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The Role of the Immune Infiltrate in Distinct Cancer Types and Its Clinical Implications

Lymphocytic Infiltration in Colorectal Cancer
  • Jérôme GalonEmail author
  • Daniela Bruni
Chapter
Part of the Cancer Treatment and Research book series (CTAR, volume 180)

Abstract

Colorectal cancer (CRC) represents a major public health challenges, with one of the highest incidences worldwide. The two affected anatomical sites in CRC, i.e. the colon and the rectum, share important underlying features, but often differ in terms of therapeutic management. Current guidelines for CRC define its clinical stratification according to classical, tumor cell-based and pathological parameters. Novel ground-breaking findings in the recent years revealed the prominent role of the immune system in shaping CRC development. This chapter provides a detailed overview of the main genomic and immune features driving (or hampering) CRC progression, with a focus on the main immune cells and factors shaping its evolution. Furthermore, we discuss how tumor-infiltrating immunity could be leveraged both for therapeutic and stratification purposes.

References

  1. 1.
    Abbasi J (2018) Immunotherapy leads to complete regression in late-stage breast cancer. JAMA 320:127PubMedGoogle Scholar
  2. 2.
    Acikalin MF, Oner U, Topcu I, Yasar B, Kiper H, Colak E (2005) Tumour angiogenesis and mast cell density in the prognostic assessment of colorectal carcinomas. Dig Liver Dis 37:162–169CrossRefGoogle Scholar
  3. 3.
    Adua D, Di Fabio F, Ercolani G, Fiorentino M, Gruppioni E, Altimari A, Rojas Limpe FL, Normanno N, Pinna AD, Pinto C (2017) Heterogeneity in the colorectal primary tumor and the synchronous resected liver metastases prior to and after treatment with an anti-EGFR monoclonal antibody. Mol Clin Oncol 7:113–120CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Amicarella F, Muraro MG, Hirt C, Cremonesi E, Padovan E, Mele V, Governa V, Han J, Huber X, Droeser RA et al (2017) Dual role of tumour-infiltrating T helper 17 cells in human colorectal cancer. Gut 66:692–704CrossRefGoogle Scholar
  5. 5.
    Angelova M, Mlecnik B, Vasaturo A, Bindea G, Fredriksen T, Lafontaine L, Buttard B, Morgand E, Bruni D, Jouret-Mourin A et al (2018) Evolution of metastases in space and time under immune selection. Cell 175(751–765):e716Google Scholar
  6. 6.
    Bae JM, Kim JH, Kwak Y, Lee DW, Cha Y, Wen X, Lee TH, Cho NY, Jeong SY, Park KJ et al (2017) Distinct clinical outcomes of two CIMP-positive colorectal cancer subtypes based on a revised CIMP classification system. Br J Cancer 116:1012–1020CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Becht E, de Reynies A, Giraldo NA, Pilati C, Buttard B, Lacroix L, Selves J, Sautes-Fridman C, Laurent-Puig P, Fridman WH (2016) Immune and stromal classification of colorectal cancer is associated with molecular subtypes and relevant for precision immunotherapy. Clin Cancer Res 22:4057–4066CrossRefGoogle Scholar
  8. 8.
    Bindea G, Mlecnik B, Angell HK, Galon J (2014) The immune landscape of human tumors: Implications for cancer immunotherapy. Oncoimmunology 3:e27456CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, Obenauf AC, Angell H, Fredriksen T, Lafontaine L, Berger A et al (2013) Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 39:782–795CrossRefGoogle Scholar
  10. 10.
    Boland CR, Goel A (2010) Microsatellite instability in colorectal cancer. Gastroenterology 138(2073–2087):e2073CrossRefGoogle Scholar
  11. 11.
