Enhanced T-cell activation and differentiation in lymphocytes from transgenic mice expressing ubiquitination-resistant 2KR LAT molecules

Gene Therapy

Volumn 22, Issue 10, 2015, Pages 781-792

  Rodriguez Pena A B ^a,b,c   Gomez Rodriguez, J ^d   Kortum, R L ^a,e   Palmer, D C ^a   Yu, Z ^a   Guittard, G C ^a   Wohlfert, E A ^f,g   Silver, P B ^h   Misplon, J A ⁱ   Sommers, C L ^a   Feigenbaum, L ^j   Epstein, S L ⁱ   Caspi, R R ^h   Belkaid, Y ^f   Restifo, N P ^a   Samelson, L E ^a   Balagopalan, L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Centro de Investigacion del Cancer   (Spain)

^c CSIC   (Spain)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^e UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^g UNIVERSITY AT BUFFALO   (United States)

^h NATIONAL EYE INSTITUTE   (United States)

ⁱ CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^j FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

LAT PROTEIN; T LYMPHOCYTE RECEPTOR; LAT PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOLYSIS; FEMALE; IMMUNOTHERAPY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TRANSGENIC MOUSE; TUMOR IMMUNITY; UBIQUITINATION; VIRAL CLEARANCE; WILD TYPE MOUSE; AMINO ACID SUBSTITUTION; ANIMAL; CELL DIFFERENTIATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE; LYMPHOCYTE ACTIVATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SUBSTITUTION; ANIMALS; CELL DIFFERENTIATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; PHOSPHOPROTEINS; RECEPTORS, ANTIGEN, T-CELL; UBIQUITINATION;

EID: 84943454184     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2015.48     Document Type: Article

References (47)

