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Original Research

Phenotypic characterization of spatial immune infiltration niches in non-small cell lung cancer

ORCID Icon, , , , &
Article: 2206725 | Received 19 Jan 2023, Accepted 21 Apr 2023, Published online: 27 Apr 2023

References

  • Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–11. doi:10.3322/caac.21708.
  • Ramalingam SS, Vansteenkiste J, Planchard D, Cho BC, Gray JE, Ohe Y, Zhou C, Reungwetwattana T, Cheng Y, Chewaskulyong B, et al. Overall survival with osimertinib in untreated, EGFR-Mutated advanced NSCLC. N Engl J Med. 2020;382(1):41–50. doi:10.1056/NEJMoa1913662.
  • Camidge DR, Dziadziuszko R, Peters S, Mok T, Noe J, Nowicka M, Gadgeel SM, Cheema P, Pavlakis N, de Marinis F, et al. Updated efficacy and safety data and impact of the EML4-ALK fusion variant on the efficacy of alectinib in untreated ALK-Positive advanced non–small cell lung cancer in the global Phase III ALEX study. J Thorac Oncol. 2019;14(7):1233–1243. doi:10.1016/j.jtho.2019.03.007.
  • Liu L, Bai H, Wang C, Seery S, Wang Z, Duan J, Li S, Xue P, Wang G, Sun Y, et al. Efficacy and Safety Of First-Line Immunotherapy Combinations For Advanced NSCLC: a systematic review and network meta-analysis. J Thorac Oncol. 2021;16(7):1099–1117. doi:10.1016/j.jtho.2021.03.016.
  • Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, et al. Nivolumab versus docetaxel in advanced nonsquamous non–small-cell lung cancer. N Engl J Med. 2015;373(17):1627–1639. doi:10.1056/NEJMoa1507643.
  • Genova C, Dellepiane C, Carrega P, Sommariva S, Ferlazzo G, Pronzato P, Gangemi R, Filaci G, Coco S, Croce M. Therapeutic implications of tumor microenvironment in lung cancer: focus on immune checkpoint blockade. Front Immunol. 2021;12:799455. doi:10.3389/fimmu.2021.799455.
  • Altorki NK, Markowitz GJ, Gao D, Port JL, Saxena A, Stiles B, McGraw T, Mittal V. The lung microenvironment: an important regulator of tumour growth and metastasis. Nat Rev Cancer. 2019;19(1):9–31. doi:10.1038/s41568-018-0081-9.
  • Zugazagoitia J, Gupta S, Liu Y, Fuhrman K, Gettinger S, Herbst RS, Schalper KA, Rimm DL. Biomarkers associated with beneficial PD-1 checkpoint blockade in non–small cell lung cancer (NSCLC) identified using high-plex digital spatial profiling. Clin Cancer Res. 2020;26(16):4360–4368. doi:10.1158/1078-0432.CCR-20-0175.
  • Allam M, Hu T, Lee J, Aldrich J, Badve SS, Gokmen-Polar Y, Bhave M, Ramalingam SS, Schneider F, Coskun AF. Spatially variant immune infiltration scoring in human cancer tissues. NPJ Precis Oncol. 2022;6(1):60. doi:10.1038/s41698-022-00305-4.
  • Wu F, Fan J, He Y, Xiong A, Yu J, Li Y, Zhang Y, Zhao W, Zhou F, Li W, et al. Single-cell profiling of tumor heterogeneity and the microenvironment in advanced non-small cell lung cancer. Nat Commun. 2021;12(1):2540. doi:10.1038/s41467-021-22801-0.
  • Lewis SM, Asselin-Labat ML, Nguyen Q, Berthelet J, Tan X, Wimmer VC, Merino D, Rogers KL, Naik SH. Spatial omics and multiplexed imaging to explore cancer biology. Nat Methods. 2021;18(9):997–1012. doi:10.1038/s41592-021-01203-6.
  • Brunnstrom H, Johansson A, Westbom-Fremer S, Backman M, Djureinovic D, Patthey A, Isaksson-Mettävainio M, Gulyas M, Micke P. PD-L1 immunohistochemistry in clinical diagnostics of lung cancer: inter-pathologist variability is higher than assay variability. Mod Pathol. 2017;30(10):1411–1421. doi:10.1038/modpathol.2017.59.
  • La Fleur L, Falk-Sorqvist E, Smeds P, Berglund A, Sundstrom M, Mattsson JS, Brandén E, Koyi H, Isaksson J, Brunnström H, et al. Mutation patterns in a population-based non-small cell lung cancer cohort and prognostic impact of concomitant mutations in KRAS and TP53 or STK11. Lung Cancer. 2019;130:50–58. doi:10.1016/j.lungcan.2019.01.003.
  • Djureinovic D, Hallstrom BM, Horie M, Mattsson JSM, La Fleur L, Fagerberg L, Brunnström H, Lindskog C, Madjar K, Rahnenführer J, et al. Profiling cancer testis antigens in non–small-cell lung cancer. JCI Insight. 2016;1(10):e86837. doi:10.1172/jci.insight.86837.
  • Beechem JM. High-Plex spatially resolved RNA and protein detection using digital spatial profiling: a technology designed for immuno-oncology biomarker discovery and translational research. Methods Mol Biol. 2020;2055:563–583.
  • Backman M, La Fleur L, Kurppa P, Djureinovic D, Elfving H, Brunnstrom H, Mattsson JSM, Lindberg A, Pontén V, Eltahir M, et al. Infiltration of NK and plasma cells is associated with a distinct immune subset in non-small cell lung cancer. J Pathol. 2021;255(3):243–256. doi:10.1002/path.5772.
