1887

Abstract

Plague is an ancient, serious, infectious disease which is still endemic in regions of the modern world and is a potential biothreat agent. This paper discusses the natural history of the bacterium and its evolution into a flea-vectored bacterium able to transmit bubonic plague. It reviews the incidence of plague in the modern world and charts the history of vaccines which have been used to protect against the flea-vectored disease, which erupts as bubonic plague. Current approaches to vaccine development to protect against pneumonic, as well as bubonic, plague are also reviewed. The considerable challenges in achieving a vaccine which is licensed for human use and which will comprehensively protect against this serious human pathogen are assessed.

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2012-07-01
2020-01-27
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References

  1. Achtman M. , Zurth K. , Morelli G. , Torrea G. , Guiyoule A. , Carniel E. . ( 1999; ). Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis . . Proc Natl Acad Sci U S A 96:, 14043–14048. [CrossRef] [PubMed]
    [Google Scholar]
  2. Achtman M. , Morelli G. , Zhu P. , Wirth T. , Diehl I. , Kusecek B. , Vogler A. J. , Wagner D. M. , Allender C. J. . & other authors ( 2004; ). Microevolution and history of the plague bacillus, Yersinia pestis . . Proc Natl Acad Sci U S A 101:, 17837–17842. [CrossRef] [PubMed]
    [Google Scholar]
  3. Alvarez M. L. , Cardineau G. A. . ( 2010; ). Prevention of bubonic and pneumonic plague using plant-derived vaccines. . Biotechnol Adv 28:, 184–196. [CrossRef] [PubMed]
    [Google Scholar]
  4. Anderson G. W. Jr , Leary S. E. C. , Williamson E. D. , Titball R. W. , Welkos S. L. , Worsham P. L. , Friedlander A. M. . ( 1996; ). Recombinant V antigen protects mice against pneumonic and bubonic plague caused by F1-capsule-positive and negative strains of Yersinia pestis . . Infect Immun 64:, 4580–4585.[PubMed]
    [Google Scholar]
  5. Anderson D. M. , Ciletti N. A. , Lee-Lewis H. , Elli D. , Segal J. , DeBord K. L. , Overheim K. A. , Tretiakova M. , Brubaker R. R. , Schneewind O. . ( 2009; ). Pneumonic plague pathogenesis and immunity in brown Norway rats. . Am J Pathol 174:, 910–921. [CrossRef] [PubMed]
    [Google Scholar]
  6. Andrews G. P. , Heath D. G. , Anderson G. W. Jr , Welkos S. L. , Friedlander A. M. . ( 1996; ). Fraction 1 capsular antigen (F1) purification from Yersinia pestis CO92 and from an Escherichia coli recombinant strain and efficacy against lethal plague challenge. . Infect Immun 64:, 2180–2187.[PubMed]
    [Google Scholar]
  7. Andrews G. P. , Strachan S. T. , Benner G. E. , Sample A. K. , Anderson G. W. Jr , Adamovicz J. J. , Welkos S. L. , Pullen J. K. , Friedlander A. M. . ( 1999; ). Protective efficacy of recombinant Yersinia outer proteins against bubonic plague caused by encapsulated and nonencapsulated Yersinia pestis . . Infect Immun 67:, 1533–1537.[PubMed]
    [Google Scholar]
  8. Anisimov A. P. , Dentovskaya S. V. , Panfertsev E. A. , Svetoch T. E. , Kopylov P. Kh. , Segelke B. W. , Zemla A. , Telepnev M. V. , Motin V. L. . ( 2010; ). Amino acid and structural variability of Yersinia pestis LcrV protein. . Infect Genet Evol 10:, 137–145. [CrossRef] [PubMed]
    [Google Scholar]
