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PMID: 15544038 Published · ppublish English Journal Article Review

Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase.

Molecular and cellular biochemistry ·Vol. 264 ·No. 1-2 ·2004-09-00 ·Pages 85-97

Ushio-Fukai M, Alexander RW

Abstract

Angiogenesis, a process of new blood vessel growth, contributes to various pathophysiologies such as cancer, diabetic retinopathy and atherosclerosis. Accumulating evidence suggests that cardiovascular diseases are associated with increased oxidative stress in blood vessels. Reactive oxygen species (ROS) such as superoxide and H2O2 cause blood vessels to thicken, produce inflammation in the vessel wall, and thus are regarded as "risk factors" for vascular disease, whereas ROS also act as signaling molecules in many aspects of growth factor-mediated physiological responses. Recent reports suggest that ROS play an important role in angiogenesis; however, its underlying molecular mechanisms remain unknown. Vascular endothelial growth factor (VEGF) induces angiogenesis by stimulating endothelial cell (EC) proliferation and migration primarily through the receptor tyrosine kinase VEGF receptor2 (Flk1/KDR). VEGF binding initiates tyrosine phosphorylation of KDR, which results in activation of downstream signaling enzymes including ERK1/2, Akt and eNOS, which contribute to angiogenic-related responses in EC. Importantly, the major source of ROS in EC is a NAD(P)H oxidase and EC express all the components of phagocytic NAD(P)H oxidase including gp91phox, p22phox, p47phox, p67phox and the small G protein Rac1. We have recently demonstrated that ROS derived from NAD(P)H oxidase are critically important for VEGF signaling in vitro and angiogenesis in vivo. Furthermore, a peptide hormone, angiotensin II, a major stimulus for vascular NAD(P)H oxidase, also plays an important role in angiogenesis. Because EC migration and proliferation are primary features of the process of myocardial angiogenesis, we would like to focus on the recent progress that has been made in the emerging area of NAD(P)H oxidase-derived ROS-dependent signaling in ECs, and discuss the possible roles in angiogenesis. Understanding these mechanisms may provide insight into the components of NAD(P)H oxidase as potential therapeutic targets for treatment of angiogenesis-dependent diseases such as cancer and atherosclerosis and for promoting myocardial angiogenesis in ischemic heart diseases.

MeSH Terms
Angiotensins/metabolism Animals Endothelium, Vascular/metabolism Humans Hydrogen Peroxide/pharmacology Inflammation Membrane Glycoproteins/metabolism Models, Biological NADPH Oxidase 2 NADPH Oxidases/metabolism Neovascularization, Pathologic Neovascularization, Physiologic Phosphorylation Reactive Oxygen Species Signal Transduction Transcription, Genetic Tyrosine/metabolism Vascular Endothelial Growth Factor A/metabolism
Chemicals
Angiotensins Membrane Glycoproteins Reactive Oxygen Species Vascular Endothelial Growth Factor A Tyrosine Hydrogen Peroxide CYBB protein, human NADPH Oxidase 2 NADPH Oxidases
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Ushio-Fukai Masuko
Division of Cardiology, Department of Medicine, Emory University School of Medicine, Atlanta, GA 30322, USA. [email protected]
Alexander R Wayne
References (151)
151 references, click to expand
  1. Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis.
    Circ Res. 2002 Dec 13;91(12):1160-7 PMID: 12480817
  2. Novel human homologues of p47phox and p67phox participate in activation of superoxide-producing NADPH oxidases.
    J Biol Chem. 2003 Jul 4;278(27):25234-46 PMID: 12716910
  3. Cell transformation by the superoxide-generating oxidase Mox1.
    Nature. 1999 Sep 2;401(6748):79-82 PMID: 10485709
  4. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly.
    Circ Res. 2002 Feb 22;90(3):251-62 PMID: 11861412
  5. Mechanism of endothelial cell NADPH oxidase activation by angiotensin II. Role of the p47phox subunit.
    J Biol Chem. 2003 Apr 4;278(14):12094-100 PMID: 12560337
  6. Sequential development of angiotensin receptors and angiotensin I converting enzyme during angiogenesis in the rat subcutaneous sponge granuloma.
