PL EN


Preferences help
enabled [disable] Abstract
Number of results
2003 | 50 | 1 | 49-59
Article title

Reciprocal regulation between nitric oxide and vascular endothelial growth factor in angiogenesis.

Content
Title variants
Languages of publication
EN
Abstracts
EN
Physiologically, angiogenesis is tightly regulated, or otherwise it leads to pathological processes, such as tumors, inflammatory diseases, gynecological diseases and diabetic retinopathy. The vascular endothelial growth factor (VEGF) is a potent and critical inducer of angiogenesis. The VEGF gene expression is regulated by a variety of stimuli. Hypoxia is one of the most potent inducers of the VEGF expression. The hypoxia inducible factor 1 (HIF-1) plays as a key transcription factor in hypoxia-mediated VEGF gene upregulation. Nitric oxide (NO) as well as hypoxia is reported to upregulate the VEGF gene by enhancing HIF-1 activity. The Akt/protein kinase B (PKB) pathway may be involved in NO-mediated HIF-1 activation in limited cell lines. There are some reports of negative effects of NO on HIF-1 and VEGF activity. These conflicting data of NO effects may be attributed mainly to the amount of released NO. Indeed, NO can be a positive or negative modulator of the VEGF gene under the same conditions simply by changing its amounts. The VEGF-mediated angiogenesis requires NO production from activated endothelial NO synthase (eNOS). Activation of eNOS by VEGF involves several pathways including Akt/PKB, Ca2+/calmodulin, and protein kinase C. The NO-mediated VEGF expression can be regulated by HIF-1 and heme oxygenase 1 (HO-1) activity, and the VEGF-mediated NO production by eNOS can be also modulated by HIF-1 and HO-1 activity, depending upon the amount of produced NO. These reciprocal relations between NO and VEGF may contribute to regulated angiogenesis in normal tissues.
Year
Volume
50
Issue
1
Pages
49-59
Physical description
Dates
published
2003
received
2003-01-02
accepted
2003-03-04
References
  • Adam MF, Dorie MJ, Brown JM. (1999) Oxygen tension measurements of tumors growing in mice. Int J Radiat Oncol Biol Phys.; 45: 171-80.
  • Alvarez-Tejado M, Alfranca A, Aragones J, Vara A, Landazuri MO, del Peso L. (2002) 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.; 277: 13508-17.
  • Arsham AM, Plas DR, Thompson CB, Simon MC. (2002) 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.; 277: 15162-70.
  • Berra E, Milanini J, Richard DE, Le Gall M, Vinals F, Gothie E, Roux D, Pages G, Pouyssegur J. (2000) Signaling angiogenesis via p42/p44 MAP kinase and hypoxia. Biochem Pharmacol.; 60: 1171-8.
  • Blancher C, Moore JW, Robertson N, Harris AL. (2001) Effects of ras and von Hippel-Lindau. (VHL) gene mutations on hypoxia-inducible factor (HIF)-1alpha HIF-2alpha and vascular endothelial growth factor expression and their regulation by the phosphatidylinositol 3'-kinase/Akt signaling pathway. Cancer Res.; 61: 7349-55.
  • Brann DW, Bhat GK, Lamar CA, Mahesh VB. (1997) Gaseous transmitters and neuroendocrine regulation. Neuroendocrinology.; 65: 385-95.
  • Brouet A, Sonveaux P, Dessy C, Balligand JL, Feron O. (2001) Hsp90 ensures the transition from the early Ca2+-dependent to the late phosphorylation-dependent activation of the endothelial nitric-oxide synthase in vascular endothelial growth factor-exposed endothelial cells. J Biol Chem.; 276: 32663-9.
  • Bruick RK, McKnight SL. (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science.; 294: 1337-40.
  • Busse R, Mulsch A. (1990) Induction of nitric oxide synthase by cytokines in vascular smooth muscle cells. FEBS Lett.; 275: 87-90.
  • Carmeliet P. (2000) Mechanisms of angiogenesis and arteriogenesis. Nat Med.; 6: 389-95.
