Chapter 14 : Regional Immune Response to Microbial Pathogens

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The distribution of organized mucos-aassociated lymphoid tissues (MALT) in mucosal tissues of the body varies among species, but there are certain consistent patterns. The sequence of events involved in processing and presentation of foreign antigens by professional antigen-presenting cells and the responses and interactions of local lymphocytes that lead to the production of effector and memory cells are likely to be similar in the mucosal and systemic branches of the immune system. Alternatively, dendritic cells (DCs) located in the epithelium over organized MALT, such as those that are abundant in the tonsils, could present antigens either in local MALT or after migration to draining lymph nodes. In addition, the class I-related molecule CD1d is expressed at the basolateral surfaces of intestinal epithelial cells and appears to function as an antigen presenting molecule by interacting with specialized populations of T cells. The possible role of antigen uptake by enterocytes in induction of immune responses or immune tolerance is discussed. The mucosal addressin MadCam-1 (mucosal addressin cell adhesion molecule 1) is preferentially expressed in human and mouse intestinal flat postcapillary venules of the lamina propria and high endothelial venules of organized MALT but not in other mucosal tissues. When microbial pathogens adhere to or invade the epithelial cells that line mucosal surfaces, the cells release proinflammatory cytokines and chemokines and upregulate chemokine receptors and adhesion molecules.

Citation: Neutra M, Kraehenbuhl J. 2002. Regional Immune Response to Microbial Pathogens, p 191-206. In Kaufmann S, Sher A, Ahmed R (ed), Immunology of Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817978.ch14

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1. Allan, C. H.,, D. L. Mendrick,, and J. S. Trier. 1993. Rat intestinal epithelial M cells contain acidic endosomal-lysosomal compartments and express class II major histocompatibility complex determinants. Gastroenterology 104: 698 708.
2. Allan, C. H.,, and J. S. Trier. 1991. Structure and permeability differ in subepithelial villus and Peyer’s patch follicle capillaries. Gastroenterology 100: 1172 1179.
3. Amerongen, H. M.,, R. A. Weltzin,, C. M. Farnet,, P. Michetti,, W. A. Haseltine,, and M. R. Neutra. 1991. Transepithelial transport of HIV-1 by intestinal M cells: a mechanism for transmission of AIDS. J. Acquired Immune Defic. Syndr. 4: 760 765.
4. Amerongen, H. M.,, G. A. R. Wilson,, B. N. Fields,, and M. R. Neutra. 1994. Proteolytic processing of reovirus is required for adherence to intestinal M cells. J. Virol. 68: 8428 8432.
5. Arstila, T.,, T. P. Arstila,, S. Calbo,, F. Selz,, M. Malassis-Seris,, P. Vassalli,, P. Kourilsky,, and D. Guy-Grand. 2000. Identical T cell clones are located within the mouse gut epithelium and lamina propria and circulate in the thoracic duct lymph. J. Exp. Med. 191: 823 834.
6. Baggiolini, M. 1998. Chemokines and leukocyte traffic. Nature 392: 565 568.
7. Bäumler, A. J.,, R. M. Tsolis,, F. A. Bowe,, J. G. Kusters,, S. Hoffmann,, and F. Heffron. 1996. The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infect. Immun. 64: 61 68.
8. Belyakov, I. M.,, B. Moss,, W. Strober,, and J. A. Berzofsky. 1999. Mucosal vaccination overcomes the barrier to recombinant vaccinia immunization caused by preexisting poxvirus immunity. Proc. Natl. Acad. Sci. USA 96: 4512 4517.
9. Belyakov, I. M.,, L. S. Wyatt,, J. D. Ahlers,, P. Earl,, C. D. Pendleton,, B. L. Kelsall,, W. Strober,, B. Moss,, and J. A. Berzofsky. 1998. Induction of a mucosal cytotoxic T-lymphocyte response by intrarectal immunization with a replication-deficient recombinant vaccinia virus expressing human immunodeficiency virus 89.6 envelope protein. J. Virol. 72: 8264 8272.
10. Berstad, A. K. H.,, J. Holst,, B. Møgster,, I. L. Haugen,, and B. Haneberg. 1997. A nasal whole-cell pertussis vaccine can induce strong systemic and mucosal antibody responses which are not enhanced by cholera toxin. Vaccine 15: 1473.
11. Bienenstock, J.,, M. R. McDermott,, and R. L. Clancy,. 1999. Respiratory tract defenses: role of mucoal lymphoid tissues, p. 283 292. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology. Academic Press, Inc., New York, N.Y.
12. Blumberg, R. S.,, W. I. Lencer,, X. Zhu,, H. S. Kim,, S. Claypool,, S. P. Balk,, L. J. Saubermann,, and S. P. Colgan. 1999. Antigen presentation by intestinal epithelial cells. Immunol. Lett. 69: 7 11.
13. Boismenu, R.,, L. Feng,, Y. Y. Xia,, J. C. Chang,, and W. L. Havran. 1996. Chemokine expression by intraepithelial gamma delta T cells. Implications for the recruitment of inflammatory cells to damaged epithelia. J. Immunol. 157: 985 992.
