Characterization of Francisella tularensis Schu S4 mutants identified from a transposon library screened for O-antigen and capsule deficiencies

Frontiers in Microbiology

Volumn 6, Issue MAY, 2015, Pages

  Rasmussen, Jed A ^a   Fletcher, Joshua R ^a   Long, Matthew E ^a,b   Allen, Lee Ann H ^a   Jones, Bradley D ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Capsule; Francisella tularensis; Innate immunity; Intracellular growth; Mouse virulence; O antigen; Transposon mutagenesis

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; MONOCLONAL ANTIBODY; O ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; BONE MARROW DERIVED MACROPHAGE; CELL FUNCTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEMALE; FRANCISELLA TULARENSIS; GENE MUTATION; IMMUNE RESPONSE; IMMUNOBLOTTING; IN VITRO STUDY; INNATE IMMUNITY; MOUSE; MUTAGENESIS; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; QUANTITATIVE ASSAY; SEQUENCE ANALYSIS;

FRANCISELLA TULARENSIS; MUS;

EID: 84931271128     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00338     Document Type: Article

References (54)

1. Allen, L. A., and Aderem, A. (1996). Molecular definition of distinct cytoskeletal structures involved in complement-and Fc receptor-mediated phagocytosis in macrophages. J. Exp. Med. 184, 627-637. doi: 10.1084/jem.184.2.627.
2. Apicella, M. A., Post, D. M., Fowler, A. C., Jones, B. D., Rasmussen, J. A., Hunt, J. R., et al. (2010). Identification, characterization and immunogenicity of an O-antigen capsular polysaccharide of Francisella tularensis. PLoS ONE 5:e11060. doi: 10.1371/journal.pone.0011060.
3. Barker, J. R., and Klose, K. E. (2007). Molecular and genetic basis of pathogenesis in Francisella tularensis. Ann. N.Y. Acad. Sci. 1105, 138-159. doi: 10.1196/annals.1409.010.
4. Buchan, B. W., McLendon, M. K., and Jones, B. D. (2008). Identification of differentially regulated Francisella tularensis genes by use of a newly developed Tn5-based transposon delivery system. Appl. Environ. Microbiol. 74, 2637-2645. doi: 10.1128/AEM.02882-07.
5. Cahoon, L. A., Stohl, E. A., and Seifert, H. S. (2011). The Neisseria gonorrhoeae photolyase orthologue phrB is required for proper DNA supercoiling but does not function in photo-reactivation. Mol. Microbiol. 79, 729-742. doi: 10.1111/j.1365-2958.2010.07481.x.
6. Carvalho, C. L., Lopes de Carvalho, I., Ze-Ze, L., Nuncio, M. S., and Duarte, E. L. (2014). Tularaemia: a challenging zoonosis. Comp. Immunol. Microbiol. Infect. Dis. 37, 85-96. doi: 10.1016/j.cimid.2014.01.002.
7. Case, E. D., Chong, A., Wehrly, T. D., Hansen, B., Child, R., Hwang, S., et al. (2013). The Francisella O-antigen mediates survival in the macrophage cytosol via autophagy avoidance. Cell. Microbiol.
8. Center for Disease Control and Prevention. (2013). Tularemia-United States, 2001-2010. MMWR Morb. Mortal. Wkly. Rep. 62, 963-966.
9. Clay, C. D., Soni, S., Gunn, J. S., and Schlesinger, L. S. (2008). Evasion of complement-mediated lysis and complement C3 deposition are regulated by Francisella tularensis lipopolysaccharide O antigen. J. Immunol. 181, 5568-5578. doi: 10.4049/jimmunol.181.8.5568.
10. Comstock, L. E., and Kasper, D. L. (2006). Bacterial glycans: key mediators of diverse host immune responses. Cell 126, 847-850. doi: 10.1016/j.cell.2006.08.021.
