111
Views
62
CrossRef citations to date
0
Altmetric
Article

The Leukocyte Activation Receptor CD69 Controls T Cell Differentiation through Its Interaction with Galectin-1

, , , , , , , , , , & show all
Pages 2479-2487 | Received 13 Mar 2014, Accepted 14 Apr 2014, Published online: 20 Mar 2023

REFERENCES

  • Lopez-Cabrera M, Santis AG, Fernandez-Ruiz E, Blacher R, Esch F, Sanchez-Mateos P, Sanchez-Madrid F. 1993. Molecular cloning, expression, and chromosomal localization of the human earliest lymphocyte activation antigen AIM/CD69, a new member of the C-type animal lectin superfamily of signal-transmitting receptors. J. Exp. Med. 178:537–547. http://dx.doi.org/10.1084/jem.178.2.537.
  • Radulovic K, Manta C, Rossini V, Holzmann K, Kestler HA, Wegenka UM, Nakayama T, Niess JH. 2012. CD69 regulates type I IFN-induced tolerogenic signals to mucosal CD4 T cells that attenuate their colitogenic potential. J. Immunol. 188:2001–2013. http://dx.doi.org/10.4049/jimmunol.1100765.
  • Sancho D, Gomez M, Viedma F, Esplugues E, Gordon-Alonso M, Garcia-Lopez MA, de la Fuente H, Martinez AC, Lauzurica P, Sanchez-Madrid F. 2003. CD69 downregulates autoimmune reactivity through active transforming growth factor-beta production in collagen-induced arthritis. J. Clin. Invest. 112:872–882. http://dx.doi.org/10.1172/JCI19112.
  • Cruz-Adalia A, Jimenez-Borreguero LJ, Ramirez-Huesca M, Chico-Calero I, Barreiro O, Lopez-Conesa E, Fresno M, Sanchez-Madrid F, Martin P. 2010. CD69 limits the severity of cardiomyopathy after autoimmune myocarditis. Circulation 122:1396–1404. http://dx.doi.org/10.1161/CIRCULATIONAHA.110.952820.
  • Martin P, Gomez M, Lamana A, Cruz-Adalia A, Ramirez-Huesca M, Ursa MA, Yanez-Mo M, Sanchez-Madrid F. 2010. CD69 association with Jak3/Stat5 proteins regulates Th17 cell differentiation. Mol. Cell. Biol. 30:4877–4889. http://dx.doi.org/10.1128/MCB.00456-10.
  • Shiow LR, Rosen DB, Brdickova N, Xu Y, An J, Lanier LL, Cyster JG, Matloubian M. 2006. CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440:540–544. http://dx.doi.org/10.1038/nature04606.
  • Lamana A, Martin P, de la Fuente H, Martinez-Munoz L, Cruz-Adalia A, Ramirez-Huesca M, Escribano C, Gollmer K, Mellado M, Stein JV, Rodriguez-Fernandez JL, Sanchez-Madrid F, del Hoyo GM. 2011. CD69 modulates sphingosine-1-phosphate-induced migration of skin dendritic cells. J. Investig. Dermatol. 131:1503–1512. http://dx.doi.org/10.1038/jid.2011.54.
  • Bankovich AJ, Shiow LR, Cyster JG. 2010. CD69 suppresses sphingosine 1-phosophate receptor-1 (S1P1) function through interaction with membrane helix 4. J. Biol. Chem. 285:22328–22337. http://dx.doi.org/10.1074/jbc.M110.123299.
  • Barondes SH, Castronovo V, Cooper DN, Cummings RD, Drickamer K, Feizi T, Gitt MA, Hirabayashi J, Hughes C, Kasai K, Leffler H, Liu FT, Lotan R, Mercurio AM, Monsigny M, Pillai S, Poirer F, Raz A, Rigby PWJ, Rini JM, Wang JL. 1994. Galectins: a family of animal beta-galactoside-binding lectins. Cell 76:597–598. http://dx.doi.org/10.1016/0092-8674(94)90498-7.
  • Rabinovich GA, Toscano MA, Jackson SS, Vasta GR. 2007. Functions of cell surface galectin-glycoprotein lattices. Curr. Opin. Struct. Biol. 17:513–520. http://dx.doi.org/10.1016/j.sbi.2007.09.002.
