Tetraspanin CD9 links junctional adhesion molecule-A to αvβ3 integrin to mediate basic fibroblast growth factor-specific angiogenic signaling

Molecular Biology of the Cell

Volumn 24, Issue 7, 2013, Pages 933-944

  Peddibhotla, Swetha S D ^a   Brinkmann, Benjamin F ^a   Kummer, Daniel ^a   Tuncay, Hüseyin ^a   Nakayama, Masanori ^a   Adams, Ralf H ^a   Gerke, Volker ^a   Ebnet, Klaus ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAVBETA5 INTEGRIN; ANGIOGENIC FACTOR; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; CD9 ANTIGEN; JUNCTIONAL ADHESION MOLECULE A; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; VASCULOTROPIN; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ARTICLE; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD9; CELL ADHESION MOLECULES; CELL MOVEMENT; CELLS, CULTURED; CHO CELLS; CRICETINAE; CRICETULUS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTOR 2; HEK293 CELLS; HELA CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOBLOTTING; INTEGRIN ALPHAVBETA3; MICE; MICROSCOPY, FLUORESCENCE; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84875465330     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-06-0481     Document Type: Article

References (54)

1. Arnaoutova I, Kleinman HK (2010). In vitro angiogenesis: endothelial cell tube formation on gelled basement membrane extract. Nature Protoc 5, 628-635.
2. Barreiro O, Yanez-Mo M, Sala-Valdes M, Gutierrez-Lopez MD, Ovalle S, Higginbottom A, Monk PN, Cabanas C, Sanchez-Madrid F (2005). Endothelial tetraspanin microdomains regulate leukocyte firm adhesion during extravasation. Blood 105, 2852-2861. (Pubitemid 40446279)
3. Barreiro O, Zamai M, Yanez-Mo M, Tejera E, Lopez-Romero P, Monk PN, Gratton E, Caiolfa VR, Sanchez-Madrid F (2008). Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplatforms. J Cell Biol 183, 527-542.
4. Bazzoni G (2003). The JAM family of junctional adhesion molecules. Curr Opin Cell Biol 15, 525-530. (Pubitemid 37176960)
5. Bazzoni G, Martinez-Estrada OM, Orsenigo F, Cordenonsi M, Citi S, Dejana E (2000). Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occludin. J Biol Chem 275, 20520-20526. (Pubitemid 30457633)
6. Boucheix C, Rubinstein E (2001). Tetraspanins. Cell Mol Life Sci 58, 1189-1205. (Pubitemid 32844093)
7. Bradbury LE, Goldmacher VS, Tedder TF (1993). The CD19 signal transduction complex of B lymphocytes. Deletion of the CD19 cytoplasmic domain alters signal transduction but not complex formation with TAPA-1 and Leu 13. J Immunol 151, 2915-2927. (Pubitemid 23282605)
8. Cailleteau L et al. (2010). α2β1 integrin controls association of Rac with the membrane and triggers quiescence of endothelial cells. J Cell Sci 123, 2491-2501.
9. Charrin S, le Naour F, Silvie O, Milhiet PE, Boucheix C, Rubinstein E (2009). Lateral organization of membrane proteins: tetraspanins spin their web. Biochem J 420, 133-154.
10. Cooke VG, Naik MU, Naik UP (2006). Fibroblast growth factor-2 failed to induce angiogenesis in junctional adhesion molecule-A-deficient mice. Arterioscler Thromb Vasc Biol 26, 2005-2011. (Pubitemid 44253781)
11. Ebnet K, Aurrand-Lions M, Kuhn A, Kiefer F, Butz S, Zander K, Meyer Zu Brickwedde MK, Suzuki A, Imhof BA, Vestweber D (2003). The junctional adhesion molecule (JAM) family members JAM-2 and JAM-3 associate with the cell polarity protein PAR-3: a possible role for JAMs in endothelial cell polarity. J Cell Sci 116, 3879-3891. (Pubitemid 37279304)
12. Ebnet K, Schulz CU, Meyer Zu Brickwedde MK, Pendl GG, Vestweber D (2000). Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J Biol Chem 275, 27979-27988.
13. Ebnet K, Suzuki A, Horikoshi Y, Hirose T, Meyer Zu Brickwedde MK, Ohno S, Vestweber D (2001). The cell polarity protein ASIP/PAR-3 directly associates with junctional adhesion molecule (JAM). EMBO J 20, 3738-3748. (Pubitemid 32691785)
14. Ebnet K, Suzuki A, Ohno S, Vestweber D (2004). Junctional adhesion molecules (JAMs): more molecules with dual functions. J Cell Sci 117, 19-29. (Pubitemid 38072117)
