Abstract
The infection of mice with the wild-type (WT) strain of Y. pseudotuberculosis did not induce polyclonal activation of B lymphocytes. Suppression in the production of certain isotypes of Ig was observed, provoked mainly by YopH, YopJ and YpkA. The WT strain induced a progressive increase in the serum-specific IgG, which peaked after 4 weeks after infection, IgM being produced only after 1 week. Autoantibodies against phosphorylcholine, myelin, thyroglobulin and cardiolipin could be detected in the serum of mice infected with the WT strain. The infection of mice provoked suppression in the production of immunoglobulins by splenic B cells and that YopH, YopJ and YpkA must be involved here.
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Abbreviations
- Ab(s):
-
antibody(ies)
- BCIP:
-
5-bromo-4-chloro-3-indolylphosphate
- BSA:
-
bovine serum albumin
- ELISA:
-
enzyme-linked immunosorbent assay
- ELISPOT:
-
enzyme-linked spot assay
- ERK:
-
extracellular receptor-activated kinase
- HRP:
-
horseradish peroxidase
- ICAM-1:
-
intercellular adhesion molecule-1
- Ig:
-
immunoglobulin
- IL-8:
-
interleukin 8
- JNK:
-
c-Jun N-terminal kinase
- LAT:
-
linker for activation of T cells
- LD50 :
-
lethal dose 50 %
- MAPK:
-
mitogen-activated protein kinases
- NF-κB:
-
nuclear factor κB
- NK:
-
natural killer cell
- PBS:
-
phosphate-buffered saline
- PBS/T PBS:
-
containing 500 ppm Tween 20
- PBS/T/BSA PBS/T:
-
containing 1 % BSA
- PVDF:
-
polyvinylidene fluoride
- RANTES:
-
regulated by activation, normal T cell expressed and secreted
- SLP-76:
-
SH2-domain-containing leukocyte protein of 76 kDa
- TCR:
-
T cell antigen receptor
- TNF-α:
-
tumor necrosis factor α
- WT:
-
wild type
- Yops:
-
Yersinia outer proteins
References
Alonso A., Bottini N., Bruckner S., Rahmouni S., Williams S., Schoenberger P., Mustelin T.: Lck dephosphorylation at Tyr-394 and inhibition of T cell antigen receptor signaling by Yersinia phosphatase YopH. J.Biol.Chem. 279, 4922–4928 (2004).
Arencibia I., Suarez N.C., Wolf-Watz H., Sundqvist K.G.: Yersinia invasin, a bacterial beta1-integrin ligand, is a potent inducer of lymphocyte motility and migration to collagen type IV and fibronectin. J.Immunol. 159, 1853–1859 (1997).
Autenrieth I.B., Firsching R.: Penetration of M cells and destruction of Peyer’s patches by Yersinia enterocolitica: an ultrastructural and histological study. J.Med.Microbiol. 44, 285–294 (1996).
Autenrieth I.B., Hantschmann P., Heymer B., Heesemann J.: Imunohistological characterization of the cellular immune response against Yersinia enterocolitica in mice: evidence for the involvement of T lymphocytes. Immunobiology 187, 1–16 (1993).
Cornelis G.R., Boland A., Boyd A.P., Geuijen C., Iriarte M., Neyt C., Sory M.-P., Stainier I.: The virulence plasmid of Yersinia, an antihost genome. Microbiol.Mol.Biol. 62, 1315–1352 (1998).
Costa A.M.: Células esplênicas secretoras de imunoglobulinas e anticorpos séricos em camundongos Swiss livres de patógenos específicos inoculados com Yersinia enterocolitica O:3 ou derivados. MSc Thesis. Instituto de Biologia, Universidade Estadual de Campinas, Campinas (SP) 1995.
Crespo A.M.C., Falcão D.P., Araújo P.M.F., Medeiros B.M.M.: Effects of Yersinia enterocolitica O:3 derivatives on B lymphocyte activation in vivo. Microbiol.Immunol. 46, 95–100 (2002).
