Colitis-associated cancer: The role of T cells in tumor development

Seminars in Immunopathology

Volumn 31, Issue 2, 2009, Pages 249-256

  Waldner, Maximilian J ^a,b   Neurath, Markus F ^a,b  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

CD4 positive T lymphocytes; CD8 positive T lymphocytes; Colitis; Colon cancer; Cytokine; Immunosurveillance; Interleukin 10; Interleukin 12; Interleukin 23; Interleukin 27; Interleukin 6; TGF beta; TNF alpha

Indexed keywords

INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA;

CANCER GROWTH; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COLITIS; CYTOTOXIC T LYMPHOCYTE; DISEASE ASSOCIATION; ENTERITIS; HUMAN; IMMUNE SYSTEM; IMMUNOSURVEILLANCE; NEOPLASM; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; TUMOR GROWTH; TUMOR PROMOTION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CHRONIC DISEASE; HUMANS; IMMUNITY, CELLULAR; INFLAMMATION; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-6; INTESTINAL NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR NECROSIS FACTOR-ALPHA;

EID: 70349292140     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-009-0161-8     Document Type: Review

References (87)

1. S Gyde P Prior MJ Dew V Saunders JA Waterhouse RN Allan 1982 Mortality in ulcerative colitis Gastroenterology 83 36 43 7075944 1:STN:280: DyaL387oslOqsA%3D%3D
2. PM Choi MP Zelig 1994 Similarity of colorectal cancer in Crohn's disease and ulcerative colitis: implications for carcinogenesis and prevention Gut 35 950 954 doi: 10.1136/gut.35.7.950 8063223 doi: 10.1136/gut.35.7.950 1:STN:280:DyaK2czktFKqsA%3D%3D
3. CN Bernstein JF Blanchard E Kliewer A Wajda 2001 Cancer risk in patients with inflammatory bowel disease: a population-based study Cancer 91 854 862 doi: 10.1002/1097-0142(20010215) 91:4<854::AID-CNCR1073>3.0.CO;2-Z 11241255 doi: 10.1002/1097-0142(20010215)91:4<854::AID-CNCR1073>3.0.CO;2-Z 1:STN:280:DC%2BD3M3hsFWluw%3D%3D
4. JA Eaden KR Abrams JF Mayberry 2001 The risk of colorectal cancer in ulcerative colitis: a meta-analysis Gut 48 526 535 doi: 10.1136/gut.48.4.526 11247898 doi: 10.1136/gut.48.4.526 1:STN:280:DC%2BD3M3hs1Orsw%3D%3D (Pubitemid 32234798)
5. DC Baumgart SR Carding 2007 Inflammatory bowel disease: cause and immunobiology Lancet 369 1627 1640 doi: 10.1016/S0140-6736(07)60750-8 17499605 doi: 10.1016/S0140-6736(07)60750-8 1:CAS:528:DC%2BD2sXltF2qsrc%3D (Pubitemid 46722636)
6. RJ Xavier DK Podolsky 2007 Unravelling the pathogenesis of inflammatory bowel disease Nature 448 427 434 doi: 10.1038/nature06005 17653185 doi: 10.1038/nature06005 1:CAS:528:DC%2BD2sXotFajurs%3D (Pubitemid 47123518)
7. DK Podolsky 2002 Inflammatory bowel disease N Engl J Med 347 417 429 doi: 10.1056/NEJMra020831 12167685 doi: 10.1056/NEJMra020831 1:CAS:528: DC%2BD38XlvFKrt7s%3D (Pubitemid 34851835)
8. IJ Fuss M Neurath M Boirivant JS Klein C de la Motte SA Strong, et al. 1996 Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5 J Immunol 157 1261 1270 8757634 1:CAS:528:DyaK28XksFKhtLY%3D
