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Abstract:

This past decade has brought considerable progress towards elucidating the molecular mechanisms of oxygen sensing pathways by which mammalian cells are able to detect and adjust, or succumb, to hypoxia. In contrast, far less is known about the protein and DNA constituents that endow many invertebrate species to withstand and recover from even more severe and prolonged O2 limitations. In spite of these differences in hypoxia tolerance, inadequacy in oxygen supply is, from mammals to insects to nematodes, signaled onto the DNA level predominantly by hypoxia-inducible factors (HIFs). Across the animal kingdom, HIF accumulates in hypoxic, but not normoxic, cells and functions in a remarkably conserved pathway. Using crustacean (Daphnia magna) and insect (Drosophila melanogaster) models, work by us and others has implicated HIF in restoring O2 delivery via stimulated hemoglobin synthesis (Daphnia) or tracheal remodeling (Drosophila). HIF is essential for these arthropods to adapt and survive during moderate O2 limitations. A similar life-preserving role for HIF-signaling in hypoxic, but not anoxic, environments had previously been established for another stress-tolerant invertebrate model, the nematode Caenorhabditis elegans. Exploring regulations of oxygen-dependent Daphnia and Drosophila genes in cell culture and in vivo have furthermore aided in uncovering novel HIF-targeting mechanisms that might operate to fine-tune the activity of this transcription factor under steadily hypoxic, rather than changing, oxygen tensions. We conclude our review with yet another addition to the growing list of HIF's many functions: the control of cellular growth during fly development. © 2006 Elsevier Ltd. All rights reserved.

Registro:

Documento: Artículo
Título:Sensing and responding to hypoxia via HIF in model invertebrates
Autor:Gorr, T.A.; Gassmann, M.; Wappner, P.
Filiación:Institute of Veterinary Physiology, Vetsuisse Faculty, Zurich Center for Integrative Human Physiology (ZIHP), Winterthurerstrasse 260, CH-8057 Zurich, Switzerland
Instituto Leloir, CONICET, Facultad de Ciencias Exactas y Naturales, Patricias Argentinas 435, Buenos Aires, 1405, Argentina
Palabras clave:Daphnia; Drosophila; Hypometabolism; Hypoxia-inducible factor; Tracheogenesis; basic helix loop helix transcription factor; oxygen; procollagen proline 2 oxoglutarate 4 dioxygenase; fly; hypoxia; invertebrate; mammal; oxygen; protein; animal; Caenorhabditis elegans; Daphnia; Drosophila melanogaster; genetics; growth, development and aging; invertebrate; mammal; physiology; review; signal transduction; Animals; Basic Helix-Loop-Helix Transcription Factors; Caenorhabditis elegans; Daphnia; Drosophila melanogaster; Invertebrates; Mammals; Oxygen; Procollagen-Proline Dioxygenase; Signal Transduction; Animalia; Arthropoda; Caenorhabditis elegans; Crustacea; Daphnia; Daphnia magna; Drosophila melanogaster; Hexapoda; Insecta; Invertebrata; Mammalia; Nematoda
Año:2006
Volumen:52
Número:4
Página de inicio:349
Página de fin:364
DOI: http://dx.doi.org/10.1016/j.jinsphys.2006.01.002
Título revista:Journal of Insect Physiology
Título revista abreviado:J. Insect Physiol.
ISSN:00221910
CODEN:JIPHA
CAS:oxygen, 7782-44-7; procollagen proline 2 oxoglutarate 4 dioxygenase, 9028-06-2; Basic Helix-Loop-Helix Transcription Factors; Oxygen, 7782-44-7; Procollagen-Proline Dioxygenase, EC 1.14.11.2
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00221910_v52_n4_p349_Gorr

Referencias:

  • Acker, T., Acker, H., Cellular oxygen sensing need in Cns function: physiological and pathological implications (2004) Journal of Experimental Biology, 207, pp. 3171-3188
  • Adelman, D.M., Gertsenstein, M., Nagy, A., Simon, M.C., Maltepe, E., Placental cell fates are regulated in vivo by Hif-mediated hypoxia responses (2000) Genes & Development, 14, pp. 3191-3203
  • Ameri, K., Lewis, C.E., Raida, M., Sowter, H., Hai, T., Harris, A.L., Anoxic induction of Atf-4 through Hif-1-independent pathways of protein stabilization in human cancer cells (2004) Blood, 103, pp. 1876-1882
  • An, W.G., Kanekal, M., Simon, M.C., Maltepe, E., Blagosklonny, M.V., Neckers, L.M., Stabilization of wild-type P53 by hypoxia-inducible factor 1alpha (1998) Nature, 392, pp. 405-408
  • Arquier, N., Vigne, P., Duplan, E., Hsu, T., Therond, P.P., Frelin, C., D'Angelo, G., Analysis of the hypoxia-sensing pathway in Drosophila melanogaster (2006) Biochemical Journal, 393, pp. 471-480
