Waiting in the wings: the emerging role of molecular biomarkers in bladder cancer

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67:7–30.
   PubMed Web of Science ®Google Scholar
• Kamat AM, Hegarty PK, Gee JR, et al. ICUD-EAU International consultation on bladder cancer 2012: screening, diagnosis, and molecular markers. Eur Urol. 2013;63:4–15.
   PubMed Web of Science ®Google Scholar
• Svatek R S, Hollenbeck BK, Holmäng S, et al. The economics of bladder cancer: costs and considerations of caring for this disease. Eur Urol. 2014;66:253–262.
   PubMed Web of Science ®Google Scholar
• Babjuk M, Böhle A, Burger M, et al. EAU guidelines on non–muscle-invasive urothelial carcinoma of the bladder: update 2016. Eur Urol. 2016;1–15. DOI:10.1016/j.eururo.2016.05.041.
   Google Scholar
• Burger M, Catto JWF, Dalbagni G, et al. Epidemiology and risk factors of urothelial bladder cancer. Eur Urol. 2013;63:234–241.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Margulis V, Lotan Y, et al. Nomograms for bladder cancer. Eur Urol. 2008;54:41–53.
   PubMed Web of Science ®Google Scholar
• Karakiewicz PI, Shariat SF, Palapattu GS, et al. Precystectomy nomogram for prediction of advanced bladder cancer stage. Eur Urol. 2006;50:1254–1262.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Craig Z, Gerson L, et al. Nomograms including nuclear matrix protein 22 for prediction of disease recurrence and progression in patients with Ta, T1 or CIS transitional cell carcinoma of the bladder. J Urol. 2005;173:1518–1525.
   PubMed Web of Science ®Google Scholar
• Xylinas E, Kent M, Kluth L, et al. Accuracy of the EORTC risk tables and of the CUETO scoring model to predict outcomes in non-muscle-invasive urothelial carcinoma of the bladder. Br J Cancer. 2013;109:1460–1466.
   PubMed Web of Science ®Google Scholar
• Ballman KV. Biomarker: predictive or prognostic? J Clin Oncol. 2015;33:3968–3971.
   PubMed Web of Science ®Google Scholar
• Bensalah K, Montorsi F, Shariat SF. Challenges of cancer biomarker profiling. Eur Urol. 2007;52:1601–1609.
   PubMed Web of Science ®Google Scholar
• Babjuk M, Böhle A, Burger M, et al. eau guidelines on non–muscle-invasive urothelial carcinoma of the bladder: update 2016. Eur Urol. 2017;71:447–461.
   PubMed Web of Science ®Google Scholar
• Kamat AM, Sylvester RJ, Böhle A, et al. Definitions, end points, and clinical trial designs for non–muscle-invasive bladder cancer: recommendations from the international bladder cancer group. J Clin Oncol. 2016;34:1935–1944.
   PubMed Web of Science ®Google Scholar
• Redelman-Sidi G, Glickman MS, Bochner BH. The mechanism of action of BCG therapy for bladder cancer–a current perspective. Nat Rev Urol. 2014;11:153–162.
   PubMed Web of Science ®Google Scholar
• De Boer EC, De Jong WH, Van Der Meijden APM, et al. Presence of activated lymphocytes in the urine of patients with superficial bladder cancer after intravesical immunotherapy with bacillus Calmette-Guérin. Cancer Immunol Immunother. 1991;33:411–416.
   PubMed Web of Science ®Google Scholar
• Kamat AM, Briggman J, Urbauer DL, et al. Platinum priority – brief correspondence cytokine panel for response to intravesical therapy (CyPRIT): nomogram of changes in urinary cytokine levels predicts patient response to bacillus calmette-Gué rin. Eur Urol. 2016;69:197–200.
   PubMed Web of Science ®Google Scholar
• Mbeutcha A, Shariat SF, Rieken M, et al. Prognostic significance of markers of systemic inflammatory response in patients with non–muscle-invasive bladder cancer. Urol Oncol Semin Orig Investig. 2016;34:483.e17–483.e24.
   PubMed Web of Science ®Google Scholar
• Nunez-Nateras R, Castle EP, Protheroe CA, et al. Predicting response to bacillus Calmette-Guérin (BCG) in patients with carcinoma in situ of the bladder. Urol Oncol Semin Orig Investig. 2014;32:45.e23–45.e30.