9. MF Neurath 2007 IL-23: a master regulator in Crohn disease Nat Med 13 26 28 doi: 10.1038/nm0107-26 17206128 doi: 10.1038/nm0107-26 1:CAS:528: DC%2BD2sXhvFSruw%3D%3D (Pubitemid 46067378)
10. M Philip DA Rowley H Schreiber 2004 Inflammation as a tumor promoter in cancer induction Semin Cancer Biol 14 433 439 doi: 10.1016/j.semcancer.2004.06. 006 15489136 doi: 10.1016/j.semcancer.2004.06.006 1:CAS:528:DC%2BD2cXos1Kkt7s%3D (Pubitemid 39360991)
11. JK Kundu YJ Surh 2008 Inflammation: gearing the journey to cancer Mutat Res 659 15 30 doi: 10.1016/j.mrrev.2008.03.002 18485806 doi: 10.1016/j.mrrev.2008.03.002 1:CAS:528:DC%2BD1cXpsVamsro%3D
12. A Roessner D Kuester P Malfertheiner R Schneider-Stock 2008 Oxidative stress in ulcerative colitis-associated carcinogenesis Pathol Res Pract 204 511 524 doi: 10.1016/j.prp.2008.04.011 18571874 doi: 10.1016/j.prp.2008.04.011 1:STN:280:DC%2BD1cvks1KnsQ%3D%3D
13. M Wong D Ziring Y Korin S Desai SJ Kim J Lin, et al. 2008 TNFalpha blockade in human diseases: mechanisms and future directions Clin Immunol 126 121 136 doi: 10.1016/j.clim.2007.08.013 17916444 doi: 10.1016/j.clim.2007.08.013 1:CAS:528:DC%2BD1cXlsFKntQ%3D%3D
14. D Tracey L Klareskog EH Sasso JG Salfeld PP Tak 2008 Tumor necrosis factor antagonist mechanisms of action: a comprehensive review Pharmacol Ther 117 244 279 doi: 10.1016/j.pharmthera.2007.10.001 18155297 doi: 10.1016/j.pharmthera.2007.10.001 1:CAS:528:DC%2BD1cXhtV2it74%3D
15. P Rutgeerts S Vermeire G Van Assche 2009 Biological therapies for inflammatory bowel diseases Gastroenterology 136 1182 1197 doi: 10.1053/j.gastro.2009.02.001 19249397 doi: 10.1053/j.gastro.2009.02.001 1:CAS:528:DC%2BD1MXkslWgsbw%3D
16. BK Popivanova K Kitamura Y Wu T Kondo T Kagaya S Kaneko, et al. 2008 Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis J Clin Invest 118 560 570 doi: 10.1172/JCI32453 18219394 1:CAS:528:DC%2BD1cXhsFOmsr0%3D (Pubitemid 351206546)
17. MF Neurath S Pettersson KH Meyer Zum Büschenfelde W Strober 1996 Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice Nat Med 2 998 1004 doi: 10.1038/nm0996-998 8782457 doi: 10.1038/nm0996-998 1:CAS:528:DyaK28XlsFenurg%3D (Pubitemid 26306838)
18. FR Greten L Eckmann TF Greten JM Park ZW Li LJ Egan, et al. 2004 IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer Cell 118 285 296 doi: 10.1016/j.cell.2004.07.013 15294155 doi: 10.1016/j.cell.2004.07.013 1:CAS:528:DC%2BD2cXmslKrs7o%3D (Pubitemid 39061110)
19. I Atreya R Atreya MF Neurath 2008 NF-kappaB in inflammatory bowel disease J Intern Med 263 591 596 doi: 10.1111/j.1365-2796.2008.01953.x 18479258 doi: 10.1111/j.1365-2796.2008.01953.x 1:CAS:528:DC%2BD1cXnvVOltb8%3D (Pubitemid 351678589)
20. K Mitsuyama E Sasaki A Toyonaga H Ikeda O Tsuruta A Irie, et al. 1991 Colonic mucosal interleukin-6 in inflammatory bowel disease Digestion 50 104 111 doi: 10.1159/000200747 1804734 doi: 10.1159/000200747 1:STN:280: DyaK383gvF2isw%3D%3D
