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Immune complexes of E. coli antigens and maternal IgG in the bursa of Fabricius

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Abstract

The bursa of Fabricius of the chicken is known to be both a primary lymphoid organ and a secondary lymphoid tissue. Bursal follicles are equipped with antigen-trapping follicle-associated epithelium. However, bioactive antigens such as protein and bacteria have not been detected in the bursal parenchyma. By immunoperoxidase staining with a polyspecific antibody (Ab) against Escherichia coli, we detected aggregated E. coli antigens in the medulla of bursal follicles after hatching. The distribution of aggregated E. coli antigens is restricted to the medulla of bursal follicles. The antigens are not found in the spleen or the parenchyma of the caecal tonsil. The bursa is thus a trapping site for E. coli antigens from the external environment. Furthermore, two-color immunostaining clarified that these antigens form immune complexes with maternal IgG (MIgG) and are retained by reticular cells. Additionally, immune complexes in the bursa were shown to induce the rapid development of serum IgM Ab for indigenous E. coli. Our results suggest that immune complexes of MIgG and environmental antigens in the medulla of bursal follicles exert positive effects on B-cell differentiation in the bursa in situ.

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Abbreviations

Ab:

Antibody

BDL:

Bursal duct ligation

CLSM:

Confocal laser scanning microscopy

ELISA:

Enzyme-linked immunosorbent assay

FAE:

Follicle-associated epithelium

FDC:

Follicular dendritic cell

MIgG:

Maternal IgG

TPBS:

Phosphate-buffered saline with 0.05 % Tween 20

References

  • Bockman DE, Cooper MD (1973) Pinocytosis by epithelium associated with lympoid follicles in the bursa of Fabricius, appendix, and Peyer’s patches. An electron microscopic study. Am J Anat 136:455–478

    Article  PubMed  CAS  Google Scholar 

  • Boes M, Prodeus AP, Schmidt T, Carroll MC, Chen J (1998) A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J Exp Med 188:2381–2386

    Article  PubMed  CAS  Google Scholar 

  • Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23:282–288

    Article  PubMed  Google Scholar 

  • Brambell FWR (1970) Transmission of immunity in birds. The transmission of passive immunity from mother to young. North Holland, Amsterdam

    Google Scholar 

  • Castillo CB, Bruckner DA (1984) Comparative evaluation of the Eiken and API 20E systems and conventional methods for identification of members of the family Enterobacteriaceae. J Clin Microbiol 20:754–757

    PubMed  CAS  Google Scholar 

  • Chen CH, Lehmeyer JE, Cooper MD (1982) Evidence for an IgD homologous on chicken lymphocytes. J Immunol 129:2580–2585

    PubMed  CAS  Google Scholar 

  • Ekino S, Matsuno K, Kotani M (1979a) Distribution and role of lymph vessels of the bursa of Fabricii. Lymphology 12:247–252

    PubMed  CAS  Google Scholar 

  • Ekino S, Matsuno K, Harada S, Fujii H, Nawa Y, Kotani M (1979b) Amplification of plaque-forming cells in the spleen after intracloacal antigen stimulation in neonatal chicken. Immunology 37:811–815

    PubMed  CAS  Google Scholar 

  • Ekino S, Nawa Y, Tanaka K, Matsuno K, Fujii H, Kotani M (1980) Suppression of immune response by isolation of the bursa of Fabricius from environmental stimuli. Aus J Exp Biol Med Sci 58:289–296

    Article  CAS  Google Scholar 

  • Ekino S, Suginohara K, Urano T, Fujii H, Matsuno K, Kotani M (1985) The bursa of Fabricius: a trapping site for environmental antigens. Immunology 55:405–410

    PubMed  CAS  Google Scholar 

  • Ekino S, Riwar B, Kroese FGM, Schwander EH, Koch G, Niuwenhuis P (1995) Role of environmental antigen in the development of IgG+ cells in the bursa of Fabricius. J Immunol 155:4551–4558

    PubMed  CAS  Google Scholar 

  • Ekino S, Arakawa H, Sonoda K, Noguchi K, Inui S, Yokoyama H, Kodama Y (2012) The origin of IgG-containing cells in the bursa of Fabricius. Cell Tissue Res 348:537–550

    Article  PubMed  CAS  Google Scholar 

  • Fuller R (1973) Differences in the microfloras of the intestine and the bursa of Fabricius as illustrated by the E. coliform/lacto-bacillus ratio in the two sites. Br Poult Sci 14:221–224

    Article  PubMed  CAS  Google Scholar 

  • Grossi CE, Lydyard PM, Cooper MD (1977) Medullary localization of extracellular immunoglobulin and aminopeptidase in lymphoepithelial follicles of the chicken bursa of Fabricius and rabbit appendix. Dev Comp Immunol 1:157–164

    Article  PubMed  CAS  Google Scholar 

  • Hamal K, Burgess SC, Pevzner IY, Erf GF (2006) Maternal antibody transfer from dams to their egg yolks, egg whites, and chicks in meat lines of chickens. Poult Sci 85:1364–1372

    PubMed  CAS  Google Scholar 

  • Hasselquist D, Nilsson J-A (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos Trans R Soc Lond Biol 364:51–60

    Article  PubMed  Google Scholar 

  • Haycock KH, Roth J, Gagnon J, Finzer WF, Soper C (1992) StatView. Abacus Concepts, Berkeley

