Clinical Significance of Tumor-Infiltrating T Cells and Programed Death Ligand-1 in Patients with Pancreatic Cancer

References

• Spadi R, Brusa F, Ponzetti A, Chiappino I, Birocco N, Ciuffreda L, et al. Current therapeutic strategies for advanced pancreatic cancer: a review for clinicians. WJCO. 2016;7(1):27–43. doi:10.5306/wjco.v7.i1.27.
   Web of Science ®Google Scholar
• Tamburrino D, Partelli S, Crippa S, Manzoni A, Maurizi A, Falconi M. Selection criteria in resectable pancreatic cancer: a biological and morphological approach. WJG. 2014;20(32):11210–11215. doi:10.3748/wjg.v20.i32.11210.
   PubMed Web of Science ®Google Scholar
• Hsu CC, Herman JM, Corsini MM, Winter JM, Callister MD, Haddock MG, et al. Adjuvant chemoradiation for pancreatic adenocarcinoma: the Johns Hopkins Hospital-Mayo Clinic collaborative study. Ann Surg Oncol. 2010;17(4):981–990. doi:10.1245/s10434-009-0743-7.
   PubMed Web of Science ®Google Scholar
• Wolfgang CL, Herman JM, Laheru DA, Klein AP, Erdek MA, Fishman EK, et al. Recent progress in pancreatic cancer. CA Cancer J Clin. 2013;63(5):318–348. doi:10.3322/caac.21190.
   PubMed Web of Science ®Google Scholar
• Shin SH, Kim SC, Hong S-M, Song K-B, Lee JH, Park K-M, et al. Can statistically determined prognostic factors predict the long-term survival of patients with pancreatic ductal adenocarcinoma following surgical resection? Clinicopathological analysis of 82 long-term survivors. Pancreas. 2014;43(4):571–577. doi:10.1097/MPA.0000000000000063.
   PubMed Web of Science ®Google Scholar
• Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature. 2008;454(7203):436–444. doi:10.1038/nature07205.
   PubMed Web of Science ®Google Scholar
• Clark CE, Hingorani SR, Mick R, Combs C, Tuveson DA, Vonderheide RH. Dynamics of the immune reaction to pancreatic cancer from inception to invasion. Cancer Res. 2007;67(19):9518–9527. doi:10.1158/0008-5472.CAN-07-0175.
   PubMed Web of Science ®Google Scholar
• Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA. The pancreas cancer microenvironment. Clin Cancer Res. 2012;18(16):4266–4276. doi:10.1158/1078-0432.CCR-11-3114.
   PubMed Web of Science ®Google Scholar
• Ansari D, Carvajo M, Bauden M, Andersson R. Pancreatic cancer stroma: controversies and current insights. Scand J Gastroenterol. 2017;52(6-7):641–646. doi:10.1080/00365521.2017.1293726.
   PubMed Web of Science ®Google Scholar
• Koido S, Homma S, Okamoto M, Takakura K, Mori M, Yoshizaki S, et al. Treatment with chemotherapy and dendritic cells pulsed with multiple Wilms’ tumor gene 1 (WT1)-specific MHC class I/II-restricted epitopes for pancreatic cancer. Clin Cancer Res. 2014;20(16):4228–4239.
   PubMed Web of Science ®Google Scholar
• Kajihara M, Takakura K, Kanai T, Ito Z, Matsumoto Y, Shimodaira S, et al. Advances in inducing adaptive immunity using cell-based cancer vaccines: clinical applications in pancreatic cancer. WJG. 2016;22(18):4446–4458. doi:10.3748/wjg.v22.i18.4446.
   PubMed Web of Science ®Google Scholar
• Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359(6382):1350–1355. doi:10.1126/science.aar4060.
   PubMed Web of Science ®Google Scholar
• Sun C, Mezzadra R, Schumacher TN. Regulation and function of the PD-L1 checkpoint. Immunity. 2018;48(3):434–452. doi:10.1016/j.immuni.2018.03.014.
   PubMed Web of Science ®Google Scholar
• Kabacaoglu D, Ciecielski KJ, Ruess DA, Algul H. Immune checkpoint inhibition for pancreatic ductal adenocarcinoma: current limitations and future options. Front Immunol. 2018;9:1878. doi:10.3389/fimmu.2018.01878.
   PubMed Web of Science ®Google Scholar
• Royal RE, Levy C, Turner K, Mathur A, Hughes M, Kammula US, et al. Phase 2 trial of single agent Ipilimumab (anti-CTLA-4) for locally advanced or metastatic pancreatic adenocarcinoma. J Immunother. 2010;33(8):828–833. doi:10.1097/CJI.0b013e3181eec14c.
   PubMed Web of Science ®Google Scholar
• Nomi T, Sho M, Akahori T, Hamada K, Kubo A, Kanehiro H, et al. Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res. 2007;13(7):2151. doi:10.1158/1078-0432.CCR-06-2746.