  9. Ben Ari T. , Gershunov A. , Gage K. L. , Snäll T. , Ettestad P. , Kausrud K. L. , Stenseth N. C. . ( 2008; ). Human plague in the USA: the importance of regional and local climate. . Biol Lett 4:, 737–740. [CrossRef] [PubMed]
    [Google Scholar]
  10. Benner G. E. , Andrews G. P. , Byrne W. R. , Strachan S. D. , Sample A. K. , Heath D. G. , Friedlander A. M. . ( 1999; ). Immune response to Yersinia outer proteins and other Yersinia pestis antigens after experimental plague infection in mice. . Infect Immun 67:, 1922–1928.[PubMed]
    [Google Scholar]
  11. Bos K. I. , Schuenemann V. J. , Golding G. B. , Burbano H. A. , Waglechner N. , Coombes B. K. , McPhee J. B. , DeWitte S. N. , Meyer M. . & other authors ( 2011; ). A draft genome of Yersinia pestis from victims of the Black Death. . Nature 478:, 506–510. [CrossRef] [PubMed]
    [Google Scholar]
  12. Cavanaugh D. C. , Randall R. . ( 1959; ). The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of flea-borne plague. . J Immunol 83:, 348–363.[PubMed]
    [Google Scholar]
  13. CDC ( 2006; ). Human plague – four states, 2006. . MMWR Morb Mortal Wkly Rep 55:, 940–943.[PubMed]
    [Google Scholar]
  14. Chalton D. A. , Musson J. A. , Flick-Smith H. , Walker N. , McGregor A. , Lamb H. K. , Williamson E. D. , Miller J. , Robinson J. H. , Lakey J. H. . ( 2006; ). Immunogenicity of a Yersinia pestis vaccine antigen monomerized by circular permutation. . Infect Immun 74:, 6624–6631. [CrossRef] [PubMed]
    [Google Scholar]
  15. Chichester J. A. , Musiychuk K. , Farrance C. E. , Mett V. , Lyons J. , Mett V. , Yusibov V. . ( 2009; ). A single component two-valent LcrV-F1 vaccine protects non-human primates against pneumonic plague. . Vaccine 27:, 3471–3474. [CrossRef] [PubMed]
    [Google Scholar]
  16. Comer J. E. , Sturdevant D. E. , Carmody A. B. , Virtaneva K. , Gardner D. , Long D. , Rosenke R. , Porcella S. F. , Hinnebusch B. J. . ( 2010; ). Transcriptomic and innate immune responses to Yersinia pestis in the lymph node during bubonic plague. . Infect Immun 78:, 5086–5098. [CrossRef] [PubMed]
    [Google Scholar]
  17. Cornelis G. R. . ( 1998; ). The Yersinia Yop virulon, a bacterial system to subvert cells of the primary host defense. . Folia Microbiol (Praha) 43:, 253–261. [CrossRef]
    [Google Scholar]
  18. Cornelius C. A. , Quenee L. E. , Overheim K. A. , Koster F. , Brasel T. L. , Elli D. , Ciletti N. A. , Schneewind O. . ( 2008; ). Immunization with recombinant V10 protects cynomolgus macaques from lethal pneumonic plague. . Infect Immun 76:, 5588–5597. [CrossRef] [PubMed]
    [Google Scholar]
  19. DeBord K. L. , Anderson D. M. , Marketon M. R. , Overheim K. A. , DePalo R. W. , Ciletti N. A. , Jabri B. , Schneewind O. . ( 2006; ). Immunogenicity and protective immunity against bubonic plague and pneumonic plague by immunization of mice with the recombinant V10 antigen, a variant of LcrV. . Infect Immun 74:, 4910–4914. [CrossRef] [PubMed]
    [Google Scholar]
  20. Deng W. , Burland V. , Plunkett G. III , Boutin A. , Mayhew G. F. , Liss P. , Perna N. T. , Rose D. J. , Mau B. . & other authors ( 2002; ). Genome sequence of Yersinia pestis KIM. . J Bacteriol 184:, 4601–4611. [CrossRef] [PubMed]
    [Google Scholar]
  21. Devignat R. . ( 1951; ). Variétés de l’espèce Pasteurella pestis. Nouvelle hypothèse. . Bull Wld Hlth Org 4:, 247–263.
