The post-translational modification of the Clostridium difficile flagellin affects motility, cell surface properties and virulence

Molecular Microbiology

Volumn 94, Issue 2, 2014, Pages 272-289

  Faulds Pain, Alexandra ^a   Twine, Susan M ^b   Vinogradov, Evgeny ^b   Strong, Philippa C R ^b   Dell, Anne ^c   Buckley, Anthony M ^d   Douce, Gillian R ^d   Valiente, Esmeralda ^a   Logan, Susan M ^b   Wren, Brendan W ^a  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; N ACETYLGLUCOSAMINE; PHOSPHOTHREONINE; THREONINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CATALYSIS; CELL AGGREGATION; CELL MOTILITY; CELL SURFACE; CONTROLLED STUDY; GENE FUNCTION; GENE LOCUS; GENE MUTATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OPEN READING FRAME; PEPTOCLOSTRIDIUM DIFFICILE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; RECURRENT DISEASE; ANIMAL; CHEMISTRY; CLOSTRIDIUM INFECTION; DISEASE MODEL; LOCOMOTION; METABOLISM; MICROBIOLOGY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATHOLOGY; PHYSIOLOGY; SURFACE PROPERTY; TANDEM MASS SPECTROMETRY; VIRULENCE;

CLOSTRIDIUM DIFFICILE;

ANIMALS; CHROMATOGRAPHY, LIQUID; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; DISEASE MODELS, ANIMAL; FLAGELLIN; LOCOMOTION; MAGNETIC RESONANCE SPECTROSCOPY; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECURRENCE; SURFACE PROPERTIES; TANDEM MASS SPECTROMETRY; VIRULENCE;

EID: 84988214464     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12755     Document Type: Article

References (50)

