Molecular pathways: Targeting B7-H3 (CD276) for human cancer immunotherapy

Clinical Cancer Research

Volumn 22, Issue 14, 2016, Pages 3425-3431

  Picarda, Elodie ^a   Ohaegbulam, Kim C ^a   Zang, Xingxing ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; B7 H3 ANTIGEN; BISPECIFIC ANTIBODY; CHIMERIC ANTIGEN RECEPTOR; CYTARABINE; DACARBAZINE; ENOBLITUZUMAB; IPILIMUMAB; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 8H9; NIVOLUMAB; PACLITAXEL; PEMBROLIZUMAB; PLACEBO; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CD276 PROTEIN, HUMAN;

ADOPTIVE TRANSFER; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ARTICLE; BLADDER CANCER; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GRADING; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER STAGING; CENTRAL NERVOUS SYSTEM TUMOR; DRUG DOSE ESCALATION; DRUG TARGETING; GLIOMA; HISTIOCYTIC LYMPHOMA; HUMAN; KIDNEY CARCINOMA; MELANOMA; METASTATIC MELANOMA; MOLECULARLY TARGETED THERAPY; MONOTHERAPY; NEUROBLASTOMA; NONHUMAN; OVERALL SURVIVAL; PANCREAS CANCER; PERITONEUM CANCER; PRIORITY JOURNAL; RECURRENCE FREE SURVIVAL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ESCAPE; TUMOR GROWTH; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR RECURRENCE; ANTIGEN PRESENTING CELL; DRUG EFFECTS; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASM; PHASE 1 CLINICAL TRIAL (TOPIC); PROCEDURES; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANTIBODIES, MONOCLONAL; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGEN-PRESENTING CELLS; B7 ANTIGENS; CLINICAL TRIALS, PHASE I AS TOPIC; HUMANS; IMMUNOTHERAPY; NEOPLASMS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84978376878     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2428     Document Type: Article

References (70)

1. Steinberger P, Majdic O, Derdak SV, Pfistershammer K, Kirchberger S, Klauser C, et al. Molecular characterization of human 4Ig-B7-H3, a member of the B7 family with four Ig-like domains. J Immunol 2004;172:2352-9.
2. Sun M, Richards S, Prasad DVR, Mai XM, Rudensky A, Dong C. Characterization of mouse and human B7-H3 genes. J Immunol 2002;168: 6294-7.
3. Chapoval AI, Ni J, Lau JS, Wilcox RA, Flies DB, Liu D, et al. B7-H3: a costimulatory molecule for T cell activation and IFN-g production. Nat Immunol 2001;2:269-74.
4. Sun J, Fu F, Gu W, Yan R, Zhang G, Shen Z, et al. Origination of new immunological functions in the costimulatory molecule B7-H3: the role of exon duplication in evolution of the immune system. PLoS One 2011;6: e24751.
5. Zhang G, Hou J, Shi J, Yu G, Lu B, Zhang X. Soluble CD276 (B7-H3) is released from monocytes, dendritic cells and activated T cells and is detectable in normal human serum. Immunology 2008;123:538-46.
6. Chen W, Liu P, Wang Y, Nie W, Li Z, Xu W, et al. Characterization of a soluble B7-H3 (sB7-H3) spliced from the intron and analysis of sB7-H3 in the sera of patients with hepatocellular carcinoma. PLoS One 2013;8: e76965.
7. Mahnke K, Ring S, Johnson TS, Schallenberg S, Schönfeld K, Storn V, et al. Induction of immunosuppressive functions of dendritic cells in vivo by CD4+CD25+ regulatory T cells: role of B7-H3 expression and antigen presentation. Eur J Immunol 2007;37:2117-26.
8. Suh W-K, Gajewska BU, Okada H, Gronski MA, Bertram EM, Dawicki W, et al. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat Immunol 2003;4:899-906.
9. Zhang G, Dong Q, Xu Y, Yu G, Zhang X. B7-H3: another molecule marker for Mo-DCs? Cell Mol Immunol 2005;2:307-11.
10. Castriconi R, Dondero A, Augugliaro R, Cantoni C, Carnemolla B, Sementa AR, et al. Identification of 4Ig-B7-H3 as a neuroblastoma-associated molecule that exerts a protective role from an NK cell-mediated lysis. Proc Natl Acad Sci U S A 2004;101:12640-5.
