Endothelial adapter proteins in leukocyte transmigration

Jaap D. van Buul; Peter L. Hordijk

doi:10.1160/TH08-11-0714

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2009; 101(04): 649-655
DOI: 10.1160/TH08-11-0714

Theme Issue Article

Schattauer GmbH

Endothelial adapter proteins in leukocyte transmigration

Jaap D. van Buul

,

Peter L. Hordijk

Abstract

Summary

Leukocyte transendothelial migration (TEM) requires endothelial signalling. This signalling is initiated by clustering of cell-surface adhesion molecules and transmitted into the endothelium by a group of associated or co-clustered adapter proteins. These adapter proteins, such as cortactin and filamin, connect the adhesion molecules to the actin cytoskeleton as well as to signalling enzymes and downstream pathways. This short review aims to define common themes in adapter protein binding in endothelial cells and to propose critical functions that are exerted by these adapters in leukocyte transendothelial migration.

Keywords

Adhesion receptors - endothelial cells - signal transduction - inflammation - leukocyte trafficking / recruitment

Full Text

References

References
1 Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 1994; 76: 301-314.
2 van Buul JD, Kanters E, Hordijk PL. Endothelial signalling by Ig-like cell adhesion molecules. Arterioscler Thromb Vasc Biol 2007; 27: 1870-1876.
3 Ley K, Laudanna C, Cybulsky MI. et al. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-689.
4 Vestweber D. Adhesion and signalling molecules controlling the transmigration of leukocytes through endothelium. Immunol Rev 2007; 218: 178-196.
5 Orlova VV, Chavakis T. Regulation of vascular endothelial permeability by junctional adhesion molecules (JAM). Thromb Haemost 2007; 98: 327-332.
6 Yoshida M, Westlin WF, Wang N. et al. Leukocyte adhesion to vascular endothelium induces E-selectin linkage to the actin cytoskeleton. J Cell Biol 1996; 133: 445-455.
7 Kaplanski G, Farnarier C, Benoliel AM. et al. A novel role for E- and P-selectins: shape control of endothelial cell monolayers. J Cell Sci. 1994; 107: 2449-2457.
8 Hu Y, Kiely JM, Szente BE. et al. E-selectin-dependent signalling via the mitogen-activated protein kinase pathway in vascular endothelial cells. J Immunol 2000; 165: 2142-2148.
9 Tilghman RW, Hoover RL. The Src-cortactin pathway is required for clustering of E-selectin and ICAM-1 in endothelial cells. FASEB J 2002; 16: 1257-1259.
10 Hu Y, Szente B, Kiely JM. et al. Molecular events in transmembrane signalling via E-selectin. SHP2 association, adaptor protein complex formation and ERK1/2 activation. J Biol Chem 2001; 276: 48549-48553.
11 Rivera-Nieves J, Burcin TL, Olson TS. et al. Critical role of endothelial P-selectin glycoprotein ligand 1 in chronic murine ileitis. J Exp Med 2006; 203: 907-917.
12 da Costa MP, Garcia-Vallejo JJ, van Thienen JV. et al. P-selectin glycoprotein ligand-1 is expressed on endothelial cells and mediates monocyte adhesion to activated endothelium. Arterioscler Thromb Vasc Biol 2007; 27: 1023-1029.
13 Alonso-Lebrero JL, Serrador JM, Dominguez-Jimenez C. et al. Polarization and interaction of adhesion molecules P-selectin glycoprotein ligand 1 and intercellular adhesion molecule 3 with moesin and ezrin in myeloid cells. Blood 2000; 95: 2413-2419.
14 Serrador JM, Urzainqui A, Alonso-Lebrero JL. et al. A juxta-membrane amino acid sequence of P-selectin glycoprotein ligand-1 is involved in moesin binding and ezrin/radixin/moesin-directed targeting at the trailing edge of migrating lymphocytes. Eur J Immunol 2002; 32: 1560-1566.
15 Urzainqui A, Serrador JM, Viedma F. et al. ITAM-based interaction of ERM proteins with Syk mediates signalling by the leukocyte adhesion receptor PSGL-1. Immunity 2002; 17: 401-412.
