Abstract
Extracellular matrix (ECM) proteins are highly abundant in the human body and can be found in various tissues, most prominently in connective tissue and basement membrane. For invasive bacterial pathogens, these structures function as physical barriers that block access to underlying tissues. The ability to bind and degrade these barriers is important for the establishment of infections and migration to other body sites. In the oral cavity, the ECM and the basement membrane (BM) are important components of the Junctional epithelium (JE) that closes the gap between the teeth surface and the mucosa. In periodontitis, the JE is breached by invading pathogenic bacteria, particularly strict anaerobic species. In periodontitis, invading microorganisms induce an unregulated and destructive host response through polymicrobial synergism and dysbiosis that attracts immune cells and contributes to the destruction of connective tissue and bone in the periodontal pocket. Colonization of the periodontal pocket is the first step to establish this infection, and binding to ECM is a major advantage in this site. Several species of strict anaerobic bacteria are implicated in acute and chronic periodontitis, and although binding to ECM proteins was studied in these species, few adhesins were identified so far, and the mechanisms involved in adhesion are largely unidentified. This review summarizes the data available on the interaction of strict anaerobic bacteria and components of the ECM.
Similar content being viewed by others
Data availability
All data generated or analyzed during this study are included in this published article (and its supplementary information files).
References
Ofek I, Bayer EA, Abraham SN (2013) Bacterial adhesion. In: The Prokaryotes. Springer Berlin Heidelberg, Berlin, pp 107–123. https://doi.org/10.1007/978-3-642-30144-5_50
Paulsson M, Riesbeck K (2018) How bacteria hack the matrix and dodge the bullets of immunity. Eur Respir Rev 27(148):180018. https://doi.org/10.1183/16000617.0018-2018
Allen BL (1994) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48(1):585–617. https://doi.org/10.1146/annurev.micro.48.1.585
Groeger SE, Meyle J (2015) Epithelial barrier and oral bacterial infection. Periodontol 69(1):46–67. https://doi.org/10.1111/prd.12094
Groeger S, Meyle J (2019) Oral mucosal epithelial cells. Front Immunol 10. https://doi.org/10.3389/fimmu.2019.00208
Frantz C, Stewart KM, Weaver VM (2010) The extracellular matrix at a glance. J Cell Sci 123(24):4195–4200. https://doi.org/10.1242/jcs.023820
Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK (2016) Extracellular matrix structure. Adv Drug Deliv Rev 97:4–27. https://doi.org/10.1016/j.addr.2015.11.001
Badylak SF, Freytes DO, Gilbert TW (2015) Reprint of: extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 23:S17–S26. https://doi.org/10.1016/j.actbio.2015.07.016
Deshmukh S, Dive A, Moharil R, Munde P (2016) Enigmatic insight into collagen. J Oral Maxillofac Pathol 20(2):276–283. https://doi.org/10.4103/0973-029X.185932
Pozzi A, Yurchenco PD, Iozzo RV (2017) The nature and biology of basement membranes. Matrix Biol 57–58:1–11. https://doi.org/10.1016/j.matbio.2016.12.009
LeBleu VS, MacDonald B, Kalluri R (2007) Structure and function of basement membranes. Exp Biol Med 232(9):1121–1129. https://doi.org/10.3181/0703-MR-72
Chung AE, Jaffe R, Freeman IL, Vergnes J-P, Braginski JE, Carlin B (1979) Properties of a basement membrane-related glycoprotein synthesized in culture by a mouse embryonal carcinoma-derived cell line. Cell. 16(2):277–287. https://doi.org/10.1016/0092-8674(79)90005-9
Kleinman HK, McGarvey ML, Liotta LA, Robey PG, Tryggvason K, Martin GR (1982) Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry. 21(24):6188–6193. https://doi.org/10.1021/bi00267a025
Poschl E (2004) Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development. 131(7):1619–1628. https://doi.org/10.1242/dev.01037
Yurchenco PD (2011) Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb Perspect Biol 3(2):a004911–a004911. https://doi.org/10.1101/cshperspect.a004911
