Inflammatory bowel disease: Dysfunction of GALT and gut bacterial flora (I)

Surgeon

Volumn 1, Issue 2, 2003, Pages 63-75

  Chandran, P ^a   Satthaporn, S ^a   Robins, A ^a   Eremin, O ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Commensal bacteria; Dendritic cell; Gut associated lymphoid tissue; Immune tolerance; Inflammatory bowel disease

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; CELL INTERACTION; COMMENSALISM; CROHN DISEASE; DENDRITIC CELL; DISEASE PREDISPOSITION; ENTERITIS; FOOD; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE DEFICIENCY; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOLOGY; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; LYMPHATIC SYSTEM DISEASE; MEDICAL DOCUMENTATION; MESENTERY LYMPH NODE; NONHUMAN; PATHOGENESIS; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; ULCERATIVE COLITIS;

EID: 0037650130     PISSN: 1479666X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1479-666X(03)80118-X     Document Type: Review

References (130)

1. Weiner HL, van Rees EP. Mucosal tolerance. Immunol Lett 1999; 69:3-4.
2. Duchmann R, Neurath MF, Meyer zum Buschenfelde KH. Responses to self and non-self intestinal microflora in health and inflammatory bowel disease. Res Immunol 1997; 148: 589-94.
3. Mayer L. Mucosal immunity and gastrointestinal antigen processing. J Pediatr Gastroenterol Nutr 2000; 30: S4-12.
4. Bjerke K, Brandtzaeg P, Fausa O. T cell distribution is different in follicle-associated epithelium of human Peyer's patches and villous epithelium. Clin Exp Immunol 1988; 74: 270-75.
5. Owen RL, Pierce NF, Apple RT, Cray WC Jr. M cell transport of Vibrio cholerae from the intestinal lumen into Peyer's patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis 1986; 153: 1108-18.
6. Cepek KL, Parker CM, Madara JL, Brenner MB. Integrin alpha E beta 7 mediates adhesion of T lymphocytes to epithelial cells. J Immunol 1993; 150: 3459-70.
7. Janossy G, Tidman N, Selby WS, Thomas JA, Granger S, Kung PC et al. Human T lymphocytes of inducer and suppressor type occupy different microenvironments. Nature 1980; 288: 81-84.
8. Selby WS, Janossy G, Bofill M, Jewell DP. Intestinal lymphocyte subpopulations in inflammatory bowel disease: an analysis by immunohistological and cell isolation techniques. Gut 1984; 25: 32-40.
9. Jany A, Cerf-Bensussan N, Brousse N, Selz F, Guy-Grand D. Subsets of CD3+ (T cell receptor alpha/beta or gamma/delta) and CD3-lymphocytes isolated from normal human gut epithelium display phenotypical features different from their counterparts in peripheral blood. Eur J Immunol 1990; 20: 1097-103.
10. Trejdosiewicz LK, Smart CJ, Oakes DJ, Howdle PD, Malizia G, Campana D et al. Expression of T-cell receptors TcR1 (gamma/delta) and TcR2 (alpha/beta) in the human intestinal mucosa. Immunology 1989; 68: 7-12.
11. Budhraja M, Levendoglu H, Kocka F, Mangkornkanok M, Sherer R. Duodenal mucosal T cell subpopulation and bacterial cultures in acquired immune deficiency syndrome. Am J Gastroenterol 1987; 82: 427-31.
12. Janossy G, Bofill M, Rowe D, Muir J, Beverley PC. The tissue distribution of T lymphocytes expressing different CD45 polypeptides. Immunology 1989; 66: 517-25.
13. Streeter PR, Berg EL, Rouse BT, Bargatze RF, Butcher EC. A tissue-specific endothelial cell molecule involved in lymphocyte homing. Nature 1988; 331: 41-46.
14. Nakache M, Berg EL, Streeter PR, Butcher EC. The mucosal vascular addressin is a fissue-specific endothelial cell adhesion molecule for circulating lymphocytes. Nature 1989; 337: 179-81.
15. Briskin M, Winsor-Hines D, Shyjan A, Cochran N, Bloom S, Wilson J et al. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am J Pathol 1997; 151: 97-110.
16. Williams MB, Butcher EC. Homing of naive and memory T lymphocyte subsets to Peyer's patches, lymph nodes, and spleen. J Immunol 1997; 159: 1746-52.
17. Stagg AJ, Kamm MA, Knight SC. Intestinal dendritic cells increase T cell expression of alpha4beta7 integrin. Eur J Immunol 2002; 32: 1445-54.