    Brahmer JR, Drake CG, Wollner I, Powderly JD, Picus J, Sharfman WH, Stankevich E, Pons A, Salay TM, McMiller TL et al (2010) Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol 28:3167–3175CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K et al (2012) Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366:2455–2465CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Burns MB, Montassier E, Abrahante J, Priya S, Niccum DE, Khoruts A, Starr TK, Knights D, Blekhman R (2018) Colorectal cancer mutational profiles correlate with defined microbial communities in the tumor microenvironment. PLoS Genet 14:e1007376CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Camus M, Tosolini M, Mlecnik B, Pages F, Kirilovsky A, Berger A, Costes A, Bindea G, Charoentong P, Bruneval P et al (2009) Coordination of intratumoral immune reaction and human colorectal cancer recurrence. Cancer Res 69:2685–2693CrossRefGoogle Scholar
  15. 15.
    Carbone DP, Gandara DR, Antonia SJ, Zielinski C, Paz-Ares L (2015) Non-small-cell lung cancer: role of the immune system and potential for immunotherapy. J Thorac Oncol 10:974–984CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Catakovic K, Klieser E, Neureiter D, Geisberger R (2017) T cell exhaustion: from pathophysiological basics to tumor immunotherapy. Cell Commun Signal 15:1CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Chaput N, Svrcek M, Auperin A, Locher C, Drusch F, Malka D, Taieb J, Goere D, Ducreux M, Boige V (2013) Tumour-infiltrating CD68+ and CD57+ cells predict patient outcome in stage II-III colorectal cancer. Br J Cancer 109:1013–1022CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Chen DS, Mellman I (2013) Oncology meets immunology: the cancer-immunity cycle. Immunity 39:1–10CrossRefGoogle Scholar
  19. 19.
    Chun E, Lavoie S, Michaud M, Gallini CA, Kim J, Soucy G, Odze R, Glickman JN, Garrett WS (2015) CCL2 promotes colorectal carcinogenesis by enhancing polymorphonuclear myeloid-derived suppressor cell population and function. Cell Rep 12:244–257CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Coca S, Perez-Piqueras J, Martinez D, Colmenarejo A, Saez MA, Vallejo C, Martos JA, Moreno M (1997) The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer 79:2320–2328CrossRefGoogle Scholar
  21. 21.
    Cohen SA, Yu M, Baker K, Redman M, Wu C, Heinzerling TJ, Wirtz RM, Charalambous E, Pentheroudakis G, Kotoula V et al (2017) The CpG island methylator phenotype is concordant between primary colorectal carcinoma and matched distant metastases. Clin Epigenetics 9:46CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Cremonesi E, Governa V, Garzon JFG, Mele V, Amicarella F, Muraro MG, Trella E, Galati-Fournier V, Oertli D, Daster SR et al (2018) Gut microbiota modulate T cell trafficking into human colorectal cancer. Gut 67:1984–1994CrossRefGoogle Scholar
  23. 23.
    de Vries NL, Swets M, Vahrmeijer AL, Hokland M, Kuppen PJ (2016) The immunogenicity of colorectal cancer in relation to tumor development and treatment. Int J Mol Sci 17Google Scholar
  24. 24.
    Ding C, Tang W, Fan X, Wu G (2018) Intestinal microbiota: a novel perspective in colorectal cancer biotherapeutics. Onco Targets Ther 11:4797–4810CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Dinu D, Dobre M, Panaitescu E, Birla R, Iosif C, Hoara P, Caragui A, Boeriu M, Constantinoiu S, Ardeleanu C (2014) Prognostic significance of KRAS gene mutations in colorectal cancer–preliminary study. J Med Life 7:581–587PubMedPubMedCentralGoogle Scholar
  26. 26.
    Edin S, Wikberg ML, Oldenborg PA, Palmqvist R (2013) Macrophages: good guys in colorectal cancer. Oncoimmunology 2:e23038CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Elkord E, Abd Al Samid M, Chaudhary B (2015) Helios, and not FoxP3, is the marker of activated Tregs expressing GARP/LAP. Oncotarget 6:20026–20036Google Scholar
  28. 28.
    Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61:759–767CrossRefGoogle Scholar
  29. 29.
