PHD1 interacts with ATF4 and negatively regulates its transcriptional activity without prolyl hydroxylation

Experimental Cell Research

Volumn 317, Issue 20, 2011, Pages 2789-2799

  Hiwatashi, Yusuke ^a   Kanno, Kohei ^a   Takasaki, Chikahisa ^a   Goryo, Kenji ^a   Sato, Takuya ^a   Torii, Satoru ^a   Sogawa, Kazuhiro ^a   Yasumoto, Ken ichi ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

ATF4; HIF prolyl hydroxylation; Hypoxia; PHD1; PHD3

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ALANINE; OXYGENASE; PROLINE DERIVATIVE; PROLYL HYDROXYLASE DOMAIN CONTAINING PROTEIN 1; PROLYL HYDROXYLASE DOMAIN CONTAINING PROTEIN 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYDROXYLATION; HYPOXIA; IN VITRO STUDY; MOUSE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; TRANSCRIPTION REGULATION;

EID: 82555179130     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2011.09.005     Document Type: Article

References (44)

1. Huang L.E., Bunn H.F. Hypoxia-inducible factor and its biomedical relevance. J. Biol. Chem. 2003, 278:19575-19578.
2. Hirota K., Semenza G.L. Regulation of hypoxia-inducible factor 1 by prolyl and asparaginyl hydroxylases. Biochem. Biophys. Res. Commun. 2005, 338:610-616.
3. Schofield C.J., Ratcliffe P.J. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 2004, 5:343-354.
4. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 2008, 30:393-402.
5. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001, 294:1337-1340.
6. Epstein A.C., Gleadle J.M., McNeill L.A., Hewitson K.S., O'Rourke J., Mole D.R., Mukherji M., Metzen E., Wilson M.I., Dhanda A., Tian Y.-M., Masson N., Hamilton D.L., Jaakkola P., Barstead R., Hodgkin J., Maxwell P.H., Pugh C.W., Schofield C.J., Ratcliffe P.J. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:43-54.
7. Berra E., Ginouvès A., Pouysségur J. The hypoxia-inducible-factor hydroxylases bring fresh air into hypoxia signalling. EMBO Rep. 2006, 7:41-45.
8. 2-regulated prolyl hydroxylation. Science 2001, 292:468-472.
9. 2 sensing. Science 2001, 292:464-468.
10. Brown J.M., Giaccia A.J. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res. 1998, 58:1408-1416.
11. Bi M., Naczki C., Koritzinsky M., Fels D., Blais J., Hu N., Harding H., Novoa I., Varia M., Raleigh J., Scheuner D., Kaufman R.J., Bell J., Ron D., Wouters B.G., Koumenis C. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 2005, 24:3470-3481.
12. 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. Blood 2004, 103:1876-1882.
13. Kilberg M.S., Shan J., Su N. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol. Metab. 2009, 20:436-443.
14. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 2000, 6:1099-1108.
15. He C.H., Gong P., Hu B., Stewart D., Choi M.E., Choi A.M.K., Alam J. Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation. J. Biol. Chem. 2001, 276:20858-20865.
16. Ohoka N., Yoshii S., Hattori T., Onozaki K., Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 2005, 24:1243-1255.
17. Chen H., Pan Y.-X., Dudenhausen E.E., Kilberg M.S. Amino acid deprivation induces the transcriptionrate of the human asparagine synthetase gene through a timed program of expression and promoter binding of nutrient-responsive basic region/leucine zipper transcription factors as well as localized histone acetylation. J. Biol. Chem. 2004, 279:50829-50839.
18. Lopez A.B., Wang C., Huang C.C., Yaman I., Li Y., Chakravarty K., Johnson P.F., Chiang C.-M., Snider M.D., Wek R.C., Hatzoglou M. A feedback transcriptional mechanism controls the level of the arginine/lysine transporter cat-1 during amino acid starvation. Biochem. J. 2007, 402:163-173.
19. Ye J., Kumanova M., Hart L.S., Sloane K., Zhang H., De Panis D.N., Bobrovnikova-Marjon E., Diehl J.A., Ron D., Koumenis C. The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J. 2010, 29:2082-2096.
20. Ema M., Hirota K., Mimura J., Abe H., Yodoi J., Sogawa K., Poellinger L., Fujii-Kuriyama Y. 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. 1999, 18:1905-1914.
21. Mimura J., Ema M., Sogawa K., Fujii-Kuriyama Y. Identification of a novel mechanism of regulation of Ah (dioxin) receptor function. Genes Dev. 1999, 13:20-25.
22. Yasumoto K., Kowata Y., Yoshida A., Torii S., Sogawa K. Role of the intracellular localization of HIF-prolyl hydroxylases. Biochim. Biophys. Acta - Mol. Cell Res. 2009, 1793:792-797.
