Biogenesis of Type V pili.
bacterial components
lipoprotein
periodontal pathogen
pili
Journal
Microbiology and immunology
ISSN: 1348-0421
Titre abrégé: Microbiol Immunol
Pays: Australia
ID NLM: 7703966
Informations de publication
Date de publication:
Oct 2020
Oct 2020
Historique:
received:
23
06
2020
revised:
11
08
2020
accepted:
13
08
2020
pubmed:
21
8
2020
medline:
9
6
2021
entrez:
21
8
2020
Statut:
ppublish
Résumé
Pili or fimbriae, which are filamentous structures present on the surface of bacteria, were purified from a periodontal pathogen, Porphyromonas gingivalis, in 1980s. The protein component of pili (stalk pilin), which is its major component, was named FimA; it has a molecular weight of approximately 41 kDa. Because the molecular weight of the pilin from P. gingivalis is twice that of pilins from other bacterial pili, the P. gingivalis Fim pili were suggested to be formed via a novel mechanism. In earlier studies, we reported that the FimA pilin is secreted on the cell surface as a lipoprotein precursor, and the subsequent N-terminal processing of the FimA precursor by arginine-specific proteases is necessary for Fim pili formation. The crystal structures of FimA and its related proteins were determined recently, which show that Fim pili are formed by a protease-mediated strand-exchange mechanism. The most recent study conducted by us, wherein we performed cryoelectron microscopy of the pilus structure, provided evidence in support of this mechanism. As the P. gingivalis Fim pili are formed through novel transport and assembly mechanisms, such pili are now designated as Type V pili. Surface lipoproteins, including the anchor pilin FimB of Fim pili that are present on the outer membrane, have been detected in certain Gram-negative bacteria. Here, we describe the assembly mechanisms of pili, including those of Type V and other pili, as well as the lipoprotein transport mechanisms.
Identifiants
pubmed: 32816331
doi: 10.1111/1348-0421.12838
doi:
Substances chimiques
Lipoproteins
0
fimbrillin
0
Fimbriae Proteins
147680-16-8
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
643-656Subventions
Organisme : Japan Society for the Promotion of Science
ID : 19K10072
Organisme : Japan Society for the Promotion of Science
ID : 19K10083
Informations de copyright
© 2020 The Societies and John Wiley & Sons Australia, Ltd.
Références
8020zaidan. The second national survey on the reasons for extraction of permanent teeth, 2018.
Nazir MA. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int J Health Sci. 2017;11:72-80.
Tonetti MS, Bottenberg P, Conrads G, et al. Dental caries and periodontal diseases in the ageing population: call to action to protect and enhance oral health and well-being as an essential component of healthy ageing-Consensus report of group 4 of the joint EFP/ORCA workshop on the boundaries between caries and periodontal diseases. J Clin Periodontol. 2017;44:S135-44. https://doi.org/10.1111/jcpe.12681
Könönen E, Gursoy M, Gursoy UK. Periodontitis: a multifaceted disease of tooth-supporting tissues. J Clin Med. 2019;8(8):1135. https://doi.org/10.3390/jcm8081135
Rodenburg JP, van Winkelhoff AJ, Winkel EG, Goené RJ, Abbas F, de Graff J. Occurrence of Bacteroides gingivalis, Bacteroides intermedius and Actinobacillus actinomycetemcomitans in severe periodontitis in relation to age and treatment history. J Clin Periodontol. 1990;17:392-9. https://doi.org/10.1111/j.1600-051x.1990.tb00036.x
Slots J, Feik D, Rams TE. Actinobacillus actinomycetemcomitans and Bacteroides intermedius in human periodontitis: age relationship and mutual association. J Clin Periodontol. 1990;17:659-62.
