Strand-specific mismatch correction in nuclear extracts of human and Drosophila melanogaster cell lines (original) (raw)

Abstract

Nuclear extracts derived from HeLa and Drosophila melanogaster KC cell lines have been found to correct single base-base mispairs within open circular DNA heteroduplexes containing a strand-specific, site-specific incision located 808 base pairs from the mismatch. Correction in both extract systems is strand specific, being highly biased to the incised DNA strand. Different mispairs within a homologous set of heteroduplexes were processed with different efficiencies (G.T greater than G.G approximately equal to A.C greater than C.C), and correction was accompanied by mismatch-dependent DNA synthesis localized to the region spanning the mispair and the strand break, thus demonstrating that mismatch recognition is associated with the repair reaction. Correction of each of these heteroduplexes was abolished by aphidicolin but was relatively insensitive to the presence of high concentrations of ddTTP, indicating probable involvement of alpha and/or delta class DNA polymerase(s). These findings suggest that higher eukaryotic cells possess a general, strand-specific mismatch repair system analogous to the Escherichia coli mutHLS and the Streptococcus pneumoniae hexAB pathways, systems that contribute in a major way to the genetic stability of these bacterial species.

5837

Images in this article

Selected References

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

  1. Bishop D. K., Andersen J., Kolodner R. D. Specificity of mismatch repair following transformation of Saccharomyces cerevisiae with heteroduplex plasmid DNA. Proc Natl Acad Sci U S A. 1989 May;86(10):3713–3717. doi: 10.1073/pnas.86.10.3713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brooks P., Dohet C., Almouzni G., Méchali M., Radman M. Mismatch repair involving localized DNA synthesis in extracts of Xenopus eggs. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4425–4429. doi: 10.1073/pnas.86.12.4425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown T. C., Jiricny J. Different base/base mispairs are corrected with different efficiencies and specificities in monkey kidney cells. Cell. 1988 Aug 26;54(5):705–711. doi: 10.1016/s0092-8674(88)80015-1. [DOI] [PubMed] [Google Scholar]
  4. Challberg M. D., Kelly T. J., Jr Adenovirus DNA replication in vitro. Proc Natl Acad Sci U S A. 1979 Feb;76(2):655–659. doi: 10.1073/pnas.76.2.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Claverys J. P., Lacks S. A. Heteroduplex deoxyribonucleic acid base mismatch repair in bacteria. Microbiol Rev. 1986 Jun;50(2):133–165. doi: 10.1128/mr.50.2.133-165.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DePamphilis M. L., Wassarman P. M. Replication of eukaryotic chromosomes: a close-up of the replication fork. Annu Rev Biochem. 1980;49:627–666. doi: 10.1146/annurev.bi.49.070180.003211. [DOI] [PubMed] [Google Scholar]
  7. Edenberg H. J., Anderson S., DePamphilis M. L. Involvement of DNA polymerase alpha in simian virus 40 DNA replication. J Biol Chem. 1978 May 10;253(9):3273–3280. [PubMed] [Google Scholar]
  8. Fujii H., Shimada T. Isolation and characterization of cDNA clones derived from the divergently transcribed gene in the region upstream from the human dihydrofolate reductase gene. J Biol Chem. 1989 Jun 15;264(17):10057–10064. [PubMed] [Google Scholar]
  9. Glazer P. M., Sarkar S. N., Chisholm G. E., Summers W. C. DNA mismatch repair detected in human cell extracts. Mol Cell Biol. 1987 Jan;7(1):218–224. doi: 10.1128/mcb.7.1.218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hare J. T., Taylor J. H. One role for DNA methylation in vertebrate cells is strand discrimination in mismatch repair. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7350–7354. doi: 10.1073/pnas.82.21.7350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kelly T. J. SV40 DNA replication. J Biol Chem. 1988 Dec 5;263(34):17889–17892. [PubMed] [Google Scholar]
  12. Kramer B., Kramer W., Williamson M. S., Fogel S. Heteroduplex DNA correction in Saccharomyces cerevisiae is mismatch specific and requires functional PMS genes. Mol Cell Biol. 1989 Oct;9(10):4432–4440. doi: 10.1128/mcb.9.10.4432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kramer W., Kramer B., Williamson M. S., Fogel S. Cloning and nucleotide sequence of DNA mismatch repair gene PMS1 from Saccharomyces cerevisiae: homology of PMS1 to procaryotic MutL and HexB. J Bacteriol. 1989 Oct;171(10):5339–5346. doi: 10.1128/jb.171.10.5339-5346.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lahue R. S., Au K. G., Modrich P. DNA mismatch correction in a defined system. Science. 1989 Jul 14;245(4914):160–164. doi: 10.1126/science.2665076. [DOI] [PubMed] [Google Scholar]