14. Boismenu, R.,, and W. L. Havran. 1994. Modulation of epithelial cell growth by intraepithelial gamma delta T cells. Science 266: 1253 1255.
15. Bomsel, M. 1997. Transcytosis of infectious human immunodeficiency virus across a tight human epithelial cell line barrier. Nat. Med. 3: 42 47.
16. Borghesi, C.,, M. J. Taussig,, and C. Nicoletti. 1999. Rapid appearance of M cells after microbial challenge is restricted at the periphery of the follicle-associated epithelium of Peyer’s patch. Lab. Investig. 79: 1393 1401.
17. Brandtzaeg, P.,, E. S. Baekkevold,, I. N. Farstad,, F. L. Jahnsen,, F. E. Johansen,, E. M. Nilsen,, and T. Yamanaka. 1999a. Regional specialization in the mucosal immune system: what happens in the microcompartments? Immunol. Today 20: 141 151.
18. Brandtzaeg, P.,, and I. N. Farstad,. 1999. The human mucosal B cell system, p. 439 468. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology. Academic Press, Inc., New York, N.Y.
19. Brandtzaeg, P.,, I. N. Farstad,, and G. Haraldsen. 1999b. Regional specialization in the mucosal immune system: primed cells do not always home along the same track. Immunol. Today 20: 267 277.
20. Briskin, M.,, D. Winsorhines,, A. Shyjan,, N. Cochran,, S. Bloom,, J. Wilson,, L. M. McEvoy,, E. C. Butcher,, N. Kassam,, C. R. Mackay,, W. Newman,, and D. J. Ringler. 1997. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am. J. Pathol. 151: 97 110.
21. Bromander, A. K.,, L. Ekman,, M. Kopf,, J. G. Nedrud,, and N. Y. Lycke. 1996. IL-6-deficient mice exhibit normal mucosal IgA responses to local immunizations and Helicobacter felis infection. J. Immunol. 156: 4290 4297.
22. Butcher, E. C.,, and L. J. Picker. 1996. Lymphocyte homing and homeostasis. Science 272: 60 66.
23. Bye, W. A.,, C. H. Allan,, and J. S. Trier. 1984. Structure, distribution and origin of M cells in Peyer’s patches of mouse ileum. Gastroenterology 86: 789 801.
24. Campbell, N.,, X. Y. Yio,, L. P. So,, Y. Li,, and L. Mayer. 1999. The intestinal epithelial cell: processing and presentation of antigen to the mucosal immune system. Immunol. Rev. 172: 315 324.
25. Chen, Y. H.,, J. Inobe,, R. Marks,, P. Gonnella,, V. K. Kuchroo,, and H. L. Weiner. 1995. Peripheral deletion of antigen-reactive t cells in oral tolerance. Nature 376: 177 180.
26. Choudari, C. P.,, S. O’Mahony,, G. Brydon,, O. Mwantembe,, and A. Ferguson. 1993. Gut lavage fluid protein concentrations: objective measures of disease activity in inflammatory bowel disease. Gastroenterology 104: 1064 1071.
27. Cone, R. A., 1999. Mucus, p. 43 64. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.) Mucosal Immunology. Academic Press, Inc., New York, N.Y.
Corthésy, B.,, M. Kaufmann,, A. Phalipon,, M. C. Peitsch,, M. R. Neutra,, and J.-P. Kraehenbuhl. 1996. A pathogen-specific epitope inserted into recombinant secretory immunoglobulin A is immunogenic by the oral route. J. Biol. Chem. 271: 3367033677..
29. Cui, Z.-D.,, D. Tristram,, L. J. LaScolea,, T. J. Kwiatkovski,, S. Kopti,, and P. L. Ogra. 1991. Induction of antibody response to Chlamydia trachomatis in the genital tract by oral immunization. Infect. Immun. 59: 1465 1469.
30. Czerkinsky, C.,, J. B. Sun,, and J. Holmgren. 1999. Oral tolerance and anti-pathological vaccines. Curr. Top. Microbiol. Immunol. 236: 79 92.
31. Desvignes, C.,, F. Esteves,, N. Etchart,, C. Bella,, C. Czerkinsky,, and D. Kaiserlian. 1998. The murine buccal mucosa is an inductive site for priming class I restricted CD8(+) effector T cells in vivo. Clin. Exp. Immunol. 113: 386 393.
32. Dickinson, B. L.,, K. Badizadegan,, Z. Wu,, J. C. Ahouse,, X. P. Zhu,, N. E. Simister,, R. S. Blumberg,, and W. I. Lencer. 1999. Bidirectional FcRn-dependent IgG transport in a polarized human intestinal epithelial cell line. J. Clin. Investig. 104: 903 911.
33. Dunn-Walters, D. K.,, M. Hackett,, L. Boursier,, P. J. Ciclitira,, P. Morgan,, S. J. Challacombe,, and J. Spencer. 2000. Characteristics of human IgA and IgM genes used by plasma cells in the salivary gland resemble those used in duodenum but not those used in the spleen. J. Immunol. 164: 1595 1601.
34. Dwinell, M. B.,, L. Eckmann,, J. D. Leopard,, N. M. Varki,, and M. F. Kagnoff. 1999. Chemokine receptor expression by human intestinal epithelial cells. Gastroenterology 117: 359 367.
