References

microbe

Проблемы особо опасных инфекций

Problems of Particularly Dangerous Infections

0370-10692658-719X

Russian Research Anti-Plague Institute “Microbe”

10.21055/0370-1069-2016-3-13-20

microbe-319

Research Article

ОБЗОРЫ

REVIEWS

Активатор плазминогена – многофункциональный белок возбудителя чумы

Plasminogen Activator – Multifunctional Protein of Plague Pathogen

Куклева

Л. М.

Kukleva

L. M.

Российская Федерация, 410005, Саратов, ул. Университетская, 46

46, Universitetskaya St., Saratov, 410005, Russian Federation

usrapi@microbe.ru

Бойко

А. В.

Boiko

A. V.

Российская Федерация, 410005, Саратов, ул. Университетская, 46

46, Universitetskaya St., Saratov, 410005, Russian Federation

ФКУЗ «Российский научно-исследовательский противочумный институт «Микроб»РоссияRussian Research Anti-Plague Institute “Microbe”Russian Federation

2016

20092016

031320

2016

Куклева Л.М., Бойко А.В.

Kukleva L.M., Boiko A.V.

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/319

Активатор плазминогена Yersinia pestis – поверхностная протеаза (Pla) кодируется видоспецифической плазмидой pPla. Этот фермент принадлежит к семейству белков омптинов и имеет β-баррельную структуру. Протеаза Pla осуществляет комплексное взаимодействие с системой гомеостаза организма хозяина и является важным фактором вирулентности возбудителя чумы. Представлены литературные данные об участии активатора плазминогена в развитии бубонной и легочной форм чумы. Описано участие R-формы ЛПС в проявлении активности протеазы Pla. Активатор плазминогена непосредственно способствует фибринолизу, активируя плазминоген, инактивируя ингибитор активатора плазминогена-1 (PAI-1) и α2-антиплазмин, а также активируемый тромбином ингибитор фибринолиза (TAFI). Прокоагулянтная активность белка Pla обусловлена разрушением ингибитора каскада тканевого фактора (TFPI). Представлены данные о непротеолитических функциях активатора плазминогена.

Yersinia pestis plasminogen activator, a surface protease (Pla) is encoded by species-specific plasmid pPla. This enzyme belongs to outer membrane protein family and has a ß-barrel structure. Pla protease interacts complexly with homeostasis system of a hostorganism and is an important factor of plague agent virulence. Represented are the literature data on the part of plasminogen activator in the development of bubonic and pneumonic plague. Described is the role of R-form lipopolysaccharide in protease Pla activity manifestation. Plasminogen activator directly contributes to fibrinolysis by activating plasminogen and inactivating plasminogen-1 activator inhibitor (PAI-1) and ά2-anti-plasmin, as well as promoted by thrombin fibrinolysis inhibitor (TAFI). Pro-coagulant Pla protein activity is caused by the destruction of tissue factor pathway inhibitor (TFPI). In addition, given is the information on non-proteolytic functions of plasminogen activator.

возбудитель чумыактиватор плазминогенапатогенность

plague agentplasminogen activatorpathogenicity

References1

Дентовская С.В., Платонов М.Е., Бахтеева И.В., Анисимов А.П. Наличие полной структуры кора липополисахарида необходимо для активации плазминогена возбудителем чумы. Пробл. особо опасных инф. 2007; 1(93):49–51.

Dentovskaya S.V., Platonov M.E., Bakhteyeva I.V., Anissimov A.P. [The presence of the complete lipopolysaccharide core structure is necessary for the activation of Yersinia pestis plasminogen]. Probl. Osobo Opasn. Infek. 2007; 1:49–51.

Ерошенко Г.А., Одиноков Г.Н., Анисимова Л.В., Шавина Н.Ю., Виноградова Н.А., Кутырев В.В. Антибиотикоустойчивые штаммы возбудителя чумы и разработка способа их детекции методом полимеразной цепной реакции. Пробл. особо опасных инф. 2011; 1(107):53–7.

Eroshenko G.A., Odinokov G.N., Anisimova L.V., Shavina N.Yu., Vinogradova N.A., Kutyrev V.V. [Antibiotic-resistant strains of plague agent and development of procedure for their detection by PCR method]. Probl. Osobo Opasn. Infek. 2011; 1:53– 7.

Beesley E., Brubaker R., Janssen W., Surgalla M. Pesticins. III. Expression of coagulase and mechanisms of fibrinolysis. J. Bacteriol. 1967; 94(1):19–26.

Benedek O., Nagy G., Emody L. Intracellular signalling and cytoskeletal rearrangement involved in Yersinia pestis plasminogen activator (Pla) mediated HeLa cell invasion. Microb. Pathog. 2004; 37(1):47–54. DOI: 10.1016/j.micpath.2004.04.001.

