Significantly different immunological score in lung adenocarcinoma and squamous cell carcinoma and a proposal for a new immune staging system

References

• Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2). doi:10.3322/caac.21262.
   PubMed Web of Science ®Google Scholar
• Herbst RS, Heymach JV, Lippman SM. Lung cancer. N Engl J Med. 2008;359(13):1367–12. doi:10.1056/NEJMra0802714.
   PubMed Web of Science ®Google Scholar
• Davidson MR, Gazdar AF, Clarke BE. The pivotal role of pathology in the management of lung cancer. J Thorac Dis. 2013;5(Suppl 5):S463–78. doi:10.3978/j..2072-1439.2013.08.43.
   PubMed Web of Science ®Google Scholar
• Langer CJ, Besse B, Gualberto A, Brambilla E, Soria JC. The evolving role of histology in the management of advanced non-small-cell lung cancer. J Clin Oncol Off J Am Soc Clin Oncol. 2010;28(36):5311–5320. doi:10.1200/jco.2010.28.8126.
   PubMed Web of Science ®Google Scholar
• Chen Z, Fillmore CM, Hammerman PS, Kim CF, Wong -K-K. Non-small-cell lung cancers: a heterogeneous set of diseases. Nat Rev Cancer. 2014;14(8):535–546. doi:10.1038/nrc3775.
   PubMed Web of Science ®Google Scholar
• Mlecnik B, Bindea G, Pagès F, Galon J. Tumor immunosurveillance in human cancers. Cancer Metastasis Rev. 2011;30(1). doi:10.1007/s10555-011-9270-7.
   PubMed Web of Science ®Google Scholar
• Pilotto S, Sperduti I, Novello S, Peretti U, Milella M, Facciolo F, Vari S, Leuzzi G, Vavalà T, Marchetti A, et al. Risk stratification model for resected squamous-cell lung cancer patients according to clinical and pathological factors. J Thorac Oncol. 2015;10(9):1341–1348. doi:10.1097/jto.0000000000000628.
   PubMed Web of Science ®Google Scholar
• Pilotto S, Sperduti I, Leuzzi G, Chiappetta M, Mucilli F, Ratto GB, Lococo F, Filosso PL, Spaggiari L, Novello S, et al. Prognostic model for resected squamous cell lung cancer: external multicenter validation and propensity score analysis exploring the impact of adjuvant and neoadjuvant treatment. J Thorac Oncol. 2018;13(4):568–575. doi:10.1016/j.jtho.2017.12.003.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12(4):298–306. doi:10.1038/nrc3245.
   PubMed Web of Science ®Google Scholar
• Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006;313(5795):1960–1964. doi:10.1126/science.1129139.
   PubMed Web of Science ®Google Scholar
• Angell H, Galon J. From the immune contexture to the Immunoscore: the role of prognostic and predictive immune markers in cancer. Curr Opin Immunol. 2013;25(2):261–267. doi:10.1016/j.coi.2013.03.004.
   PubMed Web of Science ®Google Scholar
• Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science. 2011;331(6024):1565–1570. doi:10.1126/science.1203486.
   PubMed Web of Science ®Google Scholar
• Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, Lugli A, Zlobec I, Hartmann A, Bifulco C, et al. Towards the introduction of the ‘Immunoscore’ in the classification of malignant tumours. J Pathol. 2014;232(2):199–209. doi:10.1002/path.4287.
   PubMed Web of Science ®Google Scholar
• Galon J, Pagès F, Marincola FM, Thurin M, Trinchieri G, Fox BA, Gajewski TF, Ascierto PA. The immune score as a new possible approach for the classification of cancer. J Transl Med. 2012;10(1):1. doi:10.1186/1479-5876-10-1.
   PubMed Web of Science ®Google Scholar
• Galon J, Pagès F, Marincola FM, Angell HK, Thurin M, Lugli A, Zlobec I, Berger A, Bifulco C, Botti G, et al. Cancer classification using the Immunoscore: a worldwide task force. J Transl Med. 2012;10(1):205. doi:10.1186/1479-5876-10-205.
