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New Strategies in Bladder Cancer: a Second Coming for Immunotherapy Ali Ghasemzadeh1, Trinity J

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New Strategies in Bladder Cancer: a Second Coming for Immunotherapy Ali Ghasemzadeh1, Trinity J Published OnlineFirst December 18, 2015; DOI: 10.1158/1078-0432.CCR-15-1135 CCR New Strategies Clinical Cancer Research New Strategies in Bladder Cancer: A Second Coming for Immunotherapy Ali Ghasemzadeh1, Trinity J. Bivalacqua1,2,3, Noah M. Hahn1,3, and Charles G. Drake1,3 Abstract Urothelial bladder cancer (UBC) remains one of the most prolonged survival for patients with several different can- common and deadly cancers worldwide, and platinum- cers, including UBC. In this review, we discuss new findings based chemotherapy, which has been the standard-of- in bladder cancer immunotherapy, including recent suc- care in metastatic bladder cancer, has had limited success cesses with immune checkpoint blockade. We also discuss in improving outcomes for patients. The recent develop- therapeutic cancer vaccines and highlight several additional ment and translation of therapeutic strategies aimed at immunotherapy modalities in early stages of development. harnessing the immune system have led to durable and Clin Cancer Res; 22(4); 1–9. Ó2015 AACR. Background mutational burden (11). Mutations can provide neoantigens that can be recognized by the immune system (12). Indeed, a higher Urothelial bladder cancer (UBC) is the sixth most common mutational load has been correlated with better response rates to cancer in the United States, with 74,690 cases diagnosed and immune checkpoint blockade in patients with lung cancer and 15,580 deaths in the year 2014. Similar to many cancers, it is a melanoma (13, 14). These observations and the historically poor disease of the elderly, with a median age of 73 years at diagnosis performance of current therapies in UBC provide a unique oppor- (1). Risk factors for the development of bladder cancer include tunity for the use of immunotherapy. Although a number of cigarette smoking and exposure to cyclic chemicals, dyes, rubbers, excellent reviews have recently described emerging data in tumor textiles, and paints (2). Smoking is the number one environmen- immunology (15–17), the focus of this review is to more specif- tal risk factor and may be associated with the relatively high ically highlight recent advances in immunotherapy for UBC. mutation rate noted in UBC (3, 4). Consequently, this review first provides a brief overview of con- Approximately 70% of bladder cancers are diagnosed when ventional immunotherapy for UBC [bacillus Calmette–Guerin they are non–muscle-invasive (NMIBC; ref. 5). For these (BCG)], and then discusses immune checkpoint blockade as well tumors, transurethral resection of bladder tumor is the standard as agonists and vaccines intended to initiate an antitumor of care and aids in proper staging of the disease. For more immune response. advanced (muscle-invasive disease), the last major therapeutic BCG is an attenuated form of the bovine tuberculosis bacterium advance was the introduction of platinum-based chemotherapy Mycobacterium bovis. The first clinical trial of BCG in bladder cancer almost 30 years ago (6). For patients with advanced UBC, in 1980 showed a 20% reduction in recurrence rate (18). Despite treatment options are limited and often ineffective, and out- its long history, the mechanism of action of BCG is not yet fully comes remain poor (7, 8). Furthermore, for patients for whom understood and is beyond the scope of this article but has recently first-line chemotherapy is not successful, no clearly defined been reviewed (19, 20). Clinically, randomized controlled trials second-line option exists and none have definitively been (RCT) have shown that in NMIBC, BCG immunotherapy reduces shown to prolong overall survival (OS; refs. 9, 10). rates of recurrence and progression while positively affecting Recent understanding of the genomic alterations underlying mortality. RCTs comparing monthly, quarterly, and biannual bladder cancer have not yet led to new targeted therapies, but BCG maintenance showed no sign of increased efficacy compared these insights show UBC to be a cancer with high somatic with induction BCG alone (21–23); however, the 3-week main- tenance schedule of the Southwest Oncology Group demonstrat- ed significant benefit with a 76.8-month recurrence-free survival 1 Department of Oncology, Johns Hopkins Sidney Kimmel Compre- duration (RFS) in the maintenance arm of the study compared hensive Cancer Center, Baltimore, Maryland. 2Department of Surgery, Johns Hopkins Sidney Kimmel Comprehensive Cancer Center, Balti- with 35.7 months with induction therapy alone (24). The 5-year more, Maryland. 