Circulating Regulatory T Cells in Endometrial Cancer: A Role for Age and Menopausal Status

REFERENCES

• Arruvito, L., Sanz, M., Banham, A. H., Fainboim, L. (2007). Expansion of CD4+CD25+and FOXP3+ Regulatory T cells during the follicular phase of the menstrual cycle: Implications for human reproduction. J. Immunol. 178:2572–2578.
   PubMed Web of Science ®Google Scholar
• Bacchetta, R., Gambineri, E., Roncarolo, M.-G. (2007). Role of regulatory T cells and FOXP3 in human diseases. J. Allergy Clin. Immunol. 120:227.
   PubMed Web of Science ®Google Scholar
• Baecher-Allan, C., Brown, J. A., Freeman, G. J., Hafler, D. A. (2001). CD4+CD25 high regulatory cells in human peripheral blood. J. Immunol. 167:1245–1253.
   PubMed Web of Science ®Google Scholar
• Berendt, M. J., North, R. J. (1980). T-cell-mediated suppression of anti-tumor immunity. An explanation for progressive growth of an immunogenic tumor. J. Exp. Med. 151:69–80.
   PubMed Web of Science ®Google Scholar
• Beyer, M., Kochanek, M., Giese, T., Endl, E., Weihrauch, M. R., Knolle, P. A., Classen, S., Schultze, J. L. (2006). In vivo peripheral expansion of naive CD4+CD25high FoxP3+ regulatory T cells in patients with multiple myeloma. Blood 107:3940–3949.
   PubMed Web of Science ®Google Scholar
• Bursuker, I., North, R. J. (1984). Generation and decay of the immune response to a progressive fibrosarcoma. II. Failure to demonstrate postexcision immunity after the onset of T cell-mediated suppression of immunity. J. Exp. Med. 159:1312–1321.
   Google Scholar
• Carr, M. (2003). The emergence of the metabolic syndrome with menopause. J. Clin. Endocrinol. Metabol. 88:2404.
   PubMed Web of Science ®Google Scholar
• de Jong, R. A., Leffers, N., Boezen, H. M., ten Hoor, K. A., van der Zee, A. G. J., Hollema, H., Nijman, H. W. (2009). Presence of tumor-infiltrating lymphocytes is an independent prognostic factor in type I and II endometrial cancer. Gynecol. Oncol 114:105.
   PubMed Web of Science ®Google Scholar
• Dejaco, C., Duftner, C., Schirmer, M. (2006). Are regulatory T-cells linked with aging? Exper. Gerontol. 41:339.
   Google Scholar
• Fattorossi, A., Battaglia, A., Ferrandina, G., Buzzonetti, A., Legge, F., Salutari, V., Scambia, G. (2004). Lymphocyte composition of tumor draining lymph nodes from cervical and endometrial cancer patients. Gynecol. Oncol. 92:106.
   Google Scholar
• Feuerer, M., Hill, J. A., Mathis, D., Benoist, C. (2009). Foxp3+ regulatory T cells: differentiation, specification, subphenotypes. Nat. Immunol. 10:689.
   PubMed Web of Science ®Google Scholar
• Fontenot, J., Gavin, M., Rudensky, A., 2003, Foxp3 programs the development and function of CD4+ regulatory T cells. Nat. Immunol. 4:330.
   PubMed Web of Science ®Google Scholar
• Fujimoto, S., Greene, M. and Sehon, A.H., 1974, Immunosuppressor T Cells in tumor bearing hosts. immunological investigations. J. Mol. Cell. Immunol. 4:201–217.
   Google Scholar
• Giatromanolaki, A., Bates, G., Koukourakis, M., Sivridis, E., Gatter, K., Harris, A., Banham, A. (2008). The presence of tumor-infiltrating FOXP3+ lymphocytes correlates with intratumoral angiogenesis in endometrial cancer. Gynecol. Oncol. 110:216.
   PubMed Web of Science ®Google Scholar
• Gregg, R., Smith, C.M., Clark, F.J., Dunnion, D., Khan, N., Chakraverty, R., Nayak, L. and Moss, P.A., 2005, The number of human peripheral blood CD4+ CD25high regulatory T cells increases with age. Clin. Exper. Immunol. 140:540–546.
   PubMed Web of Science ®Google Scholar
• Griffiths, R., Elkord, E., Gilham, D., Ramani, V., Clarke, N., Stern, P., Hawkins, R. (2007). Frequency of regulatory T cells in renal cell carcinoma patients and investigation of correlation with survival. Cancer Immunol. Immunother. 56:1743.