Bertherat E. Plague in Madagascar: overview of the 2014–2015 epidemic season. WHO. Weekly Epidemiol. Rec. 2015; 90(20):250–2

Bishop J., Finlay B. Friend or foe? Antimicrobial peptides trigger pathogen virulence. Trends Mol. Med. 2006; 12(1):3–6. DOI: 10.1016/j.molmed.2005.11.001.

Butler Т. Plague gives surprises in the first decade of the 21st century in the United States and worldwide. Am. J. Trop. Med. Hyg. 2013; 89(4):788–93. DOI: 10.4269/ajtmh.13-0191.

Butler Т. Plague gives surprises in the first decade of the 21st century in the United States and worldwide. Am. J. Trop. Med. Hyg. 2013; 89(4):788– 93. DOI: 10.4269/ajtmh.13-0191.

Caulfield A., Lathem W. Substrates of the plasminogen activator protease of Yersinia pestis. Adv. Exp. Med. Biol. 2012; 954:253– 60. DOI: 10.1007/978-1-4614-3561-7_32.

Caulfield A., Lathem W. Substrates of the plasminogen activator protease of Yersinia pestis. Adv. Exp. Med. Biol. 2012; 954:253–60. DOI: 10.1007/978-1-4614-3561-7_32.

Chromy B., Choi M., Murphy G., Gonzales A., Corzett C., Chang B., Fitch J., McCutchen-Maloney S. Proteomic characterization of Yersinia pestis virulence. J. Bacteriol. 2005; 187(23):8172–80. DOI: 10.1128/JB.187.23.8172-8180.2005.

Cowan C., Jones H., Kaya Y., Perry R., Straley S. Invasion of epithelial cells by Yersinia pestis: evidence for a Y. pestis-specific invasion. Infect. Immun. 2000; 68(8):4523–30. DOI: 10.1128/IAI.68.8.4523-4530.2000.

Degen J., Bugge T., Goguen J. Fibrin and fibrinolysis in infection and host defense. J. Thromb. Haemost. 2007; 5(Suppl 1):24–31. DOI: 10.1111/j.1538-7836.2007.02519.x.

Eren E., van den Berg B. Structural basis for activation of an integral membrane protease by lipopolysaccharide. J. Biol. Chem. 2012; 287(28):23971–6. DOI: 10.1074/jbc.M112.376418.

Felek S., Tsang T., Krukonis E. 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.

Galvan E., Lasaro M., Schifferli D. Capsular antigen fraction 1 and Pla modulate the susceptibility of Yersinia pestis to pulmonary antimicrobial peptides such as cathelicidin. Infect. Immun. 2008; 76(4):1456–64. DOI: 10.1128/IAI.01197-07.

Haiko J., Suomalainen M., Ojala T., Lahteenmaki K., Korhonen T. Breaking barriers – attack on innate immune defences by omptin surface proteases of enterobacterial pathogens. Innate Immun. 2009; 15(2):67–80. DOI: 10.1177/1753425909102559.

Haiko J, Laakkonen L., Juuti K., Kalkkinen N., Korhonen T. The omptins of Yersinia pestis and Salmonella enterica cleave the reactive center loop of plasminogen activator inhibitor 1. J. Bacteriol. 2010; 192(18):4553–61. DOI: 10.1128/JB.00458-10.

Hritonenko V., Stathopoulos C. Omptin proteins: an expanding family of outer membrane proteases in Gram-negative Enterobacteriaceae. Mol. Membr. Biol. 2007; 24(5–6):395–406. DOI: 10.1080/09687680701443822.

Kienle Z., Emödy L., Svanborg C. and O´Toole P. Adhesive properties conferred by the plasminogen activator of Yersinia pestis. J. Gen. Microbiol. 1992; 138. Pt.8:1679–87.

Kim T., Chauhan S., Motin V., Goh E., Igo M., Young G. Direct transcriptional control of the plasminogen activator gene of Yersinia pestis by the cyclic AMP receptor protein. J. Bacteriol. 2007; 189(24):8890–900. DOI: 10.1128/JB.00972-07.

Knirel Y., Lindner B., Vinogradov E., Kocharova N., Senchenkova S., Shaikhutdinova R., Dentovskaya S., Fursova N., Bakhteeva I., Titareva G., Balakhonov S., Holst O., Gremyakova T., Pier G., Anisimov A. Temperature-dependent variations and intraspecies diversity of the structure of the lipopolysaccharide of Yersinia pestis. Biochemistry. 2005; 44(5):1731–43. DOI: 10.1021/bi048430f.

