B7DC/PDL2 promotes tumor immunity by a PD-1-independent mechanism

Journal of Experimental Medicine

Volumn 197, Issue 12, 2003, Pages 1721-1730

  Liu, Xingluo ^a   Xin Gao, Jian ^a   Wen, Jing ^a   Yin, Lijie ^a   Li, Ou ^a   Zuo, Tao ^a   Gajewski, Thomas F ^b   Fu, Yang Xin ^b   Zheng, Pan ^a   Liu, Yang ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

Author keywords

Costimulatory molecules; Cytolytic T lymphocytes; Tumor immunity

Indexed keywords

B7 ANTIGEN; B7DC ANTIGEN; B7H1 ANTIGEN; COMPLEMENTARY DNA; PROTEIN PD 1; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL KILLING; CHO CELL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; FLOW CYTOMETRY; MOUSE; NONHUMAN; PLASMACYTOMA; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN CELL; TRANSGENIC MOUSE; TUMOR IMMUNITY; TUMOR REJECTION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD80; ANTIGENS, NEOPLASM; ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; BLOOD PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; CHO CELLS; CRICETINAE; CYTOTOXICITY, IMMUNOLOGIC; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; NEOPLASMS, EXPERIMENTAL; PEPTIDES; PROTEINS; RECEPTORS, ANTIGEN, T-CELL; SPLEEN; T-LYMPHOCYTES, CYTOTOXIC; TRANSGENES; TRANSPLANTATION CHIMERA; TUMOR CELLS, CULTURED;

EID: 0037867039     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20022089     Document Type: Article

References (34)

