Prolyl-hydroxylase 3: evolving roles for an ancient signaling protein

References

• Taylor CT, McElwain JC. Ancient atmospheres and the evolution of oxygen sensing via the hypoxia-inducible factor in metazoans. Physiology (Bethesda). 2010;25(5):272–279.
   PubMed Web of Science ®Google Scholar
• Catling DC, Claire MW. How Earth’s atmosphere evolved to an oxic state: a status report. Earth Planet Sci Lett. 2006;237(1–2):1–20.
   Google Scholar
• Holland HD. The oxygenation of the atmosphere and oceans. Philos Trans R Soc LondB Biol Sci. 2006;361(1470):903–915.
   PubMed Web of Science ®Google Scholar
• Parfrey LW, Lahr DJ, Knoll AH, Katz LA. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci U S A. 2011;108(33):13624—13629.
   PubMedGoogle Scholar
• West CM, van der Wel H, Wang ZA. Prolyl 4-hydroxylase-1 mediates O2 signaling during development of Dictyostelium. Development. 2007;134(18):3349–3358.
   PubMedGoogle Scholar
• Hughes BT, Espenshade PJ. Oxygen-regulated degradation of fission yeast SREBP by Ofd1, a prolyl hydroxylase family member. EMBO J. 2008;27(10):1491–1501.
   PubMed Web of Science ®Google Scholar
• Rytkönen KT, Williams TA, Renshaw GM, Primmer CR, Nikinmaa M. Molecular evolution of the metazoan PHD-HIF oxygen-sensing system. Mol Biol Evol. 2011;28(6):1913–1926.
   PubMed Web of Science ®Google Scholar
• Myllyharju J. Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol. 2003;22(1):15–24.
   PubMed Web of Science ®Google Scholar
• Koivunen P, Tiainen P, Hyvärinen J, et al. An endoplasmic reticulum transmembrane prolyl 4-hydroxylase is induced by hypoxia and acts on hypoxia-inducible factor alpha. J Biol Chem. 2007;282(42):30544–30552.
   PubMed Web of Science ®Google Scholar
• Cardinale GJ, Rhoads RE, Udenfriend S. Simultaneous incorporation of 18 O into succinate and hydroxyproline catalyzed by collagen proline hydroxylase. Biochem Biophys Res Commun. 1971;43(3):537–543.
   PubMedGoogle Scholar
• Pollard PJ, Brière JJ, Alam NA, et al. Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum Mol Genet. 2005;14(15):2231–2239.
   PubMed Web of Science ®Google Scholar
• Dang L, Jin S, Su SM. IDH mutations in glioma and acute myeloid leukemia. Trends Mol Med. 2010;16(9):387–397.
   PubMed Web of Science ®Google Scholar
• Maxwell PH. A common pathway for genetic events leading to pheochromocytoma. Cancer Cell. 2005;8(2):91–93.
   PubMedGoogle Scholar
• Tuderman L, Myllylä R, Kivirikko KI. Mechanism of the prolyl hydroxylase reaction. 1. Role of co-substrates. Eur J Biochem. 1977;80(2):341–348.
   PubMedGoogle Scholar
• Schofield CJ, Ratcliffe PJ. Signalling hypoxia by HIF hydroxylases. Biochem Biophys Res Commun. 2005;338(1):617–626.
   PubMedGoogle Scholar
• Spitz DR, Azzam EI, Li JJ, Gius D. Metabolic oxidation/reduction reactions and cellular responses to ionizing radiation: a unifying concept in stress response biology. Cancer Metastasis Rev. 2004;23(3—4):311–322.
   PubMed Web of Science ®Google Scholar
• Guzy RD, Hoyos B, Robin E, et al. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab. 2005;1(6):401—408.
   Google Scholar
• Kaewpila S, Venkataraman S, Buettner GR, Oberley LW. Manganese superoxide dismutase modulates hypoxia-inducible factor-1 alpha induction via superoxide. Cancer Res. 2008;68(8):2781–2788.
   PubMedGoogle Scholar
• Myllylä R, Kuutti-Savolainen ER, Kivirikko KI. The role of ascorbate in the prolyl hydroxylase reaction. Biochem Biophys Res Commun. 1978;83(2):441–448.
   PubMed Web of Science ®Google Scholar
• Peterkofsky B. Ascorbate requirement for hydroxylation and secretion of procollagen: relationship to inhibition of collagen synthesis in scurvy. Am J Clin Nutr. 1991;54(Suppl 6):1135S-1140S.
