Immunology: Antigen-Presenting Cells in the Gut

Journal of Biomedical Science

Volumn 11, Issue 2, 2004, Pages 130-141

  Makala, Levi H C ^a   Nishikawa, Yoshifumi ^a   Suzuki, Naoyoshi ^a   Nagasawa, Hideyuki ^a  

^a OBIHIRO UNIVERSITY OF AGRICULTURE AND VETERINARY MEDICINE   (Japan)

Author keywords

Antigen presenting cell; Gut; Lamina propria; Mouse; Peyer's patch

Indexed keywords

ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; CELLULAR IMMUNITY; HUMAN; HUMORAL IMMUNITY; IMMUNITY; IMMUNOREGULATION; INTESTINE; INTESTINE MUCOSA; LAMINA PROPRIA; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PEYER PATCH; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE;

ANIMALS; ANTIGEN-PRESENTING CELLS; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; HUMANS; INTESTINES; LYMPHOID TISSUE; MACROPHAGES;

EID: 1442304347     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1159/000076025     Document Type: Review

References (138)

1. Allan CH, Mendrick DL, Trier JS. Rat intestinal M cells contain acidic endosomal-lysosomal compartments and express class II major histocompatibility complex determinants. Gastroenterology 104:698-708;1993.
2. Bailey M, Plunkett FJ, Rothkotter HJ, Vega-Lopez MA, Haverson K, Stokes CR. Regulation of mucosal immune responses in effector sites. Proc Nutr Soc 60:427-435;2001.
3. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 392:245-252;1998.
4. Besredka A. De la vaccination contre les états typhoídes par la voie buccale. Annals Inst Pasteur, Paris 33:882;1919.
5. Besredka A. Local Immunization. Bailliere, Tyndal & Cox, p 48, 1927.
6. Binns RM, Licence ST. Patterns of migration of labeled blood lymphocyte subpopulations: Evidence for two types of Peyer's patches in the young pigs. Adv Exp Med Biol 186:661-668;1985.
7. 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 74:270-275;1988.
8. Bjerke K, Halstensen TS, Jahnsen F, Pulford K, Brandtzaeg P. Distribution of macrophages and granulocytes expressing L1 protein (calprotectin) in human Peyer's patches compared with normal ileal lamina propria and mesenteric lymph nodes. Gut 34:1357-1363;1993.
9. Bland PW, Bailey M. Immunology of the small intestine. Transplant Proc 30:2560-2561;1998.
10. Bland PW, Warren LG. Antigen presentation by epithelial cells of the rat small intestine. II. Selective induction of suppressor T cells. Immunology 58:9-14;1986.
11. Bland PW, Warren LG. Antigen presentation by epithelial cells of the rat small intestine. I. Kinetics, antigen specificity and blocking by anti-Ia antisera. Immunology 58:1-7;1986.
12. Blumberg RS, Terhorst C, Bleicher P, McDermott FV, Allan CH, Landau SB, Trier JS, Balk SP. Expression of a nonpolymorphic MHC class I-like molecule, CD1D, by human intestinal epithelial cells. J Immunol 147:2518-2524;1991.
13. Boismenu R, Chen Y, Havran WL. The role of intraepithelial gamma-delta T cells: A gut-feeling. Microbes Infect 1:235-240;1999.
14. Boismenu R, Havran WL. An innate view of gamma-delta T cells. Curr Opin Immunol 9: 57-63;1997.
15. Boismenu R, Havran WL. Modulation of epithelial cell growth by intraepithelial gamma delta T cells. Science 266:1253-1255 ;1994.
16. Boismenu R, Semeniuk D, Murgita RA. Purification and characterization of human and mouse recombinant alpha-fetoproteins expressed in Escherichia coli. Protein Expr Purif 10:10-26;1997.
17. Boismenu R, Wu T, Havran WL, Chen Y. Role of gamma-delta T cells in a murine colitis model. Fed Proc 12:A593-A595;1998.
18. Borghesi C, Regoli M, Bertelli E, Nicoletti C. Modifications of the follicle-associated epithelium by short-term exposure to a non-intestinal bacterium. J Pathol 180:326-332;1996.
