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
. 1992 Aug 1;89(15):6891–6895. doi: 10.1073/pnas.89.15.6891

A single-stranded DNA-binding protein from Crithidia fasciculata recognizes the nucleotide sequence at the origin of replication of kinetoplast DNA minicircles.

Y Tzfati 1, H Abeliovich 1, I Kapeller 1, J Shlomai 1
PMCID: PMC49610  PMID: 1323120

Abstract

A sequence-specific single-stranded DNA-binding protein from the trypanosomatid protozoan Crithidia fasciculata binds to a sequence of 12 nucleotides located at the origin of replication of kinetoplast DNA minicircles. This sequence, termed the universal minicircle sequence (UMS), is conserved in the kinetoplast DNA minicircles among species of the family Trypanosomatidae. The purified protein binds specifically to the heavy strand of the DNA at this site, which consists of the sequence 5'-GGGGTTGGTGTA-3'. Binding analyses using mutated UMS dodecamers have revealed the significant contribution of each of the individual residues at the binding site, with the exception of the 3'-terminal adenine residue, to the generation of specific protein-DNA complexes. The possible role of this sequence-specific single-stranded DNA-binding protein in replication of kinetoplast DNA minicircles and the relation of the UMS to chromosomal telomeric sequences are discussed.

Full text

PDF
6895

Images in this article

6892Image
on p.6892
6893Image
on p.6893

Selected References

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

  1. Birkenmeyer L., Ray D. S. Replication of kinetoplast DNA in isolated kinetoplasts from Crithidia fasciculata. Identification of minicircle DNA replication intermediates. J Biol Chem. 1986 Feb 15;261(5):2362–2368. [PubMed] [Google Scholar]
  2. Birkenmeyer L., Sugisaki H., Ray D. S. Structural characterization of site-specific discontinuities associated with replication origins of minicircle DNA from Crithidia fasciculata. J Biol Chem. 1987 Feb 15;262(5):2384–2392. [PubMed] [Google Scholar]
  3. Blackburn E. H. Telomeres: structure and synthesis. J Biol Chem. 1990 Apr 15;265(11):5919–5921. [PubMed] [Google Scholar]
  4. Buchman A. R., Kornberg R. D. A yeast ARS-binding protein activates transcription synergistically in combination with other weak activating factors. Mol Cell Biol. 1990 Mar;10(3):887–897. doi: 10.1128/mcb.10.3.887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Collick A., Dunn M. G., Jeffreys A. J. Minisatellite binding protein Msbp-1 is a sequence-specific single-stranded DNA-binding protein. Nucleic Acids Res. 1991 Dec 11;19(23):6399–6404. doi: 10.1093/nar/19.23.6399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coren J. S., Epstein E. M., Vogt V. M. Characterization of a telomere-binding protein from Physarum polycephalum. Mol Cell Biol. 1991 Apr;11(4):2282–2290. doi: 10.1128/mcb.11.4.2282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Englund P. T. Free minicircles of kinetoplast DNA in Crithidia fasciculata. J Biol Chem. 1979 Jun 10;254(11):4895–4900. [PubMed] [Google Scholar]
  8. Englund P. T., Hajduk S. L., Marini J. C. The molecular biology of trypanosomes. Annu Rev Biochem. 1982;51:695–726. doi: 10.1146/annurev.bi.51.070182.003403. [DOI] [PubMed] [Google Scholar]
  9. Englund P. T. The replication of kinetoplast DNA networks in Crithidia fasciculata. Cell. 1978 May;14(1):157–168. doi: 10.1016/0092-8674(78)90310-0. [DOI] [PubMed] [Google Scholar]
  10. Fang G. W., Cech T. R. Molecular cloning of telomere-binding protein genes from Stylonychia mytilis. Nucleic Acids Res. 1991 Oct 25;19(20):5515–5518. doi: 10.1093/nar/19.20.5515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gottschling D. E., Zakian V. A. Telomere proteins: specific recognition and protection of the natural termini of Oxytricha macronuclear DNA. Cell. 1986 Oct 24;47(2):195–205. doi: 10.1016/0092-8674(86)90442-3. [DOI] [PubMed] [Google Scholar]
