Abstract
The ability of Bvg(-)-phase and Bvg(+)-phase Bordetella bronchiseptica swine isolates, grown under modulating or nonmodulating conditions, to adhere to swine ciliated nasal epithelial cells was determined. When virulent strains were cultivated at 37 degrees C in the Bvg+ phase, numerous adherent bacteria (approximately eight per cell, depending on the strain used) were observed. However, when such strains were grown under modulating conditions (23 degrees C), a significant increase in the level of attachment was seen, suggesting that B. bronchiseptica produces a Bvg-repressed adhesin under these conditions. bvg mutant strains, including an isogenic bvgS mutant, adhered minimally. Western blots indicated that two putative B. bronchiseptica adhesins, filamentous hemagglutinin and pertactin, were not detectable in cultures displaying the highly adherent phenotype. Several proteins apparent in Western blots obtained by using bacterial extracts enriched in outer membrane proteins derived from B. bronchiseptica grown at 23 degrees C were not present in similar extracts prepared from an isogenic bvgS mutant grown at 23 degrees C or from the parent strain grown at 37 degrees C. Adherence of bacteria cultivated at 23 degrees C was almost completely abolished by pretreatment of organisms at 60 degrees C; adherence was reduced by 57% when bacteria were pretreated with pronase E. Temperature shift experiments revealed that the heightened level of adhesion that occurs following growth at 23 degrees C was maintained for up to 18 h when bacteria were subsequently incubated at 37 degrees C. We propose that a Bvg-repressed adhesin, expressed only by modulated bvg+ strains of B. bronchiseptica, may play a key role in the initial colonization of naturally infected swine.
Full Text
The Full Text of this article is available as a PDF (620.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Ackermann M. R., Register K. B., Gentry-Weeks C., Gwaltney S. M., Magyar T. A porcine model for the evaluation of virulence of Bordetella bronchiseptica. J Comp Pathol. 1997 Jan;116(1):55–61. doi: 10.1016/s0021-9975(97)80043-6. [DOI] [PubMed] [Google Scholar]
- Ackermann M. R., Rimler R. B., Thurston J. R. Experimental model of atrophic rhinitis in gnotobiotic pigs. Infect Immun. 1991 Oct;59(10):3626–3629. doi: 10.1128/iai.59.10.3626-3629.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Akerley B. J., Cotter P. A., Miller J. F. Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell. 1995 Feb 24;80(4):611–620. doi: 10.1016/0092-8674(95)90515-4. [DOI] [PubMed] [Google Scholar]
- Akerley B. J., Miller J. F. Flagellin gene transcription in Bordetella bronchiseptica is regulated by the BvgAS virulence control system. J Bacteriol. 1993 Jun;175(11):3468–3479. doi: 10.1128/jb.175.11.3468-3479.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aricò B., Nuti S., Scarlato V., Rappuoli R. Adhesion of Bordetella pertussis to eukaryotic cells requires a time-dependent export and maturation of filamentous hemagglutinin. Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9204–9208. doi: 10.1073/pnas.90.19.9204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Aricó B., Miller J. F., Roy C., Stibitz S., Monack D., Falkow S., Gross R., Rappuoli R. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6671–6675. doi: 10.1073/pnas.86.17.6671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beattie D. T., Shahin R., Mekalanos J. J. A vir-repressed gene of Bordetella pertussis is required for virulence. Infect Immun. 