СОВРЕМЕННЫЕ ПРЕДСТАВЛЕНИЯ О МОЛЕКУЛЯРНЫХ МЕХАНИЗМАХ ПАТОГЕНЕЗА ЧУМЫ

СтатьяПРОБ ОСОБ ОПАС ИНФ. 2017; № 3: 33–40. DOI:10.21055/0370-1069-2017-3-33-40

Подладчикова О.Н.^[1]

^[1]Ростовский-на-Дону научно-исследовательский противочумный институт Роспотребнадзора

В обзоре проведен краткий анализ опубликованных за последние десять лет результатов исследований, посвященных изучению молекулярных механизмов действия известных на сегодняшний день факторов вирулентности возбудителя чумы Yersinia pestis. Проанализированы разные компоненты Y. pestis, синтезирующиеся бактериями на четырех этапах инфекционного процесса при бубонной форме чумы: в коже, лимфоузлах, паренхиматозных органах и крови. Описаны факторы и механизмы, которые лежат в основе защиты микробов от бактерицидного действия гуморальных и клеточных факторов врожденного иммунитета хозяина, которые по-разному воздействуют на организм животных, стимулируя проили противовоспалительную реакцию хозяина на инфекцию, и способствуют смене жизненного цикла бактерий внутри хозяина, обеспечивая переход от внутриклеточного размножения в фагоцитах на первых этапах инфекции к внеклеточному размножению в лимфоузле, селезенке, печени и крови на последующих. В обзоре рассматриваются только те факторы Y. pestis, взаимодействие которых с молекулами и клетками хозяина на разных этапах инфекционного процесса экспериментально доказано.

возбудитель чумы

Yersinia pestis

инфекционный процесс при бубонной чуме

факторы вирулентности

механизмы действия факторов вирулентности

Siphonaptera

Бактерии

Вирулентность

Жизни цикла стадии

Кожа

Комплемент

Кровь

Липопротеины

Макрофаги

Микробиота

Нейтрофилы

Обзор

Особо опасные инфекции

Пептид-гидролазы

Печень

Репродукция

Селезенка

Фагоцитоз

Цитокины

Чума

Юбилеи и другие важные события

Тынянова В.И., Зюзина В.П., Демидова Г.В., Соколова Е.П. Специфичность иммуномодулирующего действия эндотоксина. Yersinia pestis. Журн. микробиол., эпидемиол. и иммунобиол. 2016; 3:104–12.

Abramov V.M., Khlebnikov V.S., Vasiliev A.M., Kosarev I.V., Vasilenko R.N., Kulikova N.L., Khodyakova A.V., Evstigneev V.I., Uversky V.N., Motin V.L., Smirnov G.B., Brubaker R.R. Attachment of LcrV from Yersinia pestis at dual binding sites to human TLR-2 and human IFN-gamma receptor. J. Proteome Res. 2007; 6:2222–31.

Bartra S.S., Gong X., Lorica C.D., Jain C., Nair M.K., Schifferli D., Qian L., Li Z., Plano G.V., Schesser K. The outer membrane protein A (OmpA) of Yersinia pestis promotes intracellular survival and virulence in mice. Microb. Pathog. 2012; 52(1):41–6. DOI: 10.1016/j.micpath.2011.09.009..
DOI: 10.1016/j.micpath.2011.09.009

Bergsbaken T., Cookson B.T. Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog. 2007; 3(11):e161.