  • Bacon, N., Wappner, P., O'Rourke, J., Bartlett, S., Shilo, B., Pugh, C., Ratcliffe, P., Regulation of the Drosophila bHLH-PAS protein Sima by hypoxia: functional evidence for homology with mammalian Hif-1α (1998) Biochemical and Biophysical Research Communications, 249, pp. 811-816
  • Berra, E., Benizri, E., Ginouves, A., Volmat, V., Roux, D., Pouyssegur, J., Hif prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of Hif-1alpha in normoxia (2003) EMBO Journal, 22, pp. 4082-4090
  • Blanchard, K.L., Acquaviva, A.M., Galson, D.L., Bunn, H.F., Hypoxic induction of the human erythropoietin gene: cooperation between the promoter and enhancer, each of which contains steroid receptor response elements (1992) Molecular and Cellular Biology, 12, pp. 5373-5385
  • Bohni, R., Riesgo-Escovar, J., Oldham, S., Brogiolo, W., Stocker, H., Andruss, B.F., Beckingham, K., Hafen, E., Autonomous control of cell and organ size by chico, a Drosophila homolog of vertebrate irs1-4 (1999) Cell, 97, pp. 865-875
  • Boutilier, R., St-Pierre, J., Surviving hypoxia without really dying (2000) Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 126, pp. 481-490
  • Britton, J.S., Lockwood, W.K., Li, L., Cohen, S.M., Edgar, B.A., Drosophila's insulin/Pi3-kinase pathway coordinates cellular metabolism with nutritional conditions (2002) Developmental Cell, 2, pp. 239-249
  • Brugarolas, J., Lei, K., Hurley, R.L., Manning, B.D., Reiling, J.H., Hafen, E., Witters, L.A., Kaelin Jr., W.G., Regulation of mTOR function in response to hypoxia by Redd1 and the Tsc1/Tsc2 tumor suppressor complex (2004) Genes & Development, 18, pp. 2893-2904
  • Bruick, R., McKnight, S., A conserved family of prolyl-4-hydroxylases that modify Hif (2001) Science, 294, pp. 1337-1340
  • Buck, L., Land, S., Hochachka, P., Anoxia-tolerant hepatocytes: model system for study of reversible metabolic suppression (1993) American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 265, pp. R49-R56
  • Bunn, H., Poyton, R., Oxygen sensing and molecular adaptation to hypoxia (1996) Physiological Reviews, 76, pp. 839-885
  • Centanin, L., Ratcliffe, P.J., Wappner, P., Reversion of lethality and growth defects in fatiga oxygen-sensor mutant flies by loss of hypoxia-inducible factor-alpha/Sima (2005) EMBO Reports, 6, pp. 1070-1075
  • Chadwick, L., Gilmour, D., Respiration during flight in Drosophila Repleta Wollaston: the oxygen consumption considered in relation to the wing-rate (1940) Physiological Zoology, 13, pp. 398-410
  • Childress, J.J., The respiratory rates of midwater crustaceans as a function of depth of occurrence and relation to the oxygen minimum layer off Southern California (1975) Comparative Biochemistry and Physiology Part A: Physiology, 50, pp. 787-799
  • Covello, K.L., Simon, M.C., Hifs, hypoxia, and vascular development (2004) Current Topics in Developmental Biology, 62, pp. 37-54
  • Crews, S., Control of cell lineage-specific development and transcription by bHLH-PAS proteins (1998) Genes & Development, 12, pp. 607-620
  • Csik, L., The susceptibility to oxygen want of different Drosophila species (1939) Zeitschrift für vergleichende Physiologie, 27, pp. 304-310
  • Cummins, E.P., Taylor, C.T., Hypoxia-responsive transcription factors (2005) Pflügers Archiv European Journal of Physiology, 450, pp. 363-371
  • D'Angelo, G., Duplan, E., Boyer, N., Vigne, P., Frelin, C., Hypoxia up-regulates prolyl hydroxylase activity: a feedback mechanism that limits Hif-1 responses during reoxygenation (2003) Journal of Biological Chemistry, 278, pp. 38183-38187
  • Dekanty, A., Lavista-Llanos, S., Irisarri, M., Oldham, S., Wappner, P., The Insulin/Pi3k/Tor pathway induces a Hif-dependent transcriptional response in Drosophila by promoting nuclear localization of Hif-1alpha/Sima (2005) Journal of Cell Science, 118, pp. 5431-5441
  • del Peso, L., Castellanos, M.C., Temes, E., Martin-Puig, S., Cuevas, Y., Olmos, G., Landazuri, M.O., The von Hippel Lindau/hypoxia-inducible factor (Hif) pathway regulates the transcription of the Hif-proline hydroxylase genes in response to low oxygen (2003) Journal of Biological Chemistry, 278, pp. 48690-48695
  • DiGregorio, P.J., Ubersax, J.A., O'Farrell, P.H., Hypoxia and nitric oxide induce a rapid, reversible cell cycle arrest of the Drosophila syncytial divisions (2001) Journal of Biological Chemistry, 276, pp. 1930-1937
