CD29 and CD7 Mediate Galectin-3-Induced Type II T-Cell Apoptosis

Cancer Research

Volumn 63, Issue 23, 2003, Pages 8302-8311

  Fukumori, Tomoharu ^a,b   Takenaka, Yukinori ^a   Yoshii, Tadashi ^c   Kim, Hyeong Reh Choi ^d   Hogan, Victor ^a   Inohara, Hidenori ^c   Kagawa, Susumu ^b   Raz, Avraham ^a,e  

^a WAYNE STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e KARMANOS CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CARBOHYDRATE; CASPASE 3; CASPASE 8; CD7 ANTIGEN; CELL SURFACE RECEPTOR; CERAMIDE; CYTOCHROME C; GALECTIN; GALECTIN 3; GLYCOCONJUGATE; GLYCOCONJUGATE RECEPTOR; LACTOSE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIAPOPTOTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER INFILTRATION; CELL ADHESION; CELL SURFACE; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNE ESCAPE; IMMUNOLOGICAL TOLERANCE; LEUKEMIA CELL LINE; LEUKEMIA CEM LINE; LEUKEMIA H 9 CELL; LEUKEMIA MOLT 4 CELL; LEUKEMIA SKW 6.4 CELL; MITOCHONDRION; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; RECEPTOR BINDING; T CELL LEUKEMIA; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR GROWTH;

ANIMALS; ANTIGENS, CD29; ANTIGENS, CD7; APOPTOSIS; CASPASES; ENZYME ACTIVATION; GALECTIN 3; HUMANS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; T-LYMPHOCYTES; TRANSFECTION;

EID: 0345734273     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (69)

