Redox signaling in vascular angiogenesis.

Angiogenesis is thought to be regulated by several growth factors (EGF, TGF-alpha, beta-FGF, VEGF). Induction of these angiogenic factors is triggered by various stresses. For instance, tissue hypoxia exerts its pro-angiogenic action through various angiogenic factors, the most notable being vascular endothelial growth factor, which has been mainly associated with initiating the process of angiogenesis through the recruitment and proliferation of endothelial cells. Recently, reactive oxygen species (ROS) have been found to stimulate angiogenic response in the ischemic reperfused hearts. Short exposure to hypoxia/reoxygenation, either directly or indirectly, produces ROS that induce oxidative stress which is associated with angiogenesis or neovascularization. ROS can cause tissue injury in one hand and promote tissue repair in another hand by promoting angiogenesis. It thus appears that after causing injury to the cells, ROS promptly initiate the tissue repair process by triggering angiogenic response.

[1]  J. Martinou,et al.  The Bcl-2 protein family. , 2000, Experimental cell research.

[2]  B. Price,et al.  An essential role of NFκB in tyrosine kinase signaling of p38 MAP kinase regulation of myocardial adaptation to ischemia , 1998, FEBS letters.

[3]  N. Voelkel,et al.  Increased gene expression for VEGF and the VEGF receptors KDR/Flk and Flt in lungs exposed to acute or to chronic hypoxia. Modulation of gene expression by nitric oxide. , 1995, The Journal of clinical investigation.

[4]  G. Christensen,et al.  Myocardial expression of CC- and CXC-chemokines and their receptors in human end-stage heart failure. , 2000, Cardiovascular research.

[5]  P. O'dwyer,et al.  Involvement of NF-κB in the induction of NAD(P)H: Quinone oxidoreductase (DT-diaphorase) by hypoxia, oltipraz and mitomycin C , 1995 .

[6]  I. Hemo,et al.  In vivo angiogenic activity of interleukins. , 1990, Archives of ophthalmology.

[7]  N. Maulik,et al.  Anti‐apoptotic protein survivin plays a significant role in tubular morphogenesis of human coronary arteriolar endothelial cells by hypoxic preconditioning , 2001, FEBS letters.

[8]  D. Das,et al.  Oxygen-derived free radicals and hemolysis during open heart surgery , 1992, Molecular and Cellular Biochemistry.

[9]  S. Kawamoto,et al.  Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C. , 1984, Biochemistry.

[10]  D. Das,et al.  The red wine antioxidant resveratrol protects isolated rat hearts from ischemia reperfusion injury. , 1999, Free radical biology & medicine.

[11]  F. Kafatos,et al.  The ovo gene of Drosophila encodes a zinc finger protein required for female germ line development. , 1991, The EMBO journal.

[12]  J. Martial,et al.  Activation of mitogen-activated protein kinases by vascular endothelial growth factor and basic fibroblast growth factor in capillary endothelial cells is inhibited by the antiangiogenic factor 16-kDa N-terminal fragment of prolactin. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Vishva Dixit,et al.  Vascular Endothelial Growth Factor Regulates Endothelial Cell Survival through the Phosphatidylinositol 3′-Kinase/Akt Signal Transduction Pathway , 1998, The Journal of Biological Chemistry.

[14]  J. Pober,et al.  Control of apoptosis during angiogenesis by survivin expression in endothelial cells. , 2000, The American journal of pathology.

[15]  N. Maulik,et al.  Nitric oxide signaling in ischemic heart. , 1995, Cardiovascular research.

[16]  D. Mukhopadhyay,et al.  Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation , 1995, Nature.

[17]  E. Kohmura,et al.  Brief exposure to hypoxia induces bFGF mRNA and protein and protects rat cortical neurons from prolonged hypoxic stress , 1995, Neuroscience Research.

[18]  M. Fini,et al.  Transforming growth factor-beta and interleukin-1 modulate metalloproteinase expression by corneal stromal cells. , 1991, Investigative ophthalmology & visual science.

[19]  Y. Shimada,et al.  Apoptosis of vascular endothelial cells by fibroblast growth factor deprivation. , 1990, Biochemical and biophysical research communications.

[20]  C. Frelin,et al.  Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heart. , 1993, Biochemical and biophysical research communications.

[21]  N. Maulik,et al.  Early effects of hypoxia/reoxygenation on VEGF, Ang-1, Ang-2 and their receptors in the rat myocardium: Implications for myocardial angiogenesis , 2000, Molecular and Cellular Biochemistry.