    [Google Scholar]
  22. Du Y. , Rosqvist R. , Forsberg A. . ( 2002; ). Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. . Infect Immun 70:, 1453–1460. [CrossRef] [PubMed]
    [Google Scholar]
  23. Easterbrook T. J. , Reddin K. , Robinson A. , Modi N. . ( 1995; ). Studies on the immunogenicity of the Pla protein from Yersinia pestis . . Contrib Microbiol Immunol 13:, 214–215.[PubMed]
    [Google Scholar]
  24. Eisen R. J. , Enscore R. E. , Biggerstaff B. J. , Reynolds P. J. , Ettestad P. , Brown T. , Pape J. , Tanda D. , Levy C. E. . & other authors ( 2007; ). Human plague in the southwestern United States, 1957–2004: spatial models of elevated risk of human exposure to Yersinia pestis . . J Med Entomol 44:, 530–537. [CrossRef] [PubMed]
    [Google Scholar]
  25. Elvin S. J. , Williamson E. D. . ( 2000; ). The F1 and V subunit vaccine protects against plague in the absence of IL-4 driven immune responses. . Microb Pathog 29:, 223–230. [CrossRef] [PubMed]
    [Google Scholar]
  26. Elvin S. J. , Williamson E. D. . ( 2004; ). Stat 4 but not Stat 6 mediated immune mechanisms are essential in protection against plague. . Microb Pathog 37:, 177–184. [CrossRef] [PubMed]
    [Google Scholar]
  27. Fellows P. , Adamovicz J. , Hartings J. , Sherwood R. , Mega W. , Brasel T. , Barr E. , Holland L. , Lin W. . & other authors ( 2010; ). Protection in mice passively immunized with serum from cynomolgus macaques and humans vaccinated with recombinant plague vaccine (rF1V). . Vaccine 28:, 7748–7756. [CrossRef] [PubMed]
    [Google Scholar]
  28. Garcia E. , Worsham P. , Bearden S. , Malfatti S. , Lang D. , Larimer F. , Lindler L. , Chain P. . ( 2007; ). Pestoides F, an atypical Yersinia pestis strain from the former Soviet Union. . Adv Exp Med Biol 603:, 17–22. [CrossRef] [PubMed]
    [Google Scholar]
  29. Hawgood B. J. . ( 2008; ). Alexandre Yersin (1863–1943): discoverer of the plague bacillus, explorer and agronomist. . J Med Biogr 16:, 167–172. [CrossRef] [PubMed]
    [Google Scholar]
  30. Heath D. G. , Anderson G. W. Jr , Mauro J. M. , Welkos S. L. , Andrews G. P. , Adamovicz J. , Friedlander A. M. . ( 1998; ). Protection against experimental bubonic and pneumonic plague by a recombinant capsular F1-V antigen fusion protein vaccine. . Vaccine 16:, 1131–1137. [CrossRef] [PubMed]
    [Google Scholar]
  31. Hill J. , Copse C. , Leary S. , Stagg A. J. , Williamson E. D. , Titball R. W. . ( 2003; ). Synergistic protection of mice against plague with monoclonal antibodies specific for the F1 and V antigens of Yersinia pestis . . Infect Immun 71:, 2234–2238. [CrossRef] [PubMed]
    [Google Scholar]
  32. Hill J. , Leary S. E. C. , Smither S. , Best A. , Pettersson J. , Forsberg A. , Lingard B. , Lipka A. , Brown K. A. . & other authors ( 2009; ). N255 is a key residue for recognition by a monoclonal antibody which protects against Yersinia pestis infection. . Vaccine 27:, 7073–7079. [CrossRef] [PubMed]
    [Google Scholar]
  33. Hinnebusch B. J. , Fischer E. R. , Schwan T. G. . ( 1998; ). Evaluation of the role of the Yersinia pestis plasminogen activator and other plasmid-encoded factors in temperature-dependent blockage of the flea. . J Infect Dis 178:, 1406–1415. [CrossRef] [PubMed]
