Streptomyces telomeres contain a promoter

Yuh-Ru Lin, Mi-Young Hahn, Jung-Hye Roe, Tzu-Wen Huang, H.-H. Tsai, Y.-F. Lin, T.-S. Su, Y.-J. Chan, C.W. Chen

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Bidirectional replication of the linear chromosomes and plasmids of Streptomyces spp. results in single-strand overhangs at their 3′ ends, which contain extensive complex palindromic sequences. The overhangs are believed to be patched by DNA synthesis primed by a terminal protein that remains covalently bound to the 5′ ends of the telomeres. We discovered that in vitro a conserved 167-bp telomere DNA binds strongly to RNA polymerase holoenzyme and exhibits promoter activities stronger than those of an rRNA operon. In vivo, the telomere DNA exhibited promoter activity in both orientations on a circular plasmid in Streptomyces. The telomere promoter is also active on a linear plasmid during exponential growth. Such promoter activity in a telomere has not hitherto been observed in eukaryotic or prokaryotic replicons. Streptomyces telomere promoters may be involved in priming the terminal Okazaki fragment (during replication) replicative transfer (during conjugation), or expression of downstream genes (including a conserved ttrA helicase-like gene involved in conjugal transfer). Interestingly, the Streptomyces telomeres also function as a promoter in Escherichia coli and as a transcription enhancer in yeast. Copyright © 2009, American Society for Microbiology. All Right Reserved.
Original languageEnglish
Pages (from-to)773-781
Number of pages9
JournalJournal of Bacteriology
Volume191
Issue number3
DOIs
Publication statusPublished - 2009
Externally publishedYes

Fingerprint

Telomere
Streptomyces
Plasmids
DNA
rRNA Operon
Replicon
Holoenzymes
DNA-Directed RNA Polymerases
Microbiology
Chromosomes
Yeasts
Escherichia coli
Gene Expression
Growth
Genes
Proteins

Keywords

  • DNA
  • helicase
  • holoenzyme
  • Okazaki fragment
  • ribosome RNA
  • RNA polymerase
  • DNA directed RNA polymerase
  • article
  • bacterium conjugation
  • controlled study
  • DNA binding
  • downstream processing
  • enhancer region
  • Escherichia coli
  • eukaryote
  • gene activity
  • gene expression
  • genetic transcription
  • growth
  • in vitro study
  • in vivo study
  • nonhuman
  • operon
  • plasmid
  • priority journal
  • prokaryote
  • promoter region
  • replicon
  • Streptomyces
  • telomere
  • yeast
  • biological model
  • cell line
  • gel mobility shift assay
  • genetics
  • human
  • metabolism
  • polymerase chain reaction
  • protein binding
  • Eukaryota
  • Prokaryota
  • Cell Line
  • DNA-Directed RNA Polymerases
  • Electrophoretic Mobility Shift Assay
  • Humans
  • Models, Genetic
  • Polymerase Chain Reaction
  • Promoter Regions, Genetic
  • Protein Binding
  • Telomere

Cite this

Lin, YR., Hahn, M-Y., Roe, J-H., Huang, T-W., Tsai, H-H., Lin, Y-F., ... Chen, C. W. (2009). Streptomyces telomeres contain a promoter. Journal of Bacteriology, 191(3), 773-781. https://doi.org/10.1128/JB.01299-08

Streptomyces telomeres contain a promoter. / Lin, Yuh-Ru; Hahn, Mi-Young; Roe, Jung-Hye; Huang, Tzu-Wen; Tsai, H.-H.; Lin, Y.-F.; Su, T.-S.; Chan, Y.-J.; Chen, C.W.

In: Journal of Bacteriology, Vol. 191, No. 3, 2009, p. 773-781.