1. Barondes, S. H., Cooper, D. N., Gitt, M. A., and Leffier, H. Galectins: structure and function of a large family of animal lectins. J. Biol. Chem., 269: 20807-20810, 1994.
2. Barondes, S. H., Castronovo, V., Cooper, D. N., Cummings, R. D., Drickamer, K., Feizi, T., Gitt, M. A., Hirabayashi, J., Hughes, C., Kasai, K., Leffier, H., Liu, F., Lotan, R., Mercurio, A. M., Monsigny, M., Pillai, S., Poirer, F., Raz, A., Rigby, P. W., Rini, J. M., and Wang, J. L. Galectins: a family of animal β-galactoside-binding lectins. Cell, 76: 597-598, 1994.
3. Hughes, R. C. Galectins as modulators of cell adhesion. Biochimie (Paris). 83: 667-676, 2001.
4. Perillo, N. L., Marcus, M. E., and Baum, L. G. Galectins: versatile modulators of cell adhesion, cell proliferation, and cell death. J Mol. Med., 76: 402-412, 1998.
5. Yang, R. Y., and Liu, F. T. Galectins in cell growth and apoptosis. Cell Mol. Life Sci., 60: 267-276, 2003.
6. Inohara, H., Akahani, S., and Raz, A. Galectin-3 stimulates cell proliferation. Exp. Cell Res., 245: 294-302, 1998.
7. Hughes, R. C. Secretion of the galectin family of mammalian carbohydrate-binding proteins. Biochim. Biophys. Acta, 1473: 172-185, 1999.
8. Inohara, H., and Raz, A. Functional evidence that cell surface galectin-3 mediate homotypic cell adhesion. Cancer Res., 55: 3267-3271, 1995.
9. Sano, H., Hsu, D. K., Yu, L., Apgar, J. R., Kuwabara, I., Yamanaka, T., Hirashima, M., and Liu, F. T. Human galectin-3 is a novel chemoattractant for monocytes and macrophages. J. Immunol., 165: 2156-2164, 2000.
10. Démetriou, M., Granovsky, M., Quaggin, S., and Dennis, J. W. Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature (Lond.), 409: 733-739, 2001.
11. Sano, H., Hsu, D. K., Apgar, J. R., Yu, L., Sharma, B. B., Kuwabara, I., Izui, S., and Liu, F. T. Critical role of galectin-3 in phagocytosis by macrophages. J. Clin. Investig., 112: 389-397, 2003.
12. Perillo, N. L., Uittenbogaart, C., Nguyen, J., and Baum, L. G. Galectin-1, an endogenous lectin produced by thymic epithelial cells, induces apoptosis of human thymocytes. J. Exp. Med., 185: 1851-1858, 1997.
13. Perillo, N. L., Pace, K. E., Seilhamer, J. J., and Baum, L. G. Apoptosis of T cells mediated by galectin-1. Nature (Lond.), 378: 736-739, 1995.
14. Wells, V., Davies, D., and Mallucci, L. Cell cycle arrest and induction of apoptosis by β galactoside binding protein (β GBP) in human mammary cancer cells. A potential new approach to cancer control. Eur. J. Cancer, 35: 978-983, 1999.
15. Wada, J., Ota, K., Kumar, A., Wallner, E. I., and Kanwar, Y. S. Developmental regulation, expression, and apoptotic potential of galectin-9, a β-galactoside binding lectin. J. Clin. Investig., 99: 2452-2461, 1997.
16. Kuwabara, I., Kuwabara, Y., Yang, R. Y., Schuler, M., Green, D. R., Zuraw, B. L., Hsu, D. K., and Liu, F. T. Galectin-7 (PIGI) exhibits pro-apoptotic function through JNK activation and mitochondrial cytochrome c release. J. Biol. Chem., 277: 3487-3497, 2002.
17. Inohara, H., Akahani, S., Koths, K., and Raz, A. Interactions between galectin-3 and Mac-2-binding protein mediate cell-cell adhesion. Cancer Res., 56: 4530-4534, 1996.
18. Kuwabara, I., and Liu, F. T. Galectin-3 promotes adhesion of human neutrophils to laminin. J. Immunol., 156: 3939-3944, 1996.
19. Akahani, S., Nangia-Makker, P., Inohara, H., Kim, H. R., and Raz, A. Galectin-3: a novel anti-apoptotic molecule with a functional BHI (NWGR) domain of Bcl-2 family. Cancer Res., 57: 5272-5276, 1997.
20. Kim, H. R., Lin, H. M., Biliran, H., and Raz, A. Cell cycle arrest and inhibition of anoikis by galectin-3 in human breast epithelial cells. Cancer Res., 59: 4148-4154, 1999.
21. 2/M arrest and inhibits apoptosis. Carcinogenesis (Lond.), 21: 1941-1945, 2000.
22. 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, 93: 6737-6742, 1996.
23. Iurisci, I., Tinari, N., Natoli, C., Angelucci, D., Cianchetti, E., and Iacobelli, S. Concentrations of galectin-3 in the sera of normal controls and cancer patients. Clin. Cancer Res., 6: 1389-1393, 2000.
