Environmental adaptation of Francisella tularensis

Microbes and Infection

Volumn 11, Issue 10-11, 2009, Pages 828-834

  Hazlett, Karsten R O ^a   Cirillo, Kerry A ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

Adaptation; Gene expression; Molecular signatures; Select agents

Indexed keywords

CHAPERONE; IRON; MESSENGER RNA; RNA BINDING PROTEIN; SIDEROPHORE;

BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; ECOLOGY; ENVIRONMENTAL TEMPERATURE; EVOLUTIONARY ADAPTATION; FRANCISELLA TULARENSIS; GENE EXPRESSION; GENE REPRESSION; GRAM NEGATIVE BACTERIUM; HEAT SHOCK; HOST PATHOGEN INTERACTION; IRON METABOLISM; MICROARRAY ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; FRANCISELLA TULARENSIS; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS;

ARTHROPODA; FRANCISELLA TULARENSIS; MAMMALIA; PROTOZOA;

EID: 68849101852     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2009.06.001     Document Type: Review

References (55)

1. Oyston P.C., Sjostedt A., and Titball R.W. Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat. Rev. Microbiol. 2 (2004) 967-978
2. Petersen J.M., Mead P.S., and Schriefer M.E. Francisella tularensis: an arthropod-borne pathogen. Vet. Res. 40 (2009) 7
3. Abd H., Johansson T., Golovliov I., Sandstrom G., and Forsman M. Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl. Environ. Microbiol. 69 (2003) 600-606
4. Bar-Haim E., Gat O., Markel G., Cohen H., Shafferman A., and Velan B. Interrelationship between dendritic cell trafficking and Francisella tularensis dissemination following airway infection. PLoS Pathog. 4 (2008) e1000211
5. Forestal C.A., Malik M., Catlett S.V., Savitt A.G., Benach J.L., Sellati T.J., and Furie M.B. Francisella tularensis has a significant extracellular phase in infected mice. J. Infect. Dis. 196 (2007) 134-137
6. Thelaus J., Andersson A., Mathisen P., Forslund A.L., Noppa L., and Forsman M. Influence of nutrient status and grazing pressure on the fate of Francisella tularensis in lake water. FEMS Microbiol. Ecol 67 (2009) 69-80
7. Yu J.J., Raulie E.K., Murthy A.K., Guentzel M.N., Klose K.E., and Arulanandam B.P. The presence of infectious extracellular Francisella tularensis subsp. novicida in murine plasma after pulmonary challenge. Eur. J. Clin. Microbiol. Infect. Dis (2007)
8. Chong A., Wehrly T.D., Nair V., Fischer E.R., Barker J.R., Klose K.E., and Celli J. The early phagosomal stage of Francisella tularensis determines optimal phagosomal escape and Francisella pathogenicity island protein expression. Infect. Immun. 76 (2008) 5488-5499
9. de Bruin O.M., Ludu J.S., and Nano F.E. The Francisella pathogenicity island protein IglA localizes to the bacterial cytoplasm and is needed for intracellular growth. BMC. Microbiol. 7 (2007) 1
10. Wehrly T.D., Chong A., Virtaneva K., Sturdevant D.E., Child R., Edwards J.A., Brouwer D., Nair V., Fischer E.R., Wicke L., Curda A.J., Kupko Iii J.J., Martens C., Crane D.D., Bosio C.M., Porcella S.F., and Celli J. Intracellular biology and virulence determinants of Francisella tularensis revealed by transcriptional profiling inside macrophages. Cell Microbiol. (2009)
11. Kirillina O., Fetherston J.D., Bobrov A.G., Abney J., and Perry R.D. HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis. Mol. Microbiol. 54 (2004) 75-88
12. Perry R.D., Bobrov A.G., Kirillina O., Jones H.A., Pedersen L., Abney J., and Fetherston J.D. Temperature regulation of the hemin storage (Hms+) phenotype of Yersinia pestis is posttranscriptional. J. Bacteriol 186 (2004) 1638-1647
13. Schwan T.G., Piesman J., Golde W.T., Dolan M.C., and Rosa P.A. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. U.S.A 92 (1995) 2909-2913
14. Horzempa J., Carlson Jr. P.E., O'Dee D.M., Shanks R.M., and Nau G.J. Global transcriptional response to mammalian temperature provides new insight into Francisella tularensis pathogenesis. BMC. Microbiol. 8 (2008) 172
15. Ericsson M., Tarnvik A., Kuoppa K., Sandstrom G., and Sjostedt A. Increased synthesis of DnaK, GroEL, and GroES homologs by Francisella tularensis LVS in response to heat and hydrogen peroxide. Infect. Immun 62 (1994) 178-183
16. Lauriano C.M., Barker J.R., Yoon S.S., Nano F.E., Arulanandam B.P., Hassett D.J., and Klose K.E. MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc. Natl. Acad. Sci. U.S.A 101 (2004) 4246-4249