   PubMed Web of Science ®Google Scholar
• Gruver, A. L., Hudson, L. L., Sempowski, G. D. (2007). Immunosenescence of ageing. J. Pathol. 211:144–156.
   PubMed Web of Science ®Google Scholar
• Hori, S., Nomura, T., Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057–1061.
   PubMed Web of Science ®Google Scholar
• Hwang, K.-A., Kim, H.-R., Kang, I. (2009). Aging and human CD4+ regulatory T cells. Mech. Age. Develop. 130:509.
   PubMedGoogle Scholar
• Ichihara, F., Kono, K., Takahashi, A., Kawaida, H., Sugai, H., Fujii, H. (2003). Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers. Clin. Cancer Res. 9:4404.
   PubMed Web of Science ®Google Scholar
• Jacobson, G. F., Shaber, R. E., Armstrong, M. A., Hung, Y.-Y. (2006). Hysterectomy rates for benign indications. Obstet. Gynecol. 107:1278–1283.
   PubMed Web of Science ®Google Scholar
• Jeron, A., Pfoertner, S., Bruder, D., Geffers, R., Hammerer, P., Hofmann, R., Buer, J., Schrader, A. J. (2009). Frequency and gene expression profile of regulatory T cells in renal cell carcinoma. Tumor Biol. 30:160.
   PubMed Web of Science ®Google Scholar
• Kajsa, W., Ann, E., Helen, K., Anna, R., Elisabeth, S.-P. (2002). Characterization of human CD25+ CD4+ T cells in thymus, cord and adult blood. Immunology 106:190–199.
   Google Scholar
• Kallikourdis, M., Betz, A. G. (2007). Periodic Accumulation of regulatory T cells in the uterus: Preparation for the implantation of a semi-allogeneic fetus? PLoS ONE 2:e382.
   PubMed Web of Science ®Google Scholar
• Khong, H., Restifo, N. (2002). Natural selection of tumor variants in the generation of “tumor escape” phenotypes. Nat. Immunol. 3:999.
   PubMed Web of Science ®Google Scholar
• Kitchener, H. (2006). Management of endometrial cancer. Euro. J. Surg. Oncol. 32:838–843.
   Google Scholar
• Kondratiev, S., Sabo, E., Yakirevich, E., Lavie, O., Resnick, M. (2004). Intratumoral CD8+ T lymphocytes as a prognostic factor of survival in endometrial carcinoma. Clin. Cancer Res. 10:44–50.
   Google Scholar
• Kono, K., Kawaida, H., Takahashi, A., Sugai, H., Mimura, K., Miyagawa, N., Omata, H. and Fujii, H., 2006, CD4(+)CD25high regulatory T cells increase with tumor stage in patients with gastric and esophageal cancers. Cancer Immunol. Immunother. 55, 1064.
   PubMed Web of Science ®Google Scholar
• Kryczek, I., Liu, R., Wang, G., Wu, K., Shu, X., Szeliga, W., Vatan, L., Finlayson, E., Huang, E., Simeone, D., Redman, B., Welling, T., Chang, A. and Zou, W. (2009). FOXP3 defines regulatory T cells in human tumor and autoimmune disease. Cancer Res. 69:3995.
   PubMedGoogle Scholar
• Ling, K., Pratap, S., Bates, G., Singh, B., Mortensen, N., George, B., Warren, B., Piris, J., Roncador, G., Fox, S., Banham, A., Cerundolo, V. (2007). Increased frequency of regulatory T cells in peripheral blood and tumour infiltrating lymphocytes in colorectal cancer patients. Cancer Immun. 7:7.
   PubMedGoogle Scholar
• Liu, W., Putnam, A. L., Xu-Yu, Z., Szot, G. L., Lee, M. R., Zhu, S., Gottlieb, P. A., Kapranov, P., Gingeras, T. R., de St. Groth, B. F., Clayberger, C., Soper, D. M., Ziegler, S. F., Bluestone, J. A. (2006). CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J. Exp. Med. 203:1701–1711.
   PubMed Web of Science ®Google Scholar
• Liyanage, U. K., Moore, T. T., Joo, H.-G., Tanaka, Y., Herrmann, V., Doherty, G., Drebin, J. A., Strasberg, S. M., Eberlein, T. J., Goedegebuure, P. S., Linehan, D. C. (2002). Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma. J. Immunol. 169:2756–2761.
   PubMed Web of Science ®Google Scholar
• Lobo, R. (2008). Metabolic syndrome after menopause and the role of hormones. Maturitas 60:10.
