Control of the Hypoxic Response in Drosophila melanogaster by the Basic Helix-Loop-Helix PAS Protein Similar

REFERENCES

• Bacon, N. C., P. Wappner, J. F. O'Rourke, S. M. Bartlett, B.-Z. Shilo, C. W. Pugh, and P. J. Ratcliffe. 1998. Regulation of the Drosophila bHLH-PAS protein Sima by hypoxia: functional evidence for homology with mammalian HIF-1α. Biochem. Biophys. Res. Commun. 249: 811–816.
   PubMedGoogle Scholar
• Berra, E., D. Roux, D. E. Richard, and J. Pouyssegur. 2001. Hypoxia-inducible factor-1α (HIF-1α) escapes O2-driven proteasomal degradation irrespective of its subcellular localization: nucleus or cytoplasm. EMBO Rep. 2: 615–620.
   PubMed Web of Science ®Google Scholar
• Brand, A. H., and N. Perrimon. 1993. Targeted gene expression as means of altering cell fates and generating dominant phenotypes. Development 118: 401–415.
   PubMed Web of Science ®Google Scholar
• Bruick, R. K., and S. L. McKnight. 2001. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294: 1337–1340.
   PubMed Web of Science ®Google Scholar
• Carmeliet, P., Y. Dor, J. M. Herbert, D. Fukumura, K. Brusselmans, M. Dewerchin, M. Neeman, F. Bono, R. Abramovitch, P. Maxwell, C. J. Koch, P. Ratcliffe, L. Moons, R. K. Jain, D. Collen, and E. Keshet. 1998. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation, and tumour angiogenesis. Nature 394: 485–490.
   PubMed Web of Science ®Google Scholar
• Carrero, P., K. Okamoto, P. Coumailleau, S. O'Brien, H. Tanaka, and L. Poellinger. 2000. Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1α. Mol. Cell. Biol. 20: 402–415.
   PubMed Web of Science ®Google Scholar
• Crews, S. T., R. Franks, S. Hu, B. Matthews, and J. Nambu. 1992. Drosophila single-minded gene and the molecular genetics of CNS midline development. J. Exp. Zool. 261: 234–244.
   PubMedGoogle Scholar
• Crews, S. T. 1998. Control of cell lineage-specific development and transcription by bHLH-PAS proteins. Genes Dev. 12: 607–620.
   PubMed Web of Science ®Google Scholar
• Crews, S. T., and C. M. Fan. 1999. Remembrance of things PAS: regulation of development by bHLH-PAS proteins. Curr. Opin. Genet. Dev. 9: 580–587.
   PubMed Web of Science ®Google Scholar
• DiGregorio, P. J., J. A. Ubersax, and P. H. O'Farrell. 2001. Hypoxia and nitric oxide induce a rapid, reversible cell cycle arrest of the Drosophila syncytial divisions. J. Biol. Chem. 276: 1930–1937.
   PubMed Web of Science ®Google Scholar
• Douglas, R. M., T. Xu, and G. G. Haddad. 2001. Cell cycle progression and cell division are sensitive to hypoxia in Drosophila melanogaster embryos. Am. J. Physiol. Regul. Integr. 280: R1555–R1563.
   PubMedGoogle Scholar
• Elson, D. A., G. Thurston, L. E. Huang, D. G. Ginzinger, D. M. McDonald, R. S. Johnson, and J. M. Arbeit. 2001. Induction of hypervascularity without leakage or inflammation in transgenic mice overexpressing hypoxia-inducible factor-1α. Genes Dev. 15: 2520–2532.
   PubMed Web of Science ®Google Scholar
• Ema, M., K. Hirota, J. Mimura, H. Abe, J. Yodoi, K. Sogawa, L. Poellinger, and Y. Fujii-Kuriyama. 1999. Molecular mechanisms of transcription activation by HLF and HIF1α in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J. 18: 1905–1914.
   PubMed Web of Science ®Google Scholar
• Englund, C., A. E. Uv, R. Cantera, L. D. Mathies, M. A. Krasnow, and C. Samakovlis. 1999. adrift, a novel bnl-induced Drosophila gene, required for tracheal pathfinding into the Cns. Development 126: 1505–1514.
   PubMedGoogle Scholar
• Epstein, A. C., J. M. Gleadle, L. A. McNeill, K. S. Hewitson, J. O'Rourke, D. R. Mole, M. Mukherji, E. Metzen, M. I. Wilson, A. Dhanda, Y. M. Tian, N. Masson, D. L. Hamilton, P. Jaakkola, R. Barstead, J. Hodgkin, P. H. Maxwell, C. W. Pugh, C. J. Schofield, and P. J. Ratcliffe. 2001. Caenorhabditis elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43–54.
   PubMed Web of Science ®Google Scholar
• Firth, J. D., B. L. Ebert, and P. J. Ratcliffe. 1995. Hypoxic regulation of lactate dehydrogenase A: interaction between hypoxia-inducible factor 1 and cAMP response elements. J. Biol. Chem. 270: 21021–21027.