17. Read A., Vogl S.J., Hueffer K., Gallagher L.A., and Happ G.M. Francisella genes required for replication in mosquito cells. J. Med. Entomol 45 (2008) 1108-1116
18. Barker J.R., and Klose K.E. Molecular and genetic basis of pathogenesis in Francisella tularensis. Ann. N.Y. Acad. Sci 1105 (2007) 138-159
19. Meibom K.L., Dubail I., Dupuis M., Barel M., Lenco J., Stulik J., Golovliov I., Sjostedt A., and Charbit A. 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 (2008) 1384-1401
20. Rebeil R., Ernst R.K., Gowen B.B., Miller S.I., and Hinnebusch B.J. Variation in lipid A structure in the pathogenic yersiniae. Mol. Microbiol. 52 (2004) 1363-1373
21. Shaffer S.A., Harvey M.D., Goodlett D.R., and Ernst R.K. Structural heterogeneity and environmentally regulated remodeling of Francisella tularensis subspecies novicida lipid A characterized by tandem mass spectrometry. J. Am. Soc. Mass Spectrom 18 (2007) 1080-1092
22. Hajjar A.M., Harvey M.D., Shaffer S.A., Goodlett D.R., Sjostedt A., Edebro H., Forsman M., Bystrom M., Pelletier M., Wilson C.B., Miller S.I., Skerrett S.J., and Ernst R.K. Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect. Immun. 74 (2006) 6730-6738
23. Payne S.M. Iron acquisition in microbial pathogenesis. Trends Microbiol. 1 (1993) 66-69
24. Deng K., Blick R.J., Liu W., and Hansen E.J. Identification of Francisella tularensis genes affected by iron limitation. Infect. Immun. 74 (2006) 4224-4236
25. Hazlett K.R., Caldon S.D., McArthur D.G., Cirillo K.A., Kirimanjeswara G.S., Magguilli M.L., Malik M., Shah A., Broderick S., Golovliov I., Metzger D.W., Rajan K., Sellati T.J., and Loegering D.J. Adaptation of Francisella tularensis to the mammalian environment is governed by cues which can be mimicked in vitro. Infect. Immun 76 (2008) 4479-4488
26. Kiss K., Liu W., Huntley J.F., Norgard M.V., and Hansen E.J. Characterization of fig operon mutants of Francisella novicida U112. FEMS Microbiol. Lett. 285 (2008) 270-277
27. Lenco J., Hubalek M., Larsson P., Fucikova A., Brychta M., Macela A., and Stulik J. Proteomics analysis of the Francisella tularensis LVS response to iron restriction: induction of the F. tularensis pathogenicity island proteins IglABC. FEMS Microbiol. Lett. 269 (2007) 11-21
28. Ramakrishnan G., Meeker A., and Dragulev B. fslE is necessary for siderophore-mediated iron acquisition in Francisella tularensis Schu S4. J. Bacteriol. 190 (2008) 5353-5361
29. Sullivan J.T., Jeffery E.F., Shannon J.D., and Ramakrishnan G. Characterization of the siderophore of Francisella tularensis and role of fslA in siderophore production. J. Bacteriol. 188 (2006) 3785-3795
30. Buchan B.W., McCaffrey R.L., Lindemann S.R., Allen L.A., and Jones B.D. Identification of migR, a regulatory element of the Francisella tularensis Live Vaccine Strain iglABCD virulence operon required for normal replication and trafficking in macrophages. Infect. Immun (2009)
31. Brotcke A., and Monack D.M. Identification of fevR, a novel regulator of virulence gene expression in Francisella novicida. Infect. Immun. 76 (2008) 3473-3480
32. Golovliov I., Ericsson M., Sandstrom G., Tarnvik A., and Sjostedt A. Identification of proteins of Francisella tularensis induced during growth in macrophages and cloning of the gene encoding a prominently induced 23-kilodalton protein. Infect. Immun. 65 (1997) 2183-2189
33. Lenco J., Pavkova I., Hubalek M., and Stulik J. Insights into the oxidative stress response in Francisella tularensis LVS and its mutant DeltaiglC1 + 2 by proteomics analysis. FEMS Microbiol. Lett. 246 (2005) 47-54
34. Twine S.M., Mykytczuk N.C., Petit M.D., Shen H., Sjostedt A., Wayne C.J., and Kelly J.F. In vivo proteomic analysis of the intracellular bacterial pathogen, Francisella tularensis, isolated from mouse spleen. Biochem. Biophys. Res. Commun 345 (2006) 1621-1633
35. Higuchi M., Yamamoto Y., Poole L.B., Shimada M., Sato Y., Takahashi N., and Kamio Y. Functions of two types of NADH oxidases in energy metabolism and oxidative stress of Streptococcus mutans. J. Bacteriol. 181 (1999) 5940-5947
36. Niimura Y., Poole L.B., and Massey V. Amphibacillus xylanus NADH oxidase and Salmonella typhimurium alkyl-hydroperoxide reductase flavoprotein components show extremely high scavenging activity for both alkyl hydroperoxide and hydrogen peroxide in the presence of S. typhimurium alkyl-hydroperoxide reductase 22-kDa protein component. J. Biol. Chem. 270 (1995) 25645-25650