   PubMed Web of Science ®Google Scholar
• Lu, L.-F., Rudensky, A. (2009). Molecular orchestration of differentiation and function of regulatory T cells. Genes Develop. 23:1270–1282.
   PubMedGoogle Scholar
• Mandapathil, M., Lang, S., Gorelik, E., Whiteside, T. L. (2009). Isolation of functional human regulatory T cells (Treg) from the peripheral blood based on the CD39 expression. J. Immunol. Meth. 346:55.
   PubMed Web of Science ®Google Scholar
• Mao, C., Wang, S., Jiang, Q., Tong, J., Ma, J., Yang, M., Xu, X., Qiu, G., Shao, Q., Li, L., Xu, H. (2008). Increased CD4+CD25+FOXP3+ regulatory T cells in cancer patients from conversion of CD4+CD25- T cells through tumor-derived factors. Onkologie 31:243.
   PubMedGoogle Scholar
• Montejo, M., Werner, T. L., Gaffney, D. (2009). Current challenges in clinical management of endometrial cancer. Adv. Drug Deliv. Rev. 61:883.
   Google Scholar
• North, R. J., Bursuker, I. (1984). Generation and decay of the immune response to a progressive fibrosarcoma. I. Ly-1+2- suppressor T cells down-regulate the generation of Ly-1-2+ effector T cells. J. Exp. Med. 159:1295–1311.
   PubMed Web of Science ®Google Scholar
• Ormandy, L. A., Hillemann, T., Wedemeyer, H., Manns, M. P., Greten, T. F., Korangy, F. (2005). Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma. Cancer Res. 65:2457–2464.
   PubMed Web of Science ®Google Scholar
• Prieto, G. A., Rosenstein, Y. (2006). Oestradiol potentiates the suppressive function of human CD4 CD25 regulatory T cells by promoting their proliferation. Immunology 118:58.
   PubMed Web of Science ®Google Scholar
• Quinn, M., Babb, P., Brock, A., Kirby, L. and Jones, J. (2001) Cancer trends in England and Wales 1950–1999. In: Studies on Medical and Population Subjects Vol. No. 66. The office for National Statistics, http://www.statistics.gov.uk/downloads/theme_health/cancertrends_5099.pdf
   Google Scholar
• Rech, A., Mick, R., Kaplan, D., Chang, K.-M., Domchek, S., Vonderheide, R. (2010). Homeostasis of peripheral FoxP3+ CD4+ regulatory T cells in patients with early and late stage breast cancer. Cancer Immunol. Immunother. 59:599.
   PubMed Web of Science ®Google Scholar
• Sakaguchi, S. (2004). Naturally arising CD4+ Regulatory T cells for immunologic self‐tolerance and negative control of immune responses. Ann. Rev. Immunol. 22:531–562.
   PubMed Web of Science ®Google Scholar
• Saltzman, B. S., Doherty, J. A., Hill, D. A., Beresford, S. A., Voigt, L. F., Chen, C., Weiss, N. S. (2008). Diabetes and endometrial cancer: An evaluation of the modifying effects of other known risk factors. Am. J. Epidemiol 167:607–614.
   PubMed Web of Science ®Google Scholar
• Santner-Nanan, B., Seddiki, N., Zhu, E., Quent, V., Kelleher, A., Fazekas de St Groth, B., Nanan, R., (2008). Accelerated age-dependent transition of human regulatory T cells to effector memory phenotype. Inter. Immunol. 20:375.
   Google Scholar
• Schaefer, C., Kim, G. G., Albers, A., Hoermann, K., Myers, E. N., Whiteside, T. L. (2005). Characteristics of CD4+CD25+ regulatory T cells in the peripheral circulation of patients with head and neck cancer. Br. J. Cancer 92:913.
   PubMed Web of Science ®Google Scholar
• Shen, L.-S., Wang, J., Shen, D.-F., Yuan, X.-L., Dong, P., Li, M.-X., Xue, J., Zhang, F.-M., Ge, H.-L. Xu, D. (2009). CD4+CD25+CD127low/- regulatory T cells express Foxp3 and suppress effector T cell proliferation and contribute to gastric cancers progression. Clin. Immunol. 131:109.
   PubMed Web of Science ®Google Scholar
• Somasundaram, R., Jacob, L., Swoboda, R., Caputo, L., Song, H., Basak, S., Monos, D., Peritt, D., Marincola, F., Cai, D., Birebent, B., Bloome, E., Kim, J., Berencsi, K., Mastrangelo, M., Herlyn, D. (2002). Inhibition of cytolytic T lymphocyte proliferation by autologous CD4+/CD25+ regulatory T cells in a colorectal carcinoma patient is mediated by transforming growth factor-{beta}. Cancer Res. 62:5267–5272.
