The search for early markers of plague: Evidence for accumulation of soluble Yersinia pestis LcrV in bubonic and pneumonic mouse models of disease

FEMS Immunology and Medical Microbiology

Volumn 59, Issue 2, 2010, Pages 197-206

  Flashner, Yehuda ^a   Fisher, Morly ^a   Tidhar, Avital ^a   Mechaly, Adva ^a   Gur, David ^a   Halperin, Gideon ^a   Zahavy, Eran ^a   Mamroud, Emanuelle ^a   Cohen, Sara ^a  

^a ISRAEL INSTITUTE FOR BIOLOGICAL RESEARCH   (Israel)

Author keywords

Mouse model; Plague; Soluble F1; Soluble LcrV; Yersinia pestis

Indexed keywords

BACTERIAL ANTIGEN; UNCLASSIFIED DRUG; V ANTIGEN; BACTERIAL PROTEIN; BIOLOGICAL MARKER; CAF1 PROTEIN, YERSINIA PESTIS; LCRV PROTEIN, YERSINIA; PORE FORMING CYTOTOXIC PROTEIN; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; CONTROLLED STUDY; DISEASE COURSE; DISEASE MARKER; EARLY DIAGNOSIS; FEMALE; LUNG LAVAGE; MOUSE; NONHUMAN; PLAGUE; PNEUMONIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; SPLEEN; YERSINIA PESTIS; ANIMAL; CHEMISTRY; DISEASE MODEL; SERUM;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; BIOLOGICAL MARKERS; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODELS, ANIMAL; FEMALE; MICE; PLAGUE; PORE FORMING CYTOTOXIC PROTEINS; SERUM; VIRULENCE FACTORS;

EID: 77953600850     PISSN: 09288244     EISSN: 1574695X     Source Type: Journal    
DOI: 10.1111/j.1574-695X.2010.00687.x     Document Type: Article

References (55)

