microbeПроблемы особо опасных инфекцийProblems of Particularly Dangerous Infections0370-10692658-719XRussian Research Anti-Plague Institute “Microbe”10.21055/0370-1069-2018-2-14-22microbe-474Research ArticleОБЗОРЫREVIEWSАдгезины возбудителя чумыAdhesines of the Plague AgentКуклеваЛ. М.KuklevaL. M.rusrapi@microbe.ruФКУЗ «Российский научно-исследовательский противочумный институт «Микроб», СаратовРоссияRussian Research Anti-Plague Institute “Microbe”, SaratovRussian Federation201803072018021422Copyright © Куклева Л.М., 20182018Куклева Л.М.Kukleva L.M.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://journal.microbe.ru/jour/article/view/474

Возбудитель чумы обладает комплексом адгезинов, обеспечивающих прикрепление возбудителя к клеткаммишеням в организме хозяина и во многом определяющих начало, характер и течение болезни. Наличие адгезинов обеспечивает транслокацию эффекторных белков в клетки-мишени млекопитающих. В обзоре представлены литературные данные как о наиболее изученных адгезинах Yersinia pestis (белках Ail и pH6 антиген), так и о недавно выявленных аутотранспортных белках различных классов, участвующих в процессах адгезии (YadBC, Yaps, Ilp). Описано их значение для патогенеза чумы, генетическая детерминированность, структура и локализация в клетке. Отмечено, что адгезины возбудителя чумы действуют на разных стадиях инфекционного процесса, выполняют множественные функции, участвуют не только в процессах прикрепления к клеткам хозяина, но также обеспечивают устойчивость к действию иммунных механизмов хозяина.

 

Plague agent has a complex of adhesines providing for anchoring of the pathogen to target cells in a host organism and in many ways defining the onset, character, and development of the disease. The presence of adhesines ensures translocation of effector proteins into target cells of mammalians. The review covers the literature data, both on the most studied Yersinia pestis adhesines (Ail proteins and pH6 antigen), and on recently identified auto transporting proteins of various classes, involved in adhesion processes (YadBC, Yaps, IlpP). Their significance for plague pathogenesis, genetic determinacy, structure and localization in a cell are also described in the paper. It is noted that plague agent adhesines work at different phases of infection process, have multiple functions and take part not only in anchoring to host cells, but provide for resistance to influence of immune mechanisms of a host too.

 

возбудитель чумыадгезиныпатогенностьplague agentadhesinespathogenicityReferencesВодопьянов С.О., Мишанькин Б.Н. Пили адгезии у Yersinia pestis. Журнал микробиологии, эпидемиологии и иммунобиологии. 1985; 6:13–7.Vodop’yanov S.O., Mishan’kin B.N. [Pilus of adhesion in Yersinia pestis]. Zhurnal Mikrobiologii, Epidemiologii i Immunobiologii. 1985; 6:13–7.Евсеева В.В., Платонов М.Е., Копылов П.Х., Дентовская С.В., Анисимов А.П. Активатор плазминогена чумного микроба. Инфекция и иммунитет. 2015; 5(1):27–36. DOI: 10.15789/2220- 7619-2015-1-27-36.Evseeva V.V., Platonov M.E., Kopylov P.Kh., Dentovskaya S.V., Anisimov A.P. [Plasminogen activator of plague agent]. Infektsiya i Immunitet. 2015; 5(1):27–36. DOI: 10.15789/2220-7619 -201501-27-36.Ерошенко Г.А., Одиноков Г.