Rapid Induction of Protective Immunity against Pneumonic Plague by Yersinia pestis Polymeric F1 and LcrV Antigens
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethics Statement
2.2. Animals
2.3. Animal Immunization with Purified Antigens
2.4. Characterization of the Serological Response
2.5. Mouse Infection
2.6. Characterization of the Mouse Model of the Pneumonic Plague
2.7. Statistical Analysis
3. Results
3.1. Rapid Protective Immunity Afforded by F1 and LcrV in the Mouse Model of the Pneumonic Plague
3.2. Kinetics of the Humoral Response Following Vaccination with F1 and LcrV
3.3. The Importance of the F1 Polymeric Structure for the Rapid Onset of Protective Immunity
3.4. Characterization of the Long-Term Protective Immunity Induced by a Single Vaccination with F1 and LcrV
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Butler, T. Plague and Other Yersinia Infections; Greenough, W., Merigan, T.C., Eds.; Plenum Medical Book Company: New York, NY, USA, 1983. [Google Scholar]
- Randremanana, R.; Andrianaivoarimanana, V.; Nikolay, B.; Ramasindrazana, B.; Paireau, J.; Ten Bosch, Q.A.; Rakotondramanga, J.M.; Rahajandraibe, S.; Rahelinirina, S.; Rakotomanana, F.; et al. Epidemiological characteristics of an urban plague epidemic in Madagascar, August-November, 2017: An outbreak report. Lancet Infect. Dis. 2019, 19, 537–545. [Google Scholar] [CrossRef]
- Kugeler, K.J.; Staples, J.E.; Hinckley, A.F.; Gage, K.L.; Mead, P.S. Epidemiology of human plague in the United States, 1900–2012. Emerg. Infect. Dis. 2015, 21, 16–22. [Google Scholar] [CrossRef]
- Kugeler, K.J.; Mead, P.S.; Campbell, S.B.; Nelson, C.A. Antimicrobial Treatment Patterns and Illness Outcome Among United States Patients With Plague, 1942–2018. Clin. Infect. Dis. 2020, 70, S20–S26. [Google Scholar] [CrossRef]
- Godfred-Cato, S.; Cooley, K.M.; Fleck-Derderian, S.; Becksted, H.A.; Russell, Z.; Meaney-Delman, D.; Mead, P.S.; Nelson, C.A. Treatment of Human Plague: A Systematic Review of Published Aggregate Data on Antimicrobial Efficacy, 1939–2019. Clin. Infect. Dis. 2020, 70, S11–S19. [Google Scholar] [CrossRef]
- Galimand, M.; Guiyoule, A.; Gerbaud, G.; Rasoamanana, B.; Chanteau, S.; Carniel, E.; Courvalin, P. Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N. Engl. J. Med. 1997, 337, 677–680. [Google Scholar] [CrossRef]
- Welch, T.J.; Fricke, W.F.; McDermott, P.F.; White, D.G.; Rosso, M.L.; Rasko, D.A.; Mammel, M.K.; Eppinger, M.; Rosovitz, M.J.; Wagner, D.; et al. Multiple antimicrobial resistance in plague: An emerging public health risk. PLoS ONE 2007, 2, e309. [Google Scholar] [CrossRef]
- Lei, C.; Kumar, S. Yersinia pestis antibiotic resistance: A systematic review. Osong Public Health Res. Perspect. 2022, 13, 24–36. [Google Scholar] [CrossRef]
- Zauberman, A.; Gur, D.; Levy, Y.; Aftalion, M.; Vagima, Y.; Tidhar, A.; Chitlaru, T.; Mamroud, E. Postexposure Administration of a Yersinia pestis Live Vaccine for Potentiation of Second-Line Antibiotic Treatment Against Pneumonic Plague. J. Infect. Dis. 2019, 220, 1147–1151. [Google Scholar] [CrossRef]
