The ratios of CD8+ T cells to CD4+CD25+ FOXP3+ and FOXP3- T cells correlate with poor clinical outcome in human serous ovarian cancer

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Preston, Claudia C ^a   Maurer, Matthew J ^b   Oberg, Ann L ^b   Visscher, Daniel W ^b   Kalli, Kimberly R ^b   Hartmann, Lynn C ^b   Goode, Ellen L ^b   Knutson, Keith L ^a,c  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c Vaccine and Gene Therapy Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; AGED, 80 AND OVER; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYSTADENOCARCINOMA, SEROUS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; HUMANS; IMMUNOPHENOTYPING; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE COUNT; MIDDLE AGED; OVARIAN NEOPLASMS; OVARY; PROGNOSIS; SURVIVAL ANALYSIS; T-LYMPHOCYTES, REGULATORY;

EID: 84893573894     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080063     Document Type: Article

References (44)

1. Aletti GD, Gallenberg MM, Cliby WA, Jatoi A, Hartmann LC (2007) Current management strategies for ovarian cancer. Mayo Clin Proc 82: 751-770. doi:10.1016/S0025-6196(11)61196-8. PubMed: 17550756. (Pubitemid 46878099)
2. Cannistra SA (2004) Cancer of the ovary. N Engl J Med 351: 2519-2529. doi:10.1056/NEJMra041842. PubMed: 15590954.
3. Ozols RF, Bundy BN, Greer BE, Fowler JM, Clarke-Pearson D et al. (2003) Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a Gynecologic Oncology Group study. J Clin Oncol 21: 3194-3200. doi:10.1200/JCO.2003.02.153. PubMed: 12860964. (Pubitemid 46606249)
4. Hoskins P, Vergote I, Cervantes A, Tu D, Stuart G et al. (2010) Advanced ovarian cancer: phase III randomized study of sequential cisplatin-topotecan and carboplatin-paclitaxel vs carboplatin-paclitaxel. J Natl Cancer Inst 102: 1547-1556. doi:10.1093/jnci/djq362. PubMed: 20937992.
5. Trimble EL, Birrer MJ, Hoskins WJ, Marth C, Petryshyn R et al. (2010) Current academic clinical trials in ovarian cancer: Gynecologic Cancer InterGroup and US National Cancer Institute Clinical Trials Planning Meeting, May 2009. Int J Gynecol Cancer 20: 1290-1298. doi:10.1111/IGC.0b013e3181ee1c01. PubMed: 21151709.
6. Winter WE 3rd, Maxwell GL, Tian C, Carlson JW, Ozols RF, et al. (2007) Prognostic factors for stage III epithelial ovarian cancer: a Gynecologic Oncology Group Study. J Clin Oncol 25: 3621-3627. doi: 10.1200/JCO.2006.10.2517. PubMed: 17704411. (Pubitemid 47372600)
7. Zhang L, Conejo-Garcia JR, Katsaros D, Gimotty PA, Massobrio M et al. (2003) Intratumoral T cells, recurrence, and survival in epithelial ovarian cancer. N Engl J Med 348: 203-213. doi:10.1056/NEJMoa020177. PubMed: 12529460. (Pubitemid 36077915)
8. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H et al. (2005) Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/ regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc Natl Acad Sci U S A 102: 18538-18543. doi: 10.1073/pnas.0509182102. PubMed: 16344461. (Pubitemid 43011261)
9. Coleman S, Clayton A, Mason MD, Jasani B, Adams M et al. (2005) Recovery of CD8+ T-cell function during systemic chemotherapy in advanced ovarian cancer. Cancer Res 65: 7000-7006. doi: 10.1158/0008-5472.CAN-04-3792. PubMed: 16061686. (Pubitemid 41060740)
10. Ho M, Hassan R, Zhang J, Wang QC, Onda M et al. (2005) Humoral immune response to mesothelin in mesothelioma and ovarian cancer patients. Clin Cancer Res 11: 3814-3820. doi: 10.1158/1078-0432.CCR-04-2304. PubMed: 15897581. (Pubitemid 40685601)
11. Goodell V, Salazar LG, Urban N, Drescher CW, Gray H et al. (2006) Antibody immunity to the p53 oncogenic protein is a prognostic indicator in ovarian cancer. J Clin Oncol 24: 762-768. doi:10.1200/JCO.2005.03.2813. PubMed: 16391298. (Pubitemid 46622043)
12. Preston CC, Goode EL, Hartmann LC, Kalli KR, Knutson KL (2011) Immunity and immune suppression in human ovarian cancer. J Immunother 3: 539-556. doi:10.2217/imt.11.20. PubMed: 21463194.