11. Creuzenet, C., and Lam, J. S. (2001). Topological and functional characterization of WbpM, an inner membrane UDP-GlcNAc C6 dehydratase essential for lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 41, 1295-1310. doi: 10.1046/j.1365-2958.2001.02589.x.
12. Creuzenet, C., Schur, M. J., Li, J., Wakarchuk, W. W., and Lam, J. S. (2000). FlaA1, a new bifunctional UDP-GlcNAc C6 Dehydratase/C4 reductase from Helicobacter pylori. J. Biol. Chem. 275, 34873-34880. doi: 10.1074/jbc.M006369200.
13. Cryz, S. J. Jr. Pitt, T. L., Furer, E., and Germanier, R. (1984). Role of lipopolysaccharide in virulence of Pseudomonas aeruginosa. Infect. Immun. 44, 508-513.
14. Dasgupta, T., de Kievit, T. R., Masoud, H., Altman, E., Richards, J. C., Sadovskaya, I., et al. (1994). Characterization of lipopolysaccharide-deficient mutants of Pseudomonas aeruginosa derived from serotypes O3, O5, and O6. Infect. Immun. 62, 809-817.
15. de Bruin, O. M., Duplantis, B. N., Ludu, J. S., Hare, R. F., Nix, E. B., Schmerk, C. L., 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. doi: 10.1099/mic.0.052308-0.
16. Gaidenko, T. A., Kim, T. J., Weigel, A. L., Brody, M. S., and Price, C. W. (2006). The blue-light receptor YtvA acts in the environmental stress signaling pathway of Bacillus subtilis. J. Bacteriol. 188, 6387-6395. doi: 10.1128/JB.00691-06.
17. Ho, T. D., and Waldor, M. K. (2007). Enterohemorrhagic Escherichia coli O157:H7 gal mutants are sensitive to bacteriophage P1 and defective in intestinal colonization. Infect. Immun. 75, 1661-1666. doi: 10.1128/IAI.01342-06.
18. Iredell, J. R., Stroeher, U. H., Ward, H. M., and Manning, P. A. (1998). Lipopolysaccharide O-antigen expression and the effect of its absence on virulence in rfb mutants of Vibrio cholerae O1. FEMS Immunol. Med. Microbiol. 20, 45-54. doi: 10.1016/S0928-8244(97)00106-5.
19. Jones, B. D., Faron, M., Rasmussen, J. A., and Fletcher, J. R. (2014). Uncovering the components of the Francisella tularensis virulence stealth strategy. Front. Cell. Infect. Microbiol. 4:32. doi: 10.3389/fcimb.2014.00032.
20. Kim, T. H., Pinkham, J. T., Heninger, S. J., Chalabaev, S., and Kasper, D. L. (2012). Genetic modification of the O-polysaccharide of Francisella tularensis results in an avirulent live attenuated vaccine. J. Infect. Dis. 205, 1056-1065. doi: 10.1093/infdis/jir620.
21. Kim, T. H., Sebastian, S., Pinkham, J. T., Ross, R. A., Blalock, L. T., and Kasper, D. L. (2010). Characterization of the O-antigen polymerase (Wzy) of Francisella tularensis. J. Biol. Chem. 285, 27839-27849. doi: 10.1074/jbc.M110.143859.
22. Lai, X. H., Shirley, R. L., Crosa, L., Kanistanon, D., Tempel, R., Ernst, R. K., et al. (2010). Mutations of Francisella novicida that alter the mechanism of its phagocytosis by murine macrophages. PLoS ONE 5:e11857. doi: 10.1371/journal.pone.0011857.
23. Li, J., Ryder, C., Mandal, M., Ahmed, F., Azadi, P., Snyder, D. S., et al. (2007). Attenuation and protective efficacy of an O-antigen-deficient mutant of Francisella tularensis LVS. Microbiology 153, 3141-3153. doi: 10.1099/mic.0.2007/006460-0.
24. Lindemann, S. R., Peng, K., Long, M. E., Hunt, J. R., Apicella, M. A., Monack, D. M., 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. doi: 10.1128/IAI.00863-10.
