869
Views
0
CrossRef citations to date
0
Altmetric
Original research

A novel Fc-enhanced humanized monoclonal antibody targeting B7-H3 suppresses the growth of ESCC

, , , , , , , , , , , , , & show all
Article: 2282250 | Received 20 Apr 2023, Accepted 07 Nov 2023, Published online: 27 Nov 2023

References

  • Abnet CC, Arnold M, Wei WQ. Epidemiology of esophageal squamous cell carcinoma. Gastroenterology. 2018;154(2):360–11. doi:10.1053/j.gastro.2017.08.023.
  • Hsieh CH, Kuan WH, Chang WL, Kuo I-Y, Liu H, Shieh D-B, Liu H, Tan B, Wang Y-C. Dysregulation of SOX17/NRF2 axis confers chemoradiotherapy resistance and emerges as a novel therapeutic target in esophageal squamous cell carcinoma. J Biomed Sci. 2022;29:90. doi:10.1186/s12929-022-00873-4.
  • Dong P, Xiong Y, Yue J, Hanley S, Watari H. B7H3 as a promoter of metastasis and promising therapeutic target. Front Oncol. 2018;8:264. doi:10.3389/fonc.2018.00264.
  • Wang J, Chong KK, Nakamura Y, Nguyen L, Huang SK, Kuo C, Zhang W, Yu H, Morton DL, Hoon DSB, et al. B7-H3 associated with tumor progression and epigenetic regulatory activity in cutaneous melanoma. J Invest Dermatol. 2013;133(8):2050–2058. doi:10.1038/jid.2013.114.
  • Kontos F, Michelakos T, Kurokawa T, Sadagopan A, Schwab JH, Ferrone CR, Ferrone S. B7-H3: an attractive target for antibody-based immunotherapy. Clin Cancer Res. 2021;27:1227–1235. doi:10.1158/1078-0432.CCR-20-2584.
  • Zhou WT, Jin WL. B7-H3/CD276: An Emerging Cancer Immunotherapy. Front Immunol. 2021;12:701006. doi:10.3389/fimmu.2021.701006.
  • Janakiram M, Shah UA, Liu W, Zhao A, Schoenberg MP, Zang X. The third group of the B7-CD28 immune checkpoint family: HHLA2, TMIGD2, B7x, and B7-H3. Immunol Rev. 2017;276(1):26–39. doi:10.1111/imr.12521.
  • Leitner J, Klauser C, Pickl WF, Stöckl J, Majdic O, Bardet AF, Kreil DP, Dong C, Yamazaki T, Zlabinger G, 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(7):1754–1764. doi:10.1002/eji.200839028.
  • Picarda E, Ohaegbulam KC, Zang X. Molecular pathways: targeting B7-H3 (CD276) for human cancer immunotherapy. Clin Cancer Res. 2016;22(14):3425–3431. doi:10.1158/1078-0432.CCR-15-2428.
  • Chen L, Chen J, Xu B, Wang, Qi, Zhou W, Zhang G, Sun J, Shi L, Pei H, Wu C, Jiang J, et al. B7-H3 expression associates with tumor invasion and patient’s poor survival in human esophageal cancer. Am J Transl Res. 2015;7:2646–60.
  • Ahmed M, Cheng M, Zhao Q, Goldgur Y, Cheal SM, Guo H-F, Larson SM, Cheung NKV. Humanized affinity-matured monoclonal antibody 8H9 has potent antitumor activity and binds to FG loop of tumor antigen B7-H3. J Biol Chem. 2015;290:30018–30029. doi:10.1074/jbc.M115.679852.
  • Stavenhagen JB, Gorlatov S, Tuaillon N, Rankin CT, Li H, Burke S, Huang L, Johnson S, Bonvini E, Koenig S, et al. Fc Optimization of therapeutic antibodies enhances their ability to kill tumor cells in vitro and controls tumor expansion in vivo via low-affinity activating Fcγ receptors. Cancer Res. 2007;67:8882–8890. doi:10.1158/0008-5472.CAN-07-0696.
  • Lazar GA, Dang W, Karki S, Vafa O, Peng JS, Hyun L, Chan C, Chung HS, Eivazi A, Yoder SC, et al. Engineered antibody Fc variants with enhanced effector function. Proc Natl Acad Sci USA. 2006;103(11):4005–4010. doi:10.1073/pnas.0508123103.
  • Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873):583–589. doi:10.1038/s41586-021-03819-2.
  • Varadi M, Anyango S, Deshpande M, Nair S, Natassia C, Yordanova G, Yuan D, Stroe O, Wood G, Laydon A, et al. AlphaFold protein structure database: massively expanding the structural coverage of protein-sequence space with high-accuracy models. Nucleic Acids Res. 2022;50(D1):D439–D444. doi:10.1093/nar/gkab1061.
  • Sivasubramanian A, Sircar A, Chaudhury S, Gray JJ. Toward high-resolution homology modeling of antibody fv regions and application to antibody-antigen docking. Proteins. 2009;74:497–514. doi:10.1002/prot.22309.
  • Marze NA, Lyskov S, Gray JJ. Improved prediction of antibody VL-VH orientation. Protein Eng Des Sel. 2016;29:409–418. doi:10.1093/protein/gzw013.
  • Weitzner BD, Gray JJ. Accurate structure prediction of CDR H3 loops enabled by a novel structure-based C-Terminal constraint. J Immunol. 2017;198(1):505–515. doi:10.4049/jimmunol.1601137.
  • Weitzner BD, Jeliazkov JR, Lyskov S, Marze N, Kuroda D, Frick R, Adolf-Bryfogle J, Biswas N, Dunbrack RL, Gray JJ, et al. Modeling and docking of antibody structures with Rosetta. Nat Protoc. 2017;12(2):401–416. doi:10.1038/nprot.2016.180.
  • Lyskov S, Chou FC, Conchuir SO, Der BS, Drew K, Kuroda D, Xu J, Weitzner BD, Renfrew PD, Sripakdeevong P, et al. Serverification of molecular modeling applications: the Rosetta online server that includes everyone (ROSIE). PloS One. 2013;8:e63906. doi:10.1371/journal.pone.0063906.
  • Pierce BG, Hourai Y, Weng Z, Keskin O. Accelerating protein docking in ZDOCK using an advanced 3D convolution library. PloS One. 2011;6(9):e24657. doi:10.1371/journal.pone.0024657.
  • Steinberger P, Majdic O, Derdak SV, Pfistershammer K, Kirchberger S, Klauser C, Zlabinger G, Pickl WF, Stöckl J, Knapp W, et al. Molecular characterization of human 4Ig-B7-H3, a member of the B7 family with four ig-like domains. J Immunol. 2004;172(4):2352–2359. doi:10.4049/jimmunol.172.4.2352.
  • Zhou YH, Chen YJ, Ma ZY, Xu L, Wang Q, Zhang G-B, Xie F, Ge Y, Wang X-F, Zhang X-G, et al. 4IgB7-H3 is the major isoform expressed on immunocytes as well as malignant cells. Tissue Antigens. 2007;70(2):96–104. doi:10.1111/j.1399-0039.2007.00853.x.
  • Sun J, Fu F, Gu W, Yan R, Zhang G, Shen Z, Zhou Y, Wang H, Shen B, Zhang X, 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(9):e24751. doi:10.1371/journal.pone.0024751.
  • Yuan H, Wei X, Zhang G, Li C, Zhang X, Hou J. B7-H3 over expression in prostate cancer promotes tumor cell progression. J Urol. 2011;186(3):1093–1099. doi:10.1016/j.juro.2011.04.103.
  • Zhao X, Li DC, Zhu XG, GAN W-J, LI Z, XIONG F, ZHANG Z-X, ZHANG G-B, ZHANG X-G, ZHAO H, et al. B7-H3 overexpression in pancreatic cancer promotes tumor progression. Int J Mol Med. 2013;31(2):283–291. doi:10.3892/ijmm.2012.1212.
  • Zang X, Thompson RH, Al-Ahmadie HA, Serio AM, Reuter VE, Eastham JA, Scardino PT, Sharma P, Allison JP. B7-H3 and B7x are highly expressed in human prostate cancer and associated with disease spread and poor outcome. Proc Natl Acad Sci USA. 2007;104:19458–19463. doi:10.1073/pnas.0709802104.
  • 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;131:2528–2536. doi:10.1002/ijc.27566.
