Genomic dissection of mucosal immunobiology in the porcine small intestine

Physiological Genomics

Volumn 28, Issue 1, 2006, Pages 5-14

  Dvorak, Cheryl M T ^a   Hirsch, Geoffrey N ^a   Hyland, Kendra A ^a   Hendrickson, Julie A ^a   Thompson, Beth S ^a   Rutherford, Mark S ^a   Murtaugh, Michael P ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Enteric system; Gene expression; Gut associated lymphoid tissue; Mucosal immunity; Salmonella; Swine

Indexed keywords

CONFERENCE PAPER; ENVIRONMENTAL FACTOR; GENE EXPRESSION; IMMUNE SYSTEM; IMMUNOBIOLOGY; INTESTINE FLORA; INTESTINE INFECTION; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEYER PATCH; PRIORITY JOURNAL; SMALL INTESTINE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CHROMOSOME MAP; CONTIG MAPPING; EXPRESSED SEQUENCE TAG; GENE EXPRESSION PROFILING; GENETICS; GENOMICS; IMMUNOLOGY; INTESTINE MUCOSA; METABOLISM; MUCOSAL IMMUNITY; RADIATION HYBRID MAPPING; SWINE;

SALMONELLA; SUIDAE; SUS;

ANIMALS; CHROMOSOME MAPPING; CONTIG MAPPING; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENOMICS; IMMUNITY, MUCOSAL; INTESTINAL MUCOSA; INTESTINE, SMALL; MICROARRAY ANALYSIS; MODELS, BIOLOGICAL; PEYER'S PATCHES; RADIATION HYBRID MAPPING; SUS SCROFA;

EID: 33847035801     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00104.2006     Document Type: Conference Paper

References (100)