15. Eliceiri BP, Puente XS, Hood JD, Stupack DG, Schlaepfer DD, Huang XZ, Sheppard D, Cheresh DA (2002). Src-mediated coupling of focal adhesion kinase to integrin αvβ5 in vascular endothelial growth factor signaling. J Cell Biol 157, 149-160.
16. Friedlander M, Brooks PC, Shaffer RW, Kincaid CM, Varner JA, Cheresh DA (1995). Definition of two angiogenic pathways by distinct alpha v integrins. Science 270, 1500-1502. (Pubitemid 3005294)
17. Hamazaki Y, Itoh M, Sasaki H, Furuse M, Tsukita S (2002). Multi-PDZ domain protein 1 (MUPP1) is concentrated at tight junctions through its possible interaction with claudin-1 and junctional adhesion molecule. J Biol Chem 277, 455-461. (Pubitemid 34952079)
18. Hemler ME (2005). Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 6, 801-811. (Pubitemid 41726118)
19. Hollenberg SM, Sternglanz R, Cheng PF, Weintraub H (1995). Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol Cell Biol 15, 3813-3822.
20. Hood JD, Frausto R, Kiosses WB, Schwartz MA, Cheresh DA (2003). Differential αv integrin-mediated Ras-ERK signaling during two pathways of angiogenesis. J Cell Biol 162, 933-943. (Pubitemid 37087732)
21. Iden S, Misselwitz S, Peddibhotla SS, Tuncay H, Rehder D, Gerke V, Robenek H, Suzuki A, Ebnet K (2012). aPKC phosphorylates JAM-A at Ser285 to promote cell contact maturation and tight junction formation. J Cell Biol 196, 623-639.
22. Itoh M, Sasaki H, Furuse M, Ozaki H, Kita T, Tsukita S (2001). Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J Cell Biol 154, 491-498.
23. Kamisasanuki T, Tokushige S, Terasaki H, Khai NC, Wang Y, Sakamoto T, Kosai K (2011). Targeting CD9 produces stimulus-independent antiangiogenic effects predominantly in activated endothelial cells during angiogenesis: a novel antiangiogenic therapy. Biochem Biophys Res Commun 413, 128-135.
24. Laukoetter MG et al. (2007). JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 204, 3067-3076.
25. Levy S, Shoham T (2005a). Protein-protein interactions in the tetraspanin web. Physiology (Bethesda) 20, 218-224. (Pubitemid 41215195)
26. Levy S, Shoham T (2005b). The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol 5, 136-148. (Pubitemid 40208903)
27. Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, Pochet M, Parkos CA (2000). Human junction adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 113, 2363-2374. (Pubitemid 30599341)
28. Luissint AC, Lutz PG, Calderwood DA, Couraud PO, Bourdoulous S (2008). JAM-L-mediated leukocyte adhesion to endothelial cells is regulated in cis by α4β1 integrin activation. J Cell Biol 183, 1159-1173.
29. Malergue F, Galland F, Martin F, Mansuelle P, Aurrand-Lions M, Naquet P (1998). A novel immunoglobulin superfamily junctional molecule expressed by antigen presenting cells, endothelial cells and platelets. Mol Immunol 35, 1111-1119. (Pubitemid 29057150)
30. Mandell KJ, Babbin BA, Nusrat A, Parkos CA (2005). Junctional adhesion molecule 1 regulates epithelial cell morphology through effects on β1 integrins and Rap1 activity. J Biol Chem 280, 11665-11674. (Pubitemid 40418481)
31. Mandell KJ, McCall IC, Parkos CA (2004). Involvement of the junctional adhesion molecule-1 (JAM1) homodimer interface in regulation of epithelial barrier function. J Biol Chem 279, 16254-16262. (Pubitemid 38509319)
32. Moog-Lutz C, Cave-Riant F, Guibal FC, Breau MA, Di Gioia Y, Couraud PO, Cayre YE, Bourdoulous S, Lutz PG (2003). JAML, a novel protein with characteristics of a junctional adhesion molecule, is induced during differentiation of myeloid leukemia cells. Blood 102, 3371-3378. (Pubitemid 37314780)
33. Naik MU, Mousa SA, Parkos CA, Naik UP (2003). Signaling through JAM-1 and αvβ3 is required for the angiogenic action of bFGF: dissociation of the JAM-1 and αvβ3 complex. Blood 102, 2108-2114. (Pubitemid 37122387)
