Publication Cover
Endothelium
Journal of Endothelial Cell Research
Volume 15, 2008 - Issue 4
34
Views
33
CrossRef citations to date
0
Altmetric
Regular Articles

Protein Kinase C–Mediated Phosphorylation of p47phox Modulates Platelet-Derived Growth Factor–Induced H2O2 Generation and Cell Proliferation in Human Umbilical Vein Endothelial Cells

&
Pages 175-188 | Received 10 Feb 2008, Accepted 29 Apr 2008, Published online: 13 Jul 2009

REFERENCES

  • Adachi T., Togashi H., Suzuki A., Kasai S., Ito J., Sugahara K., Kawata S. NAD(P)H oxidase plays a crucial role in PDGF-induced proliferation of hepatic stellate cells. Hepatology 2005; 41: 1272–1281
  • Ago T., Nunoi H., Ito T., Sumimoto H. Mechanism for phosphorylation-induced activation of the phagocyte NADPH oxidase protein p47phox. Triple replacement of serines 303, 304, and 328 with aspartates disrupts the SH3 domain-mediated intramolecular interaction in p47phox, thereby activating the oxidase. Journal of Biological Chemistry 1999; 274: 33644–33653
  • Al-Shabrawey M., Bartoli M., El-Remessy A. B., Platt D. H., Matragoon S., Behzadian M. A., Caldwell R. W., Caldwell R. B. Inhibition of NAD(P)H oxidase activity blocks vascular endothelial growth factor overexpression and neovascularization during ischemic retinopathy. American Journal of Pathology 2005; 167: 599–607
  • Arnold R. S., Shi J., Murad E., Whalen A. M., Sun C. Q., Polavarapu R., Parthasarathy S., Petros J. A., Lambeth J. D. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proceedings of the National Academy of Sciences of the United States of America 2001; 98: 5550–5555
  • Aw T. Y. Cellular redox: A modulator of intestinal epithelial cell proliferation. News in Physiological Science 2003; 18: 201–204
  • Babior B. M. The activity of leukocyte NADPH oxidase: Regulation by p47phox cysteine and serine residues. Antioxidants and Redox Signaling 2002; 4: 35–38
  • Babior B. M. NADPH oxidase. Current Opinion in Immunology 2004; 16: 42–47
  • Babior B. M., Lambeth J. D., Nauseef W. The neutrophil NADPH oxidase. Archives in Biochemistry and Biophysics 2002; 397: 342–344
  • Bae G. U., Seo D. W., Kwon H. K., Lee H. Y., Hong S., Lee Z. W., Ha K. S., Lee H. W., Han J. W. Hydrogen peroxide activates p70(S6k) signaling pathway. Journal of Biological Chemistry 1999; 274: 32596–32602
  • Bae Y. S., Kang S. W., Seo M. S., Baines I. C., Tekle E., Chock P. B., Rhee S. G. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. Journal of Biological Chemistry 1997; 272: 217–221
  • Becker T. C., Noel R. J., Coats W. S., Gomez-Foix A. M., Alam T., Gerard R. D., Newgard C. B. Use of recombinant adenovirus for metabolic engineering of mammalian cells. Methods in Cell Biology 1994; 43: 161–189
  • Beers R. F., Jr., Sizer I. W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. Journal of Biological Chemistry 1952; 195: 133–140
  • Bennett M. R. Reactive oxygen species and death: Oxidative DNA damage in atherosclerosis. Circulation Research 2001; 88: 648–650
  • Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976; 72: 248–254
  • Burdon R. H. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radical Biology and Medicine 1995; 18: 775–794
  • Burdon R. H. Control of cell proliferation by reactive oxygen species. Biochemical Society Transactions 1996; 24: 1028–1032
  • Catarzi S., Biagioni C., Giannoni E., Favilli F., Marcucci T., Iantomasi T., Vincenzini M. T. Redox regulation of platelet-derived-growth-factor-receptor: Role of NADPH-oxidase and c-Src tyrosine kinase. Biochimica et Biophysica Acta 2005; 1745: 166–175
  • Chen K. C., Zhou Y., Xing K., Krysan K., Lou M. F. Platelet derived growth factor (PDGF)-induced reactive oxygen species in the lens epithelial cells: The redox signaling. Experimental Eye Research 2004; 78: 1057–1067