1. Andrews, J.M. (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48 (Suppl. 1): 5-16.
2. Asakura, H., Churin, Y., Bauer, B., Boettcher, J.P., Bartfeld, S., Hashii, N., etal. (2010) Helicobacter pylori HP0518 affects flagellin glycosylation to alter bacterial motility. Mol Microbiol 78: 1130-1144.
3. Aubry, A., Hussack, G., Chen, W., KuoLee, R., Twine, S.M., Fulton, K.M., etal. (2012) Modulation of toxin production by the flagellar regulon in Clostridium difficile. Infect Immun 80: 3521-3532.
4. Baban, S.T., Kuehne, S.A., Barketi-Klai, A., Cartman, S.T., Kelly, M.L., Hardie, K.R., etal. (2013) The role of flagella in Clostridium difficile pathogenesis: comparison between a non-epidemic and an epidemic strain. PLoS ONE 8: e73026.
5. Balonova, L., Mann, B.F., Cerveny, L., Alley, W.R., Jr, Chovancova, E., Forslund, A.L., etal. (2012) Characterization of protein glycosylation in Francisella tularensis subsp. holarctica: identification of a novel glycosylated lipoprotein required for virulence. Mol Cell Proteomics 11 (M111): 015016.
6. Cartman, S.T., and Minton, N.P. (2010) A mariner-based transposon system for in vivo random mutagenesis of Clostridium difficile. Appl Environ Microbiol 76: 1103-1109.
7. Chen, X., Katchar, K., Goldsmith, J.D., Nanthakumar, N., Cheknis, A., Gerding, D.N., and Kelly, C.P. (2008) A mouse model of Clostridium difficile-associated disease. Gastroenterology 135: 1984-1992.
8. Cobb, L.M., Mychaleckyj, J.C., Wozniak, D.J., and Lopez-Boado, Y.S. (2004) Pseudomonas aeruginosa flagellin and alginate elicit very distinct gene expression patterns in airway epithelial cells: implications for cystic fibrosis disease. J Immunol 173: 5659-5670.
9. Dawson, L.F., Valiente, E., Faulds-Pain, A., Donahue, E.H., and Wren, B.W. (2012) Characterisation of Clostridium difficile biofilm formation, a role for Spo0A. PLoS ONE 7: e50527.
10. Deakin, L.J., Clare, S., Fagan, R.P., Dawson, L.F., Pickard, D.J., West, M.R., etal. (2012) The Clostridium difficile spo0A gene is a persistence and transmission factor. Infect Immun 80: 2704-2711.
11. Dingle, T.C., Mulvey, G.L., and Armstrong, G.D. (2011) Mutagenic analysis of the Clostridium difficile flagellar proteins, FliC and FliD, and their contribution to virulence in hamsters. Infect Immun 79: 4061-4067.
12. Drudy, D., Fanning, S., and Kyne, L. (2007) Toxin A-negative, toxin B-positive Clostridium difficile. Int J Infect Dis 11: 5-10.
13. Eidhin, D.N., Ryan, A.W., Doyle, R.M., Walsh, J.B., and Kelleher, D. (2006) Sequence and phylogenetic analysis of the gene for surface layer protein, slpA, from 14 PCR ribotypes of Clostridium difficile. J Med Microbiol 55: 69-83.
14. Ewing, C.P., Andreishcheva, E., and Guerry, P. (2009) Functional characterization of flagellin glycosylation in Campylobacter jejuni 81-176. J Bacteriol 191: 7086-7093.
15. Faulds-Pain, A., and Wren, B.W. (2013) Improved bacterial mutagenesis by high-frequency allele exchange, demonstrated in Clostridium difficile and Streptococcus suis. Appl Environ Microbiol 79: 4768-4771.
16. Faulds-Pain, A., Birchall, C., Aldridge, C., Smith, W.D., Grimaldi, G., Nakamura, S., etal. (2011) Flagellin redundancy in Caulobacter crescentus and its implications for flagellar filament assembly. J Bacteriol 193: 2695-2707.
17. Goorhuis, A., Van der Kooi, T., Vaessen, N., Dekker, F.W., Van den Berg, R., Harmanus, C., etal. (2007) Spread and epidemiology of Clostridium difficile polymerase chain reaction ribotype 027/toxinotype III in The Netherlands. Clin Infect Dis 45: 695-703.
18. Grant, C.C., Konkel, M.E., Cieplak, W., Jr, and Tompkins, L.S. (1993) Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect Immun 61: 1764-1771.
19. He, M., Sebaihia, M., Lawley, T.D., Stabler, R.A., Dawson, L.F., Martin, M.J., etal. (2010) Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci USA 107: 7527-7532.
20. Heap, J.T., Pennington, O.J., Cartman, S.T., Carter, G.P., and Minton, N.P. (2007) The ClosTron: a universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70: 452-464.
21. Heap, J.T., Pennington, O.J., Cartman, S.T., and Minton, N.P. (2009) A modular system for Clostridium shuttle plasmids. J Microbiol Methods 78: 79-85.
22. Heap, J.T., Kuehne, S.A., Ehsaan, M., Cartman, S.T., Cooksley, C.M., Scott, J.C., and Minton, N.P. (2010) The ClosTron: mutagenesis in Clostridium refined and streamlined. J Microbiol Methods 80: 49-55.
23. Hennequin, C., Janoir, C., Barc, M.C., Collignon, A., and Karjalainen, T. (2003) Identification and characterization of a fibronectin-binding protein from Clostridium difficile. Microbiology 149: 2779-2787.
24. Hitchen, P.G., Twigger, K., Valiente, E., Langdon, R.H., Wren, B.W., and Dell, A. (2010) Glycoproteomics: a powerful tool for characterizing the diverse glycoforms of bacterial pilins and flagellins. Biochem Soc Trans 38: 1307-1313.
25. Howard, S.L., Jagannathan, A., Soo, E.C., Hui, J.P., Aubry, A.J., Ahmed, I., etal. (2009) Campylobacter jejuni glycosylation island important in cell charge, legionaminic acid biosynthesis, and colonization of chickens. Infect Immun 77: 2544-2556.
26. Hussain, H.A., Roberts, A.P., and Mullany, P. (2005) Generation of an erythromycin-sensitive derivative of Clostridium difficile strain 630 (630Deltaerm) and demonstration that the conjugative transposon Tn916DeltaE enters the genome of this strain at multiple sites. J Med Microbiol 54: 137-141.
27. Iwashkiw, J.A., Seper, A., Weber, B.S., Scott, N.E., Vinogradov, E., Stratilo, C., etal. (2012) Identification of a general O-linked protein glycosylation system in Acinetobacter baumannii and its role in virulence and biofilm formation. PLoS Pathog 8: e1002758.
28. Kirby, J.M., Ahern, H., Roberts, A.K., Kumar, V., Freeman, Z., Acharya, K.R., and Shone, C.C. (2009) Cwp84, a surface-associated cysteine protease, plays a role in the maturation of the surface layer of Clostridium difficile. J Biol Chem 284: 34666-34673.
29. Kuehne, S.A., Cartman, S.T., Heap, J.T., Kelly, M.L., Cockayne, A., and Minton, N.P. (2010) The role of toxin A and toxin B in Clostridium difficile infection. Nature 467: 711-713.
30. Kuijper, E.J., van Dissel, J.T., and Wilcox, M.H. (2007) Clostridium difficile: changing epidemiology and new treatment options. Curr Opin Infect Dis 20: 376-383.
31. Lawley, T.D., Clare, S., Walker, A.W., Goulding, D., Stabler, R.A., Croucher, N., etal. (2009) Antibiotic treatment of Clostridium difficile carrier mice triggers a supershedder state, spore-mediated transmission, and severe disease in immunocompromised hosts. Infect Immun 77: 3661-3669.
32. Lawley, T.D., Clare, S., Deakin, L.J., Goulding, D., Yen, J.L., Raisen, C., etal. (2010) Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens. Appl Environ Microbiol 76: 6895-6900.
33. Lithgow, K.V., Scott, N.E., Iwashkiw, J.A., Thomson, E.L., Foster, L.J., Feldman, M.F., and Dennis, J.J. (2014) A general protein O-glycosylation system within the Burkholderia cepacia complex is involved in motility and virulence. Mol Microbiol 92: 116-137.
34. Liu, S.L., Ezaki, T., Miura, H., Matsui, K., and Yabuuchi, E. (1988) Intact motility as a Salmonella typhi invasion-related factor. Infect Immun 56: 1967-1973.
35. Logan, S.M. (2006) Flagellar glycosylation - a new component of the motility repertoire? Microbiology 152: 1249-1262.
36. Loo, V.G., Poirier, L., Miller, M.A., Oughton, M., Libman, M.D., Michaud, S., etal. (2005) A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 353: 2442-2449.
37. Lyras, D., O'Connor, J.R., Howarth, P.M., Sambol, S.P., Carter, G.P., Phumoonna, T., etal. (2009) Toxin B is essential for virulence of Clostridium difficile. Nature 458: 1176-1179.
38. Osman, C., Haag, M., Wieland, F.T., Brugger, B., and Langer, T. (2010) A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J 29: 1976-1987.
39. Parker, J.L., Day-Williams, M.J., Tomas, J.M., Stafford, G.P., and Shaw, J.G. (2012) Identification of a putative glycosyltransferase responsible for the transfer of pseudaminic acid onto the polar flagellin of Aeromonas caviae Sch3N. MicrobiologyOpen 1: 149-160.
40. Pizarro-Cerda, J., and Cossart, P. (2006) Bacterial adhesion and entry into host cells. Cell 124: 715-727.
41. Reynolds, C.B., Emerson, J.E., de la Riva, L., Fagan, R.P., and Fairweather, N.F. (2011) The Clostridium difficile cell wall protein CwpV is antigenically variable between strains, but exhibits conserved aggregation-promoting function. PLoS Pathog 7: e1002024.
42. Schirm, M., Arora, S.K., Verma, A., Vinogradov, E., Thibault, P., Ramphal, R., and Logan, S.M. (2004) Structural and genetic characterization of glycosylation of type a flagellin in Pseudomonas aeruginosa. J Bacteriol 186: 2523-2531.
43. Smith, C.J., Markowitz, S.M., and Macrina, F.L. (1981) Transferable tetracycline resistance in Clostridium difficile. Antimicrob Agents Chemother 19: 997-1003.
44. Stabler, R.A., He, M., Dawson, L., Martin, M., Valiente, E., Corton, C., etal. (2009) Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol 10: R102.
45. Stabler, R.A., Dawson, L.F., Valiente, E., Cairns, M.D., Martin, M.J., Donahue, E.H., etal. (2012) Macro and micro diversity of Clostridium difficile isolates from diverse sources and geographical locations. PLoS ONE 7: e31559.
46. Sun, L., Jin, M., Ding, W., Yuan, J., Kelly, J., and Gao, H. (2013) Posttranslational modification of flagellin FlaB in Shewanella oneidensis. J Bacteriol 195: 2550-2561.
47. Twine, S.M., Reid, C.W., Aubry, A., McMullin, D.R., Fulton, K.M., Austin, J., and Logan, S.M. (2009) Motility and flagellar glycosylation in Clostridium difficile. J Bacteriol 191: 7050-7062.
48. Verma, A., Schirm, M., Arora, S.K., Thibault, P., Logan, S.M., and Ramphal, R. (2006) Glycosylation of b-Type flagellin of Pseudomonas aeruginosa: structural and genetic basis. J Bacteriol 188: 4395-4403.
49. Voth, D.E., and Ballard, J.D. (2005) Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev 18: 247-263.
50. Williams, D.R., Young, D.I., and Young, M. (1990) Conjugative plasmid transfer from Escherichia coli to Clostridium acetobutylicum. J Gen Microbiol 136: 819-826.