Board-invited review: Porcine mucosal immunity of the gastrointestinal tract

Journal of Animal Science

Volumn 87, Issue 4, 2009, Pages 1493-1501

  Burkey, T E ^a   Skjolaas, K A ^b   Minton, J E ^c  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b Talecris Biotherapeutics Inc   (United States)

^c KANSAS STATE UNIVERSITY   (United States)

Author keywords

Gut associated lymphoid tissue; Intestinal epithelial cell; Mucosal immunity; Pig

Indexed keywords

ANIMAL; ANIMAL DISEASE; DIET; EPITHELIUM CELL; GASTROINTESTINAL TRACT; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LYMPHOID TISSUE; MUCOSAL IMMUNITY; REVIEW; SWINE;

ANIMALS; DIET; EPITHELIAL CELLS; GASTROINTESTINAL TRACT; IMMUNITY, MUCOSAL; LYMPHOID TISSUE; SWINE;

MAMMALIA; SUIDAE; SUS;

EID: 63849284114     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2008-1330     Document Type: Review

References (115)

1. Andersen, J. K., H. Takamatsu, C. A. Oura, S. M. Brookes, L. Pullen, and R. E. Parkhouse. 1999. Systematic characterization of porcine ileal Peyer's patch, I. Apoptosis-sensitive immature B cells are the predominant cell type. Immunology 98:612-621.
2. Artis, D. 2008. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8:411-420.
3. Bailey, M., L. Hall, P. W. Bland, and C. R. Stokes. 1994. Production of cytokines by lymphocytes from spleen, mesenteric lymph node and intestinal lamina propria of pigs. Immunology 82:577-583.
4. Bailey, M., K. Haverson, C. Inman, C. Harris, P. Jones, G. Corfield, B. Miller, and C. Stokes. 2005. The influence of environment on development of the mucosal immune system. Vet. Immunol. Immunopathol. 108:189-198.
5. Bailey, M., F. J. Plunkett, H. J. Rothkotter, M. A. Vega-Lopez, K. Haverson, and C. R. Stokes. 2001. Regulation of mucosal immune responses in effector sites. Proc. Nutr. Soc. 60:427-435.
6. Binns, R. M., and S. T. Licence. 1985. Patterns of migration of labelled blood lymphocyte subpopulations: Evidence for two types of Fever's patch in the young pig. Adv. Exp. Med. Biol. 186:661-668.
7. Blecha, F. 2001. Immunology. Pages 688-711 in Biology of the Domestic Pig. W. G. Pond and H. J. Mersmann, ed. Cornell Univ. Press, Ithaca, NY.
8. + cells. J. Immunol. 169:6085-6091.
9. Brandtzaeg, P., I. N. Farstad, and L. Helgeland. 1998. Phenotypes of T cells in the gut. Chem. Immunol. 71:1-26.
10. Brandtzaeg, P., T. S. Halstensen, K. Kett, P. Krajci, D. Kvale, T. O. Rognum, H. Scott, and L. M. Sollid. 1989. Immunobiology and immunopathology of the human gut mucosa: Humoral immunity and intraepithelial lymphocytes. Gastroenterology 97:1562-1584.
11. Brandtzaeg, P., and R. Pabst. 2004. Let's go mucosal: Communication on slippery ground. Trends Immunol. 25:570-577.
12. Bucy, R. P., C. L. Chen, J. Cihak, U. Losch, and M. D. Cooper. 1988. Avian T cells expressing gamma delta receptors localize in the splenic sinusoids and the intestinal epithelium. J. Immunol. 141:2200-2205.
13. Butler, J. E., M. Sinkora, N. Wertz, W. Holtmeier, and C. D. Lemke. 2006b. Development of the neonatal B and T cell repertoire in swine: Implications for comparative and veterinary immunology. Vet. Res. 37:417-441.
14. Butler, J. E., J. Sun, N. Wertz, and M. Sinkora. 2006a. Antibody repertoire development in swine. Dev. Comp. Immunol. 30:199-221.
15. Cepek, K. L., S. K. Shaw, C. M. Parker, G. J. Russell, J. S. Morrow, D. L. Rimm, and M. B. Brenner. 1994. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372:190-193.