21. H Ito M Takazoe Y Fukuda T Hibi K Kusugami A Andoh, et al. 2004 A pilot randomized trial of a human anti-interleukin-6 receptor monoclonal antibody in active Crohn's disease Gastroenterology 126 989 996 doi: 10.1053/j.gastro.2004. 01.012 15057738 doi: 10.1053/j.gastro.2004.01.012 1:CAS:528:DC%2BD2cXkt1Krsbo%3D discussion 947 (Pubitemid 38451170)
22. M Yamamoto K Yoshizaki T Kishimoto H Ito 2000 IL-6 is required for the development of Th1 cell-mediated murine colitis J Immunol 164 4878 4882 10779797 1:CAS:528:DC%2BD3cXivFWmu7g%3D
23. S Rose-John J Scheller G Elson SA Jones 2006 Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer J Leukoc Biol 80 227 236 doi: 10.1189/jlb.1105674 16707558 doi: 10.1189/jlb.1105674 1:CAS:528:DC%2BD28Xot1Ons7c%3D (Pubitemid 44835496)
24. N Nishimoto T Kishimoto 2006 Interleukin 6: from bench to bedside Nat Clin Pract Rheumatol 2 619 626 doi: 10.1038/ncprheum0338 17075601 doi: 10.1038/ncprheum0338 1:CAS:528:DC%2BD28Xht1emtLnI (Pubitemid 44650950)
25. J Van Snick 1990 Interleukin-6: an overview Annu Rev Immunol 8 253 278 doi: 10.1146/annurev.iy.08.040190.001345 2188664 doi: 10.1146/annurev.iy.08. 040190.001345
26. PC Heinrich I Behrmann S Haan HM Hermanns G Müller-Newen F Schaper 2003 Principles of interleukin (IL)-6-type cytokine signalling and its regulation Biochem J 374 1 20 doi: 10.1042/BJ20030407 12773095 doi: 10.1042/BJ20030407 1:CAS:528:DC%2BD3sXmtF2hurs%3D (Pubitemid 37046923)
27. YC Chung YF Chang 2003 Serum interleukin-6 levels reflect the disease status of colorectal cancer J Surg Oncol 83 222 226 doi: 10.1002/jso.10269 12884234 doi: 10.1002/jso.10269 (Pubitemid 36936007)
28. G Galizia M Orditura C Romano E Lieto P Castellano L Pelosio, et al. 2002 Prognostic significance of circulating IL-10 and IL-6 serum levels in colon cancer patients undergoing surgery Clin Immunol 102 169 178 doi: 10.1006/clim.2001.5163 11846459 doi: 10.1006/clim.2001.5163 1:CAS:528: DC%2BD38XisFWmtLk%3D (Pubitemid 34171516)
29. C Becker MC Fantini C Schramm HA Lehr S Wirtz A Nikolaev, et al. 2004 TGF-beta suppresses tumor progression in colon cancer by inhibition of IL-6 trans-signaling Immunity 21 491 501 doi: 10.1016/j.immuni.2004.07.020 15485627 doi: 10.1016/j.immuni.2004.07.020 1:CAS:528:DC%2BD2cXpvVygt7c%3D (Pubitemid 39370505)
30. J Bollrath TJ Phesse VA von Burstin T Putoczki M Bennecke T Bateman, et al. 2009 gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis Cancer Cell 15 91 102 doi: 10.1016/j.ccr.2009.01.002 19185844 doi: 10.1016/j.ccr.2009.01.002 1:CAS:528:DC%2BD1MXltFSmtLo%3D
31. S Grivennikov E Karin J Terzic D Mucida GY Yu S Vallabhapurapu, et al. 2009 IL-6 and stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer Cancer Cell 15 103 113 doi: 10.1016/j.ccr.2009.01.001 19185845 doi: 10.1016/j.ccr.2009.01.001 1:CAS:528:DC%2BD1MXltFSmtLs%3D
