Defects in CD4+ T cell LFA-1 integrin-dependent adhesion and proliferation protect Cd47-/- mice from EAE

Journal of Leukocyte Biology

Volumn 101, Issue 2, 2017, Pages 493-505

  Azcutia, Veronica ^a   Bassil, Ribal ^a   Herter, Jan M ^a   Engelbertsen, Daniel ^a   Newton, Gail ^a   Autio, Anu ^a   Mayadas, Tanya ^a   Lichtman, Andrew H ^a   Khoury, Samia J ^a,b   Parkos, Charles A ^c   Elyaman, Wassim ^a   Luscinskas, Francis W ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Autoimmune; Neuroinflammation; T lymphocytes; TCR activation

Indexed keywords

CASPASE 3; CD47 ANTIGEN; CD69 ANTIGEN; GAMMA INTERFERON; HERMES ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 9; IONOMYCIN; L SELECTIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN BCL XL; PROTEIN KINASE B; PROTEIN KINASE LCK; PROTEIN KINASE ZAP 70; SECONDARY LYMPHOID TISSUE CHEMOKINE; VASCULAR CELL ADHESION MOLECULE 1; VERY LATE ACTIVATION ANTIGEN 4; CD28 ANTIGEN; CHEMOKINE; LYMPHOCYTE ANTIGEN RECEPTOR; MONOCLONAL ANTIBODY; MYELIN OLIGODENDROCYTE GLYCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL ADHESION; CELL COUNT; CELL CYCLE PROGRESSION; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSPOT ASSAY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; HUMAN; HUMAN CELL; IMMUNIZATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE ACTIVATION; ADOPTIVE TRANSFER; ANIMAL; ANTIGEN PRESENTATION; C57BL MOUSE; CELL PROLIFERATION; DRUG EFFECTS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNOLOGY; LYMPH NODE; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN PRESENTATION; ANTIGENS, CD28; ANTIGENS, CD47; CD4-POSITIVE T-LYMPHOCYTES; CELL ADHESION; CELL PROLIFERATION; CHEMOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; HUMANS; IMMUNIZATION; INTEGRIN ALPHA4BETA1; INTERCELLULAR ADHESION MOLECULE-1; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MICE, INBRED C57BL; MYELIN-OLIGODENDROCYTE GLYCOPROTEIN; RECEPTORS, ANTIGEN, T-CELL; VASCULAR CELL ADHESION MOLECULE-1;

EID: 85011395650     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A1215-546RR     Document Type: Article

References (58)

