Structure and cancer immunotherapy of the B7 family member B7x

Cell Reports

Volumn 9, Issue 3, 2014, Pages 1089-1098

  Jeon, Hyungjun ^a   Vigdorovich, Vladimir ^a,c   Garrett Thomson, Sarah C ^a   Janakiram, Murali ^a   Ramagopal, Udupi A ^a   Abadi, Yael M ^a,d   Lee, Jun Sik ^a,e   Scandiuzzi, Lisa ^a   Ohaegbulam, Kim C ^a   Chinai, Jordan M ^a   Zhao, Ruihua ^a,f   Yao, Yu ^b   Mao, Ying ^b   Sparano, Joseph A ^a   Almo, Steven C ^a   Zang, Xingxing ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b FUDAN UNIVERSITY   (China)

^c Seattle BioMed   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Chosun University   (South Korea)

^f FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; B7X PROTEIN; IMMUNOGLOBULIN F(AB) FRAGMENT; IMMUNOMODULATING AGENT; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 12D11; MONOCLONAL ANTIBODY 15D12; MONOCLONAL ANTIBODY 1H3; MUTANT PROTEIN; UNCLASSIFIED DRUG; EPITOPE; PROTEIN BINDING; V SET DOMAIN CONTAINING T CELL ACTIVATION INHIBITOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN BINDING; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG EFFICACY; DRUG MECHANISM; DRUG PROTEIN BINDING; DRUG SCREENING; EMBRYO; EPITOPE MAPPING; FEMALE; HUMAN; HUMAN CELL; IMMUNOGLOBULIN VARIABLE REGION; IN VIVO STUDY; LUNG METASTASIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN TARGETING; TUMOR CELL DESTRUCTION; TUMOR VOLUME; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; IMMUNOTHERAPY; METABOLISM; NATURAL KILLER CELL; NEOPLASMS; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; SURFACE PLASMON RESONANCE; SURVIVAL; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; X RAY CRYSTALLOGRAPHY;

MUS;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; CELL PROLIFERATION; CRYSTALLOGRAPHY, X-RAY; DISEASE MODELS, ANIMAL; EPITOPE MAPPING; EPITOPES; HUMANS; IMMUNOSUPPRESSION; IMMUNOTHERAPY; KILLER CELLS, NATURAL; LYMPHOCYTES, TUMOR-INFILTRATING; MICE, INBRED BALB C; MODELS, MOLECULAR; NEOPLASMS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SURFACE PLASMON RESONANCE; SURVIVAL ANALYSIS; T-LYMPHOCYTES; TUMOR MICROENVIRONMENT; V-SET DOMAIN-CONTAINING T-CELL ACTIVATION INHIBITOR 1;

EID: 84919775114     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.09.053     Document Type: Article

References (54)

