Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function

European Journal of Immunology

Volumn 38, Issue 11, 2008, Pages 3015-3027

  Motran, Claudia C ^a,b   Molinder, Karen M ^a   Liu, Scot D ^a   Poirier, Françoise ^a,c   Miceli, M Carrie ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^c INSTITUT JACQUES MONOD   (France)

Author keywords

Apoptosis; CD4 T cells; Cell differentiation; Cytokines; Galectin 1

Indexed keywords

EPITOPE; GALECTIN 1; GALECTIN 3; T LYMPHOCYTE RECEPTOR; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL LEVEL; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME ACTIVITY; FLOW CYTOMETRY; LYMPHOCYTE CULTURE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; TH1 CELL; TH2 CELL; ANIMAL; C57BL MOUSE; HUMAN; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL SURVIVAL; GALECTIN 1; HUMANS; MICE; MICE, INBRED C57BL; RECEPTORS, ANTIGEN, T-CELL; TH1 CELLS; TH2 CELLS;

EID: 58149326953     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200838295     Document Type: Article

References (40)

1. Abbas, A. K., Murphy, K. M. and Sher, A., Functional diversity of helper T lymphocytes. Nature 1996. 383: 787-793.
2. Constant, S. L. and Bottomly, K., Induction of Th1 and Th2 CD4+T cell responses: The alternative approaches. Annu. Rev. Immunol. 1997. 15: 297-322.
3. Glimcher, L. H. and Murphy, K. M., Lineage commitment in the immune system: The T helper lymphocyte grows up. Genes Dev. 2000. 14: 1693-1711.
4. Constant, S., Pfeiffer, C., Woodard, A., Pasqualini, T. and Bottomly, K., Extent of T cell receptor ligation can determine the functional differentiation of naive CD4+T cells. J. Exp. Med. 1995. 182: 1591-1596.
5. Pfeiffer, C., Stein, J., Southwood, S., Ketelaar, H., Sette, A. and Bottomly, K., Altered peptide ligands can control CD4 T lymphocyte differentiation in vivo. J. Exp. Med. 1995. 181: 1569-1574.
6. Bashyam, H., Th1/Th2 cross-regulation and the discovery of IL-10. J. Exp. Med. 2007. 204: 237.
7. Yang, R. Y., Hsu, D. K. and Liu, F. T., Expression of galectin-3 modulates T-cell growth and apoptosis. Proc. Natl. Acad. Sci. USA 1996. 93: 6737-6742.
8. Hahn, H. P., Pang, M., He, J., Hernandez, J. D., Yang, R. Y., Li, L. Y., Wang, X. et al., Galectin-1 induces nuclear translocation of endonuclease G in caspase- and cytochrome c-independent T cell death. Cell Death Differ. 2004. 12: 1277-1286.
9. Vespa, G. N., Lewis, L. A., Kozak, K. R., Moran, M., Nguyen, J. T., Baum, L. G. and Miceli, M. C., Galectin-1 specifically modulates TCR signals to enhance TCR apoptosis but inhibit IL-2 production and proliferation. J. Immunol. 1999. 162: 799-806.
10. Blaser, C., Kaufmann, M., Muller, C., Zimmermann, C., Wells, V., Mallucci, L. and Pircher, H., Beta-galactoside-binding protein secreted by activated T cells inhibits antigen-induced proliferation of T cells. Eur. J. Immunol. 1998. 28: 2311-2319.
11. Pace, K. E., Hahn, H. P., Pang, M., Nguyen, J. T. and Baum, L. G., CD7 delivers a pro-apoptotic signal during galectin-1-induced T cell death. J. Immunol. 2000. 165: 2331-2334.
12. Perillo, N. L., Uittenbogaart, C. H., Nguyen, J. T. and Baum, L. G., Galectin-1, an endogenous lectin produced by thymic epithelial cells, induces apoptosis of human thymocytes. J. Exp. Med. 1997. 185: 1851-1858.