Murphy-Ullrich JE, Sage EH (2014) Revisiting the matricellular concept. Matrix Biol 37:1–14. https://doi.org/10.1016/j.matbio.2014.07.005
Bos IR, Burkhardt A (1980) Interepithelial cells of the oral mucosa light and electron microscopic observations in germfree, specific pathogen-free and conventionalized mice. J Oral Pathol Med 9(2):65–81. https://doi.org/10.1111/j.1600-0714.1980.tb01389.x
Wade WG (2013) Characterisation of the human oral microbiome. J Oral Biosci 55(3):143–148. https://doi.org/10.1016/j.job.2013.06.001
Lamont RJ, Koo H, Hajishengallis G (2018) The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol 16(12):745–759. https://doi.org/10.1038/s41579-018-0089-x
Bowen WH, Burne RA, Wu H, Koo H (2018) Oral biofilms: pathogens, matrix, and polymicrobial interactions in microenvironments. Trends Microbiol 26(3):229–242. https://doi.org/10.1016/j.tim.2017.09.008
Simón-Soro A, Mira A (2015) Solving the etiology of dental caries. Trends Microbiol 23(2):76–82. https://doi.org/10.1016/j.tim.2014.10.010
Armitage GC (2004) Periodontal diagnoses and classification of periodontal diseases. Periodontol 34(1):9–21. https://doi.org/10.1046/j.0906-6713.2002.003421.x
Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, Greenwell H, Herrera D, Kao RT, Kebschull M, Kinane DF, Kirkwood KL, Kocher T, Kornman KS, Kumar PS, Loos BG, Machtei E, Meng H, Mombelli A, Needleman I, Offenbacher S, Seymour GJ, Teles R, Tonetti MS (2018) Periodontitis: consensus report of workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol 45:S162–S170. https://doi.org/10.1111/jcpe.12946
Chee B, Park B, Bartold MP (2013) Periodontitis and type II diabetes: a two-way relationship. Int J Evid Based Healthc 11(4):317–329. https://doi.org/10.1111/1744-1609.12038
Berlin-Broner Y, Febbraio M, Levin L (2017) Association between apical periodontitis and cardiovascular diseases: a systematic review of the literature. Int Endod J 50(9):847–859. https://doi.org/10.1111/iej.12710
Peddis N, Musu D, Ideo F, Rossi-Fedele G, Cotti E (2019) Interaction of biologic therapy with apical periodontitis and periodontitis: a systematic review. Aust Dent J 64(2):122–134. https://doi.org/10.1111/adj.12684
Amano A (2007) Disruption of epithelial barrier and impairment of cellular function by Porphyromonas gingivalis. Front Biosci 12(8–12):3965. https://doi.org/10.2741/2363
Connolly E, Millhouse E, Doyle R, Culshaw S, Ramage G, Moran GP (2017) The Porphyromonas gingivalis hemagglutinins HagB and HagC are major mediators of adhesion and biofilm formation. Mol Oral Microbiol 32(1):35–47. https://doi.org/10.1111/omi.12151
Nishiyama S-I, Murakami Y, Nagata H, Shizukuishi S, Kawagishi I, Yoshimura F (2007) Involvement of minor components associated with the FimA fimbriae of Porphyromonas gingivalis in adhesive functions. Microbiology. 153(6):1916–1925. https://doi.org/10.1099/mic.0.2006/005561-0
Amano A, Sojar HT, Lee JY, Sharma A, Levine MJ, Genco RJ (1994) Salivary receptors for recombinant fimbrillin of Porphyromonas gingivalis. Infect Immun
Murakami Y (1998) Fibronectin in saliva inhibits Porphyromonas gingivalis fimbria-induced expression of inflammatory cytokine gene in mouse macrophages. FEMS Immunol Med Microbiol 22(3):257–262. https://doi.org/10.1016/S0928-8244(98)00098-4
Al-Taweel FBH, Al-Magsoosi MJN, Douglas CWI, Whawell SA (2018) Identification of key determinants in Porphyromonas gingivalis host-cell invasion assays. Eur J Oral Sci 126(5):367–372. https://doi.org/10.1111/eos.12557
Nakamura T (1999) Specific interactions between Porphyromonas gingivalis fimbriae and human extracellular matrix proteins. FEMS Microbiol Lett 175(2):267–272. https://doi.org/10.1016/S0378-1097(99)00205-0
Li N, Collyer CA (2011) Gingipains from Porphyromonas gingivalis — complex domain structures confer diverse functions. Eur J Microbiol Immunol 1(1):41–58. https://doi.org/10.1556/EuJMI.1.2011.1.7
Hočevar K, Potempa J, Turk B (2018) Host cell-surface proteins as substrates of gingipains, the main proteases of Porphyromonas gingivalis. Biol Chem 399(12):1353–1361. https://doi.org/10.1515/hsz-2018-0215