25. Maier, T. M., Casey, M. S., Becker, R. H., Dorsey, C. W., Glass, E. M., Maltsev, N., et al. (2007). Identification of Francisella tularensis Himar1-based transposon mutants defective for replication in macrophages. Infect. Immun. 75, 5376-5389. doi: 10.1128/IAI.00238-07.
26. Maier, T. M., Havig, A., Casey, M., Nano, F. E., Frank, D. W., and Zahrt, T. C. (2004). Construction and characterization of a highly efficient Francisella shuttle plasmid. Appl. Environ. Microbiol. 70, 7511-7519. doi: 10.1128/AEM.70.12.7511-7519.2004.
27. McLendon, M. K., Apicella, M. A., and Allen, L. A. (2006). Francisella tularensis: taxonomy, genetics, and Immunopathogenesis of a potential agent of biowarfare. Annu. Rev. Microbiol. 60, 167-185. doi: 10.1146/annurev.micro.60.080805.142126.
28. Oyston, P. C. (2008). Francisella tularensis: unravelling the secrets of an intracellular pathogen. J. Med. Microbiol. 57, 921-930. doi: 10.1099/jmm.0.2008/000653-0.
29. Oyston, P. C., Sjostedt, A., and Titball, R. W. (2004). Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat. Rev. Microbiol. 2, 967-978. doi: 10.1038/nrmicro1045.
30. Post, D. M., Yu, L., Krasity, B. C., Choudhury, B., Mandel, M. J., Brennan, C. A., et al. (2012). O-antigen and core carbohydrate of Vibrio fischeri lipopolysaccharide: composition and analysis of their role in Euprymna scolopes light organ colonization. J. Biol. Chem. 287, 8515-8530. doi: 10.1074/jbc.M111.324012.
31. Prior, J. L., Prior, R. G., Hitchen, P. G., Diaper, H., Griffin, K. F., Morris, H. R., et al. (2003). Characterization of the O antigen gene cluster and structural analysis of the O antigen of Francisella tularensis subsp. tularensis. J. Med. Microbiol. 52, 845-851. doi: 10.1099/jmm.0.05184-0.
32. Purcell, E. B., and Crosson, S. (2008). Photoregulation in prokaryotes. Curr. Opin. Microbiol. 11, 168-178. doi: 10.1016/j.mib.2008.02.014.
33. Purcell, E. B., Siegal-Gaskins, D., Rawling, D. C., Fiebig, A., and Crosson, S. (2007). A photosensory two-component system regulates bacterial cell attachment. Proc. Natl. Acad. Sci. U.S.A. 104, 18241-18246. doi: 10.1073/pnas.0705887104.
34. Rasmussen, J. A., Post, D. M., Gibson, B. W., Lindemann, S. R., Apicella, M. A., Meyerholz, D. K., et al. (2014). Francisella tularensis Schu S4 LPS core sugar and O-antigen mutants are attenuated in a mouse model of Tularemia. Infect. Immun. 82, 1523-1539. doi: 10.1128/IAI.01640-13.
35. Raynaud, C., Meibom, K. L., Lety, M. A., Dubail, I., Candela, T., Frapy, E., et al. (2007). Role of the wbt locus of Francisella tularensis in lipopolysaccharide O-antigen biogenesis and pathogenicity. Infect. Immun. 75, 536-541. doi: 10.1128/IAI.01429-06.
36. Reed, L. J., and Muench, H. (1938). A simple method of estimating fifty per cent endpoints. Am. J. Epidemiol. 27, 493-497.
37. Rietschel, E. T. (1984). Chemistry of Endotoxin. New York, NY: Elsevier; Sole distributor for the USA and Canada, Elsevier Science Pub. Co., Amsterdam; New York.
38. Sandstrom, G., Lofgren, S., and 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.
39. Saslaw, S., Eigelsbach, H. T., Prior, J. A., Wilson, H. E., and Carhart, S. (1961). Tularemia vaccine study. II. Respiratory challenge. Arch. Intern. Med. 107, 702-714. doi: 10.1001/archinte.1961.03620050068007.
40. Schulert, G. S., and Allen, L. A. (2006). Differential infection of mononuclear phagocytes by Francisella tularensis: role of the macrophage mannose receptor. J. Leukoc. Biol. 80, 563-571. doi: 10.1189/jlb.0306219.
