Prevention of pneumonic plague in mice, rats, guinea pigs and non-human primates with clinical grade rV10, rV10-2 or F1-V vaccines

Vaccine

Volumn 29, Issue 38, 2011, Pages 6572-6583

  Quenee, Lauriane E ^a,b   Ciletti, Nancy A ^a,b   Elli, Derek ^a,b   Hermanas, Timothy M ^a,b   Schneewind, Olaf ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

African Green monkeys; Cynomolgus; GMP manufacturing; LcrV; Macaques; Plague; Protective antigen; Yersinia pestis

Indexed keywords

ALUMINUM HYDROXIDE; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; F1 V VACCINE; HYBRID PROTEIN; NEW DRUG; PLAGUE VACCINE; PROTEIN LCRV; PROTEIN SUBUNIT; RV10 2 VACCINE; RV10 VACCINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTERIAL PNEUMONIA; BACTERIUM PILUS; CONTROLLED STUDY; DRUG DESIGN; DRUG EFFICACY; DRUG FORMULATION; DRUG PURITY; DRUG SCREENING; DRUG STABILITY; DRUG STRUCTURE; DRUG SYNTHESIS; FOOD AND DRUG ADMINISTRATION; GOOD MANUFACTURING PRACTICE; GUINEA PIG; IMMUNIZATION; MOUSE; MOUSE STRAIN; NONHUMAN; PLAGUE; PRIMATE; PRIORITY JOURNAL; RAT; RAT STRAIN; TREATMENT OUTCOME; YERSINIA PESTIS;

ADJUVANTS, IMMUNOLOGIC; ALUMINUM HYDROXIDE; ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; DISEASE MODELS, ANIMAL; GUINEA PIGS; MACACA; MICE; MICE, INBRED BALB C; PLAGUE; PLAGUE VACCINE; PRIMATE DISEASES; RATS; RODENT DISEASES; SURVIVAL ANALYSIS; VACCINATION; VACCINES, SUBUNIT; VACCINES, SYNTHETIC; YERSINIA PESTIS;

EID: 80051670228     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.06.119     Document Type: Article

References (59)

