Prospects for new plague vaccines

Expert Review of Vaccines

Volumn 8, Issue 12, 2009, Pages 1721-1738

  Feodorova, Valentina A ^a   Corbel, Michael J ^b  

^a Saratov Scientific Center of the Russian Academy of Sciences   (Russian Federation)

^b NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

Author keywords

Aerosol; Fraction 1 antigen; LcrV antigen; Lipopolysaccharide; Plague; Regulation; Respiratory protection; TS33; Vaccine; Yersinia pestis

Indexed keywords

BACTERIAL PROTEIN; CHLORAMPHENICOL; CIPROFLOXACIN; COAGULASE; COTRIMOXAZOLE; DNA VACCINE; ENDOTOXIN; GENE PRODUCT; GENTAMICIN; HEMIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INACTIVATED VACCINE; LIPOPOLYSACCHARIDE; LIVE VACCINE; PH6 ANTIGEN; PHOSPHOLIPASE D; PLAGUE VACCINE; PLASMINOGEN ACTIVATOR; RECOMBINANT VACCINE; STREPTOMYCIN; SUBUNIT VACCINE; TETRACYCLINE; UNCLASSIFIED DRUG; V ANTIGEN; YBT ANTIGEN; YERSINIA OUTER PROTEIN E; YFE PROTIEN; YOPD PROTEIN; YOPO PROTEIN; YSCF PROTEIN;

ABDOMINAL PAIN; ADENOVIRUS; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIBODY TITER; BACTEREMIA; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CHILL; COLLAPSE; CYANOSIS; DISEASE MODEL; DNA IMMUNIZATION; DNA MODIFICATION; DRUG EFFICACY; DRUG MEGADOSE; ENZYME ACTIVITY; FEVER; GASTROINTESTINAL DISEASE; GENE LOCUS; GENE MUTATION; HEADACHE; HUMAN; HYPOTENSION; HYPOXIA; IMMUNIZATION; INCUBATION TIME; INNATE IMMUNITY; KIDNEY HEMORRHAGE; LACTOCOCCUS; LD 50; LICENSING; LIVER HEMORRHAGE; MALAISE; MENINGITIS; MENTAL DISEASE; MYALGIA; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PIGMENTATION; PLAGUE; PNEUMONIA; PRIORITY JOURNAL; PURPURA; REVIEW; SALMONELLA; SEPTICEMIA; SINGLE DRUG DOSE; TH2 CELL; TYPE III SECRETION SYSTEM; VESICULAR STOMATITIS; YERSINIA ENTEROCOLITICA; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BIOTERRORISM; DISEASE MODELS, ANIMAL; HUMANS; PLAGUE; PLAGUE VACCINE; PORE FORMING CYTOTOXIC PROTEINS; TREATMENT OUTCOME; VACCINES, SUBUNIT; YERSINIA PESTIS;

EID: 73849101080     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.09.129     Document Type: Review

References (202)

1. Achtman M, Zurth K, Morelli C, Torrea G, Guiyoule A, Carniel E. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl Acad. Sci. USA 96, 14043-14048 (1999).
2. Perry RD, Fetherston JD. Yersinia pestis -etiologic agent of plague. Clin. Microbiol. Rev. 10(1), 35-66 (1997).
3. Prevention of plague. Recommendation of the Advisory Committee on Immunization Practices (ACIP). MMWR 45(14), 1-15 (1996).
4. Pollitzer R. Plague. WHO, Geneva, Switzerland (Monograph series) (1954).
5. Stenseth NC, Atshabar BB, Begon M et al. Plague: past, present, and future. PLoS Med. 5(1), e3 (2008).
6. Alibek K, Handelman S. Biohazard. Random House, NY, USA (1999).
7. Inglesby TV, Dennis DT, Henderson DA et al. Plague as a biological weapon. JAMA 283(17), 2281-2290 (2000).
8. Nikolaev NI. Plague (Clinical, Diagnostic, Treatment and Prophylaxis Aspects). Meditcina, Moscow, USSR (1968).
9. USAMRIID's Medical Management of Biological Casualties Handbook (4th Edition). Kortepeter M, Christopher G, Cieslak T et al. (Eds). US Army Medical Research Institute of Infectious Diseases, Fort Detrick, MD, USA, 2-31 (2001).
10. Smiley ST. Current challenges in the development of vaccines for pneumonic plague. Expert Rev. Vaccines 7(2), 209-221 (2008).
11. Titball RW, Leary SE. Plague. Br. Med. Bull. 54(3), 625-633 (1998).
12. Butler T. Yersinia species (including plague). In: Principles and Practice of Infectious Diseases. Mandell GL, Bennett JE, Dolin E (Eds). Churchill Livingstone, NY, USA, 2070-2078 (1995).
13. Feodorova VA, Devdariani ZL. The interaction of Yersinia pestis with erythrocytes. J. Med. Microbiol. 51, 150-158 (2002).
14. Chain PS, Carniel E, Larimer FW et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl Acad. Sci. USA 101, 13826-13831 (2004).
15. Anisimov AP, Lindler LE, Pier GB. Intraspecific diversity of Yersinia pestis. Clin. Microbiol. Rev. 17, 434-464 (2004).
16. Aikimbajev A, Meka-Mechenko T, Temiralieva G et al. Plague in Kazakhstan at the present time. Przegl. Epidemiol. 57(4), 593-598 (2003).
17. Cleri DJ, Vernaleo JR, Lombardi LJ et al. Plague pneumonia disease caused by Yersinia pestis. Semin. Respir. Infect. 12(1), 12-23 (1997).
