Prognostic role of FOXP3+ regulatory T cells infiltrating human carcinomas: The paradox of colorectal cancer

Cancer Immunology, Immunotherapy

Volumn 60, Issue 7, 2011, Pages 909-918

  Ladoire, Sylvain ^a,b   Martin, François ^a   Ghiringhelli, François ^a,b,c  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b Biologie Moléculaire Centre de Lutte Anti cancereux Georges François Leclerc   (France)

^c Chu   (France)

Author keywords

Colorectal cancer; FOXP3; Immune response; Prognosis; Regulatory T cells

Indexed keywords

TRANSCRIPTION FACTOR FOXP3; TUMOR ANTIGEN;

CANCER GROWTH; CANCER STAGING; CANCER SURVIVAL; CELL DENSITY; CELL INTERACTION; CELLULAR IMMUNITY; COLORECTAL CANCER; DISEASE FREE SURVIVAL; HUMAN; INFLAMMATION; LYMPHOCYTE FUNCTION; LYMPHOCYTIC INFILTRATION; MISMATCH REPAIR; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGNOSIS; REGULATORY T LYMPHOCYTE; REVIEW; SURVIVAL TIME; TH17 CELL;

COLORECTAL NEOPLASMS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; PROGNOSIS; T-LYMPHOCYTES, REGULATORY;

EID: 79959742164     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-011-1046-y     Document Type: Review

References (62)