3The Brady Urological Institute, Johns Hopkins Sid- survival rate was 78% with induction therapy alone compared ney Kimmel Comprehensive Cancer Center, Baltimore, Maryland. with 83% with maintenance. Thus, only 3-week BCG mainte- Corresponding Author: Charles G. Drake, Departments of Oncology, Immunol- nance has been shown in RCTs to reduce disease progression and ogy, and Urology, Johns Hopkins University School of Medicine, 1650 Orleans improve overall and disease-specific mortality (24, 25). Three- Street, CRB 4M51, Baltimore, MD 21287. Phone: 410-614-3616; Fax: 443-287- week maintenance BCG has also been shown to be superior to 4653; E-mail: [email protected] maintenance with epirubicin chemotherapy and combination doi: 10.1158/1078-0432.CCR-15-1135 treatment with epirubicin and IFNa (25, 26). Intravesical BCG Ó2015 American Association for Cancer Research. immunotherapy remains the gold standard for the treatment of www.aacrjournals.org OF1 Downloaded from clincancerres.aacrjournals.org on September 30, 2021. © 2015 American Association for Cancer Research. Published OnlineFirst December 18, 2015; DOI: 10.1158/1078-0432.CCR-15-1135 Ghasemzadeh et al. NMIBC, and exciting possibilities exist for improving outcomes non–small cell lung cancer (NSCLC), renal cell carcinoma, and in patients with superficial disease by combining BCG with bladdercancer(30–33). other immune-modulatory therapies (Table 1). CTLA-4: the first immune checkpoint. CTL-associated antigen 4 (CTLA4) was the first immune checkpoint for which blockade was On The Horizon shown to enhance antitumor immunity (34). Because CTLA-4 Immune checkpoint blockade functions by dampening T-cell activation, blocking of CTLA-4 The genetic alterations that occur during carcinogenesis enhances T-cell activation. This process is complex; normally, T- provide numerous antigenic targets that can be recognized by cell activation requires two signals; the first is a signal delivered the immune system (12). However, cells of the adaptive when the T-cell receptor recognizes its specific antigen. A second immune system are often inhibited by pathways that are signal is required for full T-cell activation; this signal 2 is delivered dysregulated in tumors and act to suppress their effector func- when B7 molecules on a mature dendritic cell (DC) bind to CD28 tions (27). Over the past 20 years, we have gained greater on the partially activated T cell. T-cell expression of CTLA-4 hijacks understanding of these pathways, which are mediated by cell this process, binding with high affinity to B7 molecules and surface molecules collectively termed "immune checkpoints." preventing the T cell from receiving signal 2 (Fig. 1; ref. 35). In These entities represent a group of functionally related but patients, administration of anti-CTLA-4 leads to increased T-cell biologically distinct cell surface receptors with important phys- activation, a significant rate of objective responses, and a consid- iologic roles in maintaining self-tolerance, modulating the erable rate of immune-related adverse events (irAE; refs. 36, 37). immune response to pathogens, and preventing autoimmunity In that regard, the rate of irAEs induced by CTLA-4 blockade is (28, 29). Blocking antibodies targeting immune checkpoints higher than that observed in patients treated with agents that have shown promise in several cancers, including melanoma, block the checkpoint mediated by the interaction between PD-1 Table 1. Selected immunotherapy trials in UBC Trial ID Immunotherapy Phase n Primary endpoint Remarks CTLA-4 NCT00362713 Ipilimumab I 12 Safety Neoadjuvant therapy; completed NCT01524991 Ipilimumab II 36 OS In combination with gemcitabine and cisplatin; ongoing PD-1 NCT01848834 Pembrolizumab I 297 Safety response rate Bladder cancer cohort in a large phase I trial; ongoing NCT02324582 Pembrolizumab I 15 Safety In combination with BCG vaccine; ongoing NCT01928394 Nivolumab I/II 410 Objective response rate In combination with ipilimumab; ongoing NCT02351739 Pembrolizumab II 74 Objective response rate In combination with ACP-196 (Btk inhibitor); ongoing NCT02256436 Pembrolizumab III 470 OS In comparison to: paclitaxel, vinflunine, docetaxel in patients with disease recurrence or progression following platinum-based therapy; ongoing PD-L1 NCT01375842 Atezolizumab I 344 Dose-limiting toxicities Bladder cancer patients accepted in a large phase I trial; ongoing NCT02108652 Atezolizumab II 439 Objective response rate Potential registration trial; ongoing NCT02451423 Atezolizumab II 42 Change in T-cell count Neoadjuvant therapy in BCG-refractory NMIBC or MIBC prior to Pathologic T0 rate cystectomy; ongoing Pathologic absence of disease in the bladder NCT02450331 Atezolizumab III 440 DFS Patients with MIBC at high risk of recurrence following cystectomy; ongoing NCT02302807 Atezolizumab III 767 OS In comparison to: paclitaxel, vinflunine, docetaxel in patients who have progressed during or following platinum-based therapy; ongoing B7-H3 NCT01391143 MGA271 I 151 Safety In patients
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