Download PDF
Thromb Haemost 2003; 89(01): 13-17
DOI: 10.1055/s-0037-1613537
Review Article
Schattauer GmbH

Leukocyte trans-endothelial migration: JAMs add new pieces to the puzzle

Triantafyllos Chavakis
1   Department of Medicine I, University Hospital, Heidelberg, Medical Faculty, Justus Liebig University, Giessen, Germany
,
Klaus T. Preissner
2   Institute for Biochemistry, Medical Faculty, Justus Liebig University, Giessen, Germany
,
Sentot Santoso
3   Institute for Clinical Immunology and Transfusion Medicine, Medical Faculty, Justus Liebig University, Giessen, Germany
› Author Affiliations
Further Information

Publication History

Received 24 October 2002

Accepted 05 November 2002

Publication Date:
09 December 2017 (online)

    Permissions and Reprints

Summary

The molecular details of leukocyte transmigration through the endothelial barrier (also called diapedesis), which is the final step of leukocyte extravasation from the circulation to a given site of inflammation, are by far not well understood. The present review will focus on the different mechanisms potentially involved in leukocyte trans-endothelial migration. Both homophilic and heterophilic interactions between leukocyte and endothelial cell receptors will be covered, with a particular focus on the growing gene family of junctional adhesion molecules (JAM). Deciphering their mechanisms of interaction will also allow to unravel novel strategies for therapeutic intervention in inflammatory or atherothrombotic diseases.