  • Chen Q., Powell D. W., Rane M. J., Singh S., Butt W., Klein J. B., McLeish K. R. Akt phosphorylates p47phox and mediates respiratory burst activity in human neutrophils. Journal of Immunology 2003; 170: 5302–5308
  • Cheng G., Cao Z., Xu X., van Meir E. G., Lambeth J. D. Homologs of gp91phox: Cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 2001; 269: 131–140
  • Combadiere C., El B. J., Pedruzzi E., Hakim J., Perianin A. Stimulation of the human neutrophil respiratory burst by formyl peptides is primed by a protein kinase inhibitor, staurosporine. Blood 1993; 82: 2890–2898
  • Crow J. M., Lima P. H., Agapitos P. J., Nelson J. D. Effects of insulin and EGF on DNA synthesis in bovine endothelial cultures: Flow cytometric analysis. Investigative Ophthalmology and Visual Sciences 1994; 35: 128–133
  • Dang P. M., Fontayne A., Hakim J., El B. J., Perianin A. Protein kinase Cζ phosphorylates a subset of selective sites of the NADPH oxidase component p47phox and participates in formyl peptide-mediated neutrophil respiratory burst. Journal of Immunology 2001; 166: 1206–1213
  • Edgell C. J., McDonald C. C., Graham J. B. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proceedings of the National Academy of Sciences of the United States of America 1983; 80: 3734–3737
  • El Benna J., Faust L. P., Babior B. M. The phosphorylation of the respiratory burst oxidase component p47phox during neutrophil activation. Phosphorylation of sites recognized by protein kinase C and by proline-directed kinases. Journal of Biological Chemistry 1994; 269: 23431–23436
  • El Benna J., Faust R. P., Johnson J. L., Babior B. M. Phosphorylation of the respiratory burst oxidase subunit p47phox as determined by two-dimensional phosphopeptide mapping. Phosphorylation by protein kinase C, protein kinase A, and a mitogen-activated protein kinase. Journal of Biological Chemistry 1996; 271: 6374–6378
  • Faust L. R., El Benna J., Babior B. M., Chanock S. J. The phosphorylation targets of p47phox, a subunit of the respiratory burst oxidase. Functions of the individual target serines as evaluated by site-directed mutagenesis. Journal of Clinical Investigation 1995; 96: 1499–1505
  • Fernández-Pol J. A., Hamilton P. D., Klos D. J. Correlation between the loss of the transformed phenotype and an increase in superoxide dismutase activity in a revertant subclone of sarcoma virus-infected mammalian cells. Cancer Research 1982; 42: 609–617
  • Finkel T. Oxygen radicals and signaling. Curr.Opin.Cell Biol. 1998; 10: 248–253
  • Fontayne A., Dang P. M., Gougerot-Pocidalo M. A., El Benna J. Phosphorylation of p47phox sites by PKCα, β II, δ, and ζ : Effect on binding to p22phox and on NADPH oxidase activation. Biochemistry 2002; 41: 7743–7750
  • Ginnan R., Singer H. A. PKCδ -dependent pathways contribute to PDGF-stimulated ERK1/2 activation in vascular smooth muscle. American Journal of Physiology 2005; 288: C1193–C1201
  • Gotoh Y., Noda T., Iwakiri R., Fujimoto K., Rhoads C. A., Aw T. Y. Lipid peroxide-induced redox imbalance differentially mediates CaCo-2 cell proliferation and growth arrest. Cell Proliferation 2002; 35: 221–235
  • Hayakawa T., Suzuki K., Suzuki S., Andrews P. C., Babior B. M. A possible role for protein phosphorylation in the activation of the respiratory burst in human neutrophils. Evidence from studies with cells from patients with chronic granulomatous disease. Journal of Biological Chemistry 1986; 261: 9109–9115
  • Hoyal C. R., Gutiérrez A., Young B. M., Catz S. D., Lin J. H., Tsichlis P. N., Babior B. M. Modulation of p47phox activity by site-specific phosphorylation: Akt-dependent activation of the NADPH oxidase. Proceedings of the National Academy of Sciences of the United States of America 2003; 100: 5130–5135
