Long-term persistence of CD4+ but rapid disappearance of CD8+ T cells expressing an MHC class I-restricted TCR of nanomolar affinity

Molecular Therapy

Volumn 20, Issue 3, 2012, Pages 652-660

  Engels, Boris ^a   Chervin, Adam S ^b   Sant, Andrea J ^c   Kranz, David M ^b   Schreiber, Hans ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE; SERYLISOLEUCYLTYROSYLARGINYLTYROSYLTYROSYLGLYCYLLEUCINE LYSINE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; CONTROLLED STUDY; GRAFT VERSUS HOST REACTION; HAPLOTYPE; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN BINDING; PROTEIN EXPRESSION; RETROVIRUS; SIGNAL TRANSDUCTION;

EID: 84857792441     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2011.286     Document Type: Article

References (49)

1. Jameson, SC, Hogquist, KA and Bevan, MJ (1995). Positive selection of thymocytes. Annu Rev Immunol 13: 93-126.
2. Kyewski, B and Klein, L (2006). A central role for central tolerance. Annu Rev Immunol 24: 571-606.
3. Mueller, DL (2010). Mechanisms maintaining peripheral tolerance. Nat Immunol 11: 21-27.
4. Peterson, P, Org, T and Rebane, A (2008). Transcriptional regulation by AIRE: molecular mechanisms of central tolerance. Nat Rev Immunol 8: 948-957.
5. Cohen, JN, Guidi, CJ, Tewalt, EF, Qiao, H, Rouhani, SJ, Ruddell, A et al. (2010). Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aireindependent direct antigen presentation. J Exp Med 207: 681-688.
6. Fletcher, AL, Lukacs-Kornek, V, Reynoso, ED, Pinner, SE, Bellemare-Pelletier, A, Curry, MS et al. (2010). Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J Exp Med 207: 689-697.
7. Davis, MM, Boniface, JJ, Reich, Z, Lyons, D, Hampl, J, Arden, B et al. (1998). Ligand recognition by alpha beta T cell receptors. Annu Rev Immunol 16: 523-544. (Pubitemid 28183375)
8. Williams, CB, Engle, DL, Kersh, GJ, Michael White, J and Allen, PM (1999). A kinetic threshold between negative and positive selection based on the longevity of the T cell receptor-ligand complex. J Exp Med 189: 1531-1544. (Pubitemid 29240878)
9. Foote, J and Eisen, HN (2000). Breaking the affinity ceiling for antibodies and T cell receptors. Proc Natl Acad Sci USA 97: 10679-10681.
10. Holler, PD, Chlewicki, LK and Kranz, DM (2003). TCRs with high affinity for foreign pMHC show self-reactivity. Nat Immunol 4: 55-62. (Pubitemid 36104709)
11. Varela-Rohena, A, Molloy, PE, Dunn, SM, Li, Y, Suhoski, MM, Carroll, RG et al. (2008). Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat Med 14: 1390-1395.
12. Li, Y, Moysey, R, Molloy, PE, Vuidepot, AL, Mahon, T, Baston, E et al. (2005). Directed evolution of human T-cell receptors with picomolar affinities by phage display. Nat Biotechnol 23: 349-354. (Pubitemid 41094424)
13. Chervin, AS, Aggen, DH, Raseman, JM and Kranz, DM (2008). Engineering higher affinity T cell receptors using a T cell display system. J Immunol Methods 339: 175-184.
14. Robbins, PF, Li, YF, El-Gamil, M, Zhao, Y, Wargo, JA, Zheng, Z et al. (2008). Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions. J Immunol 180: 6116-6131.
15. Zhao, Y, Bennett, AD, Zheng, Z, Wang, QJ, Robbins, PF, Yu, LY et al. (2007). Highaffinity TCRs generated by phage display provide CD4+ T cells with the ability to recognize and kill tumor cell lines. J Immunol 179: 5845-5854.
16. Holler, PD and Kranz, DM (2003). Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18: 255-264. (Pubitemid 36263000)
17. Kranz, DM, Sherman, DH, Sitkovsky, MV, Pasternack, MS and Eisen, HN (1984). Immunoprecipitation of cell surface structures of cloned cytotoxic T lymphocytes by clone-specific antisera. Proc Natl Acad Sci USA 81: 573-577. (Pubitemid 14186607)
18. Udaka, K, Tsomides, TJ and Eisen, HN (1992). A naturally occurring peptide recognized by alloreactive CD8+ cytotoxic T lymphocytes in association with a class I MHC protein. Cell 69: 989-998.
19. Udaka, K, Wiesmüller, KH, Kienle, S, Jung, G and Walden, P (1996). Self-MHCrestricted peptides recognized by an alloreactive T lymphocyte clone. J Immunol 157: 670-678. (Pubitemid 26231370)
20. Tallquist, MD, Yun, TJ and Pease, LR (1996). A single T cell receptor recognizes structurally distinct MHC/peptide complexes with high specificity. J Exp Med 184: 1017-1026. (Pubitemid 26313559)
21. Dutz, JP, Tsomides, TJ, Kageyama, S, Rasmussen, MH and Eisen, HN (1994). A cytotoxic T lymphocyte clone can recognize the same naturally occurring self peptide in association with a self and nonself class I MHC protein. Mol Immunol 31: 967-975.
22. Udaka, K, Tsomides, TJ, Walden, P, Fukusen, N and Eisen, HN (1993). A ubiquitous protein is the source of naturally occurring peptides that are recognized by a CD8+ T-cell clone. Proc Natl Acad Sci USA 90: 11272-11276. (Pubitemid 23354411)
23. Sykulev, Y, Brunmark, A, Jackson, M, Cohen, RJ, Peterson, PA and Eisen, HN (1994). Kinetics and affinity of reactions between an antigen-specific T cell receptor and peptide-MHC complexes. Immunity 1: 15-22.
