Intraepithelial Effector (CD3+)/Regulatory (FoxP3+) T-Cell Ratio Predicts a Clinical Outcome of Human Colon Carcinoma

Gastroenterology

Volumn 137, Issue 4, 2009, Pages 1270-1279

  Sinicrope, Frank A ^a   Rego, Rafaela L ^a   Ansell, Stephen M ^a   Knutson, Keith L ^a   Foster, Nathan R ^a   Sargent, Daniel J ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; DNA; FLUOROURACIL; FOLINIC ACID; LEVAMISOLE; LYMPHOCYTE SURFACE MARKER; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN;

AGE DISTRIBUTION; AGED; ANTIGEN EXPRESSION; ARTICLE; CANCER SURVIVAL; CD3+ T LYMPHOCYTE; CELL DENSITY; COLON CARCINOMA; COLON MUCOSA; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DISEASE SEVERITY; DRUG MEGADOSE; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MISMATCH REPAIR; OUTCOME ASSESSMENT; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY T LYMPHOCYTE; SEX DIFFERENCE; SURVIVAL TIME; TUMOR DIFFERENTIATION; ADENOCARCINOMA; AGE; CANCER STAGING; CELL DIFFERENTIATION; COLON TUMOR; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; KAPLAN MEIER METHOD; LYMPHOCYTE COUNT; MORTALITY; PATHOLOGY; PREDICTION AND FORECASTING; PROPORTIONAL HAZARDS MODEL; RISK ASSESSMENT; RISK FACTOR; TIME; TREATMENT OUTCOME;

ADENOCARCINOMA; AGE FACTORS; AGED; ANTIGENS, CD3; CELL DIFFERENTIATION; COLONIC NEOPLASMS; DISEASE-FREE SURVIVAL; DNA MISMATCH REPAIR; EPITHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; KAPLAN-MEIERS ESTIMATE; LYMPHOCYTE COUNT; MALE; MICROSCOPY, FLUORESCENCE; NEOPLASM STAGING; PREDICTIVE VALUE OF TESTS; PROPORTIONAL HAZARDS MODELS; RISK ASSESSMENT; RISK FACTORS; SEX FACTORS; T-LYMPHOCYTES, REGULATORY; TIME FACTORS; TREATMENT OUTCOME;

EID: 70349423483     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2009.06.053     Document Type: Article

References (62)