   PubMed Web of Science ®Google Scholar
• Pichler R, Gruenbacher G, Culig Z, et al. Intratumoral Th2 predisposition combines with an increased Th1 functional phenotype in clinical response to intravesical BCG in bladder cancer. Cancer Immunol Immunother. 2017;66:427–440.
   PubMed Web of Science ®Google Scholar
• Lima L, Dinis-Ribeiro M, Longatto-Filho A, et al. Predictive biomarkers of bacillus Calmette-Guérin immunotherapy response in bladder cancer: where are we now? Adv Urol. 2012;2012. DOI:10.1155/2012/232609
   Google Scholar
• Fu C, Zhao H, Wang Y, et al. Tumor-associated antigens: tn antigen, sTn antigen, and T antigen. Hla. 2016;88:275–286.
   PubMed Web of Science ®Google Scholar
• Lima L, Severino PF, Silva M, et al. Response of high-risk of recurrence/progression bladder tumours expressing sialyl-Tn and sialyl-6-T to BCG immunotherapy. Br J Cancer. 2013;109:2106–2114.
   PubMed Web of Science ®Google Scholar
• Margulis V, Shariat SF, Ashfaq R, et al. Ki-67 is an independent predictor of bladder cancer outcome in patients treated with radical cystectomy for organ-confined disease. Clin Cancer Res. 2006;12:7369–7373.
   PubMed Web of Science ®Google Scholar
• Margulis V, Lotan Y, Karakiewicz PI, et al. multi-institutional validation of the predictive value of Ki-67 labeling index in patients with urinary bladder cancer. JNCI J Natl Cancer Inst. 2009;101:114–119.
   Web of Science ®Google Scholar
• Malmström PU, Hemdan T, Segersten U. Validation of the ezrin, CK20, and Ki-67 as potential predictive markers for BCG instillation therapy of non–muscle-invasive bladder cancer. Urol Oncol Semin Orig Investig. 2017;35:532.e1–532.e6.
   PubMed Web of Science ®Google Scholar
• Lima L, Oliveira D, Ferreira JA, et al. The role of functional polymorphisms in immune response genes as biomarkers of bacille Calmette-Guérin (BCG) immunotherapy outcome in bladder cancer: establishment of a predictive profile in a Southern Europe population. BJU Int. 2015;116:753–763.
   PubMed Web of Science ®Google Scholar
• Lima L, Ferreira JA, Tavares A, et al. FASL polymorphism is associated with response to bacillus Calmette-Guérin immunotherapy in bladder cancer. Urol Oncol Semin Orig Investig. 2014;32:1–7.
   PubMed Web of Science ®Google Scholar
• Houston A, O’Connell J. The Fas signalling pathway and its role in the pathogenesis of cancer. Curr Opin Pharmacol. 2004;4:321–326.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Ashfaq R, Karakiewicz PI, et al. Survivin expression is associated with bladder cancer presence, stage, progression, and mortality. Cancer. 2007;109:1106–1113.
   PubMed Web of Science ®Google Scholar
• Karam JA, Lotan Y, Ashfaq R, et al. survivin expression in patients with non-muscle-invasive urothelial cell carcinoma of the bladder. Urology. 2007;70:482–486.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Pierre IK, Guilherme G, et al. Survivin as a prognostic marker for urothelial carcinoma of the bladder: a multicenter external validation study. Clin Cancer Res. 2009;15:7012–7019.
   PubMed Web of Science ®Google Scholar
• Jaiswal PK, Goel A, Mandhani A, et al. Functional polymorphisms in promoter survivin gene and its association with susceptibility to bladder cancer in North Indian cohort. Mol Biol Rep. 2012;39:5615–5621.
   PubMedGoogle Scholar
• Scott SN, Ostrovnaya I, Lin CM, et al. Next-generation sequencing of urine specimens: A novel platform for genomic analysis in patients with non-muscle-invasive urothelial carcinoma treated with bacille Calmette-Guérin. Cancer. 2017;125:416–426.
   PubMed Web of Science ®Google Scholar
• Pietzak EJ, Bagrodia A, Cha EK, et al. Next-generation sequencing of nonmuscle invasive bladder cancer reveals potential biomarkers and rational therapeutic targets. Eur Urol. 2017;72:952–959. DOI:10.1016/j.eururo.2017.05.032.