16. Christ, A. D., and R. S. Blumberg. 1997. The intestinal epithelial cell: Immunological aspects. Springer Semin. Immunopathol. 18:449-461.
17. Chu, R. M., and C. H. Liu. 1984. Morphological and functional comparisons of Peyer's patches in different parts of the swine small intestine. Vet. Immunol. Immunopathol. 6:391-403.
18. Dasso, J. F., and M. D. Howell. 1997. Neonatal appendectomy impairs mucosal immunity in rabbits. Cell. Immunol. 182:29- 37.
19. Dasso, J. F., H. Obiakor, H. Bach, A. O. Anderson, and R. G. Mage. 2000. A morphological and immunohistological study of the human and rabbit appendix for comparison with the avian bursa. Dev. Comp. Immunol. 24:797-814.
20. Dekaney, C. M., F. W. Bazer, and L. A. Jaeger. 1997. Mucosal morphogenesis and cytodifferentiation in fetal porcine small intestine. Anat. Rec. 249:517-523.
21. Didierlaurent, A., J. C. Sirard, J. P. Kraehenbuhl, and M. R. Neutra. 2002. How the gut senses its content. Cell. Microbiol. 4:61-72.
22. Dvorak, C. M., G. N. Hirsch, K. A. Hyland, J. A. Hendrickson, B. S. Thompson, M. S. Rutherford, and M. P. Murtaugh. 2006. Genomic dissection of mucosal immunobiology in the porcine small intestine. Physiol. Genomics 28:5-14.
23. Dvorak, P., V. Hruban, and V. Horak. 1987. The distribution of class II molecules in the pig intestine. Folia Morphol. (Praha) 35:396-399.
24. Eckmann, L. 2004. Innate immunity and mucosal bacterial interactions in the intestine. Curr. Opin. Gastroenterol. 20:82-88.
25. Eckmann, L., M. F. Kagnoff, and J. Fierer. 1993. Epithelial cells secrete the chemokine interleukin-8 in response to bacterial entry. Infect. Immun. 61:4569-4574.
26. 2α production. J. Clin. Invest. 100:296-309.
27. Elewaut, D., J. A. DiDonato, J. M. Kim, F. Truong, L. Eckmann, and M. F. Kagnoff. 1999. 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.
28. Falk, P. G., L. V. Hooper, T. Midtvedt, and J. I. Gordon. 1998. Creating and maintaining the gastrointestinal ecosystem: What we know and need to know from gnotobiology. Microbiol. Mol. Biol. Rev. 62:1157-1170.
29. Ganz, T. 2003. Defensins: Antimicrobial peptides of innate immunity. Nat. Rev. Immunol. 3:710-720.
30. Gebert, A., H. J. Rothkotter, and R. Pabst. 1996. M cells in Peyer's patches of the intestine. Int. Rev. Cytol. 167:91-159.
31. Gewirtz, A. T., and J. L. Madara. 2001. Periscope, up! Monitoring microbes in the intestine. Nat. Immunol. 2:288-290.
32. Gewirtz, A. T., T. A. Navas, S. Lyons, P. J. Godowski, and J. L. Madara. 2001. Cutting edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167:1882-1885.
33. +)-mediated activation of the NF-kappaB pathway. J. Clin. Invest. 105:79-92.
34. Ghosh, S., M. J. May, and E, B. Kopp. 1998. NF-kappa B and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16:225-260.
35. Goldsby, R. A., T. J. Kindt, B. A. Osborne, and J. Kuby. 2003. Immunology. 5th ed. W. H. Freeman and Co., New York, NY.
36. + intraepithelial lymphocytes. Nature 333:855-858.
37. Gorbach, S. L., L. Nahas, P. I. Lerner, and L. Weinstein. 1967. Studies of intestinal microflora. I. Effects of diet, age, and periodic sampling on numbers of fecal microorganisms in man. Gastroenterology 53:845-855.
38. Griebel, P. J., and W. R. Hein. 1996. Expanding the role of Peyer's patches in B-cell ontogeny. Immunol. Today 17:30-39.
39. Gumbiner, B. 1987. Structure, biochemistry, and assembly of epithelial tight junctions. Am. J. Physiol. 253:C749-C758.