Research output: Contribution to journalArticle

Lin, YR, Hahn, M-Y, Roe, J-H, Huang, T-W, Tsai, H-H, Lin, Y-F, Su, T-S, Chan, Y-J & Chen, CW 2009, 'Streptomyces telomeres contain a promoter', Journal of Bacteriology, vol. 191, no. 3, pp. 773-781. https://doi.org/10.1128/JB.01299-08
Lin YR, Hahn M-Y, Roe J-H, Huang T-W, Tsai H-H, Lin Y-F et al. Streptomyces telomeres contain a promoter. Journal of Bacteriology. 2009;191(3):773-781. https://doi.org/10.1128/JB.01299-08
Lin, Yuh-Ru ; Hahn, Mi-Young ; Roe, Jung-Hye ; Huang, Tzu-Wen ; Tsai, H.-H. ; Lin, Y.-F. ; Su, T.-S. ; Chan, Y.-J. ; Chen, C.W. / Streptomyces telomeres contain a promoter. In: Journal of Bacteriology. 2009 ; Vol. 191, No. 3. pp. 773-781.
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title = "Streptomyces telomeres contain a promoter",
abstract = "Bidirectional replication of the linear chromosomes and plasmids of Streptomyces spp. results in single-strand overhangs at their 3′ ends, which contain extensive complex palindromic sequences. The overhangs are believed to be patched by DNA synthesis primed by a terminal protein that remains covalently bound to the 5′ ends of the telomeres. We discovered that in vitro a conserved 167-bp telomere DNA binds strongly to RNA polymerase holoenzyme and exhibits promoter activities stronger than those of an rRNA operon. In vivo, the telomere DNA exhibited promoter activity in both orientations on a circular plasmid in Streptomyces. The telomere promoter is also active on a linear plasmid during exponential growth. Such promoter activity in a telomere has not hitherto been observed in eukaryotic or prokaryotic replicons. Streptomyces telomere promoters may be involved in priming the terminal Okazaki fragment (during replication) replicative transfer (during conjugation), or expression of downstream genes (including a conserved ttrA helicase-like gene involved in conjugal transfer). Interestingly, the Streptomyces telomeres also function as a promoter in Escherichia coli and as a transcription enhancer in yeast. Copyright {\circledC} 2009, American Society for Microbiology. All Right Reserved.",
keywords = "DNA, helicase, holoenzyme, Okazaki fragment, ribosome RNA, RNA polymerase, DNA directed RNA polymerase, article, bacterium conjugation, controlled study, DNA binding, downstream processing, enhancer region, Escherichia coli, eukaryote, gene activity, gene expression, genetic transcription, growth, in vitro study, in vivo study, nonhuman, operon, plasmid, priority journal, prokaryote, promoter region, replicon, Streptomyces, telomere, yeast, biological model, cell line, gel mobility shift assay, genetics, human, metabolism, polymerase chain reaction, protein binding, Eukaryota, Prokaryota, Cell Line, DNA-Directed RNA Polymerases, Electrophoretic Mobility Shift Assay, Humans, Models, Genetic, Polymerase Chain Reaction, Promoter Regions, Genetic, Protein Binding, Telomere",
author = "Yuh-Ru Lin and Mi-Young Hahn and Jung-Hye Roe and Tzu-Wen Huang and H.-H. Tsai and Y.-F. Lin and T.-S. Su and Y.-J. Chan and C.W. Chen",