   PubMed Web of Science ®Google Scholar
• Winograd R, Byrne KT, Evans RA, Odorizzi PM, Meyer ARL, Bajor DL, et al. Induction of T-cell immunity overcomes complete resistance to PD-1 and CTLA-4 blockade and improves survival in pancreatic carcinoma. Cancer Immunol Res. 2015;3(4):399–411. doi:10.1158/2326-6066.CIR-14-0215.
   PubMed Web of Science ®Google Scholar
• Martinez-Bosch N, Vinaixa J, Navarro P. Immune evasion in pancreatic cancer: from mechanisms to therapy. Cancers. 2018;10(1):6. doi:10.3390/cancers10010006.
   PubMed Web of Science ®Google Scholar
• Soiffer R, Lynch T, Mihm M, Jung K, Rhuda C, Schmollinger JC, et al. Vaccination with irradiated autologous melanoma cells engineered to secrete human granulocyte-macrophage colony-stimulating factor generates potent antitumor immunity in patients with metastatic melanoma. Proc Natl Acad Sci USA. 1998;95(22):13141–13146. doi:10.1073/pnas.95.22.13141.
   PubMed Web of Science ®Google Scholar
• Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The eighth edition AJCC cancer staging manual: continuing to build a bridge from a population-based to a more “personalized” approach to cancer staging. CA Cancer J Clin. 2017;67(2):93–99. doi:10.3322/caac.21388.
   PubMed Web of Science ®Google Scholar
• Kanai T, Ito Z, Oji Y, Suka M, Nishida S, Takakura K, et al. Prognostic significance of Wilms’ tumor 1 expression in patients with pancreatic ductal adenocarcinoma. Oncol Lett. 2018;16:2682–2692. doi:10.3892/ol.2018.8961.
   PubMed Web of Science ®Google Scholar
• Metindir J, Dilek GB, Pak I. Staining characterization by immunohistochemistry of tumor cancer antigen in patients with endometrial cancer. Eur J Gynaecol Oncol. 2008;29(5):489–492.
   PubMed Web of Science ®Google Scholar
• Balermpas P, Michel Y, Wagenblast J, Seitz O, Weiss C, Rödel F, et al. Tumour-infiltrating lymphocytes predict response to definitive chemoradiotherapy in head and neck cancer. Br J Cancer. 2014;110(2):501–509. doi:10.1038/bjc.2013.640.
   PubMed Web of Science ®Google Scholar
• Dahlin AM, Henriksson ML, Van Guelpen B, Stenling R, Oberg A, Rutegard J, et al. Colorectal cancer prognosis depends on T-cell infiltration and molecular characteristics of the tumor. Modern pathology: an official journal of the United States and Canadian Academy of Pathology. Mod Pathol. 2011;24:671–682. doi:10.1038/modpathol.2010.234.
   PubMed Web of Science ®Google Scholar
• Teng MW, Ngiow SF, Ribas A, Smyth MJ. Classifying cancers based on T-cell infiltration and PD-L1. Cancer Res. 2015;75(11):2139–2145. doi:10.1158/0008-5472.CAN-15-0255.
   PubMed Web of Science ®Google Scholar
• Diana A, Wang LM, D'Costa Z, Allen P, Azad A, Silva MA, et al. Prognostic value, localization and correlation of PD-1/PD-L1, CD8 and FOXP3 with the desmoplastic stroma in pancreatic ductal adenocarcinoma. Oncotarget. 2016;7(27):40992–41004. doi:10.18632/oncotarget.10038.
   PubMedGoogle Scholar
• Ono T, Azuma K, Kawahara A, Sasada T, Hattori S, Sato F, et al. Association between PD-L1 expression combined with tumor-infiltrating lymphocytes and the prognosis of patients with advanced hypopharyngeal squamous cell carcinoma. Oncotarget. 2017;8(54):92699–92714. doi:10.18632/oncotarget.21564.
   PubMedGoogle Scholar
• Zhang K, Hua Y-Q, Wang D, Chen L-Y, Wu C-J, Chen Z, et al. Systemic immune-inflammation index predicts prognosis of patients with advanced pancreatic cancer. J Transl Med. 2019;17(1):30. doi:10.1186/s12967-019-1782-x.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Wei Q, Fan J, Cheng S, Ding W, Hua Z. Prognostic role of the neutrophil-to-lymphocyte ratio in pancreatic cancer: a meta-analysis containing 8252 patients. Clin Chim Acta. 2018;479:181–189. doi:10.1016/j.cca.2018.01.024.
   PubMed Web of Science ®Google Scholar
• Zhang J, Wolfgang CL, Zheng L. Precision immuno-oncology: prospects of individualized immunotherapy for pancreatic cancer. Cancers. 2018;10(2):39. doi:10.3390/cancers10020039.
