Emerging monoclonal antibody therapies in the treatment of metastatic urothelial carcinoma

References

• Amin MB. Histological variants of urothelial carcinoma: diagnostic, therapeutic and prognostic implications. Mod Pathol. 2009 Jun;22(Suppl 2):S96–S118.
   PubMedGoogle Scholar
• Miyazaki J, Nishiyama H. Epidemiology of urothelial carcinoma. Int J Urol. 2017 Oct;24(10):730–734.
   PubMed Web of Science ®Google Scholar
• Hepp Z, Shah SN, Smoyer K, et al. Epidemiology and treatment patterns for locally advanced or metastatic urothelial carcinoma: a systematic literature review and gap analysis. J Manag Care Spec Pharm. 2021 Feb;27(2):240–255.
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research N. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature. 2014 Mar 20;507(7492):315–322.
   PubMedGoogle Scholar
• Seront E, Machiels JP. Molecular biology and targeted therapies for urothelial carcinoma. Cancer Treat Rev. 2015 Apr;41(4):341–353.
   PubMed Web of Science ®Google Scholar
• Key Statistics for Bladder Cancer American Cancer Society. 2022. [Cited 2022 Dec 1; cited 2022 Jun 13]. Available from: https://www.cancer.org/cancer/bladder-cancer/about/key-statistics.html
   Google Scholar
• Cancer Institute Surveillance, Epidemiology, and End Results Program. Cancer stat facts: bladder cancer [Internet]. 2020 [cited 2022 Jun 18]. Available from: https://seer.cancer.gov/statfacts/html/urinb.html.
   Google Scholar
• Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin. 2011 March-April;61(2):69–90.
   PubMed Web of Science ®Google Scholar
• von der Maase H, Sengelov L, Roberts JT, et al. Long-term survival results of a randomized trial comparing gemcitabine plus cisplatin, with methotrexate, vinblastine, doxorubicin, plus cisplatin in patients with bladder cancer. J Clin Oncol. 2005 Jul 20;23(21):4602–4608.
   PubMed Web of Science ®Google Scholar
• Ritch CR, Velasquez MC, Kwon D, et al. Use and validation of the AUA/SUO risk grouping for nonmuscle invasive bladder cancer in a contemporary cohort. J Urol. 2020 Mar;203(3):505–511.
   PubMedGoogle Scholar
• Stein JP, Lieskovsky G, Cote R, et al. Radical cystectomy in the treatment of invasive bladder cancer: long-term results in 1,054 patients. J Clin Oncol. 2001 Feb 1;19(3):666–675.
   PubMed Web of Science ®Google Scholar
• Bellmunt J, de Wit R, Vaughn DJ, et al. Pembrolizumab as second-line therapy for advanced urothelial carcinoma. N Engl J Med. 2017 Mar 16;376(11):1015–1026.
   PubMed Web of Science ®Google Scholar
• Bellmunt J, Hussain M, Gschwend JE, et al. Adjuvant atezolizumab versus observation in muscle-invasive urothelial carcinoma (IMvigor010): a multicentre, open-label, randomised, phase 3 trial. Lancet Oncol. 2021 Apr;22(4):525–537.
   PubMed Web of Science ®Google Scholar
• Powles T, Park SH, Voog E, et al. Avelumab maintenance therapy for advanced or metastatic urothelial carcinoma. N Engl J Med. 2020 Sep 24;383(13):1218–1230.
   PubMed Web of Science ®Google Scholar
• Powles T, Rosenberg JE, Sonpavde GP, et al. Enfortumab vedotin in previously treated advanced urothelial carcinoma. N Engl J Med. 2021 Mar 25;384(12):1125–1135.
   PubMed Web of Science ®Google Scholar
• Tagawa ST, Balar AV, Petrylak DP, et al. TROPHY-U-01: a Phase II open-label study of sacituzumab govitecan in patients with metastatic urothelial carcinoma progressing after platinum-based chemotherapy and checkpoint inhibitors. J Clin Oncol. 2021 Aug 1;39(22):2474–2485.
   PubMed Web of Science ®Google Scholar
• Sharma P, Retz M, Siefker-Radtke A, et al. Nivolumab in metastatic urothelial carcinoma after platinum therapy (CheckMate 275): a multicentre, single-arm, phase 2 trial. Lancet Oncol. 2017 Jan 25;18(3):312–322.
   PubMed Web of Science ®Google Scholar
• Powles T, O’Donnell PH, Massard C, et al. Efficacy and safety of durvalumab in locally advanced or metastatic urothelial carcinoma: updated results from a phase 1/2 open-label study. JAMA Oncol. 2017 Aug;17(9):e172411.
