Involvement of Regulatory T Cells and Their Cytokines Repertoire in Chemopreventive Action of Fish Oil in Experimental Colon Cancer

References

• Markel G, Seidman R, Stern N, Cohen-Sinai T, Izhaki O, et al.: Inhibition of human tumor-infiltrating lymphocyte effector functions by the homophilic carcinoembryonic cell adhesion molecule 1 interactions. J Immunol 177, 6062–6071, 2006.
   PubMed Web of Science ®Google Scholar
• Leffers N, Gooden MJ, de Jong RA, Hoogeboom BN, ten Hoor KA, et al.: Prognostic significance of tumor-infiltrating T-lymphocytes in primary and metastatic lesions of advanced stage ovarian cancer. Cancer Immunol Immunother 58, 449–459, 2009.
   PubMed Web of Science ®Google Scholar
• Wijk FV and Cheroutre H: Intestinal T cells: Facing the mucosal immune dilemma with synergy and diversity. Semin. Immunol 21, 130–138, 2009.
   PubMed Web of Science ®Google Scholar
• Nishikawa H and Sakaguchi S: Regulatory T cells in tumour immunity. Int J Cancer 127, 759–767, 2010.
   PubMed Web of Science ®Google Scholar
• Sakaguchi S: Naturally arising CD4 + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22, 531–562, 2004.
   PubMed Web of Science ®Google Scholar
• Shevach EM: CD4 + CD25 + suppressor T cells: more questions than answers. Nat Rev Immunol 2, 389–400, 2002.
   PubMed Web of Science ®Google Scholar
• Maria A, Lafaille CD, and Lafaille JJ: Natural and adaptive Foxp3 + regulatory T cells: More of the same or a division of labor? Immunity 30, 626–635, 2009.
   PubMed Web of Science ®Google Scholar
• Beyer M and Schultze JL: Plasticity of Treg cells: Is reprogramming of Treg cells possible in the presence of FOXP3? Int Immunopharmacol 11, 555–560, 2011.
   PubMed Web of Science ®Google Scholar
• Zhou G and Levitsky HL: Natural regulatory T cells and de novo-induced regulatory T cells contribute independently to tumour-specific tolerance. J Immunol 178, 2155–2162, 2007.
   PubMed Web of Science ®Google Scholar
• Ladoire S, Martin F, and Ghiringhelli F: Prognostic role of FOXP3 + regulatory T cells infiltrating human carcinomas: the paradox of colorectal cancer. Cancer Immunol Immunother 60, 909–918, 2011.
   PubMed Web of Science ®Google Scholar
• Bates GJ, Fox SB, Han C, Leek RD, Garcia JF, 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 24, 5373–5380, 2006.
   PubMed Web of Science ®Google Scholar
• Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, et al.: Intratumoural balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 25, 2586–2593, 2007.
   PubMed Web of Science ®Google Scholar
• Li JF, Chu YW, Wang GM, Zhu TY, Rong RM, et al.: The prognostic value of peritumoural regulatory T cells and its correlation with intratumoural cyclooxygenase-2 expression in clear cell renal cell carcinoma. BJU Int 103, 399–405, 2009.
   PubMed Web of Science ®Google Scholar
• Hiraoka N, Onozato K, Kosuge T, and Hirohashi S: Prevalence of FOXP3 + regulatory T cells increases during the progression of pancreatic ductal adenocarcinoma and its premalignant lesions. Clin Cancer Res 12, 5423–5434, 2006.
   PubMed Web of Science ®Google Scholar
• Salama P, Phillips M, Grieu F, Morris M, Zeps N, et al.: Tumour-Infiltrating FOXP3 + T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 27, 186–192, 2008.
   PubMed Web of Science ®Google Scholar
• Matsuda S, Vamane T, and Hamaji M: CD4- and TCRa∼-positive T lymphocytes predominantly infiltrated into well-moderately differentiated colon adenocarcinoma tissues. Jpn J Clin 28, 97–103, 1998.
   PubMed Web of Science ®Google Scholar
• Lafont V, Sanchez F, Laprevotte E, Michaud HA, Gros L, et al.: Plasticity of γδ T cells: Impact on the anti-tumor response. Front Immunol 5, 622, 2014.
   PubMed Web of Science ®Google Scholar
• Ma C, Zhang Q, Ye J, Wang F, Zhang Y, et al.: Tumor-infiltrating γδ T lymphocytes predict clinical outcome in human breast cancer. J Immunol 189, 5029–5036, 2012.
   PubMed Web of Science ®Google Scholar
• Castiglione F, Taddei A, Buccoliero AM, Garbini F, Gheri CF, et al.: TNM staging and T-cell receptor gamma expression in colon adenocarcinoma. Correlation with disease progression? Tumori 94, 384–388, 2008.
   PubMed Web of Science ®Google Scholar
• Iwami D, Nonomura K, Shirasugi N, and Niimi M: Immunomodulatory effects of eicosapentaenoic acid through induction of regulatory T cells. Int Immunopharmacol 11, 384–389, 2011.