18. Keeling MJ, Gilligan CA. Metapopulation dynamics of bubonic plague. Nature 407, 903-906 (2000).
19. Galimand M, Guiyoule AN, Gerbaud G et al. Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N. Engl. J. Med. 337(10), 677-680 (1997).
20. Deng W, Burland V, Plunkett G et al. Genome sequence of Yersinia pestis KIM. J. Bacteriol. 84(16), 4601-4611 (2002).
21. Parkhill J, Wren BW, Thomson NR et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523-527 (2001).
22. Buchrieser C, Prentice M, Carniel E. The 102-kilobase unstable region of Yersinia pestis comprises a high-pathogenicity island linked to a pigmentation segment which undergoes internal rearrangement. J. Bacteriol. 180, 2321-2329 (1998).
23. Buchrieser C, Rusniok C, Frangeul L et al. The 102-kilobase pgm locus of Yersinia pestis: sequence analysis and comparison of selected regions among different Yersinia pestis and Yersinia pseudotuberculosis strains. Infect. Immun. 67, 4851-4861 (1999).
24. Cornelis G. The Yersinia YSC - Yop 'type III' weaponry. Nat. Rev. 2, 742-752 (2002).
25. Cornelis G, Boland A, Boyd AP et al. The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62, 1315-1352 (1998).
26. Fetherston JD, Perry RD. The pigmentation locus of Yersinia pestis KIM6+ is flanked by an insertion sequence and includes the structural genes for pesticin sensitivity and HMWP2. Mol. Microbiol. 13, 697-708 (1994).
27. Tong Z, Zhou D, Song Y et al. Pseudogene accumulation might promote the adaptive microevolution of Yersinia pestis. J. Med. Microbiol. 54(3), 259-268 (2005).
28. Balakhonov SV. Detection of pla, pst1 and caf1 gene nucleotide sequences on cryptic plasmid 33 kb of Yersinia pestis strains from tuva plague focus. In: Proceeding of 8th International Symposium on Yersinia. Turku, Finland, 4-8 September 2002, 78-79, P-64 (2002). •• Yersinia pestis strains with both unique cryptic plasmid and virulence are described.
29. Portnoy DA, Martinez RJ. Role of a plasmid in the pathogenicity of Yersinia species. Curr. Top. Microbiol. Immunol. 118, 29-51 (1985).
30. Friedlander AM, Welkos SL, Worsham PL et al. Relationship between virulence and immunity as revealed in recent studies of the F1 capsule of Yersinia pestis. Clin. Infect. Dis. 21, 178-181 (1995).
31. Du Y, Rosqvist R, Forsberg A. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect. Immun. 70, 1453-1460 (2002).
32. Galyov EE, Smirnov OY, Karlishev AV et al. Nucleotide sequence of the Yersinia pestis gene encoding FI antigen and the primary structure of the protein. Putative T and B cell epitopes. FEBS Lett. 277, 230-232 (1990).
33. Grosfeld H, Cohen S, Bino T et al. Effective protective immunity to Yersinia pestis infection conferred by DNA vaccine coding for derivatives of the F1 capsular antigen. Infect. Immun. 71, 374-383 (2003).
34. Titball RW, Howells AM, Oyston PC, Williamson ED. Expression of the Yersinia pestis capsular antigen (F1 antigen) on the surface of an aroA mutant of Salmonella typhimurium induces high levels of protection against plague. Infect. Immun. 65, 1926-1930 (1997).
35. Feodorova VA, Devdariani ZL. New genes involved in Yersinia pestis fraction I biosynthesis. J. Med. Microbiol. 50, 969-978 (2001).
36. Basova NN, Kravtsov FE, Naumovich LS. Monthly dynamics of the antitoxic immunity against diphtheria and tetanus and of normal antibodies to fraction I of the plague microbe in adults. Zh. Mikrobiol. 3, 82-86 (1982).
37. Meyer KF. Effectiveness of live or killed plague vaccines in man. Bull. WHO 42(5), 653-666 (1970).
38. Pautov VN, Chicherin YuV, Evstigneev VI, Byvalov AA, Kedrov OA. Experimental protective activity of fraction I of the plague microbe. Zh. Mikrobiol. 10, 37-42 (1979).
39. Devdariani ZL, Fedorova VA, Gromova OV, Taranenko TM. Comparative incidence of detection of specific antibodies to Yersinia pestis capsular antigen and lipopolysaccharide in humans immunized with pest vaccine. Klin. Lab. Diagn. 4, 39-41 (1997).
40. Meyer KF. Serological tests for the confirmation of plague infections: a preliminary communication. Bull. WHO 30, 750-751 (1964).
41. Benner GE, Andrews GP, Russel W et al. Immune response to Yersinia outer proteins and other Yersinia pestis antigens after experimental plague infection in mice. Infect. Immun. 67, 1922-1928 (1999).
42. Rudolph AE, Stuckey JA, Zhao Y et al. Expression, characterization amd mutagenesis of the Yersinia pestis murine toxin, a phospholipase D superfamily member. J. Biol. Chem. 274, 11824-11831 (1999).
43. Hinnebusch J, Cherepanov P, Du Y et al. Murine toxin of Yersinia pestis shows phospholipase D activity but is not required for virulence in mice. Int. J. Med. Microbiol. 290, 483-487 (2000).
44. Sinichkina NA, Kravtsov AL, Naumov AV, Kuzmichenko IA, Taranenko TM, Zadumina S. Comparative cytofluorometric analysis of leukocytes in the blood of guinea pigs under the action of Yersinia pestis phospholipase D and some Y. pestis antigens. Zh. Microbiol. 11-12, 52-54 (1992).
45. Feodorova VA, Golova AB. Antigenic and phenotypic modifications of Yersinia pestis in conditions simulating mammalian bloodstream. J. Med. Microbiol. 54, 435-441 (2005).
