O-linked glycosylation of the PilA pilin protein of Francisella tularensis: Identification of the endogenous protein-targeting oligosaccharyltransferase and characterization of the native oligosaccharide

Journal of Bacteriology

Volumn 193, Issue 19, 2011, Pages 5487-5497

  Egge Jacobsen, Wolfgang ^a   Salomonsson, Emelie Näslund ^b   Aas, Finn Erik ^a   Forslund, Anna Lena ^b   Winther Larsen, Hanne C ^a   Maier, Josef ^c   Macellaro, Anna ^b   Kuoppa, Kerstin ^b   Oyston, Petra C F ^d   Titball, Richard W ^e   Thomas, Rebecca M ^d   Forsberg, Åke ^f   Prior, Joann L ^d   Koomey, Michael ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b SWEDISH DEFENCE RESEARCH AGENCY   (Sweden)

^c IStLS Information Services to Life Science   (Germany)

^d DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^e UNIVERSITY OF EXETER   (United Kingdom)

^f UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; OLIGOSACCHARIDE; OLIGOSACCHARYLTRANSFERASE; PENTASACCHARIDE; PGLA PROTEIN; PILA PROTEIN; PILIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; ESCHERICHIA COLI; FRANCISELLA TULARENSIS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN GLYCOSYLATION; PROTEIN POLYMORPHISM; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; PROTEIN TARGETING; PROTEOBACTERIA;

BACTERIAL PROTEINS; FIMBRIAE PROTEINS; FRANCISELLA TULARENSIS; GLYCOPEPTIDES; GLYCOSYLATION; HEXOSYLTRANSFERASES; IMMUNOBLOTTING; MASS SPECTROMETRY; MEMBRANE PROTEINS; OLIGOSACCHARIDES; POLYSACCHARIDES;

ESCHERICHIA COLI; FRANCISELLA; FRANCISELLA TULARENSIS; FRANCISELLA TULARENSIS SUBSP. HOLARCTICA; FRANCISELLA TULARENSIS SUBSP. TULARENSIS; PILA; PROTEOBACTERIA;

EID: 80053602806     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00383-11     Document Type: Article

References (45)