Bobrov A.G., Kirillina O., Fetherston J.D., Miller M.C., Burlison J.A., Perry R.D. The Yersinia pestis siderophore, yersiniabactin, and the ZnuABC system both contribute to zinc acquisition and the development of lethal septicemic plague in mice. Mol. Microbiol. 2014; 93:759–75. DOI: 10.1111/mmi.12693..
DOI: 10.1111/mmi.12693

Chaturvedi K.S., Hung C.S., Crowley J.R., Stapleton A.E., Henderson J.P. The siderophore yersiniabactin binds copper to protect pathogens during infection. Nat. Chem. Biol. 2012; 8:731–6. DOI: 10.1038/nchembio..
DOI: 10.1038/nchembio

Chaturvedi K.S., Hung C.S., Giblin D.E., Urushidani S., Austin A.M., Dinauer M.C., Henderson J.P. Cupric yersiniabactin is a virulence-associated superoxide dismutase mimic. ACS Chem. Biol. 2014; 9:551–6. DOI: 10.1021/cb400658k..
DOI: 10.1021/cb400658k

Chouikha I., Hinnebusch B.J. Yersinia-flea interactions and the evolution of the arthropod-borne transmission route of plague. Curr. Opin. Microbiol. 2012; 15(3):239–46. DOI: 10.1016/j.mib.2012.02.003..
DOI: 10.1016/j.mib.2012.02.003

Eren E., van den Berg B. Structural basis for activation of an integral membrane protease by lipopolysaccharide. J. Biol. Chem. 2012; 287(28):23971–76. DOI: 10.1074/jbc.M112.376418..
DOI: 10.1074/jbc.M112.376418

Felek S., Lawrenz M.B., Krukonis E.S. The Yersinia pestis autotransporter YapC mediates host cell binding, autoaggregation and biofilm formation. Microbiology. 2008; 154(6):1802–12. DOI: 10.1099/mic.0.2007/010918-0..
DOI: 10.1099/mic.0.2007/010918-0

Galindo C.L., Sha J., Moen S.T., Agar S.L., Kirtley M.L., Foltz S.M., McIver L.J., Kozlova E.V., Garner H.R., Chopra A.K. Comparative global gene expression profiles of wild-type Yersinia pestis CO92 and its braun lipoprotein mutant at flea and human body temperatures. Comp. Funct. Genomics. 2010; 342168. DOI:10.1155/2010/342168..
DOI: 10.1155/2010/342168

Gonzalez R.J., Miller V.L. A Deadly path: bacterial spread during bubonic plague. Trends Microbiol. 2016; 24(4):239–41. DOI:10.1016/j.tim.2016.01.010..
DOI: 10.1016/j.tim.2016.01.010

Gonzalez R.J., Lane M.C., Wagner N.J., Weening E.H., Miller V.L. Dissemination of a highly virulent pathogen: tracking the early events that define infection. PLoS Pathog. 2015; 11(1):e1004587. DOI: 10.1371/journal.ppat.1004587. eCollection2015..
DOI: 10.1371/journal.ppat.1004587. eCollection2015

Gonzalez R.J., Lane M.C., Wagner N.J., Weening E.H., Miller V.L. Dissemination of a highly virulent pathogen: tracking the early events that define infection. PLoS Pathog. 2015; 11(1):e1004587. DOI: 10.1371/journal.ppat.1004587. eCollection2015..
DOI: 10.1371/journal.ppat.1004587. eCollection 2015

Hatkoff M., Runco L.M., Pujol C., Jayatilaka I., Furie M.B., Bliska J.B., Thanassi D.G. Roles of chaperone/usher pathways of Yersinia pestis in a murine model of plague and adhesion to host cells. Infect. Immun. 2012; 80(10):3490–500. DOI: 10.1128/IAI.00434-12..
DOI: 10.1128/IAI.00434-12

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..
DOI: 10.1128/IAI.05307-11

Höfling S., Grabowski B., Norkowski S., Schmidt M.A., Rüter C. Current activities of the Yersinia effector protein YopM. Int. J. Med. Microbiol. 2015; 305(3):424–32. DOI: 10.1016/j.ijmm.2015.03.009..
DOI: 10.1016/j.ijmm.2015.03.009

Houppert A.S., Bohman L., Merritt P.M., Cole C.B., Caulfield A.J., Lathem W.W., Marketon M.M. RfaL is required for Yersinia pestis type III secretion and virulence. Infect. Immun. 2013; 81(4):1186–97. DOI: 10.1128/IAI.01417-12..
DOI: 10.1128/IAI.01417-12