1. S Sakaguchi N Sakaguchi M Asano M Itoh M Toda 1995 Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases J Immunol 155 1151 1164 7636184 1:CAS:528: DyaK2MXntFWnurs%3D
2. LA Stephens D Mason 2000 CD25 is a marker for CD4+ thymocytes that prevent autoimmune diabetes in rats, but peripheral T cells with this function are found in both CD25+ and CD25- subpopulations J Immunol 165 3105 3110 10975823 1:CAS:528:DC%2BD3cXmslynsbY%3D
3. S Sakaguchi M Miyara CM Costantino DA Hafler 2010 FOXP3+ regulatory T cells in the human immune system Nat Rev Immunol 10 490 500 20559327 10.1038/nri2785 1:CAS:528:DC%2BC3cXnsFKitLY%3D
4. S Hori T Nomura S Sakaguchi 2003 Control of regulatory T cell development by the transcription factor Foxp3 Science 299 1057 1061 12522256 10.1126/science.1079490 1:CAS:528:DC%2BD3sXhtFarsbw%3D (Pubitemid 36222930)
5. UK Liyanage TT Moore HG Joo Y Tanaka V Herrmann G Doherty JA Drebin SM Strasberg TJ Eberlein PS Goedegebuure DC Linehan 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 12193750 1:CAS:528:DC%2BD38XmsF2ns7k%3D (Pubitemid 34921025)
6. TJ Curiel G Coukos L Zou X Alvarez P Cheng P Mottram M Evdemon-Hogan JR Conejo-Garcia L Zhang M Burow Y Zhu S Wei I Kryczek B Daniel A Gordon L Myers A Lackner ML Disis KL Knutson L Chen W Zou 2004 Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival Nat Med 10 942 949 15322536 10.1038/nm1093 1:CAS:528: DC%2BD2cXntFSkt7g%3D (Pubitemid 39273735)
7. F Ghiringhelli N Larmonier E Schmitt A Parcellier D Cathelin C Garrido B Chauffert E Solary B Bonnotte F Martin 2004 CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative Eur J Immunol 34 336 344 14768038 10.1002/eji.200324181 1:CAS:528:DC%2BD2cXhsFals7k%3D (Pubitemid 39255944)
8. SL Clarke GJ Betts A Plant KL Wright TM El-Shanawany R Harrop J Torkington BI Rees GT Williams AM Gallimore AJ Godkin 2006 CD4+CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer PLoS One 1 e129 17205133 10.1371/journal.pone.0000129
9. GJ Bates SB Fox C Han RD Leek JF Garcia AL Harris AH Banham 2006 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 17135638 10.1200/JCO.2006.05.9584 (Pubitemid 46623168)
10. RP Petersen MJ Campa J Sperlazza D Conlon MB Joshi DH Harpole Jr EF Patz Jr 2006 Tumor infiltrating Foxp3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients Cancer 107 2668 2672 10.1002/cncr.22282 (Pubitemid 44937041)
11. Q Gao SJ Qiu J Fan J Zhou XY Wang YS Xiao Y Xu YW Li ZY Tang 2007 Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection J Clin Oncol 25 2586 2593 17577038 10.1200/JCO.2006.09.4565 (Pubitemid 47041232)
12. JF Li YW Chu GM Wang TY Zhu RM Rong J Hou M Xu 2009 The prognostic value of peritumoral regulatory T cells and its correlation with intratumoral cyclooxygenase-2 expression in clear cell renal cell carcinoma BJU Int 103 399 405 19021626 10.1111/j.1464-410X.2008.08151.x
13. N Hiraoka K Onozato T Kosuge S Hirohashi 2006 Prevalence of FOXP3+ regulatory T cells increases during the progression of pancreatic ductal adenocarcinoma and its premalignant lesions Clin Cancer Res 12 5423 5434 17000676 10.1158/1078-0432.CCR-06-0369 1:CAS:528:DC%2BD28XpvFShsLc%3D (Pubitemid 44497257)
14. G Perrone PA Ruffini V Catalano C Spino D Santini P Muretto C Spoto C Zingaretti V Sisti P Alessandroni P Giordani A Cicetti S D'Emidio S Morini A Ruzzo M Magnani G Tonini C Rabitti F Graziano 2008 Intratumoural FOXP3-positive regulatory T cells are associated with adverse prognosis in radically resected gastric cancer Eur J Cancer 44 1875 1882 18617393 10.1016/j.ejca.2008.05.017 1:CAS:528:DC%2BD1cXhtVamt7rE
15. D Wolf AM Wolf H Rumpold H Fiegl AG Zeimet E Muller-Holzner M Deibl G Gastl E Gunsilius C Marth 2005 The expression of the regulatory T cell-specific forkhead box transcription factor FoxP3 is associated with poor prognosis in ovarian cancer Clin Cancer Res 11 8326 8331 16322292 10.1158/1078-0432.CCR-05- 1244 1:CAS:528:DC%2BD2MXht1KjsrnM (Pubitemid 41746944)
