Combined IL-21-primed polyclonal CTL plus CTLA4 blockade controls refractory metastatic melanoma in a patient

Journal of Experimental Medicine

Volumn 213, Issue 7, 2016, Pages 1133-1139

  Chapuis, Aude G ^a   Lee, Sylvia M ^a,b   Thompson, John A ^b   Roberts, Ilana M ^a,e   Margolin, Kim A ^b,f   Bhatia, Shailender ^b   Sloan, Heather L ^a,g   Lai, Ivy ^a,h   Wagener, Felecia ^a   Shibuya, Kendall ^a,i   Cao, Jianhong ^a   Wolchok, Jedd D ^c   Greenberg, Philip D ^a,d   Yee, Cassian ^a,h  

^a USA   (United States)

^b UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

^f CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^g SEATTLE CANCER CARE ALLIANCE   (United States)

^h UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

ⁱ WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DENILEUKIN DIFTITOX; INTERLEUKIN 21; IPILIMUMAB; CTLA4 PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE;

ADULT; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER PATIENT; CANCER REGRESSION; CASE REPORT; CELL THERAPY; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DRUG MEGADOSE; FIRST IN HUMAN STUDY; HUMAN; LOW DRUG DOSE; MALE; METASTATIC MELANOMA; MIDDLE AGED; PRIORITY JOURNAL; ADOPTIVE TRANSFER; CD8+ T LYMPHOCYTE; CLINICAL TRIAL; FEMALE; IMMUNOLOGY; MELANOMA; METASTASIS; PROCEDURES; TRANSPLANTATION;

ADOPTIVE TRANSFER; CD8-POSITIVE T-LYMPHOCYTES; CTLA-4 ANTIGEN; FEMALE; HUMANS; INTERLEUKINS; MALE; MELANOMA; MIDDLE AGED; NEOPLASM METASTASIS;

EID: 84977626639     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20152021     Document Type: Article

References (27)

