Human PRP19 interacts with prolyl-hydroxylase PHD3 and inhibits cell death in hypoxia

Experimental Cell Research

Volumn 316, Issue 17, 2010, Pages 2871-2882

  Sato, Masuhiro ^a   Sakota, Miki ^a   Nakayama, Koh ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Cell death; HPRP19; Hypoxia; PHD3; Prolyl hydroxylase

Indexed keywords

CASPASE; OXYGENASE; PROLYL OXYGENASE 3; PROTEIN; PRP19 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; DIOXYGENASE; EGLN3 PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; NUCLEAR PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROTEIN BINDING; PRPF19 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DEATH; CELL STRAIN; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVITY; HELA CELL; HUMAN; HUMAN CELL; HYPOXIA; PRIORITY JOURNAL; PROTEIN INTERACTION; ANIMAL; ANOXIA; ANTAGONISTS AND INHIBITORS; CELL LINE; METABOLISM; PATHOLOGY; PC12 CELL LINE; RAT;

ANIMALS; ANOXIA; CASPASES; CELL DEATH; CELL LINE; DIOXYGENASES; DNA REPAIR ENZYMES; HUMANS; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; NUCLEAR PROTEINS; PC12 CELLS; PROCOLLAGEN-PROLINE DIOXYGENASE; PROTEIN BINDING; RATS;

EID: 77956871456     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.06.018     Document Type: Article

References (35)