1. Brown, E. J., Frazier, W. A. (2001) Integrin-associated protein (CD47) and its ligands. Trends Cell Biol. 11, 130–135.
2. Barclay, A. N., Van den Berg, T. K. (2014) The interaction between signal regulatory protein alpha (SIRPa) and CD47: structure, function, and therapeutic target. Annu. Rev. Immunol. 32, 25–50.
3. Oldenborg, P. A. (2013) CD47: a cell surface glycoprotein which regulates multiple functions of hematopoietic cells in health and disease. ISRN Hematol. 2013, 614–619.
4. Oldenborg, P. A., Zheleznyak, A., Fang, Y. F., Lagenaur, C. F., Gresham, H. D., Lindberg, F. P. (2000) Role of CD47 as a marker of self on red blood cells. Science 288, 2051–2054.
5. Blazar, B. R., Lindberg, F. P., Ingulli, E., Panoskaltsis-Mortari, A., Oldenborg, P. A., Iizuka, K., Yokoyama, W. M., Taylor, P. A. (2001) CD47 (integrin-associated protein) engagement of dendritic cell and macrophage counterreceptors is required to prevent the clearance of donor lymphohematopoietic cells. J. Exp. Med. 194, 541–549.
6. Majeti, R., Chao, M. P., Alizadeh, A. A., Pang, W. W., Jaiswal, S., Gibbs, K. D., Jr., van Rooijen, N., Weissman, I. L. (2009) CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138, 286–299.
7. Chao, M. P., Tang, C., Pachynski, R. K., Chin, R., Majeti, R., Weissman, I. L. (2011) Extranodal dissemination of non-Hodgkin lymphoma requires CD47 and is inhibited by anti-CD47 antibody therapy. Blood 118, 4890–4901.
8. Chao, M. P., Weissman, I. L., Majeti, R. (2012) The CD47-SIRPa pathway in cancer immune evasion and potential therapeutic implications. Curr. Opin. Immunol. 24, 225–232.
9. Ho, C. C., Guo, N., Sockolosky, J. T., Ring, A. M., Weiskopf, K., Ozkan, E., Mori, Y., Weissman, I. L., Garcia, K. C. (2015) “Velcro” engineering of high affinity CD47 ectodomain as signal regulatory protein a (SIRPa) antagonists that enhance antibody-dependent cellular phagocytosis. J. Biol. Chem. 290, 12650–12663.
10. Azcutia, V., Routledge, M., Williams, M. R., Newton, G., Frazier, W. A., Manica, A., Croce, K. J., Parkos, C. A., Schmider, A. B., Turman, M. V., Soberman, R. J., Luscinskas, F. W. (2013) CD47 plays a critical role in T-cell recruitment by regulation of LFA-1 and VLA-4 integrin adhesive functions. Mol. Biol. Cell 24, 3358–3368.
11. Azcutia, V., Stefanidakis, M., Tsuboi, N., Mayadas, T., Croce, K. J., Fukuda, D., Aikawa, M., Newton, G., Luscinskas, F. W. (2012) Endothelial CD47 promotes vascular endothelial-cadherin tyrosine phosphorylation and participates in T cell recruitment at sites of inflammation in vivo. J. Immunol. 189, 2553–2562.
12. Kuchroo, V. K., Anderson, A. C., Waldner, H., Munder, M., Bettelli, E., Nicholson, L. B. (2002) T Cell response in experimental autoimmune encephalomyelitis (EAE): role of self and cross-reactive antigens in shaping, tuning, and regulating the autopathogenic T cell repertoire. Annu. Rev. Immunol. 20, 101–123.
13. Jäger, A., Dardalhon, V., Sobel, R. A., Bettelli, E., Kuchroo, V. K. (2009) Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 183, 7169–7177.
14. Han, M. H., Lundgren, D. H., Jaiswal, S., Chao, M., Graham, K. L., Garris, C. S., Axtell, R. C., Ho, P. P., Lock, C. B., Woodard, J. I., Brownell, S. E., Zoudilova, M., Hunt, J. F., Baranzini, S. E., Butcher, E. C., Raine, C. S., Sobel, R. A., Han, D. K., Weissman, I., Steinman, L. (2012) Janus-like opposing roles of CD47 in autoimmune brain inflammation in humans and mice. J. Exp. Med. 209, 1325–1334.
15. Bouguermouh, S., Van, V. Q., Martel, J., Gautier, P., Rubio, M., Sarfati, M. (2008) CD47 expression on T cell is a self-control negative regulator of type 1 immune response. J. Immunol. 180, 8073–8082.
16. Lindberg, F. P., Bullard, D. C., Caver, T. E., Gresham, H. D., Beaudet, A. L., Brown, E. J. (1996) Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 274, 795–798.
17. Bettelli, E., Pagany, M., Weiner, H. L., Linington, C., Sobel, R. A., Kuchroo, V. K. (2003) Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197, 1073–1081.
18. Parkos, C. A., Colgan, S. P., Liang, T. W., Nusrat, A., Bacarra, A. E., Carnes, D. K., Madara, J. L. (1996) CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia. J. Cell Biol. 132, 437–450.
19. Lindberg, F. P., Gresham, H. D., Schwarz, E., Brown, E. J. (1993) Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane-spanning domains implicated in alpha v beta 3-dependent ligand binding. J. Cell Biol. 123, 485–496.
