Tularemia vaccine development: paralysis or progress?

References

• Forsman M, Sandstrom G, Sjostedt A. Analysis of 16S ribosomal DNA sequences of Francisella strains and utilization for determination of the phylogeny of the genus and for identification of strains by PCR. Int J Syst Bacteriol. 1994;44(1):38–46.
   Google Scholar
• Svensson K, Larsson P, Johansson D, Bystrom M, Forsman M, Johansson A. Evolution of subspecies of Francisella tularensis. J Bacteriol. 2005;187(11):3903–3908.
   Web of Science ®Google Scholar
• Tindall BJ, Rossello-Mora R, Busse HJ, Ludwig W, Kampfer P. Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol. 2010;60(pt 1):249–266.
   PubMed Web of Science ®Google Scholar
• Huber B, Escudero R, Busse HJ, et al. Description of Francisella hispaniensis sp. nov., isolated from human blood, reclassification of Francisella novicida (Larson et al. 1955) Olsufiev et al. 1959 as Francisella tularensis subsp. novicida comb. nov. and emended description of the genus Francisella. Int J Syst Evol Microbiol. 2010;60(pt 8):1887–1896.
   Google Scholar
• Ellis J, Oyston PC, Green M, Titball RW. Tularemia. Clin Microbiol Rev. 2002;15(4):631–646.
   PubMed Web of Science ®Google Scholar
• Keim P, Johansson A, Wagner DM. Molecular epidemiology, evolution, and ecology of Francisella. Ann N Y Acad Sci. 2007;1105:30–66.
   PubMed Web of Science ®Google Scholar
• Farlow J, Wagner DM, Dukerich M, et al. Francisella tularensis in the United States. Emerg Infect Dis. 2005;11(12):1835–1841.
   Web of Science ®Google Scholar
• Kugeler KJ, Mead PS, Janusz AM, et al. Molecular epidemiology of Francisella tularensis in the United States. Clin Infect Dis. 2009;48(7):863–870.
   PubMed Web of Science ®Google Scholar
• Gyuranecz M, Birdsell DN, Splettstoesser W, et al. Phylogeography of Francisella tularensis subsp. holarctica, Europe. Emerg Infect Dis. 2012;18(2):290–293.
   Web of Science ®Google Scholar
• Saslaw S, Carhart S. Studies with tularemia vaccines in volunteers. III. Serologic aspects following intracutaneous or respiratory challenge in both vaccinated and nonvaccinated volunteers. Am J Med Sci. 1961;241:689–699.
   PubMed Web of Science ®Google Scholar
• Saslaw S, Eigelsbach HT, Wilson HE, Prior JA, Carhart S. Tularemia vaccine study. I. Intracutaneous challenge. Arch Intern Med. 1961;107:689–701.
   PubMed Web of Science ®Google Scholar
• Evans ME, Gregory DW, Schaffner W, McGee ZA. Tularemia: a 30-year experience with 88 cases. Medicine. 1985;64(4):251–269.
   Web of Science ®Google Scholar
• Avery FW, Barnett TB. Pulmonary tularemia. A report of five cases and consideration of pathogenesis and terminology. Am Rev Respir Dis. 1967;95(4):584–591.
   Google Scholar
• Dennis DT, Inglesby TV, Henderson DA, et al. Tularemia as a biological weapon: medical and public health management. JAMA. 2001;285(21):2763–2773.
   PubMed Web of Science ®Google Scholar
• Oyston PC, Sjostedt A, Titball RW. Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat Rev Microbiol. 2004;2(12):967–978.
   Web of Science ®Google Scholar
• Kirimanjeswara GS, Olmos S, Bakshi CS, Metzger DW. Humoral and cell-mediated immunity to the intracellular pathogen Francisella tularensis. Immunol Rev. 2008;225:244–255.
   Google Scholar
• Forestal CA, Malik M, Catlett SV, et al. Francisella tularensis has a significant extracellular phase in infected mice. J Infect Dis. 2007;196(1):134–137.
   Web of Science ®Google Scholar
• Yu JJ, Raulie EK, Murthy AK, Guentzel MN, Klose KE, Arulanandam BP. The presence of infectious extracellular Francisella tularensis subsp. novicida in murine plasma after pulmonary challenge. Eur J Clin Microbiol Infect Dis. 2008;27(4):323–325.
   Web of Science ®Google Scholar
• Dreisbach VC, Cowley S, Elkins KL. Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon. Infect Immun. 2000;68(4):1988–1996.
   Web of Science ®Google Scholar
• Waag DM, McKee KT Jr, Sandstrom G, et al. Cell-mediated and humoral immune responses after vaccination of human volunteers with the live vaccine strain of Francisella tularensis. Clin Diagn Lab Immunol. 1995;2(2):143–148.
   PubMedGoogle Scholar
• Koskela P, Salminen A. Humoral immunity against Francisella tularensis after natural infection. J Clin Microbiol. 1985;22(6):973–979.