Knirel Y., Lindner B., Vinogradov E., Kocharova N., Senchenkova S., Shaikhutdinova R., Dentovskaya S., Fursova N., Bakhteeva I., Titareva G., Balakhonov S., Holst O., Gremyakova T., Pier G., Anisimov A. Temperaturedependent variations and intraspecies diversity of the structure of the lipopolysaccharide of Yersinia pestis. Biochemistry. 2005; 44(5):1731–43. DOI: 10.1021/bi048430f.

Korhonen T., Haiko J., Leakkonen L., Jarvinen H., Westerlund-Wikstrom B. Fibrinolytic and coagulative activities of Yersinia pestis. Front. Cell Infect. Microbiol. 2013; 3(35):1–9. DOI: 10.3389/fcimb.2013.00035.

Korhonen T. Fibrinolytic and procoagulant activities of Yersinia pestis and Salmonella enteric. J. Thromb. Haemost. 2015; 13(1):115–20. DOI: 10.1111/jth.12932.

Kukkonen M., Lahteenmaki K., Suomalainen M., Kalkkinen N., Emödy L., Lång H., Korhonen T. Protein regions important for plasminogen activation and inactivation of alpha2-antiplasmin in the surface protease Pla of Yersinia pestis. Mol. Microbiol. 2001; 40(5):1097–111. DOI: 10.1046/j.1365-2958.2001.02451.x.

Kukkonen M., Korhonen T. The omptin family of enterobacterial surface proteases/adhesins: from housekeeping in Escherichia coli to systemic spread of Yersinia pestis. Int. J. Med. Microbiol. 2004; 294(1):7–14. DOI: 10.1016/j.ijmm.2004.01.003.

Kukkonen M., Suomalainen M., Kyllonen P., Lähteenmäki K., Lång H., Virkola R., Helander I., Holst O., Korhonen T. Lack of O-antigen is essential for plasminogen activation by Yersinia pestis and Salmonella enterica. Mol. Microbiol. 2004; 51(1):215–25. DOI: 10.1046/j.1365-2958.2003.03817.x.

Lahteenmaki K., Edelman S., Korhonen T. Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol. 2005; 13(2):79–85. DOI: 10.1016/j.tim.2004.12.003.

Lathem W., Price P., Miller V., Goldman W. A plasminogenactivating protease specifically controls the development of primary pneumonic plague. Science. 2007; 315(5811):509–13. DOI: 10.1126/science.1137195.

Lathem W., Price P., Miller V., Goldman W. A plasminogen-activating protease specifically controls the development of primary pneumonic plague. Science. 2007; 315(5811):509–13. DOI: 10.1126/science.1137195.

Lawrenz M., Pennington J., Miller V. 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., Pennington J., Miller V. 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.

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. 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.

Myohanen H., Vaheri A. Regulation and interactions in the activation of cell-associated plasminogen. Cell Mol. Life Sci. 2004; 61(22):2840–58. DOI: 10.1007/s00018-004-4230-9.

Myohanen H., Vaheri A. Regulation and interactions in the activation of cell- associated plasminogen. Cell Mol. Life Sci. 2004; 61(22):2840–58. DOI: 10.1007/s00018-004-4230-9.

Perry R.D., Fetherston J.D. Yersinia pestis – etiological agent of plague. Clin. Microbiol. Rev. 1997; 10(1):35–66.

Plano G., Schesser K. The Yersinia pestis type III secretion system: expression, assembly and role in the evasion of host defenses. Immunol. Res. 2013; 57(1–3):237–45. DOI: 10.1007/s12026-013-8454-3.

Renckens R., Roelofs J., Bonta P., Florquin S., de Vries C., Levi M., Carmeliet P., van’t Veer C., van der Poll T. Plasminogen activator inhibitor type 1 is protective during severe Gram- negative pneumonia. Blood. 2007; 109(4):1593–601. DOI: 10.1182/blood-2006-05-025197.

Renckens R., Roelofs J., Bonta P., Florquin S., de Vries C., Levi M., Carmeliet P., van’t Veer C., van der Poll T. Plasminogen activator inhibitor type 1 is protective during severe Gram-negative pneumonia. Blood. 2007; 109(4):1593–601. DOI: 10.1182/blood-2006-05-025197.

Sebbane F., Jarrett C., Gardner D., Long D., Hinnebusch B. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea- borne plague. Proc. Natl. Acad. Sci. USA. 2006; 103(14):5526–30. DOI: 10.1073/pnas.0509544103.

Sebbane F., Jarrett C., Gardner D., Long D., Hinnebusch B. Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc. Natl. Acad. Sci. USA. 2006; 103(14):5526–30. DOI: 10.1073/pnas.0509544103.

