Interleukin-10 increases Th1 cytokine production and cytotoxic potential in human papillomavirus-specific CD8+ cytotoxic T lymphocytes

Journal of Virology

Volumn 74, Issue 10, 2000, Pages 4729-4737

  Santin, Alessandro D ^a,b,c   Hermonat, Paul L ^a   Ravaggi, Antonella ^a,b   Bellone, Stefania ^a,b   Pecorelli, Sergio ^b   Roman, Juan J ^a   Parham, Groesbeck P ^a   Cannon, Martin J ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF BRESCIA   (Italy)

^c UNIVERSITY OF ARKANSAS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD56 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; HLA ANTIGEN CLASS 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; PERFORIN; TRANSFORMING GROWTH FACTOR BETA; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CANCER IMMUNOTHERAPY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; ERYTHROLEUKEMIA CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; PHENOTYPE; PRIORITY JOURNAL; SUPPRESSOR CELL; TH1 CELL; UTERINE CERVIX CANCER; WART VIRUS;

CELLS, CULTURED; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERLEUKIN-10; INTERLEUKIN-2; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PORE FORMING CYTOTOXIC PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TH1 CELLS; TUMOR CELLS, CULTURED; TUMOR VIRUS INFECTIONS; UTERINE CERVICAL NEOPLASMS;

EID: 0033997779     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.10.4729-4737.2000     Document Type: Article

References (55)