  12. Gray J. T., Celander D. W., Price C. M., Cech T. R. Cloning and expression of genes for the Oxytricha telomere-binding protein: specific subunit interactions in the telomeric complex. Cell. 1991 Nov 15;67(4):807–814. doi: 10.1016/0092-8674(91)90075-a. [DOI] [PubMed] [Google Scholar]
  13. Henderson E. R., Blackburn E. H. An overhanging 3' terminus is a conserved feature of telomeres. Mol Cell Biol. 1989 Jan;9(1):345–348. doi: 10.1128/mcb.9.1.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hicke B. J., Celander D. W., MacDonald G. H., Price C. M., Cech T. R. Two versions of the gene encoding the 41-kilodalton subunit of the telomere binding protein of Oxytricha nova. Proc Natl Acad Sci U S A. 1990 Feb;87(4):1481–1485. doi: 10.1073/pnas.87.4.1481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kitchin P. A., Klein V. A., Englund P. T. Intermediates in the replication of kinetoplast DNA minicircles. J Biol Chem. 1985 Mar 25;260(6):3844–3851. [PubMed] [Google Scholar]
  16. Kitchin P. A., Klein V. A., Fein B. I., Englund P. T. Gapped Minicircles. A novel replication intermediate of kinetoplast DNA. J Biol Chem. 1984 Dec 25;259(24):15532–15539. [PubMed] [Google Scholar]
  17. Kuno K., Murakami S., Kuno S. Single-strand-binding factor(s) which interact with ARS1 of Saccharomyces cerevisiae. Gene. 1990 Oct 30;95(1):73–77. doi: 10.1016/0378-1119(90)90415-n. [DOI] [PubMed] [Google Scholar]
  18. McGeoch D. J., Dalrymple M. A., Davison A. J., Dolan A., Frame M. C., McNab D., Perry L. J., Scott J. E., Taylor P. The complete DNA sequence of the long unique region in the genome of herpes simplex virus type 1. J Gen Virol. 1988 Jul;69(Pt 7):1531–1574. doi: 10.1099/0022-1317-69-7-1531. [DOI] [PubMed] [Google Scholar]
  19. Ntambi J. M., Englund P. T. A gap at a unique location in newly replicated kinetoplast DNA minicircles from Trypanosoma equiperdum. J Biol Chem. 1985 May 10;260(9):5574–5579. [PubMed] [Google Scholar]
  20. Ntambi J. M., Shapiro T. A., Ryan K. A., Englund P. T. Ribonucleotides associated with a gap in newly replicated kinetoplast DNA minicircles from Trypanosoma equiperdum. J Biol Chem. 1986 Sep 5;261(25):11890–11895. [PubMed] [Google Scholar]
  21. Pestov D. G., Gladkaya L. A., Maslov D. A., Kolesnikov A. A. Characterization of kinetoplast minicircle DNA in the lower trypanosomatid Crithidia oncopelti. Mol Biochem Parasitol. 1990 Jun;41(1):135–145. doi: 10.1016/0166-6851(90)90104-t. [DOI] [PubMed] [Google Scholar]
  22. Price C. M., Cech T. R. Properties of the telomeric DNA-binding protein from Oxytricha nova. Biochemistry. 1989 Jan 24;28(2):769–774. doi: 10.1021/bi00428a053. [DOI] [PubMed] [Google Scholar]
  23. Price C. M., Cech T. R. Telomeric DNA-protein interactions of Oxytricha macronuclear DNA. Genes Dev. 1987 Oct;1(8):783–793. doi: 10.1101/gad.1.8.783. [DOI] [PubMed] [Google Scholar]
  24. Price C. M. Telomere structure in Euplotes crassus: characterization of DNA-protein interactions and isolation of a telomere-binding protein. Mol Cell Biol. 1990 Jul;10(7):3421–3431. doi: 10.1128/mcb.10.7.3421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ray D. S. Kinetoplast DNA minicircles: high-copy-number mitochondrial plasmids. Plasmid. 1987 May;17(3):177–190. doi: 10.1016/0147-619x(87)90026-6. [DOI] [PubMed] [Google Scholar]
  26. Ryan K. A., Englund P. T. Replication of kinetoplast DNA in Trypanosoma equiperdum. Minicircle H strand fragments which map at specific locations. J Biol Chem. 1989 Jan 15;264(2):823–830. [PubMed] [Google Scholar]
  27. Ryan K. A., Englund P. T. Synthesis and processing of kinetoplast DNA minicircles in Trypanosoma equiperdum. Mol Cell Biol. 1989 Aug;9(8):3212–3217. doi: 10.1128/mcb.9.8.3212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ryan K. A., Shapiro T. A., Rauch C. A., Englund P. T. Replication of kinetoplast DNA in trypanosomes. Annu Rev Microbiol. 1988;42:339–358. doi: 10.1146/annurev.mi.42.100188.002011. [DOI] [PubMed] [Google Scholar]