Н., Куклева Л.М., Краснов Я.М., Кутырев В.В. Сравнительный анализ нуклеотидной последовательности генов yadA, inv и ail и их экспрессия в штаммах Yersinia pestis основного и неосновных подвидов и Yersinia pseudotuberculosis. Генетика. 2010; 46(6):734–41.Eroshenko G.A., Odinokov G.N., Kukleva L.M., Krasnov Ya. M., Kutyrev V.V. [Comparative analysis of the nucleotide sequence of yadA, inv, and ail genes and their expression in Yersinia pestis strains of the main and non-main subspecies and Yersinia pseudotuberculosis]. Genetika. 2010; 46(6):734–41.Куклева Л.М., Бойко А.В. Активатор плазминогена – многофункциональный белок возбудителя чумы. Проблемы особо опасных инфекций. 2016; 3:13–20. DOI: 10.21055/0370-1069- 2016-3-13-20.Kukleva L.M., Boiko A.V. [Plasminogen activator – multi- functional protein of plague pathogen]. Problemy Osobo Opasnykh Infektsii [Problems of Particularly Dangerous Infections]. 2016; 3:13–20. DOI: 10.21055/0370-1069-2016-3-13-20.Anisimov A.V., Dentovskaya S.V., Titareva G.M., Bakhteeva I.V., Shaikhutdinova R.Z., Balakhonov S.V., Lindner B., Kocharova N.A., Senchenkova S.N., Holst O., Pier G.B., Knirel Yu.A. Intraspecies and Temperature-Dependent Variations in Susceptibility of Yersinia pestis to the Bactericidal Action of Serum and to Polymyxin B. Infect. Immun. 2005; 73(11):7324–31 DOI:10.1128/ IAI.73.11.7324–7331.2005.Anisimov A.V., Dentovskaya S.V., Titareva G.M., Bakhteeva I.V., Shaikhutdinova R.Z., Balakhonov S.V., Lindner B., Kocharova N.A., Senchenkova S.N., Holst O., Pier G.B., Knirel Yu.A. Intraspecies and Temperature-Dependent Variations in Susceptibility of Yersinia pestis to the Bactericidal Action of Serum and to Polymyxin B. Infect. Immun. 2005; 73(11):7324–31 DOI:10.1128/ IAI.73.11.7324–7331.2005.Bartra S.S., Styer K.L., O’Bryant D.M., Nilles M.L., Hinnebusch B.J., Aballay A., Plano G. Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer mem- brane protein. Infect. Immun. 2008; 76(2):612–22. DOI:10.1128/ IAI.01125-07.Bartra S.S., Styer K.L., O’Bryant D.M., Nilles M.L., Hinnebusch B.J., Aballay A., Plano G. Resistance of Yersinia pestis to complement-dependent killing is mediated by the Ail outer mem- brane protein. Infect. Immun. 2008; 76(2):612–22. DOI:10.1128/ IAI.01125-07.Bartra S.S., Ding Y., Miya Fujimoto L., Ring J.G., Jain V., Ram S., Marassi F.M., Plano G.V. Yersinia pestis uses the Ail outer membrane protein to recruit vitronectin. Microbiology. 2015; 161(11):2174–83. DOI: 10.1099/mic.0.000179.Bartra S.S., Ding Y., Miya Fujimoto L., Ring J.G., Jain V., Ram S., Marassi F.M., Plano G.V. Yersinia pestis uses the Ail outer membrane protein to recruit vitronectin. Microbiology. 2015; 161(11):2174–83. DOI: 10.1099/mic.0.000179.Bertherat E., Plague around the world, 2010–2015. Weekly epidemiological record. 2016; 91(8):89–104.Bertherat E., Plague around the world, 2010–2015. Weekly epidemiological record. 