   Web of Science ®Google Scholar
• Kirimanjeswara GS, Golden JM, Bakshi CS, Metzger DW. Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J Immunol. 2007;179(1):532–539.
   Web of Science ®Google Scholar
• Baron SD, Singh R, Metzger DW. Inactivated Francisella tularensis live vaccine strain protects against respiratory tularemia by intranasal vaccination in an immunoglobulin A-dependent fashion. Infect Immun. 2007;75(5):2152–2162.
   Web of Science ®Google Scholar
• Rawool DB, Bitsaktsis C, Li Y, et al. Utilization of Fc receptors as a mucosal vaccine strategy against an intracellular bacterium, Francisella tularensis. J Immunol. 2008;180(8):5548–5557.
   Web of Science ®Google Scholar
• Rhinehart-Jones TR, Fortier AH, Elkins KL. Transfer of immunity against lethal murine Francisella infection by specific antibody depends on host gamma interferon and T cells. Infect Immun. 1994;62(8):3129–3137.
   Web of Science ®Google Scholar
• Mara-Koosham G, Hutt JA, Lyons CR, Wu TH. Antibodies contribute to effective vaccination against respiratory infection by type A Francisella tularensis strains. Infect Immun. 2011;79(4):1770–1778.
   PubMed Web of Science ®Google Scholar
• Klimpel GR, Eaves-Pyles T, Moen ST, et al. Levofloxacin rescues mice from lethal intra-nasal infections with virulent Francisella tularensis and induces immunity and production of protective antibody. Vaccine. 2008;26(52):6874–6882.
   Web of Science ®Google Scholar
• Bitsaktsis C, Rawool DB, Li Y, Kurkure NV, Iglesias B, Gosselin EJ. Differential requirements for protection against mucosal challenge with Francisella tularensis in the presence versus absence of cholera toxin B and inactivated F. tularensis. J Immunol. 2009;182(8):4899–4909.
   Google Scholar
• Drabick JJ, Narayanan RB, Williams JC, Leduc JW, Nacy CA. Passive protection of mice against lethal Francisella tularensis (live tularemia vaccine strain) infection by the sera of human recipients of the live tularemia vaccine. Am J Med Sci. 1994;308(2):83–87.
   Web of Science ®Google Scholar
• Fulop M, Mastroeni P, Green M, Titball RW. Role of antibody to lipopolysaccharide in protection against low- and high-virulence strains of Francisella tularensis. Vaccine. 2001;19(31):4465–4472.
   PubMed Web of Science ®Google Scholar
• Lavine CL, Clinton SR, Angelova-Fischer I, et al. Immunization with heat-killed Francisella tularensis LVS elicits protective antibody-mediated immunity. Eur J Immunol. 2007;37(11):3007–3020.
   PubMed Web of Science ®Google Scholar
• Sutherland MD, Goodyear AW, Troyer RM, Chandler JC, Dow SW, Belisle JT. Post-exposure immunization against Francisella tularensis membrane proteins augments protective efficacy of gentamicin in a mouse model of pneumonic tularemia. Vaccine. 2012;30(33):4977–4982.
   Web of Science ®Google Scholar
• Sjostedt A, Eriksson M, Sandstrom G, Tarnvik A. Various membrane proteins of Francisella tularensis induce interferon-gamma production in both CD4+ and CD8+ T cells of primed humans. Immunology. 1992;76(4):584–592.
   Web of Science ®Google Scholar
• Fortier AH, Polsinelli T, Green SJ, Nacy CA. Activation of macrophages for destruction of Francisella tularensis: identification of cytokines, effector cells, and effector molecules. Infect Immun. 1992;60(3):817–825.
   Web of Science ®Google Scholar
• Steiner DJ, Furuya Y, Metzger DW. Host-pathogen interactions and immune evasion strategies in Francisella tularensis pathogenicity. Infect Drug Resist. 2014;7:239–251.
   PubMed Web of Science ®Google Scholar
• Wu TH, Hutt JA, Garrison KA, Berliba LS, Zhou Y, Lyons CR. Intranasal vaccination induces protective immunity against intranasal infection with virulent Francisella tularensis biovar A. Infect Immun. 2005;73(5):2644–2654.
   Web of Science ®Google Scholar
• Wayne Conlan J, Shen H, Kuolee R, Zhao X, Chen W. Aerosol-, but not intradermal-immunization with the live vaccine strain of Francisella tularensis protects mice against subsequent aerosol challenge with a highly virulent type A strain of the pathogen by an alphabeta T cell- and interferon gamma- dependent mechanism. Vaccine. 2005;23(19):2477–2485.
   Web of Science ®Google Scholar
• Jones CL, Napier BA, Sampson TR, Llewellyn AC, Schroeder MR, Weiss DS. Subversion of host recognition and defense systems by Francisella spp. Microbiol Mol Biol Rev. 2012;76(2):383–404.
