Suppression of tumour-specific CD4 + T cells by regulatory T cells is associated with progression of human colorectal cancer

Gut

Volumn 61, Issue 8, 2012, Pages 1163-1171

  Betts, Gareth ^a   Jones, Emma ^a   Junaid, Syed ^a   El Shanawany, Tariq ^a   Scurr, Martin ^a   Mizen, Paul ^a   Kumar, Mayur ^a   Jones, Sion ^a   Rees, Brian ^b   Williams, Geraint ^a   Gallimore, Awen ^a   Godkin, Andrew ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY HOSPITAL OF WALES   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOEMBRYONIC ANTIGEN; PROTEIN 5T4; TRANSCRIPTION FACTOR FOXP3; TUMOR ANTIGEN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CANCER GROWTH; CANCER RECURRENCE; CANCER SURGERY; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CELLULAR IMMUNODEFICIENCY; COLORECTAL CARCINOMA; COLORECTAL SURGERY; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE DYSREGULATION; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TREATMENT OUTCOME; UPREGULATION;

ADENOCARCINOMA; ADULT; AGED; AGED, 80 AND OVER; ANTINEOPLASTIC AGENTS; CD4-POSITIVE T-LYMPHOCYTES; COLECTOMY; COLORECTAL NEOPLASMS; DISEASE PROGRESSION; FEMALE; FLOW CYTOMETRY; FOLLOW-UP STUDIES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNITY, CELLULAR; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; NEOPLASM RECURRENCE, LOCAL; NEOPLASM STAGING; PROGNOSIS; T-LYMPHOCYTES, REGULATORY; TIME FACTORS;

EID: 84863721491     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2011-300970     Document Type: Article

References (36)