2016; 91(8):89–104.Cathelyn, J.S., Crosby S.D., Lathem W.W., Goldman W.E., Miller V.L. RovA, a global regulator of Yersinia pestis, specifical- ly required for bubonic plague. Proc. Natl. Acad. Sci. USA. 2006; 103(36):13514–9. DOI:10.1073/pnas.0603456103.Cathelyn, J.S., Crosby S.D., Lathem W.W., Goldman W.E., Miller V.L. RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc. Natl. Acad. Sci. USA. 2006; 103(36):13514–9. DOI:10.1073/pnas.0603456103.Chauhan N., Wrobel A., Skurnik M., Leo J.C. Yersinia ad- hesins: an arsenal for infection. Proteomics Clin. Appl. 2016; 10(9– 10):949–963. DOI: 10.1002/prca.201600012.Chauhan N., Wrobel A., Skurnik M., Leo J.C. Yersinia adhesins: an arsenal for infection. Proteomics Clin. Appl. 2016; 10(9– 10):949–963. DOI: 10.1002/prca.201600012.Chauvaux S., Rosso M.L., Frangeul L., Lacroix C., Labarre L., Schiavo A., Marceau M., Dillies M.A., Foulon J., Coppée J.Y., Médigue C., Simonet M., Carniel E.. Transcriptome analysis of Yersinia pestis in human plasma: an approach for discovering bac- terial genes involved in septicaemic plague. Microbiology. 2007; 153(Pt.9):3112–24. DOI: 10.1099/mic.0.2007/006213-0.Chauvaux S., Rosso M.L., Frangeul L., Lacroix C., Labarre L., Schiavo A., Marceau M., Dillies M.A., Foulon J., Coppée J.Y., Médigue C., Simonet M., Carniel E.. Transcriptome analysis of Yersinia pestis in human plasma: an approach for discovering bacterial genes involved in septicaemic plague. Microbiology. 2007; 153(Pt.9):3112–24. DOI: 10.1099/mic.0.2007/006213-0.Chauvaux S., Dillies M.A., Marceauc M., Rosso M.L., Rousseau S., Moszer I., Simonet M., Carniel E. In silico comparison of Yersinia pestis and Yersinia pseudotuberculosis transcriptomes reveals a higher expression level of crucial virulence determinants in the plague bacillus. Intern. J. Med. Microbiol. 2011; 301(2):105–16. DOI:10.1016/j.ijmm.2010.08.013.Chauvaux S., Dillies M.A., Marceauc M., Rosso M.L., Rousseau S., Moszer I., Simonet M., Carniel E. In silico comparison of Yersinia pestis and Yersinia pseudotuberculosis transcriptomes reveals a higher expression level of crucial virulence determinants in the plague bacillus. Intern. J. Med. Microbiol. 2011; 301(2):105–16. DOI:10.1016/j.ijmm.2010.08.013.Deng W., Burland V., Plunkett G., Boutin A., Mayhew G.F., Liss P., Perna N.T., Rose D.J., Mau B., Zhou S., Schwartz D.C., Fetherston J.D, Lindler L.E., Brubaker R.R., Plano G.V., Straley S.C., McDonough K.A., Nilles M.L., Matson J.S., Blattner F.R., Perry R.D. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 2002; 184(16):4601–11. DOI: 10.1128/JB.184.16.4601-4611.2002.Deng W., Burland V., Plunkett G., Boutin A., Mayhew G.F., Liss P., Perna N.T., Rose D.J., Mau B., Zhou S., Schwartz D.C., Fetherston J.D, Lindler L.E., Brubaker R.R., Plano G.V., Straley S.C., McDonough K.A., Nilles M.L., Matson J.S., Blattner F.R., Perry R.D. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 2002; 184(16):4601–11. DOI: 10.1128/JB.184.16.4601-4611.2002.Felek S., Lawrenz M.B., Krukonis E.S. The Yersinia pes- tis autotransporter YapC mediates host cell binding, autoaggrega- tion and biofilm formation. Microbiology. 2008; 154(Pt.6):1802–12. DOI: 10.1099/mic.0.2007/010918-0.Felek S., Lawrenz M.B., Krukonis E.S. The Yersinia pes- tis autotransporter YapC mediates host cell binding, autoaggregation and biofilm formation. Microbiology. 2008; 154(Pt.6):1802–12. DOI: 10.1099/mic.0.2007/010918-0.Felek S., Tsang T.M., Krukonis E.S. Three Yersinia pes- tis adhesins facilitate Yop delivery to eukaryotic cells and contrib- ute to plague virulence. Infect. Immun. 