Yersinia pseudotuberculosis-derived adhesins

Cover Page


Cite item

Full Text

Abstract

Around fifteen surface components referred to adhesins have been identified in Yersinia pseudotuberculosis combining primarily microbiological, molecular and genetic, as well as immunochemical and biophysical methods. Y. pseudotuberculosis-derived adhesins vary in structure and chemical composition but they are mainly presented by protein molecules. Some of them were shown to participate not only in adhesive but in other pathogen-related physiological functions in the host-parasite interplay. Adhesins can mediate bacterial adhesion to eukaryotic cell either directly or via the extracellular matrix components. These adhesion molecules are encoded by chromosomal DNA excepting YadA protein which gene is located in the calcium-dependence plasmid pYV common for pathogenic yersisniae. An optimum temperature for adhesin biosynthesis is located close to the body temperature of warm-blooded animals; however, at low temperature only invasin InvA, full-length smooth lipopolysaccharide and porin OmpF are produced in Y. pseudotuberculosis. Several adhesins (Psa, InvA) can be expressed at low pH (corresponds to intracellular content), thereby defining pathogenic yersiniae as facultative intracellular parasites. Three human Yersinia genus pathogens differ by ability to produce adhesins. Y. pseudotuberculosis adherence to host cells or extracellular matrix components is determined by a cumulative adhesion-based activity, which expression depends on chemical composition and physicochemical environmental conditions. It’s proposed that at the initial stage of infectious process adherence of Y. pseudotuberculosis to intestinal epithelium is mediated by InvA protein and “smooth” LPS form. These adhesins are produced in bacterial cells at low (lower than 30°С) temperature occurring in environment from which a pathogen invades into the host. At later stages of pathogenesis, after penetrating through intestinal epithelium, bacterial cells produce other adhesins, which promote survival and dissemination primarily into the mesenteric lymph nodes and, possibly, liver and spleen. At later stages of pathogenesis, after penetrating through intestinal epithelium, bacterial cells produce other adhesins, which promote survival and dissemination primarily into the mesenteric lymph nodes and, perhaps, liver and spleen. Qualitative and quantitative spectrum of Y. pseudotuberculosis adhesins is determined by environmental parameters (intercellular space, intracellular content within the diverse eukaryotic cells).

About the authors

A. A. Byvalov

Institute of Physiology of the Komi Science Center, Ural Branch of the RAS, Vyatka State University

Author for correspondence.
Email: byvalov@nextmail.ru

PhD, MD (Medicine), Professor, Head of the Laboratory of Microbial Physiology, 

Kirov

Russian Federation

I. V. Konyshev

Institute of Physiology of the Komi Science Center, Ural Branch of the RAS, Vyatka State University