- Vagima, Y.; Gur, D.; Aftalion, M.; Moses, S.; Levy, Y.; Makovitzki, A.; Holtzman, T.; Oren, Z.; Segula, Y.; Fatelevich, E.; et al. Phage Therapy Potentiates Second-Line Antibiotic Treatment against Pneumonic Plague. Viruses 2022, 14, 688. [Google Scholar] [CrossRef]
- Levy, Y.; Flashner, Y.; Tidhar, A.; Zauberman, A.; Aftalion, M.; Lazar, S.; Gur, D.; Shafferman, A.; Mamroud, E. T cells play an essential role in anti-F1 mediated rapid protection against bubonic plague. Vaccine 2011, 29, 6866–6873. [Google Scholar] [CrossRef]
- Levy, Y.; Vagima, Y.; Tidhar, A.; Aftalion, M.; Gur, D.; Nili, U.; Chitlaru, T.; Zauberman, A.; Mamroud, E. Targeting of the Yersinia pestis F1 capsular antigen by innate-like B1b cells mediates a rapid protective response against bubonic plague. NPJ Vaccines 2018, 3, 52. [Google Scholar] [CrossRef]
- Williamson, E.D.; Stagg, A.J.; Eley, S.M.; Taylor, R.; Green, M.; Jones, S.M.; Titball, R.W. Kinetics of the immune response to the (F1+V) vaccine in models of bubonic and pneumonic plague. Vaccine 2007, 25, 1142–1148. [Google Scholar] [CrossRef]
- Holtzman, T.; Levy, Y.; Marcus, D.; Flashner, Y.; Mamroud, E.; Cohen, S.; Fass, R. Production and purification of high molecular weight oligomers of Yersinia pestis F1 capsular antigen released by high cell density culture of recombinant Escherichia coli cells carrying the caf1 operon. Microb. Cell Factories 2006, 5, P98. [Google Scholar] [CrossRef]
- 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. Immunogenicity of a Yersinia pestis vaccine antigen monomerized by circular permutation. Infect. Immun. 2006, 74, 6624–6631. [Google Scholar] [CrossRef]
- Petsch, D.; Anspach, F.B. Endotoxin removal from protein solutions. J. Biotechnol. 2000, 76, 97–119. [Google Scholar] [CrossRef]
- Leary, S.E.; Williamson, E.D.; Griffin, K.F.; Russell, P.; Eley, S.M.; Titball, R.W. Active immunization with recombinant V antigen from Yersinia pestis protects mice against plague. Infect. Immun. 1995, 63, 2854–2858. [Google Scholar] [CrossRef]
- Mechaly, A.; Vitner, E.B.; Levy, Y.; Gur, D.; Barlev-Gross, M.; Sittner, A.; Koren, M.; Levy, H.; Mamroud, E.; Fisher, M. Epitope Binning of Novel Monoclonal Anti F1 and Anti LcrV Antibodies and Their Application in a Simple, Short, HTRF Test for Clinical Plague Detection. Pathogens 2021, 10, 285. [Google Scholar] [CrossRef]
- Tidhar, A.; Flashner, Y.; Cohen, S.; Levi, Y.; Zauberman, A.; Gur, D.; Aftalion, M.; Elhanany, E.; Zvi, A.; Shafferman, A.; et al. The NlpD lipoprotein is a novel Yersinia pestis virulence factor essential for the development of plague. PLoS ONE 2009, 4, e7023. [Google Scholar] [CrossRef]
- Reed, L.J.; Muench, H. A Simple Method of Estimating Fifty Per Cent Endpoints12. Am. J. Epidemiol. 1938, 27, 493–497. [Google Scholar] [CrossRef]