23. Kimura S., Umemura T., Iyanagi T. Two-cistronic expression plasmids for high-level gene expression in Escherichia coli preventing translational initiation inhibition caused by the intramolecular local secondary structure of mRNA. J. Biochem. (Tokyo) 2005, 137:523-533.
24. Wang F., Sekine H., Kikuchi Y., Takasaki C., Miura C., Heiwa O., Shuin T., Fujii-Kuriyama Y., Sogawa K. HIF-1α-prolyl hydroxylase: molecular target of nitric oxide in the hypoxic signal transduction pathway. Biochem. Biophys. Res. Commun. 2002, 295:657-662.
25. Heikal A.A., Hess S.T., Baird G.S., Tsien R.Y., Webb W.W. Molecular spectroscopy and dynamics of intrinsically fluorescent proteins: coral red (dsRed) and yellow (Citrine). Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11996-12001.
26. Rizzo M.A., Springer G.H., Granada B., Piston D.W. An improved cyan fluorescent protein variant useful for FRET. Nat. Biotechnol. 2004, 22:445-449.
27. Li X.Y., Takasaki C., Satoh Y., Kimura S., Yasumoto K., Sogawa K. Expression, purification and characterization of human PHD1 in Escherichia coli. J. Biochem. (Tokyo) 2008, 144:555-561.
28. Sato S., Tamiya N. The amino acid sequences of Erabutoxins, neurotoxic proteins of sea-snake (Laticauda semifasciata) venom. Biochem. J. 1971, 122:453-461.
29. Myllyharju J., Kivirikko K.I. Characterization of the iron- and 2-oxoglutarate-binding sites of human prolyl 4-hydroxylase. EMBO J. 1997, 16:1173-1180.
30. Hewitson K.S., Schofield C.J., Ratcliffe P.J. Hypoxia-inducible factor prolyl hydroxylase: Purification and assays of PHD2. Methods Enzymol. 2007, 435:25-42.
31. Gratton E., Breusegem S., Sutin J., Ruan Q., Barry N. Fluorescence lifetime imaging for the two-photon microscope: time-domain and frequency-domain methods. J. Biomed. Opt. 2003, 8:381-390.
32. Lakowicz J.R. Principles of Fluorescence Spectroscopy 2006, Springer, New York. third ed.
33. Reddy T.R., Tang H., Li X., Wong-Staal F. Functional interaction of the HTLV-1 transactivator Tax with activating transcription factor-4 (ATF4). Oncogene 1997, 14:2785-2792.
34. B receptors couple directly to the transcription factor ATF4. Mol. Cell. Neurosci. 2001, 17:637-645.
35. Huang J., Zhao Q., Mooney S.M., Lee F.S. Sequence determinants in hypoxia-inducible factor-1α for hydroxylation by the prolyl hydroxylases PHD1, PHD2, and PHD3. J. Biol. Chem. 2002, 277:39792-39800.
36. βTrCP ubiquitin ligase. Mol. Cell. Biol. 2001, 21:2192-2202.
37. Köditz J., Nesper J., Wottawa M., Stiehl D.P., Camenisch G., Franke C., Mylyharju J., Wenger R.H., Katschinski D.M. Oxygen-dependent ATF-4 stability is mediated by the PHD3 oxygen sensor. Blood 2007, 110:3610-3617.
38. Chérasse Y., Maurin A.-C., Chaveroux C., Jousse C., Carraro V., Parry L., Deval C., Chambon C., Fafournoux P., Bruhat A. The p300/CBP-associated factor (PCAF) is a cofactor of ATF4 for amino acid-regulated transcription of CHOP. Nucleic Acids Res. 2007, 35:5954-5965.
39. Ye J., Koumenis C. ATF4, an ER stress and hypoxia-inducible transcription factor and its potential role in hypoxia tolerance and tumorigenesis. Curr. Mol. Med. 2009, 9:411-416.
40. Wottawa M., Köditz J., Katschinski D.M. Normoxic destabilization of ATF-4 depends on proteasomal degradation. Acta Physiol. 2010, 198:457-463.
41. Harding H.P., Zhang Y., Zeng H., Novoa I., Lu P.D., Calfon M., Sadri N., Yun C., Popko B., Paules R., Stojdl D.F., Bell J.C., Hettmann T., Leiden J.M., Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 2003, 11:619-633.
42. Erez N., Milyavsky M., Eilam R., Shats I., Goldfinger N., Rotter V. Expression of prolyl-hydroxylase-1 (PHD1/EGLN2) suppresses hypoxia inducible factor-1α activation and inhibits tumor growth. Cancer Res. 2003, 63:8777-8783.
43. Roybal C.N., Yang S., Sun C.-W., Hurtado D., Vander Jagt D.L., Townes T.M., Abcouwer S.F. Homocysteine increases the expression of vascular endothelial growth factor by a mechanism involving endoplasmic reticulum stress and transcriptional factor ATF4. J. Biol. Chem. 2004, 279:14844-14852.
44. Roybal C.N., Hunsaker L.A., Barbash O., Vander Jagt D.L., Abcouwer S.F. The oxidative stressor arsenite activates vascular endothelial growth factor mRNA transcription by an ATF4-dependent mechanism. J. Biol. Chem. 2005, 280:20331-20339.