Email: konyshevil@yandex.ru

PhD (Biology), Junior Researcher, Laboratory of Microbial Physiology, 

Kirov

Russian Federation

References

  1. Бывалов А.А., Кононенко В.Л., Конышев И.В. Влияние О-боковых цепей липополисахарида на адгезивность Yersinia pseudotuberculosis к макрофагам J774, установленное методом оптической ловушки // Прикладная биохимия и микробиология. 2017. Т. 53, № 2. С. 234–243.
  2. Бывалов А.А., Кононенко В.Л., Конышев И.В. Исследование взаимодействия липополисахаридов Yersinia pseudotuberculosis с мембраной макрофага J774 методом силовой спектроскопии с использованием оптического пинцета // Биологические мембраны: Журнал мембранной и клеточной биологии. 2018. Т. 35, № 2. С. 115–130.
  3. Бывалов А.А., Конышев И.В., Новикова О.Д., Портнягина О.Ю., Белозеров В.С., Хоменко В.А., Давыдова В.Н. Адгезивность поринов OmpF и OmpC Yersinia pseudotuberculosis к макрофагам J774 // Биофизика. 2018. Т. 63, № 5. С. 913–922.
  4. Сомов Г.П., Покровский В.И., Беседнова Н.Н., Антоненко Ф.Ф. Псевдотуберкулез. М.: Медицина, 2001. 256 с.
  5. Чернядьев А.В., Бывалов А.А., Ананченко Б.А., Бушмелева Л.Г., Литвинец С.Г. Морфологические особенности бактерий Yersinia pseudotuberculosis, выращенных при различных температурных условиях // Известия Коми НЦ УрО РАН. 2012. Т. 3, № 11. С. 57–60.
  6. Artner D., Oblak A., Ittig S., Garate J.A., Horvat S., Arrieumerlou C., Hofinger A., Oostenbrink C., Jerala R., Kosma P., Zamyatina A. Conformationally constrained lipid A mimetics for exploration of structural basis of TLR4/MD-2 activation by lipopolysaccharide. ACS Chem. Biol., 2013, vol. 8, no. 11, pp. 2423–2432. doi: 10.1021/cb4003199
  7. Bao R., Nair M.K.M., Tang W.-K., Esser L., Sadhukhan A., Holland R.L., Xia D., Schifferli D.M. Structural basis for the specific recognition of dual receptors by the homopolymeric pH 6 antigen (Psa) fimbriae of Yersinia pestis. Proc. Natl. Acad. Sci. USA, 2013, vol. 110, no. 3, pp. 1065–1070. doi: 10.1073/pnas.1212431110
  8. Ben-Efraim S., Aronson M., Bichowsky-Slomnicki L. New antigenic component of Pasteurella pestis formed under specified conditions of pH and temperature. J. Bacteriol., 1961, vol. 81, no. 5, pp. 704–714.
  9. Berne C., Ducret A., Hardy G.G., Brun Y.V. Adhesins involved in attachment to abiotic surfaces by Gram-negative bacteria. Microbiol. Spectr., 2015, vol. 3, no. 4, pp. 1–45. doi: 10.1128/microbiolspec.MB-0018-2015
  10. Berne C., Ellison C.K., Ducret A., Brun Y.V. Bacterial adhesion at the single-cell level. Nat. Rev. Microbiol., 2018, pp. 1–12. doi: 10.1038/s41579-018-0057-5
  11. Biedzka-Sarek M., Venho R., Skurnik M. Role of YadA, Ail, and lipopolysaccharide in serum resistance of Yersinia enterocolitica serotype O:3. Infect. Immun., 2005, vol. 73, no. 4, pp. 2232–2244. doi: 10.1128/IAI.73.4.2232-2244.2005
  12. Chauhan N., Wrobel A., Skurnik M., Leo J.C. Yersinia adhesins: an arsenal for infection. Proteomics Clin. Appl., 2016, vol. 10, no. 9–10, pp. 949–963. doi: 10.1002/prca.201600012
  13. Chung L.K., Bliska J.B. Yersinia versus host immunity: how a pathogen evades or triggers a protective response. Curr. Opin. Microbiol., 2016, vol. 29, pp. 56–62. doi: 10.1016/j.mib.2015.11.001
  14. Clark M.A., Hirst B.H., Jepson M.A. M-cell surface beta1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer’s patch M-cells. Infect. Immun., 2005, vol. 6, pp. 1237–1243.
