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. 1991 Jan 1;88(1):31–35. doi: 10.1073/pnas.88.1.31

A potential Z-DNA-forming sequence is located between two transcription units alternatively expressed during development of Drosophila hydei.

A Jimenez-Ruiz 1, J M Requena 1, M C Lopez 1, C Alonso 1
PMCID: PMC50741  PMID: 1840694

Abstract

Recent studies have demonstrated that Z-DNA exists in vivo in Escherichia coli as well as in Drosophila and mammalian cells. In the present paper, we show the existence in vivo of Z-DNA epitopes in the developmentally regulated subregion 4-75C of polytene chromosomes in Drosophila hydei. The Z-DNA epitopes were detected in subdivision C2 only during late third instar when the transcriptional activity of the locus was high. Accumulation of nonhistone chromosomal proteins in that locus was also detected during late third instar only at the time of the Z-DNA formation. Northern blot data and nucleotide sequence analysis indicated that the Z-DNA-forming sequence is located between two transcription units whose expression is regulated during the third instar. Our results suggest that in subdivision 4-75C2 a B- to Z-DNA flux occurs at a specific time during late third instar and that this flux may play a negative as well as a positive role in gene expression.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alcover A., Izquierdo M., Stollar D., Kitagawa Y., Miranda M., Alonso C. In situ immunofluorescent visualization of chromosomal transcripts in polytene chromosomes. Chromosoma. 1982;87(3):263–277. doi: 10.1007/BF00327629. [DOI] [PubMed] [Google Scholar]
  2. Azorin F., Rich A. Isolation of Z-DNA binding proteins from SV40 minichromosomes: evidence for binding to the viral control region. Cell. 1985 Jun;41(2):365–374. doi: 10.1016/s0092-8674(85)80009-x. [DOI] [PubMed] [Google Scholar]
  3. Banerjee R., Grunberger D. Enhanced expression of the bacterial chloramphenicol acetyltransferase gene in mouse cells cotransfected with synthetic polynucleotides able to form Z-DNA. Proc Natl Acad Sci U S A. 1986 Jul;83(14):4988–4992. doi: 10.1073/pnas.83.14.4988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berendes H. D. Salivary gland function and chromosomal puffing patterns in Drosophila hydei. Chromosoma. 1965;17(1):35–77. doi: 10.1007/BF00285155. [DOI] [PubMed] [Google Scholar]
  5. Blaho J. A., Wells R. D. Left-handed Z-DNA binding by the recA protein of Escherichia coli. J Biol Chem. 1987 May 5;262(13):6082–6088. [PubMed] [Google Scholar]
  6. Crowley T. E., Mathers P. H., Meyerowitz E. M. A trans-acting regulatory product necessary for expression of the Drosophila melanogaster 68C glue gene cluster. Cell. 1984 Nov;39(1):149–156. doi: 10.1016/0092-8674(84)90200-9. [DOI] [PubMed] [Google Scholar]
  7. Fishel R. A., Detmer K., Rich A. Identification of homologous pairing and strand-exchange activity from a human tumor cell line based on Z-DNA affinity chromatography. Proc Natl Acad Sci U S A. 1988 Jan;85(1):36–40. doi: 10.1073/pnas.85.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hamada H., Kakunaga T. Potential Z-DNA forming sequences are highly dispersed in the human genome. Nature. 1982 Jul 22;298(5872):396–398. doi: 10.1038/298396a0. [DOI] [PubMed] [Google Scholar]
  9. Hayes T. E., Dixon J. E. Z-DNA in the rat somatostatin gene. J Biol Chem. 1985 Jul 5;260(13):8145–8156. [PubMed] [Google Scholar]
  10. Jaworski A., Hsieh W. T., Blaho J. A., Larson J. E., Wells R. D. Left-handed DNA in vivo. Science. 1987 Nov 6;238(4828):773–777. doi: 10.1126/science.3313728. [DOI] [PubMed] [Google Scholar]
  11. Jimenez-Ruiz A., Requena J. M., Lancillotti F., Morales G., Lopez M. C., Alonso C. Molecular cloning of a Drosophila potential Z-DNA forming sequence hybridizing in situ to a developmentally regulated subdivision of the polytene chromosomes. Nucleic Acids Res. 1989 Jun 26;17(12):4579–4588. doi: 10.1093/nar/17.12.4579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kilpatrick M. W., Klysik J., Singleton C. K., Zarling D. A., Jovin T. M., Hanau L. H., Erlanger B. F., Wells R. D. Intervening sequences in human fetal globin genes adopt left-handed Z helices. J Biol Chem. 1984 Jun 10;259(11):7268–7274. [PubMed] [Google Scholar]
  13. Kmiec E. B., Holloman W. K. Homologous pairing of DNA molecules by Ustilago rec1 protein is promoted by sequences of Z-DNA. Cell. 1986 Feb 28;44(4):545–554. doi: 10.1016/0092-8674(86)90264-3. [DOI] [PubMed] [Google Scholar]
  14. Lafer E. M., Sousa R. J., Rich A. Z-DNA-binding proteins in Escherichia coli purification, generation of monoclonal antibodies and gene isolation. J Mol Biol. 1988 Sep 20;203(2):511–516. doi: 10.1016/0022-2836(88)90017-4. [DOI] [PubMed] [Google Scholar]