1. Aas, F. E., A. Vik, J. Vedde, M. Koomey, and W. Egge-Jacobsen. 2007. Neisseria gonorrhoeae O-linked pilin glycosylation: functional analyses define both the biosynthetic pathway and glycan structure. Mol. Microbiol. 65:607-624.
2. Abd, H., T. Johansson, I. Golovliov, G. Sandström, and M. Forsman. 2003. Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl. Environ. Microbiol. 69:600-606.
3. Alm, R. A., J. P. Hallinan, A. A. Watson, and J. S. Mattick. 1996. Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein-secretion systems and pilY1 encodes a gonococcal PilC homologue. Mol. Microbiol. 22:161-173.
4. Alm, R. A., and J. S. Mattick. 1995. Identification of a gene, pilV, required for type 4 fimbrial biogenesis in Pseudomonas aeruginosa, whose product possesses a pre-pilin-like leader sequence. Mol. Microbiol. 16:485-496.
5. Alm, R. A., and J. S. Mattick. 1996. Identification of two genes with prepilinlike leader sequences involved in type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 178:3809-3817.
6. Balonova, L., et al. 2010. Multimethodological approach to identification of glycoproteins from the proteome of Francisella tularensis, an intracellular microorganism. J. Proteome Res. 9:1995-2005.
7. Blatny, J. M., T. Brautaset, H. C. Winther-Larsen, P. Karunakaran, and S. Valla. 1997. Improved broad-host-range RK2 vectors useful for high and low regulated gene expression levels in gram-negative bacteria. Plasmid 38: 35-51.
8. Borud, B., et al. 2010. Genetic, structural, and antigenic analyses of glycan diversity in the O-linked protein glycosylation systems of human Neisseria species. J. Bacteriol. 192:2816-2829.
9. Brotcke, A., et al. 2006. Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis. Infect. Immun. 74:6642-6655.
10. Dennis, D. T., et al. 2001. Tularemia as a biological weapon: medical and public health management. JAMA 285:2763-2773.
11. DiGiandomenico, A., et al. 2002. Glycosylation of Pseudomonas aeruginosa 1244 pilin: glycan substrate specificity. Mol. Microbiol. 46:519-530.
12. Faridmoayer, A., M. A. Fentabil, D. C. Mills, J. S. Klassen, and M. F. Feldman. 2007. Functional characterization of bacterial oligosaccharyltransferases involved in O-linked protein glycosylation. J. Bacteriol. 189:8088-8098.
13. Feldman, M. F., et al. 2005. Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 102:3016-3021.
14. Forslund, A. L., et al. 2006. Direct repeat-mediated deletion of a type IV pilin gene results in major virulence attenuation of Francisella tularensis. Mol. Microbiol. 59:1818-1830.
15. Golovliov, I., V. Baranov, Z. Krocova, H. Kovarova, and A. Sjöstedt. 2003. An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells. Infect. Immun. 71:5940-5950.
16. Hager, A. J., et al. 2006. Type IV pili-mediated secretion modulates Francisella virulence. Mol. Microbiol. 62:227-237.
17. Han, X., et al. 2008. Twitching motility is essential for virulence in Dichelobacter nodosus. J. Bacteriol. 190:3323-3335.
18. Johansson, A., et al. 2004. Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J. Bacteriol. 186:5808-5818.
19. Khan, A. S., S. Morse, and S. Lillibridge. 2000. Public-health preparedness for biological terrorism in the USA. Lancet 356:1179-1182.
20. Kirn, T. J., N. Bose, and R. K. Taylor. 2003. Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol. Microbiol. 49:81-92.
21. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
22. Milton, D., R. O'Toole, P. Horstedt, and H. Wolf-Watz. 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
23. Nudleman, E., and D. Kaiser. 2004. Pulling together with type IV pili. J. Mol. Microbiol. Biotechnol. 7:52-62.
24. Pavlov, V., A. Mokrievich, and K. Volkovoy. 1996. Cryptic plasmid pFNL10 from Francisella novicida-like F6168: the base of plasmid vectors for Francisella tularensis. FEMS Immunol. Med. Microbiol. 13:253-256.
25. Petersen, J., and M. Schriefer. 2005. Tularemia: emergence/re-emergence. Vet. Res. 36:455-467.
26. Power, P. M., K. L. Seib, and M. P. Jennings. 2006. Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli. Biochem. Biophys. Res. Commun. 347: 904-908.
27. Qutyan, M., M. Paliotti, and P. Castric. 2007. PilO of Pseudomonas aeruginosa 1244: subcellular location and domain assignment. Mol. Microbiol. 66:1444-1458.
28. Rohmer, L., et al. 2007. Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol. 8:R102.
29. Salomonsson, E., et al. 2009. Functional analyses of pilin-like proteins from Francisella tularensis: complementation of type IV pilus phenotypes in Neisseria gonorrhoeae. Microbiology 155:2546-2559.
30. Salomonsson, E., 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.
31. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
32. Simon, R., U. B. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vitro genetic engineering transposon mutagenesis in gram negative bacteria. Biotechnology 1:784-791.
33. Skerker, J. M., and H. C. Berg. 2001. Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. U. S. A. 98:6901-6904.
34. Strom, M., and S. Lory. 1993. Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47:565-596.
35. Strom, M., D. Nunn, and S. Lory. 1993. A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc. Natl. Acad. Sci. U. S. A. 90:2404-2408.
36. Tärnvik, A. 1989. Nature of protective immunity to Francisella tularensis. Rev. Infect. Dis. 11:440-451.
37. Twine, S. M., et al. 2009. Motility and flagellar glycosylation in Clostridium difficile. J. Bacteriol. 191:7050-7062.
38. Verma, A., et al. 2006. Glycosylation of b-type flagellin of Pseudomonas aeruginosa: structural and genetic basis. J. Bacteriol. 188:4395-4403.
39. Weiss, D., et al. 2007. In vivo negative selection screen identifies genes required for Francisella virulence. Proc. Natl. Acad. Sci. U. S. A. 104:6037-6042.
40. Whipp, M., et al. 2003. Characterization of a novicida-like subspecies of Francisella tularensis isolated in Australia. J. Med. Microbiol. 52:839-842.
41. Winther-Larsen, H. C., et al. 2001. Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc. Natl. Acad. Sci. U. S. A. 98:15276-15281.
42. Winther-Larsen, H. C., et al. 2005. A conserved set of pilin-like molecules controls type IV pilus dynamics and organelle-associated functions in Neisseria gonorrhoeae. Mol. Microbiol. 56:903-917.
43. Wolfgang, M., J. P. van Putten, S. F. Hayes, D. Dorward, and M. Koomey. 2000. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. EMBO J. 19:6408-6418.
44. Wolfgang, M., J. P. van Putten, S. F. Hayes, and M. Koomey. 1999. The comP locus of Neisseria gonorrhoeae encodes a type IV prepilin that is dispensable for pilus biogenesis but essential for natural transformation. Mol. Microbiol. 31:1345-1357.
45. Zogaj, X., S. Chakraborty, J. Liu, D. Thanassi, and K. Klose. 2008. Characterization of the Francisella tularensis subsp. novicida type IV pilus. Microbiology 154:2139-2150.