   Google Scholar
• Bellmunt J, von der Maase H, Mead GM, et al. Randomized phase III study comparing paclitaxel/cisplatin/gemcitabine and gemcitabine/cisplatin in patients with locally advanced or metastatic urothelial cancer without prior systemic therapy: EORTC Intergroup Study 30987. J Clin Oncol. 2012 Apr 1;30(10):1107–1113.
   PubMed Web of Science ®Google Scholar
• De Santis M, Bellmunt J, Mead G, et al. Randomized phase II/III trial assessing gemcitabine/carboplatin and methotrexate/carboplatin/vinblastine in patients with advanced urothelial cancer who are unfit for cisplatin-based chemotherapy: EORTC study 30986. J Clin Oncol. 2012 Jan 10;30(2):191–199.
   PubMed Web of Science ®Google Scholar
• Galsky MD, Hahn NM, Rosenberg J, et al. Treatment of patients with metastatic urothelial cancer “unfit” for Cisplatin-based chemotherapy. J Clin Oncol. 2011 Jun 10;29(17):2432–2438.
   PubMed Web of Science ®Google Scholar
• Galsky MD, Chen GJ, Oh WK, et al. Comparative effectiveness of cisplatin-based and carboplatin-based chemotherapy for treatment of advanced urothelial carcinoma. Ann Oncol. 2012 Feb;23(2):406–410.
   PubMed Web of Science ®Google Scholar
• Sonpavde G. PD-1 and PD-L1 inhibitors as salvage therapy for urothelial carcinoma. N Engl J Med. 2017 Mar 16;376(11):1073–1074.
   PubMed Web of Science ®Google Scholar
• Rosenberg JE, Hoffman-Censits J, Powles T, et al. Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: a single-arm, multicentre, phase 2 trial. Lancet. 2016 May 07;387(10031):1909–1920.
   PubMed Web of Science ®Google Scholar
• Massard C, Gordon MS, Sharma S, et al. Safety and Efficacy of Durvalumab (MEDI4736), an anti-programmed cell death ligand-1 immune checkpoint inhibitor, in patients with advanced urothelial bladder cancer. J Clin Oncol. 2016 Sep 10;34(26):3119–3125.
   PubMed Web of Science ®Google Scholar
• Patel MR, Ellerton J, Infante JR, et al. Avelumab in metastatic urothelial carcinoma after platinum failure (JAVELIN Solid Tumor): pooled results from two expansion cohorts of an open-label, phase 1 trial. Lancet Oncol. 2018 Jan;19(1):51–64.
   PubMed Web of Science ®Google Scholar
• Balar AV, Galsky MD, Rosenberg JE, et al. Atezolizumab as first-line treatment in cisplatin-ineligible patients with locally advanced and metastatic urothelial carcinoma: a single-arm, multicentre, phase 2 trial. Lancet. 2017 Jan 7;389(10064):67–76.
   PubMed Web of Science ®Google Scholar
• Powles TPS, Voog E, Park Se Hoon, et al. Maintenance avelumab + best supportive care (BSC) versus BSC alone after platinum-based first-line (1L) chemotherapy in advanced urothelial carcinoma (UC): JAVELIN Bladder 100 phase III interim analysis.
   Google Scholar
• Powles T, van der Heijden MS, Castellano D, et al. Durvalumab alone and durvalumab plus tremelimumab versus chemotherapy in previously untreated patients with unresectable, locally advanced or metastatic urothelial carcinoma (Danube): a randomised, open-label, multicentre, phase 3 trial. Lancet Oncol. 2020 Sep 21;21(12):1574–1588.
   PubMed Web of Science ®Google Scholar
• Galsky MD, Arija JAA, Bamias A, et al. Atezolizumab with or without chemotherapy in metastatic urothelial cancer (IMvigor130): a multicentre, randomised, placebo-controlled phase 3 trial. Lancet. 2020 May 16;395(10236):1547–1557.
   PubMed Web of Science ®Google Scholar
• Powles T, Csoszi T, Ozguroglu M, et al. Pembrolizumab alone or combined with chemotherapy versus chemotherapy as first-line therapy for advanced urothelial carcinoma (KEYNOTE-361): a randomised, open-label, phase 3 trial. Lancet Oncol. 2021 May 26;22(7):931–945.