13. Chung, C. D., Patel, V. P., Moran, M., Lewis, L. A. and Miceli, M. C., Galectin-1 induces partial TCR zeta-chain phosphorylation and antagonizes processive TCR signal transduction. J. Immunol. 2000. 165: 3722-3729.
14. Rabinovich, G. A., Daly, G., Dreja, H., Tailor, H., Riera, C. M., Hirabayashi, J. and Chernajovsky, Y., Recombinant galectin-1 and its genetic delivery suppress collagen-induced arthritis via T cell apoptosis. J. Exp. Med. 1999. 190: 385-398.
15. Toscano, M. A., Bianco, G. A., Ilarregui, J. M., Croci, D. O., Correale, J., Hernandez, J. D., Zwirner, N. W. et al., Differential glycosylation of T(H)1, T(H)2 and T(H)-17 effector cells selectively regulates susceptibility to cell death. Nat. Immunol. 2007. 8: 825-834.
16. Offner, H., Celnik, B., Bringman, T. S., Casentini-Borocz, D., Nedwin, G. E. and Vandenbark, A. A., Recombinant human beta-galactoside binding lectin suppresses clinical and histological signs of experimental auto-immune encephalomyelitis. J. Neuroimmunol. 1990. 28: 177-184.
17. Levi, G., Tarrab-Hazdai, R. and Teichberg, V. I., Prevention and therapy with electrolectin of experimental autoimmune myasthenia gravis in rabbits. Eur. J. Immunol. 1983. 13: 500-507.
18. Rubinstein, N., Alvarez, M., Zwirner, N. W., Toscano, M. A., Ilarregui, J. M., Bravo, A., Mordoh, J. et al., Targeted inhibition of galectin-1 gene expression in tumor cells results in heightened T cell-mediated rejection: A potential mechanism of tumor-immune privilege. Cancer Cell 2004. 5: 241-251.
19. Morgan, R., Gao, G., Pawling, J., Dennis, J.W., Demetriou, M. and Li, B., Nacetylglucosaminyltransferase V (Mgat5)-mediated N-glycosylation negatively regulates Th1 cytokine production by T Cells. J. Immunol. 2004. 173: 7200-7208.
20. Comelli, E. M., Sutton-Smith, M., Yan, Q., Amado, M., Panico, M., Gilmartin, T., Whisenant, T. et al., Activation of murine CD4+and CD8+ T lymphocytes leads to dramatic remodeling of N-linked glycans. J. Immunol. 2006. 177: 2431-2440.
21. Daniels, M., Hogquist, K. and Jameson, S., Sweet 'n' sour: The impact of differential glycosylation on T cell responses. Nat. Immunol. 2002. 3: 903-910.
22. Amano, M., Galvan, M., He, J. and Baum, L. G., The ST6Gal I sialyltransferase selectively modifies N-glycans on CD45 to negatively regulate galectin-1-induced CD45 clustering, phosphatase modulation, and T cell death. J. Biol. Chem. 2003. 278: 7469-7475.
23. Blander, J. M., Visintin, I., Janeway Jr. C. A., and Medzhitov, R., Alpha(1,3)-fucosyltransferase VII and alpha(2,3)-sialyltransferase IV are up-regulated in activated CD4 T cells and maintained after their differentiation into Th1 and migration into inflammatory sites. J. Immunol. 1999. 163: 3746-3752.
24. Grabie, N., Delfs, M. W., Lim, Y. C., Westrich, J. R., Luscinskas, F. W. and Lichtman, A. H., Beta-galactoside alpha2,3-sialyltransferase-I gene expression during Th2 but not Th1 differentiation: Implications for core2-glycan formation on cell surface proteins. Eur. J. Immunol. 2002. 32: 2766-2772.
25. Matarrese, P., Tinari, A., Mormone, E., Bianco, G. A., Toscano, M. A., Ascione, B., Rabinovich, G. A. and Malorni, W., Galectin-1 sensitizes resting human T lymphocytes to Fas (CD95)-mediated cell death via mitochondrial hyperpolarization, budding, and fission. J. Biol. Chem. 2005. 280: 6969-6985.
