Ileal Peyer's patches are not necessary for systemic B cell development and maintenance and do not contribute significantly to the overall B cell pool in swine

Journal of Immunology

Volumn 187, Issue 10, 2011, Pages 5150-5161

  Sinkora, Marek ^a   Stepanova, Katerina ^a   Butler, John E ^b   Francis, David ^c   Santiago Mateo, Kristina ^c   Potockova, Hana ^a   Karova, Kristyna ^a   Sinkorova, Jana ^a  

^a INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^b UNIVERSITY OF IOWA   (United States)

^c SOUTH DAKOTA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; COMMENSAL; CONTROLLED STUDY; ESCHERICHIA COLI; FLOW CYTOMETRY; ILEUM; MITOSIS; NONHUMAN; PEYER PATCH; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; SWINE;

ANIMALS; ANIMALS, NEWBORN; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; CELL LINEAGE; FEMALE; GERM-FREE LIFE; ILEUM; LYMPHOCYTE COUNT; LYMPHOPOIESIS; PEYER'S PATCHES; SWINE;

EID: 81455154975     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101879     Document Type: Article

References (67)

1. Carlens, O. 1928. Studien über das lymphatische gewebe des darmkanals bei einigen haustieren, mit besonderer berüksichtigung der embryonalen entwicklung, der mengenverhältnisse und der altersinvolution dieses gewebes im dünndarm des rindes. Z. Anat. Entwicklungsgesch. 86: 393-493.
2. Yasuda, M., C. N. Jenne, L. J. Kennedy, and J. D. Reynolds. 2006. The sheep and cattle Peyer's patch as a site of B-cell development. Vet. Res. 37: 401-415.
3. Rothkoetter, H. J., and R. Pabst. 1989. Lymphocyte subsets in jejunal and ileal Peyer's patches of normal and gnotobiotic minipigs. Immunology 67: 103-108. (Pubitemid 19153138)
4. Barman, N. N., A. T. J. Bianchi, R. J. Zwart, R. Pabst, and H. J. Rothkoetter. 1997. Jejunal and ileal Peyer's patches in pigs differ in their postnatal development. Anat. Embryol. (Berl.) 195: 41-50. (Pubitemid 27032553)
5. Reynolds, J. D., and B. Morris. 1983. The evolution and involution of Peyer's patches in fetal and postnatal sheep. Eur. J. Immunol. 13: 627-635.
6. Binns, R. M. 1982. Organisation of the lymphoreticular system and lymphocyte markers in the pig. Vet. Immunol. Immunopathol. 3: 95-146.
7. Pabst, R., M. Geist, H. J. Rothkoetter, 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.
8. Hein, W. R., L. Dudler, and C. R. Mackay. 1989. Surface expression of differential antigens on lymphocytes in the ileal and jejunal Peyer's patches of lambs. Immunology 68: 365-370. (Pubitemid 19285010)
9. Reynolds, J. D. 1987. Peyer's patches and the early development of B lymphocytes. Curr. Top. Microbiol. Immunol. 135: 43-56.
10. Griebel, P. J., L. Kennedy, T. Graham, W. C. Davis, and J. D. Reynolds. 1992. Characterization of B-cell phenotypic changes during ileal and jejunal Peyer's patch development in sheep. Immunology 77: 564-570. (Pubitemid 23000478)
11. Reynolds, J. D., L. Kennedy, J. Peppard, and R. Pabst. 1991. Ileal Peyer's patch emigrants are predominately B cells and travel to all lymphoid tissues in sheep. Eur. J. Immunol. 21: 283-289.
12. Griebel, P. J., W. C. Davis, and J. D. Reynolds. 1991. Negative signaling by surface IgM on B cells isolated from ileal Peyer's patch follicles of sheep. Eur. J. Immunol. 21: 2281-2284.
13. 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.
14. 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.
15. Griebel, P. J., and W. R. Hein. 1996. Expanding the role of Peyer's patches in B-cell ontogeny. Immunol. Today 17: 30-39. (Pubitemid 26019255)