    Br J Pharmacol. 1997 Apr;120(7):1302-11 PMID: 9105706
  7. Vascular endothelial growth factor induces manganese-superoxide dismutase expression in endothelial cells by a Rac1-regulated NADPH oxidase-dependent mechanism.
    FASEB J. 2001 Nov;15(13):2548-50 PMID: 11641265
  8. VEGF-mediated angiogenesis is impaired by angiotensin type 1 receptor blockade in cardiomyopathic hamster hearts.
    Cardiovasc Res. 2003 Apr 1;58(1):203-12 PMID: 12667963
  9. Angiotensin II induces vascular cell adhesion molecule-1 expression in rat vasculature: A potential link between the renin-angiotensin system and atherosclerosis.
    Circulation. 1999 Sep 14;100(11):1223-9 PMID: 10484544
  10. Leptin induces oxidative stress in human endothelial cells.
    FASEB J. 1999 Jul;13(10):1231-8 PMID: 10385613
  11. Effect of protein kinase and phosphatase inhibitors on expression of hypoxia-inducible factor 1.
    Biochem Biophys Res Commun. 1995 Nov 13;216(2):669-75 PMID: 7488163
  12. The actin cytoskeleton reorganization induced by Rac1 requires the production of superoxide.
    Antioxid Redox Signal. 1999 Spring;1(1):29-43 PMID: 11225730
  13. Vascular endothelial growth factor causes translocation of p47phox to membrane ruffles through WAVE1.
    J Biol Chem. 2003 Sep 19;278(38):36830-40 PMID: 12855698
  14. Hydrogen peroxide induces complex formation of SHC-Grb2-SOS with receptor tyrosine kinase and activates Ras and extracellular signal-regulated protein kinases group of mitogen-activated protein kinases.
    Oncogene. 1996 Aug 15;13(4):713-9 PMID: 8761292
  15. Significance of nitric oxide and peroxynitrite in permeability changes of the retinal microvascular endothelial cell monolayer induced by vascular endothelial growth factor.
    J Vasc Res. 1999 Nov-Dec;36(6):510-5 PMID: 10629427
  16. The angiotensin-I-converting enzyme inhibitor perindopril suppresses tumor growth and angiogenesis: possible role of the vascular endothelial growth factor.
    Clin Cancer Res. 2001 Apr;7(4):1073-8 PMID: 11309359
  17. TNFalpha activates c-Jun amino terminal kinase through p47(phox).
    Exp Cell Res. 2002 Jan 1;272(1):62-74 PMID: 11740866
  18. Cytochrome P450 epoxygenases and vascular tone: novel role for HMG-CoA reductase inhibitors in the regulation of CYP 2C expression.
    Biochim Biophys Acta. 2003 Feb 17;1619(3):332-9 PMID: 12573493
  19. Stimulation of in vitro angiogenesis by hydrogen peroxide and the relation with ETS-1 in endothelial cells.
    Life Sci. 1999;64(4):249-58 PMID: 10027759
  20. Attenuation of ischemic preconditioning in pigs by scavenging of free oxyradicals with ascorbic acid.
    Am J Physiol Heart Circ Physiol. 2003 Feb;284(2):H698-703 PMID: 12388272
  21. N-acetylcysteine inhibits endothelial cell invasion and angiogenesis.
    Lab Invest. 1999 Sep;79(9):1151-9 PMID: 10496534
  22. Statins as antioxidant therapy for preventing cardiac myocyte hypertrophy.
    J Clin Invest. 2001 Nov;108(10):1429-37 PMID: 11714734
  23. Role of ANG II in coronary capillary angiogenesis at the insulin-resistant stage of a NIDDM rat model.
    Am J Physiol Heart Circ Physiol. 2002 Oct;283(4):H1387-97 PMID: 12234789
  24. On the possible role of reactive oxygen species in angiogenesis.
    Adv Exp Med Biol. 1998;454:295-310 PMID: 9889904
  25. The mechanism of cytoprotective action of lazaroids I: Inhibition of reactive oxygen species formation and lethal cell injury during periods of energy depletion.