Chigasaki O, Takeuchi Y, Aoki A, et al. A cross-sectional study on the periodontal status and prevalence of red complex periodontal pathogens in a Japanese population. J Oral Sci. 2018;60:293-303. https://doi.org/10.2334/josnusd.17-0223
Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the "red complex", a prototype polybacterial pathogenic consortium in periodontitis. Periodontology. 2005;38:72-122. https://doi.org/10.1111/j.1600-0757.2005.00113.x
Hajishengallis G, Liang S, Payne MA, et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe. 2011;10:497-506. https://doi.org/10.1016/j.chom.2011.10.006
Payne MA, Hashim A, Alsam A, et al. Horizontal and vertical transfer of oral microbial dysbiosis and periodontal disease. J Dent Res. 2019;98:1503-10. https://doi.org/10.1177/0022034519877150
Potempa J, Banbula A, Travis J. Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontology. 2000;24:153-92. https://doi.org/10.1034/j.1600-0757.2000.2240108.x
Fujimura S, Hirai K, Shibata Y, Nakayama K, Nakamura T. Comparative properties of envelope-associated arginine-gingipains and lysine-gingipain of Porphyromonas gingivalis. FEMS Microbiol Lett. 1998;163:173-9. https://doi.org/10.1111/j.1574-6968.1998.tb13042.x
Wingrove JA, DiScipio RG, Chen Z, Potempa J, Travis J, Hugli TE. Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J Biol Chem. 1992;267:18902-07.
Nakayama K, Yoshimura F, Kadowaki T, Yamamoto K. Involvement of arginine-specific cysteine proteinase (Arg-gingipain) in fimbriation of Porphyromonas gingivalis. J Bacteriol. 1996;178:2818-24. https://doi.org/10.1128/jb.178.10.2818-2824
Kadowaki T, Nakayama K, Yoshimura F, Okamoto K, Abe N, Yamamoto K. Arg-gingipain acts as a major processing enzyme for various cell surface proteins in Porphyromonas gingivalis. J Biol Chem. 1998;273:29072-76. https://doi.org/10.1074/jbc.273.44.29072
Haruyama K, Yoshimura A, Naito M, et al. Identification of a gingipain-sensitive surface ligand of Porphyromonas gingivalis that induces TLR2- and TLR4-independent NF-κB activation in CHO cells. Infect Immun. 2009;77:4414-20.
Smalley JW, Silver J, Marsh PJ, Birss AJ. The periodontopathogen Porphyromonas gingivalis binds iron protoporphyrin IX in the mu-oxo dimeric form: an oxidative buffer and possible pathogenic mechanism. Biochem J. 1998;331:681-5. https://doi.org/10.1042/bj3310681
Okamoto K, Nakayama K, Kadowaki T, Abe N, Ratnayake DB, Yamamoto K. Involvement of a lysine-specific cysteine proteinase in hemoglobin adsorption and heme accumulation by Porphyromonas gingivalis. J Biol Chem. 1998;273:21225-31. https://doi.org/10.1074/jbc.273.33.21225
Lewis JP, Dawson JA, Hannis JC, Muddiman D, Macrina FL. Hemoglobinase activity of the lysine gingipain protease (Kgp) of Porphyromonas gingivalis W83. J Bacteriol. 1999;181:4905-13.
Curtis MA, Aduse Opoku J, Rangarajan M, et al. Attenuation of the virulence of Porphyromonas gingivalis by using a specific synthetic Kgp protease inhibitor. Infect Immun. 2002;70:6968-75. https://doi.org/10.1128/iai.70.12.6968-6975.2002
Sato K, Sakai E, Veith PD, et al. Identification of a new membrane-associated protein that influences transport/maturation of gingipains and adhesins of Porphyromonas gingivalis. J Biol Chem. 2005;280:8668-77. https://doi.org/10.1074/jbc.M413544200
Sato K, Naito M, Yukitake H, et al. A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc Natl Acad Sci USA. 2010;107:276-81. https://doi.org/10.1073/pnas.0912010107
Shoji M, Sato K, Yukitake H, et al. Por secretion system-dependent secretion and glycosylation of Porphyromonas gingivalis hemin-binding protein 35. PLoS One. 2011;6:e21372. https://doi.org/10.1371/journal.pone.0021372
Sato K, Yukitake H, Narita Y, Shoji M, Naito M, Nakayama K. Identification of Porphyromonas gingivalis proteins secreted by the Por secretion system. FEMS Microbiol Lett. 2013;338:68-76. https://doi.org/10.1111/1574-6968.12028
Nakayama K. Porphyromonas gingivalis and related bacteria: from colonial pigmentation to the type IX secretion system and gliding motility. J Periodontal Res. 2015;50:1-8. https://doi.org/10.1111/jre.12255
Sato K, Kakuda S, Yukitake H, et al. Immunoglobulin-like domains of the cargo proteins are essential for protein stability during secretion by the type IX secretion system. Mol Microbiol. 2018;110:64-81. https://doi.org/10.1111/mmi.14083
Naito M, Tominaga T, Shoji M, Nakayama K. PGN_0297 is an essential component of the type IX secretion system (T9SS) in Porphyromonas gingivalis: Tn-seq analysis for exhaustive identification of T9SS-related genes. Microbiol Immunol. 2019;63:11-20. https://doi.org/10.1111/1348-0421.12665
Curtis MA, Thickett A, Slaney JM, et al. Variable carbohydrate modifications to the catalytic chains of the RgpA and RgpB proteases of Porphyromonas gingivalis W50. Infect Immun. 1999;67:3816-23.
