Immune classification of colorectal cancer patients: Impressive but how complete?

Expert Opinion on Biological Therapy

Volumn 13, Issue 4, 2013, Pages 517-526

  Baxevanis, Constantin N ^a   Papamichail, Michael ^a   Perez, Sonia A ^a  

^a SAINT SAVVAS HOSPITAL   (Greece)

Author keywords

Colorectal cancer; Immune classification; Regulatory T cells; Th17 cells; TNM classification; Tumor infiltrating lymphocytes; Tumor microenvironment

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FLUOROURACIL; INTERLEUKIN 10; INTERLEUKIN 17; IPILIMUMAB; RETINOIC ACID RECEPTOR GAMMA; STAT3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR ANTIGEN;

ADAPTIVE IMMUNITY; CANCER ADJUVANT THERAPY; CANCER CLASSIFICATION; CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER SPECIFIC SURVIVAL; CANCER STAGING; CD8+ T LYMPHOCYTE; CLASSIFICATION; COLORECTAL CANCER; CYTOTOXIC T LYMPHOCYTE; DISEASE FREE SURVIVAL; HISTOPATHOLOGY; HUMAN; IMMUNE CLASSIFICATION; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; IMMUNOSURVEILLANCE; INFLAMMATORY CELL; INFLAMMATORY INFILTRATE; INNATE IMMUNITY; LYMPHOCYTIC INFILTRATION; MELANOMA; METASTASIS; MICROSATELLITE INSTABILITY; NONHUMAN; OVERALL SURVIVAL; PHENOTYPE; PLASTICITY; PREDICTIVE VALUE; RADIOIMMUNOTHERAPY; REGULATORY T LYMPHOCYTE; REVIEW; TH17 CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR VOLUME; ANIMAL; COLORECTAL NEOPLASMS; IMMUNOLOGY; PROGNOSIS; STANDARDS; T LYMPHOCYTE;

ANIMALS; COLORECTAL NEOPLASMS; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASM STAGING; PROGNOSIS; T-LYMPHOCYTES;

EID: 84879581523     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.2013.751971     Document Type: Review

References (94)