note = "被引用次數:3 Export Date: 6 April 2016 CODEN: JOBAA 通訊地址: Chen, C. W.; Department of Life Sciences, Institute of Genome Sciences, National Yang-Ming University, Shih-Pai, Taipei 112, Taiwan; 電子郵件: cwchen@ym.edu.tw 化學物質/CAS: DNA, 9007-49-2; RNA polymerase, 9014-24-8; helicase, 42613-29-6; DNA-Directed RNA Polymerases, EC 2.7.7.6 參考文獻: Ali, N., Herron, P.R., Evans, M.C., Dyson, P.J., Osmotic regulation of the Streptomyces lividans thiostrepton-inducible promoter, ptipA (2002) Microbiology, 148, pp. 381-390; Bao, K., Cohen, S.N., Recruitment of terminal protein to the ends of Streptomyces linear plasmids and chromosomes by a novel telomere-binding protein essential for linear DNA replication (2003) Genes Dev, 17, pp. 774-785; Bao, K., Cohen, S.N., Reverse transcriptase activity innate to DNA polymerase I and DNA topoisomerase I proteins of Streptomyces telomere complex (2004) Proc. Natl. Acad. Sci. USA, 101, pp. 14361-14366; Bao, K., Cohen, S.N., Terminal proteins essential for the replication of linear plasmids and chromosomes in Streptomyces (2001) Genes Dev, 15, pp. 1518-1527; Bates, S., Roscoe, R.A., Althorpe, N.J., Brammar, W.J., Wilkins, B.M., Expression of leading region genes on IncI1 plasmid Collb-P9: Genetic evidence for single-stranded DNA transcription (1999) Microbiology, 145, pp. 2655-2662; Baylis, H.A., Bibb, M.J., Transcriptional analysis of the 16S rRNA gene of the rrnD gene set of Streptomyces coelicolor A3(2) (1988) Mol. Microbiol, 2, pp. 569-579; Bentley, S.D., Brown, S., Murphy, L.D., Harris, D.E., Quail, M.A., Parkhill, J., Barrell, B.G., Chater, K.F., SCP1, a 356,023 base pair linear plasmid adapted to the ecology and developmental biology of its host, Streptomyces coelicolor A3(2) (2004) Mol. Microbiol, 51, pp. 1615-1628; Bentley, S. D., K. F. Chater, A.-M. Cerde{\~n}o-T{\'a}rraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147Bey, S.J., Tsou, M.F., Huang, C.H., Yang, C.C., Chen, C.W., The homologous terminal sequence of the Streptomyces lividans chromosome and SLP2 plasmid (2000) Microbiology, 146, pp. 911-922; Boshart, M., Kluppel, M., Schmidt, A., Schutz, G., Luckow, B., Reporter constructs with low background activity utilizing the cat gene (1992) Gene, 110, pp. 129-130; Butler, J.E., Kadonaga, J.T., The RNA polymerase II core promoter: A key component in the regulation of gene expression (2002) Genes Dev, 16, pp. 2583-2592; Buttner, M.J., Chater, K.F., Bibb, M.J., Cloning, disruption, and transcriptional analysis of three RNA polymerase sigma factor genes of Streptomyces coelicolor A3(2) (1990) J. Bacteriol, 172, pp. 3367-3378; Buttner, M.J., Lewis, C.G., Construction and characterization of Streptomyces coelicolor A3(2) mutants that are multiply deficient in the nonessential hrd-encoded RNA polymerase sigma factors (1992) J. Bacteriol, 174, pp. 5165-5167; Buttner, M.J., Smith, A.M., Bibb, M.J., At least three different RNA polymerase holoenzymes direct transcription of the agarase gene (dagA) of Streptomyces coelicolor A3(2) (1988) Cell, 52, pp. 599-607; Chaconas, G., Chen, C.W., Linear chromosomes in bacteria: No longer going around in circles (2005) The bacterial chromosome, pp. 525-539. , N. P. Higgins ed, American Society for Microbiology. Washington, DC; Chang, P.C., Cohen, S.N., Bidirectional replication from an internal origin in a linear Streptomyces plasmid (1994) Science, 265, pp. 952-954; Chen, C.W., Complications and implications of linear bacterial chromosomes (1996) Trends Genet, 12, pp. 192-196; Chou, S.