Human intestinal Vδ1+ T lymphocytes recognize tumor cells of epithelial origin

Journal of Experimental Medicine

Volumn 183, Issue 4, 1996, Pages 1681-1696

  Maeurer, Markus J ^a,b   Martin, Dina ^b   Walter, Wolfgang ^b   Liu, Kaihong ^c   Zitvogel, Laurence ^b,d   Halusczcak, Kathy ^b   Rabinowich, Hanna ^d   Duquesnoy, Rene ^c   Storkus, Walter ^b,d   Lotze, Michael T ^b,d  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b Depts Surg Biochem Molec G   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 7; T LYMPHOCYTE RECEPTOR; CELL ADHESION MOLECULE; INTERLEUKIN 1; LYMPHOCYTE ANTIGEN RECEPTOR; MESSENGER RNA; TUMOR ANTIGEN;

ANTIBODY SPECIFICITY; ANTIGEN EXPRESSION; ARTICLE; CANCER CELL CULTURE; CELL STRAIN K 562; COLORECTAL CANCER; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOMODULATION; INTESTINE EPITHELIUM; PRIORITY JOURNAL; T LYMPHOCYTE SUBPOPULATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNOLOGY; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; COLORECTAL TUMOR; COMPARATIVE STUDY; CULTURE TECHNIQUE; CYTOLOGY; DRUG EFFECT; GENETICS; IMMUNOLOGY; KIDNEY TUMOR; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MOUSE; NEOPLASM; NUCLEOTIDE SEQUENCE; PANCREAS TUMOR; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, NEOPLASM; BASE SEQUENCE; CELL ADHESION MOLECULES; CELL LINE; COLORECTAL NEOPLASMS; CULTURE TECHNIQUES; HUMANS; INTERFERON TYPE II; INTERLEUKIN-1; INTERLEUKIN-7; KIDNEY NEOPLASMS; LYMPHOCYTES, TUMOR-INFILTRATING; MICE; MOLECULAR SEQUENCE DATA; NEOPLASMS, GLANDULAR AND EPITHELIAL; PANCREATIC NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RNA, MESSENGER; SEQUENCE HOMOLOGY; T-LYMPHOCYTE SUBSETS;

EID: 0029665819     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.183.4.1681     Document Type: Article

References (74)

1. Jitsukawa, S.F., F. Faure, M. Lipinski, F. Triebel, and T. Hercend. 1987. A novel subset of human lymphocytes with a T cell receptor-γ complex. J. Exp. Med. 166:1192-2001.
2. + Wt31-lymphocytes to express their functional program(s). J. Exp. Med. 168:1-11.
3. Wu, Y.-J., W.-T. Tian., R.M. Snider, C. Rittershaus, P. Rogers, L. LaManna, and S.H. Ip. 1988. Signal transduction of γδ T cell antigen receptor with a novel mitogenic anti-δ antibody. J. Immunol. 141:1476-1482.
4. Koning, F., M. Knot, F. Wassenaar, and P. van den Elsen. 1989. Phenotypical heterogeneity among human T cell receptor γδ-expressing clones derived from peripheral blood. Eur. J. Immunol. 19:2099-2105.
5. Deush, K., F. Luling, K. Reich, M. Classen, H. Wagner, and K. Pfeffer. 1991. A major fraction of human intraepithelial lymphocytes simultaneously expresses the γδ cell receptor, the CD8 accessory molecule and preferentially uses the Vδ1 gene segment. Eur J. Immunol. 21:1053-1060.
6. Lundqvist, C., and H.-L. Mammarstrom. 1993. T-cell receptor γδ-expressing intraepithelial lymphocytes are present in normal and chronically inflamed gingiva. Immunology 79:38-46.
7. Chowers, Y., W., Holtnieier, J. Harwood, E. Morzycka-Wroblewska, and M.F. Kagnoff. 1994. The Vd1 T cell receptor repertoire in human small intestine and colon. J. Exp. Med. 180:183-190.
8. - γδ T cells. J. Exp. Med. 177:425-432.