19. Brandtzaeg P, Berstad AE, Farstad IN, Haraldsen G, Helgeland L, Jahnsen FL, Johansen FE, Natvig IB, Nilsen EM, Rugtveit J. Mucosal immunity - a major adaptive defence mechanism. Behring Inst Mitt 98:1-23;1997.
20. Chesnut RW, Grey HM. Antigen presentation by B cells and its significance in T-B interactions. Adv Immunol 39:51-94;1986.
21. Craig SW, Cebra JJ. Peyer's patches: An enriched source of precursors for IgA-producing immunocytes in the rabbit. J Exp Med 134:188-200;1971.
22. Cumberbatch M, Kimber I. Dermal tumour necrosis factor-alpha induces dendritic cell migration to draining lymph nodes, and possibly provides one stimulus for Langerhans' cell migration. Immunology 75:257-263;1992.
23. Ermak TH, Owen RL. Differential distribution of lymphocytes and accessory cells in mouse Peyer's patches. Anat Rec 215:144-152;1986.
24. Ermak TH, Steger HJ, Pappo J. Phenotypically distinct subpopulations of T cells in domes and M-cell pockets of rabbit gut-associated lymphoid tissues. Immunology 71:530-537;1990.
25. Fagarasan S, Kinoshita K, Muramatsu M, Ikuta K, Honjo T. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413:639-643;2001.
26. Fagarasan S, Shinkura R, Kamata T, Nogaki F, Ikuta K, Honjo T. Mechanism of B1 cell differentiation and migration in GALT. Curr Top Microbiol Immunol 252:221-229;2000.
27. Farstad IN, Halstensen TS, Fausa O, Brandtzaeg P. Heterogeneity of M-cell-associated B and T cells in human Peyer's patches. Immunology 83:457-464;1994.
28. Forbes GM, Horne R, Erber WN, Collins BJ, Papadimitriou JM. Ultrastructural evidence of intestinal mucosal macrophage activation after bone marrow transplantation. Pathology 28:251-254;1996.
29. Fujihashi K, Dohi T, Rennert PD, Yamamoto M, Koga T, Kiyono H, McGhee JR. Peyer's patches are required for oral tolerance to proteins. Proc Natl Acad Sci USA 98:3310-3315;2001.
30. Fujihashi K, Kato H, van Ginkel FW, Koga T, Boyaka PN, Jackson RJ, Kato R, Hagiwara Y, Etani Y, Goma I, Fujihashi K, Kiyono H, McGhee JR. A revisit of mucosal IgA immunity and oral tolerance. Acta Odontol Scand 59:301-308;2001.
31. Gebert A, Rothkotter HJ, Pabst R. M cells in Peyer's patches of the intestine. Int Rev Cytol 167:91-159;1996.
32. Gerrard TL, Volkman DJ, Jurgensen CH, Fauci AS. Activated human T cells can present alloantigens but cannot present soluble antigens. Cell Immunol. 95:65-74;1985.
33. Griebel PJ, Hein WR. Expanding the role of Peyer's patches in B-cell ontogeny. Immunol Today 17:30-39;1996.
34. Grimm MC, Pullman WE, Bennett GM, Sullivan PJ, Pavli P, Doe WF. Direct evidence of monocyte recruitment to inflammatory bowel disease mucosa. J Gastroenterol Hepatol 10:387-395;1995.
35. Guy-Grand D, Vassalli P. Gut intraepithelial T lymphocytes. Curr Opin Immunol 5:247-252;1993.
36. Hanninen A, Harrison LC. Gamma delta T cells as mediators of mucosal tolerance: The autoimmune diabetes model. Immunol Rev 173:109-119;2000.
37. Haraldsen G, Sollid LM, Bakke O, Farstad IN, Kvale D, Molberg, Norstein J, Stang E, Brandtzaeg P. Major histocompatibility complex class II-dependent antigen presentation by human intestinal endothelial cells. Gastroenterology 114:649-656;1998.
38. Harper HM, Cochrane L, Williams NA. The role of small intestinal antigen-presenting cells in the induction of T-cell reactivity to soluble protein antigens: Association between aberrant presentation in the lamina propria and oral tolerance. Immunology 89:449-456;1996.