40. Hamada, H., T. Hiroi, Y. Nishiyama, H. Takahashi, Y. Masunaga, S. Hachimura, S. Kaminogawa, H. Takahashi-Iwanaga, T. Iwanaga, H. Kiyono, H. Yamamoto, and H. Ishikawa. 2002. Identification of multiple isolated lymphoid follicles on the antimesenteric wall of the mouse small intestine. J. Immunol. 168:57-64.
41. Hapfelmeier, S., B. Stecher, M. Barthel, M. Kremer, A. J. Muller, M. Heikenwalder, T. Stallmach, M. Hensel, K. Pfeffer, S. Akira, and W. D. Hardt. 2005. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J. Immunol. 174:1675- 1685.
42. + lamina propria T-cell lines: Phenotypic and functional characterization. Immunology 75:66-73.
43. Haverson, K., M. Bailey, and C. R. Stokes. 1999. T-cell populations in the pig intestinal lamina propria: Memory cells with unusual phenotypic characteristics. Immunology 96:66-73.
44. Havran, W. L., J. M. Jameson, and D. A. Witherden. 2005. Epithelial cells and their neighbors. III. Interactions between intraepithelial lymphocytes and neighboring epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 289:G627-G630.
45. Hayday, A., E. Theodoridis, E. Ramsburg, and J. Shires. 2001. Intraepithelial lymphocytes: Exploring the third way in immunology. Nat. Immunol. 2:997-1003.
46. Heel, K. A., R. D. McCauley, J. M. Papadimitriou, and J. C. Hall. 1997. Review: Peyer's patches. J. Gastroenterol. Hepatol. 12:122-136.
47. Hokari, R., S. Miura, H. Nagata, H. Fujimori, S. Koseki, S. Kato, I. Kurose, E. Sekizuka, D. N. Granger, and H. Ishii. 2001. Intercellular cell adhesion molecule-1 regulates lymphocyte movement into intestinal microlymphatics of rat Peyer's patches. J. Leukoc. Biol. 70:896-902.
48. Hunyady, B., E. Mezey, and M. Palkovits. 2000. Gastrointestinal immunology: Cell types in the lamina propria-A morphological review. Acta Physiol. Hung. 87:305-328.
49. Hyland, K. A., L. Kohrt, L. Vulchanova, and M. P. Murtaugh. 2006. Mucosal innate immune response to intragastric infection by Salmonella enterica serovar Choleraesuis. Mol. Immunol. 43:1890-1899.
50. James, S. P. 1993. The gastrointestinal mucosal immune system. Dig. Dis. 11:146-156.
51. 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. Invest. 95:55-65.
52. Kagnoff, M. F. 1993. Immunology of the intestinal tract. Gastroenterology 105:1275-1280.
53. + lympho-hemopoietic progenitors develop. J. Exp. Med. 184:1449-1459.
54. Kaser, T., W. Gerner, S. E. Hammer, M. Patzl, and A. Saalmuller. 2008. Phenotypic and functional characterisation of porcine CD4(+)CD25(high) regulatory T cells. Vet. Immunol. Immunopathol. 122:153-158.
55. Lorenz, R. G., and R. D. Newberry. 2004. Isolated lymphoid follicles can function as sites for induction of mucosal immune responses. Ann. N. Y. Acad. Sci. 1029:44-57.
56. Lowden, S., and T. Heath. 1994. Ileal Peyer's patches in pigs: Intercellular and lymphatic pathways. Anat. Rec. 239:297-305.
57. Maaser, C., and M. F. Kagnoff. 2002. Role of the intestinal epithelium in orchestrating innate and adaptive mucosal immunity. Z. Gastroenterol. 40:525-529.
58. Makala, L. H., T. Kamada, H. Nagasawa, I. Igarashi, K. Fujisaki, N. Suzuki, T. Mikami, K. Haverson, M. Bailey, C. R. Stokes, and P. W. Bland. 2001. Ontogeny of pig discrete Peyer's patches: Expression of surface antigens. J. Vet. Med. Sci. 63:625-636.
59. Makala, L. H., N. Suzuki, and H. Nagasawa. 2002. Peyer's patches: Organized lymphoid structures for the induction of mucosal immune responses in the intestine. Pathobiology 70:55-68.
60. Mayer, L. 2000. Mucosal immunity and gastrointestinal antigen processing. J. Pediatr. Gastroenterol. Nutr. 30(Suppl.):S4-S12.
