Hypoxia-inducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibitor-1 gene expression by insulin in primary rat hepatocytes

Blood

Volumn 101, Issue 3, 2003, Pages 907-914

  Kietzmann, Thomas ^a   Samoylenko, Anatoly ^a   Roth, Ulrike ^a   Jungermann, Kurt ^a  

^a Inst fur Biochem/Molek Zellbiol   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROPOIETIN; HYPOXIA INDUCIBLE FACTOR 1; INSULIN; LUCIFERASE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN HRE1; PROTEIN HRE2; PROTEIN KINASE B; UNCLASSIFIED DRUG; WORTMANNIN;

ANIMAL CELL; ARTICLE; CELL HYPOXIA; CELL TYPE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ELECTROPHORETIC MOBILITY; ENZYME ACTIVITY; GENE CONSTRUCT; GENE EXPRESSION; GENE ISOLATION; GENE OVEREXPRESSION; LIVER CELL; MALE; NONHUMAN; PAI1 GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INDUCTION; PROTEIN RNA BINDING; RAT; SIGNAL TRANSDUCTION;

EID: 0037307621     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2002-06-1693     Document Type: Article

References (83)

1. Lijnen HR, Collen D. Mechanisms of plasminogen activation by mammalian plasminogen activators. Enzyme. 1988;40:90-96.
2. Kruithof EK, Vassalli JD, Schleuning WD, Mattaliano RJ, Bachmann F. Purification and characterization of a plasminogen activator inhibitor from the histiocytic lymphoma cell line U-937. J Biol Chem. 1986;261:11207-11213.
3. Erickson LA, Hekman CM, Loskutoff DJ. The primary plasminogen-activator inhibitors in endothelial cells, platelets, serum, and plasma are immunologically related. Proc Natl Acad Sci U S A. 1985;82:8710-8714.
4. Reilly CF, McFall RC. Platelet-derived growth factor and transforming growth factor-β regulate plasminogen activator inhibitor-1 synthesis in vascular smooth muscle cells. J Biol Chem. 1991;266:9419-9427.
5. Heaton JH, Nebes VL, O'Dell LG, Morris S-MJ, Gelehrter TD. Glucocorticoid and cyclic nucleotide regulation of plasminogen activator and plasminogen activator-inhibitor gene expression in primary cultures of rat hepatocytes. Mol Endocrinol. 1989;3:185-192.
6. Busso N, Nicodeme E, Chesne C, et al. Urokinase and type I plasminogen activator inhibitor production by normal human hepatocytes: modulation by inflammatory agents. Hepatology. 1994;20:186-190.
7. Schneiderman J, Sawdey MS, Keeton MR, et al. Increased type 1 plasminogen activator inhibitor gene expression in atherosclerotic human arteries. Proc Natl Acad Sci U S A. 1992;89:6998-7002.
8. Carmeliet P, Stassen JM, Schoonjans L, et al. Plasminogen activator inhibitor-1 gene-deficient mice. II. Effects on hemostasis, thrombosis, and thrombolysis. J Clin Invest. 1993;92:2756-2760.
9. Eitzman DT, McCoy RD, Zheng X, et al. Bleomycin-induced pulmonary fibrosis in transgenic mice that either lack or overexpress the murine plasminogen activator inhibitor-1 gene. J Clin Invest. 1996;97:232-237.
10. Landin K, Tengborn L, Smith U. Elevated fibrinogen and plasminogen activator inhibitor (PAI-1) in hypertension are related to metabolic risk factors for cardiovascular disease. J Intern Med. 1990;227:273-278.
11. Juhan-Vague I, Alessi MC. PAI-1, obesity, insulin resistance and risk of cardiovascular events. Thromb Haemost. 1997;78:656-660.
12. Mirza AM, Kohn AD, Roth RA, McMahon M. Oncogenic transformation of cells by a conditionally active form of the protein kinase Akt/PKB. Cell Growth Differ. 2000;11:279-292.
13. Carmassi F, Morale M, Ferrini L, et al. Local insulin infusion stimulates expression of plasminogen activator inhibitor-1 and tissue-type plasminogen activator in normal subjects. Am J Med. 1999;107:344-350.
14. Kooistra T, Bosma PJ, Tons HA, et al. Plasminogen activator inhibitor 1: biosynthesis and mRNA level are increased by insulin in cultured human hepatocytes. Thromb Haemost. 1989;62:723-728.