13. Chen F, Hou M, Ye F, Lv W, Xie X (2009) Ovarian cancer cells induce peripheral mature dendritic cells to differentiate into macrophagelike cells in vitro. Int J Gynecol Cancer 19: 1487-1493. doi:10.1111/IGC.0b013e3181bb70c6. PubMed: 19955923.
14. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P et al. (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10: 942-949. doi: 10.1038/nm1093. PubMed: 15322536. (Pubitemid 39273735)
15. Li X, Ye DF, Xie X, Chen HZ, Lu WG (2005) Proportion of CD4+CD25+ regulatory T cell is increased in the patients with ovarian carcinoma. Cancer Invest 23: 399-403. doi:10.1081/CNV-200067142. PubMed: 16193639. (Pubitemid 41324357)
16. Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4: 330-336. doi:10.1038/ni904. PubMed: 12612578. (Pubitemid 36432314)
17. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299: 1057-1061. doi:10.1126/science.1079490. PubMed: 12522256. (Pubitemid 36222930)
18. Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY (2005) A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 6: 1142-1151. doi:10.1038/ni1263. PubMed: 16227984. (Pubitemid 41541792)
19. Setoguchi R, Hori S, Takahashi T, Sakaguchi S (2005) Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 201: 723-735. doi:10.1084/jem.20041982. PubMed: 15753206. (Pubitemid 40395118)
20. Milne K, Köbel M, Kalloger SE, Barnes RO, Gao D et al. (2009) Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PLOS ONE 4: e6412. doi:10.1371/journal.pone.0006412. PubMed: 19641607.
21. Ladoire S, Mignot G, Dalban C, Chevriaux A, Arnould L et al. (2012) FOXP3 expression in cancer cells and anthracyclines efficacy in patients with primary breast cancer treated with adjuvant chemotherapy in the phase III UNICANCER-PACS 01 trial. Ann Oncol 23: 2552-2561. doi:10.1093/annonc/mds028. PubMed: 22431701.
22. Noh J, Noh G, Kim HS, Kim AR, Choi WS (2012) Allergen-specific responses of CD19(+)CD5(+)Foxp3(+) regulatory B cells (Bregs) and CD4(+)Foxp3(+) regulatory T cell (Tregs) in immune tolerance of cow milk allergy of late eczematous reactions. Cell Immunol 274: 109-114. doi:10.1016/j.cellimm.2012.01. 005. PubMed: 22398308.
23. Kryczek I, Liu R, Wang G, Wu K, Shu X et al. (2009) FOXP3 defines regulatory T cells in human tumor and autoimmune disease. Cancer Res 69: 3995-4000. doi:10.1158/0008-5472.CAN-08-3804. PubMed: 19383912.
24. Knutson KL, Dang Y, Lu H, Lukas J, Almand B et al. (2006) IL-2 immunotoxin therapy modulates tumor-associated regulatory T cells and leads to lasting immune-mediated rejection of breast cancers in neu-transgenic mice. J Immunol 177: 84-91. PubMed: 16785502. (Pubitemid 43939119)
25. Knutson KL, Almand B, Dang Y, Disis ML (2004) Neu antigen-negative variants can be generated after neu-specific antibody therapy in neu transgenic mice. Cancer Res 64: 1146-1151. doi: 10.1158/0008-5472.CAN-03-0173. PubMed: 14871850. (Pubitemid 38176922)
26. Valitutti S, Müller S, Salio M, Lanzavecchia A (1997) Degradation of T cell receptor (TCR)-CD3-zeta complexes after antigenic stimulation. J Exp Med 185: 1859-1864. doi:10.1084/jem.185.10.1859. PubMed: 9151711. (Pubitemid 27242207)
27. Ebert EC (2003) Activation of human intraepithelial lymphocytes reduces CD3 expression. Clin Exp Immunol 132: 424-429. doi: 10.1046/j.1365-2249.2003. 02156.x. PubMed: 12780688.