   PubMed Web of Science ®Google Scholar
• Hoimes CJ, Flaig TW, Milowsky MI, et al. Enfortumab vedotin plus pembrolizumab in previously untreated advanced urothelial cancer. J Clin Oncol. 2023 Jan 1;41(1):22–31. DOI:10.1200/JCO.22.01643
   PubMed Web of Science ®Google Scholar
• Powles T, editor. Erdafitinib (ERDA) or ERDA plus cetrelimab (CET) for patients with metastatic or locally advanved urothelial cacinoma (mUC) and fibroblast growth factor receptor alterations (FGFRa): first phase 2 results from the NORSE study. ESMO; 2021.
   Google Scholar
• Powles T, Duran I, van der Heijden MS, et al. Atezolizumab versus chemotherapy in patients with platinum-treated locally advanced or metastatic urothelial carcinoma (IMvigor211): a multicentre, open-label, phase 3 randomised controlled trial. Lancet. 2018 Feb 24;391(10122):748–757.
   PubMed Web of Science ®Google Scholar
• Ayers M, Lunceford J, Nebozhyn M, et al. IFN-gamma-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 2017 Aug 01;127(8):2930–2940.
   PubMed Web of Science ®Google Scholar
• Teo MY, Seier K, Ostrovnaya I, et al. Alterations in DNA damage response and repair genes as potential marker of clinical benefit from PD-1/PD-L1 blockade in advanced urothelial cancers. J Clin Oncol. 2018 Jun 10;36(17):1685–1694.
   PubMed Web of Science ®Google Scholar
• Wang L, Saci A, Szabo PM, et al. EMT- and stroma-related gene expression and resistance to PD-1 blockade in urothelial cancer. Nat Commun. 2018 Aug 29;9(1):3503.
   PubMed Web of Science ®Google Scholar
• Mariathasan S, Turley SJ, Nickles D, et al. TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature. 2018 Feb 22;554(7693):544–548.
   PubMed Web of Science ®Google Scholar
• Kim J, Kwiatkowski D, McConkey DJ, et al. The cancer genome atlas expression subtypes stratify response to checkpoint inhibition in advanced urothelial cancer and identify a subset of patients with high survival probability. Eur Urol. 2019 Jun;75(6):961–964.
   PubMed Web of Science ®Google Scholar
• Galsky MDBR, Banchereau HR, Hamidi HR, et al. Tumor, immune, and stromal characteristics associated with clinical outcomes with atezolizumab (atezo) + platinum-based chemotherapy (PBC) or atezo monotherapy (mono) versus PBC in metastatic urothelial cancer (mUC) from the phase III IMvigor130 study. J Clin Oncol. 2020;38(15_suppl):5011.
   Google Scholar
• Necchi A, Raggi D, Gallina A, et al. Impact of molecular subtyping and immune infiltration on pathological response and outcome following neoadjuvant pembrolizumab in muscle-invasive bladder cancer. Eur Urol. 2020 Mar 9;77(6):701–710.
   PubMed Web of Science ®Google Scholar
• Pignot G, Bieche I, Vacher S, et al. Large-scale real-time reverse transcription-PCR approach of angiogenic pathways in human transitional cell carcinoma of the bladder: identification of VEGFA as a major independent prognostic marker. Eur Urol. 2009 Oct;56(4):678–688.
   PubMedGoogle Scholar
• Narayanan S, Srinivas S. Incorporating VEGF-targeted therapy in advanced urothelial cancer. Ther Adv Med Oncol. 2017 Jan;9(1):33–45.
   PubMedGoogle Scholar
• AVASTIN (bevacizumab) label U.S. Food and Drug Administration website. [ updated 2009]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2009/125085s0169lbl.pdf
   Google Scholar
• CYRAMZA (ramucirumab) label U.S. Food and Drug Administration website. [ updated 2014]. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2014/125477s002lbl.pdf
   Google Scholar
• Jain RK. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med. 2001 Sep;7(9):987–989.
   PubMed Web of Science ®Google Scholar
• Ghafouri S, Burkenroad A, Pantuck M, et al. VEGF inhibition in urothelial cancer: the past, present and future. World J Urol. 2021 Mar;39(3):741–749.
   PubMedGoogle Scholar
• Balar AV, Apolo AB, Ostrovnaya I, et al. Phase II study of gemcitabine, carboplatin, and bevacizumab in patients with advanced unresectable or metastatic urothelial cancer. J Clin Oncol. 2013 Feb 20;31(6):724–730.