15. Grenett HE, Benza RL, Li XN, et al. Expression of plasminogen activator inhibitor type I in genotyped human endothelial cell cultures: genotype-specific regulation by insulin. Thromb Haemost. 1999;82:1504-1509.
16. Alessi MC, Juhan-Vague I, Kooistra T, Declerck PJ, Collen D. Insulin stimulates the synthesis of plasminogen activator inhibitor 1 by the human hepatocellular cell line Hep G2. Thromb Haemost. 1988;60:491-494.
17. Anfosso F, Chomiki N, Alessi MC, Vague P, Juhan-Vague I. Plasminogen activator inhibitor-1 synthesis in the human hepatoma cell line Hep G2. Metformin inhibits the stimulating effect of insulin. J Clin Invest. 1993;91:2185-2193.
18. Schneider DJ, Nordt TK, Sobel BE. Stimulation by proinsulin of expression of plasminogen activator inhibitor type-I in endothelial cells. Diabetes. 1992;41:890-895.
19. Schneider DJ, Absher PM, Ricci MA. Dependence of augmentation of arterial endothelial cell expression of plasminogen activator inhibitor type 1 by insulin on soluble factors released from vascular smooth muscle cells. Circulation. 1997;96:2868-2876.
20. Saltiel AR, Kahn CR. Insulin signalling and the regulation of glucose and lipid metabolism. Nature. 2001;414:799-806.
21. Shepherd PR, Nave BT, Rincon J, et al. Involvement of phosphoinositide 3-kinase in insulin stimulation of MAP-kinase and phosphorylation of protein kinase-B in human skeletal muscle: implications for glucose metabolism. Diabetologia. 1997;40:1172-1177.
22. Lietzke SE, Bose S, Cronin T, et al. Structural basis of 3-phosphoinositide recognition by pleckstrin homology domains. Mol Cell. 2000;6:385-394.
23. Alessi DR, James SR, Downes CP, et al. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol. 1997;7:261-269.
24. Taha C, Liu Z, Jin J, et al. Opposite translational control of GLUT1 and GLUT4 glucose transporter mRNAs in response to insulin. Role of mammalian target of rapamycin, protein kinase B, and phosphatidylinositol 3-kinase in GLUT1 mRNA translation. J Biol Chem. 1999;274:33085-33091.
25. Granner D, Pilkis S. The genes of hepatic glucose metabolism. J Biol Chem. 1990;265:10173-10176.
26. Snyder SH, Jaffrey SR. Vessels vivified by Akt acting on NO synthase. Nat Cell Biol. 1999;1: E95-E96.
27. Masuda S, Chikuma M, Sasaki R. Insulin-like growth factors and insulin stimulate erythropoietin production in primary cultured astrocytes. Brain Res. 1997;746:63-70.
28. Sato K, Yamazaki K, Shizume K, et al. Stimulation by thyroid-stimulating hormone and Grave's immunoglobulin G of vascular endothelial growth factor mRNA expression in human thyroid follicles in vitro and fit mRNA expression in the rat thyroid in vivo. J Clin Invest. 1995;96:1295-1302.
29. Loike JD, Cao L, Brett J, et al. Hypoxia induces glucose transporter expression in endothelial cells. Am J Physiol. 1992;263:C326-C333.
30. Semenza GL, Jiang BH, Leung SW, et al. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem. 1996;271:32529-32537.
31. Melillo G, Musso T, Sica A, et al. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med. 1995;182:1683-1693.
32. Goldberg MA, Dunning SP, Bunn HF. Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science. 1988;242:1412-1415.
33. Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996;16:4604-4613.
34. 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;94:4177-4185.
35. Semenza GL. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med. 2001;7:345-350.
36. Wenger RH. Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J. 2002;16:1151-1162.
37. Zelzer E, Levy Y, Kahana C, et al. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1 alpha/ARNT. EMBO J. 1998;17:5085-5094.
38. Feldser D, Agani F, Iyer NV, et al. Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res. 1999;59:3915-3918.
