The programmed death-1 and interleukin-10 pathways play a down-modulatory role in LP-BM5 retrovirus-induced murine immunodeficiency syndrome

Journal of Virology

Volumn 82, Issue 5, 2008, Pages 2456-2469

  Green, Kathy A ^a   Okazaki, Taku ^b   Honjo, Tasuku ^b   Cook, W James ^a,d   Green, William R ^a,c  

^a NORRIS COTTON CANCER CENTER   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; INTERLEUKIN 10; PROGRAMMED DEATH 1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DOWN REGULATION; HYPERGAMMAGLOBULINEMIA; IMMUNE DEFICIENCY; INOCULATION; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RETROVIRUS; RODENT DISEASE; SPLEEN CELL; SPLENOMEGALY; VIRUS LOAD; VIRUS STRAIN; WILD TYPE;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; DOWN-REGULATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGIC DEFICIENCY SYNDROMES; INTERLEUKIN-10; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RETROVIRIDAE;

MURINAE; MUS;

EID: 39749134841     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01665-07     Document Type: Article

References (74)

1. Agata, Y., A. Kawasaki, H. Nishimura, Y. Ishida, T. Tsubata, H. Yaglta, 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.
2. Ahonen, C. L., E. M. Manning, L. D. Erickson, B. P. O'Connor, E. F. Lind, S. S. Pullen, M. R. Kehry, and R. J. Noelle. 2002. The CD40-TRAF6 axis controls affinity maturation and the generation of long-lived plasma cells. Nat. Immunol. 3:451-452.
3. Aziz, D. C., Z. Hanna, and P. Jolicoeur. 1989. Severe immunodeficiency disease induced by a defective murine leukemia virus. Nature 338:505-508.
4. Badou, A., Y. Bennasser, M. Moreau, C. Leclerc, M. Benkirane, and E. Bahraoui. 2000. Tat protein of human immunodeficiency virus type I induces interleukin-10 in human peripheral blood monocytes: implication of protein kinase C-dependent pathway. J. Virol. 74:10551-10562.
5. + T cells during chronic viral infection. Nature 439:682-687.
6. Blocki, F. A., S. Radhakrishnan, V. P. Van Keulen, K. L. Heckman, B. Ciric, C. L. Howe, M. Rodriguez, E. Kwon, and L. R. Pease. 2006. Induction of a gene expression program in dendritic cells with a cross-linking IgM antibody to the co-stimulatory molecule B7-DC. FASEB J. 20:2408-2410.
7. Brooks, D. G., M. J. Trifilo, K. H. Edelmann, L. Teyton, D. B. McGavern, and M. B. A. Oldstone. 2006. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 12:1301-1309.
8. Buller, R. M. L., R. A. Yetter, T. N. Fredrickson, and H. C. Morse III. 1987. Abrogation of resistance to severe mousepox in C57BL/6 mice infected with LP-BM5 murine leukemia viruses. J. Virol. 61:383-387.
9. Carreno, B. M., and M. Collins. 2002. The B7 family of ligands and its receptors: new pathways for costimulation and inhibition of immune responses. Annu. Rev. Immunol. 20:29-53.
10. Cerny, A. A., W. Hugin, R. R. Hardy, K. Hayakawa, R. M. Zinkernagel, M. Makino, and H. C. Morse III. 1990. B cells are required for induction of T cell abnormalities in a murine retrovirus-induced immunodeficiency syndrome. J. Exp. Med. 171:315-320.
11. Chattopadhyay, S. K., H. C. Morse III, M. Makino, S. K. Ruscetti, and J. W. Hartley. 1989. A defective virus is associated with induction of a murine retrovirus-induced immunodeficiency syndrome, MAIDS. Proc. Natl. Acad. Sci. USA 86:3862-3866.
12. Cook, W. J., K. A. Green, J. J. Obar, and W. R. Green. 2003. Quantitative analysis of LP-BM5 murine leukemia retrovirus RNA using real-time RT-PCR. J. Virol. Methods 108:49-58.
13. Curiel, T. J., S. Wei, H. Dong, X. Alvarez, P. Cheng, P. Mottram, R. Krzysiek, K. L. Knutson, B. Daniel, M. C. Zimmermann, O. David, M. Burow, A. Gordon, N. Dhurandhar, L. Myers, R. Berggren, A. Hemminki, R. D. Alvarez, D. Emilie, D. T. Curiel, L. Chen, and W. Zou. 2003. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat. Med. 9:562-567.