37. Poole L.B., and Ellis H.R. Flavin-dependent alkyl hydroperoxide reductase from Salmonella typhimurium. 1. Purification and enzymatic activities of overexpressed AhpF and AhpC proteins. Biochemistry 35 (1996) 56-64
38. Bakshi C.S., Malik M., Regan K., Melendez J.A., Metzger D.W., Pavlov V.M., and Sellati T.J. Superoxide dismutase B gene (sodB)-deficient mutants of Francisella tularensis demonstrate hypersensitivity to oxidative stress and attenuated virulence. J. Bacteriol. 188 (2006) 6443-6448
39. Lindgren H., Shen H., Zingmark C., Golovliov I., Conlan W., and Sjostedt A. Resistance of Francisella tularensis strains against reactive nitrogen and oxygen species with special reference to the role of KatG. Infect. Immun. 75 (2007) 1303-1309
40. Kadzhaev K., Zingmark C., Golovliov I., Bolanowski M., Shen H., Conlan W., and Sjostedt A. Identification of genes contributing to the virulence of Francisella tularensis SCHU S4 in a mouse intradermal infection model. PLoS ONE 4 (2009) e5463
41. Schulert G.S., McCaffrey R.L., Buchan B.W., Lindemann S.R., Hollenback C., Jones B.D., and Allen L.A. 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 (2009) 1324-1336
42. Bergstrom J., Furst P., Noree L.O., and Vinnars E. Intracellular free amino acid concentration in human muscle tissue. J. Appl. Physiol 36 (1974) 693-697
43. Checroun C., Wehrly T.D., Fischer E.R., Hayes S.F., and Celli J. Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc. Natl. Acad. Sci. U.S.A 103 (2006) 14578-14583
44. Yorimitsu T., and Klionsky D.J. Autophagy: molecular machinery for self-eating. Cell Death. Differ. 12 Suppl. 2 (2005) 1542-1552
45. Larsson P., Oyston P.C., Chain P., Chu M.C., Duffield M., Fuxelius H.H., Garcia E., Halltorp G., Johansson D., Isherwood K.E., Karp P.D., Larsson E., Liu Y., Michell S., Prior J., Prior R., Malfatti S., Sjostedt A., Svensson K., Thompson N., Vergez L., Wagg J.K., Wren B.W., Lindler L.E., Andersson S.G., Forsman M., and Titball R.W. The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat. Genet. 37 (2005) 153-159
46. Charity J.C., Costante-Hamm M.M., Balon E.L., Boyd D.H., Rubin E.J., and Dove S.L. Twin RNA polymerase-associated proteins control virulence gene expression in Francisella tularensis. PLoS Pathog. 3 (2007) e84
47. Levchenko I., Seidel M., Sauer R.T., and Baker T.A. A specificity-enhancing factor for the ClpXP degradation machine. Science 289 (2000) 2354-2356
48. Baron G.S., and Nano F.E. MglA and MglB are required for the intramacrophage growth of Francisella novicida. Mol. Microbiol. 29 (1998) 247-259
49. Su J., Yang J., Zhao D., Kawula T.H., Banas J.A., and Zhang J.R. Genome-wide identification of Francisella tularensis virulence determinants. Infect. Immun 75 (2007) 3089-3101
50. Brotcke A., Weiss D.S., Kim C.C., Chain P., Malfatti S., Garcia E., and Monack D.M. Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis. Infect. Immun. 74 (2006) 6642-6655
51. Guina T., Radulovic D., Bahrami A.J., Bolton D.L., Rohmer L., Jones-Isaac K.A., Chen J., Gallagher L.A., Gallis B., Ryu S., Taylor G.K., Brittnacher M.J., Manoil C., and Goodlett D.R. MglA regulates Francisella tularensis subsp. novicida (Francisella novicida) response to starvation and oxidative stress. J. Bacteriol. 189 (2007) 6580-6586
52. Mohapatra N.P., Soni S., Bell B.L., Warren R., Ernst R.K., Muszynski A., Carlson R.W., and Gunn J.S. Identification of an orphan response regulator required for the virulence of Francisella spp. and transcription of pathogenicity island genes. Infect. Immun. 75 (2007) 3305-3314
53. Rasko D.A., Moreira C.G., Li d.R., Reading N.C., Ritchie J.M., Waldor M.K., Williams N., Taussig R., Wei S., Roth M., Hughes D.T., Huntley J.F., Fina M.W., Falck J.R., and Sperandio V. Targeting QseC signaling and virulence for antibiotic development. Science 321 (2008) 1078-1080
54. Meibom K.L., Forslund A.L., Kuoppa K., Alkhuder K., Dubail I., Dupuis M., Forsberg A., and Charbit A. Hfq, a novel pleiotropic regulator of virulence-associated genes in Francisella tularensis. Infect. Immun. (2009)
55. Barthold S.W., Fikrig E., Bockenstedt L.K., and Persing D.H. Circumvention of outer surface protein A immunity by host-adapted Borrelia burgdorferi. Infect. Immun 63 (1995) 2255-2261