39. Stiehl DP, Jelkmann W, Wenger RH, Hellwig-Burgel T. Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1 beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett. 2002;512:157-162.
40. Zhong H, Chiles K, Feldser D, et al. Modulation of hypoxia-inducible factor 1alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 2000;60:1541-1545.
41. Bruzdzinski CJ, Riordan-Johnson M, Nordby EC, Suter SM, Gelehrter TD. Isolation and characterization of the rat plasminogen activator inhibitor-1 gene. J Biol Chem. 1990;265:2078-2085.
42. 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;354:531-537.
43. Franke TF, Yang SI, Chan TO, et al. The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell. 1995;81:727-736.
44. Makino Y, Kanopka A, Wilson WJ, Tanaka H, Poellinger L. IPAS is an hypoxia-inducible splicing variant of the HIF-3alpha locus. J Biol Chem. 2002;277:32405-32408.
45. Zeheb R, Rafferty UM, Rodriguez MA, Andreasen P, Gelehrter TD. Immunoaffinity purification of HTC rat hepatoma cell plasminogen activator-inhibitor-1. Thromb Haemost. 1987;58:1017-1023.
46. 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;334:141-146.
47. Meier R, Thelen M, Hemmings BA. Inactivation and dephosphorylation of protein kinase Balpha (PKBalpha) promoted by hyperosmotic stress. EMBO J. 1998;17:7294-7303.
48. Coffer PJ, Woodgett JR. Molecular cloning and characterlsation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur J Biochem. 1991;201:475-481.
49. Samoylenko A, Roth U, Jungermann K, Kietzmann T. The upstream stimulatory factor-2a inhibits plasminogen activator inhibitor-1 gene expression by binding to a promoter element adjacent to the hypoxia-inducible factor-1 binding site. Blood. 2001;97:2657-2666.
50. Kvietikova I, Wenger RH, Marti HH, Gassmann M. The transcription factors ATF-1 and CREB-1 bind constitutively to the hypoxia-inducible factor-1 (HIF-1) DNA recognition site. Nucleic Acids Res. 1995;23:4542-4550.
51. Alessi DR, Andjelkovic M, Caudwell B, et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 1996;15:6541-6551.
52. Semenza GL. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J Appl Physiol. 2000;88:1474-1480.
53. Pilkis SJ, Granner DK. Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Physiol. 1992;54:885-909.
54. Bunn HF, Poyton RO. Oxygen sensing and molecular adaptation to hypoxia. Physiol Rev. 1996;76:839-885.
55. Richard DE, Berra E, Pouyssegur J. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells. J Biol Chem. 2000;275:26765-26771.
56. 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.
57. Hellwig-Burgel T, Rutkowski K, Metzen E, Fandrey J, Jelkmann W. Interleukin-1 beta and tumor necrosis factor-alpha stimulate DNA binding of hypoxia-inducible factor-1. Blood. 1999;94:1561-1567.
58. Jaakkola P, Mole DR, Tian YM, et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 2001;292:468-472.
59. Ivan M, Kondo K, Yang H, et al. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001;292:464-468.
60. Lando D, Peet DJ, Whelan DA, Gorman J, Whitelaw ML. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science. 2002;295:858-861.
61. 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;19:4298-4309.
62. Richard DE, Berra E, Gothie E, Roux D, Pouyssegur J. p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1al-pha (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J Biol Chem. 1999;274:32631-32637.
63. Zundel W, Swiersz LM, Giaccia A. Caveolin 1-mediated regulation of receptor tyrosine kinase-associated phosphatidylinositol 3-kinase activity by ceramide. Mol Cell Biol. 2000;20:1507-1514.
64. Sodhi A, Montaner S, Miyazaki H, Gutkind JS. MAPK and Akt act cooperatively but independently on hypoxia inducible factor-1alpha in rasV12 upregulation of VEGF. Biochem Biophys Res Commun. 2001;287:292-300.