14. 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, Z. Mncube, J. Duraiswamy, B. Zhu, Q. Eichbaum, M. Altfeld, E. J. Wherry, H. M. Coovadia, P. J. R. Goulder, P. Klenerman, R. Ahmed, G. J. Freeman, and B. D. Walker. 2006. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443:350-354.
15. Dong, H., G. Zhu, K. Tamada, and L. Chen. 1999. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat. Med. 5:1365-1369.
16. Dong, H., S. E. Strome, D. R. Salomao, H. Tamura, F. Hirano, D. B. Flies, P. C. Roche, J. Lu, G. Zhu, K. Tamada, V. A. Lennnon, E. Celis, and L. Chen. 2002. Tumor associated B7-H1 promotes T cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8:793-800.
17. Ejrnaes, M., C. M. Filippi, M. M. Martinic, E. M. Ling, L. M. Togher, S. Crotty, and M. G. Von Herrath. 2006. Resolution of a chronic viral infection after interleukin-10 receptor blockade. J. Exp. Med. 203:2461-2472.
18. Freeman, G. J., A. J. Long, Y. Iwai, K. Bourque, T. Chernova, H. Nishimura, L. J. Fitz, N. Malenkovich, T. Okazaki, M. C. Byrne, H. F. Horton, L. Fouser, L. Carter, V. Ling, M. R. Bowman, B. M. Carreno, M. Collins, C. R. Wood, and T. Honjo. 2000. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192:1027-1034.
19. Freeman, G. J., E. J. Wherry, R. Ahmed, and A. H. Sharpe. 2006. Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J. Exp. Med. 203:2223-2227.
20. Green, K. A., C. L. Ahonen, W. J. Cook, and W. R. Green. 2004. CD40-Associated TRAF 6 signaling is required for disease induction in a retrovirus-induced murine immunodeficiency. J. Virol. 78:6055-6060.
21. Green, K. A., K. M. Crassi, J. D. Laman, A. Schoneveld, R. R. Strawbridge, T. M. Foy, R. J. Noelle, and W. R. Green. 1996. Antibody to the ligand for CD40 (gp39) inhibits murine AIDS-associated splenomegaly, hypergammaglobulinemia, and immunodeficiency in disease-susceptible C57BL/6 mice. J. Virol. 70:2569-2575.
22. Green, K. A., R. J. Noelle, and W. R. Green. 1998. Evidence for a continued requirement for CD40/CD40 ligand (CD154) interactions in the progression of LP-BM5 retrovirus-induced murine AIDS. Virology 241:260-268.
23. Green, K. A., R. J. Noelle, B. G. Durell, and W. R. Green. 2001. Characterization of the CD154-positive and CD40-positive cellular subsets required for pathogenesis in retrovirus-induced murine immunodeficiency. J. Virol. 75:3581-3589.
24. Green, K. A., W. J. Cook, A. H. Sharp, and W. R. Green. 2002. The CD154/CD40 interaction required for retrovirus-induced murine immunodeficiency syndrome is not mediated by upregulation of the CD80/CD86 costimulatory molecules. J. Virol. 76:13106-13110.
25. Greenwald, R. J., G. J. Freeman, and A. H. Sharpe. 2005. The B7 family revisited. Annu. Rev. Immunol. 23:515-548.
26. Hartley, J. W., T. N. Fredrickson, R. A. Yetter, M. Makino, and H. C. Morse III. 1989. Retrovirus-induced murine acquired immunodeficiency syndrome: natural history of infection and differing susceptibility of inbred mouse strains. J. Virol. 63:1223-1230.
27. + T cells directed against a cryptic epitope derived from a retroviral alternative reading frame confer disease protection. J. Immunol. 176:2470-2475.
28. Huang, M., C. Simard, and P. Jolicoeur. 1989. Immunodeficiency and clonal growth of target cells induced by helper-free defective retrovirus. Science 246:1614-1617.
29. Ishida, M., Y. Iwai, Y. Tanaka, T. Okazaki, G. J. Freeman, N. Minato, and T. Honjo. 2002. Differential expression of PD-L1 and PD-L2, ligands for an inhibitory receptor PD-1, in the cells of lymphohematopoietic tissues. Immunol. Lett. 84:57-62.
30. 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.
31. + T cell effectors functions after antigen recognition in the liver. Immunity 23:53-63.
32. Jones, K. W., and C. J. Hackett. 1996. Activated T hybridomas induce upregulation of B7-1 on bystander B lymphoma cells by a contact-dependent interaction utilizing CD40 ligand. Cell. Immunol. 174:42-53.