1. Abadi, Y.M., Jeon, H., Ohaegbulam, K.C., Scandiuzzi, L., Ghosh, K., Hofmeyer, K.A., Lee, J.S., Ray, A., Gravekamp, C., and Zang, X. (2013). Host b7x promotes pulmonary metastasis of breast cancer. J. Immunol. 190, 3806-3814.
2. Aslakson, C.J., and Miller, F.R. (1992). Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res. 52, 1399-1405.
3. Awadallah, N.S., Shroyer, K.R., Langer, D.A., Torkko, K.C., Chen, Y.K., Bentz, J.S., Papkoff, J., Liu, W., Nash, S.R., and Shah, R.J. (2008). Detection of B7-H4 and p53 in pancreatic cancer: potential role as a cytological diagnostic adjunct. Pancreas 36, 200-206.
4. Barach, Y.S., Lee, J.S., and Zang, X. (2011). T cell coinhibition in prostate cancer: new immune evasion pathways and emerging therapeutics. Trends Mol. Med. 17, 47-55.
5. Battye, T.G., Kontogiannis, L., Johnson, O., Powell, H.R., and Leslie, A.G. (2011). iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281.
6. Brahmer, J.R., Tykodi, S.S., Chow, L.Q., Hwu, W.J., Topalian, S.L., Hwu, P., Drake, C.G., Camacho, L.H., Kauh, J., Odunsi, K., et al. (2012). Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366, 2455-2465.
7. Chen, L.J., Sun, J., Wu, H.Y., Zhou, S.M., Tan, Y., Tan, M., Shan, B.E., Lu, B.F., and Zhang, X.G. (2011). B7-H4 expression associates with cancer progression and predicts patient's survival in human esophageal squamous cell carcinoma. Cancer Immunol. Immunother. 60, 1047-1055.
8. Choi, I.H., Zhu, G., Sica, G.L., Strome, S.E., Cheville, J.C., Lau, J.S., Zhu, Y., Flies, D.B., Tamada, K., and Chen, L. (2003). Genomic organization and expression analysis of B7-H4, an immune inhibitory molecule of the B7 family. J. Immunol. 171, 4650-4654.
9. Clynes, R.A., Towers, T.L., Presta, L.G., and Ravetch, J.V. (2000). Inhibitory Fc receptors modulate in vivo cytotoxicity against tumor targets. Nat. Med. 6, 443-446.
10. Dangaj, D., Lanitis, E., Zhao, A., Joshi, S., Cheng, Y., Sandaltzopoulos, R., Ra, H.J., Danet-Desnoyers, G., Powell, D.J., Jr., and Scholler, N. (2013). Novel recombinant human b7-h4 antibodies overcome tumoral immune escape to potentiate T-cell antitumor responses. Cancer Res. 73, 4820-4829.
11. Emsley, P., Lohkamp, B., Scott, W.G., and Cowtan, K. (2010). Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501.
12. Fiocco, U., Sfriso, P., Oliviero, F., Pagnin, E., Scagliori, E., Campana, C., Dainese, S., Cozzi, L., and Punzi, L. (2008). Co-stimulatory modulation in rheumatoid arthritis: the role of (CTLA4-Ig) abatacept. Autoimmun. Rev. 8, 76-82.
13. Fourcade, J., Sun, Z., Benallaoua, M., Guillaume, P., Luescher, I.F., Sander, C., Kirkwood, J.M., Kuchroo, V., and Zarour, H.M. (2010). Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J. Exp. Med. 207, 2175-2186.
14. Fridlender, Z.G., Sun, J., Kim, S., Kapoor, V., Cheng, G., Ling, L., Worthen, G.S., and Albelda, S.M. (2009). Polarization of tumor-associated neutrophil phenotype by TGF-beta: "N1" versus "N2" TAN. Cancer Cell 16, 183-194.
15. Goding, S.R., Wilson, K.A., Xie, Y., Harris, K.M., Baxi, A., Akpinarli, A., Fulton, A., Tamada, K., Strome, S.E., and Antony, P.A. (2013). Restoring immune function of tumor-specific CD4+ T cells during recurrence of melanoma. J. Immunol. 190, 4899-4909.
16. Greenwald, R.J., Freeman, G.J., and Sharpe, A.H. (2005). The B7 family revisited. Annu. Rev. Immunol. 23, 515-548.
17. Hodi, F.S., O'Day, S.J., McDermott, D.F., Weber, R.W., Sosman, J.A., Haanen, J.B., Gonzalez, R., Robert, C., Schadendorf, D., Hassel, J.C., et al. (2010). Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363, 711-723.
18. Hofmeyer, K.A., Scandiuzzi, L., Ghosh, K., Pirofski, L.A., and Zang, X. (2012). Tissue-expressed B7x affects the immune response to and outcome of lethal pulmonary infection. J. Immunol. 189, 3054-3063.