Shoji M, Ratnayake DB, Shi Y, et al. Construction and characterization of a nonpigmented mutant of Porphyromonas gingivalis: cell surface polysaccharide as an anchorage for gingipains. Microbiology. 2002;148:1183-91. https://doi.org/10.1099/00221287-148-4-1183
Shoji M, Yukitake H, Sato K, et al. Identification of an O-antigen chain length regulator, WzzP, in Porphyromonas gingivalis. Microbiologyopen. 2013;2:383-401. https://doi.org/10.1002/mbo3.84
Shoji M, Sato K, Yukitake H, Naito M, Nakayama K. Involvement of the Wbp pathway in the biosynthesis of Porphyromonas gingivalis lipopolysaccharide with anionic polysaccharide. Sci Rep. 2014;4:5056. https://doi.org/10.1038/srep05056
Shoji M, Nakayama K. Glycobiology of the oral pathogen Porphyromonas gingivalis and related species. Microb Pathog. 2016;94:35-41. https://doi.org/10.1016/j.micpath.2015.09.012
Shoji M, Sato K, Yukitake H, et al. Identification of genes encoding glycosyltransferases involved in lipopolysaccharide synthesis in Porphyromonas gingivalis. Mol Oral Microbiol. 2018;33:68-80. https://doi.org/10.1111/omi.12200
Nakayama K. The type IX secretion system and the type V pilus in the phylum Bacteroidetes. Japn J Bacteriol. 2017;72:219-27.
Hospenthal MK, Costa TRD, Waksman G. A comprehensive guide to pilus biogenesis in Gram-negative bacteria. Nat Rev Microbiol. 2017;15:365-79. https://doi.org/10.1038/nrmicro.2017.40
Khare B, Narayana VL, Pilus S. biogenesis of Gram-positive bacteria: roles of sortases and implications for assembly. Protein Sci. 2017;26:1458-73. https://doi.org/10.1002/pro.3191
Xu Q, Shoji M, Shibata S, et al. A distinct type of pilus from the human microbiome. Cell. 2016;165:690-703. https://doi.org/10.1016/j.cell.2016.03.016
Busch A, Waksman G. Chaperone-usher pathways: diversity and pilus assembly mechanism. Philos Trans R Soc Lond B Biol Sci. 2012;367:1112-22. https://doi.org/10.1098/rstb.2011.0206
Hansmeier N, Miskiewicz K, Elpers L, Liss V, Hensel M, Sterzenbach T. Functional expression of the entire adhesiome of Salmonella enterica serotype Typhimurium. Sci Rep. 2017;7(1):10326. https://doi.org/10.1038/s41598-017-10598-2
Werneburg GT, Thanassi DG. Pili Assembled by the Chaperone/Usher Pathway in Escherichia coli and Salmonella. EcoSal Plus. 2018;8(1):10. https://doi.org/10.1128/ecosalplus.ESP-0007-2017
Kuehn MJ, Heuser J, Normark S, Hultgren SJ. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature. 1992;356:252-5. https://doi.org/10.1038/356252a0
Mizunoe Y, Wai SN. Bacterial fimbriae in the pathogenesis of urinary tract infection. J Infect Chemother. 1998;4:1-5. https://doi.org/10.1007/BF02490057
Phan G, Remaut H, Wang T, et al. Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature. 2011;474:49-53. https://doi.org/10.1038/nature10109
Hung DL, Knight SD, Woods RM, Pinkner JS, Hultgren SJ. Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J. 1996;15:3792-805.
