Home LiteratureArticle Details
PMID: 7623835 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

A mutational analysis of the yeast proliferating cell nuclear antigen indicates distinct roles in DNA replication and DNA repair.

Molecular and cellular biology ·Vol. 15 ·No. 8 ·1995-08-00 ·Pages 4420-9

Ayyagari R, Impellizzeri KJ, Yoder BL, Gary SL, Burgers PM

Abstract

The saccharomyces cerevisiae proliferating cell nuclear antigen (PCNA), encoded by the POL30 gene, is essential for DNA replication and DNA repair processes. Twenty-one site-directed mutations were constructed in the POL30 gene, each mutation changing two adjacently located charged amino acids to alanines. Although none of the mutant strains containing these double-alanine mutations as the sole source of PCNA were temperature sensitive or cold sensitive for growth, about a third of the mutants showed sensitivity to UV light. Some of those UV-sensitive mutants had elevated spontaneous mutation rates. In addition, several mutants suppressed a cold-sensitive mutation in the CDC44 gene, which encodes the large subunit of replication factor C. A cold-sensitive mutant, which was isolated by random mutagenesis, showed a terminal phenotype at the restrictive temperature consistent with a defect in DNA replication. Several mutant PCNAs were expressed and purified from Escherichia coli, and their in vitro properties were determined. The cold-sensitive mutant (pol30-52, S115P) was a monomer, rather than a trimer, in solution. This mutant was deficient for DNA synthesis in vitro. Partial restoration of DNA polymerase delta holoenzyme activity was achieved at 37 degrees C but not at 14 degrees C by inclusion of the macromolecular crowding agent polyethylene glycol in the assay. The only other mutant (pol30-6, DD41,42AA) that showed a growth defect was partially defective for interaction with replication factor C and DNA polymerase delta but completely defective for interaction with DNA polymerase epsilon. Two other mutants sensitive to DNA damage showed no defect in vitro. These results indicate that the latter mutants are specifically impaired in one or more DNA repair processes whereas pol30-6 and pol30-52 mutants show their primary defects in the basic DNA replication machinery with probable associated defects in DNA repair. Therefore, DNA repair requires interactions between repair-specific protein(s) and PCNA, which are distinct from those required for DNA replication.