19. Huang, A.Y., Gulden, P.H., Woods, A.S., Thomas, M.C., Tong, C.D., Wang, W., Engelhard, V.H., Pasternack, G., Cotter, R., Hunt, D., et al. (1996). The immunodominant major histocompatibility complex class I-restricted antigen of a murine colon tumor derives from an endogenous retroviral gene product. Proc. Natl. Acad. Sci. USA 93, 9730-9735.
20. Isitman, G., Stratov, I., and Kent, S.J. (2012). Antibody-dependent cellular cytotoxicity and NK cell-driven immune escape in HIV infection: implications for HIV vaccine development. Adv. Virol. 2012, 637208.
21. Janakiram, M., Abadi, Y.M., Sparano, J.A., and Zang, X. (2012). T cell coinhibition and immunotherapy in human breast cancer. Discov. Med. 14, 229-236.
22. Jeon, H., Ohaegbulam, K.C., Abadi, Y.M., and Zang, X. (2013). B7x and myeloid-derived suppressor cells in the tumor microenvironment: A tale of two cities. OncoImmunology 2, e24744.
23. Jiang, J., Zhu, Y., Wu, C., Shen, Y., Wei, W., Chen, L., Zheng, X., Sun, J., Lu, B., and Zhang, X. (2010). Tumor expression of B7-H4 predicts poor survival of patients suffering from gastric cancer. Cancer Immunol. Immunother. 59, 1707-1714.
24. Kohrt, H.E., Houot, R., Marabelle, A., Cho, H.J., Osman, K., Goldstein, M., Levy, R., and Brody, J. (2012). Combination strategies to enhance antitumor ADCC. Immunotherapy 4, 511-527.
25. Krambeck, A.E., Thompson, R.H., Dong, H., Lohse, C.M., Park, E.S., Kuntz, S.M., Leibovich, B.C., Blute, M.L., Cheville, J.C., and Kwon, E.D. (2006). B7-H4 expression in renal cell carcinoma and tumor vasculature: associations with cancer progression and survival. Proc. Natl. Acad. Sci. USA 103, 10391-10396.
26. Langer, G., Cohen, S.X., Lamzin, V.S., and Perrakis, A. (2008). Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179.
27. Lázár-Molnár, E., Yan, Q., Cao, E., Ramagopal, U., Nathenson, S.G., and Almo, S.C. (2008). Crystal structure of the complex between programmed death-1 (PD-1) and its ligand PD-L2. Proc. Natl. Acad. Sci. USA 105, 10483-10488.
28. Lee, J.S., Scandiuzzi, L., Ray, A., Wei, J., Hofmeyer, K.A., Abadi, Y.M., Loke, P., Lin, J., Yuan, J., Serreze, D.V., et al. (2012). B7x in the periphery abrogates pancreas-specific damage mediated by self-reactive CD8 T cells. J. Immunol. 189, 4165-4174.
29. Lin, D.Y., Tanaka, Y., Iwasaki, M., Gittis, A.G., Su, H.P., Mikami, B., Okazaki, T., Honjo, T., Minato, N., and Garboczi, D.N. (2008). The PD-1/PD-L1 complex resembles the antigen-binding Fv domains of antibodies and T cell receptors. Proc. Natl. Acad. Sci. USA 105, 3011-3016.
30. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255.
31. Prasad, D.V., Richards, S., Mai, X.M., and Dong, C. (2003). B7S1, a novel B7 family member that negatively regulates T cell activation. Immunity 18, 863-873.
32. Quandt, D., Fiedler, E., Boettcher, D., Marsch, W.Ch., and Seliger, B. (2011). B7-h4 expression in human melanoma: its association with patients' survival and antitumor immune response. Clin. Cancer Res. 17, 3100-3111.
33. Roda, J.M., Wang, Y., Sumner, L.A., Phillips, G.S., Marsh, C.B., and Eubank, T.D. (2012). Stabilization of HIF-2a induces sVEGFR-1 production from tumorassociated macrophages and decreases tumor growth in a murine melanoma model. J. Immunol. 189, 3168-3177.
34. Roland, C.L., Lynn, K.D., Toombs, J.E., Dineen, S.P., Udugamasooriya, D.G., and Brekken, R.A. (2009). Cytokine levels correlate with immune cell infiltration after anti-VEGF therapy in preclinical mouse models of breast cancer. PLoS ONE 4, e7669.
35. Scandiuzzi, L., Ghosh, K., and Zang, X. (2011). T cell costimulation and coinhibition: genetics and disease. Discov. Med. 12, 119-128.