1. Aoe, T., Y. Okamoto, and T. Saito. 1995. Activated macrophages induce structural abnormalities of the T cell receptor-CD3 complex. J. Exp. Med. 181:1881-1886.
2. Barth, R. J. J., J. J. Mule, P. J. Spiess, and S. A. Rosenberg. 1991. Interferon gamma and tumor necrosis factor have a role in tumor regression mediated by murine CD8+ tumor infiltrating lymphocytes. J. Exp. Med. 173:647-654.
3. Baxevanis, C. N., and M. Papamichail. 1994. Characterization of an anti-tumor immune response in human cancers and strategies for immunotherapy. Crit. Rev. Oncol. Hematol. 16:157-179.
4. Berman, R. M., T. Suzuki, H. Tahara, P. D. Robbins, S. Narula, and M. T. Lotze. 1996. Systemic administration of cellular interleukin-10 induces an effective, specific, and long lived immune response against established tumors in mice. J. Immunol. 157:231-237.
5. Blazar, B. R., P. A. Taylor, S. Smith, and D. A. Vallera. 1995. Interleukin-10 administration decreases survival in murine recipients of major histocompatibility complex disparate donor bone marrow grafts. Blood 85:842-850.
6. Carson, W. E., M. J. Lindemann, R. Baiocchi, M. Linett, J. C. Tan, C.-C. Chou, S. Narula, and M. A. Caligiuri. 1995. The functional characterization of interleukin-10 receptor expression on human natural killer cells. Blood 85:3577-3585.
7. Cerwenka, A., D. Bevec, O. Majdic, W. Knapp, and W. Holter. 1994. TGF-β1 is a potent inducer of human effector T cells. J. Immunol. 153:4367-4372.
8. Chen, L., P. S. Linsley, and K. E. Hellstrom. 1993. Costimulation of T cells for tumor immunity. Immunol. Today 14:483-486.
9. Chen, L. B., B. Tourvieille, G. F. Burns, F. H. Bach, D. Mathieu-Mahul, M. Sasportes, and A. Bensussan. 1986. Interferon; a cytotoxic T lymphocyte differentiation factor. Eur. J. Immunol. 16:767-773.
10. Chen, W.-F., and A. Zlotnik, 1991. IL-10: a novel cytotoxic T cell differentiation factor. J. Immunol. 147:528-533.
11. Chouaib, S., J. Bertoglio, Y. Blay, C. Marchiol-Fournigault, and D. Fradelizi. 1988. Generation of lymphokine activated killer cells: synergy between tumor necrosis factor and interleukin-2. Proc. Natl. Acad. Sci. USA 85:6875-6880.
12. Cobbold, S., and H. Waldmann. 1998. Infectious tolerance. Curr. Opin. Immunol. 10:518-524.
13. de Smedt, T., M. van Mechelen, G. de Becker, J. Urbain, O. Leo, and M. Moser. 1997. Effects of interleukin-10 on dendritic cell maturation and function. Eur. J. Immunol. 27:1229-1234.
14. de Waal Malefyt, R., J. Haanem, H. Spits, M.-G. Roncarolo, A. te Velde, C. Figdor, K. Johnson, R. Kastelein, H. Yssel, and J. E. de Vries. 1991. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J. Exp. Med. 174:915-921.
15. de Waal Malefyt, R., J. Abrams, B. Bennet, C. Figdor, and J. E. de Vries. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1214.
16. de Waal Malefyt, R., H. Yssel, and J. E. de Vries. 1993. Direct effects of IL-10 on subsets of human CD4† T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation. J. Immunol. 150:4754-4765.
17. Fiorentino, D. F., M. W. Bond, and T. M. Mosmann. 1989. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J. Exp. Med. 170:2081-2095.
18. Gerosa, F., C. Paganin, D. Peritt, F. Paiola, M. T. Scupoli, M. Aste-Amezaga, I. Frank, and G. Trinchieri. 1996. Interleukin-12 primes human CD4 and CD8 T cell clones for high production of both interferon-γ and interleukin10. J. Exp. Med. 183:2559-2565.
19. Giovarelli, M., P. Musiani, A. Modesti, P. Dellabona, G. Casorati, A. Allione, M. Consalvo, F. Cavallo, F. di Pierro, C. de Giovanni, T. Musso, and G. Forni. 1995. Local release of IL-10 by transfected mouse mammary adenocarcinoma cells does not suppress but enhances antitumor reaction and elicits a strong cytotoxic lymphocyte and antibody-dependent immune memory. J. Immunol. 155:3112-3123.
20. Goedegebuure, P. S., M. Zuber, D. L. Leonard-Vidal, U. L. Burger, J. C. Cusack. M. P. Chang, L. M. Douville, and T. J. Eberlein. 1994. Reactivation of murine tumor-infiltrating lymphocytes with solid phase anti-CD3 anti-body: in vitro cytokine production is associated with in vivo efficacy. Surg. Oncol. 3:79-89.
