Prognostic role of FOXP3+ regulatory T cells infiltrating human carcinomas: the paradox of colorectal cancer (original) (raw)

References

  1. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M (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
    PubMed CAS Google Scholar
  2. Stephens LA, Mason D (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
    PubMed CAS Google Scholar
  3. Sakaguchi S, Miyara M, Costantino CM, Hafler DA (2010) FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol 10:490–500
    Article PubMed CAS Google Scholar
  4. Hori S, Nomura T, Sakaguchi S (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057–1061
    Article PubMed CAS Google Scholar
  5. Liyanage UK, Moore TT, Joo HG, Tanaka Y, Herrmann V, Doherty G, Drebin JA, Strasberg SM, Eberlein TJ, Goedegebuure PS, Linehan DC (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 CAS Google Scholar
  6. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, Evdemon-Hogan M, Conejo-Garcia JR, Zhang L, Burow M, Zhu Y, Wei S, Kryczek I, Daniel B, Gordon A, Myers L, Lackner A, Disis ML, Knutson KL, Chen L, Zou W (2004) Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 10:942–949
    Article PubMed CAS Google Scholar
  7. Ghiringhelli F, Larmonier N, Schmitt E, Parcellier A, Cathelin D, Garrido C, Chauffert B, Solary E, Bonnotte B, Martin F (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
    Article PubMed CAS Google Scholar
  8. Clarke SL, Betts GJ, Plant A, Wright KL, El-Shanawany TM, Harrop R, Torkington J, Rees BI, Williams GT, Gallimore AM, Godkin AJ (2006) CD4+CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS One 1:e129
    Article PubMed Google Scholar
  9. Bates GJ, Fox SB, Han C, Leek RD, Garcia JF, Harris AL, Banham AH (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
    Article PubMed Google Scholar
  10. Petersen RP, Campa MJ, Sperlazza J, Conlon D, Joshi MB, Harpole DH Jr, Patz EF Jr (2006) Tumor infiltrating Foxp3+ regulatory T-cells are associated with recurrence in pathologic stage I NSCLC patients. Cancer 107:2668–2672
    Article Google Scholar
  11. Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, Xiao YS, Xu Y, Li YW, Tang ZY (2007) Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol 25:2586–2593
    Article PubMed Google Scholar
  12. Li JF, Chu YW, Wang GM, Zhu TY, Rong RM, Hou J, Xu M (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
    Article PubMed Google Scholar
  13. Hiraoka N, Onozato K, Kosuge T, Hirohashi S (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
    Article PubMed CAS Google Scholar
  14. Perrone G, Ruffini PA, Catalano V, Spino C, Santini D, Muretto P, Spoto C, Zingaretti C, Sisti V, Alessandroni P, Giordani P, Cicetti A, D’Emidio S, Morini S, Ruzzo A, Magnani M, Tonini G, Rabitti C, Graziano F (2008) Intratumoural FOXP3-positive regulatory T cells are associated with adverse prognosis in radically resected gastric cancer. Eur J Cancer 44:1875–1882
    Article PubMed CAS Google Scholar
  15. Wolf D, Wolf AM, Rumpold H, Fiegl H, Zeimet AG, Muller-Holzner E, Deibl M, Gastl G, Gunsilius E, Marth C (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
    Article PubMed CAS Google Scholar
  16. Jordanova ES, Gorter A, Ayachi O, Prins F, Durrant LG, Kenter GG, van der Burg SH, Fleuren GJ (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
    Article PubMed CAS Google Scholar
  17. Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D, Platell C, Iacopetta B (2009) Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 27:186–192
    Article PubMed Google Scholar
  18. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilovsky A, Nilsson M, Damotte D, Meatchi T, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH, Galon J (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353:2654–2666
    Article PubMed CAS Google Scholar
  19. Frey DM, Droeser RA, Viehl CT, Zlobec I, Lugli A, Zingg U, Oertli D, Kettelhack C, Terracciano L, Tornillo L (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
    PubMed CAS Google Scholar
  20. Popat S, Hubner R, Houlston RS (2005) Systematic review of microsatellite instability and colorectal cancer prognosis. J Clin Oncol 23:609–618
    Article PubMed CAS Google Scholar