  15. Collyn F., Lety M.-A., Nair S., Escuyer V., Younes A.B., Simonet M., Marceau M. Yersinia pseudotuberculosis harbors a type IV pilus gene cluster that contributes to pathogenicity. Infect. Immun., 2002, vol. 70, no. 11, pp. 6196–6205. doi: 10.1128/IAI.70.11.6196-6205.2002
  16. Cozens D., Read R.C. Anti-adhesion methods as novel therapeutics for bacterial infections. Expert Rev. Anti Infect. Ther., 2012, vol. 10, no. 12, pp. 1457–1468. doi: 10.1586/eri.12.145
  17. Doyle R.J. Contribution of the hydrophobic effect to microbial infection. Microbes Infect., 2000, vol. 2, no. 4, pp. 391–400.
  18. Dube P. Interaction of Yersinia with the gut: mechanisms of pathogenesis and immune evasion. Curr. Top. Microbiol. Immunol., 2009, vol. 337, pp. 61–91. doi: 10.1007/978-3-642-01846-6_3
  19. El Tahir Y., Skurnik M. Yad A, the multifaceted Yersinia adhesin. Int. J. Med. Microbiol., 2001, vol. 291, pp. 209–218. doi: 10.1078/1438-4221-00119
  20. Felek S., Lawrenz M.B., Krukonis E.S. The Yersinia pestis autotransporter YapC mediates host cell binding, autoaggregation and biofilm formation. Microbiology, 2008, vol. 154, pp. 1802–1812. doi: 10.1099/mic.0.2007/010918-0
  21. 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, vol. 78, no. 10, pp. 4134–4150. doi: 10.1128/IAI.00167-10
  22. 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, vol. 76, no. 2, pp. 578–587. doi: 10.1128/IAI.00219-07
  23. Fredriksson-Ahomaa M., Joutsen S., Laukkanen-Ninios R. Identification of Yersinia at the species and subspecies levels is challenging. Curr. Clin. Microbiol. Rep., 2018, vol. 5, no. 2, pp. 135–142. doi: 10.1007/s40588-018-0088-8
  24. Galván 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, vol. 75, no. 3, pp. 1272–1279. doi: 10.1128/IAI.01153-06
  25. Haiko J., Westerlund-Wikström B. The role of the bacterial flagellum in adhesion and virulence. Biology (Basel), 2013, vol. 2, no. 4, pp. 1242–1267. doi: 10.3390/biology2041242
  26. Haji-Ghassemi O., Müller-Loennies S., Rodriguez T., Brade L., Kosma P., Brade H., Evans S.V. Structural basis for antibody recognition of lipid A: insights to polyspecificity toward single-stranded DNA. J. Biol. Chem., 2015, vol. 290, no. 32, pp. 19629– 19640. doi: 10.1074/jbc.M115.657874
  27. Heise T., Dersch P. Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrixspecific cell adhesion and uptake. Proc. Natl. Acad. Sci. USA, 2006. vol. 103, no. 9, 3375–3380. doi: 10.1073/pnas.0507749103
  28. Hoiczyk E., Roggenkamp A., Reichenbecher M., Lupas A., Heesemann J. Structure and sequence analysis of Yersinia YadA and Moraxella UspAs reveal a novel class of adhesins. EMBO J., 2000, vol. 19, no. 22, pp. 5989–5999. doi: 10.1093/emboj/19.22.5989
  29. Holtz O. Lipopolysaccharides of Yersinia. Adv. Exp. Med. Biol., 2003, vol. 529, pp. 219–228. doi: 10.1007/0-306-48416-1_43
  30. Huang X.Z., Lindler L.E. The pH 6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect. Immun., 2004, vol. 72, pp. 7212–7219. doi: 10.1128/IAI.72.12.7212-7219.2004
  31. Huber M., Kalis C., Keck S., Jiang Z., Georgel P., Du X., Shamel L., Sovath S., Mudd S., Beutler B., Galanos C., Freudenberg M.A. R-form LPS, the master key to the activation of TLR4/MD-2-positive cells. Eur. J. Immunol., 2006, vol. 36, no. 3, pp. 701–711. doi: 10.1002/eji.200535593
  32. Isberg R.R., Leong J.M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell, 1990, vol. 60, no. 5, pp. 861–871.