   Web of Science ®Google Scholar
• Bosio CM, Dow SW. Francisella tularensis induces aberrant activation of pulmonary dendritic cells. J Immunol. 2005;175(10):6792–6801.
   Web of Science ®Google Scholar
• Hall JD, Craven RR, Fuller JR, Pickles RJ, Kawula TH. Francisella tularensis replicates within alveolar type II epithelial cells in vitro and in vivo following inhalation. Infect Immun. 2007;75(2):1034–1039.
   Web of Science ®Google Scholar
• Bar-Haim E, Gat O, Markel G, Cohen H, Shafferman A, Velan B. Interrelationship between dendritic cell trafficking and Francisella tularensis dissemination following airway infection. PLoS Pathog. 2008;4(11):e1000211.
   Web of Science ®Google Scholar
• Sjostedt A, Conlan JW, North RJ. Neutrophils are critical for host defense against primary infection with the facultative intracellular bacterium Francisella tularensis in mice and participate in defense against reinfection. Infect Immun. 1994;62(7):2779–2783.
   Web of Science ®Google Scholar
• KuoLee R, Harris G, Conlan JW, Chen W. Role of neutrophils and NADPH phagocyte oxidase in host defense against respiratory infection with virulent Francisella tularensis in mice. Microbes Infect. 2011;13(5):447–456.
   Web of Science ®Google Scholar
• De Pascalis R, Taylor BC, Elkins KL. Diverse myeloid and lymphoid cell subpopulations produce gamma interferon during early innate immune responses to Francisella tularensis live vaccine strain. Infect Immun. 2008;76(9):4311–4321.
   Web of Science ®Google Scholar
• Lopez MC, Duckett NS, Baron SD, Metzger DW. Early activation of NK cells after lung infection with the intracellular bacterium, Francisella tularensis LVS. Cell Immunol. 2004;232(1–2):75–85.
   Web of Science ®Google Scholar
• Gosselin EJ, Gosselin DR, Lotz SA. Natural killer and CD8 T cells dominate the response by human peripheral blood mononuclear cells to inactivated Francisella tularensis live vaccine strain. Hum Immunol. 2005;66(10):1039–1049.
   Web of Science ®Google Scholar
• Bokhari SM, Kim KJ, Pinson DM, Slusser J, Yeh HW, Parmely MJ. NK cells and gamma interferon coordinate the formation and function of hepatic granulomas in mice infected with the Francisella tularensis live vaccine strain. Infect Immun. 2008;76(4):1379–1389.
   PubMed Web of Science ®Google Scholar
• Cowley SC, Elkins KL. Immunity to Francisella. Front Microbiol. 2011;2:26.
   PubMed Web of Science ®Google Scholar
• Koskela P, Herva E. Cell-mediated immunity against Francisella tularensis after natural infection. Scand J Infect Dis. 1980;12(4):281–287.
   PubMed Web of Science ®Google Scholar
• Surcel HM, Syrjala H, Karttunen R, Tapaninaho S, Herva E. Development of Francisella tularensis antigen responses measured as T-lymphocyte proliferation and cytokine production (tumor necrosis factor alpha, gamma interferon, and interleukin-2 and -4) during human tularemia. Infect Immun. 1991;59(6):1948–1953.
   Web of Science ®Google Scholar
• El Sahly HM, Atmar RL, Patel SM, et al. Safety, reactogenicity and immunogenicity of Francisella tularensis live vaccine strain in humans. Vaccine. 2009;27(36):4905–4911.
   PubMed Web of Science ®Google Scholar
• Hepburn MJ, Simpson AJ. Tularemia: current diagnosis and treatment options. Expert Rev Anti Infect Ther. 2008;6(2):231–240.
   PubMed Web of Science ®Google Scholar
• Eigelsbach HT, Downs CM. Prophylactic effectiveness of live and killed tularemia vaccines. I. Production of vaccine and evaluation in the white mouse and guinea pig. J Immunol. 1961;87:415–425.
   PubMed Web of Science ®Google Scholar
• Hornick RB, Eigelsbach HT. Aerogenic immunization of man with live tularemia vaccine. Bacteriol Rev. 1966;30(3):532–538.
   PubMedGoogle Scholar
• Hartley G, Taylor R, Prior J, et al. Grey variants of the live vaccine strain of Francisella tularensis lack lipopolysaccharide O-antigen, show reduced ability to survive in macrophages and do not induce protective immunity in mice. Vaccine. 2006;24(7):989–996.
   Web of Science ®Google Scholar
• Bakshi CS, Malik M, Mahawar M, et al. An improved vaccine for prevention of respiratory tularemia caused by Francisella tularensis SchuS4 strain. Vaccine. 2008;26(41):5276–5288.
   Web of Science ®Google Scholar
• Foshay L. A comparative study of the treatment of tularemia with immune serum, hyperimmune serum and streptomycin. Am J Med. 1946;1:180–188.