1. Autret N, Charbit A. Lessons from signature-tagged mutagenesis on the infectious mechanisms of pathogenic bacteria. FEMS Microbiol Rev 29: 703-717, 2005.
2. Bailey M, Haverson K. The postnatal development of the mucosal immune system and mucosal tolerance in domestic animals. Vet Res 37: 443-453, 2006.
3. Bailey M, Haverson K, Inman C, Harris C, Jones P, Corfield G, Miller B, Stokes C. The development of the mucosal immune system pre- and post-weaning: balancing regulatory and effector function. Proc Nutr Soc 64: 451-457, 2005.
4. Bailey M, Miller BG, Telemo E, Stokes CR, Bourne FJ. Altered immune response to proteins fed after neonatal exposure of piglets to the antigen. Int Arch Allergy Immunol 103: 183-187, 1994.
5. Bailey M, Miller BG, Telemo E, Stokes CR, Bourne FJ. Specific immunological unresponsiveness following active primary responses to proteins in the weaning diet of piglets. Int Arch Allergy Immunol 101: 266-271, 1993.
6. 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.
7. Binns RM. The Null/gamma delta TCR+ T cell family in the pig. Vet Immunol Immunopathol 43: 69-77, 1994.
8. Binns RM. Organisation of the lymphoreticular system and lymphocyte markers in the pig. Vet Immunol Immunopathol 3: 95-146, 1982.
9. Binns RM, Licence ST. Patterns of migration of labelled blood lymphocyte subpopulations: evidence for two types of Peyer's patch in the young pig. Adv Exp Med Biol 186: 661-668, 1985.
10. Butler JE, Sinkora M, Wertz N, Holtmeier W, Lemke CD. Development of the neonatal B and T cell repertoire in swine: implications for comparative and veterinary immunology. Vet Res 37: 417-441, 2006.
11. Chen Y, Inobe J, Marks R, Gonnella P, Kuchroo VK, Weiner HL. Peripheral deletion of antigen-reactive T cells in oral tolerance. Nature 376: 177-180, 1995.
12. Coates NJ, McColl SR. Production of chemokines in vivo in response to microbial stimulation. J Immunol 166: 5176-5182, 2001.
13. Darwin KH, Miller VL. Molecular basis of the interaction of Salmonella with the intestinal mucosa. Clin Microbiol Rev 12: 405-428, 1999.
14. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, and Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3, 2003.
15. Duchmann R, Kaiser I, Hermann E, Mayet W, Ewe K, and Meyer zum Buschenfelde KH. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease (IBD). Clin Exp Immunol 102: 448-455, 1995.
16. Dvorak CM, Flickinger GH, Hendrickson JA, Fahrenkrug SC, Murtaugh MP, Rutherford MS. Mapping of genes expressed in activated porcine Peyer's patch. Anim Genet 37: 62-65, 2006.
17. Dvorak CMT, Hyland KA, Machado JG, Zhang Y, Fahrenkrug SC, Murtaugh MP. Gene discovery and expression profiling in porcine Peyer's patch. Vet Immunol Immunopathol 105: 301-315, 2005.
18. Eckmann L, Smith JR, Housley MP, Dwinell MB, Kagnoff MF. Analysis by high density cDNA arrays of altered gene expression in human intestinal epithelial cells in response to infection with the invasive enteric bacteria Salmonella. J Biol Chem 275: 14084-14094, 2000.
19. Elewaut D, DiDonato JA, Kim JM, Truong F, Eckmann L, Kagnoff MF. NF-kappa B is a central regulator of the intestinal epithelial cell innate immune response induced by infection with enteroinvasive bacteria. J Immunol 163: 1457-1466, 1999.
20. Elson CO, Ealding W. Cholera toxin feeding did not induce oral tolerance in mice and abrogated oral tolerance to an unrelated protein antigen. J Immunol 133: 2892-2897, 1984.
21. Foss DL, Murtaugh MP. Mechanisms of vaccine adjuvanticity at mucosal surfaces. Anim Health Res Rev 1: 3-24, 2000.
22. Foss DL, Murtaugh MP. Mucosal immunogenicity and adjuvanticity of cholera toxin in swine. Vaccine 17: 788-801, 1999.
23. Friedman A, Weiner HL. Induction of anergy or active suppression following oral tolerance is determined by antigen dosage. Proc Natl Acad Sci USA 91: 6688-6692, 1994.
24. Frost AJ, Bland AP, Wallis TS. The early dynamic response of the calf ileal epithelium to Salmonella typhimurium. Vet Pathol 34: 369-386, 1997.
25. Garside P, Mowat AM. Mechanisms of oral tolerance. Crit Rev Immunol 17: 119-137, 1997.
26. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167: 1882-1885, 2001.
27. Gewirtz AT, Simon PO Jr, Schmitt CK, Taylor LJ, Hagedorn CH, O'Brien AD, Neish AS, Madara JL. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 107: 99-109, 2001.
28. Gookin JL, Rhoads JM, Argenzio RA. Inducible nitric oxide synthase mediates early epithelial repair of porcine ileum. Am J Physiol Gastrointest Liver Physiol 283: G157-G168, 2002.
29. Gregerson DS, Obritsch WF, Donoso LA. Oral tolerance in experimental autoimmune uveoretinitis. Distinct mechanisms of resistance are induced by low dose vs high dose feeding protocols. J Immunol 151: 5751-5761, 1993.
30. Guzylack-Piriou L, Balmelli C, McCullough KC, Summerfield A. Type-A CpG oligonucleotides activate exclusively porcine natural interferon-producing cells to secrete interferon-alpha, tumour necrosis factoralpha and interleukin-12. Immunology 112: 28-37, 2004.
31. Haverson K, Riffault S. Antigen presenting cells in mucosal sites of veterinary species. Vet Res 37: 339-358, 2006.
32. Hawken RJ, Murtaugh J, Flickinger GH, Yerle M, Robic A, Milan D, Gellin J, Beattie CW, Schook LB, Alexander LJ. A first-generation porcine whole-genome radiation hybrid map. Mamm Genome 10: 824-830, 1999.
33. Hecht G. Innate mechanisms of epithelial host defense: spotlight on intestine. Am J Physiol Cell Physiol 277: C351-C358, 1999.
34. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 96: 2396-2401, 1999.
35. Hershberg RM, Mayer LF. Antigen processing and presentation by intestinal epithelial cells - polarity and complexity. Immunol Today 21: 123-128, 2000.
36. Hooper LV, Bry L, Falk PG, Gordon JI. Host-microbial symbiosis in the mammalian intestine: exploring an internal ecosystem. Bioessays 20: 336-343, 1998.
37. Huang FC, Werne A, Li Q, Galyov EE, Walker WA, Cherayil BJ. Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica serovar typhimurium infection. Infect Immun 72: 5052-5062, 2004.
38. Hyland KA, Brown DR, Murtaugh MP. Salmonella enterica serovar Choleraesuis infection of the porcine jejunal Peyer's patch rapidly induces IL-1beta and IL-8 expression. Vet Immunol Immunopathol 109: 1-11, 2006.
39. Hyland KA, Kohrt L, Vulchanova L, Murtaugh MP. Mucosal innate immune response to intragastric infection by Salmonella enterica serovar Choleraesuis. Mol Immunol 43: 1890-1899, 2006.
40. 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.
41. Kacskovics I, Sun J, Butler JE. Five putative subclasses of swine IgG identified from the cDNA sequences of a single animal. J Immunol 153: 3565-3573, 1994.
42. Kaufmann SH. Immunity to intracellular bacteria. Annu Rev Immunol 11: 129-163, 1993.
43. Kehoe JM, Capra JD. Nature and significance of immunoglobulin subclasses. NY State J Med 74: 489-491, 1974.
44. Kerneis S, Pringault E. Plasticity of the gastrointestinal epithelium: the M cell paradigm and opportunism of pathogenic microorganisms. Semin Immunol 11: 205-215, 1999.
45. Kulkarni-Narla A, Brown DR. Localization of CB1-cannabinoid receptor immunoreactivity in the porcine enteric nervous system. Cell Tissue Res 302: 73-80, 2000.
46. Lamm ME. Current concepts in mucosal immunity. IV. How epithelial transport of IgA antibodies relates to host defense. Am J Physiol Gastrointest Liver Physiol 274: G614-G617, 1998.
47. Lin G, Pearson AE, Scamurra RW, Zhou Y, Baarsch MJ, Weiss DJ, Murtaugh MP. Regulation of interleukin-8 expression in porcine alveolar macrophages by bacterial lipopolysaccharide. J Biol Chem 269: 77-85, 1994.
48. Lopez-Boado YS, Espinola M, Bahr S, Belaaouaj A. Neutrophil serine proteinases cleave bacterial flagellin, abrogating its host response-inducing activity. J Immunol 172: 509-515, 2004.
49. Lundberg U, Vinatzer U, Berdnik D, von Gabain A, Baccarini M. Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J Bacteriol 181: 3433-3437, 1999.
50. Lycke N, Holmgren J. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 59: 301-308, 1986.
51. Machado JG, Hyland KA, Dvorak CM, Murtaugh MP. Gene expression profiling of jejunal Peyer's patches in juvenile and adult pigs. Mamm Genome 16: 599-612, 2005.
