Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Feb;87(4):1292–1295. doi: 10.1073/pnas.87.4.1292

Are many Z-DNA binding proteins actually phospholipid-binding proteins?

P Krishna 1, B P Kennedy 1, D M Waisman 1, J H van de Sande 1, J D McGhee 1
PMCID: PMC53460  PMID: 2406717

Abstract

We used a Z-DNA affinity column to isolate a collection of Z-DNA binding proteins from a high salt extract of Escherichia coli. We identified one of the major Z-DNA binding proteins of this fraction, not as a protein involved in gene regulation or genetic recombination, but rather as an outer membrane porin protein. We then showed that several other known phospholipid-binding proteins (bovine lung annexins and human serum lipoproteins) also bind much more tightly to Z-DNA than to B-DNA. In all cases, this Z-DNA binding was strongly blocked by competition with acidic phospholipids, such as cardiolipin. Our results raise the question whether many of the Z-DNA binding proteins previously isolated are actually phospholipid-binding proteins.

Full text

PDF
1292

Images in this article

1293Image
on p.1293

Selected References

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

  1. Allfrey V. G., Inoue A. Affinity chromatography of DNA-binding proteins on DNA covalently attached to solid supports. Methods Cell Biol. 1978;17:253–270. doi: 10.1016/s0091-679x(08)61147-4. [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. Crompton M. R., Moss S. E., Crumpton M. J. Diversity in the lipocortin/calpactin family. Cell. 1988 Oct 7;55(1):1–3. doi: 10.1016/0092-8674(88)90002-5. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Garner M. M., Felsenfeld G. Effect of Z-DNA on nucleosome placement. J Mol Biol. 1987 Aug 5;196(3):581–590. doi: 10.1016/0022-2836(87)90034-9. [DOI] [PubMed] [Google Scholar]
  6. Gut S. H., Bischoff M., Hobi R., Kuenzle C. C. Z-DNA-binding proteins from bull testis. Nucleic Acids Res. 1987 Dec 10;15(23):9691–9705. doi: 10.1093/nar/15.23.9691. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hall M. N., Silhavy T. J. Genetic analysis of the major outer membrane proteins of Escherichia coli. Annu Rev Genet. 1981;15:91–142. doi: 10.1146/annurev.ge.15.120181.000515. [DOI] [PubMed] [Google Scholar]
  8. Hoheisel J. D., Pohl F. M. Searching for potential Z-DNA in genomic Escherichia coli DNA. J Mol Biol. 1987 Feb 5;193(3):447–464. doi: 10.1016/0022-2836(87)90259-2. [DOI] [PubMed] [Google Scholar]
  9. Horbach E., Müller-Hill B. Insertion of d(pCpG)n.d(pCpG)n into the lacZ gene of Escherichia coli inhibits expression of beta-galactosidase in vivo. J Mol Biol. 1988 Jul 5;202(1):157–160. doi: 10.1016/0022-2836(88)90527-x. [DOI] [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. Khanna N. C., Tokuda M., Waisman D. M. Purification of three forms of lipocortin from bovine lung. Cell Calcium. 1987 Jun;8(3):217–228. doi: 10.1016/0143-4160(87)90020-0. [DOI] [PubMed] [Google Scholar]
  12. Kitayama S., Matsumura O., Masuda S. A Z-DNA binding protein isolated from D. radiodurans. Biochem Biophys Res Commun. 1985 Aug 15;130(3):1294–1300. doi: 10.1016/0006-291x(85)91755-3. [DOI] [PubMed] [Google Scholar]
  13. Kitayama S., Matsumura O., Masuda S. Isolation of a DNA-binding protein from Deinococcus radiodurans having an affinity for a Z-form polynucleotide. J Biochem. 1988 Jul;104(1):127–130. doi: 10.1093/oxfordjournals.jbchem.a122407. [DOI] [PubMed] [Google Scholar]
