Metastatic spread in patients with non-small cell lung cancer is associated with a reduced density of tumor-infiltrating T cells

Cancer Immunology, Immunotherapy

Volumn 65, Issue 1, 2016, Pages 1-11

  Müller, Philipp ^a   Rothschild, Sacha I ^a,b   Arnold, Walter ^c   Hirschmann, Petra ^d   Horvath, Lukas ^a   Bubendorf, Lukas ^d   Savic, Spasenija ^d   Zippelius, Alfred ^a,b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

Anti tumor immunity; Immune cells; Metastasis; Non small cell lung cancer; Primary tumor

Indexed keywords

FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LUNG TUMOR; MALE; METASTASIS; NON SMALL CELL LUNG CANCER; PATHOLOGY; PROGNOSIS; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT;

CARCINOMA, NON-SMALL-CELL LUNG; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LUNG NEOPLASMS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; NEOPLASM METASTASIS; PROGNOSIS; TUMOR MICROENVIRONMENT;

EID: 84953369260     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-015-1768-3     Document Type: Article

References (58)

1. Khong HT, Restifo NP (2002) Natural selection of tumor variants in the generation of “tumor escape” phenotypes. Nat Immunol 3:999–1005. doi:10.1038/ni1102-999
2. Lin A, Schildknecht A, Nguyen LT, Ohashi PS (2010) Dendritic cells integrate signals from the tumor microenvironment to modulate immunity and tumor growth. Immunol Lett 127:77–84. doi:10.1016/j.imlet.2009.09.003
3. Chen JJ, Lin YC, Yao PL, Yuan A, Chen HY, Shun CT, Tsai MF, Chen CH, Yang PC (2005) Tumor-associated macrophages: the double-edged sword in cancer progression. J Clin Oncol 23:953–964. doi:10.1200/JCO.2005.12.172
4. Loose D, Van de Wiele C (2009) The immune system and cancer. Cancer Biother Radiopharm 24:369–376. doi:10.1089/cbr.2008.0593
5. + T lymphocytes. Clin Exp Immunol 150:523–530. doi:10.1111/j.1365-2249.2007.03521.x
6. Theoharides TC, Conti P (2004) Mast cells: the Jekyll and Hyde of tumor growth. Trends Immunol 25:235–241. doi:10.1016/j.it.2004.02.013
7. Gavert N, Ben-Ze’ev A (2008) Epithelial-mesenchymal transition and the invasive potential of tumors. Trends Mol Med 14:199–209. doi:10.1016/j.molmed.2008.03.004
8. Solinas G, Germano G, Mantovani A, Allavena P (2009) Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 86:1065–1073. doi:10.1189/jlb.0609385
9. Galon J, Costes A, Sanchez-Cabo F et al (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313:1960–1964. doi:10.1126/science.1129139
10. Pagès F, Berger A, Camus M et al (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353:2654–2666. doi:10.1056/NEJMoa051424
11. Bindea G, Mlecnik B, Tosolini M et al (2013) Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 39:782–795. doi:10.1016/j.immuni.2013.10.003
12. Al-Shibli KI, Donnem T, Al-Saad S, Persson M, Bremnes RM, Busund LT (2008) Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 14:5220–5227. doi:10.1158/1078-0432.CCR-08-0133
13. Dieu-Nosjean MC, Antoine M, Danel C et al (2008) Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 26:4410–4417. doi:10.1200/JCO.2007.15.0284
14. + T cells is a favourable prognostic factor in non-small-cell lung carcinoma. Br J Cancer 94:275–280. doi:10.1038/sj.bjc.6602934
15. + T cells infiltrated in NSCLC tissues is associated with a favorable prognosis. Appl Immunohistochem Mol Morphol 18:24–28. doi:10.1097/PAI.0b013e3181b6a741
16. Takanami I, Takeuchi K, Giga M (2001) The prognostic value of natural killer cell infiltration in resected pulmonary adenocarcinoma. J Thorac Cardiovasc Surg 121:1058–1063. doi:10.1067/mtc.2001.113026