  • Douglas, R., Xu, T., Haddad, G., Cell cycle progression and cell division are sensitive to hypoxia in Drosophila melanogaster embryos (2001) American Journal of Physiology-Regulatory Integrative & Comparative Physiology, 280, pp. R1555-R1563
  • Drew, K.L., Harris, M.B., LaManna, J.C., Smith, M.A., Zhu, X.W., Ma, Y.L., Hypoxia tolerance in mammalian heterotherms (2004) Journal of Experimental Biology, 207, pp. 3155-3162
  • Duffy, T.E., Nelson, S.R., Lowry, O.H., Cerebral carbohydrate metabolism during acute hypoxia and recovery (1972) Journal of Neurochemistry, 19, pp. 959-977
  • Ebbesen, P., Eckardt, K.U., Ciampor, F., Pettersen, E.O., Linking measured intercellular oxygen concentration to human cell functions (2004) Acta Oncologica, 43, pp. 598-600
  • Ebert, B., Bunn, H., Regulation of the erythropoietin gene (1999) Blood, 94, pp. 1864-1877
  • Emmons, R., Duncan, D., Estes, P., Kiefel, P., Mosher, J., Sonnenfeld, K., Ward, M., Crews, S., The spinless-aristapedia and Tango bHLH-PAS proteins interact to control antennal and tarsal development in Drosophila (1999) Development, 126, pp. 3937-3945
  • Epstein, A., Gleadle, J., McNeill, L., Hewiston, K., O'Rourke, J., Mole, D., Mukherji, M., Ratcliffe, P., C. elegans Egl-9 and mammalian homologs define a family of dioxygenases that regulate Hif by prolyl hydroxylation (2001) Cell, 107, pp. 43-54
  • Erecinska, M., Silver, I.A., Tissue oxygen tension and brain sensitivity to hypoxia (2001) Respiration Physiology, 128, pp. 263-276
  • Firth, J.D., Ebert, B.L., Ratcliffe, P.J., Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and camp response elements (1995) Journal of Biological Chemistry, 270, pp. 21021-21027
  • Foe, V., Alberts, B., Reversible chromosome condensation induced in Drosophila embryos by anoxia: visualization of interphase nuclear organization (1985) The Journal of Cell Biology, 100, pp. 1623-1636
  • Frazier, M.R., Woods, H.A., Harrison, J.F., Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster (2001) Physiological and Biochemical Zoology, 74, pp. 641-650
  • Frei, C., Cyclin D/Cdk4: new insights from Drosophila (2004) Cell Cycle, 3, pp. 558-560
  • Frei, C., Edgar, B.A., Drosophila Cyclin D/Cdk4 requires Hif-1 prolyl hydroxylase to drive cell growth (2004) Developmental Cell, 6, pp. 241-251
  • Ghabrial, A., Luschnig, S., Metzstein, M.M., Krasnow, M.A., Branching morphogenesis of the Drosophila tracheal system (2003) Annual Review of Cell and Developmental Biology, 19, pp. 623-647
  • Goldberg, M.A., Dunning, S.P., Bunn, H.F., Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein (1988) Science, 242, pp. 1412-1415
  • Gorr, T., Cahn, J., Hradecky, P., Bunn, H.F., Genome-wide computational screen for candidate Hif target genes in Drosophila melanogaster and Caenorhabditis elegans (2003) Oxygen Sensing-Responses and Adaptation to Hypoxia, 175, pp. 175-199. , Lahiri S., Semenza G., and Prabhakar N. (Eds), Marcel Dekker, New York
  • Gorr, T., Cahn, J., Yamagata, H., Bunn, H., Hypoxia-induced synthesis of hemoglobin in the crustacean Daphnia magna is hypoxia-inducible factor-dependent (2004) Journal of Biological Chemistry, 279, pp. 36038-36047
  • Gorr, T., Tomita, T., Wappner, P., Bunn, H., Regulation of Drosophila hypoxia-inducible factor (Hif) activity in Sl2 cells-identification of a hypoxia-induced variant isoform of the Hifα homolog gene similar (2004) Journal of Biological Chemistry, 279, pp. 36048-36058
  • Graven, K.K., Bellur, D., Klahn, B.D., Lowrey, S.L., Amberger, E., Hif-2alpha regulates glyceraldehyde-3-phosphate dehydrogenase expression in endothelial cells (2003) Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression, 1626, pp. 10-18
  • Grieshaber, M., Hardewig, I., Kreutzer, U., Pörtner, H.-O., Physiological and metabolic responses to hypoxia in invertebrates (1994) Reviews of Physiology, Biochemistry and Pharmacology, 125, pp. 43-147
  • Guillemin, K., Krasnow, M., The hypoxic response: huffing and hifing (1997) Cell, 89, pp. 9-12
  • Guppy, M., Withers, P., Metabolic depression in animals: physiological perspectives and biochemical generalizations (1999) Biological Reviews, 74, pp. 1-40
  • Hansen, A.J., Effect of anoxia on ion distribution in the brain (1985) Physiological Reviews, 65, pp. 101-148
  • Harris, A.L., Hypoxia-a key regulatory factor in tumour growth (2002) Nature Reviews Cancer, 2, pp. 38-47
