Macrophage replication screen identifies a novel Francisella hydroperoxide resistance protein involved in virulence

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Llewellyn, Anna C ^a,b   Jones, Crystal L ^a,b   Napier, Brooke A ^a,b   Bina, James E ^c   Weiss, David S ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HYDROPEROXIDE RESISTANCE PROTEIN; UNCLASSIFIED DRUG; HYDROGEN PEROXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DELETION MUTANT; ENZYME ACTIVITY; FRANCISELLA; FRANCISELLA HOLARCTICA; FRANCISELLA NOVICIDA; FRANCISELLA TULARENSIS; GENE IDENTIFICATION; GENE LOCATION; GENE REPLICATION; GENETIC SCREENING; MACROPHAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN ANALYSIS; SEQUENCE HOMOLOGY; ANIMAL; C57BL MOUSE; CELL LINE; FEMALE; GENETICS; GENOMIC ISLAND; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; VIRULENCE;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS; MUS; NEGIBACTERIA;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; FEMALE; FRANCISELLA; GENOMIC ISLANDS; HYDROGEN PEROXIDE; MACROPHAGES; MICE; MICE, INBRED C57BL; NADPH OXIDASE; REAL-TIME POLYMERASE CHAIN REACTION; VIRULENCE;

EID: 80052479082     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024201     Document Type: Article

References (119)

1. Oyston PC, (2008) Francisella tularensis: unravelling the secrets of an intracellular pathogen. J Med Microbiol 57: 921-930.
2. Saslow S, Eigelsbach H, Wilson H, Prior J, Carhart S, (1961) Tularemia vaccine study, II: respiratory challenge. Arch Intern Med 107: 702-714.
3. Keim P, Johansson A, Wagner DM, (2007) Molecular epidemiology, evolution, and ecology of Francisella. Ann N Y Acad Sci 1105: 30-66.
4. Nigrovic LE, Wingerter SL, (2008) Tularemia. Infect Dis Clin North Am22: 489-504, ix.
5. Sjostedt A, (2007) Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann N Y Acad Sci 1105: 1-29.
6. Darling RG, Catlett CL, Huebner KD, Jarrett DG, (2002) Threats in bioterrorism. I: CDC category A agents. Emerg Med Clin North Am 20: 273-309.
7. 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.
8. Golovliov I, Sjostedt A, Mokrievich A, Pavlov V, (2003) A method for allelic replacement in Francisella tularensis. FEMS Microbiol Lett 222: 273-280.
9. 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.
10. Nano FE, Schmerk C, (2007) The Francisella pathogenicity island. Ann N Y Acad Sci 1105: 122-137.
11. 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.
12. Gray CG, Cowley SC, Cheung KK, Nano FE, (2002) The identification of five genetic loci of Francisella novicida associated with intracellular growth. FEMS Microbiol Lett 215: 53-56.
13. 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.
14. Raynaud C, Meibom KL, Lety MA, Dubail I, Candela T, et al. (2007) Role of the wbt locus of Francisella tularensis in lipopolysaccharide O-antigen biogenesis and pathogenicity. Infect Immun 75: 536-541.
15. Sandstrom G, Lofgren S, Tarnvik A, (1988) A capsule-deficient mutant of Francisella tularensis LVS exhibits enhanced sensitivity to killing by serum but diminished sensitivity to killing by polymorphonuclear leukocytes. Infect Immun 56: 1194-1202.
16. Ramakrishnan G, Meeker A, Dragulev B, (2008) fslE is necessary for siderophore-mediated iron acquisition in Francisella tularensis Schu S4. J Bacteriol 190: 5353-5361.
17. Lenco J, Pavkova I, Hubalek M, Stulik J, (2005) Insights into the oxidative stress response in Francisella tularensis LVS and its mutant DeltaiglC1+2 by proteomics analysis. FEMS Microbiol Lett 246: 47-54.