16. Butler, J. E., J. Sun, N. Wertz, and M. Sinkora. 2006. Antibody repertoire development in swine. Dev. Comp. Immunol. 30: 199-221. (Pubitemid 41408493)
17. Gerber, H. A., B. Morris, and W. Trevella. 1986. The role of gut-associated lymphoid tissues in the generation of immunoglobulin-bearing lymphocytes in sheep. Aust. J. Exp. Biol. Med. Sci. 64: 201-213.
18. Reynolds, J. D., and B. Morris. 1984. The effect of antigen on the development of Peyer's patches in sheep. Eur. J. Immunol. 14: 1-6. (Pubitemid 14184420)
19. + cells following a single injection of an anti-IgM antibody early in gestation. Immunology 88: 28-34.
20. Reynolds, J. D. 1986. Evidence of extensive lymphocyte death in sheep Peyer's patches, I: A comparison of lymphocyte proliferation and export. J. Immunol. 136: 2005-2010. (Pubitemid 16122279)
21. Reynolds, J. D. 1987. Mitotic rate maturation in the Peyer's patches of fetal sheep and in the bursa of Fabricius of the chick embryo. Eur. J. Immunol. 17: 503-507. (Pubitemid 17094148)
22. Motyka, B., and J. D. Reynolds. 1991. Apoptosis is associated with the extensive B cell death in the sheep ileal Peyer's patch and the chicken bursa of Fabricius: a possible role in B cell selection. Eur. J. Immunol. 21: 1951-1958.
23. Andersen, J. K., H. Takamatsu, C. A. L. Oura, S. M. Brookes, L. Pullen, and R. M. E. Parkhouse. 1999. Systematic characterization of porcine ileal Peyer's patches, I: Apoptosis-sensitive immature B cells are the predominant cell type. Immunology 98: 612-621. (Pubitemid 30005345)
24. Reynaud, C. A., C. R. Mackay, R. G. Muller, and J. C. Weill. 1991. Somatic generation of diversity in mammalian primary lymphoid organ: the sheep ileal Peyer's patches. Cell 64: 995-1005.
25. 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. (Pubitemid 126448968)
26. Meffre, E., and H. Wardemann. 2008. B-cell tolerance checkpoints in health and autoimmunity. Curr. Opin. Immunol. 20: 632-638.
27. Yamanaka, T., L. Helgeland, I. N. Farstad, H. Fukushima, T. Midtvedt, and P. Brandtzaeg. 2003. Microbial colonization drives lymphocyte accumulation and differentiation in the follicle-associated epithelium of Peyer's patches. J. Immunol. 170: 816-822. (Pubitemid 36070533)
28. Jenne, C. N., L. J. Kennedy, P. McCullagh, and J. D. Reynolds. 2003. A new model of sheep Ig diversification: shift in the emphasis toward combinatorial mechanisms and away from hypermutation. J. Immunol. 170: 3739-3750. (Pubitemid 36359244)
29. Sinkora, M., J. Sun, and J. E. Butler. 2000. Antibody repertoire development in fetal and neonatal piglets, V: VDJ gene chimeras resembling gene conversion products are generated at high frequency by PCR in vitro. Mol. Immunol. 37: 1025-1034. (Pubitemid 32786715)
30. Butler, J. E., J. Sun, P. Weber, P. Navarro, and D. Francis. 2000. Antibody repertoire development in fetal and newborn piglets, III: Colonization of the gastrointestinal tract selectively diversifies the preimmune repertoire in mucosal lymphoid tissues. Immunology 100: 119-130. (Pubitemid 30242890)
31. Sinkora, M., and J. E. Butler. 2009. The ontogeny of the porcine immune system. Dev. Comp. Immunol. 33: 273-283.
32. Yang, H., and R. M. Parkhouse. 1996. Phenotypic classification of porcine lymphocyte subpopulations in blood and lymphoid tissues. Immunology 89: 76-83. (Pubitemid 26284041)
33. Zuckermann, F. A., and R. J. Husmann. 1996. Functional and phenotypic analysis of porcine peripheral blood CD4/CD8 double-positive T cells. Immunology 87: 500-512. (Pubitemid 26100194)
34. Sinkora, M., J. Sinkora, Z. Rehakova, I. Splichal, H. Yang, R. M. E. Parkhouse, and I. Trebichavsky. 1998. Prenatal ontogeny of lymphocyte subpopulations in pigs. Immunology 95: 595-603. (Pubitemid 28559153)
