IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species-dependent endothelial migration and proliferation

Circulation Research

Volumn 95, Issue 3, 2004, Pages 276-283

  Yamaoka Tojo, Minako ^a   Ushio Fukai, Masuko ^a   Hilenski, Lula ^a   Dikalov, Sergey I ^a   Chen, Yuqing E ^b   Tojo, Taiki ^a   Fukai, Tohru ^a   Fujimoto, Mitsuaki ^a   Patrushev, Nikolay A ^a   Wang, Ningning ^d   Kontos, Christopher D ^c   Bloom, George S ^d   Alexander, R Wayne ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOREHOUSE SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Cell migration; Endothelial cell; IQGAP1; Reactive oxygen species; Vascular endothelial growth factor

Indexed keywords

BINDING PROTEIN; CELL ADHESION MOLECULE; CELL PROTEIN; CYTOSKELETON PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; PROTEIN KINASE B; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SCAFFOLDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTERY INJURY; ARTICLE; BALLOON DILATATION; BIOASSAY; BLOOD VESSEL; CAROTID ARTERY; CELL CULTURE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE DELETION; HUMAN; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PULLDOWN ASSAY; RAT; RECEPTOR BINDING; REENDOTHELIALIZATION; TISSUE REGENERATION; TISSUE REPAIR; VASCULAR ENDOTHELIUM;

ANIMALS; BALLOON DILATATION; CAROTID ARTERY INJURIES; CATTLE; CELL DIVISION; CELL MOVEMENT; CELL POLARITY; CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RAC1 GTP-BINDING PROTEIN; RAS GTPASE-ACTIVATING PROTEINS; RATS; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; WOUND HEALING;

EID: 4043148481     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000136522.58649.60     Document Type: Article

References (37)