   PubMed Web of Science ®Google Scholar
• Stanzer, S., Dandachi, N., Balic, M., Resel, M., Samonigg, H., Bauernhofer, T. (2008). Resistance to apoptosis and expansion of regulatory T cells in relation to the detection of circulating tumor cells in patients with metastatic epithelial cancer. J. Clin. Immunol. 28:107.
   Google Scholar
• Straub, R. (2007). The complex role of estrogens in inflammation. Endocr. Rev. 28:521.
   PubMed Web of Science ®Google Scholar
• Szczepanski, M. J., Szajnik, M., Czystowska, M., Mandapathil, M., Strauss, L., Welsh, A., Foon, K. A., Whiteside, T. L., Boyiadzis, M. (2009). Increased frequency and suppression by regulatory T cells in patients with acute myelogenous leukemia. Clin. Cancer Res 15:3325–3332.
   PubMed Web of Science ®Google Scholar
• Tetsuro, S., Motohide, K., Yuka, Y., Michiyuki, K., Arimichi, T. (2003). CD4+ CD25+ regulatory T cells in patients with gastrointestinal malignancies. Cancer 98:1089–1099.
   Google Scholar
• Trzonkowski, P. (2009) Role of Regulatory Subsets During Aging. In: T. Fulop, C. Franceschi, K. Hirokawa, G. Pawelec and P. Trzonkowski ( Eds), Handbook on Immunosenescence: Basic Understanding and Clinical Applications. Springer Netherlands, p. 343.
   Google Scholar
• Trzonkowski, P., Szmit, E., Mysliwska, J., Mysliwski, A. (2006). CD4+CD25+ T regulatory cells inhibit cytotoxic activity of CTL and NK cells in humans—impact of immunosenescence. Clin. Immunol. 119:307.
   Google Scholar
• Tsaknaridis, L., Spencer, L., Culbertson, N., Hicks, K., LaTocha, D., Chou, Y. K., Whitham, R. H., Bakke, A., Jones, R. E., Offner, H., Bourdette, D. N., Vandenbark, A. A. (2003). Functional assay for human CD4+CD25+ Treg cells reveals an age‐dependent loss of suppressive activity. J. Neurosci. Res. 74:296–308.
   PubMed Web of Science ®Google Scholar
• Viguier, M., Lemaitre, F., Verola, O., Cho, M.-S., Gorochov, G., Dubertret, L., Bachelez, H., Kourilsky, P., Ferradini, L. (2004). 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. 173:1444–1453.
   PubMed Web of Science ®Google Scholar
• Vikman, S., Sommaggio, R., De La Torre, M., Öberg, K., Essand, M., Giandomenico, V., Loskog, A., Ãtterman, T. H. (2009). Midgut carcinoid patients display increased numbers of regulatory T cells in peripheral blood with infiltration into tumor tissue. Acta Oncol. 48:391–400.
   PubMed Web of Science ®Google Scholar
• Wolf, A.M., Wolf, D., Steurer, M., Gastl, G., Gunsilius, E. and Grubeck-Loebenstein, B., 2003, Increase of regulatory T cells in the peripheral blood of cancer patients. Clin. Cancer Res. 9: 606–612.
   PubMed Web of Science ®Google Scholar
• Woo, E. Y., Chu, C. S., Goletz, T. J., Schlienger, K., Yeh, H., Coukos, G., Rubin, S. C., Kaiser, L. R. and June, C. H. (2001). Regulatory CD4+CD25+ T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res. 61:4766–4772.
   PubMed Web of Science ®Google Scholar
• Woo, E. Y., Yeh, H., Chu, C. S., Schlienger, K., Carroll, R. G., Riley, J. L., Kaiser, L. R., June, C. H. (2002). Cutting edge: Regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J. Immunol. 168:4272–4276.
   PubMed Web of Science ®Google Scholar
• Yokokawa, J., Cereda, V., Remondo, C., Gulley, J. L., Arlen, P. M., Schlom, J., Tsang, K. Y. (2008). Enhanced Functionality of CD4+CD25highFoxP3+ regulatory T cells in the peripheral blood of patients with prostate cancer. Clin. Cancer Res. 14:1032–1040.
   PubMed Web of Science ®Google Scholar
• Zhang, L., Zhao, Y. (2007). The regulation of Foxp3 expression in regulatory CD4+CD25+ T cells: Multiple pathways on the road. J. Cell. Physiol 211:590–597.
   PubMedGoogle Scholar