17. Villegas FR, Coca S, Villarrubia VG, Jiménez R, Chillón MJ, Jareño J, Zuil M, Callol L (2002) Prognostic significance of tumor infiltrating natural killer cells subset CD57 in patients with squamous cell lung cancer. Lung Cancer 35:23–28. doi:10.1016/S0169-5002(01)00292-6
18. Hasegawa T, Suzuki H, Yamaura T et al (2014) Prognostic value of peripheral and local forkhead box P3 regulatory T cells in patients with non-small-cell lung cancer. Mol Clin Oncol 2:685–694. doi:10.3892/mco.2014.299
19. Hodi FS, O’Day SJ, McDermott DF et al (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363:711–723. doi:10.1056/NEJMoa1003466
20. Robert C, Thomas L, Bondarenko I et al (2011) Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364:2517–2526. doi:10.1056/NEJMoa1104621
21. Robert C, Long GV, Brady B et al (2014) Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med 372:320–330. doi:10.1056/NEJMoa1412082
22. Brahmer J, Reckamp KL, Baas P et al (2015) Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med 373:123–135. doi:10.1056/NEJMoa1504627
23. Topalian SL, Hodi FS, Brahmer JR et al (2012) Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366:2443–2454. doi:10.1056/NEJMoa1200690
24. Brahmer JR, Tykodi SS, Chow LQ et al (2012) Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366:2455–2465. doi:10.1056/NEJMoa1200694
25. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63:11–30. doi:10.3322/caac.21166
26. Fidler IJ, Hart IR (1982) Biological diversity in metastatic neoplasms: origins and implications. Science 217:998–1003. doi:10.1126/science.7112116
27. Talmadge JE, Wolman SR, Fidler IJ (1982) Evidence for the clonal origin of spontaneous metastases. Science 217:361–363. doi:10.1126/science.6953592
28. Dunn GP, Old LJ, Schreiber RD (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21:137–148. doi:10.1016/j.immuni.2004.07.017
29. Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331:1565–1570. doi:10.1126/science.1203486
30. Smyth MJ, Dunn GP, Schreiber RD (2006) Cancer immunosurveillance and immunoediting: the roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol 90:1–50. doi:10.1016/S0065-2776(06)90001-7
31. Obeid M, Tesniere A, Ghiringhelli F et al (2007) Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13:54–61. doi:10.1038/nm1523
32. Apetoh L, Ghiringhelli F, Tesniere A et al (2007) Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13:1050–1059. doi:10.1038/nm1622
33. Ghiringhelli F, Apetoh L, Tesniere A et al (2009) Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med 15:1170–1178. doi:10.1038/nm.2028
34. Müller P, Martin K, Theurich S et al (2014) Microtubule-depolymerizing agents used in antibody-drug conjugates induce antitumor immunity by stimulation of dendritic cells. Cancer Immunol Res 2:741–755. doi:10.1158/2326-6066.CIR-13-0198
35. Martin K, Müller P, Schreiner J, Prince SS, Lardinois D, Heinzelmann-Schwarz VA, Thommen DS, Zippelius A (2014) The microtubule-depolymerizing agent ansamitocin P3 programs dendritic cells toward enhanced anti-tumor immunity. Cancer Immunol Immunother 63:925–938. doi:10.1007/s00262-014-1565-4
36. Zhang W, Guo N, Yu C, Wang H, Zhang Y, Xia H, Yu J, Lu J (2012) Differential expression of ERCC-1 in the primary tumors and metastatic lymph nodes of patients with non-small cell lung cancer adenocarcinoma. Tumour Biol 33:2209–2216. doi:10.1007/s13277-012-0482-4
37. Shimizu K, Yukawa T, Hirami Y, Okita R, Saisho S, Maeda A, Yasuda K, Nakata M (2013) Heterogeneity of the EGFR mutation status between the primary tumor and metastatic lymph node and the sensitivity to EGFR tyrosine kinase inhibitor in non-small cell lung cancer. Target Oncol 8:237–242. doi:10.1007/s11523-012-0241-x
38. Tanoue LT, Detterbeck FC (2009) New TNM classification for non-small-cell lung cancer. Expert Rev Anticancer Ther 9:413–423. doi:10.1586/era.09.11