24. 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., 163: 3801-3811, 1999.
25. 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., 165: 2331-2334, 2000.
26. Gong, H. C., Honjo, Y., Nangia-Makker, P., Hogan, V., Mazurak, N., Bresalier, R. S., and Raz, A. The NH2 terminus of galectin-3 governs cellular compartmentalization and functions in cancer cells. Cancer Res., 59: 6239-6245, 1999.
27. Yoshii, T., Fukumori, T., Honjo, Y., Inohara, H., Kim. H. R., and Raz, A. Galectin-3 phosphorylation is required for its anti-apoptotic function and cell cycle arrest. J. Biol. Chem., 277: 6852-6857, 2002.
28. Akari, H., Bour, S., Kao, S., Adachi, A., and Strebel, K. The human immunodeficiency virus type I accessory protein Vpu induces apoptosis by suppressing the nuclear factor κB-dependent expression of antiapoptotic factors. J. Exp. Med., 194: 1299-1311, 2001.
29. Yu, F., Finley, R. L., Jr., Raz, 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., 277: 15819-15827, 2002.
30. Su, X., Zhou, T., Wang, Z., Yang, P., Jope, R. S., and Mountz, J. D. Defective expression of hematopoietic cell protein tyrosine phosphatase (HCP) in lymphoid cells blocks Fas-mediated apoptosis. Immunity, 2: 353-362, 1995.
31. Scaffidi, C., Schmitz, I., Zha, J., Korsmeyer, S. J., Krammer, P. H., and Peter, M. E. Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J. Biol. Chem., 274: 22532-22538, 1999.
32. Garcia-Ruiz, C., Colell, A., Mari, M., Morales, A., and Fernandez-Checa, J. C. Direct effect of ceramide on the mitochondrial electron transport chain leads to generation of reactive oxygen species. Role of mitochondrial glutathione. J. Biol. Chem., 272: 11369-11377, 1997.
33. Quillet-Mary, A., Jaffrezou, J. P., Mansat, V., Bordier, C., Naval, J., and Laurent, G. Implication of mitochondrial hydrogen peroxide generation in ceramide-induced apoptosis. J. Biol. Chem., 272: 21388-21395, 1997.
34. Gudz, T. I., Tserng, K. Y., and Hoppel, C. L. Direct inhibition of mitochondrial respiratory chain complex III by cell-permeable ceramide. J. Biol. Chem., 272: 24154-24158, 1997.
35. Enari, M., Talanian, R. V., Wong, W. W., and Nagata, S. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature (Lond.), 380: 723-726, 1996.
36. Hsu, H., Xiong, J., and Goeddel, D. V. The TNF receptor 1-associated protein TRADD signals cell death and NF-κB activation. Cell, 81: 495-504, 1995.
37. Green, D. R. Apoptotic pathways: the roads to ruin. Cell, 94: 695-698, 1998.
38. Thornberry, N. A., and Lazebnik, Y. Caspases: enemies within. Science (Wash. DC), 281: 1312-1316, 1998.
39. Belkin, V. M., Kozlova, N. I., Bychkova, V. V., and Shekhonin, B. V. β1 Integrin subunit dimerization via disulfide bonds. Biochem. Mol. Biol. Int., 40: 53-60, 1996.
40. Dias-Baruffi, M., Zhu, H., Cho, M., Karmakar, S., McEver, R. P., and Cummings, R. D. Dimeric galectin-1 induces surface exposure of phosphatidylserine and phagocytic recognition of leukocytes without inducing apoptosis. J. Biol. Chem., 278: 41282-41293, 2003.
41. Scaffidi, C., Fulda, S., Srinivasan, A., Friesen, C., Li, F., Tomaselli, K. J., Debatin, K. M., Krammer, P. H., and Peter, M. E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J., 17: 1675-1687, 1998.
42. Cuvillier, O., Edsall, L., and Spiegel, S. Involvement of sphingosine in mitochondria-dependent Fas-induced apoptosis of type II Jurkat T cells. J. Biol. Chem., 275: 15691-15700, 2000.
43. Liu, F. T. Galectins: a new family of regulators of inflammation. Clin. Immunol., 97: 79-88, 2000.
44. Cooper, D. N., and Barondes, S. H. God must love galectins; he made so many of them. Glycobiology, 9: 979-984, 1999.
45. Salvatore, P., Benvenuto, G., Pero. R., Lembo, F., Bruni, C. B., and Chiariotti, L. Galectin-1 gene expression and methylation stale in human T leukemia cell lines. Int. J. Oncol., 17: 1015-1018, 2000.
46. Sempowski, G. D., Lee, D. M., Kaufman, R. E., and Haynes, B. F. Structure and function of the CD7 molecule. Crit. Rev. Immunol., 19: 331-348, 1999.
47. Bareena, A., Muench, M. O., Roncarolo, M. G., and Spits, H. Tracing the expression of CD7 and other antigens during T- and myeloid-cell differentiation in the human fetal liver and thymus. Leuk. Lymphoma, 17: 1-11, 1995.