35. Butler, J. E., P. Weber, M. Sinkora, D. Baker, A. Schoenherr, B. Mayer, and D. Francis. 2002. Antibody repertoire development in fetal and neonatal piglets, VIII: Colonization is required for newborn piglets to make serum antibodies to T-dependent and type 2 T-independent antigens. J. Immunol. 169: 6822-6830. (Pubitemid 36899267)
36. Sinkora, M., J. Sinkora, Z. Rehakova, and J. E. Butler. 2000. Early ontogeny of thymoctes in pigs: Sequential colonization of the thymus by T cell progenitors. J. Immunol. 165: 1832-1839. (Pubitemid 30643133)
37. Minatis, O. P., and D. Jol. 1978. Gnotobiotic pigs: derivation and rearing. Can. J. Comp. Med. 42: 428-437.
38. Mateo, K. S., J. Ayres, M. Zhao, J. E. Butler, and D. H. Francis. 2011. Intestinal resection and anastomosis in neonatal gnotobiotic piglets. J. Am. Assoc. Lab. Anim. Sci. 50: 361-364.
39. Butler, J. E., K. Santiago-Mateo, X.-Z. Sun, N. Wertz, M. Sinkora, and D. H. Francis. 2011. Antibody repertoire development in fetal and neonatal piglets. XX. B cell lymphogenesis is absent in the ileal Peyer's patches, their repertoire development is antigen dependent, and they are not required for B cell maintenance. J. Immunol. 187: 5141-5149.
40. Genovese, K. J., R. C. Anderson, R. B. Harvey, and D. J. Nisbet. 2000. Competitive exclusion treatment reduces the mortality and fecal shedding associated with enterotoxigenic Escherichia coli infection in nursery-raised neonatal pigs. Can. J. Vet. Res. 64: 204-207.
41. Sinkora, M., J. Sinkorova, and W. Holtmeier. 2005. Development of γδ thymocyte subsets during prenatal and postnatal ontogeny. Immunology 115: 544-555. (Pubitemid 41032442)
42. + thymocytes behave and diverge differently. J. Immunol. 178: 711-719.
43. Sinkora, J., Z. Rehakova, M. Sinkora, B. Cukrowska, H. Tlaskalova-Hogenova, A. T. Bianchi, and B. De Geus. 1998. Expression of CD2 on porcine B lymphocytes. Immunology 95: 443-449. (Pubitemid 28505702)
44. Gerdts, V., R. R. Uwiera, G. K. Mutwiri, D. J. Wilson, T. Bowersock, A. Kidane, L. A. Babiuk, and P. J. Griebel. 2001. Multiple intestinal "loops" provide an in vivo model to analyse multiple mucosal immune responses. J. Immunol. Methods 256: 19-33. (Pubitemid 32769914)
45. Sinkora, M., J. Sun, J. Sinkorova, R. K. Christenson, S. P. Ford, and J. E. Butler. 2003. Antibody repertoire development in fetal and neonatal piglets, VI: B-cell lymphogenesis occurs at multiple sites with differences in the frequency of inframe rearrangements. J. Immunol. 170: 1781-1788. (Pubitemid 36197393)
46. Perez, C., S. Moreno, A. Summerfield, N. Domenech, B. Alvarez, C. Correa, F. Alonso, A. Ezquerra, J. Dominguez, and C. Revilla. 2007. Characterisation of porcine bone marrow progenitor cells identified by the anti-c-kit (CD117) monoclonal antibody 2B8/BM. J. Immunol. Methods 321: 70-79. (Pubitemid 46441197)
47. Layton, D. S., A. D. Strom, T. E. O'Neil, M. M. Broadway, G. L. Stephenson, K. R. Morris, M. Muralitharan, M. S. Sandrin, F. L. Ierino, and A. G. Bean. 2007. Development of an anti-porcine CD34 monoclonal antibody that identifies hematopoietic stem cells. Exp. Hematol. 35: 171-178. (Pubitemid 46014368)
48. Sinkora, M., J. Sinkorova, and J. E. Butler. 2002. B cell development and VDJ rearrangements in the pig. Vet. Immunol. Immunopathol. 87: 341-346. (Pubitemid 34665259)
49. Gerber, H. A., B. Morris, and W. Trevella. 1986. Humoral immunity in B cell depleted sheep. In Immunology of the sheep. B. Morris, and M. Miyasaka, eds. Roche Institute of Immunology, Basel, p. 187-215.