Czerkinsky C.C., Nilsson L.A., Nygren H., Ouchterlony O., Tarkowsi A.: A solid-phase enzyme-linked immunospot (ELISPOT) assay for enumeration of specific antibody-secreting cells. J.Immunol.Meth. 65, 109–121 (1983).
Galyov E.E., Hakansson S., Forsberg A., Wolf-Watz H.: A secreted protein kinase of Yersinia pseudotuberculosis is an indispensable virulence determinant. Nature 361, 730–732 (1993).
Gerke C., Falkow S., Chien Y.: The adaptor molecules LAT and SLP-76 are specifically targeted by Yersinia to inhibit T cell activation. J.Exp.Med. 201, 361–371 (2005).
Gripenberg M., Miettinen A., Kurki P., Linder E.: Humoral immune stimulation and antiepithelial antibodies in Yersinia infection. Arthritis Rheum. 21, 904–908 (1978).
Heeseman J., Gross V., Schmidt N., Laufs R.: Immunochemical analysis of plasmid-encoded proteins released by enteropathogenic Yersinia sp. grown in calcium-deficient media. Infect.Immun. 54, 561–567 (1986).
Heesemann J., Sing A., Trulzsch K.: Yersinia’s stratagen: targeting innate and adaptive immune defense. Curr.Opin.Microbiol. 9, 55–61 (2006).
Heinicke E., Kumar U., Munoz D.G.: Quantitative dot-blot assay for proteins using enhanced chemiluminescence. J.Immunol.Meth. 152, 227–236 (1992).
Juris S.J., Rudolph A.E., Huddler D., Orth K., Dixon J.E.: A distinctive role for the Yersinia protein kinase: actin binding, kinase activation, and cytoskeleton disruption. Proc.Nat.Acad.Sci.USA 97, 9431–9436 (2000).
Juris S.J., Shah K., Shokat K., Dixon J.E., Vacratsis P.O.: Identification of otubain 1 as a novel substrate for the Yersinia protein kinase using chemical genetics and mass spectrometry. FEBS Lett. 580, 179–183 (2006).
Kerchen E.J., Cohen D.A., Kaplan A.M., Straley S.C.: The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infect.Immun. 72, 4589–4602 (2004).
Leung K.Y., Reisner B.S., Straley S.C.: YopM inhibits platelet aggregation and is necessary for virulence of Yersinia pestis in mice. Infect.Immun. 58, 3263–3271 (1990).
Longsdon L.K., Mecsas J.: Requirement of the Yersinia pseudotuberculosis effectors YopH and YopE in colonization and persistence in intestinal and lymph tissues. Infect.Immun. 71, 4595–4607 (2003).
Lundgren E., Carballeira N., Vazquez R., Dubinina E., Branden H., Person H., Wolf-Watz H.: Invasin of Yersinia pseudotuberculosis activates human peripheral B cells. Infect.Immun. 64, 829–835 (1996).
Maki-Ikola O., Lahesmaa R., Heesemann J., Merilahti-Palo R., Saario R., Toivanen A., Granfors K.: Yersinia-specific antibodies in serum and synovial fluid in patients with Yersinia-triggered reactive arthritis. Ann.Rheum.Dis. 53, 535–539 (1994).
Medeiros B.M.M., Mendes-Giannini M.J.S., Falcão D.P.: Imunoglobulin isotypes produced by mice experimentally infected with Yersinia sp. Contrib.Microbiol.Immunol. 12, 117–122 (1991).
Medeiros B.M.M., Souza C.D., Higuti L., Maia J.M., Silva E.E.C.: Papel das proteínas “Yops” de Yersinia pseudotuberculosis na ativaxão de linfócitos B. Rev.Ciênc.Farm. São Paulo 24, 53–60 (2003).
Mulder D.M., Michiels T., Simonet M., Sory M.P., Cornelis G.: Identification of additional virulence determinants on the pYV plasmid of Yersinia enterocolitica W227. Infect.Immun. 57, 2534–2541 (1989).
