CD31 exhibits multiple roles in regulating T lymphocyte trafficking in vivo

Journal of Immunology

Volumn 189, Issue 8, 2012, Pages 4104-4111

  Ma, Liang ^a   Cheung, Kenneth C P ^b   Kishore, Madhav ^b   Nourshargh, Sussan ^b   Mauro, Claudio ^b   Marelli Berg, Federica M ^b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN RECOGNITION; ARTICLE; CELL INTERACTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VIVO STUDY; INFLAMMATION; LYMPHOCYTE HOMING; LYMPHOCYTE MIGRATION; LYMPHOCYTIC INFILTRATION; LYMPHOID TISSUE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD31; CELL COMMUNICATION; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FEMALE; LYMPHOID TISSUE; MALE; MICE; ORGAN CULTURE TECHNIQUES; T-LYMPHOCYTES; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84867284723     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201739     Document Type: Article

References (49)

1. Muller, W. A. 2003. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24: 327-334.
2. Piali, L., P. Hammel, C. Uherek, F. Bachmann, R. H. Gisler, D. Dunon, and B. A. Imhof. 1995. CD31/PECAM-1 is a ligand for alpha v beta 3 integrin involved in adhesion of leukocytes to endothelium. J. Cell Biol. 130: 451-460.
3. Tanaka, Y., S. M. Albelda, K. J. Horgan, G. A. van Seventer, Y. Shimizu, W. Newman, J. Hallam, P. J. Newman, C. A. Buck, and S. Shaw. 1992. CD31 expressed on distinctive T cell subsets is a preferential amplifier of beta 1 integrin-mediated adhesion. J. Exp. Med. 176: 245-253.
4. Miller, M., K. L. Sung, W. A. Muller, J. Y. Cho, M. Roman, D. Castaneda, J. Nayar, T. Condon, J. Kim, P. Sriramarao, and D. H. Broide. 2001. Eosinophil tissue recruitment to sites of allergic inflammation in the lung is platelet endothelial cell adhesion molecule independent. J. Immunol. 167: 2292-2297. (Pubitemid 32747542)
5. Bird, I. N., J. H. Spragg, A. Ager, and N. Matthews. 1993. Studies of lymphocyte transendothelial migration: analysis of migrated cell phenotypes with regard to CD31 (PECAM-1), CD45RA and CD45RO. Immunology 80: 553-560. (Pubitemid 24010114)
6. Manes, T. D., and J. S. Pober. 2011. Identification of endothelial cell junctional proteins and lymphocyte receptors involved in transendothelial migration of human effector memory CD4+ T cells. J. Immunol. 186: 1763-1768.
7. Manes, T. D., S. Hoer, W. A. Muller, P. J. Lehner, and J. S. Pober. 2010. Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins block distinct steps in transendothelial migration of effector memory CD4+ T cells by targeting different endothelial proteins. J. Immunol. 184: 5186-5192.
8. Tada, Y., S. Koarada, F. Morito, O. Ushiyama, Y. Haruta, F. Kanegae, A. Ohta, A. Ho, T. W. Mak, and K. Nagasawa. 2003. Acceleration of the onset of collagen-induced arthritis by a deficiency of platelet endothelial cell adhesion molecule 1. Arthritis Rheum. 48: 3280-3290. (Pubitemid 37409343)
9. Wong, M. X., J. D. Hayball, P. M. Hogarth, and D. E. Jackson. 2005. The inhibitory co-receptor, PECAM-1 provides a protective effect in suppression of collagen-induced arthritis. J. Clin. Immunol. 25: 19-28.
10. Graesser, D., A. Solowiej, M. Bruckner, E. Osterweil, A. Juedes, S. Davis, N. H. Ruddle, B. Engelhardt, and J. A. Madri. 2002. Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J. Clin. Invest. 109: 383-392. (Pubitemid 34141812)
11. Behar, E., N. J. Chao, D. D. Hiraki, S. Krishnaswamy, B. W. Brown, J. L. Zehnder, and F. C. Grumet. 1996. Polymorphism of adhesion molecule CD31 and its role in acute graft-versus-host disease. N. Engl. J. Med. 334: 286-291.
