schut, G., Kengen, S. W., Hagen, W. R., Thomm, M. and de Vos, W. M. (1998). The ferredoxin-dependent conversion of glyceraldehyde-3-phosphate in the hyperthermophilic archaeon Pyrococcus furiosus represents a novel site of glycolytic regulation. J. Biol. Chem. 273, 28149-28154.
89. Vasconcelles, M. J., Jiang, Y., McDaid, K., Gilooly, L., Wretzel, S., Porter, D. L., Martin, C. E. and Goldberg, M. A. (2001). Identification and characterization of a low oxygen response element involved in the hypoxic induction of a family of Saccharomyces cerevisiae genes. Implications for the conservation of oxygen sensing in eukaryotes. J. Biol. Chem. 276, 14374-14384.
90. Vogt, M., Puntschart, A., Geiser, J., Zuleger, C., Billeter, R. and Hoppeler, H. (2001). Molecular adaptations in human skeletal muscle to endurance training under simulated hypoxic conditions. J. Appl. Physiol. 91, 173-182.
91. Webster, K. A. (1987). Regulation of glycolytic enzyme RNA transcriptional rates by oxygen availability in skeletal muscle cells. Mol. Cell. Biochem. 77, 19-28.
92. Webster, K. A., Discher, D. and Bishopric, N. H. (1993). Induction and nuclear accumulation of fos and jun proto-oncogenes in hypoxia cardiac myocytes. J. Biol. Chem. 268, 16852-16859.
93. Webster, K. A., Discher, D. J. and Bishopric, N. H. (1994). Regulation of fos and jun immediate-early genes by redox or metabolic stress in cardiac myocytes. Circ. Res. 75, 361-371.
94. Webster, K. A., Discher, D. J., Kaiser, S., Hernandez, O. M., Sato, B. and Bishopric, N. H. (1999). Hypoxia-activated apoptosis of cardiac myocytes requires reoxygenation or a pH shift and is independent of p53. J. Clin. Invest. 104, 239-252.
95. Webster, K. A., Gunning, P. W., Hardeman, E., Wallace, D. C. and Kedes, L. H. (1990). Coordinate reciprocal trends in glycolytic and mitochondrial transcript accumulations during the in vitro differentiation of human myoblasts. J. Cell. Physiol. 142, 566-573.
96. Webster, K. A. and Murphy, B. J. (1988). Regulation of tissue-specific glycolytic isozyme genes: coordinate regulation by oxygen availability in skeletal muscle cells. Can. J. Zool. 66, 1046-1058.
97. Webster, K. A., Discher, D. J., Hernandez, O. M., Yamashita, K. and Bishopric, N. H. (2000). A glycolytic pathway to apoptosis of hypoxic cardiac myocytes. Molecular pathways of increased acid production. Adv. Exp. Med. Biol. 475, 161-175.
98. Webster, K. A., Prentice, H. and Bishopric, N. H. (2001). Oxidation of zinc finger transcription factors: physiological consequences. Antiox. Redox Signal. 3, 535-548.
99. Yamashita, K., Discher, D. J., Bishopric, N. H. and Webster, K. A. (2001). 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.
100. Zitomer, R. S., Carrico, P. and Deckert, J. (1997). Regulation of hypoxic gene expression in yeast. Kidney Int. 51, 507-513.