11. Zhang G, Wang J, Kelly J, Gu G, Hou J, Zhou Y, et al. B7-H3 augments the inflammatory response and is associated with human sepsis. J Immunol 2010;185:3677-84.
12. Hofmeyer KA, Ray A, Zang X. The contrasting role of B7-H3. Proc Natl Acad Sci U S A 2008;105:10277-8.
13. Luo L, Zhu G, Xu H, Yao S, Zhou G, Zhu Y, et al. B7-H3 promotes pathogenesis of autoimmune disease and inflammation by regulating the activity of different T cell subsets. PLoS One 2015;10:e0130126.
14. Wang L, Fraser CC, Kikly K, Wells AD, Han R, Coyle AJ, et al. B7-H3 promotes acute and chronic allograft rejection. Eur J Immunol 2005;35: 428-38.
15. Chen X, Quinn EM, Ni H, Wang J, Blankson S, Redmond HP, et al. B7-H3 participates in the development of experimental pneumococcal meningitis by augmentation of the inflammatory response via a TLR2-dependent mechanism. J Immunol 2012;189:347-55.
16. Prasad DVR, Nguyen T, Li Z, Yang Y, Duong J, Wang Y, et al. Murine B7-H3 is a negative regulator of T cells. J Immunol 2004;173:2500-6.
17. Ueno T, Yeung MY, McGrath M, Yang S, Zaman N, Snawder B, et al. Intact B7-H3 signaling promotes allograft prolongation through preferential suppression of Th1 effector responses. Eur J Immunol 2012;42:2343-53.
18. Veenstra RG, Flynn R, Kreymborg K, McDonald-Hyman C, Saha A, Taylor PA, et al. B7-H3 expression in donor T cells and host cells negatively regulates acute graft-versus-host disease lethality. Blood 2015;125: 3335-46.
19. Vigdorovich V, Ramagopal UA, Lazar-Molnar E, Sylvestre E, Lee JS, Hofmeyer KA, et al. Structure and T cell inhibition properties of B7 family member, B7-H3. Structure 2013;21:707-17.
20. Leitner J, Klauser C, Pickl WF, Sẗockl J, Majdic O, Bardet AF, et al. B7-H3 is a potent inhibitor of human T cell activation: no evidence for B7-H3 and TREML2 interaction. Eur J Immunol 2009;39:1754-64.
21. Suh W-K, Wang SX, Jheon AH, Moreno L, Yoshinaga SK, Ganss B, et al. The immune regulatory protein B7-H3 promotes osteoblast differentiation and bone mineralization. Proc Natl Acad Sci U S A 2004;101:12969-73.
22. Wang J, Chong KK, Nakamura Y, Nguyen L, Huang SK, Kuo C, et al. B7-H3 associated with tumor progression and epigenetic regulatory activity in cutaneous melanoma. J Invest Dermatol 2013;133:2050-8.
23. Hu Y, Lv X, Wu Y, Xu J, Wang L, Chen W, et al. Expression of costimulatory molecule B7-H3 and its prognostic implications in human acute leukemia. Hematology 2015;20:187-95.
24. Sun J, Guo Y-D, Li X-N, Zhang Y-Q, Gu L, Wu P-P, et al. B7-H3 expression in breast cancer and upregulation of VEGF through gene silence. Onco Targets Ther 2014;7:1979-86.
25. 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.
26. Zang X, Sullivan PS, Soslow RA, Waitz R, Reuter VE, Wilton A, et al. Tumor associated endothelial expression of B7-H3 predicts survival in ovarian carcinomas. Mod Pathol 2010;23:1104-12.
27. Chen Y, Sun J, Zhao H, Zhu D, Zhi Q, Song S, et al. The coexpression and clinical significance ofcostimulatorymolecules B7-H1, B7-H3, andB7-H4 in human pancreatic cancer. Onco Targets Ther 2014;7:1465-72.
28. Ingebrigtsen VA, Boye K, Nesland JM, Nesbakken A, Flatmark K, Fodstad . B7-H3 expression in colorectal cancer: associations with clinicopathological parameters and patient outcome. BMC Cancer 2014;14:602.
29. Ingebrigtsen VA, Boye K, Tekle C, Nesland JM, Flatmark K, Fodstad O. B7-H3 expression in colorectal cancer: nuclear localization strongly predicts poor outcome in colon cancer. Int J Cancer 2012;131:2528-36.