   PubMed Web of Science ®Google Scholar
• Wolff EM, Chihara Y, Pan F, et al. Unique DNA methylation patterns distinguish noninvasive and invasive urothelial cancers and establish an epigenetic field defect in premalignant tissue. Cancer Res. 2010;70:8169–8178.
   PubMed Web of Science ®Google Scholar
• Mikeska T, Bock C, Do H, et al. DNA methylation biomarkers in cancer: progress towards clinical implementation. Expert Rev Mol Diagn. 2012;12:473–487.
   PubMed Web of Science ®Google Scholar
• Alvarez-Múgica M, Fernández-Gómez JM, Cebrian V, et al. Polyamine-modulated factor-1 methylation predicts bacillus Calmette-Guérin response in patients with high-grade non-muscle-invasive bladder carcinoma. Eur Urol. 2013;63:364–370.
   PubMed Web of Science ®Google Scholar
• Witjes JA, Lebret T, Compérat EM, et al. Updated 2016 EAU guidelines on muscle-invasive and metastatic bladder cancer. Eur Urol. 2017;71:462–475.
   PubMed Web of Science ®Google Scholar
• Kluth LA, Black PC, Bochner BH, et al. prognostic and prediction tools in bladder cancer: a comprehensive review of the literature. Eur Urol. 2015;68:238–253.
   PubMed Web of Science ®Google Scholar
• Schiffmann J, Sun M, Gandaglia G, et al. Suboptimal use of neoadjuvant chemotherapy in radical cystectomy patients: A population-based study. Can Urol Assoc J. 2016;10:82.
   PubMed Web of Science ®Google Scholar
• Moschini M, Soria F, Klatte T, et al. validation of preoperative risk grouping of the selection of patients most likely to benefit from neoadjuvant chemotherapy before radical cystectomy. Clin Genitourin Cancer. 2017;15:e267–e273.
   PubMedGoogle Scholar
• Miyake H, Hara I, Yamanaka K, et al. Synergistic enhancement of resistance to cisplatin in human bladder cancer cells by overexpression of mutant-type p53 and Bcl-2. J Urol. 1999;162:2176–2181.
   PubMed Web of Science ®Google Scholar
• Kiss B, Skuginna V, Fleischmann A, et al. Bcl-2 predicts response to neoadjuvant chemotherapy and is overexpressed in lymph node metastases of urothelial cancer of the bladder. Urol Oncol Semin Orig Investig. 2015;33:166.e1–166.e8.
   Web of Science ®Google Scholar
• Himpel S, Panzer P, Eirmbter K, et al. Identification of the autophosphorylation sites and characterization of their effects in the protein kinase DYRK1A. Biochem J. 2001;359:497–505.
   PubMed Web of Science ®Google Scholar
• Aranda S, Laguna A, de la Luna S. DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. Faseb J. 2011;25:449–462.
   PubMed Web of Science ®Google Scholar
• Oda K, Arakawa H, Tanaka T, et al. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell. 2000;102:849–862.
   PubMed Web of Science ®Google Scholar
• Taira N, Nihira K, Yamaguchi T, et al. DYRK2 is targeted to the nucleus and controls p53 via Ser46 phosphorylation in the apoptotic response to DNA damage. Mol Cell. 2007;25:725–738.
   PubMed Web of Science ®Google Scholar
• Nomura S, Suzuki Y, Takahashi R, et al. Dual-specificity tyrosine phosphorylation-regulated kinase 2 (DYRK2) as a novel marker in T1 high-grade and T2 bladder cancer patients receiving neoadjuvant chemotherapy. BMC Urol. 2015;15:53.
   PubMed Web of Science ®Google Scholar
• Hemdan T, Malmström P-U, Jahnson S, et al. Emmprin expression predicts response and survival following cisplatin containing chemotherapy for bladder cancer: a validation study. J Urol. 2015;194:1575–1581.
   PubMed Web of Science ®Google Scholar
• Ishida S, Lee J, Thiele DJ, et al. Uptake of the anticancer drug cisplatin mediated by the copper transporter Ctr1 in yeast and mammals. Proc Natl Acad Sci U S A. 2002;99:14298–14302.
   PubMed Web of Science ®Google Scholar
• Song I-S, Savaraj N, Siddik ZH, et al. Role of human copper transporter Ctr1 in the transport of platinum-based antitumor agents in cisplatin-sensitive and cisplatin-resistant cells. Mol Cancer Ther. 2004;3:1543–1549.
