The effects of CCR5 inhibition on regulatory T-cell recruitment to colorectal cancer

British Journal of Cancer

Volumn 112, Issue 2, 2015, Pages 319-328

  Ward, S T ^a   Li, K K ^b   Hepburn, E ^b   Weston, C J ^b   Curbishley, S M ^b   Reynolds, G M ^b   Hejmadi, R K ^c   Bicknell, R ^a   Eksteen, B ^d   Ismail, T ^c   Rot, A ^a   Adams, D H ^b  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b University Hospital Birmingham NHS Foundation Trust   (United Kingdom)

^c QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

Colorectal cancer; Regulatory T cells; Tumour immunology

Indexed keywords

CARBON TETRACHLORIDE; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; KRUPPEL LIKE FACTOR 2; TRANSCRIPTION FACTOR FOXP3; ANTINEOPLASTIC AGENT; CCR5 PROTEIN, MOUSE; CYCLOHEXANE DERIVATIVE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MARAVIROC; TRIAZOLE DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COLORECTAL CANCER; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CANCER TRANSPLANTATION; COLORECTAL NEOPLASMS; DRUG SCREENING; FEMALE; IMMUNOLOGY; MELANOMA, EXPERIMENTAL; METABOLISM; NEUTROPHIL CHEMOTAXIS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CCR5 RECEPTOR ANTAGONISTS; CELL LINE, TUMOR; CELL PROLIFERATION; CHEMOKINE CCL4; CHEMOTAXIS, LEUKOCYTE; COLORECTAL NEOPLASMS; CYCLOHEXANES; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; HUMANS; MELANOMA, EXPERIMENTAL; MICE, INBRED BALB C; NEOPLASM TRANSPLANTATION; RECEPTORS, CCR5; T-LYMPHOCYTES, REGULATORY; TRIAZOLES;

EID: 84921896866     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.572     Document Type: Article

References (46)

