Clinical impact of T cells, B cells and the PD-1/PD-L1 pathway in muscle invasive bladder cancer: a comparative study of transurethral resection and cystectomy specimens

References

• Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):1–14. doi:10.1002/ijc.29210.
   PubMed Web of Science ®Google Scholar
• Alfred Witjes J, Lebret T, Comperat EM, Cowan NC, De Santis M, Bruins HM, Hernandez V, Espinos EL, Dunn J, Rouanne M, et al. Updated 2016 EAU guidelines on muscle-invasive and metastatic bladder cancer. Eur Urol. 2017;71(3):462–475. doi:10.1016/j.eururo.2016.06.020.
   PubMed Web of Science ®Google Scholar
• Leal J, Luengo-Fernandez R, Sullivan R, Witjes JA. Economic burden of bladder cancer across the European union. Eur Urol. 2016;69(3):438–447. doi:10.1016/j.eururo.2015.10.024.
   PubMed Web of Science ®Google Scholar
• Raghavan D, Shipley WU, Garnick MB, Russell PJ, Richie JP. Biology and management of bladder cancer. N Engl J Med. 1990;322(16):1129–1138. doi:10.1056/NEJM199004193221607.
   PubMed Web of Science ®Google Scholar
• Stein JP, Lieskovsky G, Cote R, Groshen S, Feng AC, Boyd S, Skinner E, Bochner B, Thangathurai D, Mikhail M, et al. Radical cystectomy in the treatment of invasive bladder cancer: long-term results in 1,054 patients. J Clin Oncol. 2001;19(3):666–675. doi:10.1200/JCO.2001.19.3.666.
   PubMed Web of Science ®Google Scholar
• Grossman HB, Natale RB, Tangen CM, Speights VO, Vogelzang NJ, Trump DL, deVere White RW, Sarosdy MF, Wood DP Jr., Raghavan D, et al. Neoadjuvant chemotherapy plus cystectomy compared with cystectomy alone for locally advanced bladder cancer. N Engl J Med. 2003;349(9):859–866. doi:10.1056/NEJMoa022148.
   PubMed Web of Science ®Google Scholar
• Advanced Bladder Cancer (ABC) Meta-analysis Collaboration. Neoadjuvant chemotherapy in invasive bladder cancer: update of a systematic review and meta-analysis of individual patient data. Eur Urol. 2005;48(2):202–5. doi:10.1016/j.eururo.2005.04.006.
   Web of Science ®Google Scholar
• Baras AS, Drake C, Liu JJ, Gandhi N, Kates M, Hoque MO, Meeker A, Hahn N, Taube JM, Schoenberg MP, et al. The ratio of CD8 to Treg tumor-infiltrating lymphocytes is associated with response to cisplatin-based neoadjuvant chemotherapy in patients with muscle invasive urothelial carcinoma of the bladder. Oncoimmunology. 2016;5(5):e1134412. doi:10.1080/2162402X.2015.1134412.
   PubMed Web of Science ®Google Scholar
• Lee FC, Harris W, Cheng HH, Shenoi J, Zhao S, Wang J, Champion T, Izard J, Gore JL, Porter M, et al. Pathologic response rates of gemcitabine/cisplatin versus methotrexate/vinblastine/adriamycin/cisplatin neoadjuvant chemotherapy for muscle invasive urothelial bladder cancer. Adv Urol. 2013;2013:317190. doi:10.1155/2013/317190.
   PubMedGoogle Scholar
• Taube JM, Galon J, Sholl LM, Rodig SJ, Cottrell TR, Giraldo NA, Baras AS, Patel SS, Anders RA, Rimm DL, et al. Implications of the tumor immune microenvironment for staging and therapeutics. Mod Pathol. 2018;31(2):214–234. doi:10.1038/modpathol.2017.156.
   PubMed Web of Science ®Google Scholar
• Liu Z, Zhu Y, Xu L, Zhang J, Xie H, Fu H, Zhou Q, Chang Y, Dai B, Xu J. Tumor stroma-infiltrating mast cells predict prognosis and adjuvant chemotherapeutic benefits in patients with muscle invasive bladder cancer. Oncoimmunology. 2018;7(9):e1474317. doi:10.1080/2162402X.2018.1490854.