28. Sinicrope FA, Rego RL, Ansell SM, Knutson KL, Foster NR et al. (2009) Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 137: 1270-1279. doi:10.1053/j.gastro.2009.06.053. PubMed: 19577568.
29. Facciabene A, Motz GT, Coukos G (2012) T-regulatory cells: key players in tumor immune escape and angiogenesis. Cancer Res 72: 2162-2171. doi:10.1158/1538-7445.AM2012-2162. PubMed: 22549946.
30. Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY et al. (2007) Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 25: 2586-2593. doi:10.1200/JCO.2006.09.4565. PubMed: 17577038. (Pubitemid 47041232)
31. Knutson KL, Disis ML, Salazar LG (2007) CD4 regulatory T cells in human cancer pathogenesis. Cancer Immunol Immunother 56: 271-285. PubMed: 16819631. (Pubitemid 46035899)
32. Zou W (2006) Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol 6: 295-307. doi:10.1038/nri1806. PubMed: 16557261.
33. Quezada SA, Peggs KS, Curran MA, Allison JP (2006) CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J Clin Invest 116: 1935-1945. doi:10.1172/JCI27745. PubMed: 16778987. (Pubitemid 44033317)
34. Lipson EJ, Drake CG (2011) Ipilimumab: an anti-CTLA-4 antibody for metastatic melanoma. Clin Cancer Res 17: 6958-6962. doi: 10.1158/1078-0432.CCR- 11-1595. PubMed: 21900389.
35. Ziegler SF (2006) FOXP3: of mice and men. Annu Rev Immunol 24: 209-226. doi:10.1146/annurev.immunol.24.021605.090547. PubMed: 16551248.
36. Walker MR, Kasprowicz DJ, Gersuk VH, Benard A, Van Landeghen M et al. (2003) Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J Clin Invest 112: 1437-1443. doi:10.1172/ JCI200319441. PubMed: 14597769. (Pubitemid 38057697)
37. Walker MR, Carson BD, Nepom GT, Ziegler SF, Buckner JH (2005) De novo generation of antigen-specific CD4+CD25+ regulatory T cells from human CD4+CD25- cells. Proc Natl Acad Sci U S A 102: 4103-4108. doi:10.1073/pnas.0407691102. PubMed: 15753318. (Pubitemid 40388562)
38. Magg T, Mannert J, Ellwart JW, Schmid I, Albert MH (2012) Subcellular localization of FOXP3 in human regulatory and nonregulatory T cells. Eur J Immunol 42: 1627-1638. doi:10.1002/eji.201141838. PubMed: 22678915.
39. Pot C, Apetoh L, Kuchroo VK (2011) Type 1 regulatory T cells (Tr1) in autoimmunity. Semin Immunol 23: 202-208. doi:10.1016/j.smim. 2011.07.005. PubMed: 21840222.
40. Chen W, Jin W, Hardegen N, Lei KJ, Li L et al. (2003) Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198: 1875-1886. doi:10.1084/jem.20030152. PubMed: 14676299. (Pubitemid 38032120)
41. Davidson TS, DiPaolo RJ, Andersson J, Shevach EM (2007) Cutting Edge: IL-2 is essential for TGF-beta-mediated induction of Foxp3+ T regulatory cells. J Immunol 178: 4022-4026. PubMed: 17371955. (Pubitemid 46492349)
42. DiPaolo RJ, Brinster C, Davidson TS, Andersson J, Glass D et al. (2007) Autoantigen-specific TGFbeta-induced Foxp3+ regulatory T cells prevent autoimmunity by inhibiting dendritic cells from activating autoreactive T cells. J Immunol 179: 4685-4693. PubMed: 17878367.
43. Siddiqui SA, Frigola X, Bonne-Annee S, Mercader M, Kuntz SM et al. (2007) Tumor-infiltrating Foxp3-CD4+CD25+ T cells predict poor survival in renal cell carcinoma. Clin Cancer Res 13: 2075-2081. doi: 10.1158/1078-0432.CCR-06-2139. PubMed: 17404089. (Pubitemid 46649875)
44. Köbel M, Kalloger SE, Boyd N, McKinney S, Mehl E et al. (2008) Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLOS Med 5: e232. doi:10.1371/journal.pmed. 0050232. PubMed: 19053170.