1. Adams DH, Eksteen B (2006) Aberrant homing of mucosal T cells and extra-intestinal manifestations of inflammatory bowel disease. Nat Rev Immunol 6: 244-251.
2. Ajuebor MN, Wondimu Z, Hogaboam CM, Le T, Proudfoot AEI, Swain MG (2007) CCR5 deficiency drives enhanced natural killer cell trafficking to and activation within the liver in murine T cell-mediated hepatitis. Am J Pathol 170: 1975-1988.
3. Ambati BK, Anand A, Joussen AM, Kuziel WA, Adamis AP, Ambati J (2003) Sustained inhibition of corneal neovascularization by genetic ablation of CCR5. Invest Ophthalmol Vis Sci 44: 590-593.
4. Camargo JF, Quinones MP, Mummidi S, Srinivas S, Gaitan AA, Begum K, Jimenez F, VanCompernolle S, Unutmaz D, Ahuja SS, Ahuja SK (2009) CCR5 expression levels influence NFAT translocation, IL-2 production, and subsequent signaling events during T lymphocyte activation. J Immunol 182: 171-182.
5. Cambien B, Richard-Fiardo P, Karimdjee BF, Martini V, Ferrua B, Pitard B, Schmid-Antomarchi H, Schmid-Alliana A (2011) CCL5 neutralization restricts cancer growth and potentiates the targeting of PDGFRβ in colorectal carcinoma. PLoS One 6: e28842.
6. Chang L-Y, Lin Y-C, Mahalingam J, Huang C-T, Chen T-W, Kang C-W, Peng H-M, Chu Y-Y, Chiang J-M, Dutta A, Day Y-J, Chen T-C, Yeh C-T, Lin C-Y (2012) Tumor-derived chemokine CCL5 enhances TGF-ß mediated killing of CD8+ T cells in colon cancer by T regulatory cells. Cancer Res 72: 1092-1102.
7. Chaput N, Louafi S, Bardier A, Charlotte F, Vaillant J-C, Ménégaux F, Rosenzwajg M, Lemoine F, Klatzmann D, Taieb J (2009) Identification of CD8+CD25+Foxp3+ suppressive T cells in colorectal cancer tissue. Gut 58: 520-529.
8. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, Zou W (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10: 942-949.
9. Danke NA, Koelle DM, Yee C, Beheray S, Kwok WW (2004) Autoreactive T cells in healthy individuals. J Immunol 172: 5967-5972.
10. Darrasse-Jèze G, Marodon G, Salomon BL, Catala M, Klatzmann D (2005) Ontogeny of CD4+CD25+ regulatory/suppressor T cells in human fetuses. Blood 105: 4715-4721.
11. Deng L, Zhang H, Luan Y, Zhang J, Xing Q, Dong S, Wu X, Liu M, Wang S (2010) Accumulation of Foxp3+ T regulatory cells in draining lymph nodes correlates with disease progression and immune suppression in colorectal cancer patients. Clin Cancer Res 16: 4105-4112.
12. Diederichsen ACP, Zeuthen J, Christensen PB, Kristensen T (1999) Characterisation of tumour infiltrating lymphocytes and correlations with immunological surface molecules in colorectal cancer. Eur J Cancer 35: 721-726.
13. Dorr P (2008) Maraviroc outlook in HIV and non-HIV diseases. HIV infection and organ transplantation symposium. University Medical Center Hamburg-Eppendorf: Hamburg, Germany.
14. Dorr P, Westby M, Dobbs S, Griffin P, Irvine B, Macartney M, Mori J, Rickett G, Smith-Burchnell C, Napier C, Webster R, Armour D, Price D, Stammen B, Wood A, Perros M (2005) Maraviroc (UK-427,857), a potent, orally bioavailable, and selective small-molecule inhibitor of chemokine receptor CCR5 with broad-spectrum anti-human immunodeficiency virus type 1 activity. Antimicrob Agents Chemother 49: 4721-4732.
15. Fantini MC, Becker C, Monteleone G, Pallone F, Galle PR, Neurath MF (2004) Cutting edge: TGF-beta induces a regulatory phenotype in CD4+ CD25- T cells through Foxp3 induction and down-regulation of Smad7. J Immunol 172: 5149-5153.
16. Floess S, Freyer J, Siewert C, Baron U, Olek S, Polansky J, Schlawe K, Chang H-D, Bopp T, Schmitt E, Klein-Hessling S, Serfling E, Hamann A, Huehn J (2007) Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol 5: e38.
17. Ford AL, Foulcher E, Goodsall AL, Sedgwick JD (1996) Tissue digestion with dispase substantially reduces lymphocyte and macrophage cell-surface antigen expression. J Immunol Methods 194: 71-75.
18. Frey DM, Droeser RA, Viehl CT, Zlobec I, Lugli A, Zingg U, Oertli D, Kettelhack C, Terracciano L, Tornillo L (2010) High frequency of tumor-infiltrating FOXP3 regulatory T cells predicts improved survival in mismatch repair-proficient colorectal cancer patients. Int J Cancer 126: 2635-2643.
19. Gobert M, Treilleux I, Bendriss-Vermare N, Bachelot T, Goddard-Leon S, Arfi V, Biota C, Doffin AC, Durand I, Olive D, Perez S, Pasqual N, Faure C, Ray-Coquard I, Puisieux A, Caux C, Blay J-Y, Ménétrier-Caux C (2009) Regulatory T Cells recruited through CCL22/CCR4 are selectively activated in lymphoid infiltrates surrounding primary breast tumors and lead to an adverse clinical outcome. Cancer Res 69: 2000-2009.
20. Grange C, Létourneau J, Forget M-A, Godin-Ethier J, Martin J, Liberman M, Latour M, Widmer H, Lattouf J-B, Piccirillo CA, Cailhier J-F, Lapointe R (2011) Phenotypic characterization and functional analysis of human tumor immune infiltration after mechanical and enzymatic disaggregation. J Immunol Methods 372: 119-126.
21. Ha T-Y (2009) The role of regulatory T cells in cancer. Immune Netw 9: 209.