12. Balduini, C. L., F. Frassoni, P. Noris, C. Klersy, A. M. Iannone, A. Bacigalupo, G. Giorgiani, M. Di Pumpo, and F. Locatelli. 2001. Donor-recipient incompatibility at CD31-codon 563 is a major risk factor for acute graft-versus-host disease after allogeneic bone marrow transplantation from a human leucocyte antigen-matched donor. Br. J. Haematol. 114: 951-953. (Pubitemid 32953760)
13. Cavanagh, G., C. E. Chapman, V. Carter, A. M. Dickinson, and P. G. Middleton. 2005. Donor CD31 genotype impacts on transplant complications after human leukocyte antigen-matched sibling allogeneic bone marrow transplantation. Transplantation 79: 602-605. (Pubitemid 40365890)
14. El-Chennawi, F. A., H. A. Kamel, Y. M. Mosaad, S. M. El-Sherbini, and N. A. El-Billey. 2006. Impact of CD31 mismatches on the outcome of hematopoeitic stem cell transplant of HLA-identical sibling. Hematology 11: 227-234. (Pubitemid 44963698)
15. Goodman, R. S., J. Ewing, P. C. Evans, J. Craig, K. Poulton, P. A. Dyer, R. E. Marcus, and C. J. Taylor. 2005. Donor CD31 genotype and its association with acute graft-versus-host disease in HLA identical sibling stem cell transplantation. Bone Marrow Transplant. 36: 151-156. (Pubitemid 41030631)
16. Elrayess, M. A., K. E. Webb, G. J. Bellingan, R. A. Whittall, J. Kabir, E. Hawe, M. Syvänne, M. R. Taskinen, M. H. Frick, M. S. Nieminen, et al. 2004. R643G polymorphism in PECAM-1 influences transendothelial migration of monocytes and is associated with progression of CHD and CHD events. Atherosclerosis 177: 127-135. (Pubitemid 39361147)
17. Auer, J., T. Weber, R. Berent, E. Lassnig, G. Lamm, and B. Eber. 2003. Genetic polymorphisms in cytokine and adhesion molecule genes in coronary artery disease. Am. J. Pharmacogenomics 3: 317-328. (Pubitemid 37409105)
18. Duncan, G. S., D. P. Andrew, H. Takimoto, S. A. Kaufman, H. Yoshida, J. Spellberg, J. L. de la Pompa, A. Elia, A. Wakeham, B. Karan-Tamir, et al. 1999. Genetic evidence for functional redundancy of Platelet/Endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J. Immunol. 162: 3022-3030. (Pubitemid 29309332)
19. Marelli-Berg, F. M., M. J. James, J. Dangerfield, J. Dyson, M. Millrain, D. Scott, E. Simpson, S. Nourshargh, and R. I. Lechler. 2004. Cognate recognition of the endothelium induces HY-specific CD8+ T-lymphocyte transendothelial migration (diapedesis) in vivo. Blood 103: 3111-3116. (Pubitemid 38451688)
20. Jarmin, S. J., R. David, L. Ma, J.-G. Chai, H. Dewchand, A. Takesono, A. J. Ridley, K. Okkenhaug, and F. M. Marelli-Berg. 2008. Targeting T cell receptor-induced phosphoinositide-3-kinase p110delta activity prevents T cell localization to antigenic tissue. J. Clin. Invest. 118: 1154-1164. (Pubitemid 351364622)
21. Marelli-Berg, F. M., E. Peek, E. A. Lidington, H. J. Stauss, and R. I. Lechler. 2000. Isolation of endothelial cells from murine tissue. J. Immunol. Methods 244: 205-215.