32. P Yu YX Fu 2006 Tumor-infiltrating T lymphocytes: friends or foes? Lab Invest 86 231 245 doi: 10.1038/labinvest.3700389 16446705 doi: 10.1038/labinvest.3700389 1:CAS:528:DC%2BD28XhsFSmurk%3D (Pubitemid 43276955)
33. E Osawa A Nakajima T Fujisawa YI Kawamura N Toyama-Sorimachi H Nakagama, et al. 2006 Predominant T helper type 2-inflammatory responses promote murine colon cancers Int J Cancer 118 2232 2236 doi: 10.1002/ijc.21639 16331625 doi: 10.1002/ijc.21639 1:CAS:528:DC%2BD28XjsVCgt78%3D
34. M Strasly F Cavallo M Geuna S Mitola MP Colombo G Forni, et al. 2001 IL-12 inhibition of endothelial cell functions and angiogenesis depends on lymphocyte-endothelial cell cross-talk J Immunol 166 3890 3899 11238633 1:CAS:528:DC%2BD3MXitVGnu7Y%3D
35. DJ Verbik WW Stinson MJ Brunda A Kessinger SS Joshi 1996 In vivo therapeutic effects of interleukin-12 against highly metastatic residual lymphoma Clin Exp Metastasis 14 219 229 8674276 1:STN:280:DyaK283ms12ltQ%3D%3D
36. MJ Brunda L Luistro RR Warrier RB Wright BR Hubbard M Murphy, et al. 1993 Antitumor and antimetastatic activity of interleukin 12 against murine tumors J Exp Med 178 1223 1230 doi: 10.1084/jem.178.4.1223 8104230 doi: 10.1084/jem.178.4.1223 1:CAS:528:DyaK3sXlsFyjsL4%3D
37. CL Nastala HD Edington TG McKinney H Tahara MA Nalesnik MJ Brunda, et al. 1994 Recombinant IL-12 administration induces tumor regression in association with IFN-gamma production J Immunol 153 1697 1706 7913943 1:CAS:528: DyaK2cXlslOgsbk%3D
38. M Del Vecchio E Bajetta S Canova MT Lotze A Wesa G Parmiani, et al. 2007 Interleukin-12: biological properties and clinical application Clin Cancer Res 13 4677 4685 doi: 10.1158/1078-0432.CCR-07-0776 17699845 doi: 10.1158/1078-0432.CCR-07-0776 (Pubitemid 47294773)
39. GP Dunn AT Bruce H Ikeda LJ Old RD Schreiber 2002 Cancer immunoediting: from immunosurveillance to tumor escape Nat Immunol 3 991 998 doi: 10.1038/ni1102-991 12407406 doi: 10.1038/ni1102-991 1:CAS:528: DC%2BD38Xot1Chs70%3D (Pubitemid 35363648)
40. M Shibata T Nezu H Kanou H Abe M Takekawa M Fukuzawa 2002 Decreased production of interleukin-12 and type 2 immune responses are marked in cachectic patients with colorectal and gastric cancer J Clin Gastroenterol 34 416 420 doi: 10.1097/00004836-200204000-00006 11907352 doi: 10.1097/00004836-200204000- 00006 1:CAS:528:DC%2BD38XjtFSkt7o%3D (Pubitemid 34258317)
41. HL Kettunen AS Kettunen NE Rautonen 2003 Intestinal immune responses in wild-type and Apcmin/+ mouse, a model for colon cancer Cancer Res 63 5136 5142 12941845 1:CAS:528:DC%2BD3sXms12ntrs%3D
42. F Pagès A Berger M Camus F Sanchez-Cabo A Costes R Molidor, et al. 2005 Effector memory T cells, early metastasis, and survival in colorectal cancer N Engl J Med 353 2654 2666 doi: 10.1056/NEJMoa051424 16371631 doi: 10.1056/NEJMoa051424 (Pubitemid 41817714)
43. Y Endo H Marusawa T Kou H Nakase S Fujii T Fujimori, et al. 2008 Activation-induced cytidine deaminase links between inflammation and the development of colitis-associated colorectal cancers Gastroenterology 135 889 898 doi: 10.1053/j.gastro.2008.06.091 18691581 doi: 10.1053/j.gastro.2008.06.091 1:CAS:528:DC%2BD1cXhtFylsrvE 898.e881-883