35. Ermak, T. H.,, and R. L. Owen. 1994. Differential distribution of lymphocytes and accessory cells in mouse Peyer’s patches. Am. J. Trop. Med. Hyg. 50: S14 S28.
36. Eynon, E. E.,, and D. C. Parker. 1993. Parameters of tolerance induction by antigen targeted to B lymphocytes. J. Immunol. 151: 2958 2964.
37. Farstad, I. N.,, T. S. Halstensen,, O. Fausa,, and P. Brandtzaeg. 1994. Heterogeneity of M-cell-associated B and T cells in human Peyer’s patches. Immunology 83: 457 464.
38. Farstad, I. N.,, J. Norstein,, and P. Brandtzaeg. 1997. Phenotypes of B and T cells in human intestinal and mesenteric lymph. Gastroenterology 112: 163 173.
39. Finlay, B. B.,, and P. Cossart. 1997. Exploitation of mammalian host cell functions by bacterial pathogens. Science 276: 718 725.
40. Finzi, G.,, M. Cornaggia,, C. Capella,, R. Fiocca,, F. Bosi,, E. Solcia,, and I. M. Samloff. 1993. Cathepsin E in follicle associated epithelium of intestine and tonsils: localization to M cells and possible role in antigen processing. Histochemistry 99: 201 211.
41. Förster, R.,, A. E. Mattis,, E. Kremmer,, E. Wolf,, G. Brem,, and M. Lipp. 1996. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatamic compartments of the spleen. Cell 87: 1037 1047.
42. Forstner, J. F.,, M. G. Oliver,, and F. A. Sylvester,. 1995. Production, structure, and biological relevance of gastrointestinal mucins, p. 71 88. In M. Blaser,, P. D. Smith,, J. I. Ravdin,, H. B. Greenberg,, and R. L. Guerrant (ed.), Infections of the Gastrointestinal Tract. Raven Press, New York, N.Y.
43. Franco, M. A.,, C. Tin,, and H. B. Greenberg. 1997. CD8 + T cells can mediate almost complete short-term and partial long-term immunity to rotavirus in mice. J. Virol. 71: 4165 4170.
44. Frey, A.,, K. T. Giannasca,, R. Weltzin,, P. J. Giannasca,, H. Reggio,, W. I. Lencer,, and M. R. Neutra. 1996. Role of the glycocalyx in regulating access of microparticles to apical plasma membranes of intestinal epithelial cells—implications for microbial attachment and oral vaccine targeting. J. Exp. Med. 184: 1045 1059.
45. Fuchs, E. J.,, and P. Matzinger. 1992. B cells turn off virgin but not memory T cells. Science 258: 1156 1159.
46. Gebert, A.,, S. Fassbender,, K. Werner,, and A. Weissferdt. 1999. The development of M cells in Peyer’s patches is restricted to specialized dome-associated crypts. Am. J. Pathol. 154: 1573 1582.
47. Geijtenbeek, T. B. H.,, D. S. Kwon,, R. Torensma,, S. J. van Vliet,, G. C. F. van Duijnhoven,, J. Middel,, I. Cornelissen,, H. Nottet,, V. N. KewalRamani,, D. R. Littman,, C. G. Figdor,, and Y. van Kooyk. 2000. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 100: 587 597.
48. Giannasca, K. T.,, P. J. Giannasca,, and M. R. Neutra. 1996. Adherence of Salmonella typhimurium to Caco-2 cells: identification of a glycoconjugate receptor. Infect. Immun. 64: 135 145.
49. Giannasca, P. J.,, K. T. Giannasca,, P. Falk,, J. I. Gordon,, and M. R. Neutra. 1994. Regional differences in glycoconjugates of intestinal M cells in mice: potential targets for mucosal vaccines. Am. J. Physiol. 267: G1108 G1121.
50. Gordon, J. I.,, and M. L. Hermiston. 1994. Differentiation and self-renewal in the mouse gastrointestinal epithelium. Curr. Opin. Cell Biol. 6: 795 803.
51. Gunn, M. D.,, V. N. Ngo,, K. M. Ansel,, E. H. Ekland,, J. G. Cyster,, and L. T. Williams. 1998. A B-cell-homing chemokine made in lymphoid follicles activates Burkitts-lymphoma receptor-1. Nature 391: 799 803.
52. Haneberg, B.,, D. Kendall,, H. M. Amerongen,, F. M. Apter,, J. P. Kraehenbuhl,, and M. R. Neutra. 1994. Induction of specific immunoglobulin A in the small intestine, colon-rectum, and vagina measured by a new method for collection of secretions from local mucosal surfaces. Infect. Immun. 62: 15 23.
53. Hein, W. R. 1999. Organization of mucosal lymphoid tissue. Curr. Top. Microbiol. Immunol. 236: 1 15.
54. Hocini, H.,, A. Barra,, L. Bélec,, S. Iscaki,, J.-L. Preud’homme,, J. Pillot,, and J.-P. Bouvet. 1995. Systemic and secretory humoral immunity in the normal human vaginal tract. Scand. J. Immunol. 42: 269 274.