1. 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;313:1960-4. (Pubitemid 44498003)
2. Hole N, Stern PL. Isolation and characterization of 5T4, a tumour-associated antigen. Int J Cancer 1990;45:179-84. (Pubitemid 20032118)
3. Southall PJ, Boxer GM, Bagshawe KD, et al. Immunohistological distribution of 5T4 antigen in normal and malignant tissues. Br J Cancer 1990;61:89-95.
4. Starzynska T, Rahi V, Stern PL. The expression of 5T4 antigen in colorectal and gastric carcinoma. Br J Cancer 1992;66:867-9.
5. Hammarstrom S. The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues. Semin Cancer Biol 1999;9:67-81. (Pubitemid 29265523)
6. Campi G, Crosti M, Consogno G, et al. CD4(+) T cells from healthy subjects and colon cancer patients recognize a carcinoembryonic antigen-specific immunodominant epitope. Cancer Res 2003;63:8481-6. (Pubitemid 37549504)
7. Kobayashi H, Omiya R, Ruiz M, et al. Identification of an antigenic epitope for helper T lymphocytes from carcinoembryonic antigen. Clin Cancer Res 2002;8:3219-25. (Pubitemid 35155034)
8. Shen L, Schroers R, Hammer J, et al. Identification of a MHC class-II restricted epitope in carcinoembryonic antigen. Cancer Immunol Immunother 2004;53:391-403. (Pubitemid 38657252)
9. Rosenberg SA, Yang JC, Restifo NP. Cancer immunotherapy: moving beyond current vaccines. Nat Med 2004;10:909-15. (Pubitemid 39273730)
10. Bennett CL, Christie J, Ramsdell F, et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001;27:20-1. (Pubitemid 32044513)
11. Brunkow ME, Jeffery EW, Hjerrild KA, et al. Disruption of a new forkhead/wingedhelix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001;27:68-73. (Pubitemid 32044521)
12. Jones E, Dahm-Vicker M, Simon AK, et al. Depletion of CD25+ regulatory cells results in suppression of melanoma growth and induction of autoreactivity in mice. Cancer Immun 2002;2:1.
13. Onizuka S, Tawara I, Shimizu J, et al. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999;59:3128-33. (Pubitemid 29316012)
14. Ambrosino E, Spadaro M, Iezzi M, et al. Immunosurveillance of Erbb2 carcinogenesis in transgenic mice is concealed by a dominant regulatory T-cell selftolerance. Cancer Res 2006;66:7734-40. (Pubitemid 44289233)
15. Betts G, Twohig J, Van den Broek M, et al. The impact of regulatory T cells on carcinogen-induced sarcogenesis. Br J Cancer 2007;96:1849-54. (Pubitemid 46912032)
16. Betts GJ, Clarke SL, Richards HE, et al. Regulating the immune response to tumours. Adv Drug Deliv Rev 2006;58:948-61. (Pubitemid 44709264)
17. Clarke SL, Betts GJ, Plant A, et al. CD4+CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS One 2006;1:e129.
18. Sinicrope FA, Rego RL, Ansell SM, et al. Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 2009;137:1270-9.
19. Bonertz A, Weitz J, Pietsch DH, et al. Antigen-specific Tregs control T cell responses against a limited repertoire of tumor antigens in patients with colorectal carcinoma. J Clin Invest 2009;119:3311-21.
20. Harrop R, Ryan MG, Myers KA, et al. Active treatment of murine tumors with a highly attenuated vaccinia virus expressing the tumor associated antigen 5T4 (TroVax) is CD4+ T cell dependent and antibody mediated. Cancer Immunol Immunother 2006;55:1081-90. (Pubitemid 43800723)
21. Lalvani A, Brookes R, Hambleton S, et al. Rapid effector function in CD8+ memory T cells. J Exp Med 1997;186:859-65. (Pubitemid 27407347)
22. Baecher-Allan CM, Hafler DA. The purification and functional analysis of human CD4+CD25high regulatory T cells. Curr Protoc Immunol 2006;Chapter 7: Unit 7.4B.
23. Miyara M, Yoshioka Y, Kitoh A, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity 2009;30:899-911.
24. Wang J, Ioan-Facsinay A, van der Voort EI, et al. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 2007;37:129-38. (Pubitemid 46128793)
25. Mortarini R, Borri A, Tragni G, et al. Peripheral burst of tumor-specific cytotoxic T lymphocytes and infiltration of metastatic lesions by memory CD8+ T cells in melanoma patients receiving interleukin 12. Cancer Res 2000;60:3559-68. (Pubitemid 30482177)
26. Oo YH, Weston CJ, Lalor PF, et al. Distinct roles for CCR4 and CXCR3 in the recruitment and positioning of regulatory T cells in the inflamed human liver. J Immunol 2010;184:2886-98.
27. Lehmann J, Huehn J, de la Rosa M, et al. Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25- regulatory T cells. Proc Natl Acad Sci U S A 2002;99:13031-6.
28. Stassen M, Fondel S, Bopp T, et al. Human CD25+ regulatory T cells: two subsets defined by the integrins alpha 4 beta 7 or alpha 4 beta 1 confer distinct suppressive properties upon CD4+ T helper cells. Eur J Immunol 2004;34:1303-11. (Pubitemid 39256009)
29. Bonnin B, Correll A, Swiatek-de Lange M, et al. Large scale preparation of human MHC class II+ integrin beta(1)+ Tregs. J Immunol Methods 2010;360:96-102.
30. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005;5:263-74. (Pubitemid 40488632)
31. Nagorsen D, Thiel E. Clinical and immunologic responses to active specific cancer vaccines in human colorectal cancer. Clin Cancer Res 2006;12:3064-9. (Pubitemid 43837352)
32. Deng L, Zhang H, Luan Y, et al. Accumulation of foxp3+ T regulatory cells in draining lymph nodes correlates with disease progression and immune suppression in colorectal cancer patients. Clin Cancer Res 2010;16:4105-12.
33. Elkord E, Burt DJ, Drijfhout JW, et al. CD4+ T-cell recognition of human 5T4 oncofoetal antigen: implications for initial depletion of CD25+ T cells. Cancer Immunol Immunother 2008;57:833-47.
34. Nagorsen D, Scheibenbogen C, Letsch A, et al. T cell responses against tumor associated antigens and prognosis in colorectal cancer patients. J TranslMed 2005;3:3.
35. 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;27:186-92.
36. Erdman SE, Poutahidis T, Tomczak M, et al. CD4+ CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 2003;162:691-702. (Pubitemid 36267876)