Reactive oxygen species modulate HIF-I mediated PAI-I expression: Involvement of the GTPase RacI

Thrombosis and Haemostasis

Volumn 89, Issue 5, 2003, Pages 926-935

  Görlach, Agnes ^a   Berchner Pfannschmidt, Utta ^b   Wotzlaw, Christoph ^b   Cool, Robbert H ^b   Fandrey, Joachim ^c   Acker, Helmut ^b   Jungermann, Kurt ^d   Kietzmann, Thomas ^d  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^c UNIVERSITY OF DUISBURG ESSEN   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Fibrinolysis; Hypoxia; PAI 1; RacI; Reactive oxygen species; Thrombosis

Indexed keywords

ANTIOXIDANT; GUANOSINE TRIPHOSPHATASE; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; PYRROLIDINE DITHIOCARBAMATE; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ARTICLE; CELL ACTIVITY; CELL CULTURE; CELL HYPOXIA; CONTROLLED STUDY; DRUG EFFECT; FIBRINOLYSIS; GENE EXPRESSION; GENE OVEREXPRESSION; HYPOXIA; MALE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT; RAT STRAIN; THROMBOSIS;

EID: 0037954222     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-0037-1613480     Document Type: Article

References (59)

1. Loskutoff DJ, Quigley JP. PAI-1, fibrosis, and the elusive provisional fibrin matrix. J Clin Invest 2000; 106: 1441-3.
2. Anreasen PA, Egelund R, Petersen HH. The plasminogen activation system in tumor growth, invasion, and metastasis. Cell Mol Life Sci 2000; 57: 25-40.
3. Huber K. Plasminogen activator inhibitor type-1 (part one): Basic mechanisms, regulation, and role for thromboembolic disease. J Thromb Thrombolysis 2001; 11: 183-93.
4. Eitzman DT, Westrick RJ, Xu Z, Tyson J, Ginsburg D. Plasminogen activator inhibitor-1 deficiency protects against atherosclerosis progression in the mouse carotid artery. Blood 2000; 96: 4212-5.
5. Kietzmann T, Roth U, Jungermann K. Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia inducible factor-1 in rat hepatocytes. Blood 1999; 94: 4177-85.
6. Bunn HF, Poyton RO. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev 1996; 76: 839-85.
7. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 2000; 35: 71-103.
8. Wenger RH. Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J 2002; 16: 1151-62.
9. Gorlach A, Kietzmann T, Hess J. Redox signaling through NADPH oxidases: Involvement in vascular proliferation and coagulation. Ann N Y Acad Sci 2002; 973: 505-7.
10. Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2002; 82: 47-95.
11. Martindale JL, Holbrook NJ. Cellular response to oxidative stress: Signaling for suicide and survival. J Cell Physiol 2002; 192: 1-15.
12. Sarti P, Avigliano L, Gorlach A, Brune B. Superoxide and nitric oxide-participation in cell communication. Cell Death Differ 2002; 9: 1160-2.
13. Bowie A, O'Neill LA. Oxidative stress and nuclear factor-kappaB activation: A reassessment of the evidence in the light to recent discoveries. Biochem Pharmacol 2000; 59: 13-23.
14. Kietzmann T, Friemann S, Bratke J, Jungermann K. Regulation of the gluconeogenic phosphoenolpyruvate carboxykinase and glycolytic aldolase A gene expresion by O2 in rat hepatocyte cultures. Involvement of hydrogen peroxide as mediator in the response to O2. FEBS Lett 1996; 388: 228-32.
15. Kietzmann T, Porwol T, Zierold K, Jungermann K, Acker H. Involvement of a local Fenton reaction in the reciprocal modulation by O2 of the glucagon-dependent activation of the phosphoenolpyruvate carboxykinase gene and the insulin-dependent activation of the glucokinase gene in rat hepatocytes. Biochem J 1998; 335: 425-32.
16. Fandrey J, Frede S, Jelkmann W. Role of hydrogen peroxide in hypoxia-induced erythropoietin production. Biochem J 1994; 303: 507-10.