22. Acharya, P. S., S. Majumdar, M. Jacob, J. Hayden, P. Mrass, W. Weninger, R. K. Assoian, and E. Puré. 2008. Fibroblast migration is mediated by CD44-dependent TGF beta activation. J. Cell Sci. 121: 1393-1402. (Pubitemid 351936304)
23. Butcher, E. C., and L. J. Picker. 1996. Lymphocyte homing and homeostasis. Science 272: 60-66. (Pubitemid 26110755)
24. Pfeiffer, F., V. Kumar, S. Butz, D. Vestweber, B. A. Imhof, J. V. Stein, and B. Engelhardt. 2008. Distinct molecular composition of blood and lymphatic vascular endothelial cell junctions establishes specific functional barriers within the peripheral lymph node. Eur. J. Immunol. 38: 2142-2155.
25. Pusztaszeri, M. P., W. Seelentag, and F. T. Bosman. 2006. Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues. J. Histochem. Cytochem. 54: 385-395.
26. Ma, L., C. Mauro, G. H. Cornish, J. G. Chai, D. Coe, H. Fu, D. Patton, K. Okkenhaug, G. Franzoso, J. Dyson, et al. 2010. Ig gene-like molecule CD31 plays a nonredundant role in the regulation of T-cell immunity and tolerance. Proc. Natl. Acad. Sci. USA 107: 19461-19466.
27. Thompson, R. D., K. E. Noble, K. Y. Larbi, A. Dewar, G. S. Duncan, T. W. Mak, and S. Nourshargh. 2001. Platelet-endothelial cell adhesion molecule-1 (PECAM-1)-deficient mice demonstrate a transient and cytokine-specific role for PECAM-1 in leukocyte migration through the perivascular basement membrane. Blood 97: 1854-1860. (Pubitemid 32217254)
28. Mehta, D., and A. B. Malik. 2006. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86: 279-367.
29. Dangerfield, J. P., K. Y. Larbi, M.-T. Huang, A. Dewar, and S. Nourshargh. 2002. PECAM-1 (CD31) homophilic interaction up-regulates alpha6beta1 on transmigrated neutrophils in vivo and plays a functional role in the ability of alpha6 integrins to mediate leukocyte migration through the perivascular basement membrane. J. Exp. Med. 196: 1201-1211. (Pubitemid 35304186)
30. Nourshargh, S., and F. M. Marelli-Berg. 2005. Transmigration through venular walls: a key regulator of leukocyte phenotype and function. Trends Immunol. 26: 157-165. (Pubitemid 40312523)
31. Bogen, S., J. Pak, M. Garifallou, X. Deng, and W. A. Muller. 1994. Monoclonal antibody to murine PECAM-1 (CD31) blocks acute inflammation in vivo. J. Exp. Med. 179: 1059-1064. (Pubitemid 24065668)
32. Liao, F., J. Ali, T. Greene, and W. A. Muller. 1997. Soluble domain 1 of platelet-endothelial cell adhesion molecule (PECAM) is sufficient to block transendothelial migration in vitro and in vivo. J. Exp. Med. 185: 1349-1357. (Pubitemid 27172915)
33. Reinke, E. K., J. Lee, A. Zozulya, J. Karman, W. A. Muller, M. Sandor, and Z. Fabry. 2007. Short-term sPECAM-Fc treatment ameliorates EAE while chronic use hastens onset of symptoms. J. Neuroimmunol. 186: 86-93. (Pubitemid 46770866)
34. Ishikaw, J., Y. Okada, I. N. Bird, B. Jasani, J. H. Spragg, and T. Yamada. 2002. Use of anti-platelet-endothelial cell adhesion molecule-1 antibody in the control of disease progression in established collagen-induced arthritis in DBA/1J mice. Jpn. J. Pharmacol. 88: 332-340. (Pubitemid 34302985)
35. Qing, Z., M. Sandor, Z. Radvany, D. Sewell, A. Falus, D. Potthoff, W. A. Muller, and Z. Fabry. 2001. Inhibition of antigen-specific T cell trafficking into the central nervous system via blocking PECAM1/CD31 molecule. J. Neuropathol. Exp. Neurol. 60: 798-807. (Pubitemid 32678260)
36. Carrithers, M., S. Tandon, S. Canosa, M. Michaud, D. Graesser, and J. A. Madri. 2005. Enhanced susceptibility to endotoxic shock and impaired STAT3 signaling in CD31-deficient mice. Am. J. Pathol. 166: 185-196. (Pubitemid 40051671)
37. Jindra, P. T., Y. P. Jin, R. Jacamo, E. Rozengurt, and E. F. Reed. 2008. MHC class I and integrin ligation induce ERK activation via an mTORC2-dependent pathway. Biochem. Biophys. Res. Commun. 369: 781-787.
