Int J Stomatol

Int J Stomatol ›› 2024, Vol. 51 ›› Issue (5): 608-615.doi: 10.7518/gjkq.2024085

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Advances in the role of outer membrane vesicles of Porphyromonas gingivalis in oral diseases and its mechanism

Hongchen Mao(),Zheng Wang,Deqin Yang()   

  1. Dept. of Endodontics, Stomatological Hospital of Chongqing Medical University; Stomatological Hospital of Chongqing Medical University, Chongqing Key Laboratory of Oral Diseases and Biomedical Sciences; Chongqing Municipal Key Laboratory of Oral Biomedical Engineering of Higher Education, Chongqing 401120, China
  • Received:2023-12-07 Revised:2024-05-24 Online:2024-09-01 Published:2024-09-14
  • Contact: Deqin Yang E-mail:2020121258@stu.cqmu.edu.cn;yangdeqin@hospital.cqmu.edu.cn
  • Supported by:
    National Natural Science Foundation of China(31970783);Outstanding Distinguished Professor Program of Chongqing Medical University([2021]215);Future Medical Youth Innovation Program of Chongqing Medical College (W0060)

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Abstract:

Porphyromonas gingivalis (P. gingivalis) is a Gram-negative coccus closely related to chronic periodontitis, and the outer membrane vesicles produced by it play an important role in the pathogenesis of oral diseases as a special vi-rulent factor secretion system. Outer membrane vesicles are nanoscale spherical structures released by bacteria, which are mainly composed of the outer membrane and periplasmic components of bacteria. After being released into the environment, the outer membrane vesicles participate in the copolymerization of various bacteria in the oral cavity and in the formation of a biofilm, and they transport virulence factors to various tissues and organs of the host. The relationship between P. gingivalis outer membrane vesicles and oral diseases has not been systematically expounded in previous studies. In this review, the interaction and mechanism of P. gingivalis outer membrane vesicle virulence protein with the host in common oral diseases were discussed to provide reference for subsequent related research.

Key words: Porphyromonas gingivalis, outer membrane vesicles, periodontitis, periapical periodontitis, oral di-seases

CLC Number: 

