Functional Advantages of Porphyromonas gingivalis Vesicles
Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cel...
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Published in | PloS one Vol. 10; no. 4; p. e0123448 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
21.04.2015
Public Library of Science (PLoS) |
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Abstract | Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cells and gingival fibroblasts, in order to promote aggregation of some specific oral bacteria and to induce host immune responses. In the present study, we investigated the invasive efficiency of P. gingivalis OMVs and compared results with that of the originating cells. Results revealed that 70-90% of human primary oral epithelial cells, gingival fibroblasts, and human umbilical vein endothelial cells carried vesicles from P. gingivalis 33277 after being exposed to the vesicles for 1 h, while 20-50% of the host cells had internalized P. gingivalis cells. We also detected vesicle-associated DNA and RNA and a vesicle-mediated horizontal gene transfer in P. gingivalis strains, which represents a novel mechanism for gene transfer between P. gingivalis strains. Moreover, purified vesicles of P. gingivalis appear to have a negative impact on biofilm formation and the maintenance of Streptococcus gordonii. Our results suggest that vesicles are likely the best offence weapon of P. gingivalis for bacterial survival in the oral cavity and for induction of periodontitis. |
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AbstractList | Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P. gingivalis vesicles, are able to invade oral epithelial cells and gingival fibroblasts, in order to promote aggregation of some specific oral bacteria and to induce host immune responses. In the present study, we investigated the invasive efficiency of P. gingivalis OMVs and compared results with that of the originating cells. Results revealed that 70-90% of human primary oral epithelial cells, gingival fibroblasts, and human umbilical vein endothelial cells carried vesicles from P. gingivalis 33277 after being exposed to the vesicles for 1 h, while 20-50% of the host cells had internalized P. gingivalis cells. We also detected vesicle-associated DNA and RNA and a vesicle-mediated horizontal gene transfer in P. gingivalis strains, which represents a novel mechanism for gene transfer between P. gingivalis strains. Moreover, purified vesicles of P. gingivalis appear to have a negative impact on biofilm formation and the maintenance of Streptococcus gordonii. Our results suggest that vesicles are likely the best offence weapon of P. gingivalis for bacterial survival in the oral cavity and for induction of periodontitis. Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of this bacterium. Previous studies indicated that like their originating cells, P . gingivalis vesicles, are able to invade oral epithelial cells and gingival fibroblasts, in order to promote aggregation of some specific oral bacteria and to induce host immune responses. In the present study, we investigated the invasive efficiency of P . gingivalis OMVs and compared results with that of the originating cells. Results revealed that 70–90% of human primary oral epithelial cells, gingival fibroblasts, and human umbilical vein endothelial cells carried vesicles from P . gingivalis 33277 after being exposed to the vesicles for 1 h, while 20–50% of the host cells had internalized P . gingivalis cells. We also detected vesicle-associated DNA and RNA and a vesicle-mediated horizontal gene transfer in P . gingivalis strains, which represents a novel mechanism for gene transfer between P . gingivalis strains. Moreover, purified vesicles of P . gingivalis appear to have a negative impact on biofilm formation and the maintenance of Streptococcus gordonii . Our results suggest that vesicles are likely the best offence weapon of P . gingivalis for bacterial survival in the oral cavity and for induction of periodontitis. |
Audience | Academic |
Author | Goodwin, J. Shawn Ho, Meng-Hsuan Chen, Chin-Ho Wang, Bing-Yan Xie, Hua |
AuthorAffiliation | 2 Department of Surgery, Duke University Medical Center, Durham, North Carolina, United States of America University of Oklahoma Health Sciences Center, UNITED STATES 3 Department of Biochemistry and Cancer Biology, Meharry Medical College, Nashville, Tennessee, United States of America 1 School of Dentistry, Meharry Medical College, Nashville, Tennessee, United States of America 4 Department of Periodontics, School of Dentistry, University of Texas, Health Science Center at Houston, Houston, Texas, United States of America |
AuthorAffiliation_xml | – name: 1 School of Dentistry, Meharry Medical College, Nashville, Tennessee, United States of America – name: 2 Department of Surgery, Duke University Medical Center, Durham, North Carolina, United States of America – name: 3 Department of Biochemistry and Cancer Biology, Meharry Medical College, Nashville, Tennessee, United States of America – name: 4 Department of Periodontics, School of Dentistry, University of Texas, Health Science Center at Houston, Houston, Texas, United States of America – name: University of Oklahoma Health Sciences Center, UNITED STATES |
Author_xml | – sequence: 1 givenname: Meng-Hsuan surname: Ho fullname: Ho, Meng-Hsuan – sequence: 2 givenname: Chin-Ho surname: Chen fullname: Chen, Chin-Ho – sequence: 3 givenname: J. Shawn surname: Goodwin fullname: Goodwin, J. Shawn – sequence: 4 givenname: Bing-Yan surname: Wang fullname: Wang, Bing-Yan – sequence: 5 givenname: Hua surname: Xie fullname: Xie, Hua |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25897780$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2015 Public Library of Science 2015 Ho et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2015 Ho et al 2015 Ho et al |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: HX CHC. Performed the experiments: HX MHH JSG. Analyzed the data: HX CHC MHH. Contributed reagents/materials/analysis tools: HX BYW JSG. Wrote the paper: HX MHH CHC JSG BYW. |
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Snippet | Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of... Porphyromonas gingivalis is a keystone pathogen of periodontitis. Outer membrane vesicles (OMVs) have been considered as both offense and defense components of... |
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SubjectTerms | Atherosclerosis Bacteria Bacteroidaceae Infections - microbiology Biofilms Candida albicans Cell Membrane Cells, Cultured Dentistry Deoxyribonucleic acid DNA Endothelial cells Extracellular Vesicles - physiology Fibroblasts Fibroblasts - microbiology Fibroblasts - physiology Gene Transfer, Horizontal Genes, Bacterial Gram-negative bacteria Host-Pathogen Interactions Human Umbilical Vein Endothelial Cells - microbiology Human Umbilical Vein Endothelial Cells - physiology Humans Immune response Keratinocytes - microbiology Keratinocytes - physiology Pathogens Periodontics Periodontitis - microbiology Porphyromonas gingivalis Porphyromonas gingivalis - physiology Proteins Pseudomonas aeruginosa Ribonucleic acid RNA Vesicles |
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Title | Functional Advantages of Porphyromonas gingivalis Vesicles |
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