  33. Kim T.J., Young B.M., Young G.M. Effect of flagellar mutations on Yersinia enterocolitica biofilm formation. Appl. Environ. Microbiol., 2008, vol. 74, no. 17, pp. 5466–5474. doi: 10.1128/AEM.00222-08
  34. Klena J., Zhang P., Schwartz O., Hull S., Chen T. The core lipopolysaccharide of Escherichia coli is a ligand for the dendritic-cell-specific intercellular adhesion molecule nonintegrin CD209 receptor. J. Bacteriol., 2005, vol. 187, no. 5, pp. 1710–1715. doi: 10.1128/JB.187.5.1710-1715.2005
  35. Krachler A.-M., Ham H., Orth K. Outer membrane adhesion factor multivalent adhesion molecule 7 initiates host cell binding during infection by Gram-negative pathogens. Proc. Natl. Acad. Sci. USA, 2011, vol. 108, no. 28, pp. 11614–11619. doi: 10.1073/pnas.1102360108
  36. Krachler A.-M., Orth K. Functional characterization of the interaction between bacterial adhesin multivalent adhesion molecule 7 (MAM7) protein and its host cell ligands. J. Biol. Chem., 2007, vol. 286, no. 45, pp. 38939–38947. doi: 10.1074/jbc.M111.291377
  37. Lawrenz M.B., Lenz J.D., Miller V.L. A novel autotransporter adhesin is required for efficient colonization during bubonic plague. Infect. Immun., 2009, vol. 77, no. 1, pp. 317–326. doi: 10.1128/IAI.01206-08
  38. Leo J.C., Grin I., Linke D. Type V secretion: mechanism(s) of autotransport through the bacterial outer membrane. Phil. Trans. R. Soc. B, 2012, vol. 367, pp. 1088–1101. doi: 10.1098/rstb.2011.0208
  39. Leo J.C., Skurnik M. Adhesins of human pathogens from the genus Yersinia. Adv. Exp. Med. Biol., 2011, vol. 715, pp. 1–15. doi: 10.1007/978-94-007-0940-9_1
  40. Lu Q., Wang J., Faghihnejad A., Zeng H., Liu Y. Understanding the molecular interactions of lipopolysaccharides during E. coli initial adhesion with a surface forces apparatus. Soft Matter. 2011, vol. 7, no. 19, pp. 9366–9379. doi: 10.1039/C1SM05554B
  41. Mahmoud R.Y., Stones D.H., Li W., Emara M., El-Domany R.A., Wang D., Wang Y., Krachler A.M., Yu J. The multivalent adhesion molecule SSO1327 plays a key role in Shigella sonnei pathogenesis. Mol. Microbiol., 2016, vol. 99, no. 4, pp. 658–673. doi: 10.1111/mmi.13255
  42. Matsuura M., Kawasaki K., Kawahara K., Mitsuyama M. Evasion of human innate immunity without antagonizing TLR4 by mutant Salmonella enterica serovar typhimurium having penta-acylated lipid A. Innate Immun., 2012, vol. 18, no. 5, pp. 764–773. doi: 10.1177/1753425912440599
  43. Mikula K.M., Kolodziejczyk R., Goldman A. Yersinia infection tools — characterization of structure and function of adhesins. Front Cell Infect. Microbiol., 2012, vol. 2: 169. doi: 10.3389/fcimb.2012.00169
  44. Miller V.L., Falkow S. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect. Immun., 1988, vol. 56, no. 5, pp. 1242–1248.
  45. Muhlenkamp M., Oberhettinger P., Leo J.C., Linke D. Yersinia adhesin A (YadA) – beauty & beast. Int. J. Med. Microbiol., 2015, vol. 305, no. 2, pp. 252–258. doi: 10.1016/j.ijmm.2014.12.008
  46. Nair M.K., De Masi L., Yue M., Galván E.M., Chen H., Wang F., Schifferli D.M. Adhesive properties of YapV and paralogous autotransporter proteins of Yersinia pestis. Infect. Immun., 2015, vol. 83, no. 5, pp. 1809–1819. doi: 10.1128/IAI.00094-15
  47. Paharik A.E., Horswill A.R. The Staphylococcal biofilm: adhesins, regulation, and host response. Microbiol. Spectr., 2016, vol. 4, no. 2. doi: 10.1128/microbiolspec.VMBF-0022-2015