44. DD Weedon RG Shorter DM Ilstrup KA Huizenga WF Taylor 1973 Crohn's disease and cancer N Engl J Med 289 1099 1103 4754948 1:STN:280: DyaE2c%2FjsFSnsw%3D%3D
45. SN Gyde P Prior JC Macartney H Thompson JA Waterhouse RN Allan 1980 Malignancy in Crohn's disease Gut 21 1024 1029 doi: 10.1136/gut.21.12.1024 7461462 doi: 10.1136/gut.21.12.1024 1:STN:280:DyaL3M7hsFCnsw%3D%3D
46. CD Gillen RS Walmsley P Prior HA Andrews RN Allan 1994 Ulcerative colitis and Crohn's disease: a comparison of the colorectal cancer risk in extensive colitis Gut 35 1590 1592 doi: 10.1136/gut.35.11.1590 7828978 doi: 10.1136/gut.35.11.1590 1:STN:280:DyaK2M7ivF2ltw%3D%3D
47. G Trinchieri 2003 Interleukin-12 and the regulation of innate resistance and adaptive immunity Nat Rev Immunol 3 133 146 doi: 10.1038/nri1001 12563297 doi: 10.1038/nri1001 1:CAS:528:DC%2BD3sXot12gug%3D%3D (Pubitemid 37328691)
48. G Monteleone L Biancone R Marasco G Morrone O Marasco F Luzza, et al. 1997 Interleukin 12 is expressed and actively released by Crohn's disease intestinal lamina propria mononuclear cells Gastroenterology 112 1169 1178 doi: 10.1016/S0016-5085(97) 70128-8 9098000 doi: 10.1016/S0016-5085(97)70128-8 1:STN:280:DyaK2s3lt1Cgsw%3D%3D
49. E Stuber W Strober M Neurath 1996 Blocking the CD40L-CD40 interaction in vivo specifically prevents the priming of T helper 1 cells through the inhibition of interleukin 12 secretion J Exp Med 183 693 698 doi: 10.1084/jem.183.2.693 8627184 doi: 10.1084/jem.183.2.693 1:CAS:528: DyaK28Xht1Sntb0%3D (Pubitemid 26060800)
50. MF Neurath I Fuss BL Kelsall E Stüber W Strober 1995 Antibodies to interleukin 12 abrogate established experimental colitis in mice J Exp Med 182 1281 1290 doi: 10.1084/jem.182.5.1281 7595199 doi: 10.1084/jem.182.5.1281 1:CAS:528:DyaK2MXovFWru7s%3D
51. PJ Mannon IJ Fuss L Mayer CO Elson WJ Sandborn D Present, et al. 2004 Anti-interleukin-12 antibody for active Crohn's disease N Engl J Med 351 2069 2079 doi: 10.1056/NEJMoa033402 15537905 doi: 10.1056/NEJMoa033402 1:CAS:528:DC%2BD2cXpslegs74%3D (Pubitemid 39482500)
52. B Oppmann R Lesley B Blom JC Timans Y Xu B Hunte, et al. 2000 Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12 Immunity 13 715 725 doi: 10.1016/S1074-7613(00) 00070-4 11114383 doi: 10.1016/S1074-7613(00)00070-4 1:CAS:528:DC%2BD3cXovV2ht7c%3D
53. CO Elson Y Cong CT Weaver TR Schoeb TK McClanahan RB Fick, et al. 2007 Monoclonal anti-interleukin 23 reverses active colitis in a T cell-mediated model in mice Gastroenterology 132 2359 2370 doi: 10.1053/j.gastro.2007.03.104 17570211 doi: 10.1053/j.gastro.2007.03.104 1:CAS:528:DC%2BD2sXnvFOhtb8%3D (Pubitemid 46890867)
54. RH Duerr KD Taylor SR Brant JD Rioux MS Silverberg MJ Daly, et al. 2006 A genome-wide association study identifies IL23R as an inflammatory bowel disease gene Science 314 1461 1463 doi: 10.1126/science.1135245 17068223 doi: 10.1126/science.1135245 1:CAS:528:DC%2BD28Xht1CntrjF (Pubitemid 44871953)