    Google Scholar 

  • Kimura N, Yoshikane M, Kobayashi A (1986) Microflora of the bursa of Fabricius of chickens. Poult Sci 65:1801–1807

    Article  PubMed  CAS  Google Scholar 

  • Koch G, Jongenelen ICMA (1989) Enzyme immunospot assay for the detection of immunoglobulin- and antibody-secreting cells in chickens. In: Koch G, Bhogal B (eds) Recent advances in avian immunology research. Liss, New York, pp 67–77

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Liu Y, van Kruiningen HJ , West AB, Cartun RW, Cortot A, Colombel JF (1995) Immunocytochemical evidence of Listeria, Escherichia coli, and Streptococcus antigens in Crohn’s disease. Gastroenterology 108:1396–1404

    Article  PubMed  CAS  Google Scholar 

  • Lydyard PM, Grossi CE, Cooper MD (1976) Ontogeny of B cells in the chicken. I. Sequential development of clonal diversity in the bursa. J Exp Med 144:79–97

    Article  PubMed  CAS  Google Scholar 

  • Mandel TE, Philipps RP, Abbot A, Tew JG (1980) The folliclular dendritic cell: long term antigen retention during immunity. Immunol Rev 53:29–59

    Article  PubMed  CAS  Google Scholar 

  • Martin LN, Leslie GA (1973) Ontogeny of IgA in normal and neonatally bursectomized chickens, with corroborative data on IgY and IgM. Proc Soc Exp Biol Med 143:241–243

    Article  PubMed  CAS  Google Scholar 

  • Owen RL, Bhalla DK (1983) Lympho-epithelial organs and lymph nodes. In: Hodges GM, Carr KE (eds) Biomedical research applications of scanning electron microscopy, vol 3. Academic Press, London, pp 79–169

    Google Scholar 

  • Paramithiotis E, Ratcliffe MJH (1993) Bursa-dependent subpopulations of peripheral B lymphocytes in chicken blood. Eur J Immunol 23:96–102

    Article  PubMed  CAS  Google Scholar 

  • Rajewsky K, Foster I, Cumano A (1987) Evolutionary and somatic selection of the antibody repertoire in the mouse. Science 238:1088–1094

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe MJH, Tkalec L (1990) Cross-linking of the surface immunoglobulin on lymphocytes from the bursa of Fabricius results in second messenger generation. Eur J Immunol 20:1073–1078

    Article  PubMed  CAS  Google Scholar 

  • Ratcliffe MJH (2006) Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev Comp Immunol 30:101–118

    Article  PubMed  CAS  Google Scholar 

  • Reynaud C-A, Bertocci B, Dahan A, Weil J-C (1994) Formation of the chicken B-cell repertoire: ontogenesis, regulation of Ig gene rearrangement, and diversification by gene conversion. Adv Immunol 57:353–378

    Article  PubMed  CAS  Google Scholar 

  • Rose ME, Orlans E (1981) Immunoglobulins in the egg, embryo and young chick. Dev Comp Immunol 5:15–21

    Article  PubMed  CAS  Google Scholar 

  • Schaffner T, Mueller J, Hess MW, Cottier H, Sordat B, Ropke C (1974) The bursa of Fabricius: a central organ providing for contact between the lymphoid system and intestinal content. Cell Immunol 13:304–312

    Article  PubMed  CAS  Google Scholar 

  • Sorvari R, Sorvari TE (1977) Bursa Fabricii as a peripheral lymphoid organ. Transport of various materials from the anal lips to the bursal lymphoid follicles with reference to its immunological importance. Immunology 32:499–505

    PubMed  CAS  Google Scholar 

  • Sorvari T, Sorvari R, Ruotsalainen P, Toivanen A, Toivanen P (1975) Uptake of environmental antigens by the bursa of Fabricius. Nature 253:217–219

    Article  PubMed  CAS  Google Scholar 

  • Viertlboeck BC, Schweinsberg S, Hanczaruk MA, Schmitt R, Du Pasquier L, Herberg F, Göbel TW (2007) The chicken leucocyte receptor complex encodes a primordial, activating, high-affinity IgY Fc receptor. Proc Natl Acad Sci USA 104:11718–11723

    Article  PubMed  CAS  Google Scholar 

  • Walmsley RS, Anthony A, Sim R, Pounder RE, Wakefield AJ (1998) Absence of Escherichia coli, Listeria monocytogenes, and Klebsiella pneumoniae antigens within inflammatory bowel disease tissues. J Clini Pathol 51:657–661

    Article  CAS  Google Scholar 

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Acknowledgment

We thank Dr. S. Kawamura and Ms. M. Susa for their helpful discussions.

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Authors and Affiliations

  1. Department of Histology, Graduate School of Medical Sciences, Kumamoto University, Honjo, Kumamoto, Japan

    Kayoko Sonoda, Kazuhiro Noguchi & Shigeo Ekino

Authors
  1. Kayoko Sonoda
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  2. Kazuhiro Noguchi
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  3. Shigeo Ekino
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Corresponding author

Correspondence to Shigeo Ekino.

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This work was supported in part by the Mishima Kaiun Memorial Foundation and Nisshin Seifun Group in Japan.

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Sonoda, K., Noguchi, K. & Ekino, S. Immune complexes of E. coli antigens and maternal IgG in the bursa of Fabricius. Cell Tissue Res 354, 813–821 (2013). https://doi.org/10.1007/s00441-013-1701-z

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  • DOI: https://doi.org/10.1007/s00441-013-1701-z

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