PD-1 signalling in CD4+ T cells restrains their clonal expansion to an immunogenic stimulus, but is not critically required for peptide-induced tolerance

Immunology

Volumn 130, Issue 1, 2010, Pages 92-102

  Konkel, Joanne E ^a   Frommer, Friederike ^b   Leech, Melanie D ^a,c   Yagita, Hideo ^d   Waisman, Ari ^b   Anderton, Stephen M ^a,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Costimulation; T cells; Tolerance

Indexed keywords

PROGRAMMED DEATH 1 RECEPTOR; PROTEIN PD L1; T CELL FACTOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOSTIMULATION; MOLECULAR CLONING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSGENICS;

ANIMALS; ANTIGENS, DIFFERENTIATION; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; FLOW CYTOMETRY; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OVALBUMIN; PEPTIDE FRAGMENTS; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 77950492166     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2009.03216.x     Document Type: Article

References (38)

1. Steinman RM, Nussenzweig MC. Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci USA 2002 99 : 351 358.
2. Hochweller K, Sweenie CH, Anderton SM. Immunological tolerance using synthetic peptides - Basic mechanisms and clinical application. Curr Mol Med 2006 6 : 631 643.
3. Hochweller K, Anderton SM. Kinetics of costimulatory molecule expression by T cells and dendritic cells during the induction of tolerance versus immunity in vivo. Eur J Immunol 2005 35 : 1086 1096.
4. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008 26 : 677 704.
5. Parry RV, Chemnitz JM, Frauwirth KA et al. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol Cell Biol 2005 25 : 9543 9553.
6. Sheppard KA, Fitz LJ, Lee JM et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett 2004 574 : 37 41.
7. Freeman GJ, Long AJ, Iwai Y et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000 192 : 1027 1034.
8. Latchman Y, Wood CR, Chernova T et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001 2 : 261 268.
9. Yamazaki T, Akiba H, Iwai H et al. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 2002 169 : 5538 5545.
10. Hori J, Wang M, Miyashita M et al. B7-H1-induced apoptosis as a mechanism of immune privilege of corneal allografts. J Immunol 2006 177 : 5928 5935.
11. Magnus T, Schreiner B, Korn T et al. Microglial expression of the B7 family member B7 homolog 1 confers strong immune inhibition: implications for immune responses and autoimmunity in the CNS. J Neurosci 2005 25 : 2537 2546.
12. Liang SC, Latchman YE, Buhlmann JE, Tomczak MF, Horwitz BH, Freeman GJ, Sharpe AH. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur J Immunol 2003 33 : 2706 2716.
13. Salama AD, Chitnis T, Imitola J et al. Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J Exp Med 2003 198 : 71 8.
14. Keir ME, Liang SC, Guleria I et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 2006 203 : 883 895.
15. Wang L, Han R, Hancock WW. Programmed cell death 1 (PD-1) and its ligand PD-L1 are required for allograft tolerance. Eur J Immunol 2007 37 : 2983 2990.
16. + T cell tolerance through PD-1 and CTLA-4. Nat Immunol 2005 6 : 280 286.
17. + T cell responses to antigen in lymph nodes and tissues. J Immunol 2007 179 : 5064 5070.
18. + T cell tolerance to tissue antigens. J Immunol 2006 177 : 8291 8295.
19. Reynoso ED, Elpek KG, Francisco L, Bronson R, Bellemare-Pelletier A, Sharpe AH, Freeman GJ, Turley SJ. Intestinal tolerance is converted to autoimmune enteritis upon PD-1 ligand blockade. J Immunol 2009 182 : 2102 2112.
20. Tsushima F, Yao S, Shin T et al. Interaction between B7-H1 and PD-1 determines initiation and reversal of T-cell anergy. Blood 2007 110 : 180 185.
21. + T cell anergy in vivo. J Immunol 2009 182 : 6682 6689.
22. Liu GY, Wraith DC. Affinity for class II MHC determines the extent to which soluble peptides tolerize autoreactive T cells in naive and primed adult mice - implications for autoimmunity. Int Immunol 1995 7 : 1255 1263.
23. Liblau RS, Tisch R, Shokat K, Yang X, Dumont N, Goodnow CC, McDevitt HO. Intravenous injection of soluble antigen induces thymic and peripheral T-cells apoptosis. Proc Natl Acad Sci USA 1996 93 : 3031 3036.
24. Kearney ER, Pape KA, Loh DY, Jenkins MK. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1994 1 : 327 339.
25. Barnden MJ, Allison J, Heath WR, Carbone FR. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol Cell Biol 1998 76 : 34 40.
26. Frommer F, Heinen TJ, Wunderlich FT et al. Tolerance without clonal expansion: self-antigen-expressing B cells program self-reactive T cells for future deletion. J Immunol 2008 181 : 5748 5759.
27. Bettelli E, Pagany M, Weiner HL, Linington C, Sobel RA, Kuchroo VK. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J Exp Med 2003 197 : 1073 1081.
28. + T cell proliferation by augmenting IFN-gamma-induced nitric oxide production. J Immunol 2005 175 : 1586 1592.
29. Hochweller K, Sweenie CH, Anderton SM. Circumventing tolerance at the T cell or the antigen-presenting cell surface: antibodies that ligate CD40 and OX40 have different effects. Eur J Immunol 2006 36 : 389 396.
30. Fife BT, Guleria I, Gubbels Bupp M et al. Insulin-induced remission in new-onset NOD mice is maintained by the PD-1-PD-L1 pathway. J Exp Med 2006 203 : 2737 2747.
31. Ansari MJ, Salama AD, Chitnis T et al. The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med 2003 198 : 63 9.
32. Ito T, Ueno T, Clarkson MR et al. Analysis of the role of negative T cell costimulatory pathways in CD4 and CD8 T cell-mediated alloimmune responses in vivo. J Immunol 2005 174 : 6648 6656.
33. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity 2007 27 : 111 122.
34. Haspot F, Fehr T, Gibbons C, Zhao G, Hogan T, Honjo T, Freeman GJ, Sykes M. Peripheral deletional tolerance of alloreactive CD8 but not CD4 T cells is dependent on the PD-1/PD-L1 pathway. Blood 2008 112 : 2149 2155.
35. Carter L, Fouser LA, Jussif J et al. PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur J Immunol 2002 32 : 634 643.
36. + T cells are restricted by the up-regulation of PD-1. J Immunol 2009 182 : 4244 4254.
37. Fife BT, Bluestone JA. Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev 2008 224 : 166 182.
38. Fife BT, Pauken KE, Eagar TN et al. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat Immunol 2009 10 : 1185 1192.