Pike RN, Potempa J, Mcgraw W, Coetzer THT, Travis J (1996) Characterization of the binding activities of proteinase-adhesin complexes from Porphyromonas gingivalis. J Bacteriol 178:2876–2882. https://doi.org/10.1128/jb.178.10.2876-2882.1996
O’Brien-Simpson N, Veith P, Dashper S, Reynolds E (2003) Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci 4(6):409–426. https://doi.org/10.2174/1389203033487009
Zhang Y, Wang X, Li H, Ni C, Du Z, Yan F (2018) Human oral microbiota and its modulation for oral health. Biomed Pharmacother 99:883–893. https://doi.org/10.1016/j.biopha.2018.01.146
Arora N, Mishra A, Chugh S (2014) Microbial role in periodontitis: have we reached the top? Some unsung bacteria other than red complex. J Indian Soc Periodontol 18(1):9–13. https://doi.org/10.4103/0972-124X.128192
Ibrahim M, Subramanian A, Anishetty S (2017) Comparative pan genome analysis of oral Prevotella species implicated in periodontitis. Funct Integr Genomics 17(5):513–536. https://doi.org/10.1007/s10142-017-0550-3
Eiring P, Waller K, Widmann A, Werner H, Werner H (1998) Fibronectin and laminin binding of urogenital and oral Prevotella species. Zentrabl Bakteriol 288:361–372
Yu F, Iyer D, Anaya C, Lewis JP (2006) Identification and characterization of a cell surface protein of Prevotella intermedia 17 with broad-spectrum binding activity for extracellular matrix proteins. Proteomics. 6(22):6023–6032. https://doi.org/10.1002/pmic.200600177
Grenier D (1996) Collagen-binding activity of Prevotella intermedia measured by a microtitre plate adherence assay. Microbiology. 142(6):1537–1541. https://doi.org/10.1099/13500872-142-6-1537
Babu JP, Dean JW, Pabst MJ (1995) Attachment of Fusobacterium nucleatum to fibronectin immobilized on gingival epithelial cells or glass coverslips. J Periodontol 66(4):285–290. https://doi.org/10.1902/jop.1995.66.4.285
Gendron R, Plamondon P, Grenier D (2004) Binding of pro-matrix metalloproteinase 9 by Fusobacterium nucleatum subsp. nucleatum as a mechanism to promote the invasion of a reconstituted basement membrane. Infect Immun 72(10):6160–6163. https://doi.org/10.1128/IAI.72.10.6160-6163.2004
Tanner A, Maiden MFJ, Macuch PJ, Murray LL, Kent RL (1998) Microbiota of health, gingivitis, and initial periodontitis. J Clin Periodontol 25(2):85–98. https://doi.org/10.1111/j.1600-051X.1998.tb02414.x
Sakakibara J, Nagano K, Murakami Y, Higuchi N, Nakamura H, Shimozato K, Yoshimura F (2007) Loss of adherence ability to human gingival epithelial cells in S-layer protein-deficient mutants of Tannerella forsythensis. Microbiology. 153(3):866–876. https://doi.org/10.1099/mic.0.29275-0
Sharma A, Sojar HT, Glurich I, Honma K, Kuramitsu HK, Genco RJ (1998) Cloning, expression, and sequencing of a cell surface antigen containing a leucine-rich repeat motif from Bacteroides forsythus ATCC 43037. McGhee JR, ed. Infect Immun 66(12):5703–5710. doi:https://doi.org/10.1128/IAI.66.12.5703-5710.1998
Sharma A (2010) Virulence mechanisms of Tannerella forsythia. Periodontol 54(1):106–116. https://doi.org/10.1111/j.1600-0757.2009.00332.x
Abe T, Murakami Y, Nagano K, Hasegawa Y, Moriguchi K, Ohno N, Shimozato K, Yoshimura F (2011) OmpA-like protein influences cell shape and adhesive activity of Tannerella forsythia. Mol Oral Microbiol 26(6):374–387. https://doi.org/10.1111/j.2041-1014.2011.00625.x
Ksiazek M, Karim AY, Bryzek D, et al. (2015) Mirolase, a novel subtilisin-like serine protease from the periodontopathogen Tannerella forsythia. Biol Chem. 396(3). doi:https://doi.org/10.1515/hsz-2014-0256
Edwards AM, Jenkinson HF, Woodward MJ, Dymock D (2005) Binding properties and adhesion-mediating regions of the major sheath protein of Treponema denticola ATCC 35405. Infect Immun 73(5):2891–2898. https://doi.org/10.1128/IAI.73.5.2891-2898.2005
Chi B, Qi M, Kuramitsu HK (2003) Role of dentilisin in Treponema denticola epithelial cell layer penetration. Res Microbiol 154(9):637–643. https://doi.org/10.1016/j.resmic.2003.08.001
Bamford CV, Fenno JC, Jenkinson HF, Dymock D (2007) The chymotrypsin-like protease complex of Treponema denticola ATCC 35405 mediates fibrinogen adherence and degradation. Infect Immun 75(9):4364–4372. https://doi.org/10.1128/IAI.00258-07