1. Agar SL, Sha J, Foltz SM, Erova TE, Walberg KG, Baze WB, Suarez G, Peterson JW Chopra AK (2009) Characterization of the rat pneumonic plague model: infection kinetics following aerosolization of Yersinia pestis CO92. Microbes Infect 11 : 205-214.
2. Anderson DM, Ciletti NA, Lee-Lewis H, Elli D, Segal J, DeBord KL, Overheim KA, Tretiakova M, Brubaker RR Schneewind O (2009) Pneumonic plague pathogenesis and immunity in brown Norway rats. Am J Pathol 174 : 910-921.
3. Anisimov AP, Lindler LE Pier GB (2004) Intraspecific diversity of Yersinia pestis. Clin Microbiol Rev 17 : 434-464.
4. Broms JE, Francis MS Forsberg A (2007) Diminished LcrV secretion attenuates Yersinia pseudotuberculosis virulence. J Bacteriol 189 : 8417-8429.
5. Brubaker RR (2003) Interleukin-10 and inhibition of innate immunity to Yersiniae: roles of Yops and LcrV (V antigen). Infect Immun 71 : 3673-3681.
6. Burrows TW Bacon GA (1956) The basis of virulence in Pasteurella pestis: an antigen determining virulence. Brit J Exp Pathol 37 : 481-493.
7. Butler T (1983) Plague and other Yersinia infections. Plenum Press
8. CDC (2000) Laboratory Manual of Plague Diagnostic Tests. Centers for Disease Control and Prevention, and World Health Organization
9. Chanteau S, Rabarijaona L, O'brien T, Rahalison L, Hager J, Boisier P, Burans J Rasolomaharo M (1998) F1 antigenaemia in bubonic plague patients, a marker of gravity and efficacy of therapy. T Roy Soc Trop Med H 92 : 572-573.
10. Chanteau S, Rahalison L, Ratsitorahina M et al. 2000) Early diagnosis of bubonic plague using F1 antigen capture ELISA assay and rapid immunogold dipstick. Int J Med Microbiol 290 : 279-283.
11. Chanteau S, Rahalison L, Ralafiarisoa L, Foulon J, Ratsitorahina M, Carniel E Nato F (2003) Development and testing of a rapid diagnostic test for bubonic and pneumonic plague. Lancet 361 : 211-216.
12. Cornelis GR, Boland, Boyd AP, Geuijen C, Iriarte M, Neyt C, Sory MP Stainier I (1998) The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol R 62 : 1315-1352.
13. Davies KJ, Fritz DL, Pitt ML, Welkos SL, Worsham PL Friedlander AM (1996) Pathology of experimental pneumonic plague produced by fraction 1-positive and fraction 1-negative Yersinia pestis in African green monkeys (Cereopithecus aethiops). Arch Pathol Lab Med 120 : 156-163.
14. DePaolo RW, Tang F, Kim I, Han M, Levin N, Ciletti N, Lin A, Anderson D, Schneewind O Jabri B (2008) Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4 : 350-361.
15. DeSilva B, Smith W, Weiner R, Kelley M, Smolec JM, Lee B, Khan M, Tacey R, Hill H Celniker A (2003) Recommendations for the bioanalytical method validation of ligand-binding assays to support pharmacokinetic assessments of macromolecules. Pharm Res 20 : 1885-1900.
16. Du Y, Rosqvist R Forsberg A (2002) Role of fraction 1 antigen of Yersinia pestis in inhibition of phagocytosis. Infect Immun 70 : 1453-1460.
17. Fields KA, Nilles ML, Cowan C Straley SC (1999) Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect Immun 67 : 5395-5408.
18. Flashner Y, Mamroud E, Tidhar A et al. 2004) Generation of Yersinia pestis attenuated strains by signature-tagged mutagenesis in search of novel vaccine candidates. Infect Immun 72 : 908-915.
19. Galvan EM, Lasaro MA Schifferli DM (2008) Capsular antigen fraction 1 and Pla modulate the susceptibility of Yersinia pestis to pulmonary antimicrobial peptides such as cathelicidin. Infect Immun 76 : 1456-1464.
20. Gomes-Solecki MJ, Savitt CAG, Rowehl R, Glass JD, Bliska JB Dattwyler R (2005) LcrV capture enzyme-linked immunosorbent assay for detection of Yersinia pestis from human samples. Clin Diagn Lab Immun 12 : 339-346.
21. Guglielmo-Viret V, Attree O, Blanco-Gros V Thullier P (2005) Comparison of electrochemiluminescence assay and ELISA for the detection of Clostridium botulinum type B neurotoxin. J Immunol Methods 301 : 164-172.
22. Haihong L, Wang H, Qiu J et al. 2009) Transcriptional profiling of a mice plague model: insights into interaction between Yersinia pestis and its host. J Basic Microb 49 : 92-99.
23. Heesemann J, Sing A Trulzsch K (2006) Yersinia's stratagem: targeting innate and adaptive immune defense. Curr Opin Microbiol 9 : 56-61.
24. ICH Topic Q2B (1996) Validation of analytical procedures: Methodology. Step 4: Consensus guidelines. The European Agency for the Evaluation of Medical Products, Human Medicines Evaluation Unit
25. Inglesby T et al. 2000) Plague as a biological weapon. J Am Med Assoc 283 : 2281 -2290.
26. Jarrett CO, Isherwood KE, Oyston PC, Fischer ER, Whiney AR, Kobayashi SD, DeLeo FR Hinnebusch BJ (2004) Transmission of Yersinia pestis from an infectious biofilm into flea vector. J Infect Dis 190 : 783-792.
27. Kobiler D, Weiss S, Levy H, Fisher M, Mechaly A, Pass A Altboum Z (2006) Protective antigen as a correlative marker for Anthrax in animal models. Infect Immun 74 : 5871-5876.
28. Kool JL (2005) Risk of person-to-person transmission of pneumonic plague. Clin Infect Dis 40 : 1166-1172.