Sebbane F., Lemaite N., Sturdevant D., Rebeil R., Virtaneva K., Porcella S., Hinnebusch B. Adaptive response of Yersinia pestis to extracellular effectors of innate immunity during bubonic plague. Proc. Natl. Acad. Sci. USA. 2006; 103(31):11766–71. DOI: 10.1073/pnas.0601182103.

Schaller J., Gerber S. The plasmin–antiplasmin system: structural and functional aspects. Cell. Mol. Life Sci. 2011; 68(5):785– 801. DOI: 10.1007/s00018-010-0566-5.

Schaller J., Gerber S. The plasmin–antiplasmin system: structural and functional aspects. Cell. Mol. Life Sci. 2011; 68(5):785–801. DOI: 10.1007/s00018-010-0566-5.

Sodeinde O., Goguen J. Genetic analysis of the 9.5-kilobase virulence plasmid of Yersinia pestis. Infect. Immun. 1988; 56(10):2743–8.

Sodeinde O., Sample A., Brubaker R., Goguen J. Plasminogen activator/coagulase gene of Yersinia pestis is responsible for degradation of plasmid-encoded outer membrane proteins. Infect. Immun. 1988; 56(10):2749–52.

Sodeinde O., Goguen J. Nucleotide sequence of the plasminogen activator gene of Yersinia pestis: relationship to ompT of E. coli and gene E of Salmonella typhimurium. Infect. Immun. 1989; 57(5):1517–23.

Sodeinde O.A., Subrahmanyam Y.V., Stark K., Quan T., Bao Y., Goguen J.D. A surface protease and the invasive character of plague. Science. 1992; 258(5084):1004–7. DOI: 10.1126/science.1439793.

Stenseth N.C., Atshabar B.B., Begon M., Belmain S.R., Bertherat E., Carniel E., Gage K., Leirs H., Rahalison L. Plague: past, present, and future. PLoS Med. 2008; 5(1):e3. DOI: 10.1371/journal.pmed.0050003.

Suomalainen M., Lobo L., Brandenburg K., Lindner B., Virkola R., Knirel Y., Anisimov A., Holst O., Korhonen T. Temperature-induced changes in the lipopolysaccharide of Yersinia pestis affect plasminogen activation by the Pla surface protease. Infect. Immun. 2010; 78(6):2644–52. DOI: 10.1128/IAI.01329-09.

Titball R., Oyston P. A plague upon fibrin. Nat. Med. 2007; 13(3):253–4. DOI: 10.1038/nm0307-253.

Valls Serón M., Haiko J., de Groot P., Korhonen T., Meijers J. Thrombin-activatable fibrinolysis inhibitor is degraded by Salmonella enterica and Yersinia pestis. J. Thromb. Haemost. 2010; 8(10):2232–40. DOI: 10.1111/j.1538-7836.2010.04014.x.

Valls Serón M., Haiko J., de Groot P., Korhonen T., Meijers J. Thrombin- activatable fibrinolysis inhibitor is degraded by Salmonella enterica and Yersinia pestis. J. Thromb. Haemost. 2010; 8(10):2232–40. DOI: 10.1111/j.1538-7836.2010.04014.x.

Vandeputte-Rutten L., Kramer R., Kroon J., Dekker N., Egmond M., Gros P. Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J. 2001; 20(18):5033–9. DOI: 10.1093/emboj/20.18.5033.

Vollmer W., Pilsl H., Hantke K., Höltje J., Braun V. Pesticin displays muramidase activity. J. Bacteriol. 1997; 179(5):1580–3.

Welch T., Fricke W., McDermott P., White D., Rosso M., Rasko D., Mammel M., Eppinger M., Rosovitz M., Wagner D., Rahalison L., Leclerc J., Hinshaw J., Lindler L., Cebula T., Carniel E., Ravel J. Multiple antimicrobial resistance in plague: an emerging public health risk. PLoS One. 2007; 2(3):e309. DOI: 10.1371/journal.pone.0000309.

Welkos S., Friedlander A., Davis K. Studies on the role of plasminogen activator in systemic infection by virulent Yersinia pestis strain C092. Microb. Pathog. 1997; 23(4):211– 23. DOI: 10.1006/mpat.1997.0154.

Yun T., Cott J., Tapping R., Slauch J., Morrissey J. Proteolytic inactivation of tissue factor pathway inhibitor by bacterial omptins. Blood. 2009; 113(5):1139–48. DOI: 10.1182/blood-2008-05-157180.

Zhang S., Park C., Zhang P., Bartra S., Plano G., Klena J., Skurnik M., Hinnebusch J., Chen T. Plasminogen activator Pla of Yersinia pestis utilizes murine DEC-205 (CD205) as a receptor to promote dissemination. J. Biol. Chem. 2008; 283(46):31511–21. DOI: 10.1074/jbc.M804646200.

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