55. Holmgren, J.,, C. Czerkinsky,, N. Lycke,, and A. M. Svennerholm. 1992. Mucosal immunity: implications for vaccine development. Immunobiology 184: 157 179.
56. Holt, P. G. 1994. Immunoprophylaxis of atopy: light at the end of the tunnel? Immunol. Today 15: 484 489.
57. Holt, P. G.,, S. Haining,, D. J. Nelson,, and J. D. Sedgwick. 1994. Origin and steady-state turnover of class II MHC-bearing dendritic cells in the epithelium of the conducting airways. J. Immunol. 153: 256 261.
58. Hopkins, S.,, J. P. Kraehenbuhl,, F. Schödel,, A. Potts,, D. Peterson,, P. De Grandi,, and D. Nardelli-Haefliger. 1995. A recombinant Salmonella typhimurium vaccine induces local immunity by four different routes of immunization. Infect. Immun. 63: 3279 3286.
59. Hopkins, S.,, F. Niedergang,, I. E. Corthésy-Theulaz,, and J. P. Kraehenbuhl. 2000. A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer’s patch dendritic cells. Cell. Microbiol. 2: 56 68.
60. Hordnes, K.,, T. Tynning,, T. A. Brown,, B. Haneberg,, and R. Jonsson. 1997. Nasal immunization with group B streptococci can induce high levels of specific IgA antibodies in cervicovaginal secretions in mice. Vaccine 15: 1244 1251.
61. Hordnes, K.,, T. Tynning,, A. I. Kvam,, R. Jonsson,, and B. Haneberg. 1996. Colonization in the rectum and uterine cervix with group B streptococci may induce specific antibody responses in cervical secretions of pregnant women. Infect. Immun. 64: 1643 1652.
62. Hoyne, G. F.,, I. Le Roux,, M. Corsin-Jimenez,, K. Tan,, J. Dunne,, L. M. G. Forsyth,, M. J. Dallman,, M. J. Owen,, D. Ish-Horowicz,, and J. R. Lamb. 2000. Serrate 1-induced Notch signalling regulates the decision between immunity and tolerance made by peripheral CD4(+) T cells. Int. Immunol. 12: 177 185.
63. Huang, F. P.,, N. Platt,, M. Wykes,, J. R. Major,, T. J. Powell,, C. D. Jenkins,, and G. G. MacPherson. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J. Exp. Med. 191: 435 443.
64. Huang, G. T. J.,, L. Eckmann,, T. C. Savidge,, and M. F. Kagnoff. 1996. Infection of human intestinal epithelial cells with invasive bacteria upregulates apical intercellular adhesion molecule-1 (ICAM-1) expression and neutrophil adhesion. J. Clin. Invest. 98: 572 583.
65. Hussain, L. A.,, C. G. Kelly,, E. M. Hecht,, R. Fellowes,, M. Jourdan,, and T. Lehner. 1991. The expression of Fc receptors for immunoglobulin G in human rectal epithelium. AIDS 5: 1089 1094.
66. Iwasaki, A.,, and B. L. Kelsall. 2000. Localization of distinct Peyer’s patch dendritic cell subsets and their recruitment by chemokines macrophage inflammatory protein (MIP)-3a, MIP3b, and secondary lymphoid organ chemokine. J. Exp. Med. 191: 1381 1393.
67. Izadpanah, A.,, M. B. Dwinell,, L. Eckmann,, N. M. Varki,, and M. F. Kagnoff. 2001. Regulated MIP-3/CCL20 production by human intestinal epithelium: mechanism for modulating mucosal immunity. Am. J. Physiol. 280: G710 G719.
68. Jones, B. D.,, N. Ghori,, and S. Falkow. 1994. 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.
69. Jung, H. C.,, L. Eckmann,, S. K. Yang,, A. Panja,, J. Fierer,, E. Morzycka-Wroblewska,, and M. F. Kagnoff. 1995. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J. Clin. Investig. 95: 55 65.
70. Kaiserlian, D. 1999. Antigen sampling and presentation in mucosal tissues: epithelial cells. Curr. Top. Microbiol. Immunol. 236: 55 78.
71. Kanamori, Y.,, K. Ishimaru,, M. Nanno,, K. Maki,, K. Ikuta,, and H. Nariuchi. 1996. Identification of novel lymphoid tissues in murine intestinal mucosa where clusters of c-kit + IL-7R + Thy1 + lympho-hematopoietic progenitors develop. J. Exp. Med. 184: 1449 1459.
72. Kato, T.,, and R. L. Owen,. 1999. Structure and function of intestinal mucosal epithelium, p. 115 132. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology. Academic Press, Inc., New York, N.Y.
73. Kelsall, B.,, and W. Strober,. 1999. Gut-associated lymphois tissue: antigen handling and T cell responses, p. 293 318. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology, Academic Press, Inc., New York, N.Y.
74. Kernéis, S.,, A. Bogdanova,, J. P. Kraehenbuhl,, and E. Pringault. 1997. Conversion by Peyer’s patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 277: 948 952.