   PubMed Web of Science ®Google Scholar
• Foshay L, Hesselbrock WH, Wittenberg HJ, Rodenberg AH. Vaccine prophylaxis against tularemia in man. Am J Public Health Nations Health. 1942;32(10):1131–1145.
   Google Scholar
• Nutter JE. Effect of vaccine, route, and schedule on antibody response of rabbits to Pasteurella tularensis. Appl Microbiol. 1969;17(3):355–359.
   Google Scholar
• Eyles JE, Hartley MG, Laws TR, Oyston PC, Griffin KF, Titball RW. Protection afforded against aerosol challenge by systemic immunisation with inactivated Francisella tularensis live vaccine strain (LVS). Microb Pathog. 2008;44(2):164–168.
   Web of Science ®Google Scholar
• Bevanger L, Maeland JA, Naess AI. Agglutinins and antibodies to Francisella tularensis outer membrane antigens in the early diagnosis of disease during an outbreak of tularemia. J Clin Microbiol. 1988;26(3):433–437.
   Web of Science ®Google Scholar
• Havlasova J, Hernychova L, Halada P, et al. Mapping of immunoreactive antigens of Francisella tularensis live vaccine strain. Proteomics. 2002;2(7):857–867.
   Web of Science ®Google Scholar
• Sjostedt A, Sandstrom G, Tarnvik A. Several membrane polypeptides of the live vaccine strain Francisella tularensis LVS stimulate T cells from naturally infected individuals. J Clin Microbiol. 1990;28(1):43–48.
   Web of Science ®Google Scholar
• Conlan JW, Shen H, Webb A, Perry MB. Mice vaccinated with the O-antigen of Francisella tularensis LVS lipopolysaccharide conjugated to bovine serum albumin develop varying degrees of protective immunity against systemic or aerosol challenge with virulent type A and type B strains of the pathogen. Vaccine. 2002;20(29–30):3465–3471.
   Web of Science ®Google Scholar
• Fulop M, Manchee R, Titball R. Role of lipopolysaccharide and a major outer membrane protein from Francisella tularensis in the induction of immunity against tularemia. Vaccine. 1995;13(13):1220–1225.
   PubMed Web of Science ®Google Scholar
• Huntley JF, Conley PG, Rasko DA, Hagman KE, Apicella MA, Norgard MV. Native outer membrane proteins protect mice against pulmonary challenge with virulent type A Francisella tularensis. Infect Immun. 2008;76(8):3664–3671.
   Web of Science ®Google Scholar
• Thomas RM, Titball RW, Oyston PC, et al. The immunologically distinct O antigens from Francisella tularensis subspecies tularensis and Francisella novicida are both virulence determinants and protective antigens. Infect Immun. 2007;75(1):371–378.
   Web of Science ®Google Scholar
• Apicella MA, Post DM, Fowler AC, et al. Identification, characterization and immunogenicity of an O-antigen capsular polysaccharide of Francisella tularensis. PLoS One. 2010;5(7):e11060.
   Web of Science ®Google Scholar
• Chiavolini D, Weir S, Murphy JR, Wetzler LM. Neisseria meningitidis PorB, a toll-like receptor 2 ligand, improves the capacity of Francisella tularensis lipopolysaccharide to protect mice against experimental tularemia. Clin Vaccine Immunol. 2008;15(9):1322–1329.
   PubMedGoogle Scholar
• Prior JL, Prior RG, Hitchen PG, et al. Characterization of the O antigen gene cluster and structural analysis of the O antigen of Francisella tularensis subsp. tularensis. J Med Microbiol. 2003;52(pt 10):845–851.
   Web of Science ®Google Scholar
• Golovliov I, Ericsson M, Akerblom L, Sandstrom G, Tarnvik A, Sjostedt A. Adjuvanticity of ISCOMs incorporating a T cell-reactive lipoprotein of the facultative intracellular pathogen Francisella tularensis. Vaccine. 1995;13(3):261–267.
   Google Scholar
• Ashtekar AR, Katz J, Xu Q, Michalek SM. A mucosal subunit vaccine protects against lethal respiratory infection with Francisella tularensis LVS. PLoS One. 2012;7(11):e50460.
   Web of Science ®Google Scholar
• Hickey AJ, Hazlett KR, Kirimanjeswara GS, Metzger DW. Identification of Francisella tularensis outer membrane protein A (FopA) as a protective antigen for tularemia. Vaccine. 2011;29(40):6941–6947.
   PubMed Web of Science ®Google Scholar
• da Silva AJ, Zangirolami TC, Novo-Mansur MT, Giordano Rde C, Martins EA. Live bacterial vaccine vectors: an overview. Braz J Microbiol. 2015;45(4):1117–1129.
   Web of Science ®Google Scholar
• Ura T, Okuda K, Shimada M. Developments in viral vector-based vaccines. Vaccines (Basel). 2014;2(3):624–641.
   PubMedGoogle Scholar
• Shahabi V, Maciag PC, Rivera S, Wallecha A. Live, attenuated strains of Listeria and Salmonella as vaccine vectors in cancer treatment. Bioeng Bugs. 2010;1(4):235–243.
