Durable complete response from metastatic melanoma after transfer of autologous T cells recognizing 10 mutated tumor antigens

Cancer Immunology Research

Volumn 4, Issue 8, 2016, Pages 669-678

  Prickett, Todd D ^a   Crystal, Jessica S ^a   Cohen, Cyrille J ^b   Pasetto, Anna ^a   Parkhurst, Maria R ^a   Gartner, Jared J ^a   Yao, Xin ^a   Wang, Rong ^c   Gros, Alena ^a   Li, Yong F ^a   El Gamil, Mona ^a   Trebska McGowan, Kasia ^a   Rosenberg, Steven A ^a   Robbins, Paul F ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b BAR ILAN UNIVERSITY   (Israel)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CELL DNA; CENPLACEL L; GENOMIC DNA; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEROXIREDOXIN 3; TUMOR ANTIGEN; EPITOPE; T LYMPHOCYTE RECEPTOR;

ADULT; ARTICLE; AUTOTRANSPLANTATION; B LYMPHOCYTE; CANCER COMBINATION CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER SURGERY; CELL TRANSFER; CLINICAL EFFECTIVENESS; EXOME; GENE SEQUENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG LESION; LUNG METASTASIS; LYMPH NODE METASTASIS; LYMPHOCYTE TRANSFER; MALE; MEDICAL HISTORY; METASTATIC MELANOMA; MIDDLE AGED; MULTIPLE CANCER; RNA SEQUENCE; SEQUENCE ANALYSIS; SOMATIC MUTATION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THERAPY EFFECT; TREATMENT RESPONSE; TUMOR CELL; TUMOR REGRESSION; WHOLE BODY RADIATION; WILD TYPE; ADOPTIVE IMMUNOTHERAPY; ANIMAL; CASE REPORT; CELL LINE; GENETICS; IMMUNOLOGY; MELANOMA; METABOLISM; MULTIMODALITY CANCER THERAPY; MUTATION; TREATMENT OUTCOME; X-RAY COMPUTED TOMOGRAPHY;

ANIMALS; ANTIGENS, NEOPLASM; CELL LINE; COMBINED MODALITY THERAPY; EPITOPES, T-LYMPHOCYTE; EXOME; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MALE; MELANOMA; MIDDLE AGED; MUTATION; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES; TOMOGRAPHY, X-RAY COMPUTED; TREATMENT OUTCOME;

EID: 84985995114     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-15-0215     Document Type: Article

References (38)