61. Mayrhofer, G. 1984. Physiology of the intestinal immune system. Pages 1-96 in Local Immune Responses of the Gut. T. J. Newby and C. R. Stokes, ed. CRC Press, Boca Raton, FL.
62. Medzhitov, R., P. Preston-Hurlburt, E. Kopp, A. Stadlen, C. Chen, S. Ghosh, and C. A. Janeway Jr. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2:253-258.
63. Meylan, E., J. Tschopp, and M. Karin. 2006. Intracellular pattern recognition receptors in the host response. Nature 442:39-44.
64. Moghaddami, M., A. Cummins, and G. Mayrhofer. 1998. Lymphocyte-filled villi: Comparison with other lymphoid aggregations in the mucosa of the human small intestine. Gastroenterology 115:1414-1425.
65. Mowat, A. M., and J. L. Viney. 1997. The anatomical basis of intestinal immunity. Immunol. Rev. 156:145-166.
66. Myer, M. S. 1982. The presence of Paneth cells confirmed in the pig. Onderstepoort J. Vet. Res. 49:131-132.
67. Nagler-Anderson, C. 2001. Man the barrier! Strategic defences in the intestinal mucosa. Nat. Rev. Immunol. 1:59-67.
68. Neutra, M. R., N. J. Mantis, and J. P. Kraehenbuhl. 2001. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat. Immunol. 2:1004-1009.
69. Obremski, K., M. Gajecka, L. Zielonka, E. Jakimiuk, and M. Gajecki. 2005. Morphology and ultrastructure of small intestine mucosa in gilts with zearalenone mycotoxicosis. Pol. J. Vet. Sci. 8:301-307.
70. Oswald, I. P. 2006. Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Vet. Res. 37:359-368.
71. Owen, R. L., and A. L. Jones. 1974. Epithelial cell specialization within human Peyer's patches: An ultrastructural study of intestinal lymphoid follicles. Gastroenterology 66:189-203.
72. Pabst, O., H. Herbrand, T. Worbs, M. Friedrichsen, S. Yan, M. W. Hoffmann, H. Korner, G. Bernhardt, R. Pabst, and R. Forster. 2005. Cryptopatches and isolated lymphoid follicles: Dynamic lymphoid tissues dispensable for the generation of intraepithelial lymphocytes. Eur. J. Immunol. 35:98-107.
73. Pabst, R., M. Geist, H. J. Rothkotter, and F. J. Fritz. 1988. Postnatal development and lymphocyte production of jejunal and ileal Peyer's patches in normal and gnotobiotic pigs. Immunology 64:539-544.
74. Pabst, R., and H. J. Rothkotter. 1999. Postnatal development of lymphocyte subsets in different compartments of the small intestine of piglets. Vet. Immunol. Immunopathol. 72:167-173.
75. Par, A. 2000. Gastrointestinal tract as a part of immune defence. Acta Physiol. Hung. 87:291-304.
76. Parng, C. L, S. Hansal, R. A. Goldsby, and B. A. Osborne. 1996. Gene conversion contributes to Ig light chain diversity in cattle. J. Immunol. 157:5478-5486.
77. Pasare, C., and R. Medzhitov. 2005. Toll-like receptors: Linking innate and adaptive immunity. Adv. Exp. Med. Biol. 560:11- 18.
78. Perera, L., L. Shao, A. Patel, K. Evans, B. Meresse, R. Blumberg, D. Geraghty, V. Groh, T. Spies, B. Jabri, and L. Mayer. 2007. Expression of nonclassical class I molecules by intestinal epithelial cells. Inflamm. Bowel Dis. 13:298-307.
79. Philpott, D. J., S. E. Girardin, and P. J. Sansonetti. 2001. Innate immune responses of epithelial cells following infection with bacterial pathogens. Curr. Opin. Immunol. 13:410-416.
80. Pitman, R. S., and R. S. Blumberg. 2000. First line of defense: The role of the intestinal epithelium as an active component of the mucosal immune system. J. Gastroenterol. 35:805-814.
81. Pospisil, R., and R. G. Mage. 1998. Rabbit appendix: A site of development and selection of the B cell repertoire. Curr. Top. Microbiol. Immunol. 229:59-70.
