cis-acting elements that control expression of the master virulence regulatory gene atxA in Bacillus anthracis

Journal of Bacteriology

Volumn 194, Issue 15, 2012, Pages 4069-4079

  Dale, Jennifer L ^a   Raynor, Malik J ^a   Dwivedi, Prabhat ^a   Koehler, Theresa M ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX TOXIN; BACTERIAL PROTEIN; CIS ACTING ELEMENT; PALINDROMIC DNA; PROTEIN ATXA; REGULATOR PROTEIN; RNA POLYMERASE; SIGMA FACTOR; TRANS ACTING FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL VIRULENCE; GENE DELETION; GENE EXPRESSION REGULATION; GENE LOCATION; GENETIC TRANSCRIPTION; HOUSEKEEPING GENE; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; STEADY STATE;

ANIMALS; ANTHRAX; BACILLUS ANTHRACIS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MUTAGENESIS, SITE-DIRECTED; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REGULATORY SEQUENCES, NUCLEIC ACID; SEQUENCE DELETION; SIGMA FACTOR; SURVIVAL ANALYSIS; TRANS-ACTIVATORS; TRANSCRIPTION INITIATION SITE; VIRULENCE; VIRULENCE FACTORS;

BACILLUS ANTHRACIS; MURINAE;

EID: 84866342391     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00776-12     Document Type: Article

References (65)