   PubMedGoogle Scholar
• Bermudez-Humaran LG, Kharrat P, Chatel JM, Langella P. Lactococci and lactobacilli as mucosal delivery vectors for therapeutic proteins and DNA vaccines. Microb Cell Fact. 2011;10(suppl 1):S4.
   PubMed Web of Science ®Google Scholar
• Mielcarek N, Debrie AS, Raze D, et al. Attenuated Bordetella pertussis: new live vaccines for intranasal immunisation. Vaccine. 2006;24(suppl 2):S2–S54.
   Google Scholar
• Matsuo K, Yasutomi Y. Mycobacterium bovis Bacille Calmette-Guerin as a vaccine vector for global infectious disease control. Tuberc Res Treat. 2011;2011:574591.
   PubMedGoogle Scholar
• Jia Q, Lee BY, Clemens DL, Bowen RA, Horwitz MA. Recombinant attenuated Listeria monocytogenes vaccine expressing Francisella tularensis IglC induces protection in mice against aerosolized type A F. tularensis. Vaccine. 2009;27(8):1216–1229.
   Google Scholar
• Fulop M, Manchee R, Titball R. Role of two outer membrane antigens in the induction of protective immunity against Francisella tularensis strains of different virulence. FEMS Immunol Med Microbiol. 1996;13(3):245–247.
   Google Scholar
• Banik S, Mansour AA, Suresh RV, et al. Development of a multivalent subunit vaccine against tularemia using tobacco mosaic virus (TMV) based delivery system. PLoS One. 2015;10(6):e0130858.
   PubMed Web of Science ®Google Scholar
• Iglesias BV, Bitsaktsis C, Pham G, et al. Multiple mechanisms mediate enhanced immunity generated by mAb-inactivated F. tularensis immunogen. Immunol Cell Biol. 2013;91(2):139–148.
   Web of Science ®Google Scholar
• Bitsaktsis C, Iglesias BV, Li Y, et al. Mucosal immunization with an unadjuvanted vaccine that targets Streptococcus pneumoniae PspA to human Fcgamma receptor type I protects against pneumococcal infection through complement- and lactoferrin-mediated bactericidal activity. Infect Immun. 2012;80(3):1166–1180.
   PubMed Web of Science ®Google Scholar
• Geier H, Celli J. Phagocytic receptors dictate phagosomal escape and intracellular proliferation of Francisella tularensis. Infect Immun. 2011;79(6):2204–2214.
   Web of Science ®Google Scholar
• Bitsaktsis C, Babadjanova Z, Gosselin EJ. In vivo mechanisms involved in enhanced protection utilizing an Fc receptor-targeted mucosal vaccine platform in a bacterial vaccine and challenge model. Infect Immun. 2015;83(1):77–89.
   Web of Science ®Google Scholar
• Suresh RV, Ma Z, Sunagar R, et al. Preclinical testing of a vaccine candidate against tularemia. PLoS One. 2015;10(4):e0124326.
   Web of Science ®Google Scholar
• Franz BJ, Li Y, Bitsaktsis C, et al. Downmodulation of vaccine-induced immunity and protection against the intracellular bacterium Francisella tularensis by the inhibitory receptor FcgammaRIIB. J Immunol Res. 2015;2015:840842.
   Web of Science ®Google Scholar
• Liu MA. DNA vaccines: an historical perspective and view to the future. Immunol Rev. 2011;239(1):62–84.
   PubMed Web of Science ®Google Scholar
• Gregory SH, Mott S, Phung J, et al. Epitope-based vaccination against pneumonic tularemia. Vaccine. 2009;27(39):5299–5306.
   PubMed Web of Science ®Google Scholar
• Rotem S, Cohen O, Bar-Haim E, Bar-On L, Ehrlich S, Shafferman A. Protective immunity against lethal F. tularensis holarctica LVS provided by vaccination with selected novel CD8+ T cell epitopes. PLoS One. 2014;9(1):e85215.
   Web of Science ®Google Scholar
• Molins CR, Delorey MJ, Yockey BM, et al. Virulence differences among Francisella tularensis subsp. tularensis clades in mice. PLoS One. 2010;5(4):e10205.
   Web of Science ®Google Scholar
• Molins CR, Delorey MJ, Yockey BM, et al. Virulence difference between the prototypic Schu S4 strain (A1a) and Francisella tularensis A1a, A1b, A2 and type B strains in a murine model of infection. BMC Infect Dis. 2014;14:67.
   Web of Science ®Google Scholar
• Twine SM, Shen H, Kelly JF, Chen W, Sjostedt A, Conlan JW. Virulence comparison in mice of distinct isolates of type A Francisella tularensis. Microb Pathog. 2006;40(3):133–138.
   Web of Science ®Google Scholar
• Anderson RV, Crane DD, Bosio CM. Long lived protection against pneumonic tularemia is correlated with cellular immunity in peripheral, not pulmonary, organs. Vaccine. 2010;28(40):6562–6572.
