Novel recombinant human B7-H4 antibodies overcome tumoral immune escape to potentiate T-cell antitumor responses

Cancer Research

Volumn 73, Issue 15, 2013, Pages 4820-4829

  Dangaj, Denarda ^a,c   Lanitis, Evripidis ^a,c   Zhao, Aizhi ^a   Joshi, Shree ^a   Cheng, Yi ^a   Sandaltzopoulos, Raphael ^c   Ra, Hyun Jeong ^b   Danet Desnoyers, Gwenn ^b   Powell Jr , Daniel J ^a   Scholler, Nathalie ^d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^d SRI INTERNATIONAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TUMOR ANTIGEN; V SET DOMAIN CONTAINING T CELL ACTIVATION INHIBITOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN BINDING; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; ASCITES; CANCER CELL CULTURE; CANCER INHIBITION; CELLULAR IMMUNITY; COCULTURE; CONTROLLED STUDY; DRUG SCREENING; DRUG TARGETING; FEASIBILITY STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MOUSE; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROTEIN INDUCTION; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE; TUMOR IMMUNITY; TUMOR XENOGRAFT; YEAST;

ANIMALS; ASCITES; CELL LINE, TUMOR; FEMALE; FLOW CYTOMETRY; HUMANS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE; OVARIAN NEOPLASMS; SINGLE-CHAIN ANTIBODIES; T-LYMPHOCYTES; TUMOR ESCAPE; V-SET DOMAIN-CONTAINING T-CELL ACTIVATION INHIBITOR 1; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84881423899     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3457     Document Type: Article

References (47)