[22]  A. Koch,et al.  Inhibition of production of monocyte/macrophage-derived angiogenic activity by oxygen free-radical scavengers. , 1992, Cell biology international reports.

[23]  J. C. Fox,et al.  Antisense Inhibition of Basic Fibroblast Growth Factor Induces Apoptosis in Vascular Smooth Muscle Cells (*) , 1996, The Journal of Biological Chemistry.

[24]  Y. Ho,et al.  Glutathione peroxidase knockout mice are susceptible to myocardial ischemia reperfusion injury. , 1997, Circulation.

[25]  N. Gorbunov,et al.  Nitric oxide/carbon monoxide. A molecular switch for myocardial preservation during ischemia. , 1996, Circulation.

[26]  J. Caro,et al.  Hypoxic stimulation of vascular endothelial growth factor expression in vitro and in vivo. , 1994, Laboratory investigation; a journal of technical methods and pathology.

[27]  I. Verma,et al.  Rel/NF-kappa B/I kappa B story. , 1995, Advances in cancer research.

[28]  K. Shiraki,et al.  Survivin promotes cell proliferation in human hepatocellular carcinoma , 2000 .

[29]  C. Nathan,et al.  Production of large amounts of hydrogen peroxide by human tumor cells. , 1991, Cancer research.

[30]  H. Pahl,et al.  Oxygen and the control of gene expression , 1994, BioEssays : news and reviews in molecular, cellular and developmental biology.

[31]  M. Monte,et al.  Inhibition of lymphocyte-induced angiogenesis by free radical scavengers. , 1994, Free radical biology & medicine.

[32]  M. Abe,et al.  Ets‐1 regulates angiogenesis by inducing the expression of urokinase‐type plasminogen activator and matrix metalloproteinase‐1 and the migration of vascular endothelial cells , 1996, Journal of cellular physiology.

[33]  P Rhodes,et al.  Roles of nitric oxide in tumor growth. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[34]  N. Abraham,et al.  The role of NF-kappaB in the angiogenic response of coronary microvessel endothelial cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Y. Kira,et al.  Rapid induction of vascular endothelial growth factor expression by transient ischemia in rat heart. , 1994, The American journal of physiology.

[36]  N. Maulik,et al.  Nitric oxide — a retrograde messenger for carbon monoxide signaling in ischemic heart , 1996, Molecular and Cellular Biochemistry.

[37]  J C Reed,et al.  IAP family proteins--suppressors of apoptosis. , 1999, Genes & development.

[38]  Michael Chinkers,et al.  Signal transduction by guanylyl cyclases. , 1991, Annual review of biochemistry.

[39]  N. Maulik,et al.  Antioxidant effectiveness in ischemia-reperfusion tissue injury. , 1994, Methods in enzymology.

[40]  K. Alitalo,et al.  Vascularization of the mouse embryo: A study of flk‐1, tek, tie, and vascular endothelial growth factor expression during development , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[41]  D. Das,et al.  Molecular adaptation of cellular defences following preconditioning of the heart by repeated ischaemia. , 1993, Cardiovascular research.

[42]  P. Lelkes,et al.  On the possible role of reactive oxygen species in angiogenesis. , 1998, Advances in experimental medicine and biology.

[43]  Michael Karin,et al.  NF-κB at the crossroads of life and death , 2002, Nature Immunology.

[44]  S. Cory,et al.  The Bcl-2 protein family: arbiters of cell survival. , 1998, Science.

[45]  B. Keyt,et al.  Hypoxia-induced paracrine regulation of vascular endothelial growth factor receptor expression. , 1996, The Journal of clinical investigation.

[46]  Simon C Watkins,et al.  Vascular Gene Transfer of the Human Inducible Nitric Oxide Synthase: Characterization of Activity and Effects on Myointimal Hyperplasia , 1996, Molecular medicine.

[47]  Xing-li Wang,et al.  Nitric oxide induces and inhibits apoptosis through different pathways , 1998, FEBS letters.

[48]  R. Narayanan,et al.  Regulation of adhesion and growth of fibrosarcoma cells by NF-kappa B RelA involves transforming growth factor beta , 1994, Molecular and cellular biology.

[49]  C. Rice-Evans,et al.  Oxidative stress and tumour cell proliferation. , 1990, Free radical research communications.

[50]  S. Naito,et al.  Stimulation of in vitro angiogenesis by hydrogen peroxide and the relation with ETS-1 in endothelial cells. , 1998, Life sciences.