1. Jemal A., Siegel R., Ward E., et al. Cancer statistics, 2006. CA Cancer J Clin 56 (2006) 106-130
2. Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6 (2006) 295-307
3. Nishikawa H., Kato T., Tawara I., et al. Accelerated chemically induced tumor development mediated by CD4+CD25+ regulatory T cells in wild-type hosts. Proc Natl Acad Sci U S A 102 (2005) 9253-9257
4. Shimizu J., Yamazaki S., and Sakaguchi S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J Immunol 163 (1999) 5211-5218
5. Ziegler S.F. FOXP3: of mice and men. Annu Rev Immunol 24 (2006) 209-226
6. Hori S., Nomura T., and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3 [see comment]. Science 299 (2003) 1057-1061
7. Fontenot J.D., and Rudensky A.Y. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol 6 (2005) 331-337
8. Bensinger S.J., Walsh P.T., Zhang J., et al. Distinct IL-2 receptor signaling pattern in CD4+CD25+ regulatory T cells. J Immunol 172 (2004) 5287-5296
9. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells [see comment]. Nat Immunol 4 (2003) 330-336
10. Yagi H., Nomura T., Nakamura K., et al. Crucial role of FOXP3 in the development and function of human CD25+CD4+ regulatory T cells. Int Immunol 16 (2004) 1643-1656
11. Brunkow M.E., Jeffery E.W., Hjerrild K.A., et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 27 (2001) 68-73
12. Curiel T.J., Coukos G., Zou L., et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival [see comment]. Nat Med 10 (2004) 942-949
13. Turk M.J., Guevara-Patino J.A., Rizzuto G.A., et al. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J Exp Med 200 (2004) 771-782
14. Wolf A.M., Wolf D., Steurer M., et al. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res 9 (2003) 606-612
15. Sasada T., Kimura M., Yoshida Y., et al. CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression. Cancer 98 (2003) 1089-1099
16. Viguier M., Lemaitre F., Verola O., et al. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells. J Immunol 173 (2004) 1444-1453
17. Liyanage U.K., Moore T.T., Joo H.G., et al. Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J Immunol 169 (2002) 2756-2761
18. Yu P., Lee Y., Liu W., et al. Intratumor depletion of CD4+ cells unmasks tumor immunogenicity leading to the rejection of late-stage tumors. J Exp Med 201 (2005) 779-791
19. Wolf D., Wolf A.M., 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 [see comment]. Clin Cancer Res 11 (2005) 8326-8331
20. Bates G.J., Fox S.B., 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 [see comment]. J Clin Oncol 24 (2006) 5373-5380
21. Fu J., Xu D., Liu Z., et al. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 132 (2007) 2328-2339
22. Sato E., Olson S.H., Ahn J., et al. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 102 (2005) 18538-18543
23. Siddiqui S.A., Frigola X., Bonne-Annee S., et al. Tumor-infiltrating Foxp3-CD4+CD25+ T cells predict poor survival in renal cell carcinoma. Clin Cancer Res 13 (2007) 2075-2081
24. Yoshioka T., Miyamoto M., Cho Y., et al. Infiltrating regulatory T cell numbers is not a factor to predict patient's survival in oesophageal squamous cell carcinoma. Br J Cancer 98 (2008) 1258-1263
25. Sinicrope F.A., Rego R.L., Garrity-Park M.M., et al. Alterations in cell proliferation and apoptosis in colon cancers with microsatellite instability. Int J Cancer 120 (2007) 1232-1238
26. 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 159 (2001) 297-304
27. Baker K., Zlobec I., Tornillo L., et al. Differential significance of tumour infiltrating lymphocytes in sporadic mismatch repair deficient versus proficient colorectal cancers: a potential role for dysregulation of the transforming growth factor-beta pathway. Eur J Cancer 43 (2007) 624-631
28. Galon J., Costes A., Sanchez-Cabo F., et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313 (2006) 1960-1964
29. Ionov Y., Peinado M.A., Malkhosyan S., et al. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 363 (1993) 558-561
30. Michael-Robinson J.M., Biemer-Huttmann A., Purdie D.M., et al. Tumour infiltrating lymphocytes and apoptosis are independent features in colorectal cancer stratified according to microsatellite instability status. Gut 48 (2001) 360-366
31. Popat S., Hubner R., and Houlston R.S. Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol 23 (2005) 609-618
32. Sinicrope F.A., Rego R.L., Halling K.C., et al. Prognostic impact of microsatellite instability and DNA ploidy in human colon carcinoma patients. Gastroenterology 131 (2006) 729-737
33. Allegra C.J., Parr A.L., Wold L.E., et al. Investigation of the prognostic and predictive value of thymidylate synthase, p53, and Ki-67 in patients with locally advanced colon cancer. J Clin Oncol 20 (2002) 1735-1743