18. Hamann A, Andrew DP, Jablonski-Westrich D, Holzmann B, Butcher EC. Role of alpha 4-integrins in lymphocyte homing to mucosal tissues in vivo. J Immunol 1994; 152: 3282-93.
19. Bargatze RE, Jutila MA, Butcher EC. Distinct roles of L-selectin and integrins alpha 4 beta 7 and LFA-1 in lymphocyte homing to Peyer's patch-HEV in situ: the multistep model confirmed and refined. Immunity 1995; 3: 99-108.
20. Picarella D, Hurlbut P, Rottman J, Shi X, Butcher E, Ringler DJ. Monoclonal antibodies specific for beta 7 integrin and mucosal addressin cell adhesion molecule-1 (MAdCAM-1) reduce inflammation in the colon of scid mice reconstituted with CD45RBhigh CD4+ T cells. J Immunol 1997; 158: 2099-106.
21. Hesterberg PE, Winsor-Hines D, Briskin MJ, Soler-Ferran D, Merrill C, Mackay CR. Rapid resolution of chronic colitis in the cotton-top tamarin with an antibody to a gut-homing integrin alpha 4 beta 7. Gastroenterology 1996; 111: 1373-80.
22. Arihiro S, Ohtani H, Suzuki M, Murata M, Ejima C, Oki M et al. Differential expression of mucosal addressin cell adhesion molecule-1 (MAdCAM-1) in ulcerative colitis and Crohn's disease. Pathol Int 2002; 52: 367-74.
23. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 1994; 372: 190-93.
24. Schon MP, Arya A, Murphy EA, Adams CM, Strauch UG, Agace WW et al. Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol 1999; 162: 6641-49.
25. Folwaczny C, Noehl N, Endres SP, Heldwein W, Loeschke K, Fricke H. Antinuclear autoantibodies in patients with inflammatory bowel disease. High prevalence in first-degree relatives. Dig Dis Sci 1997; 42: 1593-97.
26. Mayer L, Eisenhardt D. Lack of induction of suppressor T cells by intestinal epithelial cells from patients with inflammatory bowel disease. J Clin Invest 1990; 86: 1255-60.
27. Rudolphi A, Bonhagen K, Reimann J. Polyclonal expansion of adoptively transferred CD4+ alpha beta T cells in the colonic lamina propria of scid mice with colitis. Eur J Immunol 1996; 26: 1156-63.
28. Claesson MH, Rudolphi A, Kofoed S, Poulsen SS, Reimann J. CD4+ T lymphocytes injected into severe combined immunodeficient (SCID) mice lead to an inflammatory and lethal bowel disease. Clin Exp Immunol 1996; 104: 491-500.
29. Palmen MJ, Wijburg OL, Kunst IH, Kroes H, van Rees EP. CD4+ T cells from 2,4,6-trinitrobenzene sulfonic acid (TNBS)-induced colitis rodents migrate to the recipient's colon upon transfer; down-regulation by CD8+ T cells. Clin Exp Immunol 1998; 112: 216-25.
30. Leithauser F, Trobonjaca Z, Moller P, Reimann J. Clustering of colonic lamina propria CD4(+) T cells to subepithelial dendritic cell aggregates precedes the development of colitis in a murine adoptive transfer model. Lab Invest 2001; 81: 1339-49.
31. Panaccione R, Sandborn WJ. Is antibody testing for inflammatory bowel disease clinically useful? Gastroenterology 1999, 116:1001-02; discussion 1002-03.
32. Cohavy O, Bruckner D, Gordon LK, Misra R, Wei B, Eggena ME et al. Colonic bacteria express an ulcerative colitis pANCA-related protein epitope. Infect Immun 2000; 68: 1542-48.
33. Rutgeerts P, Vermeire S. Clinical value of the detection of antibodies in the serum for diagnosis and treatment of inflammatory bowel disease. Gastroenterology 1998; 115: 1006-09.
34. Lombardi G, Annese V, Piepoli A, Bovio P, Latiano A, Napolitano G et al. Antineutrophil cytoplasmic antibodies in inflammatory bowel disease: clinical role and review of the literature. Dis Colon Rectum 2000; 43: 999-1007.
35. Sandborn WJ, Landers CJ, Tremaine WJ, Targan SR. Association of antineutrophil cytoplasmic antibodies with resistance to treatment of left-sided ulcerative colitis: results of a pilot study. Mayo Clin Proc 1996; 71: 431-36.