36. Schwartz, J.C., Zhang, X., Fedorov, A.A., Nathenson, S.G., and Almo, S.C. (2001). Structural basis for co-stimulation by the human CTLA-4/B7-2 complex. Nature 410, 604-608.
37. Sharma, P., Wagner, K., Wolchok, J.D., and Allison, J.P. (2011). Novel cancer immunotherapy agents with survival benefit: recent successes and next steps. Nat. Rev. Cancer 11, 805-812.
38. Sheldrick, G.M. (2008). A short history of SHELX. Acta Crystallogr. A 64, 112-122.
39. Sica, G.L., Choi, I.H., Zhu, G., Tamada, K., Wang, S.D., Tamura, H., Chapoval, A.I., Flies, D.B., Bajorath, J., and Chen, L. (2003). B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 18, 849-861.
40. Stamper, C.C., Zhang, Y., Tobin, J.F., Erbe, D.V., Ikemizu, S., Davis, S.J., Stahl, M.L., Seehra, J., Somers, W.S., and Mosyak, L. (2001). Crystal structure of the B7-1/CTLA-4 complex that inhibits human immune responses. Nature 410, 608-611.
41. Sun, Y., Wang, Y., Zhao, J., Gu, M., Giscombe, R., Lefvert, A.K., and Wang, X. (2006). B7-H3 and B7-H4 expression in non-small-cell lung cancer. Lung Cancer 53, 143-151.
42. Topalian, S.L., Hodi, F.S., Brahmer, J.R., Gettinger, S.N., Smith, D.C., McDermott, D.F., Powderly, J.D., Carvajal, R.D., Sosman, J.A., Atkins, M.B., et al. (2012). Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443-2454.
43. Tringler, B., Zhuo, S., Pilkington, G., Torkko, K.C., Singh, M., Lucia, M.S., Heinz, D.E., Papkoff, J., and Shroyer, K.R. (2005). B7-h4 is highly expressed in ductal and lobular breast cancer. Clin. Cancer Res. 11, 1842-1848.
44. Vigdorovich, V., Ramagopal, U.A., Lázár-Molnár, E., Sylvestre, E., Lee, J.S., Hofmeyer, K.A., Zang, X., Nathenson, S.G., and Almo, S.C. (2013). Structure and T cell inhibition properties of B7 family member, B7-H3. Structure 21, 707-717.
45. Vincenti, F., Dritselis, A., and Kirkpatrick, P. (2011). Belatacept. Nat. Rev. Drug Discov. 10, 655-656.
46. Wei, J., Loke, P., Zang, X., and Allison, J.P. (2011). Tissue-specific expression of B7x protects from CD4 T cell-mediated autoimmunity. J. Exp. Med. 208, 1683-1694.
47. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G., McCoy, A., et al. (2011). Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242.
48. Zang, X., and Allison, J.P. (2007). The B7 family and cancer therapy: costimulation and coinhibition. Clin. Cancer Res. 13, 5271-5279.
49. Zang, X., Loke, P., Kim, J., Murphy, K., Waitz, R., and Allison, J.P. (2003). B7x: a widely expressed B7 family member that inhibits T cell activation. Proc. Natl. Acad. Sci. USA 100, 10388-10392.
50. Zang, X., Thompson, R.H., Al-Ahmadie, H.A., Serio, A.M., Reuter, V.E., Eastham, J.A., Scardino, P.T., Sharma, P., and Allison, J.P. (2007). B7-H3 and B7x are highly expressed in human prostate cancer and associated with disease spread and poor outcome. Proc. Natl. Acad. Sci. USA 104, 19458-19463.
51. Zang, X., Sullivan, P.S., Soslow, R.A., Waitz, R., Reuter, V.E., Wilton, A., Thaler, H.T., Arul, M., Slovin, S.F., Wei, J., et al. (2010). Tumor associated endothelial expression of B7-H3 predicts survival in ovarian carcinomas. Mod. Pathol. 23, 1104-1112.
52. Zhao, R., Chinai, J.M., Buhl, S., Scandiuzzi, L., Ray, A., Jeon, H., Ohaegbulam, K.C., Ghosh, K., Zhao, A., Scharff, M.D., and Zang, X. (2013). HHLA2 is a member of the B7 family and inhibits human CD4 and CD8 T-cell function. Proc. Natl. Acad. Sci. USA 110, 9879-9884.
53. Zhou, Q., Munger, M.E., Veenstra, R.G., Weigel, B.J., Hirashima, M., Munn, D.H., Murphy, W.J., Azuma, M., Anderson, A.C., Kuchroo, V.K., and Blazar, B.R. (2011). Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia. Blood 117, 4501-4510.
54. Zhu, Y., Yao, S., Iliopoulou, B.P., Han, X., Augustine, M.M., Xu, H., Phennicie, R.T., Flies, S.J., Broadwater, M., Ruff, W., et al. (2013). B7-H5 costimulates human T cells via CD28H. Nat Commun 4, 2043.