  • Carvajal JA, Germain AM, Huidobro-Toro JP, Weiner CP. (2000) Molecular mechanism of cGMP-mediated smooth muscle relaxation. J Cell Physiol.; 184: 409-20.
  • Chin K, Kurashima Y, Ogura T, Tajiri H, Yoshida S, Esumi H. (1997) Induction of vascular endothelial growth factor by nitric oxide in human glioblastoma and hepatocellular carcinoma cells. Oncogene.; 15: 437-42.
  • Cockman ME, Masson N, Mole DR, Jaakkola P, Chang GW, Clifford SC, Maher ER, Pugh CW, Ratcliffe PJ, Maxwell PH. (2000) Hypoxia inducible factor-alpha binding and ubiquitylation by the von Hippel-Lindau tumor suppressor protein. J Biol Chem.; 275: 25733-41.
  • Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature.; 399: 601-5.
  • Dulak J, Jozkowicz A, Dembinska-Kiec A, Guevara I, Zdzienicka A, Zmudzinska- Grochot D, Florek I, Wojtowicz A, Szuba A, Cooke JP. (2000) Nitric oxide induces the synthesis of vascular endothelial growth factor by rat vascular smooth muscle cells. Arterioscler Thromb Vasc Biol.; 20: 659-66.
  • Dulak J, Jozkowicz A, Foresti R, Kasza A, Frick M, Huk I, Green CJ, Pachinger O, Weidinger F, Motterlini R. (2002) Heme oxygenase activity modulates vascular endothelial growth factor synthesis in vascular smooth muscle cells. Antioxid Redox Signal.; 4: 229-40.
  • Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, Ratcliffe PJ. (2001) C.elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell.; 107: 43-54.
  • Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL. (1999) Reciprocal positive regulation of hypoxia-inducible factor 1alpha and insulin-like growth factor 2. Cancer Res.; 59: 3915-8.
  • Feng Y, Venema VJ, Venema RC, Tsai N, Caldwell RB. (1999) VEGF induces nuclear translocation of Flk-1/KDR endothelial nitric oxide synthase and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun.; 256: 192-7.
  • Furchgott RF, Zawadzki JV. (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature.; 288: 373-6.
  • Gelinas DS, Bernatchez PN, Rollin S, Bazan NG, Sirois MG. (2002) Immediate and delayed VEGF-mediated NO synthesis in endothelial cells: role of PI3K PKC and PLC pathways. Br J Pharmacol.; 137: 1021-30.
  • Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. (1998) Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem.; 273: 30336-43.
  • Gruetter CA, Barry BK, McNamara DB, Gruetter DY, Kadowitz PJ, Ignarro L. (1979) Relaxation of bovine coronary artery and activation of coronary arterial guanylate cyclase by nitric oxide nitroprusside and a carcinogenic nitrosoamine. J Cyclic Nucleotide Res.; 5: 211-24.
  • He H, Venema VJ, Gu X, Venema RC, Marrero MB, Caldwell RB. (1999) Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J Biol Chem.; 274: 25130-5.
  • Huang LE, Gu J, Schau M, Bunn HF. (1998) Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci U S A.; 95: 7987-92.
  • Huang LE, Willmore WG, Gu J, Goldberg MA, Bunn HF. (1999) Inhibition of hypoxia-inducible factor 1 activation by carbon monoxide and nitric oxide. Implications for oxygen sensing and signaling. J Biol Chem.; 274: 9038-44.
  • Ignarro LJ. (1992) Haem-dependent activation of cytosolic guanylate cyclase by nitric oxide: a widespread signal transduction mechanism. Biochem Soc Trans.; 20: 465-9.
  • Ignarro LJ. (1996) Physiology and pathophysiology of nitric oxide. Kidney Int Suppl.; 55: S2-5.
  • Ikeda E, Achen MG, Breier G, Risau W. (1995) Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J Biol Chem.; 270: 19761-6.
  • Kallio PJ, Wilson WJ, O'Brien S, Makino Y, Poellinger L. (1999) Regulation of the hypoxia-inducible transcription factor 1alpha by the ubiquitin-proteasome pathway. J Biol Chem.; 274: 6519-25.