    Fridman WH, Pages F, Sautes-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12:298–306CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Gabrilovich DI, Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9:162–174CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Gabrilovich DI, Ostrand-Rosenberg S, Bronte V (2012) Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 12:253–268CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Galdiero MR, Bianchi P, Grizzi F, Di Caro G, Basso G, Ponzetta A, Bonavita E, Barbagallo M, Tartari S, Polentarutti N et al (2016) Occurrence and significance of tumor-associated neutrophils in patients with colorectal cancer. Int J Cancer 139:446–456CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Galon J, Angell HK, Bedognetti D, Marincola FM (2013) The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 39:11–26CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Galon J, Bruni D (2019) Approaches to treat immune hot, altered and cold tumours with combination immunotherapies. Nat Rev Drug DiscovGoogle Scholar
  35. 35.
    Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P et al (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313:1960–1964CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Galon J, Fridman WH, Pages F (2007) The adaptive immunologic microenvironment in colorectal cancer: a novel perspective. Cancer Res 67:1883–1886CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Galon J, Mlecnik B, Bindea G, Angell HK, Berger A, Lagorce C, Lugli A, Zlobec I, Hartmann A, Bifulco C et al (2014) Towards the introduction of the ‘Immunoscore’ in the classification of malignant tumours. J Pathol 232:199–209CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD et al (2015) The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med 21:938–945CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Gerlinger M, Rowan AJ, Horswell S, Math M, Larkin J, Endesfelder D, Gronroos E, Martinez P, Matthews N, Stewart A et al (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366:883–892CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Germain C, Gnjatic S, Dieu-Nosjean MC (2015) Tertiary lymphoid structure-associated b cells are key players in anti-tumor immunity. Front Immunol 6:67CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Goc J, Fridman WH, Sautes-Fridman C, Dieu-Nosjean MC (2013) Characteristics of tertiary lymphoid structures in primary cancers. Oncoimmunology 2:e26836CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Gonzalez RS, Washington K, Shi C (2017) Current applications of molecular pathology in colorectal carcinoma. Appl Cancer Res 37:13CrossRefGoogle Scholar
  43. 43.
    Grizzi F, Bianchi P, Malesci A, Laghi L (2013) Prognostic value of innate and adaptive immunity in colorectal cancer. World J Gastroenterol 19:174–184CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Gryfe R, Kim H, Hsieh ET, Aronson MD, Holowaty EJ, Bull SB, Redston M, Gallinger S (2000) Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N Engl J Med 342:69–77CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Guinney J, Dienstmann R, Wang X, de Reynies A, Schlicker A, Soneson C, Marisa L, Roepman P, Nyamundanda G, Angelino P et al (2015) The consensus molecular subtypes of colorectal cancer. Nat Med 21:1350–1356CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al (2010) Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363:711–723CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Hsu YL, Chen YJ, Chang WA, Jian SF, Fan HL, Wang JY, Kuo PL (2018) Interaction between tumor-associated dendritic cells and colon cancer cells contributes to tumor progression via CXCL1. Int J Mol Sci 19Google Scholar
  50. 50.
