Cellular mediators of inflammation: Tregs and T H 17 cells in gastrointestinal diseases

Mediators of Inflammation

Volumn 2009, Issue , 2009, Pages

  Cammarota, Giovanni ^a   Pandolfi, Franco ^a   Cianci, Rossella ^a   Pagliari, Danilo ^a   Landolfi, Raffaele ^a   Kunkel, Steven ^b  

^a CATHOLIC UNIVERSITY   (Italy)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 17;

CD4+ CD25+ T LYMPHOCYTE; CELL INTERACTION; CELLULAR IMMUNITY; CYTOTOXICITY; DIGESTIVE SYSTEM INFLAMMATION; ENTERITIS; ESOPHAGUS CANCER; GASTROINTESTINAL DISEASE; GASTROINTESTINAL TUMOR; HUMAN; LIVER CELL CARCINOMA; LIVER GRAFT; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; STOMACH CANCER; TH17 CELL; ANIMAL; IMMUNOLOGY; INFLAMMATION; METABOLISM;

ANIMALS; GASTROINTESTINAL DISEASES; HUMANS; INFLAMMATION; INTERLEUKIN-17; T-LYMPHOCYTES, REGULATORY;

EID: 77949379104     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2009/132028     Document Type: Review

References (122)

1. Gershon R. K., Kondo K., Cell interactions in the induction of tolerance: the role of thymic lymphocytes Immunology 1970 18 5 723 737
2. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M., Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor -chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases Journal of Immunology 1995 155 3 1151 1164
3. Malek T. R., Bayer A. L., Tolerance, not immunity, crucially depends on IL-2 Nature Reviews Immunology 2004 4 9 665 674
4. Borish L., Rosenwasser L., T H 1 / TH2 lymphocytes: doubt some more Journal of Allergy and Clinical Immunology 1997 99 2 161 164
5. Zhou L., Chong M. M. W., Littman D. R., Plasticity of CD4+ T cell lineage differentiation Immunity 2009 30 5 646 655
6. Shevach E. M., CD 4 + CD 25 + suppressor T cells: more questions than answers Nature Reviews Immunology 2002 2 6 389 400
7. Jonuleit H., Schmitt E., Stassen M., Tuettenberg A., Knop J., Enk A. H., Identification and functional characterization of human CD4+ CD25+ T cells with regulatory properties isolated from peripheral blood Journal of Experimental Medicine 2001 193 11 1285 1294
8. Stephens L. A., Mottet C., Mason D., Powrie F., Human CD4+ CD25+ thymocytes and peripheral T cells have immune suppressive activity in vitro European Journal of Immunology 2001 31 4 1247 1254
9. Fontenot J. D., Dooley J. L., Farr A. G., Rudensky A. Y., Developmental regulation of FoxP3 expression during ontogeny Journal of Experimental Medicine 2005 202 7 901 906
10. Baecher-Allan C., Brown J. A., Freeman G. J., Hafler D. A., CD 4 + CD 25 + high regulatory cells in human peripheral blood Journal of Immunology 2001 167 3 1245 1253
11. Xu Q., Lee J., Jankowska-Gan E., Human CD4+ CD25+ low adaptive T regulatory cells suppress delayed-type hypersensitivity during transplant tolerance Journal of Immunology 2007 178 6 3983 3995
12. Komatsu N., Mariotti-Ferrandiz M. E., Wang Y., Malissen B., Waldmann H., Hori S., Heterogeneity of natural FoxP3 + T cells: a committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity Proceedings of the National Academy of Sciences of the United States of America 2009 106 6 1903 1908
13. Sakaguchi S., Powrie F., Emerging challenges in regulatory T cell function and biology Science 2007 317 5838 627 629
14. Sakaguchi S., Regulatory T cells in the past and for the future European Journal of Immunology 2008 38 4 901 937
15. Workman C. J., Szymczak-Workman A. L., Collison L. W., Pillai M. R., Vignali D. A. A., The development and function of regulatory T cells Cellular and Molecular Life Sciences 2009 66 16 2603 2622