   PubMed Web of Science ®Google Scholar
• Pichler R, Heidegger I, Fritz J, Danzl M, Sprung S, Zelger B, Brunner A, Pircher A. PD-L1 expression in bladder cancer and metastasis and its influence on oncologic outcome after cystectomy. Oncotarget. 2017;8(40):66849–66864. doi:10.18632/oncotarget.19913.
   PubMedGoogle Scholar
• Huang HS, Su HY, Li PH, Chiang PH, Huang CH, Chen CH, Hsieh MC. Prognostic impact of tumor infiltrating lymphocytes on patients with metastatic urothelial carcinoma receiving platinum based chemotherapy. Sci Rep. 2018;8(1):7485. doi:10.1038/s41598-018-25944-1.
   PubMedGoogle Scholar
• Sharma P, Shen Y, Wen S, Yamada S, Jungbluth AA, Gnjatic S, Bajorin DF, Reuter VE, Herr H, Old LJ, et al. CD8 tumor-infiltrating lymphocytes are predictive of survival in muscle-invasive urothelial carcinoma. Proc Natl Acad Sci U S A. 2007;104(10):3967–3972. doi:10.1073/pnas.0611618104.
   PubMed Web of Science ®Google Scholar
• Yu A, Mansure JJ, Solanki S, Siemens DR, Koti M, Dias ABT, Burnier MM, Brimo F, Kassouf W. Presence of lymphocytic infiltrate cytotoxic T lymphocyte CD3+, CD8+, and immunoscore as prognostic marker in patients after radical cystectomy. PLoS One. 2018;13(10):e0205746. doi:10.1371/journal.pone.0205746.
   PubMed Web of Science ®Google Scholar
• Winerdal ME, Krantz D, Hartana CA, Zirakzadeh AA, Linton L, Bergman EA, Rosenblatt R, Vasko J, Alamdari F, Hansson J, et al. Urinary bladder cancer tregs suppress MMP2 and potentially regulate invasiveness. Cancer Immunol Res. 2018;6(5):528–538. doi:10.1158/2326-6066.CIR-17-0466.
   PubMed Web of Science ®Google Scholar
• Krantz D, Hartana CA, Winerdal ME, Johansson M, Alamdari F, Jakubczyk T, Huge Y, Aljabery F, Palmqvist K, Zirakzadeh AA, et al. Neoadjuvant chemotherapy reinforces antitumour T cell response in urothelial urinary bladder cancer. Eur Urol. 2018;74(6):688–692. doi:10.1016/j.eururo.2018.06.048.
   PubMed Web of Science ®Google Scholar
• Berntsson J, Nodin B, Eberhard J, Micke P, Jirstrom K. Prognostic impact of tumour-infiltrating B cells and plasma cells in colorectal cancer. Int J Cancer. 2016;139(5):1129–1139. doi:10.1002/ijc.30138.
   PubMed Web of Science ®Google Scholar
• Yuen GJ, Demissie E, Pillai S. B lymphocytes and cancer: a love-hate relationship. Trends Cancer. 2016;2(12):747–757. doi:10.1016/j.trecan.2016.10.010.
   PubMed Web of Science ®Google Scholar
• Al-Shibli KI, Donnem T, Al-Saad S, Persson M, Bremnes RM, Busund LT. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res. 2008;14(16):5220–5227. doi:10.1158/1078-0432.CCR-08-0133.
   PubMed Web of Science ®Google Scholar
• Felsenstein KM, Theodorescu D. Precision medicine for urothelial bladder cancer: update on tumour genomics and immunotherapy. Nat Rev Urol. 2018;15(2):92–111. doi:10.1038/nrurol.2017.179.
   PubMed Web of Science ®Google Scholar
• Kim HS, Seo HK. Immune checkpoint inhibitors for urothelial carcinoma. Investig Clin Urol. 2018;59(5):285–296. doi:10.4111/icu.2018.59.5.285.
   PubMed Web of Science ®Google Scholar
• Faraj SF, Munari E, Guner G, Taube J, Anders R, Hicks J, Meeker A, Schoenberg M, Bivalacqua T, Drake C, et al. Assessment of tumoral PD-L1 expression and intratumoral CD8+ T cells in urothelial carcinoma. Urology. 2015;85(3):703.e1–6. doi:10.1016/j.urology.2014.10.020.