  • Heldmaier, G., Ortmann, S., Elvert, R., Natural hypometabolism during hibernation and daily torpor in mammals (2004) Respiratory Physiology & Neurobiology, 141, pp. 317-329
  • Hirsilä, M., Koivunen, P., Günzler, V., Kivirikko, K.I., Myllyharju, J., Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor (2003) Journal of Biological Chemistry, 278, pp. 30772-30780
  • Hoback, W.W., Stanley, D.W., Insects in hypoxia (2001) Journal of Insect Physiology, 47, pp. 533-542
  • Hochachka, P., Metabolic arrest (1986) Intensive Care Medicine, 12, pp. 127-133
  • Hochachka, P.W., Defense strategies against hypoxia and hypothermia (1986) Science, 231, pp. 234-241
  • Hochachka, P., Buck, L., Doll, C., Land, S., Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack (1996) Proceedings of the National Academy of Sciences of the United States of America, 93, pp. 9493-9498
  • Hochachka, P.W., Somero, G.N., (2002) Biochemical adaptation-Mechanism and process in physiological evolution, , Oxford University Press, New York
  • Höpfl, G., Ogunshola, O., Gassmann, M., Hifs and tumors-causes and consequences (2004) American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 286, pp. R608-R623
  • Huang, L., Arany, Z., Livingston, D., Bunn, H., Activation of hypoxia-inducible transcription factor depends primarily upon redox sensitive stabilization of its α subunit (1996) Journal of Biological Chemistry, 271, pp. 32253-32259
  • Huang, L., Gu, J., Schau, M., Bunn, H., Regulation of hypoxia-inducible factor 1α is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway (1998) Proceedings of the National Academy of Sciences of the United States of America, 95, pp. 7987-7992
  • Huang, L.E., Bunn, H.F., Hypoxia-inducible factor and its biomedical relevance (2003) Journal of Biological Chemistry, 278, pp. 19575-19578
  • Isaac, D.D., Andrew, D.J., Tubulogenesis in Drosophila: a requirement for the trachealess gene product (1996) Genes & Development, 10, pp. 103-117
  • Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Kaelin Jr., W.G., Hifalpha targeted for Vhl-mediated destruction by proline hydroxylation: implications for O2 sensing (2001) Science, 292, pp. 464-468
  • Iyer, N., Kotch, L., Agani, F., Leung, S., Laughner, E., Wenger, R., Gassmann, M., Semenza, G., Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1α (1998) Genes & Development, 12, pp. 149-162
  • Jaakkola, P., Mole, D.R., Tian, Y.M., Wilson, M.I., Gielbert, J., Gaskell, S.J., Kriegsheim, A., Ratcliffe, P.J., Targeting of Hif-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation (2001) Science, 292, pp. 468-472
  • Jaeschke, H., Smith, C.V., Mitchell, J.R., Hypoxic damage generates reactive oxygen species in isolated perfused rat liver (1988) Biochemical and Biophysical Research Communications, 150, pp. 568-574
  • Jarecki, J., Johnson, E., Krasnow, M., Oxygen regulation of airway branching in Drosophila is mediated by branchless Fgf (1999) Cell, 99, pp. 211-220
  • Jewell, U.R., Kvietikova, I., Scheid, A., Bauer, C., Wenger, R.H., Gassmann, M., Induction of Hif-1alpha in response to hypoxia is instantaneous (2001) FASEB Journal, 15, pp. 1312-1314
  • Jiang, B.H., Semenza, G.L., Bauer, C., Marti, H.H., Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension (1996) American Journal of Physiology-Cell Physiology, 271, pp. C1172-C1180
  • Jiang, H., Guo, R., Powell-Coffman, J., The Caenorhabditis elegans Hif-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia (2001) Proceedings of the National Academy of Sciences of the United States of America, 14, pp. 7916-7921
  • Jiang, L., Crews, S.T., The Drosophila dysfusion basic helix-loop-helix (bHLH)-PAS gene controls tracheal function and levels of the trachealess bHLH-PAS protein (2003) Molecular and Cellular Biology, 23, pp. 5625-5637
  • Keister, M., Buck, J., Respiration: some exogenous and endogenous effects on rate of respiration (1974) The Physiology of Insecta, 6, pp. 469-509. , Rockstein M. (Ed), Academic Press, New York
  • Kobayashi, M., Hoshi, T., Relationship between the haemoglobin concentration of Daphnia magna and the ambient oxygen concentration (1982) Comparative Biochemistry and Physiology Part A: Physiology, 72, pp. 247-249
  • Koivunen, P., Hirsilä, M., Günzler, V., Kivirikko, K.I., Myllyharju, J., Catalytic properties of the asparaginyl hydroxylase (Fih) in the oxygen sensing pathway are distinct from those of its prolyl 4-hydroxylases (2004) Journal of Biological Chemistry, 279, pp. 9899-9904