Palmer L.E., Hobbie S., Galán J.E., Bliska J.B.: YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-α production and downregulation of the MAP kinases p38 and JNK. Mol.Microbiol. 27, 953–965 (1998).
Prehna G., Ivanov M.I., Bliska J.B., Stebbins C.E.: Yersinia virulence depends on mimicry of host Rho-family nucleotide dissociation inhibitors. Cell 126, 869–880 (2006).
Reed L.J., Muench H.: A simple method of estimating fifty per cent endpoints. Am.J.Hyg. 27, 493–497 (1938).
Rosqvist R., Bölin I., Wolf-Watz H.: Inhibition of phagocytosis in Yersinia pseudotuberculosis: a virulence plasmid-encoded ability involving the Yop2b protein. Infect.Immun. 56, 2139–2143 (1988).
Rosqvist R., Forsberg A., Wolf-Watz H.: Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect.Immun. 59, 4562–4569 (1991).
Ruckdeschel K.: Immunomodulation of macrophages by pathogenic Yersinia species. Arch.Immunol.Ther.Exp. 50, 131–137 (2002).
Schesser K., Spiik A.K., Dukuzumuremiy J.M., Neurath M.F., Petterson S., Wolf-Watz H.: The yopJ locus is required for Yersinia-mediated inhibition of NF-κB activation and cytokine expression; YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol.Microbiol. 28, 1067–1079 (1998).
Schotte P., Denecker G., Van Den Broeke A., Vandenabeele P., Cornelis G.R., Beyaert R.: Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1β. J.Biol.Chem. 279, 25134–25142(2004).
Shenkman L., Bottone E.J.: The occurrence of antibodies to Yersinia enterocolitica in thyroid diseases, pp. 135–144 in E.J. Bottone (Ed.): Yersinia enterocolitica. CRC Press, Boca Raton 1981.
Silva E.E.C., Ramos O.P., Bauab T.M., Falcão D.P., Medeiros B.M.M.: Yersinia enterocolitica O:3 isolated from patients with or without reactive arthritis induces polyclonal activation of B cells and autoantibody production in vivo. Autoimmunity 36, 261–268 (2003).
Sonnevend A., Czirok E., Pal T.: Yersinia Yop-specific IgA antibodies in Hungarian blood donors. Folia Microbiol. 50, 269–272 (2005).
Straley S.C., Bowner W.S.: Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect.Immun. 51, 445–454 (1986).
Toivanen A., Granfors K., Lahesmaa-Rantala R., Leino R., Stahlberg T., Vuento R.: Pathogenesis of Yersinia-triggered reactive arthritis: immunological, microbiological and clinical aspects. Immunol.Rev. 86, 47–70 (1985).
Trulzsch K., Sporleder T., Igwe E.I., Russmann H., Heesemann J.: Contribution of the major secreted Yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model. Infect.Immun. 72, 5227–5234 (2004).
Trulzsch K., Sporleder T., Leibiger R., Russmann H., Heesemann J.: Yersinia as oral live carrier vaccine: influence of Yersinia outer proteins (Yops) on the T-cell response. Internat.J.Med.Microbiol. 298, 59–67 (2007).
Viboud G.I., Bliska J.B.: A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J. 20, 5373–5382 (2001).
Von Pawel-Rammingen U., Telepnev M.V., Schmidt G., Aktories K., Wolf-Watz H., Rosqvist R.: GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway; a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 36, 737–748 (2000).
Yao T., Mecsas J., Healy J.I., Falkow S., Chien Y.-H.: Suppression of T and B lymphocyte activation by a Yersinia pseudotuberculosis virulence factor, YopH. J.Exp.Med. 190, 1343–1350 (1999).
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Maia, J.M.L., Monnazzi, L.G.S. & Medeiros, B.M.M. Role of Yersinia pseudotuberculosis outer proteins (Yops) in murine humoral immune response. Folia Microbiol 54, 239–245 (2009). https://doi.org/10.1007/s12223-009-0038-1
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DOI: https://doi.org/10.1007/s12223-009-0038-1