20. Rao, R. M., Betz, T. V., Lamont, D. J., Kim, M. B., Shaw, S. K., Froio, R. M., Baleux, F., Arenzana-Seisdedos, F., Alon, R., Luscinskas, F. W. (2004) Elastase release by transmigrating neutrophils deactivates endothelialbound SDF-1alpha and attenuates subsequent T lymphocyte transendothelial migration. J. Exp. Med. 200, 713–724.
21. Alcaide, P., Maganto-Garcia, E., Newton, G., Travers, R., Croce, K. J., Bu, D. X., Luscinskas, F. W., Lichtman, A. H. (2012) Difference in Th1 and Th17 lymphocyte adhesion to endothelium. J. Immunol. 188, 1421–1430.
22. Elyaman, W., Bradshaw, E. M., Wang, Y., Oukka, M., Kivisäkk, P., Chiba, S., Yagita, H., Khoury, S. J. (2007) JAGGED1 and delta1 differentially regulate the outcome of experimental autoimmune encephalomyelitis. J. Immunol. 179, 5990–5998.
23. Mueller, K. L., Thomas, M. S., Burbach, B. J., Peterson, E. J., Shimizu, Y. (2007) Adhesion and degranulation-promoting adapter protein (ADAP) positively regulates T cell sensitivity to antigen and T cell survival. J. Immunol. 179, 3559–3569.
24. Jiang, P., Lagenaur, C. F., Narayanan, V. (1999) Integrin-associated protein is a ligand for the P84 neural adhesion molecule. J. Biol. Chem. 274, 559–562.
25. Martinelli, R., Newton, G., Carman, C. V., Greenwood, J., Luscinskas, F. W. (2013) Novel role of CD47 in rat microvascular endothelium: signaling and regulation of T-cell transendothelial migration. Arterioscler. Thromb. Vasc. Biol. 33, 2566–2576.
26. Stefanidakis, M., Newton, G., Lee, W. Y., Parkos, C. A., Luscinskas, F. W. (2008) Endothelial CD47 interaction with SIRPgamma is required for human T-cell transendothelial migration under shear flow conditions in vitro. Blood 112, 1280–1289.
27. Legrand, N., Huntington, N. D., Nagasawa, M., Bakker, A. Q., Schotte, R., Strick-Marchand, H., de Geus, S. J., Pouw, S. M., Böhne, M., Voordouw, A., Weijer, K., Di Santo, J. P., Spits, H. (2011) Functional CD47/signal regulatory protein alpha (SIRP (alpha)) interaction is required for optimal human T-and natural killer-(NK) cell homeostasis in vivo. Proc. Natl. Acad. Sci. USA 108, 13224–13229.
28. Dunkle, A., He, Y. W. (2011) Apoptosis and autophagy in the regulation of T lymphocyte function. Immunol. Res. 49, 70–86.
29. Boise, L. H., Minn, A. J., Noel, P. J., June, C. H., Accavitti, M. A., Lindsten, T., Thompson, C. B. (1995) CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-xL. Immunity 3, 87–98.
30. Kerstan, A., Hünig, T. (2004) Cutting edge: distinct TCR-and CD28-derived signals regulate CD95L, Bcl-xL, and the survival of primary T cells. J. Immunol. 172, 1341–1345.
31. Khoshnan, A., Tindell, C., Laux, I., Bae, D., Bennett, B., Nel, A. E. (2000) The NF-kappa B cascade is important in Bcl-xL expression and for the anti-apoptotic effects of the CD28 receptor in primary human CD4+ lymphocytes. J. Immunol. 165, 1743–1754.
32. Rothlein, R., Springer, T. A. (1986) The requirement for lymphocyte function-associated antigen 1 in homotypic leukocyte adhesion stimulated by phorbol ester. J. Exp. Med. 163, 1132–1149.
33. Schwartz, D., Wong, R. C., Chatila, T., Arnaout, A., Miller, R., Geha, R. (1989) Proliferation of highly purified T cells in response to signaling via surface receptors requires cell-cell contact. J. Clin. Immunol. 9, 151–158.
34. Hommel, M., Kyewski, B. (2003) Dynamic changes during the immune response in T cell-antigen-presenting cell clusters isolated from lymph nodes. J. Exp. Med. 197, 269–280.
35. Kandula, S., Abraham, C. (2004) LFA-1 on CD4+ T cells is required for optimal antigen-dependent activation in vivo. J. Immunol. 173, 4443–4451.
36. Zumwalde, N. A., Domae, E., Mescher, M. F., Shimizu, Y. (2013) ICAM-1-dependent homotypic aggregates regulate CD8 T cell effector function and differentiation during T cell activation. J. Immunol. 191, 3681–3693.
37. Reinhold, M. I., Lindberg, F. P., Kersh, G. J., Allen, P. M., Brown, E. J. (1997) Costimulation of T cell activation by integrin-associated protein (CD47) is an adhesion-dependent, CD28-independent signaling pathway. J. Exp. Med. 185, 1–11.
38. Stupack, D. G., Cheresh, D. A. (2002) Get a ligand, get a life: integrins, signaling and cell survival. J. Cell Sci. 115, 3729–3738.
39. Van, V. Q., Lesage, S., Bouguermouh, S., Gautier, P., Rubio, M., Levesque, M., Nguyen, S., Galibert, L., Sarfati, M. (2006) Expression of the self-marker CD47 on dendritic cells governs their trafficking to secondary lymphoid organs. EMBO J. 25, 5560–5568.