   PubMedGoogle Scholar
• Hoffart LM, Barr EW, Guyer RB, Bollinger JM, Krebs C. Direct spectroscopic detection of a C-H-cleaving high-spin Fe(IV) complex in a prolyl-4-hydroxylase. Proc Natl Acad Sci U S A. 2006;103(40):14738–14743.
   PubMed Web of Science ®Google Scholar
• Knowles HJ, Raval RR, Harris AL, Ratcliffe PJ. Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res. 2003;63(8):1764–1768.
   PubMed Web of Science ®Google Scholar
• Pagé EL, Chan DA, Giaccia AJ, Levine M, Richard DE. Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol Biol Cell. 2008;19(1):86–94.
   PubMed Web of Science ®Google Scholar
• Ho VT, Bunn HF. Effects of transition metals on the expression of the erythropoietin gene: further evidence that the oxygen sensor is a heme protein. Biochem Biophys Res Commun. 1996;223(1):175–180.
   PubMed Web of Science ®Google Scholar
• Lipscomb EA, Sarmiere PD, Crowder RJ, Freeman RS. Expression of the SM-20 gene promotes death in nerve growth factor-dependent sympathetic neurons. J Neurochem. 1999;73(1):429–432.
   PubMedGoogle Scholar
• Epstein AC, Gleadle JM, McNeill LA, et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell. 2001;107(1):43–54.
   PubMed Web of Science ®Google Scholar
• Huang J, Zhao Q, Mooney SM, Lee FS. Sequence determinants in hypoxia-inducible factor-1alpha for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3. J Biol Chem. 2002;277(42):39792–39800.
   PubMed Web of Science ®Google Scholar
• Li D, Hirsilä M, Koivunen P, et al. Many amino acid substitutions in a hypoxia-inducible transcription factor (HIF)-1alpha-like peptide cause only minor changes in its hydroxylation by the HIF prolyl 4-hydroxylases: substitution of 3,4-dehydroproline or azetidine-2-carboxylic acid for the proline leads to a high rate of uncoupled 2-oxoglutarate decarboxylation. J Biol Chem. 2004;279(53):55051–55059.
   PubMedGoogle Scholar
• Xie L, Pi X, Mishra A, Fong G, Peng J, Patterson C. PHD3-dependent hydroxylation of HCLK2 promotes the DNA damage response. J Clin Invest. 2012;122(8):2827–2836.
   PubMed Web of Science ®Google Scholar
• Luo W, Hu H, Chang R, et al. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell. 2011;145(5):732–744.
   PubMed Web of Science ®Google Scholar
• Xie L, Xiao K, Whalen EJ, et al. Oxygen-regulated beta(2)-adrenergic receptor hydroxylation by EGLN3 and ubiquitylation by pVHL. Sci Signal. 2009;2(78):ra33.
   Web of Science ®Google Scholar
• Kivirikko KI, Myllylä R. Posttranslational enzymes in the biosynthesis of collagen: intracellular enzymes. Meth Enzymol. 1982;82 Pt A:245–304.
   PubMedGoogle Scholar
• Stadtman ER. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu Rev Biochem. 1993;62:797–821.
   PubMed Web of Science ®Google Scholar
• Nakayama K, Gazdoiu S, Abraham R, Pan ZQ, Ronai Z. Hypoxia-induced assembly of prolyl hydroxylase PHD3 into complexes: implications for its activity and susceptibility for degradation by the E3 ligase Siah2. Biochem J. 2007;401(1):217–226.
   PubMedGoogle Scholar
• Rantanen K, Pursiheimo J, Högel H, Himanen V Metzen E, Jaakkola PM. Prolyl hydroxylase PHD3 activates oxygen-dependent protein aggregation. Mol Biol Cell. 2008;19(5):2231–2240.
   PubMedGoogle Scholar
• Semenza GL. HIF-1: upstream and downstream of cancer metabolism. Curr Opin Genet Dev. 2010;20(1):51–56.
   PubMed Web of Science ®Google Scholar
• Semenza GL. Oxygen homeostasis. Wiley Interdiscip Rev Syst Biol Med. 2010;2(3):336–361.
   PubMed Web of Science ®Google Scholar
• Semenza GL. Regulation of oxygen homeostasis by hypoxia-inducible factor 1. Physiology (Bethesda). 2009;24:97–106.
