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Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17

BACKGROUND: Prevotella intermedia (P. intermedia), a gram-negative, black-pigmented anaerobic rod, has been implicated in the development of chronic oral infection. P. intermedia strain 17 was isolated from a chronic periodontitis lesion in our laboratory and described as a viscous material producin...

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Autores principales: Yamanaka, Takeshi, Furukawa, Tomoyo, Matsumoto-Mashimo, Chiho, Yamane, Kazuyoshi, Sugimori, Chieko, Nambu, Takayuki, Mori, Naoki, Nishikawa, Hiroyuki, Walker, Clay B, Leung, Kai-Poon, Fukushima, Hisanori
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2009
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2633007/
https://www.ncbi.nlm.nih.gov/pubmed/19146705
http://dx.doi.org/10.1186/1471-2180-9-11
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author Yamanaka, Takeshi
Furukawa, Tomoyo
Matsumoto-Mashimo, Chiho
Yamane, Kazuyoshi
Sugimori, Chieko
Nambu, Takayuki
Mori, Naoki
Nishikawa, Hiroyuki
Walker, Clay B
Leung, Kai-Poon
Fukushima, Hisanori
author_facet Yamanaka, Takeshi
Furukawa, Tomoyo
Matsumoto-Mashimo, Chiho
Yamane, Kazuyoshi
Sugimori, Chieko
Nambu, Takayuki
Mori, Naoki
Nishikawa, Hiroyuki
Walker, Clay B
Leung, Kai-Poon
Fukushima, Hisanori
author_sort Yamanaka, Takeshi
collection PubMed
description BACKGROUND: Prevotella intermedia (P. intermedia), a gram-negative, black-pigmented anaerobic rod, has been implicated in the development of chronic oral infection. P. intermedia strain 17 was isolated from a chronic periodontitis lesion in our laboratory and described as a viscous material producing strain. The stock cultures of this strain still maintain the ability to produce large amounts of viscous materials in the spent culture media and form biofilm-like structures. Chemical analyses of this viscous material showed that they were mainly composed of neutral sugars with mannose constituting 83% of the polysaccharides. To examine the biological effect of the extracellular viscous materials, we identified and obtained a naturally-occurring variant strain that lacked the ability to produce viscous materials in vitro from our stock culture collections of strain 17, designated as 17-2. We compared these two strains (strains 17 versus 17-2) in terms of their capacities to form biofilms and to induce abscess formation in mice as an indication of their pathogenicity. Further, gene expression profiles between these two strains in planktonic condition and gene expression patterns of strain 17 in solid and liquid cultures were also compared using microarray assays. RESULTS: Strain 17 induced greater abscess formation in mice as compared to that of the variant. Strain 17, but not 17-2 showed an ability to interfere with the phagocytic activity of human neutrophils. Expression of several genes which including those for heat shock proteins (DnaJ, DnaK, ClpB, GroEL and GroES) were up-regulated two to four-fold with statistical significance in biofilm-forming strain 17 as compared to the variant strain 17-2. Strain 17 in solid culture condition exhibited more than eight-fold up-regulated expression levels of several genes which including those for levanase, extracytoplasmic function-subfamily sigma factor (σ(E); putative) and polysialic acid transport protein (KpsD), as compared to those of strain 17 in liquid culture media. CONCLUSION: These results demonstrate that the capacity to form biofilm in P. intermedia contribute to their resistance against host innate defence responses.
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spelling pubmed-26330072009-01-30 Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17 Yamanaka, Takeshi Furukawa, Tomoyo Matsumoto-Mashimo, Chiho Yamane, Kazuyoshi Sugimori, Chieko Nambu, Takayuki Mori, Naoki Nishikawa, Hiroyuki Walker, Clay B Leung, Kai-Poon Fukushima, Hisanori BMC Microbiol Research article BACKGROUND: Prevotella intermedia (P. intermedia), a gram-negative, black-pigmented anaerobic rod, has been implicated in the development of chronic oral infection. P. intermedia strain 17 was isolated from a chronic periodontitis lesion in our laboratory and described as a viscous material producing strain. The stock cultures of this strain still maintain the ability to produce large amounts of viscous materials in the spent culture media and form biofilm-like structures. Chemical analyses of this viscous material showed that they were mainly composed of neutral sugars with mannose constituting 83% of the polysaccharides. To examine the biological effect of the extracellular viscous materials, we identified and obtained a naturally-occurring variant strain that lacked the ability to produce viscous materials in vitro from our stock culture collections of strain 17, designated as 17-2. We compared these two strains (strains 17 versus 17-2) in terms of their capacities to form biofilms and to induce abscess formation in mice as an indication of their pathogenicity. Further, gene expression profiles between these two strains in planktonic condition and gene expression patterns of strain 17 in solid and liquid cultures were also compared using microarray assays. RESULTS: Strain 17 induced greater abscess formation in mice as compared to that of the variant. Strain 17, but not 17-2 showed an ability to interfere with the phagocytic activity of human neutrophils. Expression of several genes which including those for heat shock proteins (DnaJ, DnaK, ClpB, GroEL and GroES) were up-regulated two to four-fold with statistical significance in biofilm-forming strain 17 as compared to the variant strain 17-2. Strain 17 in solid culture condition exhibited more than eight-fold up-regulated expression levels of several genes which including those for levanase, extracytoplasmic function-subfamily sigma factor (σ(E); putative) and polysialic acid transport protein (KpsD), as compared to those of strain 17 in liquid culture media. CONCLUSION: These results demonstrate that the capacity to form biofilm in P. intermedia contribute to their resistance against host innate defence responses. BioMed Central 2009-01-16 /pmc/articles/PMC2633007/ /pubmed/19146705 http://dx.doi.org/10.1186/1471-2180-9-11 Text en Copyright ©2009 Yamanaka et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research article
Yamanaka, Takeshi
Furukawa, Tomoyo
Matsumoto-Mashimo, Chiho
Yamane, Kazuyoshi
Sugimori, Chieko
Nambu, Takayuki
Mori, Naoki
Nishikawa, Hiroyuki
Walker, Clay B
Leung, Kai-Poon
Fukushima, Hisanori
Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17
title Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17
title_full Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17
title_fullStr Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17
title_full_unstemmed Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17
title_short Gene expression profile and pathogenicity of biofilm-forming Prevotella intermedia strain 17
title_sort gene expression profile and pathogenicity of biofilm-forming prevotella intermedia strain 17
topic Research article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2633007/
https://www.ncbi.nlm.nih.gov/pubmed/19146705
http://dx.doi.org/10.1186/1471-2180-9-11
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