Enhanced effector responses in activated CD8+ T cells deficient in diacylglycerol kinases

Cancer Research

Volumn 73, Issue 12, 2013, Pages 3566-3577

  Riese, Matthew J ^a,c   Wang, Liang Chuan S ^a   Moon, Edmund K ^a   Joshi, Rohan P ^b   Ranganathan, Anjana ^a   June, Carl H ^a,b   Koretzky, Gary A ^b   Albelda, Steven M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c BLOOD RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; DIACYLGLYCEROL; DIACYLGLYCEROL KINASE; DIACYLGLYCEROL KINASE ALPHA; DIACYLGLYCEROL KINASE ZETA; LYMPHOCYTE ANTIGEN RECEPTOR; MESOTHELIN; MITOGEN ACTIVATED PROTEIN KINASE; RAS PROTEIN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME DEFICIENCY; ENZYME METABOLISM; GENETIC TRANSDUCTION; LISTERIOSIS; LYMPHOCYTE FUNCTION; LYMPHOMA; MESOTHELIOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STABLE EXPRESSION; T LYMPHOCYTE ACTIVATION;

ANIMALS; BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELLS, CULTURED; DIACYLGLYCEROL KINASE; DIGLYCERIDES; FLOW CYTOMETRY; GPI-LINKED PROTEINS; HEK293 CELLS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; ISOENZYMES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOPLASMS, EXPERIMENTAL; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION;

EID: 84879097325     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3874     Document Type: Article

References (45)

