Oxygen sensing in Drosophila: Multiple isoforms of the prolyl hydroxylase fatiga have different capacity to regulate HIFαSima

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Acevedo, Julieta M ^a,c   Centanin, Lazaro ^a   Dekanty, Andrés ^a   Wappner, Pablo ^a,b,c  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; OXYGENASE; POLYHISTIDINE TAG; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROLYL 4 HYDROXYLASE 1; PROLYL 4 HYDROXYLASE 2; PROLYL 4 HYDROXYLASE 3; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; ISOENZYME; MESSENGER RNA; OXYGEN; SIMA PROTEIN, DROSOPHILA;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CELL HYPOXIA; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE EXPRESSION REGULATION; GENE LOCUS; GENE OVEREXPRESSION; IMAGO; IN VIVO STUDY; INSECT CELL CULTURE; INTRON; LOSS OF FUNCTION MUTATION; MOLECULAR DYNAMICS; NONHUMAN; OXYGEN SENSING; PHENOTYPIC VARIATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; TRANSCRIPTION INITIATION SITE; TRANSGENICS; ANIMAL; ANOXIA; CHEMISTRY; DNA RESPONSIVE ELEMENT; DROSOPHILA MELANOGASTER; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; LIFE CYCLE; METABOLISM; PROTEIN TERTIARY STRUCTURE; UPREGULATION;

MAMMALIA;

ALTERNATIVE SPLICING; ANIMALS; ANOXIA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENETIC LOCI; HUMANS; ISOENZYMES; LIFE CYCLE STAGES; OXYGEN; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN STRUCTURE, TERTIARY; RESPONSE ELEMENTS; RNA, MESSENGER; UP-REGULATION;

EID: 77957865802     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012390     Document Type: Article

References (31)

1. Wang GL, Jiang BH, Rue EA, Semenza GL (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A 92: 5510-5514.
2. Bruick RK (2003) Oxygen sensing in the hypoxic response pathway: regulation of the hypoxia-inducible transcription factor. Genes Dev 17: 2614-2623.
3. Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5: 343-354.
4. Semenza GL (2001) HIF-1, O(2), and the 3 PHDs: how animal cells signal hypoxia to the nucleus. Cell 107: 1-3.
5. Ivan M, Kondo K, Yang H, Kim W, Valiando J, et al. (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292: 464-468.
6. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, et al. (2001) Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292: 468-472.
7. Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294: 1337-1340.
8. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, et al. (2001) C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54.
9. Kallio PJ, Okamoto K, O'Brien S, Carrero P, Makino Y, et al. (1998) Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J 17: 6573-6586.
10. Maxwell PH, Pugh CW, Ratcliffe PJ (1993) Inducible operation of the erythropoietin 39 enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism. Proc Natl Acad Sci U S A 90: 2423-2427.
11. Wang GL, Semenza GL (1993) General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci U S A 90: 4304-4308.
12. Wenger RH, Stiehl DP, Camenisch G (2005) Integration of oxygen signaling at the consensus HRE. Sci STKE 2005: re12.
13. Appelhoff RJ, Tian YM, Raval RR, Turley H, Harris AL, et al. (2004) Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 279: 38458-38465.
14. Metzen E, Berchner-Pfannschmidt U, Stengel P, Marxsen JH, Stolze I, et al. (2003) Intracellular localisation of human HIF-1 alpha hydroxylases: implications for oxygen sensing. J Cell Sci 116: 1319-1326.
15. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, et al. (2003) HIF prolylhydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia. EMBO J 22: 4082-4090.
16. Fong GH, Takeda K (2008) Role and regulation of prolyl hydroxylase domain proteins. Cell Death Differ 15: 635-641.
17. Takeda K, Aguila HL, Parikh NS, Li X, Lamothe K, et al. (2008) Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood 111: 3229-3235.
18. Aragones J, Schneider M, Van Geyte K, Fraisl P, Dresselaers T, et al. (2008) Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat Genet 40: 170-180.
19. Lavista-Llanos S, Centanin L, Irisarri M, Russo DM, Gleadle JM, et al. (2002) Control of the hypoxic response in Drosophila melanogaster by the basic helixloop-helix PAS protein similar. Mol Cell Biol 22: 6842-6853.
20. Centanin L, Ratcliffe PJ, Wappner P (2005) Reversion of lethality and growth defects in Fatiga oxygen-sensor mutant flies by loss of hypoxia-inducible factoralpha/Sima. EMBO Rep 6: 1070-1075.
21. Centanin L, Dekanty A, Romero N, Irisarri M, Gorr TA, et al. (2008) Cell autonomy of HIF effects in Drosophila: tracheal cells sense hypoxia and induce terminal branch sprouting. Dev Cell 14: 547-558.
22. Frei C, Edgar BA (2004) Drosophila cyclin D/Cdk4 requires Hif-1 prolyl hydroxylase to drive cell growth. Dev Cell 6: 241-251.
23. Pescador N, Cuevas Y, Naranjo S, Alcaide M, Villar D, et al. (2005) Identification of a functional hypoxia-responsive element that regulates the expression of the egl nine homologue 3 (egln3/phd3) gene. Biochem J 390: 189-197.
24. Choi KO, Lee T, Lee N, Kim JH, Yang EG, et al. (2005) Inhibition of the catalytic activity of hypoxia-inducible factor-1alpha-prolyl-hydroxylase 2 by a MYND-type zinc finger. Mol Pharmacol 68: 1803-1809.
25. Barth S, Edlich F, Berchner-Pfannschmidt U, Gneuss S, Jahreis G, et al. (2009) Hypoxia-inducible factor prolyl-4-hydroxylase PHD2 protein abundance depends on integral membrane anchoring of FKBP38. J Biol Chem 284: 23046-23058.
26. Barth S, Nesper J, Hasgall PA, Wirthner R, Nytko KJ, et al. (2007) The peptidyl prolyl cis/trans isomerase FKBP38 determines hypoxia-inducible transcription factor prolyl-4-hydroxylase PHD2 protein stability. Mol Cell Biol 27: 3758-3768.
27. Ozer A, Wu LC, Bruick RK (2005) The candidate tumor suppressor ING4 represses activation of the hypoxia inducible factor (HIF). Proc Natl Acad Sci U S A 102: 7481-7486.
28. To KK, Huang LE (2005) Suppression of hypoxia-inducible factor 1alpha (HIF-1alpha) transcriptional activity by the HIF prolyl hydroxylase EGLN1. J Biol Chem 280: 38102-38107.
29. Ansieau S, Leutz A (2002) The conserved Mynd domain of BS69 binds cellular and oncoviral proteins through a common PXLXP motif. J Biol Chem 277: 4906-4910.
30. Ceriani MF, Darlington TK, Staknis D, Mas P, Petti AA, et al. (1999) Lightdependent sequestration of TIMELESS by CRYPTOCHROME. Science 285: 553-556.
31. Dekanty A, Lavista-Llanos S, Irisarri M, Oldham S, Wappner P (2005) The insulin-PI3K/TOR pathway induces a HIF-dependent transcriptional response in Drosophila by promoting nuclear localization of HIF-alpha/Sima. J Cell Sci 118: 5431-5441.