Structure of polymerized type V pilin reveals assembly mechanism involving protease-mediated strand exchange.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
28
08
2019
accepted:
09
03
2020
pubmed:
15
4
2020
medline:
21
10
2020
entrez:
15
4
2020
Statut:
ppublish
Résumé
Bacterial adhesion is a general strategy for host-microbe and microbe-microbe interactions. Adhesive pili are essential for colonization, biofilm formation, virulence and pathogenesis of many environmental and pathogenic bacteria
Identifiants
pubmed: 32284566
doi: 10.1038/s41564-020-0705-1
pii: 10.1038/s41564-020-0705-1
doi:
Substances chimiques
Fimbriae Proteins
147680-16-8
Peptide Hydrolases
EC 3.4.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
830-837Commentaires et corrections
Type : CommentIn
Références
Allen, W. J., Phan, G. & Waksman, G. Pilus biogenesis at the outer membrane of Gram-negative bacterial pathogens. Curr. Opin. Struct. Biol. 22, 500–506 (2012).
pubmed: 22402496
doi: 10.1016/j.sbi.2012.02.001
Hospenthal, M. K., Costa, T. R. D. & Waksman, G. A comprehensive guide to pilus biogenesis in Gram-negative bacteria. Nat. Rev. Microbiol. 15, 365–379 (2017).
pubmed: 28496159
doi: 10.1038/nrmicro.2017.40
Xu, Q. et al. A distinct type of pilus from the human microbiome. Cell 165, 690–703 (2016).
pubmed: 27062925
pmcid: 4842110
doi: 10.1016/j.cell.2016.03.016
Lamont, R. J. & Jenkinson, H. F. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol. Mol. Biol. Rev. 62, 1244–1263 (1998).
pubmed: 9841671
pmcid: 98945
doi: 10.1128/MMBR.62.4.1244-1263.1998
Wang, F. et al. Structure of microbial nanowires reveals stacked hemes that transport electrons over micrometers. Cell 177, 361–369 (2019).
pubmed: 30951668
pmcid: 6720112
doi: 10.1016/j.cell.2019.03.029
Filman, D. J. et al. Cryo-EM reveals the structural basis of long-range electron transport in a cytochrome-based bacterial nanowire. Commun. Biol. 2, 219 (2019).
pubmed: 31240257
pmcid: 6584659
doi: 10.1038/s42003-019-0448-9
Lukaszczyk, M., Pradhan, B. & Remaut, H. The biosynthesis and structures of bacterial pili. Subcell. Biochem. 92, 369–413 (2019).
pubmed: 31214993
doi: 10.1007/978-3-030-18768-2_12
Remaut, H. et al. Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted β strand displacement mechanism. Mol. Cell 22, 831–842 (2006).
pubmed: 16793551
doi: 10.1016/j.molcel.2006.05.033
Holt, S. C. & Ebersole, J. L. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the ‘red complex’, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol. 2000 38, 72–122 (2005).
pubmed: 15853938
doi: 10.1111/j.1600-0757.2005.00113.x
Demmer, R. T. & Desvarieux, M. Periodontal infections and cardiovascular disease: the heart of the matter. J. Am. Dent. Assoc. 137, 14S–20S (2006).
pubmed: 17012731
doi: 10.14219/jada.archive.2006.0402
Michaud, D. S. et al. Plasma antibodies to oral bacteria and risk of pancreatic cancer in a large European prospective cohort study. Gut 62, 1764–1770 (2013).
pubmed: 22990306
doi: 10.1136/gutjnl-2012-303006
Leech, M. T. & Bartold, P. M. The association between rheumatoid arthritis and periodontitis. Best Pr. Res. Clin. Rheumatol. 29, 189–201 (2015).
doi: 10.1016/j.berh.2015.03.001
Dominy, S. S. et al. Porphyromonas gingivalis in Alzheimer’s disease brains: evidence for disease causation and treatment with small-molecule inhibitors. Sci. Adv. 5, eaau3333 (2019).
pubmed: 30746447
pmcid: 6357742
doi: 10.1126/sciadv.aau3333
Yoshimura, F., Takahashi, K., Nodasaka, Y. & Suzuki, T. Purification and characterization of a novel type of fimbriae from the oral anaerobe Bacteroides gingivalis. J. Bacteriol. 160, 949–957 (1984).
pubmed: 6150029
pmcid: 215801
doi: 10.1128/JB.160.3.949-957.1984
Hamada, N., Sojar, H. T., Cho, M. I. & Genco, R. J. Isolation and characterization of a minor fimbria from Porphyromonas gingivalis. Infect. Immun. 64, 4788–4794 (1996).
pubmed: 8890240
pmcid: 174446
doi: 10.1128/IAI.64.11.4788-4794.1996
Hajishengallis, G., Shakhatreh, M.-A. K., Wang, M. & Liang, S. Complement receptor 3 blockade promotes IL-12-mediated clearance of Porphyromonas gingivalis and negates its virulence in vivo. J. Immunol. 179, 2359–2367 (2007).
