Two-Component Signal Transduction System CBO0787/CBO0786 Represses Transcription from Botulinum Neurotoxin Promoters in Clostridium botulinum ATCC 3502

PLoS Pathogens

Volumn 9, Issue 3, 2013, Pages

  Zhang, Zhen ^a   Korkeala, Hannu ^a   Dahlsten, Elias ^a   Sahala, Elina ^a   Heap, John T ^b   Minton, Nigel P ^b   Lindström, Miia ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BOTULINUM TOXIN;

ARTICLE; BACTERIAL STRAIN; CBO0786 GENE; CBO0787 GENE; CLOSTRIDIUM BOTULINUM; CONTROLLED STUDY; DNA FOOTPRINTING; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE; GENE EXPRESSION; GENE MUTATION; GROWTH CURVE; NONHUMAN; OPERON; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; BOTULINUM TOXINS, TYPE A; CLOSTRIDIUM BOTULINUM TYPE A; GENE EXPRESSION REGULATION, BACTERIAL; GENE SILENCING; GENES, REGULATOR; MUTAGENESIS, INSERTIONAL; NEUROTOXINS; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; RNA, BACTERIAL; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM BOTULINUM;

EID: 84875975840     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003252     Document Type: Article

References (55)

1. Schiavo G, Benfenati F, Poulain B, Rossetto O, Polverino de Laureto P, et al. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359: 832-835.
2. Blasi J, Chapman ER, Link E, Binz T, Yamasaki S, et al. (1993) Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 365: 160-163.
3. Johnson EA, (1999) Clostridial toxins as therapeutic agents: Benefits of nature's most toxic proteins. Annu Rev Microbiol 53: 551-575.
4. Lim EC, Seet RC, (2010) Use of botulinum toxin in the neurology clinic. Nat Rev Neurol 6: 624-636.
5. Diener HC, Holle D, Dodick D, (2011) Treatment of chronic migraine. Curr Pain Headache Rep 15: 64-69.
6. Chuang YC, Chancellor MB, (2006) The application of botulinum toxin in the prostate. J Urol 176: 2375-2382.
7. Ansiaux R, Gallez B, (2007) Use of botulinum toxins in cancer therapy. Expert Opin Investig Drugs 16: 209-218.
8. Smith TJ, Lou J, Geren IN, Forsyth CM, Tsai R, et al. (2005) Sequence variation within botulinum neurotoxin serotypes impacts antibody binding and neutralization. Infect Immun 73: 5450-5457.
9. Hill KK, Smith TJ, Helma CH, Ticknor LO, Foley BT, et al. (2007) Genetic diversity among botulinum neurotoxin-producing clostridial strains. J Bacteriol 189: 818-832.
10. Chen Y, Korkeala H, Aarnikunnas J, Lindström M, (2007) Sequencing the botulinum neurotoxin gene and related genes in Clostridium botulinum type E strains reveals orfx3 and a novel type E neurotoxin subtype. J Bacteriol 189: 8643-8650.
11. Dover N, Barash JR, Arnon SS, (2009) Novel Clostridium botulinum toxin gene arrangement with subtype A5 and partial subtype B3 botulinum neurotoxin genes. J Clin Microbiol 47: 2349-2350.
12. Macdonald TE, Helma CH, Shou Y, Valdez YE, Ticknor LO, et al. (2011) Analysis of Clostridium botulinum serotype E strains by using multilocus sequence typing, amplified fragment length polymorphism, variable-number tandem-repeat analysis, and botulinum neurotoxin gene sequencing. Appl Environ Microbiol 77: 8625-8634.
13. Schantz EJ, Johnson EA, (1992) Properties and use of botulinum toxin and other microbial neurotoxins in medicine. Microbiol Rev 56: 80-99.
14. Matsumura T, Jin Y, Kabumoto Y, Takegahara Y, Oguma K, et al. (2008) The HA proteins of botulinum toxin disrupt intestinal epithelial intercellular junctions to increase toxin absorption. Cell Microbiol 10: 355-364.
15. Lamanna C, (1948) Hemagglutination by botulinal toxin. Proc Soc Exp Biol Med 69: 332-336.
16. Sugii S, Sakaguchi G, (1975) Molecular construction of Clostridium botulinum type A toxins. Infect Immun 12: 1262-1270.
