Peripheral burst of tumor-specific cytotoxic T lymphocytes and infiltration of metastatic lesions by memory CD8+ T cells in melanoma patients receiving interleukin 12

Cancer Research

Volumn 60, Issue 13, 2000, Pages 3559-3568

  Mortarini, Roberta ^a   Borri, Alessandra ^a   Tragni, Gabrina ^a   Bersani, Ilaria ^a   Vegetti, Claudia ^a   Bajetta, Emilio ^a   Pilotti, Silvana ^a   Cerundolo, Vincenzo ^b   Anichini, Andrea ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; RECOMBINANT INTERLEUKIN 12; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CLINICAL ARTICLE; CYTOTOXIC T LYMPHOCYTE; HLA SYSTEM; HUMAN; HUMAN CELL; LYMPHOCYTIC INFILTRATION; MELANOMA; MEMORY CELL; METASTASIS; PRIORITY JOURNAL;

ANTIGENS, CD18; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; HLA-A ANTIGENS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGIC MEMORY; INTERLEUKIN-12; LYMPHATIC METASTASIS; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; NEOPLASM METASTASIS; NEOPLASM PROTEINS; PILOT PROJECTS; RECOMBINANT PROTEINS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0034234287     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (47)

1. Trinchieri, G. Interleukin-12: a cytokine at the interface of inflammation and immunity. Adv. Immunol., 70: 83-243, 1998.
2. Gately, M. K., Renzetti, L. M., Magram, J., Stern, A. S., Adorini, L., Gubler U., and Presky, D. H. The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu. Rev. Immunol., 16: 495-521, 1998.
3. Sgadari, C., Angiolillo, A. L., and Tosato, G. Inhibition of angiogenesis by interleukin-12 is mediated by the interferon-inducible protein 10. Blood, 87: 3877-3882, 1996.
4. Brunda, M. J., Luistro, L., Warrier, R. R., Wright, R. B., Hubbard, B. R., Murphy, M., Wolf, S. F., and Gately, M. K. Antitumor and antimetaslatic activity of interleukin 12 against murine tumors. J. Exp. Med., 178: 1223-1230, 1993.
5. Nastala, C. L., Edington, H. D., McKinney, T. G., Tahara, H., Nalesnik, M. A., Brunda, M. J., Gately, M. K., Wolf, S. F., Schreiber, R. D., Storkus W. J., and Lotze, M. T. Recombinant IL-12 administration induces tumor regression in association with IFN-γ production. J. Immunol., 153: 1697-1706, 1994.
6. Mu, J., Zou, J. P., Yamamoto, N., Tsutsui, T., Tai, X. G., Kobayashi, M., Herrmann, S., Fujiwara, H., and Hamaoka, T. Administration of recombinant interleukin 12 prevents outgrowth of tumor cells metastasizing spontaneously to lung and lymph nodes. Cancer Res., 55: 4404-4408, 1995.
7. Boggio, K., Nicoletti, G., Di Carlo, E., Cavallo, F., Landuzzi, L., Melani, C. Giovarelli, M., Rossi, I., Nanni, P., De Giovanni, C., Bouchard, P., Wolf, S., Modesti, A., Musiani, P., Lollini, P. L., Colombo, M. P., and Fomi, G. Interleukin-12-mediated prevention of spontaneous mammary adenocarcinomas in two lines of Her-2/neu transgenic mice. J. Exp. Med., 188: 589-596, 1998.
8. Tahara, H., Zeh, H, J., III, Storkus, W. J., Pappo, I., Watkins, S. C., Gubler, U., Wolf, S. F., Robbins, P. D., and Lotze, M. T. Fibroblasts genetically engineered to secrete interleukin 12 can suppress tumor growth and induce antitumor immunity to a murine melanoma in vivo. Cancer Res., 54: 182-189, 1994.
9. Tahara, H., Zitvogel, L., Storkus, W. J., Zeh, H. J., III, McKinney, T. G., Schreiber, R. D., Gubler, U., Robbins, P. D., and Lotze, M. T. Effective eradication of established murine tumors with IL-12 gene therapy using a polycistronic retroviral vector. J. Immunol., 154: 6466-6474, 1995.