   Web of Science ®Google Scholar
• Chen W, Shen H, Webb A, KuoLee R, Conlan JW. Tularemia in BALB/c and C57BL/6 mice vaccinated with Francisella tularensis LVS and challenged intradermally, or by aerosol with virulent isolates of the pathogen: protection varies depending on pathogen virulence, route of exposure, and host genetic background. Vaccine. 2003;21(25–26):3690–3700.
   PubMed Web of Science ®Google Scholar
• Eigelsbach HT, Braun W, Herring RD. Studies on the variation of bacterium tularense. J Bacteriol. 1951;61(5):557–569.
   Web of Science ®Google Scholar
• Soni S, Ernst RK, Muszynski A, et al. Francisella tularensis blue-gray phase variation involves structural modifications of lipopolysaccharide o-antigen, core and lipid a and affects intramacrophage survival and vaccine efficacy. Front Microbiol. 2010;1:129.
   Web of Science ®Google Scholar
• Zarrella TM, Singh A, Bitsaktsis C, et al. Host-adaptation of Francisella tularensis alters the bacterium’s surface-carbohydrates to hinder effectors of innate and adaptive immunity. PLoS One. 2011;6(7):e22335.
   Web of Science ®Google Scholar
• Eickhoff TC. The current status of BCG immunization against tuberculosis. Annu Rev Med. 1977;28:411–423.
   PubMed Web of Science ®Google Scholar
• Venkataswamy MM, Goldberg MF, Baena A, Chan J, Jacobs WR Jr, Porcelli SA. In vitro culture medium influences the vaccine efficacy of Mycobacterium bovis BCG. Vaccine. 2012;30(6):1038–1049.
   PubMed Web of Science ®Google Scholar
• Florio W, Batoni G, Esin S, et al. Influence of culture medium on the resistance and response of Mycobacterium bovis BCG to reactive nitrogen intermediates. Microbes Infect. 2006;8(2):434–441.
   PubMed Web of Science ®Google Scholar
• Cloete TE, de Bruyn EE. The effect of culture media on antigenic expression in sulfate-reducing bacteria. Curr Microbiol. 2001;42(5):305–309.
   Web of Science ®Google Scholar
• Geng T, Hahm BK, Bhunia AK. Selective enrichment media affect the antibody-based detection of stress-exposed Listeria monocytogenes due to differential expression of antibody-reactive antigens identified by protein sequencing. J Food Prot. 2006;69(8):1879–1886.
   Web of Science ®Google Scholar
• Geng T, Kim KP, Gomez R, et al. Expression of cellular antigens of Listeria monocytogenes that react with monoclonal antibodies C11E9 and EM-7G1 under acid-, salt- or temperature-induced stress environments. J Appl Microbiol. 2003;95(4):762–772.
   PubMed Web of Science ®Google Scholar
• Hahm BK, Bhunia AK. Effect of environmental stresses on antibody-based detection of Escherichia coli O157:H7, Salmonella enterica serotype enteritidis and Listeria monocytogenes. J Appl Microbiol. 2006;100(5):1017–1027.
   Google Scholar
• Walsh EJ, Moran AP. Influence of medium composition on the growth and antigen expression of Helicobacter pylori. J Appl Microbiol. 1997;83(1):67–75.
   Web of Science ®Google Scholar
• Hazlett KR, Caldon SD, McArthur DG, et al. Adaptation of Francisella tularensis to the mammalian environment is governed by cues which can be mimicked in vitro. Infect Immun. 2008;76(10):4479–4488.
   Web of Science ®Google Scholar
• Singh A, Rahman T, Malik M, et al. Discordant results obtained with Francisella tularensis during in vitro and in vivo immunological studies are attributable to compromised bacterial structural integrity. PLoS One. 2013;8(3):e58513.
   Web of Science ®Google Scholar
• Loegering DJ, Drake JR, Banas JA, et al. Francisella tularensis LVS grown in macrophages has reduced ability to stimulate the secretion of inflammatory cytokines by macrophages in vitro. Microb Pathog. 2006;41(6):218–225.
   Web of Science ®Google Scholar
• Garcia-Pelayo MC, Bachy VS, Kaveh DA, Hogarth PJ. BALB/c mice display more enhanced BCG vaccine induced Th1 and Th17 response than C57BL/6 mice but have equivalent protection. Tuberculosis. 2015;95(1):48–53.
   Web of Science ®Google Scholar
• Hume EB, Cole N, Khan S, et al. A Staphylococcus aureus mouse keratitis topical infection model: cytokine balance in different strains of mice. Immunol Cell Biol. 2005;83(3):294–300.
   Web of Science ®Google Scholar
• Barbi J, Brombacher F, Satoskar AR. T cells from Leishmania major-susceptible BALB/c mice have a defect in efficiently up-regulating CXCR3 upon activation. J Immunol. 2008;181(7):4613–4620.