48. Rabinowich, H., Pricop, L., Herberman, R. B., and Whiteside, T. L. Expression and function of CD7 molecule on human natural killer cells. J. Immunol., 152: 517-526. 1994.
49. Reinhold, U., Liu, L., Sesterhenn, J., and Abken, H. CD7-negative T cells represent a separate differentiation pathway in a subset of post-thymic helper T cells. Immunology, 89: 391-396, 1996.
50. Lee, D. M., Staats, H. F., Sundy, J. S., Patel, D. D., Sempowski, G. D., Scearce, R. M., Jones, D. M., and Haynes, B. F. Immunologic characterization of CD7-deficient mice. J. Immunol., 160: 5749-5756, 1998.
51. Roberts, A. A., Amano, M., Felten, C., Galvan, M., Sulur, G., Pinter-Brown, L., Dobbeling, U., Burg, G., Said, J., and Baum, L. G. Galectin-1-mediated apoptosis in mycosis fungoides: the roles of CD7 and cell surface glycosylation. Mod. Pathol., 6: 543-551, 2003.
52. - leukemic T cells from patients with Sezary syndrome are protected from galectin-1-triggered T cell death. Leukemia (Baltimore), 16: 840-845, 2002.
53. Hemler, M. E. VLA proteins in the integrin family: structures, functions, and their role on leukocytes. Annu. Rev. Immunol., 8: 365-400, 1990.
54. Shimizu, Y., and Shaw, S. Lymphocyte interactions with extracellular matrix. FASEB J., 5: 2292-2299, 1991.
55. Furtak, V., Hatcher, F., and Ochieng, J. Galectin-3 mediates the endocytosis of β-1 integrins by breast carcinoma cells. Biochem. Biophys. Res. Commun., 289: 845-850, 2001.
56. Ochieng, J., Leite-Browning, M. L., and Warfield, P. Regulation of cellular adhesion to extracellular matrix proteins by galectin-3. Biochem. Biophys. Res. Commun., 246: 788-791, 1998.
57. Hadari, Y. R., Arbel-Goren, R., Levy, Y., Amsterdam, A., Alon, R., Zakut, R., and Zick, Y. Galectin-8 binding to integrins inhibits cell adhesion and induces apoptosis. J. Cell Sci., 113: 2385-2397, 2000.
58. 1 integrin with fibronectin and laminin by L-14 lectin during skeletal muscle differentiation. J. Cell Sci., 107: 175-181, 1994.
59. Stupack, D. G., and Cheresh, D. A. Get a ligand, get a life: integrins, signalling and cell survival. J. Cell Sci., 115: 3729-3738, 2002.
60. 1-integrin signaling pathways. Hypertension, 41: 903-911, 2003.
61. Nakayamada, S., Saito, K., Fujii, K., Yasuda, M., Tamura, M., and Tanaka, Y. β1 Integrin-mediated signaling induces intercellular adhesion molecule 1 and Fas on rheumatoid synovial cells and Fas-mediated apoptosis. Arthritis Rheum., 48: 1239-1248, 2003.
62. 1-integrin. Eur. J. Immunol., 32: 1129-1138, 2002.
63. Stupack, D. G., Puente, X. S., Boutsaboualoy, S., Storgard, C. M., and Cheresh, D. A. Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. J. Cell Biol., 155: 459-470, 2001.
64. Mary, F., Moon, C., Venaille, T., Thomas, M. L., Mary, D., and Bernard, A. Modulation of TCR signaling by β1 integrins: role of the tyrosine phosphatase SHP-1. Eur. J. Immunol., 29: 3887-3897, 1999.
65. Damle, N. K., Klussman, K., Leytze, G., Aruffo, A., Linsley, P. S., and Ledbetter, J. A. Costimulation with integrin ligands intercellular adhesion molecule-1 or vascular cell adhesion molecule-1 augments activation-induced death of antigen-specific CD4+ T lymphocytes. J. Immunol., 151: 2368-2379, 1993.
66. 1 integrin stimulation is associated with impaired T-cell signaling through VLA-4 after allogeneic bone marrow transplantation. Blood, 90: 4222-4229, 1997.
67. Shimizu, Y., van Seventer, G. A., Ennis, E., Newman, W., Horgan, K. J., and Shaw, S. Crosslinking of the T cell-specific accessory molecules CD7 and CD28 modulates T cell adhesion. J. Exp. Med., 175: 577-582, 1992.
68. Leta, E., Roy, A. K., Hou. Z., and Jung, L. K. Production and characterization of the extracellular domain of human CD7 antigen: further evidence that CD7 has a role in T cell signaling. Cell. Immunol., 165: 101-109, 1995.
69. Ochieng, J., Green, B., Evans, S., James, O., and Warfield, P. Modulation of the biological functions of galectin-3 by matrix metalloproteinases. Biochim. Biophys. Acta. 1379: 97-106, 1998.