Purification, characterization, and gene expression of all sigma factors of RNA polymerase in a cyanobacterium

Journal of Molecular Biology

Volumn 325, Issue 5, 2003, Pages 857-872

  Imamura, Sousuke ^a   Yoshihara, Satoshi ^a   Nakano, Serina ^a   Shiozaki, Noriko ^a   Yamada, Akiko ^a   Tanaka, Kan ^b   Takahashi, Hideo ^b   Asayama, Munehiko ^a   Shirai, Makoto ^a  

^a IBARAKI UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cyanobacteria; Heat shock response; Light responsive expression; RNA polymerase; Sigma factor

Indexed keywords

POLYCLONAL ANTIBODY; PRIMER DNA; PROTEIN; PROTEIN RPOA; PROTEIN RPOC1; PROTEIN RPOC2; PROTEIN SUBUNIT; RNA POLYMERASE; RNA POLYMERASE BETA SUBUNIT; SIGMA FACTOR; SIGMA FACTOR A; SIGMA FACTOR B; SIGMA FACTOR C; SIGMA FACTOR D; SIGMA FACTOR E; SIGMA FACTOR F; SIGMA FACTOR G; SIGMA FACTOR H; SIGMA FACTOR I; UNCLASSIFIED DRUG;

ARTICLE; AUTOREGULATION; BACTERIAL GROWTH; CONTROLLED STUDY; CYANOBACTERIUM; ESCHERICHIA COLI; GENE; GENE EXPRESSION; GENETIC TRANSCRIPTION; GROWTH CURVE; HEAT SHOCK; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; NONHUMAN; PHOTOREACTIVITY; PHOTOSYNTHESIS; PHYLOGENY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; WESTERN BLOTTING;

CYANOBACTERIA; ESCHERICHIA COLI; SIGE; SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 0037474546     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01242-1     Document Type: Article

References (62)

