Expression of the large clostridial toxins is controlled by conserved regulatory mechanisms

International Journal of Medical Microbiology

Volumn 304, Issue 8, 2014, Pages 1147-1159

  Carter, Glen P ^a   Larcombe, Sarah ^a   Li, Lucy ^a   Jayawardena, Darshani ^a   Awad, Milena M ^a   Songer, J Glenn ^b   Lyras, Dena ^a  

^a MONASH UNIVERSITY   (Australia)

^b IOWA STATE UNIVERSITY   (United States)

Author keywords

Clostridium difficile; Clostridium disease; Clostridium perfringens; Clostridium sordellii; Large clostridial toxin; Toxin regulation

Indexed keywords

BACTERIAL TOXIN; BOTULINUM TOXIN; GLUCOSE; POLYCLONAL ANTISERUM; SIGMA FACTOR; TETANUS TOXIN;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIOPHAGE; CLOSTRIDIA; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM PERFRINGENS; CLOSTRIDIUM SORDELLII; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; CYTOTOXICITY; CYTOTOXICITY ASSAY; GENE LOCUS; HT 29 CELL LINE; NONHUMAN; PATHOGENICITY; PHYLOGENY; PLASMID; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SOUTHERN BLOTTING; SUPERNATANT; VECTOR CONTROL; VERO CELL LINE; WESTERN BLOTTING; WILD TYPE;

EID: 84940164887     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.08.008     Document Type: Article

References (57)