pubmed: 17675497
doi: 10.4049/jimmunol.179.4.2359
Amano, A. Bacterial adhesins to host components in periodontitis. Periodontol. 2000 52, 12–37 (2010).
pubmed: 20017793
doi: 10.1111/j.1600-0757.2009.00307.x
Park, Y. et al. Short fimbriae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii. Infect. Immun. 73, 3983–3989 (2005).
pubmed: 15972485
pmcid: 1168573
doi: 10.1128/IAI.73.7.3983-3989.2005
Sojar, H. T., Hamada, N. & Genco, R. J. Isolation and characterization of fimbriae from a sparsely fimbriated strain of Porphyromonas gingivalis. Appl. Environ. Microbiol. 63, 2318–2323 (1997).
pubmed: 9172351
pmcid: 168524
doi: 10.1128/AEM.63.6.2318-2323.1997
Hasegawa, Y. et al. Anchoring and length regulation of Porphyromonas gingivalis Mfa1 fimbriae by the downstream gene product Mfa2. Microbiology 155, 3333–3347 (2009).
pubmed: 19589838
pmcid: 2810400
doi: 10.1099/mic.0.028928-0
Nagano, K., Hasegawa, Y., Murakami, Y., Nishiyama, S. & Yoshimura, F. FimB regulates FimA fimbriation in Porphyromonas gingivalis. J. Dent. Res. 89, 903–908 (2010).
pubmed: 20530728
doi: 10.1177/0022034510370089
Hamada, S. et al. Molecular and immunological characterization of the fimbriae of Porphyromonas gingivalis. Microbiol. Immunol. 38, 921–930 (1994).
pubmed: 7723684
doi: 10.1111/j.1348-0421.1994.tb02148.x
Fujiwara, T., Nakagawa, I., Morishima, S., Takahashi, I. & Hamada, S. Inconsistency between the fimbrilin gene and the antigenicity of lipopolysaccharides in selected strains of Porphyromonas gingivalis. FEMS Microbiol. Lett. 124, 333–341 (1994).
pubmed: 7851739
doi: 10.1111/j.1574-6968.1994.tb07305.x
Nakagawa, I. et al. Distribution and molecular characterization of Porphyromonas gingivalis carrying a new type of fimA gene. J. Clin. Microbiol. 38, 1909–1914 (2000).
pubmed: 10790120
pmcid: 86621
doi: 10.1128/JCM.38.5.1909-1914.2000
Nakagawa, I. et al. Identification of a new variant of fimA gene of Porphyromonas gingivalis and its distribution in adults and disabled populations with periodontitis. J. Periodontal Res . 37, 425–432 (2002).
pubmed: 12472836
doi: 10.1034/j.1600-0765.2002.01637.x
Okuda, S. & Tokuda, H. Lipoprotein sorting in bacteria. Annu. Rev. Microbiol. 65, 239–259 (2011).
pubmed: 21663440
doi: 10.1146/annurev-micro-090110-102859
Korotkov, K. V. et al. Calcium is essential for the major pseudopilin in the type 2 secretion system. J. Biol. Chem. 284, 25466–25470 (2009).
pubmed: 19640838
pmcid: 2757947
doi: 10.1074/jbc.C109.037655
Shoji, M. et al. The major structural components of two cell surface filaments of Porphyromonas gingivalis are matured through lipoprotein precursors. Mol. Microbiol. 52, 1513–1525 (2004).
pubmed: 15165251
doi: 10.1111/j.1365-2958.2004.04105.x
Konovalova, A. & Silhavy, T. J. Outer membrane lipoprotein biogenesis: Lol is not the end. Phil. Trans. R. Soc. B 370, 20150030 (2015).
pubmed: 26370942
doi: 10.1098/rstb.2015.0030
Nakayama, K., Yoshimura, F., Kadowaki, T. & Yamamoto, K. Involvement of arginine-specific cysteine proteinase (Arg-gingipain) in fimbriation of Porphyromonas gingivalis. J. Bacteriol. 178, 2818–2824 (1996).
pubmed: 8631669
pmcid: 178016
doi: 10.1128/JB.178.10.2818-2824.1996
Shoji, M. et al. Recombinant Porphyromonas gingivalis FimA preproprotein expressed in Escherichia coli is lipidated and the mature or processed recombinant FimA protein forms a short filament in vitro. Can. J. Microbiol. 56, 959–967 (2010).
pubmed: 21076487
doi: 10.1139/W10-084
Thompson, J. D., Higgins, D. G. & Gibson, T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).
pubmed: 7984417
pmcid: 308517
doi: 10.1093/nar/22.22.4673
Lee, J. Y. et al. Maturation of the Mfa1 fimbriae in the oral pathogen Porphyromonas gingivalis. Front. Cell Infect. Microbiol. 8, 137 (2018).
pubmed: 29868494
pmcid: 5954841
doi: 10.3389/fcimb.2018.00137
Nishiyama, M., Ishikawa, T., Rechsteiner, H. & Glockshuber, R. Reconstitution of pilus assembly reveals a bacterial outer membrane catalyst. Science 320, 376–379 (2008).