    [Google Scholar]
  34. Hu P. , Elliott J. , McCready P. , Skowronski E. , Garnes J. , Kobayashi A. , Brubaker R. R. , Garcia E. . ( 1998; ). Structural organization of virulence-associated plasmids of Yersinia pestis . . J Bacteriol 180:, 5192–5202.[PubMed]
    [Google Scholar]
  35. Ivanov M. I. , Noel B. L. , Rampersaud R. , Mena P. , Benach J. L. , Bliska J. B. . ( 2008; ). Vaccination of mice with a Yop translocon complex elicits antibodies that are protective against infection with F1- Yersinia pestis . . Infect Immun 76:, 5181–5190. [CrossRef] [PubMed]
    [Google Scholar]
  36. Jarrett C. O. , Sebbane F. , Adamovicz J. J. , Andrews G. P. , Hinnebusch B. J. . ( 2004; ). Flea-borne transmission model to evaluate vaccine efficacy against naturally acquired bubonic plague. . Infect Immun 72:, 2052–2056. [CrossRef] [PubMed]
    [Google Scholar]
  37. Jones S. M. , Griffin K. F. , Hodgson I. , Williamson E. D. . ( 2003; ). Protective efficacy of a fully recombinant plague vaccine in the guinea pig. . Vaccine 21:, 3912–3918. [CrossRef] [PubMed]
    [Google Scholar]
  38. Lathem W. W. , Price P. A. , Miller V. L. , Goldman W. E. . ( 2007; ). A plasminogen-activating protease specifically controls the development of primary pneumonic plague. . Science 315:, 509–513. [CrossRef] [PubMed]
    [Google Scholar]
  39. Laws T. R. , Davey M. S. , Titball R. W. , Lukaszewski R. . ( 2010; ). Neutrophils are important in early control of lung infection by Yersinia pestis . . Microbes Infect 12:, 331–335. [CrossRef] [PubMed]
    [Google Scholar]
  40. Leary S. E. C. , Williamson E. D. , Griffin K. F. , Russell P. , Eley S. M. , Titball R. W. . ( 1995; ). Active immunization with recombinant V antigen from Yersinia pestis protects mice against plague. . Infect Immun 63:, 2854–2858.[PubMed]
    [Google Scholar]
  41. Leary S. E. C. , Griffin K. F. , Galyov E. E. , Hewer J. , Williamson E. D. , Holmström A. , Forsberg A. , Titball R. W. . ( 1999; ). Yersinia outer proteins (YOPS) E, K and N are antigenic but non-protective compared to V antigen, in a murine model of bubonic plague. . Microb Pathog 26:, 159–169. [CrossRef] [PubMed]
    [Google Scholar]
  42. Li B. , Zhou L. , Guo J. Y. , Wang X. , Ni B. , Ke Y. , Zhu Z. , Guo Z. , Yang R. . ( 2009; ). High-throughput identification of new protective antigens from a Yersinia pestis live vaccine by enzyme-linked immunospot assay. . Infect Immun 77:, 4356–4361. [CrossRef] [PubMed]
    [Google Scholar]
  43. Lin J.-S. , Park S. , Adamovicz J. J. , Hill J. , Bliska J. B. , Cote C. K. , Perlin D. S. , Amemiya K. , Smiley S. T. . ( 2010; ). TNFα and IFNγ contribute to F1/LcrV-targeted immune defense in mouse models of fully virulent pneumonic plague. . Vaccine 29:, 357–362. [CrossRef]
    [Google Scholar]
  44. Lin J.-S. , Szaba F. M. , Kummer L. W. , Chromy B. A. , Smiley S. T. . ( 2011; ). Yersinia pestis YopE contains a dominant CD8 T cell epitope that confers protection in a mouse model of pneumonic plague. . J Immunol 187:, 897–904. [CrossRef] [PubMed]