75. Khoury, S. J.,, W. W. Hancock,, and H. L. Weiner. 1992. Oral tolerance to myelin basic protein and natural recovery from experimental autoimmune encephalomyelitis are associated with downregulation of inflammatory cytokines and differential upregulation of TGF-β, IL-4 and PGE expression in the brain. J. Exp. Med. 176: 1355 1364.
76. Khoury, S. J.,, O. Lider,, A. Al-Sabbagh,, and H. L. Weiner. 1990. Suppression of experimental autoimmune encephalomyelitis by oral administration of myelin basic protein. III. Synergistic effect of lipopolysaccharide. Cell. Immunol. 131: 302 310.
77. Kim, J. M.,, L. Eckmann,, T. C. Savidge,, D. C. Lowe,, T. Witthoft,, and M. F. Kagnoff. 1998. Apoptosis of human intestinal epithelial cells after bacterial invasion. J. Clin. Investig. 102: 1815 1823.
78. Klavinskis, L. S.,, L. A. Bergmeier,, L. Gao,, E. Mitchell,, R. G. Ward,, G. Layton,, R. Brookes,, N. J. Meyers,, and T. Lehner. 1996. Mucosal or targeted lymph node immunization of macaques with a particulate SIVp27 protein elicits virus-specific CTL in the genito-rectal mucosa and draining lymph nodes. J. Immunol. 157: 2521 2527.
79. Kozlowski, P. A.,, S. Cu-Uvin,, M. R. Neutra,, and T. P. Flanigan. 1997. Comparison of the oral, rectal, and vaginal immunization routes for induction of antibodies in rectal and genital tract secretions of women. Infect. Immun. 65: 1387 1394.
80. Kraehenbuhl, J. P.,, and M. R. Neutra. 1992. Molecular and cellular basis of immune protection of mucosal surfaces. Physiol. Rev. 72: 853 879.
81. Kutteh, W. H.,, K. D. Hatch,, R. E. Blackwell,, and J. Mestecky. 1988. Secretory immune system of the female reproductive tract. I. Immuoglobulin and secretory component-containing cells. Obstet. Gynecol. 71: 56 60.
82. Lefrancois, L.,, and L. Puddington. 1998. Anatomy of T-cell development in the intestine. Gastroenterology 115: 1588 1591.
83. Legler, D. F.,, M. Loetscher,, R. Stuber Roos,, I. Clark-Lewis,, M. Baggiolini,, and B. Moser. 1998. B cell-attracting chemokine 1, a human CXC chemokine expressed in lymphoid tissues, selectively attracts B lymphocytes via BRL1/CxCR5. J. Exp. Med. 187: 665 660.
84. Lehner, T.,, R. Brookes,, C. Panagiotidi,, L. Tao,, L. S. Klavinskis,, J. Walker,, P. Walker,, R. Ward,, L. Hussain,, A. J. H. Gearing,, S. E. Adams,, and L. A. Bergmeier. 1993. T- and B-cell functions and epitope expression in nonhuman primates immunized with simian immunodeficiency virus antigen by the rectal route. Proc. Natl. Acad. Sci. USA 90: 8638 8642.
85. Lehner, T.,, C. Panagiotidi,, L. A. Bergmeier,, T. Ping,, R. Brookes,, and S. E. Adams. 1992. A comparison of the immune response following oral, vaginal, or rectal route of immunization with SIV antigens in nonhuman primates. Vaccine Res. 1: 319 330.
86. Lehrer, R. I.,, C. L. Bevins,, and T. Ganz,. 1999. Defensins and other antimicrobial peptides, p. 89 100. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology. Academic Press, Inc., New York, N.Y.
87. MacDonald, T. T. 1999. Effector and regulatory lymphoid cells and cytokines in mucosal sites. Curr. Top. Microbiol. Immunol. 236: 113 135.
88. MacLennan, I. C.,, Y. J. Liu,, and G. D. Johnson. 1992. Maturation and dispersal of B-cell clones during T cell-dependent antibody responses. Immunol. Rev. 126: 143 161.
89. Macpherson, A. J.,, D. Gatto,, E. Sainsbury,, G. R. Harriman,, H. Hengartner,, and R. M. Zinkernagel. 2000. A primitive T cell dependent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288: 2222 2226.
90. MacPherson, G. G.,, and L. M. Liu. 1999. Dendritic cells and Langerhans cells in the uptake of mucosal antigens. Curr. Top. Microbiol. Immunol. 256: 33 54.
91. Madara, J. L.,, S. Nash,, R. Moore,, and K. Atisook. 1990. Structure and function of the intestinal epithelial barrier in health and disease. Monogr. Pathol. 31: 306 324.
92. Mantis, N. J.,, A. Frey,, and M. R. Neutra. 2000. Accessibility of glycolipid and oligosaccharide epitopes on apical surfaces of rabbit villus and follicle-associated epithelium. Am. J. Physiol. 278: G915 G929.
93. Manz, R. A.,, A. Thiel,, and A. Radbruch. 1997. Lifetime of plasma cells in the bone marrow. Nature 388: 133 134.
94. Maury, J.,, C. Nicoletti,, L. Guzzo-Chambraud,, and S. Maroux. 1995. The filamentous brush border glycocalyx, a mucin-like marker of enterocyte hyper-polarization. Eur. J. Biochem. 228: 323 331.