  • Inanami O., Johnson J. L., McAdara J. K., Benna J. E., Faust L. R., Newburger P. E., Babior B. M. Activation of the leukocyte NADPH oxidase by phorbol ester requires the phosphorylation of p47phox on serine 303 or 304. Journal of Biological Chemistry 1998; 273: 9539–9543
  • Irani K., Xia Y., Zweier J. L., Sollott S. J., Der C. J., Fearon E. R., Sundaresan M., Finkel T., Goldschmidt-Clermont P. J. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 1997; 275: 1649–1652
  • Johnson J. L., Park J. W., Benna J. E., Faust L. P., Inanami O., Babior B. M. Activation of p47phox, a cytosolic subunit of the leukocyte NADPH oxidase. Phosphorylation of ser-359 or ser-370 precedes phosphorylation at other sites and is required for activity. Journal of Biological Chemistry 1998; 273: 35147–35152
  • Kramer I. M., Verhoeven A. J., van der Bend R. L., Weening R. S., Roos D. Purified protein kinase C phosphorylates a 47-kDa protein in control neutrophil cytoplasts but not in neutrophil cytoplasts from patients with the autosomal form of chronic granulomatous disease. Journal of Biological Chemistry 1988; 263: 2352–2357
  • Lam E. W., Zwacka R., Seftor E. A., Nieva D. R., Davidson B. L., Engelhardt J. F., Hendrix M. J., Oberley L. W. Effects of antioxidant enzyme overexpression on the invasive phenotype of hamster cheek pouch carcinoma cells. Free Radical Biology and Medicine 1999; 27: 572–579
  • Lee A. W., States D. J. Colony-stimulating factor-1 requires PI3-kinase-mediated metabolism for proliferation and survival in myeloid cells. Cell Death and Differentiation 2006; 13: 1900–1914
  • Lee S. R., Kwon K. S., Kim S. R., Rhee S. G. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. Journal of Biological Chemistry 1998; 273: 15366–15372
  • Levy R., Dana R., Leto T. L., Malech H. L. The requirement of p47 phosphorylation for activation of NADPH oxidase by opsonized zymosan in human neutrophils. Biochimica et Biophysica Acta 1994; 1220: 253–260
  • Li J. M., Shah A. M. Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. Journal of Biological Chemistry 2002; 277: 19952–19960
  • Lopes L. R., Hoyal C. R., Knaus U. G., Babior B. M. Activation of the leukocyte NADPH oxidase by protein kinase C in a partially recombinant cell-free system. Journal of Biological Chemistry 1999; 274: 15533–15537
  • Luczak K., Balcerczyk A., Soszynski M., Bartosz G. Low concentration of oxidant and nitric oxide donors stimulate proliferation of human endothelial cells in vitro. Cell Biology International 2004; 28: 483–486
  • Matsumoto T., Claesson-Welsh L. VEGF receptor signal transduction. 2001; RE21, Science STKE
  • Misra H. P., Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry 1972; 247: 3170–3175
  • Natarajan V., Taher M. M., Roehm B., Parinandi N. L., Schmid H. H., Kiss Z., García J. G. Activation of endothelial cell phospholipase D by hydrogen peroxide and fatty acid hydroperoxide. Journal of Biological Chemistry 1993; 268: 930–937
  • Nauseef W. M., Volpp B. D., McCormick S., Leidal K. G., Clark R. A. Assembly of the neutrophil respiratory burst oxidase. Protein kinase C promotes cytoskeletal and membrane association of cytosolic oxidase components. Journal of Biological Chemistry 1991; 266: 5911–5917
  • Park J. W., Babior B. M. Activation of the leukocyte NADPH oxidase subunit p47phox by protein kinase C. A phosphorylation-dependent change in the conformation of the C-terminal end of p47phox. Biochemistry 1997; 36: 7474–7480
  • Petry A., Djordjevic T., Weitnauer M., Kietzmann T., Hess J., Görlach A. NOX2 and NOX4 mediate proliferative response in endothelial cells. Antioxidant and Redox Signaling 2006; 8: 1473–1484
