Toxin synthesis by Clostridium difficile is regulated through quorum signaling

mBio

Volumn 6, Issue 2, 2015, Pages

  Darkoh, Charles ^a   Dupont, Herbert L ^a,c,d   Norris, Steven J ^b   Kaplan, Heidi B ^b  

^a UNIVERSITY OF TEXAS SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c CHI ST LUKE S HEALTH BAYLOR ST LUKE S MEDICAL CENTER   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL TOXIN; THIOLACTONE; BACTERIAL PROTEIN; ENTEROTOXIN; TCDA PROTEIN, CLOSTRIDIUM DIFFICILE; TOXB PROTEIN, CLOSTRIDIUM DIFFICILE;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM DETECTION; CLOSTRIDIUM DIFFICILE INFECTION; CONTROLLED STUDY; GENE CONTROL; GENETIC TRANSCRIPTION; HUMAN; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; PRIORITY JOURNAL; QUORUM SENSING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TCDA GENE; TCDB GENE; TCDC GENE; TOXIN SYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

CLOSTRIDIUM DIFFICILE; POSIBACTERIA;

BACTERIAL PROTEINS; BACTERIAL TOXINS; CLOSTRIDIUM DIFFICILE; ENTEROTOXINS; GENE EXPRESSION REGULATION, BACTERIAL; QUORUM SENSING; SIGNAL TRANSDUCTION;

EID: 84929485093     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.02569-14     Document Type: Article

References (50)