46. Chicherin IuV, Evstigneev VI, Lebedinskii VA. Duration and intensity of postvaccinal immunity to plague in experimental animals. Zh. Mikrobiol. 5, 95-98 (1977).
47. Smith PN. Pneumonic plague in mice: modification of the infection by antibody against specific components of Pasteurella pestis. J. Infect. Dis. 104(1), 85-91 (1959).
48. Hinnebusch BJ, Rudolph AE, Cherepanov P, Dixon JE, Schwan TG, Forsberg A. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296, 733-735 (2002).
49. Sodeinde OA, Goguen JD. Genetic analysis of the 9.5-kilobase virulence plasmid of Yersinia pestis. Infect. Immun. 56, 2743-2748 (1988).
50. Feodorova VA, Devdariani ZL. Development, characterization and diagnostic application of monoclonal antibodies against Yersinia pestis fibrinolysin and coagulase. J. Med. Microbiol. 49, 261-269 (2000).
51. McDonough KA, Falkow S. A Yersinia pestis-specific DNA fragment encodes temperature-dependent coagulase and fibrinolysin-associated phenotypes. Mol. Microbiol. 3, 767-775 (1989).
52. Kukkonen M, Korhonen TK. The Omptin family of enterobacterial surface protease/ adhesins: from housekeeping in Escherichia coli to systemic spread of Yersinia pestis. J. Med. Microbiol. 294, 7-14 (2004).
53. Lahteenmaki K, Kuusela P, Korhonen TK. Bacterial plasminogen activators and receptors. FEMS Microbiol. Rev. 25, 531-552 (2001).
54. Easterbrook TJ, Reddin K, Robinson A, Modi N. Studies on the immunogenicity of the Pla protein from Yersinia pestis. Contrib. Microbiol. Immunol. 13, 214-215 (1995).
55. Welkos S, Pitt MLM, Martinez M, Friedlander A, Vogel P, Tammariello R. Determination of the virulence of the pigmentation-deficient and pigmentation-/ plasminogen activator-deficient strains of Yersinia pestis in non-human primate and mouse models of pneumonic plague. Vaccine 20, 2206-2214 (2002).
56. Sodeinde OA, Subrahmanian YV, Stark K, Quan T, Bao Y, Goguen JD. A surface protease and the invasive character of plague. Science 258, 1004-1007 (1992).
57. Wang S, Joshi S, Mboudjeka I et al. Relative immunogenicity and protection potential of candidate Yersinia pestis antigens against lethal mucosal plague challenge in Balb/c mice. Vaccine 26, 1664-1674 (2008).
58. Broz P, Mueller CA, Muller SA et al. Function and molecular architecture of the Yersinia injectisome tip complex. Mol. Microbiol. 65, 1311-1320 (2007).
59. Leary SE, Griffin KF, Galyov EE et al. 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 (1999).
60. Brubaker RR. Interleukin-10 and inhibition of innate immunity to Yersiniae: roles of Yops and LcrV (V antigen). Infect. Immun. 71, 3673-3681 (2003).
61. Anderson GW, Leary SEC, Williamson ED et al. 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 (1996).
62. Pullen JK, Anderson GW, Welkos SL, Friedlander AM. Analysis of the Yersinia pestis V protein for the presence of linear antibody epitopes. Infect. Immun. 66, 521-527 (1998).
63. Hill J, Leary SEC, Griffin KF, Williamson ED, Titball RW. Regions of Yersinia pestis V antigen that contribute to protection against plague identified by passive and active immunization. Infect. Immun. 65, 4476-4482 (1997).
64. Motin VL, Nakajima R, Smirnov GB, Brubaker RR. Passive immunity to Yersiniae mediated by anti-recombinant V antigen and protein A-V antigen fusion peptide. Infect. Immun. 62, 4192-4201 (1994).
65. Cornelius CA, Quenee LE, Overheim KA et al. Immunization with recombinant V10 protects cynomolgus macaques from lethal pneumonic plague. Infect. Immun. 76(12), 5588-5597 (2008).
66. Vernazza C, Lingard B, Flick-Smith HC, Baillie LW, Hill J, Atkins HS. Small protective fragments of the Yersinia pestis V antigen. Vaccine 27(21), 2775-2780 (2009).
67. Schmidt A, Schaffelhofer S, Müller K, Röllinghoff M, Beuscher HU. Analysis of the Yersinia enterocolitica 0:8 V antigen for cross protectivity. Microb. Pathog. 26(4), 221-233 (1999).
68. Roggenkamp A, Geiger AM, Leitritz L, Kessler A, Heesmann J. Passive immunity to infection with Yersinia spp. mediated by polymorphism of V antigen. Infect. Immun. 65, 446-451 (1997).
69. Anisimov AP, Panfertsev EA, Svetoch TE, Dentovskaya SV. Variability of the protein sequences of lcrV between epidemic and atypical rhamnose-positive strains of Yersinia pestis. Adv. Exp. Med. Biol. 603, 23-27 (2007).
70. Andrews GP, Strachan ST, Benner GE et al. Protective efficacy of recombinant Yersinia outer proteins against bubonic plague caused by encapsulated and nonencapsulated Yersinia pestis. Infect. Immun. 67, 1533-1537 (1999).
71. Feodorova VA, Devdariani ZL. Immunogenicity and structural organization of some pLCR-encoded proteins of Yersinia pestis. J. Med. Microbiol. 50, 13-22 (2001).
72. Russmann H. Yersinia outer protein E, YopE. A versatile type III effector molecule for cytosolic targeting of heterologous antigens by attenuated Salmonella. Adv. Exp. Med. Biol. 529, 407-413 (2003).
