Angiopoietin-1 requires IQ domain gtpase-activating protein 1 to activate rac1 and promote endothelial barrier defense

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 11, 2011, Pages 2643-2652

  David, Sascha ^a   Ghosh, Chandra C ^a   Mukherjee, Aditi ^a   Parikh, Samir M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

angiopoietin; endothelium; IQGAP1; permeability; Rac1

Indexed keywords

ANGIOPOIETIN 1; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; IQ DOMAIN GTPASE ACTIVATING PROTEIN 1; MUTANT PROTEIN; RAC1 PROTEIN; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; CELL JUNCTION; CELL STIMULATION; CELL TYPE; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE SILENCING; GENETIC TRANSFECTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MICROVASCULATURE; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ADHERENS JUNCTIONS; ANGIOPOIETIN-1; CELL MEMBRANE PERMEABILITY; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; GAP JUNCTIONS; HUMANS; RAC1 GTP-BINDING PROTEIN; RAS GTPASE-ACTIVATING PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 80054953975     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.233189     Document Type: Article

References (41)

1. Aghajanian A, Wittchen ES, Allingham MJ, Garrett TA, Burridge K. Endothelial cell junctions and the regulation of vascular permeability and leukocyte transmigration. J Thromb Haemost. 2008;6:1453-1460.
2. Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev. 2006;86:279-367.
3. Majno G, Palade GE. Studies on inflammation. 1. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J Biophys Biochem Cytol. 1961;11:571-605.
4. Aird WC. The role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. Blood. 2003;101:3765-3777. (Pubitemid 36857845)
5. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD. Isolation of angiopoietin-1, a ligand for the tie2 receptor, by secretion-trap expression cloning. Cell. 1996;87:1161-1169. (Pubitemid 27010100)
6. Sato TN, Qin Y, Kozak CA, Audus KL. Tie-1 and tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system. Proc Natl Acad Sci USA. 1993;90: 9355-9358. (Pubitemid 23315782)
7. Stratmann A, Risau W, Plate KH. Cell type-specific expression of angiopoietin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. The American J Pathol. 1998;153:1459-1466. (Pubitemid 28509902)
8. Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, McDonald DM. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 1999;286:2511-2514.
9. Thurston G, Rudge JS, Ioffe E, Zhou H, Ross L, Croll SD, Glazer N, Holash J, McDonald DM, Yancopoulos GD. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med. 2000;6:460-463. (Pubitemid 30208166)
10. Gamble JR, Drew J, Trezise L, Underwood A, Parsons M, Kasminkas L, Rudge J, Yancopoulos G, Vadas MA. Angiopoietin-1 is an antipermeability and anti-inflammatory agent in vitro and targets cell junctions. Circ Res. 2000;87:603-607.
11. Pizurki L, Zhou Z, Glynos K, Roussos C, Papapetropoulos A. Angiopoietin-1 inhibits endothelial permeability, neutrophil adherence and IL-8 production. Br J Pharmacol. 2003;139:329-336. (Pubitemid 36760365)
12. Bogatcheva NV, Verin AD. The role of cytoskeleton in the regulation of vascular endothelial barrier function. Microvasc Res. 2008;76:202-207.
13. Csortos C, Kolosova I, Verin AD. Regulation of vascular endothelial cell barrier function and cytoskeleton structure by protein phosphatases of the PPP family. Am J Physiol Lung Cell Mol Physiol. 2007;293:L843-L854. (Pubitemid 47572232)
14. Lee MJ, Thangada S, Claffey KP, Ancellin N, Liu CH, Kluk M, Volpi M, Sha'afi RI, Hla T. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell. 1999;99: 301-312. (Pubitemid 29519909)
15. Burridge K, Wennerberg K. Rho and Rac take center stage. Cell. 2004; 116:167-179. (Pubitemid 38167310)
16. Wildenberg GA, Dohn MR, Carnahan RH, Davis MA, Lobdell NA, Settleman J, Reynolds AB. p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell. 2006;127:1027-1039. (Pubitemid 44792253)
17. Mammoto T, Parikh SM, Mammoto A, Gallagher D, Chan B, Mostoslavsky G, Ingber DE, Sukhatme VP. Angiopoietin-1 requires p190 RhoGAP to protect against vascular leakage in vivo. J Biol Chem. 2007;282:23910-23918. (Pubitemid 47328051)
18. Briggs MW, Sacks DB. IQGAP proteins are integral components of cytoskeletal regulation. EMBO Rep. 2003;4:571-574. (Pubitemid 36939947)
19. Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K. IQGAP1: a key regulator of adhesion and migration. J Cell Sci. 2005;118:2085-2092. (Pubitemid 40872832)
20. Watanabe T, Wang S, Noritake J, Sato K, Fukata M, Takefuji M, Nakagawa M, Izumi N, Akiyama T, Kaibuchi K. Interaction with IQGAP1 links APC to Rac1, Cdc42, and actin filaments during cell polarization and migration. Dev Cell. 2004;7:871-883. (Pubitemid 39654731)
21. Fukata M, Kuroda S, Fujii K, Nakamura T, Shoji I, Matsuura Y, Okawa K, Iwamatsu A, Kikuchi A, Kaibuchi K. Regulation of cross-linking of actin filament by IQGAP1, a target for Cdc42. J Biol Chem. 1997;272: 29579-29583. (Pubitemid 27508046)
22. 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. (Pubitemid 28376045)
23. Briggs MW, Sacks DB. IQGAP1 as signal integrator: Ca2+ , calmodulin, Cdc42 and the cytoskeleton. FEBS Lett. 2003;542:7-11. (Pubitemid 36555704)
24. Noritake J, Fukata M, Sato K, Nakagawa M, Watanabe T, Izumi N, Wang S, Fukata Y, Kaibuchi K. Positive role of IQGAP1, an effector of Rac1, in actin-meshwork formation at sites of cell-cell contact. Mol Biol Cell. 2004;15:1065-1076. (Pubitemid 38324580)
25. 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. (Pubitemid 37280951)
26. White CD, Brown MD, Sacks DB. IQGAPs in cancer: a family of scaffold proteins underlying tumorigenesis. FEBS Lett. 2009;583: 1817-1824.
27. Yamaoka-Tojo M, Ushio-Fukai M, Hilenski L, Dikalov SI, Chen YE, Tojo T, Fukai T, Fujimoto M, Patrushev NA, Wang N, Kontos CD, Bloom GS, Alexander RW. IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species-dependent endothelial migration and proliferation. Circ Res. 2004;95: 276-283. (Pubitemid 39056288)
28. Meyer RD, Sacks DB, Rahimi N. IQGAP1-dependent signaling pathway regulates endothelial cell proliferation and angiogenesis. PLoS ONE. 2008;3:e3848.
29. Ikeda S, Yamaoka-Tojo M, Hilenski L, Patrushev NA, Anwar GM, Quinn MT, Ushio-Fukai M. IQGAP1 regulates reactive oxygen speciesdependent endothelial cell migration through interacting with Nox2. Arterioscler Thromb Vasc Biol. 2005;25:2295-2300. (Pubitemid 41552645)
30. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA. 2004;101:7618-7623. (Pubitemid 38658078)
31. 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. (Pubitemid 34786002)
32. Hoang MV, Nagy JA, Senger DR. Active Rac1 improves pathologic VEGF neovessel architecture and reduces vascular leak: mechanistic similarities with angiopoietin-1. Blood. 2011;117:1751-1760.
33. Le Doux JM, Landazuri N, Yarmush ML, Morgan JR. Complexation of retrovirus with cationic and anionic polymers increases the efficiency of gene transfer. Hum Gene Ther. 2001;12:1611-1621. (Pubitemid 32911732)
34. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest. 2001;108:689-701. (Pubitemid 32906197)
35. Spindler V, Schlegel N, Waschke J. Role of GTPases in control of microvascular permeability. Cardiovasc Res. 2010;87:243-253.
36. Harfouche R, Malak NA, Brandes RP, Karsan A, Irani K, Hussain SN. Roles of reactive oxygen species in angiopoietin-1/tie-2 receptor signaling. FASEB J. 2005;19:1728-1730. (Pubitemid 41429544)
37. Nakhaei-Nejad M, Zhang QX, Murray AG. Endothelial IQGAP1 regulates efficient lymphocyte transendothelial migration. Eur J Immunol. 2010;40:204-213.
38. Usatyuk PV, Gorshkova IA, He D, Zhao Y, Kalari SK, Garcia JG, Natarajan V. Phospholipase D-mediated activation of IQGAP1 through Rac1 regulates hyperoxia-induced p47phox translocation and reactive oxygen species generation in lung endothelial cells. J Biol Chem. 2009; 284:15339-15352.
39. Yamaoka-Tojo M, Tojo T, Kim HW, Hilenski L, Patrushev NA, Zhang L, Fukai T, Ushio-Fukai M. IQGAP1 mediates VE-cadherin-based cell-cell contacts and VEGF signaling at adherence junctions linked to angiogenesis. Arterioscler Thromb Vasc Biol. 2006;26:1991-1997. (Pubitemid 44253779)
40. Fukuhara S, Sako K, Minami T, Noda K, Kim HZ, Kodama T, Shibuya M, Takakura N, Koh GY, Mochizuki N. Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat Cell Biol. 2008;10:513-526. (Pubitemid 351627371)
41. Saharinen P, Eklund L, Miettinen J, Wirkkala R, Anisimov A, Winderlich M, Nottebaum A, Vestweber D, Deutsch U, Koh GY, Olsen BR, Alitalo K. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat Cell Biol. 2008;10:527-537. (Pubitemid 351627372)