39. Ries CH, Cannarile MA, Hoves S et al (2014) Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 25:846–859. doi:10.1016/j.ccr.2014.05.016
40. Ngiow SF, von Scheidt B, Akiba H, Yagita H, Teng MW, Smyth MJ (2011) Anti-TIM3 antibody promotes T cell IFN-γ-mediated antitumor immunity and suppresses established tumors. Cancer Res 71:3540–3551. doi:10.1158/0008-5472.CAN-11-0096
41. Quatromoni JG, Eruslanov E (2012) Tumor-associated macrophages: function, phenotype, and link to prognosis in human lung cancer. Am J Transl Res 4:376–389
42. Franklin RA, Liao W, Sarkar A, Kim MV, Bivona MR, Liu K, Pamer EG, Li MO (2014) The cellular and molecular origin of tumor-associated macrophages. Science 344:921–925. doi:10.1126/science.1252510
43. Zitvogel L, Kepp O, Kroemer G (2011) Immune parameters affecting the efficacy of chemotherapeutic regimens. Nat Rev Clin Oncol 8:151–160. doi:10.1038/nrclinonc.2010.223
44. Pagès F, Galon J, Dieu-Nosjean MC, Tartour E, Sautès-Fridman C, Fridman WH (2010) Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene 29:1093–1102. doi:10.1038/onc.2009.416
45. Zitvogel L, Kepp O, Aymeric L, Ma Y, Locher C, Delahaye NF, André F, Kroemer G (2010) Integration of host-related signatures with cancer cell-derived predictors for the optimal management of anticancer chemotherapy. Cancer Res 70:9538–9543. doi:10.1158/0008-5472.CAN-10-1003
46. Germain C, Gnjatic S, Tamzalit F et al (2014) 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 189:832–844. doi:10.1164/rccm.201309-1611OC
47. Halama N, Michel S, Kloor M et al (2011) Localization and density of immune cells in the invasive margin of human colorectal cancer liver metastases are prognostic for response to chemotherapy. Cancer Res 71:5670–5677. doi:10.1158/0008-5472.CAN-11-0268
48. Ladoire S, Mignot G, Dabakuyo S et al (2011) In situ immune response after neoadjuvant chemotherapy for breast cancer predicts survival. J Pathol 224:389–400. doi:10.1002/path.2866
49. Galon J, Fridman WH, Pagès F (2007) The adaptive immunologic microenvironment in colorectal cancer: a novel perspective. Cancer Res 67:1883–1886. doi:10.1158/0008-5472.CAN-06-4806
50. Angell H, Galon J (2013) From the immune contexture to the immunoscore: the role of prognostic and predictive immune markers in cancer. Curr Opin Immunol 25:261–267. doi:10.1016/j.coi.2013.03.004
51. Restifo NP (2013) A “big data” view of the tumor “immunome”. Immunity 39:631–632. doi:10.1016/j.immuni.2013.10.002
52. Beyer I, van Rensburg R, Lieber A (2013) Overcoming physical barriers in cancer therapy. Tissue Barriers 1:e23647. doi:10.4161/tisb.23647
53. Wang A, Wang HY, Liu Y, Zhao MC, Zhang HJ, Lu ZY, Fang YC, Chen XF, Liu GT (2015) The prognostic value of PD-L1 expression for non-small cell lung cancer patients: a meta-analysis. Eur J Surg Oncol 41:450–456. doi:10.1016/j.ejso.2015.01.020
54. Tumeh PC, Harview CL, Yearley JH et al (2014) PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515:568–571. doi:10.1038/nature13954
55. + T-cell recruitment. Cancer Res 69:3077–3085. doi:10.1158/0008-5472.CAN-08-2281
56. Bald T, Landsberg J, Lopez-Ramos D et al (2014) Immune cell-poor melanomas benefit from PD-1 blockade after targeted type I IFN activation. Cancer Discov 4:674–687. doi:10.1158/2159-8290.CD-13-0458
57. Woo EY, Yeh H, Chu CS, Schlienger K, Carroll RG, Riley JL, Kaiser LR, June CH (2002) Cutting edge: regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J Immunol 168:4272–4276. doi:10.4049/jimmunol.168.9.4272
58. Mantovani A, Germano G, Marchesi F, Locatelli M, Biswas SK (2011) Cancer-promoting tumor-associated macrophages: new vistas and open questions. Eur J Immunol 41:2522–2525. doi:10.1002/eji.201141894