17. Kietzmann T, Roth U, Freimann S, Jungermann K. Arterial oxygen partial pressures reduce the insulin-dependent induction of the perivenously located glucokinase in rat hepatocyte cultures: Mimicry of arterial oxygen pressures by H2O2. Biochem J 1997; 321: 17-20.
18. Kroll SL, Czyzyk KM. Role of H2O2 and heme-containing O2 sensors in hypoxic regulation of tyrosine hydroxylase gene expression. Am J Physiol 1998; 274: C167-C74.
19. Semenza GL. HIF-1: Mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol 2000; 88: 1474-80.
20. Semenza GL. Perspectives on oxygen sensing. Cell 1999; 98: 281-4.
21. Wenger RH, Gassmann M. Oxygen(es) and the hypoxia-inducible factor-1. Biol Chem 1997; 378: 609-16.
22. Huang LE, Arany Z, Livingston DM, Bunn HF. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 1996; 271: 32253-9.
23. Ema M, Hirota K, Mimura J, Abe H, Yodoi J, Sogawa K et al. Molecular mechanisms of transcription activation by HLF and HIF1alpha in response to hypoxia: Their stabilization and redox signal-induced interaction with CBP/p300. EMBO J 1999; 18: 1905-14.
24. Carrero P, Okamoto K, Coumailleau P, O'Brien S, Tanaka H, Poellinger L. Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1alpha. Mol Cell Biol 2000; 20: 402-15.
25. Griendling KK, Harrison DG. Dual role of reactive oxygen species in vascular growth. Circ Res 1999; 85: 562-3.
26. Lambeth JD. Nox/Duox family of nicotinamide adenine dinucleotide (phosphate) oxidases. Curr Opin Hematol 2002; 9: 11-7.
27. Gorlach A, Holtermann G, Jelkmann W, Hancock JT, Jones SA, Jones Jones OT et al. Photometric characteristics of haem proteins in erythropoietin-producing hepatoma cells (HepG2). Biochem J 1993; 290: 771-6.
28. Babior BM. NADPH oxidase: An update. Blood 1999; 93: 1464-76.
29. Bokoch GM, Diebold BA. Current molecular models for NADPH oxidase regulation by Rac GTPase. Blood 2002; 100: 2692-5.
30. Cool RH, Merten E, Theiss C, Acker H. Rac1, and not Rac2, is involved in the regulation of the intracellular hydrogen peroxide level in HepG2 cells. Biochem J 1998; 332: 5-8.
31. Kietzmann T, Cornesse Y, Brechtel K, Modaressi S, Jungermann K. Perivenous expression of the mRNA of the three hypoxia-inducible factor alpha-subunits, HIF1alpha, HIF2alpha and HIF3alpha, in rat liver. Biochem J 2001; 354: 531-7.
32. Herkert O, Diebold I, Brandes RP, Hess J, Busse R, Gorlach A. NADPH oxidase medicates tissue factor-dependent surface procoagulant activity by thrombin in human vascular smooth muscle cells. Circulation 2002; 105: 2030-6.
33. Immenschuh S, Hinke V, Ohlmann A, et al. Transcriptional activation of the haem oxygenase-1 gene by cGMP via a cAMP response element/activator protein-1 element in primary cultures of rat hepatocytes. Biochem J 1998; 334: 141-6.
34. Gorlach A, Brandes RP, Bassus S, Kronemann N, Kirchmaier CM, Busse R et al. Oxidative stress and expression of p22phox are involved in the up-regulation of tissue factor in vascular smooth muscle cells in response to activated platelets. FASEB J 2000; 14: 1518-28.
35. Strohmaier AR, Porwol T, Acker H, Spiess E. Three-dimensional organization of microtubules in tumor cells studied by confocal laser scanning microscopy and computer-assisted deconvolution and image reconstruction. Cells Tissues Organs 2000; 167: 1-8.
36. Sundaresan M, Yu ZX, Ferrans VJ, Sulciner DJ, Gutkind JS, Irani K et al. Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. Biochem J 1996; 318: 379-82.