82. Rescigno, M., M. Urbano, B. Valzasina, M. Francolini, G. Rotta, R. Bonasio, F. Granucci, J. P. Kraehenbuhl, and P. Ricciardi- Castagnoli. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2:361-367.
83. Reynolds, J. D. 1987. Peyer's patches and the early development of B lymphocytes. Curr. Top. Microbiol. Immunol. 135:43-56.
84. Rothkotter, H. J., H. J. Zimmermann, and R. Pabst. 1990. Size of jejunal Peyer's patches and migration of lymphocyte subsets in pigs after resection or transposition of the continuous ileal Peyer's patch. Scand. J. Immunol. 31:191-197.
85. Sang, Y., and F. Blecha. 2008. Porcine host defense peptides: Expanding repertoire and functions. Dev. Comp. Immunol. 33:334-343.
86. Sang, Y., A. A. Patil, G. Zhang, C. R. Ross, and F. Blecha. 2006. Bioinformatic and expression analysis of novel porcine betadefensins. Mamm. Genome 17:332-339.
87. Schantz, L. D., K. Laber-Laird, S. Bingel, and M. Swindle. 1996. Pigs: Applied anatomy of the gastrointestinal tract. Pages 2611-2619 in Essentials of Experimental Surgery: Gastroenterology. S. L. Jensen, H. Gregersen, F. Moody, and M. H. Shoouh-Amiri, ed. Harwood Academic Publishers, New York, NY.
88. Scharek, L., and K. Tedin. 2007. The porcine immune system- Differences compared to man and mouse and possible consequences for infections by Salmonella serovars. Berl. Munch. Tierarztl. Wochenschr. 120:347-354.
89. Schierack, P., M. Nordhoff, M. Pollmann, K. D. Weyrauch, S. Amasheh, U. Lodemann, J. Jores, B. Tachu, S. Kleta, A. Blikslager, K. Tedin, and L. H. Wiler. 2005. Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem. Cell Biol. 125:293- 305.
90. Shanahan, F., and G. C. O'Sullivan. 1997. Appendectomy, mucosal immunity, and colitis. Gastroenterology 112:1766-1767.
91. Shaykhiev, R., and R. Bals. 2007. Interactions between epithelial cells and leukocytes in immunity and tissue homeostasis. J. Leukoc. Biol. 82:1-15.
92. Shen, L., and J. R. Turner. 2006. Role of epithelial cells in initiation and propagation of intestinal inflammation. Eliminating the static: Tight junction dynamics exposed. Am. J. Physiol. Gastrointest. Liver Physiol. 290:G577-G582.
93. Shimosato, T., M. Tohno, H. Kitazawa, S. Katoh, K. Watanabe, Y. Kawai, H. Aso, T. Yamaguchi, and T. Saito. 2005. Toll-like receptor 9 is expressed on follicle-associated epithelia containing M cells in swine Peyer's patches. Immunol. Lett. 98:83-89.
94. Simic, V., and A. Ilic. 1976. Essential comparative, morphological and topographical differences and characteristics of the cecum in man and domestic animals. Acta Anat. (Basel) 94:299- 310.
95. Skjolaas, K. A., T. E. Burkey, S. S. Dritz, and J. E. Minton. 2006. Effects of Salmonella enterica serovars Typhimurium (ST) and Choleraesusis (SC) on chemokine and cytokine expression in swine ileum and jejunal epithelial cells. Vet. Immunol. Immunopathol. 111:199-209.
96. Somekh, E., F. Serour, A. Gorenstein, M. Vohl, and D. Lehman. 2000. Phenotypic pattern of B cells in the appendix: Reduced intensity of CD19 expression. Immunobiology 201:461-469.
97. Spencer, J., T. Finn, and P. G. Isaacson. 1985. Gut associated lymphoid tissue: A morphological and immunocytochemical study of the human appendix. Gut 26:672-679.
98. Stokes, C. R., M. Bailey, and K. Haverson. 2001. Development and Function of the Pig Gastrointestinal Immune System. Pages 59-66 in Digestive Physiology of Pigs. J. E. Lindberg and B. Ogle, ed. CAB Int., New York, NY.