2010; 78(10):4134–50. DOI:10.1128/IAI.00167-10.Felek S., Tsang T.M., Krukonis E.S. Three Yersinia pestis adhesins facilitate Yop delivery to eukaryotic cells and contribute to plague virulence. Infect. Immun. 2010; 78(10):4134–50. DOI:10.1128/IAI.00167-10.Felek S., Jeong J.J., Runco L.M., Murray S., Thanassi D.G., Krukonis E.S. Contributions of chaperone/usher systems to cell bind- ing, biofilm formation, and Yersinia pestis virulence. Microbiology. 2011; 157(Pt.3):805–18. DOI: 10.1099/mic.0.044826-0.Felek S., Jeong J.J., Runco L.M., Murray S., Thanassi D.G., Krukonis E.S. Contributions of chaperone/usher systems to cell binding, biofilm formation, and Yersinia pestis virulence. Microbiology. 2011; 157(Pt.3):805–18. DOI: 10.1099/mic.0.044826-0.Forman S., Wulff C.R., Myers-Morales T., Cowan C., Perry R.D, Straley S.C. yadBC of Yersinia pestis, a new virulence determinant for bubonic plague. Infect. Immun. 2008; 76(2):578–87 DOI:10.1128/IAI.00219-07.Forman S., Wulff C.R., Myers-Morales T., Cowan C., Perry R.D, Straley S.C. yadBC of Yersinia pestis, a new virulence determinant for bubonic plague. Infect. Immun. 2008; 76(2):578–87 DOI:10.1128/IAI.00219-07.Galvan E.M., Chen H., Schifferli D.M. The Psa fimbriae of Yersinia pestis interact with phosphatidylcholine on alveolar epitheli- al cells and pulmonary surfactant. Infect. Immun. 2007; 75(3):1272– 79. DOI:10.1128/IAI.01153-06.Galvan E.M., Chen H., Schifferli D.M. The Psa fimbriae of Yersinia pestis interact with phosphatidylcholine on alveolar epithelial cells and pulmonary surfactant. Infect. Immun. 2007; 75(3):1272– 79. DOI:10.1128/IAI.01153-06.Hinnebusch B.J., Jarrett C.O., Callison J.A., Gardner D., Buchanan S.K., Plano G.V. Role of the Yersinia pestis Ail protein in preventing a protective polymorphonuclear leukocyte response during bubonic plague. Infect. Immun. 2011; 79(12):4984–89. DOI:10.1128/IAI.05307-11.Hinnebusch B.J., Jarrett C.O., Callison J.A., Gardner D., Buchanan S.K., Plano G.V. Role of the Yersinia pestis Ail protein in preventing a protective polymorphonuclear leukocyte response during bubonic plague. Infect. Immun. 2011; 79(12):4984–89. DOI:10.1128/IAI.05307-11.Huang X.Z., Lindler L.E. The pH6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect. Immun. 2004; 72(12):7212–19. DOI: 10.1128/IAI.72.12.7212-7219.2004.Huang X.Z., Lindler L.E. The pH6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect. Immun. 2004; 72(12):7212–19. DOI: 10.1128/IAI.72.12.7212-7219.2004.Kolodziejek A.M., Schnider D.R., Rohde H.N., Wojtowicz A.J., Bohach G.A., Minnich S.A., Hovde C.J. Outer membrane protein X (Ail) contributes to Yersinia pestis virulence in pneumonic plague and its activity is dependent on the lipopolysaccharide core length. Infect. Immun. 2010; 78(12):5233–43. DOI:10.1128/IAI.00783-10.Kolodziejek A.M., Schnider D.R., Rohde H.N., Wojtowicz A.J., Bohach G.A., Minnich S.A., Hovde C.J. Outer membrane protein X (Ail) contributes to Yersinia pestis virulence in pneumonic plague and its activity is dependent on the lipopolysaccharide core length. Infect. Immun. 2010; 78(12):5233–43. DOI:10.1128/IAI.00783-10.Kolodziejek A.M., Hovde C.J., Minnich S.A., Yersinia pestis Ail: multiple roles of a single protein. Front. Cell. Infect. Microbiol. 