16. Sakaguchi S., Setoguchi R., Yagi H., Nomura T., Naturally arising FoxP3-expressing CD25+ CD4+ regulatory T cells in self-tolerance and autoimmune disease Current Topics in Microbiology and Immunology 2006 305 51 66
17. Bettelli E., Dastrange M., Oukka M., FoxP3 interacts with nuclear factor of activated T cells and NF- B to repress cytokine gene expression and effector functions of T helper cells Proceedings of the National Academy of Sciences of the United States of America 2005 102 14 5138 5143
18. Bennett C. L., Christie J., Ramsdell F., The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3 Nature Genetics 2001 27 1 20 21
19. Tran D. Q., Shevach E. M., Therapeutic potential of FOXP3 + regulatory T cells and their interactions with dendritic cells Human Immunology 2009 70 5 294 299
20. Hori S., Nomura T., Sakaguchi S., Control of regulatory T cell development by the transcription factor FoxP3 Science 2003 299 5609 1057 1061
21. Liu W., Putnam A. L., Xu-Yu Z., CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells Journal of Experimental Medicine 2006 203 7 1701 1711
22. Liu Y., Zhang P., Li J., Kulkarni A. B., Perruche S., Chen W., A critical function for TGF- ß signaling in the development of natural CD4+ CD25+ FoxP3 + regulatory T cells Nature Immunology 2008 9 6 632 640
23. Josefowicz S. Z., Rudensky A., Control of regulatory T cell lineage commitment and maintenance Immunity 2009 30 5 616 625
24. Borsellino G., Kleinewietfeld M., Di Mitri D., Expression of ectonucleotidase CD39 by FoxP3 + Treg cells: hydrolysis of extracellular ATP and immune suppression Blood 2007 110 4 1225 1232
25. Deaglio S., Dwyer K. M., Gao W., Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression Journal of Experimental Medicine 2007 204 6 1257 1265
26. Lehmann J., Huehn J., de la Rosa M., Expression of the integrin E ß 7 identifies unique subsets of CD25+ as well as CD25- regulatory T cells Proceedings of the National Academy of Sciences of the United States of America 2002 99 20 13031 13036
27. Suffia I., Reckling S. K., Salay G., Belkaid Y., A role for CD103 in the retention of CD4+ CD25+ Treg and control of Leishmania major infection Journal of Immunology 2005 174 9 5444 5455
28. Chatenoud L., Bach J.-F., Adaptive human regulatory T cells: myth or reality? Journal of Clinical Investigation 2006 116 9 2325 2327
29. Wang J., Huizinga T. W., Toes R. E., De novo generation and enhanced suppression of human CD4+ CD25+ regulatory T cells by retinoic acid Journal of Immunology 2009 183 6 4119 4126
30. Zhou X., Bailey-Bucktrout S. L., Jeker L. T., Instability of the transcription factor FoxP3 leads to the generation of pathogenic memory T cells in vivo Nature Immunology 2009 10 9 1000 1007
31. Thornton A. M., Shevach E. M., Suppressor effector function of CD4+ CD25+ immunoregulatory T cells is antigen nonspecific Journal of Immunology 2000 164 1 183 190
32. Corthay A., How do regulatory T cells work? Scandinavian Journal of Immunology 2009 70 4 326 336
33. Jordan M. S., Boesteanu A., Reed A. J., Thymic selection of CD4+ CD25+ regulatory T cells induced by an agonist self-peptide Nature Immunology 2001 2 4 301 306
34. Tang Q., Bluestone J. A., The FoxP3 + regulatory T cell: a jack of all trades, master of regulation Nature Immunology 2008 9 3 239 244
35. Sojka D. K., Huang Y.-H., Fowell D. J., Mechanisms of regulatory T-cell suppressiona diverse arsenal for a moving target Immunology 2008 124 1 13 22