   PubMed Web of Science ®Google Scholar
• Sarotra P, Sharma G, Kansal S, Negi AK, Aggarwal R, et al.: Chemopreventive effect of different ratios of fish oil and corn oil in experimental colon carcinogenesis. Lipids 45, 785–798, 2010.
   PubMed Web of Science ®Google Scholar
• Sarotra P, Kansal S, Sandhir R, and Agnihotri N: Chemopreventive effect of different ratios of fish oil and corn oil on prognostic markers, DNA damage and cell cycle in colon carcinogenesis. Eur J Cancer Prev 21, 147–154, 2012.
   PubMed Web of Science ®Google Scholar
• Kansal S, Negi A, Bhatnagar A, and Agnihotri N: Ras signaling pathway in the chemopreventive action of different ratios of fish oil and corn oil in experimentally induced colon carcinogenesis. Nutr Cancer 64, 559–568, 2012.
   PubMed Web of Science ®Google Scholar
• Ly LH, Smith R, Chapkin RS, and McMurray DN: Dietary n-3 polyunsaturated fatty acids suppress splenic CD4(+) T cell function in interleukin (IL)-10(−/−) mice. Clin Exp Immunol 139, 202–209, 2005.
   PubMed Web of Science ®Google Scholar
• Chapkin RS, McMurray DN, and Lupton JR: Colon cancer, fatty acids and anti-inflammatory compounds. Curr Opin Gastroenterol 23, 48–54, 2007.
   PubMed Web of Science ®Google Scholar
• Yessoufou A, Plé A, Moutairou K, Hichami A, and Akhtar KN: Docosahexaenoic acid reduces suppressive and migratory functions of CD4+ CD25+ regulatory T-cells. J Lipid Res 50, 2377–2388, 2009.
   PubMed Web of Science ®Google Scholar
• Committee on Laboratory Animal Diets: Control of diets in laboratory animal experimentation. National Academy of Sciences, Washington, DC, 1978.
   Google Scholar
• Poussier P and Julius M: Thymus independent T cell development and selection in the intestinal epithelium. Annu Rev Immunol 12, 521–553, 1994.
   PubMed Web of Science ®Google Scholar
• Freshney RI: Culture of Animal Cells: A Manual of Basic Tecnique. Wiley-Liss, NY. 5th edition, 1994.
   Google Scholar
• Wilson R and Sargent JR: High resolution separation of polyunsaturated fatty acids by argentation thin-layer chromatography. J Chromatograph 623, 403–407, 1992.
   Web of Science ®Google Scholar
• Veldhoen M and Brucklacher-Waldert V: Dietary influences on intestinal immunity. Nat Rev Immunol 12, 696–708, 2012.
   PubMed Web of Science ®Google Scholar
• Clarke SL, Betts GJ, Plant A, Wright KL, El-Shanawany TM, et al.: CD4 + CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS One 27, 1:e129, 2006.
   Web of Science ®Google Scholar
• Frey DM, Droeser RA, Viehl CT, Zlobec I, Lugli A, et al.: High frequency of tumour-infiltrating FOXP3+ regulatory T cells predicts improved survival in mismatch repair-proficient colorectal cancer patients. Int J Cancer 126, 2635–2643, 2010.
   PubMed Web of Science ®Google Scholar
• Whiteside TL, Schuler P, and Schilling B: Induced and natural regulatory T cells in human cancer. Expert Opin Biol Ther 12, 1383–1397, 2012.
   PubMed Web of Science ®Google Scholar
• Raghavan S and Quiding-Järbrink M: Regulatory T cells in gastrointestinal tumours. Expert Rev Gastroenterol Hepatol 5, 489–501, 2011.
   PubMed Web of Science ®Google Scholar
• Erdman SE, Rao VP, Poutahidis T, Ihrig MM, Ge Z, et al.: CD4(+)CD25(+) regulatory lymphocytes require interleukin 10 to interrupt colon carcinogenesis in mice. Cancer Res 15, 6042–6050, 2003.
   Google Scholar
• Woodworth HL, McCaskey SJ, Duriancik DM, Clinthorne JF, Langohr IM, et al.: Dietary fish oil alters T lymphocyte cell populations and exacerbates disease in a mouse model of inflammatory colitis. Cancer Res 70, 7960–7969, 2010.
   PubMed Web of Science ®Google Scholar
• Han SC, Koo DH, Kang NJ, Yoon WJ, Kang GJ, et al.: Docosahexaenoic acid alleviates atopic dermatitis by generating Tregs and IL-10/TGF-β-modified macrophages via a TGF-β-dependent mechanism. J Invest Dermatol 135, 1556–1564, 2015.
   PubMed Web of Science ®Google Scholar
• Marincola FM, Jaffee EM, Hicklin DJ, and Ferrone S: Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance. Adv Immunol 74, 181–273, 2000.
   PubMedGoogle Scholar
• Yang L and Carbone DP: Tumor-host immune interactions and dendritic cell dysfunction. Adv Cancer Res 92, 13–27, 2004.