pubmed: 18369105
doi: 10.1126/science.1154994
Nishiyama, S. et al. Involvement of minor components associated with the FimA fimbriae of Porphyromonas gingivalis in adhesive functions. Microbiology 153, 1916–1925 (2007).
pubmed: 17526848
doi: 10.1099/mic.0.2006/005561-0
Hajishengallis, G., Ratti, P. & Harokopakis, E. Peptide mapping of bacterial fimbrial epitopes interacting with pattern recognition receptors. J. Biol. Chem. 280, 38902–38913 (2005).
pubmed: 16129673
doi: 10.1074/jbc.M507326200
Nakano, K. et al. Comparison of inflammatory changes caused by Porphyromonas gingivalis with distinct fimA genotypes in a mouse abscess model. Oral Microbiol. Immunol. 19, 205–209 (2004).
pubmed: 15107074
doi: 10.1111/j.0902-0055.2004.00133.x
Sugano, N. et al. Differential cytokine induction by two types of Porphyromonas gingivalis. Oral Microbiol. Immunol. 19, 121–123 (2004).
pubmed: 14871353
doi: 10.1046/j.0902-0055.2003.00119.x
Bodet, C., Chandad, F. & Grenier, D. Porphyromonas gingivalis-induced inflammatory mediator profile in an ex vivo human whole blood model. Clin. Exp. Immunol. 143, 50–57 (2006).
pubmed: 16367933
pmcid: 1809557
doi: 10.1111/j.1365-2249.2005.02956.x
Nagano, K. et al. Porphyromonas gingivalis FimA fimbriae: fimbrial assembly by fimA alone in the fim gene cluster and differential antigenicity among fimA genotypes. PLoS ONE 7, e43722 (2012).
pubmed: 22970139
pmcid: 3436787
doi: 10.1371/journal.pone.0043722
Alaei, S. R., Park, J. H., Walker, S. G. & Thanassi, D. G. Peptide-based inhibitors of fimbrial biogenesis in Porphyromonas gingivalis. Infect. Immun. 87, e00750–18 (2019).
pubmed: 30642895
pmcid: 6386548
doi: 10.1128/IAI.00750-18
Veillard, F. et al. Purification and characterisation of recombinant His-tagged RgpB gingipain from Porphymonas gingivalis. Biol. Chem. 396, 377–384 (2015).
pubmed: 25720118
pmcid: 4682895
doi: 10.1515/hsz-2014-0304
Battye, T. G. G., Kontogiannis, L., Johnson, O., Powell, H. R. & Leslie, A. G. W. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D 67, 271–281 (2011).
pubmed: 21460445
doi: 10.1107/S0907444910048675
Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235–242 (2011).
pubmed: 21460441
doi: 10.1107/S0907444910045749
McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658–674 (2007).
pubmed: 19461840
pmcid: 2483472
doi: 10.1107/S0021889807021206
Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010).
pubmed: 20383002
pmcid: 20383002
doi: 10.1107/S0907444910007493
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010).
pubmed: 20124702
doi: 10.1107/S0907444909052925
Chen, T., Nakayama, K., Belliveau, L. & Duncan, M. J. Porphyromonas gingivalis gingipains and adhesion to epithelial cells. Infect. Immun. 69, 3048–3056 (2001).
pubmed: 11292723
pmcid: 98259
doi: 10.1128/IAI.69.5.3048-3056.2001
Kikuchi, Y. et al. Novel stationary-phase-upregulated protein of Porphyromonas gingivalis influences production of superoxide dismutase, thiol peroxidase and thioredoxin. Microbiology 151, 841–853 (2005).
pubmed: 15758230
doi: 10.1099/mic.0.27589-0
Shoji, M. et al. Characterization of hemin-binding protein 35 (HBP35) in Porphyromonas gingivalis: its cellular distribution, thioredoxin activity and role in heme utilization. BMC Microbiol. 10, 152 (2010).
pubmed: 20500879
pmcid: 2907840
doi: 10.1186/1471-2180-10-152
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466
pmcid: 28250466
doi: 10.1038/nmeth.4193
Scheres, S. H. W. Processing of structurally heterogeneous Cryo-EM data in RELION. Methods Enzymol. 579, 125–157 (2016).
pubmed: 27572726
doi: 10.1016/bs.mie.2016.04.012
Grant, T., Rohou, A. & Grigorieff, N. cisTEM, user-friendly software for single-particle image processing. eLife 7, e35383 (2018).
pubmed: 29513216
pmcid: 5854467
doi: 10.7554/eLife.35383
Frank, J. et al. SPIDER and WEB: Processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190–199 (1996).
pubmed: 8742743
doi: 10.1006/jsbi.1996.0030
Pettersen, E. F. et al. UCSF chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Kyte, J. & Doolittle, R. F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105–132 (1982).
pubmed: 7108955
doi: 10.1016/0022-2836(82)90515-0
pmcid: 7108955