95. Mayer, L. 2000. Oral tolerance: new approaches, new problems. Clin. Immunol. 94: 1 8.
96. Mazzucchelli, L.,, A. Blaser,, A. Kappeler,, P. Scharli,, J. A. Laissue,, M. Baggiolini,, and M. Uguccioni. 1999. BCA-1 is highly expressed in Helicobacter pylori-induced mucosa-associated lymphoid tissue and gastric lymphoma. J. Clin. Investig. 104: R49 R54.
97. McDermott, M. R.,, L. J. Brais,, and M. J. Evelegh. 1990. Mucosal and systemic antiviral antibodies in mice inoculated intravaginally with herpes simplex virus type 2. J. Gen. Virol. 71: 1497 1504.
98. McGhee, J. R.,, M. E. Lamm,, and W. Strober,. 1999. Mucosal immune responses, p. 485 506. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology, 2nd ed. Academic Press, Inc., New York, N.Y.
99. McGhee, J. R.,, J. Mestecky,, M. T. Dertzbaugh,, J. H. Eldridge,, M. Hirasawa,, and H. Kiyono. 1992. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 10: 75 88.
100. McHeyzer-Williams, L. J.,, M. Cool,, and M. G. McHeyzer- Williams. 2000. Antigen-specific B cell memory: expression and replenishment of a novel B220(-) memory B cell compartment. J. Exp. Med. 191: 1149 1165.
101. Miller, C. J. 1994. Mucosal transmission of SIV. Curr. Top. Microbiol. Immunol. 188: 107 122.
102. Miller, C. J.,, M. McChesney,, and P. F. Moore. 1992. Langerhans cells, macrophages and lymphocyte subsets in the cervix and vagina of rhesus macaques. Lab. Investig. 67: 628 634.
103. Mowat, A. M.,, and H. L. Weiner,. 1999. Oral tolerance: physiological basis and clinical applications, p. 587 618. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology, 2nd ed. Academic Press, Inc., New York, N.Y.
104. Nelson, D. J.,, C. McMenamin,, A. S. McWilliam,, M. Brenan,, and P. G. Holt. 1994. Development of the airway intraepithelial dendritic cell network in the rat from class II major histocompatibility (Ia)-negative precursors: differential regulation of Ia expression at different levels of the respiratory tract. J. Exp. Med. 179: 203 212.
105. Neutra, M. R. 1998. HIV transmission and immune protection at mucosal surfaces. Adv. Exp. Med. Biol. 452: 169 176.
106. Neutra, M. R.,, P. J. Giannasca,, K. T. Giannasca,, and J. P. Kraehenbuhl,. 1995. M cells and microbial pathogens, p. 163 178. In M. J. Blaser,, P. D. Smith,, J. I. Ravdin,, H. B. Greenberg,, and L. Guerrant (ed.), Infections of the Gastrointestinal Tract. Raven Press, New York, N.Y.
107. Neutra, M. R.,, N. J. Mantis,, A. Frey,, and P. J. Giannasca. 1999. The composition and function of M cell apical membranes: implications for microbial pathogenesis. Semin. Immunol. 11: 171 181.
108. Neutra, M. R.,, E. Pringault,, and J. P. Kraehenbuhl. 1996. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu. Rev. Immunol. 14: 275 300.
109. Nibert, M. L.,, D. B. Furlong,, and B. N. Fields. 1991. Mechanisms of viral pathogenesis. Distinct forms of reoviruses and their roles during replication in cells and host. J. Clin. Investig. 88: 727 734.
110. Ogra, P. L.,, and D. T. Karzon. 1969. Distribution of poliovirus antibody in serum, nasopharynx and alimentary tract following segmental immunization of lower alimentary tract with poliovaccine. J. Immunol. 102: 1423 1430.
111. Okato, S.,, S. Magari,, Y. Yamamoto,, M. Sakanaka,, and H. Takahashi. 1989. An immunoelectron microscopic study on interactions among dendritic cells, macrophages and lymphocytes in the human palatine tonsil. Arch. Histol. Cytol. 52: 231 240.
112. O’Leary, A. D.,, and E. C. Sweeney. 1986. Lymphoglandular complexes of the colon: structure and distribution. Histopathology 10: 267 283.
113. Pabst, R.,, and I. Gehrke. 1990. Is the bronchus-associated lymphoid tissue (BALT) an integral structure of the lung in normal mammals, including humans? Am. J. Respir. Cell Mol. Biol. 3: 132 135.
114. Pappo, J.,, and R. L. Owen. 1988. Absence of secretory component expression by epithelial cells overlying rabbit gut-associated lymphoid tissue. Gastroenterology 95: 1173 1177.
115. Parr, M. B.,, and E. L. Parr,. 1994. Mucosal immunity in the female and male reproductive tracts, p. 677 690. In P. L. Ogra,, J. Mestecky,, M. E. Lamm,, W. Strober,, J. R. McGhee,, and J. Bienenstock (ed.), Handbook of Mucosal Immunology. Academic Press, Inc., New York, N.Y.