    [Google Scholar]
  45. Lindler L. E. , Plano G. V. , Burland V. , Mayhew G. F. , Blattner F. R. . ( 1998; ). Complete DNA sequence and detailed analysis of the Yersinia pestis KIM5 plasmid encoding murine toxin and capsular antigen. . Infect Immun 66:, 5731–5742.[PubMed]
    [Google Scholar]
  46. Matson J. S. , Durick K. A. , Bradley D. S. , Nilles M. L. . ( 2005; ). Immunization of mice with YscF provides protection from Yersinia pestis infections. . BMC Microbiol 5:, 38. [CrossRef] [PubMed]
    [Google Scholar]
  47. Mett V. , Lyons J. , Musiychuk K. , Chichester J. A. , Brasil T. , Couch R. , Sherwood R. , Palmer G. A. , Streatfield S. J. , Yusibov V. . ( 2007; ). A plant-produced plague vaccine candidate confers protection to monkeys. . Vaccine 25:, 3014–3017. [CrossRef] [PubMed]
    [Google Scholar]
  48. Mizel S. B. , Graff A. H. , Sriranganathan N. , Ervin S. , Lees C. J. , Lively M. O. , Hantgan R. R. , Thomas M. J. , Wood J. , Bell B. . ( 2009; ). Flagellin-F1-V fusion protein is an effective plague vaccine in mice and two species of nonhuman primates. . Clin Vaccine Immunol 16:, 21–28. [CrossRef] [PubMed]
    [Google Scholar]
  49. Morelli G. , Song Y. , Mazzoni C. J. , Eppinger M. , Roumagnac P. , Wagner D. M. , Feldkamp M. , Kusecek B. , Vogler A. J. . & other authors ( 2010; ). Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. . Nat Genet 42:, 1140–1143. [CrossRef] [PubMed]
    [Google Scholar]
  50. Motin V. L. , Pokrovskaya M. S. , Telepnev M. V. , Kutyrev V. V. , Vidyaeva N. A. , Filippov A. A. , Smirnov G. B. . ( 1992; ). The difference in the lcrV sequences between Y. pestis and Y. pseudotuberculosis and its application for characterization of Y. pseudotuberculosis strains. . Microb Pathog 12:, 165–175. [CrossRef] [PubMed]
    [Google Scholar]
  51. Motin V. L. , Georgescu A. M. , Elliott J. M. , Hu P. , Worsham P. L. , Ott L. L. , Slezak T. R. , Sokhansanj B. A. , Regala W. M. . & other authors ( 2002; ). Genetic variability of Yersinia pestis isolates as predicted by PCR-based IS100 genotyping and analysis of structural genes encoding glycerol-3-phosphate dehydrogenase (glpD). . J Bacteriol 184:, 1019–1027. [CrossRef] [PubMed]
    [Google Scholar]
  52. Mueller C. A. , Broz P. , Müller S. A. , Ringler P. , Erne-Brand F. , Sorg I. , Kuhn M. , Engel A. , Cornelis G. R. . ( 2005; ). The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. . Science 310:, 674–676. [CrossRef] [PubMed]
    [Google Scholar]
  53. Musson J. , Morton M. , Walker N. J. , Harper H. M. , McNeill H. E. , Williamson E. D. , Robinson J. H. . ( 2006; ). Sequential proteolytic processing of the capsular Caf1 antigen of Yersinia pestis for major histocompatibility complex class II-restricted presentation to T lymphocytes. . J Biol Chem 281:, 26129–26135. [CrossRef] [PubMed]
    [Google Scholar]
  54. Musson J. A. , Ingram R. , Durand G. , Ascough S. , Waters E. L. , Hartley M. G. , Robson T. , Maillere B. , Williamson E. D. . & other authors ( 2010; ). Repertoire of HLA-DR1-restricted CD4 T-cell responses to capsular Caf1 antigen of Yersinia pestis in human leukocyte antigen transgenic mice. . Infect Immun 78:, 4356–4362. [CrossRef] [PubMed]