  29. Ryan K. A., Shapiro T. A., Rauch C. A., Griffith J. D., Englund P. T. A knotted free minicircle in kinetoplast DNA. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5844–5848. doi: 10.1073/pnas.85.16.5844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Santoro I. M., Yi T. M., Walsh K. Identification of single-stranded-DNA-binding proteins that interact with muscle gene elements. Mol Cell Biol. 1991 Apr;11(4):1944–1953. doi: 10.1128/mcb.11.4.1944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Saucier J. M., Benard J., da Silva J., Riou G. Occurrence of a kinetoplast DNA-protein complex in Trypanosoma cruzi. Biochem Biophys Res Commun. 1981 Aug 14;101(3):988–994. doi: 10.1016/0006-291x(81)91846-5. [DOI] [PubMed] [Google Scholar]
  32. Schmidt A. M., Herterich S. U., Krauss G. A single-stranded DNA binding protein from S. cerevisiae specifically recognizes the T-rich strand of the core sequence of ARS elements and discriminates against mutant sequences. EMBO J. 1991 Apr;10(4):981–985. doi: 10.1002/j.1460-2075.1991.tb08032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sheline C., Melendy T., Ray D. S. Replication of DNA minicircles in kinetoplasts isolated from Crithidia fasciculata: structure of nascent minicircles. Mol Cell Biol. 1989 Jan;9(1):169–176. doi: 10.1128/mcb.9.1.169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sheline C., Ray D. S. Specific discontinuities in Leishmania tarentolae minicircles map within universally conserved sequence blocks. Mol Biochem Parasitol. 1989 Dec;37(2):151–157. doi: 10.1016/0166-6851(89)90147-3. [DOI] [PubMed] [Google Scholar]
  35. Shlomai J., Linial M. A nicking enzyme from trypanosomatids which specifically affects the topological linking of duplex DNA circles. Purification and characterization. J Biol Chem. 1986 Dec 5;261(34):16219–16225. [PubMed] [Google Scholar]
  36. Shore D., Stillman D. J., Brand A. H., Nasmyth K. A. Identification of silencer binding proteins from yeast: possible roles in SIR control and DNA replication. EMBO J. 1987 Feb;6(2):461–467. doi: 10.1002/j.1460-2075.1987.tb04776.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Simpson L., Braly P. Synchronization of Leishmania tarentolae by hydroxyurea. J Protozool. 1970 Nov;17(4):511–517. doi: 10.1111/j.1550-7408.1970.tb04719.x. [DOI] [PubMed] [Google Scholar]
  38. Simpson L. The mitochondrial genome of kinetoplastid protozoa: genomic organization, transcription, replication, and evolution. Annu Rev Microbiol. 1987;41:363–382. doi: 10.1146/annurev.mi.41.100187.002051. [DOI] [PubMed] [Google Scholar]
  39. Sugisaki H., Ray D. S. DNA sequence of Crithidia fasciculata kinetoplast minicircles. Mol Biochem Parasitol. 1987 Apr;23(3):253–263. doi: 10.1016/0166-6851(87)90032-6. [DOI] [PubMed] [Google Scholar]
  40. Sweder K. S., Rhode P. R., Campbell J. L. Purification and characterization of proteins that bind to yeast ARSs. J Biol Chem. 1988 Nov 25;263(33):17270–17277. [PubMed] [Google Scholar]
  41. Walker S. S., Francesconi S. C., Eisenberg S. A DNA replication enhancer in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4665–4669. doi: 10.1073/pnas.87.12.4665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zahler A. M., Prescott D. M. DNA primase and the replication of the telomeres in Oxytricha nova. Nucleic Acids Res. 1989 Aug 11;17(15):6299–6317. doi: 10.1093/nar/17.15.6299. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zakian V. A. Structure and function of telomeres. Annu Rev Genet. 1989;23:579–604. doi: 10.1146/annurev.ge.23.120189.003051. [DOI] [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