Mucosal Immunization with Live Attenuated Francisella novicida U112ΔiglB Protects against Pulmonary F. tularensis SCHU S4 in the Fischer 344 Rat Model

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Signarovitz, Aimee L ^a,b   Ray, Heather J ^a   Yu, Jieh Juen ^a   Guentzel, M N ^a   Chambers, James P ^a   Klose, Karl E ^a   Arulanandam, Bernard P ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; GAMMA INTERFERON; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; DISEASE CONTROL; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG POTENCY; FEMALE; FRANCISELLA; FRANCISELLA NOVICIDA; FRANCISELLA TULARENSIS; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IN VIVO STUDY; LD 50; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; NONHUMAN; RAT; SURVIVAL RATE; TULAREMIA; WILD TYPE;

ADMINISTRATION, ORAL; ANIMALS; BACTERIAL VACCINES; DISEASE MODELS, ANIMAL; FRANCISELLA TULARENSIS; HUMANS; IMMUNITY, MUCOSAL; IMMUNIZATION; INTERFERON-GAMMA; MICE; RATS; RATS, INBRED F344; SPECIES SPECIFICITY; TULAREMIA; VACCINES, ATTENUATED;

FRANCISELLA TULARENSIS; FRANCISELLA TULARENSIS SUBSP. NOVICIDA; RATTUS; RODENTIA;

EID: 84868113315     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047639     Document Type: Article

References (77)

1. Elkins KL, Bosio CM, Rhinehart-Jones TR, (1999) Importance of B cells, but not specific antibodies, in primary and secondary protective immunity to the intracellular bacterium Francisella tularensis live vaccine strain. Infect Immun 67: 6002-6007.
2. Bakshi CS, Malik M, Mahawar M, Kirimanjeswara GS, Hazlett KR, et al. (2008) An improved vaccine for prevention of respiratory tularemia caused by Francisella tularensis Schu S4 strain. Vaccine 26: 5276-5288.
3. Baron SD, Singh R, Metzger DW, (2007) Inactivated Francisella tularensis live vaccine strain protects against respiratory tularemia by intranasal vaccination in an immunoglobulin A-dependent fashion. Infect Immun 75: 2152-2162.
4. Chen W, Shen H, Webb A, KuoLee R, Conlan JW, (2003) 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 21: 3690-3700.
5. Pammit MA, Raulie EK, Lauriano CM, Klose KE, Arulanandam BP, (2006) Intranasal vaccination with a defined attenuated Francisella novicida strain induces gamma interferon-dependent antibody-mediated protection against tularemia. Infect Immun 74: 2063-2071.
6. Conlan JW, Shen H, Golovliov I, Zingmark C, Oyston PC, et al. (2010) 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 28: 1824-1831.
7. Ireland PM, Lebutt H, Thomas RM, Oyston PC, (2011) A Francisella tularensis SCHU S4 mutant deficient in {gamma}-glutamyl transferase activity induces protective immunity: characterisation of an attenuated vaccine candidate. Microbiology.
8. Quarry JE, Isherwood KE, Michell SL, Diaper H, Titball RW, et al. (2007) A Francisella tularensis subspecies novicida purF mutant, but not a purA mutant, induces protective immunity to tularemia in mice. Vaccine 25: 2011-2018.
9. Bitsaktsis C, Rawool DB, Li Y, Kurkure NV, Iglesias B, et al. (2009) 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 182: 4899-4909.
10. Downs CM, Coriell LL, et al. (1947) Studies on tularemia; the comparative susceptibility of various laboratory animals. J Immunol 56: 217-228.
11. Olsufiev NG, Emelyanova OS, Dunayeva TN, (1959) Comparative study of strains of B. tularense in the old and new world and their taxonomy. J Hyg Epidemiol Microbiol Immunol 3: 138-149.
12. Ray HJ, Chu P, Wu TH, Lyons CR, Murthy AK, et al. (2010) The Fischer 344 rat reflects human susceptibility to Francisella pulmonary challenge and provides a new platform for virulence and protection studies. PLoS One 5: e9952.
13. Wu TH, Zsemlye JL, Statom GL, Hutt JA, Schrader RM, et al. (2009) Vaccination of Fischer 344 rats against pulmonary infections by Francisella tularensis type A strains. Vaccine 27: 4684-4693.
14. Raymond CR, Conlan JW, (2009) Differential susceptibility of Sprague-Dawley and Fischer 344 rats to infection by Francisella tularensis. Microb Pathog 46: 231-234.
15. Hu K, Dou J, Yu F, He X, Yuan X, et al. (2011) An ocular mucosal administration of nanoparticles containing DNA vaccine pRSC-gD-IL-21 confers protection against mucosal challenge with herpes simplex virus type 1 in mice. Vaccine 29: 1455-1462.