116. Parr, M. B.,, and E. L. Parr. 1997. Protective immunity against HSV-2 in the mouse vagina. J. Reprod. Immunol. 36: 77.
117. Pavli, P.,, C. E. Woodhams,, W. F. Doe,, and D. A. Hume. 1990. Isolation and characterization of antigen-presenting dendritic cells from the mouse intestinal lamina propria. Immunology 70: 40 47.
118. Perry, M.,, and A. White. 1998. Immunology of the tonsils. Immunol. Today 19: 414 421.
119. Phalipon, A.,, and P. J. Sansonetti. 1999. Microbial-host interactions at mucosal sites. Host response to pathogenic bacteria at mucosal sites. Curr. Top. Microbiol. Immunol. 236: 163 190.
120. Phillips, D. M.,, and A. S. Bourinbaiar. 1992. Mechanism of HIV spread from lymphocytes to epithelia. Virology 186: 261 273.
121. Pierce, N. F.,, and W. C. Cray, Jr. 1982. Determinants of the localization, magnitude, and duration of a specific mucosal IgA plasma cell response in enterically immunized rats . J. Immunol. 128: 1311 1315.
122. Piguet, P. F.,, C. Vesin,, Y. Donati,, and C. Barazzone. 1999. TNFinduced enterocyte apoptosis and detachment in mice: induction of caspases and prevention by a caspase inhibitor, ZVAD-fmk. Lab. Investig. 79: 495 500.
123. Prigent-Delecourt, L.,, B. Coffin,, J. F. Colombel,, J. P. Dehennin,, J. P. Vaerman,, and J. C. Rambaud. 1995. Secretion of immunoglobulins and plasma proteins from the colonic mucosa: an in vivo study in man. Clin. Exp. Immunol. 99: 221 225.
124. Quiding, M.,, I. Nordström,, A. Kilander,, G. Andersson,, L. A. Hanson,, J. Holmgren,, and C. Czerkinsky. 1991. Intestinal immune responses in humans. Oral cholera vaccination induces strong intestinal antibody responses, gamma-interferon production, and evokes local immunological memory. J. Clin. Investig. 88: 143 148.
125. Ramsay, A. J.,, A. J. Husband,, I. A. Ramshaw,, S. Bao,, K. I. Matthaei,, G. Koehler,, and M. Kopf. 1994. The role of interleukin- 6 in mucosal IgA antibody responses in vivo. Science 264: 561 563.
126. Rasmussen, S. J.,, L. Eckmann,, A. J. Quayle,, L. Shen,, Y. X. Zhang,, D. J. Anderson,, J. Fierer,, R. S. Stephens,, and M. F. Kagnoff. 1997. Secretion of proinflammatory cytokines by epithelial cells in response to chlamydia infection suggests a central role for epithelial cells in chlamydial pathogenesis. J. Clin. Investig. 99: 77 87.
127. Reynaud, C. A.,, C. Garcia,, W. R. Hein,, and J. C. Weill. 1995. Hypermutation generating the sheep immunoglobulin repertoire is an antigen-independent process. Cell 80: 115 125.
128. Rose, J. R.,, M. B. Williams,, L. S. Rott,, E. C. Butcher,, and H. B. Greenberg. 1998. Expression of the mucosal homing receptor alpha4beta7 correlates with the ability of CD8+ memory T cells to clear rotavirus infection. J. Virol. 72: 726 730.
129. Rudin, A.,, E. L. Johansson,, C. Bergquist,, and J. Holmgren. 1998. Differential kinetics and distribution of antibodies in serum and nasal and vaginal secretions after nasal and oral vaccination of humans. Infect. Immun. 66: 3390 3396.
130. Russell, M. W.,, Z. Moldoveanu,, P. L. White,, G. J. Sibert,, J. Mestecky,, and S. M. Michalek. 1996. Salivary, nasal, genital, and systemic antibody responses in monkeys immunized intranasally with a bacterial protein antigen and the cholera toxin B subunit. Infect. Immun. 64: 1272 1283.
131. Saito, H.,, Y. Kanamori,, T. Takemori,, H. Nariuchi,, E. Kubota,, H. Takahashi-Iwanaga,, T. Iwanaga,, and H. Ishikawa. 1998. Generation of intestinal T cells from progenitors residing in gut cryptopatches. Science 280: 275 278.
132. Savidge, T. C.,, M. W. Smith,, P. S. James,, and P. Aldred. 1991. Salmonella-induced M-cell formation in germ-free mouse Peyer’s patch tissue. Am. J. Pathol. 139: 177 184.
133. Shaw, S. K.,, A. Hermanowski-Vosatka,, T. Shibahara,, B. A. Mc- Cormick,, C. A. Parkos,, S. L. Carlson,, E. C. Ebert,, M. B. Brenner,, and J. L. Madara. 1998. Migration of intestinal intraepithelial lymphocytes into a polarized epithelial monolayer. Am. J. Physiol. 38: G584 G591.
134. Sicinski, P.,, J. Rowinski,, J. B. Warchol,, Z. Jarzcabek,, W. Gut,, B. Szczygiel,, K. Bielecki,, and G. Koch. 1990. Poliovirus type 1 enters the human host through intestinal M cells. Gastroenterology 98: 56 58.