   PubMed Web of Science ®Google Scholar
• Rosenberg JE, Ballman KA, Halabi S, et al. Randomized Phase III trial of gemcitabine and cisplatin with bevacizumab or placebo in patients with advanced urothelial carcinoma: results of CALGB 90601 (Alliance). J Clin Oncol. 2021 Aug 1;39(22):2486–2496.
   PubMed Web of Science ®Google Scholar
• Petrylak DP, de Wit R, Chi KN, et al. Ramucirumab plus docetaxel versus placebo plus docetaxel in patients with locally advanced or metastatic urothelial carcinoma after platinum-based therapy (RANGE): overall survival and updated results of a randomised, double-blind, phase 3 trial. Lancet Oncol. 2020 Jan;21(1):105–120.
   PubMed Web of Science ®Google Scholar
• van der Heijden MS, Powles T, Petrylak D, et al. Predictive biomarkers for survival benefit with ramucirumab in urothelial cancer in the RANGE trial. Nat Commun. 2022 Apr 6;13(1):1878.
   PubMedGoogle Scholar
• Torres-Jimenez J, Albarran-Fernandez V, Pozas J, et al. Novel tyrosine kinase targets in urothelial carcinoma. Int J Mol Sci. 2021 Jan 13;22(2):747.
   PubMedGoogle Scholar
• Hudis CA. Trastuzumab–mechanism of action and use in clinical practice. N Engl J Med. 2007 Jul 5;357(1):39–51.
   PubMed Web of Science ®Google Scholar
• van der Geer P, Hunter T, Lindberg RA. Receptor protein-tyrosine kinases and their signal transduction pathways. Annu Rev Cell Biol. 1994;10(1):251–337.
   PubMedGoogle Scholar
• El Ochi MR, Oukabli M, Bouaiti E, et al. Expression of human epidermal growth factor receptor 2 in bladder urothelial carcinoma. BMC Clin Pathol. 2017;17(1):3.
   PubMedGoogle Scholar
• Zhao J, Xu W, Zhang Z, et al. Prognostic role of HER2 expression in bladder cancer: a systematic review and meta-analysis. Int Urol Nephrol. 2015 Jan;47(1):87–94.
   PubMed Web of Science ®Google Scholar
• Gan K, Gao Y, Liu K, et al. The clinical significance and prognostic value of HER2 expression in bladder cancer: a meta-analysis and a bioinformatic analysis. Front Oncol. 2021;11:653491.
   PubMedGoogle Scholar
• Hussain MH, MacVicar GR, Petrylak DP, et al. Trastuzumab, paclitaxel, carboplatin, and gemcitabine in advanced human epidermal growth factor receptor-2/neu-positive urothelial carcinoma: results of a multicenter phase II National Cancer Institute trial. J Clin Oncol. 2007 Jun 1;25(16):2218–2224.
   PubMed Web of Science ®Google Scholar
• Oudard S, Culine S, Vano Y, et al. Multicentre randomised phase II trial of gemcitabine+platinum, with or without trastuzumab, in advanced or metastatic urothelial carcinoma overexpressing Her2. Eur J Cancer. 2015 Jan;51(1):45–54.
   PubMed Web of Science ®Google Scholar
• Nami B, Maadi H, Wang Z. Mechanisms underlying the action and synergism of trastuzumab and pertuzumab in targeting HER2-positive breast cancer. Cancers (Basel). 2018 Sep 20;10(10):342.
   PubMed Web of Science ®Google Scholar
• Garcia-Garcia C, Ibrahim YH, Serra V, et al. Dual mTORC1/2 and HER2 blockade results in antitumor activity in preclinical models of breast cancer resistant to anti-HER2 therapy. Clin Cancer Res. 2012 May 1;18(9):2603–2612.
   PubMed Web of Science ®Google Scholar
• Meric-Bernstam F, Hainsworth J, Bose R, et al. MyPathway HER2 basket study: pertuzumab (P) + trastuzumab (H) treatment of a large, tissue-agnostic cohort of patients with HER2-positive advanced solid tumors. J clin oncol. 2021;39(15_suppl):3004.
   Web of Science ®Google Scholar
• Szklener K, Chmiel P, Michalski A, et al. New directions and challenges in targeted therapies of advanced bladder cancer: the role of FGFR inhibitors. Cancers (Basel). 2022 Mar 10;14(6):1416.
   PubMedGoogle Scholar
• Rodriguez-Vida A, Saggese M, Hughes S, et al. Complexity of FGFR signalling in metastatic urothelial cancer. J Hematol Oncol. 2015 Oct;24(8):119.
