Clinical development of an anti-GPC-1 antibody for the treatment of cancer

References

• Sarrazin S, Lamanna WC, Esko JD. Heparan sulfate proteoglycans. Cold Spring Harb Perspect Biol. 2011;3(7):a004952.
   PubMed Web of Science ®Google Scholar
• David G, Lories V, Decock B, et al. Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J Cell Biol. 1990;111(6):3165–3176.
   PubMed Web of Science ®Google Scholar
• Filmus J, Selleck SB. Glypicans: proteoglycans with a Surprise. J Clin Invest. 2001;108(4):497–501.
   PubMed Web of Science ®Google Scholar
• Kawahara R, Granato DC, Yokoo S, et al. Mass spectrometry-based proteomics revealed Glypican-1 as a novel ADAM17 substrate. J Proteomics. 2017;151:53–65.
   PubMed Web of Science ®Google Scholar
• Wang S, Qiu Y, Bai B. The expression, regulation, and biomarker potential of glypican-1 in cancer. Front Oncol. 2019;9(614).
   Google Scholar
• Pan J, Ho M. Role of glypican-1 in regulating multiple cellular signaling pathways. Am J Physiol Cell Physiol. 2021;321(5):C846–C858.
   PubMed Web of Science ®Google Scholar
• Hu J, Sheng Y, Kwak KJ, et al. A signal-amplifiable biochip quantifies extracellular vesicle-associated RNAs for early cancer detection. Nat Commun. 2017;8(1):1683.
   PubMed Web of Science ®Google Scholar
• Yang KS, Im H, Hong S, et al. Multiparametric plasma EV profiling facilitates diagnosis of pancreatic malignancy. Sci Transl Med. 2017;9(391):eaal3226.
   PubMed Web of Science ®Google Scholar
• Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523(7559):177–182.
   PubMed Web of Science ®Google Scholar
• Buscail E, Chauvet A, Quincy P, et al. CD63-GPC1-positive exosomes coupled with CA19-9 offer good diagnostic potential for resectable pancreatic ductal adenocarcinoma. Transl Oncol. 2019;12(11):1395–1403.
   PubMed Web of Science ®Google Scholar
• Frampton AE, Prado MM, Fajardo-Puerta AB, et al. Glypican-1 is enriched in circulating-exosomes in pancreatic cancer and correlates with tumor burden. Oncotarget. 2018;9(27):19006–19013.
   PubMedGoogle Scholar
• Zhang W, Jiang L, Diefenbach RJ, et al. Enabling sensitive phenotypic profiling of cancer-derived small extracellular vesicles using surface-enhanced Raman spectroscopy nanotags. ACS Sens. 2020;5(3):764–771.
   PubMed Web of Science ®Google Scholar
• Levin RA, Lund ME, Truong Q, et al. Development of a reliable assay to measure glypican-1 in plasma and serum reveals circulating glypican-1 as a novel prostate cancer biomarker. Oncotarget. 2018;9(32):22359–22367.
   PubMedGoogle Scholar
• Truong Q, Justiniano IO, Nocon AL, et al. Glypican-1 as a biomarker for prostate cancer: isolation and characterization. J Cancer. 2016;7(8):1002–1009.
   PubMed Web of Science ®Google Scholar
• Jen Y-HL, Musacchio M, Lander AD. Glypican-1 controls brain size through regulation of fibroblast growth factor signaling in early neurogenesis. Neural Dev. 2009;4(1):33.
   PubMedGoogle Scholar
• Kato D, Yaguchi T, Iwata T, et al. GPC1 specific CAR-T cells eradicate established solid tumor without adverse effects and synergize with anti-PD-1 Ab. eLife. 2020;9:e49392.
   PubMed Web of Science ®Google Scholar
• Diamandis EP, Plebani M. Glypican-1 as a highly sensitive and specific pancreatic cancer biomarker. Clin Chem Lab Med. 2016;54(1):e1–2.
   PubMed Web of Science ®Google Scholar
• Hara H, Takahashi T, Serada S, et al. Overexpression of glypican-1 implicates poor prognosis and their chemoresistance in oesophageal squamous cell carcinoma. Br J Cancer. 2016;115(1):66–75.
