Molecular mechanism of tryptophan-dependent transcriptional regulation in Chlamydia trachomatis

Journal of Bacteriology

Volumn 188, Issue 12, 2006, Pages 4236-4243

  Akers, Johnny C ^a   Tan, Ming ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; PROTEIN TRPR; REGULATOR PROTEIN; RNA POLYMERASE; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; ARTICLE; CHLAMYDIA TRACHOMATIS; HOST RESISTANCE; MOLECULAR MECHANICS; NONHUMAN; OPERON; PATHOGENESIS; PLANT GROWTH; PRIORITY JOURNAL; PROMOTER REGION; REGULATOR GENE; TRANSCRIPTION REGULATION; TRPA GENE; TRPB GENE; TRPRBA GENE; TRYPTOPHAN METABOLISM;

BACTERIAL PROTEINS; BASE SEQUENCE; CHLAMYDIA TRACHOMATIS; DNA-DIRECTED RNA POLYMERASES; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENES, REGULATOR; MOLECULAR SEQUENCE DATA; OPERON; PROMOTER REGIONS (GENETICS); REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC; TRYPTOPHAN; TRYPTOPHAN SYNTHASE;

CHLAMYDIA; CHLAMYDIA TRACHOMATIS; CHLAMYDIACEAE; CHLAMYDIAE; NEGIBACTERIA;

EID: 33744987184     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01660-05     Document Type: Article

References (43)