  • Krishnan, S., Sun, Y.-A., Mohsenin, A., Wyman, R., Haddad, G., Behavioral and electrophysiologic responses of Drosophila melanogaster to prolonged periods of anoxia (1997) Journal of Insect Physiology, 43, pp. 203-210
  • Land, S., Buck, L., Hochachka, P., Response of protein synthesis to anoxia and recovery in anoxia-tolerant hepatocytes (1993) American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 265, pp. R41-R48
  • Land, S., Hochachka, P., Protein turnover during metabolic arrest in turtle hepatocytes: role and energy dependence of proteolysis (1994) American Journal of Physiology-Cell Physiology, 266, pp. C1028-C1036
  • Lando, D., Peet, D.J., Gorman, J.J., Whelan, D.A., Whitelaw, M.L., Bruick, R.K., Fih-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor (2002) Genes & Development, 16, pp. 1466-1471
  • Lando, D., Peet, D.J., Whelan, D.A., Gorman, J.J., Whitelaw, M.L., Asparagine hydroxylation of the Hif transactivation domain a hypoxic switch (2002) Science, 295, pp. 858-861
  • Lando, D., Gorman, J.J., Whitelaw, M.L., Peet, D.J., Oxygen-dependent regulation of hypoxia-inducible factors by prolyl and asparaginyl hydroxylation (2003) European Journal of Biochemistry, 270, pp. 781-790
  • Lavista-Llanos, S., Centanin, L., Irisarri, M., Russo, D.M., Gleadle, J.M., Bocca, S.N., Muzzopappa, M., Wappner, P., Control of the hypoxic response in Drosophila melanogaster by the basic helix-loop-helix PAS protein similar (2002) Molecular & Cellular Biology, 22, pp. 6842-6853
  • Levy, A.P., Levy, N.S., Wegner, S., Goldberg, M.A., Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia (1995) Journal of Biological Chemistry, 270, pp. 13333-13340
  • Locke, M., The co-ordination of growth in the tracheal system of insects (1958) Quarterly Journal of Microscopic Science, 99, pp. 373-391
  • Loudon, C., Development of Tenebrio molitor in low oxygen levels (1988) Journal of Insect Physiology, 34, pp. 97-103
  • Ma, E., Haddad, G., Isolation and Characterization of the hypoxia-inducible factor 1β in Drosophila melanogaster (1999) Molecular Brain Research, 73, pp. 11-16
  • Ma, E., Xu, T., Haddad, G., Gene regulation by O2 deprivation: an anoxia-regulated novel gene in Drosophila melanogaster (1999) Molecular Brain Research, 63, pp. 217-224
  • Makino, Y., Cao, R., Svensson, K., Bertilsson, G., Asman, M., Tanaka, H., Cao, Y., Poellinger, L., Inhibitory PAS domain protein is a negative regulator of hypoxia-inducible gene expression (2001) Nature, 414, pp. 550-554
  • Makino, Y., Kanopka, A., Wilson, W.J., Tanaka, H., Poellinger, L., Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor 3 alpha locus (2002) Journal of Biological Chemistry, 272, pp. 32405-32408
  • Manalo, D.J., Rowan, A., Lavoie, T., Natarajan, L., Kelly, B.D., Ye, S.Q., Garcia, J.G., Semenza, G.L., Transcriptional regulation of vascular endothelial cell responses to hypoxia by Hif-1 (2005) Blood, 105, pp. 659-669
  • Marxsen, J.H., Stengel, P., Doege, K., Heikkinen, P., Jokilehto, T., Wagner, T., Jelkmann, W., Metzen, E., Hypoxia-inducible factor-1 (Hif-1) promotes its degradation by induction of Hif-alpha-prolyl-4-hydroxylases (2004) Biochemical Journal, 381, pp. 761-767
  • Masson, N., Willam, C., Maxwell, P.H., Pugh, C.W., Ratcliffe, P.J., Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation (2001) EMBO Journal, 20, pp. 5197-5206
  • Maxwell, P., Salnikow, K., Hif-1: an oxygen and metal responsive transcription factor (2004) Cancer Biology & Therapy, 3, pp. 29-35
  • Maxwell, P., Pugh, C., Ratcliffe, P., Inducible operation of the erythropoietin 3' enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism (1993) Proceedings of the National Academy of Sciences of the United States of America, 90, pp. 2423-2427
  • Maxwell, P., Wiesener, M., Chang, G., Clifford, S., Vaux, E., Cockman, M., Wykoff, C., Ratcliffe, P., The tumour suppressor protein Vhl targets hypoxia-inducible factors for oxygen-dependent proteolysis (1999) Nature, 399, pp. 271-275
  • McMahon, B.R., Respiratory and circulatory compensation to hypoxia in crustaceans (2001) Respiration Physiology, 128, pp. 349-364
  • Metzger, R., Krasnow, M., Genetic control of branching morphogenesis (1999) Science, 284, pp. 1635-1639
  • Morin Jr., P., McMullen, D.C., Storey, K.B., Hif-1alpha involvement in low temperature and anoxia survival by a freeze tolerant Insect (2005) Molecular and Cellular Biochemistry, 280, pp. 99-106