   PubMed Web of Science ®Google Scholar
• Matsuda K, Maruyama H, Guo F, et al. Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res. 2001;61(14):5562–5569.
   PubMed Web of Science ®Google Scholar
• Campbell DH, Lund ME, Nocon AL, et al. Detection of glypican-1 (GPC-1) expression in urine cell sediments in prostate cancer. PLoS One. 2018;13(4):e0196017.
   PubMed Web of Science ®Google Scholar
• Su G, Meyer K, Nandini CD, et al. Glypican-1 is frequently overexpressed in human gliomas and enhances FGF-2 signaling in glioma cells. Am J Pathol. 2006;168(6):2014–2026.
   PubMed Web of Science ®Google Scholar
• Russell PJ, Ow KT, Tam PN, et al. Immunohistochemical characterisation of the monoclonal antibody BLCA-38 for the detection of prostate cancer. Cancer Immunol Immunother. 2004;53(11):995–1004.
   PubMed Web of Science ®Google Scholar
• Amatya VJ, Kushitani K, Kai Y, et al. Glypican-1 immunohistochemistry is a novel marker to differentiate epithelioid mesothelioma from lung adenocarcinoma. Mod Pathol. 2018;31(5):809–815.
   PubMed Web of Science ®Google Scholar
• Kai Y, Amatya VJ, Kushitani K, et al. Glypican-1 is a novel immunohistochemical marker to differentiate poorly differentiated squamous cell carcinoma from solid predominant adenocarcinoma of the lung. Transl Lung Cancer Res. 2021;10(2):766–775.
   PubMed Web of Science ®Google Scholar
• Matsuzaki S, Serada S, Hiramatsu K, et al. Anti-glypican-1 antibody-drug conjugate exhibits potent preclinical antitumor activity against glypican-1 positive uterine cervical cancer. Intl J Cancer. 2018;142(5):1056–1066.
   PubMed Web of Science ®Google Scholar
• Saito T, Sugiyama K, Hama S, et al. High expression of glypican-1 predicts dissemination and poor prognosis in glioblastomas. World Neurosurg. 2017;105:282–288.
   PubMed Web of Science ®Google Scholar
• Nishigaki T, Takahashi T, Serada S, et al. Anti-glypican-1 antibody–drug conjugate is a potential therapy against pancreatic cancer. Br J Cancer. 2020;122(9):1333–1341.
   PubMed Web of Science ®Google Scholar
• Grillo PK, Győrffy B, Götte M. Prognostic impact of the glypican family of heparan sulfate proteoglycans on the survival of breast cancer patients. J Cancer Res Clin Oncol. 2021;147(7):1937–1955.
   PubMed Web of Science ®Google Scholar
• Russell PJ, Ho Shon I, Boniface GR, et al. Growth and metastasis of human bladder cancer xenografts in the bladder of nude rats. A model for intravesical radioimmunotherapy. Urol Res. 1991;19(4):207–213.
   PubMedGoogle Scholar
• Davies EJ, Blackhall FH, Shanks JH, et al. Distribution and clinical significance of heparan sulfate proteoglycans in ovarian cancer. Clin Cancer Res. 2004;10(15):5178–5186.
   PubMed Web of Science ®Google Scholar
• Kleeff J, Ishiwata T, Kumbasar A, et al. The cell-surface heparan sulfate proteoglycan glypican-1 regulates growth factor action in pancreatic carcinoma cells and is overexpressed in human pancreatic cancer. J Clin Invest. 1998;102(9):1662–1673.
   PubMed Web of Science ®Google Scholar
• Whipple CA, Young AL, Korc M. A KrasG12D-driven genetic mouse model of pancreatic cancer requires glypican-1 for efficient proliferation and angiogenesis. Oncogene. 2012;31(20):2535–2544.
   PubMed Web of Science ®Google Scholar
• de Boeck H, Lories V, David G, et al. Identification of a 64 kDa heparan sulphate proteoglycan core protein from human lung fibroblast plasma membranes with a monoclonal antibody. Biochem J. 1987;247(3):765–771.