1. Beatty, W. L., G. I. Byrne, and R. P. Morrison. 1993. Morphologic and antigenic characterization of interferon gamma-mediated persistent Chlamydia trachomatis infection in vitro. Proc. Natl. Acad. Sci. USA 90:3998-4002.
2. Beatty, W. L., R. P. Morrison, and G. I. Byrne. 1994. Persistent chlamydiae: from cell culture to a paradigm of chlamydial pathogenesis. Microbiol. Rev. 58:686-699.
3. Belland, R. J., D. E. Nelson, D. Virok, D. D. Crane, D. Hogan, D. Sturdevant, W. L. Beatty, and H. D. Caldwell. 2003. Transcriptome analysis of chlamydial growth during IFN-gamma-mediated persistence and reactivation. Proc. Natl. Acad. Sci. USA 100:15971-15976.
4. Carey, J. 1988. Gel retardation at low pH resolves trp repressor-DNA complexes for quantitative study. Proc. Natl. Acad. Sci. USA 85:975-979.
5. Carlson, J. H., H. Wood, C. Roshick, H. D. Caldwell, and G. McClarty. 2006. In vivo and in vitro studies of Chlamydia trachomatis TrpR:DNA interactions. Mol. Microbiol. 59:1678-1691.
6. Engel, J. N., and D. Ganem. 1987. Chlamydial rRNA operons: gene organization and identification of putative tandem promoters. J. Bacteriol. 169:5678-5685.
7. Fehlner-Gardiner, C., C. Roshick, J. H. Carlson, S. Hughes, R. J. Belland, H. D. Caldwell, and G. McClarty. 2002. Molecular basis defining human Chlamydia trachomatis tissue tropism. A possible role for tryptophan synthase. J. Biol. Chem. 277:26893-26903.
8. Gerard, H. C., L. Kohler, P. J. Branigan, H. Zeidler, H. R. Schumacher, and A. P. Hudson. 1998. Viability and gene expression in Chlamydia trachomatis during persistent infection of cultured human monocytes. Med. Microbiol. Immunol. 187:115-120.
9. Gerard, H. C., B. Krausse-Opatz, Z. Wang, D. Rudy, J. P. Rao, H. Zeidler, H. R. Schumacher, J. A. Whittum-Hudson, L. Kohler, and A. P. Hudson. 2001. Expression of Chlamydia trachomatis genes encoding products required for DNA synthesis and cell division during active versus persistent infection. Mol. Microbiol. 41:731-741.
10. Gieffers, J., L. Durling, S. P. Ouellette, J. Rupp, M. Maass, G. I. Byrne, H. D. Caldwell, and R. J. Belland. 2003. Genotypic differences in the Chlamydia pneumoniae tyrP locus related to vascular tropism and pathogenicity. J. Infect. Dis. 188:1085-1093.
11. Gunsalus, R. P., and C. Yanofsky. 1980. Nucleotide sequence and expression of Escherichia coli trpR, the structural gene for the trp aporepressor. Proc. Natl. Acad. Sci. USA 77:7117-7121.
12. Heatwole, V. M., and R. L. Somerville. 1992. Synergism between the Trp repressor and Tyr repressor in repression of the aroL promoter of Escherichia coli K-12. J. Bacteriol. 174:331-335.
13. Heatwole, V. M., and R. L. Somerville. 1991. The tryptophan-specific permease gene, mtr, is differentially regulated by the tryptophan and tyrosine repressors in Escherichia coli K-12. J. Bacteriol. 173:3601-3604.
14. Horn, M., A. Collingro, S. Schmitz-Esser, C. L. Beier, U. Purkhold, B. Fartmann, P. Brandt, G. J. Nyakatura, M. Droege, D. Frishman, T. Rattei, H.-W. Mewes, and M. Wagner. 2004. Illuminating the evolutionary history of chlamydiae. Science 304:728-730.
15. Jeeves, M., P. D. Evans, R. A. Parslow, M. Jaseja, and E. I. Hyde. 1999. Studies of the Escherichia coli Trp repressor binding to its five operators and to variant operator sequences. Eur. J. Biochem. 265:919-928.
16. Mathews, S., and P. Timms. In silico identification of chlamydial promoters and their role in regulation of development. In P. M. Bavoil and P. B. Wyrick (ed.). Chlamydia: genomics, pathogenesis and implications for control, in press. Horizon Scientific Press, Wymondham, United Kingdom.
17. Merino, E., and C. Yanofsky. 2005. Transcription attenuation: a highly conserved regulatory strategy used by bacteria. Trends Genet. 21:260-264.
18. Mironov, A., E. Koonin, M. Roytberg, and M. Gelfand. 1999. Computer analysis of transcription regulatory patterns in completely sequenced bacterial genomes. Nucleic Acids Res. 27:2981-2989.
19. Rau, A., S. Wyllie, J. Whittimore, and J. E. Raulston. 2005. Identification of Chlamydia trachomatis genomic sequences recognized by chlamydial divalent cation-dependent regulator A (DcrA). J. Bacteriol. 187:443-448.
20. Read, T. D., R. C. Brunham, C. Shen, S. R. Gill, J. F. Heidelberg, O. White, E. K. Hickey, J. Peterson, T. Utterback, K. Berry, S. Bass, K. Linher, J. Weidman, H. Khouri, B. Craven, C. Bowman, R. Hudson, M. Gwinn, W. Nelson, R. DeBoy, J. Kolonay, G. McClarty, S. L. Salzberg, J. Eisen, and C. M. Fraser. 2000. Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. Nucleic Acids Res. 28:1397-1406.