21. Groux, H., M. Bigler, J. E. de Vries, and M. G. Roncaralo. 1996. Interleukin-10 induces a long-term antigen-specific anergic state in human CD4† T cells. J. Exp. Med. 184:19-29.
22. Groux, H., M. Bigler, J. E. de Vries, and M. G. Roncoralo. 1998. Inhibitory and stimulatory effects of IL-10 on human CD8† T cells. J. Immunol. 160:3188-3193.
23. Hilders, C. G. J. M., L. Ras, J. D. H. van Eendenburg, Y. Nooyen, and G. J. Fleuren. 1994. Isolation and characterization of tumor-infiltrating lymphocytes from cervical carcinoma. Int. J. Cancer. 57:805-812.
24. Horiguchi, S., M. Petersson, T. Nakazaua, M. Kanda, A. H. Zea, A. C. Ochoa, and R. Kiessling. 1999. Primary chemically induced tumors induce profound immunosuppression concomitant with apoptosis and alteration in signal transduction in T cells and NK cells. Cancer Res. 59:2950-2956.
25. Jinquan, T., C. Gronhoj-Larsen, B. Gesser, K. Matsushima, and K. Thestrup-Pedersen. 1993. Human IL-10 is a chemoattractant for CD8† T lym-phocytes and an inhibitor of IL-8-induced CD4† T lymphocyte migration. J. Immunol. 151:4545-4551.
26. Kim, J., R. L. Modlin, R. L. Moy, S. M. Dubinett, T. McHugh, B. J. Nickoloff, and K. Uyemura. 1995. IL-10 production in cutaneous basal and squamous cell carcinomas. A mechanism for evading the local T cell immune response. J. Immunol. 155:2240-2247.
27. Kono, K., M. E. Ressing, R. M. P. Brandt, J. M. Melief, R. K. Potkul, B. Andersson, M. Petersson, W. M. Kast, and R. Kiessling. 1996. Decreased expression of signal-transducing ξ chain in peripheral T cells and natural killer cells in patients with cervical cancer. Clin. Cancer Res. 2:1825-1828.
28. Li, W., F. Fu, L. Lu, S. K. Narula, J. J. Fung, A. W. Thomson, and S. Qian. 1998. Systemic administration of anti-interleukin-10 antibody prolongs organ allograft survival in normal and presensitized recipients. Transplantation 66:1587-1592.
29. MacNeil, I. A., T. Suda, K. W. Moore, T. R. Mosmann, and A. Zlotnik. 1990. IL-10, a novel growth cofȧctor for mature and immature T cells. J. Immunol. 145:4167-4173.
30. Matsuda, M., F. Salazar, M. Petersson, G. Masucci, J. Hansson, P. Pisa, Q.-J. Zhang, M. G. Masucci, and R. Kiessling. 1994. Interleukin 10 pretreatment protects target cells from tumor-and allo-specific cytotoxic T cells and downregulates HLA class 1 expression. J. Exp. Med. 180:2371-2376.
31. Mehrotra, P. T., D. Wu, J. A. Crim, H. S. Mostowski, and J. P. Siegel. 1993. Effects of 1L-12 on the generation of cytotoxic activity in human CD8† T lymphocytes. J. Immunol. 151:2444-2450.
32. Mescher, M. F. 1992. Surface contact requirements for activation of cytotoxic T lymphocytes. J. Immunol. 149:2402-2405.
33. Mischer, S., T. L. Whiteside, S. Carrel, and V. Fliedner. 1986. Functional properties of tumor infiltrating and blood lymphocytes in patients with solid tumors: effects of tumor cells and their supernatants on proliferative responses of lymphocytes. J. Immunol. 136:1899-1907.
34. Mizoguchi, H., J. J. O'Shea, D. L. Longo, C. M. Loeffler, D. W. McVicar, and A. C. Ochoa. 1992. Alteration in signal transduction molecules in T lymphocytes from tumor bearing mice. Science 258:1795-1798.
35. Moore, K. W., A. O'Garra, R. de Vaal Malefyt, P. Vieira, and T. R. Mosmann. 1993. Interleukin-10. Annu. Rev. Immunol. 11:165-190.
36. Pittet, M. J., D. E. Speiser, D. Valmori, J.-C. Cerottini, and P. Romero. 2000. Cytolytic effector function in human circulating CD8† T cells closely correlated with CD56 surface expression. J. Immunol. 164:1148-1152.
37. Qian, S., W. Li, Y. Li, F. Fu, L. Lu, J. J. Fung, and A. W. Thomson. 1996. Systemic administration of cellular interleukin-10 can exacerbate cardiac allograft rejection in mice. Transplantation 62:1709-1713.
38. Renner, C., S. Ohnesorge, G. Held, S. Bauer, W. Jung, J.-P. Pfitzenmeier, and M. Pfreundschuh. 1996. T cells from patients with Hodgkin's disease have a defective T-cell receptor ξ chain expression that is reversible by T-cell stimulation with CD3 and CD28. Blood 88:236-241.