9. Sodcrstrom, K., A.N. Bucht, E. Halapi, C, Lundquist, A. Gronberg, E. Nilsson, D. L.M. Orsim, Y. van der Wal, F. Koning, M.-L. Hammarstrom, and R. Kiessling. 1994. High expression of Vγ8 is a shared feature of human γδ T cells in the epithelium of the gut and in the inflamed synovial tissue. J. Immunol. 152:6017-6027.
10. Rsut, C.J., F Verreck, H. Vietir, and F. Koning. 1990. Specific recognition of staphylococcal enterotoxin A by human T cells bearing receptors with the V gamma 9 region. Nature (Lond.). 346:572-575.
11. Tanaka, Y., C. Morita, Y. Tanaka, E. Nieves, M.B. Brenner, and B.R. Bloom. 1995. Natural and synthetic non-peptide antigens recognized by human γδ T cells. Nature (Lond.). 375:155-158.
12. Sciammas, R., R.M. Johnson, A.I. Sperling, W. Brady, P.S. Linsley, P.G. Spear, F.W. Fitch, and J.A. Bluestone. 1994. Unique antigen recognition by a herpesvius-specific TCR-γδ cell. J. Immunol. 152:5392-5397.
13. Fisch, P., M. Malkovsky, S. Kovats, E. Sturm, E. Braakman, B.S. Klein, S.D. Voss, L.W. Morrissey, R. DeMars, W.J. Welch et al. 1990. Recognition by human Vγ9/Vδ2 cells of a GroEL homolog on Daudi Burkitt's lymphoma cells. Science (Wash. DC). 250:1269-1272.
14. Balk, S.P., E.C. Ebert, R.L. Blumentthal, F.V. McDermott, K.W. Wucherpfennig, S.B. Landau, and R.S. Blumberg. 1991. Oligoclonal expansion and CD1 recognition by human intestinal intraepithelial lymphocytes. Science (Wash. DC). 253: 1411-1415.
15. Morita, A., T. Takahashi, E. Stockert, E. Nakayama, T. Tsuji, Y. Matsudaira, L.J. Old, and Y. Obata. 1994. TL antigen as a transplantation antigen recognized by TL-restricted cytotoxic T cells. J. Exp. Med 179: 777-785.
16. Eghtesady, P., C. Panwala, and M. Kronenberg. Recognition of the thymus leukemia antigen by intestinal γδ T lymphocytes. Proc Natl. Acad Sci. USA. In press.
17. Havran, W.L., and R. Boismenu. 1994. Activation and function of γδ T cells. Curr. Opin. Immunol. 6:442-146.
18. Davedeau, F., M.A. Peyrat, M.M. Hallet, J. Gaschet, I. Houde, R. Vivien, H. Vie, and M. Bonneville. 1993. Close correlation between Daudi and mycobacterial antigen recognition by human 70 T cells and expression of V9JPC1γ/ V2DJCδ-encoded T cell recptors. J. Immunol. 151:1214-1223.
19. Kronenberg. M. 1994. Antigen recognized by γδ T cells. Curr. Opin. Immunol. 6:64-71.
20. Schild, A., N. Mavaddat, C. Litzenberger, E.W. Ehrich, M.M. Davis, J.A. Bluestone, L. Matis, R.K. Draper, and Y.-H. Chien 1994. The nature of major histocompatibility complex recognition by γδ T cells. Cell. 76:29-37.
21. Rock, E.P., P.R. Sibbald, M.M. Davis, and Y.-H. Chien. 1994. CDR3 length in antigen-specific immune responses. J. Exp. Med. 179:323-328.
22. + γδ T cells. Eur. J. Immunol. 24:3199-3204.
23. + T cell expansion in the peripheral blood of HIV-infected persons. J. Immunol. 154: 1418-1431.
24. Hinz, T., D. Wesch, K. Friese, A. Reckziegel, B. Arden, and D. Kabelitz. 1994. T cell receptor γδ repertoire in HIV-1-infected individuals. Eur. J. Immunol. 24:3044-3049.
25. + T cells from leprosy skin lesions. J. Invest. Dermatol. 99:848-852.
26. Jacobs, M.R., and B.F. Haynes. 1991. Increase in TCR γδ lymphocytes in synovia from rheumatoid arthritis patients with active synovitis. J. Clin. Immunol. 12:130-138.