- Lathem, W.W.; Crosby, S.D.; Miller, V.L.; Goldman, W.E. Progression of primary pneumonic plague: A mouse model of infection, pathology, and bacterial transcriptional activity. Proc. Natl. Acad. Sci. USA 2005, 102, 17786–17791. [Google Scholar] [CrossRef]
- Olson, R.M.; Anderson, D.M. Shift from primary pneumonic to secondary septicemic plague by decreasing the volume of intranasal challenge with Yersinia pestis in the murine model. PLoS ONE 2019, 14, e0217440. [Google Scholar] [CrossRef]
- Vagima, Y.; Zauberman, A.; Levy, Y.; Gur, D.; Tidhar, A.; Aftalion, M.; Shafferman, A.; Mamroud, E. Circumventing Y. pestis Virulence by Early Recruitment of Neutrophils to the Lungs during Pneumonic Plague. PLoS Pathog. 2015, 11, e1004893. [Google Scholar] [CrossRef]
- Gur, D.; Glinert, I.; Aftalion, M.; Vagima, Y.; Levy, Y.; Rotem, S.; Zauberman, A.; Tidhar, A.; Tal, A.; Maoz, S.; et al. Inhalational Gentamicin Treatment Is Effective Against Pneumonic Plague in a Mouse Model. Front. Microbiol. 2018, 9, 741. [Google Scholar] [CrossRef]
- Galimand, M.; Carniel, E.; Courvalin, P. Resistance of Yersinia pestis to antimicrobial agents. Antimicrob. Agents Chemother. 2006, 50, 3233–3236. [Google Scholar] [CrossRef]
- Andrianaivoarimanana, V.; Wagner, D.M.; Birdsell, D.N.; Nikolay, B.; Rakotoarimanana, F.; Randriantseheno, L.N.; Vogler, A.J.; Sahl, J.W.; Hall, C.M.; Somprasong, N.; et al. Transmission of Antimicrobial Resistant Yersinia pestis During a Pneumonic Plague Outbreak. Clin. Infect. Dis. 2022, 74, 695–702. [Google Scholar] [CrossRef]
- Elvin, S.J.; Eyles, J.E.; Howard, K.A.; Ravichandran, E.; Somavarappu, S.; Alpar, H.O.; Williamson, E.D. Protection against bubonic and pneumonic plague with a single dose microencapsulated sub-unit vaccine. Vaccine 2006, 24, 4433–4439. [Google Scholar] [CrossRef]
- Williamson, E.D.; Eley, S.M.; Stagg, A.J.; Green, M.; Russell, P.; Titball, R.W. A sub-unit vaccine elicits IgG in serum, spleen cell cultures and bronchial washings and protects immunized animals against pneumonic plague. Vaccine 1997, 15, 1079–1084. [Google Scholar] [CrossRef]
- Williamson, E.D.; Eley, S.M.; Stagg, A.J.; Green, M.; Russell, P.; Titball, R.W. A single dose sub-unit vaccine protects against pneumonic plague. Vaccine 2000, 19, 566–571. [Google Scholar] [CrossRef]
- Alugupalli, K.R. A distinct role for B1b lymphocytes in T cell-independent immunity. Curr. Top. Microbiol. Immunol. 2008, 319, 105–130. [Google Scholar] [CrossRef]
- Andrews, G.P.; Heath, D.G.; Anderson, G.W., Jr.; Welkos, S.L.; Friedlander, A.M. 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. 1996, 64, 2180–2187. [Google Scholar] [CrossRef]
- Derbise, A.; Hanada, Y.; Khalife, M.; Carniel, E.; Demeure, C.E. Complete Protection against Pneumonic and Bubonic Plague after a Single Oral Vaccination. PLoS Negl. Trop. Dis. 2015, 9, e0004162. [Google Scholar] [CrossRef] [PubMed]
- Feodorova, V.A.; Motin, V.L. Plague vaccines: Current developments and future perspectives. Emerg. Microbes Infect. 2012, 1, e36. [Google Scholar] [CrossRef] [PubMed]
- Sun, W.; Singh, A.K. Plague vaccine: Recent progress and prospects. NPJ Vaccines 2019, 4, 11. [Google Scholar] [CrossRef]