33. Klinken, S. P., T. N. Fredrickson, J. W. Hartley, R. A. Yetter, and H. C. Morse III. 1988. Evolution of B cell lineage lymphomas in mice with a retrovirus-induced immunodeficiency syndrome, MAIDS. J. Immunol. 140:1123-1131.
34. Klinman, D. M., and H. C. Morse III. 1989. Characteristics of B cell proliferation and activation in murine AIDS. J. Immunol. 142:1144-1149.
35. Knoetig, S. M., T. A. Torrey, Z. Naghashfar, T. McCarty, and H. C. Morse III. 2002. CD19 signaling pathways play a major role for murine AIDS induction and progression. J. Immunol. 169:5607-56614.
36. Kühn, R., D. J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263-274.
37. Kuhné, M. R., M. Robbins, J. E. Hambor, M. F. Mackey, Y. Kosaka, T. Nishimura, J. P. Gigley, R. J. Noelle, and D. M. Calderhead. 1997. Assembly and regulation of the CD40 receptor complex in human B cells. J. Exp. Med. 186:337-342.
38. + T cell activation. Eur. J. Immunol. 36:2472-2482.
39. Latchman, Y., C. R. Wood, T. Chernova, D. Chaudhary, M. Borde, I. Chernova, Y. Iwai, A. J. Long, J. A. Brown, R. Nunes, E. A. Greenfield, K. Bourque, V. A. Boussiotis, L. L. Carter, B. M. Carreno, N. Malenkovich, H. Nishimura, T. Okazaki, T. Honjo, A. H. Sharpe, and G. J. Freeman. 2001. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2:261-268.
40. Legrand, E., R. Daculsi, and J. F. Duplan. 1981. Characteristics of the cell populations involved in extrathymic lymphosarcoma induced in C57BL/6 mice by RadLV-RS. Leuk. Res. 5:223-233.
41. + T cell receptor ligation needed? Virology 360:58-71.
42. + T cells in the pathogenesis of murine AIDS. J. Virol. 80:5777-5789.
43. + T cell clones to induce noncognate contact-dependent polyclonal B cell activation. J. Immunol. 146:3413-3418.
44. Mayrand, S. M., D. A. Schwarz, and W. R. Green. 1998. An alternative translational reading frame encodes an immunodominant retroviral CTL determinant expressed by an immunodeficiency causing retrovirus. J. Immunol. 160:39-50.
45. 1 mice. Virology 272:438-449.
46. Morse, H. C., III, R. A. Yetter, C. S. Via, R. R. Hardy, A. Cerny, K. Hayakawa, A. W. Hugin, M. W. Miller, K. L. Homes, and G. M. Shearer. 1989. Functional and phenotypic alterations in T cell subsets during the course of MAIDS, a murine retrovirus-induced immunodeficiency syndrome. J. Immunol. 143:844-850.
47. Mosier, D. E., R. A. Yetter, and H. C. Morse III. 1985. Retroviral induction of acute lymphoproliferative disease and profound immunosuppression in adult C57BL/6 mice. J. Exp. Med. 161:766-784.
48. Mosier, D. E., R. A. Yetter, and H. C. Morse III. 1987. Functional T lymphocytes are required for a murine retrovirus-induced immunodeficiency disease (MAIDS). J. Exp. Med. 165:1732-1742.
49. Müller, F., P. Aukrust, I. Nordoy, and S. S. Froland. 1998. Possible role of interleukin-10 (IL-10) and CD40 ligand expression in the pathogenesis of hypergammaglobulinemia in human immunodeficiency virus infection: modulation of IL-10 and Ig production after intravenous Ig infusion. Blood 92:3721-3729.
50. Nishimura, H., N. Minato, T. Nakano, and T. Honjo. 1998. Immunological studies on PD-1-deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int. Immunol. 10:1563-1572.
51. Okazaki, T., and T. Honjo. 2006. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol. 27:195-201.
52. Okazaki, T., Y. Iwai, and T. Honjo. 2002. New regulatory co-receptors: inducible costimulator and PD-1. Curr. Opin. Immunol. 14:779-782.
53. Okazaki, T., A. Maeda, H. Nishimura, T. Kurosaki, and T. Honjo. 2001. PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc. Natl. Acad. Sci. USA 98:13866-13871.
54. Pattengale, P. K., C. R. Taylor, P. Twomey, S. Hill, J. Jonasson, T. Beardsley, and M. Haas. 1982. Immunopathology of B cell lymphomas induced in C57BL/6 mice by dualtropic murine leukemia virus (MuLV). Am. J. Pathol. 107:362-377.
55. + T cell survival in HIV infection. J. Exp. Med. 203:2281-2292.
