Diverse populations of T cells with NK cell receptors accumulate in the human intestine in health and in colorectal cancer

European Journal of Immunology

Volumn 34, Issue 8, 2004, Pages 2110-2119

  O'Keeffe, Joan ^a   Doherty, Derek G ^b   Kenna, Tony ^c   Sheahan, Kieran ^c   O'Donoghue, Diarmuid P ^c,d   Hyland, John M ^c   O'Farrelly, Cliona ^c,d  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^c ST VINCENT S UNIVERSITY HOSPITAL   (Ireland)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Human; Intestine; NKT cells; T lymphocytes; Tumor immunity

Indexed keywords

ALPHA GALACTOSYLCERAMIDE; CD161 ANTIGEN; CD1D ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; CYTOKINE; FAS LIGAND; GAMMA INTERFERON; HLA DR ANTIGEN; INTERLEUKIN 4; LYMPHOCYTE ANTIGEN; LYMPHOCYTE RECEPTOR; NATURAL KILLER CELL RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; IMMUNOGLOBULIN RECEPTOR; LECTIN; MEMBRANE ANTIGEN;

ADULT; AGED; ARTICLE; CELL COMPARTMENTALIZATION; CELL ISOLATION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; COLON; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DUODENUM; EPITHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTESTINE; MAJOR HISTOCOMPATIBILITY COMPLEX; MALE; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; T LYMPHOCYTE SUBPOPULATION; TUMOR IMMUNITY; COLORECTAL TUMOR; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE;

ANTIGENS, SURFACE; COLORECTAL NEOPLASMS; CYTOKINES; HUMANS; INTESTINES; LECTINS, C-TYPE; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES;

EID: 4444298192     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200424958     Document Type: Article

References (52)

1. Schmidt, R. E., Murray, C., Daley, J. F., Schlossman, S. F. and Ritz, J., A subset of natural killer cells in peripheral blood displays a mature T cell phenotype. J. Exp. Med. 1986. 164: 351-356.
2. Lanier, L. L., Le, A. M., Civin, C. I., Loken, M. R. and Phillips, J. H., The relationship of CD16 (Leu-11) and Leu-19 (NKH-1) antigen expression on human peripheral NK cells and cytotoxic T lymphocytes. J. Immunol. 1986. 136: 4480-4486.
3. Dunne, J., Lynch, S., O'Farrelly, C., Hegarty, J. E., Feighery, C. and Doherty, D. G., Selective expansion and partial activation of human NK cells and NK receptor-positive T cells by IL-2 and IL-15. J. Immunol. 2001. 167: 3129-3138.
4. +T cells. Curr. Opin. Immunol. 2001. 13: 465-470.
5. + cells derived from T cells with potent in vivo anti-tumor activity in mice with severe combined immunodeficiency. J. Immunol. 1994. 153: 1687-1696.
6. Satoh, M., Seki, S., Hashimoto, W., Ogasawara, K., Kobayashi, T., Kumagai, K., Matsuno, S. and Takeda, K., Cytotoxic γδ or αβ T cells with a natural killer cell marker, CD56, induced from human peripheral lymphocytes by a combination of IL-2 and IL-12. J. Immunol. 1996. 157: 3886-3892.
7. + natural T cells with distinct cytotoxic activities and Th1, Th2, and Th0 cytokine secretion patterns. J. Immunol. 1999. 163: 2314-2321.
8. Norris, S., Doherty, D. G., Collins, C., McEntee, G., Traynor, O., Hegarty, J. E. and O'Farrelly, C., Natural T cells in the human liver: cytotoxic lymphocytes with dual T cell and natural killer cell phenotype and function are phenotypically heterogenous and include Va24-JαQ and γδ T cell receptor bearing cells. Hum. Immunol. 1999. 60: 20-31.
9. Exley, M. A., Tahir, S. M., Cheng, O., Shaulov, A., Joyce, R., Avigan, D., Sackstein, R. and Balk, S. P., A major fraction of human bone marrow lymphocytes are Th2-like CD1d-reactive T cells that can suppress mixed lymphocyte responses. J. Immunol. 2001. 167: 5531-5534.
10. Mingari, M. C., Vitale, C., Cambiaggi, A., Schiavetti, F., Melioli, G., Ferrini, S. and Poggi, A., Cytolytic T lymphocytes displaying natural killer (NK)-like activity: expression of NK-related functional receptors for HLA class I molecules (p58 and CD94) and inhibitory effect on the TCR-mediated target cell lysis or lymphokine production. Int. Immunol. 1995. 4: 697-703.
11. Ferrini, S., Cambiaggi, A., Meazza, R., Sforzini, S., Marciano, S., Mingari, M. C. and Moretta, L., T cell clones expressing the natural killer cell-related p58 receptor molecule display heterogeneity in phenotypic properties and p58 function. Eur. J. Immunol. 1994. 10: 2294-2298.
12. Moretta, L., Romagnani, C. Petra, G. Moretta, A. and Mingari, M. C., NK-CTL, a novel HLA-E-restricted T-cell subset. Trends Immunol. 2003. 3: 136-143.
13. Lopez-Botet, M., Angulo, A. and Guma, M., Natural killer cell receptors for major histocompatibility complex class I and related molecules in cytomegalovirus infection. Tissue Antigens. 2004. 3: 195-203.
14. Snyder, M. R., Weyand, C. M. and Goronzy, J. J., The double life of NK receptors: stimulation or co-stimulation? Trends Immunol. 2004. 1: 25-32.
15. + T cells by inhibitory natural killer cell receptors. Microbes Infect. 2003. 2: 169-177.
16. Ugolini, S. and Vivier, E., Regulation of T cell function by NK receptors for classical MHC class I molecules. Curr. Opin. Immunol. 2003. 3: 295-300.
17. Bendelac, A., Rivera, M. N., Park, S. H. and Roark, J. H., Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu. Rev. Immunol. 1997. 15: 535-562.
18. Porcelli, S. A. and Modlin, R. L., The CD1 system: antigen-presenting molecules for T cell recognition of lipids and glycolipids. Annu. Rev. Immunol. 1999. 17: 297-329.
19. Kronenberg, M. and Gapin, L., The unconventional lifestyle of NKT cells. Nat. Rev. Immunol. 2000. 2: 557-568.
20. Kawano, T., Cui, J., Koezuka, Y., Toura, I., Kaneko, Y., Motoki, K., Ueno, H., Nakagawa, R., Sato, H., Kondo, E., Koseki, H. and Taniguchi, M., CD1d-restricted and TCR-mediated activation of Vα14 NKT cells by glycosylceramides. Science 1997. 278: 1626-1629.
21. Brossay, L., Chioda, M., Burdin, N., Koezuka, Y., Casorati, G., Dellabona, P. and Kronenberg, M., CD1d-mediated recognition of an α-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution. J. Exp. Med. 1998. 188: 1521-1528.
22. Nakagawa, R., Nagafune, I., Tazunoki, Y., Ehara, H., Tomura, H., Iijima, R., Motoki, K., Kamishohara, M. and Seki, S., Mechanisms of the anti-metastatic effect in the liver and of the hepatocyte injury induced by α-galactosylceramide in mice. J. Immunol. 2001. 166: 6578-6584.
23. Smyth, M. J., Crowe, N. Y., Hayakawa, Y., Takeda, K., Yagita, H. and Godfrey, D. I., NKT cells - conductors of tumor immunity? Curr. Opin. Immunol. 2002. 14: 165-171.
24. Cui, J., Shin, T., Kawano, T., Sato, H., Kondo, E., Toura, I., Kaneko, Y., Koseki, H., Kanno, M. and Taniguchi, M., Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumours. Science 1997. 278: 1623-1626.
25. - α/β T cells demonstrates preferential use of several Vβ genes and an invariant TCR α chain. J. Exp. Med. 1993. 178: 1-16.
26. - T cells. J. Exp. Med. 1997. 186: 109-120.
27. Kenna, T., Golden Mason, L., Porcelli, S. A., Koezuka, Y., Hegarty, J. E., O'Farrelly, C. and Doherty, D. G., Natural killer T (NKT) cells from normal and tumor-bearing human livers are phenotypically and functionally distinct from murine NKT cells. J. Immunol. 2003. 171: 1775-1779.