Chagnot C, Zorgani MA, Astruc T, Desvaux M. Proteinaceous determinants of surface colonization in bacteria: bacterial adhesion and biofilm formation from a protein secretion perspective. Front Microbiol. 2013;4:303. https://doi.org/10.3389/fmicb.2013.00303
Chapman MR, Robinson LS, Pinkner JS, et al. Role of Escherichia coli curli operons in directing amyloid fiber formation. Science. 2002;295:851-5. https://doi.org/10.1126/science.1067484
Goyal P, Krasteva PV, Van Gerven N, et al. Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG. Nature. 2014;516:250-3. https://doi.org/10.1038/nature13768
Yan Z, Yin M, Chen J, Li X. Assembly and substrate recognition of curli biogenesis system. Nat Commun. 2020;11(1):241. https://doi.org/10.1038/s41467-019-14145-7
Albers SV, Jarrell KF. The Archaellum: an update on the unique Archaeal Motility Structure. Trends Microbiol. 2018;26:351-62. https://doi.org/10.1016/j.tim.2018.01.004
Craig L, Forest KT, Maier B. Type IV pili: dynamics, biophysics and functional consequences. Nat Rev Microbiol. 2019;17:429-40. https://doi.org/10.1038/s41579-019-0195-4
Pelicic V. Monoderm bacteria: the new frontier for type IV pilus biology. Mol Microbiol. 2019;112:1674-83. https://doi.org/10.1111/mmi.14397
Pelicic V. Type IV pili: e pluribus unum? Mol Microbiol. 2008;68:827-37. https://doi.org/10.1111/j.1365-2958.2008.06197.x
Strom MS, Nunn DN, Lory S. A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc Natl Acad Sci USA. 1993;90:2404-08. https://doi.org/10.1073/pnas.90.6.2404
Giltner CL, Nguyen Y, Burrows LL. Type IV pilin proteins: versatile molecular modules. Microbiol Mol Biol Rev. 2012;76:740-72. https://doi.org/10.1128/MMBR.00035-12
Jacobsen T, Bardiaux B, Francetic O, Izadi-Pruneyre N, Nilges M. Structure and function of minor pilins of type IV pili [published online ahead of print, 2019 Nov 29. Med Microbiol Immunol. 2019;10, https://doi.org/10.1007/s00430-019-00642-5
Takhar HK, Kemp K, Kim M, Howell PL, Burrows LL. The platform protein is essential for type IV pilus biogenesis. J Biol Chem. 2013;288:9721-28. https://doi.org/10.1074/jbc.M113.453506
Tsai CL, Tainer JA. The ATPase motor turns for type IV pilus assembly. Structure. 2016;24:1857-59. https://doi.org/10.1016/j.str.2016.10.002
Yeung MK, Donkersloot JA, Cisar JO, Ragsdale PA. Identification of a gene involved in assembly of Actinomyces naeslundii T14V type 2 fimbriae. Infect Immun. 1998;66:1482-91.