1. Atkins MB, Lotze MT, Dutcher JP, Fisher RI, Weiss G, Margolin K, et al. Highdose recombinant interleukin 2 therapy for patients with metastatic melanoma: analysis of 270 patients treated between 1985 and 1993. J Clin Oncol 1999;17:2105-16.
2. Rosenberg SA. IL-2: the first effective immunotherapy for human cancer. J Immunol 2014;192:5451-8.
3. Rosenberg SA, Yang JC, Sherry RM, Kammula US, Hughes MS, Phan GQ, et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin Cancer Res 2011;17:4550-7.
4. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, et al. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014;32:1020-30.
5. Rizvi NA, Mazieres J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, et al. Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): a phase 2, single-arm trial. Lancet Oncol 2015;16:257-65.
6. Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 2014;515:558-62.
7. Robbins PF, Lu YC, El-Gamil M, Li YF, Gross C, Gartner J, et al. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat Med 2013;19:747-52.
8. Lu YC, Yao X, Li YF, El-Gamil M, Dudley ME, Yang JC, et al. Mutated PPP1R3B is recognized by T cells used to treat a melanoma patient who experienced a durable complete tumor regression. J Immunol 2013;190: 6034-42.
9. Lu YC, Yao X, Crystal JS, Li YF, El-Gamil M, Gross C, et al. Efficient identification of mutated cancer antigens recognized by T cells associated with durable tumor regressions. Clin Cancer Res 2014;20:3401-10.
10. Tran E, Turcotte S, Gros A, Robbins PF, Lu YC, Dudley ME, et al. Cancer immunotherapy based on mutation-specific CD4+ T cells in a patient with epithelial cancer. Science 2014;344:641-5.
11. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014;371:2189-99.
12. Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, et al. Mutational landscapedetermines sensitivity to PD-1 blockade in nonsmall cell lung cancer. Science 2015;348:124-8.
13. Gubin MM, Zhang X, Schuster H, Caron E, Ward JP, Noguchi T, et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 2014;515:577-81.
14. Moss DJ, Misko IS, Burrows SR, Burman K, McCarthy R, Sculley TB. Cytotoxic T-cell clones discriminate between A- and B-type Epstein-Barr virus transformants. Nature 1988;331:719-21.
15. Dudley ME, Wunderlich JR, Shelton TE, Even J, Rosenberg SA. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J Immunother 2003;26: 332-42.
16. Lapointe R, Bellemare-Pelletier A, Housseau F, Thibodeau J, Hwu P. CD40-stimulated B lymphocytes pulsed with tumor antigens are effective antigen-presenting cells that can generate specificTcells.CancerRes 2003;63:2836-43.
17. Jones S, Wang TL, Shih Ie M, Mao TL, Nakayama K, Roden R, et al. Frequent mutations of chromatin remodeling gene ARID1A in ovarian clear cell carcinoma. Science 2010;330:228-31.
18. Pfeifer GP. Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment. Photochem Photobiol 1997;65: 270-83.
19. Bennett EM, Bennink JR, Yewdell JW, Brodsky FM. Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression. J Immunol 1999;162:5049-52.
20. Ji H, Wang TL, Chen CH, Pai SI, Hung CF, Lin KY, et al. Targeting human papillomavirus type 16 E7 to the endosomal/lysosomal compartment enhances the antitumor immunity of DNA vaccines against murine human papillomavirus type 16 E7-expressing tumors. Hum Gene Ther 1999; 10:2727-40.
21. Lundegaard C, Lamberth K, Harndahl M, Buus S, Lund O, Nielsen M. NetMHC-3.0: accurate web accessible predictions of human, mouse and monkey MHC class I affinities for peptides of length 8-11. Nucleic Acids Res 2008;36:W509-12.
22. GrosA, RobbinsPF, Yao X, LiYF, Turcotte S, Tran E, etal. PD-1 identifies the patient-specific CD8(?) tumor-reactive repertoire infiltrating human tumors. J Clin Invest 2014;124:2246-59.
23. Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J Immunol 2005;175:7046-52.
24. Wolfl M, Kuball J, Ho WY, Nguyen H, Manley TJ, Bleakley M, et al. Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities. Blood 2007;110: 201-10.
25. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, Vanin EF, et al. Correction of multi-gene deficiency in vivo using a single selfcleaving' 2A peptide-based retroviral vector. Nat Biotechnol 2004; 22:589-94.
26. Wargo JA, Robbins PF, Li Y, Zhao Y, El-Gamil M, Caragacianu D, et al. Recognition of NY-ESO-1+ tumor cells by engineered lymphocytes is enhanced by improved vector design and epigenetic modulation of tumor antigen expression. Cancer Immunol Immunother 2009;58:383-94.
27. Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, et al. Signatures of mutational processes in human cancer. Nature 2013;500:415-21.
28. Krauthammer M, Kong Y, Bacchiocchi A, Evans P, Pornputtapong N, Wu C, et al. Exome sequencing identifies recurrent mutations in NF1 and RASopathy genes in sun-exposed melanomas. Nat Genet 2015;47:996-1002.
29. Van Allen EM, Miao D, Schilling B, Shukla SA, Blank C, Zimmer L, et al. Genomic correlates of response to CTLA-4 blockade in metastatic melanoma. Science 2015;350:207-11.
30. Cohen CJ, Gartner JJ, Horovitz-Fried M, Shamalov K, Trebska-McGowan K, Bliskovsky VV, et al. Isolation of neoantigen-specific T cells from tumor and peripheral lymphocytes. J Clin Invest 2015;125:3981-91.
31. Lawrence MS, Stojanov P, Mermel CH, Robinson JT, Garraway LA, Golub TR, et al. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014;505:495-501.
32. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009;114:535-46.
33. Robbins PF, Kassim SH, Tran TL, Crystal JS, Morgan RA, Feldman SA, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res 2015;21:1019-27.
34. Morgan RA, Chinnasamy N, Abate-Daga D, Gros A, Robbins PF, Zheng Z, et al. Cancer regression and neurological toxicity following anti-MAGE-A3 TCR gene therapy. J Immunother 2013;36:133-51.
35. Huang J, El-Gamil M, Dudley ME, Li YF, Rosenberg SA, Robbins PF. T cells associated with tumor regression recognize frameshifted products of the CDKN2A tumor suppressor gene locus and a mutated HLA class I gene product. J Immunol 2004;172:6057-64.
36. Zhou J, Dudley ME, Rosenberg SA, Robbins PF. Persistence of multiple tumor-specific T-cell clones is associated with complete tumor regression in a melanoma patient receiving adoptive cell transfer therapy. J Immunother 2005;28:53-62.
37. Robbins PF, Dudley ME, Wunderlich J, El-Gamil M, Li YF, Zhou J, et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol 2004;173:7125-30.
38. Toebes M, Coccoris M, Bins A, Rodenko B, Gomez R, Nieuwkoop NJ, et al. Design and use of conditional MHC class I ligands. Nat Med 2006;12:246-51.