73. Ivanov MI, Noel BL, Rampersaud R, Mena P, Benach JL, Bliska JB. Vaccination of mice with a Yop translocon complex elicits antibodies that are protective against infection with F1-Yersinia pestis. Infect. Immun. 76, 5181-5190 (2008).
74. Burrows TW. Virulence of Pasteurella pestis. Nature 179, 1246-1247 (1957).
75. Burrows TW, Bacon GA. The basis of virulence in Pasteurella pestis: an antigen determining virulence. Br. J. Exp. Pathol. 37, 481-493 (1956).
76. Michel P, Rasoamanana B, Rasolofonirina N, Roux J. The plague: disease and vaccine? Dakar Med. 37, 183-189 (1992).
77. Ben-Efraim S, Aronson M, Bichowsky-Slomnicki L. New antigenic component of Pasteurella pestis formed under specific conditions of pH and temperature. J. Bacteriol. 81, 704-714 (1961).
78. Lindler LE, Klempner MS, Straley SC. Yersinia pestis pH 6 antigen: genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect. Immun. 58(8), 2569-2577 (1990).
79. Tores-Escobar A, Juarez-Rodriguez MD, Curtiss R. III. Biogenesis of Yersinia pestis PsaA and its expression in recombinant attenuated Salmonella typhimurium vaccine (RASV) strains. FEMS Microbiol. Lett. (2009) (Epub ahead of print).
80. Zav'yalov VP, Abramov VM, Cherepanov PG et al. pH6 antigen (PsaA protein) of Yersinia pestis, a novel bacterial Fc-receptor. FEMS Immunol. Med. Microbiol. 14(1), 53-57 (1996).
81. Cathelyn JS, Crosby SD, Lathem WW, Goldman WE, Miller VL. RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc. Natl Acad. Sci. USA 103(36), 13514-13519 (2006).
82. Anisimov AP, Bakhteeva IV, Panfertsev EA et al. The subcutaneous inoculation of pH 6 antigen mutants of Yersinia pestis does not affect virulence and immune response in mice. J. Med. Microbiol. 58, 26-36 (2009).
83. Prior JL, Parkhill J, Hitchen PG et al. The failure of different strains of Yersinia pestis to produce lipopolysaccharide O-antigen under different growth conditions is due to mutations in the O-antigen gene cluster. FEMS Microbiol. Lett. 197, 229-233 (2001).
84. Vinogradov EV, Lindner B, Kocharova NA et al. Core structure in the lipopolysaccharide of the causative agent of plague, Yersinia pestis. Carbohydr. Res. 337, 775-777 (2002).
85. Bruneteau M, Minka S. Lipopolysaccharides of bacterial pathogens from the genus Yersinia: a mini-review. Biochemistry 85, 145-152 (2003).
86. Vinogradov EV, Knirel YuA, Thomas-Oates JE, Shashkov AS, L'vov VL. The structure of the cyclic enterobacterial common antigen (ECA) from Yersinia pestis. Carbohydr. Res. 258, 223-232 (1994).
87. Skurnik M, Bengoechea JA. The biosynthesis and biological role of lipopolysaccharide O-antigens of pathogenic Yersiniae. Carbohydr. Res. 338, 2521-2529 (2003).
88. Karlyshev AV, Oyston PCF, Williams K et al. Application of high-density arraybased signature-tagged mutagenesis to discover novel Yersinia virulence-associated genes. Infect. Immun. 69, 7810-7819 (2001).
89. Dodgson C, Amor P, Whitfield C. Distribution of the rol gene encoding the regulator of lipopolysaccharide O-chain length in Escherichia coli and its influence on the expression of group I capsular K antigens. J. Bacteriol. 178, 1895-1902 (1996).
90. Feodorova VA. Theoretical and experimental aspects of the study of protein and carbohydrate antigens of Yersinia pestis and Vibrio cholerae O139 using polyclonal and monoclonal antibodies. D. Sci. Thesis, Saratov, Russia (2004).
91. Prior JL, Hitchen PG, Williamson ED et al. Characterization of the lipopolysaccharide of Yersinia pestis. Microb. Pathog. 30, 49-57 (2001).
92. Feodorova VA, Devdariani ZL, Nazarova LS. Adjuvant effect of antiidiotypic antibodies to Yersinia pestis lipopolysaccharide. J. Med. Microbiol. 48, 751-756 (1999).
93. Hitchen PG, Prior JL, Oyston PCF et al. Structural characterization of lipooligosaccharide (LOS) from Yersinia pestis: regulation of LOS structure by the PhoPQ system. Mol. Microbiol. 44, 1637-1650 (2002).
94. Feodorova VA, Devdariani ZL. Expession of acid-stable proteins and modified lipopolysaccharide of Yersinia pestis in acidic growth medium. J. Med. Microbiol. 50, 979-985 (2001).
95. Gremyakova TA, Vinogradov EV, Lindner B et al. The core structure of the lipopolysaccharide of Yersinia pestis strain KM218. Adv. Exp. Med. Biol. 529, 229-231 (2003).
96. Kawahara K, Tsukano H, Watanabe H, Lindner B, Matsuura M. Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 70, 4092-4098 (2002).
97. Feodorova VA, Pan'kina LN, Savostiva EP et al. Pleiotropic effects of the lpx mutation in Yersinia pestis resulting in modification of the biosynthesis of major immunoreactive antigens. Vaccine 27(16), 2240-2250 (2009). •• Optimal approach for the development of a new live plague vaccine with characteristics based on licensed live plague vaccine EV NIIEG is reported.
98. Montminy SW, Khan N, Mc Grath S et al. Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat. Immunol. 7(10), 1066-1073 (2006). •• Discusses key points on plague immunity are discussed.
99. Fetherston JD, Schuetze P, Perry RD. Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol. Microbiol. 6, 2693-2704 (1992).