Ton-That H, Schneewind O. Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol. 2003;50:1429-38. https://doi.org/10.1046/j.1365-2958.2003.03782.x
Nallapareddy SR, Singh KV, Sillanpää J, et al. Endocarditis and biofilm-associated pili of Enterococcus faecalis. J Clin Invest. 2006;116:2799-807. https://doi.org/10.1172/JCI29021
Lauer P, Rinaudo CD, Soriani M, et al. Genome analysis reveals pili in Group B Streptococcus. Science. 2005;309(5731):105. https://doi.org/10.1126/science.1111563
Barocchi MA, Ries J, Zogaj X, et al. A pneumococcal pilus influences virulence and host inflammatory responses. Proc Natl Acad Sci USA. 2006;103:2857-62. https://doi.org/10.1073/pnas.0511017103
Mora M, Bensi G, Capo S, et al. Group A Streptococcus produce pilus-like structures containing protective antigens and Lancefield T antigens. Proc Natl Acad Sci USA. 2005;102:15641-46. https://doi.org/10.1073/pnas.0507808102
Takamatsu D, Nishino H, Ishiji T, et al. Genetic organization and preferential distribution of putative pilus gene clusters in Streptococcus suis. Vet Microbiol. 2009;138:132-139. https://doi.org/10.1016/j.vetmic.2009.02.013
Hendrickx AP, Budzik JM, Oh SY, Schneewind O. Architects at the bacterial surface - sortases and the assembly of pili with isopeptide bonds. Nat Rev Microbiol. 2011;9:166-76. https://doi.org/10.1038/nrmicro2520
Navarre WW, Schneewind O. Proteolytic cleavage and cell wall anchoring at the LPXTG motif of surface proteins in gram-positive bacteria. Mol Microbiol. 1994;14:115-21. https://doi.org/10.1111/j.1365-2958.1994.tb01271.x
Mazmanian SK, Ton-That H, Schneewind O. Sortase-catalysed anchoring of surface proteins to the cell wall of Staphylococcus aureus. Mol Microbiol. 2001;40:1049-57. https://doi.org/10.1046/j.1365-2958.2001.02411.x
Mandlik A, Das A, Ton-That H. The molecular switch that activates the cell wall anchoring step of pilus assembly in gram-positive bacteria. Proc Natl Acad Sci USA. 2008;105:14147-52. https://doi.org/10.1073/pnas.0806350105
Amano A. Bacterial adhesins to host components in periodontitis. Periodontology. 2010;52:12-37. https://doi.org/10.1111/j.1600-0757.2009.00307.x
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. 1984;160:949-57.
Yoshimura F, Watanabe K, Takasawa T, Kawanami M, Kato H. Purification and properties of a 75-kilodalton major protein, an immunodominant surface antigen, from the oral anaerobe Bacteroides gingivalis. Infect Immun. 1989;57:3646-52.
Ogawa T, Yasuda K, Yamada K, Mori H, Ochiai K, Hasegawa M. Immunochemical characterisation and epitope mapping of a novel fimbrial protein (Pg-II fimbria) of Porphyromonas gingivalis. FEMS Immunol Med Microbiol. 1995;11:247-55. https://doi.org/10.1111/j.1574-695X.1995.tb00122.x
Hamada N, Sojar HT, Cho MI, Genco RJ. Isolation and characterization of a minor fimbria from Porphyromonas gingivalis. Infect Immun. 1996;64:4788-94.
Nagano K, Hasegawa Y, Yoshida Y, Yoshimura F. Novel fimbrilin PGN_1808 in Porphyromonas gingivalis. PLoS One. 2017;12(3):e0173541. https://doi.org/10.1371/journal.pone.0173541
Onoe T, Hoover CI, Nakayama K, Ideka T, Nakamura H, Yoshimura F. Identification of Porphyromonas gingivalis prefimbrilin possessing a long leader peptide: possible involvement of trypsin-like protease in fimbrilin maturation. Microb Pathog. 1995;19:351-64. https://doi.org/10.1016/s0882-4010(96)80006-4
Shoji M, Naito M, Yukitake H, et al. The major structural components of two cell surface filaments of Porphyromonas gingivalis are matured through lipoprotein precursors. Mol Microbiol. 2004;52:1513-25. https://doi.org/10.1111/j.1365-2958.2004.04105.x
Hasegawa Y, Iwami J, Sato K, et al. Anchoring and length regulation of Porphyromonas gingivalis Mfa1 fimbriae by the downstream gene product Mfa2. Microbiology. 2009;155:3333-47. https://doi.org/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. 2010;89:903-8. https://doi.org/10.1177/0022034510370089
Nishiyama SI, Murakami Y, Nagata H, Shizukuishi S, Kawagishi I, Yoshimura F. Involvement of minor components associated with the FimA fimbriae of Porphyromonas gingivalis in adhesive functions. Microbiology. 2007;153:1916-25. https://doi.org/10.1099/mic.0.2006/005561-0
Hasegawa Y, Nagano K, Ikai R, et al. Localization and function of the accessory protein Mfa3 in Porphyromonas gingivalis Mfa1 fimbriae. Mol Oral Microbiol. 2013;28:467-80. https://doi.org/10.1111/omi.12040
Ikai R, Hasegawa Y, Izumigawa M, et al. Mfa4, an accessory protein of Mfa1 fimbriae, modulates fimbrial biogenesis, cell auto-aggregation, and biofilm formation in Porphyromonas gingivalis. PLoS One. 2015;10:e0139454. https://doi.org/10.1371/journal.pone.0139454 Published 2015 Oct 5.