[51]  G. Dong,et al.  IL (Interleukin)-1α Promotes Nuclear Factor-κB and AP-1-induced IL-8 Expression, Cell Survival, and Proliferation in Head and Neck Squamous Cell Carcinomas , 2001 .

[52]  R. Kernoff,et al.  Local intramural delivery of L-arginine enhances nitric oxide generation and inhibits lesion formation after balloon angioplasty. , 1997, Circulation.

[53]  H. Dvorak,et al.  Vascular permeability factor/vascular endothelial growth factor inhibits anchorage-disruption-induced apoptosis in microvessel endothelial cells by inducing scaffold formation. , 1997, Experimental cell research.

[54]  H. Tajiri,et al.  Induction of vascular endothelial growth factor by nitric oxide in human glioblastoma and hepatocellular carcinoma cells , 1997, Oncogene.

[55]  M. Burdick,et al.  CXC chemokines in angiogenesis , 2000, Journal of leukocyte biology.

[56]  D. Bredesen,et al.  Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. , 1993, Science.

[57]  P. Lelkes,et al.  Hypoxia/Reoxygenation Enhances Tube Formation of Cultured Human Microvascular Endothelial Cells: the Role of Reactive Oxygen Species , 1998 .

[58]  W. Schaper,et al.  Proto-oncogene expression in porcine myocardium subjected to ischemia and reperfusion. , 1992, Circulation research.

[59]  H Ueno,et al.  The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. , 1992, Science.

[60]  A. Koch,et al.  Inhibition of production of macrophage-derived angiogenic activity by the anti-rheumatic agents gold sodium thiomalate and auranofin. , 1988, Biochemical and biophysical research communications.

[61]  J. Stone,et al.  Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity , 1995, Nature Medicine.

[62]  D. Gingras,et al.  Green tea catechins inhibit vascular endothelial growth factor receptor phosphorylation. , 2002, Cancer research.

[63]  S Amerini,et al.  Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. , 1994, The Journal of clinical investigation.

[64]  Y. Fujii‐Kuriyama,et al.  Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[65]  D. Danilenko,et al.  Long-term impaired neutrophil migration in mice overexpressing human interleukin-8. , 1994, The Journal of clinical investigation.

[66]  M. Karin,et al.  The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. , 1991, Biochimica et biophysica acta.

[67]  Á. Tósaki,et al.  Effects of SOD, catalase, and a novel antiarrhythmic drug, EGB 761, on reperfusion-induced arrhythmias in isolated rat hearts. , 1993, Free radical biology & medicine.

[68]  P. Baeuerle,et al.  Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF‐kappa B transcription factor and HIV‐1. , 1991, The EMBO journal.

[69]  Á. Tósaki,et al.  Comparisons of ESR and HPLC methods for the detection of OH. radicals in ischemic/reperfused hearts. A relationship between the genesis of free radicals and reperfusion arrhythmias. , 1993, Biochemical pharmacology.

[70]  D. Faller,et al.  Hypoxia induces AP-1-regulated genes and AP-1 transcription factor binding in human endothelial and other cell types. , 1995, Biochimica et biophysica acta.

[71]  W. Lin,et al.  Induction of Tie-1 and Tie-2 Receptor Protein Expression after Cerebral Ischemia—Reperfusion , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[72]  M. Brauchle,et al.  Ultraviolet B and H2O2 Are Potent Inducers of Vascular Endothelial Growth Factor Expression in Cultured Keratinocytes* , 1996, The Journal of Biological Chemistry.

[73]  H. Dvorak,et al.  Vascular permeability factor/vascular endothelial growth factor: a multifunctional angiogenic cytokine. , 1997, EXS.

[74]  R Bicknell,et al.  Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. , 1997, The Journal of clinical investigation.

[75]  S. Courtneidge,et al.  Association between the PDGF receptor and members of the src family of tyrosine kinases , 1990, Cell.

[76]  K. Thomas.  Vascular Endothelial Growth Factor, a Potent and Selective Angiogenic Agent (*) , 1996, The Journal of Biological Chemistry.

[77]  Y. Sun,et al.  Redox regulation of transcriptional activators. , 1996, Free radical biology & medicine.

[78]  R. Nohara,et al.  Elevated basic fibroblast growth factor in pericardial fluid of patients with unstable angina. , 1996, Circulation.

[79]  M. Shibuya,et al.  VEGF activates protein kinase C-dependent, but Ras-independent Raf-MEK-MAP kinase pathway for DNA synthesis in primary endothelial cells , 1999, Oncogene.