100. Brubaker RR. Mutation rate to non pigmentation in Pasteurella pestis. J. Bacteriol. 98, 1404-1406 (1969). 101 Flasher Y, Mamround E, Tidhar A et al. Generation of Yersinia pestis attenuated strains by signature-tagged mutagenesis in search of novel vaccine candidates. Infect. Immun. 72, 908-1015 (2004).
101. Fournier J, Paul G, Chomel J, Dodin A, Fontanges R. Experimental study of subcutaneous and aerosol vaccination against the plague in cynocephalous monkeys. Absence of correlation between hemagglutination and precipitant antibodies and protection. Ann. Microbiol. (Paris) 124, 315-328 (1973).
102. Kutyrev VV, Filippov AA, Oparina OS, Protsenko OA. Analysis of Yersinia pestis chromosomal determinants Pgm+ and Psts associated with virulence. Microb. Pathog. 12, 177-186 (1992).
103. Kutyrev VV, Filippov AA, Oparina OS, Protsenko OA. Genetic analysis and modeling of the virulence of Yersinia pestis. Mol. Genet. Microbiol. Virusol. 8, 42-47 (1989).
104. Saltykova RA, Faibich MM. Experience from a 30-year study of the stability of the properties of the plague vaccine strain EV in the USSR. Zh. Mikrobiol. 6, 3-8 (1975).
105. Byvalov AA, Pautov VN, Chicherin YV et al. Effectiveness of the revaccination of Hamadryas baboons with dried live plague vaccine NIIS and Yersinia pestis fraction 1. Zh. Microbiol. 4, 74-76 (1984).
106. Hallett AF, Issacson M, Meyer KF. Pathogenicity and immunogenic efficacy of a live attenuated plague vaccine in vervet monkeys. Infect. Immun. 8, 876-881 (1973).
107. Iteman I, Guiyoule A, De Almeida AMP, Guilvout I, Baranton G, Carniel E. Relationship between loss of pigmentation and deletion of chromosomal iron-regulated irp2 gene in Yersinia pestis: evidence for separate but related events. Infect. Immun. 61, 2717-2722 (1993).
108. Jarrett CO, Deak E, Isherwood KE et al. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Infect. Dis. 190, 783-792 (2004).
109. Joshua GW, Karlyshev AV, Smith MP, Isherwood KE, Titball RW, Wren BW. A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology 149, 3221-3229 (2003).
110. Kirillina O, Fetherston JD, Bobrov AG, Abney J, Perry RD. HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hmsdependent biofilm formation in Yersinia pestis. Mol. Microbiol. 54, 75-88 (2004).
111. Bearden SW, Fetherston JD, Perry RD. Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis. Infect. Immun. 65, 1659-1668 (1997).
112. Isupov IV, Beloborodov RA. Experimental Pathomorphology After Application of Live Plague Vaccine EV NIIEG. Institute 'Microbe', Saratov, Russia (1995).
113. Jackson S, Burrows TW. The virulenceenhancing effect of iron on non-pigmented mutants of virulent strains of Pasteurella pestis. Br. J. Exp. Pathol. 37, 577-583 (1956).
114. Lillard JW, Bearden SW, Fetherston JD, Perry RD. The haemin storage (Hms+) phenotype of Yersinia pestis is not essential for the pathogenesis of bubonic plague in mammals. Microbiology 145, 197-209 (1999).
115. Bearden SW, Perry RD. The Yfe system of Yersinia pestis transports iron and manganese and is required for full virulence of plague. Mol. Microbiol. 32, 403-414 (1999).
116. Robinson JB, Telepnev MV, Zudina IV et al. Evaluation of a Yersinia pestis mutant impaired in a thermoregulated type VI-like secretion system in flea, macrophage and murine models. Microb. Pathog. 47(5), 243-251 (2009).
117. Oyston PC, Dorrell N, Williams K et al. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68, 3419-3425 (2000).
118. Huang XZ, Lindler LE. The pH 6 antigen is an antiphagocytic factor produced by Yersinia pestis independent of Yersinia outer proteins and capsule antigen. Infect. Immun. 72(12), 7212-7219 (2004).
119. Bullen JJ. The significance of iron in infection. Rev. Infect. Dis. 3, 1127-1138 (1981).
120. Ilyukhin VI, Plekhanova NG, Senina TV, Stanovaya OV, Kislichkin NN. Experimental evidence of the possibility of using live tularemia vaccine to increase resistance to heterologous infectious diseases. Zh. Microbiol. 2, 38-42 (2004).
121. Nazarova LS, Isupov IV, Samoilova LV, Piontkovskii SA, Ovsiannikov VI, Suchkova OP. The effect of multiple plague vaccination on immune system indices. Zh. Mikrobiol. 6, 65-66 (1994).
122. Oyston PCF, Russell P, Williamson E et al. An aroA mutant of Yersinia pestis is attenuated in the guinea pig but virulent in mice. Microbiology 142, 1847-1853 (1995).
123. Lavrov VF. Mechanisms of development of immunological memory and vaccination. Epidemiol. Vaccinol. 4, 39-41 (2004).
124. Elvin SJ, Williamson ED, Scott JC et al. Evolutionary genetics: ambiguous role of CCR5 in Y. pestis infection. Nature 430(6998), 417 (2004).
125. Mecsas J, Franklin G, Kuziel WA, Brubaker RR, Falkow S, Mosier DE. Evolutionary genetics: CCR5 mutation and plague protection. Nature 427(6975), 606 (2004).
126. Tollenaere C, Rahalison L, Ranjalahy M et al. CCR5 polymorphism and plague resistance in natural populations of the black rat in Madagascar. Infect. Genet. Evol. 8(6), 891-897 (2008).