18. Bakshi CS, Malik M, Regan K, Melendez JA, Metzger DW, et al. (2006) Superoxide dismutase B gene (sodB)-deficient mutants of Francisella tularensis demonstrate hypersensitivity to oxidative stress and attenuated virulence. J Bacteriol 188: 6443-6448.
19. Guina T, Radulovic D, Bahrami AJ, Bolton DL, Rohmer L, et al. (2007) MglA regulates Francisella tularensis subsp. novicida (Francisella novicida) response to starvation and oxidative stress. J Bacteriol 189: 6580-6586.
20. Moule MG, Monack DM, Schneider DS, (2010) Reciprocal analysis of Francisella novicida infections of a Drosophila melanogaster model reveal host-pathogen conflicts mediated by reactive oxygen and imd-regulated innate immune response. PLoS Pathog 6.
21. Dieppedale J, Sobral D, Dupuis M, Dubail I, Klimentova J, et al. (2011) Identification of a putative Chaperone Involved in Stress Resistance and Virulence in Francisella tularensis. Infect Immun.
22. Clarridge JE 3rd, Raich TJ, Sjosted A, Sandstrom G, Darouiche RO, et al. (1996) Characterization of two unusual clinically significant Francisella strains. J Clin Microbiol 34: 1995-2000.
23. Hollis DG, Weaver RE, Steigerwalt AG, Wenger JD, Moss CW, et al. (1989) Francisella philomiragia comb. nov. (formerly Yersinia philomiragia) and Francisella tularensis biogroup novicida (formerly Francisella novicida) associated with human disease. J Clin Microbiol 27: 1601-1608.
24. Titball RW, Petrosino JF, (2007) Francisella tularensis genomics and proteomics. Ann N Y Acad Sci 1105: 98-121.
25. Wayne Conlan J, Oyston PC, (2007) Vaccines against Francisella tularensis. Ann N Y Acad Sci 1105: 325-350.
26. Rohmer L, Fong C, Abmayr S, Wasnick M, Larson Freeman TJ, et al. (2007) Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol 8: R102.
27. Rick Lyons C, Wu TH, (2007) Animal models of Francisella tularensis infection. Ann N Y Acad Sci 1105: 238-265.
28. Frank DW, Zahrt TC, (2007) Genetics and genetic manipulation in Francisella tularensis. Ann N Y Acad Sci 1105: 67-97.
29. Qin A, Mann BJ, (2006) Identification of transposon insertion mutants of Francisella tularensis tularensis strain Schu S4 deficient in intracellular replication in the hepatic cell line HepG2. BMC Microbiol 6: 69.
30. Fujita H, Watanabe Y, Sato T, Ohara Y, Homma M, (1993) The entry and intracellular multiplication of Francisella tularensis in cultured cells: its correlation with virulence in experimental mice. Microbiol Immunol 37: 837-842.
31. Hall JD, Craven RR, Fuller JR, Pickles RJ, Kawula TH, (2007) Francisella tularensis replicates within alveolar type II epithelial cells in vitro and in vivo following inhalation. Infect Immun 75: 1034-1039.
32. Schulert GS, McCaffrey RL, Buchan BW, Lindemann SR, Hollenback C, et al. (2009) Francisella tularensis genes required for inhibition of the neutrophil respiratory burst and intramacrophage growth identified by random transposon mutagenesis of strain LVS. Infect Immun 77: 1324-1336.
33. Santic M, Molmeret M, Klose KE, Abu Kwaik Y, (2006) Francisella tularensis travels a novel, twisted road within macrophages. Trends Microbiol 14: 37-44.
34. Clemens DL, Horwitz MA, (2007) Uptake and intracellular fate of Francisella tularensis in human macrophages. Ann N Y Acad Sci 1105: 160-186.
35. McCaffrey RL, Schwartz JT, Lindemann SR, Moreland JG, Buchan BW, et al. (2010) Multiple mechanisms of NADPH oxidase inhibition by type A and type B Francisella tularensis. J Leukoc Biol 88: 791-805.