1. Yersin A. La peste bubonique à Hong-Kong. Ann Inst Pasteur 1894, 2:428-430.
2. Simond P.L. La propagation de la peste. Ann Inst Pasteur 1898, 12:625-687.
3. Perry R.D., Fetherston J.D. Yersinia pestis-etiologic agent of plague. Clin Microbiol Rev 1997, 10:35-66.
4. Raoult D., Aboudharam G., Crubezy E., Larrouy G., Ludes B., Drancourt M. Molecular identification by "suicide PCR" of Yersinia pestis as the agent of medieval black death. Proc Natl Acad Sci USA 2000, 97:12800-12803.
5. Metcalfe N. A short history of biological warfare. Med Confl Surviv 2002, 18:271-282.
6. Haffkine W.M. Remarks on the plague prophylactic fluid. Br Med J 1897, 1:1461-1462.
7. Quenee L.E., Schneewind O. Plague vaccines and the molecular basis of immunity against Yersinia pestis. Hum Vaccin 2009, 5:817-823.
8. Burrows T.W. Virulence of Pasteurella pestis and immunity to plague. Ergebn Mikrobiol 1963, 37:59-113.
9. Wake A., Morita H., Wake M. Mechanisms of long and short term immunity to plague. Immunology 1978, 34:1045-1052.
10. Meyer K.F. Effectiveness of live or killed plague vaccines in man. Bull WHO 1970, 42:653-666.
11. Cavanaugh D.C., Elisberg B.L., Llewellyn C.H., Marshall J.D., Rust J.H., Williams J.E., et al. Plague immunization V. Indirect evidence for the efficacy of plague vaccine. J Infect Dis 1974 May, 129:S37-S40. Suppl.
12. Meyer K.F., Smith G., Foster L.E., Marshall J.D., Cavanaugh D.C. Plague immunization IV. Clinical reactions and serological responses to inoculations of Haffkine and freeze-dried plague vaccine. J Infect Dis 1974, 129:S30-S36.
13. Titball R.W., Williamson E.D. Vaccination against bubonic and pneumonic plague. Vaccine 2001, 19(July (30)):4175-4184.
14. Fetherston J.D., Schuetze P., Perry R.D. Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102kb of chromosomal DNA which is flanked by a repetitive element. Mol Microbiol 1992, 6:2693-2704.
15. 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 1998, 180:2321-2329.
16. Brubaker R.R. Mutation rate to non-pigmentation in Pasteurella pestis. J Bacteriol 1969, 98:1404-1406.
17. Girard G. Plague. Annu Rev Microbiol 1955, 9:253-277.
18. Meyer K.F., Smith G., Foster L., Brookman M., Sung M.H. Live, attenuated Yersinia pestis vaccine: virulent in non-human primates, harmless to guinea pigs. J Infect Dis 1974, 129:S85-S112.
19. Baker E.E., Sommer H., Foster L.E., Meyer E., Meyer K.F. Studies on immunization against plague I. The isolation and characterization of the soluble antigen of Pasteurella pestis. J Immunol 1952, 68:131-145.
20. Zavialov A.V., Berglund J., Pudney A.F., Fooks L.J., Ibrahim T.M., MacIntyre S., et al. Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 2003, 113:587-596.
21. Du Y., Rosqvist R., Forsberg A. Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun 2002, 70:1453-1460.
22. Liu F., Chen H., Galvan E.M., Lasaro M.A., Schifferli D.M. Effects of Psa and F1 on the adhesive and invasive interactions of Yersinia pestis with human respiratory tract epithelial cells. Infect Immun 2006, 74:5636-5644.
23. Quenee L., Cornelius C.A., Ciletti N.A., Elli D., Schneewind O. Yersinia pestis caf1 (F1) variants and the limits of plague vaccine protection. Infect Immun 2008, 76:2025-2036.
24. Anderson D.A., Ciletti N.A., Lee H., Elli D., Segal J., DeBord K.L., et al. Pneumonic plague pathogenesis and immunity in brown Norway rats. Am J Pathol 2009, 174:910-921.
25. Cornelius C.A., Quenee L.E., Elli D., Ciletti N.A., Schneewind O. Yersinia pestis IS1541 transposition provides for escape from plague immunity. Infect Immun 2009, 77:1807-1816.
26. Friedlander A.M., Welkos S.L., Worsham P.L., Andrews G.P., Heath D.G., Anderson G.W., et al. Relationship between virulence and immunity as revealed in recent studies of the F1 capsule of Yersinia pestis. Clin Infect Dis 1995, 21:S178-S181.
27. Burrows T.W. An antigen determining virulence in Pasteurella pestis. Nature 1956, 177:426-427.
28. Burrows T.W., Bacon G.A. The effect of loss of different virulence determinants on the virulence and immunogenicity of strains of Pasteurella pestis. Br J Exp Pathol 1958, 39:278-291.
29. 2+ response operon encodes the V antigen of Yersinia pestis. Infect Immun 1986, 54:428-434.
30. Mueller C.A., Broz P., Muller S.A., Ringler P., Erne-Brand F., Sorg I., et al. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 2005, 310:674-676.
31. Petterson J., Holmstrom A., Hill J., Frithz-Lindsten E., von Euler-Matell A., Carlsson E., et al. The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol Microbiol 1999, 32:961-976.
32. Lee V.T., Tam C., Schneewind O. LcrV a substrate for Yersinia enterocolitica type III secretion, is required for toxin targeting into the cytosol of HeLa cells. J Biol Chem 2000, 275:36869-36875.
33. DeBord K., Lee V.T., Schneewind O. On the role of LcrG and LcrV during the type III targeting of effector Yops by Yersinia enterocolitica. J Bacteriol 2001, 183:4588-4598.
34. Marketon M.M., DePaolo R.W., DeBord K.L., Jabri B., Schneewind O. Plague bacteria target immune cells during infection. Science 2005, 309:1739-1741.