127. Quan SF, Chen TH, Meyer KF. Protective action of antibiotics against the toxin of Pasteurella pestis in mice. Proc. Soc. Exp. Biol. Med. 75(2), 548-549 (1950).
128. Green M, Rogers D, Russell P et al. The SCID/beige mouse as a model to investigate protection against Yersinia pestis. FEMS Immunol. Med. Microbiol. 23(2), 107-113 (1999).
129. Williamson ED, Flick-Smith HC, LeButt CS et al. Human immune response to a plague vaccine comprising recombinant F1 and rV antigens. Infect. Immun. 73, 3598-3608 (2005).
130. Bashaw J, Norris S, Weeks S, Trevino S, Adamovicz JJ, Welkos S. Development of in vitro correlate assays of immunity to infection with Yersinia pestis. Clin. Vaccine Immunol. 14(5), 605-616 (2007).
131. Englesberg E, Chen TH, Levy JB, Foster LE, Meyer KF. Virulence in Pasteurella pestis. Science 119(3091), 413-414 (1954).
132. Elvin SJ, Williamson ED. Stat 4 but not Stat 6 mediated immune mechanisms are essential in protection against plague. Microb. Pathog. 37(4), 177-184 (2004).
133. Williams JE, Altieri PL, Berman S, Lowenthal JP, Cavanaugh DC. Potency of killed plague vaccines prepared from avirulent Yersinia pestis. Bull. WHO 58(5), 753-756 (1980).
134. Meyer KF. The clinical and immunological response of man to P. pestis vaccine (summary and conclusions). Proceedings of: the Symposium on Bacterial Vaccines. The Yugoslav Academy of Science and Arts, Zagreb, Croatia (1971).
135. Jones SM, Griffin KF, Williamson ED. Protective efficacy of a fully recombinant plague vaccine in the guinea pig. Vaccine 21(25-26), 3912-3918 (2003).
136. Marshall JD. Plague immunization. II. Relation of adverse clinical reactions to multiple immunizations with killed vaccine. J. Infect. Dis. 129, 19-25 (1974).
137. Haffkine WM, Bennermann WB. The testing of Haffkine's plague prophylactic vaccine in plague stricken communities in India. Br. Med. J. 1(6), 856-858 (1989).
138. Meyer KF, Cavanaugh DC, Bartelloni PJ, Marshall JD. Plague immunization. I. Past and present trends. J. Infect. Dis. 129, 13-18 (1974).
139. Russell P, Eley SM, Hibbs SE, Manchee RJ, Stagg AJ, Titball RW. A comparison of plague vaccine, USP and EV76 vaccine induced protection against Yersinia pestis in a murine model. Vaccine 13(16), 1551-1556 (1995).
140. Strong RP. Studies in plague immunity. Philipp. J. Sci. 2(3), 155-331 (1907).
141. Otten L. Immunization against plague with live vaccine. Indian J. Med. Res. 24(1), 73-101 (1936).
142. Altaryova ND, Antonov AM, Zhdanov VM et al. Alive bivalent anti-plague vaccine 1-17 and intracutaneous method of vaccination. Proceedings of: Institute 'Microbe'. Saratov, Russia, 68-122 (1958).
143. Girard G. Immunity in plague infection. Results of 30 years of work with the Pasteurella pestis EV strain (Girard and Robic). Biol. Med. (Paris) 52, 631-731 (1963).
144. Anisimov PI, Anisimova TI, Aparin GP et al. Changes of Y. pestis EV vaccine strain properties after passages trough in the organisms of pikes. In: Problems of Particularly Dangerous Diseases. Saratov, Russia, 5, 68-74 (1969).
145. Titball RW, Williamson ED. Yersinia pestis (plague) vaccines. Expert Opin. Biol. Ther. 4, 965-973 (2004).
146. Smirnov VP. Vaccination against plague via conjunctiva. Proc. Irk. Antiplague Inst. Suberia Far East (Irkutsk, USSR) 24(2), 146-161 (1962).
147. Pushkareva VI. Experimental evaluation of interactions between Yersinia pestis EV and soil infusoria and the possibility of the prolonged preservation of bacteria in the protozoa cysts. Zh. Microbiol. 4, 40-44 (2003).
148. Higuchi K, Smith JL. Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J. Bacteriol. 81, 605-608 (1961).
149. Semenova YeL. Influence of organism of the plague-resistant animals upon the Y. pestis virulence. Proc. Asian Res. Antiplague Inst. AlmaAta 4, 129-134 (1958).
150. Derteva II. Influence of the antiplague sera upon Y. pestis in vitro and in biomodels. Proceedings of: the Institute 'Microbe'. Saratov, Russia, 2, 46-53 (1958)
151. Donskov GD, Lokhov MG. Influence of ethanol upon morphological, biochemical and biological properties of B. pestis. Vestnik Microbiol. Epidemiol. Parasitol. 15, 187-194 (1936).
152. Malinina ZYe. Selection of vaccine strains during in vitro cultivation with streptomycin. In: Particularly Dangerous and Natural Focal Infections. Meditcina, Moscow, USSR, 114-119 (1962).
153. Akimovich VV, Nikolaev NI, Zykin LF, Ponomaryov NG, Popov AA. Application of the Jackson-Burrows's and Higuchi-Smith's media for selection of Yersinia pestis strains with different level of virulence. In: Microbiology and Laboratory Diagnostics of Particularly Dangerous Disease. Saratov, Russia, 44-50 (1965).
154. Williams K, Oyston PC et al. Investigation into the role of the serine protease Htr in Yersinia pestis pathogenesis. FEMS Microbiol. Lett. 186, 281-286 (2005).
