Programmed death-1 (PD-1) defines a transient and dysfunctional oligoclonal T cell population in acute homeostatic proliferation

Journal of Experimental Medicine

Volumn 204, Issue 10, 2007, Pages 2321-2333

  Lin, Sue Jane ^a   Peacock, Craig D ^a   Bahl, Kapil ^a   Welsh, Raymond M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS REGULATORY PROTEIN; GAMMA INTERFERON; INTERLEUKIN 15 RECEPTOR; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 7 RECEPTOR; INTERLEUKIN 7 RECEPTOR ALPHA; LIPOCORTIN 5; OLIGOCLONAL BAND; PADGEM PROTEIN; PROTEIN BCL 2; PROTEIN PROGRAMMED DEATH 1; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIVISION; CELL FUNCTION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; HOMEOSTASIS; IMMUNOFLUORESCENCE; LYMPHOCYTE DEPLETION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; MEMORY CELL; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; SPLEEN LYMPHOCYTE; T LYMPHOCYTE;

ANIMALS; ANNEXIN A5; ANTIGENS, LY; ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; CELL PROLIFERATION; CYTOKINES; HOMEOSTASIS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MALE; MICE; T-LYMPHOCYTES; TIME FACTORS;

EID: 34948910572     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20062150     Document Type: Article

References (43)