- Williamson, E.D.; Packer, P.J.; Waters, E.L.; Simpson, A.J.; Dyer, D.; Hartings, J.; Twenhafel, N.; Pitt, M.L. Recombinant (F1+V) vaccine protects cynomolgus macaques against pneumonic plague. Vaccine 2011, 29, 4771–4777. [Google Scholar] [CrossRef] [PubMed]
- 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. Flagellin-F1-V Fusion Protein Is an Effective Plague Vaccine in Mice and Two Species of Nonhuman Primates. Clin. Vaccine Immunol. 2009, 16, 21–28. [Google Scholar] [CrossRef] [PubMed]
- Anisimov, A.P.; Dentovskaya, S.V.; Panfertsev, E.A.; Svetoch, T.E.; Kopylov, P.; Segelke, B.W.; Zemla, A.; Telepnev, M.V.; Motin, V.L. Amino acid and structural variability of Yersinia pestis LcrV protein. Infect. Genet. Evol. 2010, 10, 137–145. [Google Scholar] [CrossRef] [PubMed]
- Wei, T.; Gong, J.; Qu, G.; Wang, M.; Xu, H. Interactions between Yersinia pestis V-antigen (LcrV) and human Toll-like receptor 2 (TLR2) in a modelled protein complex and potential mechanistic insights. BMC Immunol. 2019, 20, 48. [Google Scholar] [CrossRef]
- Moore, B.D.; Macleod, C.; Henning, L.; Krile, R.; Chou, Y.L.; Laws, T.R.; Butcher, W.A.; Moore, K.M.; Walker, N.J.; Williamson, E.D.; et al. Predictors of Survival after Vaccination in a Pneumonic Plague Model. Vaccines 2022, 10, 145. [Google Scholar] [CrossRef]
- Williamson, E.D.; Eley, S.M.; Griffin, K.F.; Green, M.; Russell, P.; Leary, S.E.; Oyston, P.C.; Easterbrook, T.; Reddin, K.M.; Robinson, A.; et al. A new improved sub-unit vaccine for plague: The basis of protection. FEMS Immunol. Med. Microbiol. 1995, 12, 223–230. [Google Scholar] [CrossRef]
- Zauberman, A.; Vagima, Y.; Tidhar, A.; Aftalion, M.; Gur, D.; Rotem, S.; Chitlaru, T.; Levy, Y.; Mamroud, E. Host Iron Nutritional Immunity Induced by a Live Yersinia pestis Vaccine Strain Is Associated with Immediate Protection against Plague. Front. Cell. Infect. Microbiol. 2017, 7, 277. [Google Scholar] [CrossRef]
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Aftalion, M.; Tidhar, A.; Vagima, Y.; Gur, D.; Zauberman, A.; Holtzman, T.; Makovitzki, A.; Chitlaru, T.; Mamroud, E.; Levy, Y. Rapid Induction of Protective Immunity against Pneumonic Plague by Yersinia pestis Polymeric F1 and LcrV Antigens. Vaccines 2023, 11, 581. https://doi.org/10.3390/vaccines11030581
Aftalion M, Tidhar A, Vagima Y, Gur D, Zauberman A, Holtzman T, Makovitzki A, Chitlaru T, Mamroud E, Levy Y. Rapid Induction of Protective Immunity against Pneumonic Plague by Yersinia pestis Polymeric F1 and LcrV Antigens. Vaccines. 2023; 11(3):581. https://doi.org/10.3390/vaccines11030581
Chicago/Turabian StyleAftalion, Moshe, Avital Tidhar, Yaron Vagima, David Gur, Ayelet Zauberman, Tzvi Holtzman, Arik Makovitzki, Theodor Chitlaru, Emanuelle Mamroud, and Yinon Levy. 2023. "Rapid Induction of Protective Immunity against Pneumonic Plague by Yersinia pestis Polymeric F1 and LcrV Antigens" Vaccines 11, no. 3: 581. https://doi.org/10.3390/vaccines11030581