Abstract
We demonstrate immunomodulatory effects, especially those involving murine intestinal IgA secretion, in Peyer's patch cells following oral administration of Bifidobacterium immunomodulator (BIM) derived from sonicated B. pseudocatenulatum 7041. BALB/c mice were administered BIM orally for 7 consecutive days. The PP cells demonstrated upregulated secretion of total IgA including BIM-specific IgA following BIM administration. In observing the response of PP cells co-cultured with BIM, we found enhanced secretion of interferon-γ (IFN-γ) and interleukin (IL)-6 in the CD4+ T cells. In contrast, IL-12 secretion by Thy1.2− PP cells was enhanced, but secretion of IFN-γ, IL-5, and IL-6 was not significantly affected. Furthermore, the population of CD4+ CD45RBhigh T cells in PP increased following oral administration of BIM. These data suggest that CD4+ T cells were affected by BIM administration. Overall, the results show that oral administration of BIM induced CD4+ PP cells to change their expression of cell surface antigen and cytokine production.
Keywords: Bifidobacterium, Helper T cell, Peyer's patch, Probiotics
Full Text
The Full Text of this article is available as a PDF (268.6 KB).
Glossary
- APCs
antigen presenting cells
- BIM
Bifidobacterium immunomodulater
- DC
dendritic cells
- IFN-c
interferon-c
- IL
interleukin
- Mφ
macrophage
- PP
PeyerÆs patch
- Th1
type 1 helper T
- Th2
type 2 helper T
References
- Aattour N., Bouras M., Tome D., Marcos A., Lemonnier D. Oral ingestion of lactic-acid bacteria by rats increases lymphocyte proliferation and interferon-gamma production. Br. J. Nutr. 2002;87:367–373. doi: 10.1079/bjnbjn2001527. [DOI] [PubMed] [Google Scholar]
- Banchereau J., Briere F., Caux C., Davoust J., Lebecque S., Liu Y.J., Pulendran B., Palucka K. Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000;18:767–811. doi: 10.1146/annurev.immunol.18.1.767. [DOI] [PubMed] [Google Scholar]
- Defrance T., Vanbervliet B., Briere F., Durand I., Rousset F., Banchereau J. Interleukin 10 and transforming growth factor beta cooperate to induce anti-CD40-activated naive human B cells to secrete immunoglobulin A. J. Exp. Med. 1992;175:671–682. doi: 10.1084/jem.175.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fukushima Y., Kawata Y., Hara H., Terada A., Mitsuoka T. Effect of a probiotic formula on intestinal immunoglobulin A production in healthy children. Int. J. Food Microbiol. 1998;42:39–44. doi: 10.1016/S0168-1605(98)00056-7. [DOI] [PubMed] [Google Scholar]
- Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., Akira S. A toll-like receptor recognizes bacterial DNA. Nature. 2000;408:740–745. doi: 10.1038/35047123. [DOI] [PubMed] [Google Scholar]
- Horgan K.J., Tanaka Y., Luce G.E., Seventer G.A., Nutman T.B., Shaw S. CD45RB expression defines two interconvertible subsets of human CD4+ T cells with memory function. Eur. J. Immunol. 1994;24:1240–1243. doi: 10.1002/eji.1830240536. [DOI] [PubMed] [Google Scholar]
- Hosono A., Lee J., Ametani A., Natsume M., Hirayama M., Adachi T., Kaminogawa S. Characterization of a water-soluble polysaccharide fraction with immunopotentiating activity from Bifidobacterium adolescentis M101–4. Biosci. Biotechnol. Biochem. 1997;61:312–316. doi: 10.1271/bbb.61.312. [DOI] [PubMed] [Google Scholar]
- Hosono A., Lee J., Ametani A., Natsume M., Hirayama M., Adachi T., Kaminogawa S. Comparison of the immunopotentiating activity with structural characteristics among water-soluble polysaccharides isolated from the genus Bifidobacterium. Biosci. Microflora. 1998;17:97–104. [Google Scholar]