21. Read, T. D., G. S. A. Myers, R. C. Brunham, W. C. Nelson, I. T. Paulsen, J. Heidelberg, E. Holtzapple, H. Khouri, N. B. Federova, H. A. Carty, L. A. Umayam, D. H. Haft, J. Peterson, M. J. Beanan, O. White, S. L. Salzberg, R.-C. Hsia, G. McClarty, R. G. Rank, P. M. Bavoil, and C. M. Fraser. 2003. Genome sequence of Chlamydophila caviae (Chlamydia psittaci GPIC): examining the role of niche-specific genes in the evolution of the Chlamydiaceae. Nucleic Acids Res. 31:2134-2147.
22. Rose, J., C. Squires, C. Yanofsky, H. Yang, and G. Zubay. 1973. Regulation of in vitro transcription of the tryptophan operon by purified RNA polymerase in the presence of partially purified repressor and tryptophan. Nat. New Biol. 245:133-137.
23. Rottenberg, M. E., A. Gigliotti-Rothfuchs, and H. Wigzell. 2002. The role of IFN-gamma in the outcome of chlamydial infection. Curr. Opin. Immunol. 14:444-451.
24. Schaumburg, C. S., and M. Tan. 2006. Arginine-dependent gene regulation via the ArgR repressor is species specific in Chlamydia. J. Bacteriol. 188:919-927.
25. Schaumburg, C. S., and M. Tan. 2003. Mutational analysis of the Chlamydia trachomatis dnaK promoter defines the optimal -35 promoter element. Nucleic Acids Res. 31:551-555.
26. Shen, L., Y. Shi, A. L. Douglas, T. P. Hatch, C. M. O'Connell, J. M. Chen, and Y. X. Zhang. 2000. Identification and characterization of promoters regulating tuf expression in Chlamydia trachomatis serovar F. Arch. Biochem. Biophys. 379:46-56.
27. Stephens, R. S., S. Kalman, C. Lamniel, J. Fan, R. Marathe, L. Aravind, W. Mitchell, L. Olinger, R. L. Tatusov, Q. Zhao, E. V. Koonin, and R. W. Davis. 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science 282:754-759.
28. Tan, M., and J. N. Engel. 1996. Identification of sequences necessary for transcription in vitro from the Chlamydia trachomatis rRNA P1 promoter. J. Bacteriol. 178:6975-6982.
29. Tan, M., T. Gaal, R. L. Gourse, and J. N. Engel. 1998. Mutational analysis of the Chlamydia trachomatis rRNA P1 promoter defines four regions important for transcription in vitro. J. Bacteriol. 180:2359-2366.
30. Tan, M., B. Wong, and J. N. Engel. 1996. Transcriptional organization and regulation of the dnaK and groE operons of Chlamydia trachomatis. J. Bacteriol. 178:6983-6990.
31. Taylor, M., and G. Feng. 1991. Relationship between interferon-gamma, indolcamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J. 5:2516-2522.
32. Wilson, A. C., and M. Tan. 2002. Functional analysis of the heat shock regulator HrcA of Chlamydia trachomatis. J. Bacteriol. 184:6566-6571.
33. Wilson, A. C., and M. Tan. 2004. Stress response gene regulation in Chlamydia is dependent on HrcA-CIRCE interactions. J. Bacteriol. 186:3384-3391.
34. Wilson, A. C., C. C. Wu, J. R. Yates III, and M. Tan. 2005. Chlamydial GroEL autoregulates its own expression through direct interactions with the HrcA repressor protein. J. Bacteriol. 187:7535-7542.
35. Wood, H., C. Fehlner-Gardner, J. Berry, E. Fischer, B. Graham, T. Hackstadt, C. Roshick, and G. McClarty. 2003. Regulation of tryptophan synthase gene expression in Chlamydia trachomatis. Mol. Microbiol. 49:1347-1359.
36. Wood, H., C. Roshick, and G. McClarty. 2004. Tryptophan recycling is responsible for the interferon-gamma resistance of Chlamydia psittaci GPIC in indolcamine dioxygenase-expressing host cells. Mol. Microbiol. 52:903-916.
37. Wyllie, S., and J. E. Raulston. 2001. Identifying regulators of transcription in an obligate intracellular pathogen: a metal-dependent repressor in Chlamydia trachomalis. Mol. Microbiol. 40:1027-1036.
38. Xie, G., C. Bonner, T. Brettin, R. Gottardo, N. Keyhani, and R. Jensen. 2003. Lateral gene transfer and ancient paralogy of operons containing redundant copies of tryptophan-pathway genes in Xylella species and in heterocystous cyanobacteria. Genome Biol. 4:R14.
39. Xie, G., C. A. Bonner, and R. A. Jensen. 2002. Dynamic diversity of the tryptophan pathway in chlamydiae: reductive evolution and a novel operon for tryptophan recapture. Genome Biol. 3:R0051.
40. Yang, J., A. Gunasekera, T. A. Lavoie, L. Jin, D. E. Lewis, and J. Carey. 1996. In vivo and in vitro studies of TrpR-DNA interactions. J. Mol. Biol. 258:37-52.
41. 2s RNA polymerase regulates hctB, a late developmental gene in Chlamydia. Mol. Microbiol. 50:577-584.
42. Zhang, R. G., A. Joachimiak, C. L. Lawson, R. W. Schevitz, Z. Otwinowski, and P. B. Sigler. 1987. The crystal structure of trp aporepressor at 1.8 Å shows how binding tryptophan enhances DNA affinity. Nature 327:591-597.
43. Zurawski, G., R. P. Gunsalus, K. D. Brown, and C. Yanofsky. 1981. Structure and regulation of aroH, the structural gene for the tryptophan-repressible 3-deoxy-D-arabino-heptulosonic acid-7-phosphate synthetase of Escherichia coli. J. Mol. Biol. 145:47-73.