   PubMed Web of Science ®Google Scholar
• Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, Goc J, Lepelley A, Becht E, Katsahian S, Bizouard G, et al. Presence of B cells in tertiary lymphoid structures is associated with a protective immunity in patients with lung cancer. Am J Respir Crit Care Med. 2014;189(7):832–844. doi:10.1164/rccm.201309-1611OC.
   PubMed Web of Science ®Google Scholar
• Dieu-Nosjean MC, Giraldo NA, Kaplon H, Germain C, Fridman WH, Sautès-Fridman C. Tertiary lymphoid structures, drivers of the anti-tumor responses in human cancers. Immunol Rev. 2016;271(1):260–275. doi:10.1111/imr.12405.
   PubMed Web of Science ®Google Scholar
• Schalper KA, Brown J, Carvajal-Hausdorf D, McLaughlin J, Velcheti V, Syrigos KN, Herbst RS, Rimm DL. Objective measurement and clinical significance of TILs in non-small cell lung cancer. J Natl Cancer Inst. 2015;107(3). doi:10.1093/jnci/dju435.
   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
• Mansuet-Lupo A, Alifano M, Pécuchet N, Biton J, Becht E, Goc J, Germain C, Ouakrim H, Régnard J, Cremer I, et al. Intratumoral immune cell densities are associated with lung adenocarcinoma gene alterations. Am J Respir Crit Care Med. 2016;194(11):1403–1412. doi:10.1164/rccm.201510-2031OC.
   PubMed Web of Science ®Google Scholar
• Kim MY, Koh J, Kim S, Go H, Jeon YK, Chung DH. Clinicopathological analysis of PD-L1 and PD-L2 expression in pulmonary squamous cell carcinoma: comparison with tumor-infiltrating T cells and the status of oncogenic drivers. Lung Cancer (Amsterdam, Neth). 2015;88(1):24–33. doi:10.1016/j.lungcan.2015.01.016.
   PubMed Web of Science ®Google Scholar
• Donnem T, Kilvaer TK, Andersen S, Richardsen E, Paulsen EE, Hald SM, Al-Saad S, Brustugun OT, Helland A, Lund-Iversen M, et al. Strategies for clinical implementation of TNM-Immunoscore in resected nonsmall-cell lung cancer. Ann Oncol. 2016;27(2):225–232. doi:10.1093/annonc/mdv560.
   PubMed Web of Science ®Google Scholar
• Paulsen -E-E, Kilvaer TK, Khanehkenari MR, Al-Saad S, Hald SM, Andersen S, Richardsen E, Ness N, Busund L-T, Bremnes RM, et al. Assessing PDL-1 and PD-1 in non–small cell lung cancer: a novel immunoscore approach. Clin Lung Cancer. 2017;18(2):220–33.e8. doi:10.1016/j.cllc.2016.09.009.
   PubMed Web of Science ®Google Scholar
• Paulsen -E-E, Kilvaer T, Khanehkenari MR, Maurseth RJ, Al-Saad S, Hald SM, Al-Shibli K, Andersen S, Richardsen E, Busund L-T, et al. CD45RO(+) memory t lymphocytes–a candidate marker for TNM-immunoscore in squamous non-small cell lung cancer. Neoplasia. 2015;17(11):839–848. doi:10.1016/j.neo.2015.11.004.
   PubMed Web of Science ®Google Scholar
• Zhang J-X, Song W, Chen Z-H, Wei J-H, Liao Y-J, Lei J, Hu M, Chen G-Z, Liao B, Lu J, et al. Prognostic and predictive value of a microRNA signature in stage II colon cancer: a microRNA expression analysis. Lancet Oncol. 2013;14(13):1295–1306. doi:10.1016/S1470-2045(13)70491-1.
   PubMed Web of Science ®Google Scholar
• Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16(4):385–395. doi:10.1002/(SICI)1097-0258(19970228)16:4<385::AID-SIM380>3.0.CO;2-3.
   PubMed Web of Science ®Google Scholar
• Tibshirani R. Regression shrinkage and selection via the lasso. J R Stat Soc Ser B (Methodol). 1996;58(1):267–288. doi:10.1111/j.2517-6161.1996.tb02080.x.