30. 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.
31. Xu H, Cheung IY, Guo H-F, Cheung N-KV. MicroRNA miR-29 modulates expression of immunoinhibitory molecule B7-H3: potential implications for immune based therapy of human solid tumors. Cancer Res 2009;69:6275-81.
32. Sun T-W, Gao Q, Qiu S-J, Zhou J, Wang X-Y, Yi Y, et al. B7-H3 is expressed in human hepatocellular carcinoma and is associated with tumor aggressiveness and postoperative recurrence. Cancer Immunol Immunother 2012;61:2171-82.
33. Zhang P, Yu S, Li H, Liu C, Li J, Lin W, et al. ILT4 drives B7-H3 expression via PI3K/AKT/mTOR signalling and ILT4/B7-H3 co-expression correlates with poor prognosis in non-small cell lung cancer. FEBS Lett 2015;589: 2248-56.
34. Chen J-T, Chen C-H, Ku K-L, Hsiao M, Chiang C-P, Hsu T-L, et al. Glycoprotein B7-H3 overexpression and aberrant glycosylation in oral cancer and immune response. Proc Natl Acad Sci U S A 2015;112: 13057-62.
35. Chen C, Shen Y, Qu Q-X, Chen X-Q, Zhang X-G, Huang J-A. Induced expression of B7-H3 on the lung cancer cells and macrophages suppresses T-cell mediating anti-tumor immune response. Exp Cell Res 2013;319: 96-102.
36. Chen Y-W, Tekle C, Fodstad O. The immunoregulatory protein human B7H3 is a tumor-associated antigen that regulates tumor cell migration and invasion. Curr Cancer Drug Targets 2008;8:404-13.
37. Liu F, Zhang T, Zou S, Jiang B, Hua D. B7-H3 promotes cell migration and invasion through the Jak2/Stat3/MMP9 signaling pathway in colorectal cancer. Mol Med Rep 2015;12:5455-60.
38. Liu H, Tekle C, Chen Y-W, Kristian A, Zhao Y, Zhou M, et al. B7-H3 silencing increases paclitaxel sensitivity by abrogating Jak2/Stat3 phosphorylation. Mol Cancer Ther 2011;10:960-71.
39. Zhang T, Jiang B, Zou S-T, Liu F, Hua D. Overexpression of B7-H3 augments anti-apoptosis of colorectal cancer cells by Jak2-STAT3. World J Gastroenterol 2015;21:1804-13.
40. Tekle C, Nygren MK, Chen Y-W, Dybsjord I, Nesland JM, Maelandsmo GM, et al. B7-H3 contributes to the metastatic capacity of melanoma cells by modulation of known metastasis-associated genes. Int J Cancer 2012;130: 2282-90.
41. Kang F-B, Wang L, Jia H-C, Li D, Li H-J, Zhang Y-G, et al. B7-H3 promotes aggression and invasion of hepatocellular carcinoma by targeting epithelial-to-mesenchymal transition via JAK2/STAT3/Slug signaling pathway. Cancer Cell Int 2015;15:45.
42. Nunes-Xavier CE, Karlsen KF, Tekle C, Pedersen C, yjord T, Hongisto V, et al. Decreased expression of B7-H3 reduces the glycolytic capacity and sensitizes breast cancer cells to AKT/mTOR inhibitors. Oncotarget 2016;7:6891-901.
43. Zang X, Allison JP. The B7 family and cancer therapy: costimulation and coinhibition. Clin Cancer Res 2007;13:5271-9.
44. Brahmer JR, Tykodi SS, Chow LQM, Hwu W-J, 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.
45. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
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. Loo D, Alderson RF, Chen FZ, Huang L, Zhang W, Gorlatov S, et al. Development of an Fc-enhanced anti-B7-H3 monoclonal antibody with potent antitumor activity. Clin Cancer Res 2012;18:3834-45.
48. Enoblituzumab (anti-B7-H3); [Internet]. [cited 2016 Feb 24]. Available from: http://www.macrogenics.com/enoblituzumab-anti-b7-h3/.
49. Kramer K, Kushner BH, Modak S, Pandit-Taskar N, Smith-Jones P, Zanzonico P, et al. Compartmental intrathecal radioimmunotherapy: results for treatment for metastatic CNS neuroblastoma. J Neurooncol 2010;97: 409-18.