26. Zhang, X., Zhang, L., Devadas, S., Li, L., Keegan, A. and Shi, Y., Reciprocal expression of TRAIL and CD95L in Th1 and Th2 cells: Role of apoptosis in T helper subset differentiation. Cell Death Differ. 2003. 10: 203-210.
27. Rogge, L., Bianchi, E., Biffi, M., Bono, E., Chang, S., Alexander, H., Santini, C. et al., Transcript imaging of the development of human T helper cells using oligonucleotide arrays. Nat. Genet. 2000. 25: 96-101.
28. Joo, H. G., Goedegebuure, P. S., Sadanaga, N., Nagoshi, M., von Bernstorff, W. and Eberlein, T. J., Expression and function of galectin-3, a betagalactoside-binding protein in activated T lymphocytes. J. Leukoc. Biol. 2001. 69: 555-564.
29. Rabinovich, G. and Gruppi, A., Galectins as immunoregulators during infectious processes: From microbial invasion to the resolution of the disease. Parasite Immunol. 2005. 27: 103-114.
30. Ilarregui, J. M., Bianco, G. A., Toscano, M. A. and Rabinovich, G. A., The coming of age of galectins as immunomodulatory agents: impact of these carbohydrate binding proteins in T cell physiology and chronic inflammatory disorders. Ann. Rheum. Dis. 2005. 64: iv96-103.
31. Santucci, L., Fiorucci, S., Rubinstein, N., Mencarelli, A., Palazzetti, B., Federici, B., Rabinovich, G. A. and Morelli, A., Galectin-1 suppresses experimental colitis in mice. Gastroenterology 2003. 124: 1381-1394.
32. Hernandez, J. D., Nguyen, J. T., He, J., Wang, W., Ardman, B., Green, J. M., Fukuda, M. and Baum, L. G., Galectin-1 binds different CD43 glycoforms to cluster CD43 and regulate T cell death. J. Immunol. 2006. 177: 5328-5336.
33. Pace, K. E., Lee, C., Stewart, P. L. and Baum, L. G., Restricted receptor segregation into membrane microdomains occurs on human T cells during apoptosis induced by galectin-1. J. Immunol. 1999. 163: 3801-3811.
34. Balamuth, F., Leitenberg, D., Unternaehrer, J., Mellman, I. and Bottomly, K., Distinct patterns of membrane microdomain partitioning in Th1 and Th2 cells. Immunity 2001. 15: 729-738.
35. Miceli, M. C., Moran, M., Chung, C. D., Patel, V. P., Low, T. and Zinnanti, W., Co-stimulation and counter-stimulation: Lipid raft clustering controls TCR signaling and functional outcomes. Semin. Immunol. 2001. 13: 115-128.
36. Yu, F., Finley, R. L., Raz, Jr., A., and Kim, H. R., Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome c release from the mitochondria. A role for synexin in galectin-3 translocation. J. Biol. Chem. 2002. 277: 15819-15827.
37. Acosta-Rodriguez, E. V., Montes, C. L., Motran, C. C., Zuniga, E. I., Liu, F. T., Rabinovich, G. A. and Gruppi, A., Galectin-3 mediates IL-4-induced survival and differentiation of B cells: Functional cross-talk and implications during Trypanosoma cruzi infection. J. Immunol. 2004. 172: 493-502.
38. Poirier, F. and Robertson, E. J., Normal development of mice carrying a null mutation in the gene encoding the L14 S-type lectin. Development 1993. 119: 1229-1236.
39. Perillo, N. L., Pace, K. E., Seilhamer, J. J. and Baum, L. G., Apoptosis of T cells mediated by galectin-1. Nature 1995. 378: 736-739.
40. Nicoletti, I., Migliorati, G., Pagliacci, M. C., Grignani, F. and Riccardi, C., A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 1991. 139: 271-279.