  • Mortola, J.P., Implications of hypoxic hypometabolism during mammalian ontogenesis (2004) Respiratory Physiology & Neurobiology, 141, pp. 345-356
  • Murphy, B.J., Regulation of malignant progression by the hypoxia-sensitive transcription factors Hif-1alpha and Mtf-1 (2004) Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 139, pp. 495-507
  • Nagao, M., Ebert, B., Ratcliffe, P., Pugh, C., Drosophila melanogaster Sl2 cells contain a hypoxically inducible DNA binding complex which recognises mammalian Hif-1 binding sites (1996) FEBS Letters, 387, pp. 161-166
  • Nambu, J.R., Lewis, J.O., Wharton Jr., K.A., Crews, S.T., The Drosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of Cns midline development (1991) Cell, 67, pp. 1157-1167
  • Nambu, J., Chen, W., Hu, S., Crews, S., The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1α and Drosophila single-minded (1996) Gene, 172, pp. 249-254
  • Nikinmaa, M., Rees, B.B., Oxygen-dependent gene expression in fishes (2005) American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 288, pp. R1079-R1090
  • Nikinmaa, M., Pursiheimo, S., Soitamo, A.J., Redox state regulates Hif-1alpha and its DNA binding and phosphorylation in salmonid cells (2004) Journal of Cell Science, 117, pp. 3201-3206
  • Ohshiro, T., Saigo, K., Transcriptional regulation of breathless Fgf receptor gene by binding of trachealess/darnt heterodimers to three central midline elements in Drosophila developing trachea (1997) Development, 124, pp. 3975-3986
  • Oldham, S., Hafen, E., Insulin/Igf and target of rapamycin signaling: a Tor de force in growth control (2003) Trends in Cell Biology, 13, pp. 79-85
  • Padilla, P.A., Nystul, T.G., Zager, R.A., Johnson, A.C., Roth, M.B., Dephosphorylation of cell cycle-regulated proteins correlates with anoxia-induced suspended animation in Caenorhabditis elegans (2002) Molecular Biology of the Cell, 13, pp. 1473-1483
  • Paul, R.J., Colmorgen, M., Hüller, S., Tyroller, F., Zinkler, D., Circulation and respiratory control in millimetre-sized animals (Daphnia magna, Folsomia candida) studied by optical methods (1997) Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology, 167, pp. 399-408
  • Paul, R., Colmorgen, M., Pirow, R., Chen, Y.-H., Tsai, M.-C., Systemic and metabolic responses in Daphnia magna to anoxia (1998) Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 120, pp. 519-530
  • Pfander, D., Kobayashi, T., Knight, M.C., Zelzer, E., Chan, D.A., Olsen, B.R., Giaccia, A.J., Schipani, E., Deletion of Vhlh in chondrocytes reduces cell proliferation and increases matrix deposition during growth plate development (2004) Development, 131, pp. 2497-2508
  • Pirow, R., Bäumer, C., Paul, R.J., Benefits of heamoglobin in the Cladoceran custacean Daphnia magna (2001) Journal of Experimental Biology, 204, pp. 3425-3441
  • Powell-Coffman, J., Bradfield, C., Wood, W., Caenorhabditis elegans orthologs of the aryl hydrocarbon receptor and its heterodimers partner the aryl hydrocarbon receptor nuclear translocator (1998) Proceedings of the National Academy of Sciences of the United States of America, 95, pp. 2844-2849
  • Pugh, C.W., Ratcliffe, P.J., Regulation of angiogenesis by hypoxia: role of the Hif system (2003) Nature Medicine, 9, pp. 677-684
  • Reiling, J.H., Hafen, E., The hypoxia-induced paralogs scylla and charybdis inhibit growth by down-regulating S6k activity upstream of Tsc in Drosophila (2004) Genes & Development, 18, pp. 2879-2892
  • Ribeiro, C., Petit, V., Affolter, M., Signaling systems, guided cell migration, and organogenesis: insights from genetic studies in Drosophila (2003) Developmental Biology, 260, pp. 1-8
  • Rolfe, D., Brown, G., Cellular energy utilization and molecular origin of standard metabolic rate in mammals (1997) Physiological Reviews, 77, pp. 731-758
  • Rosenberger, C., Heyman, S.N., Rosen, S., Shina, A., Goldfarb, M., Griethe, W., Frei, U., Eckardt, K.U., Up-regulation of Hif in experimental acute renal failure: evidence for a protective transcriptional response to hypoxia (2005) Kidney International, 67, pp. 531-542
  • Salceda, S., Caro, J., Hypoxia-inducible factor 1α (Hif-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions (1997) Journal of Biological Chemistry, 272, pp. 22642-22647
  • Samakovlis, C., Hacohen, N., Manning, G., Sutherland, D.C., Guillemin, K., Krasnow, M.A., Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events (1996) Development, 122, pp. 1395-1407
  • Schmidt, H., Kamp, G., The Pasteur effect in facultative anaerobic metazoa (1996) Experientia, 52, pp. 440-448