-H., Zhu, L., Reid, B.R., Sheared purine-purine pairing in biology (1997) J. Mol. Biol, 267, pp. 1055-1067; Dai, X., Greizerstein, M.B., Nadas-Chinni, K., Rothman-Denes, L.B., Supercoil-induced extrusion of a regulatory DNA hairpin (1997) Proc. Natl. Acad. Sci. USA, 94, pp. 2174-2179; Fujita, N., Nomura, T., Ishihama, A., Promoter selectivity of Escherichia coli RNA polymerase. Purification and properties of holoenzyme containing the heat-shock sigma subunit (1987) J. Biol. Chem, 262, pp. 1855-1859; Glucksmann, M.A., Malone, C., Markiewicz, P., Rothman-Denes, L.B., Specific sequences and a hairpin structure in the template strand are required for N4 virion RNA polymerase promoter recognition (1992) Cell, 70, pp. 491-500; Glucksmann-Kuis, M. A., X. Dai, P. Markiewicz, and L. B. Rothman-Denes. 1996. E. coli SSB activates N4 virion RNA polymerase promoters by stabilizing a DNA hairpin required for promoter recognition. Cell 84:147-154Goshi, K., Uchida, T., Lezhava, A., Yamasaki, M., Hiratsu, K., Shinkawa, H., Kinashi, H., Cloning and analysis of the telomere and terminal inverted repeat of the linear chromosome of Streptomyces griseus (2002) J. Bacteriol, 184, pp. 3411-3415; Hawley, D., McClure, W., Compilation and analysis of Escherichia coli promoter DNA sequences (1983) Nucleic Acids Res, 11, pp. 2237-2255; Hirao, I., Kawai, G., Oshizawa, S., Nishimura, Y., Ishido, Y., Watanabe, K., Miura, K.-I., Most compact hairpin-turn structure exerted by a short DNA fragment, d(GCGAAGC), in solution: An extraordinarily stable structure resistant to nucleases and heat (1994) Nucleic Acids Res, 22, pp. 576-582; Hopwood, D.A., Kieser, T., Wright, H.M., Bibb, M.J., Plasmids, recombination, and chromosomal mapping in Streptomyces Hvidans 66 (1983) J. Gen. Microbiol, 129, pp. 2257-2269; Huang, C.-H., Lin, Y.-S., Yang, Y.-L., Huang, S.-W., Chen, C.W., The telomeres of Streptomyces chromosomes contain conserved palindromic sequences with potential to form complex secondary structures (1998) Mol. Microbiol, 28, pp. 905-926; Huang, C.-H., Chen, C.-Y., Tsai, H.H., Chen, C., Lin, Y.-S., Chen, C.W., Linear plasmid SLP2 of Streptomyces lividans is a composite replicon (2003) Mol. Microbiol, 47, pp. 1563-1576; Ikeda, H., Ishikawa, J., Hanamoto, A., Shinose, M., Kikuchi, H., Shiba, T., Sakaki, Y., Omura, S., Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermiti-lis (2003) Nat. Biotechnol, 21, pp. 526-531; Kang, J.G., Hahn, M.Y., Ishihama, A., Roe, J.H., Identification of sigma factors for growth phase-related promoter selectivity of RNA polymerases from Streptomyces coelicolor A3(2) (1997) Nucleic Acids Res, 25, pp. 2566-2573; Kieser, T., Bibb, M., Buttner, M.J., Chater, K.F., Hopwood, D.A., (2000) Practical Streptomyces genetics, , The John Innes Foundation, Norwich, United Kingdom; Kinashi, H., Shimaji-Murayama, M., Hanafusa, T., Nucleotide sequence analysis of the unusually long terminal inverted repeats of a giant linear plasmid, SCP1 (1991) Plasmid, 26, pp. 123-130; Lin, Y.