16. Kweon MN, (2011) Sublingual mucosa: A new vaccination route for systemic and mucosal immunity. Cytokine 54: 1-5.
17. Song JH, Nguyen HH, Cuburu N, Horimoto T, Ko SY, et al. (2008) Sublingual vaccination with influenza virus protects mice against lethal viral infection. Proc Natl Acad Sci U S A 105: 1644-1649.
18. Cuburu N, Kweon MN, Hervouet C, Cha HR, Pang YY, et al. (2009) Sublingual immunization with nonreplicating antigens induces antibody-forming cells and cytotoxic T cells in the female genital tract mucosa and protects against genital papillomavirus infection. J Immunol 183: 7851-7859.
19. Huang CF, Wang CC, Wu TC, Wu KG, Lee CC, et al. (2008) Neonatal sublingual vaccination with Salmonella proteins and adjuvant cholera toxin or CpG oligodeoxynucleotides induces mucosal and systemic immunity in mice. J Pediatr Gastroenterol Nutr 46: 262-271.
20. Huang CF, Wu TC, Wu CC, Lee CC, Lo WT, et al. (2011) Sublingual vaccination with sonicated Salmonella proteins and mucosal adjuvant induces mucosal and systemic immunity and protects mice from lethal enteritis. APMIS 119: 468-478.
21. Tanaka N, Fukuyama S, Fukuiwa T, Kawabata M, Sagara Y, et al. (2007) Intranasal immunization with phosphorylcholine induces antigen specific mucosal and systemic immune responses in mice. Vaccine 25: 2680-2687.
22. Sabirov A, Metzger DW, (2006) Intranasal vaccination of neonatal mice with polysaccharide conjugate vaccine for protection against pneumococcal otitis media. Vaccine 24: 5584-5592.
23. Sabirov A, Metzger DW, (2008) Intranasal vaccination of infant mice induces protective immunity in the absence of nasal-associated lymphoid tissue. Vaccine 26: 1566-1576.
24. Hara H, Mouri A, Yonemitsu Y, Nabeshima T, Tabira T, (2011) Mucosal immunotherapy in an Alzheimer mouse model by recombinant Sendai virus vector carrying Abeta1-43/IL-10 cDNA. Vaccine 29: 7474-7482.
25. Hara H, Monsonego A, Yuasa K, Adachi K, Xiao X, et al. (2004) Development of a safe oral Aβ vaccine using recombinant adeno-associated virus vector for Alzheimer's disease. J Alzheimers Dis 6: 483-488.
26. Branger CG, Torres-Escobar A, Sun W, Perry R, Fetherston J, et al. (2009) Oral vaccination with LcrV from Yersinia pestis KIM delivered by live attenuated Salmonella enterica serovar Typhimurium elicits a protective immune response against challenge with Yersinia pseudotuberculosis and Yersinia enterocolitica. Vaccine 27: 5363-5370.
27. Ray HJ, Cong Y, Murthy AK, Selby DM, Klose KE, et al. (2009) Oral live vaccine strain-induced protective immunity against pulmonary Francisella tularensis challenge is mediated by CD4+ T cells and antibodies, including immunoglobulin A. Clin Vaccine Immunol 16: 444-452.
28. KuoLee R, Harris G, Conlan JW, Chen W, (2007) Oral immunization of mice with the live vaccine strain (LVS) of Francisella tularensis protects mice against respiratory challenge with virulent type A F. tularensis. Vaccine 25: 3781-3791.
29. Cazorla SI, Becker PD, Frank FM, Ebensen T, Sartori MJ, et al. (2008) Oral vaccination with Salmonella enterica as a cruzipain-DNA delivery system confers protective immunity against Trypanosoma cruzi. Infect Immun 76: 324-333.
30. Cha HR, Ko HJ, Kim ED, Chang SY, Seo SU, et al. (2011) Mucosa-associated epithelial chemokine/CCL28 expression in the uterus attracts CCR10+ IgA plasma cells following mucosal vaccination via estrogen control. J Immunol 187: 3044-3052.
31. Sedgmen BJ, Meeusen EN, Lofthouse SA, (2004) Alternative routes of mucosal immunization in large animals. Immunol Cell Biol 82: 10-16.
32. Wu TH, Hutt JA, Garrison KA, Berliba LS, Zhou Y, et al. (2005) Intranasal vaccination induces protective immunity against intranasal infection with virulent Francisella tularensis biovar A. Infect Immun 73: 2644-2654.
33. Pechous R, Celli J, Penoske R, Hayes SF, Frank DW, et al. (2006) Construction and characterization of an attenuated purine auxotroph in a Francisella tularensis live vaccine strain. Infect Immun 74: 4452-4461.