   PubMed Web of Science ®Google Scholar
• Villar D, Vara-Vega A, Landazuri MO, Del Peso L. Identification of a region on hypoxia-inducible-factor prolyl 4-hydroxylases that determines their specificity for the oxygen degradation domains. Biochem J. 2007;408(2):231–240.
   PubMedGoogle Scholar
• Appelhoff RJ, Tian YM, Raval RR, et al. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem. 2004;279(37):38458–38465.
   PubMed Web of Science ®Google Scholar
• Kallio PJ, Okamoto K, O’Brien S, et al. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J. 1998;17(22):6573–6586.
   PubMed Web of Science ®Google Scholar
• Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A. 1995;92(12):5510–5514.
   PubMed Web of Science ®Google Scholar
• Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem. 1995;270(3):1230–1237.
   PubMed Web of Science ®Google Scholar
• Arany Z, Huang LE, Eckner R, et al. An essential role for p300/CBP in the cellular response to hypoxia. Proc Natl Acad Sci U S A. 1996;93(23):12969–12973.
   PubMed Web of Science ®Google Scholar
• Metzen E, Stiehl DP Doege K, Marxsen JH, Hellwig-Bürgel T, Jelkmann W. Regulation of the prolyl hydroxylase domain protein 2 (phd2/egln-1) gene: identification of a functional hypoxia-responsive element. Biochem J. 2005;387(Pt 3):711–717.
   PubMedGoogle Scholar
• Pescador N, Cuevas Y, Naranjo S, et al. Identification of a functional hypoxia-responsive element that regulates the expression of the egl nine homologue 3 (egln3/phd3) gene. Biochem J. 2005;390(Pt 1):189–197.
   PubMedGoogle Scholar
• Schödel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, Mole DR. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood. 2011;117(23):e207-e217.
   PubMed Web of Science ®Google Scholar
• Villar D, Ortiz-Barahona A, Gômez-Maldonado L, et al. Cooperativity of stress-responsive transcription factors in core hypoxia-inducible factor binding regions. PLoS ONE. 2012;7(9):e45708.
   PubMedGoogle Scholar
• Meyer LR, Zweig AS, Hinrichs AS, et al. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res. 2013;41(Database issue):D64-D69.
   PubMedGoogle Scholar
• Rosenbloom KR, Sloan CA, Malladi VS, et al. ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res. 2013;41(Database issue):D56-D63.
   PubMedGoogle Scholar
• Millonig G, Hegedüsch S, Becker L, Seitz HK, Schuppan D, Mueller S. Hypoxia-inducible factor 1 alpha under rapid enzymatic hypoxia: cells sense decrements of oxygen but not hypoxia per se. Free Radic Biol Med. 2009;46(2):182–191.
   PubMedGoogle Scholar
• Luo W, Semenza GL. Pyruvate kinase M2 regulates glucose metabolism by functioning as a coactivator for hypoxia-inducible factor 1 in cancer cells. Oncotarget. 2011;2(7):551–556.
   PubMedGoogle Scholar
• Chen N, Rinner O, Czernik D, et al. The oxygen sensor PHD3 limits glycolysis under hypoxia via direct binding to pyruvate kinase. Cell Res. 2011;21(6):983–986.
   PubMed Web of Science ®Google Scholar
• Wax SD, Rosenfield CL, Taubman MB. Identification of a novel growth factor-responsive gene in vascular smooth muscle cells. J Biol Chem. 1994;269(17):13041–13047.
   PubMedGoogle Scholar
• Menzies K, Liu B, Kim WJ, Moschella MC, Taubman MB. Regulation of the SM-20 prolyl hydroxylase gene in smooth muscle cells. Biochem Biophys Res Commun. 2004;317(3):801–810.
   PubMedGoogle Scholar
• Kyo S, Takakura M, Taira T, et al. Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Res. 2000;28(3):669–677.
   PubMedGoogle Scholar
• Gerber SA, Yatsula B, Maier CL, Sadler TJ, Whittaker LW, Pober JS. Interferon-gamma induces prolyl hydroxylase (PHD)3 through a STAT1-dependent mechanism in human endothelial cells. Arterioscler Thromb Vasc Biol. 2009;29(9):1363–1369.
   PubMedGoogle Scholar
• Madden SL, Galella EA, Riley D, Bertelsen AH, Beaudry GA. Induction of cell growth regulatory genes by p53. Cancer Res. 1996;56(23):5384–5390.