  48. Pakharukova N., Roy S., Tuittila M., Rahman M.M., Paavilainen S., Ingars A.K., Skaldin M., Lamminmäki U., Härd T., Teneberg S., Zavialov A.V. Structural basis for Myf and Psa fimbriae-mediated tropism of pathogenic strains of Yersinia for host tissues. Mol. Microbiol., 2016, vol. 102, no. 4, pp. 593–610. doi: 10.1111/mmi.13481
  49. Palumbo R.N., Wang C. Bacterial invasin: structure, function, and implication for targeted oral gene delivery. Curr. Drug Deliv., 2006, vol. 3, no. 1, pp. 47–53. doi: 10.2174/156720106775197475
  50. Patel S., Mathivanan N., Goyal A. Bacterial adhesins, the pathogenic weapons to trick host defense arsenal. Biomed. Pharmacother., 2017, vol. 93, pp. 763–771. doi: 10.1016/j.biopha.2017.06.102
  51. Payne D., Tatham D., Williamson E.D., Titball R.W. The pH 6 antigen of Yersinia pestis binds to beta1-linked galactosyl residues in glycosphingolipids. Infect. Immun., 1998, vol. 66, no. 9, pp. 4545–4548.
  52. Pierson D.E., Falkow S. The ail gene of Yersinia enterocolitica has a role in the ability of the organism to survive serum killing. Infect. Immun., 1993, vol. 61, no. 5, pp. 1846–1852.
  53. Pisano F., Kochut A., Uliczka F., Geyer R., Stolz T., Thiermann T., Rohde M., Dersch P. In vivo-induced InvA-like autotransporters Ifp and InvC of Yersinia pseudotuberculosis promote interactions with intestinal epithelial cells and contribute to virulence. Infect. Immun., 2012, vol. 80, no. 3, pp. 1050–1064. doi: 10.1128/IAI.05715-11
  54. Prokaryotes; vol. 2. Ed. Dworkin M. New York: Springer, 2006. 1107 p.
  55. Reis R.S., Horn F. Enteropathogenic Escherichia coli, Samonella, Shigella and Yersinia: cellular aspects of host-bacteria interactions in enteric diseases. Gut Pathog., 2010, vol. 2, no. 1: 8. doi: 10.1186/1757-4749-2-8
  56. Ren Y., Wang C., Chen Z., Allan E., van der Mei H.C., Busscher H.J. Emergent heterogeneous microenvironments in biofilms: substratum surface heterogeneity and bacterial adhesion force-sensing. FEMS Microbiol. Rev., 2018, vol. 42, no. 3, pp. 259–272. doi: 10.1093/femsre/fuy001
  57. Rossez Y., Wolfson E.B., Holmes A., Gally D.L., Holden N.J. Bacterial flagella: twist and stick, or dodge across the kingdoms. PLoS Pathog., 2015, vol. 11, no. 1: e1004483. doi: 10.1371/journal.ppat.1004483
  58. Sadana P., Geyer R., Pezoldt J., Helmsing S., Huehn J., Hust M., Dersch P., Scrima A. The invasin D protein from Yersinia pseudotuberculosis selectively binds the Fab region of host antibodies and affects colonization of the intestine. J. Biol. Chem., 2018, vol. 293, no. 22, pp. 8672–8690. doi: 10.1074/jbc.RA117.001068
  59. Sadana P., Mönnich M., Unverzagt C., Scrima A. Structure of the Y. pseudotuberculosis adhesin Invasin E. Protein Sci., 2017, vol. 26, no. 6, pp. 1182–1195. doi: 10.1002/pro.3171
  60. Schade J., Weidenmaier C. Cell wall glycopolymers of Firmicutes and their role as nonprotein adhesins. FEBS Letters, 2016, vol. 590, pp. 3758–3771. doi: 10.1002/1873-3468.12288
  61. Shoaf-Sweeney K.D., Hutkins R.W. Adherence, anti-adherence, and oligosaccharides preventing pathogens from sticking to the host. Adv. Food Nutr. Res., 2009, vol. 55, pp. 101–161. doi: 10.1016/S1043-4526(08)00402-6
  62. Skurnik M. Molecular genetics, biochemistry and biological role of Yersinia lipopolysaccharide. Adv. Exp. Med. Biol., 2003, vol. 529, pp. 187–197. doi: 10.1007/0-306-48416-1_38
  63. Solanki V., Tiwari M., Tiwari V. Host-bacteria interaction and adhesin study for development of therapeutics. Int. J. Biol. Macromol., 2018, vol. 112, pp. 54–64. doi: 10.1016/j.ijbiomac.2018.01.151