28. Winnock, M., Garcia-Barcina, M., Huet, S., Bernard, P., Saric, J., Biolac-Sage, P. and Gualde, N., Functional characterisation of liver-associated lymphocytes in patients with liver metastasis. Gastroenterology 1993. 105: 1152-1158.
29. + T cells in patients with malignancy. Clin. Exp. Immunol. 1994. 97: 522-527.
30. Viney, J., MacDonald, T. T. and Spencer, J., γδ T cells in the gut epithelium. Gut 1990. 31: 841-844.
31. + cells. Eur. J. Gastroenterol. Hepatol. 1993. 5: 907-913.
32. + T cells for helper activity. Int. Immunol. 1993. 5: 1473-1481.
33. Guy-Grand, D. and Vassalli, P., Gut intraepithelial lymphocyte development. Curr. Opin. Immunol. 2002. 14: 255-259.
34. Roberts, A. I., O'Connell, S. M. and Ebert, E. C., Intestinal intraepithelial lymphocytes bind to colon cancer cells by HML-1 and CD11a. Cancer Res. 1993. 53: 1608-1611.
35. Sunagawa, T., Yonamine, Y., Kinjo, F., Watanabe, M., Hibi, T. and Saito, A., HLA class-I-restricted and colon-specific cytotoxic T cells from lamina propria lymphocytes of patients with ulcerative colitis. J. Clin. Immunol. 2001. 21: 381-389.
36. + T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res. 1998. 58: 3491-3494.
37. - and TCRαβ-positive T lymphocytes predominantly infiltrated into well-moderately differentiated colon adenocarcinoma tissues. Jpn. J. Clin. Oncol. 1998. 28: 97-103.
38. Jabri, B., de Serre, N. P., Cellier, C., Evans, K., Gache, C., Carvalho, C., Mougenot, J. F., Allez, M., Jian, R., Desreumaux, P., Colombel, J. F., Matuchansky, C., Cugnenc, H., Lopez-Botet, M., Vivier, E., Moretta, A., Roberts, A. I., Ebert, E. C., Guy-Grand, D., Brousse, N., Schmitz, J. and Cerf-Bensussan, N., Selective expansion of intraepithelial lymphocytes expressing the HLA-E-specific natural killer receptor CD94 in celiac disease. Gastroenterology 2000. 118: 867-879.
39. + T (NT) cells exist predominantly in human intestinal epithelium as well as in liver. Clin. Exp. Immunol. 2002. 129: 92-98.
40. + natural killer T cells in the large intestine. Eur. J. Immunol. 2001. 31: 3361-3369.
41. Benlagha, K., Weiss, A., Beavis, A., Teyton, L. and Bendelac, A., In vivo identification of glycolipid antigen-specific T cells using fluorescent CD1d tetramers. J. Exp. Med. 2000. 191: 1895-1903.
42. Karadimitris, A., Gadola, S., Altamirano, M., Brown, D., Woolfson, A., Klenerman, P., Chen, J. L., Koezuka, Y., Roberts, I. A., Price, D. A., Dusheiko, G., Milstein, C., Fersht, A., Luzzatto, L. and Cerundolo, V., Human CD1d-glycolipid tetramers generated by in vitro oxidative refolding chromatography. Proc. Natl. Acad. Sci. USA 2001. 98: 3294-3298.
43. Van de Wal, Y., Corazza, N., Allez, M., Mayer, L. F., Iijima, H., Ryan, M., Cornwall, S., Kaiserlian, D., Hershberg, R., Koezuka, Y., Colgan, S. P. and Blumberg, R. S., Delineation of a CD1d-restricted antigen presentation pathway associated with human and mouse intestinal epithelial cells. Gastroenterology 2003. 124: 1420-1431.
44. Bleicher, P. A., Balk, S. P., Hagen, S. J., Blumberg, R. S., Flotte, T. J. and Terhorst, C., Expression of murine CD1 on gastrointestinal epithelium. Science 1990. 250: 679-682.
45. Blumberg, R. S., Terhorst, C., Bleicher, P., McDermott, F. V., Allan, C. H., Landau, S. B., Trier, J. S. and Balk, S. P., Expression of a nonpolymorphic MHC class I-like molecule, CD1d, by human intestinal epithelial cells. J. Immunol. 1991. 147: 2518-2524.
46. Balk, S. P., Burke, S., Polischuk, J. E., Frantz, M. E., Yang, L., Porcelli, S., Colgan, S. P. and Blumberg, R. S., β2-microglobulin-independent MHC class Ib molecule expressed by human intestinal epithelium. Science 1994. 265: 259-262.
47. Exley, M. A., He, Q., Cheng, O., Wang, R. J., Cheney, C. P., Balk, S. P. and Koziel, M. J., Cutting edge: Compartmentalization of Th1-like noninvariant CD1d-reactive T cells in hepatitis C virus-infected liver. J. Immunol. 2002. 168: 1519-1523.
48. Metelitsa, L. S., Naidenko, O. V., Kant, A., Wu, H. W., Loza, M. J., Perussia, B., Kronenberg, M. and Seeger, R. C., Human NKT cells mediate antitumor cytotoxicity directly by recognizing target cell CD1d with bound ligand or indirectly by producing IL-2 to activate NK cells. J. Immunol. 2001. 167: 3114-3122.
49. Song, E., Chen, J., Ouyang, N., Su, F., Wang, M. and Heemann, U., Soluble Fas ligand released by colon adenocarcinoma cells induces host lymphocyte apoptosis: an active mode of immune evasion in colon cancer. Br. J. Cancer. 2001. 85: 1047-1054.
50. Tahir, S. M., Cheng, O., Shaulov, A., Koezuka, Y., Bubley, G. J., Wilson, S. B., Balk, S. P. and Exley, M. A., Loss of IFN-γ production by invariant NK T cells in advanced cancer. J. Immunol. 2001. 167: 4046-4050.
51. Madrigal, L., Lynch, S., Feighery, C., Weir, D., Kelleher, D. and O'Farrelly, C., Flow cytometric analysis of surface major histocompatibility complex class II expression on human epithelial cells prepared from small intestinal biopsies. J. Immunol. Methods 1993. 158: 207-214.
52. Abuzakouk, M., Kelleher, D., Feighery, C. and O'Farrelly, C., Increased HLA-DR and decreased CD3 on human intestinal intraepithelial lymphocytes: evidence of activation? Gut 1996. 39: 396-400.