1. Dubberke ER, Olsen MA. 2012. Burden of Clostridium difficile on the healthcare system. Clin Infect Dis 55(Suppl 2):S88-S92. http://dx.doi.org/10.1093/cid/cis335.
2. DuPont HL. 2011. The search for effective treatment of Clostridium difficile infection. N Engl J Med 364:473-475. http://dx.doi.org/10.1056/NEJMe1013236.
3. Kyne L, Hamel MB, Polavaram R, Kelly CP. 2002. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis 34:346–353. http://dx.doi.org/10.1086/338260.
4. O’Brien JA, Lahue BJ, Caro JJ, Davidson DM. 2007. The emerging infectious challenge of Clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences. Infect Control Hosp Epidemiol 28:1219–1227. http://dx.doi.org/10.1086/522676.
5. Wilkins TD, Lyerly DM. 2003. Clostridium difficile testing: after 20 years, still challenging. J Clin Microbiol 41:531–534. http://dx.doi.org/10.1128/JCM.41.2.531-534.2003.
6. Ananthakrishnan AN. 2011. Clostridium difficile infection: epidemiology, risk factors and management. Nat Rev Gastroenterol Hepatol 8:17–26. http://dx.doi.org/10.1038/nrgastro.2010.190.
7. McDonald LC, Killgore GE, Thompson A, Owens RC, Jr, Kazakova SV, Sambol SP, Johnson S, Gerding DN. 2005. An epidemic, toxin genevariant strain of Clostridium difficile. N Engl J Med 353:2433–2441. http://dx.doi.org/10.1056/NEJMoa051590.
8. Redelings MD, Sorvillo F, Mascola L. 2007. Increase in Clostridium difficile-related mortality rates, United States, 1999–2004. Emerg Infect Dis 13:1417–1419. http://dx.doi.org/10.3201/eid1309.061116.
9. Bartlett JG, Perl TM. 2005. The new Clostridium difficile—what does it mean? N Engl J Med 353:2503–2505. http://dx.doi.org/10.1056/NEJMe058221.
10. Burke KE, Lamont JT. 2013. Fecal transplantation for recurrent Clostridium difficile infection in older adults: a review. J Am Geriatr Soc 61: 1394–1398. http://dx.doi.org/10.1111/jgs.12378.
11. Hansen D, Pollan LD, Fernando H. 2013. Fulminant Clostridium difficile colitis: a complication of perioperative antibiotic prophylaxis. J Oral Maxillofac Surg 71:1880–1885. http://dx.doi.org/10.1016/j.joms.2013.04.035.
12. Geric B, Rupnik M, Gerding DN, Grabnar M, Johnson S. 2004. Distribution of Clostridium difficile variant toxinotypes and strains with binary toxin genes among clinical isolates in an American Hospital. J Med Microbiol 53:887–894. http://dx.doi.org/10.1099/jmm.0.45610-0.
13. Rupnik M, Brazier JS, Duerden BI, Grabnar M, Stubbs SL. 2001. Comparison of toxinotyping and PCR ribotyping of Clostridium difficile strains and description of novel toxinotypes. Microbiology 147:439–447.
14. Voth DE, Ballard JD. 2005. Clostridium difficile toxins: mechanism of action and role in disease. Clin Microbiol Rev 18:247–263. http://dx.doi.org/10.1128/CMR.18.2.247-263.2005.
15. Kuehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A, Minton NP. 2010. The role of toxin A and toxin B in Clostridium difficile infection. Nature 467:711–713. http://dx.doi.org/10.1038/nature09397.
16. Mani N, Dupuy B. 2001. Regulation of toxin synthesis in Clostridium difficile by an alternativeRNApolymerase sigma factor. Proc Natl Acad Sci USA 98:5844–5849. http://dx.doi.org/10.1073/pnas.101126598.
17. Mani N, Lyras D, Barroso L, Howarth P, Wilkins T, Rood JI, Sonenshein AL, Dupuy B. 2002. Environmental response and autoregulation of Clostridium difficile TxeR, a sigma factor for toxin gene expression. J Bacteriol 184:5971–5978. http://dx.doi.org/10.1128/JB.184.21.5971-5978.2002.
18. Carter GP, Douce GR, Govind R, Howarth PM, Mackin KE, Spencer J, Buckley AM, Antunes A, Kotsanas D, Jenkin GA, Dupuy B, Rood JI, Lyras D. 2011. The anti-sigma factor TcdC modulates hypervirulence in an epidemic BI/NAP1/027 clinical isolate of Clostridium difficile. PLoS Pathog. 7:e1002317. http://dx.doi.org/10.1371/journal.ppat.1002317.
19. Hundsberger T, Braun V, Weidmann M, Leukel P, Sauerborn M, von Eichel-Streiber C. 1997. Transcription analysis of the genes tcdA-E of the pathogenicity locus of Clostridium difficile. Eur J Biochem 244:735–742. http://dx.doi.org/10.1111/j.1432-1033.1997.t01-1-00735.x.
20. Matamouros S, England P, Dupuy B. 2007. Clostridium difficile toxin expression is inhibited by the novel regulator TcdC. Mol Microbiol 64: 1274–1288. http://dx.doi.org/10.1111/j.1365-2958.2007.05739.x.
21. Curry SR, Marsh JW, Muto CA, O’Leary MM, Pasculle AW, Harrison LH. 2007. Tcdc genotypes associated with severe TcdC truncation in an epidemic clone and other strains of Clostridium difficile. J Clin Microbiol 45:215–221. http://dx.doi.org/10.1128/JCM.01599-06.
22. Jarraud S, Lyon GJ, Figueiredo AM, Lina G, Vandenesch F, Etienne J, Muir TW, Novick RP. 2000. Exfoliation-producing strains define a fourth agr specificity group in Staphylococcus aureus. J Bacteriol 182:6517–6522. http://dx.doi.org/10.1128/JB.182.22.6517-6522.2000.
23. Warny M, Pepin J, Fang A, Killgore G, Thompson A, Brazier J, Frost E, McDonald LC. 2005. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 366:1079-1084. http://dx.doi.org/10.1016/S0140-6736(05)67420-X.
24. Bakker D, Smits WK, Kuijper EJ, Corver J. 2012. TcdC does not significantly repress toxin expression in Clostridium difficile 630 Erm. PLoS One 7:e43247. http://dx.doi.org/10.1371/journal.pone.0043247.