-S., Kieser, H.M., Hopwood, D.A., Chen, C.W., The chromosomal DNA of Streptomyces lividans 66 is linear (1993) Mol. Microbiol, 10, pp. 923-933; Lisser, S., Margalit, H., Compilation of E. coli mRNA promoter sequences (1993) Nucleic Acids Res, 21, pp. 1507-1516; Masai, H., Arai, K., Frpo: A novel single-stranded DNA promoter for transcription and for primer RNA synthesis of DNA replication (1997) Cell, 89, pp. 897-907; Nakabayashi, H., Taketa, K., Miyano, K., Yamane, T., Sato, J., Growth of human hepatoma cells lines with differentiated functions in chemically defined medium (1982) Cancer Res, 42, pp. 3858-3863; Qin, Z., Cohen, S.N., Survival mechanisms for Streptomyces linear replicons after telomere damage (2002) Mol. Microbiol, 45, pp. 785-794; Sakaguchi, K., Invertrons, a class of structurally and functionally related genetic elements that include linear plasmids. transposable elements, and genomes of adeno-type viruses (1990) Microbiol. Rev, 54, pp. 66-74; Salas, M., Protein-primed DNA replication (1991) Annu. Rev. Biochem, 60, pp. 37-91; Sambrook, J., Fritsch, E.F., Maniatis, T., (1989) Molecular cloning: A laboratory manual, , 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor. NY; Sambrook, J., Russell, D.W., (2001) Molecular cloning: A laboratory manual, , 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY; Smale, S.T., Core promoters: Active contributors to combinatorial gene regulation (2001) Genes Dev, 15, pp. 2503-2508; Ward, J.M., Janssen, G.R., Kieser, T., Bibb, M.J., Buttner, M.J., Bibb, M.J., Construction and characterization of a series of multi-copy promoter-probe plasmid vectors for Streptomyces using the aminoglycoside phosphotransferase gene from Tn5 as indicator (1986) Mol. Gen. Genet, 203, pp. 468-478; Weaver, D., Karoonuthaisiri, N., Tsai, H.H., Huang, C.H., Ho, M.L., Gai, S., Patel, K.G., Kao, C.M., Genome plasticity in Streptomyces: Identification of 1 Mb TIRs in the S. coelicolor A3(2) chromosome (2004) Mol. Microbiol, 51, pp. 1530-1550; Yang, C.-C., Huang, C.-H., Li, C.-Y., Tsay, Y.-G., Lee, S.-C., Chen, C.W., The terminal proteins of linear Streptomyces chromosomes and plasmids: A novel class of replication priming proteins (2002) Mol. Microbiol, 43, pp. 297-305; Yang, C.-C., Chen, Y.-H., Tsai, H.-H., Huang, C.-H., Huang, T.-W., Chen, C.W., In vitro deoxynucleotidylation of the terminal protein of Streptomyces linear chromosomes (2006) Appl. Environ. Microbiol, 72, pp. 7959-7961; Zhang, R., Yang, Y., Fang, P., Jiang, C., Xu, L., Zhu, Y., Shen, M., Qin, Z., Diversity of telomere palindromic sequences and replication genes among Streptomyces linear plasmids (2006) Appl. Environ. Microbiol, 72, pp. 5728-5733; Zhou, X., Deng, Z., Firmin, J.L., Hopwood, D.A., Kieser, T., Site-specific degradation of Streptomyces lividans DNA during electrophoresis in buffers contaminated with ferrous iron (1988) Nucleic Acids Res, 16, pp. 4341-4354",
year = "2009",
doi = "10.1128/JB.01299-08",
language = "English",
volume = "191",
pages = "773--781",
journal = "Journal of Bacteriology",
issn = "0021-9193",
publisher = "American Society for Microbiology",
number = "3",