39. Haverson K, Bailey M, Stokes CR. T-cell populations in the pig intestinal lamina propria: Memory cells with unusual phenotypic characteristics. Immunology 96:66-73;1999.
40. Haverson K, Singha S, Stokes CR, Bailey M. Professional and non-professional antigen presenting cells in the porcine small intestine. Immunology 101:492-500;2000.
41. Holt PG, Britten D, Sedgwick JD. Suppression of IgE responses by antigen inhalation: Studies on the role of genetic and environmental factors. Immunology 60:97-102;1987.
42. Hummel KP. The structure and development of the lymphatic tissues in the intestine of the albino rat. Am J Anat 57:351-364;1965.
43. Jarry A, Robaszkiewicz M, Brousse N, Potet F. Immune cells associated with M cells in the follicle-associated epithelium of Peyer's patches in the rat. An electron- and immuno-electronmicroscopic study. Cell Tissue Res 255:293-298;1989.
44. Jones BD, Ghori N, Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 180:15-23;1994.
45. Kambarage D, Bland P, Stokes C. The accessory cell activity of porcine intestinal macrophages in the induction of T cell responses. J Vet Med Sci 56:1135-1138;1994.
46. Kambarage DM, Bland P, Stokes C. Comparison of the requirement of porcine peripheral blood monocytes and intestinal lamina propria macrophages as accessory cells in primary allogeneic mixed leukocyte responses and oxidative mitogenesis. J Vet Med Sci 57:617-621;1995.
47. Kelly RH. Localization of afferent lymph cells within the draining node during a primary immune response. Nature 227:510-513;1970.
48. Kelsall BL, Strober W. Dendritic cells of the gastrointestinal tract. Springer Semin Immunopathol 18:409-420;1997.
49. Kelsall BL, Strober W. Peyer's patch dendritic cells and the induction of mucosal immune responses. Res Immunol 148:490-498;1997b.
50. Kerneis S, Bogdanova A, Kraehenbuhl JP, Pringault E. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277:949-952;1997.
51. Kerneis S, Caliot E, Stubbe H, Bogdanova A, Kraehenbuhl J, Pringault E. Molecular studies of the intestinal mucosal barrier physiopathology using cocultures of epithelial and immune cells: A technical update. Microbes Infect 2:1119-1124;2000.
52. Kilshaw PJ. Expression of the mucosal T cell integrin alpha M290 beta 7 by a major subpopulation of dendritic cells in mice. Eur J Immunol 23:3365-3368;1993.
53. Kimber I, Cumberbatch M. Stimulation of Langerhans cell migration by tumor necrosis factor alpha (TNF-alpha). J Invest Dermatol 99:48S-50S;1992.
54. Knight SC, Farrant J, Bryant A, Edwards AJ, Burman S, Lever A, Clarke J, Webster AD. Non-adherent, low-density cells from human peripheral blood contain dendritic cells and monocytes, both with veiled morphology. Immunology 57:595-603;1986.
55. Kraehenbuhl JP, Neutra MR. Epithelial M cells: Differentiation and function. Annu Rev Cell Dev Biol 16:301-332;2000.
56. Lampert IA, Suitters AJ, Chisholm PM. Expression of Ia antigen on epidermal keratinocytes in graft-versus-host disease. Nature 293:149-150;1981.
57. Lanzavecchia A. Antigen-specific interaction between T and B cells. Nature 314:537-539;1985.
58. Larsen CP, Steinman RM, Witmer-Pack M, Hankins DF, Morris PJ, Austyn JM. Migration and maturation of Langerhans cells in skin transplants and explants. J Exp Med 172:1483-1493;1990.
59. Lefrancois L, Puddington L. Extrathymic intestinal T-cell development: Virtual reality? Immunol Today 16:16-21;1995.
60. Liu LM, MacPherson GG. Antigen acquisition by dendritic cells: Intestinal dendritic cells acquire antigen administered orally and can prime naive T cells in vivo. J Exp Med 177:1299-1307;1993.