   PubMedGoogle Scholar
• Lipscomb EA, Sarmiere PD, Freeman RS. SM-20 is a novel mitochondrial protein that causes caspase-dependent cell death in nerve growth factor-dependent neurons. J Biol Chem. 2001;276(7):5085–5092.
   PubMedGoogle Scholar
• Place TL, Fitzgerald MP, Venkataraman S, et al. Aberrant promoter CpG methylation is a mechanism for impaired PHD3 expression in a diverse set of malignant cells. PLoS ONE. 2011;6(1):e14617.
   PubMedGoogle Scholar
• Hatzimichael E, Dasoula A, Shah R, et al. The prolyl-hydroxylase EGLN3 and not EGLN1 is inactivated by methylation in plasma cell neoplasia. Eur J Haematol. 2010;84(1):47—51.
   PubMedGoogle Scholar
• Cervera AM, Apostolova N, Luna-Crespo F, Sanjuan-Pla A, Garcia-Bou R, McCreath KJ. An alternatively spliced transcript of the PHD3 gene retains prolyl hydroxylase activity. Cancer Lett. 2006;233(1):131—138.
   PubMedGoogle Scholar
• Nakayama K, Frew IJ, Hagensen M, et al. Siah2 regulates stability of prolyl-hydroxylases, controls HIF1alpha abundance, and modulates physiological responses to hypoxia. Cell. 2004;117(7):941—952.
   PubMedGoogle Scholar
• Metzen E, Berchner-Pfannschmidt U, Stengel P, et al. Intracellular localisation of human HIF-1 alpha hydroxylases: implications for oxygen sensing. J Cell Sci. 2003;116(Pt 7):1319—1326.
   PubMedGoogle Scholar
• Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol. 2006;26(22):8336—8346.
   Google Scholar
• Dunwoodie SL. The role of hypoxia in development of the Mammalian embryo. Dev Cell. 2009;17(6):755—773.
   PubMedGoogle Scholar
• Kiss J, Mollenhauer M, Walmsley SR, et al. Loss of the oxygen sensor PHD3 enhances the innate immune response to abdominal sepsis. J Immunol. 2012;189(4):1955—1965.
   PubMedGoogle Scholar
• Fu J, Menzies K, Freeman RS, Taubman MB. EGLN3 prolyl hydroxylase regulates skeletal muscle differentiation and myogenin protein stability. J Biol Chem. 2007;282(17):12410—12418.
   Google Scholar
• Fu J, Taubman MB. Prolyl hydroxylase EGLN3 regulates skeletal myoblast differentiation through an NF-kappaB-dependent pathway. J Biol Chem. 2010;285(12):8927—8935.
   Google Scholar
• Liu Y, Huo Z, Yan B, et al. Prolyl hydroxylase 3 interacts with Bcl-2 to regulate doxorubicin-induced apoptosis in H9c2 cells. Biochem Biophys Res Commun. 2010;401(2):231—237.
   Google Scholar
• Frank D, Gantenberg J, Boomgaarden I, et al. MicroRNA-20a inhibits stress-induced cardiomyocyte apoptosis involving its novel target Egln3/PHD3. J Mol Cell Cardiol. 2012;52(3):711—717.
   PubMedGoogle Scholar
• Escribese MM, Sierra-Filardi E, Nieto C, et al. The prolyl hydroxylase PHD3 identifies proinflammatory macrophages and its expression is regulated by activin A. J Immunol. 2012;189(4):1946—1954.
   PubMedGoogle Scholar
• Walmsley SR, Chilvers ER, Thompson AA, et al. Prolyl hydroxylase 3 (PHD3) is essential for hypoxic regulation of neutrophilic inflammation in humans and mice. J Clin Invest. 2011;121(3):1053—1063.
   PubMedGoogle Scholar
• Sternfeld J, David CN. Oxygen gradients cause pattern orientation in Dictyostelium cell clumps. J Cell Sci. 1981;50:9—17.
   PubMedGoogle Scholar
• Bishop T, Gallagher D, Pascual A, et al. Abnormal sympathoadrenal development and systemic hypotension in PHD3-/— mice. Mol Cell Biol. 2008;28(10):3386—3400.
   Google Scholar
• Su Y, Loos M, Giese N, et al. PHD3 regulates differentiation, tumour growth and angiogenesis in pancreatic cancer. Br J Cancer. 2010;103(10):1571—1579.
