Erythropoietin Inhibits HIF-1α Expression via Upregulation of PHD-2 Transcription and Translation in an In Vitro Model of Hypoxia-Ischemia

Translational Stroke Research

Volumn 5, Issue 1, 2014, Pages 118-127

  Souvenir, Rhonda ^a   Flores, Jerry J ^a   Ostrowski, Robert P ^a   Manaenko, Anatol ^a   Duris, Kamil ^a   Tang, Jiping ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

EPO; HIF 1 ; OGD; PHD 2

Indexed keywords

GELATINASE B; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MESSENGER RNA; NERVE GROWTH FACTOR; OXYGEN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE DOMAIN 2; REACTIVE OXYGEN METABOLITE; RECOMBINANT ERYTHROPOIETIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; GENE SILENCING; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IN VITRO STUDY; INHIBITION KINETICS; NEUROPROTECTION; NONHUMAN; PC12 CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; UPREGULATION;

ANIMALS; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-ISCHEMIA, BRAIN; NEUROPROTECTIVE AGENTS; PC12 CELLS; PROCOLLAGEN-PROLINE DIOXYGENASE; RATS; REACTIVE OXYGEN SPECIES; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84893749290     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-013-0312-z     Document Type: Article

References (42)

1. Agani FH, Puchowicz M, Chavez JC, Pichiule P, LaManna J. Role of nitric oxide in the regulation of HIF-1alpha expression during hypoxia. Am J Physiol Cell Physiol. 2002;283: C178-86.
2. Appelhoff RJ, Tian YM, Raval RR, Turley H, Harris AL, Pugh CW, et al. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem. 2004;279: 38458-65.
3. Baranova O, Miranda LF, Pichiule P, Dragatsis I, Johnson RS, Chavez JC. Neuron-specific inactivation of the hypoxia inducible factor 1 alpha increases brain injury in a mouse model of transient focal cerebral ischemia. J Neurosci. 2007;27: 6320-32.
4. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, Pouyssergur J. HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1 α in normoxia. EMBO J. 2003;22: 4082-90.
5. Bruick RK. Oxygen sensing in the hypoxic response pathway: regulation of the hypoxia-inducible transcription factor. Genes Dev. 2003;17: 2614-23.
6. Calvert JW, Cahill J, Yamaguchi-Okada M, Zhang JH. Oxygen treatment after experimental hypoxia-ischemia in neonatal rats alters the expression of HIF-1alpha and its downstream target genes. J Appl Physiol. 2006;101: 853-65.
7. Cash TP, Pan Y, Simon MC. Reactive oxygen species and cellular oxygen sensing. Free Radic Biol Med. 2007;43: 1219-25.
8. Chang TC, Huang CJ, Tam K, Chen SF, Tan KT, Tsai MS, et al. Stabilization of hypoxia-inducible factor-1{alpha} by prostacyclin under prolonged hypoxia via reducing reactive oxygen species level in endothelial cells. J Biol Chem. 2005;280: 36567-74.
9. DeNiro M, Al-Halafi A, Al-Mohanna FH, Alsmadi O, Al-Mohanna FA. Pleiotropic effects of YC-1 selectively inhibit pathological retinal neovascularization and promote physiological revascularization in a mouse model of oxygen-induced retinopathy. Mol Pharmacol. 2010;77: 348-67.
10. Dickson G, Prentice H, Julien JP, Ferrari G, Leon A, Walsh FS. Nerve growth factor activates Thy-1 and neurofilament gene transcription in rat PC12 cells. EMBO J. 1986;5: 3449-53.
11. Dominguez E, Rivat C, Pommier B, Mauborgne A, Pohl M. JAK/STAT3 pathway is activated in spinal cord microglia after peripheral nerve injury and contributes to neuropathic pain development in rat. J Neurochem. 2008;107: 50-60.
12. Ehrenreich H, Weissenborn K, Prange H, Schneider D, Weimar C, Wartenberg K, et al. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke. 2009;40: e647-56.
13. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, et al. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell. 2001;107: 43-54.
14. 2-sensing cells? J Biol Chem. 2005;280: 41504-11.
15. Halterman MW, Federoff HJ. HIF-1alpha and p53 promote hypoxia-induced delayed neuronal death in models of CNS ischemia. Exp Neurol. 1999;159: 65-72.
16. Hirsila M, Koivunen P, Gunzler V, Kivirikko KI, Myllyharju J. Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem. 2003;278: 30772-80.
17. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci U S A. 1998;95: 7987-92.
18. Hull MA, Thomson JL, Hawkey. Expression of cyclooxygenase 1 and 2 by human gastric endothelial cells. Gut. 1999;45: 529-36.