- Hosono A., Ozawa A., Kato R., Ohnishi Y., Nakanishi Y., Kimura T., Nakamura R. Dietary fructooligosaccharides induce immunoregulation of intestinal IgA secretion by murine Peyer’s patch cells. Biosci. Biotechnol. Biochem. 2003;67:758–764. doi: 10.1271/bbb.67.758. [DOI] [PubMed] [Google Scholar]
- Ibnou-Zekri N., Blum S., Schiffrin E.J., Der Weid T. Divergent patterns of colonization and immune response elicited from two intestinal Lactobacillus strains that display similar properties in vitro. Infect. Immun. 2003;71:428–436. doi: 10.1128/IAI.71.1.428-436.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janeway C.A., Jr. Presidential address to the american association of immunologists. The road less traveled by: the role of innate immunity in the adaptive immune response. J. Immunol. 1998;161:539–544. [PubMed] [Google Scholar]
- Kaila M., Isolauri E., Soppi E., Virtanen E., Laine S., Arvilommi H. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr. Res. 1992;32:141–144. doi: 10.1203/00006450-199208000-00002. [DOI] [PubMed] [Google Scholar]
- Kalliomaki M., Salminen S., Arvilommi H., Kero P., Koskinen P., Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet. 2001;357:1076–1079. doi: 10.1016/S0140-6736(00)04259-8. [DOI] [PubMed] [Google Scholar]
- Kiyono H., Bienenstock J., Mcghee J.R., Ernst P.B. The mucosal immune system: features of inductive and effector sites to consider in mucosal immunization and vaccine development. Reg. Immunol. 1992;4:54–62. [PubMed] [Google Scholar]
- Kuraoka M., Hashiguchi M., Hachimura S., Kaminogawa S. CD4(−)c-kit(−)CD3epsilon(−)IL-2Ralpha(+) Peyer’s patch cells are a novel cell subset which secrete IL-5 in response to IL-2: implications for their role in IgA production. Eur. J. Immunol. 2004;34:1920–1929. doi: 10.1002/eji.200324696. [DOI] [PubMed] [Google Scholar]
- Lee J., Ametani A., Enomoto A., Sato Y., Motosima H., Ike F., Kaminogawa S. Screening for the immunopotentiating activity of the immune response by Bifidobacterium adolescentis M101–4. Biosci. Biotech. Biochem. 1993;57:2127–2132. [Google Scholar]
- Mcghee J.R., Mestecky J., Dertzbaugh M.T., Eldridge J.H., Hirasawa M., Kiyono H. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine. 1992;10:75–88. doi: 10.1016/0264-410X(92)90021-B. [DOI] [PubMed] [Google Scholar]
- Park J.H., Um J.I., Lee B.J., Goh J.S., Park S.Y., Kim W.S., Kim P.H. Encapsulated Bifidobacterium bifidum potentiates intestinal IgA production. Cell Immunol. 2002;219:22–27. doi: 10.1016/S0008-8749(02)00579-8. [DOI] [PubMed] [Google Scholar]
- Poltorak A., He X., Smirnova I., Liu M.Y., Huffel C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282:2085–2088. doi: 10.1126/science.282.5396.2085. [DOI] [PubMed] [Google Scholar]
- Powrie F. T cells in inflammatory bowel disease: protective and pathogenic roles. Immunity. 1995;3:171–174. doi: 10.1016/1074-7613(95)90086-1. [DOI] [PubMed] [Google Scholar]
- Salminen S., Bouley C., Boutron-Ruault M.C., Cummings J.H., Franck A., Gibson G.R., Isolauri E., Moreau M.C., Roberfroid M., Rowland I. Functional food science and gastrointestinal physiology and function. Br. J. Nutr. 1998;80:S147–S171. doi: 10.1079/BJN19980108. [DOI] [PubMed] [Google Scholar]