Hasegawa Y, Iijima Y, Persson K, et al. Role of Mfa5 in expression of Mfa1 fimbriae in Porphyromonas gingivalis. J Dent Res. 2016;95:1291-97. https://doi.org/10.1177/0022034516655083
Nelson KE, Fleischmann RD, DeBoy RT, et al. Complete genome sequence of the oral pathogenic Bacterium porphyromonas gingivalis strain W83. J Bacteriol. 2003;185:5591-5601. https://doi.org/10.1128/jb.185.18.5591-5601.2003
Naito M, Hirakawa H, Yamashita A, et al. Determination of the genome sequence of Porphyromonas gingivalis strain ATCC 33277 and genomic comparison with strain W83 revealed extensive genome rearrangements in P. gingivalis. DNA Res. 2008;15:215-25. https://doi.org/10.1093/dnares/dsn013
Kloppsteck P, Hall M, Hasegawa Y, Persson K. Structure of the fimbrial protein Mfa4 from Porphyromonas gingivalis in its precursor form: implications for a donor-strand complementation mechanism. Sci Rep. 2016;6:22945. https://doi.org/10.1038/srep22945
Hall M, Hasegawa Y, Yoshimura F, Persson K. Structural and functional characterization of shaft, anchor, and tip proteins of the Mfa1 fimbria from the periodontal pathogen Porphyromonas gingivalis. Sci Rep. 2018;8(1):1793. https://doi.org/10.1038/s41598-018-20067-z
Alaei SR, Park JH, Walker SG, Thanassi DG. Peptide-based inhibitors of fimbrial biogenesis in Porphyromonas gingivalis. Infect Immun. 2019;87(3):e00750-18. https://doi.org/10.1128/IAI.00750-18
Shibata S, Shoji M, Okada K, et al. Structure of polymerized type V pilin reveals assembly mechanism involving protease-mediated strand exchange. Nat Microbiol. 2020;5:830-7. https://doi.org/10.1038/s41564-020-0705-1
Braun V, Wu HC. Lipoproteins: structure function, biosynthesis and model for protein export. New Comp Biochem. 1994;27:319-41.
Yamagata H, Ippolito C, Inukai M, Inouye M. Temperature-sensitive processing of outer membrane lipoprotein in an Escherichia coli mutant. J Bacteriol. 1982;152:1163-68.
Petit CM, Brown JR, Ingraham K, Bryant AP, Holmes DJ. Lipid modification of prelipoproteins is dispensable for growth in vitro but essential for virulence in Streptococcus pneumoniae. FEMS Microbiol Lett. 2001;200:229-33. https://doi.org/10.1111/j.1574-6968.2001.tb10720.x
Réglier-Poupet H, Frehel C, Dubail I, et al. Maturation of lipoproteins by type II signal peptidase is required for phagosomal escape of Listeria monocytogenes. J Biol Chem. 2003;278:49469-77. https://doi.org/10.1074/jbc.M307953200
Armbruster KM, Meredith TC. Identification of the lyso-form N-acyl intramolecular transferase in low-GC Firmicutes. J Bacteriol. 2017;199(11):e00099-17. https://doi.org/10.1128/JB.00099-17
Nakayama H, Kurokawa K, Lee BL. Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J. 2012;279:4247-68. https://doi.org/10.1111/febs.12041
Hashimoto M, Asai Y, Ogawa T. Separation and structural analysis of lipoprotein in a lipopolysaccharide preparation from Porphyromonas gingivalis. Int Immunol. 2004;16:1431-37. https://doi.org/10.1093/intimm/dxh146
Matsuyama S, Tajima T, Tokuda H. A novel periplasmic carrier protein involved in the sorting and transport of Escherichia coli lipoproteins destined for the outer membrane. EMBO J. 1995;14:3365-72.