52. Macpherson A, Khoo UY, Forgacs I, Philpott-Howard J, Bjarnason I. Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria. Gut 38: 365-375, 1996.
53. Marth T, Strober W, Kelsall BL. High dose oral tolerance in ovalbumin TCR-transgenic mice: systemic neutralization of IL-12 augments TGF-beta secretion and T cell apoptosis. J Immunol 157: 2348-2357, 1996.
54. McCormick BA, Colgan SP, Delp-Archer C, Miller SI, Madara JL. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123: 895-907, 1993.
55. McKay DM, Baird AW. Cytokine regulation of epithelial permeability and ion transport. Gut 44: 283-289, 1999.
56. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 1: 135-145, 2001.
57. Miller BG, Newby TJ, Stokes CR, Bourne FJ. Influence of diet on postweaning malabsorption and diarrhoea in the pig. Res Vet Sci 36: 187-193, 1984.
58. Monack DM, Raupach B, Hromockyj AE, Falkow S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838, 1996.
59. Mowat AM, Viney JL. The anatomical basis of intestinal immunity. Immunol Rev 156: 145-166, 1997.
60. Murtaugh MP, Foss DL. Inflammatory cytokines and antigen presenting cell activation. Vet Immunol Immunopathol 87: 109-121, 2002.
61. Neutra MR. Current concepts in mucosal immunity. V. Role of M cells in transepithelial transport of antigens and pathogens to the mucosal immune system. Am J Physiol Gastrointest Liver Physiol 274: G785-G791, 1998.
62. Neutra MR, Frey A, Kraehenbuhl JP. Epithelial M cells: gateways for mucosal infection and immunization. Cell 86: 345-348, 1996.
63. Neutra MR, Pringault E, Kraehenbuhl JP. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 14: 275-300, 1996.
64. Newberry RD, Lorenz RG. Organizing a mucosal defense. Immunol Rev 206: 6-21, 2005.
65. Nguyen VK, Desmyter A, Muyldermans S. Functional heavy-chain antibodies in Camelidae. Adv Immunol 79: 261-296, 2001.
66. Noma T, Yoshizawa I, Aoki K, Yamaguchi K, Baba M. Cytokine production in children outgrowing hen egg allergy. Clin Exp Allergy 26: 1298-1307, 1996.
67. Oswald IP. Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Vet Res 37: 359-368, 2006.
68. Pabst R, Rothkotter HJ. Postnatal development of lymphocyte subsets in different compartments of the small intestine of piglets. Vet Immunol Immunopathol 72: 167-173, 1999.
69. Pampusch MS, Bennaars AM, Harsch S, Murtaugh MP. Inducible nitric oxide synthase expression in porcine immune cells. Vet Immunol Immunopathol 61: 279-289, 1998.
70. Pastoret P, Griebel P, Bazin H, Govaerts A. Handbook of Vertebrate Immunology. San Diego, CA: Academic, 1998.
71. Perdue MH, McKay DM. Integrative immunophysiology in the intestinal mucosa. Am J Physiol Gastrointest Liver Physiol 267: G151-G165, 1994.
72. Pescovitz MD, Sakopoulos AG, Gaddy JA, Husmann RJ, Zuckermann FA. Porcine peripheral blood CD4+/CD8+ dual expressing T-cells. Vet Immunol Immunopathol 43: 53-62, 1994.
73. Podolsky DK. Mucosal immunity and inflammation. V. Innate mechanisms of mucosal defense and repair: the best offense is a good defense. Am J Physiol Gastrointest Liver Physiol 277: G495-G499, 1999.
74. Pospischil A, Wood RL, Anderson TD. Peroxidase-antiperoxidase and immunogold labeling of Salmonella typhimurium and Salmonella choleraesuis var kunzendorf in tissues of experimentally infected swine. Am J Vet Res 51: 619-624, 1990.
75. Rennick DM, Fort MM, Davidson NJ. Studies with IL-10-/- mice: an overview. J Leukoc Biol 61: 389-396, 1997.
76. Rosenberger CM, Scott MG, Gold MR, Hancock RE, Finlay BB. Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J Immunol 164: 5894-5904, 2000.
77. Rothkotter HJ, Pabst R. Lymphocyte subsets in jejunal and ileal Peyer's patches of normal and gnotobiotic minipigs. Immunology 67: 103-108, 1989.
78. Saalmuller A, Reddehase MJ, Buhring HJ, Jonjic S, Koszinowski UH. Simultaneous expression of CD4 and CD8 antigens by a substantial proportion of resting porcine T lymphocytes. Eur J Immunol 17: 1297-1301, 1987.