  • Schmitz, A., Harrison, J.F., Hypoxic tolerance in air-breathing invertebrates (2004) Respiratory Physiology & Neurobiology, 141, pp. 229-242
  • Schneider, I., Cell lines derived from late embryonic stages of Drosophila melanogaster (1972) Journal of Embryology and Experimental Morphology, 27, pp. 353-365
  • Schofield, C.J., Ratcliffe, P.J., Oxygen sensing by Hif hydroxylases (2004) Nature Reviews Molecular Cell Biology, 5, pp. 343-354
  • Scholz, F., Zerbst-Boroffka, I., Environmental hypoxia affects osmotic and ionic regulation in freshwater midge-larvae (1998) Journal of Insect Physiology, 44, pp. 427-436
  • Seagroves, T., Ryan, H., Lu, H., Wouters, B., Knapp, M., Thibault, P., Laderoute, K., Johnson, R., Transcription factor Hif-1 is a necessary mediator of the Pasteur effect in mammalian cells (2001) Molecular and Cellular Biology, 21, pp. 3436-3444
  • Semenza, G., Regulation of mammalian O2 homeostasis by hypoxia-inducible factor 1 (1999) Annual Review of Cell and Developmental Biology, 15, pp. 551-578
  • Semenza, G.L., Hif-1 and tumor progression: pathophysiology and therapeutics (2002) Trends in Molecular Medicine, 8, pp. S62-S67
  • Semenza, G.L., Targeting Hif-1 for cancer therapy (2003) Nature Reviews Cancer, 3, pp. 721-732
  • Semenza, G.L., Wang, G.L., 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 (1992) Molecular and Cellular Biology, 12, pp. 5447-5454
  • Shen, C., Powell-Coffman, J.A., Genetic analysis of hypoxia signaling and response in C. elegans (2003) Annals of the New York Academy of Sciences, 995, pp. 191-199
  • Shen, C., Nettleton, D., Jiang, M., Kim, S.K., Powell-Coffman, J.A., Roles of the Hif-1 hypoxia-inducible factor during hypoxia response in Caenorhabditis elegans (2005) Journal of Biological Chemistry, 280, pp. 20580-20588
  • Shweiki, D., Itin, A., Soffer, D., Keshet, E., Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis (1992) Nature, 359, pp. 843-845
  • Shweiki, D., Neeman, M., Itin, A., Keshet, E., Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis (1995) Proceedings of the National Academy of Sciences of the United States of America, 92, pp. 768-772
  • Singer, D., Neonatal tolerance to hypoxia: a comparative-physiological approach (1999) Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 123, pp. 221-234
  • Sonnenfeld, M., Ward, M., Nystrom, G., Mosher, J., Stahl, S., Crews, S., The Drosophila Tange gene encodes a bHLH-PAS protein that is orthologous to mammalian arnt and controls Cns midline and tracheal development (1997) Development, 124, pp. 4571-4582
  • Srinivas, V., Zhang, L., Zhu, X., Caro, J., Characterization of an oxygen/redox-dependent degradation domain of hypoxia-inducible factor α (Hif-α) proteins (1999) Biochemical and Biophysical Research Communications, 260, pp. 557-561
  • Stolze, I.P., Tian, Y.M., Appelhoff, R.J., Turley, H., Wykoff, C.C., Gleadle, J.M., Ratcliffe, P.J., Genetic analysis of the role of the asparaginyl hydroxylase factor inhibiting hypoxia-inducible factor (Hif) in regulating Hif transcriptional target genes (2004) Journal of Biological Chemistry, 279, pp. 42719-42725
  • Storey, K., A re-evaluation of the pasteur effect: new mechanisms in anaerobic metabolism (1985) Molecular Physiology, 8, pp. 439-461
  • Suarez, R., Doll, C., Buie, A., West, T., Funk, G., Hochachka, P., Turtles and rats: a biochemical comparison of anoxia-tolerant and anoxia-sensitive brains (1989) American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 257, pp. R1083-R1088
  • Sutherland, S., Samakovlis, Krasnow, M., Branchless encodes a Drosophila Fgf homolog that controls tracheal cell migration and the pattern of branching (1996) Cell, 87, pp. 1091-1101
  • Taylor, B., Zhulin, I., PAS domains: internal sensors of oxygen, redox potential, and light (1999) Microbiology and Molecular Biology Reviews, 63, pp. 479-506
  • Tomita, S., Ueno, M., Sakamoto, M., Kitahama, Y., Ueki, M., Maekawa, N., Sakamoto, H., Takahama, Y., Defective brain development in mice lacking the Hif-1alpha gene in neural cells (2003) Molecular and Cellular Biology, 23, pp. 6739-6749
  • Vaupel, P., The role of hypoxia-induced factors in tumor progression (2004) Oncologist, 9 (SUPPL. 5), pp. 10-17
  • Vogelstein, B., Kinzler, K.W., Cancer genes and the pathways they control (2004) Nature Medicine, 10, pp. 789-799