16 da Costa MP, van den Berk N, Ulfman LH. et al. Platelet-monocyte complexes support monocyte adhesion to endothelium by enhancing secondary tethering and cluster formation. Arterioscler Thromb Vasc Biol 2004; 24: 193-199.
17 Barreiro O, Zamai M, Yanez-Mo M. et al. Endothelial adhesion receptors are recruited to adherent leukocytes by inclusion in preformed tetraspanin nanoplat-forms. J Cell Biol 2008; 183: 527-542.
18 Durieu-Trautmann O, Chaverot N, Cazaubon S. et al. Intercellular adhesion molecule 1 activation induces tyrosine phosphorylation of the cytoskeleton-associated protein cortactin in brain microvessel endothelial cells. J Biol Chem 1994; 269: 12536-12540.
19 Yang L, Kowalski JR, Yacono P. et al. Endothelial cell cortactin coordinates intercellular adhesion molecule-1 clustering and actin cytoskeleton remodeling during polymorphonuclear leukocyte adhesion and transmigration. J Immunol 2006; 177: 6440-6449.
20 Yang L, Kowalski JR, Zhan X. et al. Endothelial cell cortactin phosphorylation by Src contributes to polymorphonuclear leukocyte transmigration in vitro. Circ Res 2006; 98: 394-402.
21 Daly RJ. Cortactin signalling and dynamic actin networks. Biochem J 2004; 382: 13-25.
22 Bryce NS, Clark ES, Leysath JL. et al. Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol 2005; 15: 1276-1285.
23 Etienne S, Adamson P, Greenwood J. et al. ICAM-1 signalling pathways associated with Rho activation in microvascular brain endothelial cells. J Immunol 1998; 161: 5755-5761.
24 Heiska L, Alfthan K, Gronholm M. et al. Association of ezrin with intercellular adhesion molecule-1 and –2 (ICAM-1 and ICAM-2). Regulation by phosphatidylinositol 4, 5-bisphosphate. J Biol Chem 1998; 273: 21893-21900.
25 Romero IA, Amos CL, Greenwood J. et al. Ezrin and moesin co-localise with ICAM-1 in brain endothelial cells but are not directly associated. Brain Res Mol Brain Res 2002; 105: 47-59.
26 Barreiro O, Yanez-Mo M, Serrador JM. et al. Dynamic interaction of VCAM-1 and ICAM-1 with moesin and ezrin in a novel endothelial docking structure for adherent leukocytes. J Cell Biol 2002; 157: 1233-1245.
27 Bretscher A, Edwards K, Fehon RG. ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 2002; 3: 586-599.
28 Oh HM, Lee S, Na BR. et al. RKIKK motif in the intracellular domain is critical for spatial and dynamic organization of ICAM-1: functional implication for the leukocyte adhesion and transmigration. Mol Biol Cell 2007; 18: 2322-2335.
29 Heiska L, Kantor C, Parr T. et al. Binding of the cytoplasmic domain of intercellular adhesion molecule-2 (ICAM-2) to alpha-actinin. J Biol Chem 1996; 271: 26214-26219.
30 Nyman-Huttunen H, Tian L, Ning L. et al. alpha-Actinin-dependent cytoskeletal anchorage is important for ICAM-5-mediated neuritic outgrowth. J Cell Sci 2006; 119: 3057-3066.
31 Stanley P, Smith A, McDowall A. et al. Intermediate-affinity LFA-1 binds alpha-actinin-1 to control migration at the leading edge of the T cell. EMBO J 2008; 27: 62-75.
32 Carpen O, Pallai P, Staunton DE. et al. Association of intercellular adhesion molecule-1 (ICAM-1) with actin-containing cytoskeleton and alpha-actinin. J Cell Biol 1992; 118: 1223-1234.
33 Celli L, Ryckewaert JJ, Delachanal E. et al. Evidence of a functional role for interaction between ICAM-1 and nonmuscle alpha-actinins in leukocyte diapedesis. J Immunol 2006; 177: 4113-4121.
34 Kanters E, van Rijssel J, Hensbergen PJ. et al. Filamin B mediates ICAM-1-driven leukocyte transendothelial migration. J Biol Chem 2008; 283: 31830-31839.
35 Stahlhut M, van Deurs B. Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton. Mol Biol Cell 2000; 11: 325-337.
36 Millan J, Hewlett L, Glyn M. et al. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat Cell Biol 2006; 8: 113-123.
37 van Buul JD, Allingham MJ, Samson T. et al. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J Cell Biol 2007; 178: 1279-1293.