34. O'Connell M.J., Sargent D.J., Windschitl H.E., et al. Randomized clinical trial of high-dose levamisole combined with 5-fluorouracil and leucovorin as surgical adjuvant therapy for high-risk colon cancer. Clin Colorectal Cancer 6 (2006) 133-139
35. Halling K.C., French A.J., McDonnell S.K., et al. Microsatellite instability and 8p allelic imbalance in stage B2 and C colorectal cancers [see comment]. J Natl Cancer Inst 91 (1999) 1295-1303
36. Thibodeau S.N., French A.J., Cunningham J.M., et al. Microsatellite instability in colorectal cancer: different mutator phenotypes and the principal involvement of hMLH1. Cancer Res 58 (1998) 1713-1718
37. de la Chapelle A. Testing tumors for microsatellite instability. Eur J Hum Genet 7 (1999) 407-408
38. Bluestone J.A., and Abbas A.K. Natural versus adaptive regulatory T cells. Nat Rev Immunol 3 (2003) 253-257
39. Weisenberger D.J., Siegmund K.D., Campan M., et al. CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38 (2006) 787-793
40. Aaltonen L.A., Salovaara R., Kristo P., et al. Incidence of hereditary nonpolyposis colorectal cancer and the feasibility of molecular screening for the disease. N Engl J Med 338 (1998) 1481-1487
41. Cao X., Cai S.F., Fehniger T.A., et al. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 27 (2007) 635-646
42. Clarke S.L., Betts G.J., Plant A., et al. CD4+CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS ONE 1 (2006) e129
43. Ling K.L., Pratap S.E., Bates G.J., et al. Increased frequency of regulatory T cells in peripheral blood and tumour infiltrating lymphocytes in colorectal cancer patients. Cancer Immunity 7 (2007) 7
44. O'Connell J.B., Maggard M.A., and Ko C.Y. Colon cancer survival rates with the new American Joint Committee on Cancer sixth edition staging. J Natl Cancer Inst 96 (2004) 1420-1425
45. Petersen R.P., Campa M.J., Sperlazza J., et al. Tumor infiltrating Foxp3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients. Cancer 107 (2006) 2866-2872
46. Gao Q., Qiu S.J., Fan J., et al. Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 25 (2007) 2586-2593
47. Yang Z.Z., Novak A.J., Ziesmer S.C., et al. Attenuation of CD8(+) T-cell function by CD4(+)CD25(+) regulatory T cells in B-cell non-Hodgkin's lymphoma. Cancer Res 66 (2006) 10145-10152
48. Quezada S.A., Peggs K.S., Curran M.A., et al. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest 116 (2006) 1935-1945
49. Petrini B., Wasserman J., Blomgren H., et al. Changes of blood T cell subsets in patients receiving postoperative adjuvant chemotherapy for breast cancer. Eur J Cancer Clin Oncol 20 (1984) 1485-1487
50. Naito Y., Saito K., Shiiba K., et al. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res 58 (1998) 3491-3494
51. Chiba T., Ohtani H., Mizoi T., et al. Intraepithelial CD8+ T-cell-count becomes a prognostic factor after a longer follow-up period in human colorectal carcinoma: possible association with suppression of micrometastasis. Br J Cancer 91 (2004) 1711-1717
52. Tomsova M., Melichar B., Sedlakova I., et al. Prognostic significance of CD3+ tumor-infiltrating lymphocytes in ovarian carcinoma. Gynecol Oncol 108 (2008) 415-420
53. Takemoto N., Konishi F., Yamashita K., et al. The correlation of microsatellite instability and tumor-infiltrating lymphocytes in hereditary non-polyposis colorectal cancer (HNPCC) and sporadic colorectal cancers: the significance of different types of lymphocyte infiltration. Jpn J Clin Oncol 34 (2004) 90-98
54. Quinn E., Hawkins N., Yip Y.L., et al. CD103+ intraepithelial lymphocytes--a unique population in microsatellite unstable sporadic colorectal cancer. Eur J Cancer 39 (2003) 469-475
55. Ebert E.C., and Roberts A.I. Lymphokine-activated killing by human intestinal lymphocytes. Cell Immunol 146 (1993) 107-116
56. Golby S.J., Chinyama C., and Spencer J. Proliferation of T-cell subsets that contact tumour cells in colorectal cancer. Clin Exp Immunol 127 (2002) 85-91
57. Zhang L., Conejo-Garcia J.R., Katsaros D., et al. Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348 (2003) 203-213
58. Reiman J.M., Kmieciak M., Manjili M.H., et al. Tumor immunoediting and immunosculpting pathways to cancer progression. Semin Cancer Biol 17 (2007) 275-287
59. Brandacher G., Perathoner A., Ladurner R., et al. Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T cells. Clin Cancer Res 12 (2006) 1144-1151
60. Jass J.R., Do K.A., Simms L.A., et al. Morphology of sporadic colorectal cancer with DNA replication errors [see comment]. Gut 42 (1998) 673-679
61. Schwitalle Y., Kloor M., Eiermann S., et al. Immune response against frameshift-induced neopeptides in HNPCC patients and healthy HNPCC mutation carriers. Gastroenterology 134 (2008) 988-997
62. Baker K., Foulkes W.D., and Jass J.R. MSI-H colorectal cancers preferentially retain and expand intraepithelial lymphocytes rather than peripherally derived CD8+ T cells. Cancer Immunol Immunother 58 (2009) 135-144