17. Dineen SS, Bradshaw M, Johnson EA, (2003) Neurotoxin gene clusters in Clostridium botulinum type A strains: sequence comparison and evolutionary implications. Curr Microbiol 46: 345-352.
18. Gu S, Rumpel S, Zhou J, Strotmeier J, Bigalke H, et al. (2012) Botulinum neurotoxin is shielded by NTNHA in an interlocked complex. Science 335: 977-981.
19. Bradshaw M, Dineen SS, Maks ND, Johnson EA, (2004) Regulation of neurotoxin complex expression in Clostridium botulinum strains 62A, Hall A-hyper, and NCTC 2916. Anaerobe 10: 321-333.
20. Raffestin S, Dupuy B, Marvaud JC, Popoff MR, (2005) BotR/A and TetR are alternative RNA sigma factors controlling the expression of the neurotoxin and associated protein genes in Clostridium botulinum type A and Clostridium tetani. Mol Microbiol 55: 235-249.
21. Pattersoncurtis SI, Johnson EA, (1989) Regulation of neurotoxin and protease formation in Clostridium botulinum Okra B and Hall A by arginine. Appl Environ Microbiol 55: 1544-1548.
22. Leyer GJ, Johnson EA, (1990) Repression of toxin production by tryptophan in Clostridium botulinum type E. Arch Microbiol 154: 443-447.
23. Bonventre PF, Kempe LL, (1959) Physiology of toxin production by Clostridium botulinum types A and B. II. Effect of carbohydrate source on growth, autolysis, and toxin production. Appl Microbiol 7: 372-374.
24. Chen Y, Korkeala H, Lindén J, Lindström M, (2008) Quantitative real-time reverse transcription PCR analysis reveals stable and prolonged neurotoxin complex gene activity in Clostridium botulinum type E at refrigeration temperature. Appl Environ Microbiol 74: 6132-6137.
25. Marvaud JC, Gibert M, Inoue K, Fujinaga Y, Oguma K, et al. (1998) botR/A is a positive regulator of botulinum neurotoxin and associated non-toxin protein genes in Clostridium botulinum A. Mol Microbiol 29: 1009-1018.
26. Cooksley CM, Davis IJ, Winzer K, Chan WC, Peck MW, et al. (2010) Regulation of neurotoxin production and sporulation by a putative agrBD signaling system in proteolytic Clostridium botulinum. Appl Environ Microbiol 76: 4448-4460.
27. Beier D, Gross R, (2006) Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 9: 143-152.
28. Connan C, Brueggemann H, Mazuet C, Raffestin S, Cayet N, Popoff MR, (2012) Two-component systems are involved in the regulation of Botulinum neurotoxin synthesis in Clostridium botulinum type A strain Hall. PLoS One 7: e41848 doi:10.1371/journal.pone.0041848.
29. Sebaihia M, Peck MW, Minton NP, Thomson NR, Holden MT, et al. (2007) Genome sequence of a proteolytic (Group I) Clostridium botulinum strain Hall A and comparative analysis of the clostridial genomes. Genome Res 17: 1082-1092.
30. Wörner K, Szurmant H, Chiang C, Hoch JA, (2006) Phosphorylation and functional analysis of the sporulation initiation factor Spo0A from Clostridium botulinum. Mol Microbiol 59: 1000-1012.
31. Selby K, Lindström M, Somervuo P, Heap JT, Minton NP, et al. (2011) Important role of Class I heat shock genes hrcA and dnaK in the heat shock response and the response to pH and NaCl stress of Group I Clostridium botulinum strain ATCC 3502. Appl Environ Microbiol 77: 2823-2830.
32. Söderholm H, Lindström M, Somervuo P, Heap J, Minton NP, et al. (2011) cspB encodes a major cold shock protein in Clostridium botulinum ATCC 3502. Int J Food Microbiol 146: 23-30.
33. Heap JT, Pennington OJ, Cartman ST, Carter GP, Minton NP, (2007) The ClosTron: a universal gene knock-out system for the genus Clostridium. J Microbiol Methods 70: 452-464.
34. Couesnon A, Raffestin S, Popoff MR, (2006) Expression of botulinum neurotoxins A and E, and associated non-toxin genes, during the transition phase and stability at high temperature: analysis by quantitative reverse transcription-PCR. Microbiol 152: 759-770.