   PubMed Web of Science ®Google Scholar
• Walker KZ, Russell PJ, Kingsley EA, et al. Detection of malignant cells in voided urine from patients with bladder cancer, a novel monoclonal assay. J Urol. 1989;142(6):1578–1583.
   PubMed Web of Science ®Google Scholar
• Ovacik M, Lin K. Tutorial on monoclonal antibody pharmacokinetics and its considerations in early development. Clin Transl Sci. 2018;11(6):540–552.
   PubMed Web of Science ®Google Scholar
• Harding FA, Stickler MM, Razo J, et al. The immunogenicity of humanized and fully human antibodies: residual immunogenicity resides in the CDR regions. MAbs. 2010;2(3):256–265.
   PubMed Web of Science ®Google Scholar
• Mullard A. FDA approves 100th monoclonal antibody product. Nat Rev Drug Discov. 2021;20(7):491–495.
   PubMed Web of Science ®Google Scholar
• Harada E, Serada S, Fujimoto M, et al. Glypican-1 targeted antibody-based therapy induces preclinical antitumor activity against esophageal squamous cell carcinoma. Oncotarget. 2017;8(15):24741–24752.
   PubMedGoogle Scholar
• Cheng F, Mani K, van den Born J, et al. Nitric oxide-dependent processing of heparan sulfate in recycling S-nitrosylated glypican-1 takes place in caveolin-1-containing endosomes. J Biol Chem. 2002;277(46):44431–44439.
   PubMed Web of Science ®Google Scholar
• Carter T, Sterling-Levis K, Ow K, et al. Biodistributions of intact monoclonal antibodies and fragments of BLCA-38, a new prostate cancer directed antibody. Cancer Immunol Immunother. 2004;53(6):533–542.
   PubMed Web of Science ®Google Scholar
• Sabanathan D, Campbell DH, and Velonas VM, et al. Safety and tolerability of Miltuximab® - a first in human study in patients with advanced solid cancers. Asia Ocean J Nucl Med Biol. 2021;9(2):86–100.
   PubMedGoogle Scholar
• Munekage E, Serada S, Tsujii S, et al. A glypican-1-targeted antibody-drug conjugate exhibits potent tumor growth inhibition in glypican-1-positive pancreatic cancer and esophageal squamous cell carcinoma. Neoplasia. 2021;23(9):939–950.
   PubMed Web of Science ®Google Scholar
• Li N, Gao W, Zhang Y-F, et al. Glypicans as cancer therapeutic targets. Trends Cancer. 2018;4(11):741–754.
   PubMed Web of Science ®Google Scholar
• Li N, Li D, Ren H, et al. Abstract 2309: chimeric antigen receptor T-cell therapy targeting glypican-1 in pancreatic cancer. Cancer Res. 2019;79(13 Supplement):2309.
   Web of Science ®Google Scholar
• Li N, Spetz MR, Ho M. The role of glypicans in cancer progression and therapy. J Histochem Cytochem. 2020;68(12):841–862.
   PubMed Web of Science ®Google Scholar
• Li N, Li D, Pan J, et al. Abstract 1541: incorporation of an IgG4-derived spacer improves the activity of nanobody-based CAR T cells targeting a membrane-distal epitope of glypican 1 in pancreatic cancer. Cancer Res. 2021;81(13 Supplement):1541.
   Web of Science ®Google Scholar
• Yokota K, Serada S, Tsujii S, et al. Anti-glypican-1 antibody–drug conjugate as potential therapy against tumor cells and tumor vasculature for glypican-1–positive cholangiocarcinoma. Mol Cancer Ther. 2021;20(9):1713–1722.
   PubMed Web of Science ®Google Scholar
• Fransson LÅ, Belting M, Cheng F, et al. Novel aspects of glypican glycobiology. Cell Mol Life Sci. 2004;61(9):1016–1024.
   PubMed Web of Science ®Google Scholar
• Tsujii S, Serada S, Fujimoto M, et al. Glypican-1 Is a novel target for stroma and tumor cell dual-targeting antibody–drug conjugates in pancreatic cancer. Mol Cancer Ther. 2021;20(12):2495.