[80]  Von der Leyen.  Gene therapy inhibiting neointimal vascular lesion , 1995 .

[81]  A. Koch,et al.  Production of angiogenic activity by human monocytes requires an L-arginine/nitric oxide-synthase-dependent effector mechanism. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[82]  P. Ratcliffe,et al.  Inducible operation of the erythropoietin 3' enhancer in multiple cell lines: evidence for a widespread oxygen-sensing mechanism. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[83]  N. Maulik,et al.  Part IX • Chapter 24 – Protection against free radical injury in the heart and cardiac performance , 2000 .

[84]  T. Coleman,et al.  Antisense inhibition of the p65 subunit of NF-kappa B blocks tumorigenicity and causes tumor regression. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[85]  N. Maulik,et al.  Ischemic preconditioning triggers the activation of MAP kinases and MAPKAP kinase 2 in rat hearts , 1996, FEBS letters.

[86]  R. Berne,et al.  Protective Effects of Adenosine In Myocardial Ischemia , 1992, Circulation.

[87]  T. Shono,et al.  Involvement of the transcription factor NF-kappaB in tubular morphogenesis of human microvascular endothelial cells by oxidative stress , 1996, Molecular and cellular biology.

[88]  J. Isner,et al.  Reciprocal relation between VEGF and NO in the regulation of endothelial integrity , 1997, Nature Medicine.

[89]  G. Poli,et al.  Oxidative damage and fibrogenesis. , 1997, Free radical biology & medicine.

[90]  N. Maulik,et al.  Reactive oxygen species function as second messenger during ischemic preconditioning of heart , 1999, Molecular and Cellular Biochemistry.

[91]  A. Ullrich,et al.  Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant , 1994, Nature.

[92]  M. Marrero,et al.  Vascular Endothelial Growth Factor Signals Endothelial Cell Production of Nitric Oxide and Prostacyclin through Flk-1/KDR Activation of c-Src* , 1999, The Journal of Biological Chemistry.

[93]  Toshinori Yamamoto,et al.  Reduction by NG‐nitro‐L‐arginine of H2O2‐induced endothelial cell injury , 1994, British journal of pharmacology.

[94]  Eugene M. Johnson,et al.  Superoxide dismutase delays neuronal apoptosis: A role for reactive oxygen species in programmed neuronal death , 1995, Neuron.

[95]  R. Strieter,et al.  Interleukin-8 as a macrophage-derived mediator of angiogenesis. , 1992, Science.

[96]  L. Brown,et al.  VEGF, flk-1, and flt-1 expression in a rat myocardial infarction model of angiogenesis. , 1996, The American journal of physiology.

[97]  N. Maulik,et al.  Hypoxic preconditioning triggers myocardial angiogenesis , 2000 .

[98]  R C Hamdy,et al.  Upregulation of vascular endothelial growth factor by H2O2 in rat heart endothelial cells. , 1998, Free radical biology & medicine.

[99]  E. Keshet,et al.  Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis , 1992, Nature.

[100]  Y. Kihara,et al.  Marked elevation of vascular endothelial growth factor and basic fibroblast growth factor in pericardial fluid of patients with angina pectoris , 2004, Angiogenesis.

[101]  R. K. Fidelus.  The generation of oxygen radicals: a positive signal for lymphocyte activation. , 1988, Cellular immunology.

[102]  Yihai Cao,et al.  Angiogenesis inhibited by drinking tea , 1999, Nature.

[103]  A. Karsan,et al.  Fibroblast growth factor-2 inhibits endothelial cell apoptosis by Bcl-2-dependent and independent mechanisms. , 1997, The American journal of pathology.

[104]  C. Frelin,et al.  Expression of vascular endothelial growth factor by cultured endothelial cells from brain microvessels. , 1993, Biochemical and biophysical research communications.

[105]  J. LaManna,et al.  Prolonged hypoxia increases vascular endothelial growth factor mRNA and protein in adult mouse brain. , 1999, Journal of applied physiology.

[106]  I. Moraru,et al.  Gene expression in acute myocardial stress. Induction by hypoxia, ischemia, reperfusion, hyperthermia and oxidative stress. , 1995, Journal of molecular and cellular cardiology.

[107]  P. Baeuerle,et al.  H2O2 and antioxidants have opposite effects on activation of NF‐kappa B and AP‐1 in intact cells: AP‐1 as secondary antioxidant‐responsive factor. , 1993, The EMBO journal.