    J Pharmacol Exp Ther. 1996 Mar;276(3):1224-31 PMID: 8786555
  26. Lysophosphatidylcholine increases the secretion of matrix metalloproteinase 2 through the activation of NADH/NADPH oxidase in cultured aortic endothelial cells.
    Atherosclerosis. 2001 Mar;155(1):45-52 PMID: 11223425
  27. Influence of the angiotensin system on endothelial and smooth muscle cell migration.
    Am J Pathol. 1990 Jul;137(1):7-12 PMID: 2164777
  28. A redox-based mechanism for cardioprotection induced by ischemic preconditioning in perfused rat heart.
    Circ Res. 1995 Aug;77(2):424-9 PMID: 7614726
  29. NADPH oxidase activity is required for endothelial cell proliferation and migration.
    FEBS Lett. 2000 Dec 15;486(3):252-6 PMID: 11119713
  30. Impact of HMG CoA reductase inhibition on small GTPases in the heart.
    Cardiovasc Res. 2002 Mar;53(4):911-20 PMID: 11922901
  31. Angiogenesis in cancer, vascular, rheumatoid and other disease.
    Nat Med. 1995 Jan;1(1):27-31 PMID: 7584949
  32. Epidermal growth factor receptor transactivation by angiotensin II requires reactive oxygen species in vascular smooth muscle cells.
    Arterioscler Thromb Vasc Biol. 2001 Apr;21(4):489-95 PMID: 11304462
  33. Reactive oxygen species are critical mediators of coronary collateral development in a canine model.
    Am J Physiol Heart Circ Physiol. 2003 Oct;285(4):H1582-9 PMID: 12816750
  34. Green tea catechins and vitamin E inhibit angiogenesis of human microvascular endothelial cells through suppression of IL-8 production.
    Nutr Cancer. 2001;41(1-2):119-25 PMID: 12094614
  35. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure.
    Hypertension. 2002 Oct;40(4):477-84 PMID: 12364350
  36. Expression of p22-phox and gp91-phox, essential components of NADPH oxidase, increases after myocardial infarction.
    Biochem Biophys Res Commun. 2001 Mar;281(5):1200-6 PMID: 11243862
  37. p38 Mitogen-activated protein kinase is a critical component of the redox-sensitive signaling pathways activated by angiotensin II. Role in vascular smooth muscle cell hypertrophy.
    J Biol Chem. 1998 Jun 12;273(24):15022-9 PMID: 9614110
  38. Angiogenesis induced by electrical stimulation is mediated by angiotensin II and VEGF.
    Microcirculation. 2001 Feb;8(1):57-67 PMID: 11296854
  39. Reversible inactivation of the tumor suppressor PTEN by H2O2.
    J Biol Chem. 2002 Jun 7;277(23 ):20336-42 PMID: 11916965
  40. Redox regulation of protein tyrosine phosphatases during receptor tyrosine kinase signal transduction.
    Trends Biochem Sci. 2003 Sep;28(9):509-14 PMID: 13678963
  41. Two vicinal cysteines confer a peculiar redox regulation to low molecular weight protein tyrosine phosphatase in response to platelet-derived growth factor receptor stimulation.
    J Biol Chem. 2001 Sep 7;276(36):33478-87 PMID: 11429404
  42. Role of cysteine residues in regulation of p53 function.
    Mol Cell Biol. 1995 Jul;15(7):3892-903 PMID: 7791795
  43. Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt.
    Circ Res. 2000 Apr 28;86(8):892-6 PMID: 10785512
  44. Regulation of receptor tyrosine kinase signaling by protein tyrosine phosphatases.
    Trends Cell Biol. 2001 Jun;11(6):258-66 PMID: 11356362
  45. The NADPH oxidase of endothelial cells.
    IUBMB Life. 2000 Oct-Nov;50(4-5):267-9 PMID: 11327320
  46. Calcium-dependent epidermal growth factor receptor transactivation mediates the angiotensin II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells.
    J Biol Chem. 1998 Apr 10;273(15):8890-6 PMID: 9535870
  47. Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice.