38. Jindra, P. T., Y. P. Jin, E. Rozengurt, and E. F. Reed. 2008. HLA class I antibody-mediated endothelial cell proliferation via the mTOR pathway. J. Immunol. 180: 2357-2366.
39. Etienne, S., S. Bourdoulous, A. D. Strosberg, and P. O. Couraud. 1999. MHC class II engagement in brain endothelial cells induces protein kinase A-dependent IL-6 secretion and phosphorylation of cAMP response element-binding protein. J. Immunol. 163: 3636-3641. (Pubitemid 29450884)
40. Adamson, P., S. Etienne, P. O. Couraud, V. Calder, and J. Greenwood. 1999. Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a rho-dependent pathway. J. Immunol. 162: 2964-2973. (Pubitemid 29309325)
41. Boulday, G., J. Fitau, S. Coupel, J. P. Soulillou, and B. Charreau. 2004. Exogenous tissue inhibitor of metalloproteinase-1 promotes endothelial cell survival through activation of the phosphatidylinositol 3-kinase/Akt pathway. Ann. N. Y. Acad. Sci. 1030: 28-36. (Pubitemid 40378893)
42. Biswas, P., S. Canosa, D. Schoenfeld, J. Schoenfeld, P. Li, L. C. Cheas, J. Zhang, A. Cordova, B. Sumpio, and J. A. Madri. 2006. PECAM-1 affects GSK-3beta-mediated beta-catenin phosphorylation and degradation. Am. J. Pathol. 169: 314-324.
43. Orlova, V. V., M. Economopoulou, F. Lupu, S. Santoso, and T. Chavakis. 2006. Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherin-mediated cell-cell contacts. J. Exp. Med. 203: 2703-2714. (Pubitemid 44833346)
44. Marelli-Berg, F. M., L. Frasca, L. Weng, G. Lombardi, and R. I. Lechler. 1999. Antigen recognition influences transendothelial migration of CD4+ T cells. J. Immunol. 162: 696-703. (Pubitemid 29035389)
45. Greening, J. E., T. I. Tree, K. T. Kotowicz, A. G. van Halteren, B. O. Roep, N. J. Klein, and M. Peakman. 2003. Processing and presentation of the islet autoantigen GAD by vascular endothelial cells promotes transmigration of autoreactive T-cells. Diabetes 52: 717-725. (Pubitemid 36323579)
46. Manes, T. D., and J. S. Pober. 2008. Antigen presentation by human microvascular endothelial cells triggers ICAM-1-dependent transendothelial protrusion by, and fractalkine-dependent transendothelial migration of, effector memory CD4+ T cells. J. Immunol. 180: 8386-8392.
47. Savinov, A. Y., F. S. Wong, A. C. Stonebraker, and A. V. Chervonsky. 2003. Presentation of antigen by endothelial cells and chemoattraction are required for homing of insulin-specific CD8+ T cells. J. Exp. Med. 197: 643-656. (Pubitemid 36314659)
48. Sobel, R.A., B.W. Blanchette, A.K. Bhan, and R.B. Colvin. 1984. The immunopathology of experimental allergic encephalomyelitis. II. Endothelial cell Ia increases prior to inflammatory cell infiltration. J. Immunol. 132: 2402-2407. (Pubitemid 14137630)
49. David, R., L. Ma, A. Ivetic, A. Takesono, A. J. Ridley, J. G. Chai, V. L. Tybulewicz, and F. M. Marelli-Berg. 2009. T-cell receptor- and CD28-induced Vav1 activity is required for the accumulation of primed T cells into antigenic tissue. Blood 113: 3696-3705.