29. Krakauer T Heath D (1998) Lack of IL-1 receptor antagonistic activity of the capsular F1 antigen of Yersinia pestis. Immunol Lett 60 : 137-142. (Pubitemid 28157257)
30. Mueller CA, Broz P, Muller SA, Ringler P, Erne-Brand F, Sorg I, Kuhn M, Engel A Cornelis GR (2005) The V antigen of Yersinia forms a distinct structure at the tip of injectosome needles. Science 310 : 674-676.
31. Nakajima R Brubaker RR (1993) Association between virulence of Yersinia pestis and suppression of gamma interferon and tumor necrosis factor alpha. Infect Immun 61 : 23-31.
32. Nakajima R, Motin VL Brubaker RR (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.
33. Nedialkov YA, Motin VL Brubaker RR (1997) Resistance to lipopolysaccharide mediated by the Yersinia pestis V antigen-polyhistidine fusion peptide: amplification of interleukin-10. Infect Immun 65 : 1196-1203.
34. Overheim KA, DePaolo RW, DeBord KL, Morrin EM, Anderson DM, Green NM, Brubaker RR, Jabri B Schneewind O (2005) LcrV plague vaccine with altered immunomodulatory properties. Infect Immun 73 : 5152-5159.
35. Perry RD Fetherston D (1997) Yersinia pestis - etiologic agent of plague. Clin Microbiol Rev 10 : 35-66.
36. Pettersson J, Holmstrom A, Hill J, Leary S, Frithz-Lindsten E, von Euler-Mattel A, Carlsson E, Titball R, Forsberg A Wolf-Watz H (1999) The V-antigen of Yersinia is surface exposed before target cell contact and involved in virulence protein translocation. Mol Microbiol 32 : 961-976.
37. Philipovskiy AV, Cowen C, Wulff-Strobel CR, Burnett SH, Kerschen EJ, Cohen DA, Kaplan AM Straley SC (2005) Antibody against V antigen prevents Yop-dependent growth of Y. pestis. Infect Immun 73 : 1532 1542.
38. Pollitzer R (1954) Plague. WHO
39. Pouliot K, Pan N, Wang S, Lu S, Lien E Goguen JD (2007) Evaluation of the role of LcrV-Toll-like receptor 2-mediated immunomodulation in the virulence of Yersinia pestis. Infect Immun 75 : 3571-3580.
40. Ratstorahina M, Chanteau S, Rahalison L, Ratsifasoamanana L Boisier P (2000) Epidemiological and diagnostic aspects of the outbreak of pneumonic plague in Madagascar. Lancet 355 : 111-113.
41. Reithmeier-Rost D, Hill J, Elvin SL, 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.
42. Rivera VR, Gamez FJ, Keener WK, White JA Poli MA (2006) Rapid detection of Clostridium botulinum toxins A, B, E, and F in clinical samples, selected food matrices, and buffer using paramagnetic bead-based electrochemiluminescence detection. Anal Biochem 353 : 248-256.
43. Sabhnani L, Manocha M, Sridevi K, Shashikiran D, Rayanade R Rao DN (2003) Developing subunit immunogens using B and T cell epitopes and their constructs derived from the F1 antigen of Yersinia pestis using novel delivery vehicles. FEMS Immunol Med Mic 38 : 215-229.
44. ++ response and virulence of Yersinia pestis. J Bacteriol 177 : 2530-2542.
45. Splettstoesser WD, Rahalison L, Grunow R, Neubauer H Chanteau S (2004) Evaluation of a standardized F1 capsular antigen capture ELISA test kit for the rapid diagnosis of plague. FEMS Immunol Med Mic 41 : 149-155.
46. Titball RW Williamson ED (2004) Yersinia pestis (plague) vaccines. Expert Opin Biol Th 4 : 965-973.
47. Viswanathan CT, Bansal S, Booth B, DeStefano AJ, Rose MJ, Sailstad J, Shah VP, Skelly JP, Swann PG Weiner R (2007) Workshop/conference report - quantitative bioanalytical methods validation and implementation: best practices for chromatographic and ligand binding assays. AAPS J 9 : E30-E42. (Pubitemid 46296546)
48. Welkos S, Friedlander AM, McDowell D, Weeks J Tobery S (1998) V antigen of Yersinia pestis inhibits neutrophil chemotaxis. Microb Pathogenesis 24 : 185-196.
49. White JE, Harrison DN, Quan TJ, Mullins JL, Barnes AM Cavanaugh DC (1978) Atypical plague bacilli isolated from rodents, fleas, and man. Am J Public Health 68 : 262 264.
50. Williams JE, Arntzen L, Tyndal GL Isaacson M (1986) Application of enzyme immunoassays for the confirmation of clinically suspect plague in Namibia, 1982. B World Health Organ 64 : 745-752.
51. Winter CC, Cherry WB Moody MD (1960) An unusual strain of Pasteurella pestis isolated from a fatal human case of plague. B World Health Organ 23 : 408-409.
52. Zauberman A, Cohen S, Levy Y, Halperin G, Lazar S, Velan B, Shafferman A, Flashner Y Mamroud E (2008) Neutralization of Y. pestis mediated macrophage cytotoxicity by anti-LcrV antibodies and its correlation with protective immunity in a mouse model of bubonic plague. Vaccine 26 : 1616-1625.
53. Zauberman A, Tidhar A, Levy Y, Bar-Haim E, Halperin G, Flashner Y, Cohen S, Shafferman A Mamroud E (2009) Yersinia pestis endowed with increased cytotoxicity is avirulent in a bubonic plague model and induces rapid protection against pneumonic plague. PLoS ONE 4 : e5938.
54. Zav'yalov VP, Chernovskaya TV, Navolotskaya EV, Karlyshev AV, MacIntyre S, Vasiliev AM Abramov VM (1995a) Specific high affinity binding of human interleukin 1β by Caf1A usher protein of Yersinia pestis. FEBS Lett 371 : 65-68.
55. Zav'yalov V, Denesyuk A, Zav'yalova G Korpela T (1995b) Molecular modeling of the steric structure of the envelope F1 antigen of Yersinia pestis. Immunol Lett 45 : 19-22.