Functional Advantages of Porphyromonas gingivalis Vesicles

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.

Biogenesis and Function of Porphyromonas Gingivalis Outer Membrane Vesicles

“…showed earlier that Prochlorococcus vesicles contain DNA fragments covering 50% of the entire chromosomal sequence and RNA from 95% of all open reading frames [40]. Recently, we observed presence of ribonucleic acids in P. gingivalis vesicles [41]. DNA fragments of genes encoding the major subunit of fimbriae ( fimA and mfa1 ), superoxide dismutase ( sod ) and gingipains were detected, using PCR at relatively higher levels.…”

“…RNAs were also isolated and identified from purified vesicles of P. gingivalis . Furthermore, vesicle-mediated horizontal gene transfer was detected between P. gingivalis strains with efficiency at 1.9 × 10 −7 [41], suggesting that packing DNA and RNA within vesicles could be one of the driving forces for the evolution of bacteria in the oral cavity ecosystem.…”

“…Several well-known membrane proteins involved in P. gingivalis attachment to, and invasion of, host cells have been identified within vesicles, including FimA, hemagglutinin A and heat-stress protein (HtrA) [50 –53]. Not surprisingly, therefore, vesicles derived from P. gingivalis have been found to invade human primary oral epithelial cells, gingival fibroblasts and human umbilical vein endothelial cells [20,54–56]. Consistent with the invasive activity of P. gingivalis cells, 33277 vesicles, a strain with relatively high invasive activity was found to enter gingival epithelial cells and fibroblasts more efficiently than W83 vesicles.…”

“…However, it has not been confirmed if live cells of P. gingivalis cause low-grade inflammation in the walls of arterial vessels. With recent findings, including the efficient invasive activity of vesicles and the presence of vesicle-associated major outer membrane proteins, DNA and RNA in P. gingivalis vesicles [20,41,42], it is likely that vesicles serve a significant role in atherosclerosis and represent a ‘Trojan horse’ to induce infections at secondary sites, such as in the walls of vessels than intact P. gingivalis cells. This concept is supported by in vitro studies that P. gingivalis vesicles, like their originating cells, were able to induce macrophages to form foam cells [71] and to serve as an activator of platelet aggregation [72].…”

The RNA Complement of Outer Membrane Vesicles From Salmonella enterica Serovar Typhimurium Under Distinct Culture Conditions

“…Interestingly, OMVs contain a wide range of RNAs including ribosomal RNA (rRNA), transfer RNA (tRNA), messenger RNA (mRNA), and small non-coding RNA (sRNA) (Ghosal et al, 2015; Ho et al, 2015; Sjöström et al, 2015; Blenkiron et al, 2016; Choi et al, 2017; Soares et al, 2017; Dauros-Singorenko et al, 2018), which indicates that OMVs are important to study in the context of extracellular RNA communication.…”