  21. Nosho K, Baba Y, Tanaka N, Shima K, Hayashi M, Meyerhardt JA, Giovannucci E, Dranoff G, Fuchs CS, Ogino S (2010) Tumour-infiltrating T-cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review. J Pathol 222:350–366
    Article PubMed Google Scholar
  22. Jonuleit H, Schmitt E, Stassen M, Tuettenberg A, Knop J, Enk AH (2001) Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood. J Exp Med 193:1285–1294
    Article PubMed CAS Google Scholar
  23. Lee WS, Park S, Lee WY, Yun SH, Chun HK (2010) Clinical impact of tumor-infiltrating lymphocytes for survival in stage II colon cancer. Cancer 116:5188–5199
    Article PubMed Google Scholar
  24. Correale P, Rotundo MS, Del Vecchio MT, Remondo C, Migali C, Ginanneschi C, Tsang KY, Licchetta A, Mannucci S, Loiacono L, Tassone P, Francini G, Tagliaferri P (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
    Article PubMed Google Scholar
  25. Sinicrope FA, Rego RL, Ansell SM, Knutson KL, Foster NR, Sargent DJ (2009) Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 137:1270–1279
    Article PubMed CAS Google Scholar
  26. Suzuki H, Chikazawa N, Tasaka T, Wada J, Yamasaki A, Kitaura Y, Sozaki M, Tanaka M, Onishi H, Morisaki T, Katano M (2010) Intratumoral CD8(+) T/FOXP3 (+) cell ratio is a predictive marker for survival in patients with colorectal cancer. Cancer Immunol Immunother 59:653–661
    Article PubMed CAS Google Scholar
  27. Roncarolo MG, Gregori S (2008) Is FOXP3 a bona fide marker for human regulatory T cells? Eur J Immunol 38:925–927
    Article PubMed CAS Google Scholar
  28. Chaput N, Louafi S, Bardier A, Charlotte F, Vaillant JC, Menegaux F, Rosenzwajg M, Lemoine F, Klatzmann D, Taieb J (2009) Identification of CD8+CD25+Foxp3+ suppressive T cells in colorectal cancer tissue. Gut 58:520–529
    Article PubMed CAS Google Scholar
  29. Walker MR, Kasprowicz DJ, Gersuk VH, Benard A, Van Landeghen M, Buckner JH, Ziegler SF (2003) Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells. J Clin Invest 112:1437–1443
    PubMed CAS Google Scholar
  30. Kryczek I, Liu R, Wang G, Wu K, Shu X, Szeliga W, Vatan L, Finlayson E, Huang E, Simeone D, Redman B, Welling TH, Chang A, Zou W (2009) FOXP3 defines regulatory T cells in human tumor and autoimmune disease. Cancer Res 69:3995–4000
    Article PubMed CAS Google Scholar
  31. Erdman SE, Sohn JJ, Rao VP, Nambiar PR, Ge Z, Fox JG, Schauer DB (2005) CD4+CD25+ regulatory lymphocytes induce regression of intestinal tumors in ApcMin/+ mice. Cancer Res 65:3998–4004
    Article PubMed CAS Google Scholar
  32. Grossman WJ, Verbsky JW, Barchet W, Colonna M, Atkinson JP, Ley TJ (2004) Human T regulatory cells can use the perforin pathway to cause autologous target cell death. Immunity 21:589–601
    Article PubMed CAS Google Scholar
  33. Sartor RB (2008) Microbial influences in inflammatory bowel diseases. Gastroenterology 134:577–594
    Article PubMed CAS Google Scholar
  34. Terzic J, Grivennikov S, Karin E, Karin M (2010) Inflammation and colon cancer. Gastroenterology 138:2101–2114 e5
    Google Scholar
  35. Soler AP, Miller RD, Laughlin KV, Carp NZ, Klurfeld DM, Mullin JM (1999) Increased tight junctional permeability is associated with the development of colon cancer. Carcinogenesis 20:1425–1431
    Article PubMed CAS Google Scholar
  36. Ivanov II, de Frutos RL, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR (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
    Article PubMed CAS Google Scholar
  37. Wu S, Rhee KJ, Albesiano E, Rabizadeh S, Wu X, Yen HR, Huso DL, Brancati FL, Wick E, McAllister F, Housseau F, Pardoll DM, Sears CL (2009) A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 15:1016–1022
    Article PubMed CAS Google Scholar
  38. Numasaki M, Fukushi J, Ono M, Narula SK, Zavodny PJ, Kudo T, Robbins PD, Tahara H, Lotze MT (2003) Interleukin-17 promotes angiogenesis and tumor growth. Blood 101:2620–2627
    Article PubMed CAS Google Scholar
  39. Wang S, Liu Z, Wang L, Zhang X (2009) NF-kappaB signaling pathway, inflammation and colorectal cancer. Cell Mol Immunol 6:327–334
    Article PubMed CAS Google Scholar
  40. Bromberg J, Wang TC (2009) Inflammation and cancer: IL-6 and STAT3 complete the link. Cancer Cell 15:79–80
    Article PubMed CAS Google Scholar
  41. Erdman SE, Poutahidis T, Tomczak M, Rogers AB, Cormier K, Plank B, Horwitz BH, Fox JG (2003) CD4+CD25+ regulatory T lymphocytes inhibit microbially induced colon cancer in Rag2-deficient mice. Am J Pathol 162:691–702