16. ES Jordanova A Gorter O Ayachi F Prins LG Durrant GG Kenter SH van der Burg GJ Fleuren 2008 Human leukocyte antigen class I, MHC class I chain-related molecule A, and CD8+/regulatory T-cell ratio: which variable determines survival of cervical cancer patients? Clin Cancer Res 14 2028 2035 18381941 10.1158/1078-0432.CCR-07-4554 1:CAS:528:DC%2BD1cXkt1akurs%3D (Pubitemid 351551112)
17. P Salama M Phillips F Grieu M Morris N Zeps D Joseph C Platell B Iacopetta 2009 Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer J Clin Oncol 27 186 192 19064967 10.1200/JCO.2008.18.7229
18. F Pages A Berger M Camus F Sanchez-Cabo A Costes R Molidor B Mlecnik A Kirilovsky M Nilsson D Damotte T Meatchi P Bruneval PH Cugnenc Z Trajanoski WH Fridman J Galon 2005 Effector memory T cells, early metastasis, and survival in colorectal cancer N Engl J Med 353 2654 2666 16371631 10.1056/NEJMoa051424 1:CAS:528:DC%2BD2MXhtlarsrrE (Pubitemid 41817714)
19. DM Frey RA Droeser CT Viehl I Zlobec A Lugli U Zingg D Oertli C Kettelhack L Terracciano L Tornillo 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 19856313 1:CAS:528:DC%2BC3cXjvFKlsLk%3D
20. S Popat R Hubner RS Houlston 2005 Systematic review of microsatellite instability and colorectal cancer prognosis J Clin Oncol 23 609 618 15659508 10.1200/JCO.2005.01.086 1:CAS:528:DC%2BD2MXitVartLY%3D (Pubitemid 46224239)
21. K Nosho Y Baba N Tanaka K Shima M Hayashi JA Meyerhardt E Giovannucci G Dranoff CS Fuchs S Ogino 2010 Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review J Pathol 222 350 366 20927778 10.1002/path.2774
22. H Jonuleit E Schmitt M Stassen A Tuettenberg J Knop AH Enk 2001 Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood J Exp Med 193 1285 1294 11390435 10.1084/jem.193.11.1285 1:CAS:528:DC%2BD3MXktFyiurs%3D (Pubitemid 32524778)
23. WS Lee S Park WY Lee SH Yun HK Chun 2010 Clinical impact of tumor-infiltrating lymphocytes for survival in stage II colon cancer Cancer 116 5188 5199 20665489 10.1002/cncr.25293
24. P Correale MS Rotundo MT Del Vecchio C Remondo C Migali C Ginanneschi KY Tsang A Licchetta S Mannucci L Loiacono P Tassone G Francini P Tagliaferri 2010 Regulatory (FoxP3+) T-cell tumor infiltration is a favorable prognostic factor in advanced colon cancer patients undergoing chemo or chemoimmunotherapy J Immunother 33 435 441 20386463 10.1097/CJI.0b013e3181d32f01
25. FA Sinicrope RL Rego SM Ansell KL Knutson NR Foster DJ Sargent 2009 Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma Gastroenterology 137 1270 1279 19577568 10.1053/j.gastro.2009.06.053 1:CAS:528:DC%2BD1MXht12gtr%2FP
26. H Suzuki N Chikazawa T Tasaka J Wada A Yamasaki Y Kitaura M Sozaki M Tanaka H Onishi T Morisaki M Katano 2010 Intratumoral CD8(+) T/FOXP3 (+) cell ratio is a predictive marker for survival in patients with colorectal cancer Cancer Immunol Immunother 59 653 661 19908042 10.1007/s00262-009-0781-9 1:CAS:528:DC%2BC3cXis1yhtro%3D
27. MG Roncarolo S Gregori 2008 Is FOXP3 a bona fide marker for human regulatory T cells? Eur J Immunol 38 925 927 18395862 10.1002/eji.200838168 1:CAS:528:DC%2BD1cXlvFems7c%3D
28. N Chaput S Louafi A Bardier F Charlotte JC Vaillant F Menegaux M Rosenzwajg F Lemoine D Klatzmann J Taieb 2009 Identification of CD8+CD25+Foxp3+ suppressive T cells in colorectal cancer tissue Gut 58 520 529 19022917 10.1136/gut.2008.158824 1:CAS:528:DC%2BC3cXivFWlsbw%3D
29. MR Walker DJ Kasprowicz VH Gersuk A Benard M Van Landeghen JH Buckner SF Ziegler 2003 Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells J Clin Invest 112 1437 1443 14597769 1:CAS:528:DC%2BD3sXovVGqsL4%3D (Pubitemid 38057697)
30. I Kryczek R Liu G Wang K Wu X Shu W Szeliga L Vatan E Finlayson E Huang D Simeone B Redman TH Welling A Chang W Zou 2009 FOXP3 defines regulatory T cells in human tumor and autoimmune disease Cancer Res 69 3995 4000 19383912 10.1158/0008-5472.CAN-08-3804 1:CAS:528:DC%2BD1MXltFOksbc%3D