  • Q93

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1 Amano A, Chen C, Honma K, et al. Genetic characteristics and pathogenic mechanisms of periodontal pathogens[J]. Adv Dent Res, 2014, 26(1): 15-22.
2 Ishikawa M, Yoshida K, Okamura H, et al. Oral Porphyromonas gingivalis translocates to the liver and regulates hepatic glycogen synthesis through the Akt/GSK-3β signaling pathway[J]. Biochim Biophys Acta, 2013, 1832(12): 2035-2043.
3 Takamura H, Yoshida K, Okamura H, et al. Porphyromonas gingivalis attenuates the insulin-induced phosphorylation and translocation of forkhead box protein O1 in human hepatocytes[J]. Arch Oral Biol, 2016, 69: 19-24.
4 Beveridge TJ. Structures of gram-negative cell walls and their derived membrane vesicles[J]. J Bacteriol, 1999, 181(16): 4725-4733.
5 Mantri CK, Chen CH, Dong XH, et al. Fimbriae-mediated outer membrane vesicle production and invasion of Porphyromonas gingivalis [J]. Microbiologyopen, 2015, 4(1): 53-65.
6 Aguayo S, Schuh CMAP, Vicente B, et al. Association between Alzheimer’s disease and oral and gut microbiota: are pore forming proteins the missing link[J]. J Alzheimers Dis, 2018, 65(1): 29-46.
7 Martos R, Tar I, Nagy AC, et al. Hypercitrullination and anti-citrullinated protein antibodies in chronic apical periodontitis, a laboratory investigation. Does autoimmunity contribute to the pathogenesis[J]. Int Endod J, 2023, 56(5): 584-592.
8 Zhang ZY, Liu DJ, Liu S, et al. The role of Porphyromonas gingivalis outer membrane vesicles in pe-riodontal disease and related systemic diseases[J]. Front Cell Infect Microbiol, 2020, 10: 585917.
9 Toyofuku M, Schild S, Kaparakis-Liaskos M, et al. Composition and functions of bacterial membrane vesicles[J]. Nat Rev Microbiol, 2023, 21(7): 415-430.
10 Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles[J]. Microbiol Mol Biol Rev, 2010, 74(1): 81-94.
11 Turnbull L, Toyofuku M, Hynen AL, et al. Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms[J]. Nat Commun, 2016, 7: 11220.
12 Tsolakos N, Lie K, Bolstad K, et al. Characterization of meningococcal serogroup B outer membrane vesicle vaccines from strain 44/76 after growth in different media[J]. Vaccine, 2010, 28(18): 3211-3218.
13 Smalley JW, Birss AJ, McKee AS, et al. Haemin-restriction influences haemin-binding, haemagglutination and protease activity of cells and extracellular membrane vesicles of Porphyromonas gingivalis W50[J]. FEMS Microbiol Lett, 1991, 69(1): 63-67.
14 Kerr JE, Abramian JR, Dao DH, et al. Genetic exchange of fimbrial alleles exemplifies the adaptive virulence strategy of Porphyromonas gingivalis [J]. PLoS One, 2014, 9(3): e91696.
15 Sartorio MG, Pardue EJ, Feldman MF, et al. Bacte-rial outer membrane vesicles: from discovery to applications[J]. Annu Rev Microbiol, 2021, 75: 609-630.
16 Haurat MF, Aduse-Opoku J, Rangarajan M, et al. Selective sorting of cargo proteins into bacterial me-mbrane vesicles[J]. J Biol Chem, 2011, 286(2): 1269-1276.
17 Sato K, Naito M, Yukitake H, et al. A protein secretion system linked to bacteroidete gliding motility and pathogenesis[J]. Proc Natl Acad Sci U S A, 2010, 107(1): 276-281.
18 Guo Y, Nguyen KA, Potempa J. Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon’s knife to a meat chopper-like brutal degradation of proteins[J]. Periodontol 2000, 2010, 54(1): 15-44.
19 Potempa J, Pavloff N, Travis J. Porphyromonas gingivalis: a proteinase/gene accounting audit[J]. Trends Microbiol, 1995, 3(11): 430-434.
20 Rahman S, Bunning RA, Dobson PR, et al. Bradykinin stimulates the production of prostaglandin E2 and interleukin-6 in human osteoblast-like cells[J]. Biochim Biophys Acta, 1992, 1135(1): 97-102.
21 de Diego I, Veillard F, Sztukowska MN, et al. Structure and mechanism of cysteine peptidase gingipain K (Kgp), a major virulence factor of Porphyromo-nas gingivalis in periodontitis[J]. J Biol Chem, 2014, 289(46): 32291-32302.
22 Mikolajczyk-Pawlinska J, Travis J, Potempa J. Modu-lation of interleukin-8 activity by gingipains from Porphyromonas gingivalis: implications for pathogenicity of periodontal disease[J]. FEBS Lett, 1998, 440(3): 282-286.
23 Cecil JD, O’Brien-Simpson NM, Lenzo JC, et al. Differential responses of pattern recognition receptors to outer membrane vesicles of three periodontal pathogens[J]. PLoS One, 2016, 11(4): e0151967.