    Article PubMed CAS Google Scholar
  42. Poutahidis T, Haigis KM, Rao VP, Nambiar PR, Taylor CL, Ge Z, Watanabe K, Davidson A, Horwitz BH, Fox JG, Erdman SE (2007) Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma. Carcinogenesis 28:2614–2623
    Article PubMed CAS Google Scholar
  43. Kullberg MC, Jankovic D, Feng CG, Hue S, Gorelick PL, McKenzie BS, Cua DJ, Powrie F, Cheever AW, Maloy KJ, Sher A (2006) IL-23 plays a key role in Helicobacter hepaticus-induced T cell-dependent colitis. J Exp Med 203:2485–2494
    Article PubMed CAS Google Scholar
  44. Erdman SE, Poutahidis T (2010) Cancer inflammation and regulatory T cells. Int J Cancer 127:768–779
    PubMed CAS Google Scholar
  45. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM (2006) Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24:677–688
    Article PubMed CAS Google Scholar
  46. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman DR (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485–498
    Article PubMed CAS Google Scholar
  47. Blaschitz C, Raffatellu M (2010) Th17 cytokines and the gut mucosal barrier. J Clin Immunol 30:196–203
    Article PubMed CAS Google Scholar
  48. Su X, Ye J, Hsueh EC, Zhang Y, Hoft DF, Peng G (2010) Tumor microenvironments direct the recruitment and expansion of human Th17 cells. J Immunol 184:1630–1641
    Article PubMed CAS Google Scholar
  49. Murugaiyan G, Saha B (2009) Protumor vs antitumor functions of IL-17. J Immunol 183:4169–4175
    Article PubMed CAS Google Scholar
  50. Rao VP, Poutahidis T, Ge Z, Nambiar PR, Horwitz BH, Fox JG, Erdman SE (2006) Proinflammatory CD4+ CD45RB(hi) lymphocytes promote mammary and intestinal carcinogenesis in Apc(Min/+) mice. Cancer Res 66:57–61
    Article PubMed CAS Google Scholar
  51. Erdman SE, Rao VP, Olipitz W, Taylor CL, Jackson EA, Levkovich T, Lee CW, Horwitz BH, Fox JG, Ge Z, Poutahidis T (2010) Unifying roles for regulatory T cells and inflammation in cancer. Int J Cancer 126:1651–1665
    PubMed CAS Google Scholar
  52. Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman WH, Pages F, Galon J (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
    Article PubMed CAS Google Scholar
  53. Crome SQ, Clive B, Wang AY, Kang CY, Chow V, Yu J, Lai A, Ghahary A, Broady R, Levings MK (2010) Inflammatory effects of ex vivo human Th17 cells are suppressed by regulatory T cells. J Immunol 185:3199–3208
    Article PubMed CAS Google Scholar
  54. Badoual C, Hans S, Rodriguez J, Peyrard S, Klein C, Agueznay Nel H, Mosseri V, Laccourreye O, Bruneval P, Fridman WH, Brasnu DF, Tartour E (2006) Prognostic value of tumor-infiltrating CD4+ T-cell subpopulations in head and neck cancers. Clin Cancer Res 12:465–472
    Article PubMed CAS Google Scholar
  55. Zhang YL, Li J, Mo HY, Qiu F, Zheng LM, Qian CN, Zeng YX (2010) Different subsets of tumor infiltrating lymphocytes correlate with NPC progression in different ways. Mol Cancer 9:4
    Article PubMed Google Scholar
  56. Hooper SJ, Wilson MJ, Crean SJ (2009) Exploring the link between microorganisms and oral cancer: a systematic review of the literature. Head Neck 31:1228–1239
    Article PubMed Google Scholar
  57. Kesselring R, Thiel A, Pries R, Trenkle T, Wollenberg B (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
    Article PubMed CAS Google Scholar
  58. MacLean GD, Miles DW, Rubens RD, Reddish MA, Longenecker BM (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
    PubMed CAS Google Scholar
  59. Berd D, Maguire HC Jr, Mastrangelo MJ (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
    PubMed CAS Google Scholar
  60. Rech AJ, Vonderheide RH (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
    Article PubMed CAS Google Scholar
  61. Gerena-Lewis M, Crawford J, Bonomi P, Maddox AM, Hainsworth J, McCune DE, Shukla R, Zeigler H, Hurtubise P, Chowdhury TR, Fletcher B, Dyehouse K, Ghalie R, Jazieh AR (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
    Article PubMed CAS Google Scholar
  62. Morse MA, Hobeika AC, Osada T, Serra D, Niedzwiecki D, Lyerly HK, Clay TM (2008) Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines. Blood 112:610–618
    Article PubMed CAS Google Scholar

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