Haapasalo M, Hannam P, McBride BC, Uitto V-J (1996) Hyaluronan, a possible ligand mediating Treponema denticola binding to periodontal tissue. Oral Microbiol Immunol 11(3):156–160. https://doi.org/10.1111/j.1399-302X.1996.tb00351.x
Fenno JC, Tamura M, Hannam PM, Wong GWK, Chan RA, McBride BC (2000) Identification of a Treponema denticola OppA homologue that binds host proteins present in the subgingival environment. Infect Immun 68(4):1884–1892. https://doi.org/10.1128/IAI.68.4.1884-1892.2000
Berbari EF, Cockerill FR, Steckelberg JM (1997) Infective endocarditis due to unusual or fastidious microorganisms. Mayo Clin Proc 72(6):532–542. https://doi.org/10.4065/72.6.532
Tang G, Kitten T, Munro CL, Wellman GC, Mintz KP (2008) EmaA, a potential virulence determinant of Aggregatibacter actinomycetemcomitans in infective endocarditis. Infect Immun 76(6):2316–2324. https://doi.org/10.1128/IAI.00021-08
Fine DH, Kaplan JB, Kachlany SC, Schreiner HC (2006) How we got attached to Actinobacillus actinomycetemcomitans: a model for infectious diseases. Periodontol 42(1):114–157. https://doi.org/10.1111/j.1600-0757.2006.00189.x
Ferreira E d O, Araújo Lobo L, Barreiros Petrópolis D et al (2006) A Bacteroides fragilis surface glycoprotein mediates the interaction between the bacterium and the extracellular matrix component laminin-1. Res Microbiol 157(10):960–966. https://doi.org/10.1016/j.resmic.2006.09.005
Galvão BPG V., Weber BW, Rafudeen MS, Ferreira EO, Patrick S, Abratt VR (2014) Identification of a collagen type I adhesin of Bacteroides fragilis. Tunney M, ed. PLoS One. 9(3):e91141. doi:https://doi.org/10.1371/journal.pone.0091141
Pauer H, Ferreira EDO, dos Santos-Filho J et al (2009) A TonB-dependent outer membrane protein as a Bacteroides fragilis fibronectin-binding molecule. FEMS Immunol Med Microbiol 55(3):388–395. https://doi.org/10.1111/j.1574-695X.2009.00532.x
Calabi E, Calabi F, Phillips AD, Fairweather NF (2002) Binding of Clostridium difficile surface layer proteins to gastrointestinal tissues. Infect Immun 70(10):5770–5778. https://doi.org/10.1128/IAI.70.10.5770-5778.2002
Hennequin C (2003) Identification and characterization of a fibronectin-binding protein from Clostridium difficile. Microbiology. 149(10):2779–2787. https://doi.org/10.1099/mic.0.26145-0
Sillanpaa J, Martinez B, Antikainen J et al (2000) Characterization of the collagen-binding S-layer protein CbsA of Lactobacillus crispatus. J Bacteriol 182(22):6440–6450. https://doi.org/10.1128/JB.182.22.6440-6450.2000
Horie M, Murakami T, Sato T, Tarusawa Y, Nakamura S, Toba T (2005) Anaerobic induction of adherence to laminin in Lactobacillus gasseri strains by contact with solid surface. Curr Microbiol 51(4):275–282. https://doi.org/10.1007/s00284-005-4572-z
Lobo LA (2006) Adhesive properties of the puri ¢ ed plasminogen activator Pla of Yersinia pestis. 262:158–162. doi:https://doi.org/10.1111/j.1574-6968.2006.00382.x
Ferreira E d O, Teixeira FL, Cordeiro F et al (2013) The Bfp60 surface adhesin is an extracellular matrix and plasminogen protein interacting in Bacteroides fragilis. Int J Med Microbiol. https://doi.org/10.1016/j.ijmm.2013.06.007
Ofek I, Hasty DL, Sharon N (2003) Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunol Med Microbiol 38(3):181–191. https://doi.org/10.1016/S0928-8244(03)00228-1
Funding
This work was funded by Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro—FAPERJ, Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq, and Coordenação de Aperfeiçoamento de Pessoal de Pós-Graduação—CAPES.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interests
The author declares that there is no conflict of interest.
Consent for publication
Not applicable.
Additional information
Responsible Editor: Waldir P. Elias.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Marre, A.T., Domingues, R.M.C.P. & Lobo, L.A. Adhesion of anaerobic periodontal pathogens to extracellular matrix proteins. Braz J Microbiol 51, 1483–1491 (2020). https://doi.org/10.1007/s42770-020-00312-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42770-020-00312-2