135. Siebers, A.,, and B. B. Finlay. 1996. M cells and the pathogenesis of mucosal and systemic infections. Trends Microbiol. 4: 22 29.
136. Sierro, F.,, E. Pringault,, P. Simon Assman,, J. P. Kraehenbuhl,, and N. Debard. 2000. Transient expression of M-cell phenotype by enterocyte-like cells of the follicle-associated epithelium of mouse Peyer’s patches. Gastroenterology 119: 734 743.
137. Sirard, J. C.,, F. Niedergang,, and J. P. Kraehenbuhl. 1999. Live attenuated Salmonella: a paradigm of mucosal vaccines. Immunol. Rev. 171: 5 26.
138. Slifka, M. K.,, R. Antia,, J. K. Whitmire,, and R. Ahmed. 1998. Humoral immunity due to long-lived plasma cells. Immunity 8: 363 372.
139. Sminia, T.,, and G. Kraal,. 1999. Nasal-associated lymphoid tissue, p. 357 364. In R. Ogra,, J. Mestecky,, J. McGhee,, J. Bienenstock,, M. Lamm,, and W. Strober (ed.), Mucosal Immunology, 2nd ed. Academic Press, Inc., New York, N.Y.
140. Spira, A. I.,, P. A. Marx,, B. K. Patterson,, J. Mahoney,, R. A. Koup,, S. M. Wolinsky,, and D. D. Ho. 1996. Cellular targets of infection and route of viral dissemination after an intravaginal inoculation of simian immunodeficiency virus into rhesus macaques. J. Exp. Med. 183: 215 225.
141. Steinman, R. M. 2000. DC-SIGN: a guide to some mysteries of dendritic cells. Cell 100: 491 494.
142. Steinman, R. M.,, S. Turley,, I. Mellman,, and K. Inaba. 2000. The induction of tolerance by dendritic cells that have captured apoptotic cells. J. Exp. Med. 191: 411 416.
143. Szabo, M. C.,, E. C. Butcher,, and L. M. McEvoy. 1997. Specialization of mucosal follicular dendritic cells revealed by mucosal adressin-cell adhesion molecule-1 display. J. Immunol. 158: 5584 5588.
144. Vajdy, M.,, and N. Y. Lycke. 1992. Cholera toxin adjuvant promotes long-term immunological memory in the gut mucosa to unrelated immunogens after oral immunization. Immunology 75: 488 492.
145. Van Klinken, B. N.,, J. Dekker,, H. A. Buller,, and A. W. Einerhand. 1995. Mucin gene structure and expression: protection vs. adhesion. Am. J. Physiol. 269: G613 G627.
146. Velin, D.,, G. Fotopoulos,, J. P. Kraehenbuhl,, and H. Acha Orbea. 1999. Systemic antibodies can inhibit MMTV driven superantigen response in mucosal associated lymphoid tissues. J. Virol. 73: 1729 1733.
147. Wassen, L.,, K. Schon,, J. Holmgren,, M. Jertborn,, and N. Lycke. 1996. Local intravaginal vaccination of the female genital tract. Scand. J. Immunol. 44: 408 414.
148. Whitacre, C.,, C. Gienapp,, I. E. Orosz,, and D. Bitar. 1991. Oral tolerance in experimental autoimmune encephalomyelitis. III. Evidence for clonal anergy. J. Immunol. 147: 2155 2163.
149. Williams, M. B.,, J. R. Rose,, L. S. Rott,, M. A. Franco,, H. B. Greenberg,, and E. C. Butcher. 1998. The memory B cell subset responsible for the secretory IgA response and protective humoral immunity to rotavirus expresses the intestinal homing receptor, alpha(4)beta(7). J. Immunol. 161: 4227 4235.
150. Witthoft, T.,, L. Eckmann,, J. M. Kim,, and M. F. Kagnoff. 1998. Enteroinvasive bacteria directly activate expression of iNOS and NO production in human colon epithelial cells. Am. J. Physiol. 275: G564 G571.
151. Wold, A. E.,, J. Mestecky,, M. Tomana,, A. Kobata,, H. Ohbayashi,, T. Endo,, and C. Svanborg-Eden. 1990. Secretory immunoglobulin A carries oligosaccharide receptors for Escherichia coli type 1 fimbrial lectin. Infect. Immun. 58: 3073 3077.
152. Wolf, J. L.,, D. H. Rubin,, R. Finberg,, R. S. Kauffman,, A. H. Sharpe,, J. S. Trier,, and B. N. Fields. 1981. Intestinal M cells: a pathway for entry of reovirus into the host. Science 212: 471 472.
153. Yahi, N.,, S. Baghdiguian,, C. Bolmont,, and J. Fantini. 1992. Inhibition of human immunodeficiency virus infection in human colon epithelial cells by recombinant interferon-gamma. Eur. J. Immunol. 22: 2495 2499.
154. Zhou, F.,, J.-P. Kraehenbuhl,, and M. R. Neutra. 1995. Mucosal IgA response to rectally administered antigen formulated in IgAcoated liposomes. Vaccine 13: 637 644.

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