1. Agaisse H, Lereclus D. 1994. Structural and functional analysis of the promoter region involved in full expression of the cryIIIA toxin gene of Bacillus thuringiensis. Mol. Microbiol. 13:97-107.
2. Almengor AC, Kinkel TL, Day SJ, McIver KS. 2007. The catabolite control protein CcpA binds to Pmga and influences expression of the virulence regulator Mga in the group A streptococcus. J. Bacteriol. 189:8405-8416.
3. Arantes O, Lereclus D. 1991. Construction of cloning vectors for Bacillus thuringiensis. Gene 108:115-119.
4. Ausubel FM. 1993. Current protocols in molecular biology. Wiley-Interscience, New York, NY.
5. Bertin M, Chateau A, Fouet A. 2010. Full expression of Bacillus anthracis toxin gene in the presence of bicarbonate requires a 2.7-kb-long atxA mRNAthat contains a terminator structure. Res. Microbiol. 161:249-259.
6. Blatter EE, Ross W, Tang H, Gourse RL, Ebright RH. 1994. Domain organization of RNA polymerase alpha subunit: C-terminal 85 amino acids constitute a domain capable of dimerization and DNA binding. Cell 78:889-896.
7. Bongiorni C, et al. 2008. Dual promoters control expression of the Bacillus anthracis virulence factor AtxA. J. Bacteriol. 190:6483-6492.
8. Bourgogne A, Drysdale M, Hilsenbeck SG, Peterson SN, Koehler TM. 2003. Global effects of virulence gene regulators in a Bacillus anthracis strain with both virulence plasmids. Infect. Immun. 71:2736-2743.
9. Chiang C, Bongiorni C, Perego M. 2011. Glucose-dependent activation of Bacillus anthracis toxin gene expression and virulence requires the carbon catabolite protein CcpA. J. Bacteriol. 193:52-62.
10. 2/bicarbonate, affects AtxA synthesis. Infect. Immun. 65:2576-2582.
11. Dai Z, Sirard JC, Mock M, Koehler TM. 1995. The atxA gene product activates transcription of the anthrax toxin genes and is essential for virulence. Mol. Microbiol. 16:1171-1181.
12. Drysdale M, Bourgogne A, Hilsenbeck SG, Koehler TM. 2004. atxA controls Bacillus anthracis capsule synthesis via acpA and a newly discovered regulator, acpB. J. Bacteriol. 186:307-315.
13. Drysdale M, Bourgogne A, Koehler TM. 2005. Transcriptional analysis of the Bacillus anthracis capsule regulators. J. Bacteriol. 187:5108-5114.
14. Fouet A, Mock M. 1996. Differential influence of the two Bacillus anthracis plasmids on regulation of virulence gene expression. Infect. Immun. 64:4928-4932.
15. Frisby D, Zuber P. 1991. Analysis of the upstream activating sequence and site of carbon and nitrogen source repression in the promoter of an early-induced sporulation gene of Bacillus subtilis. J. Bacteriol. 173:7557-7564.
16. Fujita M, Sadaie Y. 1998. Feedback loops involving Spo0A and AbrB in in vitro transcription of the genes involved in the initiation of sporulation in Bacillus subtilis. J. Biochem. 124:98-104.
17. Fujita Y. 2009. Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci. Biotechnol. Biochem. 73:245-259.
18. Glomski IJ, et al. 2008. Inhaled non-capsulated Bacillus anthracis in A/J. mice: nasopharynx and alveolar space as dual portals of entry, delayed dissemination, and specific organ targeting. Microbes Infect. 10:1398-1404.
19. Gourse RL, Ross W, Gaal T. 2000. UPs and downs in bacterial transcription initiation: the role of the alpha subunit of RNA polymerase in promoter recognition. Mol. Microbiol. 37:687-695.
20. Green J, Paget MS. 2004. Bacterial redox sensors. Nat. Rev. Microbiol. 2:954-966.
21. Greene EA, Spiegelman GB. 1996. The Spo0A protein of Bacillus subtilis inhibits transcription of the abrB gene without preventing binding of the polymerase to the promoter. J. Biol. Chem. 271:11455-11461.
22. Guignot J, Mock M, Fouet A. 1997. AtxA activates the transcription of genes harbored by both Bacillus anthracis virulence plasmids. FEMS Microbiol. Lett. 147:203-207.
23. Hadjifrangiskou M, Chen Y, Koehler TM. 2007. The alternative sigma factor sigma H is required for toxin gene expression by Bacillus anthracis. J. Bacteriol. 189:1874-1883.
24. 2 signalling. Mol. Microbiol. 82:634-647.
25. Iuchi S, Lin EC. 1988. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc. Natl. Acad. Sci. U. S. A. 85:1888-1892.
26. Koehler TM. 2009. Bacillus anthracis physiology and genetics. Mol. Aspects Med. 30:386-396.
27. Koehler TM, Dai Z, Kaufman-Yarbray M. 1994. Regulation of the Bacillus anthracis protective antigen gene: CO2 and a trans-acting element activate transcription from one of two promoters. J. Bacteriol. 176:586-595.
28. Lloyd G, Landini P, Busby S. 2001. Activation and repression of transcription initiation in bacteria. Essays Biochem. 37:17-31.
29. Marrero R, Welkos SL. 1995. The transformation frequency of plasmids into Bacillus anthracis is affected by adenine methylation. Gene 152:75-78.
30. Martin DW, Holloway BW, Deretic V. 1993. Characterization of a locus determining the mucoid status of Pseudomonas aeruginosa: AlgU shows sequence similarities with a Bacillus sigma factor. J. Bacteriol. 175:1153-1164.
31. Mignot T, Mock M, Fouet A. 2003. A plasmid-encoded regulator couples the synthesis of toxins and surface structures in Bacillus anthracis. Mol. Microbiol. 47:917-927.
32. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, New York, NY.
33. Molle V, et al. 2003. The Spo0A regulon of Bacillus subtilis. Mol. Microbiol. 50:1683-1701.