  • Rad HS, Rad HS, Shiravand Y, Radfar P, Arpon D, Warkiani ME, O’Byrne K, Kulasinghe A. The Pandora’s box of novel technologies that may revolutionize lung cancer. Lung Cancer. 2021;159:34–41. doi:10.1016/j.lungcan.2021.06.022.
  • Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21(3):309–322. doi:10.1016/j.ccr.2012.02.022.
  • Merritt CR, Ong GT, Church SE, Barker K, Danaher P, Geiss G, Hoang M, Jung J, Liang Y, McKay-Fleisch J, et al. Multiplex digital spatial profiling of proteins and RNA in fixed tissue. Nat Biotechnol. 2020;38(5):586–599. doi:10.1038/s41587-020-0472-9.
  • Zhang ML, Kem M, Mooradian MJ, Eliane JP, Huynh TG, Iafrate AJ, Gainor JF, Mino-Kenudson M. Differential expression of PD-L1 and IDO1 in association with the immune microenvironment in resected lung adenocarcinomas. Mod Pathol. 2019;32(4):511–523. doi:10.1038/s41379-018-0160-1.
  • Ladomersky E, Zhai L, Lenzen A, Lauing KL, Qian J, Scholtens DM, Gritsina G, Sun X, Liu Y, Yu F, et al. IDO1 inhibition synergizes with radiation and PD-1 blockade to durably increase survival against advanced glioblastoma. Clin Cancer Res. 2018;24(11):2559–2573. doi:10.1158/1078-0432.CCR-17-3573.
  • Rotondo R, Barisione G, Mastracci L, Grossi F, Orengo AM, Costa R, Truini M, Fabbi M, Ferrini S, Barbieri O. IL-8 induces exocytosis of arginase 1 by neutrophil polymorphonuclears in nonsmall cell lung cancer. Int J Cancer. 2009;125(4):887–893. doi:10.1002/ijc.24448.
  • Miret JJ, Kirschmeier P, Koyama S, Zhu M, Li YY, Naito Y, Wu M, Malladi VS, Huang W, Walker W, et al. Suppression Of myeloid cell arginase activity leads to therapeutic response in a NSCLC mouse model by activating anti-tumor immunity. J ImmunoTher Cancer. 2019;7(1):32. doi:10.1186/s40425-019-0504-5.
  • Kargl J, Busch SE, Yang GH, Kim KH, Hanke ML, Metz HE, Hubbard JJ, Lee SM, Madtes DK, McIntosh MW, et al. Neutrophils dominate the immune cell composition in non-small cell lung cancer. Nat Commun. 2017;8:14381. doi:10.1038/ncomms14381.
  • Shen M, Jiang K, Sui Y, Xu Z, Cui H, Wang Y, Zhang H, Xu Z, Xu W, Ding Q, et al. Characterization of CD66b and its relationship between immune checkpoints and their synergistic impact in the prognosis of surgically resected lung adenocarcinoma. Lung Cancer. 2021;160:84–91. doi:10.1016/j.lungcan.2021.08.012.
  • Flieswasser T, Van den Eynde A, Van Audenaerde J, De Waele J, Lardon F, Riether C, de Haard H, Smits E, Pauwels P, Jacobs J. The CD70-CD27 axis in oncology: the new kids on the block. J Exp Clin Cancer Res. 2022;41(1):12. doi:10.1186/s13046-021-02215-y.
  • Lutfi F, Wu L, Sunshine S, Cao X. Targeting the CD27-CD70 pathway to improve outcomes in both checkpoint immunotherapy and allogeneic hematopoietic cell transplantation. Front Immunol. 2021;12:715909. doi:10.3389/fimmu.2021.715909.
  • Starzer AM, Berghoff AS. New emerging targets in cancer immunotherapy: cD27 (TNFRSF7). ESMO Open. 2020;4(Suppl 3):e000629. doi:10.1136/esmoopen-2019-000629.
  • de Chaisemartin L, Goc J, Damotte D, Validire P, Magdeleinat P, Alifano M, de Chaisemartin L, Cremer I, Fridman W-H, Sautès-Fridman C, et al. Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res. 2011;71(20):6391–6399. doi:10.1158/0008-5472.CAN-11-0952.
  • 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.
  • Goc J, Germain C, Vo-Bourgais TK, Lupo A, Klein C, Knockaert S, de Chaisemartin L, Ouakrim H, Becht E, Alifano M, et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8+ T cells. Cancer Res. 2014;74(3):705–715. doi:10.1158/0008-5472.CAN-13-1342.
  • Vanhersecke L, Brunet M, Guegan JP, Rey C, Bougouin A, Cousin S, Le Moulec S, Besse B, Loriot Y, Larroquette M, et al. Mature tertiary lymphoid structures predict immune checkpoint inhibitor efficacy in solid tumors independently of PD-L1 expression. Nat Cancer. 2021;2(8):794–802. doi:10.1038/s43018-021-00232-6.
  • Kontos F, Michelakos T, Kurokawa T, Sadagopan A, Schwab JH, Ferrone CR, Ferrone S. B7-H3: an attractive target for antibody-based immunotherapy. Clin Cancer Res. 2021;27(5):1227–1235. doi:10.1158/1078-0432.CCR-20-2584.
  • Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS, et al. Mutational landscape determines sensitivity to PD-1 blockade in non–small cell lung cancer. Science. 2015;348(6230):124–128. doi:10.1126/science.aaa1348.