34. Naik MA, Naik UP (2006). Junctional adhesion molecule-A-induced endothelial cell migration on vitronectin is integrin avb3 specific. J Cell Sci 119, 490-499.
35. Nava P et al. (2011). JAM-A regulates epithelial proliferation through Akt/β-catenin signalling. EMBO Rep 12, 314-320.
36. Nishiuchi R, Sanzen N, Nada S, Sumida Y, Wada Y, Okada M, Takagi J, Hasegawa H, Sekiguchi K (2005). Potentiation of the ligand-binding activity of integrin α3β1 via association with tetraspanin CD151. Proc Natl Acad Sci USA 102, 1939-1944. (Pubitemid 40261991)
37. Ostermann G, Weber KS, Zernecke A, Schroder A, Weber C (2002). JAM-1 is a ligand of the β2 integrin LFA-1 involved in transendothelial migration of leukocytes. Nat Immunol 3, 151-158. (Pubitemid 34141445)
38. Prota AE, Campbell JA, Schelling P, Forrest JC, Watson MJ, Peters TR, Aurrand-Lions M, Imhof BA, Dermody TS, Stehle T (2003). Crystal structure of human junctional adhesion molecule 1: implications for reovirus binding. Proc Natl Acad Sci USA 100, 5366-5371. (Pubitemid 36542711)
39. Rehder D, Iden S, Nasdala I, Wegener J, Brickwedde MK, Vestweber D, Ebnet K (2006). Junctional adhesion molecule-A participates in the formation of apico-basal polarity through different domains. Exp Cell Res 312, 3389-3403. (Pubitemid 44380238)
40. Rubinstein E, Billard M, Plaisance S, Prenant M, Boucheix C (1993). Molecular cloning of the mouse equivalent of CD9 antigen. Thrombosis Res 71, 377-383. (Pubitemid 23244326)
41. Sahni A, Francis CW (2004). Stimulation of endothelial cell proliferation by FGF-2 in the presence of fibrinogen requires αvβ3. Blood 104, 3635-3641. (Pubitemid 39564439)
42. Severson EA, Jiang L, Ivanov AI, Mandell KJ, Nusrat A, Parkos CA (2008). Cis-dimerization mediates function of junctional adhesion molecule A. Mol Biol Cell 19, 1862-1872.
43. Severson EA, Lee WY, Capaldo CT, Nusrat A, Parkos CA (2009). Junctional adhesion molecule A interacts with Afadin and PDZ-GEF2 to activate Rap1A, regulate β1 integrin levels, and enhance cell migration. Mol Biol Cell 20, 1916-1925.
44. Shattil SJ, Kim C, Ginsberg MH (2010). The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 11, 288-300.
45. Shaw SK et al. (2004). Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J Exp Med 200, 1571-1580. (Pubitemid 40094181)
46. Stipp CS, Kolesnikova TV, Hemler ME (2001). EWI-2 is a major CD9 and CD81 partner and member of a novel Ig protein subfamily. J Biol Chem 276, 40545-40554.
47. Stipp CS, Kolesnikova TV, Hemler ME (2003). Functional domains in tetraspanin proteins. Trends Biochem Sci 28, 106-112. (Pubitemid 36165140)
48. Vetrano S et al. (2008). Unique role of junctional adhesion molecule-A in maintaining mucosal homeostasis in inflammatory bowel disease. Gastroenterology 135, 173-184. (Pubitemid 351899025)
49. Wang Y et al. (2010). Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486.
50. Weber C, Fraemohs L, Dejana E (2007). The role of junctional adhesion molecules in vascular inflammation. Nat Rev Immunol 7, 467-477. (Pubitemid 46834851)
51. Yan W, Bentley B, Shao R (2008). Distinct angiogenic mediators are required for basic fibroblast growth factor- and vascular endothelial growth factor-induced angiogenesis: the role of cytoplasmic tyrosine kinase c-Abl in tumor angiogenesis. Mol Biol Cell 19, 2278-2288.
52. Yanez-Mo M, Barreiro O, Gordon-Alonso M, Sala-Valdes M, Sanchez-Madrid F (2009). Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 19, 434-446.
53. Yauch RL, Kazarov AR, Desai B, Lee RT, Hemler ME (2000). Direct extracellular contact between integrin α3β1 and TM4SF protein CD151. J Biol Chem 275, 9230-9238. (Pubitemid 30185141)
54. Zen K, Liu Y, McCall IC, Wu T, Lee W, Babbin BA, Nusrat A, Parkos CA (2005). Neutrophil migration across tight junctions is mediated by adhesive interactions between epithelial coxsackie and adenovirus receptor and a junctional adhesion molecule-like protein on neutrophils. Mol Biol Cell 16, 2694-2703. (Pubitemid 40741217)