19. Ivan MG, Scaiano JC. A new approach for the detection of carbon-centered radicals in enzymatic processes using prefluorescent probes. Photochem Photobiol. 2003;78: 416-9.
20. 2-regulated prolyl hydroxylation. Science. 2001;292: 468-72.
21. Jones NM, Bergeron M. Hypoxic preconditioning induces changes in HIF-1 target genes in neonatal rat brain. J Cereb Blood Flow Metab. 2001;21: 1105-14.
22. Kallio PJ, Wilson WJ, 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: 6519-25.
23. Kamura T, Sakai K, Kaku T, Kobayashi H, Mitsumoto M, Tsuneyoshi M, et al. Comparison of p53 and CD44 variant 6 expression between paired primary and recurrent ovarian cancer: an immunohistochemical analysis. Oncol Rep. 1999;6: 97-101.
24. Krieg M, Haas R, Brauch H, Acker T, Flamme I, Plate KH. Up-regulation of hypoxia-inducible factors HIF-1alpha and HIF-2alpha under normoxic conditions in renal carcinoma cells by von Hippel-Lindau tumor suppressor gene loss of function. Oncogene. 2000;19: 5435-43.
25. Lee C, Kim SJ, Jeong DG, Lee SM, Ryu SE. Structure of human FIH-1 reveals a unique active site pocket and interaction sites for HIF-1 and von Hippel-Lindau. J Biol Chem. 2003;278: 7558-63.
26. Lee DW, Rajagopalan S, Siddiq A, Gwiazda R, Yang L, Beal MF, et al. Inhibition of prolyl hydroxylase protects against 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-induced neurotoxicity: model for the potential involvement of the hypoxia-inducible factor pathway in Parkinson disease. J Biol Chem. 2009;284: 29065-76.
27. Leker RR, Aharonowiz M, Greig NH, Ovadia H. The role of p53-induced apoptosis in cerebral ischemia: effects of the p53 inhibitor pifithrin alpha. Exp Neurol. 2004;187: 478-86.
28. Li Y, Zhou C, Calvert JW, Colohan AR, Zhang JH. Multiple effects of hyperbaric oxygen on the expression of HIF-1 alpha and apoptotic genes in a global ischemia-hypotension rat model. Exp Neurol. 2005;191: 198-210.
29. Lisztwan J, Imbert G, Wirbelauer C, Gstaiger M, Krek W. The von Hippel-Lindau tumor suppressor protein is a component of an E3 ubiquitin-protein ligase activity. Genes Dev. 1999;13: 1822-33.
30. Mu X, Chang C. TR3 orphan nuclear receptor mediates apoptosis through up-regulating E2F1 in human prostate cancer LNCaP cells. J Biol Chem. 2003;278: 42840-5.
31. Prass K, Scharff A, Ruscher K, Lowl D, Muselmann C, Victorov I, et al. Hypoxia-induced stroke tolerance in the mouse is mediated by erythropoietin. Stroke. 2003;34: 1981-6.
32. Ratan RR, Siddiq A, Aminova L, Langley B, McConoughey S, Karpisheva K, et al. Small molecule activation of adaptive gene expression: tilorone or its analogs are novel potent activators of hypoxia inducible factor-1 that provide prophylaxis against stroke and spinal cord injury. AnnuNYAcadSci. 2008;1147: 383-94.
33. 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: 22642-7.
34. Semenza GL. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr Opin Genet Dev. 1998;8: 588-94.
35. Siddiq A, Aminova LR, Troy CM, Suh K, Messer Z, Semenza GL, et al. Selective inhibition of hypoxia-inducible factor (HIF) prolyl-hydroxylase 1 mediates neuroprotection against normoxic oxidative death via HIF- and CREB-independent pathways. J Neurosci. 2009;29: 8828-38.
36. Souvenir R, Fathali N, Ostrowski RP, Lekic T, Zhang JH, Tang J. Tissue inhibitor of matrix metalloproteinase-1 mediates erythropoietin-induced neuroprotection in hypoxia ischemia. Neurobiol Dis. 2011;44: 28-37.
37. Sowers JR, Epstein M, Frohlich ED. Diabetes, hypertension, and cardiovascular disease: an update. Hypertension. 2001;37: 1053-9.
38. Stebbins GT, Goetz CG, Lang AE, Cubo E. Factor analysis of the motor section of the unified Parkinson's disease rating scale during the off-state. Mov Disord. 1999;14: 585-9.
39. Sun Y, Calvert JW, Zhang JH. Neonatal hypoxia/ischemia is associated with decreased inflammatory mediators after erythropoietin administration. Stroke. 2005;36: 1672-8.
40. Wang L, Chopp M, Gregg SR, Zhang RL, Teng H, Jiang A, et al. Neural progenitor cells treated with EPO induce angiogenesis through the production of VEGF. J Cereb Blood Flow Metab. 2008;28: 1361-8.
41. Yeo EJ, Cho YS, Kim MS, Park JW. Contribution of HIF-1alpha or HIF-2alpha to erythropoietin expression: in vivo evidence based on chromatin immunoprecipitation. Ann Hematol. 2008;87: 11-7.
42. Zagorska A, Dulak J. HIF-1: the knowns and unknowns of hypoxia sensing. Acta Biochim Pol. 2004;51: 563-85.