27. Bucht, A., K. Soderstrom, T. Hultman, M. Uhlen, E. Nilsson, R. Kiessling, and A. Gronberg. 1992. T-cell receptor diversity and activation markers in the V 61 subset of rheumatoid synovial fluid and peripheral blood T lymphocytes. Eur. J. Immunol. 22:657-662.
28. Hvas, J., J.R. Oksenberg, R. Fernando, L. Steinman, and C.C. Bernard. 1993. Gamma delta T cell receptor repertoire in brain lesion of patients with multiple sclerosis. J. Neuroimmunol. 46:225-245.
29. Shimonkevitz, R., C. Loburnm, J.A. Burnham, R.S. Murray, and B.L. Kotzin. 1993. Clonal expansion of activated gamma/ delta T cells in recent onset mutiple sclerosis. Proc. Natl. Acad. Sci. USA. 90:923-927.
30. + phenotypes are increased in coeliac disease. Scan. J. Immunol. 30:65-72.
31. Trejdosiewicz, L.K., A. Calabrese, C.J. Smart, D.J. Oakes, P.D. Howdle, J.E. Crabtree, M.S. Losowsky, F. Lancaster, and A.W. Boylston. 1991. γδ T cell receptor-positive cells of human gastrointestinal mucosa: occurence and V region gene expression in helicobacter pylori-associated gastritis, coeliac disease and inflammatory bowel disease. Clin. Exp. Immunol. 84:440-448.
32. Moliterno, R., W. Woan, C. Bentlejewski, J. Qian, A. Zeevi, S. Pham, B.P Griffith, and R.J. Duquesnoy. 1994. Heat shock protein-induced T-lymphocytes propagation from endomyocardial biopsies in heart transplantation. J. Heart Lung Transplant. 14 :329-337.
33. + tumour infiltrating lymphocytes from human lung carcinomas. Eur. J. Immunol. 20:2685-2689.
34. Zocchi, M.R., M. Ferrarini, N. Migone, and G. Casorati. 1994, T-cell receptor V δ gene usage by tumour reactive γδ T lymphocytes infiltrating human lung cancer. Immunology. 81:234-239.
35. Choudhary, A., F. Davodeau, A. Moreau, M.-A. Peyrat, M. Bonneville, and F. Joterau. 1995. Selective lysis of autologous tumor cells by recurrent γδ tumor-infiltrating lymphocytes from renal cell carcinomas. J. Immunol. 154:3932-3940.
36. Jerome, K.R., N. Domenech, and O.J. Finn. 1993. Tumorspecific cytotoxic T cell clones from patients with breast and pancreatic adenocarcinoma recognize EBV-immortalized B cells transfected with polymorphic epithelial mucin complementary DNA. J. Immunol. 151:1654-1662.
37. Elder, E.M., and T.L. Whiteside. 1992. Processing of tumors for vaccine and/or tumor infiltrating lymphocytes. In Manual of Clinical Laboratory Immunology. 4th ed. N R. Rose, E. Conway de Macaio, J.L. Fahey, H. Friedman, and G.M. Penn, editors. American Society for Microbiology, Washington, DC 817-819.
38. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
39. Skeen, M.J., and H.K. Ziegler. 1993. Intercellular interaction and cytokine responsiveness of peritoneal αβ and γδ T cells from listeria-infected mice: Synergistic effects of interleukin 1 and 7 on γδ T cells. J. Exp. Med. 178:985-996.
40. Skeen, M.J., and H.K. Ziegler. 1993. Induction of murine peritoneal gamma/delta T cells and their role in bacterial infection. J. Exp. Med 178:971-984.
41. Takamizawa, M., F. Fagnoni, A. Mehta-Damam, A. Rivas, and E.G. Englman. 1995. Cellular and molecular basis of human γδ T cell activation: role of accessory molecules in allo-activation. J. Clin Invest. 95:296-303.
42. Lynch, D.H., and R.E. Miller. 1994. Interleukin 7 promotes long-term in vitro growth of anti-tumor cytotoxic T lymphocytes with immunotherapeutic efficacy in vivo. J. Exp. Med. 179:31-42.