31. SE Erdman JJ Sohn VP Rao PR Nambiar Z Ge JG Fox DB Schauer 2005 CD4+CD25+ regulatory lymphocytes induce regression of intestinal tumors in ApcMin/+ mice Cancer Res 65 3998 4004 15899788 10.1158/0008-5472.CAN-04-3104 1:CAS:528:DC%2BD2MXktlSmsLw%3D (Pubitemid 40775635)
32. WJ Grossman JW Verbsky W Barchet M Colonna JP Atkinson TJ Ley 2004 Human T regulatory cells can use the perforin pathway to cause autologous target cell death Immunity 21 589 601 15485635 10.1016/j.immuni.2004.09.002 1:CAS:528:DC%2BD2cXpvVygtLk%3D (Pubitemid 39370513)
33. RB Sartor 2008 Microbial influences in inflammatory bowel diseases Gastroenterology 134 577 594 18242222 10.1053/j.gastro.2007.11.059 1:CAS:528:DC%2BD1cXivFOjs7o%3D (Pubitemid 351173057)
34. Terzic J, Grivennikov S, Karin E, Karin M (2010) Inflammation and colon cancer. Gastroenterology 138:2101-2114 e5
35. AP Soler RD Miller KV Laughlin NZ Carp DM Klurfeld JM Mullin 1999 Increased tight junctional permeability is associated with the development of colon cancer Carcinogenesis 20 1425 1431 10426787 10.1093/carcin/20.8.1425 1:CAS:528:DyaK1MXltlKgtbc%3D (Pubitemid 29385425)
36. II Ivanov RL de Frutos N Manel K Yoshinaga DB Rifkin RB Sartor BB Finlay DR Littman 2008 Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine Cell Host Microbe 4 337 349 18854238 10.1016/j.chom.2008.09.009 1:CAS:528: DC%2BD1cXht12iurbO
37. S Wu KJ Rhee E Albesiano S Rabizadeh X Wu HR Yen DL Huso FL Brancati E Wick F McAllister F Housseau DM Pardoll CL Sears 2009 A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses Nat Med 15 1016 1022 19701202 10.1038/nm.2015 1:CAS:528:DC%2BD1MXhtVersbvJ
38. M Numasaki J Fukushi M Ono SK Narula PJ Zavodny T Kudo PD Robbins H Tahara MT Lotze 2003 Interleukin-17 promotes angiogenesis and tumor growth Blood 101 2620 2627 12411307 10.1182/blood-2002-05-1461 1:CAS:528: DC%2BD3sXivVWgu70%3D (Pubitemid 36857622)
39. S Wang Z Liu L Wang X Zhang 2009 NF-kappaB signaling pathway, inflammation and colorectal cancer Cell Mol Immunol 6 327 334 19887045 10.1038/cmi.2009.43 1:CAS:528:DC%2BD1MXhsF2isbfP
40. J Bromberg TC Wang 2009 Inflammation and cancer: IL-6 and STAT3 complete the link Cancer Cell 15 79 80 19185839 10.1016/j.ccr.2009.01.009 1:CAS:528:DC%2BD1MXltFSmtL4%3D
41. SE Erdman T Poutahidis M Tomczak AB Rogers K Cormier B Plank BH Horwitz JG Fox 2003 CD4+CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice Am J Pathol 162 691 702 12547727 10.1016/S0002-9440(10)63863-1 1:CAS:528:DC%2BD3sXhtlKqsrc%3D (Pubitemid 36267876)
42. T Poutahidis KM Haigis VP Rao PR Nambiar CL Taylor Z Ge K Watanabe A Davidson BH Horwitz JG Fox SE Erdman 2007 Rapid reversal of interleukin-6- dependent epithelial invasion in a mouse model of microbially induced colon carcinoma Carcinogenesis 28 2614 2623 17724375 10.1093/carcin/bgm180 1:CAS:528:DC%2BD2sXhsVWgsrfP (Pubitemid 350238965)
43. MC Kullberg D Jankovic CG Feng S Hue PL Gorelick BS McKenzie DJ Cua F Powrie AW Cheever KJ Maloy A Sher 2006 IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis J Exp Med 203 2485 2494 17030948 10.1084/jem.20061082 1:CAS:528:DC%2BD28XhtFGqtL7J (Pubitemid 44664618)
44. SE Erdman T Poutahidis 2010 Cancer inflammation and regulatory T cells Int J Cancer 127 768 779 20518013 1:CAS:528:DC%2BC3cXnvFKru7Y%3D
45. CT Weaver LE Harrington PR Mangan M Gavrieli KM Murphy 2006 Th17: an effector CD4 T cell lineage with regulatory T cell ties Immunity 24 677 688 16782025 10.1016/j.immuni.2006.06.002 1:CAS:528:DC%2BD28Xms1Crt7s%3D (Pubitemid 43867371)
46. II Ivanov K Atarashi N Manel EL Brodie T Shima U Karaoz D Wei KC Goldfarb CA Santee SV Lynch T Tanoue A Imaoka K Itoh K Takeda Y Umesaki K Honda DR Littman 2009 Induction of intestinal Th17 cells by segmented filamentous bacteria Cell 139 485 498 19836068 10.1016/j.cell.2009.09.033 1:CAS:528:DC%2BD1MXhsFKltL%2FL
47. C Blaschitz M Raffatellu 2010 Th17 cytokines and the gut mucosal barrier J Clin Immunol 30 196 203 20127275 10.1007/s10875-010-9368-7 1:CAS:528:DC%2BC3cXjs1aqurg%3D