34. Twine S, Bystrom M, Chen W, Forsman M, Golovliov I, et al. (2005) 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 73: 8345-8352.
35. Jia Q, Lee BY, Bowen R, Dillon BJ, Som SM, et al. (2010) 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 78: 4341-4355.
36. Shen H, Harris G, Chen W, Sjostedt A, Ryden P, et al. (2010) Molecular immune responses to aerosol challenge with Francisella tularensis in mice inoculated with live vaccine candidates of varying efficacy. PLoS One 5: e13349.
37. Conlan JW, Shen H, Golovliov I, Zingmark C, Oyston PC, et al. (2009) 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.
38. Isherwood KE, Titball RW, Davies DH, Felgner PL, Morrow WJ, (2005) Vaccination strategies for Francisella tularensis. Adv Drug Deliv Rev 57: 1403-1414.
39. Powell HJ, Cong Y, Yu JJ, Guentzel MN, Berton MT, et al. (2008) CD4+ T cells are required during priming but not the effector phase of antibody-mediated IFN-γ-dependent protective immunity against pulmonary Francisella novicida infection. Immunol Cell Biol 86: 515-522.
40. Gosselin EJ, Gosselin DR, Lotz SA, (2005) Natural killer and CD8 T cells dominate the response by human peripheral blood mononuclear cells to inactivated Francisella tularensis live vaccine strain. Hum Immunol 66: 1039-1049.
41. Nallaparaju KC, Yu JJ, Rodriguez SA, Zogaj X, Manam S, et al. (2011) Evasion of IFN-gamma signaling by Francisella novicida is dependent upon Francisella outer membrane protein C. PLoS One 6: e18201.
42. Duckett NS, Olmos S, Durrant DM, Metzger DW, (2005) Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect Immun 73: 2306-2311.
43. Kiyono H, Fukuyama S, (2004) NALT- versus Peyer's-patch-mediated mucosal immunity. Nat Rev Immunol 4: 699-710.
44. Liu J, Zogaj X, Barker JR, Klose KE, (2007) Construction of targeted insertion mutations in Francisella tularensis subsp. novicida. Biotechniques 43: 487-490, 492.
45. Nano FE, Zhang N, Cowley SC, Klose KE, Cheung KK, et al. (2004) A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186: 6430-6436.
46. Barker JR, Chong A, Wehrly TD, Yu JJ, Rodriguez SA, et al. (2009) The Francisella tularensis pathogenicity island encodes a secretion system that is required for phagosome escape and virulence. Mol Microbiol 74: 1459-1470.
47. de Bruin OM, Duplantis BN, Ludu JS, Hare RF, Nix EB, et al. (2011) The biochemical properties of the Francisella pathogenicity island (FPI)-encoded proteins IglA, IglB, IglC, PdpB and DotU suggest roles in type VI secretion. Microbiology 157: 3483-3491.
48. Cong Y, Yu JJ, Guentzel MN, Berton MT, Seshu J, et al. (2009) Vaccination with a defined Francisella tularensis subsp. novicida pathogenicity island mutant (ΔiglB) induces protective immunity against homotypic and heterotypic challenge. Vaccine 27: 5554-5561.
49. Boltz-Nitulescu G, Wiltschke C, Holzinger C, Fellinger A, Scheiner O, et al. (1987) Differentiation of rat bone marrow cells into macrophages under the influence of mouse L929 cell supernatant. J Leukoc Biol 41: 83-91.
50. Engwall KS, Li AP, (1983) Isolation and Culturing of Rat Pulmonary Alveolar Macrophages. Journal of Tissue Culture Methods 8: 91-94.
51. Robinson AP, White TM, Mason DW, (1986) Macrophage heterogeneity in the rat as delineated by two monoclonal antibodies MRC OX-41 and MRC OX-42, the latter recognizing complement receptor type 3. Immunology 57: 239-247.
52. Dijkstra CD, Dopp EA, Joling P, Kraal G, (1985) The heterogeneity of mononuclear phagocytes in lymphoid organs: distinct macrophage subpopulations in the rat recognized by monoclonal antibodies ED1, ED2 and ED3. Immunology 54: 589-599.
53. Damoiseaux JG, Dopp EA, Neefjes JJ, Beelen RH, Dijkstra CD, (1989) Heterogeneity of macrophages in the rat evidenced by variability in determinants: two new anti-rat macrophage antibodies against a heterodimer of 160 and 95 kd (CD11/CD18). J Leukoc Biol 46: 556-564.
54. National Research Council (US) Committee on Animal Models for Testing Interventions Against Aerosolized Bioterrorism Agents (2006). Overcoming Challenges to Develop Countermeasures Against Aerosolized Bioterrorism Agents: Appropriate Use of Animal Models. Washington, DC: National Academies Press (US).