36. Pandolfi F., Pierdominici M., Marziali M., Low-dose IL-2 reduces lymphocyte apoptosis and increases naive CD4 cells in HIV-1 patients treated with HAART Clinical Immunology 2000 94 3 153 159
37. Bours M. J. L., Swennen E. L. R., Di Virgilio F., Cronstein B. N., Dagnelie P. C., Adenosine 5-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation Pharmacology and Therapeutics 2006 112 2 358 404
38. Vignali D. A. A., How many mechanisms do regulatory T cells need? European Journal of Immunology 2008 38 4 908 911
39. Wing K., Onishi Y., Prieto-Martin P., CTLA-4 control over FoxP3 + regulatory T cell function Science 2008 322 5899 271 275
40. Shevach E. M., Immunology: regulating suppression Science 2008 322 5899 202 203
41. Read S., Malmstrom V., Powrie F., Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25+ CD4+ regulatory cells that control intestinal inflammation Journal of Experimental Medicine 2000 192 2 295 302
42. Takahashi T., Tagami T., Yamazaki S., Immunologic self-tolerance maintained by CD25+ CD4+ regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4 Journal of Experimental Medicine 2000 192 2 303 310
43. Ziegler S. F., FOXP3: of mice and men Annual Review of Immunology 2006 24 209 226
44. Horwitz D. A., Zheng S. G., Gray J. D., Natural and TGF- ß -induced FoxP3 + CD4+ CD25+ regulatory T cells are not mirror images of each other Trends in Immunology 2008 29 9 429 435
45. McHugh R. S., Whitters M. J., Piccirillo C. A., CD 4 + CD 25 + immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor Immunity 2002 16 2 311 323
46. Shimizu J., Yamazaki S., Takahashi T., Ishida Y., Sakaguchi S., Stimulation of CD25+ CD4+ regulatory T cells through GITR breaks immunological self-tolerance Nature Immunology 2002 3 2 135 142
47. Huang C.-T., Workman C. J., Flies D., Role of LAG-3 in regulatory T cells Immunity 2004 21 4 503 513
48. B. Liang, C. Workman, J. Lee, et al., "Regulatory T cells inhibit dendritic cells by lymphocyte activation gene-3 engagement of MHC class II," Journal of Immunology, vol. 180, no. 9, pp. 5916-5926, 2008.
49. R. S. Bystry, V. Aluvihare, K. A. Welch, M. Kallikourdis, and A. G. Betz, "B cells and professional APCs recruit regulatory T cells via CCL4," Nature Immunology, vol. 2, no. 12, pp. 1126-1132, 2001.
50. A. Y. Rudensky and D. J. Campbell, "In vivo sites and cellular mechanisms of T reg cell-mediated suppression," Journal of Experimental Medicine, vol. 203, no. 3, pp. 489-492, 2006.
51. P. Pandiyan, L. Zheng, S. Ishihara, J. Reed, and M. J. Lenardo, "CD4+CD25+FoxP3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells," Nature Immunology, vol. 8, no. 12, pp. 1353-1362, 2007.
52. A. Giovannetti, M. Pierdominici, A. Di Iorio, et al., "Apoptosis in the homeostasis of the immune system and in human immune mediated diseases," Current Pharmaceutical Design, vol. 14, no. 3, pp. 253-268, 2008.
53. W. J. Grossman, J. W. Verbsky, W. Barchet, M. Colonna, J. P. Atkinson, and T. J. Ley, "Human T regulatory cells can use the perforin pathway to cause autologous target cell death," Immunity, vol. 21, no. 4, pp. 589-601, 2004.
54. X. Cao, S. F. Cai, T. A. Fehniger, et al., "Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance," Immunity, vol. 27, no. 4, pp. 635-646, 2007.
55. M. Miyara and S. Sakaguchi, "Natural regulatory T cells: mechanisms of suppression," Trends in Molecular Medicine, vol. 13, no. 3, pp. 108-116, 2007.