41. Sebastian, S., Dillon, S. T., Lynch, J. G., Blalock, L. T., Balon, E., Lee, K. T., et al. (2007). A defined O-antigen polysaccharide mutant of Francisella tularensis live vaccine strain has attenuated virulence while retaining its protective capacity. Infect. Immun. 75, 2591-2602. doi: 10.1128/IAI.01789-06.
42. Sheng, H., Lim, J. Y., Watkins, M. K., Minnich, S. A., and Hovde, C. J. (2008). Characterization of an Escherichia coli O157:H7 O-antigen deletion mutant and effect of the deletion on bacterial persistence in the mouse intestine and colonization at the bovine terminal rectal mucosa. Appl. Environ. Microbiol. 74, 5015-5022. doi: 10.1128/AEM.00743-08.
43. Sjostedt, A. (2007). Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann. N.Y. Acad. Sci. 1105, 1-29. doi: 10.1196/annals.1409.009.
44. Stawski, G., Nielsen, L., Orskov, F., and Orskov, I. (1990). Serum sensitivity of a diversity of Escherichia coli antigenic reference strains. Correlation with an LPS variation phenomenon. APMIS 98, 828-838.
45. Su, J., Yang, J., Zhao, D., Kawula, T. H., Banas, J. A., and Zhang, J. R. (2007). Genome-wide identification of Francisella tularensis virulence determinants. Infect. Immun. 75, 3089-3101. doi: 10.1128/IAI.01865-06.
46. Swartz, T. E., Tseng, T. S., Frederickson, M. A., Paris, G., Comerci, D. J., Rajashekara, G., et al. (2007). Blue-light-activated histidine kinases: two-component sensors in bacteria. Science 317, 1090-1093. doi: 10.1126/science.1144306.
47. Tarnvik, A., and Berglund, L. (2003). Tularaemia. Eur. Respir. J. 21, 361-373. doi: 10.1183/09031936.03.00088903.
48. Thomas, R. M., Titball, R. W., Oyston, P. C., Griffin, K., Waters, E., Hitchen, P. G., et al. (2007). The immunologically distinct O antigens from Francisella tularensis subspecies tularensis and Francisella novicida are both virulence determinants and protective antigens. Infect. Immun. 75, 371-378. doi: 10.1128/IAI.01241-06.
49. Vinogradov, E., Perry, M. B., and Conlan, J. W. (2002). Structural analysis of Francisella tularensis lipopolysaccharide. Eur. J. Biochem. 269, 6112-6118. doi: 10.1046/j.1432-1033.2002.03321.x.
50. Wang, Q., Shi, X., Leymarie, N., Madico, G., Sharon, J., Costello, C. E., et al. (2011). A typical preparation of Francisella tularensis O-antigen yields a mixture of three types of saccharides. Biochemistry 50, 10941-10950. doi: 10.1021/bi201450v.
51. Wehrly, T. D., Chong, A., Virtaneva, K., Sturdevant, D. E., Child, R., Edwards, J. A., et al. (2009). Intracellular biology and virulence determinants of Francisella tularensis revealed by transcriptional profiling inside macrophages. Cell. Microbiol. 11, 1128-1150. doi: 10.1111/j.1462-5822.2009.01316.x.
52. Weiss, D. S., Brotcke, A., Henry, T., Margolis, J. J., Chan, K., and Monack, D. M. (2007). In vivo negative selection screen identifies genes required for Francisella virulence. Proc. Natl. Acad. Sci. U.S.A. 104, 6037-6042. doi: 10.1073/pnas.0609675104.
53. Whitfield, C. (2006). Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu. Rev. Biochem. 75, 39-68. doi: 10.1146/annurev.biochem.75.103004.142545.
54. Zogaj, X., and Klose, K. E. (2010). Genetic manipulation of Francisella tularensis. Front. Microbiol. 1:142. doi: 10.3389/fmicb.2010.00142.