40. Hagnerud, S., Manna, P. P., Cella, M., Stenberg, A., Frazier, W. A., Colonna, M., Oldenborg, P. A. (2006) Deficit of CD47 results in a defect of marginal zone dendritic cells, blunted immune response to particulate antigen and impairment of skin dendritic cell migration. J. Immunol. 176, 5772–5778.
41. De Vries, H. E., Hendriks, J. J., Honing, H., De Lavalette, C. R., van der Pol, S. M., Hooijberg, E., Dijkstra, C. D., van den Berg, T. K. (2002) Signal-regulatory protein alpha-CD47 interactions are required for the transmigration of monocytes across cerebral endothelium. J. Immunol. 168, 5832–5839.
42. Lee, W. Y., Weber, D. A., Laur, O., Severson, E. A., McCall, I., Jen, R. P., Chin, A. C., Wu, T., Gernert, K. M., Parkos, C. A. (2007) Novel structural determinants on SIRP alpha that mediate binding to CD47. J. Immunol. 179, 7741–7750.
43. Hatherley, D., Graham, S. C., Turner, J., Harlos, K., Stuart, D. I., Barclay, A. N. (2008) Paired receptor specificity explained by structures of signal regulatory proteins alone and complexed with CD47. Mol. Cell 31, 266–277.
44. Liu, Y., Carlsson, R., Comabella, M., Wang, J., Kosicki, M., Carrion, B., Hasan, M., Wu, X., Montalban, X., Dziegiel, M. H., Sellebjerg, F., Sørensen, P. S., Helin, K., Issazadeh-Navikas, S. (2014) FoxA1 directs the lineage and immunosuppressive properties of a novel regulatory T cell population in EAE and MS. Nat. Med. 20, 272–282.
45. Wohler, J. E., Smith, S. S., Zinn, K. R., Bullard, D. C., Barnum, S. R. (2009) Gammadelta T cells in EAE: early trafficking events and cytokine requirements. Eur. J. Immunol. 39, 1516–1526.
46. Bassil, R., Zhu, B., Lahoud, Y., Riella, L. V., Yagita, H., Elyaman, W., Khoury, S. J. (2011) Notch ligand delta-like 4 blockade alleviates experimental autoimmune encephalomyelitis by promoting regulatory T cell development. J. Immunol. 187, 2322–2328.
47. McGeachy, M. J., Stephens, L. A., Anderton, S. M. (2005) Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+CD25+ regulatory cells within the central nervous system. J. Immunol. 175, 3025–3032.
48. O’Connor, R. A., Malpass, K. H., Anderton, S. M. (2007) The inflamed central nervous system drives the activation and rapid proliferation of Foxp3+ regulatory T cells. J. Immunol. 179, 958–966.
49. Liu, X., Pu, Y., Cron, K., Deng, L., Kline, J., Frazier, W. A., Xu, H., Peng, H., Fu, Y. X., Xu, M. M. (2015) CD47 blockade triggers T cell-mediated destruction of immunogenic tumors. Nat. Med. 21, 1209–1215.
50. Vonderheide, R. H. (2015) CD47 blockade as another immune checkpoint therapy for cancer. Nat. Med. 21, 1122–1123.
51. Tomizawa, T., Kaneko, Y., Kaneko, Y., Saito, Y., Ohnishi, H., Okajo, J., Okuzawa, C., Ishikawa-Sekigami, T., Murata, Y., Okazawa, H., Okamoto, K., Nojima, Y., Matozaki, T. (2007) Resistance to experimental autoimmune encephalomyelitis and impaired T cell priming by dendritic cells in Src homology 2 domain-containing protein tyrosine phosphatase substrate-1 mutant mice. J. Immunol. 179, 869–877.
52. Verdrengh, M., Lindberg, F. P., Ryden, C., Tarkowski, A. (1999) Integrinassociated protein (IAP)-deficient mice are less susceptible to developing Staphylococcus aureus-induced arthritis. Microbes Infect. 1, 745–751.
53. Vallejo, A. N., Yang, H., Klimiuk, P. A., Weyand, C. M., Goronzy, J. J. (2003) Synoviocyte-mediated expansion of inflammatory T cells in rheumatoid synovitis is dependent on CD47-thrombospondin 1 interaction. J. Immunol. 171, 1732–1740.
54. Yang, K., Vega, J. L., Hadzipasic, M., Schatzmann Peron, J. P., Zhu, B., Carrier, Y., Masli, S., Rizzo, L. V., Weiner, H. L. (2009) Deficiency of thrombospondin-1 reduces Th17 differentiation and attenuates experimental autoimmune encephalomyelitis. J. Autoimmun. 32, 94–103.
55. Racke, M. K., Scott, D. E., Quigley, L., Gray, G. S., Abe, R., June, C. H., Perrin, P. J. (1995) Distinct roles for B7-1 (CD-80) and B7-2 (CD-86) in the initiation of experimental allergic encephalomyelitis. J. Clin. Invest. 96, 2195–2203.
56. Theien, B. E., Vanderlugt, C. L., Eagar, T. N., Nickerson-Nutter, C., Nazareno, R., Kuchroo, V. K., Miller, S. D. (2001) Discordant effects of anti-VLA-4 treatment before and after onset of relapsing experimental autoimmune encephalomyelitis. J. Clin. Invest. 107, 995–1006.
57. Hünig, T. (2012) The storm has cleared: lessons from the CD28 superagonist TGN1412 trial. Nat. Rev. Immunol. 12, 317–318.
58. Suntharalingam, G., Perry, M. R., Ward, S., Brett, S. J., Castello-Cortes, A., Brunner, M. D., Panoskaltsis, N. (2006) Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N. Engl. J. Med. 355, 1018–1028