1. Rahir G, Moser M. Tumor microenvironment and lymphocyte infiltration. Cancer Immunol Immunother 2012;61(6):751-9
2. Galon J, Costes A, Sanchez-Cabo F, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313(5795):1960-4
3. Zhang L, Conejo-Garcia JR, Katsaros D, et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 2003;348(3):203-13
4. Denkert C, Loibl S, Noske A, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2010;28(1):105-13
5. Hornychova H, Melichar B, Tomsova M, et al. Tumor-infiltrating lymphocytes predict response to neoadjuvant chemotherapy in patients with breast carcinoma. Cancer Invest 2008;26(10):1024-31
6. Al-Shibli KI, Donnem T, Al-Saad S, et al. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 2008;14(16):5220-7
7. Marrogi AJ, Munshi A, Merogi AJ, et al. Study of tumor infiltrating lymphocytes and transforming growth factor-beta as prognostic factors in breast carcinoma. Int J Cancer 1997;74(5):492-501
8. Kusmartsev S, Gabrilovich DI. Role of immature myeloid cells in mechanisms of immune evasion in cancer. Cancer Immunol Immunother 2006;55(3):237-45
9. Whiteside TL. Disarming suppressor cells to improve immunotherapy. Cancer Immunol Immunother 2012;61(2):283-8
10. Wilke CM, Kryczek I, Wei S, et al. Th17 cells in cancer: help or hindrance? Carcinogenesis 2011;32(5):643-9
11. Strauss L, Bergmann C, Szczepanski M, et al. A unique subset of CD4 +CD25highFoxp3+ T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin Cancer Res 2007;13(15 Pt 1):4345-54
12. Zou W, Restifo NP. T(H)17 cells in tumour immunity and immunotherapy. Nat Rev Immunol 2010;10(4):248-56
13. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008;133(5):775-87
14. Sato T, Terai M, Tamura Y, et al. Interleukin 10 in the tumor microenvironment: a target for anticancer immunotherapy. Immunol Res 2011;51(2-3):170-82
15. Quezada SA, Peggs KS, Curran MA, Allison JP. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest 2006;116(7):1935-45
16. Gritzapis AD, Voutsas IF, Lekka E, et al. Peptide vaccination breaks tolerance to HER-2/neu by generating vaccine-specific FasL(+) CD4(+) T cells: first evidence for intratumor apoptotic regulatory T cells. Cancer Res 2010;70(7):2686-96
17. Mahalingam J, Lin YC, Chiang JM, et al. LAP+CD4+ T Cells Are Suppressors Accumulated in the Tumor Sites and Associated with the Progression of Colorectal Cancer. Clin Cancer Res 2012;18(19):5224-33
18. Emmerich J, Mumm JB, Chan IH, et al. IL-10 directly activates and expands tumor-resident CD8(+) T cells without de novo infiltration from secondary lymphoid organs. Cancer Res 2012;72(14):3570-81
19. Kryczek I, Wei S, Szeliga W, et al. Endogenous IL-17 contributes to reduced tumor growth and metastasis. Blood 2009;114(2):357-9
20. Nam JS, Terabe M, Kang MJ, et al. Transforming growth factor beta subverts the immune system into directly promoting tumor growth through interleukin-17. Cancer Res 2008;68(10):3915-23
21. Higgins CA, Hatton WJ, McKerr G, et al. Macrophages and apoptotic cells in human colorectal tumours. Biologicals 1996;24(4):329-32
22. Hung K, Hayashi R, Lafond-Walker A, et al. The central role of CD4(+) T cells in the antitumor immune response. J Exp Med 1998;188(12):2357-68
23. Klintrup K, Makinen JM, Kauppila S, et al. Inflammation and prognosis in colorectal cancer. Eur J Cancer 2005;41(17):2645-54
24. George S, Primrose J, Talbot R, et al. Will Rogers revisited: prospective observational study of survival of 3592 patients with colorectal cancer according to number of nodes examined by pathologists. Br J Cancer 2006;95(7):841-7
25. Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA. Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 2007;99(6):433-41
26. Popat S, Hubner R, Houlston RS. Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol 2005;23(3):609-18
27. Ogino S, Nosho K, Kirkner GJ, et al. CpG island methylator phenotype, microsatellite instability, BRAF mutation and clinical outcome in colon cancer. Gut 2009;58(1):90-6
28. Ogino S, Nosho K, Irahara N, et al. Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res 2009;15(20):6412-20
29. Roxburgh CS, Salmond JM, Horgan PG, et al. Comparison of the prognostic value of inflammation-based pathologic and biochemical criteria in patients undergoing potentially curative resection for colorectal cancer. Ann Surg 2009;249(5):788-93
30. Huh JW, Lee JH, Kim HR. Prognostic significance of tumor-infiltrating lymphocytes for patients with colorectal cancer. Arch Surg 2012;147(4):366-72
31. Guidoboni M, Gafa R, Viel A, et al. Microsatellite instability and high content of activated cytotoxic lymphocytes identify colon cancer patients with a favorable prognosis. Am J Pathol 2001;159(1):297-304
32. Zlobec I, Terracciano LM, Lugli A. Local recurrence in mismatch repair-proficient colon cancer predicted by an infiltrative tumor border and lack of CD8+ tumor-infiltrating lymphocytes. Clin Cancer Res 2008;14(12):3792-7
