Abstract
The interaction between purified calf thymus poly(ADP-ribose) polymerase and its activating co-purified DNA (sDNA) was investigated by electron microscopy. We have shown that the enzyme-DNA complex possesses a nucleosome-like structure. The enzyme-bound DNA (sDNA) was found to be enriched in single-stranded regions and branched structures, presumed to be replication forks. The auto-ribosylated polymerase as well as the branched poly(ADP-ribose) formed were visualized by dark field electron microscopy during the auto-ADP-ribosylation reaction and the possible mechanism of this phenomenon is discussed.
Full text
PDF![543](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8c98/555058/15be9199b6f5/emboj00257-0064.png)
![544](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8c98/555058/d670b338b34d/emboj00257-0065.png)
![545](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8c98/555058/65f74a596843/emboj00257-0066.png)
![546](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8c98/555058/0abe07c1f49d/emboj00257-0067.png)
![547](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8c98/555058/e6c47cc7780f/emboj00257-0068.png)
![548](https://cdn.ncbi.nlm.nih.gov/pmc/blobs/8c98/555058/2d10835dc892/emboj00257-0069.png)
Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Benjamin R. C., Gill D. M. Poly(ADP-ribose) synthesis in vitro programmed by damaged DNA. A comparison of DNA molecules containing different types of strand breaks. J Biol Chem. 1980 Nov 10;255(21):10502–10508. [PubMed] [Google Scholar]
- Burzio L., Koide S. S. A functional role of polyADPR in DNA synthesis. Biochem Biophys Res Commun. 1970 Sep 10;40(5):1013–1020. doi: 10.1016/0006-291x(70)90894-6. [DOI] [PubMed] [Google Scholar]
- Caplan A. I., Rosenberg M. J. Interrelationship between poly (ADP-Rib) synthesis, intracellular NAD levels, and muscle or cartilage differentiation from mesodermal cells of embryonic chick limb. Proc Natl Acad Sci U S A. 1975 May;72(5):1852–1857. doi: 10.1073/pnas.72.5.1852. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Murcia G., Wilhelm B., Wilhelm F. X., Daune M. P. Effect of tetramethylammonium ions on conformational changes of DNA in the premelting temperature range. Biophys Chem. 1978 Sep;8(4):377–383. doi: 10.1016/0301-4622(78)80019-2. [DOI] [PubMed] [Google Scholar]
- Dubochet J., Ducommun M., Zollinger M., Kellenberger E. A new preparation method for dark-field electron microscopy of biomacromolecules. J Ultrastruct Res. 1971 Apr;35(1):147–167. doi: 10.1016/s0022-5320(71)80148-x. [DOI] [PubMed] [Google Scholar]
- Durkacz B. W., Omidiji O., Gray D. A., Shall S. (ADP-ribose)n participates in DNA excision repair. Nature. 1980 Feb 7;283(5747):593–596. doi: 10.1038/283593a0. [DOI] [PubMed] [Google Scholar]
- Ferro A. M., Olivera B. M. Poly(ADP-ribosylation) in vitro. Reaction parameters and enzyme mechanism. J Biol Chem. 1982 Jul 10;257(13):7808–7813. [PubMed] [Google Scholar]
- Hashida T., Ohgushi H., Yoshihara K. Highly effective DNA in stimulating poly-(ADP-ribose) polymerase reaction. Biochem Biophys Res Commun. 1979 May 14;88(1):305–311. doi: 10.1016/0006-291x(79)91730-3. [DOI] [PubMed] [Google Scholar]
- Hayaishi O., Ueda K. Poly(ADP-ribose) and ADP-ribosylation of proteins. Annu Rev Biochem. 1977;46:95–116. doi: 10.1146/annurev.bi.46.070177.000523. [DOI] [PubMed] [Google Scholar]
- Hilz H. ADP-ribosylation of proteins--a multifunctional process. Hoppe Seylers Z Physiol Chem. 1981 Nov;362(11):1415–1425. [PubMed] [Google Scholar]
- Hilz H., Stone P. Poly(ADP-ribose) and ADP-ribosylation of proteins. Rev Physiol Biochem Pharmacol. 1976;76:1-58, 177. doi: 10.1007/BFb0027686. [DOI] [PubMed] [Google Scholar]
- Juarez-Salinas H., Levi V., Jacobson E. L., Jacobson M. K. Poly(ADP-ribose) has a branched structure in vivo. J Biol Chem. 1982 Jan 25;257(2):607–609. [PubMed] [Google Scholar]
- Jump D. B., Butt T. R., Smulson M. Nuclear protein modification and chromatin substructure. 3. Relationship between poly(adenosine diphosphate) ribosylation and different functional forms of chromatin. Biochemistry. 1979 Mar 20;18(6):983–990. doi: 10.1021/bi00573a008. [DOI] [PubMed] [Google Scholar]
- Kanai M., Miwa M., Kuchino Y., Sugimura T. Presence of branched portion in poly(adenosine diphosphate ribose) in vivo. J Biol Chem. 1982 Jun 10;257(11):6217–6223. [PubMed] [Google Scholar]
- Kawaichi M., Ueda K., Hayaishi O. Multiple autopoly(ADP-ribosyl)ation of rat liver poly(ADP-ribose) synthetase. Mode of modification and properties of automodified synthetase. J Biol Chem. 1981 Sep 25;256(18):9483–9489. [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Mandel P., Okazaki H., Niedergang C. Poly(adenosine diphosphate ribose). Prog Nucleic Acid Res Mol Biol. 1982;27:1–51. doi: 10.1016/s0079-6603(08)60596-6. [DOI] [PubMed] [Google Scholar]