}

TY - JOUR

T1 - Streptomyces telomeres contain a promoter

AU - Lin, Yuh-Ru

AU - Hahn, Mi-Young

AU - Roe, Jung-Hye

AU - Huang, Tzu-Wen

AU - Tsai, H.-H.

AU - Lin, Y.-F.

AU - Su, T.-S.

AU - Chan, Y.-J.

AU - Chen, C.W.

N1 - 被引用次數:3 Export Date: 6 April 2016 CODEN: JOBAA 通訊地址: Chen, C. W.; Department of Life Sciences, Institute of Genome Sciences, National Yang-Ming University, Shih-Pai, Taipei 112, Taiwan; 電子郵件: cwchen@ym.edu.tw 化學物質/CAS: DNA, 9007-49-2; RNA polymerase, 9014-24-8; helicase, 42613-29-6; DNA-Directed RNA Polymerases, EC 2.7.7.6 參考文獻: Ali, N., Herron, P.R., Evans, M.C., Dyson, P.J., Osmotic regulation of the Streptomyces lividans thiostrepton-inducible promoter, ptipA (2002) Microbiology, 148, pp. 381-390; Bao, K., Cohen, S.N., Recruitment of terminal protein to the ends of Streptomyces linear plasmids and chromosomes by a novel telomere-binding protein essential for linear DNA replication (2003) Genes Dev, 17, pp. 774-785; Bao, K., Cohen, S.N., Reverse transcriptase activity innate to DNA polymerase I and DNA topoisomerase I proteins of Streptomyces telomere complex (2004) Proc. Natl. Acad. Sci. USA, 101, pp. 14361-14366; Bao, K., Cohen, S.N., Terminal proteins essential for the replication of linear plasmids and chromosomes in Streptomyces (2001) Genes Dev, 15, pp. 1518-1527; Bates, S., Roscoe, R.A., Althorpe, N.J., Brammar, W.J., Wilkins, B.M., Expression of leading region genes on IncI1 plasmid Collb-P9: Genetic evidence for single-stranded DNA transcription (1999) Microbiology, 145, pp. 2655-2662; Baylis, H.A., Bibb, M.J., Transcriptional analysis of the 16S rRNA gene of the rrnD gene set of Streptomyces coelicolor A3(2) (1988) Mol. Microbiol, 2, pp. 569-579; Bentley, S.D., Brown, S., Murphy, L.D., Harris, D.E., Quail, M.A., Parkhill, J., Barrell, B.G., Chater, K.F., SCP1, a 356,023 base pair linear plasmid adapted to the ecology and developmental biology of its host, Streptomyces coelicolor A3(2) (2004) Mol. Microbiol, 51, pp. 1615-1628; Bentley, S. D., K. F. Chater, A.-M. Cerdeño-Tárraga, G. L. Challis, N. R. Thomson, K. D. James, D. E. Harris, M. A. Quail, H. Kieser, D. Harper, A. Bateman, S. Brown, G. Chandra, C. W. Chen, M. Collins, A. Cronin, A. Fraser, A. Goble, J. Hidalgo, T. Hornsby, S. Howarth, C. H. Huang, T. Kieser, L. Larke, L. Murphy, K. Oliver, S. O'Neil, E. Rabbinowitsch, M. A. Rajandream, K. Rutherford, S. Rutter, K. Seeger, D. Saunders, S. Sharp, R. Squares, S. Squares, K. Taylor, T. Warren, A. Wietzorrek, J. Woodward, B. G. Barrell, J. Parkhill, and D. A. Hopwood. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141-147Bey, S.J., Tsou, M.F., Huang, C.H., Yang, C.C., Chen, C.W., The homologous terminal sequence of the Streptomyces lividans chromosome and SLP2 plasmid (2000) Microbiology, 146, pp. 911-922; Boshart, M., Kluppel, M., Schmidt, A., Schutz, G., Luckow, B., Reporter constructs with low background activity utilizing the cat gene (1992) Gene, 110, pp. 129-130; Butler, J.E., Kadonaga, J.T., The RNA polymerase II core promoter: A key component in the regulation of gene expression (2002) Genes Dev, 16, pp. 2583-2592; Buttner, M.J., Chater, K.F., Bibb, M.J., Cloning, disruption, and transcriptional analysis of three RNA polymerase sigma factor genes of Streptomyces coelicolor A3(2) (1990) J. Bacteriol, 172, pp. 3367-3378; Buttner, M.J., Lewis, C.G., Construction and characterization of Streptomyces coelicolor A3(2) mutants that are multiply deficient in the nonessential hrd-encoded RNA polymerase sigma factors (1992) J. Bacteriol, 174, pp. 5165-5167; Buttner, M.J., Smith, A.M., Bibb, M.J., At least three different RNA polymerase holoenzymes direct transcription of the agarase gene (dagA) of Streptomyces coelicolor A3(2) (1988) Cell, 52, pp. 599-607; Chaconas, G., Chen, C.W., Linear chromosomes in bacteria: No longer going around in circles (2005) The bacterial chromosome, pp. 525-539. , N. P. Higgins ed, American Society for Microbiology. Washington, DC; Chang, P.C., Cohen, S.N., Bidirectional replication from an internal origin in a linear Streptomyces plasmid (1994) Science, 265, pp. 952-954; Chen, C.W., Complications and implications of linear bacterial chromosomes (1996) Trends Genet, 12, pp. 192-196; Chou, S.