Circulating regulatory T cells in endometrial cancer: A role for age and menopausal status

Immunological Investigations

Volumn 40, Issue 1, 2011, Pages 62-75

  Sawan, Saladin ^a,b   Burt, Deborah J ^b   Stern, Peter L ^b   Holland, Cathrine ^a   Elkord, Eyad ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Age; Endometrial cancer; Menopause; Treg cells

Indexed keywords

ADULT; AGE; AGED; ARTICLE; BENIGN TUMOR; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOMETRIUM CANCER; FEMALE; FLOW CYTOMETRY; HUMAN; HYSTERECTOMY; MENOPAUSE; POSTMENOPAUSE; PREMENOPAUSE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ADULT; AGED; AGED, 80 AND OVER; AGING; ANTIGENS, CD4; ENDOMETRIAL NEOPLASMS; FEMALE; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; HYSTERECTOMY; LYMPHOCYTE COUNT; MENOPAUSE; MIDDLE AGED; POSTMENOPAUSE; PREMENOPAUSE; T-LYMPHOCYTES, REGULATORY;

EID: 78650071023     PISSN: 08820139     EISSN: 15324311     Source Type: Journal    
DOI: 10.3109/08820139.2010.513022     Document Type: Article

References (62)

1. 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.
2. Bacchetta, R., Gambineri, E., Roncarolo, M.-G. (2007). Role of regulatory T cells and FOXP3 in human diseases.J. Allergy Clin. Immunol. 120:227.
3. 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.
4. 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.
5. 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.
6. 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.
7. Carr, M. (2003). The emergence of the metabolic syndrome with menopause.J. Clin. Endocrinol. Metabol. 88:2404.
8. 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.
9. Dejaco, C., Duftner, C., Schirmer, M. (2006). Are regulatory T-cells linked with aging? Exper. Gerontol. 41:339.
10. 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.
11. Feuerer, M., Hill, J.A., Mathis, D., Benoist, C. (2009). Foxp3+ regulatory T cells: Differentiation, specification, subphenotypes. Nat. Immunol. 10:689.
12. Fontenot, J., Gavin, M., Rudensky, A., 2003, Foxp3 programs the development and function of CD4+ regulatory T cells. Nat. Immunol. 4:330.
13. 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.
14. 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.
15. 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.
16. 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.
17. Gruver, A.L., Hudson, L.L., Sempowski, G.D. (2007). Immunosenescence of ageing.J.Pathol. 211:144-156.
18. Hori, S., Nomura, T., Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057-1061.
19. Hwang, K.-A., Kim, H.-R., Kang, I. (2009). Aging and human CD4+ regulatory T cells.Mech. Age. Develop. 130:509.
20. 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.
21. Jacobson, G.F., Shaber, R.E., Armstrong, M.A., Hung, Y.-Y. (2006). Hysterectomy rates for benign indications. Obstet. Gynecol. 107:1278-1283.
22. 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.
23. 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.
24. 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.
25. Khong, H., Restifo, N. (2002). Natural selection of tumor variants in the generation of "tumor escape" phenotypes. Nat. Immunol. 3:999.
26. Kitchener, H. (2006). Management of endometrial cancer. Euro.J. Surg. Oncol.32:838-843.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. Lobo, R. (2008). Metabolic syndrome after menopause and the role of hormones. Maturitas 60:10.
34. Lu, L.-F., Rudensky, A. (2009). Molecular orchestration of differentiation and function of regulatory T cells. Genes Develop. 23:1270-1282.
35. 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.
36. 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.
37. Montejo, M., Werner, T.L., Gaffney, D. (2009). Current challenges in clinical management of endometrial cancer. Adv. Drug Deliv. Rev. 61:883.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. Straub, R. (2007). The complex role of estrogens in inflammation. Endocr. Rev. 28:521.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. Vikman, S., Sommaggio, R., De La Torre, M., Ã-berg, 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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.