Ke Y., Chen Z., Yang R. Yersinia pestis: mechanisms of entry into and resistance to the host cell. Front. Cell. Infect. Microbiol. 2013; 3:106. DOI: 10.3389/fcimb.2013.00106. eCollection 2013..
DOI: 10.3389/fcimb.2013.00106. eCollection 2013

Klein K.A., Fukuto H.S., Pelletier M., Romanov G., Grabenstein J.P., Palmer L.E., Ernst R., Bliska J.B. A transposon site hybridization screen identifies galU and wecBC as important for survival of Yersinia pestis in murine macrophages. J. Bacteriol. 2012; 194(3):653–62. DOI: 10.1128/JB.06237-11..
DOI: 10.1128/JB.06237-11

Knirel Y.A., Anisimov A.P. Lipopolysaccharide of Yersinia pestis, the cause of plague: structure, genetics, biological properties. Acta Naturae. 2012; 4:46–58.

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. DOI: 10.3389/fcimb.2012.00103. eCollection 2012..
DOI: 10.3389/fcimb.2012.00103. eCollection 2012

Korhonen T.K., Haiko J., Laakkonen L., Jarvinen H.M., Westerlund-Wikstrom B. Fibrinolytic and coagulative activities of Yersinia pestis. Front. Cell. Infect. Microbiol. 2013; 3:35. DOI: 10.3389/fcimb.2013.00035. eCollection 2013..
DOI: 10.3389/fcimb.2013.00035. eCollection 2013

LaRock C.N., Cookson B.T. The Yersinia virulence effector YopM binds caspase-1 to arrest inflammasome assembly and processing. Cell Host Microbe. 2012; 12(6):799–805. DOI: 10.1016/j.chom.2012.10.020..
DOI: 10.1016/j.chom.2012.10.020

Lawrenz M.B., Lenz J.D., Miller V.L. A novel autotrans-porter adhesin is required for efficient colonization during bubonic plague. Infect. Immun. 2009; 77(1):317–26. DOI: 10.1128/IAI.01206-08..
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..
DOI: 10.1111/mmi.12273

Merritt P.M., Nero T., Bohman L., Felek S., Krukonis E.S., Marketon M.M. Yersinia pestis targets neutrophils via complement receptor 3. Cell. Microbiol. 2015; 17(5):666–87. DOI: 10.1111/cmi.12391..
DOI: 10.1111/cmi.12391

Mikula K.M., Kolodziejczyk R., Goldman A. Yersinia infection tools – characterization of structure and function of adhesins. Front. Cell. Infect. Microbiol. 2013; 2:169. DOI: 10.3389/fcimb.2012.00169. eCollection 2012..
DOI: 10.3389/fcimb.2012.00169. eCollection 2012

Nham T., Filali S., Danne C., Derbise A., Carniel E. Imaging of bubonic plague dynamics by in vivo tracking of bioluminescent Yersinia pestis. PLoS ONE. 2012; 7(4):e34714. DOI: 10.1371/journal.pone.0034714..
DOI: 10.1371/journal.pone.0034714

O’Loughlin J.L., Spinner J.L., Minnich S.A., Kobayashi S.D. Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect. Immun. 2010; 78(2):773–82. DOI: 10.1128/IAI.00718-09..
DOI: 10.1128/IAI.00718-09

Paauw A., Leverstein-van Hall M.A., van Kessel K.P.M., Verhoef J., Fluit A.C. Yersiniabactin reduces the respiratory oxidative stress response of innate immune cells. PLoS ONE. 2009; 4(12):e8240. DOI: 10.1371/journal.pone.0008240..
DOI: 10.1371/journal.pone.0008240

Perry R., Fetherston J. Yersiniabactin iron uptake: mechanisms and role in Yersinia pestis pathogenesis. Microbes Infect. 2011; 13(10):808–17. DOI: 10.1016/j.micinf.2011.04.008..
DOI: 10.1016/j.micinf.2011.04.008