36. Mohapatra NP, Soni S, Rajaram MV, Dang PM, Reilly TJ, et al. (2010) Francisella acid phosphatases inactivate the NADPH oxidase in human phagocytes. J Immunol 184: 5141-5150.
37. Storz G, Tartaglia LA, Farr SB, Ames BN, (1990) Bacterial defenses against oxidative stress. Trends Genet 6: 363-368.
38. Halliwell B, Gutteridge JM, (1984) Lipid peroxidation, oxygen radicals, cell damage, and antioxidant therapy. Lancet 1: 1396-1397.
39. Girotti AW, (1998) Lipid hydroperoxide generation, turnover, and effector action in biological systems. J Lipid Res 39: 1529-1542.
40. Akaike T, Sato K, Ijiri S, Miyamoto Y, Kohno M, et al. (1992) Bactericidal activity of alkyl peroxyl radicals generated by heme-iron-catalyzed decomposition of organic peroxides. Arch Biochem Biophys 294: 55-63.
41. Splettstoesser WD, Schuff-Werner P, (2002) Oxidative stress in phagocytes-"the enemy within". Microsc Res Tech 57: 441-455.
42. Moslen MT, (1994) Reactive oxygen species in normal physiology, cell injury and phagocytosis. Adv Exp Med Biol 366: 17-27.
43. Lindgren H, Stenman L, Tarnvik A, Sjostedt A, (2005) The contribution of reactive nitrogen and oxygen species to the killing of Francisella tularensis LVS by murine macrophages. Microbes Infect 7: 467-475.
44. Lindgren H, Stenmark S, Chen W, Tarnvik A, Sjostedt A, (2004) Distinct roles of reactive nitrogen and oxygen species to control infection with the facultative intracellular bacterium Francisella tularensis. Infect Immun 72: 7172-7182.
45. Lee RK, Harris G, Conlan JW, Chen W, (2011) Role of neutrophils and NADPH phagocyte oxidase in host defense against respiratory infection with virulent Francisella tularensis in mice. Microbes Infect.
46. Kuolee R, Harris G, Conlan JW, Chen W, (2011) Role of neutrophils and NADPH phagocyte oxidase in host defense against respiratory infection with virulent Francisella tularensis in mice. Microbes Infect.
47. McCaffrey RL, Allen LA, (2006) Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. J Leukoc Biol 80: 1224-1230.
48. Lindgren H, Shen H, Zingmark C, Golovliov I, Conlan W, et al. (2007) Resistance of Francisella tularensis strains against reactive nitrogen and oxygen species with special reference to the role of KatG. Infect Immun 75: 1303-1309.
49. Melillo AA, Mahawar M, Sellati TJ, Malik M, Metzger DW, et al. (2009) Identification of Francisella tularensis live vaccine strain CuZn superoxide dismutase as critical for resistance to extracellularly generated reactive oxygen species. J Bacteriol 191: 6447-6456.
50. Weiss DS, Brotcke A, Henry T, Margolis JJ, Chan K, et al. (2007) In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci U S A 104: 6037-6042.
51. Su J, Yang J, Zhao D, Kawula TH, Banas JA, et al. (2007) Genome-wide identification of Francisella tularensis virulence determinants. Infect Immun 75: 3089-3101.
52. Kraemer PS, Mitchell A, Pelletier MR, Gallagher LA, Wasnick M, et al. (2009) Genome-wide screen in Francisella novicida for genes required for pulmonary and systemic infection in mice. Infect Immun 77: 232-244.
53. Sullivan JT, Jeffery EF, Shannon JD, Ramakrishnan G, (2006) Characterization of the siderophore of Francisella tularensis and role of fslA in siderophore production. J Bacteriol 188: 3785-3795.
54. Deng K, Blick RJ, Liu W, Hansen EJ, (2006) Identification of Francisella tularensis genes affected by iron limitation. Infect Immun 74: 4224-4236.
55. Kiss K, Liu W, Huntley JF, Norgard MV, Hansen EJ, (2008) Characterization of fig operon mutants of Francisella novicida U112. FEMS Microbiol Lett 285: 270-277.