1. Kryczek I, Zou L, Rodriguez P, Zhu G, Wei S, Mottram P, et al. B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 2006;203:871-81.
2. Allavena P, Mantovani A. Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin Exp Immunol 2012;167: 195-205.
3. Coffelt SB, Hughes R, Lewis CE. Tumor-associated macrophages: effectors of angiogenesis and tumor progression. Biochim Biophys Acta 2009;1796:11-8.
4. Zeisberger SM, Odermatt B, Marty C, Zehnder-Fjallman AH, Ballmer- Hofer K, Schwendener RA. Clodronate-liposome-mediated depletion of tumour-associated macrophages: a new and highly effective antiangiogenic therapy approach. Br J Cancer 2006;95:272-81.
5. LobergRD, YingC, Craig M,Day LL,Sargent E,Neeley C, et al. Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo. Cancer Res 2007;67:9417-24.
6. Beatty GL, Chiorean EG, Fishman MP, Saboury B, Teitelbaum UR, Sun W, et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011; 331:1612-6.
7. Rolny C, Mazzone M, Tugues S, Laoui D, Johansson I, Coulon C, et al. HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 2011;19:31-44.
8. Dangaj D, Abbott KL, Mookerjee A, Zhao A, Kirby PS, Sandaltzopoulos R, et al. Mannose receptor (MR) engagement by mesothelin GPI anchor polarizes tumor-associated macrophages and is blocked by anti-MR human recombinant antibody. PLoS ONE 2011;6:e28386.
9. Sica GL, Choi IH, Zhu G, Tamada K, Wang SD, Tamura H, et al. B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 2003;18:849-61.
10. Prasad DV, Richards S, Mai XM, Dong C. B7-S1, a novel B7 family member that negatively regulates T cell activation. Immunity 2003;18: 863-73.
11. Zang X, Loke P, Kim J, Murphy K, Waitz R, Allison JP. B7x: a widely expressed B7 family member that inhibits T cell activation. Proc Natl Acad Sci U S A 2003;100:10388-92.
12. Kryczek I, Wei S, Zou L, Zhu G, Mottram P, Xu H, et al. Cutting edge: induction of B7-H4 on APCs through IL-10: novel suppressive mode for regulatory T cells. J Immunol 2006;177:40-4.
13. Wei J, Loke P, Zang X, Allison JP. Tissue-specific expression of B7x protects from CD4 T cell-mediated autoimmunity. J Exp Med 2011;208:1683-94.
14. Zhu G, Augustine MM, Azuma T, Luo L, Yao S, Anand S, et al. B7-H4- deficient mice display augmented neutrophil-mediated innate immunity. Blood 2009;113:1759-67.
15. Tringler B, Zhuo S, Pilkington G, Torkko KC, Singh M, Lucia MS, et al. B7-h4 is highly expressed in ductal and lobular breast cancer. Clin Cancer Res 2005;11:1842-8.
16. Choi IH, Zhu G, Sica GL, Strome SE, Cheville JC, Lau JS, et al. Genomic organization and expression analysis of B7-H4, an immune inhibitory molecule of the B7 family. J Immunol 2003;171:4650-4.
17. Sun Y, Wang Y, Zhao J, Gu M, Giscombe R, Lefvert AK, et al. B7-H3 and B7-H4 expression in non-small-cell lung cancer. Lung Cancer 2006;53:143-51.
18. Quandt D, Fiedler E, Boettcher D, Marsch W, Seliger B. B7-h4 expression in human melanoma: its association with patients' survival and antitumor immune response. Clin Cancer Res 2011;17:3100-11.
19. Krambeck AE, Thompson RH, Dong H, Lohse CM, Park ES, Kuntz SM, et al. B7-H4 expression in renal cell carcinoma and tumor vasculature: associations with cancer progression and survival. Proc Natl Acad Sci U S A 2006;103:10391-6.
20. Jiang J, Zhu Y,WuC, Shen Y, Wei W,Chen L, et al. Tumor expression of B7-H4 predicts poor survival of patients suffering from gastric cancer. Cancer Immunol Immunother 2010;59:1707-14.
21. Miyatake T, Tringler B, Liu W, Liu SH, Papkoff J, Enomoto T, et al. B7- H4 (DD-O110) is overexpressed in high risk uterine endometrioid adenocarcinomas and inversely correlated with tumor T-cell infiltration. Gynecol Oncol 2007;106:119-27.
22. Zang X, Thompson RH, Al-Ahmadie HA, Serio AM, Reuter VE, Eastham JA, et al. B7-H3 and B7x are highly expressed in human prostate cancer and associated with disease spread and poor outcome. Proc Natl Acad Sci U S A 2007;104:19458-63.
23. Simon I, Zhuo S, Corral L, Diamandis EP, Sarno MJ, Wolfert RL, et al. B7-H4 is a novel membrane-bound protein and a candidate serum and tissue biomarker for ovarian cancer. Cancer Res 2006;66:1570-5.
24. Thompson RH, Zang X, LohseCM, Leibovich BC, Slovin SF, Reuter VE, et al. Serum-soluble B7x is elevated in renal cell carcinoma patients and is associated with advanced stage. Cancer Res 2008;68:6054-8.
25. Zhang Y, Satterlee A, Huang L. In vivo gene delivery by nonviral vectors: overcoming hurdles? Mol Ther 2012;20:1298-304
26. van der Meel R, Gallagher WM, Oliveira S, O'Connor AE, Schiffelers RM, Byrne AT. Recent advances in molecular imaging biomarkers in cancer: application of bench to bedside technologies. Drug Discov Today 2010;15:102-14.
27. Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011;365:725-33.
28. Zhao A, Nunez-Cruz S, Li C, Coukos G, Siegel DL, Scholler N. Rapid isolation of high-affinity human antibodies against the tumor vascular marker Endosialin/TEM1, using a paired yeast-display/secretory scFv library platform. J Immunol Methods 2011;363:221-32.
29. Wang XX, Cho YK, Shusta EV. Mining a yeast library for brain endothelial cell-binding antibodies. Nat Methods 2007;4:143-5.
30. Andris-Widhopf J, Steinberger P, Fuller R, Rader C, Barbas CF III. Generation of human scFv antibody libraries: PCR amplification and assembly of light- and heavy-chain coding sequences. Cold Spring Harb Protoc 2011;2011:pii: pdb.prot065573.
31. Scholler N, Garvik B, Quarles T, Jiang S, Urban N. Method for generation of in vivo biotinylated recombinant antibodies by yeast mating. J Immunol Methods 2006;317:132-43.
32. Bergan L, Gross JA, Nevin B, Urban N, Scholler N. Development and in vitro validation of anti-mesothelin biobodies that prevent CA125/ Mesothelin-dependent cell attachment. Cancer Lett 2007;255:263-74.
33. Cheng C, Qu QX, Shen Y, Lv YT, Zhu YB, Zhang XG, et al. Overexpression of B7-H4 in tumor infiltrated dendritic cells. J Immunoassay Immunochem 2011;32:353-64.
34. Salter RD, Cresswell P. Impaired assembly and transport of HLA-A and -B antigens in a mutant TxB cell hybrid. EMBO J 1986;5:943-9.
35. Levine BL, Bernstein WB, Connors M, Craighead N, Lindsten T, Thompson CB, et al. Effects of CD28 costimulation on long-term proliferation of CD4+ T cells in the absence of exogenous feeder cells. J Immunol 1997;159:5921-30.
36. Johnson LA, Heemskerk B, Powell DJ Jr, Cohen CJ, Morgan RA, Dudley ME, et al. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J Immunol 2006;177:6548-59.
37. Hagemann T, Wilson J, Burke F, Kulbe H, Li NF, Pluddemann A, et al. Ovarian cancer cells polarize macrophages toward a tumor-associated phenotype. J Immunol 2006;176:5023-32.
38. Liang X, Weigand LU, Schuster IG, Eppinger E, van der Griendt JC, Schub A, et al. A single TCR alpha-chain with dominant peptide recognition in the allorestricted HER2/neu-specific T-cell repertoire. J Immunol 2010;184:1617-29.
39. Lanitis E, Dangaj D, Hagemann IS, Song DG, Best A, Sandaltzopoulos R, et al. Primary human ovarian epithelial cancer cells broadly express HER2 at immunologically-detectable levels. PLoS ONE 2012;7: e49829.
40. Kryczek I, Wei S, Zhu G, Myers L, Mottram P, Cheng P, et al. Relationship between B7-H4, regulatory T cells, and patient outcome in human ovarian carcinoma. Cancer Res 2007;67:8900-5.
41. Chen C, Qu QX, Shen Y, Mu CY, Zhu YB, Zhang XG, et al. Induced expression of B7-H4 on the surface of lung cancer cell by the tumorassociated macrophages: a potential mechanism of immune escape. Cancer Lett 2012;317:99-105.
42. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012;12:252-64.
43. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M, Regnani G, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348:203-13.
44. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10: 942-9.
45. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
46. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
47. Ribas A. Tumor immunotherapy directed at PD-1. N Engl J Med 2012;366:2517-9.