43. Maenpaa, A., J. Jaaslelainen, O. Carpten, M. Patarroyo, and T. Timonen. 1993. Expression of integrin and other adhesion molecules on NK cells; impact of IL-2 on short- and long-term cultures. Int. J. Cancer. 53:850-855.
44. Chao, C.-C., M. Sandor, and M.O. Dailey. 1994. Expression and regulation of adhesion molecules by γδ T cells from lymphoid tissues and intestinal epithelium. Eur. J. Immunol. 24: 3180-3187.
45. + synovial fluid gamma delta T cells in juvenile rheumatoid arthritis patients express the very early activation marker CD69, but carry the high molecular weight isoform of the leucocyte common antigen CD45RA. Clin. Exp. Immunol. 91:202-211.
46. + T cells in tumour-infiltrating lymphocytes (TIL) of human pancreatic cancer. Clin. Exp. Immunol. 93: 442-447.
47. Nanno, M., H. Seki, G. Mathioudakis, R. Suzuki, K. Itoh, G.G. Ionmdes, S. Suzuki, P.-F. Chen, and C.D. Platsoucas. 1992. γ/δ T cell antigen receptors expressed on tumor-infiltrating lymphocytes from patients with solid tumors. Eur. J. Immunol. 22:679-687.
48. Seki, S., T. Abo, T. Masuda, T. Ohteki, A. Kanno, K. Takeda, H. Rikiishi, H. Nagura, and K. Kumagi. 1990. Identification of activated T cell receptor γδ lymphocytes in the liver of tumor-bearing hosts. J. Clin. Invest. 86:409-415.
49. Fisch, P., K. Oettel, N. Fudim, J.E. Surfus, M. Malkowsky, and P.M. Sondel. 1992. MHC unrestricted cytotoxic and proliferative responses of two distinct human γ/δ T cell subsets to Daudi cells. J. Immunol. 148:2315-2323.
50. Ferrick, D.A., L. Gemmell-Hori., B. Sydora, T. Mulvania, J.M. Penninger, M. Kronenberg, and T.W. Mak. 1994. Tolerance and self-reactivity in V gamma 1.1C gamma 4 transgenic mice. Int. Rev. Immunol. 11:295-304.
51. Garrett, T.A., M.L. Delvy, D.M. Kennedy, L. Lefrancois, L.A. Matis, A.L. Dent, S.M. Hendrick, and J.A. Bluestone. 1992. Mechanisms of self tolerance of γδ T cells in epithelial tissue. J. Exp. Med. 175:65-72.
52. + tumor-infiltrating lymphocytes. J. Immunol. 153:1202-1215.
53. Bernhard, H.J. Karbach, T. Wölfel, S. Stoerkel, C. Huber, J.-H. zum Büschenfelde, and A. Knuth. 1995. Human renal cell carcinomas and normal kidney cells share antigens recognized by HLA-A2 restricted cytotoxic T lymphocyte CTL clones. Int. J. Cancer 59:837-842.
54. Anichim, A., C. Maccalli, R. Mortanni, S. Salvi, A. Mazzocchi, P. Squarcma, M. Herlyn, and G. Parmiani. 1993. Melanoma cells and normal melanocytes share antigens recognized by HLA-A2 restricted cytotoxic T cell clones from melanoma patients. J. Exp. Med. 177:265-272.
55. Faure, F , S. Jitsukawa, C. Miossec, and T. Hercend. 1990. CD1c as a target recognition structure for human T lymphocytes: analysis with peripheral blood γ/δ cells. Eur. J. Immunol. 20:703-706.
56. Havran, W.L., Y.H. Chen, and J.P. Allison. 1991. Recognition of self antigen by skin-derived T cells with invariant γδ antigen receptors. Science (Wash. DC). 52:1430-1432.
57. Kim, H.T., E.L. Nelson, C. Clayberger, M. Sanjanwala, J. Sklar, and A.M. Krensky. 1995. γδ T cell recognition of tumor Ig peptide. J. Immunol. 154:1614-1623.
58. Mahvi, D.M., S.W. Carper, F.K. Storm, S.R. Teal, and P.M. Sondel. 1993. Overexpression of 27-kDa heat-shock protein in MCF-7 breast cancer cells: effects on lymphocyte-mediated killing by natural killer and γδ T cells. Cancer Immunol. Immunother. 37:181-186.