61. Liu LM, MacPherson GG. Antigen processing by rat lymph-borne dendritic cells. Adv Exp Med Biol 378:215-217;1995a.
62. Liu LM, MacPherson GG. Antigen processing: Cultured lymph-borne dendritic cells can process and present native protein antigens. Immunology 84:241-246;1995b.
63. Liu LM, MacPherson GG. Lymph-borne (veiled) dendritic cells can acquire and present intestinally administered antigens. Immunology 73:281-286;1991.
64. Liu LM, MacPherson GG. Rat intestinal dendritic cells: Immunostimulatory potency and phenotypic characterization. Immunology 85:88-93;1995c.
65. Macatonia SE, Knight SC, Edwards AJ, Griffiths S, Fryer P. Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate. Functional and morphological studies. J Exp Med 166:1654-1667;1987.
66. MacDonald TT, Monteleone G. IL-12 and Th1 immune responses in human Peyer's patches. Trends Immunol 22:244-247;2001.
67. MacPherson GG, Jenkins CD, Stein MJ, Edwards C. Endotoxin-mediated dendritic cell release from the intestine. Characterization of released dendritic cells and TNF dependence. J Immunol 154:1317-1322;1995.
68. MacPherson GG. Properties of lymph-borne (veiled) dendritic cells in culture. I. Modulation of phenotype, survival and function: Partial dependence on GM-CSF. Immunology 68:102-107;1989.
69. Maeda Y, Noda S, Tanaka K, Sawamura S, Aiba Y, Ishikawa H, Hasegawa H, Kawabe N, Miyasaka M, Koga Y. The failure of oral tolerance induction is functionally coupled to the absence of T cells in Peyer's patches under germfree conditions. Immunobiology 204:442-457;2001.
70. Makala LH, Kamada T, Nagasawa H, Igarashi I, Fujisaki K, Suzuki N, Mikami T, Haverson K, Bailey M, Stokes CR, Bland PW. Ontogeny of pig discrete Peyer's patches: Expression of surface antigens. J Vet Med Sci 63:625-636;2001.
71. Makala LH, Reyes JC, Nishikawa Y, Tsushima Y, Xuan X, Huang X, Nagasawa H. A comparison of the phenotype of dendritic cells derived from discrete Peyer's patch macrophages of non-infected and Toxoplasma gondii infected mice. J Vet Med Sci 65:591-597;2003.
72. Makala LH, Reyes JC, Nishikawa Y, Tsushima Y, Xuan X, Huang X, Battsetseg B, Matsuo T, Nagasawa H. Phenotype and function of murine discrete Peyer's patch macrophage derived dendritic cells. J Vet Med Sci 65:491-499;2003.
73. Makala LH, Suzuki N, Nagasawa H. Peyer's patches: Organized lymphoid structures for the induction of mucosal immune responses. Pathobiology 70:58-68;2002/2003.
74. Makala LHC, Haverson K, Stokes CR, Bailey M, Bland PW. Isolation and characterization of pig Peyer's patch dendritic cells. Vet Immunol Immunopathol 61:67-81;1998.
75. Makala LHC, Kamada T, Nishikawa Y, Nagasawa H, Igarashi I, Fujisaki K, Suzuki N, Mikami T, Haverson K, Bailey M, Stokes CR, Bland PW. Ontogeny of pig discrete Peyer's patches: Distribution and morphometric analysis. Pathobiology 68:275-282;2000a.
76. Makala LHC, Nishikawa Y, Kamada T, Mishima M, Xuan X, Suzuki H, Fujisaki K, Nagasawa H. 2001. Phenotype and function of murine peritoneal cavity macrophage derived dendritic cells using growth factors. J Vet Med Sci 64:813-820;2002.
77. + dendritic cell populations in spleens of mice infected with Toxoplasma gondii. J Protozool Res 2000b, in press.
78. Makala LHC. Isolation and characterization of pig Peyer's patch dendritic cells, PhD thesis, University of Bristol, Bristol, 1996.
79. Maric I, Holt PG, Perdue MH, Bienenstock J. Class II MHC antigen (Ia)-bearing dendritic cells in the epithelium of the rat intestine. J Immunol 156:1408-1414;1996.