Related Genes
MeSH Terms
Cell Cycle Proteins/genetics Cell Division/genetics Cold Temperature DNA Damage DNA Mutational Analysis DNA Polymerase II DNA Polymerase III DNA Repair DNA Replication/drug effects DNA-Binding Proteins DNA-Directed DNA Polymerase/metabolism Genes, Dominant Homeodomain Proteins Minor Histocompatibility Antigens Models, Molecular Phenotype Polyethylene Glycols/pharmacology Proliferating Cell Nuclear Antigen/genetics,immunology Protein Binding Protein Folding Proto-Oncogene Proteins c-bcl-2 Replication Protein C Repressor Proteins Saccharomyces cerevisiae/genetics,growth & development,immunology Saccharomyces cerevisiae Proteins Structure-Activity Relationship Suppression, Genetic Ultraviolet Rays/adverse effects
Chemicals
BCL2-related protein A1 Cell Cycle Proteins DNA-Binding Proteins Homeodomain Proteins MATA1 protein, S cerevisiae Minor Histocompatibility Antigens Proliferating Cell Nuclear Antigen Proto-Oncogene Proteins c-bcl-2 RFC1 protein, S cerevisiae Repressor Proteins Saccharomyces cerevisiae Proteins Polyethylene Glycols DNA Polymerase II DNA Polymerase III DNA-Directed DNA Polymerase Replication Protein C
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Ayyagari R
Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Impellizzeri K J
Yoder B L
Gary S L
Burgers P M
References (44)
44 references, click to expand
  1. A positive selection for mutants lacking orotidine-5'-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance.
    Mol Gen Genet. 1984;197(2):345-6 PMID: 6394957
  2. Cloning, expression, and chromosomal localization of the 140-kilodalton subunit of replication factor C from mice and humans.
    Mol Cell Biol. 1994 Mar;14(3):1626-34 PMID: 8114700
  3. An auxiliary protein for DNA polymerase-delta from fetal calf thymus.
    J Biol Chem. 1986 Sep 15;261(26):12310-6 PMID: 3745189
  4. The characterization of a mammalian DNA structure-specific endonuclease.
    EMBO J. 1994 Mar 1;13(5):1235-46 PMID: 8131753
  5. The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA.
    Nature. 1994 Jun 16;369(6481):574-8 PMID: 7911228
  6. Proliferating cell nuclear antigen (pol30) mutations suppress cdc44 mutations and identify potential regions of interaction between the two encoded proteins.
    Mol Cell Biol. 1994 Jul;14(7):4390-7 PMID: 7516465
  7. Crystallization of proliferating cell nuclear antigen (PCNA) from Saccharomyces cerevisiae.
    J Mol Biol. 1994 Aug 12;241(2):265-8 PMID: 7914545
  8. Cdk-interacting protein 1 directly binds with proliferating cell nuclear antigen and inhibits DNA replication catalyzed by the DNA polymerase delta holoenzyme.
    Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8655-9 PMID: 7915843
  9. Differential effects by the p21 CDK inhibitor on PCNA-dependent DNA replication and repair.
    Nature. 1994 Oct 6;371(6497):534-7 PMID: 7935768
  10. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA.
    Cell. 1994 Dec 30;79(7):1233-43 PMID: 8001157
  11. Characterization of a mutant strain of Saccharomyces cerevisiae with a deletion of the RAD27 gene, a structural homolog of the RAD2 nucleotide excision repair gene.
    J Bacteriol. 1995 Jan;177(2):364-71 PMID: 7814325
  12. Conditional lethality of null mutations in RTH1 that encodes the yeast counterpart of a mammalian 5'- to 3'-exonuclease required for lagging strand DNA synthesis in reconstituted systems.
    J Biol Chem. 1995 Mar 3;270(9):4193-6 PMID: 7876174
  13. DNA polymerases required for repair of UV-induced damage in Saccharomyces cerevisiae.
    Mol Cell Biol. 1995 Apr;15(4):2173-9 PMID: 7891712
  14. Three-dimensional structure of the beta subunit of E. coli DNA polymerase III holoenzyme: a sliding DNA clamp.
    Cell. 1992 May 1;69(3):425-37 PMID: 1349852
  15. In vitro mutagenesis of the yeast SUP4-o gene to identify all substitutions that can be detected in vivo with the SUP4-o system.
    Environ Mol Mutagen. 1992;19(4):282-7 PMID: 1600954
  16. Purification of PCNA as a nucleotide excision repair protein.
    Nucleic Acids Res. 1992 Jul 11;20(13):2441-6 PMID: 1352873
  17. Calf thymus RF-C as an essential component for DNA polymerase delta and epsilon holoenzymes function.
    Nucleic Acids Res. 1992 Aug 25;20(16):4159-65 PMID: 1354854
  18. Systematic mutational analysis of the yeast ACT1 gene.
    Genetics. 1992 Oct;132(2):337-50 PMID: 1427032
  19. Isolation and analysis of the fission yeast gene encoding polymerase delta accessory protein PCNA.
    EMBO J. 1992 Dec;11(13):5111-20 PMID: 1361173