    Ibrahim AE, Arends MJ, Silva AL, Wyllie AH, Greger L, Ito Y, Vowler SL, Huang TH, Tavare S, Murrell A et al (2011) Sequential DNA methylation changes are associated with DNMT3B overexpression in colorectal neoplastic progression. Gut 60:499–508CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Imai K, Matsuyama S, Miyake S, Suga K, Nakachi K (2000) Natural cytotoxic activity of peripheral-blood lymphocytes and cancer incidence: an 11-year follow-up study of a general population. Lancet 356:1795–1799CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Jobin G, Rodriguez-Suarez R, Betito K (2017) Association between natural killer cell activity and colorectal cancer in high-risk subjects undergoing colonoscopy. Gastroenterology 153:980–987CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Kalyan A, Kircher S, Shah H, Mulcahy M, Benson A (2018) Updates on immunotherapy for colorectal cancer. J Gastrointest Oncol 9:160–169CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Kanterman J, Sade-Feldman M, Biton M, Ish-Shalom E, Lasry A, Goldshtein A, Hubert A, Baniyash M (2014) Adverse immunoregulatory effects of 5FU and CPT11 chemotherapy on myeloid-derived suppressor cells and colorectal cancer outcomes. Cancer Res 74:6022–6035CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Karpinski P, Rossowska J, Sasiadek MM (2017) Immunological landscape of consensus clusters in colorectal cancer. Oncotarget 8:105299–105311CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Katlinski KV, Gui J, Katlinskaya YV, Ortiz A, Chakraborty R, Bhattacharya S, Carbone CJ, Beiting DP, Girondo MA, Peck AR et al (2017) Inactivation of interferon receptor promotes the establishment of immune privileged tumor microenvironment. Cancer Cell 31:194–207CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kawakami H, Zaanan A, Sinicrope FA (2015) Microsatellite instability testing and its role in the management of colorectal cancer. Curr Treat Options Oncol 16:30CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Kim TM, Jung SH, An CH, Lee SH, Baek IP, Kim MS, Park SW, Rhee JK, Lee SH, Chung YJ (2015) Subclonal genomic architectures of primary and metastatic colorectal cancer based on intratumoral genetic heterogeneity. Clin Cancer Res 21:4461–4472CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Koelzer VH, Canonica K, Dawson H, Sokol L, Karamitopoulou-Diamantis E, Lugli A, Zlobec I (2016) Phenotyping of tumor-associated macrophages in colorectal cancer: Impact on single cell invasion (tumor budding) and clinicopathological outcome. Oncoimmunology 5:e1106677CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Le DT, Durham JN, Smith KN, Wang H, Bartlett BR, Aulakh LK, Lu S, Kemberling H, Wilt C, Luber BS et al (2017) Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science 357:409–413CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D et al (2015) PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med 372:2509–2520CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lee JJ, Chu E (2018) Recent advances in the clinical development of immune checkpoint blockade therapy for mismatch repair proficient (pMMR)/non-MSI-H metastatic colorectal cancer. Clin Colorectal Cancer 17:258–273CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Legitimo A, Consolini R, Failli A, Orsini G, Spisni R (2014) Dendritic cell defects in the colorectal cancer. Hum Vaccin Immunother 10:3224–3235CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Ling A, Lundberg IV, Eklof V, Wikberg ML, Oberg A, Edin S, Palmqvist R (2016) The infiltration, and prognostic importance, of Th1 lymphocytes vary in molecular subgroups of colorectal cancer. J Pathol Clin Res 2:21–31CrossRefGoogle Scholar
  65. 65.
    Lipson EJ (2013) Re-orienting the immune system: Durable tumor regression and successful re-induction therapy using anti-PD1 antibodies. Oncoimmunology 2:e23661CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Malfettone A, Silvestris N, Saponaro C, Ranieri G, Russo A, Caruso S, Popescu O, Simone G, Paradiso A, Mangia A (2013) High density of tryptase-positive mast cells in human colorectal cancer: a poor prognostic factor related to protease-activated receptor 2 expression. J Cell Mol Med 17:1025–1037CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Malietzis G, Lee GH, Jenkins JT, Bernardo D, Moorghen M, Knight SC, Al-Hassi HO (2015) Prognostic value of the tumour-infiltrating dendritic cells in colorectal cancer: a systematic review. Cell Commun Adhes 22:9–14CrossRefGoogle Scholar
  68. 68.
    Mao Y, Feng Q, Zheng P, Yang L, Zhu D, Chang W, Ji M, He G, Xu J (2018) Low tumor infiltrating mast cell density confers prognostic benefit and reflects immunoactivation in colorectal cancer. Int J Cancer 143:2271–2280CrossRefGoogle Scholar
  69. 69.
    McGranahan N, Swanton C (2017) Cancer evolution constrained by the immune microenvironment. Cell 170:825–827CrossRefGoogle Scholar
  70. 70.
    Mehdawi L, Osman J, Topi G, Sjolander A (2016) High tumor mast cell density is associated with longer survival of colon cancer patients. Acta Oncol 55:1434–1442CrossRefGoogle Scholar
  71. 71.