  • Vuori, K.A., Soitamo, A., Vuorinen, P.J., Nikinmaa, M., Baltic Salmon (Salmo Salar) Yolk-Sac Fry mortality is associated with disturbances in the function of hypoxia-inducible transcription factor (Hif-1alpha) and consecutive gene expression (2004) Aquatic Toxicology, 68, pp. 301-313
  • Wang, G.L., Semenza, G.L., General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia (1993) Proceedings of the National Academy of Sciences of the United States of America, 90, pp. 4304-4308
  • Wang, G., Semenza, G., Purification and characterization of hypoxia-inducible factor 1 (1995) Journal of Biological Chemistry, 270, pp. 1230-1237
  • Wang, G., Jiang, B., Rue, E., Semenza, G., Hypoxia-inducible factor 1 is a basic helix-loop-helix-Pas heterodimer regulated by cellular O2 tension (1995) Proceedings of the National Academy of Sciences of the United States of America, 92, pp. 5510-5514
  • Wappner, P., Ratcliffe, P., Development of branched structures and the cellular response to hypoxia-an evolutionary perspective (2001) Genetic Models in Cardiorespiratory Biology, pp. 91-138. , Haddad G., and Xu T. (Eds), Marcel Dekker Inc., New York
  • Ward, M., Mosher, J., Crews, S., Regulation of bHLH-PAS protein subcellular localization during Drosophila embryogenesis (1998) Development, 125, pp. 1599-1608
  • Webster, K., Evolution of the coordinate regulation of glycolytic enzyme genes by hypoxia (2003) Journal of Experimental Biology, 206, pp. 2911-2922
  • Webster, K.A., Regulation of glycolytic enzyme Rna transcriptional rates by oxygen availability in skeletal muscle cells (1987) Molecular and Cellular Biochemistry, 77, pp. 19-28
  • Wegener, G., Oxygen availability, energy metabolism and metabolic rate in invertebrates and vertebrates (1988) Oxygen Sensing in Tissues, pp. 13-35. , Acker H. (Ed), Springer, Berlin
  • Wegener, G., Hypoxia and posthypoxic recovery in insects: physiological and metabolic aspects (1993) Surviving Hypoxia: Mechanisms of Control and Adaptation, pp. 417-434. , Hochachka P., Lutz P., Sick T., Rosenthal M., and Thillart G.V.D. (Eds), CRC Press, Boca Raton, FL
  • Wenger, R., Gassmann, M., Oxygen(es) and the hypoxia-inducible factor-1 (1997) Biological Chemistry, 378, pp. 1-8
  • Wenger, R.H., Camenisch, G., Desbaillets, I., Chilov, D., Gassmann, M., Up-regulation of hypoxia-inducible factor-1alpha is not sufficient for hypoxic/anoxic P53 induction (1998) Cancer Research, 58, pp. 5678-5680
  • Wenger, R.H., Stiehl, D.P., Camenisch, G., Integration of oxygen signaling at the consensus HRE (2005) Science STKE 2005, 306. , p. re12
  • Wiesener, M.S., Turley, H., Allen, W.E., Willam, C., Eckardt, K.U., Talks, K.L., Wood, S.M., Maxwell, P.H., Induction of endothelial Pas domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha (1998) Blood, 92, pp. 2260-2268
  • Wigglesworth, V., Growth and regeneration in the tracheal system of an insect, Rhodnius Prolixus (Hemiptera) (1954) Quarterly Journal of Microscopical Science, 95, pp. 115-137
  • Wigglesworth, V., The physiology of tracheoles (1983) Advances in Insect Physiology, 17, pp. 86-148
  • Wilk, R., Weizman, I., Shilo, B., Trachealess encodes bHLH-PAS protein that is an inducer of tracheal cell fates in Drosophila (1996) Genes & Development, 10, pp. 93-102
  • Wingrove, J., O'Farrell, P., Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila (1999) Cell, 98, pp. 105-114
  • Zelzer, E., Wappner, P., Shilo, B., The PAS domain confers target gene specificity of Drososphila bHLH-PAS proteins (1997) Genes & Development, 11, pp. 2079-2089

Citas:

---------- APA ----------
Gorr, T.A., Gassmann, M. & Wappner, P. (2006) . Sensing and responding to hypoxia via HIF in model invertebrates. Journal of Insect Physiology, 52(4), 349-364.
http://dx.doi.org/10.1016/j.jinsphys.2006.01.002
---------- CHICAGO ----------
Gorr, T.A., Gassmann, M., Wappner, P. "Sensing and responding to hypoxia via HIF in model invertebrates" . Journal of Insect Physiology 52, no. 4 (2006) : 349-364.
http://dx.doi.org/10.1016/j.jinsphys.2006.01.002
---------- MLA ----------
Gorr, T.A., Gassmann, M., Wappner, P. "Sensing and responding to hypoxia via HIF in model invertebrates" . Journal of Insect Physiology, vol. 52, no. 4, 2006, pp. 349-364.
http://dx.doi.org/10.1016/j.jinsphys.2006.01.002
---------- VANCOUVER ----------
Gorr, T.A., Gassmann, M., Wappner, P. Sensing and responding to hypoxia via HIF in model invertebrates. J. Insect Physiol. 2006;52(4):349-364.
http://dx.doi.org/10.1016/j.jinsphys.2006.01.002