36. Sutton CL, Yang H, Li Z, Rotter JI, Targan SR, Braun J. Familial expression of anti-Saccharomyces cerevisiae mannan antibodies in affected and unaffected relatives of patients with Crohn's disease. Gut 2000; 46: 58-63.
37. Sendid B, Quinton JF, Charrier G, Goulet O, Cortot A, Grandbastien B et al. Anti-Saccharomyces cerevisiae mannan antibodies in familial Crohn's disease. Am J Gastroenterol 1998; 93: 1306-10.
38. Steinman RM, The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 1991; 9: 271-96.
39. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-52.
40. Bell D, Young JW, Banchereau J. Dendritic cells. Adv Immunol 1999; 72: 255-324.
41. Cook DN, Prosser DM, Forster R, Zhang J, Kuklin NA, Abbondanzo SJ et al. CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity 2000; 12: 495-503.
42. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001; 2: 361-67.
43. Viney JL, Mowat AM, O'Malley JM, Williamson E, Fanger NA. Expanding dendrific cells in vivo enhances the induction of oral tolerance. J Immunol 1998; 160: 5815-25.
44. Salio M, Cella M, Suter M, Lanzavecchia A. Inhibition of dendritic cell maturation by herpes simplex virus. Eur J Immunol 1999; 29: 3245-53.
45. Andrews DM, Andoniou CE, Granucci F, Ricciardi-Castagnoli P, Degli-Esposti MA. Infection of dendritic cells by murine cytomegalovirus induces functional paralysis. Nat Immunol 2001; 2: 1077-84.
46. Urban BC, Ferguson DJ, Pain A, Willcox N, Plebanski M, Austyn JM et al. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 1999; 400: 73-77.
47. Steinman RM, Nussenzweig MC. Inaugural Article: Avoiding horror autotoxicus: The importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci U S A 2002; 99: 351-58.
48. Janeway CA, Jr. The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today 1992; 13: 11-16.
49. Janeway CA, Jr. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 1989; 54: 1-13.
50. Kopan R, Cagan R. Notch on the cutting edge. Trends Genet 1997, 13:465-467.
51. Osborne B, Miele L: Notch and the immune system. Immunity 1999; 11: 653-63.
52. Artavanis-Tsakonas S, Rand MD, Lake RJ. Notch signaling: cell fate control and signal integration in development. Science 1999; 284: 770-76.
53. Hoyne GF, Dallman MJ, Lamb JR. Linked suppression in peripheral T cell tolerance to the house dust mite derived allergen Der p 1. Int Arch Allergy Immunol 1999; 118: 122-24.
54. Hoyne GF, Dallman MJ, Lamb JR. T-cell regulation of peripheral tolerance and immunity: the potential role for Notch signalling. Immunology 2000; 100: 281-88.
55. Bell SJ, Rigby R, English N, Mann SD, Knight SC, Kamm MA et al. Migration and maturation of human colonic dendritic cells. J Immunol 2001; 166:4958-67.
56. Ikeda Y, Akbar F, Matsui H, Onji M. Characterization of antigen-presenting dendritic cells in the peripheral blood and colonic mucosa of patients with ulcerative colitis. Eur J Gastroenterol Hepatol 2001; 13: 841-50.
57. Vuckovic S, Florin TH, Khalil D, Zhang MF, Patel K, Hamilton I et al. CD40 and CD86 upregulation with divergent CMRF44 expression on blood dendritic cells in inflammatory bowel diseases. Am J Gastroenterol 2001; 96: 2946-56.
58. Boirivant M, Pica R, DeMaria R, Testi R, Pallone F, Strober W. Stimulated human lamina propria T cells manifest enhanced Fas-mediated apoptosis. J Clin Invest 1996; 98: 2616-22.
59. Garside P, Steel M, Worthey EA, Kewin PJ, Howie SE, Harrison DJ et al. Lymphocytes from orally tolerized mice display enhanced susceptibility to death by apoptosis when cultured in the absence of antigen in vitro. Am J Pathol 1996; 149: 1971-79.
60. Bu P, Keshavarzian A, Stone DD, Liu J, Le PT, Fisher S, Qiao L. Apoptosis: one of the mechanisms that maintains unresponsiveness of the intestinal mucosal immune system. J Immunol 2001; 166: 6399-403.
61. Brady HJ, Salomons GS, Bobeldijk RC, Berns AJ. T cells from baxalpha, transgenic mice show accelerated apoptosis in response to stimuli but do not show restored DNA damage-induced cell death in the absence of p53. gene product in. Embo J 1996; 15:1221-30.