1992 Feb;60(2):571–577. doi: 10.1128/iai.60.2.571-577.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brennan M. J., Li Z. M., Cowell J. L., Bisher M. E., Steven A. C., Novotny P., Manclark C. R. Identification of a 69-kilodalton nonfimbrial protein as an agglutinogen of Bordetella pertussis. Infect Immun. 1988 Dec;56(12):3189–3195. doi: 10.1128/iai.56.12.3189-3195.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chung W. B., Collins M. T., Bäckström L. R. Adherence of Bordetella bronchiseptica and Pasteurella multocida to swine nasal ciliated epithelial cells in vitro. APMIS. 1990 May;98(5):453–461. [PubMed] [Google Scholar]
- Collings L. A., Rutter J. M. Virulence of Bordetella bronchiseptica in the porcine respiratory tract. J Med Microbiol. 1985 Apr;19(2):247–255. doi: 10.1099/00222615-19-2-247. [DOI] [PubMed] [Google Scholar]
- Cotter P. A., Miller J. F. A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. Mol Microbiol. 1997 May;24(4):671–685. doi: 10.1046/j.1365-2958.1997.3821741.x. [DOI] [PubMed] [Google Scholar]
- Cotter P. A., Miller J. F. BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect Immun. 1994 Aug;62(8):3381–3390. doi: 10.1128/iai.62.8.3381-3390.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Deeb B. J., DiGiacomo R. F., Bernard B. L., Silbernagel S. M. Pasteurella multocida and Bordetella bronchiseptica infections in rabbits. J Clin Microbiol. 1990 Jan;28(1):70–75. doi: 10.1128/jcm.28.1.70-75.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doucet J. P., Murphy B. J., Tuana B. S. Modification of a discontinuous and highly porous sodium dodecyl sulfate-polyacrylamide gel system for minigel electrophoresis. Anal Biochem. 1990 Nov 1;190(2):209–211. doi: 10.1016/0003-2697(90)90182-9. [DOI] [PubMed] [Google Scholar]
- Foster L. A., Dyer D. W. A siderophore production mutant of Bordetella bronchiseptica cannot use lactoferrin as an iron source. Infect Immun. 1993 Jun;61(6):2698–2702. doi: 10.1128/iai.61.6.2698-2702.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gagné S., Martineau-Doizé B. Nasal epithelial changes induced in piglets by acetic acid and by Bordetella bronchiseptica. J Comp Pathol. 1993 Jul;109(1):71–81. doi: 10.1016/s0021-9975(08)80241-1. [DOI] [PubMed] [Google Scholar]
- Giardina P. C., Foster L. A., Musser J. M., Akerley B. J., Miller J. F., Dyer D. W. bvg Repression of alcaligin synthesis in Bordetella bronchiseptica is associated with phylogenetic lineage. J Bacteriol. 1995 Nov;177(21):6058–6063. doi: 10.1128/jb.177.21.6058-6063.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goodnow R. A. Biology of Bordetella bronchiseptica. Microbiol Rev. 1980 Dec;44(4):722–738. doi: 10.1128/mr.44.4.722-738.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ishikawa H., Isayama Y. Bovine erythrocyte-agglutinin as a possible adhesin of Bordetella bronchiseptica responsible for binding to porcine nasal epithelium. J Med Microbiol. 1988 Jul;26(3):205–209. doi: 10.1099/00222615-26-3-205. [DOI] [PubMed] [Google Scholar]
- Ishikawa H., Isayama Y. Effect of antigenic modulation and phase variation on adherence of Bordetella bronchiseptica to porcine nasal epithelial cells. Am J Vet Res. 1987 Dec;48(12):1689–1691. [PubMed] [Google Scholar]