48. X Su J Ye EC Hsueh Y Zhang DF Hoft G Peng 2010 Tumor microenvironments direct the recruitment and expansion of human Th17 cells J Immunol 184 1630 1641 20026736 10.4049/jimmunol.0902813 1:CAS:528:DC%2BC3cXhtVGitLk%3D
49. G Murugaiyan B Saha 2009 Protumor vs antitumor functions of IL-17 J Immunol 183 4169 4175 19767566 10.4049/jimmunol.0901017 1:CAS:528: DC%2BD1MXhtFGjs7jF
50. VP Rao T Poutahidis Z Ge PR Nambiar BH Horwitz JG Fox SE Erdman 2006 Proinflammatory CD4+ CD45RB(hi) lymphocytes promote mammary and intestinal carcinogenesis in Apc(Min/+) mice Cancer Res 66 57 61 16397216 10.1158/0008-5472.CAN-05-3445 1:CAS:528:DC%2BD28XhsFWktQ%3D%3D (Pubitemid 43166009)
51. SE Erdman VP Rao W Olipitz CL Taylor EA Jackson T Levkovich CW Lee BH Horwitz JG Fox Z Ge T Poutahidis 2010 Unifying roles for regulatory T cells and inflammation in cancer Int J Cancer 126 1651 1665 19795459 1:CAS:528: DC%2BC3cXhtl2itL0%3D
52. M Tosolini A Kirilovsky B Mlecnik T Fredriksen S Mauger G Bindea A Berger P Bruneval WH Fridman F Pages J Galon 2011 Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer Cancer Res 71 1263 1271 21303976 10.1158/0008-5472.CAN- 10-2907 1:CAS:528:DC%2BC3MXhvFSjsLw%3D
53. SQ Crome B Clive AY Wang CY Kang V Chow J Yu A Lai A Ghahary R Broady MK Levings 2010 Inflammatory effects of ex vivo human Th17 cells are suppressed by regulatory T cells J Immunol 185 3199 3208 20720207 10.4049/jimmunol.1000557 1:CAS:528:DC%2BC3cXhtFSntL%2FM
54. C Badoual S Hans J Rodriguez S Peyrard C Klein H Agueznay Nel V Mosseri O Laccourreye P Bruneval WH Fridman DF Brasnu E Tartour 2006 Prognostic value of tumor-infiltrating CD4+ T-cell subpopulations in head and neck cancers Clin Cancer Res 12 465 472 16428488 10.1158/1078-0432.CCR-05-1886 1:CAS:528:DC%2BD28XmtlKitg%3D%3D (Pubitemid 43166137)
55. YL Zhang J Li HY Mo F Qiu LM Zheng CN Qian YX Zeng 2010 Different subsets of tumor infiltrating lymphocytes correlate with NPC progression in different ways Mol Cancer 9 4 20064222 10.1186/1476-4598-9-4
56. SJ Hooper MJ Wilson SJ Crean 2009 Exploring the link between microorganisms and oral cancer: a systematic review of the literature Head Neck 31 1228 1239 19475550 10.1002/hed.21140
57. R Kesselring A Thiel R Pries T Trenkle B Wollenberg 2010 Human Th17 cells can be induced through head and neck cancer and have a functional impact on HNSCC development Br J Cancer 103 1245 1254 20877351 10.1038/sj.bjc.6605891 1:CAS:528:DC%2BC3cXht1KqtrfM
58. GD MacLean DW Miles RD Rubens MA Reddish BM Longenecker 1996 Enhancing the effect of THERATOPE STn-KLH cancer vaccine in patients with metastatic breast cancer by pretreatment with low-dose intravenous cyclophosphamide J Immunother Emphasis Tumor Immunol 19 309 316 8877724 1:CAS:528: DyaK28XlvFOgtL0%3D (Pubitemid 26313521)
59. D Berd HC Maguire Jr MJ Mastrangelo 1986 Induction of cell-mediated immunity to autologous melanoma cells and regression of metastases after treatment with a melanoma cell vaccine preceded by cyclophosphamide Cancer Res 46 2572 2577 3697996 1:STN:280:DyaL287ovFGkug%3D%3D (Pubitemid 16120733)
60. AJ Rech RH Vonderheide 2009 Clinical use of anti-CD25 antibody daclizumab to enhance immune responses to tumor antigen vaccination by targeting regulatory T cells Ann NY Acad Sci 1174 99 106 19769742 10.1111/j.1749-6632. 2009.04939.x 1:CAS:528:DC%2BD1MXhtlehs7vL
61. M Gerena-Lewis J Crawford P Bonomi AM Maddox J Hainsworth DE McCune R Shukla H Zeigler P Hurtubise TR Chowdhury B Fletcher K Dyehouse R Ghalie AR Jazieh 2009 A Phase II trial of Denileukin Diftitox in patients with previously treated advanced non-small cell lung cancer Am J Clin Oncol 32 269 273 19433964 10.1097/COC.0b013e318187dd40 1:CAS:528:DC%2BD1MXotlShtbc%3D
62. MA Morse AC Hobeika T Osada D Serra D Niedzwiecki HK Lyerly TM Clay 2008 Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines Blood 112 610 618 18519811 10.1182/blood-2008-01-135319 1:CAS:528:DC%2BD1cXpsVaju78%3D