79. Sato A, Iwasaki A. Peyer's patch dendritic cells as regulators of mucosal adaptive immunity. Cell Mol Life Sci 62: 1333-1338, 2005.
80. Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31: 107-133, 1977.
81. Sierro F, Dubois B, Coste A, Kaiserlian D, Kraehenbuhl JP, Sirard JC. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci USA 98: 13722-13727, 2001.
82. Snoeck V, Peters IR, Cox E. The IgA system: a comparison of structure and function in different species. Vet Res 37: 455-467, 2006.
83. Stokes CR, Bailey M. The porcine gastrointestinal lamina propria: an appropriate target for mucosal immunisation? J Biotechnol 83: 51-55, 2000.
84. Stokes CR, Bailey M, Wilson AD. Immunology of the porcine gastrointestinal tract. Vet Immunol Immunopathol 43: 143-150, 1994.
85. Stokes CR, Miller BG, Bailey M, Wilson AD, Bourne FJ. The immune response to dietary antigens and its influence on disease susceptibility in farm animals. Vet Immunol Immunopathol 17: 413-423, 1987.
86. Stokes CR, Miller BG, Bourne FJ. Animal models of food sensitivity. In: Food Allergy and Intolerance, edited by Brostoff J and Challacombe SJ. Philadelphia, PA: Bailliere Tindall, 1987, p. 286-300.
87. Van der Waaij D. The ecology of the human intestine and its consequences for overgrowth by pathogens such as Clostridium difficile. Annu Rev Microbiol 43: 69-87, 1989.
88. Ward LA, Yuan L, Rosen BI, To TL, Saif LJ. Development of mucosal and systemic lymphoproliferative responses and protective immunity to human group A rotaviruses in a gnotobiotic pig model. Clin Diagn Lab Immunol 3: 342-350, 1996.
89. Weiner HL. Oral tolerance: immune mechanisms and treatment of autoimmune diseases. Immunol Today 18: 335-343, 1997.
90. Weiner HL, Friedman A, Miller A, Khoury SJ, al-Sabbagh A, Santos L, Sayegh M, Nussenblatt RB, Trentham DE, Hafler DA. Oral tolerance: immunologic mechanisms and treatment of animal and human organ-specific autoimmune diseases by oral administration of autoantigens. Annu Rev Immunol 12: 809-837, 1994.
91. Yang SK, Eckmann L, Panja A, Kagnoff MF. Differential and regulated expression of C-X-C, C-C, and C-chemokines by human colon epithelial cells. Gastroenterology 113: 1214-1223, 1997.
92. Yuan L, Geyer A, Hodgins DC, Fan Z, Qian Y, Chang KO, Crawford SE, Parreno V, Ward LA, Estes MK, Conner ME, Saif LJ. Intranasal administration of 2/6-rotavirus-like particles with mutant Escherichia coli heat-labile toxin (LT-R192G) induces antibody-secreting cell responses but not protective immunity in gnotobiotic pigs. J Virol 74: 8843-8853, 2000.
93. Yuan L, Iosef C, Azevedo MS, Kim Y, Qian Y, Geyer A, Nguyen TV, Chang KO, Saif LJ. Protective immunity and antibody-secreting cell responses elicited by combined oral attenuated Wa human rotavirus and intranasal Wa 2/6-VLPs with mutant Escherichia coli heat-labile toxin in gnotobiotic pigs. J Virol 75: 9229-9238, 2001.
94. Yuan L, Kang SY, Ward LA, To TL, Saif LJ. Antibody-secreting cell responses and protective immunity assessed in gnotobiotic pigs inoculated orally or intramuscularly with inactivated human rotavirus. J Virol 72: 330-338, 1998.
95. Yuan L, Saif LJ. Induction of mucosal immune responses and protection against enteric viruses: rotavirus infection of gnotobiotic pigs as a model. Vet Immunol Immunopathol 87: 147-160, 2002.
96. Yuan L, Ward LA, Rosen BI, To TL, Saif LJ. Systematic and intestinal antibody-secreting cell responses and correlates of protective immunity to human rotavirus in a gnotobiotic pig model of disease. J Virol 70: 3075-3083, 1996.
97. Zhang S, Adams LG, Nunes J, Khare S, Tsolis RM, Baumler AJ. Secreted effector proteins of Salmonella enterica serotype typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect Immun 71: 4795-4803, 2003.
98. Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity 12: 121-127, 2000.
99. Zuckermann FA, Gaskins HR. Distribution of porcine CD4/CD8 double-positive T lymphocytes in mucosa-associated lymphoid tissues. Immunology 87: 493-499, 1996.
100. Zuckermann FA, Husmann RJ. Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 87: 500-512, 1996.