  15. Lieb M., Allen E., Read D. Very short patch mismatch repair in phage lambda: repair sites and length of repair tracts. Genetics. 1986 Dec;114(4):1041–1060. doi: 10.1093/genetics/114.4.1041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Linton J. P., Yen J. Y., Selby E., Chen Z., Chinsky J. M., Liu K., Kellems R. E., Crouse G. F. Dual bidirectional promoters at the mouse dhfr locus: cloning and characterization of two mRNA classes of the divergently transcribed Rep-1 gene. Mol Cell Biol. 1989 Jul;9(7):3058–3072. doi: 10.1128/mcb.9.7.3058. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lu A. L., Clark S., Modrich P. Methyl-directed repair of DNA base-pair mismatches in vitro. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4639–4643. doi: 10.1073/pnas.80.15.4639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lu A. L., Welsh K., Clark S., Su S. S., Modrich P. Repair of DNA base-pair mismatches in extracts of Escherichia coli. Cold Spring Harb Symp Quant Biol. 1984;49:589–596. doi: 10.1101/sqb.1984.049.01.066. [DOI] [PubMed] [Google Scholar]
  19. Längle-Rouault F., Maenhaut-Michel G., Radman M. GATC sequences, DNA nicks and the MutH function in Escherichia coli mismatch repair. EMBO J. 1987 Apr;6(4):1121–1127. doi: 10.1002/j.1460-2075.1987.tb04867.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Modrich P. DNA mismatch correction. Annu Rev Biochem. 1987;56:435–466. doi: 10.1146/annurev.bi.56.070187.002251. [DOI] [PubMed] [Google Scholar]
  21. Modrich P. Methyl-directed DNA mismatch correction. J Biol Chem. 1989 Apr 25;264(12):6597–6600. [PubMed] [Google Scholar]
  22. Muster-Nassal C., Kolodner R. Mismatch correction catalyzed by cell-free extracts of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7618–7622. doi: 10.1073/pnas.83.20.7618. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Price D. H., Sluder A. E., Greenleaf A. L. Fractionation of transcription factors for RNA polymerase II from Drosophila Kc cell nuclear extracts. J Biol Chem. 1987 Mar 5;262(7):3244–3255. [PubMed] [Google Scholar]
  24. Radman M., Wagner R. Mismatch repair in Escherichia coli. Annu Rev Genet. 1986;20:523–538. doi: 10.1146/annurev.ge.20.120186.002515. [DOI] [PubMed] [Google Scholar]
  25. Randahl H., Elliott G. C., Linn S. DNA-repair reactions by purified HeLa DNA polymerases and exonucleases. J Biol Chem. 1988 Sep 5;263(25):12228–12234. [PubMed] [Google Scholar]
  26. Rayssiguier C., Thaler D. S., Radman M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature. 1989 Nov 23;342(6248):396–401. doi: 10.1038/342396a0. [DOI] [PubMed] [Google Scholar]
  27. Su S. S., Lahue R. S., Au K. G., Modrich P. Mispair specificity of methyl-directed DNA mismatch correction in vitro. J Biol Chem. 1988 May 15;263(14):6829–6835. [PubMed] [Google Scholar]
  28. Su S. S., Modrich P. Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5057–5061. doi: 10.1073/pnas.83.14.5057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Syvaoja J., Linn S. Characterization of a large form of DNA polymerase delta from HeLa cells that is insensitive to proliferating cell nuclear antigen. J Biol Chem. 1989 Feb 15;264(5):2489–2497. [PubMed] [Google Scholar]
  30. Welsh K. M., Lu A. L., Clark S., Modrich P. Isolation and characterization of the Escherichia coli mutH gene product. J Biol Chem. 1987 Nov 15;262(32):15624–15629. [PubMed] [Google Scholar]
  31. Wiebauer K., Jiricny J. In vitro correction of G.T mispairs to G.C pairs in nuclear extracts from human cells. Nature. 1989 May 18;339(6221):234–236. doi: 10.1038/339234a0. [DOI] [PubMed] [Google Scholar]
  32. Wong S. W., Syvaoja J., Tan C. K., Downey K. M., So A. G., Linn S., Wang T. S. DNA polymerases alpha and delta are immunologically and structurally distinct. J Biol Chem. 1989 Apr 5;264(10):5924–5928. [PubMed] [Google Scholar]
  33. van der Vliet P. C., Kwant M. M. Role of DNA polymerase gamma in adenovirus DNA replication. Nature. 1978 Nov 30;276(5687):532–534. doi: 10.1038/276532a0. [DOI] [PubMed] [Google Scholar]