1. Kaelin W.G., Ratcliffe P.J. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol. Cell 2008, 30:393-402.
2. Wang G.L., Jiang B.H., Rue E.A., Semenza G.L. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl Acad. Sci. USA 1995, 92:5510-5514.
3. Huang L.E., Gu J., Schau M., Bunn H.F. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl Acad. Sci. USA 1998, 95:7987-7992.
4. Kallio P.J., Wilson W.J., O'Brien S., Makino Y., Poellinger L. Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J. Biol. Chem. 1999, 274:6519-6525.
5. Salceda S., Caro J. Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem. 1997, 272:22642-22647.
6. Kamura T., Sato S., Iwai K., Czyzyk-Krzeska M., Conaway R.C., Conaway J.W. Activation of HIF1alpha ubiquitination by a reconstituted von Hippel-Lindau (VHL) tumor suppressor complex. Proc. Natl Acad. Sci. USA 2000, 97:10430-10435.
7. Maxwell P.H., Wiesener M.S., Chang G.W., Clifford S.C., Vaux E.C., Cockman M.E., Wykoff C.C., Pugh C.W., Maher E.R., Ratcliffe P.J. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271-275.
8. 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., Elegans C. EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:43-54.
9. 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. EMBO J. 2003, 22:4082-4090.
10. Appelhoff R.J., Tian Y.M., Raval R.R., Turley H., Harris A.L., Pugh C.W., Ratcliffe P.J., Gleadle J.M. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J. Biol. Chem. 2004, 279:38458-38465.
11. Nakayama K., Frew I.J., Hagensen M., Skals M., Habelhah H., Bhoumik A., Kadoya T., Erdjument-Bromage H., Tempst P., Frappell P.B., Bowtell D.D., Ronai Z. Siah2 regulates stability of prolyl-hydroxylases, controls HIF1alpha abundance, and modulates physiological responses to hypoxia. Cell 2004, 117:941-952.
12. Lieb M.E., Menzies K., Moschella M.C., Ni R., Taubman M.B. Mammalian EGLN genes have distinct patterns of mRNA expression and regulation. Biochem. Cell Biol. 2002, 80:421-426.
13. Minamishima Y.A., Moslehi J., Padera R.F., Bronson R.T., Liao R., Kaelin W.G. A feedback loop involving the Phd3 prolyl hydroxylase tunes the mammalian hypoxic response in vivo. Mol. Cell. Biol. 2009, 29:5729-5741.
14. Aragones J., Schneider M., Van Geyte K., Fraisl P., Dresselaers T., Mazzone M., Dirkx R., Zacchigna S., Lemieux H., Jeoung N.H., Lambrechts D., Bishop T., Lafuste P., Diez-Juan A., Harten S.K., Van Noten P., De Bock K., Willam C., Tjwa M., Grosfeld A., Navet R., Moons L., Vandendriessche T., Deroose C., Wijeyekoon B., Nuyts J., Jordan B., Silasi-Mansat R., Lupu F., Dewerchin M., Pugh C., Salmon P., Mortelmans L., Gallez B., Gorus F., Buyse J., Sluse F., Harris R.A., Gnaiger E., Hespel P., Van Hecke P., Schuit F., Van Veldhoven P., Ratcliffe P., Baes M., Maxwell P., Carmeliet P. Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat. Genet. 2008, 40:170-180.
15. Knowles H.J., Raval R.R., Harris A.L., Ratcliffe P.J. Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res. 2003, 63:1764-1768.
16. Koivunen P., Hirsila M., Remes A.M., Hassinen I.E., Kivirikko K.I., Myllyharju J. Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J. Biol. Chem. 2007, 282:4524-4532.
17. Lee S., Nakamura E., Yang H., Wei W., Linggi M.S., Sajan M.P., Farese R.V., Freeman R.S., Carter B.D., Kaelin W.G., Schlisio S. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 2005, 8:155-167.
18. Rantanen K., Pursiheimo J., Hogel H., Himanen V., Metzen E., Jaakkola P.M. Prolyl hydroxylase PHD3 activates oxygen-dependent protein aggregation. Mol. Biol. Cell 2008, 19:2231-2240.
19. Hopfer U., Hopfer H., Jablonski K., Stahl R.A., 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, 281:8645-8655.
20. Koditz J., Nesper J., Wottawa M., Stiehl D.P., Camenisch G., Franke C., Myllyharju J., Wenger R.H., Katschinski D.M. Oxygen-dependent ATF-4 stability is mediated by the PHD3 oxygen sensor. Blood 2007, 110:3610-3617.
21. Masson N., Appelhoff R.J., Tuckerman J.R., Tian Y.M., Demol H., Puype M., Vandekerckhove J., Ratcliffe P.J., Pugh C.W. The HIF prolyl hydroxylase PHD3 is a potential substrate of the TRiC chaperonin. FEBS Lett. 2004, 570:166-170.
22. Xie L., Xiao K., Whalen E.J., Forrester M.T., Freeman R.S., Fong G., Gygi S.P., Lefkowitz R.J., Stamler J.S. Oxygen-regulated beta(2)-adrenergic receptor hydroxylation by EGLN3 and ubiquitylation by pVHL. Sci. Signal. 2009, 2:ra33.
23. Nakayama K., Gazdoiu S., Abraham R., Pan Z.Q., 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, 401:217-226.
24. Grillari J., Ajuh P., Stadler G., Loscher M., Voglauer R., Ernst W., Chusainow J., Eisenhaber F., Pokar M., Fortschegger K., Grey M., Lamond A.I., Katinger H. SNEV is an evolutionarily conserved splicing factor whose oligomerization is necessary for spliceosome assembly. Nucleic Acids Res. 2005, 33:6868-6883.
25. Ohi M.D., Vander Kooi C.W., Rosenberg J.A., Ren L., Hirsch J.P., Chazin W.J., Walz T., Gould K.L. Structural and functional analysis of essential pre-mRNA splicing factor Prp19p. Mol. Cell. Biol. 2005, 25:451-460.
26. Straub J.A., Lipscomb E.A., Yoshida E.S., Freeman R.S. 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, 85:318-328.
27. de Andrade H.H., Marques E.K., Schenberg A.C., Henriques J.A. The PSO4 gene is responsible for an error-prone recombinational DNA repair pathway in Saccharomyces cerevisiae. Mol. Gen. Genet. 1989, 217:419-426.
28. Vijayraghavan U., Company M., Abelson J. Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae. Genes Dev. 1989, 3:1206-1216.
29. Mahajan K.N., Mitchell B.S. Role of human Pso4 in mammalian DNA repair and association with terminal deoxynucleotidyl transferase. Proc. Natl Acad. Sci. USA 2003, 100:10746-10751.
30. Lu X., Legerski R.J. The Prp19/Pso4 core complex undergoes ubiquitylation and structural alterations in response to DNA damage. Biochem. Biophys. Res. Commun. 2007, 354:968-974.
31. Schlisio S., Kenchappa R.S., Vredeveld L.C., George R.E., Stewart R., Greulich H., Shahriari K., Nguyen N.V., Pigny P., Dahia P.L., Pomeroy S.L., Maris J.M., Look A.T., Meyerson M., Peeper D.S., Carter B.D., Kaelin W.G. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes Dev. 2008, 22:884-893.
32. Ginouves A., Ilc K., Macias N., Pouyssegur J., Berra E. PHDs overactivation during chronic hypoxia "desensitizes" HIFalpha and protects cells from necrosis. Proc. Natl Acad. Sci. USA 2008, 105:4745-4750.
33. Kleinridders A., Pogoda H.M., Irlenbusch S., Smyth N., Koncz C., Hammerschmidt M., Bruning J.C. PLRG1 is an essential regulator of cell proliferation and apoptosis during vertebrate development and tissue homeostasis. Mol. Cell. Biol. 2009, 29(11):3173-3185.
34. Fortschegger K., Wagner B., Voglauer R., Katinger H., Sibilia M., Grillari J. Early embryonic lethality of mice lacking the essential protein SNEV. Mol. Cell. Biol. 2007, 27:3123-3130.
35. Cho S.Y., Shin E.S., Park P.J., Shin D.W., Chang H.K., Kim D., Lee H.H., Lee J.H., Kim S.H., Song M.J., Chang I.S., Lee O.S., Lee T.R. Identification of mouse Prp19p as a lipid droplet-associated protein and its possible involvement in the biogenesis of lipid droplets. J. Biol. Chem. 2007, 282:2456-2465.