1. Ishihama A. Protein-protein communication within the transcription apparatus. J. Bacteriol. 175:1993;2483-2489.
2. 70 family: sequence conservation and evolutionary relationships. J. Bacteriol. 174:1992;3843-3849.
3. Tanaka K., Shiina T., Takahashi H. Multiple principal sigma factor homologs in eubacteria: identification of the "rpoD"box. Science. 242:1988;1040-1042.
4. Schneider G.J., Tumer N.E., Richaud C., Borbely G., Haselkorn R. Purification and characterization of RNA polymerase from the cyanobacterium Anabaena 7120. J. Biol. Chem. 262:1987;14633-14639.
5. Campbell E.L., Brahamsha B., Meeks J.C. Mutation of an alternative sigma factor in the cyanobacterium Nostoc punctiforme results in increased infection of its symbiotic plant partner, Anthoceros punctatus. J. Bacteriol. 180:1998;4938-4941.
6. Tanaka K., Masuda S., Takahashi H. The complete nucleotide sequence of the gene (rpoD1) encoding the principal sigma factor of the RNA polymerase from the cyanobacterium Synechococcus sp. strain PCC7942. Biochim. Biophys. Acta. 1132:1992;94-96.
7. Tsinoreman N.F., Ishiura M., Kondo T., Andersson C.R., Tanaka K., Takahashi H., et al. A sigma factor that modifies the circadian expression of a subset of genes in cyanobacteria. EMBO J. 15:1996;2488-2495.
8. Sugimoto Y., Tanaka K., Masuda S., Takahashi H. The rpoD1 gene of Synechococcus sp. strain PCC 7942 encodes the principal sigma factor of RNA polymerase. J. Genet. Appl. Microbiol. 43:1997;17-21.
9. Caslake L.F., Bryant D.A. The sigA gene encoding the major sigma factor of RNA polymerase from the marine cyanobacterium Synechococcus sp. strain PCC 7002: cloning and characterization. Microbiology. 142:1996;347-357.
10. Gruber T.M., Bryant D.A. Characterization of the alternative sigma-factors SigD and SigE in Synechococcus sp. strain PCC 7002. SigE is implicated in transcription of post-exponential-phase-specific genes. Arch. Microbiol. 169:1998;211-219.
11. Asayama M., Suzuki H., Sato A., Aida T., Tanaka K., Takahashi H., Shirai M. The rpoD1 gene product is a principal sigma factor of RNA polymerase in Microcystis aeruginosa K-81. J. Biochem. 120:1996;752-758.
12. Asayama M., Suzuki A., Nozawa S., Yamada A., Tanaka K., Takahashi H., et al. A new sigma factor homolog in a cyanobacterium: cloning, sequencing, and light-responsive transcripts of rpoD2 from Microcystis aeruginosa K-81. Biochim. Biophys. Acta. 1351:1997;31-36.
13. Brahamsha B., Haselkorn R. Isolation and characterization of the gene encoding the principal sigma factor of the vegetative cell RNA polymerase from the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 173:1991;2442-2450.
14. Brahamsha B., Haselkorn R. Identification of multiple RNA polymerase sigma factor homologs in the cyanobacterium Anabaena sp. strain PCC 7120: cloning, expression, and inactivation of the sigB and sigC genes. J. Bacteriol. 174:1992;7273-7282.
15. Kaneko T., Nakamura Y., Wolk C.P., Kuritz T., Sasamoto S., et al. Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8:2001;205-213.
16. Kaneko T., Sato S., Kotani H., Tanaka A., Asamizu E., Nakamura Y., et al. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3:1996;109-136.
17. Caslake L.F., Gruber T.M., Bryant D.A. Expression of two alternative sigma factors of Synechococcus sp. strain PCC 7002 is modulated by carbon and nitrogen stress. Microbiology. 143:1997;3807-3818.
18. Goto-Seki A., Shirokane M., Masuda S., Tanaka K., Takahashi H. Specificity crosstalk among group 1 and group 2 sigma factors in the cyanobacterium Synechococcus sp. PCC7942: in vitro specificity and a phylogenetic analysis. Mol. Microbiol. 34:1999;473-484.
19. Bhaya D., Watanabe N., Ogawa T., Grossman A.R. The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC6803. Proc. Natl Acad. Sci. USA. 96:1999;3188-3193.
20. Haldenwang W.G. The sigma factors of Bacillus subtilis. Microbiol. Rev. 59:1995;1-30.
21. Huckauf J., Nomura C., Forchhammer K., Hagemann M. Stress responses of Synechocystis sp. strain PCC 6803 mutants impaired in genes encoding putative alternative sigma factors. Microbiology. 146:2000;2877-2889.
22. Khudyakov I.Y., Golden J.W. Identification and inactivation of three group 2 sigma factor genes in Anabaena sp. strain PCC 7120. J. Bacteriol. 183:2001;6667-6675.
23. Shibato J., Asayama M., Shirai M. Specific recognition of the cyanobacterial psbA promoter by RNA polymerases containing principal sigma factors. Biochim. Biophys. Acta. 8:1998;296-303.
24. Shibato J., Agrawal G.K., Kato H., Asayama M., Shirai M. The 5′-upstream cis-sequences of cyanobacterial psbA: analysis of their roles in basal, light-dependent and circadian rhythmic transcription. Mol. Genet. Genomics. 267:2002;684-694.
25. 32. Nature. 329:1987;348-351.
26. Jishage M., Iwata A., Ueda S., Ishihama A. Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli: intracellular levels of four species of sigma subunit under various growth conditions. J. Bacteriol. 178:1996;5447-5451.
27. Lee S., Prochaska D.J., Fang F., Barnum S.R. A 16.6-kilodalton protein in the Cyanobacterium Synechocystis sp. PCC 6803 plays a role in the heat shock response. Curr. Microbiol. 37:1998;403-407.