2012; 2(103):1–10. DOI: 10.3389/fcimb.2012.00103.Kolodziejek A.M., Hovde C.J., Minnich S.A., Yersinia pestis Ail: multiple roles of a single protein. Front. Cell. Infect. Microbiol. 2012; 2(103):1–10. DOI: 10.3389/fcimb.2012.00103.Lane M., Lenz J.D., Miller V.L. Proteolytic processing of the Yersinia pestis YapG autotransporter by the omptin protease Pla and the contribution of YapG to murine plague pathogenesis. J. Med. Microbiol. 2013; 62(Pt8):1124–34. DOI: 10.1099/jmm.0.056275-0.Lane M., Lenz J.D., Miller V.L. Proteolytic processing of the Yersinia pestis YapG autotransporter by the omptin protease Pla and the contribution of YapG to murine plague pathogenesis. J. Med. Microbiol. 2013; 62(Pt8):1124–34. DOI: 10.1099/jmm.0.056275-0.Lawrenz M.B., Lenz J.D, Miller V.L. A Novel Autotransporter adhesin is required for efficient colonization during bubonic plague. Infect. Immun. 2009; 77(1):317–26. DOI:10.1128/ IAI.01206-08.Lawrenz M.B., Lenz J.D, Miller V.L. A Novel Autotransporter adhesin is required for efficient colonization during bubonic plague. Infect. Immun. 2009; 77(1):317–26. DOI:10.1128/ IAI.01206-08.Lawrenz M.B., Pennington J., Miller V.L. Acquisition of omptin reveals cryptic virulence function of autotransporter YapE in Yersinia pestis. Mol. Microbiol. 2013; 89(2):276–87. DOI:10.1111/ mmi.12273.Lawrenz M.B., Pennington J., Miller V.L. Acquisition of omptin reveals cryptic virulence function of autotransporter YapE in Yersinia pestis. Mol. Microbiol. 2013; 89(2):276–87. DOI:10.1111/ mmi.12273.Lenz J.D., Lawrenz M.B., Cotter D.G., Lane M.C., Gonzalez R.J., Palacios M., Miller V.L. Expression during host in- fection and localization of Yersinia pestis autotransporter proteins. J. Bacteriol. 2011; 193(21):5936–49. DOI:10.1128/JB.05877-11.Lenz J.D., Lawrenz M.B., Cotter D.G., Lane M.C., Gonzalez R.J., Palacios M., Miller V.L. Expression during host in- fection and localization of Yersinia pestis autotransporter proteins. J. Bacteriol. 2011; 193(21):5936–49. DOI:10.1128/JB.05877-11.Lenz J.D., Temple B., Miller V.L. Evolution and viru- lence contributions of the autotransporter proteins YapJ and YapK of Yersinia pestis CO92 and their homologs in Y. pseudotuberculo- sis IP32953. Infect. Immun. 2012; 80(10):3693–705. DOI:10.1128/ IAI.00529-12.Lenz J.D., Temple B., Miller V.L. Evolution and virulence contributions of the autotransporter proteins YapJ and YapK of Yersinia pestis CO92 and their homologs in Y. pseudotuberculosis IP32953. Infect. Immun. 2012; 80(10):3693–705. DOI:10.1128/ IAI.00529-12.Leo J.C., Grin I., Linke D. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Phil. Trans. R. Soc. B. Biol. Sci. 2012; 367(1592):1088–101. DOI:10.1098/ rstb.2011.0208.Leo J.C., Grin I., Linke D. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Phil. Trans. R. Soc. B. Biol. Sci. 2012; 367(1592):1088–101. DOI:10.1098/ rstb.2011.0208.Leo J.C., Oberhettinger P, Schütz M, Linke D. The in- verse autotransporter family: intimin, invasin and related proteins. Int. J. Med. Microbiol. 2015; 305(2):276–82. DOI: 10.1016/j. ijmm.2014.12.011.Leo J.C., Oberhettinger P, Schütz M, Linke D. The in- verse autotransporter family: intimin, invasin and related proteins. Int. J. Med. Microbiol. 