    Melero I, Rouzaut A, Motz GT, Coukos G (2014) T-cell and NK-cell infiltration into solid tumors: a key limiting factor for efficacious cancer immunotherapy. Cancer Discov 4:522–526CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Menon AG, Janssen-van Rhijn CM, Morreau H, Putter H, Tollenaar RA, van de Velde CJ, Fleuren GJ, Kuppen PJ (2004) Immune system and prognosis in colorectal cancer: a detailed immunohistochemical analysis. Lab Invest 84:493–501CrossRefGoogle Scholar
  73. 73.
    Mlecnik B, Bindea G, Angell HK, Maby P, Angelova M, Tougeron D, Church SE, Lafontaine L, Fischer M, Fredriksen T et al (2016) Integrative analyses of colorectal cancer show Immunoscore is a stronger predictor of patient survival than microsatellite instability. Immunity 44:698–711CrossRefGoogle Scholar
  74. 74.
    Mlecnik B, Bindea G, Angell HK, Sasso MS, Obenauf AC, Fredriksen T, Lafontaine L, Bilocq AM, Kirilovsky A, Tosolini M et al (2014) Functional network pipeline reveals genetic determinants associated with in situ lymphocyte proliferation and survival of cancer patients. Sci Transl Med 6:228ra237Google Scholar
  75. 75.
    Mlecnik B, Bindea G, Kirilovsky A, Angell HK, Obenauf AC, Tosolini M, Church SE, Maby P, Vasaturo A, Angelova M et al (2016b) The tumor microenvironment and Immunoscore are critical determinants of dissemination to distant metastasis. Sci Transl Med 8:327ra326Google Scholar
  76. 76.
    Mlecnik B, Bindea G, Pages F, Galon J (2011) Tumor immunosurveillance in human cancers. Cancer Metastasis Rev 30:5–12CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, Bruneval P, Trajanoski Z, Fridman WH, Pages F et al (2011) Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 29:610–618CrossRefGoogle Scholar
  78. 78.
    Mlecnik B, Van den Eynde M, Bindea G, Church SE, Vasaturo A, Fredriksen T, Lafontaine L, Haicheur N, Marliot F, Debetancourt D et al (2018) Comprehensive intrametastatic immune quantification and major impact of Immunoscore on survival. J Natl Cancer Inst 110Google Scholar
  79. 79.
    Network TCGA (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487:330–337CrossRefGoogle Scholar
  80. 80.
    Niccolai E, Ricci F, Russo E, Nannini G, Emmi G, Taddei A, Ringressi MN, Melli F, Miloeva M, Cianchi F et al (2017) the different functional distribution of “Not Effector” T cells (Treg/Tnull) in colorectal cancer. Front Immunol 8:1900CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Nieuwenhuis MH, Vasen HF (2007) Correlations between mutation site in APC and phenotype of familial adenomatous polyposis (FAP): a review of the literature. Crit Rev Oncol Hematol 61:153–161CrossRefGoogle Scholar
  82. 82.
    Olivier M, Hollstein M, Hainaut P (2010) TP53 mutations in human cancers: origins, consequences, and clinical use. Cold Spring Harb Perspect Biol 2:a001008CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Ostroumov D, Fekete-Drimusz N, Saborowski M, Kuhnel F, Woller N (2018) CD4 and CD8 T lymphocyte interplay in controlling tumor growth. Cell Mol Life Sci 75:689–713CrossRefGoogle Scholar
  84. 84.
    Ottaiano A, Napolitano M, Capozzi M, Tafuto S, Avallone A, Scala S (2017) Natural killer cells activity in a metastatic colorectal cancer patient with complete and long lasting response to therapy. World J Clin Cases 5:390–396CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D et al (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353:2654–2666CrossRefGoogle Scholar
  86. 86.
    Pages F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, Bindea G, Lagorce C, Wind P, Marliot F, Bruneval P et al (2009) In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 27:5944–5951CrossRefGoogle Scholar
  87. 87.
