NKG2D CAR T-cell therapy inhibits the growth of NKG2D ligand heterogeneous tumors

Immunology and Cell Biology

Volumn 91, Issue 6, 2013, Pages 435-440

  Spear, Paul ^a   Barber, Amorette ^a   Rynda Apple, Agnieszka ^a   Sentman, Charles L ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

adoptive T cell therapy; CD8 T cells; chimeric antigen receptors; chNKG2D; epitope spreading; immunotherapy

Indexed keywords

NATURAL KILLER CELL RECEPTOR NKG2D;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNIZATION; CANCER INHIBITION; CANCER SURVIVAL; CELL THERAPY; CELL TRANSFER; CONTROLLED STUDY; FEMALE; IN VIVO STUDY; LYMPHOMA; MOUSE; NONHUMAN; OVARY TUMOR; PROTEIN EXPRESSION; T LYMPHOCYTE; TREATMENT RESPONSE;

ANIMALS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERFERON-GAMMA; LYMPHOMA; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; OVARIAN NEOPLASMS; RECOMBINANT FUSION PROTEINS;

MUS;

EID: 84879844341     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2013.17     Document Type: Article

References (34)

1. Bosslet K, Schirrmacher V. Escape of metastasizing clonal tumor cell variants from tumor-specific cytolytic T lymphocytes. J Exp Med 1981; 154: 557-562. (Pubitemid 11044187)
2. Hines DL. Failure of specific adoptive immunotherapy owing to survival and outgrowth of variant cells. Cancer Immunol Immunother 1989; 28: 241-247. (Pubitemid 19077063)
3. Norell H, Carlsten M, Ohlum T, Malmberg KJ, Masucci G, Schedvins K et al. Frequent loss of HLA-A2 expression in metastasizing ovarian carcinomas associated with genomic haplotype loss and HLA-A2-restricted HER-2/neu-specific immunity. Cancer Res 2006; 66: 6387-6394.
4. Mackensen A, Meidenbauer N, Vogl S, Laumer M, Berger J, Andreesen R. Phase I study of adoptive T-cell therapy using antigen-specific CD8+ T cells for the treatment of patients with metastatic melanoma. J Clin Oncol 2006; 24: 5060-5069. (Pubitemid 46631410)
5. Yee C, Thompson JA, Byrd D, Riddell SR, Roche P, Celis E et al. 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 2002; 99: 16168-16173. (Pubitemid 35462767)
6. Rosenberg SA, Dudley ME. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr Opin Immunol 2009; 21: 233-240.
7. Rosenberg SA, Restifo NP, Yang JC, Morgan RA, Dudley ME. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 2008; 8: 299-308. (Pubitemid 351430867)
8. Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 2003; 3: 666-675. (Pubitemid 37328821)
9. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011; 365: 725-733.
10. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366: 2455-2465.
11. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366: 2443-2454.
12. Phan GQ, Yang JC, Sherry RM, Hwu P, Topalian SL, Schwartzentruber DJ et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci USA 2003; 100: 8372-8377. (Pubitemid 36842552)
13. Scarlett UK, Cubillos-Ruiz JR, Nesbeth YC, Martinez DG, Engle X, Gewirtz AT et al. In situ stimulation of CD40 and Toll-like receptor 3 transforms ovarian cancer-infiltrating dendritic cells from immunosuppressive to immunostimulatory cells. Cancer Res 2009; 69: 7329-7337.
14. Vonderheide RH, Flaherty KT, Khalil M, Stumacher MS, Bajor DL, Hutnick NA et al. Clinical activity and immune modulation in cancer patients treated with CP-870,893, a novel CD40 agonist monoclonal antibody. J Clin Oncol 2007; 25: 876-883. (Pubitemid 350002889)
15. Boon T, Van Pel A. Teratocarcinoma cell variants rejected by syngeneic mice: protection of mice immunized with these variants against other variants and against the original malignant cell line. Proc Natl Acad Sci USA 1978; 75: 1519-1523. (Pubitemid 8301589)