1. Aldape M.J., Bryant A.E., Stevens D.L. Clostridium sordellii infection: epidemiology, clinical findings, and current perspectives on diagnosis and treatment. Clin. Infect. Dis. 2006, 43:1436-1446.
2. Amimoto K., Noro T., Oishi E., Shimizu M. A novel toxin homologous to large clostridial cytotoxins found in culture supernatant of Clostridium perfringens type C. Microbiology 2007, 153:1198-1206.
3. Antunes A., Camiade E., Monot M., Courtois E., Barbut F., Sernova N.V., Rodionov D.A., Martin-Verstraete I., Dupuy B. Global transcriptional control by glucose and carbon regulator CcpA in Clostridium difficile. Nucleic Acids Res. 2012, 40:10701-10718.
4. Antunes A., Martin-Verstraete I., Dupuy B. CcpA-mediated repression of Clostridium difficile toxin gene expression. Mol. Microbiol. 2011, 79:882-899.
5. Bakker D., Smits W.K., Kuijper E.J., Corver J. TcdC does not significantly repress toxin expression in Clostridium difficile 630DeltaErm. PLoS One 2012, 7:e43247.
6. Boyer H.W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 1969, 41:459-472.
7. Braun V., Hundsberger T., Leukel P., Sauerborn M., von Eichel-Streiber C. Definition of the single integration site of the pathogenicity locus in Clostridium difficile. Gene 1996, 181:29-38.
8. Brouwer M.S., Roberts A.P., Hussain H., Williams R.J., Allan E., Mullany P. Horizontal gene transfer converts non-toxigenic Clostridium difficile strains into toxin producers. Nat. Commun. 2013, 4:2601.
9. Busch C., Schomig K., Hofmann F., Aktories K. Characterization of the catalytic domain of Clostridium novyi alpha-toxin. Infect. Immun. 2000, 68:6378-6383.
10. Carter G.P., Awad M.M., Hao Y., Thelen T., Bergin I.L., Howarth P.M., Seemann T., Rood J.I., Aronoff D.M., Lyras D. TcsL is an essential virulence factor in Clostridium sordellii ATCC9714. Infect. Immun. 2011, 79:1025-1032.
11. Carter G.P., Douce G.R., Govind R., Howarth P.M., Mackin K.E., Spencer J., Buckley A.M., Antunes A., Kotsanas D., Jenkin G.A., Dupuy B., Rood J.I., Lyras D. The anti-sigma factor TcdC modulates hypervirulence in an epidemic BI/NAP1/027 clinical isolate of Clostridium difficile. PLoS Pathog. 2011, 7:e1002317.
12. Carter G.P., Lyras D., Allen D.L., Mackin K.E., Howarth P.M., O'Connor J.R., Rood J.I. Binary toxin production in Clostridium difficile is regulated by CdtR, a LytTR family response regulator. J. Bacteriol. 2007, 189:7290-7301.
13. Cartman S.T., Kelly M.L., Heeg D., Heap J.T., Minton N.P. Precise manipulation of the Clostridium difficile chromosome reveals a lack of association between the tcdC genotype and toxin production. Appl. Environ. Microbiol. 2012, 78:4683-4690.
14. Chen J., McClane B.A. Role of the Agr-like quorum-sensing system in regulating toxin production by Clostridium perfringens type B strains CN1793 and CN1795. Infect. Immun. 2012, 80:3008-3017.
15. Chen J., Rood J.I., McClane B.A. Epsilon-toxin production by Clostridium perfringens type D strain CN3718 is dependent upon the agr operon but not the VirS/VirR two-component regulatory system. mBio 2011, 2.
16. Cheung J.K., Keyburn A.L., Carter G.P., Lanckriet A.L., Van Immerseel F., Moore R.J., Rood J.I. The VirSR two-component signal transduction system regulates NetB toxin production in Clostridium perfringens. Infect. Immun. 2010, 78:3064-3072.
17. Cooksley C.M., Davis I.J., Winzer K., Chan W.C., Peck M.W., Minton N.P. Regulation of neurotoxin production and sporulation by a Putative agrBD signaling system in proteolytic Clostridium botulinum. Appl. Environ. Microbiol. 2010, 76:4448-4460.
18. Dang L.H., Bettegowda C., Huso D.L., Kinzler K.W., Vogelstein B. Combination bacteriolytic therapy for the treatment of experimental tumors. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:15155-15160.
19. Dupuy B., Govind R., Antunes A., Matamouros S. Clostridium difficile toxin synthesis is negatively regulated by TcdC. J. Med. Microbiol. 2008, 57:685-689.
20. Dupuy B., Mani N., Katayama S., Sonenshein A.L. Transcription activation of a UV-inducible Clostridium perfringens bacteriocin gene by a novel sigma factor. Mol. Microbiol. 2005, 55:1196-1206.
21. Dupuy B., Raffestin S., Matamouros S., Mani N., Popoff M.R., Sonenshein A.L. Regulation of toxin and bacteriocin gene expression in Clostridium by interchangeable RNA polymerase sigma factors. Mol. Microbiol. 2006, 60:1044-1057.
22. Dupuy B., Sonenshein A.L. Regulated transcription of Clostridium difficile toxin genes. Mol. Microbiol. 1998, 27:107-120.
23. Eklund M.W., Poysky F.T., Meyers J.A., Pelroy G.A. Interspecies conversion of Clostridium botulinum type C to Clostridium novyi type A by bacteriophage. Science (New York, NY) 1974, 186:456-458.
24. Eklund M.W., Poysky F.T., Peterson M.E., Meyers J.A. Relationship of bacteriophages to alpha toxin production in Clostridium novyi types A and B. Infect. Immun. 1976, 14:793-803.
25. Govind R., Dupuy B. Secretion of Clostridium difficile toxins A and B requires the holin-like protein TcdE. PLoS Pathog. 2012, 8:e1002727.
26. Gurjar A., Li J., McClane B.A. Characterization of toxin plasmids in Clostridium perfringens type C isolates. Infect. Immun. 2010, 78:4860-4869.
27. Hall I.C., Scott A.L. The serologic agglutination of Bacillus Sordellii and Clostridium oedematoides. J. Bacteriol. 1931, 22:375-385.
28. Hao Y., Senn T., Opp J.S., Young V.B., Thiele T., Srinivas G., Huang S.K., Aronoff D.M. Lethal toxin is a critical determinant of rapid mortality in rodent models of Clostridium sordellii endometritis. Anaerobe 2010, 16:155-160.
29. Hundsberger T., Braun V., Weidmann M., Leukel P., Sauerborn M., von Eichel-Streiber C. Transcription analysis of the genes tcdA-E of the pathogenicity locus of Clostridium difficile. Eur. J. Biochem. 1997, 244:735-742.