38 Alcaide P, Auerbach S, Luscinskas FW. Neutrophil Recruitment under Shear Flow: It’s All about Endothelial Cell Rings and Gaps. Microcirculation 2009; 16: 43-57.
39 Ellerbroek SM, Wennerberg K, Arthur WT. et al. SGEF, a RhoG guanine nucleotide exchange factor that stimulates macropinocytosis. Mol Biol Cell 2004; 15: 3309-3319.
40 Bellanger JM, Astier C, Sardet C. et al. The Rac1– and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin. Nat Cell Biol 2000; 2: 888-892.
41 Allingham MJ, van Buul JD, Burridge K. ICAM-1-mediated, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol 2007; 179: 4053-4064.
42 Turowski P, Martinelli R, Crawford R. et al. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci 2008; 121: 29-37.
43 Cook-Mills JM, Deem TL. Active participation of endothelial cells in inflammation. J Leukoc Biol 2005; 77: 487-495.
44 Ebnet K, Schulz CU, Meyer zu Brickwedde MK. et al. Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J Biol Chem 2000; 275: 27979-27988.
45 Weber C, Fraemohs L, Dejana E. The role of junctional adhesion molecules in vascular inflammation. Nat Rev Immunol 2007; 7: 467-477.
46 Ebnet K, Aurrand-Lions M, Kuhn A. et al. 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 2003; 116: 3879-3891.
47 Orlova VV, Economopoulou M, Lupu F. et al. Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherin-mediated cell-cell contacts. J Exp. Med 2006; 203: 2703-2714.
48 Hirata K, Ishida T, Penta K. et al. Cloning of an immunoglobulin family adhesion molecule selectively expressed by endothelial cells. J Biol Chem 2001; 276: 16223-16231.
49 Wegmann F, Ebnet K, Du PL. et al. Endothelial adhesion molecule ESAM binds directly to the multi-domain adaptor MAGI-1 and recruits it to cell contacts. Exp Cell Res 2004; 300: 121-133.
50 Patrie KM, Drescher AJ, Welihinda A. et al. Interaction of two actin-binding proteins, synaptopodin and alpha-actinin-4, with the tight junction protein MAGI-1. J Biol Chem 2002; 277: 30183-30190.
51 Woodfin A, Voisin MB, Nourshargh S. PECAM-1: a multi-functional molecule in inflammation and vascular biology. Arterioscler Thromb Vasc Biol 2007; 27: 2514-2523.
52 O’Brien CD, Lim P, Sun J. et al. PECAM-1-dependent neutrophil transmigration is independent of mono-layer PECAM-1 signalling or localization. Blood 2003; 101: 2816-2825.
53 Gamulescu MA, Seifert K, Tingart M. et al. Platelet moesin interacts with PECAM-1 (CD31). Platelets 2003; 14: 211-217.
54 Matsumura T, Wolff K, Petzelbauer P. Endothelial cell tube formation depends on cadherin 5 and CD31 interactions with filamentous actin. J Immunol 1997; 158: 3408-3416.
55 Ilan N, Cheung L, Pinter E. et al. Platelet-endothelial cell adhesion molecule-1 (CD31), a scaffolding molecule for selected catenin family members whose binding is mediated by different tyrosine and serine/ threonine phosphorylation. J Biol Chem 2000; 275: 21435-21443.
56 Mamdouh Z, Chen X, Pierini LM. et al. Targeted recycling of PECAM from endothelial surface-connected compartments during diapedesis. Nature 2003; 421: 748-753.
57 Mamdouh Z, Kreitzer GE, Muller WA. Leukocyte transmigration requires kinesin-mediated microtubule-dependent membrane trafficking from the lateral border recycling compartment. J Exp Med 2008; 205: 951-966.
58 Dasgupta B, Muller WA. Endothelial Src kinase regulates membrane recycling from the lateral border recycling compartment during leukocyte transendothelial migration. Eur J Immunol 2008; 38: 3499-3507.
59 Nottebaum AF, Cagna G, Winderlich M. et al. VEPTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF. J Exp Med 2008; 205: 2929-2945.
60 Wojciak-Stothard B, Williams L, Ridley AJ. Monocyte adhesion and spreading on human endothelial cells is dependent on Rho-regulated receptor clustering. J Cell Biol 1999; 145: 1293-1307.