2015; 305(2):276–82. DOI: 10.1016/j. ijmm.2014.12.011.Leo J.C., Oberhettinger P., Chaubey M., Schütz M., Kühner D., Bertsche U., Schwarz H., Götz F., Autenrieth I.B., Coles M., Linke D. The intimin periplasmic domain mediates dimerisation and binding to peptidoglycan. Mol. Microbiol. 2015; 95(1):80–100. DOI: 10.1111/mmi.12840.Leo J.C., Oberhettinger P., Chaubey M., Schütz M., Kühner D., Bertsche U., Schwarz H., Götz F., Autenrieth I.B., Coles M., Linke D. The intimin periplasmic domain mediates dimerisation and binding to peptidoglycan. Mol. Microbiol. 2015; 95(1):80–100. DOI: 10.1111/mmi.12840.Lindler L.E., Klempner M.S., Straley S.C. Yersinia pestis pH6 antigen: genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect. Immun. 1990; 58(8):2569–77.Lindler L.E., Klempner M.S., Straley S.C. Yersinia pestis pH6 antigen: genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect. Immun. 1990; 58(8):2569–77.Lindler L., Tall B. Yersinia pestis pH6 antigen forms fimbriae and is induced by intracellular association with macrophages. Mol. Microbiol. 1993; 8(2):311–24.Lindler L., Tall B. Yersinia pestis pH6 antigen forms fimbriae and is induced by intracellular association with macrophages. Mol. Microbiol. 1993; 8(2):311–24.Liu F., Chen H., Galvan E.M., Lasaro M.A., Schifferli D.M. Effects of Psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells. Infect. Immun. 2006; 74(10):5636–44. DOI: 10.1128/IAI.00612-06.Liu F., Chen H., Galvan E.M., Lasaro M.A., Schifferli D.M. Effects of Psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells. Infect. Immun. 2006; 74(10):5636–44. DOI: 10.1128/IAI.00612-06.Liu H., Wang H., Qiu J., Wang X., Guo Z., Qiu Y., Zhou D., Han Y., Du Z., Li C., Song Y., Yang R. Transcriptional profiling of a mice plague model: insights into interaction between Yersinia pestis and its host. J. Basic. Microbiol. 2009; 49(1):92–9. DOI: 10.1002/ jobm.200800027.Liu H., Wang H., Qiu J., Wang X., Guo Z., Qiu Y., Zhou D., Han Y., Du Z., Li C., Song Y., Yang R. Transcriptional profiling of a mice plague model: insights into interaction between Yersinia pestis and its host. J. Basic. Microbiol. 2009; 49(1):92–9. DOI: 10.1002/ jobm.200800027.Lobo L.A. Adhesive properties of the purified plasmino- gen activator Pla of Yersinia pestis. FEMS Microbiol. Lett. 2006; 262(2):158–62. DOI: 10.1111/j.1574-6968.2006.00382.x.Lobo L.A. Adhesive properties of the purified plasminogen activator Pla of Yersinia pestis. FEMS Microbiol. Lett. 2006; 262(2):158–62. DOI: 10.1111/j.1574-6968.2006.00382.x.Makoveichuk E., Cherepanov P., Lundberg S., Forsberg A., Olivecrona G. pH6 antigen of Yersinia pestis interacts with plasma lipoproteins and cell membranes. J. Lipid. Res. 2003; 44(2):320–30. DOI: 10.1194/jlr.M200182-JLR200.Makoveichuk E., Cherepanov P., Lundberg S., Forsberg A., Olivecrona G. pH6 antigen of Yersinia pestis interacts with plasma lipoproteins and cell membranes. J. Lipid. Res. 2003; 44(2):320–30. DOI: 10.1194/jlr.M200182-JLR200.Mikula K.M., Kolodziejczyk R., Goldman A. Yersinia in- fection tools – characterization of structure and function of adhesions. Front. Cell Infect. Microbiol. 