80. Mason DW, Dallman M, Barclay AN. Graft-versus-host disease induces expression of Ia antigen in rat epidermal cells and gut epithelium. Nature 293:150-151;1981.
81. Maus MV, Riley JL, Kwok WW, Nepom GT, June CH. HLA tetramer-based artificial antigen-presenting cells for stimulation of CD4+ T cells. Clin Immunol 106:16-22;2003.
82. Mayrhofer G, Spargo LD. Subcellular distribution of class II major histocompatibility antigens in enterocytes of the human and rat small intestine. Immunol Cell Biol 67:251-260;1989.
83. McCarron RM, Racke M, Spatz M, McFarlin DE. Cerebral vascular endothelial cells are effective targets for in vitro lysis by encephalitogenic T lymphocytes. J Immunol 147:503-508;1991.
84. McCarron RM, Wang L, Cowan EP, Spatz M. Class II MHC antigen expression by cultured human cerebral vascular endothelial cells. Brain Res 566:325-328;1991.
85. McMenamin C, Holt PG. The natural immune response to inhaled soluble protein antigens involves major histocompatibility complex (MHC) class I-restricted CD8+ T cell-mediated but MHC class II-restricted CD4+ T celldependent immune deviation resulting in selective suppression of immunoglobulin E production. J Exp Med 178:889-899;1993.
86. McMenamin C, Pimm C, McKersey M, Holt PG. Regulation of IgE responses to inhaled antigen in mice by antigen-specific gamma delta T cells. Science 265:1869-1871;1994.
87. Mellman I, Steinman RM. Dendritic cells: Specialized and regulated antigen processing machines. Cell 106:255-258;2001.
88. Mukasa A, Lahn M, Pflum EK, Born W, O'Brien RL. Evidence that the same gamma delta T cells respond during infection-induced and autoimmune inflammation. J Immunol 159:5787-5794;1997.
89. Nadler PI, Klingenstein RJ, Hodes RJ. Ontogeny of murine accessory cells: Ia antigen expression and accessory cell function in in vitro primary antibody responses. J Immunol 125:914-920;1980.
90. Nagura H, Ohtani H, Masuda T, Kimura M, Nakamura S. HLA-DR expression on M cells overlying Peyer's patches is a common feature of human small intestine. Acta Pathol Jpn 41:818-823;1991.
91. Neutra MR, Mantis NJ, Kraehenbuhl JP. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat Immunol 2:1004-1009;2001.
92. Nicoletti C. Unsolved mysteries of intestinal M cells. Gut 47:735-739;2000.
93. Nussenzweig MC, Steinman RM, Gutchinov B, Cohn ZA. Dendritic cells are accessory cells for the development of anti-trinitrophenyl cytotoxic T lymphocytes. J Exp Med 152:1070-1084;1980a.
94. Nussenzweig MC, Steinman RM. Contribution of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction. J Exp Med 151:1196-1212;1980b.
95. Onori P, Franchitto A, Sferra R, Vetuschi A, Gaudio E. Peyer's patches epithelium in the rat: A morphological, immunohistochemical, and morphometrical study. Dig Dis Sci 46:1095-1104;2001.
96. Owen JJ, Wright DE, Habu S, Raff MC, Cooper MD. Studies on the generation of B lymphocytes in fetal liver and bone marrow. J Immunol 118:2067-2072;1977.
97. Owen RL, Apple RT, Bhalla DK. Morphometric and cytochemical analysis of lysosomes in rat Peyer's patch follicle epithelium: Their reduction in volume fraction and acid phosphatase content in M cells compared to adjacent enterocytes. Anat Rec 216:521-527;1986a.
98. Owen RL, Nemanic P. Antigen processing structures of the mammalian intestinal tract: An SEM study of lymphoepithelial organs; in Scanning Electron Microscopy, SEM Inc., AMFO Hare, USA, Vol. II, 1978.
99. 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 153:1108-1118;1986b.
100. Owen RL. Sequential uptake of horseradish peroxidase by lymphoid follicle epithelium of Peyer's patches in the normal unobstructed mouse intestine: An ultrastructural study. Gastroenterology 72:440-451;1977.