62. Williams O, Norton T, Halligey M, Kioussis D, Brady HJ. The action of Bax and bcl-2 on T cell selection. J Exp Med 1998; 188:1125-33.
63. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 1997; 3: 614-20.
64. ten Hove T, van Montfrans C, Peppelenbosch MP, van Deventer SJ. Infliximab treatment induces apoptosis of lamina propria T lymphocytes in Crohn's disease. Gut 2002; 50: 206-11.
65. Suzuki A, Sugimura K, Ohtsuka K, Hasegawa K, Suzuki K, Ishizuka K et al. Fas/Fas ligand expression and characteristics of primed CD45RO+ T cells in the inflamed mucosa of ulcerative colitis. Scand J Gastroenterol 2000; 35: 1278-83.
66. Vella AT, Dow S, Potter TA, Kappler J, Marrack P. Cytokine-induced survival of activated T cells in vitro and in vivo. Proc Natl Acad Sci U S A 1998; 95: 3810-15.
67. Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo. Nat Med 2000; 6: 583-88.
68. Weiner HL, Friedman A, Miller A, Khoury SJ, al-Sabbagh A, Santos L et al. Oral tolerance: immunologic mechanisms and treatment of animal and human organ-specific autoimmune diseases by oral administration of autoantigens. Annu Rev Immunol 1994; 12: 809-37.
69. Garside P, Mowat AM. Mechanisms of oral tolerance. Crit Rev Immunol 1997; 17: 119-37.
70. Seder RA, Paul WE. Acquisition of lymphokine-producing phenotype by CD4+ T cells. Annu Rev Immunol 1994-112: 635-73.
71. Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature 1996; 383: 787-93.
72. Constant SL, Bottomly K. Induction of Th1 and Th2 CD4+ T cell responses: the alternative approaches. Annu Rev Immunol 1997; 15:297-322.
73. O'Garra A. Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 1998; 8: 275-83.
74. Cella M, Scheidegger D, Palmer-Lehmann K, Lane P, Lanzavecchia A, Alber G: Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 1996; 184: 747-52.
75. Koch F, Stanzl U, Jennewein P, Janke K, Heufler C, Kampgen E et al. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med 1996; 184: 741-46.
76. Corinti S, Albanesi C, la Sala A, Pastore S, Girolomoni G. Regulatory activity of autocrine IL-10 on dendritic cell functions. J Immunol 2001; 166: 4312-18.
77. Gasche C, Bakos S, Dejaco C, Tillinger W, Zakeri S, Reinisch W. IL-10 secretion and sensitivity in normal human intestine and inflammatory bowel disease. J Clin Immunol 2000; 20: 362-70.
78. Tsuji NM, Mizumachi K, Kurisaki J. Interleukin-10-secreting Peyer's patch cells are responsible for active suppression in low-dose oral tolerance. Immunology 2001; 103: 458-64.
79. Garside P. Cytokines in experimental colitis. Clin Exp Immunol 1999; 118: 337-39.
80. Berg DJ, Davidson N, Kuhn R, Muller W, Menon S, Holland G et al. Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J Clin Invest 1996; 98: 1010-20.
81. Steidler L, Hans W, Schotte L, Neirynck S, Obermeier F, Falk W et al. Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 2000; 289: 1352-55.
82. Iwasaki A, Kelsall BL. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J Exp Med 1999; 190: 229-39.
83. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 1994; 265: 1237-40.
84. 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. J Exp Med 2000; 192:295-302.
85. Chen W, Jin W, Wahl SM. Engagement of cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) induces transforming growth factor beta (TGF-beta) production by murine CD4(+) T cells. J Exp Med 1998; 188: 1849-57.
86. Hahm KB, Im YH, Parks TW, Park SH, Markowitz S, Jung HY et al. Loss of transforming growth factor beta signalling in the intestine contributes to tissue injury in inflammatory bowel disease. Gut 2001; 49:190-98.
87. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW et al. The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 1997; 89: 1165-73.
88. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R et al: Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 1997; 389: 631-35.
89. Monteleone G, Kumberova A, Croft NM, McKenzie C, Steer HW, MacDonald TT. Blocking Smad7 restores TGF-beta 1 signaling in chronic inflammatory bowel disease. J Clin Invest 2001, 108: 601-09.
90. Wiercinska-Drapalo A, Flisiak R, Prokopowicz D. Effect of ulcerative colitis activity on plasma concentration of transforming growth factor beta 1. Cytokine 2001; 14: 343-46.