    Circulation. 2002 Jan 22;105(3):293-6 PMID: 11804982
  48. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells.
    J Biol Chem. 1999 Aug 6;274(32):22699-704 PMID: 10428852
  49. Heme histidine ligands within gp91(phox) modulate proton conduction by the phagocyte NADPH oxidase.
    J Biol Chem. 2001 Aug 10;276(32):30277-84 PMID: 11389135
  50. 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 Jul 6;89(1):47-54 PMID: 11440977
  51. Angiotensin AT(1) receptor signalling modulates reparative angiogenesis induced by limb ischaemia.
    Br J Pharmacol. 2002 Jan;135(1):87-92 PMID: 11786483
  52. Role of NAD(P)H oxidase in angiotensin II-induced JAK/STAT signaling and cytokine induction.
    Circ Res. 2000 Dec 8;87(12):1195-201 PMID: 11110778
  53. Induction of NAD(P)H oxidase by oxidized low-density lipoprotein in human endothelial cells: antioxidative potential of hydroxymethylglutaryl coenzyme A reductase inhibitor therapy.
    Circulation. 2001 Oct 9;104(15):1767-72 PMID: 11591612
  54. Escape from redox regulation enhances the transforming activity of Fos.
    Oncogene. 1993 Mar;8(3):695-701 PMID: 8437852
  55. Akt-dependent phosphorylation of serine 1179 and mitogen-activated protein kinase kinase/extracellular signal-regulated kinase 1/2 cooperatively mediate activation of the endothelial nitric-oxide synthase by hydrogen peroxide.
    Mol Pharmacol. 2003 Feb;63(2):325-31 PMID: 12527803
  56. Cardiac myofibroblasts: a novel source of vascular endothelial growth factor (VEGF) and its receptors Flt-1 and KDR.
    J Mol Cell Cardiol. 2003 Mar;35(3):277-86 PMID: 12676542
  57. Proteins homologous to p47phox and p67phox support superoxide production by NAD(P)H oxidase 1 in colon epithelial cells.
    J Biol Chem. 2003 May 30;278(22):20006-12 PMID: 12657628
  58. Coronary microvascular endothelial cell redox state in left ventricular hypertrophy : the role of angiotensin II.
    Circ Res. 2000 Mar 3;86(4):463-9 PMID: 10700452
  59. c-Src induces phosphorylation and translocation of p47phox: role in superoxide generation by angiotensin II in human vascular smooth muscle cells.
    Arterioscler Thromb Vasc Biol. 2003 Jun 1;23(6):981-7 PMID: 12663375
  60. NADPH oxidase-derived superoxide anion mediates angiotensin II-induced cardiac hypertrophy.
    J Mol Cell Cardiol. 2003 Jul;35(7):851-9 PMID: 12818576
  61. Biological activity and phosphorylation sites of the bacterially expressed cytosolic domain of the KDR VEGF-receptor.
    Biochem Biophys Res Commun. 1994 Nov 30;205(1):728-38 PMID: 7999104
  62. NAD(P)H oxidase: role in cardiovascular biology and disease.
    Circ Res. 2000 Mar 17;86(5):494-501 PMID: 10720409
  63. Apoptotic cascade initiated by angiotensin II in neonatal cardiomyocytes: role of DNA damage.
    Am J Physiol Heart Circ Physiol. 2003 Dec;285(6):H2364-72 PMID: 12919932
  64. 17beta-estradiol inhibition of NADPH oxidase expression in human endothelial cells.
    FASEB J. 2001 Oct;15(12):2121-30 PMID: 11641238
  65. Oxidative inactivation of CD45 protein tyrosine phosphatase may contribute to T lymphocyte dysfunction in the elderly.
    Mech Ageing Dev. 2003 Feb;124(2):191-8 PMID: 12633939
  66. Oscillatory shear stress stimulates endothelial production of O2- from p47phox-dependent NAD(P)H oxidases, leading to monocyte adhesion.