   PubMed Web of Science ®Google Scholar
• Haddad, G. G. 2000. Enhancing our understanding of the molecular responses to hypoxia in mammals using Drosophila melanogaster. J. Appl. Physiol. 88: 1481–1487.
   PubMedGoogle Scholar
• Hu, B., E. Wright, L. Campbell, and K. L. Blanchard. 1997. In vivo analysis of DNA-protein interactions on the human erythropoietin enhancer. Mol. Cell. Biol. 17: 851–856.
   PubMedGoogle Scholar
• Huang, L. E., J. Gu, M. Schau, and H. F. Bunn. 1998. Regulation of hypoxia-inducible factor 1α is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 95: 7987–7992.
   PubMed Web of Science ®Google Scholar
• Isaac, D. D., and D. J. Andrew. 1996. Tubulogenesis in Drosophila: a requirement for the trachealess gene product. Genes Dev. 10: 103–117.
   PubMed Web of Science ®Google Scholar
• Ivan, M., K. Kondo, H. Yang, W. Kim, J. Valiando, M. Ohh, A. Salic, J. M. Asara, W. S. Lane, and W. S. Kaelin, Jr. 2001. HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for oxygen sensing. Science 292: 464–468.
   PubMed Web of Science ®Google Scholar
• Iyer, N. V., L. E. Kotch, F. Agani, S. W. Leung, E. Laughner, R. H. Wenger, M. Gassmann, J. D. Gearhart, A. M. Lawler, A. Y. Yu, and G. L. Semenza. 1998. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12: 149–162.
   PubMed Web of Science ®Google Scholar
• Jaakkola, P., D. R. Mole, Y. M. Tian, M. I. Wilson, J. Gielbert, S. J. Gaskell, A. V. Kriegsheim, H. F. Heberstreit, M. Mukherji, C. J. Schofield, P. H. Maxwell, C. W. Pugh, and P. J. Ratcliffe. 2001. Targeting of HIF-alpha to the Von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468–472.
   PubMed Web of Science ®Google Scholar
• Jarecki, J., E. Johnson, and M. A. Krasnow. 1999. Oxygen regulation of airway branching in Drosophila is mediated by Branchless FGF. Cell 99: 211–220.
   PubMed Web of Science ®Google Scholar
• Jiang, B. H., J. Z. Zheng, S. W. Leung, R. Roe, and G. L. Semenza. 1997. Transactivation and inhibitory domains of hypoxia-inducible factor 1α: modulation of transcriptional activity by oxygen tension. J. Biol. Chem. 272: 19253–19260.
   PubMed Web of Science ®Google Scholar
• Kallio, P. J., K. Okamoto, S. O'Brien, P. Carrero, Y. Makino, H. Tanaka, and L. Poellinger. 1998. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1α. EMBO J. 17: 6573–6586.
   PubMed Web of Science ®Google Scholar
• Klagsbrun, M., D. Knighton, and J. Folkman. 1976. Tumor angiogenesis activity in cells grown in tissue culture. Cancer Res. 36: 110–114.
   PubMed Web of Science ®Google Scholar
• Klambt, C., L. Glazer, and B.-Z. Shilo. 1992. breathless, a Drosophila Fgf receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev. 6: 1668–1678.
   PubMed Web of Science ®Google Scholar
• Kozak, K. R., B. Abbott, and O. Hankinson. 1997. ARNT-deficient mice and placental differentiation. Dev. Biol. 191: 297–305.
   PubMed Web of Science ®Google Scholar
• Lando, D., D. J. Peet, D. A. Whelan, J. J. Gorman, and M. L. Whitelaw. 2002. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295: 858–861.
   PubMed Web of Science ®Google Scholar
• Luo, J. C., and M. Shibuya. 2001. A variant of nuclear localization signal of bipartite-type is required for the nuclear translocation of hypoxia-inducible factors (1α, 2α, and 3α). Oncogene 20: 1435–1444.
   PubMed Web of Science ®Google Scholar
• Maltepe, E., J. V. Schmidt, D. Baunoch, C. A. Bradfield, and M. C. Simon. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386: 403–407.
   PubMed Web of Science ®Google Scholar
• Manning, G., and M. A. Krasnow. 1993. Development of the Drosophila tracheal system, p. 609–685. In A. Martinez-Arias and M. Bate (ed.), The development of Drosophila melanogaster, vol. 1. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Masson, N., C. Willam, P. H. Maxwell, C. W. Pugh, and P. J. Ratcliffe. 2001. Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 20: 5197–5206.
   PubMed Web of Science ®Google Scholar
• Maxwell, P. H., C. W. Pugh, and P. J. Ratcliffe. 1993. Inducible operation of the erythropoietin 3′ enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism. Proc. Natl. Acad. Sci. USA 90: 2423–2427.
   PubMed Web of Science ®Google Scholar
• Maxwell, P. H., M. S. Wiesener, G. W. Chang, S. C. Clifford, E. C. Vaux, M. E. Cockman, C. C. Wykoff, C. W. Pugh, E. R. Maher, and P. J. Ratcliffe. 1999. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399: 271–275.