91. Sambuelli A, Diez RA, Sugai E, Boerr L, Negreira S, Gil A et al. Serum transforming growth factor-beta 1 levels increase in response to successful anti-inflammatory therapy in ulcerative colitis. Aliment Pharmacol Ther 2000; 14: 1443-49.
92. Funakoshi K, Sugimura K, Anezaki K, Bannai H, Ishizuka K, Asakura H. Spectrum of cytokine gene expression in intestinal macosal lesions of Crohn's disease and ulcerative colitis. Digestion 1998; 59: 73-78.
93. Masuda H, Iwai S, Tanaka T, Hayakawa S. Expression of IL-8, TNF-alpha and IFN-gamma m-RNA in ulcerative colitis, particularly in patients with inactive phase. J Clin Lab Immunol 1995; 46: 111-23.
94. Akazawa A, Sakaida I, Higaki S, Kubo Y, Uchida K, Okita K. Increased expression of tumor necrosis factor-alpha messenger RNA in the intestinal mucosa of inflammatory bowel disease, particularly in patients with disease in the inactive phase. J Gastroenterol 2002; 37: 345-53.
95. Reinecker HC, Steffen M, Witthoeft T, Pflueger I, Schreiber S, MacDermott RP et al. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol 1993; 94: 174-81.
96. Reimund JM, Wittersheim C, Dumont S, Muller CD, Baumann R, Poindron P et al. Mucosal inflammatory cytokine production by intestinal biopsies in patients with ulcerative colitis and Crolin's disease. J Clin Immunol 1996; 16: 144-50.
97. Inoue S, Matsumoto T, Iida M, Mizuno M, Kuroki F, Hoshika K et al. Characterization of cytokine expression in the rectal mucosa of ulcerative colitis: correlation with disease activity. Am J Gastroenterol 1999; 94: 2441-46.
98. Seegert D, Rosenstiel P, Pfahler H, Pfefferkorn P, Nikolaus S, Schreiber S. Increased expression of IL-16 in inflammatory bowel disease. Gut 2001; 48: 326-32.
99. Okamura H, Tsutsi H, Komatsu T, Yutsudo M, Hakura A, Tanimoto T et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature 1995; 378: 88-91.
100. Dinarello CA. IL-18: A TH1-inducing, proinflammatory cytokine and new member of the IL-1 family. J Allergy Clin Immunol 1999; 103: 11-24.
101. Lebel-Binay S, Berger A, Zinzindohoue F, Cugnenc P, Thiounn N, Fridman WH et al. Interleukin-18: biological properties and clinical implications. Eur Cytokine Netw 2000; 11: 15-26.
102. Wallace VA, Fung-Leung WP, Timms E, Gray D, Kishihara K, Loh DY et al. CD45RA and CD45RBhigh expression induced by thymic selection events. J Exp Med 1992; 176: 1657-63.
103. Lee WT, Yin XM, Vitetta ES. Functional and ontogenetic analysis of murine CD45Rhi and CD45R1o CD4+ T cells. J Immunol 1990; 144: 3288-95.
104. Morrissey PJ, Charrier K, Braddy S, Liggitt D, Watson JD. CD4+ T cells that express high levels of CD45RB induce wasting disease when transferred into congenic severe combined immunodeficient mice. Disease development is prevented by cotransfer of purified CD4+ T cells. J Exp Med 1993; 178: 237-44.
105. Powrie F, Leach MW, Mauze S, Caddle LB, Coffman RL. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 1993; 5: 1461-71.
106. Leach MW, Bean AG, Mauze S, Coffman RL, Powrie F. Inflammatory bowel disease in C.B-17 scid mice reconstituted with the CD45RBhigh subset of CD4+ T cells. Am J Pathol 1996; 148: 1503-15.
107. Claesson MH, Rudolphi A, Kofoed S, Poulsen SS, Reimann J. CD4+ T lymphocytes injected into severe combined immunodeficient (SCID) mice lead to an inflammatory and lethal bowel disease. Clin Exp Immunol 1996; 104: 491-500.
108. Morrissey PJ, Charrier K. Induction of wasting disease in SCID mice by the transfer of normal CD4+/CD45RBhi T cells and the regulation of this autoreactivity by CD4+/CD45RB1o T cells. Res Immunol 1994; 145: 357-62.
109. Zhang X, Izikson L, Liu L, Weiner HL. Activation of CD25(+)CD4(+) regulatory T cells by oral antigen administration. J Immunol 2001; 167: 4245-53.