1. 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.
2. Freeman, G.J., A.J. Long, Y. Iwai, K. Bourque, T. Chernova, H. Nishimura, L.J. Fitz, N. Malenkovich, T. Okazaki, M.C. Byrne, et al. 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.
3. Yoshinaga, S.K., J.S. Whoriskey, S.D. Khare, U. Sarmiento, J. Guo, T. Horan, G. Shih, M. Zhang, M.A. Coccia, T. Kohno, et al. 1999. T-cell co-stimulation through B7RP-1 and ICOS. Nature. 402:827-832.
4. Swallow, M.M., J.J. Wallin, and W.C. Sha. 1999. B7h, a novel costimulatory homolog of B7.1 and B7.2, is induced by TNFalpha. Immunity. 11:423-432.
5. Chapoval, A.I., J. Ni, J.S. Lau, R.A. Wilcox, D.B. Flies, D. Liu, H. Dong, G.L. Sica, G. Zhu, K. Tamada, et al. 2001. B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production. Nat. Immunol. 2:269-274.
6. Tseng, S.Y., M. Otsuji, K. Gorski, X. Huang, J.E. Slansky, S.I. Pai, A. Shalabi, T. Shin, D.M. Pardoll, and H. Tsuchiya. 2001. B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J. Exp. Med. 193:839-846.
7. Latchman, Y., C.R. Wood, T. Chernova, D. Chaudhary, M. Borde, I. Chernova, Y. Iwai, A.J. Long, J.A. Brown, R. Nunes, et al. 2001. PD-L2 is a second ligand for PD-I and inhibits T cell activation. Nat. Immunol. 2:261-268.
8. Okazaki, T., A. Maeda, H. Nishimura, T. Kurosaki, and T. Honjo. 2001. PD-1 immunoreceptor inhibits B cell receptormediated signaling by recruiting src homology 2-domaincontaining tyrosine phosphatase 2 to phosphotyrosine. Proc. Natl. Acad. Sci. USA. 98:13866-13871.
9. Nishimura, H., and T. Honjo. 2001. PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol. 22:265-268.
10. Nishimura, H., Y. Agata, A. Kawasaki, M. Sato, S. Imamura, N. Minato, H. Yagita, T. Nakano, and T. Honjo. 1996. Developmentally regulated expression of the PD-1 protein on the surface of double-negative (CD4-CD8-) thymocytes. Int. Immunol. 8:773-780.
11. Hudoff, A., A.M. Dittrich, K.C. Beier, B. Eljaschewitsch, R. Kraft, I. Anagnostopoulos, and R.A. Kroczek. 1999. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature. 397:263-266.
12. Ozkaynak, E., W. Gao, N. Shemmeri, C. Wang, J.C. Gutierrez-Ramos, J. Amaral, S. Qin, J.B. Rottman, A.J. Coyle, and W.W. Hancock. 2001. Importance of ICOS-B7RP-1 costimulation in acute and chronic allograft rejection. Nat. Immunol. 2:591-596.
13. Wallin, J.J., L. Liang, A. Bakardjiev, and W.C. Sha. 2001. Enhancement of CD8+ T cell responses by ICOS/B7h costimulation. J. Immunol. 167:132-139.
14. + T lymphocytes in vivo. J. Exp. Med. 194:1339-1348.
15. McAdam, A.J., R.J. Greenwald, M.A. Levin, T. Chernova, N. Malenkovich, V. Ling, G.J. Freeman, and A.H. Sharpe. 2001. ICOS is critical for CD40-mediated antibody class switching. Nature. 409:102-105.
16. Tafuri, A., A. Shahinian, F. Bladt, S.K. Yoshinaga, M. Jordana, A. Wakeham, L.M. Boucher, D. Bouchard, V.S. Chan, G. Duncan, et al. 2001. ICOS is essential for effective T-helpercell responses. Nature. 409:105-109.
17. Dong, C., A.E. Juedes, U.A. Temann, S. Shresta, J.P. Allison, N.H. Ruddle, and R.A. Flavell. 2001. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature. 409:97-101.
18. Iwai, Y., M. Ishida, Y. Tanaka, T. Okazaki, T. Honjo, and N. Minato. 2002. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. USA. 99:12293-12297.
19. Dong, H., S.E. Strome, D.R. Salomao, H. Tamura, F. Hirano, D.B. Flies, P.C. Roche, J. Lu, G. Zhu, K. Tamada, et al. 2002. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8:793-800.
20. Sarma, S., Y. Guo, Y. Guilloux, C. Lee, X.-F. Bai, and Y. Liu. 1999. Cytotoxic T lymphocytes to an unmutated tumor antigen P1A: normal development but restrained effector function. J. Exp. Med. 189:811-820.
21. 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.
22. Cho, B.K., C. Wang, S. Sugawa, H.N. Eisen, and J. Chen. 1999. Functional differences between memory and naive CD8 T cells. Proc. Natl. Acad. Sci. USA. 96:2976-2981.
23. Lyons, A.B., and C.R. Parish. 1994. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods. 171:131-137.
24. Ramarathinam, L., M. Castle, Y. Wu, and Y. Liu. 1994. T cell costimulation by B7/BB1 induces CD8 T cell-dependent tumor rejection: an important role of B7/BB1 in the induction, recruitment, and effector function of antitumor T cells. J. Exp. Med. 179:1205-1214.
25. Ramarathinam, L., S. Sarma, M. Maric, M. Zhao, G. Yang, L. Chen, and Y. Liu. 1995. Multiple lineages of tumors express a common tumor antigen, P1A, but they are not crossprotected. J. Immunol. 155:5323-5329.
26. Zheng, P., Y. Guo, Q. Niu, D.E. Levy, J.A. Dyck, S. Lu, L.A. Sheiman, and Y. Liu. 1998. Proto-oncogene PML controls genes devoted to MHC class I antigen presentation. Nature. 396:373-376.
27. Bai, X.-F., J.-X. Gao, Q. Liu, J. Wen, P. Zheng, and Y. Liu. 2001. On the site and mode of antigen presentation for the initiation of clonal expansion of CD8 T cells specific for a natural tumor antigen. Cancer Res. 61:6860-6867.
28. Ishida, M., Y. Iwai, Y. Tanaka, T. Okazaki, G. Freeman, N. Minato, and T. Honjo. 2002. Differential expression of PDL1 and PD-L2, ligands for an inhibitory receptor PD-1, in the cells of lymphohematopoietic tissues. Immunol. Lett. 84:57-62.
29. Zheng, P., S. Sarma, Y. Guo, and Y. Liu. 1999. Two mechanisms for tumor evasion of preexisting cytotoxic T-cell responses: lessons from recurrent tumors. Cancer Res. 59:3461-3467.
30. Lee, P.P., C. Yee, P.A. Savage, L. Fong, D. Brockstedt, J.S. Weber, D. Johnson, S. Swetter, J. Thompson, P.D. Greenberg, et al. 1999. Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 5:677-685.
31. Romero, P., P.R. Dunbar, D. Valmori, M. Pittet, G.S. Ogg, D. Rimoldi, J.L. Chen, D. Lienard, J.C. Cerottini, and V. Cerundolo. 1998. Ex vivo staining of metastatic lymph nodes by class I major histocompatibility complex tetramers reveals high numbers of antigen-experienced tumor-specific cytolytic T lymphocytes. J. Exp. Med. 188:1641-1650.
32. Nishimura, H., T. Honjo, and N. Minato. 2000. Facilitation of beta selection and modification of positive selection in the thymus of PD-1-deficient mice. J. Exp. Med. 191:891-898.
33. Guo, Y., Y. Wu, M. Zhao, X.P. Kong, and Y. Liu. 1995. Mutational analysis and an alternatively spliced product of B7 defines its CD28/CTLA4-binding site on immunoglobulin C-like domain. J. Exp. Med. 181:1345-1355.
34. Peach, R.J., J. Bajorath, J. Naemura, G. Leytze, J. Greene, A. Aruffo, and P.S. Linsley. 1995. Both extracellular immunoglobin-like domains of CD80 contain residues critical for binding T cell surface receptors CTLA-4 and CD28. J. Biol. Chem. 270:21181-21187.