  • Russell C., Acevedo-Duncan M. Effects of the PKC inhibitor PD 406976 on cell cycle progression, proliferation, PKC isozymes and apoptosis in glioma and SVG-transformed glial cells. Cell Proliferation 2005; 38: 87–106
  • Saito S., Frank G. D., Mifune M., Ohba M., Utsunomiya H., Motley E. D., Inagami T., Eguchi S. Ligand-independent trans-activation of the platelet-derived growth factor receptor by reactive oxygen species requires protein kinase Cδ and c-Src. Journal of Biological Chemistry 2002; 277: 44695–44700
  • Sauer H., Wartenberg M., Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cellular Physiology and Biochemistry 2001; 11: 173–186
  • Shi M., Yang H., Motley E. D., Guo Z. Overexpression of Cu/Zn-superoxide dismutase and/or catalase in mice inhibits aorta smooth muscle cell proliferation. American Journal of Hypertension 2004; 17: 450–456
  • Simon A. R., Rai U., Fanburg B. L., Cochran B. H. Activation of the JAK-STAT pathway by reactive oxygen species. American Journal of Physiology 1998; 275: C1640–C1652
  • Suh Y. A., Arnold R. S., Lassegue B., Shi J., Xu X., Sorescu D., Chung A. B., Griendling K. K., Lambeth J. D. Cell transformation by the superoxide-generating oxidase Mox1. Nature 1999; 401: 79–82
  • Sumimoto H., Miyano K., Takeya R. Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochemical and Biophysical Research Communications 2005; 338: 677–686
  • Sundaresan M., Yu Z. X., Ferrans V. J., Irani K., Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995; 270: 296–299
  • Suzukawa K., Miura K., Mitsushita J., Resau J., Hirose K., Crystal R., Kamata T. Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. Journal of Biological Chemistry 2000; 275: 13175–13178
  • Suzuki R., Gopalrao R. K., Maeda H., Rao P., Yamamoto M., Xing Y., Mizobuchi S., Sasaguri S. MCI-186 inhibits tumor growth through suppression of EGFR phosphorylation and cell cycle arrest. Anticancer Research 2005; 25: 1131–1138
  • Ushio-Fukai M., Alexander R. W. Reactive oxygen species as mediators of angiogenesis signaling: Role of NAD(P)H oxidase. Molecular and Cellular Biochemistry 2004; 264: 85–97
  • Vaquero E. C., Edderkaoui M., Pandol S. J., Gukovsky I., Gukovskaya A. S. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. Journal of Biological Chemistry 2004; 279: 34643–34654
  • Wolfson M., McPhail L. C., Nasrallah V. N., Snyderman R. Phorbol myristate acetate mediates redistribution of protein kinase C in human neutrophils: Potential role in the activation of the respiratory burst enzyme. Journal of Immunology 1985; 135: 2057–2062
  • Wright G. E., Hubscher U., Khan N. N., Focher F., Verri A. Inhibitor analysis of calf thymus DNA polymerases α, δ and ε. FEBS Letters 1994; 341: 128–130
  • Yan T., Oberley L. W., Zhong W., St Clair D. K. Manganese-containing superoxide dismutase overexpression causes phenotypic reversion in SV40-transformed human lung fibroblasts. Cancer Research 1996; 56: 2864–2871
  • Zafari A. M., Ushio-Fukai M., Akers M., Yin Q., Shah A., Harrison D. G., Taylor W. R., Griendling K. K. Role of NADH/NADPH oxidase-derived H2O2 in angiotensin II-induced vascular hypertrophy. Hypertension 1998; 32: 488–495
  • Zanetti M., Katusic Z. S., O'Brien T. Adenoviral-mediated overexpression of catalase inhibits endothelial cell proliferation. American Journal of Physiology 2002; 283: H2620–H2626
  • Zwacka R. M., Dudus L., Epperly M. W., Greenberger J. S., Engelhardt J. F. Redox gene therapy protects human IB-3 lung epithelial cells against ionizing radiation-induced apoptosis. Human Gene Therapy 1998; 9: 1381–1386

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.