30. Jank T., Aktories K. Structure and mode of action of clostridial glucosylating toxins: the ABCD model. Trends Microbiol. 2008, 16:222-229.
31. Kuehne S.A., Cartman S.T., Heap J.T., Kelly M.L., Cockayne A., Minton N.P. The role of toxin A and toxin B in Clostridium difficile infection. Nature 2010, 467:711-713.
32. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
33. Li J., Chen J., Vidal J.E., McClane B.A. 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. 2011, 79:2451-2459.
34. Lyras D., O'Connor J.R., Howarth P.M., Sambol S.P., Carter G.P., Phumoonna T., Poon R., Adams V., Vedantam G., Johnson S., Gerding D.N., Rood J.I. Toxin B is essential for virulence of Clostridium difficile. Nature 2009, 458:1176-1179.
35. Lyras D., Rood J.I. Conjugative transfer of RP4-oriT shuttle vectors from Escherichia coli to Clostridium perfringens. Plasmid 1998, 39:160-164.
36. Lyristis M., Bryant A.E., Sloan J., Awad M.M., Nisbet I.T., Stevens D.L., Rood J.I. Identification and molecular analysis of a locus that regulates extracellular toxin production in Clostridium perfringens. Mol. Microbiol. 1994, 12:761-777.
37. Majumdar S., Woodcock S., Cheesbrough J. Severe sepsis following wound infection by an unusual organism-Clostridium novyi. Int. J. Clin. Pract. 2004, 58:892-893.
38. Mani N., Dupuy B. Regulation of toxin synthesis in Clostridium difficile by an alternative RNA polymerase sigma factor. Proc. Natl. Acad. Sci. U.S.A 2001, 98:5844-5849.
39. Mani N., Lyras D., Barroso L., Howarth P., Wilkins T., Rood J.I., Sonenshein A.L., Dupuy B. Environmental response and autoregulation of Clostridium difficile TxeR, a sigma factor for toxin gene expression. J. Bacteriol. 2002, 184:5971-5978.
40. Martin M.J., Clare S., Goulding D., Faulds-Pain A., Barquist L., Browne H.P., Pettit L., Dougan G., Lawley T.D., Wren B.W. The agr locus regulates virulence and colonization genes in Clostridium difficile 027. J. Bacteriol. 2013, 195:3672-3681.
41. Marvaud J.C., Eisel U., Binz T., Niemann H., Popoff M.R. TetR is a positive regulator of the tetanus toxin gene in Clostridium tetani and is homologous to BotR. Infect. Immun. 1998, 66:5698-5702.
42. Marvaud J.C., Gibert M., Inoue K., Fujinaga Y., Oguma K., Popoff M.R. BotR/A is a positive regulator of botulinum neurotoxin and associated non-toxin protein genes in Clostridium botulinum A. Mol. Microbiol. 1998, 29:1009-1018.
43. Matamouros S., England P., Dupuy B. Clostridium difficile toxin expression is inhibited by the novel regulator TcdC. Mol. Microbiol. 2007, 64:1274-1288.
44. Missiakas D., Raina S. The extracytoplasmic function sigma factors: role and regulation. Mol. Microbiol. 1998, 28:1059-1066.
45. Myers G.S., Rasko D.A., Cheung J.K., Ravel J., Seshadri R., DeBoy R.T., Ren Q., Varga J., Awad M.M., Brinkac L.M., Daugherty S.C., Haft D.H., Dodson R.J., Madupu R., Nelson W.C., Rosovitz M.J., Sullivan S.A., Khouri H., Dimitrov G.I., Watkins K.L., Mulligan S., Benton J., Radune D., Fisher D.J., Atkins H.S., Hiscox T., Jost B.H., Billington S.J., Songer J.G., McClane B.A., Titball R.W., Rood J.I., Melville S.B., Paulsen I.T. Skewed genomic variability in strains of the toxigenic bacterial pathogen, Clostridium perfringens. Genome Res. 2006, 16:1031-1040.
46. O'Connor J.R., Lyras D., Farrow K.A., Adams V., Powell D.R., Hinds J., Cheung J.K., Rood J.I. Construction and analysis of chromosomal Clostridium difficile mutants. Mol. Microbiol. 2006, 61:1335-1351.
47. Olling A., Seehase S., Minton N.P., Tatge H., Schroter S., Kohlscheen S., Pich A., Just I., Gerhard R. Release of TcdA and TcdB from Clostridium difficile cdi 630 is not affected by functional inactivation of the tcdE gene. Microb. Pathog. 2012, 52:92-100.
48. Palombo E.A., Yusoff K., Stanisich V.A., Krishnapillai V., Willetts N.S. Cloning and genetic analysis of tra cistrons of the Tra 2/Tra 3 region of plasmid RP1. Plasmid 1989, 22:59-69.
49. Reddy B.L., Saier M.H. Topological and phylogenetic analyses of bacterial holin families and superfamilies. Biochim. Biophys. Acta 2013, 1828:2654-2671.
50. Redelings M.D., Sorvillo F., Mascola L. Increase in Clostridium difficile-related mortality rates, United States, 1999-2004. Emerg. Infect. Dis. 2007, 13:1417-1419.
51. Sirigi Reddy A.R., Girinathan B.P., Zapotocny R., Govind R. Identification and characterization of Clostridium sordellii toxin gene regulator. J. Bacteriol. 2013, 195:4246-4254.
52. Smith C.J., Markowitz S.M., Macrina F.L. Transferable tetracycline resistance in Clostridium difficile. Antimicrob. Agents Chemother. 1981, 19:997-1003.
53. Tan K.S., Wee B.Y., Song K.P. Evidence for holin function of tcdE gene in the pathogenicity of Clostridium difficile. J. Med. Microbiol. 2001, 50:613-619.
54. Vidal J.E., Chen J., Li J., McClane B.A. Use of an EZ-Tn5-based random mutagenesis system to identify a novel toxin regulatory locus in Clostridium perfringens strain 13. PLoS One 2009, 4:e6232.
55. Voth D.E., Martinez O.V., Ballard J.D. Variations in lethal toxin and cholesterol-dependent cytolysin production correspond to differences in cytotoxicity among strains of Clostridium sordellii. FEMS Microbiol. Lett. 2006, 259:295-302.
56. Walk S.T., Jain R., Trivedi I., Grossman S., Newton D.W., Thelen T., Hao Y., Songer J.G., Carter G.P., Lyras D., Young V.B., Aronoff D.M. Non-toxigenic Clostridium sordellii: clinical and microbiological features of a case of cholangitis-associated bacteremia. Anaerobe 2011, 17:252-256.
57. Wust J., Hardegger U. Transferable resistance to clindamycin, erythromycin, and tetracycline in Clostridium difficile. Antimicrob. Agents Chemother. 1983, 23:784-786.