56. E. M. Shevach, "Mechanisms of FoxP3+ T regulatory cellmediated suppression," Immunity, vol. 30, no. 5, pp. 636-645, 2009.
57. L. W. Collison, C. J. Workman, T. T. Kuo, et al., "The inhibitory cytokine IL-35 contributes to regulatory T-cell function," Nature, vol. 450, no. 7169, pp. 566-569, 2007.
58. A. K. Abbas, J. Lohr, B. Knoechel, and V. Nagabhushanam, "T cell tolerance and autoimmunity," Autoimmunity Reviews, vol. 3, no. 7-8, pp. 471-475, 2004.
59. F. Sallusto and A. Lanzavecchia, "Human Th17 cells in infection and autoimmunity,"Microbes and Infection, vol. 11, no. 5, pp. 620-624, 2009.
60. C. Dong, "Differentiation and function of pro-inflammatory Th17 cells," Microbes and Infection, vol. 11, no. 5, pp. 584- 588, 2009.
61. K. S. Voo, Y.-H. Wang, F. R. Santori, et al., "Identification of IL-17-producing FOXP3+ regulatory T cells in humans," Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 12, pp. 4793-4798, 2009.
62. L. Zhou and D. R. Littman, "Transcriptional regulatory networks in Th17 cell differentiation," Current Opinion in Immunology, vol. 21, no. 2, pp. 146-152, 2009.
63. A. Awasthi and V. K. Kuchroo, "Th17 cells: from precursors to players in inflammation and infection," International Immunology, vol. 21, no. 5, pp. 489-498, 2009.
64. L. Cosmi, R. De Palma, V. Santarlasci, et al., "Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor," Journal of ExperimentalMedicine, vol. 205, no. 8, pp. 1903-1916, 2008.
65. P. Miossec, "IL-17 and Th17 cells in human inflammatory diseases," Microbes and Infection, vol. 11, no. 5, pp. 625-630, 2009.
66. H. J. P. M. Koenen, R. L. Smeets, P. M. Vink, E. van Rijssen, A. M. H. Boots, and I. Joosten, "Human CD25highFoxP3pos regulatory T cells differentiate into IL-17 producing cells," Blood, vol. 112, no. 6, pp. 2340-2352, 2008.
67. J. L. Langowski, X. Zhang, L. Wu, et al., "IL-23 promotes tumour incidence and growth," Nature, vol. 442, no. 7101, pp. 461-465, 2006.
68. Y. K. Lee, R. Mukasa, R. D. Hatton, and C. T. Weaver, "Developmental plasticity of Th17 and Treg cells," Current Opinion in Immunology, vol. 21, no. 3, pp. 274-280, 2009.
69. L.Zhou, J. E. Lopes, M. M.W. Chong, et al., "TGF-?-induced FoxP3 inhibits TH17 cell differentiation by antagonizing ROR?t function," Nature, vol. 453, no. 7192, pp. 236-240, 2008.
70. D. Mucida, Y. Park, G. Kim, et al., "Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid," Science, vol. 317, no. 5835, pp. 256-260, 2007.
71. T. Sasada, M. Kimura, Y. Yoshida, M. Kanai, and A. Takabayashi, "CD4+CD25+ regulatory T cells in patients with gastrointestinal malignancies: possible involvement of regulatory T cells in disease progression," Cancer, vol. 98, no. 5, pp. 1089-1099, 2003.
72. F. Pandolfi, G. Corte, and I. Quinti, "Defect of T helper lymphocytes, as identified by the 5/9 monoclonal antibody, in patients with common variable hypogammaglobulinaemia," Clinical and Experimental Immunology, vol. 51, no. 3, pp. 470-474, 1983.
73. W. T. Bennett, F. Pandolfi, B. H. Grove, et al., "Dominant rearrangements among human tumor-infiltrating lymphocytes: analysis of T-cells derived from 32 patients with melanoma, lung, and renal cell carcinoma," Cancer, vol. 69, no. 9, pp. 2379-2384, 1992.