25. Cartman ST, Kelly ML, Heeg D, Heap JT, Minton NP. 2012. Precise manipulation of the Clostridium difficile chromosome reveals a lack of association between the tcdC genotype and toxin production. Appl Environ Microbiol 78:4683–4690. http://dx.doi.org/10.1128/AEM.00249-12.
26. Chung WO, Park Y, Lamont RJ, McNab R, Barbieri B, Demuth DR. 2001. Signaling system in Porphyromonas gingivalis based on a LuxS protein. J Bacteriol 183:3903–3909. http://dx.doi.org/10.1128/JB.183.13.3903-3909.2001.
27. Fong KP, Chung WO, Lamont RJ, Demuth DR. 2001. Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect Immun 69:7625–7634. http://dx.doi.org/10.1128/IAI.69.12.7625-7634.2001.
28. Ohtani K, Hayashi H, Shimizu T. 2002. The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Mol Microbiol 44:171–179. http://dx.doi.org/10.1046/j.1365-2958.2002.02863.x.
29. Sperandio V, Mellies JL, Nguyen W, Shin S, Kaper JB. 1999. Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci USA 96:15196–15201. http://dx.doi.org/10.1073/pnas.96.26.15196.
30. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA. 99:3129–3134. http://dx.doi.org/10.1073/pnas.052694299.
31. Miller MB, Bassler BL. 2001. Quorum sensing in bacteria. Annu Rev Microbiol 55:165–199. http://dx.doi.org/10.1146/annurev.micro.55.1.165.
32. Schauder S, Bassler BL. 2001. The languages of bacteria. Genes Dev 15:1468–1480. http://dx.doi.org/10.1101/gad.899601.
33. Darkoh C, Kaplan HB, DuPont HL. 2011. Harnessing the glucosyltransferase activities of Clostridium difficile for functional studies of toxins A and B. J Clin Microbiol 49:2933–2941. http://dx.doi.org/10.1128/JCM.00037-11.
34. Ng WL, Bassler BL. 2009. Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222. http://dx.doi.org/10.1146/annurev-genet-102108-134304.
35. Novick RP, Geisinger E. 2008. Quorum sensing in staphylococci. Annu Rev Genet 42:541–564. http://dx.doi.org/10.1146/annurev.genet.42.110807.091640.
36. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2:pii_a012427. http://dx.doi.org/10.1101/cshperspect.a012427.
37. Bouhenni R, Gehrke A, Saffarini D. 2005. Identification of genes involved in cytochrome c biogenesis in Shewanella oneidensis, using a modified mariner transposon. Appl Environ Microbiol 71:4935–4937. http://dx.doi.org/10.1128/AEM.71.8.4935-4937.2005.
38. Liu ZM, Tucker AM, Driskell LO, Wood DO. 2007. Mariner-based transposon mutagenesis of Rickettsia prowazekii. Appl Environ Microbiol 73:6644–6649. http://dx.doi.org/10.1128/AEM.01727-07.
39. Darkoh C, DuPont HL, Kaplan HB. 2011. Novel one-step method for detection and isolation of active-toxin-producing Clostridium difficile strains directly from stool samples. J Clin Microbiol 49:4219–4224. http://dx.doi.org/10.1128/JCM.01033-11.
40. Martin MJ, Clare S, Goulding D, Faulds-Pain A, Barquist L, Browne HP, Pettit L, Dougan G, Lawley TD, Wren BW. 2013. The agr locus regulates virulence and colonization genes in Clostridium difficile. J Bacteriol 195:3672–3681. http://dx.doi.org/10.1128/JB.00473-13.
41. Chen J, McClane BA. 2012. Role of the Agr-like quorum-sensing system in regulating toxin production by Clostridium perfringens type B strains CN1793 and CN1795. Infect Immun 80:3008-3017. http://dx.doi.org/10.1128/IAI.00438-12.
42. Li J, Chen J, Vidal JE, McClane BA. 2011. The Agr-like quorum-sensing system regulates sporulation and production of enterotoxin and beta2 toxin by Clostridium perfringens type A non-food-borne human gastrointestinal disease strain F5603. Infect Immun 79:2451–2459. http://dx.doi.org/10.1128/IAI.00169-11.
43. Buddelmeijer N, Young R. 2010. The essential Escherichia coli apolipoprotein N-acyltransferase (Lnt) exists as an extracytoplasmic thioester acyl-enzyme intermediate. Biochemistry 49:341–346. http://dx.doi.org/10.1021/bi9020346.
44. List F, Bocola M, Haeger MC, Sterner R. 2012. Constitutively active glutaminase variants provide insights into the activation mechanism of anthranilate synthase. Biochemistry 51:2812–2818. http://dx.doi.org/10.1021/bi201618v.
45. Skaff DA, Ramyar KX, McWhorter WJ, Barta ML, Geisbrecht BV, Miziorko HM. 2012. Biochemical and structural basis for inhibition of Enterococcus faecalis hydroxymethylglutaryl-CoA synthase, mvaS, by hymeglusin. Biochemistry 51:4713-4722. http://dx.doi.org/10.1021/bi300037k.
46. Geisinger E, George EA, Chen J, Muir TW, Novick RP. 2008. Identification of ligand specificity determinants in AgrC, the Staphylococcus aureus quorum-sensing receptor. J Biol Chem 283:8930-8938. http://dx.doi.org/10.1074/jbc.M710227200.
47. Shikita M, Fahey JW, Golden TR, Holtzclaw WD, Talalay P. 1999. An unusual case of “uncompetitive activation” by ascorbic acid: purification and kinetic properties of a myrosinase from Raphanus sativus seedlings. Biochem J 341:725–732. http://dx.doi.org/10.1042/0264-6021:3410725.
48. Wemmer DE, Kern D. 2005. Beryllofluoride binding mimics phosphorylation of aspartate in response regulators. J Bacteriol 187:8229–8230. http://dx.doi.org/10.1128/JB.187.24.8229-8230.2005.
49. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98.
50. Lyerly DM, Saum KE, MacDonald DK, Wilkins TD. 1985. Effects of Clostridium difficile toxins given intragastrically to animals. Infect Immun 47:349–352.