56. Pullen, S. S., H. G. Miller, D. S. Everdeen, T. T. Dang, J. J. Crute, and M. R. Kehry. 1998. CD40-tumor necrosis factor receptor-associated factor (TRAF) interactions: regulation of CD40 signaling through multiple TRAF binding sites and TRAF hetero-oligomerization. Biochemistry 37:11836-11845.
57. Pullen, S. S., T. T. Dang, J. J. Crute, and M. R. Kehry. 1999. CD40 signaling through tumor necrosis factor receptor-associated factors (TRAFs). Binding specificity and activation of downstream pathways by distinct TRAFs. J. Biol. Chem. 274:14246-14254.
58. Ranheim, E. A., and T. J. Kipps. 1995. Tumor necrosis factor facilitates induction of CD80 (B7-1) and CD54 on human B cells by activated T cells: complex regulation by IL-4, IL-10 and CD40L. Cell. Immunol. 161:226-235.
59. Ranheim, E. A., and T. J. Kipps. 1993. Activated T cells induce expression of B7/BB1 on normal or leukemic B cells through a CD40-dependent signal. J. Exp. Med. 177:925-935.
60. Rowe, W. P., W. E. Pugh, and J. W. Hartley. 1970. Plaque assay techniques for murine leukemia viruses. Virology 42:1136.
61. Roy, M., A. Aruffo, J. Ledbetter, P. Linsley, M. Kehry, and R. Noelle. 1995. Studies on the interdependence of gp39 and B7 expression and function during antigen-specific immune responses. Eur. J. Immunol. 25:596-603.
62. Saunders, P. A., V. R. Hendrycks, W. A. Lindinsky, and M. L. Woods. 2005. PD-L2:PD-1 involvement in T cell proliferation, cytokine production, and integrin-mediated adhesion. Eur. J. Immunol. 35:3561-3569.
63. Schwarz, D. A., and W. R. Green. 1994. CTL responses to the gag polyprotein encoded by the murine AIDS defective retrovirus are strain dependent. J. Immunol. 153:436-441.
64. Selenko-Gebauer, N., O. Majdic, A. Szekeres, G. Höfler, E. Guthann, U. Korthäuer, G. Zlabinger, P. Steinberger, W. F. Pickl, H. Stockinger, W. Knapp, and J. Stöckt 2003. B7-H1 (programmed death-1 ligand) on dendritic cells is involved in the induction and maintenance of T cell anergy. J. Immunol. 170:3637-3644.
65. Sharpe, A. H., E. J. Wherry, R. Ahmed, and G. J. Freeman. 2007. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat. Immunol. 8:239-245.
66. Simard, C., S. J. Klein, T. Mak, and P. Jolicoeur. 1997. Studies of the susceptibility of nude, CD4 knockout, and SCID mutant mice to the disease induced by the murine AIDS defective virus. J. Virol. 71:3013-3022.
67. Strome, S. E., H. Dong, H. Tamura, S. G. Voss, D. B. Flies, K. Tamada, D. Salomao, J. Cheville, F. Hirano, W. Lin, J. L. Kasperbauer, K. V. Ballman, and L. Chen. 2003. B7-H1 blockade augments adoptive T-cell immunotherapy for squamous cell carcinoma. Cancer Res. 63:6501-6505.
68. Tamura, H., H. Dong, G. Zhu, G. L. Sica, D. B. Flies, K. Tamada, and L. Chen. 2001. B7-H1 costimulation preferentially enhances CD28-independent T-helper cell function. Blood 97:1809-1816.
69. + T cells leads to reversible immune dysfunction. Nat. Med. 12:1198-1202.
70. Urbani, S., B. Amadei, D. Tola, M. Massari, S. Schivazappa, G. Missale, and C. Ferrari. 2006. PD-1 expression in acute hepatitis C virus (HCV) infection is associated with HCV-specific CD8 exhaustion. J. Virol. 80:11398-11403.
71. Van Keulen, V. P., B. Ciric, S. Radhakrishnan, K. L. Heckman, Y. Mitsunaga, K. Iijima, H. Kita, M. Rodriquez, and L. R. Pease. 2006. Immunomodulation using the recombinant monoclonal human B7-DC cross-linking antibody rHIgM12. Clin. Exp. Immunol. 143:314-321.
72. Yamazaki, T., A. Hisaya, H. Iwai, H. Matsuda, M. Aoki, Y. Tanno, T. Shin, H. Tsuchiya, D. Pardoll, K. Okumura, M. Azuma, and H. Yagita. 2002. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 169:5538-5545.
73. + T cells are required for development of a murine retrovirus-induced immunodeficiency syndrome (MAIDS). J. Exp. Med. 168:623-635.
74. Yu, P., R. A. Morawetz, S. Chattopadhyay, M. Makino, T. Kishimoto, and H. Kikutani. 1999. CD40-deficient mice infected with the defective murine leukemia virus LP-BM5def do not develop murine AIDS but produce IgE and IgG1 in vivo. Eur. J. Immunol. 29:615-625.