- Sekine K., Watanabe-Sekine E., Toida T., Kasashima T., Kataoka T., Hashimoto Y. Adjuvant activity of the cell wall of Bifidobacterium infantis for in vivo immune responses in mice. Immunopharmacol. Immunotoxicol. 1994;16:589–609. doi: 10.3109/08923979409019741. [DOI] [PubMed] [Google Scholar]
- Shida K., Takahashi R., Iwadate E., Takamizawa K., Yasui H., Sato T., Habu S., Hachimura S., Kaminogawa S. Lactobacillus casei strain Shirota suppresses serum immunoglobulin E and immunoglobulin G1 responses and systemic anaphylaxis in a food allergy model. Clin. Exp. Allergy. 2002;32:563–570. doi: 10.1046/j.0954-7894.2002.01354.x. [DOI] [PubMed] [Google Scholar]
- Shroff K.E., Meslin K., Cebra J.J. Commensal enteric bacteria engender a self-limiting humoral mucosal immune response while permanently colonizing the gut. Infect. Immun. 1995;63:3904–3913. doi: 10.1128/iai.63.10.3904-3913.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shu Q., Gill H.S. A dietary probiotic (Bifidobacterium lactis HN019) reduces the severity of Escherichia coli O157:H7 infection in mice. Med. Microbiol. Immunol. (Berl) 2001;189:147–152. doi: 10.1007/s430-001-8021-9. [DOI] [PubMed] [Google Scholar]
- Silva A.M., Barbosa F.H., Duarte R., Vieira L.Q., Arantes R.M., Nicoli J.R. Effect of Bifidobacterium longum ingestion on experimental salmonellosis in mice. J. Appl. Microbiol. 2004;97:29–37. doi: 10.1111/j.1365-2672.2004.02265.x. [DOI] [PubMed] [Google Scholar]
- Sutas Y., Autio S., Rantala I., Isolauri E. IFN-gamma enhances macromolecular transport across Peyer's patches in suckling rats: implications for natural immune responses to dietary antigens early in life. J. Pediatr. Gastroenterol. Nutr. 1997;24:162–169. doi: 10.1097/00005176-199702000-00009. [DOI] [PubMed] [Google Scholar]
- Takahashi T., Nakagawa E., Nara T., Yajima T., Kuwata T. Effects of orally ingested Bifidobacterium longum on the mucosal IgA response of mice to dietary antigens. Biosci. Biotechnol. Biochem. 1998;62:10–15. doi: 10.1271/bbb.62.10. [DOI] [PubMed] [Google Scholar]
- Takeuchi O., Akira S. Genetic approaches to the study of Toll-like receptor function. Microbe. Infect. 2002;4:887–895. doi: 10.1016/S1286-4579(02)01615-5. [DOI] [PubMed] [Google Scholar]
- Ten Hove T., The Olle F., Berkhout M., Bruggeman J.P., Vyth-Dreese F.A., Slors J.F., Deventer S.J., Te Velde A.A. Expression of CD45RB functionally distinguishes intestinal T lymphocytes in inflammatory bowel disease. J. Leukoc. Biol. 2004;75:1010–1015. doi: 10.1189/jlb.0803400. [DOI] [PubMed] [Google Scholar]
- Xu-Amano J., Beagley K.W., Mega J., Fujihashi K., Kiyono H., Mcghee J.R. Induction of T helper cells and cytokines for mucosal IgA responses. Adv. Exp. Med. Biol. 1992;327:107–117. doi: 10.1007/978-1-4615-3410-5_13. [DOI] [PubMed] [Google Scholar]
- Yang R.B., Mark M.R., Gray A., Huang A., Xie M.H., Zhang M., Goddard A., Wood W.I., Gurney A.L., Godowski P.J. Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature. 1998;395:284–288. doi: 10.1038/26239. [DOI] [PubMed] [Google Scholar]
- Yoshida T., Hachimura S., Ishimori M., Kinugasa F., Ise W., Totsuka M., Ametani A., Kaminogawa S. Antigen presentation by Peyer's patch cells can induce both Th1- and Th2-type responses depending on antigen dosagebut a different cytokine response pattern from that of spleen cells. Biosci. Biotechnol. Biochem. 2002;66:963–969. doi: 10.1271/bbb.66.963. [DOI] [PubMed] [Google Scholar]
- Yoshimura A., Lien E., Ingalls R.R., Tuomanen E., Dziarski R., Golenbock D. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 1999;163:1–5. [PubMed] [Google Scholar]