1. Chapuis, A.G., J.A. Thompson, K.A. Margolin, R. Rodmyre, I.P. Lai, K. Dowdy, E.A. Farrar, S. Bhatia, D.E. Sabath, J. Cao, et al. 2012. Transferred melanoma-specific CD8+ T cells persist, mediate tumor regression, and acquire central memory phenotype. Proc. Natl. Acad. Sci. USA. 109:4592-4597. http://dx.doi.org/10.1073/pnas.1113748109
2. Chapuis, A.G., G.B. Ragnarsson, H.N. Nguyen, C.N. Chaney, J.S. Pufnock, T.M. Schmitt, N. Duerkopp, I.M. Roberts, G.L. Pogosov, W.Y. Ho, et al. 2013. Transferred WT1-reactive CD8+ T cells can mediate antileukemic activity and persist in post-transplant patients. Sci. Transl. Med. 5:174ra27. http://dx.doi.org/10.1126/scitranslmed.3004916
3. Cui, W., Y. Liu, J.S. Weinstein, J. Craft, and S.M. Kaech. 2011. An interleukin-21-interleukin-10-STAT3 pathway is critical for functional maturation of memory CD8+ T cells. Immunity. 35:792-805. http://dx.doi.org/10.1016/j.immuni.2011.09.017
4. Freeman, G.J., A.J. Long, Y. Iwai, K. Bourque, T. Chernova, H. Nishimura, L.J. Fitz, N. Malenkovich, T. Okazaki, M.C. Byrne, et al. 2000. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192:1027-1034. http://dx.doi.org/10.1084/jem.192.7.1027
5. Ho, W.Y., H.N. Nguyen, M. Wolfl, J. Kuball, and P.D. Greenberg. 2006. In vitro methods for generating CD8+ T-cell clones for immunotherapy from the naïve repertoire. J. Immunol. Methods. 310:40-52. http://dx.doi.org/10.1016/j.jim.2005.11.023
6. Hodi, F.S., S.J. O'Day, D.F. McDermott, R.W. Weber, J.A. Sosman, J.B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J.C. Hassel, et al. 2010. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363:711-723. http://dx.doi.org/10.1056/NEJMoa1003466
7. Kvistborg, P., D. Philips, S. Kelderman, L. Hageman, C. Ottensmeier, D. Joseph-Pietras, M.J. Welters, S. van der Burg, E. Kapiteijn, O. Michielin, et al. 2014. Anti-CTLA-4 therapy broadens the melanoma-reactive CD8+ T cell response. Sci. Transl. Med. 6:254ra128. http://dx.doi.org/10.1126/scitranslmed.3008918
8. Li, Y., M. Bleakley, and C. Yee. 2005. IL-21 influences the frequency, phenotype, and affinity of the antigen-specific CD8 T cell response. J. Immunol. 175:2261-2269. http://dx.doi.org/10.4049/jimmunol.175.4.2261
9. Papagno, L., J.R. Almeida, E. Nemes, B. Autran, and V. Appay. 2007. Cell permeabilization for the assessment of T lymphocyte polyfunctional capacity. J. Immunol. Methods. 328:182-188. http://dx.doi.org/10.1016/j.jim.2007.09.001
10. Pollack, S.M., R.L. Jones, E.A. Farrar, I.P. Lai, S.M. Lee, J. Cao, V.G. Pillarisetty, B.L. Hoch, A. Gullett, M. Bleakley, et al. 2014. Tetramer guided, cell sorter assisted production of clinical grade autologous NY-ESO-1 specific CD8(+) T cells. J. Immunother. Cancer. 2:36. http://dx.doi.org/10.1186/s40425-014-0036-y
11. Prieto, P.A., J.C. Yang, R.M. Sherry, M.S. Hughes, U.S. Kammula, D.E. White, C.L. Levy, S.A. Rosenberg, and G.Q. Phan. 2012. CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma. Clin. Cancer Res. 18:2039-2047. http://dx.doi.org/10.1158/1078-0432.CCR-11-1823
12. Restifo, N.P., M.E. Dudley, and S.A. Rosenberg. 2012. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12:269-281. http://dx.doi.org/10.1038/nri3191
13. Ribas, A., J.M. Timmerman, L.H. Butterfield, and J.S. Economou. 2003. Determinant spreading and tumor responses after peptide-based cancer immunotherapy. Trends Immunol. 24:58-61. http://dx.doi.org/10.1016/S1471-4906(02)00029-7
14. Riddell, S.R., K.S. Watanabe, J.M. Goodrich, C.R. Li, M.E. Agha, and P.D. Greenberg. 1992. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science. 257:238-241. http://dx.doi.org/10.1126/science.1352912
15. Robins, H.S., P.V. Campregher, S.K. Srivastava, A. Wacher, C.J. Turtle, O. Kahsai, S.R. Riddell, E.H. Warren, and C.S. Carlson. 2009. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood. 114:4099-4107. http://dx.doi.org/10.1182/blood-2009-04-217604
16. Robins, H., C. Desmarais, J. Matthis, R. Livingston, J. Andriesen, H. Reijonen, C. Carlson, G. Nepom, C. Yee, and K. Cerosaletti. 2012. Ultra-sensitive detection of rare T cell clones. J. Immunol. Methods. 375:14-19. http://dx.doi.org/10.1016/j.jim.2011.09.001
17. Schadendorf, D., F.S. Hodi, C. Robert, J.S. Weber, K. Margolin, O. Hamid, D. Patt, T.T. Chen, D.M. Berman, and J.D. Wolchok. 2015. Pooled Analysis of Long-Term Survival Data From Phase II and Phase III Trials of Ipilimumab in Unresectable or Metastatic Melanoma. J. Clin. Oncol. 33:1889-1894. http://dx.doi.org/10.1200/JCO.2014.56.2736
18. Scheibenbogen, C., P. Romero, L. Rivoltini, W. Herr, A. Schmittel, J.C. Cerottini, T. Woelfel, A.M. Eggermont, and U. Keilholz. 2000. Quantitation of antigen-reactive T cells in peripheral blood by IFNgamma-ELI SPOT assay and chromium-release assay: a four-centre comparative trial. J. Immunol. Methods. 244:81-89. http://dx.doi.org/10.1016/S0022-1759(00)00257-X
19. Schreiber, R.D., L.J. Old, and M.J. Smyth. 2011. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science. 331:1565-1570. http://dx.doi.org/10.1126/science.1203486
20. Sharma, P., K. Wagner, J.D. Wolchok, and J.P. Allison. 2011. Novel cancer immunotherapy agents with survival benefit: recent successes and next steps. Nat. Rev. Cancer. 11:805-812. http://dx.doi.org/10.1038/nrc3153
21. Topp, M.S., S.R. Riddell, Y. Akatsuka, M.C. Jensen, J.N. Blattman, and P.D. Greenberg. 2003. Restoration of CD28 expression in CD28-CD8+ memory effector T cells reconstitutes antigen-induced IL-2 production. J. Exp. Med. 198:947-955. http://dx.doi.org/10.1084/jem.20021288
22. Unsoeld, H., S. Krautwald, D. Voehringer, U. Kunzendorf, and H. Pircher. 2002. Cutting edge: CCR7+ and CCR7-memory T cells do not differ in immediate effector cell function. J. Immunol. 169:638-641. http://dx.doi.org/10.4049/jimmunol.169.2.638
23. Wallen, H., J.A. Thompson, J.Z. Reilly, R.M. Rodmyre, J. Cao, and C. Yee. 2009. Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8 T cells in patients with metastatic melanoma. PLoS One. 4:e4749. http://dx.doi.org/10.1371/journal.pone.0004749
24. Wolchok, J.D., A. Hoos, S. O'Day, J.S. Weber, O. Hamid, C. Lebbé, M. Maio, M. Binder, O. Bohnsack, G. Nichol, et al. 2009. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin. Cancer Res. 15:7412-7420. http://dx.doi.org/10.1158/1078-0432.CCR-09-1624
25. Wolchok, J.D., J.S. Weber, M. Maio, B. Neyns, K. Harmankaya, K. Chin, L. Cykowski, V. de Pril, R. Humphrey, and C. Lebbé. 2013. Four-year survival rates for patients with metastatic melanoma who received ipilimumab in phase II clinical trials. Ann. Oncol. 24:2174-2180. http://dx.doi.org/10.1093/annonc/mdt161
26. Wölfl, M., K. Merker, H. Morbach, S.W. Van Gool, M. Eyrich, P.D. Greenberg, and P.G. Schlegel. 2011. Primed tumor-reactive multifunctional CD62L+ human CD8+ T cells for immunotherapy. Cancer Immunol. Immunother. 60:173-186. http://dx.doi.org/10.1007/s00262-010-0928-8
27. Yee, C., J.A. Thompson, D. Byrd, S.R. Riddell, P. Roche, E. Celis, and P.D. Greenberg. 2002. Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: in vivo persistence, migration, and antitumor effect of transferred T cells. Proc. Natl. Acad. Sci. USA. 99:16168-16173. http://dx.doi.org/10.1073/pnas.242600099