74. M. Hishii, D. Andrews, L. A. Boyle, et al., "In vivo accumulation of the same anti-melanoma T cell clone in two different metastatic sites," Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 4, pp. 1378-1383, 1997.
75. K. Kono, H. Kawaida, A. Takahashi, et al., "CD4+CD25+high regulatory T cells increase with tumor stage in patients with gastric and esophageal cancers," Cancer Immunology, Immunotherapy, vol. 55, no. 9, pp. 1064-1071, 2006.
76. Y. Mizukami, K. Kono, Y. Kawaguchi, et al., "Localisation pattern of FoxP3+ regulatory T cells is associated with clinical behaviour in gastric cancer," British Journal of Cancer, vol. 98, no. 1, pp. 148-153, 2008.
77. U. K. Liyanage, T. T. Moore, H.-G. Joo, et al., "Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma," Journal of Immunology, vol. 169, no. 5, pp. 2756-2761, 2002.
78. L. Ormandy, T. Hillemann, H.Wedemeyer, M. P.Manns, T. F. Greten, and F. Korangy, "Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma," Cancer Research, vol. 65, no. 6, pp. 2457-2464, 2005.
79. B. Zhang, G. Rong, H. Wei, et al., "The prevalence of Th17 cells in patients with gastric cancer," Biochemical and Biophysical Research Communications, vol. 374, no. 3, pp. 533-537, 2008.
80. J.-P. Zhang, J. Yan, J. Xu, et al., "Increased intratumoral IL- 17-producing cells correlate with poor survival in hepatocellular carcinoma patients," Journal of Hepatology, vol. 50, no. 5, pp. 980-989, 2009.
81. I. Kryczek, M. Banerjee, P. Cheng, et al., "Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments," Blood, vol. 114, no. 6, pp. 1141-1149, 2009.
82. F. Ichihara, K. Kono, A. Takahashi, H. Kawaida, H. Sugai, and H. Fujii, "Increased populations of regulatory T cells in peripheral blood and tumor-infiltrating lymphocytes in patients with gastric and esophageal cancers," Clinical Cancer Research, vol. 9, no. 12, pp. 4404-4408, 2003.
83. N. Hiraoka, K. Onozato, T. Kosuge, and S. Hirohashi, "Prevalence of FOXP3+ regulatory T cells increases during the progression of pancreatic ductal adenocarcinoma and its premalignant lesions," Clinical Cancer Research, vol. 12, no. 18, pp. 5423-5434, 2006.
84. S. Hinz, L. Pagerols-Raluy, H.-H. Oberg, et al., "FoxP3 expression in pancreatic carcinoma cells as a novel mechanism of immune evasion in cancer," Cancer Research, vol. 67, no. 17, pp. 8344-8350, 2007.
85. V. Chew, C. Tow, M. Teo, et al., "Inflammatory tumor microenvironment is associated with superior survival in hepatocellular carcinoma patients," Journal of Hepatology. In press.
86. J. A. Pons, B. Revilla-Nuin, A. Baroja-Mazo, et al., "FoxP3 in peripheral blood is associated with operational tolerance in liver transplant patients during immunosuppression withdrawal," Transplantation, vol. 86, no. 10, pp. 1370-1378, 2008.
87. K. J. Wood and S. Sakaguchi, "Regulatory T cells in transplantation tolerance," Nature Reviews Immunology, vol. 3, no. 3, pp. 199-210, 2003.
88. G. Frisullo, V. Nociti, R. Iorio, et al., "Increased CD4+CD25+FoxP3+ T cells in peripheral blood of celiac disease patients: correlation with dietary treatment," Human Immunology, vol. 70, no. 6, pp. 430-435, 2009.
89. T. Kanai, Y. Nemoto, N. Kamada, et al., "Homeostatic (IL-7) and effector (IL-17) cytokines as distinct but complementary target for an optimal therapeutic strategy in inflammatory bowel disease," Current Opinion in Gastroenterology, vol. 25, no. 4, pp. 306-313, 2009.