22. Ishida Y, Kimura A, Kuninaka Y, Inui M, Matsushima K, Mukaida N, Kondo T (2012) Pivotal role of the CCL5/CCR5 interaction for recruitment of endothelial progenitor cells in mouse wound healing. J Clin Invest 122: 711-721.
23. Kroetz DN, Deepe GS (2011) An aberrant thymus in CCR5(-/-) mice is coupled with an enhanced adaptive immune response in fungal infection. J Immunol 186: 5949-5955.
24. Kuziel WA, Dawson TC, Quinones M, Garavito E, Chenaux G, Ahuja SS, Reddick RL, Maeda N (2003) CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. Atherosclerosis 167: 25-32.
25. Ling KL, Pratap SE, Bates GJ, Singh B, Mortensen NJ, George BD, Warren BF, Piris J, Roncador G, Fox SB, Banham AH, Cerundolo V (2007) Increased frequency of regulatory T cells in peripheral blood and tumour infiltrating lymphocytes in colorectal cancer patients. Cancer Immun 7: 7.
26. Liu VC, Wong LY, Jang T, Shah AH, Park I, Yang X, Zhang Q, Lonning S, Teicher BA, Lee C (2007) Tumor evasion of the immune system by converting CD4+CD25- T cells into CD4+CD25+ T regulatory cells: role of tumor-derived TGF-beta. J Immunol 178: 2883-2892.
27. Loddenkemper C, Schernus M, Noutsias M, Stein H, Thiel E, Nagorsen D (2006) In situ analysis of FOXP3+ regulatory T cells in human colorectal cancer. J Transl Med 4: 52.
28. Mansfield R, Able S, Griffin P, Irvine B, James I, Macartney M, Miller K, Mills J, Napier C, Navratilova I, Perros M, Rickett G, Root H, van der Ryst E, Westby M, Dorr P (2009) CCR5 pharmacology methodologies and associated applications. Methods Enzymol 460: 17-55.
29. McMurchy AN, Levings MK (2012) Suppression assays with human T regulatory cells: A technical guide. Eur J Immunol 42: 27-34.
30. Mizukami Y, Kono K, Kawaguchi Y, Akaike H, Kamimura K, Sugai H, Fujii H (2008) CCL17 and CCL22 chemokines within tumor microenvironment are related to accumulation of Foxp3+ regulatory T cells in gastric cancer. Int J Cancer 122: 2286-2293.
31. Mueller A, Strange PG (2004) Mechanisms of internalization and recycling of the chemokine receptor, CCR5. Eur J Biochem FEBS 271: 243-252.
32. Mulder WMC, Koenen H, Muysenberg AJC, Bloemena E, Wagsfaff J, Scheper RJ (1994) Reduced expression of distinct T-cell CD molecules by collagenase/DNase treatment. Cancer Immunol Immunother 38: 253-258.
33. Ray N (2009) Maraviroc in the treatment of HIV infection. Drug Des Devel Ther 2: 151-161.
34. Richardson MW, Jadlowsky J, Didigu CA, Doms RW, Riley JL (2012) KLF2 modulates CCR5 expression and susceptibility to HIV-1 infection. J Immunol 189: 3815-3821.
35. Saita Y, Kondo M, Shimizu Y (2007) Species selectivity of small-molecular antagonists for the CCR5 chemokine receptor. Int Immunopharmacol 7: 1528-1534.
36. Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D, Platell C, Iacopetta B (2009) Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 27: 186-192.
37. Schlecker E, Stojanovic A, Eisen C, Quack C, Falk CS, Umansky V, Cerwenka A (2012) Tumor-infiltrating monocytic myeloid-derived suppressor cells mediate CCR5-dependent recruitment of regulatory T cells favoring tumor growth. J Immunol 189: 5602-5611.
38. Sinicrope FA, Rego RL, Ansell SM, Knutson KL, Foster NR, Sargent DJ (2009) Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 137: 1270-1279.
39. Song JK, Park MH, Choi D-Y, Yoo HS, Han SB, Yoon DY, Hong JT (2012) Deficiency of C-C chemokine receptor 5 suppresses tumor development via inactivation of NF-κB and upregulation of IL-1Ra in melanoma model. PLoS One 7: e33747.
40. Spring H, Schüler T, Arnold B, Hämmerling GJ, Ganss R (2005) Chemokines direct endothelial progenitors into tumor neovessels. Proc Natl Acad Sci USA 102: 18111-18116.
41. Tan MCB, Goedegebuure PS, Belt BA, Flaherty B, Sankpal N, Gillanders WE, Eberlein TJ, Hsieh C-S, Linehan DC (2009) Disruption of CCR5- dependent homing of regulatory T cells inhibits tumor growth in a murine model of pancreatic cancer. J Immunol 182: 1746-1755.
42. Tatura R, Zeschnigk M, Adamzik M, Probst-Kepper M, Buer J, Kehrmann J (2012) Quantification of regulatory T cells in septic patients by real-time PCR-based methylation assay and flow cytometry. PLoS One 7: e49962.
43. Terme M, Pernot S, Marcheteau E, Sandoval F, Benhamouda N, Colussi O, Dubreuil O, Carpentier AF, Tartour E, Taieb J (2013) VEGFA-VEGFR pathway blockade inhibits tumor-induced regulatory T-cell proliferation in colorectal cancer. Cancer Res 73: 539-549.
44. Wainwright DA, Sengupta S, Han Y, Lesniak MS (2011) Thymus-derived rather than tumor-induced regulatory T cells predominate in brain tumors. Neuro-Oncol 13: 1308-1323.
45. Wierda RJ, Kuipers HF, van Eggermond MCJA, Benard A, van Leeuwen JC, Carluccio S, Geutskens SB, Jukema JW, Marquez VE, Quax PHA, van den Elsen PJ (2012) Epigenetic control of CCR5 transcript levels in immune cells and modulation by small molecules inhibitors. J Cell Mol Med 16: 1866-1877.
46. Yoon HH, Orrock JM, Foster NR, Sargent DJ, Smyrk TC, Sinicrope FA (2012) Prognostic impact of FoxP3+ regulatory T cells in relation to CD8+ T lymphocyte density in human colon carcinomas. PloS One 7: e42274.