    [Google Scholar]
  55. Nakajima R. , Motin V. L. , Brubaker R. R. . ( 1995; ). Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunization. . Infect Immun 63:, 3021–3029.[PubMed]
    [Google Scholar]
  56. Oyston P. C. F. , Williamson E. D. . ( 2011; ). Plague: infections of companion animals and opportunities for intervention. . Animals 1:, 242–255. [CrossRef]
    [Google Scholar]
  57. Parent M. A. , Berggren K. N. , Kummer L. W. , Wilhelm L. B. , Szaba F. M. , Mullarky I. K. , Smiley S. T. . ( 2005; ). Cell-mediated protection against pulmonary Yersinia pestis infection. . Infect Immun 73:, 7304–7310. [CrossRef] [PubMed]
    [Google Scholar]
  58. Parkhill J. , Wren B. W. , Thomson N. R. , Titball R. W. , Holden M. T. G. , Prentice M. B. , Sebaihia M. , James K. D. , Churcher C. . & other authors ( 2001; ). Genome sequence of Yersinia pestis, the causative agent of plague. . Nature 413:, 523–527. [CrossRef] [PubMed]
    [Google Scholar]
  59. Perry R. D. , Fetherston J. D. . ( 1997; ). Yersinia pestis – etiologic agent of plague. . Clin Microbiol Rev 10:, 35–66.[PubMed]
    [Google Scholar]
  60. Perry R. D. , Straley S. C. , Fetherston J. D. , Rose D. J. , Gregor J. , Blattner F. R. . ( 1998; ). DNA sequencing and analysis of the low-Ca2+-response plasmid pCD1 of Yersinia pestis KIM5. . Infect Immun 66:, 4611–4623.[PubMed]
    [Google Scholar]
  61. Pitt M. L. . ( 2004; ). Non-human primates as a model for pneumonic plague; Animal Models and Correlates of Protection for Plague Vaccines Workshop, Gaithersburg, MD, USA.
  62. Pollitzer R. . ( 1960; ). A review of recent literature on plague. . Bull World Health Organ 23:, 313–400.[PubMed]
    [Google Scholar]
  63. Powell B. S. , Andrews G. P. , Enama J. T. , Jendrek S. , Bolt C. , Worsham P. , Pullen J. K. , Ribot W. , Hines H. . & other authors ( 2005; ). Design and testing for a nontagged F1-V fusion protein as vaccine antigen against bubonic and pneumonic plague. . Biotechnol Prog 21:, 1490–1510. [CrossRef] [PubMed]
    [Google Scholar]
  64. Quenee L. E. , Ciletti N. A. , Elli D. , Hermanas T. M. , Schneewind O. . ( 2011; ). Prevention of pneumonic plague in mice, rats, guinea pigs and non-human primates with clinical grade rV10, rV10-2 or F1-V vaccines. . Vaccine 29:, 6572–6583. [CrossRef] [PubMed]
    [Google Scholar]
  65. Qiu Y. , Liu Y. , Qi Z. , Wang W. , Kou Z. , Zhang Q. , Liu G. , Liu T. , Yang Y. . & other authors ( 2010; ). Comparison of immunological responses of plague vaccines F1+rV270 and EV76 in Chinese-origin rhesus macaque, Macaca mulatta. . Scand J Immunol 72:, 425–433. [CrossRef] [PubMed]
    [Google Scholar]
  66. Reithmeier-Rost D. , Hill J. , Elvin S. J. , Williamson D. , Dittmann S. , Schmid A. , Wilharm G. , Sing A. . ( 2007; ). The weak interaction of LcrV and TLR2 does not contribute to the virulence of Yersinia pestis . . Microbes Infect 9:, 997–1002. [CrossRef] [PubMed]
    [Google Scholar]