    J Biol Chem. 2003 Nov 21;278(47):47291-8 PMID: 12958309
  67. Cellular antioxidant effects of atorvastatin in vitro and in vivo.
    Arterioscler Thromb Vasc Biol. 2002 Feb 1;22(2):300-5 PMID: 11834532
  68. Inhibition of vascular endothelial growth factor-induced angiogenesis by resveratrol through interruption of Src-dependent vascular endothelial cadherin tyrosine phosphorylation.
    Mol Pharmacol. 2003 Nov;64(5):1029-36 PMID: 14573751
  69. HCPTPA, a protein tyrosine phosphatase that regulates vascular endothelial growth factor receptor-mediated signal transduction and biological activity.
    J Biol Chem. 1999 Dec 31;274(53):38183-8 PMID: 10608891
  70. Involvement of the transcription factor NF-kappaB in tubular morphogenesis of human microvascular endothelial cells by oxidative stress.
    Mol Cell Biol. 1996 Aug;16(8):4231-9 PMID: 8754823
  71. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo.
    Mol Cell. 2002 Feb;9(2):387-99 PMID: 11864611
  72. Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR.
    J Biol Chem. 2002 Feb 1;277(5):3101-8 PMID: 11719508
  73. Oxygen free radical release in human failing myocardium is associated with increased activity of rac1-GTPase and represents a target for statin treatment.
    Circulation. 2003 Sep 30;108(13):1567-74 PMID: 12963641
  74. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction.
    Science. 1995 Oct 13;270(5234):296-9 PMID: 7569979
  75. Reactive oxygen and NF-kappaB in VEGF-induced migration of human vascular smooth muscle cells.
    Biochem Biophys Res Commun. 2001 Jul 20;285(3):669-74 PMID: 11453645
  76. Signaling transduction mechanisms mediating biological actions of the vascular endothelial growth factor family.
    Cardiovasc Res. 2001 Feb 16;49(3):568-81 PMID: 11166270
  77. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation.
    J Biol Chem. 1997 Jan 3;272(1):217-21 PMID: 8995250
  78. Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species.
    Circ Res. 2003 Jun 13;92(11):e80-6 PMID: 12750313
  79. Secretion of extracellular superoxide dismutase from muscle transduced with recombinant adenovirus inhibits the growth of B16 melanomas in mice.
    Mol Cancer Res. 2003 Oct;1(12):871-81 PMID: 14573788
  80. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor.
    J Biol Chem. 1998 Jun 19;273(25):15366-72 PMID: 9624118
  81. Inhibition of geranylgeranylation reduces angiotensin II-mediated free radical production in vascular smooth muscle cells: involvement of angiotensin AT1 receptor expression and Rac1 GTPase.
    Mol Pharmacol. 2001 Mar;59(3):646-54 PMID: 11179461
  82. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall.
    Circ Res. 2000 Jul 7;87(1):26-32 PMID: 10884368
  83. VEGF receptor signal transduction.
    Sci STKE. 2001 Dec 11;2001(112):re21 PMID: 11741095
  84. Suppression of retinal neovascularization by the NF-kappaB inhibitor pyrrolidine dithiocarbamate in mice.
    Invest Ophthalmol Vis Sci. 1999 Jun;40(7):1624-9 PMID: 10359349
  85. A Ca(2+)-activated NADPH oxidase in testis, spleen, and lymph nodes.
    J Biol Chem. 2001 Oct 5;276(40):37594-601 PMID: 11483596
  86. NADPH oxidase in endothelial cells: impact on atherosclerosis.
    Antioxid Redox Signal. 2003 Apr;5(2):171-80 PMID: 12716477
  87. Increased Nox2 expression in human cardiomyocytes after acute myocardial infarction.
    J Clin Pathol. 2003 Mar;56(3):194-9 PMID: 12610097
  88. A non-hypoxic, ROS-sensitive pathway mediates TNF-alpha-dependent regulation of HIF-1alpha.
    FEBS Lett. 2001 Sep 14;505(2):269-74 PMID: 11566189
  89. Modulation of protein kinase activity and gene expression by reactive oxygen species and their role in vascular physiology and pathophysiology.