   Google Scholar
• Han Y, Ye X, Cheng J, Zhang S, Feng W, Han Z, Zhang J, Huang K. Integrative analysis based on survival associated co-expression gene modules for predicting Neuroblastoma patients’ survival time. Biol Direct. 2019;14(1):4. doi:10.1186/s13062-018-0229-2.
   PubMed Web of Science ®Google Scholar
• Giese MA, Hind LE, Huttenlocher A. Neutrophil plasticity in the tumor microenvironment. Blood. 2019;133(20):2159–2167. doi:10.1182/blood-2018-11-844548.
   PubMed Web of Science ®Google Scholar
• Rakaee M, Busund L-T, Paulsen -E-E, Richardsen E, Al-Saad S, Andersen S, Donnem T, Bremnes RM, Kilvaer TK. Prognostic effect of intratumoral neutrophils across histological subtypes of non-small cell lung cancer. Oncotarget. 2016;7(44):72184–72196. doi:10.18632/oncotarget.12360.
   PubMedGoogle Scholar
• Mita Y, Kimura MY, Hayashizaki K, Koyama-Nasu R, Ito T, Motohashi S, Okamoto Y, Nakayama T. Crucial role of CD69 in anti-tumor immunity through regulating the exhaustion of tumor-infiltrating T cells. Int Immunol. 2018;30(12):559–567. doi:10.1093/intimm/dxy050.
   PubMed Web of Science ®Google Scholar
• Allard B, Longhi MS, Robson SC, Stagg J. The ectonucleotidases CD39 and CD73: novel checkpoint inhibitor targets. Immunol Rev. 2017;276(1):121–144. doi:10.1111/imr.12528.
   PubMed Web of Science ®Google Scholar
• Burugu S, Dancsok AR, Nielsen TO. Emerging targets in cancer immunotherapy. Semin Cancer Biol. 2018;52(Pt 2):39–52. doi:10.1016/j.semcancer.2017.10.001.
   PubMed Web of Science ®Google Scholar
• Anderson AC, Joller N, Kuchroo VK. Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation. Immunity. 2016;44(5):989–1004. doi:10.1016/j.immuni.2016.05.001.
   PubMed Web of Science ®Google Scholar
• Yang L, Yang Y, Ma P, Zheng B, Liu W, Zhang Z, Ding N, Liu L, Mao Y, Lv N, et al. Spread through air spaces predicts a worse survival in patients with stage I adenocarcinomas >2 cm after radical lobectomy. J Thorac Dis. 2018;10(9):5308–5317. doi:10.21037/jtd.2018.09.22.
   PubMed Web of Science ®Google Scholar
• Jia L, Zhang Q, Zhang R. PD-1/PD-L1 pathway blockade works as an effective and practical therapy for cancer immunotherapy. Cancer Biol Med. 2018;15(2):116–123. doi:10.20892/j..2095-3941.2017.0086.
   PubMed Web of Science ®Google Scholar
• Chen W. IDO: more than an enzyme. Nat Immunol. 2011;12(9):809–811. doi:10.1038/ni.2088.
   PubMed Web of Science ®Google Scholar
• Yu H, Boyle TA, Zhou C, Rimm DL, Hirsch FR. PD-L1 expression in lung cancer. J Thorac Oncol. 2016;11(7):964–975. doi:10.1016/j.jtho.2016.04.014.
   PubMed Web of Science ®Google Scholar
• Zhang M, Li G, Wang Y, Wang Y, Zhao S, Haihong P, Zhao H, Wang Y. PD-L1 expression in lung cancer and its correlation with driver mutations: a meta-analysis. Sci Rep. 2017;7(1):10255. doi:10.1038/s41598-017-10925-7.
   PubMed Web of Science ®Google Scholar
• Tang Y, Fang W, Zhang Y, Hong S, Kang S, Yan Y, Chen N, Zhan J, He X, Qin T, et al. The association between PD-L1 and EGFR status and the prognostic value of PD-L1 in advanced non-small cell lung cancer patients treated with EGFR-TKIs. Oncotarget. 2015;6(16):14209–14219. doi:10.18632/oncotarget.3694.