59. Ferrarini, M., S.M. Pupa, M.R. Zocchi, C. Rugarli, and S. Menard. 1994. Distinct pattern of HSP72 and monomeric laminin receptor expression in human lung cancers infiltrated by gamma/delta T lymphocytes. Int. J. Cancer. 57:486-490.
60. Gismondi, A., M. Milella, G. Palmieri, M. Piccoh, L. Frati, and A. Santoni. 1995. Stimulation of protein tyrosine phosphorylation by interaction of NK cells with fibronectin via α4β1 and α5β1. J. Immunol. 154:3128-3137.
61. Ostergaard, H.L, and E.A. Ma. 1995. Fibronectin induces phosphorylation of a 120 kDa protein and synergizes with the T cell receptor to activated cytotoxic T cell clones. Eur. J. Immunol. 25:252-256.
62. Andrew, D.P., C. Berlin, S. Honda, T. Yoshino, A. Hamann, B. Holzmann, P.J. Kilshaw, and B.C. Butcher. 1994. Distinct but overlapping epitopes are involved in alpha 4 and beta 7-mediated adhesion to vascular cell adhesion molecule-1, mucosal addressin-1, fibronectin, and lymphocyte aggregation. J. Immunol. 153:3847-3861.
63. Moretta, A., C. Bottino, E. Ciccone, G. Tambussi, M.C. Mingari, S. Ferrini, G. Casorati, P. Varese, O. Viale, N. Migone, and L. Moretta. 1988. Human peripheral blood lymphocytes bearing T cell receptor γ/β: expression of CD8 differentiation antigen correlates with the expression of the 55-kDa, Cγ2-encoded γ chain. J. Exp. Mid. 168:2349-2354.
64. + T cell clones. Nature (Lond.). 335:642-644.
65. + T cells. Sem. Immunol. 3:119-129.
66. Bucy, R.P., C.-L. Chen, and M.D. Cooper. 1991. Analysis of γδ T cells in the chicken. Sem. Immunol. 3:109-117.
67. + cytotoxic T lymphocyte (CTL) clones recognizing HLA-A2 and HLA-A2 mutants: recognition of TCR-γδ CTL clones is affected by mutations at positions 152 and 156. J. Immunol. 144:4156-4162.
68. Bukowski, J.F., C.T. Morita, Y. Tanaka, B.R. Bloom, M.B. Brenner, and H. Band. 1995. Vγ2Vδ2 TCR dependent recognition of non-peptide antigens and Daudi cells analyzed by TCR gene transfer. J. Immunol. 154:998-1006.
69. Bjorge, L., C.A. Vedeler, E. Ulvestad, and R. Matre. 1994. Expression and function of CD59 on colonic adenocarcinoma cells. Eur. J. Immunol. 24:1597-1603
70. Askenaze, P.W., M. Szczepanik, M. Ptak, V. Paliwal, and W Ptak. 1995. γδ T cells in normal spleen assist immunized αβ T cells in the adoptive transfer of contact sensitivity. Effect of Bordatella pertussis, cyclophosphamide, and antibodies to determinants on suppressor cells. J. Immunol. 154:1644-1653.
71. Ferrick, D.A., M.D. Schrenzel, T. Mulvania, B. Hsieh, W.G. Ferlin, and H. Lepper. 1995. Differential production of interferon-γ and interleukin-4 in response to Th1- and Th2-stimulating pathogens by γδ T cells in vivo. Nature (Lond.). 373: 255-257.
72. Dieli, F., G.L. Asherson, G.C. Romano, G. Sireci, F. Gervasi, and A. Salermo. 1994. IL-4 is essential for the systemic transfer of delayed hypersensitivity by T cell lines. Role of γ/δ cells. J. Immunol. 152:2698-2704.
73. Kaufmann, S.H.E, C. Blum, and S. Yamamoto. 1993 Crosstalk between α/β T cells and γ/δ T cells in vivo: activation of α/β T-cell responses after γ/δ T-cell modulation with the monoclonal antibody GL3. Proc. Natl. Acad. Sci. USA. 90:9620-9624.
74. + T cells provide B cell help. J. Exp. Med. 175: 695-707.