    Pages F, Mlecnik B, Marliot F, Bindea G, Ou FS, Bifulco C, Lugli A, Zlobec I, Rau TT, Berger MD et al (2018a) International validation of the consensus Immunoscore for the classification of colon cancer: a prognostic and accuracy study. LancetGoogle Scholar
  88. 88.
    Pages F, Mlecnik B, Marliot F, Bindea G, Ou FS, Bifulco C, Lugli A, Zlobec I, Rau TT, Berger MD et al (2018) International validation of the consensus Immunoscore for the classification of colon cancer: a prognostic and accuracy study. Lancet 391:2128–2139CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Posch F, Silina K, Leibl S, Mundlein A, Moch H, Siebenhuner A, Samaras P, Riedl J, Stotz M, Szkandera J et al (2018) Maturation of tertiary lymphoid structures and recurrence of stage II and III colorectal cancer. Oncoimmunology 7:e1378844CrossRefGoogle Scholar
  90. 90.
    Poulogiannis G, Ichimura K, Hamoudi RA, Luo F, Leung SY, Yuen ST, Harrison DJ, Wyllie AH, Arends MJ (2010) Prognostic relevance of DNA copy number changes in colorectal cancer. J Pathol 220:338–347CrossRefGoogle Scholar
  91. 91.
    Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR, Thibodeau SN, Vogelstein B, Kinzler KW (1992) APC mutations occur early during colorectal tumorigenesis. Nature 359:235–237CrossRefGoogle Scholar
  92. 92.
    Puppa G, Sonzogni A, Colombari R, Pelosi G (2010) TNM staging system of colorectal carcinoma: a critical appraisal of challenging issues. Arch Pathol Lab Med 134:837–852PubMedGoogle Scholar
  93. 93.
    Resch A, Langner C (2013) Lymph node staging in colorectal cancer: old controversies and recent advances. World J Gastroenterol 19:8515–8526CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Saito T, Nishikawa H, Wada H, Nagano Y, Sugiyama D, Atarashi K, Maeda Y, Hamaguchi M, Ohkura N, Sato E et al (2016) Two FOXP3(+)CD4(+) T cell subpopulations distinctly control the prognosis of colorectal cancers. Nat Med 22:679–684CrossRefGoogle Scholar
  95. 95.
    Sandel MH, Dadabayev AR, Menon AG, Morreau H, Melief CJ, Offringa R, van der Burg SH, Janssen-van Rhijn CM, Ensink NG, Tollenaar RA et al (2005) Prognostic value of tumor-infiltrating dendritic cells in colorectal cancer: role of maturation status and intratumoral localization. Clin Cancer Res 11:2576–2582CrossRefGoogle Scholar
  96. 96.
    Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331:1565–1570CrossRefGoogle Scholar
  97. 97.
    Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD (2001) IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410:1107–1111CrossRefGoogle Scholar
  98. 98.
    Shitara K, Nishikawa H (2018) Regulatory T cells: a potential target in cancer immunotherapy. Ann N Y Acad Sci 1417:104–115CrossRefGoogle Scholar
  99. 99.
    Sica A, Mantovani A (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787–795CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Smyrk TC, Watson P, Kaul K, Lynch HT (2001) Tumor-infiltrating lymphocytes are a marker for microsatellite instability in colorectal carcinoma. Cancer 91:2417–2422CrossRefGoogle Scholar
  101. 101.
    Sottoriva A, Kang H, Ma Z, Graham TA, Salomon MP, Zhao J, Marjoram P, Siegmund K, Press MF, Shibata D et al (2015) A Big Bang model of human colorectal tumor growth. Nat Genet 47:209–216CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Stevanovic S, Pasetto A, Helman SR, Gartner JJ, Prickett TD, Howie B, Robins HS, Robbins PF, Klebanoff CA, Rosenberg SA et al (2017) Landscape of immunogenic tumor antigens in successful immunotherapy of virally induced epithelial cancer. Science 356:200–205CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Strasser K, Birnleitner H, Beer A, Pils D, Gerner MC, Schmetterer KG, Bachleitner-Hofmann T, Stift A, Bergmann M, Oehler R (2018) Immunological differences between colorectal cancer and normal mucosa uncover a prognostically relevant immune cell profile. OncoImmunology 1–13Google Scholar
  104. 104.