   PubMed Web of Science ®Google Scholar
• Schmidt LH, Kümmel A, Görlich D, Mohr M, Bröckling S, Mikesch JH, Grünewald I, Marra A, Schultheis AM, Wardelmann E, et al. PD-1 and PD-L1 expression in NSCLC indicate a favorable prognosis in defined subgroups. PLoS ONE. 2015;10(8):e0136023. doi:10.1371/journal.pone.0136023.
   PubMed Web of Science ®Google Scholar
• Leclerc BG, Charlebois R, Chouinard G, Allard B, Pommey S, Saad F, Stagg J. CD73 expression is an independent prognostic factor in prostate cancer. Clin Cancer Res. 2016;22(1):158–166. doi:10.1158/1078-0432.CCR-15-1181.
   PubMed Web of Science ®Google Scholar
• Wang CM, Ploia C, Anselmi F, Sarukhan A, Viola A. Adenosine triphosphate acts as a paracrine signaling molecule to reduce the motility of T cells. Embo J. 2014;33(12):1354–1364. doi:10.15252/embj.201386666.
   PubMed Web of Science ®Google Scholar
• Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med. 2010;207(10):2187–2194. doi:10.1084/jem.20100643.
   PubMed Web of Science ®Google Scholar
• Jia K, He Y, Dziadziuszko R, Zhao S, Zhang X, Deng J, Wang H, Hirsch FR, Zhou C, Yu H, et al. T cell immunoglobulin and mucin-domain containing-3 in non-small cell lung cancer. Transl Lung Cancer Res. 2019;8(6):895–906. doi:10.21037/tlcr.2019.11.17.
   PubMed Web of Science ®Google Scholar
• Li H, Wu K, Tao K, Chen L, Zheng Q, Lu X, Liu J, Shi L, Liu C, Wang G, et al. Tim-3/galectin-9 signaling pathway mediates T-cell dysfunction and predicts poor prognosis in patients with hepatitis B virus-associated hepatocellular carcinoma. Hepatology. 2012;56(4):1342–1351. doi:10.1002/hep.25777.
   PubMed Web of Science ®Google Scholar
• Rakaee M, Kilvaer TK, Dalen SM, Richardsen E, Paulsen -E-E, Hald SM, Al-Saad S, Andersen S, Donnem T, Bremnes RM, et al. Evaluation of tumor-infiltrating lymphocytes using routine H&E slides predicts patient survival in resected non-small cell lung cancer. Hum Pathol. 2018;79:188–198. doi:10.1016/j.humpath.2018.05.017.
   PubMed Web of Science ®Google Scholar
• Meng X, Gao Y, Yang L, Jing H, Teng F, Huang Z, Xing L. Immune microenvironment differences between squamous and non-squamous non–small-cell lung cancer and their influence on the prognosis. Clin Lung Cancer. 2019;20(1):48–58. doi:10.1016/j.cllc.2018.09.012.
   PubMed Web of Science ®Google Scholar
• Azuma K, Ota K, Kawahara A, Hattori S, Iwama E, Harada T, Matsumoto K, Takayama K, Takamori S, Kage M, et al. Association of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancer. Ann Oncol. 2014;25(10):1935–1940. doi:10.1093/annonc/mdu242.
   PubMed Web of Science ®Google Scholar
• Faruki H, Mayhew GM, Serody JS, Hayes DN, Perou CM, Lai-Goldman M. Lung adenocarcinoma and squamous cell carcinoma gene expression subtypes demonstrate significant differences in tumor immune landscape. J Thorac Oncol. 2017;12(6):943–953. doi:10.1016/j.jtho.2017.03.010.
   PubMed Web of Science ®Google Scholar
• Gkountakos A, Pilotto S, Mafficini A, Vicentini C, Simbolo M, Milella M, Tortora G, Scarpa A, Bria E, Corbo V, et al. Unmasking the impact of Rictor in cancer: novel insights of mTORC2 complex. Carcinogenesis. 2018;39(8):971–980. doi:10.1093/carcin/bgy086.
   PubMed Web of Science ®Google Scholar
• Chen W, Zheng R, Zhang S, Zhao P, Li G, Wu L, He J. Report of incidence and mortality in China cancer registries, 2009. Chin J Cancer Res. 2013;25(1):10–21. doi:10.3978/j..1000-9604.2012.12.04.
   PubMed Web of Science ®Google Scholar