50. Ahmed M, Cheng M, Zhao Q, Goldgur Y, Cheal SM, Guo H-F, et al. Humanized affinity-matured monoclonal antibody 8H9 has potent antitumor activity and binds to FG loop of tumor antigen B7-H3. J Biol Chem 2015;290:30018-29.
51. Weidle UH, Kontermann RE, Brinkmann U. Tumor-antigen-binding bispecific antibodies for cancer treatment. Semin Oncol 2014;41:653-60.
52. Adams JL, Smothers J, Srinivasan R, Hoos A. Big opportunities for small molecules in immuno-oncology. Nat Rev Drug Discov 2015;14: 603-22.
53. Gill S, June CH. Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol Rev 2015;263:68-89.
54. Sadelain M. CAR therapy: the CD19 paradigm. J Clin Invest 2015;125: 3392-400.
55. Kakarla S, Gottschalk S. CAR T cells for solid tumors: armed and ready to go? Cancer J 2014;20:151-5.
56. Beatty GL, O'Hara MH, Nelson AM, McGarvey M, Torigian DA, Lacey SF, et al. Safety and antitumor activity of chimeric antigen receptor modified T cells in patients with chemotherapy refractory metastatic pancreatic cancer. J Clin Oncol 33, 2015 (suppl; abstr 3007).
57. Robert C, Thomas L, Bondarenko I, O'Day S, Weber J, Garbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364:2517-26.
58. Zhang W, Wang J, Wang Y, Dong F, Zhu M, Wan W, et al. B7-H3 silencing by RNAi inhibits tumor progression and enhances chemosensitivity in U937 cells. Onco Targets Ther 2015;8:1721-33.
59. Larkin J, Hodi FS, Wolchok JD. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 2015;373: 1270-1.
60. Postow MA, Callahan MK, Barker CA, Yamada Y, Yuan J, Kitano S, et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 2012;366:925-31.
61. Twyman-Saint Victor C, Rech AJ, Maity A, Rengan R, Pauken KE, Stelekati E, et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 2015;520:373-7.
62. Roth TJ, Sheinin Y, Lohse CM, Kuntz SM, Frigola X, Inman BA, et al. B7-H3 ligand expression by prostate cancer: a novel marker of prognosis and potential target for therapy. Cancer Res 2007;67:7893-900.
63. Wang L, Zhang Q, Chen W, Shan B, Ding Y, Zhang G, et al. B7-H3 is overexpressed in patients suffering osteosarcoma and associated with tumor aggressiveness and metastasis. PLoS One 2013;8:e70689.
64. Liu C, Liu J, Wang J, Liu Y, Zhang F, Lin W, et al. B7-H3 expression in ductal and lobular breast cancer and its association with IL-10. Mol Med Rep 2013;7:134-8.
65. Brunner A, Hinterholzer S, Riss P, Heinze G, Brustmann H. Immunoexpression of B7-H3 in endometrial cancer: relation to tumor T-cell infiltration and prognosis. Gynecol Oncol 2012;124:105-11.
66. Huang C, Zhou L, Chang X, Pang X, Zhang H, Zhang S. B7-H3, B7-H4, Foxp3 and IL-2 expression in cervical cancer: associations with patient outcome and clinical significance. Oncol Rep 2016;35:2183-90.
67. Mao Y, Li W, Chen K, Xie Y, Liu Q, Yao M, et al. B7-H1 and B7-H3 are independent predictors of poor prognosis in patients with non-small cell lung cancer. Oncotarget 2015;6:3452-61.
68. Xylinas E, Robinson BD, Kluth LA, Volkmer BG, Hautmann R, Küfer R, et al. Association of T-cell co-regulatory protein expression with clinical outcomes following radical cystectomy for urothelial carcinoma of the bladder. Eur J Surg Oncol 2014;40:121-7.
69. Qin X, Zhang H, Ye D, Dai B, Zhu Y, Shi G. B7-H3 is a new cancer-specific endothelial marker in clear cell renal cell carcinoma. Onco Targets Ther 2013;6:1667-73.
70. Baral A, Ye HX, Jiang PC, Yao Y, Mao Y. B7-H3 and B7-H1 expression in cerebral spinal fluid and tumor tissue correlates with the malignancy grade of glioma patients. Oncol Lett 2014;8:1195-201.