33. Prall F, Duhrkop T, Weirich V, et al. Prognostic role of CD8+ tumor-infiltrating lymphocytes in stage III colorectal cancer with and without microsatellite instability. Hum Pathol 2004;35(7):808-16
34. Morris M, Platell C, Iacopetta B. Tumor-infiltrating lymphocytes and perforation in colon cancer predict positive response to 5-fluorouracil chemotherapy. Clin Cancer Res 2008;14(5):1413-17
35. Pages F, Berger A, Camus M, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005;353(25):2654-66
36. Salama P, Phillips M, Grieu F, et al. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 2009;27(2):186-92
37. Tosolini M, Kirilovsky A, Mlecnik B, et al. Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, Th2, Treg, Th17) in patients with colorectal cancer. Cancer Res 2011;71(4):1263-71
38. Levy EM, Roberti MP, Mordoh J. Natural killer cells in human cancer: from biological functions to clinical applications. J Biomed Biotechnol 2011;2011:676198
39. Gulubova M, Manolova I, Kyurkchiev D, et al. Decrease in intrahepatic CD56+ lymphocytes in gastric and colorectal cancer patients with liver metastases. Apmis 2009;117(12):870-9
40. Halama N, Braun M, Kahlert C, et al. Natural killer cells are scarce in colorectal carcinoma tissue despite high levels of chemokines and cytokines. Clin Cancer Res 2011;17(4):678-89
41. Menon AG, Janssen-van Rhijn CM, Morreau H, et al. Immune system and prognosis in colorectal cancer: a detailed immunohistochemical analysis. Lab Invest 2004;84(4):493-501
42. Kondo T, Takata H, Matsuki F, Takiguchi M. Cutting edge: phenotypic characterization and differentiation of human CD8+ T cells producing IL-17. J Immunol 2009;182(4):1794-8
43. Intlekofer AM, Banerjee A, Takemoto N, et al. Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 2008;321(5887):408-11
44. Tajima M, Wakita D, Noguchi D, et al. IL-6-dependent spontaneous proliferation is required for the induction of colitogenic IL-17-producing CD8+ T cells. J Exp Med 2008;205(5):1019-27
45. Weaver CT, Hatton RD. Interplay between the TH17 and TReg cell lineages: a (co-)evolutionary perspective. Nat Rev Immunol 2009;9(12):883-9
46. Dubin PJ, Kolls JK. Th17 cytokines and mucosal immunity. Immunol Rev 2008;226:160-71
47. Beriou G, Costantino CM, Ashley CW, et al. IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood 2009;113(18):4240-9
48. Voo KS, Wang YH, Santori FR, et al. Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc Natl Acad Sci USA 2009;106(12):4793-8
49. Huang C, Fu ZX. Localization of IL-17 +Foxp3+ T cells in esophageal cancer. Immunol Invest 2011;40(4):400-12
50. Kryczek I, Banerjee M, Cheng P, et al. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 2009;114(6):1141-9
51. Sfanos KS, Bruno TC, Maris CH, et al. Phenotypic analysis of prostate-infiltrating lymphocytes reveals TH17 and Treg skewing. Clin Cancer Res 2008;14(11):3254-61
52. Koyama K, Kagamu H, Miura S, et al. Reciprocal CD4+ T-cell balance of effector CD62Llow CD4+ and CD62LhighCD25+ CD4+ regulatory T cells in small cell lung cancer reflects disease stage. Clin Cancer Res 2008;14(21):6770-9
53. Muranski P, Boni A, Antony PA, et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 2008;112(2):362-73
54. Kottke T, Sanchez-Perez L, Diaz RM, et al. Induction of hsp70-mediated Th17 autoimmunity can be exploited as immunotherapy for metastatic prostate cancer. Cancer Res 2007;67(24):11970-9
55. Gnerlich JL, Mitchem JB, Weir JS, et al. Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer. J Immunol 2010;185(7):4063-71
56. Numasaki M, Watanabe M, Suzuki T, et al. IL-17 enhances the net angiogenic activity and in vivo growth of human non-small cell lung cancer in SCID mice through promoting CXCR-2-dependent angiogenesis. J Immunol 2005;175(9):6177-89
57. Numasaki M, Fukushi J, Ono M, et al. Interleukin-17 promotes angiogenesis and tumor growth. Blood 2003;101(7):2620-7
58. Wang L, Yi T, Kortylewski M, et al. IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway. J Exp Med 2009;206(7):1457-64
59. Derhovanessian E, Adams V, Hahnel K, et al. Pretreatment frequency of circulating IL-17+ CD4+ T-cells, but not Tregs, correlates with clinical response to whole-cell vaccination in prostate cancer patients. Int J Cancer 2009;125(6):1372-9
60. Zhang B, Rong G, Wei H, et al. The prevalence of Th17 cells in patients with gastric cancer. Biochem Biophys Res Commun 2008;374(3):533-7
61. Zhang YL, Li J, Mo HY, et al. Different subsets of tumor infiltrating lymphocytes correlate with NPC progression in different ways. Mol Cancer 2010;9:4
62. Ye ZJ, Zhou Q, Gu YY, et al. Generation and differentiation of IL-17-producing CD4+ T cells in malignant pleural effusion. J Immunol 2010;185(10):6348-54
63. Zhou X, Bailey-Bucktrout S, Jeker LT, Bluestone JA. Plasticity of CD4(+) FoxP3(+) T cells. Curr Opin Immunol 2009;21(3):281-5