24. Degano, M, Garcia, KC, Apostolopoulos, V, Rudolph, MG, Teyton, L and Wilson, IA (2000). A functional hot spot for antigen recognition in a superagonist TCR/MHC complex. Immunity 12: 251-261.
25. Daniels, MA and Jameson, SC (2000). Critical role for CD8 in T cell receptor binding and activation by peptide/major histocompatibility complex multimers. J Exp Med 191: 335-346.
26. Hahn, S, Gehri, R and Erb, P (1995). Mechanism and biological significance of CD4-mediated cytotoxicity. Immunol Rev 146: 57-79.
27. Pardoll, DM and Topalian, SL (1998). The role of CD4+ T cell responses in antitumor immunity. Curr Opin Immunol 10: 588-594. (Pubitemid 28479193)
28. Steiner, LA and Eisen, HN (1967). Sequential changes in the relative affinity of antibodies synthesized during the immune response. J Exp Med 126: 1161-1183.
29. Baumgarth, N (2000). A two-phase model of B-cell activation. Immunol Rev 176: 171-180.
30. Janssen, EM, Lemmens, EE, Wolfe, T, Christen, U, von Herrath, MG and Schoenberger, SP (2003). CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421: 852-856. (Pubitemid 36254145)
31. Shedlock, DJ and Shen, H (2003). Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300: 337-339. (Pubitemid 36433726)
32. Sun, JC, Williams, MA and Bevan, MJ (2004). CD4+ T cells are required for the maintenance, not programming, of memory CD8+ T cells after acute infection. Nat Immunol 5: 927-933. (Pubitemid 39276237)
33. Walter, EA, Greenberg, PD, Gilbert, MJ, Finch, RJ, Watanabe, KS, Thomas, ED et al. (1995). Reconstitution of cellular immunity against cytomegalovirus in recipients of allogeneic bone marrow by transfer of T-cell clones from the donor. N Engl J Med 333: 1038-1044.
34. Morris, EC, Tsallios, A, Bendle, GM, Xue, SA and Stauss, HJ (2005). A critical role of T cell antigen receptor-transduced MHC class I-restricted helper T cells in tumor protection. Proc Natl Acad Sci USA 102: 7934-7939. (Pubitemid 40781041)
35. Schietinger, A, Philip, M, Liu, RB, Schreiber, K and Schreiber, H (2010). Bystander killing of cancer requires the cooperation of CD4(+) and CD8(+) T cells during the effector phase. J Exp Med 207: 2469-2477.
36. Nakanishi, Y, Lu, B, Gerard, C and Iwasaki, A (2009). CD8(+) T lymphocyte mobilization to virus-infected tissue requires CD4(+) T-cell help. Nature 462: 510-513.
37. Bos, R and Sherman, LA (2010). CD4+ T-cell help in the tumor milieu is required for recruitment and cytolytic function of CD8+ T lymphocytes. Cancer Res 70: 8368-8377.
38. Kohm, AP, Carpentier, PA, Anger, HA and Miller, SD (2002). Cutting edge: CD4+CD25+ regulatory T cells suppress antigen-specific autoreactive immune responses and central nervous system inflammation during active experimental autoimmune encephalomyelitis. J Immunol 169: 4712-4716. (Pubitemid 35217131)
39. Mottet, C, Uhlig, HH and Powrie, F (2003). Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells. J Immunol 170: 3939-3943. (Pubitemid 36428153)
40. Tang, Q, Henriksen, KJ, Bi, M, Finger, EB, Szot, G, Ye, J et al. (2004). In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 199: 1455-1465. (Pubitemid 38780401)
41. Brusko, TM, Koya, RC, Zhu, S, Lee, MR, Putnam, AL, McClymont, SA et al. (2010). Human antigen-specific regulatory T cells generated by T cell receptor gene transfer. PLoS ONE 5: e11726.
42. Zhang, ZX, Yang, L, Young, KJ, DuTemple, B and Zhang, L (2000). Identification of a previously unknown antigen-specific regulatory T cell and its mechanism of suppression. Nat Med 6: 782-789. (Pubitemid 30469427)
43. Chervin, AS, Stone, JD, Holler, PD, Bai, A, Chen, J, Eisen, HN et al. (2009). The impact of TCR-binding properties and antigen presentation format on T cell responsiveness. J Immunol 183: 1166-1178.
44. Sykulev, Y, Joo, M, Vturina, I, Tsomides, TJ and Eisen, HN (1996). Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity 4: 565-571. (Pubitemid 26233310)
45. Bendle, GM, Linnemann, C, Hooijkaas, AI, Bies, L, de Witte, MA, Jorritsma, A et al. (2010). Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat Med 16: 565-70, 1p following 570.
46. Daniels, MA, Teixeiro, E, Gill, J, Hausmann, B, Roubaty, D, Holmberg, K et al. (2006). Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 444: 724-729. (Pubitemid 44949596)
47. Zhao, Y, Zheng, Z, Robbins, PF, Khong, HT, Rosenberg, SA and Morgan, RA (2005). Primary human lymphocytes transduced with NY-ESO-1 antigen-specific TCR genes recognize and kill diverse human tumor cell lines. J Immunol 174: 4415-4423. (Pubitemid 40396025)
48. Kershaw, MH, Westwood, JA and Hwu, P (2002). Dual-specific T cells combine proliferation and antitumor activity. Nat Biotechnol 20: 1221-1227. (Pubitemid 35462486)
49. Pule, MA, Savoldo, B, Myers, GD, Rossig, C, Russell, HV, Dotti, G et al. (2008). Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 14: 1264-1270.