55. CL Langrish Y Chen WM Blumenschein J Mattson B Basham JD Sedgwick, et al. 2005 IL-23 drives a pathogenic T cell population that induces autoimmune inflammation J Exp Med 201 233 240 doi: 10.1084/jem.20041257 15657292 doi: 10.1084/jem.20041257 1:CAS:528:DC%2BD2MXot12mtA%3D%3D (Pubitemid 40189432)
56. LA Fouser JF Wright K Dunussi-Joannopoulos M Collins 2008 Th17 cytokines and their emerging roles in inflammation and autoimmunity Immunol Rev 226 87 102 doi: 10.1111/j.1600-065X.2008.00712.x 19161418 doi: 10.1111/j.1600-065X.2008. 00712.x
57. F Fossiez J Banchereau R Murray C Van Kooten P Garrone S Lebecque 1998 Interleukin-17 Int Rev Immunol 16 541 551 10.3109/08830189809043008 9646176 10.3109/08830189809043008 1:CAS:528:DyaK1cXktlCktL4%3D
58. T Korn M Oukka V Kuchroo E Bettelli 2007 Th17 cells: effector T cells with inflammatory properties Semin Immunol 19 362 371 doi: 10.1016/j.smim.2007. 10.007 18035554 doi: 10.1016/j.smim.2007.10.007 1:CAS:528:DC%2BD1cXisVSrsLs%3D (Pubitemid 351274046)
59. D Yen J Cheung H Scheerens F Poulet T McClanahan B McKenzie, et al. 2006 IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6 J Clin Invest 116 1310 1316 doi: 10.1172/JCI21404 16670770 doi: 10.1172/JCI21404 1:CAS:528:DC%2BD28XksVWns78%3D
60. M Leppkes C Becker II Ivanov S Hirth S Wirtz C Neufert, et al. 2008 RORgamma-expressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F Gastroenterology doi: 10.1053/j.gastro.2008.10.018 18992745
61. J Seiderer I Elben J Diegelmann J Glas J Stallhofer C Tillack, et al. 2008 Role of the novel Th17 cytokine IL-17F in inflammatory bowel disease (IBD): upregulated colonic IL-17F expression in active Crohn's disease and analysis of the IL17F p.His161Arg polymorphism in IBD Inflamm Bowel Dis 14 437 445 doi: 10.1002/ibd.20339 18088064 doi: 10.1002/ibd.20339 (Pubitemid 351571823)
62. JL Langowski X Zhang L Wu JD Mattson T Chen K Smith, et al. 2006 IL-23 promotes tumour incidence and growth Nature 442 461 465 doi: 10.1038/nature04808 16688182 doi: 10.1038/nature04808 1:CAS:528:DC%2BD28XnsVajtbk%3D (Pubitemid 44264796)
63. M Numasaki J Fukushi M Ono SK Narula PJ Zavodny T Kudo, et al. 2003 Interleukin-17 promotes angiogenesis and tumor growth Blood 101 2620 2627 doi: 10.1182/blood-2002-05-1461 12411307 doi: 10.1182/blood-2002-05-1461 1:CAS:528:DC%2BD3sXivVWgu70%3D (Pubitemid 36857622)
64. M Chabaud P Garnero JM Dayer PA Guerne F Fossiez P Miossec 2000 Contribution of interleukin 17 to synovium matrix destruction in rheumatoid arthritis Cytokine 12 1092 1099 doi: 10.1006/cyto.2000.0681 10880256 doi: 10.1006/cyto.2000.0681 1:CAS:528:DC%2BD3cXksV2msLw%3D (Pubitemid 30479493)
65. GP Dunn LJ Old RD Schreiber 2004 The immunobiology of cancer immunosurveillance and immunoediting Immunity 21 137 148 doi: 10.1016/j.immuni.2004.07.017 15308095 doi: 10.1016/j.immuni.2004.07.017 1:CAS:528:DC%2BD2cXnsVKltrY%3D (Pubitemid 39094044)