35. Henderson I, Whelan SM, Davis TO, Minton NP, (1996) Genetic characterisation of the botulinum toxin complex of Clostridium botulinum strain NCTC 2916. FEMS Microbiol Lett 140: 151-158.
36. Johnson EA, Bradshaw M, (2001) Clostridium botulinum and its neurotoxins: a metabolic and cellular perspective. Toxicon 39: 1703-1722.
37. Raffestin S, Couesnon A, Pereira Y, Mazuet C, Popoff MR (2009) Botulinum and tetanus neurotoxins: molecular biology, toxin gene regulation and mode of action. In Brüggemann H, Gottschalk G, editors. Clostridia: molecular biology in the post-genomic era. Norfolk: Caister Academic Press. pp. 1-28.
38. Dupuy B, Raffestin S, Matamouros S, Mani N, Popoff MR, Sonenshein AL, (2006) Regulation of toxin and bacteriocin gene expression in Clostridium by interchangeable RNA polymerase sigma factors. Mol Microbiol 60: 1044-1057.
39. Marvaud JC, Eisel U, Binz T, Niemann H, Popoff MR, (1998) tetR is a positive regulator of the tetanus toxin gene in Clostridium tetani and is homologous to botR. Infect Immun 66: 5698-5702.
40. Mani N, Dupuy B, (2001) Regulation of toxin synthesis in Clostridium difficile by an alternative RNA polymerase sigma factor. Proc Natl Acad Sci U S A 98: 5844-5849.
41. Garnier T, Cole ST, (1988) Studies of UV-inducible promoters from Clostridium perfringens in vivo and in vitro. Mol Microbiol 2: 607-614.
42. Gryllos I, Levin JC, Wessels MR, (2003) The CsrR/CsrS two-component system of group A Streptococcus responds to environmental Mg2+. Proc Natl Acad Sci U S A 100: 4227-4232.
43. Gao R, Stock AM, (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63: 133-154.
44. He H, Zahrt TC, (2005) Identification and characterization of a regulatory sequence recognized by Mycobacterium tuberculosis persistence regulator MprA. J Bacteriol 187: 202-212.
45. Mittal S, Kroos L, (2009) A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression. Proc Natl Acad Sci U S A 106: 1965-1970.
46. Sinha A, Gupta S, Bhutani S, Pathak A, Sarkar D, (2008) PhoP-PhoP interaction at adjacent PhoP binding sites is influenced by protein phosphorylation. J Bacteriol 190: 1317-1328.
47. Antunes A, Martin-Verstraete I, Dupuy B, (2011) CcpA-mediated repression of Clostridium difficile toxin gene expression. Mol Microbiol 79: 882-899.
48. Antunes A, Camiade E, Monot M, Courtois E, Barbut F, et al. (2012) Global transcriptional control by glucose and carbon regulator CcpA in Clostridium difficile. Nucleic Acids Res pp. 10.1093/nar/gks864.
49. Kunehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A, et al. (2010) The role of toxin A and toxin B in Clostridium difficile infection. Nature 467: 711-713.
50. Carter GP, Douce GR, Govind R, Howarth PM, Mackin KE, et al. (2011) The anti-sigma factor TcdC modulates hypervirulence in an epidemic BI/NAP1/027 clinical isolate of Clostridium difficile. PLoS Pathog 7e1002317: 10.1371/journal.ppat.1002317.
51. Purdy D, O'keeffe TAT, Elmore M, Herbert M, McLeod A, et al. (2002) Conjugative transfer of clostridial shuttle vectors from Escherichia coli to Clostridium difficile through circumvention of the restriction barrier. Mol Microbiol 46: 439-452.
52. Heap JT, Pennington OJ, Cartman ST, Minton NP, (2009) A modular system for Clostridium shuttle plasmids. J Microbiol Methods 78: 79-85.
53. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45 doi:10.1093/nar/29.9.e45.
54. Mccleary WR, Stock JB, (1994) Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 269: 31567-31572.
55. Zianni M, Tessanne K, Merighi M, Laguna R, Tabita FR, (2006) Identification of the DNA bases of a DNase I footprint by the use of dye primer sequencing on an automated capillary DNA analysis instrument. J Biomol Tech 17: 103-113.