   Google Scholar
• Bellmunt J, Picus J, Kohli M, et al. FIERCE-21: phase 1b/2 study of docetaxel + b-701, a selective inhibitor of FGFR3, in relapsed or refractory (R/R) metastatic urothelial carcinoma (mUCC). J clin oncol. 2018;36(15_suppl):4534.
   Google Scholar
• Necchi A, Castellano DE, Mellado B, et al. Fierce-21: phase II study of vofatmab (B-701), a selective inhibitor of FGFR3, as salvage therapy in metastatic urothelial carcinoma (mUC). J clin oncol. 2019;37(7_suppl):409.
   Google Scholar
• Siefker-Radtke AO, Currie G, Abella E, et al. FIERCE-22: clinical activity of vofatamab (V) a FGFR3 selective inhibitor in combination with pembrolizumab (P) in WT metastatic urothelial carcinoma, preliminary analysis. J clin oncol. 2019;37(15_suppl):4511.
   Web of Science ®Google Scholar
• Alderton GK. FGFR3 is key. Nat Rev Cancer. 2009;9(6):387.
   Google Scholar
• Odonnell P, Goldman JW, Gordon MS, et al. 621 A phase i dose-escalation study of MFGR1877S, a Human Monoclonal Anti-fibroblast Growth Factor Receptor 3 (FGFR3) Antibody, in Patients (pts) with advanced solid tumors. Eur J Cancer. 2012;48:191–192.
   Web of Science ®Google Scholar
• Krook MA, Reeser JW, Ernst G, et al. Fibroblast growth factor receptors in cancer: genetic alterations, diagnostics, therapeutic targets and mechanisms of resistance. Br J Cancer. 2021 Mar;124(5):880–892.
   PubMed Web of Science ®Google Scholar
• Vey N, Karlin L, Sadot-Lebouvier S, et al. A phase 1 study of lirilumab (antibody against killer immunoglobulin-like receptor antibody KIR2D; IPH2102) in patients with solid tumors and hematologic malignancies. Oncotarget. 2018 Apr 3;9(25):17675–17688.
   PubMedGoogle Scholar
• Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011 Mar 25;331(6024):1565–1570.
   PubMed Web of Science ®Google Scholar
• Xu Y, Wang L, Li W, et al. Killer immunoglobulin-like receptors/human leukocyte antigen class-I, a crucial immune pathway in cancer. Ann Transl Med. 2020 Mar;8(5):244.
   PubMedGoogle Scholar
• Grivas P, Yin J, Koshkin VS, et al. PrE0807: a phase Ib feasibility trial of neoadjuvant nivolumab (N) without or with lirilumab (L) in cisplatin-ineligible patients (pts) with muscle-invasive bladder cancer (MIBC). J clin oncol. 2021;39(15_suppl):4518.
   Google Scholar
• Abdel-Wahab N, Montazari E, Spillson C, et al. Tocilizumab in combination with ipilimumab and nivolumab in solid tumors. J clin oncol. 2022;40(16_suppl):9600.
   Google Scholar
• Diab A, Abdel-Wahab N, Bentebibel SE, et al. 169TiP Tocilizumab, ipilimumab, and nivolumab for the treatment of advanced melanoma, non-small cell lung cancer, or urothelial carcinoma. Ann Oncol. 2021;32:S1456.
   Google Scholar
• Benjamin JE, Higgins N, Millward C, et al. First-in-human phase Ib study of ATRC-101, an engineered version of a patient-derived antibody targeting a tumor-restricted ribonucleoprotein complex. J clin oncol. 2020;38(15_suppl):3168–3168.
   Google Scholar
• Benjamin JE, Higgins N, Millward C, et al. Abstract CT203: first-in-human phase 1b study of ATRC-101, a patient-derived antibody with a tumor-specific target, as monotherapy or in combination with pembrolizumab, in patients with solid tumors. Cancer Res. 2021;81(13_Supplement):CT203–CT203.
   Google Scholar
• Sheng X, He Z, Shi Y, et al. RC48-ADC for metastatic urothelial carcinoma with HER2-positive: combined analysis of RC48-C005 and RC48-C009 trials. J clin oncol. 2022;40(16_suppl):4520.
   Google Scholar
• Rosenberg JE, Milowsky M, Ramamurthy C, et al. LBA73 - Study EV-103 Cohort K: antitumor activity of enfortumab vedotin (EV) monotherapy or in combination with pembrolizumab (P) in previously untreated cisplatin-ineligible patients (pts) with locally advanced or metastatic urothelial cancer (la/mUC). Ann Oncol. 2022;33(suppl_7):S808–S869.
   Google Scholar