   PubMed Web of Science ®Google Scholar
• Metzger, R. J., and M. A. Krasnow. 1999. Genetic control of branching morphogenesis. Science 284: 1635–1639.
   PubMed Web of Science ®Google Scholar
• Nagao, M., B. L. Ebert, P. J. Ratcliffe, and C. W. Pugh. 1996. Drosophila melanogaster SL2 cells contain a hypoxically inducible DNA binding complex which recognizes mammalian HIF-binding sites. FEBS Lett. 387: 161–166.
   PubMed Web of Science ®Google Scholar
• Nambu, J. R., W. Chen, S. Hu, and S. T. Crews. 1996. The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1 alpha and Drosophila single-minded. Gene 172: 249–254.
   PubMedGoogle Scholar
• Pugh, C. W., J. F. O'Rourke, M. Nagao, J. M. Gleadle, and P. J. Ratcliffe. 1997. Activation of hypoxia-inducible factor-1: definition of regulatory domains within the alpha subunit. J. Biol. Chem. 272: 11205–11214.
   PubMed Web of Science ®Google Scholar
• Ryan, H. E., J. Lo, and R. S. Johnson. 1998. HIF-1 alpha is required for solid tumor formation and embryonic vascularization. EMBO J. 17: 3005–3015.
   PubMed Web of Science ®Google Scholar
• Shiga, Y., M. Tanaka-Matakatu, and S. Hayashi. 1996. A nuclear GFP/β-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differentiation 38: 99–106.
   Web of Science ®Google Scholar
• Shilo, B.-Z., L. Gabay, L. Glazer, M. Reichman-Fried, P. Wappner, R. Wilk, and E. Zelzer. 1997. Branching morphogenesis in the Drosophila tracheal system. Cold Spring Harbor Symp. Quant. Biol. 62: 241–247.
   Google Scholar
• Shweiki, D., A. Itin, D. Soffer, and E. Keshet. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359: 843–845.
   PubMed Web of Science ®Google Scholar
• Shweiki, D., M. Neeman, A. Itin, and E. Keshet. 1995. Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc. Natl. Acad. Sci. USA 92: 768–772.
   PubMed Web of Science ®Google Scholar
• Sonnenfeld, M., M. Ward, G. Nystrom, J. Mosher, S. Stahl, and S. Crews. 1997. The Drosophila tango gene encodes a bHLH-PAS protein that is orthologous to mammalian Arnt and controls CNS midline and tracheal development. Development 124: 4571–4582.
   PubMed Web of Science ®Google Scholar
• Sutherland, D., C. Samakovlis, and M. A. Krasnow. 1996. Branchless encodes a Drosophila Fgf homolog that controls tracheal cell migration and the pattern of branching. Cell 87: 1091–1101.
   PubMed Web of Science ®Google Scholar
• Taylor, M. S. 2001. Characterization and comparative analysis of the EGLN gene family. Gene 275: 125–132.
   PubMed Web of Science ®Google Scholar
• Wang, G. L., B. H. Jiang, E. A. Rue, and G. L. Semenza. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. USA 92: 5510–5514.
   PubMed Web of Science ®Google Scholar
• Wang, G. L., and G. L. Semenza. 1995. Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 270: 1230–1237.
   PubMed Web of Science ®Google Scholar
• Wappner, P., L. Gabay, and B.-Z. Shilo. 1997. Interactions between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 124: 4707–4716.
   PubMedGoogle Scholar
• Wappner, P., and P. J. Ratcliffe. 2001. Development of branched structures and the cellular response to hypoxia: an evolutionary perspective, p. 91–137. In G. G. Haddad and T. Xu (ed.), Genetic models in cardiorespiratory biology. Lung Biology in Health and Disease series, vol. 156. Marcel Dekker, Inc., New York, N.Y.
   Google Scholar
• Wilk, R., I. Weizman, and B.-Z. Shilo. 1996. Trachealess encodes a bHLH-PAS protein that is an inducer of tracheal cell fates in Drosophila. Genes Dev. 10: 93–102.
   PubMedGoogle Scholar
• Wingrove, J. A., and P. H. O'Farrell. 1999. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98: 105–114.
   PubMed Web of Science ®Google Scholar
• Wood, S. M., J. M. Gleadle, C. W. Pugh, O. Hankinson, and P. J. Ratcliffe. 1996. The role of the aryl hydrocarbon receptor nuclear translocator (ARNT) in hypoxic induction of gene expression. Studies in ARNT-deficient cells. J. Biol. Chem. 271: 15117–15123.
   PubMed Web of Science ®Google Scholar
• Zelzer, E., P. Wappner, and B. Z. Shilo. 1997. The PAS domain confers target gene specificity of Drosophila bHLH/PAS proteins. Genes Dev. 11: 2079–2089.
   PubMedGoogle Scholar
• Zwiebel, L. J., P. E. Hardin, X. Liu, J. C. Hall, and M. Rosbash. 1991. A posttranscriptional mechanism contributes to circadian cycling of a per-β-galactosidase fusion protein. Proc. Natl. Acad. Sci. USA 88: 3882–3886.
   PubMed Web of Science ®Google Scholar