50. Rothkötter, 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. (Pubitemid 20049606)
51. Yasuda, M., M. Fujino, T. Nasu, and T. Murakami. 2004. Histological studies on the ontogeny of bovine gut-associated lymphoid tissue: appearance of T cells and development of IgG+ and IgA+ cells in lymphoid follicles. Dev. Comp. Immunol. 28: 357-369. (Pubitemid 38091469)
52. Caro, M. R., M. C. Gallego, A. J. Buendia, E. Navarro, and J. A. Navarro. 1998. Postnatal evolution of lymphocyte subpopulations in peripheral blood and lymphoid organs in the goat. Res. Vet. Sci. 65: 145-148. (Pubitemid 128515677)
53. Dobson, B. J., C. G. Mackintosh, and J. F. Griffin. 2010. Development of the thymus and Peyer's patches in the first year of life in red deer (Cervus elaphus). Vet. Immunol. Immunopathol. 137: 93-98.
54. Bianchi, A. T., R. J. Zwart, S. H. Jeurissen, and H. W. Moonene-Leusen. 1992. Development of the B- and T-cell compartments in porcine lymphoid organs from birth to adult life: an immunohistological approach. Vet. Immunol. Immunopathol. 33: 201-221.
55. Miyasaka, M., L. Dudler, G. Bordmann, W. M. Leiserson, H. A. Gerber, J. Reynolds, and Z. Trnka. 1984. Differentiation of B lymphocytes in sheep, I: Phenotypic analysis of ileal Peyer's patch cells and the demonstration of a precursor population for sIg+ cells in the ileal Peyer's patches. Immunology 53: 515-523. (Pubitemid 14020558)
56. Fagarasan, S., K. Kinoshita, M. Muramatsu, K. Ikuta, and T. Honjo. 2001. In situ class switching and differentiation to IgA-producing cells in the gut lamina propria. Nature 413: 639-643. (Pubitemid 32964064)
57. Pillai, S., A. Cariappa, and S. T. Moran. 2004. Positive selection and lineage commitment during peripheral B-lymphocyte development. Immunol. Rev. 197: 206-218. (Pubitemid 38142178)
58. Hao, W. L., and Y. K. Lee. 2004. Microflora of the gastrointestinal tract: a review. Methods Mol. Biol. 268: 491-502.
59. Glick, B., T. S. Chang, and R. G. A. Jaap. 1956. The bursa of Fabricius and antibody production on the domestic fowl. Poult. Sci. 35: 224-225.
60. Archer, O. K., D. E. Sutherland, and R. A. Good. 1963. Appendix of the rabbit: a homologue of the bursa in the chicken? Nature 200: 337-339.
61. Owen, J. J., D. E. Wright, S. Habu, M. C. Raff, and M. D. Cooper. 1977. Studies on the generation of B lymphocytes in fetal liver and bone marrow. J. Immunol. 118: 2067-2072. (Pubitemid 8110548)
62. Friedberg, S. H., and I. L. Weissman. 1974. Lymphoid tissue architecture, II: Ontogeny of peripheral T and B cells in mice: evidence against Peyer's patches as the site of generation of B cells. J. Immunol. 113: 1477-1492.
63. Ekman, A., T. Pessa-Morikawa, J. Liljavirta, M. Niku, and A. Iivanainen. 2010. B-cell development in bovine fetuses proceeds via a pre-B like cell in bone marrow and lymph nodes. Dev. Comp. Immunol. 34: 896-903.
64. Studdert, M. J. 1978. Primary, severe, combined immunodeficiency disease of Arabian foals. Aust. Vet. J. 54: 411-417.
65. Pabst, R., M. Miyasaka, and L. Dudler. 1986. Numbers and phenotype of lymphocytes emigrating from sheep bone marrow after in situ labelling with fluorescein isothiocyanate. Immunology 59: 217-222.
66. Butler, J. E., Y. Zhao, M. Sinkora, N. Wertz, and I. Kacskovics. 2009. Immunoglobulins, antibody repertoire and B cell development. Dev. Comp. Immunol. 33: 321-333.
67. Butler, J. E., and M. Sinkora. 2007. The isolator piglet: a model for studying the development of adaptive immunity. Immunol. Res. 39: 33-51. (Pubitemid 47574895)