  67. Roggenkamp A. , Geiger A. M. , Leitritz L. , Kessler A. , Heesemann J. . ( 1997; ). Passive immunity to infection with Yersinia spp. mediated by anti-recombinant V antigen is dependent on polymorphism of V antigen. . Infect Immun 65:, 446–451.[PubMed]
    [Google Scholar]
  68. Rosenzweig J. A. , Jejelowo O. , Sha J. , Erova T. E. , Brackman S. M. , Kirtley M. L. , van Lier C. J. , Chopra A. K. . ( 2011; ). Progress on plague vaccine development. . Appl Microbiol Biotechnol 91:, 265–286. [CrossRef] [PubMed]
    [Google Scholar]
  69. Shim H. K. , Musson J. A. , Harper H. M. , McNeill H. V. , Walker N. , Flick-Smith H. C. , von Delwig A. , Williamson E. D. , Robinson J. H. . ( 2006; ). Mechanisms of major histocompatibility complex class II-restricted processing and presentation of the V antigen of Yersinia pestis . . Immunology 119:, 385–392. [CrossRef] [PubMed]
    [Google Scholar]
  70. Smiley S. T. . ( 2007; ). Cell-mediated defense against Yersinia pestis infection. . Adv Exp Med Biol 603:, 376–386. [CrossRef] [PubMed]
    [Google Scholar]
  71. Stacy S. , Pasquali A. , Sexton V. L. , Cantwell A. M. , Kraig E. , Dube P. H. . ( 2008; ). An age-old paradigm challenged: old baboons generate vigorous humoral immune responses to LcrV, a plague antigen. . J Immunol 181:, 109–115.[PubMed] [CrossRef]
    [Google Scholar]
  72. Sun W. , Roland K. L. , Curtiss R. . ( 2011; ). Developing live vaccines against plague. . J Infect Dev Ctries 5:, 614–627.
    [Google Scholar]
  73. Swietnicki W. , Powell B. S. , Goodin J. . ( 2005; ). Yersinia pestis Yop secretion protein F: purification, characterization, and protective efficacy against bubonic plague. . Protein Expr Purif 42:, 166–172. [CrossRef] [PubMed]
    [Google Scholar]
  74. Tito M. A. , Miller J. , Griffin K. F. , Williamson E. D. , Titball R. W. , Robinson C. V. . ( 2001a; ). Macromolecular organization of the Yersinia pestis capsular F1 antigen: insights from time-of-flight mass spectrometry. . Protein Sci 10:, 2408–2413. [CrossRef] [PubMed]
    [Google Scholar]
  75. Tito M. A. , Miller J. , Walker N. , Griffin K. F. , Williamson E. D. , Despeyroux-Hill D. , Titball R. W. , Robinson C. V. . ( 2001b; ). Probing molecular interactions in intact antibody:antigen complexes, an electrospray time-of-flight mass spectrometry approach. . Biophys J 81:, 3503–3509. [CrossRef] [PubMed]
    [Google Scholar]
  76. Wang S. , Goguen J. D. , Li F. , Lu S. . ( 2011; ). Involvement of CD8+ T cell-mediated immune responses in LcrV DNA vaccine induced protection against lethal Yersinia pestis challenge. . Vaccine 29:, 6802–6809. [CrossRef] [PubMed]
    [Google Scholar]
  77. Welkos S. , Norris S. , Adamovicz J. . ( 2008; ). Modified caspase-3 assay indicates correlation of caspase-3 activity with immunity of nonhuman primates to Yersinia pestis infection. . Clin Vaccine Immunol 15:, 1134–1137. [CrossRef] [PubMed]
    [Google Scholar]
  78. WHO ( 2005; ). Plague, Democratic Republic of the Congo. . Wkly Epidemiol Rec 80:, 65.[PubMed]
    [Google Scholar]
  79. Williams R. C. Jr , Gewurz H. , Quie P. G. . ( 1972; ). Effects of fraction I from Yersinia pestis on phagocytosis in vitro. . J Infect Dis 126:, 235–241. [CrossRef] [PubMed]