  • Kimura H, Ogura T, Kurashima Y, Weisz A, Esumi H. (2002) Effects of nitric oxide donors on vascular endothelial growth factor gene induction. Biochem Biophys Res Commun.; 296: 976-82.
  • Kimura H, Weisz A, Kurashima Y, Hashimoto K, Ogura T, D'Acquisto F, Addeo R, Makuuchi M, Esumi H. (2000) Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood.; 95: 189-97.
  • Kimura H, Weisz A, Ogura T, Hitomi Y, Kurashima Y, Hashimoto K, D'Acquisto F, Makuuchi M, Esumi H. (2001) Identification of hypoxia-inducible factor 1 ancillary sequence and its function in vascular endothelial growth factor gene induction by hypoxia and nitric oxide. J Biol Chem.; 276: 2292-8.
  • Klagsbrun M, D'Amore PA. (1996) Vascular endothelial growth factor and its receptors. Cytokine Growth Factor Rev.; 7: 259-70.
  • Knowles RG, Moncada S. (1994) Nitric oxide synthases in mammals. Biochem J.; 298: 249-58.
  • Kramer BK, Bucher M, Sandner P, Ittner KP, Riegger GA, Ritthaler T, Kurtz A. (1997) Effects of hypoxia on growth factor expression in the rat kidney in vivo. Kidney Int.; 51: 444-7.
  • Kroll J, Waltenberger J. (1998) VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2. (KDR). Biochem Biophys Res Commun.; 252: 743-6.
  • Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL. (2001) 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.; 21: 3995-4004.
  • Levy AP, Levy NS, Goldberg MA. (1996) Post-transcriptional regulation of vascular endothelial growth factor by hypoxia. J Biol Chem.; 271: 2746-53.
  • Liu Y, Christou H, Morita T, Laughner E, Semenza GL, Kourembanas S. (1998) Carbon monoxide and nitric oxide suppress the hypoxic induction of vascular endothelial growth factor gene via the 5' enhancer. J Biol Chem.; 273: 15257-62.
  • Marti HH, Risau W. (1998) Systemic hypoxia changes the organ-specific distribution of vascular endothelial growth factor and its receptors. Proc Natl Acad Sci U S A.; 95: 15809-14.
  • Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature.; 399: 271-5.
  • Mayer B. (1994) Nitric oxide/cyclic GMP-mediated signal transduction. Ann N Y Acad Sci.; 733: 357-64.
  • McNeill LA, Hewitson KS, Gleadle JM, Horsfall LE, Oldham NJ, Maxwell PH, Pugh CW, Ratcliffe PJ, Schofield CJ. (2002) The use of dioxygen by HIF prolyl hydroxylase (PHD1). Bioorg Med Chem Lett.; 12: 1547-50.
  • Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM. (1998) Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest.; 101: 2567-78.
  • Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC. (1997) Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest.; 100: 3131-9.
  • Parenti A, Morbidelli L, Cui XL, Douglas JG, Hood JD, Granger HJ, Ledda F, Ziche M. (1998) Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase1/2 activation in postcapillary endothelium. J Biol Chem.; 273: 4220-6.
  • Richard DE, Berra E, Gothie E, Roux D, Pouyssegur J. (1999) p42/p44 mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1alpha. (HIF-1alpha) and enhance the transcriptional activity of HIF-1. J Biol Chem.; 274: 32631-7.
  • Rosenberger C, Mandriota S, Jurgensen JS, Wiesener MS, Horstrup JH, Frei U, Ratcliffe PJ, Maxwell PH, Bachmann S, Eckardt KU. (2002) Expression of hypoxia-inducible factor-1alpha and -2alpha in hypoxic and ischemic rat kidneys. J Am Soc Nephrol.; 13: 1721-32.
  • Salceda S, Caro J. (1997) 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.; 272: 22642-7.
  • Sandau KB, Fandrey J, Brune B. (2001) Accumulation of HIF-1alpha under the influence of nitric oxide. Blood.; 97: 1009-15.