110. Zeitz M, Greene WC, Peffer NJ, James SP. Lymphocytes isolated from the intestinal lamina propria of normal nonhuman primates have increased expression of genes associated with T-cell activation. Gastroenterology 1988; 94: 647-55.
111. Kojima A, Prehn RT: Genetic susceptibility to post-thymectomy autoimmune diseases in mice. Immunogenetics 1981; 14: 15-27.
112. Sakaguchi S, Fukuma K, Kuribayashi K, Masuda T. Organ-specific autoimmune diseases induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J Exp Med 1985; 161: 72-87.
113. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. 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 1995; 155: 1151-64.
114. Sugihara S, Izumi Y, Yoshioka T, Yagi H, Tsujimura T, Tarutani O et al. Autoimmune thyroiditis induced in mice depleted of particular T cell subsets. I. Requirement of Lyt-1 dull L3T4 bright normal T cells for the induction of thyroiditis. J Immunol 1988; 141: 105-13.
115. McKeever U, Mordes JP, Greiner DL, Appel MC, Rozing J, Handler ES et al. Adoptive transfer of autoimmune diabetes and thyroiditis to athymic rats. Proc Natl Acad Sci U S A 1990; 87: 7618-22.
116. Asano M, Toda M, Sakaguchi N, Sakaguchi S: Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 1996; 184: 387-96.
117. Smith H, Lou YH, Lacy P, Tung KS. Tolerance mechanism in experimental ovarian and gastric autoimmune diseases. J Immunol 1992; 149: 2212-18.
118. Sakaguchi S, Takahashi T, Nishizuka Y. Study on cellular events in post-thymectomy autoimmune oophoritis in mice. II. Requirement of Lyt-1 cells in normal female mice for the prevention of oophoritis. J Exp Med 1982; 156: 1577-86.
119. Mordes JP, Gallina DL, Handler ES, Greiner DL, Nakamura N, Pelletier A et al. Transfusions enriched for W3/25+ helper/inducer T lymphocytes prevent spontaneous diabetes in the BB/W rat. Diabetologia 1987; 30: 22-26.
120. Boitard C, Yasunami R, Dardenne M, Bach JF. T cell-mediated inhibition of the transfer of autoimmune diabetes in NOD mice. J Exp Med 1989; 169: 1669-80.
121. Sakaguchi N, Miyai K, Sakaguchi S. Ionizing radiation and autoimmunity. Induction of autoimmume disease in mice by high dose fractionated total lymphoid irradiation and its prevention by inoculating normal T cells. J Immunol 1994; 152: 2586-95.
122. Fowell D, Mason D. Evidence that the T cell repertoire of normal rats contains cells with the potential to cause diabetes. Characterization of the CD4+ T cell subset that inhibits this autoimmune potential. J Exp Med 1993; 177: 627-36.
123. Stephens LA, Mottet C, Mason D, Powrie F. Human CD4(+)CD25(+) thymocytes and peripheral T cells have immune suppressive activity in vitro. Eur J Immunol 2001; 31: 1247-54.
124. Tivol EA, Boyd SD, McKeon S, Borriello F, Nickerson P, Strom TB. CTLA4Ig prevents lymphoproliferation and fatal multiorgan tissue destruction in CTLA-4-deficient mice. J Immunol 1997; 158: 5091-94.
125. Greenwald RJ, Boussiotis VA, Lorsbach RB, Abbas AK, Sharpe AH. CTLA-4 regulates induction of anergy in vivo. Immunity 2001; 14: 145-55.
126. Perez VL, Van Parijs L, Biuckians A, Zheng XX, Strom TB, Abbas AK. Induction of peripheral T cell tolerance in vivo requires CTLA-4 engagement. Immunity 1997; 6: 411-17.
127. Karandikar NJ, Vanderlugt CL, Walunas TL, Miller SD, Bluestone JA. CTLA-4: a negative regulator of autoimmune disease. J Exp Med 1996; 184: 783-88.
128. Beverly B, Kang SM, Lenardo MJ, Schwartz RH. Reversal of in vitro T cell clonal anergy by IL-2 stimulation. Int Immunol 1992; 4: 661-71.
129. Thornton AM, Shevach EM: CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998, 188: 287-96.
130. Ermann J, Szanya V, Ford GS, Paragas V, Fathman CG, Lejon K. CD4(+)CD25(+) T cells facilitate the induction of T cell anergy. J Immunol 2001; 167: 4271-75.