28. Burgess R.R., Jendrisak J.J. A procedure for the rapid, large-scale purification of Escherichia coli DNA-dependent RNA polymerase involving Polymin P precipitation and DNA-cellulose chromatography. Biochemistry. 14:1975;4634-4638.
29. Davison B.L., Leighton T., Rabinowitz J.C. Purification of Bacillus subtilis RNA polymerase with heparin-agarose. In vitro transcription of phi 29 DNA. J. Biol. Chem. 254:1979;9220-9226.
30. 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli. Proc. Natl Acad. Sci. USA. 90:1993;3511-3515.
31. S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev. 8:1994;1600-1612.
32. Becker G., Klauck E., Hengge-Aronis R. Regulation of RpoS proteolysis in Escherichia coli: the response regulator RssB is a recognition factor that interacts with the turnover element in RpoS. Proc. Natl Acad. Sci. USA. 96:1999;6439-6444.
33. S factor. Mol. Microbiol. 35:2000;657-666.
34. Muro-Pastor A.M., Herrero A., Flores E. Nitrogen-regulated group 2 sigma factor from Synechocystis sp. strain PCC 6803 involved in survival under nitrogen stress. J. Bacteriol. 183:2001;1090-1095.
35. 32 in Escherichia coli: structural and functional dissection of rpoH mRNA secondary structure. J. Bacteriol. 181:1999;401-410.
36. Chen X., Widger W.R. Physical genome map of the unicellular cyanobacterium Synechococcus sp. strain PCC 7002. J. Bacteriol. 175:1993;5106-5116.
37. Agrawal G.K., Kato H., Asayama M., Shirai M. An AU-box motif upstream of the SD sequence of light-dependent psbA transcripts confers mRNA instability in darkness in cyanobacteria. Nucl. Acids Res. 29:2001;1835-1843.
38. Nair U., Thomas C., Golden S.S. Functional elements of the strong psbAI promoter of Synechococcus elongatus PCC 7942. J. Bacteriol. 183:2001;1740-1747.
39. Hager D.A., Burgess R.R. Elution of proteins from sodium dodecyl sulfate-polyacrylamide gels, removal of sodium dodecyl sulfate, and renaturation of enzymatic activity: results with sigma subunit of Escherichia coli RNA polymerase, wheat germ DNA topoisomerase, and other enzymes. Anal. Biochem. 190:1980;76-86.
40. Mishra R.K., Chatterji D. Mechanism of initiation of transcription by Escherichia coli RNA polymerase on supercoiled template. Mol. Microbiol. 8:1993;507-515.
41. 38 holoenzymes. J. Biol. Chem. 271:1996;1998-2004.
42. Sippola K., Aro E.M. Thiol redox state regulates expression of psbA genes in Synechococcus sp. PCC 7942. Plant Mol. Biol. 41:1999;425-433.
43. 6/f complex. Plant Physiol. 122:2000;505-516.
44. El Bissati K., Kirilovsky D. Regulation of psbA and psaE expression by light quality in Synechocystis species PCC 6803. A redox control mechanism. Plant Physiol. 125:2001;1988-2000.
45. Hecker M., Schumann W., Volker U. Heat-shock and general stress response in Bacillus subtilis. Mol. Microbiol. 19:1996;417-428.
46. Derre I., Rapoport G., Msadek T. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria. Mol. Microbiol. 31:1999;117-131.
47. A-like promoter and the roles of the inverted repeat sequence (CIRCE). J. Bacteriol. 177:1995;5427-5433.
48. Zuber U., Schumann W. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J. Bacteriol. 176:1994;1359-1363.
49. Schulz A., Schumann W. hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J. Bacteriol. 178:1996;1088-1093.
50. Webb R., Reddy K.J., Sherman L.A. Regulation and sequence of the Synechococcus sp. strain PCC 7942 groESL operon, encoding a cyanobacterial chaperonin. J. Bacteriol. 172:1990;5079-5088.
51. Lehel C., Los D., Wada H., Gyorgyei J., Horvath I., Kovacs E., et al. A second groEL-like gene, organized in a groESL operon is present in the genome of Synechocystis sp. PCC 6803. J. Biol. Chem. 268:1993;1799-1804.
52. Rippka R. Isolation and purification of cyanobacteria. Methods Enzymol. 167:1988;3-27.
53. Ish-Horowicz D., Burke J.F. Rapid and efficient cosmid cloning. Nucl. Acids Res. 9:1981;2989-2998.
54. Asayama M., Tanaka K., Takahashi H., Sato A., Aida T., Shirai M. Cloning, sequencing and characterization of the gene encoding a principal sigma factor homolog from the cyanobacterium Microcystis aeruginosa K-81. Gene. 181:1996;213-217.
55. Asayama M., Hayasaka Y., Kabasawa M., Shirai M., Ohyama T. An intrinsic DNA curvature found in the cyanobacterium Microcystis aeruginosa K-81 affects the promoter activity of rpoD1 encoding a principal sigma factor. J. Biochem. 125:1999;460-468.
56. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16:1980;111-120.
57. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:1994;4673-4680.
58. Guerout-Fleury A.M., Shazand K., Frandsen N., Stragier P. Antibiotic-resistance cassettes for Bacillus subtilis. Gene. 167:1995;335-336.
59. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 153:1987;3-11.
60. Wösten M.M.S.M. Eubacterial sigma-factors. FEMS Microbiol. 22:1998;127-150.
61. García-Domínguez M., Florencio F.J. Nitrogen availability and electron transport control the expression of glnB gene (encoding PII protein) in the cyanobacterium Synechocystis sp. PCC 6803. Plant Mol. Biol. 35:1997;723-734.
62. Amann E., Brosius J., Ptashne M. Vectors bearing a hybrid trp-lac promoter useful for regulated expression of cloned genes in Escherichia coli. Gene. 25:1983;167-178.