35. Brubaker R.R. Interleukin-10 and the inhibition of innate immunity to yersiniae: roles of Yops and LcrV (V antigen). Infect Immun 2003, 3673-3681.
36. Nakajima R., Motin V.L., Brubaker R.R. Suppression of cytokines in mice by protein A-V antigen fusion peptide and restoration of synthesis by active immunization. Infect Immun 1995, 63:3021-3029.
37. DePaolo R.W., Tang F., Kim I.Y., Han M., Levine N., Ciletti N.A., et al. TLR6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 2008, 4:350-361.
38. Heath D.G., Anderson G.W., Mauro J.M., Welkos S.L., Andrews G.P., Adamovicz J.J., et al. Protection against experimental bubonic and pneumonic plague by a recombinant capsular F1-V antigen fusion protein vaccine. Vaccine 1998, 16:1131-1137.
39. Williamson E.D., Eley S.M., Griffin K.F., Green M., Russell P., Leary S.E., et al. A new improved sub-unit vaccine for plague: the basis of protection. FEMS Immunol Med Microbiol 1995, 12:223-230.
40. Williamson E.D., Packer P.J., Waters E.L., Simpson A.J., Dyer D., Hartings J., et al. Recombinant (F1+V) vaccine protects cynomolgus macaques against pneumonic plague. Vaccine 2011, 29:4771-4777.
41. Powell B.S., Andrews G.P., Enama J.T., Jendrek S., Bolt C., Worsham P., et al. Design and testing for a non-tagged F1-V fusion protein as vaccine antigen against bubonic and pneumonic plage. Biotechnol Prog 2005, 21:1490-1510.
42. Warren R., Lockman H., Barnewall R., Krile R., Blanco O.B., Vasconcelos D., et al. Cynomolgus macaque model for pneumonic plague. Microb Pathog 2011, 50:12-22.
43. Chichester J.A., Musiychuk K., Farrance C.E., Mett V., Lyons J., Mett V., et al. A single component two-valent LcrV-F1 vaccine protects non-human primates against pneumonic plague. Vaccine 2009, 27:3471-3474.
44. Goodin J.L., Powell B.S., Enama J.Y., Raab R.W., McKnown R.L., Coffman G.L., et al. Purification and characterization of a recombinant Yersinia pestis V-F1 "reversed" fusion protein for use as a new subunit vaccine against plague. Protein Expr Purif 2011, 76:136-144.
45. Overheim K.A., Depaolo R.W., Debord K.L., Morrin E.M., Anderson D.M., Green N.M., et al. LcrV plague vaccine with altered immunomodulatory properties. Infect Immun 2005, 73:5152-5159.
46. DeBord K.L., Anderson D.M., Marketon M.M., Overheim K.A., DePaolo R.W., Ciletti N.A., et al. Immunogenicity and protective immunity against bubonic and pneumonic plague by immunization of mice with the recombinant V10 antigen, a variant of LcrV. Infect Immun 2006, 74:4910-4914.
47. Quenee L.E., Ciletti N.A., Berube B.J., Krausz T., Elli D., Hermanas T., et al. Pneumonic plague in guinea pigs and its prevention by subunit vaccines. Am J Pathol 2011, 178:1689-1700.
48. Cornelius C.A., Quenee L.E., Elli D., Ciletti N.A., Schneewind O. V10 subunit vaccine protects cynomolgus macaques from lethal pneumonic plague. Infect Immun 2008, 76:5588-5597.
49. Quenee L.E., Berube B., Segal J., Elli D., Ciletti N.A., Anderson D.M., et al. Amino acid residues 196-225 of LcrV represent a plague protective epitope. Vaccine 2010, 28:1870-1876.
50. Doll J.M., Zeitz P.S., Ettestad P., Bucholtz A.L., Davis T., Gage K.L. Cat-transmitted fatal pneumonic plague in a person who traveled from Colorado to Arizona. Am J Trop Med Hyg 1994, 51:109-114.
51. Parkhill J., Wren B.W., Thompson N.R., Titball R.W., Holden M.T., Prentice M.B., et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 2001, 413:523-527.
52. Samoilova S.V., Samoilova L.V., Yezhov I.N., Drozdov I.G., Anisimov A.P. Virulence of pPst+ and pPst- strains of Yersinia pestis for guinea-pigs. J Med Microbiol 1996, 45:440-444.
53. Koster F., Perlin D.S., Park S., Brasel T., Gigliotti A., Barr E., et al. Milestones in progression of primary pneumonic plague in cynomolgus macaques. Infect Immun 2010, 78:2946-2955.
54. Layton R.C., Brasel T., Gigliotti A., Barr E., Storch S., Myers L., et al. Primary pneumonic plague in the African Green monkey as a model for treatment efficacy evaluation. J Med Primatol 2011, 40:6-17.
55. Layton R.C., Mega W., McDonald J.D., Brasel T.L., Barr E.B., Gigliotti A.P., et al. Levofloxacin cures experimental pneumonic plague in African Green monkeys. PLoS Negl Trop Dis 2011, 5:e959.
56. Williamson E.D., Vesey P.M., Gillhespy K.J., Eley S.M., Green M., Titball R.W. An IgG1 titre to the F1 and V antigens correlates with protection against plague in the mouse model. Clin Exp Immunol 1999, 116:107-114.
57. Motin V.L., Nakajima R., Smirvov G.B., Brubaker R.R. Passive immunity to yersiniae mediated by anti-recombinant V antigen and Protein A-V antigen fusion peptide. Infect Immun 1994, 62:4192-4201.
58. Sebbane F., Gardner D., Long D., Gowen B.B., Hinnebusch B.J. Kinetics of disease progression and host response in a rat model of bubonic plague. Am J Pathol 2005, 166:1427-1439.
59. Hill J., Leary S., Smither S., Best A., Petterson J., Forsberg A., et al. N255 is a key residue for recognition by a monoclonal antibody which protects against Yersinia pestis infection. Vaccine 2009, 27:7073-7079.