Pha K., Navarro L. Yersinia type III effectors perturb host innate immune responses. World J. Biol. Chem. 2016; 7(1):1–13. DOI: 10.4331/wjbc.v7.i1.1..
DOI: 10.4331/wjbc.v7.i1.1

Plano G.V., 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..
DOI: 10.1007/s12026-013-8454-3

Pujol C., Klein K.A., Romanov G.A., Palmer L.E., Cirota C., Zhao Z., Bliska J.B. Yersinia pestis can reside in autophagosomes and avoid xenophagy in murine macrophages by preventing vacuole acidification. Infect. Immun. 2009; 77(6):2251–61. DOI: 10.1128/IAI.00068-09..
DOI: 10.1128/IAI.00068-09

Ratner D., Orning M.P., Starheim K.K., Marty-Roix R., Proulx M.K., Goguen J.D., Lien E. Manipulation of interleukin-1β and interleukin-18 production by Yersinia pestis effectors YopJ and YopM and redundant impact on virulence. J. Biol. Chem. 2016; 291(19):9894–905. DOI: 10.1074/jbc.M115.697698..
DOI: 10.1074/jbc.M115.697698

Sebbane F., Jarrett C., Gardner D., Long D., Hinnebusch B.J. The Yersinia pestis caf1M1A1 fimbrial capsule operon promotes transmission by flea bite in a mouse model of bubonic plague. Infect.Immun. 2009; 77 (3):1222–29. DOI: 10.1128/IAI.00950-08..
DOI: 10.1128/IAI.00950-08

Sha J., Kirtley M.L., van Lier C.J., Wang S., Erova T.E., Kozlova E.V., Cao A., Cong Y., Fitts E.C., Rosenzweig J.A., Chopra A.K. Deletion of the Braun lipoprotein-encoding gene and altering the function of lipopolysaccharide attenuate the plague bacterium. Infect. Immun. 2013; 81(3):815–28. DOI:10.1128/IAI.01067-12..
DOI: 10.1128/IAI.01067-12

Shannon J.G., Bosio C.F., Hinnebusch B.J. Dermal neutrophil, macrophage and dendritic cell responses to Yersinia pestis transmitted by fleas. PLoS Pathog. 2015; 11(3):e1004734. DOI: 10.1371/journal.ppat.1004734..
DOI: 10.1371/journal.ppat.1004734

Shannon J.G., Hasenkrug A.M., Dorward D.W., Nair V., Carmody A.B., Hinnebusch B.J. Yersinia pestis subverts the dermal neutrophil response in a mouse model of bubonic plague. mBio. 2013; 4(5):e00170–13. DOI: 10.1128/mBio.00170-13..
DOI: 10.1128/mBio.00170-13

Spinner J.L., Winfree S., Starr T., Shannon J.G., Nair V., Steele-Mortimer O., Hinnebusch B.J. Yersinia pestis survival and replication within human neutrophil phagosomes and uptake of infected neutrophils by macrophages. J. Leukoc. Biol. 2014; 95(3):389–98. DOI: 10.1189/jlb.1112551..
DOI: 10.1189/jlb.1112551

Spinner J.L., Carmody A.B., Jarrett C.O., Hinnebusch B.J. Role of Yersinia pestis toxin complex family proteins in resistance to phagocytosis by polymorphonuclear leukocytes. Infect. Immun. 2013; 81(11):4041–52. DOI: 10.1128/IAI.00648-13..
DOI: 10.1128/IAI.00648-13

Spinner J.L., Hasenkrug A.M., Shannon J.G., Kobayashi S.D., Hinnebusch B.J. Role of the Yersinia YopJ protein in suppressing interleukin-8 secretion by human polymorphonuclear leukocytes. Microbes Infect. 2016; 18(1):21–9. DOI: 10.1016/j.micinf.2015.08.015..
DOI: 10.1016/j.micinf.2015.08.015