1. Smith-Garvin JE, Koretzky GA, Jordan MS. T cell activation. Annu Rev Immunol 2009;27:591-619.
2. Turcotte S, Rosenberg SA. Immunotherapy for metastatic solid cancers. Adv Surg 2011;45:341-60.
3. June CH. Adoptive T cell therapy for cancer in the clinic. J Clin Invest 2007;117:1466-76. (Pubitemid 46871329)
4. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
5. Quezada SA, Peggs KS, Simpson TR, Allison JP. Shifting the equilibrium in cancer immunoediting: from tumor tolerance to eradication. Immunol Rev 2011;241:104-18.
6. Milone MC, Fish JD, Carpenito C, Carroll RG, Binder GK, Teachey D, et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther 2009;17:1453-64.
7. Dower NA, Stang SL, Bottorff DA, Ebinu JO, Dickie P, Ostergaard HL, et al. RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat Immunol 2000;1:317-21.
8. Topham MK, Prescott SM. Diacylglycerol kinase zeta regulates Ras activation by a novel mechanism. J Cell Biol 2001;152:1135-43. (Pubitemid 34280172)
9. Zhong X-P, Hainey EA, Olenchock BA, Jordan MS, Maltzman JS, Nichols KE, et al. Enhanced T cell responses due to diacylglycerol kinase zeta deficiency. Nat Immunol 2003;4:882-90. (Pubitemid 37098659)
10. Olenchock BA, Guo R, Carpenter JH, Jordan M, Topham MK, Koretzky GA, et al. Disruption of diacylglycerol metabolism impairs the induction of T cell anergy. Nat Immunol 2006;7:1174-81. (Pubitemid 44594313)
11. Zha Y, Marks R, Ho AW, Peterson AC, Janardhan S, Brown I, et al. T cell anergy is reversed by active Ras and is regulated by diacylglycerol kinase-alpha. Nat Immunol 2006;7:1166-73. (Pubitemid 44594312)
12. Riese MJ, Grewal J, Das J, Zou T, Patil V, Chakraborty AK, et al. Decreased diacylglycerol metabolism enhances ERK activation and augments CD8+ T cell functional responses. J Biol Chem 2011;286:5254-65.
13. Moore MW, Carbone FR, Bevan MJ. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 1988;54:777-85.
14. Moon EK, Carpenito C, Sun J, Wang L-CS, Kapoor V, Predina J, et al. Expression of a functional CCR2 receptor enhances tumor localization and tumor eradication by retargeted human T cells expressing a mesothelin-specific chimeric antibody receptor. Clin Cancer Res 2011;17:4719-30.
15. Pear WS, Nolan GP, Scott ML, Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc Natl Acad Sci U S A 1993;90:8392-6. (Pubitemid 23277674)
16. Chowdhury PS, Pastan I. Improving antibody affinity by mimicking somatic hypermutation in vitro. Nat Biotechnol 1999;17:568-72. (Pubitemid 29262920)
17. Jordan MS, Sadler J, Austin JE, Finkelstein LD, Singer AL, Schwartzberg PL, et al. Functional hierarchy of the N-terminal tyrosines of SLP-76. J Immunol 2006;176:2430-8. (Pubitemid 43201693)
18. Tchou J, Wang L-C, Selven B, Zhang H, Conejo-Garcia J, Borghaei H, et al. Mesothelin, a novel immunotherapy target for triple negative breast cancer. Breast Cancer Res Treat 2012;133:799-804.
19. DeLong P, Tanaka T, Kruklitis R, Henry AC, Kapoor V, Kaiser LR, et al. Use of cyclooxygenase-2 inhibition to enhance the efficacy of immunotherapy. Cancer Res 2003;63:7845-52. (Pubitemid 37466718)
20. Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limón P. The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol 2010;10:554-67.
21. Nakamura M, Kitaura J, Enomoto Y, Lu Y, Nishimura K, Isobe M, et al. Transforming growth factor-b-stimulated clone-22 is a negative-feedback regulator of Ras/Raf signaling: implications for tumorigenesis. Cancer Sci 2012;103:26-33.
22. di Bari MG, Lutsiak MEC, Takai S, Mostböck S, Farsaci B, Semnani RT, et al. TGF-beta modulates the functionality of tumor-infiltrating CD8+ T cells through effects on TCR signaling and Spred1 expression. Cancer Immunol Immunother 2009;58:1809-18.
23. Bedi A, Chang X, Noonan K, Pham V, Bedi R, Fertig EJ, et al. Inhibition of transforming growth factor-β enhances the in vivo antitumor efficacy of epidermal growth factor receptor-targeted therapy. Mol Cancer Ther 2012;11:2429-39.
24. Cartellieri M, Bachmann M, Feldmann A, Bippes C, Stamova S, Wehner R, et al. Chimeric antigen receptor-engineered T cells for immunotherapy of cancer. J Biomed Biotechnol 2010;2010:956304.
25. Bennett SR, Carbone FR, Karamalis F, Flavell RA, Miller JF, Heath WR. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 1998;393:478-80.
26. Schoenberger SP, Toes RE, van der Voort EI, Offringa R, Melief CJ. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998;393:480-3.
27. Ridge JP, Di Rosa F, Matzinger P. A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell. Nature 1998;393:474-8.
28. Chambers CA, Sullivan TJ, Truong T, Allison JP. Secondary but not primary T cell responses are enhanced in CTLA-4-deficient CD8+ T cells. Eur J Immunol 1998;28:3137-43. Available from: http://dx.doi.org/10.1002/(SICI)1521- 4141(199810)28:10〈3137::AID-IMMU3137〉3.0.CO;2-X.
29. Gajewski TF, Fallarino F, Fields PE, Rivas F, Alegre ML. Absence of CTLA-4 lowers the activation threshold of primed CD8+ TCR-transgenic T cells: lack of correlation with Src homology domain 2-containing protein tyrosine phosphatase. J Immunol 2001;166:3900-7. (Pubitemid 32224916)
30. Chiang JY, Jang IK, Hodes R, Gu H. Ablation of Cbl-b provides protection against transplanted and spontaneous tumors. J Clin Invest 2007;117:1029-36. (Pubitemid 46556759)
31. Loeser S, Loser K, Bijker MS, Rangachari M, van der Burg SH, Wada T, et al. Spontaneous tumor rejection by cbl-b-deficient CD8+ T cells. J Exp Med 2007;204:879-91. (Pubitemid 46631616)
32. Stromnes IM, Blattman JN, Tan X, Jeevanjee S, Gu H, Greenberg PD. Abrogating Cbl-b in effector CD8(+) T cells improves the efficacy of adoptive therapy of leukemia in mice. J Clin Invest 2010;120:3722-34.
33. Wallner S, Gruber T, Baier G, Wolf D. Releasing the brake: targeting Cbl-b to enhance lymphocyte effector functions. Clin Dev Immunol 2012;2012:692639.
34. Das J, Ho M, Zikherman J, Govern C, Yang M, Weiss A, et al. Digital signaling and hysteresis characterize ras activation in lymphoid cells. Cell 2009;136:337-51.
35. Kalos M, Levine BL, Porter DL, Katz S, Grupp SA, Bagg A, et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 2011;3:95ra73.
36. 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;365:725-33.
37. Kershaw MH, Westwood JA, Parker LL, Wang G, Eshhar Z, Mavroukakis SA, et al. A phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin Cancer Res 2006;12(20 Pt 1):6106-15. (Pubitemid 44703776)
38. Lamers CHJ, Sleijfer S, Vulto AG, Kruit WHJ, Kliffen M, Debets R, et al. Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J Clin Oncol 2006;24:e20-2.
39. Carpenito C, Milone MC, Hassan R, Simonet JC, Lakhal M, Suhoski MM, et al. Control of large, established tumor xenografts with genetically retargeted human T cells containing CD28 and CD137 domains. Proc Natl Acad Sci U S A 2009;106:3360-5.
40. Gorelik L, Flavell RA. Immune-mediated eradication of tumors through the blockade of transforming growth factor-beta signaling in T cells. Nat Med 2001;7:1118-22. (Pubitemid 33010019)
41. Bollard CM, Rössig C, Calonge MJ, Huls MH, Wagner H-J, Massague J, et al. Adapting a transforming growth factor beta-related tumor protection strategy to enhance antitumor immunity. Blood 2002;99:3179-87. (Pubitemid 34525296)
42. Wikström P, Stattin P, Franck-Lissbrant I, Damber JE, Bergh A. Transforming growth factor beta1 is associated with angiogenesis, metastasis, and poor clinical outcome in prostate cancer. Prostate 1998;37:19-29. (Pubitemid 28385181)
43. Eastham JA, Truong LD, Rogers E, Kattan M, Flanders KC, Scardino PT, et al. Transforming growth factor-beta 1: comparative immunohistochemical localization in human primary and metastatic prostate cancer. Lab Invest 1995;73:628-35. (Pubitemid 3018923)
44. Chen C-H, Seguin-Devaux C, Burke NA, Oriss TB, Watkins SC, Clipstone N, et al. Transforming growth factor beta blocks Tec kinase phosphorylation, Ca2+ influx, and NFATc translocation causing inhibition of T cell differentiation. J Exp Med 2003;197:1689-99. (Pubitemid 36745344)
45. Zhao Y, Moon E, Carpenito C, Paulos CM, Liu X, Brennan AL, et al. Multiple injections of electroporated autologous T cells expressing a chimeric antigen receptor mediate regression of human disseminated tumor. Cancer Res 2010;70:9053-61.