1. Peacock, C.D., S.K. Kim, and R.M. Welsh. 2003. Attrition of virusspecific memory CD8+ T cells during reconstitution of lymphopenic environments. J. Immunol. 171:655-663.
2. Ernst, B., D.S. Lee, J.M. Chang, J. Sprent, and C.D. Surh. 1999. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity. 11:173-181.
3. Ge, Q., V.P. Rao, B.K. Cho, H.N. Eisen, and J. Chen. 2001. Dependence of lymphopenia-induced T cell proliferation on the abundance of peptide/ MHC epitopes and strength of their interaction with T cell receptors. Proc. Natl. Acad. Sci. USA. 98:1728-1733.
4. Kieper, W.C., A. Troy, J.T. Burghardt, C. Ramsey, J.Y. Lee, H.Q. Jiang, W. Dummer, H. Shen, J.J. Cebra, and C.D. Surh. 2005. Recent immune status determines the source of antigens that drive homeostatic T cell expansion. J. Immunol. 174:3158-3163.
5. Goldrath, A.W., L.Y. Bogatzki, and M.J. Bevan. 2000. Naive T cells transiently acquire a memory-like phenotype during homeostasis-driven proliferation. J. Exp. Med. 192:557-564.
6. Cho, B.K., V.P. Rao, Q. Ge, H.N. Eisen, and J. Chen. 2000. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J. Exp. Med. 192:549-556.
7. Murali-Krishna, K., and R. Ahmed. 2000. Cutting edge: naive T cells masquerading as memory cells. J. Immunol. 165:1733-1737.
8. Kieper, W.C., J.T. Burghardt, and C.D. Surh. 2004. A role for TCR affinity in regulating naive T cell homeostasis. J. Immunol. 172:40-44.
9. King, C., A. Ilic, K. Koelsch, and N. Sarvetnick. 2004. Homeostatic expansion of T cells during immune insufficiency generates autoimmunity. Cell. 117:265-277.
10. Goronzy, J.J., and C.M. Weyand. 2001. Thymic function and peripheral T-cell homeostasis in rheumatoid arthritis. Trends Immunol. 22:251-255.
11. Khoruts, A., and J.M. Fraser. 2005. A causal link between lymphopenia and autoimmunity. Immunol. Lett. 98:23-31.
12. Baccala, R., and A.N. Theofilopoulos. 2005. The new paradigm of Tcell homeostatic proliferation-induced autoimmunity. Trends Immunol. 26:5-8.
13. Schulze-Koops, H. 2004. Lymphopenia and autoimmune diseases. Arthritis Res. Ther. 6:178-180.
14. Ishida, Y., Y. Agata, K. Shibahara, and T. Honjo. 1992. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11:3887-3895.
15. Greenwald, R.J., G.J. Freeman, and A.H. Sharpe. 2005. The B7 family revisited. Annu. Rev. Immunol. 23:515-548.
16. Okazaki, T., and T. Honjo. 2006. Rejuvenating exhausted T cells during chronic viral infection. Cell. 124:459-461.
17. Okazaki, T., and T. Honjo. 2006. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol. 27:195-201.
18. Blattman, J.N., and P.D. Greenberg. 2006. PD-1 blockade: rescue from a near-death experience. Nat. Immunol. 7:227-228.
19. Nishimura, H., M. Nose, H. Hiai, N. Minato, and T. Honjo. 1999. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity. 11:141-151.
20. Nishimura, H., T. Okazaki, Y. Tanaka, K. Nakatani, M. Hara, A. Matsumori, S. Sasayama, A. Mizoguchi, H. Hiai, N. Minato, and T. Honjo. 2001. Autoimmune dilated cardiomyopathy in PD-1 receptordeficient mice. Science. 291:319-322.
21. Okazaki, T., Y. Tanaka, R. Nishio, T. Mitsuiye, A. Mizoguchi, J. Wang, M. Ishida, H. Hiai, A. Matsumori, N. Minato, and T. Honjo. 2003. Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat. Med. 9:1477-1483.
22. Johansson, M., L. Arlestig, B. Moller, and S. Rantapaa-Dahlqvist. 2005. Association of a PDCD1 polymorphism with renal manifestations in systemic lupus erythematosus. Arthritis Rheum. 52:1665-1669.
23. Nielsen, C., D. Hansen, S. Husby, B.B. Jacobsen, and S.T. Lillevang. 2003. Association of a putative regulatory polymorphism in the PD-1 gene with susceptibility to type 1 diabetes. Tissue Antigens. 62:492-497.
24. Lin, S.C., J.H. Yen, J.J. Tsai, W.C. Tsai, T.T. Ou, H.W. Liu, and C.J. Chen. 2004. Association of a programmed death 1 gene polymorphism with the development of rheumatoid arthritis, but not systemic lupus erythematosus. Arthritis Rheum. 50:770-775.
25. Wherry, E.J., and R. Ahmed. 2004. Memory CD8 T-cell differentiation during viral infection. J. Virol. 78:5535-5545.
26. Surh, C.D., and J. Sprent. 2000. Homeostatic T cell proliferation: how far can T cells be activated to self-ligands? J. Exp. Med. 192:F9-F14.
27. Bosco, N., F. Agenes, and R. Ceredig. 2005. Effects of increasing IL-7 availability on lymphocytes during and after lymphopenia-induced proliferation. J. Immunol. 175:162-170.
28. Goldrath, A.W., P.V. Sivakumar, M. Glaccum, M.K. Kennedy, M.J. Bevan, C. Benoist, D. Mathis, and E.A. Butz. 2002. Cytokine requirements for acute and Basal homeostatic proliferation of naive and memory CD8+ T cells. J. Exp. Med. 195:1515-1522.
29. Wang, X.Z., M.A. Brehm, and R.M. Welsh. 2004. Preapoptotic phenotype of viral epitope-specific CD8 T cells precludes memory development and is an intrinsic property of the epitope. J. Immunol. 173:5138-5147.
30. Kaech, S.M., J.T. Tan, E.J. Wherry, B.T. Konieczny, C.D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4:1191-1198.
31. Grayson, J.M., A.J. Zajac, J.D. Altman, and R. Ahmed. 2000. Cutting edge: increased expression of Bcl-2 in antigen-specific memory CD8+ T cells. J. Immunol. 164:3950-3954.
32. Barber, D.L., E.J. Wherry, D. Masopust, B. Zhu, J.P. Allison, A.H. Sharpe, G.J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 439:682-687.
33. Day, C.L., D.E. Kaufmann, P. Kiepiela, J.A. Brown, E.S. Moodley, S. Reddy, E.W. Mackey, J.D. Miller, A.J. Leslie, C. DePierres, et al. 2006. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature. 443:350-354.
34. Trautmann, L., L. Janbazian, N. Chomont, E.A. Said, G. Wang, S. Gimmig, B. Bessette, M.R. Boulassel, E. Delwart, H. Sepulveda, et al. 2006. Upregulation of PD-1 expression on HIV-specific CD8 + T cells leads to reversible immune dysfunction. Nat. Med. 12:1198-1202.
35. Blazar, B.R., B.M. Carreno, A. Panoskaltsis-Mortari, L. Carter, Y. Iwai, H. Yagita, H. Nishimura, and P.A. Taylor. 2003. Blockade of programmed death-1 engagement accelerates graft-versus-host disease lethality by an IFN-gamma-dependent mechanism. J. Immunol. 171:1272-1277.
36. Agata, Y., A. Kawasaki, H. Nishimura, Y. Ishida, T. Tsubata, H. Yagita, and T. Honjo. 1996. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int. Immunol. 8:765-772.
37. Yamazaki, T., H. Akiba, H. Iwai, H. Matsuda, M. Aoki, Y. Tanno, T. Shin, H. Tsuchiya, D.M. Pardoll, K. Okumura, et al. 2002. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169:5538-5545.
38. Wang, X.Z., S.E. Stepp, M.A. Brehm, H.D. Chen, L.K. Selin, and R.M. Welsh. 2003. Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity. 18:631-642.
39. + memory T cells in virus-infected hosts. J. Exp. Med. 183:1367-1375.
40. Mombaerts, P., J. Arnoldi, F. Russ, S. Tonegawa, and S.H. Kaufmann. 1993. Different roles of alpha beta and gamma delta T cells in immunity against an intracellular bacterial pathogen. Nature. 365:53-56.
41. Markiewicz, M.A., C. Girao, J.T. Opferman, J. Sun, Q. Hu, A.A. Agulnik, C.E. Bishop, C.B. Thompson, and P.G. Ashton-Rickardt. 1998. Long-term T cell memory requires the surface expression of self-peptide/major histocompatibility complex molecules. Proc. Natl. Acad. Sci. USA. 95:3065-3070.
42. Rocha, B., and H. von Boehmer. 1991. Peripheral selection of the T cell repertoire. Science. 251:1225-1228.
43. Fleming, T.J., M.L. Fleming, and T.R. Malek. 1993. Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte-differentiation antigen (Gr-1) detects members of the Ly-6 family. J. Immunol. 151:2399-2408.