155. Sha J, Agar SL, Baze WB et al. Braun lipoprotein (Lpp) contributes to virulence of Yersiniae: potential role of Lpp in inducing bubonic and pneumonic plague. Infect. Immun. 76, 1390-1409 (2008).
156. Szaba FM, Kummer LW, Wilhelm LB et al. D27-pLpxL, an avirulent strain of Yersinia pestis, primes T cells that protect against pneumonic plague. Infect. Immun. 77(10), 4295-4304 (2009).
157. Garmory HS, Griffin KF, Brown KA, Titball RW. Oral immunization with live aroA Salmonella enterica serovar Typhimurium expressing the Yersinia pestis V antigen protects mice against plague. Vaccine 21, 3051-3057 (2003).
158. Garmory HS, Leary SE, Griffin KF, Williamson ED, Brown KA, Titball RW. The use of live attenuated bacteria as a delivery system for heterologous antigens. J. Drug Target. 11, 471-479 (2003).
159. Osorio JE, Powell TD, Frank RS et al. Recombinant raccoon pox vaccine protects mice against lethal plague. Vaccine 21, 1232-1238 (2003).
160. Sofer-Podesta C, Ang J, Hackett NR et al. Adenovirus-mediated delivery of an anti-V antigen monoclonal antibody protects mice against a lethal Yersinia pestis challenge. Infect. Immun. 77, 1561-1568 (2009).
161. Palin A, Chattopadhyay A, Park S et al. An optimized vaccine vector based on recombinant vesicular stomatitis virus gives high-level, long-term protection against Yersinia pestis challenge. Vaccine 25, 741-750 (2007).
162. Alvarez ML, Pinyerd HL, Crisantes JD et al. Plant-made subunit vaccine against pneumonic and bubonic plague is orally immunogenic in mice. Vaccine 24, 2477-2490 (2006).
163. Arlen PA, Singleton M, Adamovicz JJ, Ding Y, Davoodi-Semiromi A, Daniell H. Effective plague vaccination via oral delivery of plant cells expressing F1-V antigens in chloroplasts. Infect. Immun. 76(8), 3640-3650 (2008).
164. Del Prete G, Santi L, Andrianaivoarimanana V et al. Plantderived recombinant F1, V, and F1-V fusion antigens of Yersinia pestis activate human cells of the innate and adaptive immune system. Int. J. Immunopathol. Pharmacol. 22, 133-143 (2009).
165. Mizel SB, Graff AH, Sriranganathan N et al. Flagellin-F1-V fusion protein is an effective plague vaccine in mice and two species of nonhuman primates. Clin. Vaccine Immunol. 16, 21-28 (2009).
166. Alonso JM. Ecological interaction among Yersinia in their common reservoir, the rodent. Bull. Soc. Pathol. Exot. 92, 414-417 (1999).
167. Ellis J, Oyston PCF, Green M, Titball RW. Tularemia. Clin. Microbiol. Rev. 15, 631-646 (2002).
168. Williamson ED. Plague vaccine research and development. J. Appl. Microbiol. 91(4) (2001).
169. Williamson ED, Eley SM, Griffin KF et al. A new improved sub-unit vaccine for plague: the basis of protection. FEMS Immunol. Med. Microbiol. 12(3-4), 223-230 (1995).
170. Williamson ED, Vesey PM, Gillhespy KJ, Eley SM, Green M, Titball RW. An IgG1 titre to the F1 and V antigens correlates with protection against plague in the mouse model. Clin. Exp. Immunol. 116, 107-114 (1999).
171. Eyles JE, Williamson ED, Spier ID, Stagg AJ, Jones SM, Alpar HO. Generation of protective immune response to plague by mucosal administration of microsphere coencapsulated recombinant subunits. J. Control. Release 63, 191-200 (2000).
172. Eyles JE, Williamson ED, Spier ID, Alpar HO. Protection studies following bronchopulmonary and intramuscular immunization with Yersinia pestis F1 and V subunit vaccines coencapsulated in biodegradable microspheres: a comparison of efficacy. Vaccine 18, 3266-3271 (2000).
173. Griffin KF, Eyles JE, Spiers ID, Alpar HO, Williamson ED. Protection against plague following immunization with microencapsulated V antigen is reduced by co-encapsulation with IFN-g or IL-4, but not IL-6. Vaccine 20, 3650-3657 (2002).
174. Baca-Estrada ME, Foldvari MM, Snider MM, Harding KK, Kournikakis BB, Griebel PP. Intranasal immunization with liposome-formulated Yersinia pestis vaccine enhances mucosal immune responses. Vaccine 18, 2203-2211 (2000).
175. Heath DG, Anderson GW Jr, Mauro JM et al. Protection against experimental bubonic and pneumonic plague by a recombinant capsular F1-V antigen fusion protein vaccine. Vaccine 16(11-12), 1131-1137 (1998).
176. Powell BS, Andrews GP, Enama JT et al. Design and testing for a nontagged F1-V fusion protein as vaccine antigen against bubonic and pneumonic plague. Biotechnol. Prog. 21(5), 1490-1510 (2005).
177. Jones T, Adamovicz JJ, Cyr SL et al. Intranasal protollin/F1-V vaccine elicits respiratory and serum antibody responses and protects mice against lethal aerosolized plague infection. Vaccine 24(10), 1625-1632 (2006). •• New surrogate methods of evaluation of plague immunogenicity are presented.
178. Glynn A, Roy CJ, Powell BS, Adamovicz JJ, Freytag LC, Clements JD. Protection against aerosolized Yersinia pestis challenge following homologous and heterologous prime-boost with recombinant plague antigens. Infect. Immun. 73(8), 5256-5261 (2005). •• New surrogate methods of evaluation of plague immunogenicity are presented.