61 Matsui T, Yonemura S, Tsukita S. et al. Activation of ERM proteins in vivo by Rho involves phosphatidylinositol 4-phosphate 5-kinase and not ROCK kinases. Curr Biol 1999; 9: 1259-1262.
62 Ito K, Hirao A, Arai F. et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 2004; 431: 997-1002.
63 Hirao M, Sato N, Kondo T. et al. Regulation mechanism of ERM (ezrin/radixin/moesin) protein/plasma membrane association: possible involvement of phosphatidylinositol turnover and Rho-dependent signalling pathway. J Cell Biol 1996; 135: 37-51.
64 Takahashi K, Sasaki T, Mammoto A. et al. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J Biol Chem 1997; 272: 23371-23375.
65 Tolias KF, Couvillon AD, Cantley LC. et al. Characterization of a Rac1– and RhoGDI-associated lipid kinase signalling complex. Mol Cell Biol 1998; 18: 762-770.
66 van Hennik PB, ten Klooster JP, Halstead JR. et al. The C-terminal domain of Rac1 contains two motifs that control targeting and signalling specificity. J Biol Chem 2003; 278: 39166-39175.
67 Serrador JM, Alonso-Lebrero JL, del Pozo MA. et al. Moesin interacts with the cytoplasmic region of intercellular adhesion molecule-3 and is redistributed to the uropod of T lymphocytes during cell polarization. J Cell Biol 1997; 138: 1409-1423.
68 Tsukita S, Oishi K, Sato N. et al. ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J Cell Biol 1994; 126: 391-401.
69 Yonemura S, Hirao M, Doi Y. et al. Ezrin/radixin/ moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J Cell Biol 1998; 140: 885-895.
70 Weihing RR. Actin-binding and dimerization domains of HeLa cell filamin. Biochemistry 1988; 27: 1865-1869.
71 Stossel TP, Condeelis J, Cooley L. et al. Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2001; 2: 138-145.
72 Feng Y, Chen MH, Moskowitz IP. et al. Filamin A (FLNA) is required for cell-cell contact in vascular development and cardiac morphogenesis. Proc Natl Acad Sci USA 2006; 103: 19836-19841.
73 Ohta Y, Suzuki N, Nakamura S. et al. The small GTPase RalA targets filamin to induce filopodia. Proc Natl Acad Sci USA 1999; 96: 2122-2128.
74 Mammoto A, Huang S, Ingber DE. Filamin links cell shape and cytoskeletal structure to Rho regulation by controlling accumulation of p190RhoGAP in lipid rafts. J Cell Sci 2007; 120: 456-467.
75 Tilghman RW, Hoover RL. E-selectin and ICAM-1 are incorporated into detergent-insoluble membrane domains following clustering in endothelial cells. FEBS Lett 2002; 525: 83-87.
76 Sjoblom B, Salmazo A, Djinovic-Carugo K. Alpha-actinin structure and regulation. Cell Mol Life Sci 2008; 65: 2688-2701.
77 Fraley TS, Tran TC, Corgan AM. et al. Phosphoinositide binding inhibits alpha-actinin bundling activity. J Biol Chem 2003; 278: 24039-24045.
78 Otey CA, Carpen O. Alpha-actinin revisited: a fresh look at an old player. Cell Motil Cytoskeleton 2004; 58: 104-111.
79 Pfau S, Leitenberg D, Rinder H. et al. Lymphocyte adhesion-dependent calcium signalling in human endothelial cells. J Cell Biol 1995; 128: 969-978.
80 Uruno T, Liu J, Li Y. et al. Sequential interaction of actin-related proteins 2 and 3 (Arp2/3) complex with neural Wiscott-Aldrich syndrome protein (N-WASP) and cortactin during branched actin filament network formation. J Biol Chem 2003; 278: 26086-26093.
81 Ammer AG, Weed SA. Cortactin branches out: roles in regulating protrusive actin dynamics. Cell Motil Cytoskeleton 2008; 65: 687-707.
82 Etienne-Manneville S, Manneville JB, Adamson P. et al. ICAM-1-coupled cytoskeletal rearrangements and transendothelial lymphocyte migration involve intracellular calcium signalling in brain endothelial cell lines. J Immunol 2000; 165: 3375-3383.
83 Carman CV, Sage PT, Sciuto TE. et al. Transcellular diapedesis is initiated by invasive podosomes. Immunity 2007; 26: 784-797.
84 Carman CV, Springer TA. Trans-cellular migration: cell-cell contacts get intimate. Curr Opin Cell Biol 2008; 20: 533-540.