1. Balagopalan L, Coussens NP, Sherman E, Samelson LE, Sommers CL. The LAT story: a tale of cooperativity, coordination, and choreography. Cold Spring Harb Perspect Biol 2010; 2: a005512.
2. Samelson LE. Signal transduction mediated by the T cell antigen receptor: the role of adapter proteins. Annu Rev Immunol 2002; 20: 371-394.
3. Balagopalan L, Barr VA, Sommers CL, Barda-Saad M, Goyal A, Isakowitz MS et al. c-Cbl-mediated regulation of LAT-nucleated signaling complexes. Mol Cell Biol 2007; 27: 8622-8636.
4. Jang IK, Gu H. Negative regulation of TCR signaling and T-cell activation by selective protein degradation. Curr Opin Immunol 2003; 15: 315-320.
5. Ma A, Malynn BA. A20: linking a complex regulator of ubiquitylation to immunity and human disease. Nat Rev Immunol 2012; 12: 774-785.
6. Malynn BA, Ma A. Ubiquitin makes its mark on immune regulation. Immunity 2010; 33: 843-852.
7. Balagopalan L, Ashwell BA, Bernot KM, Akpan IO, Quasba N, Barr VA et al. Enhanced T-cell signaling in cells bearing linker for activation of T-cell (LAT) molecules resistant to ubiquitylation. Proc Natl Acad Sci USA 2011; 108: 2885-2890.
8. Kunii N, Zhao Y, Jiang S, Liu X, Scholler J, Balagopalan L et al. Enhanced function of redirected human T cells expressing linker for activation of T cells that is resistant to ubiquitylation. Hum Gene Ther 2013; 24: 27-37.
9. Kortum RL, Sommers CL, Pinski JM, Alexander CP, Merrill RK, Li W et al. Deconstructing Ras signaling in the thymus. Mol Cell Biol 2012; 32: 2748-2759.
10. Wildin RS, Wang HU, Forbush KA, Perlmutter RM. Functional dissection of the murine lck distal promoter. J Immunol 1995; 155: 1286-1295.
11. Kortum RL, Sommers CL, Alexander CP, Pinski JM, Li W, Grinberg A et al. Targeted Sos1 deletion reveals its critical role in early T-cell development. Proc Natl Acad Sci USA 2011; 108: 12407-12412.
12. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR. T cell receptor antagonist peptides induce positive selection. Cell 1994; 76: 17-27.
13. Cannons JL, Yu LJ, Jankovic D, Crotty S, Horai R, Kirby M et al. SAP regulates T cellmediated help for humoral immunity by a mechanism distinct from cytokine regulation. J Exp Med 2006; 203: 1551-1565.
14. Epstein SL, Price GE. Cross-protective immunity to influenza A viruses. Expert Rev Vaccines 2010; 9: 1325-1341.
15. Gazzinelli R, Xu Y, Hieny S, Cheever A, Sher A. Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J Immunol 1992; 149: 175-180.
16. t Hart BA, Gran B, Weissert R. EAE: imperfect but useful models of multiple sclerosis. Trends Mol Med 2011; 17: 119-125.
17. Caspi RR. A look at autoimmunity and inflammation in the eye. J Clin Invest 2010; 120: 3073-3083.
18. Overwijk WW, Theoret MR, Finkelstein SE, Surman DR, de Jong LA, Vyth-Dreese FA et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med 2003; 198: 569-580.
19. Palmer DC, Chan CC, Gattinoni L, Wrzesinski C, Paulos CM, Hinrichs CS et al. Effective tumor treatment targeting a melanoma/melanocyte-associated antigen triggers severe ocular autoimmunity. Proc Natl Acad Sci USA 2008; 105: 8061-8066.
20. Klebanoff CA, Gattinoni L, Restifo NP. Sorting through subsets: which T-cell populations mediate highly effective adoptive immunotherapy? J Immunother 2012; 35: 651-660.
21. Gattinoni L, Klebanoff CA, Palmer DC, Wrzesinski C, Kerstann K, Yu Z et al. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest 2005; 115: 1616-1626.
22. Hinrichs CS, Borman ZA, Cassard L, Gattinoni L, Spolski R, Yu Z et al. Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci USA 2009; 106: 17469-17474.
23. Hinrichs CS, Borman ZA, Gattinoni L, Yu Z, Burns WR, Huang J et al. Human effector CD8+ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood 2011; 117: 808-814.
24. Klebanoff CA, Gattinoni L, Torabi-Parizi P, Kerstann K, Cardones AR, Finkelstein SE et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci USA 2005; 102: 9571-9576.
25. Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat Rev Immunol 2012; 12: 269-281.
26. Gattinoni L, Powell DJ Jr., Rosenberg SA, Restifo NP. Adoptive immunotherapy for cancer: building on success. Nat Rev Immunol 2006; 6: 383-393.
27. Kalos M, June CH. Adoptive T cell transfer for cancer immunotherapy in the era of synthetic biology. Immunity 2013; 39: 49-60.
28. 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: 3722-3734.
29. Riese MJ, Wang LC, Moon EK, Joshi RP, Ranganathan A, June CH et al. Enhanced effector responses in activated CD8+ T cells deficient in diacylglycerol kinases. Cancer Res 2013; 73: 3566-3577.
30. Zhou P, Shaffer DR, Alvarez Arias DA, Nakazaki Y, Pos W, Torres AJ et al. In vivo discovery of immunotherapy targets in the tumour microenvironment. Nature 2014; 506: 52-57.
31. Price GE, Soboleski MR, Lo CY, Misplon JA, Quirion MR, Houser KV et al. Singledose mucosal immunization with a candidate universal influenza vaccine provides rapid protection from virulent H5N1, H3N2 and H1N1 viruses. PloS One 2010; 5: e13162.
32. Cerwenka A, Morgan TM, Dutton RW. Nave, effector, and memory CD8 T cells in protection against pulmonary influenza virus infection: homing properties rather than initial frequencies are crucial. J Immunol 1999; 163: 5535-5543.
33. Price GE, Soboleski MR, Lo CY, Misplon JA, Pappas C, Houser KV et al. Vaccination focusing immunity on conserved antigens protects mice and ferrets against virulent H1N1 and H5N1 influenza A viruses. Vaccine 2009; 27: 6512-6521.
34. Wherry EJ, Ahmed R. Memory CD8 T-cell differentiation during viral infection. J Virol 2004; 78: 5535-5545.
35. Zhang L, Kerkar SP, Yu Z, Zheng Z, Yang S, Restifo NP et al. Improving adoptive T cell therapy by targeting and controlling IL-12 expression to the tumor environment. Mol Ther 2011; 19: 751-759.
36. Araki K, Youngblood B, Ahmed R. Programmed cell death 1-directed immunotherapy for enhancing T-cell function. Cold Spring Harb Symp Quant Biol 2014.
37. Hinrichs CS, Spolski R, Paulos CM, Gattinoni L, Kerstann KW, Palmer DC et al. IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 2008; 111: 5326-5333.
38. Sun CM, Hall JA, Blank RB, Bouladoux N, Oukka M, Mora JR et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 2007; 204: 1775-1785.
39. Gomez-Rodriguez J, Sahu N, Handon R, Davidson TS, Anderson SM, Kirby MR et al. Differential expression of interleukin-17A and -17F is coupled to T cell receptor signaling via inducible T cell kinase. Immunity 2009; 31: 587-597.
40. Oldenhove G, Bouladoux N, Wohlfert EA, Hall JA, Chou D, Dos Santos L et al. Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 2009; 31: 772-786.
41. Wange RL, Guitian R, Isakov N, Watts JD, Aebersold R, Samelson LE. Activating and inhibitory mutations in adjacent tyrosines in the kinase domain of ZAP-70. J Biol Chem 1995; 270: 18730-18733.
42. Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE. LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 998; 92, 83-92.
43. Gomez-Rodriguez J, Wohlfert EA, Handon R, Meylan F, Wu JZ, Anderson SM et al. Itk-mediated integration of T cell receptor and cytokine signaling regulates the balance between Th17 and regulatory T cells. J Exp Med 2014; 211: 529-543.
44. Miller SD, Karpus WJ, Davidson TS. Experimental autoimmune encephalomyelitis in the mouse. In John E. Coligan et al. (eds). Current protocols in immunology. Chapter 15: Unit 15 1, 2010.
45. Pepperberg DR, Okajima TL, Ripps H, Chader GJ, Wiggert B. Functional properties of interphotoreceptor retinoid-binding protein. Photochem Photobiol 1991; 54: 1057-1060.
46. Caspi RR Experimental autoimmune uveoretinitis in the rat and mouse. In John E. Coligan et al. (eds). Current protocols in immunology. Chapter 15: Unit 15 6, 2003.
47. Misplon JA, Lo CY, Gabbard JD, Tompkins SM, Epstein SL. Genetic control of immune responses to influenza A matrix 2 protein (M2). Vaccine 2010; 28: 5817-5827.