   Google Scholar
• Högel H, Rantanen K, Jokilehto T, Grenman R, Jaakkola PM. Prolyl hydroxylase PHD3 enhances the hypoxic survival and G1 to S transition of carcinoma cells. PLoS ONE. 2011;6(11):e27112.
   PubMed Web of Science ®Google Scholar
• Chen S, Zhang J, Li X, Luo X, Fang J, Chen H. The expression of prolyl hydroxylase domain enzymes are up-regulated and negatively correlated with Bcl-2 in non-small cell lung cancer. Mol Cell Biochem. 2011;358(1—2):257—263.
   Google Scholar
• Su C, Huang K, Sun L, et al. Overexpression of the HIF hydroxylase PHD3 is a favorable prognosticator for gastric cancer. Med Oncol. 2012;29(4):2710—2715.
   Google Scholar
• Couvelard A, Deschamps L, Rebours V, et al. Overexpression of the oxygen sensors PHD-1, PHD-2, PHD-3, and FIH Is associated with tumor aggressiveness in pancreatic endocrine tumors. Clin Cancer Res. 2008;14(20):6634—6639.
   PubMedGoogle Scholar
• Gossage L, Zaitoun A, Fareed KR, et al. Expression of key hypoxia sensing prolyl-hydroxylases PHD1, -2 and -3 in pancreaticobiliary cancer. Histopathology. 2010;56(7):908—920.
   PubMedGoogle Scholar
• Lee S, Nakamura E, Yang H, et al. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell. 2005;8(2):155—167.
   Google Scholar
• Straub JA, Lipscomb EA, Yoshida ES, Freeman RS. Induction of SM-20 in PC12 cells leads to increased cytochrome c levels, accumulation of cytochrome c in the cytosol, and caspase-dependent cell death. J Neurochem. 2003;85(2):318—328.
   PubMedGoogle Scholar
• Schlisio S, Kenchappa RS, Vredeveld LC, et al. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes Dev. 2008;22(7):884—893.
   PubMedGoogle Scholar
• Dang L, White DW, Gross S, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature. 2009;462(7274):739—744.
   PubMed Web of Science ®Google Scholar
• Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science. 2001;294(5545):1337—1340.
   PubMedGoogle Scholar
• Sato M, Sakota M, Nakayama K. Human PRP19 interacts with prolyl-hydroxylase PHD3 and inhibits cell death in hypoxia. Exp Cell Res. 2010;316(17):2871—2882.
   Google Scholar
• Xue J, Li X, Jiao S, Wei Y, Wu G, Fang J. Prolyl hydroxylase-3 is down-regulated in colorectal cancer cells and inhibits IKKbeta independent of hydroxylase activity. Gastroenterology. 2010;138(2):606—615.
   PubMedGoogle Scholar
• Tennant DA, Gottlieb E. HIF prolyl hydroxylase-3 mediates alpha-ketoglutarate-induced apoptosis and tumor suppression. J Mol Med. 2010;88(8):839—849.
   PubMedGoogle Scholar
• Hopfer U, Hopfer H, Jablonski K, Stahl RA, Wolf G. The novel WD-repeat protein Morg1 acts as a molecular scaffold for hypoxia-inducible factor prolyl hydroxylase 3 (PHD3). J Biol Chem. 2006;281(13):8645—8655.
   PubMedGoogle Scholar
• Köditz J, Nesper J, Wottawa M, et al. Oxygen-dependent ATF-4 stability is mediated by the PHD3 oxygen sensor. Blood. 2007;110(10):3610—3617.
   PubMedGoogle Scholar
• Baek JH, Mahon PC, Oh J, et al. OS-9 interacts with hypoxia-inducible factor 1alpha and prolyl hydroxylases to promote oxygen-dependent degradation of HIF-1alpha. Mol Cell. 2005;17(4):503—512.
   PubMedGoogle Scholar
• Aprelikova O, Pandolfi S, Tackett S, et al. Melanoma antigen-11 inhibits the hypoxia-inducible factor prolyl hydroxylase 2 and activates hypoxic response. Cancer Res. 2009;69(2):616—624.
   PubMedGoogle Scholar
• Masson N, Appelhoff RJ, Tuckerman JR, et al. The HIF prolyl hydroxylase PHD3 is a potential substrate of the TRiC chaperonin. FEBS Lett. 2004;570(1—3):166—170.
   PubMedGoogle Scholar