  • Sandau KB, Faus HG, Brune B. (2000) Induction of hypoxia-inducible-factor 1 by nitric oxide is mediated via the PI 3K pathway. Biochem Biophys Res Commun.; 278: 263-7.
  • Schmidt HH, Walter U. (1994) NO at work. Cell.; 78: 919-25.
  • Semenza GL, Agani F, Booth G, Forsythe J, Iyer N, Jiang BH, Leung S, Roe R, Wiener C, Yu A. (1997) Structural and functional analysis of hypoxiainducible factor 1. Kidney Int.; 51: 553-5.
  • Shen BQ, Lee DY, Zioncheck TF. (1999) Vascular endothelial growth factor governs endothelial nitric-oxide synthase expression via a KDR/Flk-1 receptor and a protein kinase C signaling pathway. J Biol Chem.; 274: 33057-63.
  • Sodhi A, Montaner S, Miyazaki H, Gutkind JS. (2001) MAPK and Akt act cooperatively but independently on hypoxia inducible factor- 1alpha in rasV12 upregulation of VEGF. Biochem Biophys Res Commun.; 287: 292-300.
  • Sogawa K, Numayama-Tsuruta K, Ema M, Abe M, Abe H, Fujii-Kuriyama Y. (1998) Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc Natl Acad Sci U S A. 95: 7368-73.
  • Stiehl DP, Jelkmann W, Wenger RH, Hellwig-Burgel T. (2002) Normoxic induction of the hypoxia-inducible factor 1alpha by insulin and interleukin-1beta involves the phosphatidylinositol 3-kinase pathway. FEBS Lett.; 512: 157-62.
  • Tanimoto K, Makino Y, Pereira T, Poellinger L. (2000) Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J.; 19: 4298-309.
  • Thakker GD, Hajjar DP, Muller WA, Rosengart TK. (1999) The role of phosphatidylinositol 3-kinase in vascular endothelial growth factor signaling. J Biol Chem.; 274: 10002-7.
  • Thuringer D, Maulon L, Frelin C. (2002) Rapid transactivation of the vascular endothelial growth factor receptor KDR/Flk-1 by the bradykinin B2 receptor contributes to endothelial nitric-oxide synthase activation in cardiac capillary endothelial cells. J Biol Chem.; 277: 2028-32.
  • Tsurumi Y, Murohara T, Krasinski K, Chen D, Witzenbichler B, Kearney M, Couffinhal T, Isner JM. (1997) Reciprocal relation between VEGF and NO in the regulation of endothelial integrity. Nat Med.; 3: 879-86.
  • Wang GL, Semenza GL. (1995) Purification and characterization of hypoxia-inducible factor 1. J Biol Chem.; 270: 1230-7.
  • Wink DA, Mitchell JB. (1998) Chemical biology of nitric oxide: Insights into regulatory cytotoxic and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med.; 25: 434-56.
  • Wu HM, Yuan Y, Zawieja DC, Tinsley J, Granger HJ. (1999) Role of phospholipase C protein kinase C and calcium in VEGF-induced venular hyperpermeability. Am J Physiol.; 276: H535-42.
  • Xia P, Aiello LP, Ishii H, Jiang ZY, Park DJ, Robinson GS, Takagi H, Newsome WP, Jirousek MR, King GL. (1996) Characterization of vascular endothelial growth factor's effect on the activation of protein kinase C its isoforms and endothelial cell growth. J Clin Invest.; 98: 2018-26.
  • Zelzer E, Levy Y, Kahana C, Shilo BZ, Rubinstein M, Cohen B. (1998) Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO J.; 17: 5085-94.
  • Zhong H, Chiles K, Feldser D, Laughner E, Hanrahan C, Georgescu MM, Simons JW, Semenza GL. (2000) 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.; 60: 1541-5.
  • Zundel W, Schindler C, Haas-Kogan D, Koong A, Kaper F, Chen E, Gottschalk AR, Ryan HE, Johnson RS, Jefferson AB, Stokoe D, Giaccia AJ. (2000) Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev.; 14: 391-6.
Document Type
Publication order reference
YADDA identifier
bwmeta1.element.bwnjournal-article-abpv50i1p49kz
Identifiers
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.