  • Zang X, Sullivan PS, Soslow RA, Waitz R, Reuter VE, Wilton A, Thaler HT, Arul M, Slovin SF, Wei J, et al. Tumor associated endothelial expression of B7-H3 predicts survival in ovarian carcinomas. Mod Pathol. 2010;23(8):1104–1112. doi:10.1038/modpathol.2010.95.
  • Xylinas E, Robinson BD, Kluth LA, Volkmer BG, Hautmann R, Küfer R, Zerbib M, Kwon E, Thompson RH, Boorjian SA, 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(1):121–127. doi:10.1016/j.ejso.2013.08.023.
  • Kramer K, Pandit-Taskar N, Kushner BH, Zanzonico P, Humm JL, Tomlinson U, Donzelli M, Wolden SL, Haque S, Dunkel I, et al. Phase 1 study of intraventricular (131)I-omburtamab targeting B7H3 (CD276)-expressing CNS malignancies. J Hematol Oncol. 2022;15:165. doi:10.1186/s13045-022-01383-4.
  • Kimiz-Gebologlu I, Gulce-Iz S, Biray-Avci C. Monoclonal antibodies in cancer immunotherapy. Mol Biol Rep. 2018;45(6):2935–2940. doi:10.1007/s11033-018-4427-x.
  • Harris TJ, Drake CG. Primer on tumor immunology and cancer immunotherapy. J Immunother Cancer. 2013;1:12. doi:10.1186/2051-1426-1-12.
  • Mossner E, Brunker P, Moser S, Püntener U, Schmidt C, Herter S, Grau R, Gerdes C, Nopora A, van Puijenbroek E, et al. Increasing the efficacy of CD20 antibody therapy through the engineering of a new type II anti-CD20 antibody with enhanced direct and immune effector cell–mediated B-cell cytotoxicity. Blood. 2010;115:4393–4402. doi:10.1182/blood-2009-06-225979.
  • Schlam I, Nunes R, Lynce F. Profile of Margetuximab: evidence to date in the targeted treatment of metastatic HER2-positive breast cancer. Onco Targets Ther. 2022;15:471–478. doi:10.2147/OTT.S272197.
  • Loo D, Alderson RF, Chen FZ, Huang L, Zhang W, Gorlatov S, Burke S, Ciccarone V, Li H, Yang Y, et al. Development of an Fc-enhanced anti–B7-H3 monoclonal antibody with potent antitumor activity. Clin Cancer Res. 2012;18:3834–3845. doi:10.1158/1078-0432.CCR-12-0715.
  • Awan FT, Lapalombella R, Trotta R, Butchar JP, Yu B, Benson DM, Roda JM, Cheney C, Mo X, Lehman A, et al. CD19 targeting of chronic lymphocytic leukemia with a novel Fc-domain–engineered monoclonal antibody. Blood. 2010;115:1204–1213. doi:10.1182/blood-2009-06-229039.
  • Zhang W, Zhang L, Qian J, Lin J, Chen Q, Yuan Q, Zhou J, Zhang T, Shi J, Zhou H, et al. Expression characteristic of 4Ig B7-H3 and 2Ig B7-H3 in acute myeloid leukemia. Bioengineered. 2021;12(2):11987–12002. doi:10.1080/21655979.2021.2001182.
  • Nagase-Zembutsu A, Hirotani K, Yamato M, Yamaguchi J, Takata T, Yoshida M, Fukuchi K, Yazawa M, Takahashi S, Agatsuma T, et al. Development of DS-5573a: a novel afucosylated mAb directed at B7-H3 with potent antitumor activity. Cancer Sci. 2016;107(5):674–681. doi:10.1111/cas.12915.
  • Cleary K, Chan H, James S, Glennie MJ, Cragg MS. Antibody distance from the cell membrane regulates antibody effector mechanisms. J Immunol. 2017;198(10):3999–4011. doi:10.4049/jimmunol.1601473.
  • Seaman S, Zhu Z, Saha S, Zhang XM, Yang MY, Hilton MB, Morris K, Szot C, Morris H, Swing DA, et al. Eradication of tumors through simultaneous ablation of CD276/B7-H3-positive tumor cells and tumor vasculature. Cancer Cell. 2017;31:501–515. doi:10.1016/j.ccell.2017.03.005.