2013; 2(169):1–14. DOI: 10.3389/ fcimb.2012.00169.Mikula K.M., Kolodziejczyk R., Goldman A. Yersinia infection tools – characterization of structure and function of adhesions. Front. Cell Infect. Microbiol. 2013; 2(169):1–14. DOI: 10.3389/ fcimb.2012.00169.Nair M.K., De Masi L., Yue M., Galván E.M., Chen H., Wang F., Schifferli D.M. Adheive properties of YapV and paralo- gous autotransporter proteins of Yersinia pestis. Infect. Immun. 2015; 83(5):1809–19. DOI: 10.1128/IAI.00094-15.Nair M.K., De Masi L., Yue M., Galván E.M., Chen H., Wang F., Schifferli D.M. Adheive properties of YapV and paralogous autotransporter proteins of Yersinia pestis. Infect. Immun. 2015; 83(5):1809–19. DOI: 10.1128/IAI.00094-15.Payne D., Tatham D., Williamson D.E., Titball R.W. The pH6 antigen of Yersinia pestis binds to b1-linked galactosyl residues in glycosphingolipids. Infect. Immun. 1998; 66(9):4545–8.Payne D., Tatham D., Williamson D.E., Titball R.W. The pH6 antigen of Yersinia pestis binds to b1-linked galactosyl residues in glycosphingolipids. Infect. Immun. 1998; 66(9):4545–8.Perry R.D., Fetherston J.D. Yersinia pestis – etiologic agent of plague. Clin. Microbiol. Rev. 1997; 10(1):35–66.Perry R.D., Fetherston J.D. Yersinia pestis – etiologic agent of plague. Clin. Microbiol. Rev. 1997; 10(1):35–66.Plesniak L.A., Mahalakshmi R., Rypien C., Yang Y., Racic J., Marassi F.M. Expression, refolding, and initial structural characterization of the Y. pestis Ail outer membrane protein in lip- ids. Biochim. Biophys. Acta. 2011; 1808(1):482–9. DOI: 10.1016/j. bbamem.2010.09.017.Plesniak L.A., Mahalakshmi R., Rypien C., Yang Y., Racic J., Marassi F.M. Expression, refolding, and initial structural characterization of the Y. pestis Ail outer membrane protein in lip- ids. Biochim. Biophys. Acta. 2011; 1808(1):482–9. DOI: 10.1016/j. bbamem.2010.09.017.Seo S.K., Kim J.W., Park J.Y., Viall A.K., Minnich S.S., Rohde H.N., Schnider D.R., Lim S.Y., Hong J.B., Hinnebusch B.J., O’Loughlin J.L., Deobald C.F., Bohach G.A., Hovde C.J., Minnichb S.A. Role of a new intimin/invasin-like protein in Yersinia pes- tis virulence. Infect. Immun. 2012; 80(10):3559–69. DOI:10.1128/ IAI.00294-12.Seo S.K., Kim J.W., Park J.Y., Viall A.K., Minnich S.S., Rohde H.N., Schnider D.R., Lim S.Y., Hong J.B., Hinnebusch B.J., O’Loughlin J.L., Deobald C.F., Bohach G.A., Hovde C.J., Minnichb S.A. Role of a new intimin/invasin-like protein in Yersinia pestis virulence. Infect. Immun. 2012; 80(10):3559–69. DOI:10.1128/ IAI.00294-12.Touchman J.W., Wagner D.M., Hao J., Mastrian S.D., Shah M.K., Vogler A.J., Allender C.J., Clark E.A., Benitez D.S., Youngkin D.J., Girard D.J., Auerbach R.K., Beckstrom-Sternberg S.M., Keim P. A North American Yersinia pestis draft genome sequence: SNPs and phylogenetic analysis. PLoS One. 2007; 2(2):e220. DOI: 10.1371/ journal.pone.0000220.Touchman J.W., Wagner D.M., Hao J., Mastrian S.D., Shah M.K., Vogler A.J., Allender C.J., Clark E.A., Benitez D.S., Youngkin D.J., Girard D.J., Auerbach R.K., Beckstrom-Sternberg S.M., Keim P. A North American Yersinia pestis draft genome sequence: SNPs and phylogenetic analysis. PLoS One. 2007; 2(2):e220. DOI: 10.1371/ journal.pone.0000220.Tsang T.M., Annis D.S., Kronshage M., Fenno J.T., Usselman L.D., Mosher D.F., Krukonis E.S. Ail protein binds ninth type