56. Mongkolsuk S, Praituan W, Loprasert S, Fuangthong M, Chamnongpol S, (1998) Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J Bacteriol 180: 2636-2643.
57. Fuangthong M, Atichartpongkul S, Mongkolsuk S, Helmann JD, (2001) OhrR is a repressor of ohrA, a key organic hydroperoxide resistance determinant in Bacillus subtilis. J Bacteriol 183: 4134-4141.
58. Rince A, Giard JC, Pichereau V, Flahaut S, Auffray Y, (2001) Identification and characterization of gsp65, an organic hydroperoxide resistance (ohr) gene encoding a general stress protein in Enterococcus faecalis. J Bacteriol 183: 1482-1488.
59. Ochsner UA, Hassett DJ, Vasil ML, (2001) Genetic and physiological characterization of ohr, encoding a protein involved in organic hydroperoxide resistance in Pseudomonas aeruginosa. J Bacteriol 183: 773-778.
60. Shea RJ, Mulks MH, (2002) ohr, Encoding an organic hydroperoxide reductase, is an in vivo-induced gene in Actinobacillus pleuropneumoniae. Infect Immun 70: 794-802.
61. Dorsey CW, Tomaras AP, Actis LA, (2006) Sequence and organization of pMAC, an Acinetobacter baumannii plasmid harboring genes involved in organic peroxide resistance. Plasmid 56: 112-123.
62. Jenkins C, Samudrala R, Geary SJ, Djordjevic SP, (2008) Structural and functional characterization of an organic hydroperoxide resistance protein from Mycoplasma gallisepticum. J Bacteriol 190: 2206-2216.
63. Cussiol JR, Alegria TG, Szweda LI, Netto LE, (2010) Ohr (organic hydroperoxide resistance protein) possesses a previously undescribed activity, lipoyl-dependent peroxidase. J Biol Chem 285: 21943-21950.
64. Saikolappan S, Sasindran SJ, Yu HD, Baseman JB, Dhandayuthapani S, (2009) The Mycoplasma genitalium MG_454 gene product resists killing by organic hydroperoxides. J Bacteriol 191: 6675-6682.
65. Baron GS, Nano FE, (1998) MglA and MglB are required for the intramacrophage growth of Francisella novicida. Mol Microbiol 29: 247-259.
66. Baker CN, Hollis DG, Thornsberry C, (1985) Antimicrobial susceptibility testing of Francisella tularensis with a modified Mueller-Hinton broth. J Clin Microbiol 22: 212-215.
67. Chamberlain RE, (1965) Evaluation of Live Tularemia Vaccine Prepared in a Chemically Defined Medium. Appl Microbiol 13: 232-235.
68. Schaible UE, Kaufmann SHE, (2002) Studying trafficking of intracellular pathogens in antigen-presenting cells. Methods Microbiol 31: 3434-3360.
69. Gallagher LA, Ramage E, Jacobs MA, Kaul R, Brittnacher M, et al. (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci U S A 104: 1009-1014.
70. Anthony LS, Gu MZ, Cowley SC, Leung WW, Nano FE, (1991) Transformation and allelic replacement in Francisella spp. J Gen Microbiol 137: 2697-2703.
71. Gallagher LA, McKevitt M, Ramage ER, Manoil C, (2008) Genetic dissection of the Francisella novicida restriction barrier. J Bacteriol 190: 7830-7837.
72. Rodriguez SA, Davis G, Klose KE, (2009) Targeted gene disruption in Francisella tularensis by group II introns. Methods 49: 270-274.
73. LoVullo ED, Sherrill LA, Perez LL, Pavelka MS Jr, (2006) Genetic tools for highly pathogenic Francisella tularensis subsp. tularensis. Microbiology 152: 3425-3435.
74. Bina XR, Lavine CL, Miller MA, Bina JE, (2008) The AcrAB RND efflux system from the live vaccine strain of Francisella tularensis is a multiple drug efflux system that is required for virulence in mice. FEMS Microbiol Lett 279: 226-233.