   Web of Science ®Google Scholar
• Twine S, Shen H, Harris G, et al. BALB/c mice, but not C57BL/6 mice immunized with a ΔclpB mutant of Francisella tularensis subspecies tularensis are protected against respiratory challenge with wild-type bacteria: association of protection with post-vaccination and post-challenge immune responses. Vaccine. 2012;30(24):3634–3645.
   PubMed Web of Science ®Google Scholar
• Huffnagle GB, Boyd MB, Street NE, Lipscomb MF. IL-5 is required for eosinophil recruitment, crystal deposition, and mononuclear cell recruitment during a pulmonary Cryptococcus neoformans infection in genetically susceptible mice (C57BL/6). J Immunol. 1998;160(5):2393–2400.
   PubMed Web of Science ®Google Scholar
• Hoag KA, Street NE, Huffnagle GB, Lipscomb MF. Early cytokine production in pulmonary Cryptococcus neoformans infections distinguishes susceptible and resistant mice. Am J Respir Cell Mol Biol. 1995;13(4):487–495.
   PubMed Web of Science ®Google Scholar
• De Pascalis R, Mittereder L, Chou AY, Kennett NJ, Elkins KL. Francisella tularensis vaccines elicit concurrent protective T- and B-cell immune responses in BALB/cByJ mice. PLoS One. 2015;10(5):e0126570.
   Web of Science ®Google Scholar
• Conlan JW, Shen H, Golovliov I, et al. Differential ability of novel attenuated targeted deletion mutants of Francisella tularensis subspecies tularensis strain SCHU S4 to protect mice against aerosol challenge with virulent bacteria: effects of host background and route of immunization. Vaccine. 2010;28(7):1824–1831.
   Web of Science ®Google Scholar
• Aronova NV, Pavlovich NV. [Comparative analysis of the immune response of a rabbit to antigens to live and killed Francisella species bacteria]. Mol Gen Mikrobiol Virusol. 2001;2:26–30. Russian.
   Google Scholar
• Rick Lyons C, Wu TH. Animal models of Francisella tularensis infection. Ann N Y Acad Sci. 2007;1105:238–265.
   Web of Science ®Google Scholar
• Nelson M, Lever MS, Savage VL, et al. Establishment of lethal inhalational infection with Francisella tularensis (tularaemia) in the common marmoset (Callithrix jacchus). Int J Exp Pathol. 2009;90(2):109–118.
   PubMed Web of Science ®Google Scholar
• Kadioglu A, Cuppone AM, Trappetti C, et al. Sex-based differences in susceptibility to respiratory and systemic pneumococcal disease in mice. J Infect Dis. 2011;204(12):1971–1979.
   PubMed Web of Science ®Google Scholar
• Shankar J, Restrepo A, Clemons KV, Stevens DA. Hormones and the resistance of women to paracoccidioidomycosis. Clin Microbiol Rev. 2011;24(2):296–313.
   Web of Science ®Google Scholar
• Frisancho-Kiss S, Nyland JF, Davis SE, et al. Sex differences in coxsackievirus B3-induced myocarditis: IL-12Rbeta1 signaling and IFN-gamma increase inflammation in males independent from STAT4. Brain Res. 2006;1126(1):139–147.
   Google Scholar
• Rohrbach BW, Westerman E, Istre GR. Epidemiology and clinical characteristics of tularemia in Oklahoma, 1979 to 1985. South Med J. 1991;84(9):1091–1096.
   Web of Science ®Google Scholar
• Sunagar R, Kumar S, Franz BJ, Gosselin EJ. 2016. Vaccination evokes gender-dependent protection against tularemia infection in C57BL6/Tac mice. Vaccine. In Press 2016.
   Google Scholar
• Engler RJ, Nelson MR, Klote MM, et al. Half- vs full-dose trivalent inactivated influenza vaccine (2004-2005): age, dose, and sex effects on immune responses. Arch Intern Med. 2008;168(22):2405–2414.
   Google Scholar
• Cook IF. Sexual dimorphism of humoral immunity with human vaccines. Vaccine. 2008;26(29–30):3551–3555.
   PubMed Web of Science ®Google Scholar
• Lorenzo ME, Hodgson A, Robinson DP, Kaplan JB, Pekosz A, Klein SL. Antibody responses and cross protection against lethal influenza A viruses differ between the sexes in C57BL/6 mice. Vaccine. 2011;29(49):9246–9255.
   PubMed Web of Science ®Google Scholar
• Daniels CW, Belosevic M. Serum antibody responses by male and female C57Bl/6 mice infected with Giardia muris. Clin Exp Immunol. 1994;97(3):424–429.
   Web of Science ®Google Scholar
• Griffin AJ, Crane DD, Wehrly TD, Bosio CM. Successful protection against tularemia in C57BL/6 mice is correlated with expansion of Francisella tularensis-specific effector T cells. Clin Vaccine Immunol. 2015;22(1):119–128.