Keywords

Leukocyte - transmigration - JAM - junction - endothelium
 

  • References

  • 1 Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: a multistep paradigm. Cell 1994; 76: 301-14.
    CrossrefPubMedGoogle Scholar
  • 2 Carlos TM, Harlan JM. Leukocyte-endothelial adhesion molecules. Blood 1994; 84: 2068-101.
    PubMedGoogle Scholar
  • 3 Stewart M, Thiel M, Hogg N. Leukocyte integrins. Curr Opin Cell Biol 1995; 7: 690-6.
    CrossrefPubMedGoogle Scholar
  • 4 Muller WA. Leukocyte-endothelial cell interactions in the inflammatory response. Lab Invest 2002; 82: 521-33.
    CrossrefPubMedGoogle Scholar
  • 5 Etzioni A, Doerschuk CM, Harlan JM. Of man and mouse: Leukocyte and endothelial adhesion molecule deficiencies. Blood 1999; 94: 3281-88.
    PubMedGoogle Scholar
  • 6 Anderson DC, Springer TA. Leukocyte adhesion deficiency: An inherited defect in the Mac-1, LFA-1 and p150, 95 glycoproteins. Ann Rev Med 1987; 38: 175-94.
    CrossrefPubMedGoogle Scholar
  • 7 Feng D, Nagy JA, Pyne K, Dvorak HF, Dvorak AM. Neutrophils emigrate from venules by a transendothelial cell pathway in response to fMLP. J Exp Med 1998; 187: 903-15.
    CrossrefPubMedGoogle Scholar
  • 8 Dejana E, Spagnuolo R, Bazzoni G. Interendothelial junctions and their role in the control of angiogenesis, vascular permeability and leukocyte transmigration. Thromb Haemost 2001; 86: 308-15.
    Article in Thieme ConnectPubMedGoogle Scholar
  • 9 Kemler R. From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet 1993; 9: 317-21.
    CrossrefPubMedGoogle Scholar
  • 10 Johnson-Léger C, Aurrand-Lions M, Imhof BA. The parting of the endothelium: miracle, or simply a junctional affair?. J Cell Sci 2000; 113: 921-33.
    PubMedGoogle Scholar
  • 11 Dejana E, Corada M, Lampugnani M. Endothelial cell-to-cell junctions. FASEB J 1995; 9: 910-8.
    CrossrefPubMedGoogle Scholar
  • 12 Burns AR, Walker DC, Brwon ES, Thurmon LT, Bowden RA, Keese CR, Simon SI, Entman ML, Smith CW. Neutrophil transendothelial migration is independent of tight junctions and occurs preferentially at tricellular corners. J Immunol 1997; 159: 2893-903.
    PubMedGoogle Scholar
  • 13 Muller WA, Ratti CM, McDonnell SL, Cohn ZA. A human endothelial cell-restricted, externaly disposed plasmalemmal protein enriched in intercellular junctions. J Exp Med 1989; 170: 399-414.
    CrossrefPubMedGoogle Scholar
  • 14 Newman PJ, Berndt MC, Gorski J, White II GC, Lyman S, Paddock C, Muller WA. PECAM-1 (CD31) cloning and relation to adhesion molecules of the immunoglobulin gene superfamily. Science 1990; 247: 1219-22.
    CrossrefPubMedGoogle Scholar
  • 15 Liao F, Ali J, Greene T, Muller WA. Soluble domain 1 of PECAM is sufficient to block transendothelial migration in vitro and in vivo. J Exp Med 1997; 185: 1349-57.
    CrossrefPubMedGoogle Scholar
  • 16 Bogen S, Pak J, Garifallou M, Deng X, Muller WA. Monoclonal antibody to murine PECAM-1 (CD31) blocks acute inflammation in vivo. J Exp Med 1994; 179: 1059-64.
    CrossrefPubMedGoogle Scholar
  • 17 Duncan GS, Andrew DP, Takimoto H, Kaufman SA, Yoshida H, Spellberg J, de la Pompa JL, Elia A, Wakeham A, Karan-Tamir B, Muller WA, Sendali G, Zukowski MM, Mak TW. Genetic evidence for functional redundancy of PECAM-1: CD31-deficient mice reveal PECAM-1 dependent and PECAM-1-independent functions. J Immunol 1999; 162: 3022-30.
    PubMedGoogle Scholar
  • 18 Schenkel AR, Mamdouh Z, Chen X, Liebman RM, Muller WA. CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat Immunol 2002; 3: 143-50.
    PubMedGoogle Scholar
  • 19 Hahn JH, Kim MK, Choi EY, Kim SH, Sohn HW, Ham DI, Chung DH, Kim TJ, Lee WJ, Park CK, Ree HJ, Park SH. CD99 (MIC2) regulates the LFA-1/ICAM-1-mediated adhesion of lymphocytes, and its gene encodes both positive and negative regulators of cellular adhesion. J Immunol 1997; 159: 2250-8.
    PubMedGoogle Scholar
  • 20 Gotsch U, Borges E, Bosse R, Boggemeyer E, Simon M, Mossmann H, Vestweber D. VE-cadherin antibody accelerates neutrophil recruitment in vivo. J Cell Sci 1997; 110: 583-8.
    PubMedGoogle Scholar