55. Dietrich G, Griot-Wenk M, Metcalfe IC, Lang AB, Viret JF, (2003) Experience with registered mucosal vaccines. Vaccine 21: 678-683.
56. Chong A, Wehrly TD, Nair V, Fischer ER, Barker JR, et al. (2008) The early phagosomal stage of Francisella tularensis determines optimal phagosomal escape and Francisella pathogenicity island protein expression. Infect Immun 76: 5488-5499.
57. Ludu JS, de Bruin OM, Duplantis BN, Schmerk CL, Chou AY, et al. (2008) The Francisella pathogenicity island protein PdpD is required for full virulence and associates with homologues of the type VI secretion system. J Bacteriol 190: 4584-4595.
58. Santic M, Molmeret M, Barker JR, Klose KE, Dekanic A, et al. (2007) A Francisella tularensis pathogenicity island protein essential for bacterial proliferation within the host cell cytosol. Cell Microbiol 9: 2391-2403.
59. Santic M, Molmeret M, Klose KE, Jones S, Kwaik YA, (2005) The Francisella tularensis pathogenicity island protein IglC and its regulator MglA are essential for modulating phagosome biogenesis and subsequent bacterial escape into the cytoplasm. Cell Microbiol 7: 969-979.
60. Schmerk CL, Duplantis BN, Wang D, Burke RD, Chou AY, et al. (2009) Characterization of the pathogenicity island protein PdpA and its role in the virulence of Francisella novicida. Microbiology 155: 1489-1497.
61. Barker JR, Klose KE, (2007) Molecular and genetic basis of pathogenesis in Francisella tularensis. Ann N Y Acad Sci 1105: 138-159.
62. de Bruin OM, Ludu JS, Nano FE, (2007) The Francisella pathogenicity island protein IglA localizes to the bacterial cytoplasm and is needed for intracellular growth. BMC Microbiol 7: 1.
63. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312: 1526-1530.
64. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, et al. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103: 1528-1533.
65. Bosio CM, Elkins KL, (2001) Susceptibility to secondary Francisella tularensis live vaccine strain infection in B-cell-deficient mice is associated with neutrophilia but not with defects in specific T-cell-mediated immunity. Infect Immun 69: 194-203.
66. Dreisbach VC, Cowley S, Elkins KL, (2000) Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon. Infect Immun 68: 1988-1996.
67. Cole LE, Shirey KA, Barry E, Santiago A, Rallabhandi P, et al. (2007) Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages. Infect Immun 75: 4127-4137.
68. Elkins KL, Cowley SC, Bosio CM, (2003) Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect 5: 135-142.
69. Salomonsson E, Kuoppa K, Forslund AL, Zingmark C, Golovliov I, et al. (2009) Reintroduction of two deleted virulence loci restores full virulence to the live vaccine strain of Francisella tularensis. Infect Immun 77: 3424-3431.
70. Tempel R, Lai XH, Crosa L, Kozlowicz B, Heffron F, (2006) Attenuated Francisella novicida transposon mutants protect mice against wild-type challenge. Infect Immun 74: 5095-5105.
71. West TE, Pelletier MR, Majure MC, Lembo A, Hajjar AM, et al. (2008) Inhalation of Francisella novicida ΔmglA causes replicative infection that elicits innate and adaptive responses but is not protective against invasive pneumonic tularemia. Microbes Infect 10: 773-780.
72. Mohapatra NP, Soni S, Bell BL, Warren R, Ernst RK, et al. (2007) Identification of an orphan response regulator required for the virulence of Francisella spp. and transcription of pathogenicity island genes. Infect Immun 75: 3305-3314.
73. Kadzhaev K, Zingmark C, Golovliov I, Bolanowski M, Shen H, et al. (2009) Identification of genes contributing to the virulence of Francisella tularensis SCHU S4 in a mouse intradermal infection model. PLoS One 4: e5463.
74. Kim TH, Pinkham JT, Heninger SJ, Chalabaev S, Kasper DL, (2011) Genetic modification of the O-polysaccharide of Francisella tularensis results in an avirulent live attenuated vaccine. J Infect Dis.
75. Qin A, Scott DW, Thompson JA, Mann BJ, (2009) Identification of an essential Francisella tularensis subsp. tularensis virulence factor. Infect Immun 77: 152-161.
76. Corr SC, Gahan CC, Hill C, (2008) M-cells: origin, morphology and role in mucosal immunity and microbial pathogenesis. FEMS Immunol Med Microbiol 52: 2-12.
77. Neutra MR, Mantis NJ, Kraehenbuhl JP, (2001) Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat Immunol 2: 1004-1009.