  • Ilarregui JM, Croci DO, Bianco GA, Toscano MA, Salatino M, Vermeulen ME, Geffner JR, Rabinovich GA. 2009. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat. Immunol. 10:981–991. http://dx.doi.org/10.1038/ni.1772.
  • Rabinovich GA, Daly G, Dreja H, Tailor H, Riera CM, Hirabayashi J, Chernajovsky Y. 1999. Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis. J. Exp. Med. 190:385–398. http://dx.doi.org/10.1084/jem.190.3.385.
  • Santucci L, Fiorucci S, Rubinstein N, Mencarelli A, Palazzetti B, Federici B, Rabinovich GA, Morelli A. 2003. Galectin-1 suppresses experimental colitis in mice. Gastroenterology 124:1381–1394. http://dx.doi.org/10.1016/S0016-5085(03)00267-1.
  • Baum LG, Blackall DP, Arias-Magallano S, Nanigian D, Uh SY, Browne JM, Hoffmann D, Emmanouilides CE, Territo MC, Baldwin GC. 2003. Amelioration of graft versus host disease by galectin-1. Clin. Immunol. 109:295–307. http://dx.doi.org/10.1016/j.clim.2003.08.003.
  • Toscano MA, Bianco GA, Ilarregui JM, Croci DO, Correale J, Hernandez JD, Zwirner NW, Poirier F, Riley EM, Baum LG, Rabinovich GA. 2007. Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat. Immunol. 8:825–834. http://dx.doi.org/10.1038/ni1482.
  • Blois SM, Ilarregui JM, Tometten M, Garcia M, Orsal AS, Cordo-Russo R, Toscano MA, Bianco GA, Kobelt P, Handjiski B, Tirado I, Markert UR, Klapp BF, Poirier F, Szekeres-Bartho J, Rabinovich GA, Arck PC. 2007. A pivotal role for galectin-1 in fetomaternal tolerance. Nat. Med. 13:1450–1457. http://dx.doi.org/10.1038/nm1680.
  • Sallusto F, Lanzavecchia A. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179:1109–1118. http://dx.doi.org/10.1084/jem.179.4.1109.
  • Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N, Schuler G. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods 223:77–92. http://dx.doi.org/10.1016/S0022-1759(98)00204-X.
  • Cebrian M, Yague E, Rincon M, Lopez-Botet M, de Landazuri MO, Sanchez-Madrid F. 1988. Triggering of T cell proliferation through AIM, an activation inducer molecule expressed on activated human lymphocytes. J. Exp. Med. 168:1621–1637. http://dx.doi.org/10.1084/jem.168.5.1621.
  • Sanchez-Mateos P, Sanchez-Madrid F. 1991. Structure-function relationship and immunochemical mapping of external and intracellular antigenic sites on the lymphocyte activation inducer molecule, AIM/CD69. Eur. J. Immunol. 21:2317–2325. http://dx.doi.org/10.1002/eji.1830211005.
  • Rossi NE, Reine J, Pineda-Lezamit M, Pulgar M, Meza NW, Swamy M, Risueno R, Schamel WW, Bonay P, Fernandez-Malave E, Regueiro JR. 2008. Differential antibody binding to the surface alphabetaTCR.CD3 complex of CD4+ and CD8+ T lymphocytes is conserved in mammals and associated with differential glycosylation. Int. Immunol. 20:1247–1258. http://dx.doi.org/10.1093/intimm/dxn081.
  • Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. 2007. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8:942–949. http://dx.doi.org/10.1038/ni1496.
  • Bonzon-Kulichenko E, Perez-Hernandez D, Nunez E, Martinez-Acedo P, Navarro P, Trevisan-Herraz M, del Carmen Ramos M, Sierra S, Martinez-Martinez S, Ruiz-Meana M, Miro-Casas E, Garcia-Dorado D, Redondo JM, Burgos JS, Vazquez J. 2011. A robust method for quantitative high-throughput analysis of proteomes by 18O labeling. Mol. Cell. Proteomics 10:M110.003335. http://dx.doi.org/10.1074/mcp.M110.003335.
  • Jorge I, Casas EM, Villar M, Ortega-Perez I, Lopez-Ferrer D, Martinez-Ruiz A, Carrera M, Marina A, Martinez P, Serrano H, Canas B, Were F, Gallardo JM, Lamas S, Redondo JM, Garcia-Dorado D, Vazquez J. 2007. High-sensitivity analysis of specific peptides in complex samples by selected MS/MS ion monitoring and linear ion trap mass spectrometry: application to biological studies. J. Mass Spectrom. 42:1391–1403. http://dx.doi.org/10.1002/jms.1314.