75. Dringen R, Kussmaul L, Hamprecht B, (1998) Rapid clearance of tertiary butyl hydroperoxide by cultured astroglial cells via oxidation of glutathione. Glia 23: 139-145.
76. Chuchue T, Tanboon W, Prapagdee B, Dubbs JM, Vattanaviboon P, et al. (2006) ohrR and ohr are the primary sensor/regulator and protective genes against organic hydroperoxide stress in Agrobacterium tumefaciens. J Bacteriol 188: 842-851.
77. Lai XH, Golovliov I, Sjostedt A, (2004) Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis. Microb Pathog 37: 225-230.
78. Ahlund MK, Ryden P, Sjostedt A, Stoven S, (2010) A directed screen of Francisella novicida virulence determinants using Drosophila melanogaster. Infect Immun.
79. Brotcke A, Weiss DS, Kim CC, Chain P, Malfatti S, et al. (2006) Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis. Infect Immun 74: 6642-6655.
80. 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.
81. Pelegrin P, Barroso-Gutierrez C, Surprenant A, (2008) P2X7 receptor differentially couples to distinct release pathways for IL-1beta in mouse macrophage. J Immunol 180: 7147-7157.
82. Mariathasan S, Weiss DS, Dixit VM, Monack DM, (2005) Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J Exp Med 202: 1043-1049.
83. Atichartpongkul S, Loprasert S, Vattanaviboon P, Whangsuk W, Helmann JD, et al. (2001) Bacterial Ohr and OsmC paralogues define two protein families with distinct functions and patterns of expression. Microbiology 147: 1775-1782.
84. Hall JD, Woolard MD, Gunn BM, Craven RR, Taft-Benz S, et al. (2008) Infected-host-cell repertoire and cellular response in the lung following inhalation of Francisella tularensis Schu S4, LVS, or U112. Infect Immun 76: 5843-5852.
85. Craven RR, Hall JD, Fuller JR, Taft-Benz S, Kawula TH, (2008) Francisella tularensis invasion of lung epithelial cells. Infect Immun 76: 2833-2842.
86. Schmerk CL, Duplantis BN, Howard PL, Nano FE, (2009) A Francisella novicida pdpA mutant exhibits limited intracellular replication and remains associated with the lysosomal marker LAMP-1. Microbiology 155: 1498-1504.
87. 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.
88. Read A, Vogl SJ, Hueffer K, Gallagher LA, Happ GM, (2008) Francisella genes required for replication in mosquito cells. J Med Entomol 45: 1108-1116.
89. Asare R, Abu Kwaik Y, (2010) Molecular complexity orchestrates modulation of phagosome biogenesis and escape to the cytosol of macrophages by Francisella tularensis. Environ Microbiol.
90. 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.
91. Maier TM, Casey MS, Becker RH, Dorsey CW, Glass EM, et al. (2007) Identification of Francisella tularensis Himar1-based transposon mutants defective for replication in macrophages. Infect Immun 75: 5376-5389.
92. Meibom KL, Dubail I, Dupuis M, Barel M, Lenco J, et al. (2008) The heat-shock protein ClpB of Francisella tularensis is involved in stress tolerance and is required for multiplication in target organs of infected mice. Mol Microbiol 67: 1384-1401.
93. Rengarajan J, Murphy E, Park A, Krone CL, Hett EC, et al. (2008) Mycobacterium tuberculosis Rv2224c modulates innate immune responses. Proc Natl Acad Sci U S A 105: 264-269.
94. Sassetti CM, Rubin EJ, (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100: 12989-12994.
95. Beckett D, (2007) Biotin sensing: universal influence of biotin status on transcription. Annu Rev Genet 41: 443-464.
96. Asare R, Akimana C, Jones S, Abu Kwaik Y, (2010) Molecular bases of proliferation of Francisella tularensis in arthropod vectors. Environ Microbiol.