66. JE Talmadge M Donkor E Scholar 2007 Inflammatory cell infiltration of tumors: Jekyll or Hyde Cancer Metastasis Rev 26 373 400 doi: 10.1007/s10555-007-9072-0 17717638 doi: 10.1007/s10555-007-9072-0 (Pubitemid 350115102)
67. Y Naito K Saito K Shiiba A Ohuchi K Saigenji H Nagura, et al. 1998 CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer Cancer Res 58 3491 3494 9721846 1:CAS:528:DyaK1cXlsFajsb4%3D
68. I Atreya CC Schimanski C Becker S Wirtz H Dornhoff E Schnürer, et al. 2007 The T-box transcription factor eomesodermin controls CD8 T cell activity and lymph node metastasis in human colorectal cancer Gut 56 1572 1578 doi: 10.1136/gut.2006.117812 17566017 doi: 10.1136/gut.2006.117812 1:CAS:528:DC%2BD2sXhtlyiu7vO (Pubitemid 350033196)
69. CL Smith N Dulphy M Salio V Cerundolo 2002 Immunotherapy of colorectal cancer Br Med Bull 64 181 200 doi: 10.1093/bmb/64.1.181 12421733 doi: 10.1093/bmb/64.1.181 1:CAS:528:DC%2BD38XosFOgs70%3D (Pubitemid 35238587)
70. ES Bergmann-Leitner EH Duncan WW Leitner 2003 Identification and targeting of tumor escape mechanisms: a new hope for cancer therapy? Curr Pharm Des 9 2009 2023 10.2174/1381612033454199 14529412 10.2174/1381612033454199 1:CAS:528:DC%2BD3sXnsV2gu70%3D (Pubitemid 37142438)
71. JM Michael-Robinson N Pandeya MD Walsh AE Biemer-Huttmann RD Eri RL Buttenshaw, et al. 2006 Characterization of tumour-infiltrating lymphocytes and apoptosis in colitis-associated neoplasia: comparison with sporadic colorectal cancer J Pathol 208 381 387 doi: 10.1002/path.1895 16315333 doi: 10.1002/path.1895 1:STN:280:DC%2BD28%2FpsFOiug%3D%3D (Pubitemid 43216107)
72. S Müller J Lory N Corazza GM Griffiths K Z'graggen L Mazzucchelli, et al. 1998 Activated CD4+ and CD8+ cytotoxic cells are present in increased numbers in the intestinal mucosa from patients with active inflammatory bowel disease Am J Pathol 152 261 268 9422543
73. HS Souza CJ Tortori MT Castelo-Branco AT Carvalho VS Margallo CF Delgado, et al. 2005 Apoptosis in the intestinal mucosa of patients with inflammatory bowel disease: evidence of altered expression of FasL and perforin cytotoxic pathways Int J Colorectal Dis 20 277 286 doi: 10.1007/s00384-004-0639-8 15503066 doi: 10.1007/s00384-004-0639-8 (Pubitemid 40558036)
74. K Okazaki M Morita I Nishimori S Sano M Toyonaga Y Nakazawa, et al. 1993 Major histocompatibility antigen-restricted cytotoxicity in inflammatory bowel disease Gastroenterology 104 384 391 8425680 1:STN:280:DyaK3s7ks1aksA%3D%3D
75. R Bacchetta L Passerini E Gambineri M Dai SE Allan L Perroni, et al. 2006 Defective regulatory and effector T cell functions in patients with FOXP3 mutations J Clin Invest 116 1713 1722 doi: 10.1172/JCI25112 16741580 doi: 10.1172/JCI25112 1:CAS:528:DC%2BD28XlsFWqs7g%3D (Pubitemid 43911026)
76. SF Ziegler 2006 FOXP3: of mice and men Annu Rev Immunol 24 209 226 doi: 10.1146/annurev.immunol.24.021605.090547 16551248 doi: 10.1146/annurev.immunol. 24.021605.090547 1:CAS:528:DC%2BD28XkvFSqt7s%3D