    Arterioscler Thromb Vasc Biol. 2000 Oct;20(10):2175-83 PMID: 11031201
  90. Regulation of receptor protein-tyrosine phosphatase alpha by oxidative stress.
    EMBO J. 2002 Feb 15;21(4):493-503 PMID: 11847098
  91. Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells.
    J Biol Chem. 2002 May 31;277(22):19952-60 PMID: 11893732
  92. HMG-CoA reductase inhibitors improve endothelial dysfunction in normocholesterolemic hypertension via reduced production of reactive oxygen species.
    Hypertension. 2001 Jun;37(6):1450-7 PMID: 11408394
  93. The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells.
    J Biol Chem. 1997 Dec 19;272(51):32521-7 PMID: 9405464
  94. Angiotensin AT(1) and AT(2) receptors differentially regulate angiopoietin-2 and vascular endothelial growth factor expression and angiogenesis by modulating heparin binding-epidermal growth factor (EGF)-mediated EGF receptor transactivation.
    Circ Res. 2001 Jan 19;88(1):22-9 PMID: 11139469
  95. Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148.
    J Cell Biol. 2003 May 26;161(4):793-804 PMID: 12771128
  96. Redox signaling in vascular angiogenesis.
    Free Radic Biol Med. 2002 Oct 15;33(8):1047-60 PMID: 12374616
  97. Upregulation of vascular endothelial growth factor by H2O2 in rat heart endothelial cells.
    Free Radic Biol Med. 1998 Nov 15;25(8):891-7 PMID: 9840733
  98. The role of hydrogen peroxide in endothelial proliferative responses.
    Endothelium. 2002;9(4):231-8 PMID: 12572854
  99. Increased H2O2, vascular endothelial growth factor and receptors in the retina of the BBZ/Wor diabetic rat.
    Free Radic Biol Med. 2000 Jan 1;28(1):91-101 PMID: 10656295
  100. Mechanism of preconditioning by isoflurane in rabbits: a direct role for reactive oxygen species.
    Anesthesiology. 2002 Dec;97(6):1485-90 PMID: 12459675
  101. The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases.
    Trends Pharmacol Sci. 2003 Sep;24(9):471-8 PMID: 12967772
  102. Upregulation of p67(phox) and gp91(phox) in aortas from angiotensin II-infused mice.
    Am J Physiol Heart Circ Physiol. 2000 Nov;279(5):H2234-40 PMID: 11045958
  103. Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa B transcription factor and HIV-1.
    EMBO J. 1991 Aug;10(8):2247-58 PMID: 2065663
  104. Analysis of VEGF-responsive genes involved in the activation of endothelial cells.
    Mol Cancer. 2003 Jul 09;2:25 PMID: 12904264
  105. Redox regulation of vascular angiogenesis.
    Antioxid Redox Signal. 2002 Oct;4(5):783-4 PMID: 12470505
  106. Redox regulation of HIF-1alpha levels and HO-1 expression in renal medullary interstitial cells.
    Am J Physiol Renal Physiol. 2003 Jun;284(6):F1207-15 PMID: 12595275
  107. p21ras as a common signaling target of reactive free radicals and cellular redox stress.
    J Biol Chem. 1995 Sep 8;270(36):21195-8 PMID: 7673152
  108. Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade.
    J Biol Chem. 2001 Jun 15;276(24):21938-42 PMID: 11297536
  109. Green tea catechins inhibit VEGF-induced angiogenesis in vitro through suppression of VE-cadherin phosphorylation and inactivation of Akt molecule.
    Int J Cancer. 2003 Oct 10;106(6):871-8 PMID: 12918064
  110. Statins have biphasic effects on angiogenesis.
    Circulation. 2002 Feb 12;105(6):739-45 PMID: 11839631
  111. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation.
    Sci STKE. 2000 Oct 10;2000(53):pe1 PMID: 11752613
  112. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5.
    Gene. 2001 May 16;269(1-2):131-40 PMID: 11376945
  113. Induction of vascular endothelial growth factor in balloon-injured baboon arteries. A novel role for reactive oxygen species in atherosclerosis.