    Sundstrom P, Stenstad H, Langenes V, Ahlmanner F, Theander L, Ndah TG, Fredin K, Borjesson L, Gustavsson B, Bastid J et al (2016) Regulatory T cells from colon cancer patients inhibit effector T-cell migration through an adenosine-dependent mechanism. Cancer Immunol Res 4:183–193CrossRefGoogle Scholar
  105. 105.
    Tallerico R, Todaro M, Di Franco S, Maccalli C, Garofalo C, Sottile R, Palmieri C, Tirinato L, Pangigadde PN, La Rocca R et al (2013) Human NK cells selective targeting of colon cancer-initiating cells: a role for natural cytotoxicity receptors and MHC class I molecules. J Immunol 190:2381–2390CrossRefGoogle Scholar
  106. 106.
    Tamas K, Walenkamp AM, de Vries EG, van Vugt MA, Beets-Tan RG, van Etten B, de Groot DJ, Hospers GA (2015) Rectal and colon cancer: not just a different anatomic site. Cancer Treat Rev 41:671–679CrossRefGoogle Scholar
  107. 107.
    Taylor ES, McCall JL, Girardin A, Munro FM, Black MA, Kemp RA (2016) Functional impairment of infiltrating T cells in human colorectal cancer. Oncoimmunology 5:e1234573CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Thirlwell C, Will OC, Domingo E, Graham TA, McDonald SA, Oukrif D, Jeffrey R, Gorman M, Rodriguez-Justo M, Chin-Aleong J et al (2010) Clonality assessment and clonal ordering of individual neoplastic crypts shows polyclonality of colorectal adenomas. Gastroenterology 138:1441–1454, 1454 e1441–1447Google Scholar
  109. 109.
    Thommen DS, Schumacher TN (2018) T cell dysfunction in cancer. Cancer Cell 33:547–562CrossRefGoogle Scholar
  110. 110.
    Timmermann B, Kerick M, Roehr C, Fischer A, Isau M, Boerno ST, Wunderlich A, Barmeyer C, Seemann P, Koenig J et al (2010) Somatic mutation profiles of MSI and MSS colorectal cancer identified by whole exome next generation sequencing and bioinformatics analysis. PLoS ONE 5:e15661CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al (2012) Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366:2443–2454CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman WH, Pages F et al (2011) Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, Treg, th17) in patients with colorectal cancer. Cancer Res 71:1263–1271CrossRefGoogle Scholar
  113. 113.
    Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP (1999) CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci USA 96:8681–8686CrossRefGoogle Scholar
  114. 114.
    Tran Janco JM, Lamichhane P, Karyampudi L, Knutson KL (2015) Tumor-infiltrating dendritic cells in cancer pathogenesis. J Immunol 194:2985–2991CrossRefGoogle Scholar
  115. 115.
    Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K et al (2013) Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 369:122–133CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Zeinalian M, Hashemzadeh-Chaleshtori M, Salehi R, Emami MH (2018) Clinical aspects of microsatellite instability testing in colorectal cancer. Adv Biomed Res 7:28CrossRefPubMedPubMedCentralGoogle Scholar
  117. 117.
    Zhang L, Zhao Y, Dai Y, Cheng JN, Gong Z, Feng Y, Sun C, Jia Q, Zhu B (2018) Immune landscape of colorectal cancer tumor microenvironment from different primary tumor location. Front Immunol 9:1578CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.INSERM Laboratory of Integrative Cancer ImmunologyEquipe Labellisée Ligue Contre le Cancer, Sorbonne Université, Sorbonne Paris Cité, Université Paris Descartes, Université Paris Diderot, Centre de Recherche des CordeliersParisFrance

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