16. el-Shami K, Tirosh B, Bar-Haim E, Carmon L, Vadai E, Fridkin M et al. MHC class I-restricted epitope spreading in the context of tumor rejection following vaccination with a single immunodominant CTL epitope. Eur J Immunol 1999; 29: 3295-3301. (Pubitemid 29484220)
17. Butterfield LH, Ribas A, Dissette VB, Amarnani SN, Vu HT, Oseguera D et al. Determinant spreading associated with clinical response in dendritic cell-based immunotherapy for malignant melanoma. Clin Cancer Res 2003; 9: 998-1008. (Pubitemid 36323703)
18. Disis ML, Grabstein KH, Sleath PR, Cheever MA. Generation of immunity to the HER- 2/neu oncogenic protein in patients with breast and ovarian cancer using a peptidebased vaccine. Clin Cancer Res 1999; 5: 1289-1297. (Pubitemid 29282931)
19. Lally KM, Mocellin S, Ohnmacht GA, Nielsen MB, Bettinotti M, Panelli MC et al. Unmasking cryptic epitopes after loss of immunodominant tumor antigen expression through epitope spreading. Int J Cancer 2001; 93: 841-847. (Pubitemid 32756754)
20. Disis ML, Gooley TA, Rinn K, Davis D, Piepkorn M, Cheever MA et al. Generation of T-cell immunity to the HER-2/neu protein after active immunization with HER-2/neu peptide-based vaccines. J Clin Oncol 2002; 20: 2624-2632. (Pubitemid 34575634)
21. Sadelain M. T-cell engineering for cancer immunotherapy. Cancer J 2009; 15: 451-455.
22. Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr Opin Immunol 2009; 21: 215-223.
23. Barber A, Meehan KR, Sentman CL. Treatment of multiple myeloma with adoptively transferred chimeric NKG2D receptor-expressing T cells. Gene Ther 2011; 18: 509-516.
24. Barber A, Sentman CL. Chimeric NKG2D T cells require both T cell- and host-derived cytokine secretion and perforin expression to increase tumor antigen presentation and systemic immunity. J Immunol 2009; 183: 2365-2372.
25. Zhang T, Lemoi BA, Sentman CL. Chimeric NK-receptor-bearing T cells mediate antitumor immunotherapy. Blood 2005; 106: 1544-1551. (Pubitemid 41208564)
26. Barber A, Rynda A, Sentman CL. Chimeric NKG2D expressing T cells eliminate immunosuppression and activate immunity within the ovarian tumor microenvironment. J Immunol 2009; 183: 6939-6947.
27. Spear P, Barber A, Sentman CL. Collaboration of chimeric antigen receptor (CAR)- expressing T cells and host T cells for optimal elimination of established ovarian tumors. OncoImmunology 2013; 2: e23564.
28. Khong HT, Restifo NP. Natural selection of tumor variants in the generation of 'tumor escape' phenotypes. Nat Immunol 2002; 3: 999-1005. (Pubitemid 35363649)
29. Heppner GH. Tumor heterogeneity. Cancer Res 1984; 44: 2259-2265. (Pubitemid 14110633)
30. Barber A, Zhang T, DeMars LR, Conejo-Garcia J, Roby KF, Sentman CL. Chimeric NKG2D receptor-bearing T cells as immunotherapy for ovarian cancer. Cancer Res 2007; 67: 5003-5008. (Pubitemid 46910210)
31. Spear P, Barber A, Rynda-Apple A, Sentman CL. Chimeric antigen receptor T Cells shape myeloid cell function within the tumor microenvironment through IFN-gamma and GM-CSF. J Immunol 2012; 188: 6389-6398.
32. Zhang T, Barber A, Sentman CL. Chimeric NKG2D modified T cells inhibit systemic T-cell lymphoma growth in a manner involving multiple cytokines and cytotoxic pathways. Cancer Res 2007; 67: 11029-11036. (Pubitemid 350145933)
33. Barber A, Zhang T, Sentman CL. Immunotherapy with chimeric NKG2D receptors leads to long-term tumor-free survival and development of host antitumor immunity in murine ovarian cancer. J Immunol 2008; 180: 72-78.
34. Zhang T, Barber A, Sentman CL. Generation of antitumor responses by genetic modification of primary human T cells with a chimeric NKG2D receptor. Cancer Res 2006; 66: 5927-5933. (Pubitemid 43927148)