101. Pavli P, Hume DA, Van De Pol E, Doe WF. Dendritic cells, the major antigen-presenting cells of the human colonic lamina propria. Immunology 78:132-141;1993.
102. Pavli P, Woodhams CE, Doe WF, Hume DA. Isolation and characterization of antigen-presenting dendritic cells from the mouse intestinal lamina propria. Immunology 70:40-47;1990.
103. Pober JS, Collins T, Gimbrone MA Jr, Cotran RS, Gitlin JD, Fiers W, Clayberger C, Krensky AM, Burakoff SJ, Reiss CS. Lymphocytes recognize human vascular endothelial and dermal fibroblast Ia antigens induced by recombinant immune interferon. Nature 305:726-729;1983.
104. Pober JS, Gimbrone MA Jr, Cotran RS, Reiss CS, Burakoff SJ, Fiers W, Ault KA. Ia expression by vascular endothelium is inducible by activated T cells and by human gamma interferon. J Exp Med 157:1339-1353;1983.
105. Poussier P, Julius M. Thymus independent T cell development and selection in the intestinal epithelium. Annu Rev Immunol 12:521-553;1994.
106. Pugh CW, MacPherson GG, Steer HW. Characterization of non-lymphoid cells derived from rat peripheral lymph. J Exp Med 157:1758-1779;1983.
107. Regoli M, Borghesi C, Bertelli E, Nicoletti C. A morphological study of the lymphocyte traffic in Peyer's patches after an in vivo antigenic stimulation. Anat Rec 239:47-54;1994.
108. Rosenwasser LJ, Rosenthal AS. Adherent cell function in murine T lymphocyte antigen recognition. II. Definition of genetically restricted and nonrestricted macrophage functions in T cell proliferation. J Immunol 121:2497-2501;1978.
109. Rosenwasser LJ, Rosenthal AS. Adherent cell function in murine T lymphocyte antigen recognition. I. A. macrophage-dependent T cell proliferation assay in the mouse. J Immunol 120:1991-1995;1978.
110. Rugtveit J, Nilsen EM, Bakka A, Carlsen H, Brandtzaeg P, Scott H. Cytokine profiles differ in newly recruited and resident subsets of mucosal macrophages from inflammatory bowel disease. Gastroenterology 112:1493-1505;1997.
111. Shortman K, Caux C. Dendritic cell development: Multiple pathways to nature's adjuvants. Stem Cells 15:409-419;1997.
112. Smith PD, Janoff EN, Mosteller-Barnum M, Merger M, Orenstein JM, Kearney JF, Graham MF. Isolation and purification of CD14-negative mucosal macrophages from normal human small intestine. J Immunol Methods 202:1-11;1997.
113. Smith PD, Meng G, Shaw GM, Li L. Infection of gastrointestinal tract macrophages by HIV-1. J Leukoc Biol 62:72-77;1997.
114. Sobhon P. The light and electron microscopic studies of Peyer's patches in non-germ free adult mice. J Morphol 135:457-481;1971.
115. Spalding DM, Koopman WJ, Eldridge JH, McGhee JR, Steinman RM. Accessory cells in murine Peyer's patch. I. Identification and enrichment of a functional dendritic cell. J Exp Med 157:1646-1659;1983.
116. Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 9:271-296;1991.
117. Stingl G, Katz SI, Shevach EM, Wolff-Schreiner E, Green I. Detection of Ia antigens on Langerhans cells in guinea pig skin. J Immunol 120:570-578;1978.
118. Stokes CR, Bailey M, Wilson AD. Immunology of the porcine gastro-intestinal tract. Vet Immunol Immunopathol 43:143-150;1994.
119. Stokes CR, Bailey M. The porcine gastrointestinal lamina propria: An appropriate target for mucosal immunisation? J Biotechnol 83:51-55;2000.
120. Stokes CR, Haverson K, Bailey M. Antigen presenting cells in the porcine gut. Vet Immunol Immunopathol 54:171-177;1996.
121. Szczepanik M, Anderson LR, Ushio H, Ptak W, Owen MJ, Hayday AC, Askenase PW. Gamma delta T cells from tolerized alpha beta T cell receptor (TCR)-deficient mice inhibit contact sensitivity-effector T cells in vivo, and their interferon-gamma production in vitro. J Exp Med 184:2129-2139;1996.