64. Pan F, Yu H, Dang EV, et al. Eos mediates Foxp3-dependent gene silencing in CD4+ regulatory T cells. Science 2009;325(5944):1142-6
65. Bettelli E, Dastrange M, Oukka M. Foxp3 interacts with nuclear factor of activated T cells and NF-kappa B to repress cytokine gene expression and effector functions of T helper cells. Proc Natl Acad Sci USA 2005;102(14):5138-43
66. Ono M, Yaguchi H, Ohkura N, et al. Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 2007;446(7136):685-9
67. Zhou L, Lopes JE, Chong MM, et al. TGF-beta-induced Foxp3 inhibits T(H) 17 cell differentiation by antagonizing RORgammat function. Nature 2008;453(7192):236-40
68. Mantel PY, Kuipers H, Boyman O, et al. GATA3-driven Th2 responses inhibit TGF-beta1-induced FOXP3 expression and the formation of regulatory T cells. PLoS Biol 2007;5(12):e329
69. Huang B, Pan PY, Li Q, et al. Gr-1 +CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res 2006;66(2):1123-31
70. Pan PY, Ma G, Weber KJ, et al. Immune stimulatory receptor CD40 is required for T-cell suppression and T regulatory cell activation mediated by myeloid-derived suppressor cells in cancer. Cancer Res 2010;70(1):99-108
71. Mandapathil M, Hilldorfer B, Szczepanski MJ, et al. Generation and accumulation of immunosuppressive adenosine by human CD4 +CD25highFOXP3+ regulatory T cells. J Biol Chem 2010;285(10):7176-86
72. Curiel TJ, Coukos G, Zou L, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10(9):942-9
73. Wolf D, Wolf AM, Rumpold H, et al. The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer. Clin Cancer Res 2005;11(23):8326-31
74. Bates GJ, Fox SB, Han C, et al. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol 2006;24(34):5373-80
75. deLeeuw RJ, Kost SE, Kakal JA, Nelson BH. The prognostic value of FoxP3+ tumor-infiltrating lymphocytes in cancer: a critical review of the literature. Clin Cancer Res 2012;18(11):3022-9
76. Milne K, Kobel M, Kalloger SE, et al. Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLoS One 2009;4(7):e6412
77. Correale P, Rotundo MS, Del Vecchio MT, et al. Regulatory (FoxP3+) T-cell tumor infiltration is a favorable prognostic factor in advanced colon cancer patients undergoing chemo or chemoimmunotherapy. J Immunother 2010;33(4):435-41
78. Haas M, Dimmler A, Hohenberger W, et al. Stromal regulatory T-cells are associated with a favourable prognosis in gastric cancer of the cardia. BMC Gastroenterol 2009;9:65
79. Ladoire S, Martin F, Ghiringhelli F. Prognostic role of FOXP3+ regulatory T cells infiltrating human carcinomas: the paradox of colorectal cancer. Cancer Immunol Immunother 2011;60(7):909-18
80. Whiteside TL. Immune responses to malignancies. J Allergy Clin Immunol 2010;125(2 Suppl 2):S272-83
81. Winerdal ME, Marits P, Winerdal M, et al. FOXP3 and survival in urinary bladder cancer. BJU Int 2011;108(10):1672-8
82. Shah W, Yan X, Jing L, et al. A reversed CD4/CD8 ratio of tumor-infiltrating lymphocytes and a high percentage of CD4(+)FOXP3(+) regulatory T cells are significantly associated with clinical outcome in squamous cell carcinoma of the cervix. Cell Mol Immunol 2011;8(1):59-66
83. Watanabe Y, Katou F, Ohtani H, et al. Tumor-infiltrating lymphocytes, particularly the balance between CD8(+) T cells and CCR4(+) regulatory T cells, affect the survival of patients with oral squamous cell carcinoma. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109(5):744-52
84. Iliopoulou EG, Karamouzis MV, Missitzis I, et al. Increased frequency of CD4+ cells expressing CD161 in cancer patients. Clin Cancer Res 2006;12(23):6901-9
85. Solstad T, Bains SJ, Landskron J, et al. CD147 (Basigin/Emmprin) identifies FoxP3+CD45RO+CTLA4+-activated human regulatory T cells. Blood 2011;118(19):5141-51
86. Goldstein MJ, Kohrt HE, Houot R, et al. Adoptive cell therapy for lymphoma with CD4 T cells depleted of CD137-expressing regulatory T cells. Cancer Res 2012;72(5):1239-47
87. Smith SE, Hoelzinger DB, Dominguez AL, et al. Signals through 4-1BB inhibit T regulatory cells by blocking IL-9 production enhancing antitumor responses. Cancer Immunol Immunother 2011;60(12):1775-87
88. Purwar R, Schlapbach C, Xiao S, et al. Robust tumor immunity to melanoma mediated by interleukin-9-producing T cells. Nat Med 2012
89. Vanneman M, Dranoff G. Combining immunotherapy and targeted therapies in cancer treatment. Nat Rev Cancer 2012;12(4):237-51
90. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol 2008;8(1):59-73
91. Whiteside TL. Down-regulation of zeta-chain expression in T cells: a biomarker of prognosis in cancer? Cancer Immunol Immunother 2004;53(10):865-78
92. Fridman WH, Pages F, Sautes-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012;12(4):298-306
93. Cipponi A, Wieers G, van Baren N, Coulie PG. Tumor-infiltrating lymphocytes: apparently good for melanoma patients. But why? Cancer Immunol Immunother 2011;60(8):1153-60
94. Hodi FS, O'Day SJ, McDermott DF, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363(8):711-23