- Mandel P., Okazaki H., Niedergang C. Purification and properties of calf thymus poly adenosine diphosphate ribose polymerase. FEBS Lett. 1977 Dec 15;84(2):331–336. doi: 10.1016/0014-5793(77)80719-9. [DOI] [PubMed] [Google Scholar]
- Maniatis T., Jeffrey A., van deSande H. Chain length determination of small double- and single-stranded DNA molecules by polyacrylamide gel electrophoresis. Biochemistry. 1975 Aug 26;14(17):3787–3794. doi: 10.1021/bi00688a010. [DOI] [PubMed] [Google Scholar]
- Miwa M., Saikawa N., Yamaizumi Z., Nishimura S., Sugimura T. Structure of poly(adenosine diphosphate ribose): identification of 2'-[1''-ribosyl-2''-(or 3''-)(1'''-ribosyl)]adenosine-5',5'',5'''-tris(phosphate) as a branch linkage. Proc Natl Acad Sci U S A. 1979 Feb;76(2):595–599. doi: 10.1073/pnas.76.2.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moyne G., Freeman R., Saragosti S., Yaniv M. A high-resolution electron microscopy study of nucleosomes from simian virus 40 chromatin. J Mol Biol. 1981 Jul 15;149(4):735–744. doi: 10.1016/0022-2836(81)90355-7. [DOI] [PubMed] [Google Scholar]
- Niedergang C., Okazaki H., Mandel P. Properties of purified calf thymus poly(adenosine diphosphate ribose) polymerase. Comparison of the DNA-independent and the DNA-dependent enzyme. Eur J Biochem. 1979 Dec;102(1):43–57. doi: 10.1111/j.1432-1033.1979.tb06261.x. [DOI] [PubMed] [Google Scholar]
- Nishikimi M., Ogasawara K., Kameshita I., Taniguchi T., Shizuta Y. Poly(ADP-ribose) synthetase. The DNA binding domain and the automodification domain. J Biol Chem. 1982 Jun 10;257(11):6102–6105. [PubMed] [Google Scholar]
- Ohgushi H., Yoshihara K., Kamiya T. Bovine thymus poly(adenosine diphosphate ribose) polymerase. Physical properties and binding to DNA. J Biol Chem. 1980 Jul 10;255(13):6205–6211. [PubMed] [Google Scholar]
- Okazaki H., Niedergang C., Mandel P. Adenosine diphosphate ribosylation of histone H1 by purified calf thymus polyadenosine diphosphate ribose polymerase. Biochimie. 1980;62(2-3):147–157. doi: 10.1016/s0300-9084(80)80190-8. [DOI] [PubMed] [Google Scholar]
- Okazaki H., Niedergang C., Mandel P. Purification and properties of calf thymus polyadenosine diphosphate ribose polymerase. FEBS Lett. 1976 Mar 1;62(3):255–258. doi: 10.1016/0014-5793(76)80069-5. [DOI] [PubMed] [Google Scholar]
- Petzold S. J., Booth B. A., Leimbach G. A., Berger N. A. Purification and properties of poly(ADP-ribose) polymerase from lamb thymus. Biochemistry. 1981 Dec 8;20(25):7075–7081. doi: 10.1021/bi00528a004. [DOI] [PubMed] [Google Scholar]
- Poirier G. G., de Murcia G., Jongstra-Bilen J., Niedergang C., Mandel P. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3423–3427. doi: 10.1073/pnas.79.11.3423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Purnell M. R., Stone P. R., Whish W. J. ADP-ribosylation of nuclear proteins. Biochem Soc Trans. 1980 Apr;8(2):215–227. doi: 10.1042/bst0080215. [DOI] [PubMed] [Google Scholar]
- Saragosti S., Moyne G., Yaniv M. Absence of nucleosomes in a fraction of SV40 chromatin between the origin of replication and the region coding for the late leader RNA. Cell. 1980 May;20(1):65–73. doi: 10.1016/0092-8674(80)90235-4. [DOI] [PubMed] [Google Scholar]
- Smulson M., Stark P., Gazzoli M., Roberts J. Release of template restriction for DNA synthesis by poly ADP(ribose) polymerase during the HeLa cell cycle. Exp Cell Res. 1975 Jan;90(1):175–182. doi: 10.1016/0014-4827(75)90371-7. [DOI] [PubMed] [Google Scholar]
- Whish W. J., Davies M. I., Shall S. Stimulation of poly(ADP-ribose) polymerase activity by the anti-tumour antibiotic, streptozotocin. Biochem Biophys Res Commun. 1975 Jul 22;65(2):722–730. doi: 10.1016/s0006-291x(75)80205-1. [DOI] [PubMed] [Google Scholar]
- Yoshihara K., Hashida T., Tanaka Y., Matsunami N., Yamaguchi A., Kamiya T. Mode of enzyme-bound poly(ADP-ribose) synthesis and histone modification by reconstituted poly(ADP-ribose) polymerase-DNA-cellulose complex. J Biol Chem. 1981 Apr 10;256(7):3471–3478. [PubMed] [Google Scholar]
- Zahradka P., Ebisuzaki K. A shuttle mechanism for DNA-protein interactions. The regulation of poly(ADP-ribose) polymerase. Eur J Biochem. 1982 Oct;127(3):579–585. [PubMed] [Google Scholar]
- de Murcia G., Das G. C., Erard M., Daune M. Superstructure and CD spectrum as probes of chromatin integrity. Nucleic Acids Res. 1978 Feb;5(2):523–535. doi: 10.1093/nar/5.2.523. [DOI] [PMC free article] [PubMed] [Google Scholar]