77. F Powrie MW Leach S Mauze LB Caddle RL Coffman 1993 Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice Int Immunol 5 1461 1471 doi: 10.1093/intimm/5.11.1461 7903159 doi: 10.1093/intimm/5.11.1461 1:STN:280:DyaK2c%2Fotlektg%3D%3D
78. F Powrie MW Leach S Mauze S Menon LB Caddle RL Coffman 1994 Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells Immunity 1 553 562 doi: 10.1016/1074-7613(94) 90045-0 7600284 doi: 10.1016/1074-7613(94)90045-0 1:CAS:528:DyaK2cXmvFyqurY%3D
79. S Read V Malmström F Powrie 2000 Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+) CD4(+) regulatory cells that control intestinal inflammation J Exp Med 192 295 302 doi: 10.1084/jem.192.2.295 10899916 doi: 10.1084/jem.192.2.295 1:CAS:528: DC%2BD3cXkvFGiu7Y%3D (Pubitemid 30470312)
80. IL Huibregtse AU van Lent SJ van Deventer 2007 Immunopathogenesis of IBD: insufficient suppressor function in the gut? Gut 56 584 592 doi: 10.1136/gut.2006.103523 17047100 doi: 10.1136/gut.2006.103523 1:CAS:528:DC%2BD2sXks1Ghsrs%3D (Pubitemid 46580517)
81. R Kühn J Löhler D Rennick K Rajewsky W Müller 1993 Interleukin-10-deficient mice develop chronic enterocolitis Cell 75 263 274 doi: 10.1016/0092-8674(93) 80068-P 8402911 doi: 10.1016/0092-8674(93)80068-P
82. DJ Berg N Davidson R Kühn W Müller S Menon G Holland, et al. 1996 Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses J Clin Invest 98 1010 1020 doi: 10.1172/JCI118861 8770874 doi: 10.1172/JCI118861 1:CAS:528:DyaK28XlsFOgt7w%3D
83. T Poutahidis KM Haigis VP Rao PR Nambiar CL Taylor Z Ge, et al. 2007 Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma Carcinogenesis 28 2614 2623 doi: 10.1093/carcin/bgm180 17724375 doi: 10.1093/carcin/bgm180 1:CAS:528: DC%2BD2sXhsVWgsrfP (Pubitemid 350238965)
84. C Becker MC Fantini MF Neurath 2006 TGF-beta as a T cell regulator in colitis and colon cancer Cytokine Growth Factor Rev 17 97 106 doi: 10.1016/j.cytogfr.2005.09.004 16298544 doi: 10.1016/j.cytogfr.2005.09.004 1:CAS:528:DC%2BD28Xos1Cruw%3D%3D (Pubitemid 43117519)
85. D Wolf AM Wolf H Rumpold H Fiegl AG Zeimet E Muller-Holzner, et al. 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 doi: 10.1158/1078-0432.CCR-05-1244 16322292 doi: 10.1158/1078-0432.CCR-05-1244 1:CAS:528:DC%2BD2MXht1KjsrnM (Pubitemid 41746944)
86. Y Ishibashi S Tanaka K Tajima T Yoshida H Kuwano 2006 Expression of Foxp3 in non-small cell lung cancer patients is significantly higher in tumor tissues than in normal tissues, especially in tumors smaller than 30 mm Oncol Rep 15 1315 1319 16596204 1:CAS:528:DC%2BD28XksFKitbw%3D
87. SE Erdman JJ Sohn VP Rao PR Nambiar Z Ge JG Fox, et al. 2005 CD4+ CD25+ regulatory lymphocytes induce regression of intestinal tumors in ApcMin/+ mice Cancer Res 65 3998 4004 doi: 10.1158/0008-5472.CAN-04-3104 15899788 doi: 10.1158/0008-5472.CAN-04-3104 1:CAS:528:DC%2BD2MXktlSmsLw%3D (Pubitemid 40775635)