   PubMed Web of Science ®Google Scholar
• Erlmeier F, Seitz AK, Hatzichristodoulou G, Stecher L, Retz M, Gschwend JE, Weichert W, Kubler HR, Horn T. The role of PD-L1 expression and intratumoral lymphocytes in response to perioperative chemotherapy for urothelial carcinoma. Bladder Cancer. 2016;2(4):425–432. doi:10.3233/BLC-160067.
   PubMed Web of Science ®Google Scholar
• Topalian SL, Taube JM, Anders RA, Pardoll DM. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer. 2016;16(5):275–287. doi:10.1038/nrc.2016.36.
   PubMed Web of Science ®Google Scholar
• Mukherji D, Jabbour MN, Saroufim M, Temraz S, Nasr R, Charafeddine M, Assi R, Shamseddine A, Tawil AN. Programmed death-ligand 1 expression in muscle-invasive bladder cancer cystectomy specimens and lymph node metastasis: a reliable treatment selection biomarker? Clin Genitourin Cancer. 2016;14(2):183–187. doi:10.1016/j.clgc.2015.12.002.
   PubMed Web of Science ®Google Scholar
• Burgess EF, Livasy C, Hartman A, Robinson MM, Symanowski J, Naso C, Doherty S, Guerrieri R, Riggs S, Grigg CM, et al. Discordance of high PD-L1 expression in primary and metastatic urothelial carcinoma lesions. Urol Oncol. 2019. doi:10.1016/j.urolonc.2019.01.002.
   PubMed Web of Science ®Google Scholar
• Pottier C, Wheatherspoon A, Roncarati P, Longuespee R, Herfs M, Duray A, Delvenne P, Quatresooz P. The importance of the tumor microenvironment in the therapeutic management of cancer. Expert Rev Anticancer Ther. 2015;15(8):943–954. doi:10.1586/14737140.2015.1059279.
   PubMed Web of Science ®Google Scholar
• Koti M, Xu AS, Ren KYM, Visram K, Ren R, Berman DM, Siemens DR. Tertiary lymphoid structures associate with tumour stage in urothelial bladder cancer. Bladder Cancer. 2017;3(4):259–267. doi:10.3233/BLC-170120.
   PubMed Web of Science ®Google Scholar
• Cheng W, Fu D, Xu F, Zhang Z. Unwrapping the genomic characteristics of urothelial bladder cancer and successes with immune checkpoint blockade therapy. Oncogenesis. 2018;7(1):2. doi:10.1038/s41389-017-0013-7.
   PubMedGoogle Scholar
• Shang B, Liu Y, Jiang SJ, Liu Y. Prognostic value of tumor-infiltrating FoxP3+ regulatory T cells in cancers: a systematic review and meta-analysis. Sci Rep. 2015;5:15179. doi:10.1038/srep15179.
   PubMed Web of Science ®Google Scholar
• Shen M, Sun Q, Wang J, Pan W, Ren X. Positive and negative functions of B lymphocytes in tumors. Oncotarget. 2016;7(34):55828–55839. doi:10.18632/oncotarget.10094.
   PubMedGoogle Scholar
• Drayton DL, Liao S, Mounzer RH, Ruddle NH. Lymphoid organ development: from ontogeny to neogenesis. Nat Immunol. 2006;7(4):344–353. doi:10.1038/ni1330.
   PubMed Web of Science ®Google Scholar
• Pimenta EM, Barnes BJ. Role of tertiary lymphoid structures (TLS) in anti-tumor immunity: potential tumor-induced cytokines/chemokines that regulate TLS formation in epithelial-derived cancers. Cancers. 2014;6(2):969–997. doi:10.3390/cancers6020969.
   PubMed Web of Science ®Google Scholar
• Jiang Q, Fu Q, Chang Y, Liu Z, Zhang J, Xu L, Zhu Y, Wang Y, Zhang W, Xu J. CD19(+) tumor-infiltrating B-cells prime CD4(+) T-cell immunity and predict platinum-based chemotherapy efficacy in muscle-invasive bladder cancer. Cancer Immunol Immunother. CII. 2019;68(1):45-56. doi:10.1007/s00262-018-2250-9.
   Web of Science ®Google Scholar
• Ou Z, Wang Y, Liu L, Li L, Yeh S, Qi L, Chang C. Tumor microenvironment B cells increase bladder cancer metastasis via modulation of the IL-8/androgen receptor (AR)/MMPs signals. Oncotarget. 2015;6(28):26065–26078. doi:10.18632/oncotarget.4569.
   PubMedGoogle Scholar
• Xiang X, Yu PC, Long D, Liao XL, Zhang S, You XM, Zhong JH, Li LQ. Prognostic value of PD -L1 expression in patients with primary solid tumors. Oncotarget. 2018;9(4):5058–5072. doi:10.18632/oncotarget.23580.
   PubMedGoogle Scholar
• Tretiakova M, Fulton R, Kocherginsky M, Long T, Ussakli C, Antic T, Gown A. Concordance study of PD-L1 expression in primary and metastatic bladder carcinomas: comparison of four commonly used antibodies and RNA expression. Mod Pathol. 2018;31(4):623–632. doi:10.1038/modpathol.2017.188.
   PubMed Web of Science ®Google Scholar
• Wu Y, Cao D, Qu L, Cao X, Jia Z, Zhao T, Wang Q, Jiang J. PD-1 and PD-L1 co-expression predicts favorable prognosis in gastric cancer. Oncotarget. 2017;8(38):64066–64082. doi:10.18632/oncotarget.19318.
   PubMedGoogle Scholar
• Ghatalia P, Zibelman M, Geynisman DM, Plimack E. Approved checkpoint inhibitors in bladder cancer: which drug should be used when? Ther Adv Med Oncol. 2018;10:1758835918788310. doi:10.1177/1758835918788310.
   Web of Science ®Google Scholar
• Katz H, Wassie E, Alsharedi M. Checkpoint inhibitors: the new treatment paradigm for urothelial bladder cancer. Med Oncol. 2017;34(10):170. doi:10.1007/s12032-017-1029-8.
   PubMed Web of Science ®Google Scholar
• Balar AV, Castellano D, O’Donnell PH, Grivas P, Vuky J, Powles T, Plimack ER, Hahn NM, de Wit R, Pang L, et al. First-line pembrolizumab in cisplatin-ineligible patients with locally advanced and unresectable or metastatic urothelial cancer (KEYNOTE-052): a multicentre, single-arm, phase 2 study. Lancet Oncol. 2017;18(11):1483–1492. doi:10.1016/S1470-2045(17)30616-2.
   PubMed Web of Science ®Google Scholar
• Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, Bruneval P, Trajanoski Z, Fridman WH, Pages F, et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol. 2011;29(6):610–618. doi:10.1200/JCO.2010.30.5425.
   PubMed Web of Science ®Google Scholar
• Poch M, Hall M, Joerger A, Kodumudi K, Beatty M, Innamarato PP, Bunch BL, Fishman MN, Zhang J, Sexton WJ, et al. Expansion of tumor infiltrating lymphocytes (TIL) from bladder cancer. Oncoimmunology. 2018;7(9):e1476816. doi:10.1080/2162402X.2018.1490854.
   PubMed Web of Science ®Google Scholar
• Sherif A, Winerdal M, Winqvist O. Immune responses to neoadjuvant chemotherapy in muscle invasive bladder cancer. Bladder Cancer. 2018;4(1):1–7. doi:10.3233/BLC-170123.
   PubMed Web of Science ®Google Scholar
• Zirakzadeh AA, Kinn J, Krantz D, Rosenblatt R, Winerdal ME, Hu J, Hartana CA, Lundgren C, Bergman EA, Johansson M, et al. Doxorubicin enhances the capacity of B cells to activate T cells in urothelial urinary bladder cancer. Clin Immunol. 2017;176:63–70. doi:10.1016/j.clim.2016.12.003.
   PubMed Web of Science ®Google Scholar
• Jakobsson L, Chebil G, Marzouka NA, Liedberg F, Sjodahl G. Low frequency of intratumor heterogeneity in bladder cancer tissue microarrays. Bladder Cancer. 2018;4(3):327–337. doi:10.3233/BLC-180176.
   PubMed Web of Science ®Google Scholar