65. Mazure NM, Chen EY, Laderoute KR, Giaccia AJ. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-rastransformed cells through a hypoxia inducible factor-1 transcriptional element. Blood. 1997;90:3322-3331.
66. Chen EY, Mazure NM, Cooper JA, Giaccia AJ. Hypoxia activates a platelet-derived growth factor receptor/phosphatidylinositol 3-kinase/Akt pathway that results in glycogen synthase kinase-3 inactivation. Cancer Res. 2001;61:2429-2433.
67. Sandau KB, Faus HG, Brune B. Induction of hypoxia-inducible-factor 1 by nitric oxide is mediated via the PI 3K pathway. Biochem Biophys Res Commun. 2000;278:263-267.
68. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1alpha (HIF-1alpha) synthesis: Novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol. 2001;21:3995-4004.
69. Treins C, Giorgetti-Peraldi S, Murdaca J, Semenza GL, Van Obberghen E. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J Biol Chem. 2002;277:27975-27981.
70. Jiang BH, Jiang G, Zheng JZ, et al. Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1. Cell Growth Differ. 2001;12:363-369.
71. Arsham AM, Plas DR, Thompson CB, Simon MC. Phosphatidylinositol 3-kinase/Akt signaling is neither required for hypoxic stabilization of HIF-1 alpha nor sufficient for HIF-1-dependent target gene transcription. J Biol Chem. 2002;277:15162-15170.
72. Alvares-Tejado M, Alfranca A, Aragones J, et al. Lack of evidence for the involvement of the phosphoinositide 3-kinase/Akt pathway in the activation of hypoxia-inducible factors by low oxygen tension. J Biol Chem. 2002;277:13508-13517.
73. Takahashi H, Uno S, Watanabe Y, Arakawa K, Nakagawa S. Expression of nerve growth factor-induced type 1 plasminogen activator inhibitor (PAI-1) mRNA is inhibited by genistein and wortmannin. Neuroreport. 2000;11:1111-1115.
74. Banfi C, Eriksson P, Giandomenico G, et al. Transcriptional regulation of plasminogen activator inhibitor type 1 gene by insulin: insights into the signaling pathway. Diabetes. 2001;50:1522-1530.
75. Fink T, Kazlauskas A, Poellinger L, Ebbesen P, Zachar V. Identification of a tightly regulated hypoxia-response element in the promoter of human plasminogen activator inhibitor-1. Blood. 2002;99:2077-2083.
76. Lee SH, Wolf PL, Escudero R, et al. Early expression of angiogenesis factors in acute myocardial ischemia and infarction. N Engl J Med. 2000;342:626-633.
77. Bastard JP, Pieroni L, Hainque B. Relationship between plasma plasminogen activator inhibitor 1 and insulin resistance. Diabetes Metab Res Rev. 2000;16:192-201.
78. Kohler HP, Grant PJ. Plasminogen-activator inhibitor type 1 and coronary artery disease. N Engl J Med. 2000;342:1792-1801.
79. Wiman B. Plasminogen activator inhibitor 1 (PAI-1) in plasma: its role in thrombotic disease. Thromb Haemost. 1995;74:71-76.
80. Grant PJ, Kruithof EK, Felley CP, Felber JP, Bachmann F. Short-term infusions of insulin, triacylglycerol and glucose do not cause acute increases in plasminogen activator inhibitor-1 concentrations in man. Clin Sci (Lond). 1990;79:513-516.
81. Landin K, Tengborn L, Chmielewska J, von-Schenck H, Smith U. The acute effect of insulin on tissue plasminogen activator and plasminogen activator inhibitor in man. Thromb Haemost. 1991;65:130-133.
82. Vuorinen-Markkola H, Puhakainen I, Yki-Jarvinen H. No evidence for short-term regulation of plasminogen activator inhibitor activity by insulin in man. Thromb Haemost. 1992;67:117-120.
83. Calles-Escandon J, Mirza SA, Sobel BE, Schneider DJ. Induction of hyperinsulinemia combined with hyperglycemia and hypertriglyceridemia increases plasminogen activator inhibitor 1 in blood in normal human subjects. Diabetes. 1998;47:290-293.