39. Salazar-Onfray, F., J. Charo, S. Freland, G. Noffz, Z. Qin, T. Blankenstein, H.-G. Ljunggren, and R. Kiessling. 1997. Down-regulation of the expression and function of the transporter associated with antigen processing in murine tumor cell lines expressing IL-10. J. lmmunol. 159:3195-3202.
40. Santin, A. D., P. L. Hermonat, A. Ravaggi, M. Chiriva-Internati, D. Zhan, S. Pecorelli, G. P. Parham, and M. J. Cannon. 1999. Induction of human papillomavirus-specific CD4† and CD8† lymphocytes by E7-pulsed autologous dendritic cells in patients with human papillomavirus type 16-and 18-positive cervical cancer. J. Virol. 73:5402-5410.
41. Santin, A. D., P. L. Hermonat, A. Ravaggi, S. Bellone, C. Cowan, S. Korourian, S. Pecorelli, M. J. Cannon, and G. P. Parham. 2000. Development, characterization, and distribution of adoptively transferred peripheral blood lymphocytes primed by human papillomavirus 18 E7-pulsed autologous dendritic cells in a patient with metastatic adenocarcinoma of the uterine cervix. Eur. J. Gynaecol. Oncol. 21:17-23.
42. Santin, A. D., P. L. Hermonat, A. Ravaggi, M. Chiriva-Internati, M. J. Cannon, J. C. Hiserod, S. Pecorelli, and G. P. Parham. 1999. Expression of surface antigens during the differentiation of human dendritic cells vs macrophages from blood monocytes in vitro. Immunobiology 200:187-204.
43. Santin, A. D., P. L. Hermonat, A. Ravaggi, M. J. Cannon, S. Pecorelli, and G. P. Parham. 1999. Secretion of vascular endothelial growth factor in adenocarcinoma and squamous cell carcinoma of uterine cervix. Obstet. Gynecol. 94:78-82.
44. Slaveley-O'Carrol, K., E. Sotomayor, J. Montgomery, I. Borrello, L. Hwang, S. Fein, D. Pardoll, and H. Levitsky. 1998. Induction of antigen-specific T cell anergy: an early event in the course of tumor progression. Proc. Natl. Acad. Sci. USA 95:1178-1183.
45. Stewart, J. P., and C. M. Rooney. 1992. The interleukin-10 homolog encoded by Epstein-Barr virus enhances the reactivation of virus-specific cytotoxic T cell and HLA-unrestricted killer cell responses. Virology 191:773-782.
46. Stuntman, O. Immunodepression and malignancy. 1975. Adv. Cancer Res. 22:261-272.
47. Suzuki, T., H. Tahara, S. Narula, K. W. Moore, P. D. Robbins, and M. T. Lotze. 1995. Viral interleukin-10 (IL-10), the human herpes virus 4 cellular IL-10 homologue, induces local anergy to allogeneic and syngeneic tumors. J. Exp. Med. 182:477-486.
48. Taga, K., H. Mostowski, and G. Tosato. 1993. Human interleukin-10 can directly inhibit T-cell growth. Blood 81:2964-2971.
49. Takashi, N., K. Iwakabe, M. Sekimoto, Y. Ohrni, T. Yahata, M. Nakui, T. Sato, S. Habu, H. Tashiro, M. Sato, and A. Ohta. 1999. Distinct role of antigen-specific T helper type 1 (Th1) and Th2 cells in tumor eradication in vivo. J. Exp. Med. 190:617-624.
50. Tartour, E., S. Latour, C. Mathiot, N. Thiounn, V. Mosseri, I. Joyeux, C. Dubois D'Enghien, R. Lee, B. Debre, and W. H. Fridman. 1995. Variable expression of CD3-Cξ chain in tumor infiltrating lymphocytes (TIL) derived from renal-cell carcinoma: relationship with TIL phenotype and function. Int. J. Cancer 63:205-212.
51. Trinchieri, G. 1993. Interleukin-12 and its role in the generation of Th1 cells. Immunol. Today 14:335-339.
52. Walter, E. A., P. D. Greenberg, M. J. Gilbert, R. J. Finch, K. S. Watanabe, E. D. Thomas, and S. R. Riddel. 1995. Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cel) clones from the donor. N. Engl. J. Med. 333:1038-1044.
53. Whal, S. M. 1994. Transforming growth factor β: the good, the bad, and the ugly. J. Exp. Med. 180:1587-1590.
54. Wogensen, L., M.-S. Lee, and N. Sarvetnick. 1994. Production of interleukin-10 by islet cells accelerates immune-mediated destruction of β cells in nonobese diabetic mice. J. Exp. Med. 179:1379-1384.
55. Zheng, L. M., D. M. Ojcius, F. Graud, C. Roth, E. Maxwell, Z. Li, H. Rong, J. Chen, X. Y. Wang, J. J. Catino, and I. King. 1996. Interleukin-10 inhibits tumor metastasis through an NK cell-dependent mechanism. J. Exp. Med. 184:579-584.