St John A.L., Ang W.X., Huang M.N., Kunder C.A., Chan E.W., Gunn M.D., Abraham S.N. S1P-Dependent trafficking of intracellular Yersinia pestis through lymph nodes establishes Buboes and systemic infection. Immunity. 2014; 41(3):440–50. DOI: 10.1016/j.immuni.2014.07.013..
DOI: 10.1016/j.immuni.2014.07.013

Torres R., Lan B., Latif Y., Chim N., Goulding C.W. Structu ral snapshots along the reaction pathway of Yersinia pestis RipA, a putative butyryl-CoA transferase. Acta Crystallogr. D. Biol. Crystallogr. 2014; 70(4):1074–85. DOI: 10.1107/S1399004714000911..
DOI: 10.1107/S1399004714000911

Tsang T.M., Felek S., Krukonis E.S. Ail binding to fibronectin facilitates Yersinia pestis binding to host cells and Yop delivery. Infect. Immun. 2010; 78(8):3358–68. DOI: 10.1128/IAI.00238-10..
DOI: 10.1128/IAI.00238-10

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. Microbioljgy. 2014; 160(2):396–405. DOI: 10.1099/mic.0.073205-0..
DOI: 10.1099/mic.0.073205-0

Vadyvaloo V., Jarrett C., Sturdevant D.E., Sebbane F., Hinnebusch B.J. Transit through the flea vector induces a pretransmission innate immunity resistance phenotype in Yersinia pestis. PLoS Pathog. 2010; 6(2):e1000783. DOI: 10.1371/journal.ppat.1000783..
DOI: 10.1371/journal.ppat.1000783

van Lier C.J., Sha J., Kirtley M.L., Cao A., Tiner B.L., Erova T.E., Cong Y., Kozlova E.V., Popov V.L., Baze W.B., Chopra A.K. Deletion of Braun lipoprotein and plasminogen-activating protease-encoding genes attenuates Yersinia pestis in mouse models of bubonic and pneumonic plague. Infect. Immun. 2014; 82(6):2485– 503. DOI: 10.1128/IAI.01595-13..
DOI: 10.1128/IAI.01595-13

van Lier C.J., Tiner B.L., Chauhan S., Motin V.L., Fitts E.C., Huante M.B., Endsley J.J., Ponnusamy D., Sha J., Chopra A.K. Further characterization of a highly attenuated Yersinia pestis CO92 mutant deleted for the genes encoding Braun lipoprotein and plasminogen activator protease in murine alveolar and primary human macrophages. Microb. Pathog. 2015; 80:27–38. DOI:10.1016/j.micpath.2015.02.005..
DOI: 10.1016/j.micpath.2015.02.005

Vetter S.M., Eisen R.J., Schotthoefer A.M., Montenieri J.A., Holmes J.L., Bobrov A.G., Bearden S.W., Perry R.D., Gage K.L. Biofilm formation is not required for early-phase transmission of Yersinia pestis. Microbiology. 2010; 56(7):2216–25. DOI: 10.1099/mic.0.037952-0..
DOI: 10.1099/mic.0.037952-0

Ye Z., Gorm an A.A., Uittenbogaard A.M., Myers-Morales T., Kaplan A.M., Cohen D.A., Straley S.C. Caspase-3 mediates the pathogenic effect of Yersinia pestis YopM in liver of C57BL/6 mice and contributes to YopM’s function in spleen. PLoS ONE. 2014; 9(11):e110956. DOI: 10.1371/journal.pone.0110956. eCollection 2014..
DOI: 10.1371/journal.pone.0110956. eCollection 2014

Zhang S., Park C.G., Zhang P., Bartra S.S., Plano G.V., Klena J.D., Skurnik M., Hinnebusch B.J., Chen T. The 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..
DOI: 10.1074/jbc.M804646200

Язык текста: Русский

ISSN: 0370-1069