[108]  M. Burdick,et al.  Inhibition of interleukin-8 reduces tumorigenesis of human non-small cell lung cancer in SCID mice. , 1996, The Journal of clinical investigation.

[109]  D. Das,et al.  Detection of oxidative DNA damage to ischemic reperfused rat hearts by 8-hydroxydeoxyguanosine formation. , 1998, Journal of molecular and cellular cardiology.

[110]  P. Peristeris,et al.  Evidence that nitric oxide is an endogenous antiangiogenic mediator , 1994, British journal of pharmacology.

[111]  N. Maulik,et al.  Hypoxia/reoxygenation promotes myocardial angiogenesis via an NF kappa B-dependent mechanism in a rat model of chronic myocardial infarction. , 2001, Journal of molecular and cellular cardiology.

[112]  L. Aiello,et al.  Hypoxia regulates vascular endothelial growth factor receptor KDR/Flk gene expression through adenosine A2 receptors in retinal capillary endothelial cells. , 1996, Investigative ophthalmology & visual science.

[113]  S. Yoshida,et al.  Suppression of retinal neovascularization by the NF-kappaB inhibitor pyrrolidine dithiocarbamate in mice. , 1999, Investigative ophthalmology & visual science.

[114]  Michael Karin,et al.  NF-κB in cancer: from innocent bystander to major culprit , 2002, Nature Reviews Cancer.

[115]  T. Billiar,et al.  Adenoviral transfer of the inducible nitric oxide synthase gene blocks endothelial cell apoptosis. , 1997, Surgery.

[116]  I. Fridovich.  The biology of oxygen radicals. , 1978, Science.

[117]  G. Karakiulakis,et al.  Inhibition of angiogenesis, tumour growth and metastasis by the NO‐releasing vasodilators, isosorbide mononitrate and dinitrate , 1995, British journal of pharmacology.

[118]  M. Fini,et al.  Competence for collagenase gene expression by tissue fibroblasts requires activation of an interleukin 1 alpha autocrine loop. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[119]  N. Maulik,et al.  Ischemic preconditioning triggers tyrosine kinase signaling: a potential role for MAPKAP kinase 2. , 1998, American journal of physiology. Heart and circulatory physiology.

[120]  E. Keshet,et al.  Upregulation of vascular endothelial growth factor expression induced by myocardial ischaemia: implications for coronary angiogenesis. , 1994, Cardiovascular research.

[121]  C. Garcia,et al.  Release of bFGF, an endothelial cell survival factor, by osmotic shock. , 1999, Investigative ophthalmology & visual science.

[122]  D. Das,et al.  Protection of ischemic heart from reperfusion injury by myo-inositol hexaphosphate, a natural antioxidant. , 1991, The Annals of thoracic surgery.

[123]  L. Ellis,et al.  Inhibition of tumour invasion and angiogenesis by epigallocatechin gallate (EGCG), a major component of green tea , 2001, International journal of experimental pathology.

[124]  J. Isner,et al.  Chemotactic Properties of Angiopoietin-1 and -2, Ligands for the Endothelial-specific Receptor Tyrosine Kinase Tie2* , 1998, The Journal of Biological Chemistry.

[125]  Á. Tósaki,et al.  Grape seed proanthocyanidin reduces cardiomyocyte apoptosis by inhibiting ischemia/reperfusion-induced activation of JNK-1 and C-JUN. , 2001, Free Radical Biology & Medicine.

[126]  Y. Kaneda,et al.  Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[127]  M. Monte,et al.  Hydrogen peroxide is involved in lymphocyte activation mechanisms to induce angiogenesis. , 1997, European journal of cancer.

[128]  N. Maulik,et al.  Hypoxic preconditioning triggers myocardial angiogenesis: a novel approach to enhance contractile functional reserve in rat with myocardial infarction. , 2002, Journal of molecular and cellular cardiology.

[129]  C. Cetrulo,et al.  Vascular endothelial growth factor inhibits endothelial cell apoptosis induced by tumor necrosis factor-alpha: balance between growth and death signals. , 1997, Journal of molecular and cellular cardiology.

[130]  N. Maulik,et al.  Oxygen Free Radical Signaling in Ischemic Preconditioning a , 1999, Annals of the New York Academy of Sciences.

[131]  E. Masini,et al.  Role of nitric oxide in angiogenesis and tumor progression in head and neck cancer. , 1998, Journal of the National Cancer Institute.