10. Caruso, M., Pham-Nguyen, K., Kwong, Y. L., Xu, B., Kosai, K. I., Finegold, M., Woo, S. L., and Chen, S. H. Adenovirus-mediated interleukin-12 gene therapy for metastatic colon carcinoma. Proc. Natl. Acad. Sci. USA, 93: 11302-11306, 1996.
11. Bramson, J. L., Hitt, M., Addison, C. L., Muller, W. J., Gauldie, J., and Graham, F. L. Direct intratumoral injection of an adenovirus expressing inlerleukin-12 induces regression and long-lasting immunity that is associated with highly localized expression of interleukin-12. Hum. Gene Ther. 7: 1995-2002, 1996.
12. Chen, L., Chen, D., Block, E., O'Donnell, M., Kufe, D. W., and Clinton, S. K. Eradication of murine bladder carcinoma by intratumor injection of a bicistronic adenoviral vector carrying cDNAs for the IL-12 heterodimer and its inhibition by the IL-12 p40 subunit homodimer. J. Immunol., 159: 351-359, 1997.
13. Atkins, M. B., Robertson, M. J., Gordon, M., Lotze, M. T., DeCoste, M., DuBois, J. S., Ritz, J., Sandler, A. B., Edington, H. D., Garzone, P. D., Mier, J. W., Canning, C. M., Battiato, L., Tahara, H., and Sherman, M. L. Phase I evaluation of intravenous recombinant human interleukin 12 in patients with advanced malignancies. Clin. Cancer Res., 3: 409-417, 1997.
14. Bajetta, E., Del Vecchio, M., Mortarini, R., Nadeau, R., Rakhit, A., Rimassa, L., Fowst, C., Borri, A., Anichini, A., and Parmiani, G. Pilot study of subcutaneous recombinant human interleukin 12 in metastatic melanoma. Clin. Cancer Res., 4: 75-85, 1998.
15. Motzer, R. J., Rakhit, A., Schwartz, L. H., Olencki, T., Malone, T. M., Sandstrom, K., Nadeau, R., Parmar, H., and Bukowski, R. Phase I trial of subcutaneous recombinant human interleukin-12 in patients with advanced renal cell carcinoma. Clin. Cancer Res., 4: 1183-1191, 1998.
16. Leonard, J. P., Sherman, M. L., Fisher, G. L., Buchanan, L. J., Larsen, G., Atkins, M. B., Sosman, J. A., Dutcher, J. P., Vogelzang, N. J., and Ryan, J. L. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-γ production. Blood, 90: 2541-2548, 1997.
17. Robertson, M. J., Cameron, C., Atkins, M. B., Gordon, M. S., Lotze, M. T., Sherman, M. L., and Ritz, J. Immunological effects of interleukin 12 administered by bolus intravenous injection in patients with cancer. Clin. Cancer Res., 5: 9-16, 1999.
18. Rook, A. H., Wood, G. S., Yoo, E. K., Elenitsas, R., Kao, D. M. F., Sherman, M. L., Wilmer, W. K., Rockwell, K. A., Shane, R. B., Lessin, S. R., and Vonderheid, E. C. Interleukin-12 therapy of cutaneous T-cell lymphoma induces lesion regression and cytotoxic T cell responses. Blood, 94: 902-908, 1999.
19. Anichini, A., Mortarini, R., Maccalli, C., Squarcina, P., Fleischhauer, K., Mascheroni, L., and Parmiani, G. Cytotoxic T cells directed to tumor antigens not expressed on normal melanocytes dominate HLA-A*0201-restricted immune repertoire to melanoma. J. Immunol., 156: 208-217, 1996.
20. Maccalli, C., Pisarra, P., Vegetti, C., Sensi, M., Parmiani, G., and Anichini, A. Differential loss of T cell signaling molecules in metastatic melanoma patients' T lymphocyte subsets expressing distinct TCR variable regions. J. Immunol., 163: 6912-6923, 1999.