97. Payne SM, (1993) Iron acquisition in microbial pathogenesis. Trends Microbiol 1: 66-69.
98. Schaible UE, Kaufmann SH, (2004) Iron and microbial infection. Nat Rev Microbiol 2: 946-953.
99. Horzempa J, O'Dee DM, Shanks RM, Nau GJ, (2010) Francisella tularensis DeltapyrF mutants show that replication in nonmacrophages is sufficient for pathogenesis in vivo. Infect Immun 78: 2607-2619.
100. Oliveira MA, Guimaraes BG, Cussiol JR, Medrano FJ, Gozzo FC, et al. (2006) Structural insights into enzyme-substrate interaction and characterization of enzymatic intermediates of organic hydroperoxide resistance protein from Xylella fastidiosa. J Mol Biol 359: 433-445.
101. Lesniak J, Barton WA, Nikolov DB, (2002) Structural and functional characterization of the Pseudomonas hydroperoxide resistance protein Ohr. EMBO J 21: 6649-6659.
102. Cussiol JR, Alves SV, de Oliveira MA, Netto LE, (2003) Organic hydroperoxide resistance gene encodes a thiol-dependent peroxidase. J Biol Chem 278: 11570-11578.
103. Ochsner UA, Vasil ML, Alsabbagh E, Parvatiyar K, Hassett DJ, (2000) Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J Bacteriol 182: 4533-4544.
104. Steele KH, Baumgartner JE, Valderas MW, Roop RM, 2nd, (2010) Comparative study of the roles of AhpC and KatE as respiratory antioxidants in Brucella abortus 2308. J Bacteriol 192: 4912-4922.
105. Parsonage D, Karplus PA, Poole LB, (2008) Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin. Proc Natl Acad Sci U S A 105: 8209-8214.
106. 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.
107. Wolfram TJ, Leveque RM, Kastenmayer RJ, Mulks MH, (2009) Ohr, an in vivo-induced gene in Actinobacillus pleuropneumoniae, is located on a genomic island and requires glutathione-S-transferase for activity. FEMS Immunol Med Microbiol 57: 59-68.
108. Wehrly TD, Chong A, Virtaneva K, Sturdevant DE, Child R, et al. (2009) Intracellular biology and virulence determinants of Francisella tularensis revealed by transcriptional profiling inside macrophages. Cell Microbiol 11: 1128-1150.
109. Allen LA, McCaffrey RL, (2007) To activate or not to activate: distinct strategies used by Helicobacter pylori and Francisella tularensis to modulate the NADPH oxidase and survive in human neutrophils. Immunol Rev 219: 103-117.
110. 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 SchuS4 strain. Vaccine 26: 5276-5288.
111. Dubbs JM, Mongkolsuk S, (2007) Peroxiredoxins in bacterial antioxidant defense. Subcell Biochem 44: 143-193.
112. 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.
113. 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.
114. Lindemann SR, Peng K, Long ME, Hunt JR, Apicella MA, et al. (2011) Francisella tularensis Schu S4 O-antigen and capsule biosynthesis gene mutants induce early cell death in human macrophages. Infect Immun 79: 581-594.
115. Kanistanon D, Hajjar AM, Pelletier MR, Gallagher LA, Kalhorn T, et al. (2008) A Francisella mutant in lipid A carbohydrate modification elicits protective immunity. PLoS Pathog 4: e24.
116. Lauriano CM, Barker JR, Yoon SS, Nano FE, Arulanandam BP, et al. (2004) MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc Natl Acad Sci U S A 101: 4246-4249.
117. Cong Y, Yu JJ, Guentzel MN, Berton MT, Seshu J, et al. (2009) Vaccination with a defined Francisella tularensis subsp. novicida pathogenicity island mutant (DeltaiglB) induces protective immunity against homotypic and heterotypic challenge. Vaccine 27: 5554-5561.
118. Bell BL, Mohapatra NP, Gunn JS, (2010) Regulation of Virulence Gene Transcripts by the Francisella Orphan Response Regulator PmrA: Role of Phosphorylation and Evidence of MglA/SspA Interaction. Infect Immun.
119. 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.