    Circ Res. 1997 Jul;81(1):24-33 PMID: 9201024
  114. Vascular endothelial growth factor (VEGF)-driven actin-based motility is mediated by VEGFR2 and requires concerted activation of stress-activated protein kinase 2 (SAPK2/p38) and geldanamycin-sensitive phosphorylation of focal adhesion kinase.
    J Biol Chem. 2000 Apr 7;275(14):10661-72 PMID: 10744763
  115. Reactive oxygen intermediates induce monocyte chemotactic protein-1 in vascular endothelium after brief ischemia.
    Am J Pathol. 2001 Oct;159(4):1301-11 PMID: 11583958
  116. Angiotensin II induces migration and Pyk2/paxillin phosphorylation of human monocytes.
    Hypertension. 2001 Feb;37(2 Pt 2):587-93 PMID: 11230339
  117. Opposing actions of angiotensin II on microvascular growth and arterial blood pressure.
    Hypertension. 1996 Mar;27(3 Pt 2):760-5 PMID: 8613237
  118. Impaired endothelial regulation of ventricular relaxation in cardiac hypertrophy: role of reactive oxygen species and NADPH oxidase.
    Circulation. 2001 Dec 11;104(24):2967-74 PMID: 11739314
  119. Angiotensin II potentiates vascular endothelial growth factor-induced angiogenic activity in retinal microcapillary endothelial cells.
    Circ Res. 1998 Mar 23;82(5):619-28 PMID: 9529167
  120. Blockade of angiotensin AT1a receptor signaling reduces tumor growth, angiogenesis, and metastasis.
    Biochem Biophys Res Commun. 2002 Jun 7;294(2):441-7 PMID: 12051731
  121. Reactive oxygen generated by Nox1 triggers the angiogenic switch.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):715-20 PMID: 11805326
  122. The vascular NADPH oxidase subunit p47phox is involved in redox-mediated gene expression.
    Free Radic Biol Med. 2002 Jun 1;32(11):1116-22 PMID: 12031896
  123. Reactive oxygen species modulate HIF-1 mediated PAI-1 expression: involvement of the GTPase Rac1.
    Thromb Haemost. 2003 May;89(5):926-35 PMID: 12719791
  124. FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition.
    Trends Pharmacol Sci. 2001 Apr;22(4):201-7 PMID: 11282421
  125. HIF-1alpha mRNA and protein upregulation involves Rho GTPase expression during hypoxia in renal cell carcinoma.
    J Cell Sci. 2003 Jun 1;116(Pt 11):2247-60 PMID: 12697836
  126. NAD(P)H oxidase-derived hydrogen peroxide mediates endothelial nitric oxide production in response to angiotensin II.
    J Biol Chem. 2002 Dec 13;277(50):48311-7 PMID: 12377764
  127. Induction of hypoxia-inducible factor-1alpha by transcriptional and translational mechanisms.
    J Biol Chem. 2002 Dec 13;277(50):48403-9 PMID: 12379645
  128. Angiotensin II angiogenic effect in vivo involves vascular endothelial growth factor- and inflammation-related pathways.
    Lab Invest. 2002 Jun;82(6):747-56 PMID: 12065685
  129. Integrating the VEGF signals leading to actin-based motility in vascular endothelial cells.
    Trends Cardiovasc Med. 2000 Nov;10(8):321-7 PMID: 11369257
  130. Reactive oxygen species mediate Rac-induced loss of cell-cell adhesion in primary human endothelial cells.
    J Cell Sci. 2002 May 1;115(Pt 9):1837-46 PMID: 11956315
  131. Nonhypoxic pathway mediates the induction of hypoxia-inducible factor 1alpha in vascular smooth muscle cells.
    J Biol Chem. 2000 Sep 1;275(35):26765-71 PMID: 10837481
  132. Evidence for the importance of angiotensin II type 1 receptor in ischemia-induced angiogenesis.
    J Clin Invest. 2002 Mar;109(5):603-11 PMID: 11877468
  133. Endothelin-1 induces NAD(P)H oxidase in human endothelial cells.
    Biochem Biophys Res Commun. 2000 Mar 24;269(3):713-7 PMID: 10720482
  134. Nitric oxide and angiogenesis in cardiovascular disease.
    Antioxid Redox Signal. 2002 Oct;4(5):825-31 PMID: 12470511
  135. Angiogenesis inhibited by drinking tea.
    Nature. 1999 Apr 1;398(6726):381 PMID: 10201368
  136. Tumor necrosis factor employs a protein-tyrosine phosphatase to inhibit activation of KDR and vascular endothelial cell growth factor-induced endothelial cell proliferation.