  • Cedeno-Laurent F, Barthel SR, Opperman MJ, Lee DM, Clark RA, Dimitroff CJ. 2010. Development of a nascent galectin-1 chimeric molecule for studying the role of leukocyte galectin-1 ligands and immune disease modulation. J. Immunol. 185:4659–4672. http://dx.doi.org/10.4049/jimmunol.1000715.
  • Iizuka K, Naidenko OV, Plougastel BF, Fremont DH, Yokoyama WM. 2003. Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat. Immunol. 4:801–807. http://dx.doi.org/10.1038/ni954.
  • Carlyle JR, Jamieson AM, Gasser S, Clingan CS, Arase H, Raulet DH. 2004. Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc. Natl. Acad. Sci. U. S. A. 101:3527–3532. http://dx.doi.org/10.1073/pnas.0308304101.
  • Rosen DB, Bettadapura J, Alsharifi M, Mathew PA, Warren HS, Lanier LL. 2005. Cutting edge: lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor. J. Immunol. 175:7796–7799. http://dx.doi.org/10.4049/jimmunol.175.12.7796.
  • Welte S, Kuttruff S, Waldhauer I, Steinle A. 2006. Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nat. Immunol. 7:1334–1342. http://dx.doi.org/10.1038/ni1402.
  • Plougastel BF, Yokoyama WM. 2006. Extending missing-self? Functional interactions between lectin-like NKrp1 receptors on NK cells with lectin-like ligands. Curr. Top. Microbiol. Immunol. 298:77–89. http://dx.doi.org/10.1007/3-540-27743-9_4.
  • Bezouska K, Nepovim A, Horvath O, Pospisil M, Hamann J, Feizi T. 1995. CD 69 antigen of human lymphocytes is a calcium-dependent carbohydrate-binding protein. Biochem. Biophys. Res. Commun. 208:68–74. http://dx.doi.org/10.1006/bbrc.1995.1306.
  • Bajorath J, Aruffo A. 1994. Molecular model of the extracellular lectin-like domain in CD69. J. Biol. Chem. 269:32457–32463.
  • Lanier LL, Buck DW, Rhodes L, Ding A, Evans E, Barney C, Phillips JH. 1988. Interleukin 2 activation of natural killer cells rapidly induces the expression and phosphorylation of the Leu-23 activation antigen. J. Exp. Med. 167:1572–1585. http://dx.doi.org/10.1084/jem.167.5.1572.
  • Pace KE, Hahn HP, Pang M, Nguyen JT, Baum LG. 2000. CD7 delivers a pro-apoptotic signal during galectin-1-induced T cell death. J. Immunol. 165:2331–2334. http://dx.doi.org/10.4049/jimmunol.165.5.2331.
  • Walzel H, Blach M, Hirabayashi J, Kasai KI, Brock J. 2000. Involvement of CD2 and CD3 in galectin-1 induced signaling in human Jurkat T-cells. Glycobiology 10:131–140. http://dx.doi.org/10.1093/glycob/10.2.131.
  • Pace KE, Lee C, Stewart PL, Baum LG. 1999. Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin-1. J. Immunol. 163:3801–3811.
  • Camby I, Le Mercier M, Lefranc F, Kiss R. 2006. Galectin-1: a small protein with major functions. Glycobiology 16:137R–157R. http://dx.doi.org/10.1093/glycob/cwl025.
  • Battig P, Saudan P, Gunde T, Bachmann MF. 2004. Enhanced apoptotic activity of a structurally optimized form of galectin-1. Mol. Immunol. 41:9–18. http://dx.doi.org/10.1016/j.molimm.2004.02.004.
  • Cedeno-Laurent F, Opperman M, Barthel SR, Kuchroo VK, Dimitroff CJ. 2012. Galectin-1 triggers an immunoregulatory signature in Th cells functionally defined by IL-10 expression. J. Immunol. 188:3127–3137. http://dx.doi.org/10.4049/jimmunol.1103433.
  • Martin P, Sanchez-Madrid F. 2011. CD69: an unexpected regulator of TH17 cell-driven inflammatory responses. Sci. Signal. 4:pe14. http://dx.doi.org/10.1126/scisignal.2001825.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.