   PubMed Web of Science ®Google Scholar
• Sabanathan D, Lund ME, Campbell DH, et al. Radioimmunotherapy for solid tumors: spotlight on glypican-1 as a radioimmunotherapy target. Ther Adv Med Oncol. 2021;13:17588359211022918.
   Web of Science ®Google Scholar
• Yeh M-C, Tse BWC, Fletcher NL, et al. Targeted beta therapy of prostate cancer with 177Lu-labelled Miltuximab® antibody against glypican-1 (GPC-1). EJNMMI Res. 2020;10(1):46.
   PubMed Web of Science ®Google Scholar
• Tinklepaugh J, Jeitner T, Kelly J, et al. Evaluation of the anti glypican 1 chimeric antibody miltuximab for delivery of radioisotopes in cancer treatment. J Nucl Med. 2020;61(supplement 1):1074.
   Google Scholar
• Russell PJ, Plomley J, Shon IH, et al. Monoclonal antibodies for intravesical radioimmunotherapy of human bladder cancer. Cell Biophys. 1993;22(1):27–47.
   PubMedGoogle Scholar
• Lightfoot D, Walker K, Boniface G, et al. Dosimetric and therapeutic studies in nude mice xenograft models with 153Samarium-labelled monoclonal antibody, BLCA-38. Antib Immunoconjugates Radiopharm. 1991;4:319–330.
   Google Scholar
• Wang J, Abbas Rizvi SM, Madigan MC, et al. Control of prostate cancer spheroid growth using 213Bi-labeled multiple targeted alpha radioimmunoconjugates. Prostate. 2006;66(16):1753–1767.
   PubMed Web of Science ®Google Scholar
• Wolf E, Hofmeister R, Kufer P, et al. BiTEs: bispecific antibody constructs with unique anti-tumor activity. Drug Discov Today. 2005;10(18):1237–1244.
   PubMed Web of Science ®Google Scholar
• Lund ME, Howard CB, Thurecht KJ, et al. A bispecific T cell engager targeting Glypican-1 redirects T cell cytolytic activity to kill prostate cancer cells. BMC Cancer. 2020;20(1):1214.
   PubMed Web of Science ®Google Scholar
• Polikarpov DM, Campbell DH, Lund ME, et al. The feasibility of Miltuximab®-IRDye700DX-mediated photoimmunotherapy of solid tumors. Photodiagnosis Photodyn Ther. 2020;32:102064.
   PubMed Web of Science ®Google Scholar
• Huang X, Fan C, Zhu H, et al. Glypican-1-antibody-conjugated Gd-Au nanoclusters for FI/MRI dual-modal targeted detection of pancreatic cancer. Int J Nanomedicine. 2018;13:2585–2599.
   PubMed Web of Science ®Google Scholar
• Polikarpov DM, Campbell DH, McRobb LS, et al. Near-infrared molecular imaging of glioblastoma by Miltuximab®-IRDye800CW as a potential tool for fluorescence-guided surgery. Cancers (Basel). 2020;12(4):984.
   Web of Science ®Google Scholar
• Collins DM, Bossenmaier B, Kollmorgen G, et al. Acquired resistance to antibody-drug conjugates. Cancers (Basel). 2019;11(3):394.
   Web of Science ®Google Scholar
• Konings K, Vandevoorde C, Baselet B, et al. Combination therapy with charged particles and molecular targeting: a promising avenue to overcome radioresistance. Front Oncol. 2020;10(128). DOI:https://doi.org/10.3389/fonc.2020.00128.
   Google Scholar
• Chavez JC, Bachmeier C, Kharfan-Dabaja MA. CAR T-cell therapy for B-cell lymphomas: clinical trial results of available products. Ther Adv Hematol. 2019;10:2040620719841581.
   Web of Science ®Google Scholar
• Mikkilineni L, Kochenderfer JN. CAR T cell therapies for patients with multiple myeloma.Nat Rev Clin Oncol. 2021 [2021 February 01];18(2):71–84.
   PubMed Web of Science ®Google Scholar
• Zaslavsky A, Adams M, Wissmueller S, et al. Glypican-1 as a novel immunotherapeutic target in prostate cancer. J Clin Oncol. 2018;36(6_suppl):174.
   Web of Science ®Google Scholar