Matsuyama S, Yokota N, Tokuda H. A novel outer membrane lipoprotein, LolB (HemM), involved in the LolA (p20)-dependent localization of lipoproteins to the outer membrane of Escherichia coli. EMBO J. 1997;16:6947-55. https://doi.org/10.1093/emboj/16.23.6947
Narita SI, Tokuda H. Bacterial lipoproteins; biogenesis, sorting and quality control. Biochim Biophys Acta Mol Cell Biol Lipids. 2017;1862:1414-23. https://doi.org/10.1016/j.bbalip.2016.11.009
Takeda K, Miyatake H, Yokota N, Matsuyama S, Tokuda H, Miki K. Crystal structures of bacterial lipoprotein localization factors, LolA and LolB. EMBO J. 2003;22:3199-209. https://doi.org/10.1093/emboj/cdg324
Tajima T, Yokota N, Matsuyama S, Tokuda H. Genetic analyses of the in vivo function of LolA, a periplasmic chaperone involved in the outer membrane localization of Escherichia coli lipoproteins. FEBS Lett. 1998;439:51-4. https://doi.org/10.1016/s0014-5793(98)01334-9
Fernández-Piñar R, Lo Sciuto A, Rossi A, Ranucci S, Bragonzi A, Imperi F. In vitro and in vivo screening for novel essential cell-envelope proteins in Pseudomonas aeruginosa. Sci Rep. 2015;5:17593. https://doi.org/10.1038/srep17593
Chalker AF, Minehart HW, Hughes NJ, et al. Systematic identification of selective essential genes in Helicobacter pylori by genome prioritization and allelic replacement mutagenesis. J Bacteriol. 2001;183:1259-68. https://doi.org/10.1128/JB.183.4.1259-1268.2001
Rhodes RG, Samarasam MN, Van Groll EJ, McBride MJ. Mutations in Flavobacterium johnsoniae sprE result in defects in gliding motility and protein secretion. J Bacteriol. 2011;193:5322-27. https://doi.org/10.1128/JB.05480-11
Zhu Y, McBride MJ. Comparative analysis of Cellulophaga algicola and Flavobacterium johnsoniae gliding motility. J Bacteriol. 2016;198:1743-54. https://doi.org/10.1128/JB.01020-15
Liao CT, Chiang YC, Hsiao YM. Functional characterization and proteomic analysis of lolA in Xanthomonas campestris pv. campestris. BMC Microbiol. 2019;19(1):20. https://doi.org/10.1186/s12866-019-1387-9
Grabowicz M, Silhavy TJ. Redefining the essential trafficking pathway for outer membrane lipoproteins. Proc Natl Acad Sci USA. 2017;114:4769-74. https://doi.org/10.1073/pnas.1702248114
Okuda S, Watanabe S, Tokuda H. A short helix in the C-terminal region of LolA is important for the specific membrane localization of lipoproteins. FEBS Lett. 2008;582:2247-51. https://doi.org/10.1016/j.febslet.2008.05.022
Hayashi Y, Tsurumizu R, Tsukahara J, et al. Roles of the protruding loop of factor B essential for the localization of lipoproteins (LolB) in the anchoring of bacterial triacylated proteins to the outer membrane. J Biol Chem. 2014;289:10530-39. https://doi.org/10.1074/jbc.M113.539270
Sutcliffe IC, Harrington DJ, Hutchings MI. A phylum level analysis reveals lipoprotein biosynthesis to be a fundamental property of bacteria. Protein Cell. 2012;3:163-70. https://doi.org/10.1007/s13238-012-2023-8
Webb CT, Heinz E, Lithgow T. Evolution of the β-barrel assembly machinery. Trends Microbiol. 2012;20:612-20. https://doi.org/10.1016/j.tim.2012.08.006
Klein BA, Tenorio EL, Lazinski DW, Camilli A, Duncan MJ, Hu LT. Identification of essential genes of the periodontal pathogen Porphyromonas gingivalis. BMC Genomics. 2012;13:578. https://doi.org/10.1186/1471-2164-13-578
Hutcherson JA, Gogeneni H, Yoder-Himes D, et al. Comparison of inherently essential genes of Porphyromonas gingivalis identified in two transposon-sequencing libraries. Mol Oral Microbiol. 2016;31:354-64. https://doi.org/10.1111/omi.12135
Levine TP. Remote homology searches identify bacterial homologues of eukaryotic lipid transfer proteins, including Chorein-N domains in TamB and AsmA and Mdm31p. BMC Mol Cell Biol. 2019;20(1):43. https://doi.org/10.1186/s12860-019-0226-z
Okuda S, Tokuda H. Lipoprotein sorting in bacteria. Annu Rev Microbiol. 2011;65:239-59. https://doi.org/10.1146/annurev-micro-090110-102859
Konovalova A, Perlman DH, Cowles CE, Silhavy TJ. Transmembrane domain of surface-exposed outer membrane lipoprotein RcsF is threaded through the lumen of β-barrel proteins. Proc Natl Acad Sci USA. 2014;111:E4350-58. https://doi.org/10.1073/pnas.1417138111
Michel LV, Shaw J, MacPherson V, et al. Dual orientation of the outer membrane lipoprotein Pal in Escherichia coli. Microbiology. 2015;161:1251-59. https://doi.org/10.1099/mic.0.000084
Schulze RJ, Zückert WR. Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol Microbiol. 2006;59:1473-84.