24 Gui MJ, Dashper SG, Slakeski N, et al. Spheres of influence: Porphyromonas gingivalis outer membrane vesicles[J]. Mol Oral Microbiol, 2016, 31(5): 365-378.
25 Enersen M, Nakano K, Amano A. Porphyromonas gingivalis fimbriae[J]. J Oral Microbiol, 2013, 5: 10.3402/jom.v5i0.20265.
26 Nagano K, Hasegawa Y, Yoshida Y, et al. A major fimbrilin variant of Mfa1 fimbriae in Porphyromo-nas gingivalis [J]. J Dent Res, 2015, 94(8): 1143-1148.
27 Alaei SR, Park JH, Walker SG, et al. Peptide-based inhibitors of fimbrial biogenesis in Porphyromonas gingivalis [J]. Infect Immun, 2019, 87(3): e00750-e00718.
28 Nagano K. FimA fimbriae of the periodontal di-sease-associated bacterium Porphyromonas gingivalis [J]. Yakugaku Zasshi, 2013, 133(9): 963-974.
29 Harokopakis E, Albzreh MH, Martin MH, et al. TLR2 transmodulates monocyte adhesion and transmigration via Rac1- and PI3K-mediated inside-out signaling in response to Porphyromonas gingivalis fimbriae[J]. J Immunol, 2006, 176(12): 7645-7656.
30 Meghil MM, Tawfik OK, Elashiry M, et al. Disruption of immune homeostasis in human dendritic cells via regulation of autophagy and apoptosis by Porphyromonas gingivalis [J]. Front Immunol, 2019, 10: 2286.
31 El-Awady A, de Sousa Rabelo M, Meghil MM, et al. Polymicrobial synergy within oral biofilm promotes invasion of dendritic cells and survival of consortia members[J]. NPJ Biofilms Microbiomes, 2019, 5(1): 11.
32 Iwami J, Murakami Y, Nagano K, et al. Further evidence that major outer membrane proteins homologous to OmpA in Porphyromonas gingivalis stabilize bacterial cells[J]. Oral Microbiol Immunol, 2007, 22(5): 356-360.
33 Schwechheimer C, Sullivan CJ, Kuehn MJ. Envelope control of outer membrane vesicle production in Gram-negative bacteria[J]. Biochemistry, 2013, 52(18): 3031-3040.
34 Confer AW, Ayalew S. The OmpA family of proteins: roles in bacterial pathogenesis and immunity[J]. Vet Microbiol, 2013, 163(3/4): 207-222.
35 Bélanger M, Kozarov E, Song H, et al. Both the unique and repeat regions of the Porphyromonas gingivalis hemagglutin A are involved in adhesion and invasion of host cells[J]. Anaerobe, 2012, 18(1): 128-134.
36 Roy F, Vanterpool E, Fletcher HM. HtrA in Porphyromonas gingivalis can regulate growth and gingipain activity under stressful environmental conditions[J]. Microbiology (Reading), 2006, 152(Pt 11): 3391-3398.
37 Yuan LH, Rodrigues PH, Bélanger M, et al. Porphyromonas gingivalis htrA is involved in cellular invasion and in vivo survival[J]. Microbiology (Rea-ding), 2008, 154(Pt 4): 1161-1169.
38 Schwechheimer C, Kuehn MJ. Outer-membrane ve-sicles from Gram-negative bacteria: biogenesis and functions[J]. Nat Rev Microbiol, 2015, 13: 605-619.
39 Lim G, Janu U, Chiou LL, et al. Periodontal health and systemic conditions[J]. Dent J (Basel), 2020, 8(4): E130.
40 Kamaguchi A, Nakayama K, Ichiyama S, et al. Effect of Porphyromonas gingivalis vesicles on coaggregation of Staphylococcus aureus to oral microorganisms[J]. Curr Microbiol, 2003, 47(6): 485-491.
41 Park Y, Simionato MR, Sekiya K, et al. Short fim-briae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii [J]. Infect Immun, 2005, 73(7): 3983-3989.
42 Bartruff JB, Yukna RA, Layman DL. Outer membrane vesicles from Porphyromonas gingivalis affect the growth and function of cultured human gingival fibroblasts and umbilical vein endothelial cells[J]. J Periodontol, 2005, 76(6): 972-979.
43 Uemura Y, Hiroshima Y, Tada A, et al. Porphyromonas gingivalis outer membrane vesicles stimulate gingival epithelial cells to induce pro-inflammatory cytokines via the MAPK and STING pathways[J]. Biomedicines, 2022, 10(10): 2643.
44 Fleetwood AJ, Lee MKS, Singleton W, et al. Metabolic remodeling, inflammasome activation, and pyroptosis in macrophages stimulated by Porphyromonas gingivalis and its outer membrane vesicles[J]. Front Cell Infect Microbiol, 2017, 7: 351.
45 Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries[J]. CA Cancer J Clin, 2021, 71(3): 209-249.
46 Irfan M, Delgado RZR, Frias-Lopez J. The oral microbiome and cancer[J]. Front Immunol, 2020, 11: 591088.
47 Zhang L, Liu Y, Zheng HJ, et al. The oral microbiota may have influence on oral cancer[J]. Front Cell Infect Microbiol, 2019, 9: 476.
48 Katz J, Onate MD, Pauley KM, et al. Presence of Porphyromonas gingivalis in gingival squamous cell carcinoma[J]. Int J Oral Sci, 2011, 3(4): 209-215.