   PubMed Web of Science ®Google Scholar
• Kilari D, Iczkowski KA, Pandya C, et al. Copper transporter-CTR1 expression and pathological outcomes in platinum-treated muscle-invasive bladder cancer patients. Anticancer Res. 2016;36:495–501.
   PubMed Web of Science ®Google Scholar
• De Sousa Cavalcante L, Gemcitabine: MG. Metabolism and molecular mechanisms of action, sensitivity and chemoresistance in pancreatic cancer. Eur J Pharmacol. 2014;741:8–16.
   PubMed Web of Science ®Google Scholar
• North S, El-Gehani F, Santos C, et al. Expression of nucleoside transporters and deoxycytidine kinase proteins in muscle invasive urothelial carcinoma of the bladder: correlation with pathological response to neoadjuvant platinum/gemcitabine combination chemotherapy. J Urol. 2014;191:35–39.
   PubMed Web of Science ®Google Scholar
• Guarino M. Epithelial-mesenchymal transition and tumour invasion. Int J Biochem Biol. 2007;39:2153–2160.
   PubMed Web of Science ®Google Scholar
• Nomura S, Suzuki Y, Takahashi R, et al. Snail expression and outcome in T1 high-grade and T2 bladder cancer: a retrospective immunohistochemical analysis. BMC Urol. 2013;13:73.
   PubMed Web of Science ®Google Scholar
• Marteijn JA, Lans H, Vermeulen W, et al. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol. 2014;15:465–481.
   PubMed Web of Science ®Google Scholar
• Kawashima A, Takayama H, Kawamura N, et al. Co-expression of ERCC1 and snail is a prognostic but not predictive factor of cisplatin-based neoadjuvant chemotherapy for bladder cancer. Oncol Lett. 2012;4:15–21.
   PubMed Web of Science ®Google Scholar
• Ozcan MF, Dizdar O, Dincer N, et al. Low ERCC1 expression is associated with prolonged survival in patients with bladder cancer receiving platinum-based neoadjuvant chemotherapy. Urol Oncol. 2013;31:1709–1715.
   PubMed Web of Science ®Google Scholar
• Klatte T, Seitz C, Rink M, et al. ERCC1 as a prognostic and predictive biomarker for urothelial carcinoma of the bladder following radical cystectomy. J Urol. 2015;194:1456–1462.
   PubMed Web of Science ®Google Scholar
• Choueiri TK, Jacobus S, Bellmunt J, et al. Neoadjuvant dose-dense methotrexate, vinblastine, doxorubicin, and cisplatin with pegfilgrastim support in muscle-invasive urothelial cancer: pathologic, radiologic, and biomarker correlates. J Clin Oncol. 2014;32:1889–1894.
   PubMed Web of Science ®Google Scholar
• Baras AS, Gandhi N, Munari E, et al. Identification and validation of protein biomarkers of response to neoadjuvant platinum chemotherapy in muscle invasive urothelial carcinoma. PLoS One. 2015;10:e0131245.
   PubMed Web of Science ®Google Scholar
• Van Allen EM, Mouw KW, Kim P, et al. Somatic ERCC2 mutations correlate with cisplatin sensitivity in muscle-invasive urothelial carcinoma. Cancer Discov. 2014;4:1140–1153.
   PubMed Web of Science ®Google Scholar
• Liu D, Plimack ER, Hoffman-Censits J, et al. Clinical validation of chemotherapy response biomarker ercc2 in muscle-invasive urothelial bladder carcinoma. JAMA Oncol. 2016;2:1094.
   PubMed Web of Science ®Google Scholar
• Plimack ER, Dunbrack RL, Brennan TA, et al. Defects in DNA repair genes predict response to neoadjuvant cisplatin-based chemotherapy in muscle-invasive bladder cancer. Eur Urol. 2015;68:959–967.
   PubMed Web of Science ®Google Scholar
• Hynes NE, Lane HA. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer. 2005;5:341–354.
   PubMed Web of Science ®Google Scholar
• Forbes SA, Beare D, Boutselakis H, et al.COSMIC: somatic cancer genetics at high-resolution.Nucleic Acids Res.2017;45.