  15. Lancillotti F., Lopez M. C., Alonso C., Stollar B. D. Locations of Z-DNA in polytene chromosomes. J Cell Biol. 1985 May;100(5):1759–1766. doi: 10.1083/jcb.100.5.1759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lancillotti F., Lopez M. C., Arias P., Alonso C. Z-DNA in transcriptionally active chromosomes. Proc Natl Acad Sci U S A. 1987 Mar;84(6):1560–1564. doi: 10.1073/pnas.84.6.1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  18. Liu L. F., Wang J. C. Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7024–7027. doi: 10.1073/pnas.84.20.7024. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. MacGillivray A. J., Cameron A., Krauze R. J., Rickwood D., Paul J. The non-histone proteins of chromatin, their isolation and composition in a number of tissues. Biochim Biophys Acta. 1972 Aug 25;277(2):384–402. [PubMed] [Google Scholar]
  20. Morales G., Requena J. M., Jimenez-Ruiz A., Lopez M. C., Ugarte M., Alonso C. Sequence and expression of the Drosophila phenylalanine hydroxylase mRNA. Gene. 1990 Sep 14;93(2):213–219. doi: 10.1016/0378-1119(90)90227-i. [DOI] [PubMed] [Google Scholar]
  21. Naylor L. H., Clark E. M. d(TG)n.d(CA)n sequences upstream of the rat prolactin gene form Z-DNA and inhibit gene transcription. Nucleic Acids Res. 1990 Mar 25;18(6):1595–1601. doi: 10.1093/nar/18.6.1595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nordheim A., Rich A. The sequence (dC-dA)n X (dG-dT)n forms left-handed Z-DNA in negatively supercoiled plasmids. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1821–1825. doi: 10.1073/pnas.80.7.1821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pardue M. L., Lowenhaupt K., Rich A., Nordheim A. (dC-dA)n.(dG-dT)n sequences have evolutionarily conserved chromosomal locations in Drosophila with implications for roles in chromosome structure and function. EMBO J. 1987 Jun;6(6):1781–1789. doi: 10.1002/j.1460-2075.1987.tb02431.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Peck L. J., Nordheim A., Rich A., Wang J. C. Flipping of cloned d(pCpG)n.d(pCpG)n DNA sequences from right- to left-handed helical structure by salt, Co(III), or negative supercoiling. Proc Natl Acad Sci U S A. 1982 Aug;79(15):4560–4564. doi: 10.1073/pnas.79.15.4560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Peck L. J., Wang J. C. Transcriptional block caused by a negative supercoiling induced structural change in an alternating CG sequence. Cell. 1985 Jan;40(1):129–137. doi: 10.1016/0092-8674(85)90316-2. [DOI] [PubMed] [Google Scholar]
  26. Rahmouni A. R., Wells R. D. Stabilization of Z DNA in vivo by localized supercoiling. Science. 1989 Oct 20;246(4928):358–363. doi: 10.1126/science.2678475. [DOI] [PubMed] [Google Scholar]
  27. Rich A., Nordheim A., Wang A. H. The chemistry and biology of left-handed Z-DNA. Annu Rev Biochem. 1984;53:791–846. doi: 10.1146/annurev.bi.53.070184.004043. [DOI] [PubMed] [Google Scholar]
  28. Riddihough G., Pelham H. R. An ecdysone response element in the Drosophila hsp27 promoter. EMBO J. 1987 Dec 1;6(12):3729–3734. doi: 10.1002/j.1460-2075.1987.tb02707.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shen L. P., Rutter W. J. Sequence of the human somatostatin I gene. Science. 1984 Apr 13;224(4645):168–171. doi: 10.1126/science.6142531. [DOI] [PubMed] [Google Scholar]
  31. Silver L. M., Elgin S. C. A method for determination of the in situ distribution of chromosomal proteins. Proc Natl Acad Sci U S A. 1976 Feb;73(2):423–427. doi: 10.1073/pnas.73.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thomas T., Kiang D. T. A twenty-two-fold increase in the relative affinity of estrogen receptor to poly (dA-dC).poly (dG-dT) in the presence of polyamines. Nucleic Acids Res. 1988 May 25;16(10):4705–4720. doi: 10.1093/nar/16.10.4705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tsao Y. P., Wu H. Y., Liu L. F. Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell. 1989 Jan 13;56(1):111–118. doi: 10.1016/0092-8674(89)90989-6. [DOI] [PubMed] [Google Scholar]
  34. Vasicek T. J., McDevitt B. E., Freeman M. W., Fennick B. J., Hendy G. N., Potts J. T., Jr, Rich A., Kronenberg H. M. Nucleotide sequence of the human parathyroid hormone gene. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2127–2131. doi: 10.1073/pnas.80.8.2127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wells R. D. Unusual DNA structures. J Biol Chem. 1988 Jan 25;263(3):1095–1098. [PubMed] [Google Scholar]
  36. Wittig B., Dorbic T., Rich A. The level of Z-DNA in metabolically active, permeabilized mammalian cell nuclei is regulated by torsional strain. J Cell Biol. 1989 Mar;108(3):755–764. doi: 10.1083/jcb.108.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Zacharias W., Jaworski A., Larson J. E., Wells R. D. The B- to Z-DNA equilibrium in vivo is perturbed by biological processes. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7069–7073. doi: 10.1073/pnas.85.19.7069. [DOI] [PMC free article] [PubMed] [Google Scholar]

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