   PubMed Web of Science ®Google Scholar
• Hamidullah Changkija B and Konwar R: Role of interleukin-10 in breast cancer. Breast Cancer Res Treat 133, 11–21, 2012.
   PubMed Web of Science ®Google Scholar
• Sredni B, Weil M, Khomenok G, Lebenthal I, Teitz S, et al.: Ammonium trichloro(dioxoethylene-o,o’)tellurate (AS101) sensitizes tumors to chemotherapy by inhibiting the tumor interleukin 10 autocrine loop. Cancer Res 64, 1843–1852, 2004.
   PubMed Web of Science ®Google Scholar
• Alas S, Emmanouilides C, and Bonavida B: Inhibition of interleukin 10 by rituximab results in down-regulation of bcl-2 and sensitization of B-cell non-Hodgkin's lymphoma to apoptosis. Clin Cancer Res 7, 709–723, 2001.
   PubMed Web of Science ®Google Scholar
• Bohlen H, Kessler M, Sextro M, Diehl V, and Tesch H: Poor clinical outcome of patients with Hodgkin's disease and elevated interleukin-10 serum levels. Clinical significance of interleukin-10 serum levels for Hodgkin's disease. Ann Hematol 79, 110–113, 2000.
   PubMed Web of Science ®Google Scholar
• Lech-Maranda E, Baseggio L, Bienvenu J, Charlot C, Berger F, et al.: Interleukin-10 gene promoter polymorphisms influence the clinical outcome of diffuse large B-cell lymphoma. Blood 103, 3529–3534, 2004.
   PubMed Web of Science ®Google Scholar
• Nemunaitis J, Fong T, Shabe P, Martineau D, and Ando D: Comparison of serum interleukin-10 (IL-10) levels between normal volunteers and patients with advanced melanoma. Cancer Invest 19, 239–247, 2001.
   PubMed Web of Science ®Google Scholar
• Chau GY, Wu CW, Lui WY, Chang TJ, Kao HL, et al.: Serum interleukin-10 but not interleukin-6 is related to clinical outcome in patients with resectable hepatocellular carcinoma. Ann Surg 231, 552–558, 2000.
   PubMed Web of Science ®Google Scholar
• Mapara MY and Sykes M: Tolerance and cancer: mechanisms of tumor evasion and strategies for breaking tolerance. J Clin. Oncol 22, 1136–1151, 2004.
   PubMed Web of Science ®Google Scholar
• Wang X, Li W, Zhang F, Pan L, Li N, and Li J: Fish oil–supplemented parenteral nutrition in severe acute pancreatitis patients and effects on immune function and infectious risk: a randomized controlled trial. Inflammation 32, 304–309, 2009.
   PubMed Web of Science ®Google Scholar
• Kansal S, Vaiphei K, and Agnihotri N: Alterations in lipid mediated signaling and Wnt/β-catenin signaling in DMH induced colon cancer on supplementation of fish oil. BioMed Res Int 2014, 832025, 2014.
   PubMed Web of Science ®Google Scholar
• Moon Y and Pestka JJ: Deoxynivalenol-induced mitogen-activated protein kinase phosphorylation and IL-6 expression in mice suppressed by fish oil. JNB 14, 717–726, 2003.
   Google Scholar
• Balkwill FR and Mantovani A: Cancer-related inflammation: Common themes and therapeutic opportunities. Seminars Cancer Biol 22, 33–40, 2012.
   PubMed Web of Science ®Google Scholar
• Scheller J, Ohnesorge N, and Rose-John S: Interleukin-6 trans-signalling in chronic inflammation and cancer. Scand J Immunol 63, 321–329, 2006.
   PubMed Web of Science ®Google Scholar
• Presti LE, Dieli F, and Meraviglia S: Tumor-Infiltrating γδ T Lymphocytes: pathogenic role, clinical significance, and differential programing in the tumor microenvironment. Front Immunol 24, 5:607, 2014.
   Google Scholar
• Corvaisier M, Moreau-Aubry A, Diez E, Bennouna J, Mosnier JF, Scotet E, et al.: Vγ9 Vδ2 T cell response to colon carcinoma cells. J Immunol 175, 5481–5488, 2005.
   PubMed Web of Science ®Google Scholar
• Watanabe N, Hizuta A, Tanaka N, Orita K: Localization of T cell receptor (TCR)-gamma delta + T cells into human colorectal cancer: flow cytometric analysis of TCR-gamma delta expression in tumour-infiltrating lymphocytes. Clin Exp Immunol 102, 167–73, 1995.
   PubMed Web of Science ®Google Scholar
• Schüle JM, Leif B, Håkansson L, Gustafsson B, and Håkansson A: CD28 expression in sentinel node biopsies from breast cancer patients in comparison with CD3-ζ chain expression. J Translation Med 2, 45, 2004.
   PubMedGoogle Scholar
• Shaikh SR and Edidin M: Polyunsaturated fatty acids, membrane organization, T cells, and antigen presentation. Am J Clin Nutr 84, 1277–1289, 2006.
   PubMed Web of Science ®Google Scholar