122. Szczepanik M, Nowak B, Askenase PW, Ptak W. Cross-talk between gamma delta T lymphocytes and immune cells in humoral response. Immunology 95:612-617;1998.
123. Thomas AK, Maus MV, Shalaby WS, June CH, Riley JL. A cell-based artificial antigenpresenting cell coated with anti-CD3 and CD28 antibodies enables rapid expansion and long-term growth of CD4 T lymphocytes. Clin Immunol 105:259-272;2002.
124. Unanue ER, Beller DI, Lu CY, Allen PM. Antigen presentation: Comments on its regulation and mechanism. J Immunol 132:1-5;1984.
125. Viney JL, Mowat AM, O'Malley JM, Williamson E, Fanger NA. Expanding dendritic cells in vivo enhances the induction of oral tolerance. J Immunol 160:5815-5825;1998.
126. Waraich T, Sarsfield P, Wright DH. The accessory cell populations in ulcerative colitis: A comparison between the colon and appendix in colitis and acute appendicitis. Hum Pathol 28:297-303;1997.
127. Wilcox CE, Baker D, Butter C, Willoughby DA, Turk JL. Differential expression of guinea pig class II major histocompatibility complex antigens on vascular endothelial cells in vitro and in experimental allergic encephalomyelitis. Cell Immunol 120:82-91;1989.
128. Wilders MM, Drexhage HA, Weltevreden EF, Mullink H, Duijvestijn A, Meuwissen SG. Large mononuclear Ia-positive veiled cells in Peyer's patches. I. Isolation and characterization in the rat, guinea-pig and pig. Immunology 48:453-460;1983.
129. Wilders MM, Sminia T, Plesch BE, Drexhage HA, Weltevreden EF, Meuwissen SG. Large mononuclear Ia-positive veiled cells in Peyer's patches. II. Localization in rat Peyer's patches. Immunology 48:461-467;1983.
130. Williams NA, Wilson AD, Bailey M, Bland PW, Stokes CR. Primary antigen-specific Tcell proliferative responses following presentation of soluble protein antigen by cells from the murine small intestine. Immunology 75:608-613;1992.
131. Wilson AD, Bailey M, Williams NA, Stokes CR. The in vitro production of cytokines by mucosal lymphocytes immunized by oral administration of keyhole limpet hemocyanin using cholera toxin as an adjuvant. Eur J Immunol 21:2333-2339;1991.
132. Wilson AD, Haverson K, Southgate K, Bland PW, Stokes CR, Bailey M. Expression of major histocompatibility complex class II antigens on normal porcine intestinal endothelium. Immunology 88:98-103;1996.
133. Woodhead VE, Binks MH, Chain BM, Katz DR. From sentinel to messenger: An extended phenotypic analysis of the monocyte to dendritic cell transition. Immunology 94:552-559;1998.
134. Yamamoto M, Rennert P, McGhee JR, Kweon MN, Yamamoto S, Dohi T, Otake S, Bluethmann H, Fujihashi K, Kiyono H. Alternate mucosal immune system: Organized Peyer's patches are not required for IgA responses in the gastrointestinal tract. J Immunol 164:5184-5191;2000.
135. Yamanaka T, Straumfors A, Morton H, Fausa O, Brandtzaeg P, Farstad I. M cell pockets of human Peyer's patches are specialized extensions of germinal centers. Eur J Immunol 31:107-117;2001.
136. Zeitz M, Schieferdecker HL, James SP, Riecken EO. Special functional features of Tlymphocyte subpopulations in the effector compartment of the intestinal mucosa and their relation to mucosal transformation. Digestion 46:280-289;1990.
137. Zeitz M, Schieferdecker HL, Ullrich R, Jahn HU, James SP, Riecken EO. Phenotype and function of lamina propria T lymphocytes. Immunol Res 10:199-206;1991.
138. Zembala M, Uracz W, Ruggiero I, Mytar B, Pryjma J. Isolation and functional characteristics of FcR+ and FcR- human monocyte subsets. J Immunol 133:1293-1299;1984.