49 Sharma M, Bairy I, Pai K, et al. Salivary IL-6 levels in oral leukoplakia with dysplasia and its clinical re-levance to tobacco habits and periodontitis[J]. Clin Oral Investig, 2011, 15(5): 705-714.
50 Champagne CM, Buchanan W, Reddy MS, et al. Potential for gingival crevice fluid measures as predictors of risk for periodontal diseases[J]. Periodontol 2000, 2003, 31: 167-180.
51 Cao XY, Xu J. Insights into inflammasome and its research advances in cancer[J]. Tumori, 2019, 105(6): 456-464.
52 Irani S, Barati I, Badiei M. Periodontitis and oral cancer-current concepts of the etiopathogenesis[J]. Oncol Rev, 2020, 14(1): 465.
53 Kuboniwa M, Hasegawa Y, Mao S, et al. P. gingivalis accelerates gingival epithelial cell progression through the cell cycle[J]. Microbes Infect, 2008, 10(2): 122-128.
54 Al-Attar A, Alimova Y, Kirakodu S, et al. Activation of Notch-1 in oral epithelial cells by P. gingivalis triggers the expression of the antimicrobial protein PLA2-ⅡA[J]. Mucosal Immunol, 2018, 11(4): 1047-1059.
55 Zhou Y, Sztukowska M, Wang Q, et al. Noncanonical activation of β-catenin by Porphyromonas gingivalis [J]. Infect Immun, 2015, 83(8): 3195-3203.
56 Liu DJ, Liu S, Liu JC, et al. sRNA23392 packaged by Porphyromonas gingivalis outer membrane vesicles promotes oral squamous cell carcinomas migration and invasion by targeting desmocollin-2[J]. Mol Oral Microbiol, 2021, 36(3): 182-191.
57 Siqueira JF, Rôças IN, Silva MG. Prevalence and clonal analysis of Porphyromonas gingivalis in primary endodontic infections[J]. J Endod, 2008, 34(11): 1332-1336.
58 Ran SJ, Liu B, Gu SS, et al. Analysis of the expression of NLRP3 and AIM2 in periapical lesions with apical periodontitis and microbial analysis outside the apical segment of teeth[J]. Arch Oral Biol, 2017, 78: 39-47.
59 Imai M, Murakami Y, Nagano K, et al. Major outer membrane proteins from Porphyromonas gingivalis: strain variation, distribution, and clinical significance in periradicular lesions[J]. Eur J Oral Sci, 2005, 113(5): 391-399.
60 Aw V. Discuss the role of microorganisms in the aetiology and pathogenesis of periapical disease[J]. Aust Endod J, 2016, 42(2): 53-59.
61 Martin FE, Nadkarni MA, Jacques NA, et al. Quantitative microbiological study of human carious dentine by culture and real-time PCR: association of anaerobes with histopathological changes in chronic pul-pitis[J]. J Clin Microbiol, 2002, 40(5): 1698-1704.
62 Zargar N, Ashraf H, Amin Marashi SMA, et al. Identification of microorganisms in irreversible pulpitis and primary endodontic infections with respect to clinical and radiographic findings[J]. Clin Oral Investig, 2020, 24(6): 2099-2108.
63 Tsai YL, Wang CY, Chuang FH, et al. Stimulation phosphatidylinositol 3-kinase/protein kinase B signaling by Porphyromonas gingivalis lipopolysacch aride mediates interleukin-6 and interleukin-8 mRNA/protein expression in pulpal inflammation[J]. J Formos Med Assoc, 2023, 122(1): 47-57.
64 Zhu Y, Dashper SG, Chen YY, et al. Porphyromonas gingivalis and Treponema denticola synergistic poly-microbial biofilm development[J]. PLoS One, 2013, 8(8): e71727.
65 Kamaguchi A, Ohyama T, Sakai E, et al. Adhesins encoded by the gingipain genes of Porphyromonas gingivalis are responsible for co-aggregation with Prevotella intermedia [J]. Microbiology (Reading), 2003, 149(Pt 5): 1257-1264.
66 Tsuda K, Amano A, Umebayashi K, et al. Molecular dissection of internalization of Porphyromonas gingivalis by cells using fluorescent beads coated with bacterial membrane vesicle[J]. Cell Struct Funct, 2005, 30(2): 81-91.
67 Furuta N, Tsuda K, Omori H, et al. Porphyromonas gingivalis outer membrane vesicles enter human epithelial cells via an endocytic pathway and are sorted to lysosomal compartments[J]. Infect Immun, 2009, 77(10): 4187-4196.
68 Cecil JD, Sirisaengtaksin N, O’Brien-Simpson NM, et al. Outer membrane vesicle-host cell interactions[J]. Microbiol Spectr, 2019, 7(1): 10.1128/microbiolspec.PSIB-0001-2018.
69 Kou YR, Inaba H, Kato T, et al. Inflammatory responses of gingival epithelial cells stimulated with Porphyromonas gingivalis vesicles are inhibited by hop-associated polyphenols[J]. J Periodontol, 2008, 79(1): 174-180.
70 Cecil JD, O’Brien-Simpson NM, Lenzo JC, et al. Outer membrane vesicles prime and activate macrophage inflammasomes and cytokine secretion in vitro and in vivo [J]. Front Immunol, 2017, 8: 1017.
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