21. Lakhanpal, S., Gonchoroff, N. J., Katzmann, J. A., and Handwerger, B. S. A flow cytofluorometric double staining technique for simultaneous determination of human mononuclear cell surface phenotype and cell cycle phase. J. Immunol. Methods. 96: 35-40, 1987.
22. Anichini. A., Molla, A., Mortarini, R., Tragni, G., Bersani, I., Di Nicola, M., Gianni, A. M., Pilotti, S., Dunbar, R., Cerundolo, V., and Parmiani, G. An expanded peripheral T cell population to a CTL-defined melanocyte-specific antigen in metastatic melanoma patients impacts on generation of peptide-specific CTL, but does not overcome tumor escape from immune surveillance in metastatic lesions. J. Exp. Med., 190: 651-668, 1999.
23. Ogg, G. S., Dunbar, P. R., Romero, P., Chen, J. L., and Cerundolo, V. High frequency of skin-homing melanocyte-specific cytotoxic T lymphocytes in autoimmune vitiligo. J. Exp. Med., 188: 1203-1208, 1998.
24. Valmori, D., Fontaneau, J. F., Lizana, C. M., Gervois, N., Lienard, D., Rimoldi, D., Jongeneel, V., Jotereau, F., Cerottini J. C., and Romero, P. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/Mart-1 immunodominant peptide analogues. J. Immunol., 160: 1750-1758, 1998.
25. 27-35-specific CTL from PBL of melanoma patients with low frequency of CTL precursors. Cancer Res., 57: 5534-5541, 1997.
26. Kawakami, Y., Eliyahu, S., Sakaguchi, K., Robbins, P. F., Yannelli, J. R., Appella, E., and Rosenberg, S. A. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2 restricted tumor infiltrating lymphocytes. J. Exp. Med., 180: 347-352, 1994.
27. Parham, P., Barnstable, C. J., and Bodmer, W. F. Use of monoclonal antibody (W6/32) in structural studies of HLA-A, -B, -C antigens. J. Immunol., 123: 342-349, 1979.
28. Clark, W. H., Jr., Elder, D. E., Guerry IV, D., Braitman, L. E., Trock, B. J., Schultz, D., Synnestvedt, M., and Halpern, A. C. Model predicting survival in stage I melanoma based on tumor progression. J. Natl. Cancer Inst., 81: 1893-1904, 1989.
29. + T lymphocytes. J. Immunol., 144: 574-582, 1990.
30. 1ck in T-cells infiltrating human renal cell carcinoma. Cancer Res., 53: 5613-5616, 1993.
31. Zea, A. H., Cutri, B. D., Longo, D. L., Alvord, W. G., Strobl, S. L., Mizoguchi, H., Creekmore, S. P., O'Shea, J. J., Powers, G. C., Urba, W. J., and Ochoa, A. C. Alterations in T cell receptor and signal transduction molecules in melanoma patients. Clin. Cancer Res., I: 1327-1335, 1995.
32. Van Parijs, L., Perez, V. L., Biuckians, A., Maki, R. G., London, C. A., and Abbas, A.K. Role of interleukin 12 and costimulators in T cell anergy in vivo. J. Exp. Med., 186: 1119-1128, 1997.
33. Ushio, H. R., Tsuji, F., Szczepanik, M., Kawamoto, K., Matsuda, H., and Askenase, P. W. IL-12 reverses established antigen-specific tolerance of contact sensitivity by affecting costimulatory molecules B7-I (CD80) and B7-2 (CD86). J. Immunol., 160: 2080-2088, 1998.
34. + T cell anergy in vitro. J. Exp. Med., 187: 89-96, 1998.
35. Gollob, J. A., Schnipper, C. P., Orsini, E., Murphy, E., Daley, J. F., Lazo, S. B., Frank, D. A., Neuberg, D., and Ritz, J. Characterization of a novel subset of CD8(+) T cells that expands in patients receiving interleukin-12. J. Clin. Investig., 102: 561-575, 1998.