  20. DNA repair synthesis during base excision repair in vitro is catalyzed by DNA polymerase epsilon and is influenced by DNA polymerases alpha and delta in Saccharomyces cerevisiae.
    Mol Cell Biol. 1993 Feb;13(2):1051-8 PMID: 8423775
  21. Randomization of genes by PCR mutagenesis.
    PCR Methods Appl. 1992 Aug;2(1):28-33 PMID: 1490172
  22. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein.
    Nature. 1987 Apr 2-8;326(6112):517-20 PMID: 2882424
  23. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains.
    Genetics. 1987 Aug;116(4):541-5 PMID: 3305158
  24. The yeast analog of mammalian cyclin/proliferating-cell nuclear antigen interacts with mammalian DNA polymerase delta.
    Proc Natl Acad Sci U S A. 1988 Oct;85(20):7506-10 PMID: 2902631
  25. Molecular cloning and primary structure of the uracil-DNA-glycosylase gene from Saccharomyces cerevisiae.
    J Biol Chem. 1989 Feb 15;264(5):2593-8 PMID: 2644266
  26. REV3, a Saccharomyces cerevisiae gene whose function is required for induced mutagenesis, is predicted to encode a nonessential DNA polymerase.
    J Bacteriol. 1989 Oct;171(10):5659-67 PMID: 2676986
  27. Multiple replication factors augment DNA synthesis by the two eukaryotic DNA polymerases, alpha and delta.
    EMBO J. 1989 Dec 1;8(12):3883-9 PMID: 2573521
  28. Functions of replication factor C and proliferating-cell nuclear antigen: functional similarity of DNA polymerase accessory proteins from human cells and bacteriophage T4.
    Proc Natl Acad Sci U S A. 1990 Feb;87(3):1023-7 PMID: 1967833
  29. Molecular cloning, structure and expression of the yeast proliferating cell nuclear antigen gene.
    Nucleic Acids Res. 1990 Jan 25;18(2):261-5 PMID: 1970160
  30. Drosophila proliferating cell nuclear antigen. Structural and functional homology with its mammalian counterpart.
    J Biol Chem. 1990 Jul 15;265(20):11948-54 PMID: 1973166
  31. Mechanism of elongation of primed DNA by DNA polymerase delta, proliferating cell nuclear antigen, and activator 1.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5672-6 PMID: 1974050
  32. Studies on the activator 1 protein complex, an accessory factor for proliferating cell nuclear antigen-dependent DNA polymerase delta.
    J Biol Chem. 1991 Jan 5;266(1):594-602 PMID: 1670772
  33. Replication factors required for SV40 DNA replication in vitro. I. DNA structure-specific recognition of a primer-template junction by eukaryotic DNA polymerases and their accessory proteins.
    J Biol Chem. 1991 Jan 25;266(3):1950-60 PMID: 1671045
  34. The spectrum of spontaneous mutations in a Saccharomyces cerevisiae uracil-DNA-glycosylase mutant limits the function of this enzyme to cytosine deamination repair.
    J Bacteriol. 1991 Nov;173(21):6807-10 PMID: 1938887
  35. Saccharomyces cerevisiae replication factor C. I. Purification and characterization of its ATPase activity.
    J Biol Chem. 1991 Nov 25;266(33):22689-97 PMID: 1682321
  36. Saccharomyces cerevisiae replication factor C. II. Formation and activity of complexes with the proliferating cell nuclear antigen and with DNA polymerases delta and epsilon.
    J Biol Chem. 1991 Nov 25;266(33):22698-706 PMID: 1682322
  37. Synthesis of DNA by DNA polymerase epsilon in vitro.
    J Biol Chem. 1991 Nov 25;266(33):22707-17 PMID: 1682323
  38. Identification of replication factor C from Saccharomyces cerevisiae: a component of the leading-strand DNA replication complex.
    Mol Cell Biol. 1992 Jan;12(1):155-63 PMID: 1346062
  39. Proliferating cell nuclear antigen is required for DNA excision repair.
    Cell. 1992 Apr 17;69(2):367-74 PMID: 1348971
  40. Interaction of DNA polymerase delta, proliferating cell nuclear antigen, and synthetic oligonucleotide template-primers. Analysis by polyacrylamide gel electrophoresis-band mobility shift assay.
    J Biol Chem. 1993 Jun 25;268(18):13571-6 PMID: 8099910
  41. ATP-independent loading of the proliferating cell nuclear antigen requires DNA ends.
    J Biol Chem. 1993 Sep 25;268(27):19923-6 PMID: 8104181
  42. Yeast DNA replication.
    J Biol Chem. 1993 Dec 5;268(34):25261-4 PMID: 8244955
  43. CDC44: a putative nucleotide-binding protein required for cell cycle progression that has homology to subunits of replication factor C.
    Mol Cell Biol. 1994 Jan;14(1):255-67 PMID: 8264593
  44. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074-8 PMID: 3156376
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1995-08-00
Pages
4420-9
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC230682
Subset
IM
Grants
NIGMS NIH HHS · R01 GM032431 · United States
NIGMS NIH HHS · GM32431 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]