   PubMed Web of Science ®Google Scholar
• Barrigan LM, Tuladhar S, Brunton JC, et al. Infection with Francisella tularensis LVS clpB leads to an altered yet protective immune response. Infect Immun. 2013;81(6):2028–2042.
   Web of Science ®Google Scholar
• Jia Q, Lee BY, Bowen R, Dillon BJ, Som SM, Horwitz MA. A Francisella tularensis live vaccine strain (LVS) mutant with a deletion in capB, encoding a putative capsular biosynthesis protein, is significantly more attenuated than LVS yet induces potent protective immunity in mice against F. tularensis challenge. Infect Immun. 2010;78(10):4341–4355.
   Web of Science ®Google Scholar
• Golovliov I, Twine SM, Shen H, Sjostedt A, Conlan W. A ΔclpB mutant of Francisella tularensis subspecies holarctica strain, FSC200, is a more effective live vaccine than F. tularensis LVS in a mouse respiratory challenge model of tularemia. PLoS One. 2013;8(11):e78671.
   Web of Science ®Google Scholar
• Straskova A, Spidlova P, Mou S, et al. Francisella tularensis type B ΔdsbA mutant protects against type A strain and induces strong inflammatory cytokine and Th1-like antibody response in vivo. Pathog Dis. 2015;73(8):ftv058.
   Web of Science ®Google Scholar
• Sebastian S, Dillon ST, Lynch JG, et al. A defined O-antigen polysaccharide mutant of Francisella tularensis live vaccine strain has attenuated virulence while retaining its protective capacity. Infect Immun. 2007;75(5):2591–2602.
   Web of Science ®Google Scholar
• Kim TH, Pinkham JT, Heninger SJ, Chalabaev S, Kasper DL. Genetic modification of the O-polysaccharide of Francisella tularensis results in an avirulent live attenuated vaccine. J Infect Dis. 2012;205(7):1056–1065.
   Web of Science ®Google Scholar
• Sanapala S, Yu JJ, Murthy AK, et al. Perforin- and granzyme-mediated cytotoxic effector functions are essential for protection against Francisella tularensis following vaccination by the defined F. tularensis subsp. novicida ΔfopC vaccine strain. Infect Immun. 2012;80(6):2177–2185.
   Web of Science ®Google Scholar
• Chu P, Cunningham AL, Yu JJ, et al. Live attenuated Francisella novicida vaccine protects against Francisella tularensis pulmonary challenge in rats and non-human primates. PLoS Pathog. 2014;10(10):e1004439.
   PubMed Web of Science ®Google Scholar
• Signarovitz AL, Ray HJ, Yu JJ, et al. Mucosal immunization with live attenuated Francisella novicida U112ΔiglB protects against pulmonary F. tularensis SCHU S4 in the Fischer 344 rat model. PLoS One. 2012;7(10):e47639.
   Web of Science ®Google Scholar
• Cunningham AL, Dang KM, Yu JJ, et al. Enhancement of vaccine efficacy by expression of a TLR5 ligand in the defined live attenuated Francisella tularensis subsp. novicida strain U112ΔiglB:fljB. Vaccine. 2014;32(40):5234–5240.
   PubMed Web of Science ®Google Scholar
• Qin A, Scott DW, Thompson JA, Mann BJ. Identification of an essential Francisella tularensis subsp. tularensis virulence factor. Infect Immun. 2009;77(1):152–161.
   PubMed Web of Science ®Google Scholar
• Rockx-Brouwer D, Chong A, Wehrly TD, et al. Low dose vaccination with attenuated Francisella tularensis strain SchuS4 mutants protects against tularemia independent of the route of vaccination. PLoS One. 2012;7(5):e37752.
   PubMed Web of Science ®Google Scholar
• Michell SL, Dean RE, Eyles JE, et al. Deletion of the Bacillus anthracis capB homologue in Francisella tularensis subspecies tularensis generates an attenuated strain that protects mice against virulent tularaemia. J Med Microbiol. 2010;59(pt 11):1275–1284.
   Web of Science ®Google Scholar
• Twine S, Bystrom M, Chen W, et al. A mutant of Francisella tularensis strain SCHU S4 lacking the ability to express a 58-kilodalton protein is attenuated for virulence and is an effective live vaccine. Infect Immun. 2005;73(12):8345–8352.
   PubMed Web of Science ®Google Scholar
• Ireland PM, LeButt H, Thomas RM, Oyston PC. A Francisella tularensis SCHU S4 mutant deficient in gamma-glutamyltransferase activity induces protective immunity: characterization of an attenuated vaccine candidate. Microbiology. 2011;157(pt 11):3172–3179.
   Google Scholar
• Reed DS, Smith LP, Cole KS, Santiago AE, Mann BJ, Barry EM. Live attenuated mutants of Francisella tularensis protect rabbits against aerosol challenge with a virulent type A strain. Infect Immun. 2014;82(5):2098–2105.
   PubMed Web of Science ®Google Scholar