- Knapp S., Mekalanos J. J. Two trans-acting regulatory genes (vir and mod) control antigenic modulation in Bordetella pertussis. J Bacteriol. 1988 Nov;170(11):5059–5066. doi: 10.1128/jb.170.11.5059-5066.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leininger E., Ewanowich C. A., Bhargava A., Peppler M. S., Kenimer J. G., Brennan M. J. Comparative roles of the Arg-Gly-Asp sequence present in the Bordetella pertussis adhesins pertactin and filamentous hemagglutinin. Infect Immun. 1992 Jun;60(6):2380–2385. doi: 10.1128/iai.60.6.2380-2385.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leininger E., Probst P. G., Brennan M. J., Kenimer J. G. Inhibition of Bordetella pertussis filamentous hemagglutinin-mediated cell adherence with monoclonal antibodies. FEMS Microbiol Lett. 1993 Jan 1;106(1):31–38. doi: 10.1111/j.1574-6968.1993.tb05931.x. [DOI] [PubMed] [Google Scholar]
- Leininger E., Roberts M., Kenimer J. G., Charles I. G., Fairweather N., Novotny P., Brennan M. J. Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):345–349. doi: 10.1073/pnas.88.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Magyar T., Chanter N., Lax A. J., Rutter J. M., Hall G. A. The pathogenesis of turbinate atrophy in pigs caused by Bordetella bronchiseptica. Vet Microbiol. 1988 Oct;18(2):135–146. doi: 10.1016/0378-1135(88)90059-4. [DOI] [PubMed] [Google Scholar]
- Magyar T. Virulence and lienotoxicity of Bordetella bronchiseptica in mice. Vet Microbiol. 1990 Nov;25(2-3):199–207. doi: 10.1016/0378-1135(90)90077-9. [DOI] [PubMed] [Google Scholar]
- Nakai T., Kume K., Yoshikawa H., Oyamada T., Yoshikawa T. Adherence of Pasteurella multocida or Bordetella bronchiseptica to the swine nasal epithelial cell in vitro. Infect Immun. 1988 Jan;56(1):234–240. doi: 10.1128/iai.56.1.234-240.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Porter J. F., Parton R., Wardlaw A. C. Growth and survival of Bordetella bronchiseptica in natural waters and in buffered saline without added nutrients. Appl Environ Microbiol. 1991 Apr;57(4):1202–1206. doi: 10.1128/aem.57.4.1202-1206.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Porter J. F., Wardlaw A. C. Long-term survival of Bordetella bronchiseptica in lakewater and in buffered saline without added nutrients. FEMS Microbiol Lett. 1993 Jun 1;110(1):33–36. doi: 10.1111/j.1574-6968.1993.tb06291.x. [DOI] [PubMed] [Google Scholar]
- Rappuoli R. Pathogenicity mechanisms of Bordetella. Curr Top Microbiol Immunol. 1994;192:319–336. doi: 10.1007/978-3-642-78624-2_14. [DOI] [PubMed] [Google Scholar]
- Ross R. F., Switzer W. P., Duncan J. R. Comparison of pathogenicity of various isolates of Bordetella bronchiseptica in young pigs. Can J Comp Med Vet Sci. 1967 Feb;31(2):53–57. [PMC free article] [PubMed] [Google Scholar]
- Scarlato V., Aricó B., Domenighini M., Rappuoli R. Environmental regulation of virulence factors in Bordetella species. Bioessays. 1993 Feb;15(2):99–104. doi: 10.1002/bies.950150205. [DOI] [PubMed] [Google Scholar]
- Schilowa B., Krüger M., Horsch F. Untersuchungen zur Differenzierung von Bordetella-bronchiseptica-Stämmen. 6. Mitteilung: Nachweis von Adhäsinen bei Bordetella bronchiseptica. Arch Exp Veterinarmed. 1988 Nov;42(6):867–876. [PubMed] [Google Scholar]
- Semjén G., Magyar T. A bovine haemagglutinin of Bordetella bronchiseptica responsible for adherence. Acta Vet Hung. 1985;33(3-4):129–136. [PubMed] [Google Scholar]
- Stibitz S., Weiss A. A., Falkow S. Genetic analysis of a region of the Bordetella pertussis chromosome encoding filamentous hemagglutinin and the pleiotropic regulatory locus vir. J Bacteriol. 1988 Jul;170(7):2904–2913. doi: 10.1128/jb.170.7.2904-2913.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yokomizo Y., Shimizu T. Adherence of Bordetella bronchiseptica to swine nasal epithelial cells and its possible role in virulence. Res Vet Sci. 1979 Jul;27(1):15–21. [PubMed] [Google Scholar]