90. P. Felaco, M. L. Castellani, M. A. De Lutiis, et al., "IL-32: a newly-discovered proinflammatory cytokine," Journal of Biological Regulators & Homeostatic Agents, vol. 23, no. 3, pp. 141-147, 2009.
91. S. Brand, "Crohn's disease: Th1, Th17 or both? The change of a paradigmml: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease," Gut, vol. 58, no. 8, pp. 1152-1167, 2009.
92. J. Dambacher, F. Beigel, K. Zitzmann, et al., "The role of the novel Th17 cytokine IL-26 in intestinal inflammation," Gut, vol. 58, no. 9, pp. 1207-1217, 2009.
93. J. Pene, S. Chevalier, L. Preisser, et al., "Chronically inflamed human tissues are infiltrated by highly differentiated Th17 lymphocytes," Journal of Immunology, vol. 180, no. 11, pp. 7423-7430, 2008.
94. A. Bai, N. Lu, Y. Guo, Z. Liu, J. Chen, and Z. Peng, "Alltrans retinoic acid down-regulates inflammatory responses by shifting the Treg/Th17 profile in human ulcerative and murine colitis," Journal of Leukocyte Biology, vol. 86, no. 4, pp. 959-969, 2009.
95. K. M. Elias, A. Laurence, T. S. Davidson, et al., "Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway," Blood, vol. 111, no. 3, pp. 1013-1020, 2008.
96. M. J. Benson, K. Pino-Lagos, M. Rosemblatt, and R. J. Noelle, "All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation," Journal of Experimental Medicine, vol. 204, no. 8, pp. 1765-1774, 2007.
97. W. O'Connor Jr., M. Kamanaka, C. J. Booth, et al., "A protective function for interleukin 17A in T cell-mediated intestinal inflammation," Nature Immunology, vol. 10, no. 6, pp. 603-609, 2009.
98. S. Ardizzone, A. Cassinotti, D. Trabattoni, et al., " Immunomodulatory effects of 1,25-dihydroxyvitamin D3 on TH1 /TH2 cytokines in inflammatory bowel disease: an in vitro study," International Journal of Immunopathology and Pharmacology, vol. 22, no. 1, pp. 63-71, 2009.
99. J. H. Cho, "The genetics and immunopathogenesis of inflammatory bowel disease," Nature Reviews Immunology, vol. 8, no. 6, pp. 458-466, 2008.
100. W. Strober, I. Fuss, and P. Mannon, "The fundamental basis of inflammatory bowel disease," Journal of Clinical Investigation, vol. 117, no. 3, pp. 514-521, 2007.
101. M. E. Himmel, G. Hardenberg, C. A. Piccirillo, T. S. Steiner, and M. K. Levings, "The role of T-regulatory cells and Tolllike receptors in the pathogenesis of human inflammatory bowel disease," Immunology, vol. 125, no. 2, pp. 145-153, 2008.
102. N. N. Kristensen, J. Olsen, M. Gad, and M. H. Claesson, "Genome-wide expression profiling during protection from colitis by regulatory T cells," Inflammatory Bowel Diseases, vol. 14, no. 1, pp. 75-87, 2008.
103. P. Vieira and A. O'Garra, "Regula'ten' the gut," Nature Immunology, vol. 8, no. 9, pp. 905-907, 2007.
104. K. J. Maloy, L. Salaun, R. Cahill, G. Dougan, N. J. Saunders, and F. Powrie, "CD4+CD25+ TR cells suppress innate immune pathology through cytokine-dependent mechanisms," Journal of Experimental Medicine, vol. 197, no. 1, pp. 111-119, 2003.
105. J. Buning, N. Homann, D. von Smolinski, et al., "Helminths as governors of inflammatory bowel disease," Gut, vol. 57, no. 8, pp. 1182-1183, 2008.
106. M. Saruta, Q. T. Yu, P. R. Fleshner, et al., "Characterization of FOXP3+CD4+ regulatory T cells in Crohn's disease," Clinical Immunology, vol. 125, no. 3, pp. 281-290, 2007.