1. Ross R. Atherosclerosis: an inflammatory disease. N Engl J Med. 1999;340:115-126.
2. Folkman J. Angiogenesis: initiation and control. Ann N|Y Acad Sci. 1982;401:212-227.
3. Senger DR, Brown LF, Claffey KP, Dvorak HF. Vascular permeability factor, tumor angiogenesis and stroma generation. Invasion Metastasis. 1994;14:385-394.
4. Matsumoto T, Claesson-Welsh L. VEGF receptor signal transduction. Science's STKE. 2001;112:1-12.
5. Asahara T, Takahashi T, Masuda H, Kalka C, Chen D, Iwaguro H, Inai Y, Silver M, Isner JM. VEGF contributes to postnatal neovascularization by mobilizing bone marrow-derived endothelial progenitor cells. EMBO J. 1999;18:3964-3972.
6. Iwaguro H, Yamaguchi J, Kalka C, Murasawa S, Masuda H, Hayashi S, Silver M, Li T, Isner JM, Asahara T. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation. 2002;105:732-738.
7. Asahara T, Bauters C, Pastore C, Kearney M, Rossow S, Bunting S, Ferrara N, Symes JF, Isner JM. Local delivery of vascular endothelial growth factor accelerates reendothelialization and attenuates intimal hyperplasia in balloon-injured rat carotid artery. Circulation. 1995;91:2793-2801.
8. Gennaro G, Menard C, Michaud SE, Rivard A. Age-dependent impairment of reendothelialization after arterial injury: role of vascular endothelial growth factor. Circulation. 2003;107:230-233.
9. Abid MR, Tsai JC, Spokes KC, Deshpande SS, Irani K, Aird WC. Vascular endothelial growth factor induces manganese-superoxide dismutase expression in endothelial cells by a Rac1-regulated NADPH oxidase-dependent mechanism. FASEB J. 2001;15:2548-2550.
10. Colavitti R, Pani G, Bedogni B, Anzevino R, Borrello S, Waltenberger J, Galeotti T. Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/KDR. J Biol Chem. 2002;277:3101-3108.
11. Ushio-Fukai M, Tang Y, Fukai T, Dikalov S, Ma Y, Fujimoto M, Quinn MT, Pagano PJ, Johnson C, Alexander RW. Novel role of gp91phox-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res. 2002;91:1160-1167.
12. Mateer SC, Wang N, Bloom GS. IQGAPs: integrators of the cytoskeleton, cell adhesion machinery, and signaling networks. Cell Motil Cytoskeleton. 2003;55:147-155.
13. Joyal JL, Annan RS, Ho YD, Huddleston ME, Carr SA, Hart MJ, Sacks DB. Calmodulin modulates the interaction between IQGAP1 and Cdc42. Identification of IQGAP1 by nanoelectrospray tandem mass spectrometry. J Biol Chem. 1997;272:15419-15425.
14. 2+/ calmodulin and Cdc42 signaling. J Biol Chem. 1999;274:464-470.
15. Hart MJ, Callow MG, Souza B, Polakis P. IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J. 1996;15:2997-3005.
16. Mateer SC, McDaniel AE, Nicolas V, Habermacher GM, Lin MJ, Cromer DA, King ME, Bloom GS. The mechanism for regulation of the F-actin binding activity of IQGAP1 by calcium/calmodulin. J Biol Chem. 2002;277:12324-12333.
17. Fukata M, Kuroda S, Nakagawa M, Kawajiri A, Itoh N, Shoji I, Matsuura Y, Yonehara S, Fujisawa H, Kikuchi A, Kaibuchi K. Cdc42 and Rac1 regulate the interaction of IQGAP1 with beta-catenin. J Biol Chem. 1999;274:26044-26050.
18. Briggs MW, Li Z, Sacks DB. IQGAP1-mediated stimulation of transcriptional co-activation by beta-catenin is modulated by calmodulin. J Biol Chem. 2002;277:7453-7465.
19. Kuroda S, Fukata M, Nakagawa M, Fujii K, Nakamura T, Ookubo T, Izawa I, Nagase T, Nomura N, Tani H, Shoji I, Matsuura Y, Yonehara S, Kaibuchi K. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin- mediated cell-cell adhesion. Science. 1998;281:832-835.
20. Fukata M, Watanabe T, Noritake J, Nakagawa M, Yamaga M, Kuroda S, Matsuura Y, Iwamatsu A, Perez F, Kaibuchi K. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell. 2002;109:873-885.
21. Bashour AM, Fullerton AT, Hart MJ, Bloom GS. IQGAP1, a Rac- and Cdc42-binding protein, directly binds and cross-links microfilaments. J Cell Biol. 1997;137:1555-1566.
22. Weissbach L, Settleman J, Kalady MF, Snijders AJ, Murthy AE, Yan YX, Bernards A. Identification of a human rasGAP-related protein containing calmodulin-binding motifs. J Biol Chem. 1994;269:20517-20521.
23. Mataraza JM, Briggs MW, Li Z, Entwistle A, Ridley AJ, Sacks DB. IQGAP1 promotes cell motility and invasion. J Biol Chem. 2003;278:41237-41245.
24. Ushio-Fukai M, Alexander RW, Akers M, Griendling KK. p38MAP kinase is a critical component of the redox-sensitive signaling pathways by angiotensin II: role in vascular smooth muscle cell hypertrophy. J Biol Chem. 1998;273:15022-15029.
25. Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, Yamada KM. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science. 1998;280:1614-1617.
26. Dougher-Vermazen M, Hulmes JD, Bohlen P, Terman BI. Biological activity and phosphorylation sites of the bacterially expressed cytosolic domain of the KDR VEGF-receptor. Biochem Biophys Res Commun. 1994;205:728-738.
27. 2+, calmodulin, Cdc42 and the cytoskeleton. FEBS Lett. 2003;542:7-11.
28. Mateer SC, Morris LE, Cromer DA, Bensenor LB, Bloom GS. Actin filament binding by a monomeric IQGAP1 fragment with a single calponin homology domain. Cell Motil Cytoskeleton. In press.
29. Roy M, Li Z, Sacks DB. IQGAP1 binds ERK2 and modulates its activity. J Biol Chem. 2004;279:17329-17337.
30. Pawson T, Scott JD. Signaling through scaffold, anchoring, and adaptor proteins. Science. 1997;278:2075-2080.
31. Li Z, Kim SH, Higgins JM, Brenner MB, Sacks DB. IQGAP1 and calmodulin modulate E-cadherin function. J Biol Chem. 1999;274:37885-37892.
32. Fukata M, Nakagawa M, Kuroda S, Kaibuchi K. Effects of Rho family GTPases on cell-cell adhesion. Methods Mol Biol. 2002;189:121-128.
33. Xiao Z, Zhang N, Murphy DB, Devreotes PN. Dynamic distribution of chemoattractant receptors in living cells during chemotaxis and persistent stimulation. J Cell Biol. 1997;139:365-374.
34. Servant G, Weiner OD, Neptune ER, Sedat JW, Bourne HR. Dynamics of a chemoattractant receptor in living neutrophils during chemotaxis. Mol Biol Cell. 1999;10:1163-1178.
35. Kraynov VS, Chamberlain C, Bokoch GM, Schwartz MA, Slabaugh S, Hahn KM. Localized Rac activation dynamics visualized in living cells. Science. 2000;290:333-337.
36. Moldovan L, Moldovan NI, Sohn RH, Parikh SA, Goldschmidt-Clermont PJ. Redox changes of cultured endothelial cells and actin dynamics. Circ Res. 2000;86:549-557.
37. Abid MR, Kachra Z, Spokes KC, Aird WC. NADPH oxidase activity is required for endothelial cell proliferation and migration. FEBS Lett. 2000;486:252-256.