  14. Klee C. B. Ca2+-dependent phospholipid- (and membrane-) binding proteins. Biochemistry. 1988 Sep 6;27(18):6645–6653. doi: 10.1021/bi00418a001. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Krishna P., Kennedy B. P., van de Sande J. H., McGhee J. D. Yolk proteins from nematodes, chickens, and frogs bind strongly and preferentially to left-handed Z-DNA. J Biol Chem. 1988 Dec 15;263(35):19066–19070. [PubMed] [Google Scholar]
  17. Kuenzle C. C., Heizmann C. W., Hübscher U., Hobi R., Winkler G. C., Jaeger A. W., Morgenegg G. Chromatin changes accompanying neuronal differentiation. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):493–499. doi: 10.1101/sqb.1983.048.01.054. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Lafer E. M., Sousa R., Rosen B., Hsu A., Rich A. Isolation and characterization of Z-DNA binding proteins from wheat germ. Biochemistry. 1985 Sep 10;24(19):5070–5076. doi: 10.1021/bi00340a017. [DOI] [PubMed] [Google Scholar]
  20. Leith I. R., Hay R. T., Russell W. C. Detection of Z DNA binding proteins in tissue culture cells. Nucleic Acids Res. 1988 Sep 12;16(17):8277–8289. doi: 10.1093/nar/16.17.8277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mahley R. W., Innerarity T. L., Rall S. C., Jr, Weisgraber K. H. Plasma lipoproteins: apolipoprotein structure and function. J Lipid Res. 1984 Dec 1;25(12):1277–1294. [PubMed] [Google Scholar]
  22. Nikaido H. Proteins forming large channels from bacterial and mitochondrial outer membranes: porins and phage lambda receptor protein. Methods Enzymol. 1983;97:85–100. doi: 10.1016/0076-6879(83)97122-7. [DOI] [PubMed] [Google Scholar]
  23. Nordheim A., Lafer E. M., Peck L. J., Wang J. C., Stollar B. D., Rich A. Negatively supercoiled plasmids contain left-handed Z-DNA segments as detected by specific antibody binding. Cell. 1982 Dec;31(2 Pt 1):309–318. doi: 10.1016/0092-8674(82)90124-6. [DOI] [PubMed] [Google Scholar]
  24. Nordheim A., Rich A. Negatively supercoiled simian virus 40 DNA contains Z-DNA segments within transcriptional enhancer sequences. Nature. 1983 Jun 23;303(5919):674–679. doi: 10.1038/303674a0. [DOI] [PubMed] [Google Scholar]
  25. 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]
  26. Nordheim A., Tesser P., Azorin F., Kwon Y. H., Möller A., Rich A. Isolation of Drosophila proteins that bind selectively to left-handed Z-DNA. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7729–7733. doi: 10.1073/pnas.79.24.7729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Raag R., Appelt K., Xuong N. H., Banaszak L. Structure of the lamprey yolk lipid-protein complex lipovitellin-phosvitin at 2.8 A resolution. J Mol Biol. 1988 Apr 5;200(3):553–569. doi: 10.1016/0022-2836(88)90542-6. [DOI] [PubMed] [Google Scholar]
  29. Ramesh N., Shouche Y. S., Brahmachari S. K. Recognition of B and Z forms of DNA by Escherichia coli DNA polymerase I. J Mol Biol. 1986 Aug 20;190(4):635–638. doi: 10.1016/0022-2836(86)90248-2. [DOI] [PubMed] [Google Scholar]
  30. Rodriguez-Campos A., Ellison M. J., Pérez-Grau L., Azorin F. DNA conformation and chromatin organization of a d(CA/GT)30 sequence cloned in SV40 minichromosomes. EMBO J. 1986 Jul;5(7):1727–1734. doi: 10.1002/j.1460-2075.1986.tb04417.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sinden R. R., Kochel T. J. Reduced 4,5',8-trimethylpsoralen cross-linking of left-handed Z-DNA stabilized by DNA supercoiling. Biochemistry. 1987 Mar 10;26(5):1343–1350. doi: 10.1021/bi00379a021. [DOI] [PubMed] [Google Scholar]
  32. Stockton J. F., Miller F. D., Jorgenson K. F., Zarling D. A., Morgan A. R., Rattner J. B., van de Sande J. H. Left-handed Z-DNA regions are present in negatively supercoiled bacteriophage PM2 DNA. EMBO J. 1983;2(12):2123–2128. doi: 10.1002/j.1460-2075.1983.tb01712.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES