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The distributions of nucleotides near bacterial transcription initiation and termination sites show distinct signals that may affect DNA geometry

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Summary

Compilation and analysis of all bacterial sequences which are aligned by their transcription initiation sites show a dramatic behavior of the four nucleotides. Large peaks of T and A are observed. This highly nonrandom distribution is likely to affect the DNA geometry in addition to affecting the strength of binding between the two DNA strands. Following this site, the G and C rise above their overall bacterial mean. Alignment by transcription termination sites indicates that this behavior continues till the mRNA 3′ termini. At this site the concentrations of A and T rise again above the mean. Analysis of the distributions of the 256 quartets in the 1000 nucleotide regions surrounding both transcription initiation and termination sites has been carried out. Some A/T combination sequences may serve as signals to the bacterial transcription machinery, in addition to the well-established T T G A C A and T A T A A T at positions −35 and −10, respectively, and a run of Ts at the transcription termination site. The frequent occurrences of (dA)/(dT) runs in the vicinity of these sites may result in curved DNA structures, affecting recognition and the nature of the interaction between the RNA polymerase and the DNA.

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References

  • Arnott S, Chandrasekaran R, Hall IH, Puigjaner LC (1983) Heteronomous DNA. Nucleic Acids Res 11:4141–4155

    PubMed  Google Scholar 

  • Bossi L, Smith DM (1984) Conformational change in the DNA associated with an unusual promoter mutation in an tRNA operon ofSalmonella. Cell 39:643–652

    Article  PubMed  Google Scholar 

  • Brendel V, Trifonov EN (1984) A computer algorithm for testing potential prokaryotic terminators. Nucleic Acids Res 12: 4411–4427

    PubMed  Google Scholar 

  • Briat J-F, Chamberlin MJ (1984) Identification and characterization of a new transcription termination factor fromEscherichia coli. Proc Natl Acad Sci USA 81:7373–7377

    PubMed  Google Scholar 

  • Collins FS, Metherall JE, Yamakawa M, Pan J, Weissman SM, Forget BG (1985) A point mutation in theAgamma-globin gene promoter in Greek hereditary persistence of fetal hemoglobin. Nature 313:325–326

    Article  PubMed  Google Scholar 

  • Diekmann S, Wang JC (1985) On the sequence determination and flexibility of the kinetoplast DNA fragment with abnormal gel electrophoretic mobilities. J Mol Biol 186:1–11

    Article  PubMed  Google Scholar 

  • Gelinas R, Endlich B, Pfeiffer C, Yagi M, Stamatoyannopoulos G (1985) G to A substitution in the distal CCAAT box of theAgamma-globin gene in Greek hereditary persistence of fetal hemoglobin. Nature 313:323–325

    Article  PubMed  Google Scholar 

  • Gilbert W (1976) In: Losick R, Chamberlin M (eds) RNA polymerase. Cold Spring Harbor Laboratory, Cold Spring Harbor NY, pp 193–205

    Google Scholar 

  • Hagerman PJ (1984) Evidence for the existence of stable curvature of DNA in solution. Proc Natl Acad Sci USA 81:4632–4636

    PubMed  Google Scholar 

  • Hagerman PJ (1985) Sequence dependence of the curvature of DNA: a test of the phasing hypothesis. Biochemistry 24:7033–7037

    Article  PubMed  Google Scholar 

  • Hagerman PJ (1986) Sequence directed curvature of DNA. Nature 321:449–450

    Article  PubMed  Google Scholar 

  • Hawley DK, McClure WR (1983) Compilation and analysis ofEscherichia coli promoter DNA sequences. Nucleic Acids Res 11:2237–2255

    PubMed  Google Scholar 

  • Jernigan RL, Sarai A, Ting K-L, Nussinov R (1986) Hydrophobic interactions in the major groove can influence DNA local structure. J Biomol Str Dyn 4:41–48

    Google Scholar 

  • Jernigan RL, Sarai A, Shapiro B, Nussinov R (1987) Relationship between curved DNA conformations and slow gel migration J Biomol Str Dyn 4:561–567

    Google Scholar 

  • Kingston RE, Chamberlin MJ (1981) Pausing and attenuation of in vitro transcription in the rrnB operon ofE. coli. Cell 27:523–531

    Article  PubMed  Google Scholar 

  • Koo H-S, Wu H-M, Crothers D (1986) DNA bending at adenine thymine tracts. Nature 320:501–506.

    Article  PubMed  Google Scholar 

  • Lamond AI, Travers AA (1985a) Stringent control of bacterial transcription. Cell 41:4–8.

    Article  Google Scholar 

  • Lamond AI, Travers AA (1985b) Genetically separable functional elements mediate the optimal expression and stringent regulation of a bacterial gene. Cell 40:319–326

    Article  PubMed  Google Scholar 

  • Landy A, Ross W (1977) Viral integration and excision: structure of the lambda att sites. Science 197:1147–1160

    PubMed  Google Scholar 

  • Lennon GG, Nussinov R (1984) Homonyms, synonyms and mutations of the sequence/structure vocabulary. J Mol Biol 175:425–430

    Article  PubMed  Google Scholar 

  • Levene SD, Crothers DM (1983) A computer graphics study of sequence-directed bending of DNA. J Biomol Str Dyn 1: 429–435

    Google Scholar 

  • Levene SD, Wu H-M, Crothers DM (1986) Bending and flexibility of kinetoplast DNA. Biochemistry 25:3988–3995.

    Article  PubMed  Google Scholar 

  • Lilley D (1986) Bent molecules how and why? Nature 320:487–488

    Article  PubMed  Google Scholar 

  • Maniatis T, Ptashne M, Backmann K, Kleid D, Flashman S, Jeffrey A, Maurer R (1975) Recognition sequences of repressor and polymerase in the operators of bacteriophage lambda. Cell 5:109–113.

    Article  PubMed  Google Scholar 

  • Martin FH, Tinoco I Jr (1980) DNA-RNA hybrid duplexes containing oligo(dA:rU) sequences are exceptionally unstable and may facilitate termination of transcription. Nucleic Acids Res 8:2295–2299

    PubMed  Google Scholar 

  • McCall M, Brown R, Kennard O (1985) The crystal structure of d(G-G-G-G-C-C-C-C) a model for poly(dG)·poly(dc). J Mol Biol 183:385–396

    Article  PubMed  Google Scholar 

  • McKnight SL, Kingsbury R (1982) The transcriptional control of a eukaryotic protein-coding gene. Science 217:316–324

    PubMed  Google Scholar 

  • Miller JH, Reznikoff WS (eds) (1978) The operon. Cold Spring Harbor Laboratory, Cold Spring Harbor NY

    Google Scholar 

  • Nussinov R (1984a) Promoter helical structure variation at theE. coli polymerase interaction sites. J Biol Chem 259:6798–6805

    PubMed  Google Scholar 

  • Nussinov R (1984b) Strong doublet preferences in nucleotide sequences and DNA geometry. J Mol Evol 20:111–119

    PubMed  Google Scholar 

  • Nussinov R (1984c) Doublet frequencies in evolutionary distinct groups. Nucleic Acids Res 12:1749–1763

    PubMed  Google Scholar 

  • Nussinov R (1985) Large helical conformational deviation from ideal B-DNA and prokaryotic regulatory sites. J Theor Biol 115:179–189

    PubMed  Google Scholar 

  • Nussinov R, Owens J, Maizel JV Jr (1986) Sequence signals in eukaryotic upstream regions. Biochim Biophys Acta 866:109–119

    PubMed  Google Scholar 

  • Platt T (1981) Termination of transcription and its regulation in the tryptophan operon ofE. coli. Cell 24:10–23

    Article  PubMed  Google Scholar 

  • Pribnow D (1975) Nucleotide sequence of an RNA polymerase binding site at an early T7 promoter. Proc Natl Acad Sci USA 72:784–788

    PubMed  Google Scholar 

  • Roberts JW (1969) Termination factor for RNA synthesis. Nature 224:1168–1174

    PubMed  Google Scholar 

  • Rosenberg M, Court D (1979) Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet 13:319–353

    Article  PubMed  Google Scholar 

  • Ross W, Landy A (1982) Bacteriophage lambda int protein recognizes two classes of sequence in the phageatt site: characterization of the arm-type sites. Proc Natl Acad Sci USA 79:7724–7728

    PubMed  Google Scholar 

  • Sarma MH, Gupta G, Sarma RH (1985) Untenability of the heteronomous DNA model for poly(dA)·poly(dT) in solution. This DNA adopts a right-handed B-DNA duplex in which the two strands are conformationally equivalent. A 500 MHz NMR study using one dimensional NOE. J Biomol Str Dyn 2:1057–1084

    Google Scholar 

  • Satchwell SC, Drew HR, Travers AA (1986) Sequence periodicities in chicken nucleosome core DNA. J Mol Biol 191:659–675

    Article  PubMed  Google Scholar 

  • Schaller H, Gray C, Hermann K (1975) Nucleotide sequence of an RNA polymerase binding site from the DNA of bacteriophage Fd. Proc Natl Acad Sci USA 72:737–741

    PubMed  Google Scholar 

  • Shih M-C, Gussin GN (1984) Differential effects of mutations on discrete steps in transcription initiation at the λ Pre promoter. Cell 34:941–949

    Article  Google Scholar 

  • Siebenlist U (1979) Nucleotide sequence of the three major early promoters of bacteriophage T7. Nucleic Acids Res 6: 1895–1907

    PubMed  Google Scholar 

  • Siebenlist U, Simpson RB, Gilbert W (1980)E. coli RNA polymerase interacts homologously with two different promoters. Cell 20:269–281

    Article  PubMed  Google Scholar 

  • Travers A (1980) A tRNA tyr promoter with an altered in vitro response to ppGpp. J Mol Biol 141:91–97

    PubMed  Google Scholar 

  • Trifonov EN (1986) Curved DNA. CRC Crit Rev Biochem 19: 89–106

    Google Scholar 

  • Wada A, Suyama A (1986a) Homogeneous double-helix-stability in individual genes. In: Sarma RH (ed) Proceedings of the 4th conversation in the discipline of biomolecular stereodynamics. Adenine Press, New York, pp 255–269

    Google Scholar 

  • Wada A, Suyama A (1986b) Local stability of DNA and RNA secondary structure and its relation to biological functions. Prog Biophys Mol Biol 47:113–157

    Article  PubMed  Google Scholar 

  • Wu H-M, Crothers DM (1984) The locus of sequence directed and protein induced DNA bending. Nature 308:509–513

    Article  PubMed  Google Scholar 

  • Zahn K, Blattner FR (1985) Sequence induced DNA curvature at the bacteriophage lambda origin of replication. Nature 317: 451–453

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Mathematical Biology, Building 10, Room 4B-56, National Cancer Institute, National Institutes of Health, 20205, Bethesda, Maryland, USA

    Ruth Nussinov, Ann Barber & Jacob V. Maizel Jr.

  2. Sackler Institute of Molecular Medicine, Sackler Faculty of Medicine, Tel Aviv University, Ramat Aviv, Israel

    Ruth Nussinov

Authors
  1. Ruth Nussinov
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  2. Ann Barber
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  3. Jacob V. Maizel Jr.
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Nussinov, R., Barber, A. & Maizel, J.V. The distributions of nucleotides near bacterial transcription initiation and termination sites show distinct signals that may affect DNA geometry. J Mol Evol 26, 187–197 (1987). https://doi.org/10.1007/BF02099851

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  • DOI: https://doi.org/10.1007/BF02099851

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