107. J. Maul, C. Loddenkemper, P. Mundt, et al., "Peripheral and intestinal regulatory CD4+CD25+high T cells in inflammatory bowel disease," Gastroenterology, vol. 128, no. 7, pp. 1868-1878, 2005.
108. S. Makita, T. Kanai, S. Oshima, et al., "CD4+CD25+bright T cells in human intestinal lamina propria as regulatory cells," Journal of Immunology, vol. 173, no. 5, pp. 3119-3130, 2004.
109. V. Muratov, A.-K. Ulfgren, M. Engstrom, et al., "Decreased numbers of FoxP3-positive and TLR-2-positive cells in intestinal mucosa are associated with improvement in patients with active inflammatory bowel disease following selective leukocyte apheresis," Journal of Gastroenterology, vol. 43, no. 4, pp. 277-282, 2008.
110. K. Kamikozuru, K. Fukunaga, S. Hirota, et al., "The expression profile of functional regulatory T cells, CD4+CD25+high+/forkhead box protein P3+, in patients with ulcerative colitis during active and quiescent disease," Clinical and Experimental Immunology, vol. 156, no. 2, pp. 320-327, 2009.
111. Q. T. Yu, M. Saruta, A. Avanesyan, P. R. Fleshner, A. H. Banham, and K. A. Papadakis, "Expression and functional characterization of FOXP3+CD4+ regulatory T cells in ulcerative colitis," Inflammatory Bowel Diseases, vol. 13, no. 2, pp. 191-199, 2007.
112. M. A. Gavin, T. R. Torgerson, E. Houston, et al., "Singlecell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development," Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 17, pp. 6659-6664, 2006.
113. D. Q. Tran, H. Ramsey, and E. M. Shevach, "Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor- β-dependent but does not confer a regulatory phenotype," Blood, vol. 110, no. 8, pp. 2983-2990, 2007.
114. R. H. Duerr, K. D. Taylor, S. R. Brant, et al., "A genomewide association study identifies IL23R as an inflammatory bowel disease gene," Science, vol. 314, no. 5804, pp. 1461- 1463, 2006.
115. S. Hue, P. Ahern, S. Buonocore, et al., "Interleukin-23 drives innate and T cell-mediated intestinal inflammation," Journal of Experimental Medicine, vol. 203, no. 11, pp. 2473-2483, 2006.
116. C. O. Elson, Y. Cong, C. T. Weaver, et al., "Monoclonal antiinterleukin 23 reverses active colitis in a T cell-mediated model in mice," Gastroenterology, vol. 132, no. 7, pp. 2359- 2370, 2007.
117. E. K. Boden and S. B. Snapper, "Regulatory T cells in inflammatory bowel disease," Current Opinion in Gastroenterology, vol. 24, no. 6, pp. 733-741, 2008.
118. I. Ricciardelli, K. J. Lindley, M. Londei, and S. Quaratino, "Anti tumour necrosis-? therapy increases the number of FOXP3+ regulatory T cells in children affected by Crohn's disease," Immunology, vol. 125, no. 2, pp. 178-183, 2008.
119. H. H. Smits, A. Engering, D. van der Kleij, et al., "Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3- grabbing nonintegrin," Journal of Allergy and Clinical Immunology, vol. 115, no. 6, pp. 1260-1267, 2005.
120. L. A. Zenewicz, A. Antov, and R. A. Flavell, "CD4 T-cell differentiation and inflammatory bowel disease," Trends in Molecular Medicine, vol. 15, no. 5, pp. 199-207, 2009.
121. A. Mizoguchi and E. Mizoguchi, "Inflammatory bowel disease, past, present and future: lessons from animal models," Journal of Gastroenterology, vol. 43, no. 1, pp. 1-17, 2008.
122. K. J. Maloy, "The Interleukin-23/Interleukin-17 axis in intestinal inflammation," Journal of Internal Medicine, vol. 263, no. 6, pp. 584-590, 2008.