179. Amemiya K, Meyers JL, Rogers TE et al. CpG oligodeoxynucleotides augment the murine immune response to the Yersinia pestis F1-V vaccine in bubonic and pneumonic models of plague. Vaccine 27(16), 2220-2229 (2009). •• New surrogate methods of evaluation of plague immunogenicity are presented.
180. Kummer LW, Szaba FM, Parent MA et al. Antibodies and cytokines independently protect against pneumonic plague. Vaccine 26(52), 6901-6907 (2008). •• New surrogate methods of evaluation of plague immunogenicity are presented.
181. Morton M, Galmory HS, Perkins SD et al. A Salmonella enterica serovar Typhi vaccine expressing Yersinia pestis F1 antigen on its surface provides protection against plague in mice. Vaccine 22, 2524-2532 (2004).
182. Oyston PCF, Williamson ED, Leary SEC, Eley SM, Griffin KF, Titball RW. Immunization with live recombinant Salmonella typhimurium aroA producing F1 antigen protects against plague. Infect. Immun. 63, 563-568 (1995).
183. Simpson WJ, Thomas RE, Schwan TG. Recombinant capsular antigen (fraction 1) from Yersinia pestis induces a protective antibody response in BALB/c mice. Am. J. Trop. Med. Hyg. 43, 389-396 (1990).
184. Gremiakova TA, Amel'chenko VA, Anisimov AP. Early protection of animals immunized by a recombinant plague vaccine from experimental plague. Bull. Eksp. Biol. Med. 119, 54-57 (1995).
185. Cleri DJ, Vernaleo JR, Lombardi LJ et al. Plague pneumonia disease caused by Yersinia pestis. Semin. Respir. Infect. 12(1), 12-23 (1997).
186. Leary SE, Williamson ED, Griffin KF, Russell P, Eley SM, Titball RW. Active immunization with recombinant V antigen from Yersinia pestis protects mice against plague. Infect. Immun. 63, 2854-2858 (1995).
187. Motin VL, Nedialkov YuA, Brubaker RR. V antigen-polyhistidine fusion peptide: binding to LcrH and active immunity against plague. Infect. Immun. 64, 4313-4318 (1996).
188. Leary SE, Griffin KF, Garmory HS, Williamson ED, Titball RW. Expression of an F1/V fusion protein in attenuated Salmonella typhimurium and protection of mice against plague. Microb. Pathog. 23, 167-178 (1997).
189. Daniel C, Sebbane F, Poiret S et al. Protection against Yersinia pseudotuberculosis infection conferred by a Lactococcus lactis mucosal delivery vector secreting LcrV. Vaccine 27, 1141-1144 (2009).
190. Do Y, Park CG, Kang YS et al. Broad T cell immunity to the LcrV virulence protein is induced by targeted delivery to DEC-205/ CD205-positive mouse dendritic cells. Eur. J. Immunol. 38, 20-29 (2008).
191. Wang S, Heilman D, Liu F et al. A DNA vaccine producing LcrV antigen in oligomers is effective in protecting mice from lethal mucosal challenge of plague. Vaccine 22, 3348-3357 (2004).
192. Wang S, Joshi S, Mboudjeka I et al. Relative immunogenicity and protection potential of candidate Yersinia pestis antigens against lethal mucosal plague challenge in Balb/c mice. Vaccine 26, 1664-1674 (2008).
193. Yamanaka H, Hoyt T, Bowen R et al. An IL-12 DNA vaccine co-expressing Yersinia pestis antigens protects against pneumonic plague. Vaccine 27, 80-87 (2009).
194. Yamanaka H, Hoyt T, Yang X et al. A nasal interleukin-12 DNA vaccine coexpressing Yersinia pestis F1-V fusion protein confers protection against pneumonic plague. Infect. Immun. 76, 4564-4573 (2008).
195. Garmory HS, Freeman D, Brown KA, Titball RW. Protection against plague afforded by immunization with DNA vaccines optimized for expression of the Yersinia pestis V antigen. Vaccine 22, 947-957 (2004).
196. WHO Expert Committee on Biological Standardisation 2005/BS/05.2013 Guidelines for assuring the quality and nonclinical safety evaluation of DNA vaccines. In: WHO Expert Commitee on Biological Standardization: 56th Report. WHO, Geneva, Switzerland, 20-21 (2007).
197. Dalvadyants SM, Dubrovin MYu, Byvalov AA et al. A study of immunization against plague. Communication 3. Revaccination properties of the plague vaccine and the preparations of plague chemical vaccines for Hamadryas baboons. In: Problems of Particularly Dangerous Infections. Saratov, Russia, 89, 62-67 (2005).
198. Corbel MJ. The regulatory control and quality assurance of immunological products. Section S2. In: Industrial Pharmaceutical Microbiology. Euromed Communications Ltd, Haslemere, UK, S2.1-S2.16 (2004).
199. Williamson ED, Flick-Smith HC, Waters E et al. Immunogenicity of the rF1+rV vaccine for plague with identification of potential immune correlates. Microb. Pathog. 42(1), 11-21 (2007).
200. Zauberman A, Cohen S, Levy Y et al. Neutralization of Yersinia pestis-mediated macrophage cytotoxicity by anti-LcrV antibodies and its correlation with protective immunity in a mouse model of bubonic plague. Vaccine 26(13), 1616-1625 (2008).
201. Hill J, Copse C, Leary S, Stagg AJ, Williamson ED, Titball RW. Synergistic protection of mice against plague with monoclonal antibodies specific for the F1 and V antigens of Yersinia pestis. Infect. Immun. 71(4), 2234-2238 (2003).
202. Plague Manual: epidemiology, distribution, surveillance and control. WHO/CDS/ CSR/EDC/99.2 www.who.int/emc