III fibronectin repeat (9FNIII) within central 120-kDa region of fibronectin to facilitate cell binding by Yersinia pestis. J. Biol. Chem. 2012; 287(20):16759–67. DOI: 10.1074/jbc.M112.358978.Tsang T.M., Annis D.S., Kronshage M., Fenno J.T., Usselman L.D., Mosher D.F., Krukonis E.S. Ail protein binds ninth type III fibronectin repeat (9FNIII) within central 120-kDa region of fibronectin to facilitate cell binding by Yersinia pestis. J. Biol. Chem. 2012; 287(20):16759–67. DOI: 10.1074/jbc.M112.358978.Tsang T.M. Wiese J.S., Felek S., Kronshage M., Krukonis E.S. Ail proteins of Yersinia pestis and Y. pseudotuberculosis have different cell binding and invasion activities. PLoS One. 2013; 8(12):e83621. DOI: 10.1371/journal.pone.0083621.Tsang T.M. Wiese J.S., Felek S., Kronshage M., Krukonis E.S. Ail proteins of Yersinia pestis and Y. pseudotuberculosis have different cell binding and invasion activities. PLoS One. 2013; 8(12):e83621. DOI: 10.1371/journal.pone.0083621.Tsai J.C., Yen M.R., Castillo R., Leyton D.L., Henderson I.R., Saier M.H. Jr. The bacterial intimins and invasins: a large and novel family of secreted proteins. PLoS One. 2010; 5(12):e14403. DOI: 10.1371/journal.pone.0014403.Tsai J.C., Yen M.R., Castillo R., Leyton D.L., Henderson I.R., Saier M.H. Jr. The bacterial intimins and invasins: a large and novel family of secreted proteins. PLoS One. 2010; 5(12):e14403. DOI: 10.1371/journal.pone.0014403.Uittenbogaard A.M., Myers-Morales T., Gorman A.A. Welsh E., Wulff C., Hinnebusch B.J., Korhonen T.K., Straley S.C. Temperature-dependence of yadBC phenotypes in Yersinia pestis. Microbiology 2014; 160(Pt.2):396–405. DOI: 10.1099/ mic.0.073205-0.Uittenbogaard A.M., Myers-Morales T., Gorman A.A. Welsh E., Wulff C., Hinnebusch B.J., Korhonen T.K., Straley S.C. Temperature-dependence of yadBC phenotypes in Yersinia pestis. Microbiology 2014; 160(Pt.2):396–405. DOI: 10.1099/ mic.0.073205-0.Yamashita S., Lukacik P., Barnard T.J., Noinaj N., Felek S., Tsang T.M., Krukonis E.S., Hinnebusch B.J., Buchanan S. Structural insights into Ail-mediated adhesion in Yersinia pestis. Structure. 2011; 19(11):1672–82. DOI: 10.1016/j.str.2011.08.010.Yamashita S., Lukacik P., Barnard T.J., Noinaj N., Felek S., Tsang T.M., Krukonis E.S., Hinnebusch B.J., Buchanan S. Structural insights into Ail-mediated adhesion in Yersinia pestis. Structure. 2011; 19(11):1672–82. DOI: 10.1016/j.str.2011.08.010.Yen Y.T., Karkal A., Bhattacharya M., Fernandez R.C., Stathopoulos C. Identification and characterization of autotransport- er proteins of Yersinia pestis KIM. Mol. Membr. Biol., 2007; 24(1): 28–40. DOI: 10.1080/09687860600927626.Yen Y.T., Karkal A., Bhattacharya M., Fernandez R.C., Stathopoulos C. Identification and characterization of autotransporter proteins of Yersinia pestis KIM. Mol. Membr. Biol., 2007; 24(1): 28–40. DOI: 10.1080/09687860600927626.Zav’yalov V.P. Fimbrial polyadhesins: anti-immune arma- ment of Yersinia. Adv. Exp. Med. Biol. 2012;.954:183–201. DOI: 10.1007/978-1-4614-3561-7_24.Zav’yalov V.P. Fimbrial polyadhesins: anti-immune armament of Yersinia. Adv. Exp. Med. Biol. 2012;.954:183–201. DOI: 10.1007/978-1-4614-3561-7_24.

The authors declare that there are no conflicts of interest present.