Dowdell AS, Murphy MD, Azodi C, et al. Comprehensive spatial analysis of the Borrelia burgdorferi lipoproteome reveals a compartmentalization bias toward the bacterial surface. J Bacteriol. 2017;199(6):e00658-16. https://doi.org/10.1128/JB.00658-16 Published 2017 Feb 28.
Chen S, Zückert WR. Probing the Borrelia burgdorferi surface lipoprotein secretion pathway using a conditionally folding protein domain. J Bacteriol. 2011;193:6724-32. https://doi.org/10.1128/JB.06042-11
Kumru OS, Schulze RJ, Rodnin MV, Ladokhin AS, Zückert WR. Surface localization determinants of Borrelia OspC/Vsp family lipoproteins. J Bacteriol. 2011;193:2814-25. https://doi.org/10.1128/JB.00015-11
Zückert WR. Protein secretion in Spirochetes. Microbiol Spectr. 2019;7(3) https://doi.org/10.1128/microbiolspec.PSIB-0026-2019
Anderson KL, Salyers AA. Biochemical evidence that starch breakdown by Bacteroides thetaiotaomicron involves outer membrane starch-binding sites and periplasmic starch-degrading enzymes. J Bacteriol. 1989;171:3192-98. https://doi.org/10.1128/jb.171.6.3192-3198.1989
Wilson MM, Anderson DE, Bernstein HD. Analysis of the outer membrane proteome and secretome of Bacteroides fragilis reveals a multiplicity of secretion mechanisms. PLoS One. 2015;10(2):e0117732. https://doi.org/10.1371/journal.pone.0117732 Published 2015 Feb 6.
Valguarnera E, Scott NE, Azimzadeh P, Feldman MF. Surface exposure and packing of lipoproteins into outer membrane vesicles are coupled processes in Bacteroides. mSphere. 2018;3(6):e00559-18. https://doi.org/10.1128/mSphere.00559-18 pii.
Lauber F, Cornelis GR, Renzi F. Identification of a new lipoprotein export signal in Gram-negative bacteria. mBio. 2016;7:e01232-16. https://doi.org/10.1128/mBio.01232-16 Published 2016 Oct 25.
Berven FS, Karlsen OA, Straume AH, et al. Analysing the outer membrane subproteome of Methylococcus capsulatus (Bath) using proteomics and novel biocomputing tools. Arch Microbiol. 2006;184:362-77. https://doi.org/10.1007/s00203-005-0055-7
Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 2003;12:1652-62. https://doi.org/10.1110/ps.0303703
Gorasia DG, Veith PD, Hanssen EG, et al. Structural insights into the PorK and PorN components of the Porphyromonas gingivalis type IX secretion system. PLoS Pathog. 2016;12(8):e1005820. https://doi.org/10.1371/journal.ppat.1005820
Hooda Y, Lai CC, Judd A, et al. Slam is an outer membrane protein that is required for the surface display of lipidated virulence factors in Neisseria. Nat Microbiol. 2016;1:16009. https://doi.org/10.1038/nmicrobiol.2016.9
Hooda Y, Lai CCL, Moraes TF. Identification of a large family of Slam-dependent surface lipoproteins in Gram-negative bacteria. Front Cell Infect Microbiol. 2017;7:207. https://doi.org/10.3389/fcimb.2017.00207