   Web of Science ®Google Scholar
• de Martino M, Zhuang D, Klatte T, et al. Impact of ERBB2 mutations on in vitro sensitivity of bladder cancer to lapatinib. Cancer Biol Ther. 2014;15:1239–1247.
   PubMed Web of Science ®Google Scholar
• Kiss B, Wyatt AW, Douglas J, et al. Her2 alterations in muscle-invasive bladder cancer: patient selection beyond protein expression for targeted therapy. Sci Rep. 2017;7:42713.
   PubMed Web of Science ®Google Scholar
• Groenendijk FH, De Jong J, Fransen Van De Putte EE, et al. ERBB2 mutations characterize a subgroup of muscle-invasive bladder cancers with excellent response to neoadjuvant chemotherapy. Eur Urol. 2016;69:384–388.
   PubMed Web of Science ®Google Scholar
• Choi W, Porten S, Kim S, et al. Identification of Distinct Basal and Luminal Subtypes of Muscle-Invasive Bladder Cancer with Different Sensitivities to Frontline Chemotherapy. Cancer Cell. 2014;25:152–165.
   PubMed Web of Science ®Google Scholar
• McConkey DJ, Choi W, Shen Y, et al. A prognostic gene expression signature in the molecular classification of chemotherapy-naïve urothelial cancer is predictive of clinical outcomes from neoadjuvant chemotherapy: a phase 2 trial of dose-dense methotrexate, vinblastine, doxorubicin, and cisplatin with bevacizumab in urothelial cancer. Eur Urol. 2016;69:855–862.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Chade DC, Karakiewicz PI, et al. Combination of multiple molecular markers can improve prognostication in patients with locally advanced and lymph node positive bladder cancer. J Urol. 2010;183:68–75.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Zlotta AR, Ashfaq R, et al. Cooperative effect of cell-cycle regulators expression on bladder cancer development and biologic aggressiveness. Mod Pathol. 2007;20:445–459.
   PubMed Web of Science ®Google Scholar
• Seiler R, Ashab HAD, Erho N, et al. Impact of molecular subtypes in muscle-invasive bladder cancer on predicting response and survival after neoadjuvant chemotherapy. Eur Urol. 2017;72:544–554.
   PubMed Web of Science ®Google Scholar
• Xylinas E, Hassler M, Zhuang D, et al. An epigenomic approach to improving response to neoadjuvant cisplatin chemotherapy in bladder cancer. Biomolecules. 2016;6:37.
   Web of Science ®Google Scholar
• Sun J-M, Sung J-Y, Park SH, et al. ERCC1 as a biomarker for bladder cancer patients likely to benefit from adjuvant chemotherapy. BMC Cancer. 2012;12:187.
   PubMed Web of Science ®Google Scholar
• Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer. 2009;9:153–166.
   PubMed Web of Science ®Google Scholar
• Jirawatnotai S, Hu Y, Michowski W, et al. A function for cyclin D1 in DNA repair uncovered by protein interactome analyses in human cancers. Nature. 2011;474:230–234.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Ashfaq R, Sagalowsky AI, et al. Correlation of cyclin D1 and E1 expression with bladder cancer presence, invasion, progression, and metastasis. Hum Pathol. 2006;37:1568–1576.
   PubMed Web of Science ®Google Scholar
• Ren B, Li W, Yang Y, et al. The impact of cyclin D1 overexpression on the prognosis of bladder cancer: a meta-analysis. World J Surg Oncol. 2014;12:55.
   PubMed Web of Science ®Google Scholar
• Seiler R, Thalmann GN, Rotzer D, et al. CCND1/CyclinD1 status in metastasizing bladder cancer: a prognosticator and predictor of chemotherapeutic response. Mod Pathol. 2014;27:87–95.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Gust KM. Immune therapy meets precision medicine. Lancet Oncol. 2017;18:271–273.
   PubMed Web of Science ®Google Scholar
• Abufaraj M, Dalbagni G, Daneshmand S, et al. The role of surgery in metastatic bladder cancer: a systematic review. Eur Urol. 2017. DOI:10.1016/j.eururo.2017.09.030.
   PubMed Web of Science ®Google Scholar
• Shariat SF, Kim J, Raptidis G, et al. Association of p53 and p21 expression with clinical outcome in patients with carcinoma in situ of the urinary bladder. Urology. 2003;61:1140–1145.
   PubMed Web of Science ®Google Scholar