    [Google Scholar]
  80. Williamson E. D. , Eley S. M. , Griffin K. F. , Green M. , Russell P. , Leary S. E. C. , Oyston P. C. F. , Easterbrook T. , Reddin K. M. . & other authors ( 1995; ). A new improved sub-unit vaccine for plague: the basis of protection. . FEMS Immunol Med Microbiol 12:, 223–230. [CrossRef] [PubMed]
    [Google Scholar]
  81. Williamson E. D. . ( 2009; ). Plague. . Vaccine 27: (Suppl. 4), D56–D60. [CrossRef] [PubMed]
    [Google Scholar]
  82. Williamson E. D. , Eley S. M. , Stagg A. J. , Green M. , Russell P. , Titball R. W. . ( 1997; ). A sub-unit vaccine elicits IgG in serum, spleen cell cultures and bronchial washings and protects immunized animals against pneumonic plague. . Vaccine 15:, 1079–1084. [CrossRef] [PubMed]
    [Google Scholar]
  83. Williamson E. D. , Vesey P. M. , Gillhespy K. J. , Eley S. M. , Green M. , Titball R. W. . ( 1999; ). An IgG1 titre to the F1 and V antigens correlates with protection against plague in the mouse model. . Clin Exp Immunol 116:, 107–114. [CrossRef] [PubMed]
    [Google Scholar]
  84. Williamson E. D. , Eley S. M. , Stagg A. J. , Green M. , Russell P. , Titball R. W. . ( 2000; ). A single dose sub-unit vaccine protects against pneumonic plague. . Vaccine 19:, 566–571. [CrossRef] [PubMed]
    [Google Scholar]
  85. Williamson E. D. , Flick-Smith H. C. , Lebutt C. S. , Rowland C. A. , Jones S. M. , Waters E. L. , Gwyther R. J. , Miller J. , Packer P. J. , Irving M. . ( 2005; ). Human immune response to a plague vaccine comprising recombinant F1 and V antigens. . Infect Immun 73:, 3598–3608. [CrossRef] [PubMed]
    [Google Scholar]
  86. Williamson E. D. , Flick-Smith H. C. , Waters E. , Miller J. , Hodgson I. , Le Butt C. S. , Hill J. . ( 2007; ). Immunogenicity of the rF1+rV vaccine for plague with identification of potential immune correlates. . Microb Pathog 42:, 11–21. [CrossRef]
    [Google Scholar]
  87. Williamson E. D. , Packer P. J. , Waters E. L. , Simpson A. J. , Dyer D. , Hartings J. , Twenhafel N. , Pitt M. L. M. . ( 2011; ). Recombinant (F1+V) vaccine protects cynomolgus macaques against pneumonic plague. . Vaccine 29:, 4771–4777. [CrossRef] [PubMed]
    [Google Scholar]
  88. Worsham P. L. , Roy C. . ( 2003; ). Pestoides F, a Yersinia pestis strain lacking plasminogen activator, is virulent by the aerosol route. . Adv Exp Med Biol 529:, 129–131. [CrossRef] [PubMed]
    [Google Scholar]
  89. Wren B. W. . ( 2003; ). The Yersiniae – a model genus to study the rapid evolution of bacterial pathogens. . Nat Rev Microbiol 1:, 55–64. [CrossRef] [PubMed]
    [Google Scholar]
  90. Zhou D. , Yang R. . ( 2009; ). Molecular Darwinian evolution of virulence in Yersinia pestis . . Infect Immun 77:, 2242–2250. [CrossRef] [PubMed]
    [Google Scholar]
  91. Zhou D. , Tong Z. , Song Y. , Han Y. , Pei D. , Pang X. , Zhai J. , Li M. , Cui B. . & other authors ( 2004; ). Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. . J Bacteriol 186:, 5147–5152. [CrossRef] [PubMed]
    [Google Scholar]
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