   Web of Science ®Google Scholar
• Ino Y, Yamazaki-Itoh R, Shimada K, Iwasaki M, Kosuge T, Kanai Y, et al. Immune cell infiltration as an indicator of the immune microenvironment of pancreatic cancer. Br J Cancer. 2013;108(4):914–923. doi:10.1038/bjc.2013.32.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Zitvogel L, Sautes-Fridman C, Kroemer G. The immune contexture in cancer prognosis and treatment. Nat Rev Clin Oncol. 2017;14(12):717–734. doi:10.1038/nrclinonc.2017.101.
   PubMed Web of Science ®Google Scholar
• Sideras K, Biermann K, Yap K, Mancham S, Boor PPC, Hansen BE, et al. Tumor cell expression of immune inhibitory molecules and tumor-infiltrating lymphocyte count predict cancer-specific survival in pancreatic and ampullary cancer. Int J Cancer. 2017;141(3):572–582. doi:10.1002/ijc.30760.
   PubMed Web of Science ®Google Scholar
• Imai D, Yoshizumi T, Okano S, Uchiyama H, Ikegami T, Harimoto N, et al. The prognostic impact of programmed cell death ligand 1 and human leukocyte antigen class I in pancreatic cancer. Cancer Med. 2017;6(7):1614–1626. doi:10.1002/cam4.1087.
   PubMed Web of Science ®Google Scholar
• Cullen SP, Martin SJ. Mechanisms of granule-dependent killing. Cell Death Differ. 2008;15(2):251–262. doi:10.1038/sj.cdd.4402244.
   PubMed Web of Science ®Google Scholar
• Church SE, Jensen SM, Antony PA, Restifo NP, Fox BA. Tumor-specific CD4+ T cells maintain effector and memory tumor-specific CD8+ T cells. Eur J Immunol. 2014;44(1):69–79. doi:10.1002/eji.201343718.
   PubMed Web of Science ®Google Scholar
• Kleeff J, Beckhove P, Esposito I, Herzig S, Huber PE, Löhr JM, et al. Pancreatic cancer microenvironment. Int J Cancer. 2007;121(4):699–705. doi:10.1002/ijc.22871.
   PubMed Web of Science ®Google Scholar
• Birnbaum DJ, Finetti P, Lopresti A, Gilabert M, Poizat F, Turrini O, et al. Prognostic value of PDL1 expression in pancreatic cancer. Oncotarget. 2016;7(44):71198–71210. doi:10.18632/oncotarget.11685.
   PubMedGoogle Scholar
• Takakura K, Ito Z, Suka M, Kanai T, Matsumoto Y, Odahara S, et al. Comprehensive assessment of the prognosis of pancreatic cancer: peripheral blood neutrophil-lymphocyte ratio and immunohistochemical analyses of the tumour site. Scand J Gastroenterol. 2016;51(5):610–617. doi:10.3109/00365521.2015.1121515.
   PubMed Web of Science ®Google Scholar
• Kalbasi A, June CH, Haas N, Vapiwala N. Radiation and immunotherapy: a synergistic combination. J Clin Invest. 2013;123(7):2756–2763. doi:10.1172/JCI69219.
   PubMed Web of Science ®Google Scholar
• Koido S, Homma S, Takahara A, Namiki Y, Tsukinaga S, Mitobe J, et al. Current immunotherapeutic approaches in pancreatic cancer. Clin Dev Immunol. 2011;2011:267539. doi:10.1155/2011/267539.
   PubMed Web of Science ®Google Scholar
• Blando J, Sharma A, Higa MG, Zhao H, Vence L, Yadav SS, et al. Comparison of immune infiltrates in melanoma and pancreatic cancer highlights VISTA as a potential target in pancreatic cancer. Proc Natl Acad Sci USA. 2019;116(5):1692–1697. doi:10.1073/pnas.1811067116.
   PubMed Web of Science ®Google Scholar
• Ott PA, Hodi FS, Kaufman HL, Wigginton JM, Wolchok JD. Combination immunotherapy: a road map. J Immunother Cancer. 2017;5:16. doi:10.1186/s40425-017-0218-5.
   PubMed Web of Science ®Google Scholar
• Zhang P, Zou M, Wen X, Gu F, Li J, Liu G, et al. Development of serum parameters panels for the early detection of pancreatic cancer. Int J Cancer. 2014;134(11):2646–2655. doi:10.1002/ijc.28584.
   PubMed Web of Science ®Google Scholar
• Hanada S, Tsuruta T, Haraguchi K, Okamoto M, Sugiyama H, Koido S. Long-term survival of pancreatic cancer patients treated with multimodal therapy combined with WT1-targeted dendritic cell vaccines. Hum Vaccin Immunother. 2019;15:397–406. doi:10.1080/21645515.2018.1524238.
   PubMed Web of Science ®Google Scholar
• Lutz ER, Wu AA, Bigelow E, Sharma R, Mo G, Soares K, et al. Immunotherapy converts nonimmunogenic pancreatic tumors into immunogenic foci of immune regulation. Cancer Immunol Res. 2014;2(7):616–631. doi:10.1158/2326-6066.CIR-14-0027.
   PubMed Web of Science ®Google Scholar