  • 21 Shaw SK, Bamba PS, Perkins BN, Luscinskas FW. Real-time imaging of vascular endothelial-cadherin during leukocyte transmigration across endothelium. J Immunol 2001; 167: 2323-30.
    CrossrefPubMedGoogle Scholar
  • 22 Esser S, Lampugnani MG, Corada M, Dejana E, Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci 1998; 111: 1853-65.
    PubMedGoogle Scholar
  • 23 Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E. Junctional adhesion molecule, a novel member of the immunoglobulin super-family that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 1998; 142: 117-27.
    CrossrefPubMedGoogle Scholar
  • 24 Liu Y, Nusrat A, Schnell FJ, Reaves TA, Walsh S, Pochet M, Parkos CA. Human junctional adhesion molecule regulates tight junction resealing in epithelia. J Cell Sci 2000; 113: 2363-74.
    PubMedGoogle Scholar
  • 25 Bazzoni G, Martinez-Estrada OM, Orsenigo F, Cordenonsi M, Citi S, Dejana E. Interaction of junctional adhesion molecule with the tight junction components ZO-1, cingulin, and occluding. J Biol Chem 2000; 275: 20520-6.
    CrossrefPubMedGoogle Scholar
  • 26 Ebnet K, Schulz CU, zu Brickwedel M-KM, Pendl GG, Vestweber D. Junctional adhesion molecule interacts with PDZ domain-containing proteins AF-6 and ZO-1. J Biol Chem 2000; 275: 27979-88.
    PubMedGoogle Scholar
  • 27 Ostermann G, Weber KS, Zernecke A, Schroder A, Weber C. JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in trans-endothelial migration of leukocytes. Nat Immunol 2002; 3: 151-8.
    PubMedGoogle Scholar
  • 28 Ozaki H, Ishii K, Horiuchi H, Arai H, Kawamoto T, Okawa K, Iwamatsu A, Kita T. Cutting edge: combined treatment of TNF-alpha and IFN-gamma causes redistribution of junctional adhesion molecule in human endothelial cells. J Immunol 1999; 15: 553-7.
    PubMedGoogle Scholar
  • 29 Cunningham SA, Arrate MP, Rodriguez JM, Bjercke RJ, Vanderslice P, Morris AP, Brock TA. A novel protein with homology to the junctional adhesion molecule. Characterization of leukocyte interactions. J Biol Chem 2000; 275: 34750-6.
    CrossrefPubMedGoogle Scholar
  • 30 Palmeri D, van Zante A, Huang CC, Hemmerich S, Rosen SD. Vascular endothelial junction-associated molecule, a novel member of the immunoglobulin superfamily, is local-ized to intercellular boundaries of endothelial cells. J Biol Chem 2000; 275: 19139-45.
    CrossrefPubMedGoogle Scholar
  • 31 Cunningham SA, Rodriguez JM, Arrate MP, Tran TM, Brock TA. JAM2 interacts with alpha4beta1. Facilitation by JAM3. J Biol Chem 2002; 277: 27589-92.
    CrossrefPubMedGoogle Scholar
  • 32 Santoso S, Sachs UJ, Kroll H, Linder M, Ruf A, Preissner KT, Chavakis T. The junctional adhesion molecule 3 (JAM-3) on human platelets is a counterreceptor for the leukocyte integrin Mac-1. J Exp Med 2002; 196: 679-91.
    CrossrefPubMedGoogle Scholar
  • 33 Liang TW, Chiu HH, Gurney A, Sidle A, Tumas DB, Schow P, Foster J, Klassen T, Dennis K, DeMarco RA, Pham T, Frantz G, Fong S. Vascular endothelial-junctional adhesion molecule (VE-JAM)/JAM 2 interacts with T, NK, and dendritic cells through JAM 3. J Immunol 2002; 168: 1618-26.
    CrossrefPubMedGoogle Scholar
  • 34 Bazzoni G, Martinez-Estrada OM, Mueller F, Nelboeck P, Schmid G, Bartfai T, Dejana E, Brockhaus M. Homophilic interaction of junctional adhesion molecule. J Biol Chem 2000; 275: 30970-6.
    CrossrefPubMedGoogle Scholar
  • 35 Johnson-Leger CA, Aurrand-Lions M, Beltraminelli N, Fasel N, Imhof BA. Junctional adhesion molecule-2 (JAM-2) promotes lymphocyte transendothelial migration. Blood 2002; 100: 2479-86.
    CrossrefPubMedGoogle Scholar
  • 36 Simon DI, Chen CP, Xu H, Li CQ, Dong JF, McIntire LV, Ballantyne CM, Zhang L, Furman MI, Berndt MC, Lopez JA. Platelet glycoprotein Ibα is a counterreceptor for the leukocyte integrin Mac-1 (CD11b/CD18). J Exp Med 2000; 192: 193-204.
    CrossrefPubMedGoogle Scholar
  • 37 Phillips HM, Renforth GL, Spalluto C, Hearn T, Curtis AR, Craven L, Havarani B, Clement-Jones M, English C, Stumper O, Salmon T, Hutchinson S, Jackson MS, Wilson DI. Narrowing the critical region within 11q24-qter for hypoplastic left heart and identification of a candidate gene, JAM3, expressed during cardiogenesis. Genomics 2002; 79: 475-8.
    CrossrefPubMedGoogle Scholar