36. 1 into syngeneic mice. Cancer Res., 58: 5795-5802, 1998.
37. Fernandez, N. C., Levraud, J. P., Haddada, H., Perricaudet, M., and Kourilsky, P. Higher frequency of specific CD8+ T cells in the tumor and blood is associated with efficient local IL-12 gene therapy of cancer. J. Immunol., 162: 609-617, 1999.
38. + T cells. J. Immunol., 162: 3256-3262, 1999.
39. Ogawa, M., Tsuitsui, T., Zou, J. P., Mu, J., Wijesuriya, R., Yu, W. G., Hermann, S., Kubo, T., Fujiwara, H., and Hamaoka, T. Enhanced induction of very late antigen 4/lymphocyte function-associated antigen 1-dependent T cell migration to tumor sites after administration of interleukin 12. Cancer Res., 57: 2216-2222, 1997.
40. Myers, K. J., Eppihimer, M. J., Hall, L., and Wolitzky, B. Interleukin-12-induced adhesion molecule expression in murine liver. Am. J. Pathol., 152: 457-468, 1998.
41. Fogler, W. E., Volker, K., Watanabe, M., Wigginton, J. M., Roessler, P., Brunda, M. J., Ortaldo, J. R., and Wiltrout, R. H. Recruitment of hepatic NK cells by IL-12 is dependent on IFN-γ and VCAM-1 and is rapidly down-regulated by a mechanism involving T cells and expression of Fas. J. Immunol., 161: 6014-6021, 1998.
42. Leung, D. Y., Gately, M., Trumble, A., Ferguson-Darnell, B., Schlievert, P. M., and Picker, L. J. Bacterial superantigens induce T cell expression of the skin-selective homing receptor, the cutaneous lymphocyte-associated antigen, via stimulation of interleukin-12 production. J. Exp. Med., 181: 747-753, 1995.
43. Santamaria Babi, L. F., Moser, R., Perez Soler, M. T., Picker, L. J., Blaser, K., and Hauser, C. Migration of skin-homing T cells across cytokine-activated human endothelial cell layers involves interaction of the cutaneous lymphocyte-associated antigen (CLA), the very late antigen-4 (VLA-4), and the lymphocyte function-associated antigen-1 (LFA-1). J. Immunol. 154: 1543-1550, 1995.
44. Picker, L. J., Treer, J. R., Ferguson-Darnell, B. B., Collins, P. A., Bergstresser, P. R., and Terstappen, L. W. Control of lymphocyte recirculation in man. II. Differential regulation of the cutaneous lymphocyte-associated antigen, a tissue-selective homing receptor for skin-homing T cells. J. Immunol., 150: 1122-1136, 1993.
45. Cavallo, F., Signorelli, P., Giovarelli, M., Musiani, P., Modesti, A., Brunda, M. J., Colombo, M. P., and Forni, G. Antitumor efficacy of adenocarcinoma cells engineered to produce interleukin 12 (IL-12) or other cytokines compared with exogenous IL-12. J. Natl. Cancer Inst., 89: 1049-1058, 1997.
46. Rakhit, A., Yeon, M. M., Ferrante, J., Fettner, S., Nadeau, R., Motzer, R., Bukowski, R., Carvajal, D. M., Wilkinson, V. L., Presky, D. H., Magram, J., and Gately, M. K. Down-regulation of the pharmacokinetic-pharmacodynamic response to interleukin-12 during long-term administration to patients with renal cell carcinoma and evaluation of the mechanism of this "adaptive response" in mice. Clin. Pharmacol. Ther., 65:615-629, 1999.
47. Koblish, H. K., Hunter, C. A., Wysocka M., Trinchieri, G., and Lee, W. M. Immune suppression by recombinant inlerleukin (rIL)-12 involves interferon y induction of nitric oxide synthase 2 (iNOS) activity: inhibitors of NO generation reveal the extent of rIL-12 vaccine adjuvant effect. J. Exp. Med., 188: 1603-1610, 1998.