    J Biol Chem. 2000 Apr 14;275(15):11216-21 PMID: 10753929
  137. Angiotensin II activates NADPH oxidase in isolated rat hearts subjected to ischaemia-reperfusion.
    Eur J Pharmacol. 2003 Feb 21;462(1-3):145-54 PMID: 12591107
  138. Superoxide production and expression of nox family proteins in human atherosclerosis.
    Circulation. 2002 Mar 26;105(12):1429-35 PMID: 11914250
  139. Protein tyrosine phosphatases: mechanisms of catalysis and regulation.
    Curr Opin Chem Biol. 1998 Oct;2(5):633-41 PMID: 9818190
  140. Pigment epithelium-derived factor inhibits leptin-induced angiogenesis by suppressing vascular endothelial growth factor gene expression through anti-oxidative properties.
    Microvasc Res. 2003 May;65(3):186-90 PMID: 12711260
  141. Two novel proteins activate superoxide generation by the NADPH oxidase NOX1.
    J Biol Chem. 2003 Feb 7;278(6):3510-3 PMID: 12473664
  142. Nox/Duox family of nicotinamide adenine dinucleotide (phosphate) oxidases.
    Curr Opin Hematol. 2002 Jan;9(1):11-7 PMID: 11753072
  143. Withdrawal of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors elicits oxidative stress and induces endothelial dysfunction in mice.
    Circ Res. 2002 Jul 26;91(2):173-9 PMID: 12142351
  144. Phosphorylation of the endothelial nitric oxide synthase at ser-1177 is required for VEGF-induced endothelial cell migration.
    FEBS Lett. 2000 Jul 21;477(3):258-62 PMID: 10908731
  145. Science review: redox and oxygen-sensitive transcription factors in the regulation of oxidant-mediated lung injury: role for hypoxia-inducible factor-1alpha.
    Crit Care. 2003 Feb;7(1):47-54 PMID: 12617740
  146. Essential role of the NADPH oxidase subunit p47(phox) in endothelial cell superoxide production in response to phorbol ester and tumor necrosis factor-alpha.
    Circ Res. 2002 Feb 8;90(2):143-50 PMID: 11834706
  147. Increased NADH oxidase activity in the retina of the BBZ/Wor diabetic rat.
    Free Radic Biol Med. 1998 Jan 1;24(1):111-20 PMID: 9436620
  148. Role of p47(phox) in vascular oxidative stress and hypertension caused by angiotensin II.
    Hypertension. 2002 Oct;40(4):511-5 PMID: 12364355
  149. Insulin prevents cardiomyocytes from oxidative stress-induced apoptosis through activation of PI3 kinase/Akt.
    Circulation. 2000 Dec 5;102(23):2873-9 PMID: 11104747
  150. Chymase as a proangiogenic factor. A possible involvement of chymase-angiotensin-dependent pathway in the hamster sponge angiogenesis model.
    J Biol Chem. 2000 Feb 25;275(8):5545-52 PMID: 10681534
  151. Angiotensin II induces monocyte chemoattractant protein-1 gene expression in rat vascular smooth muscle cells.
    Circ Res. 1998 Nov 2;83(9):952-9 PMID: 9797345
Article Info
Journal
Molecular and cellular biochemistry
Abbr.
Mol Cell Biochem
ISSN
0300-8177
DOI
10.1023/b:mcbi.0000044378.09409.b5
Email
[email protected]
Published
2004-09-00
Pages
85-97
Language
English
Region
Netherlands
NLM ID
0364456
Subset
IM
External Links
PubMed source DOI: 10.1023/b:mcbi.0000044378.09409.b5 View journal details
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