-H., Zhu, L., Reid, B.R., Sheared purine-purine pairing in biology (1997) J. Mol. Biol, 267, pp. 1055-1067; Dai, X., Greizerstein, M.B., Nadas-Chinni, K., Rothman-Denes, L.B., Supercoil-induced extrusion of a regulatory DNA hairpin (1997) Proc. Natl. Acad. Sci. USA, 94, pp. 2174-2179; Fujita, N., Nomura, T., Ishihama, A., Promoter selectivity of Escherichia coli RNA polymerase. Purification and properties of holoenzyme containing the heat-shock sigma subunit (1987) J. Biol. Chem, 262, pp. 1855-1859; Glucksmann, M.A., Malone, C., Markiewicz, P., Rothman-Denes, L.B., Specific sequences and a hairpin structure in the template strand are required for N4 virion RNA polymerase promoter recognition (1992) Cell, 70, pp. 491-500; Glucksmann-Kuis, M. A., X. Dai, P. Markiewicz, and L. B. Rothman-Denes. 1996. E. coli SSB activates N4 virion RNA polymerase promoters by stabilizing a DNA hairpin required for promoter recognition. Cell 84:147-154Goshi, K., Uchida, T., Lezhava, A., Yamasaki, M., Hiratsu, K., Shinkawa, H., Kinashi, H., Cloning and analysis of the telomere and terminal inverted repeat of the linear chromosome of Streptomyces griseus (2002) J. Bacteriol, 184, pp. 3411-3415; Hawley, D., McClure, W., Compilation and analysis of Escherichia coli promoter DNA sequences (1983) Nucleic Acids Res, 11, pp. 2237-2255; Hirao, I., Kawai, G., Oshizawa, S., Nishimura, Y., Ishido, Y., Watanabe, K., Miura, K.-I., Most compact hairpin-turn structure exerted by a short DNA fragment, d(GCGAAGC), in solution: An extraordinarily stable structure resistant to nucleases and heat (1994) Nucleic Acids Res, 22, pp. 576-582; Hopwood, D.A., Kieser, T., Wright, H.M., Bibb, M.J., Plasmids, recombination, and chromosomal mapping in Streptomyces Hvidans 66 (1983) J. Gen. Microbiol, 129, pp. 2257-2269; Huang, C.-H., Lin, Y.-S., Yang, Y.-L., Huang, S.-W., Chen, C.W., The telomeres of Streptomyces chromosomes contain conserved palindromic sequences with potential to form complex secondary structures (1998) Mol. Microbiol, 28, pp. 905-926; Huang, C.-H., Chen, C.-Y., Tsai, H.H., Chen, C., Lin, Y.-S., Chen, C.W., Linear plasmid SLP2 of Streptomyces lividans is a composite replicon (2003) Mol. Microbiol, 47, pp. 1563-1576; Ikeda, H., Ishikawa, J., Hanamoto, A., Shinose, M., Kikuchi, H., Shiba, T., Sakaki, Y., Omura, S., Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermiti-lis (2003) Nat. Biotechnol, 21, pp. 526-531; Kang, J.G., Hahn, M.Y., Ishihama, A., Roe, J.H., Identification of sigma factors for growth phase-related promoter selectivity of RNA polymerases from Streptomyces coelicolor A3(2) (1997) Nucleic Acids Res, 25, pp. 2566-2573; Kieser, T., Bibb, M., Buttner, M.J., Chater, K.F., Hopwood, D.A., (2000) Practical Streptomyces genetics, , The John Innes Foundation, Norwich, United Kingdom; Kinashi, H., Shimaji-Murayama, M., Hanafusa, T., Nucleotide sequence analysis of the unusually long terminal inverted repeats of a giant linear plasmid, SCP1 (1991) Plasmid, 26, pp. 123-130; Lin, Y.-S., Kieser, H.M., Hopwood, D.A., Chen, C.W., The chromosomal DNA of Streptomyces lividans 66 is linear (1993) Mol. Microbiol, 10, pp. 923-933; Lisser, S., Margalit, H., Compilation of E. coli mRNA promoter sequences (1993) Nucleic Acids Res, 21, pp. 1507-1516; Masai, H., Arai, K., Frpo: A novel single-stranded DNA promoter for transcription and for primer RNA synthesis of DNA replication (1997) Cell, 89, pp. 897-907; Nakabayashi, H., Taketa, K., Miyano, K., Yamane, T., Sato, J., Growth of human hepatoma cells lines with differentiated functions in chemically defined medium (1982) Cancer Res, 42, pp. 3858-3863; Qin, Z., Cohen, S.N., Survival mechanisms for Streptomyces linear replicons after telomere damage (2002) Mol. Microbiol, 45, pp. 785-794; Sakaguchi, K., Invertrons, a class of structurally and functionally related genetic elements that include linear plasmids. transposable elements, and genomes of adeno-type viruses (1990) Microbiol. Rev, 54, pp. 66-74; Salas, M., Protein-primed DNA replication (1991) Annu. Rev. 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PY - 2009