34. Munch R, et al. 2003. PRODORIC: prokaryotic database of gene regulation. Nucleic Acids Res. 31:266-269.
35. Okstad OA, Hegna I, Lindback T, Rishovd AL, Kolsto AB. 1999. Genome organization is not conserved between Bacillus cereus and Bacillus subtilis. Microbiology 145:621-631.
36. Perego M, Spiegelman GB, Hoch JA. 1988. Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis. Mol. Microbiol. 2:689-699.
37. Pflughoeft KJ, Sumby P, Koehler TM. 2011. Bacillus anthracis sin locus and regulation of secreted proteases. J. Bacteriol. 193:631-639.
38. Phillips ZE, Strauch MA. 2002. Bacillus subtilis sporulation and stationary phase gene expression. Cell. Mol. Life Sci. 59:392-402.
39. Predich M, Nair G, Smith I. 1992. Bacillus subtilis early sporulation genes kinA, spo0F, and spo0A are transcribed by theRNApolymerase containing sigma H. J. Bacteriol. 174:2771-2778.
40. Robertson JB, Gocht M, Marahiel MA, Zuber P. 1989. AbrB, a regulator of gene expression in Bacillus, interacts with the transcription initiation regions of a sporulation gene and an antibiotic biosynthesis gene. Proc. Natl. Acad. Sci. U. S. A. 86:8457-8461.
41. Ross W, et al. 1993. A third recognition element in bacterial promoters: DNA binding by the alpha subunit of RNA polymerase. Science 262:1407-1413.
42. Rowe-Magnus DA, Spiegelman GB. 1998. DNA strand separation during activation of a developmental promoter by the Bacillus subtilis response regulator Spo0A. Proc. Natl. Acad. Sci. U. S. A. 95:5305-5310.
43. Saile E, Koehler TM. 2002. Control of anthrax toxin gene expression by the transition state regulator abrB. J. Bacteriol. 184:370-380.
44. Sirard JC, Guidi-Rontani C, Fouet A, Mock M. 2000. Characterization of a plasmid region involved in Bacillus anthracis toxin production and pathogenesis. Int. J. Med. Microbiol. 290:313-316.
45. Stephenson K, Hoch JA. 2002. Evolution of signalling in the sporulation phosphorelay. Mol. Microbiol. 46:297-304.
46. Stratagene. 2007. QuikChange site-directed mutagenesis kit: instruction manual. Stratagene, LaJolla, CA.
47. Strauch M, Webb V, Spiegelman G, Hoch JA. 1990. The SpoOA protein of Bacillus subtilis is a repressor of the abrB gene. Proc. Natl. Acad. Sci. U. S. A. 87:1801-1805.
48. Strauch MA. 1995. Delineation of AbrB-binding sites on the Bacillus subtilis spo0H, kinB, ftsAZ, and pbpE promoters and use of a derived homology to identify a previously unsuspected binding site in the bsuB1 methylase promote. J. Bacteriol. 177:6999-7002.
49. Strauch MA. 1993. Regulation of Bacillus subtilis gene expression during the transition from exponential growth to stationary phase. Prog. Nucleic Acid Res. Mol. Biol. 46:121-153.
50. Strauch MA, Ballar P, Rowshan AJ, Zoller KL. 2005. The DNA-binding specificity of the Bacillus anthracis AbrB protein. Microbiology 151:1751-1759.
51. Strauch MA, Hoch JA. 1993. Transition-state regulators: sentinels of Bacillus subtilis post-exponential gene expression. Mol. Microbiol. 7:337-342.
52. Strauch MA, Trach KA, Day J, Hoch JA. 1992. Spo0A activates and represses its own synthesis by binding at its dual promoters. Biochimie 74:619-626.
53. Thorne CB. 1985. Genetics of Bacillus anthracis, p 56-62. In Leive L (ed), Microbiology 1985. American Society for Microbiology, Washington, DC.
54. Thorne CB, Belton FC. 1957. An agar-diffusion method for titrating Bacillus anthracis immunizing antigen and its application to a study of antigen production. J. Gen. Microbiol. 17:505-516.
55. Tinsley E, Khan SA. 2007. A Bacillus anthracis-based in vitro system supports replication of plasmid pXO2 as well as rolling-circle-replicating plasmids. Appl. Environ. Microbiol. 73:5005-5010.
56. Tsvetanova B, et al. 2007. Opposing effects of histidine phosphorylation regulate the AtxA virulence transcription factor in Bacillus anthracis. Mol. Microbiol. 63:644-655.
57. Uchida I, Hornung JM, Thorne CB, Klimpel KR, Leppla SH. 1993. Cloning and characterization of a gene whose product is a trans-activator of anthrax toxin synthesis. J. Bacteriol. 175:5329-5338.
58. Uchida I, Makino S, Sekizaki T, Terakado N. 1997. Cross-talk to the genes for Bacillus anthracis capsule synthesis by atxA, the gene encoding the trans-activator of anthrax toxin synthesis. Mol. Microbiol. 23:1229-1240.
59. van Schaik W, et al. 2009. The global regulator CodY regulates toxin gene expression in Bacillus anthracis and is required for full virulence. Infect. Immun. 77:4437-4445.
60. Warner JB, Lolkema JS. 2003. CcpA-dependent carbon catabolite repression in bacteria. Microbiol. Mol. Biol. Rev. 67:475-490.
61. Welkos S, Little S, Friedlander A, Fritz D, Fellows P. 2001. The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology 147:1677-1685.
62. Welkos SL, Keener TJ, Gibbs PH. 1986. Differences in susceptibility of inbred mice to Bacillus anthracis. Infect. Immun. 51:795-800.
63. Wilson AC, Hoch JA, Perego M. 2009. Two small c-type cytochromes affect virulence gene expression in Bacillus anthracis. Mol. Microbiol. 72:109-123.
64. Wong HC, Chang S. 1986. Identification of a positive retroregulator that stabilizes mRNAs in bacteria. Proc. Natl. Acad. Sci. U. S. A. 83:3233-3237.
65. Zalieckas JM, Wray LV, Jr, Fisher SH. 1998. Expression of the Bacillus subtilis acsA gene: position and sequence context affect cre-mediated carbon catabolite repression. J. Bacteriol. 180:6649-6654.