99. Stokes, C. R., M. Bailey, and A. D. Wilson. 1994. Immunology of the porcine gastrointestinal tract. Vet. Immunol. Immunopathol. 43:143-150.
100. Suau, A., R. Bonnet, M. Sutren, J. J. Godon, G. R. Gibson, M. D. Collins, and J. Dore. 1999. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl. Environ. Microbiol. 65:4799-4807.
101. Suzuki, K., T. Oida, H. Hamada, O. Hitotsumatsu, M. Watanabe, T. Hibi, H. Yamamoto, E. Kubota, S. Kaminogawa, and H. Ishikawa. 2000. Gut cryptopatches: Direct evidence of extrathymic anatomical sites for intestinal T lymphopoiesis. Immunity 13:691-702.
102. Takeda, K., and S. Akira. 2003. Toll receptors and pathogen resistance. Cell. Microbiol. 5:143-153.
103. Tohno, M., T. Shimazu, H. Aso, A. Uehara, H. Takada, A. Kawasaki, Y. Fujimoto, K. Fukase, T. Saito, and H. Kitazawa. 2008a. Molecular cloning and functional characterization of porcine nucleotide-binding oligomerization domain-1 (NODI) recognizing minimum agonists, meso-diaminopimelic acid and mesolanthionine. Mol. Immunol. 45:1807-1817.
104. Tohno, M., T. Shimosato, H. Kitazawa, S. Katoh, I. D. Iliev, T. Kimura, Y. Kawai, K. Watanabe, H. Aso, T. Yamaguchi, and T. Saito. 2005. Toll-like receptor 2 is expressed on the intestinal M cells in swine. Biochem. Biophys. Res. Commun. 330:547- 554.
105. Tohno, M., W. Ueda, Y. Azuma, T. Shimazu, S. Katoh, J. M. Wang, H. Aso, H. Takada, Y. Kawai, T. Saito, and H. Kitazawa. 2008b. Molecular cloning and functional characterization of porcine nucleotide-binding oligomerization domain-2 (NOD2). Mol. Immunol. 45:194-203.
106. Turner, J. R. 2003. Functional morphology of the intestinal mucosae: From crypts to tips. Pages 1-22 in Microbial Pathogenesis and the Intestinal Epithelial Cell. G. Hecht, ed. ASM Press, Washington, DC.
107. Tyrer, P., A. R. Foxwell, A. W. Cripps, M. A. Apicella, and J. M. Kyd. 2006. Microbial pattern recognition receptors mediate M-cell uptake of a gram-negative bacterium. Infect. Immun. 74:625-631.
108. Uenishi, H., and H. Shinkai. 2008. Porcine Toll-like receptors: The front line of pathogen monitoring and possible implications for disease resistance. Dev. Comp. Immunol. In press.
109. Vega-Lopez, M. A., G. Arenas-Contreras, M. Bailey, S. Gonzalez- Pozos, C. R. Stokes, M. G. Ortega, and R. Mondragon-Flores. 2001. Development of intraepithelial cells in the porcine small intestine. Dev. Immunol. 8:147-158.
110. Vega-Lopez, M. A., E. Telemo, M. Bailey, K. Stevens, and C. R. Stokes. 1993. Immune cell distribution in the small intestine of the pig: Immunohistological evidence for an organized compartmentalization in the lamina propria. Vet. Immunol. Immunopathol. 37:49-60.
111. Vora, P., A. Youdim, L. S. Thomas, M. Fukata, S. Y. Tesfay, K. Lukasek, K. S. Michelsen, A. Wada, T. Hirayama, M. Arditi, and M. T. Abreu. 2004. Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J. Immunol. 173:5398-5405.
112. W'erling, D., and T. W. Jungi. 2003. Toll-like receptors linking innate and adaptive immune response. Vet. Immunol. Immunopathol. 91:1-12.
113. Wittig, B. M., and M. Zeitz. 2003. The gut as an organ of immunology. Int. J. Colorectal Dis. 18:181-187.
114. Zhang, G., H. Wu, J. Shi, T. Ganz, C. R. Ross, and F. Blecha. 1998. Molecular cloning and tissue expression of porcine betadefensin-1. FEES Lett. 424:37-40.
115. Zhu, J., K. Lai, R. Brownile, L. A. Babiuk, and G. K. Mutwiri. 2008. Porcine TLR8 and TLR7 are both activated by a selective TLR7 ligand, imiquimod. Mol. Immunol. 45:3238-3243.