  64. Strauss J., Burnham N.A., Camesano T.A. Atomic force microscopy study of the role of LPS O-antigen on adhesion of E. coli. J. Mol. Recognit., 2009, vol. 22, no. 5, pp. 347–355. doi: 10.1002/jmr.955
  65. Strong P.C., Hinchliffe S.J., Patrick H., Atkinson S., Champion O.L., Wren B.W. Identification and characterisation of a novel adhesin Ifp in Yersinia pseudotuberculosis. BMC Microbiol., 2011, vol. 11: 85. doi: 10.1186/1471-2180-11-85
  66. 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, vol. 5, no. 12: e14403. doi: 10.1371/journal.pone.0014403
  67. 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, vol. 8, no. 12: e83621. doi: 10.1371/journal.pone.0083621
  68. Visser L.G., Annema A., van Furth R. Role of Yops in inhibition of phagocytosis and killing of opsonized Yersinia enterocolitica by human granulocytes. Infect. Immun., 1995, vol. 63, no. 7, pp. 2570–2575.
  69. Wang J., Katani R., Li L., Hegde N., Roberts E.L., Kapur V., DebRoy C. Rapid detection of Escherichia coli O157 and shiga toxins by lateral flow immunoassays. Toxins (Basel), 2016, vol. 8, no. 4: 92. doi: 10.3390/toxins8040092
  70. Williamson D.A., Baines S.L., Carter G.P., da Silva A.G., Ren X., Sherwood J., Dufour M., Schultz M.B., French N.P., Seemann T., Stinear T.P., Howden B.P. Genomic insights into a sustained national outbreak of Yersinia pseudotuberculosis. Genome Biol. Evol., 2016, vol. 8, no. 12, pp. 3806–3814. doi: 10.1093/gbe/evw285
  71. Yamashita S., Lukacik P., Barnard T.J., Noinaj N., Felek S., Tsang T.M., Krukonis E.S., Hinnebusch B.J., Buchanan S.K. Structural insights into Ail-mediated adhesion in Yersinia pestis. Structure, 2011, vol. 19, no. 11, pp. 1672–1682. doi: 10.1016/ j.str.2011.08.010
  72. Yang K., Park C.G., Cheong C., Bulgheresi S., Zhang S., Zhang P., He Y., Jiang L., Huang H., Ding H., Wu Y., Wang S., Zhang L., Li A., Xia L., Bartra S.S., Plano G.V., Skurnik M., Klena J.D., Chen T. Host Langerin (CD207) is a receptor for Yersinia pestis phagocytosis and promotes dissemination. Immunol. Cell Biol., 2015, vol. 93, no. 9, pp. 815–824. doi: 10.1038/icb.2015.46
  73. Yang Y., Merriam J.J., Mueller J.P., Isberg R.R. The psa locus is responsible for thermoinducible binding of Yersinia pseudotuberculosis to cultured cells. Infect. Immun., 1996, vol. 64, no. 7, pp. 2483–2489.
  74. Zhang P., Skurnik M., Zhang S.S., Schwartz O., Kalyanasundaram R., Bulgheresi S., He J.J., Klena J.D., Hinnebusch B.J., Chen T. Human dendritic cell-specific intercellular adhesion molecule-grabbing nonintegrin (CD209) is a receptor for Yersinia pestis that promotes phagocytosis by dendritic cells. Infect. Immun., 2008, vol. 76, no. 5, pp. 2070–2079.
  75. Zhang P., Snyder S., Feng P., Azadi P., Zhang S., Bulgheresi S., Sanderson K.E., He J., Klena J., Chen T. Role of N-acetylglucosamine within core lipopolysaccharide of several species of gram-negative bacteria in targeting the DC-SIGN (CD209). J. Immunol., 2006, vol. 177, no. 6, pp. 4002–4011. doi: 10.4049/jimmunol.177.6.4002
  76. Zhang S.S., Park C.G., Zhang P., Bartra S.S., Plano G.V., Klena J.D., Skurnik M., Hinnebusch B.J., Chen T. Plasminogen activator Pla of Yersinia pestis utilizes murine DEC-205 (CD205) as a receptor to promote dissemination. J. Biol. Chem., 2008, vol. 283, no. 46, pp. 31511–31521. doi: 10.1074/jbc.M804646200

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2019 Byvalov A.A., Konyshev I.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies