PrsW is required for colonization, resistance to antimicrobial peptides, and expression of extracytoplasmic function σ factors in Clostridium difficile

Infection and Immunity

Volumn 79, Issue 8, 2011, Pages 3229-3238

  Ho, Theresa D ^a   Ellermeier, Craig D ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACITRACIN; LYSOZYME; PROTEINASE; SIGMA FACTOR; SIGMA FACTOR CSFT; SIGMA FACTOR CSFU; SIGMA FACTOR CSFV; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL VIRULENCE; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; CONTROLLED STUDY; GENE MUTATION; INTRON; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PRSW GENE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACITRACIN; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; CRICETINAE; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, BACTERIAL; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; MESOCRICETUS; PEPTIDE HYDROLASES; RODENT DISEASES; SIGMA FACTOR; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; SURVIVAL ANALYSIS; VIRULENCE FACTORS;

EID: 79961111087     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00019-11     Document Type: Article

References (61)

1. Akiyama, Y., K. Kanehara, and K. Ito. 2004. RseP (YaeL), an Escherichia coli RIP protease, cleaves transmembrane sequences. EMBO J. 23:4434-4442.
2. Alba, B. M., J. A. Leeds, C. Onufryk, C. Z. Lu, and C. A. Gross. 2002. DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev. 16:2156-2168.
3. Bartlett, J. G. 1992. Antibiotic-associated diarrhea. Clin. Infect. Dis. 15:573-581.
4. Boyartchuk, V. L., M. N. Ashby, and J. Rine. 1997. Modulation of Ras and a-factor function by carboxyl-terminal proteolysis. Science 275:1796-1800.
5. Britton, R., et al. 2002. Genome-wide analysis of the stationary-phase sigma factor (sigma-H) regulon of Bacillus subtilis. J. Bacteriol. 184:4881-4890.
6. Butcher, B. G., and J. D. Helmann. 2006. Identification of Bacillus subtilis sigma-dependent genes that provide intrinsic resistance to antimicrobial compounds produced by bacilli. Mol. Microbiol. 60:765-782.
7. Callewaert, L., and C. Michiels. 2010. Lysozymes in the animal kingdom. J. Biosci. 35:127-160.
8. Chen, X., et al. 2008. A mouse model of Clostridium difficile-associated disease. Gastroenterology 135:1984-1992.
9. Chen, Y., B. A. McClane, D. J. Fisher, J. I. Rood, and P. Gupta. 2005. Construction of an alpha toxin gene knockout mutant of Clostridium perfringens type A by use of a mobile group II intron. Appl. Environ. Microbiol. 71:7542-7547.
10. Crouch, M., et al. 2005. The alternative sigma factor sigma is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides. Mol. Microbiol. 56:789-799.
11. Dann, S. M., and L. Eckmann. 2007. Innate immune defenses in the intestinal tract. Curr. Opin. Gastroenterol. 23:115-120.
12. Dineen, S. S., A. C. Villapakkam, J. T. Nordman, and A. L. Sonenshein. 2007. Repression of Clostridium difficile toxin gene expression by CodY. Mol. Microbiol. 66:206-219.
13. Dubberke, E. R., and A. I. Wertheimer. 2009. Review of current literature on the economic burden of Clostridium difficile infection. Infect. Control Hosp. Epidemiol. 30:57-66.
14. Ellermeier, C. D., E. C. Hobbs, J. E. Gonzalez-Pastor, and R. Losick. 2006. A three-protein signaling pathway governing immunity to a bacterial cannibalism toxin. Cell 124:549-559.
15. Ellermeier, C. D., and R. Losick. 2006. Evidence for a novel protease governing regulated intramembrane proteolysis and resistance to antimicrobial peptides in Bacillus subtilis. Genes Dev. 20:1911-1922.
16. Goulding, D., et al. 2009. Distinctive profiles of infection and pathology in hamsters infected with Clostridium difficile strains 630 and B1. Infect. Immun. 77:5478-5485.
17. Guerout-Fleury, A. M., N. Frandsen, and P. Stragier. 1996. Plasmids for ectopic integration in Bacillus subtilis. Gene 180:57-61.
18. Gupta, P., and Y. Chen. 2008. Chromosomal engineering of Clostridium perfringens using group II introns. Methods Mol. Biol. 435:217-228.
19. Hahn, M. Y., S. Raman, M. Anaya, and R. N. Husson. 2005. The Mycobacterium tuberculosis extracytoplasmic-function sigma factor SigL regulates polyketide synthases and secreted or membrane proteins and is required for virulence. J. Bacteriol. 187:7062-7071.
20. Harwood, C. 1990. Molecular biological methods for Bacillus. Wiley, Chichester, NY.
21. Heap, J. T., O. J. Pennington, S. T. Cartman, G. P. Carter, and N. P. Minton. 2007. The ClosTron: a universal gene knock-out system for the genus Clostridium. J. Microbiol. Methods 70:452-464.
22. Hebert, L., et al. 2007. Enterococcus faecalis constitutes an unusual bacterial model in lysozyme resistance. Infect. Immun. 75:5390-5398.
23. Heinrich, J., and T. Wiegert. 2006. YpdC determines site-1 degradation in regulated intramembrane proteolysis of the RsiW anti-sigma factor of Bacillus subtilis. Mol. Microbiol. 62:566-579.
24. Helmann, J. D. 2006. Deciphering a complex genetic regulatory network: the Bacillus subtilis sigmaW protein and intrinsic resistance to antimicrobial compounds. Sci. Prog. 89:243-266.
25. Helmann, J. D. 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46:47-110.
26. Hookman, P., and J. S. Barkin. 2009. Clostridium difficile associated infection, diarrhea and colitis. World J. Gastroenterol. 15:1554-1580.
27. Kanehara, K., K. Ito, and Y. Akiyama. 2002. YaeL (EcfE) activates the sigma(E) pathway of stress response through a site-2 cleavage of antisigma(E), RseA. Genes Dev. 16:2147-2155.
28. Keel, M. K., and J. G. Songer. 2006. The comparative pathology of Clostridium difficile-associated disease. Vet. Pathol. 43:225-240.
29. Kelly, C. P., and J. T. LaMont. 1998. Clostridium difficile infection. Annu. Rev. Med. 49:375-390.
30. Kovacikova, G., and K. Skorupski. 2002. The alternative sigma factor sigma(E) plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect. Immun. 70:5355-5362.
31. Kuehne, S., et al. 2010. The role of toxin A and toxin B in Clostridium difficile infection. Nature 467:711-713.
32. Kyne, L., M. B. Hamel, R. Polavaram, and C. P. Kelly. 2002. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin. Infect. Dis. 34:346-353.
33. Loo, V. G., et al. 2005. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N. Engl. J. Med. 353:2442-2449.
34. Lyras, D., et al. 2009. Toxin B is essential for virulence of Clostridium difficile. Nature 458:1176-1179.
35. Manganelli, R., et al. 2002. Role of the extracytoplasmic-function sigma factor sigma(H) in Mycobacterium tuberculosis global gene expression. Mol. Microbiol. 45:365-374.
36. Manganelli, R., M. I. Voskuil, G. K. Schoolnik, and I. Smith. 2001. The Mycobacterium tuberculosis ECF sigma factor sigmaE: role in global gene expression and survival in macrophages. Mol. Microbiol. 41:423-437.
37. Mathur, J., B. M. Davis, and M. K. Waldor. 2007. Antimicrobial peptides activate the Vibrio cholerae sigmaE regulon through an OmpU-dependent signalling pathway. Mol. Microbiol. 63:848-858.
38. McFarland, L. V. 2008. Antibiotic-associated diarrhea: epidemiology, trends and treatment. Future Microbiol. 3:563-578.
39. McFarland, L. V., H. W. Beneda, J. E. Clarridge, and G. J. Raugi. 2007. Implications of the changing face of Clostridium difficile disease for health care practitioners. Am. J. Infect. Control 35:237-253.
40. Miller, V. L., and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
41. O'Connor, J. R., et al. 2006. Construction and analysis of chromosomal Clostridium difficile mutants. Mol. Microbiol. 61:1335-1351. doi:10.1111/j.1365-2958.2006.05315.x.
42. Ozaki, E., et al. 2004. Clostridium difficile colonization in healthy adults: transient colonization and correlation with enterococcal colonization. J. Med. Microbiol. 53:167-172.
43. Pepin, J., et al. 2004. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 171:466-472.
44. Pietiainen, M., et al. 2005. Cationic antimicrobial peptides elicit a complex stress response in Bacillus subtilis that involves ECF-type sigma factors and two-component signal transduction systems. Microbiology 151:1577-1592.
45. Sambol, S. P., M. M. Merrigan, J. K. Tang, S. Johnson, and D. N. Gerding. 2002. Colonization for the prevention of Clostridium difficile disease in hamsters. J. Infect. Dis. 186:1781-1789.
46. Schobel, S., S. Zellmeier, W. Schumann, and T. Wiegert. 2004. The Bacillus subtilis sigmaW anti-sigma factor RsiW is degraded by intramembrane proteolysis through YluC. Mol. Microbiol. 52:1091-1105.
47. Sebaihia, M., et al. 2006. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 38:779-786.
48. Shaw, L. N., et al. 2008. Identification and characterization of sigma, a novel component of the Staphylococcus aureus stress and virulence responses. PLoS One 3:e3844-e3844.
49. Slauch, J. M., and T. J. Silhavy. 1991. cis-Acting ompF mutations that result in OmpR-dependent constitutive expression. J. Bacteriol. 173:4039-4048.
50. Staron, A., et al. 2009. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) sigma factor protein family. Mol. Microbiol. 74:557-581.
51. Sun, R., et al. 2004. Mycobacterium tuberculosis ECF sigma factor sigC is required for lethality in mice and for the conditional expression of a defined gene set. Mol. Microbiol. 52:25-38.
52. Testerman, T. L., et al. 2002. The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol. Microbiol. 43:771-782.
53. Ulrich, L. E., and I. B. Zhulin. 2007. MiST: a microbial signal transduction database. Nucleic Acids Res. 35:D386-D390.
54. Voth, D. E., and J. D. Ballard. 2005. Clostridium difficile toxins: mechanism of action and role in disease. Clin. Microbiol. Rev. 18:247-263.
55. Walsh, N. P., B. M. Alba, B. Bose, C. A. Gross, and R. T. Sauer. 2003. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113:61-71.
56. Wilken, C., K. Kitzing, R. Kurzbauer, M. Ehrmann, and T. Clausen. 2004. Crystal structure of the DegS stress sensor: How a PDZ domain recognizes misfolded protein and activates a protease. Cell 117:483-494.
57. Wilson, G. A., and K. F. Bott. 1968. Nutritional factors influencing the development of competence in the Bacillus subtilis transformation system. J. Bacteriol. 95:1439-1449.
58. Youngman, P., J. B. Perkins, and R. Losick. 1984. Construction of a cloning site near one end of Tn917 into which foreign DNA may be inserted without affecting transposition in Bacillus subtilis or expression of the transposonborne erm gene. Plasmid 12:1-9.
59. Zellmeier, S., C. Hofmann, S. Thomas, T. Wiegert, and W. Schumann. 2005. Identification of sigma(V)-dependent genes of Bacillus subtilis. FEMS Microbiol. Lett. 253:221-229.
60. Zhong, J., M. Karberg, and A. M. Lambowitz. 2003. Targeted and random bacterial gene disruption using a group II intron (targetron) vector containing a retrotransposition-activated selectable marker. Nucleic Acids Res. 31: 1656-1664.
61. Zweers, J., T. Wiegert, and J. van Dijl. 2009. Stress-responsive systems set specific limits to the overproduction of membrane proteins in Bacillus subtilis. Appl. Environ. Microbiol. 75:7356-7364.