Y1 - 2009

N2 - Bidirectional replication of the linear chromosomes and plasmids of Streptomyces spp. results in single-strand overhangs at their 3′ ends, which contain extensive complex palindromic sequences. The overhangs are believed to be patched by DNA synthesis primed by a terminal protein that remains covalently bound to the 5′ ends of the telomeres. We discovered that in vitro a conserved 167-bp telomere DNA binds strongly to RNA polymerase holoenzyme and exhibits promoter activities stronger than those of an rRNA operon. In vivo, the telomere DNA exhibited promoter activity in both orientations on a circular plasmid in Streptomyces. The telomere promoter is also active on a linear plasmid during exponential growth. Such promoter activity in a telomere has not hitherto been observed in eukaryotic or prokaryotic replicons. Streptomyces telomere promoters may be involved in priming the terminal Okazaki fragment (during replication) replicative transfer (during conjugation), or expression of downstream genes (including a conserved ttrA helicase-like gene involved in conjugal transfer). Interestingly, the Streptomyces telomeres also function as a promoter in Escherichia coli and as a transcription enhancer in yeast. Copyright © 2009, American Society for Microbiology. All Right Reserved.

AB - Bidirectional replication of the linear chromosomes and plasmids of Streptomyces spp. results in single-strand overhangs at their 3′ ends, which contain extensive complex palindromic sequences. The overhangs are believed to be patched by DNA synthesis primed by a terminal protein that remains covalently bound to the 5′ ends of the telomeres. We discovered that in vitro a conserved 167-bp telomere DNA binds strongly to RNA polymerase holoenzyme and exhibits promoter activities stronger than those of an rRNA operon. In vivo, the telomere DNA exhibited promoter activity in both orientations on a circular plasmid in Streptomyces. The telomere promoter is also active on a linear plasmid during exponential growth. Such promoter activity in a telomere has not hitherto been observed in eukaryotic or prokaryotic replicons. Streptomyces telomere promoters may be involved in priming the terminal Okazaki fragment (during replication) replicative transfer (during conjugation), or expression of downstream genes (including a conserved ttrA helicase-like gene involved in conjugal transfer). Interestingly, the Streptomyces telomeres also function as a promoter in Escherichia coli and as a transcription enhancer in yeast. Copyright © 2009, American Society for Microbiology. All Right Reserved.

KW - DNA

KW - helicase

KW - holoenzyme

KW - Okazaki fragment

KW - ribosome RNA

KW - RNA polymerase

KW - DNA directed RNA polymerase

KW - article

KW - bacterium conjugation

KW - controlled study

KW - DNA binding

KW - downstream processing

KW - enhancer region

KW - Escherichia coli

KW - eukaryote

KW - gene activity

KW - gene expression

KW - genetic transcription

KW - growth

KW - in vitro study

KW - in vivo study

KW - nonhuman

KW - operon

KW - plasmid

KW - priority journal

KW - prokaryote

KW - promoter region

KW - replicon

KW - Streptomyces

KW - telomere

KW - yeast

KW - biological model

KW - cell line

KW - gel mobility shift assay

KW - genetics

KW - human

KW - metabolism

KW - polymerase chain reaction

KW - protein binding

KW - Eukaryota

KW - Prokaryota

KW - Cell Line

KW - DNA-Directed RNA Polymerases

KW - Electrophoretic Mobility Shift Assay

KW - Humans

KW - Models, Genetic

KW - Polymerase Chain Reaction

KW - Promoter Regions, Genetic

KW - Protein Binding

KW - Telomere

U2 - 10.1128/JB.01299-08

DO - 10.1128/JB.01299-08

M3 - Article

VL - 191

SP - 773

EP - 781

JO - Journal of Bacteriology

JF - Journal of Bacteriology

SN - 0021-9193

IS - 3

ER -