37. Sulciner DJ, Irani K, Yu ZX, Ferrans VJ, Goldschmidt-Clermont P, Finkel T. Rac1 regulates a cytokine-stimulated, redox-dependent pathway necessary for NF-kappaB activation. Mol Cell Biol 1996; 16: 7115-21.
38. Ozaki M, Deshpande SS, Angkeow P, Suzuki S, Irani K. Rac1 regulates stress-induced, redox-dependent heat shock factor activation. J Biol Chem 2000; 275: 35377-83.
39. Price MO, Atkinson SJ, Knaus UG, Dinauer MC. Rac activation induces NADPH oxidase activity in transgenic COSphox cells and levels of superoxide production is exchange factor-dependent. J Biol Chem 2002; 277: 19220-8.
40. Rosner JL, Storz G. Regulation of bacterial responses to oxidative stress. Curr Top Cell Regul 1997; 35: 163-77.
41. Demple B. Study of redox-regulated transcription factors in prokaryotes. Methods 1997; 11: 267-78.
42. Ridley AJ. Rho proteins: Linking signaling with membrane trafficking. Traffic 2001; 2: 303-10.
43. Feig LA. Tools of the trade: Use of dominant-inhibitory mutants of Ras-family GTPases. Nat Cell Biol 1999; 1: E25-E27.
44. Bowie A, Moynagh PN, O'Neill LA. Mechanism of NF kappa B activation by interleukin-1 and tumour necrosis factor in endothelial cells. Biochem Soc Trans 1996; 24: 2S.
45. Nathens AB, Bitar R, Davreaux C, Bujard M, Marshall JC, Dackiw AP et al. Pyrrolidine dithiocarbamate attenuates endotoxin-induced acute lung injury. Am J Respir Cell Mol Biol 1997; 17: 608-16.
46. Nobel CS, Kimland M, Lind B, Orrenius S, Slater AFG. Dithiocarbamates induce apoptosis in thymocytes by raising the intracellular level of redox-active copper. J Biol Chem 1995; 270: 26202-8.
47. Orrenius S, Nobel CS, Van Den Dobbelsteen DJ, Burkitt MJ, Slater AF. Dithiocarbamates and the redox regulation of cell death. Biochem Soc Trans 1996; 24: 1032-8.
48. Haddad JJ, Olver RE, Land SC. Antioxidant/pro-oxidant equilibrium regulates HIF-1alpha and NF-kappa B redox sensitivity. Evidence for inhibition by glutathione oxidation in alveolar epithelial cells. J Biol Chem 2000; 275: 21130-9.
49. Tanimoto K, Makino Y, Pereira T, Poellinger L. Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J 2000; 19: 4298-309.
50. Hirota K, Semenza GL. Rac1 activity is required for the activation of hypoxia-inducible factor 1. J Biol Chem 2001; 276: 21166-72.
51. Chandel NS, Schumacker PT. Cellular oxygen sensing by mitochondria: Old questions, new insight. J Appl Physiol 2000; 88: 1880-9.
52. Haddad JJ, Land SC. O(2)-evoked regulation of HIF-1alpha and NF-kappaB in perinatal lung epithelium requires glutathione biosynthesis. Am J Physiol Lung Cell Mol Physiol 2000; 278: L492-L503.
53. Vaux EC, Metzen E, Yeates KM, Ratcliffe PJ. Regulation of hypoxia-inducible factor is preserved in the absence of a functioning mitochondrial respiratory chain. Blood 2001; 98: 296-302.
54. 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: 43-54.
55. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001; 294: 1337-40.
56. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 2002; 16: 1466-71.
57. Zhu H, Qiu H, Yoon HW, Huang S, Bunn HF. Identification of a cytochrome b-type NAD(P)H oxidoreductase ubiquitously expressed in human cells. Proc Natl Acad Sci U S A 1999; 96: 14742-7.
58. Wenger RH, Marti HH, Schuerer MC, et al.. Hypoxic induction of gene expression in chronic granulomatous disease-derived B-cell lines: Oxygen sensing is independent of the cytochrome b558-containing nicotinamide adenine dinucleotide phosphate oxidase. Blood 1996; 87: 756-61.
59. Gorlach A, Diebold I, Schini-Kerth VB, et al.. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: Role of the p22(phox)-containing NADPH oxidase. Circ Res 2001; 89: 47-54.