Home LiteratureArticle Details
PMID: 9111307 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

The Schizosaccharomyces pombe rad11+ gene encodes the large subunit of replication protein A.

Molecular and cellular biology ·Vol. 17 ·No. 5 ·1997-05-00 ·Pages 2381-90

Parker AE, Clyne RK, Carr AM, Kelly TJ

Abstract

Replication protein A (RPA) is a heterotrimeric single-stranded DNA-binding protein present in all eukaryotes. In vitro studies have implicated RPA in simian virus 40 DNA synthesis and nucleotide excision repair, but little direct information is available about the in vivo roles of the protein. We report here the cloning of the largest subunit of RPA (rpa1+) from the fission yeast Schizosaccharomyces pombe. The rpa1+ gene is essential for viability and is expressed specifically at S phase of the cell cycle. Genetic analysis revealed that rpa1+ is the locus of the S. pombe radiation-sensitive mutation rad11. The rad11 allele exhibits pleiotropic effects consistent with an in vivo role for RPA in both DNA repair and DNA synthesis. The mutant is sensitive to both UV and ionizing radiation but is not defective in the DNA damage-dependent checkpoint, consistent with the hypothesis that RPA is part of the enzymatic machinery of DNA repair. When incubated in hydroxyurea, rad11 cells initially arrest with a 1C DNA content but then lose viability coincident with reentry into S phase, suggesting that DNA synthesis is aberrant under these conditions. A significant fraction of the mutant cells subsequently undergo inappropriate mitosis in the presence of hydroxyurea, indicating that RPA also plays a role in the checkpoint mechanism that monitors the completion of S phase. We propose that RPA is required to maintain the integrity of replication complexes when DNA replication is blocked. We further suggest that the rad11 mutation leads to the premature breakdown of such complexes, thereby preventing recovery from the hydroxyurea arrest and eliminating a signal recognized by the S-phase checkpoint mechanism.

MeSH Terms
Alleles Amino Acid Sequence Base Sequence Chromosome Mapping Cloning, Molecular DNA Damage DNA Helicases/metabolism DNA Replication DNA, Fungal/chemistry,metabolism DNA-Binding Proteins/genetics Fungal Proteins/genetics Meiosis Molecular Sequence Data Phenotype Recombination, Genetic Replication Protein A S Phase Schizosaccharomyces/genetics
Chemicals
DNA, Fungal DNA-Binding Proteins Fungal Proteins Replication Protein A DNA Helicases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Parker A E
Department of Molecular Biology and Genetics, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA.
Clyne R K
Carr A M
Kelly T J
References (50)
50 references, click to expand
  1. Genetic control of radiation sensitivity in Schizosaccharomyces pombe.
    Genetics. 1975 Apr;79(4):573-82 PMID: 166019
  2. The ionizing radiation-induced replication protein A phosphorylation response differs between ataxia telangiectasia and normal human cells.
    Mol Cell Biol. 1993 Dec;13(12):7222-31 PMID: 8246944
  3. Isolation of the genes encoding the 51-kilodalton and 28-kilodalton subunits of Crithidia fasciculata replication protein A.
    Mol Biochem Parasitol. 1994 Jan;63(1):135-42 PMID: 8183313
  4. UV light-induced DNA synthesis arrest in HeLa cells is associated with changes in phosphorylation of human single-stranded DNA-binding protein.
    EMBO J. 1994 May 1;13(9):2114-23 PMID: 8187764
  5. Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast.
    Mol Biol Cell. 1994 Feb;5(2):147-60 PMID: 8019001
  6. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair.
    Genes Dev. 1994 Mar 15;8(6):652-65 PMID: 7926756
  7. Replication factor A is required in vivo for DNA replication, repair, and recombination.
    Mol Cell Biol. 1994 Dec;14(12):7884-90 PMID: 7969128
  8. The DNA-activated protein kinase is required for the phosphorylation of replication protein A during simian virus 40 DNA replication.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12520-4 PMID: 7809070
  9. DNA polymerase epsilon links the DNA replication machinery to the S phase checkpoint.
    Cell. 1995 Jan 13;80(1):29-39 PMID: 7813016
  10. A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52.
    Mol Cell Biol. 1995 Mar;15(3):1620-31 PMID: 7862153
  11. A mutation in the gene encoding the Saccharomyces cerevisiae single-stranded DNA-binding protein Rfa1 stimulates a RAD52-independent pathway for direct-repeat recombination.
    Mol Cell Biol. 1995 Mar;15(3):1632-41 PMID: 7862154
  12. A kinase from fission yeast responsible for blocking mitosis in S phase.
    Nature. 1995 Apr 27;374(6525):817-9 PMID: 7723827
  13. DNA structure checkpoints in fission yeast.
    Semin Cell Biol. 1995 Apr;6(2):65-72 PMID: 7548844
  14. Fission yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins.
    EMBO J. 1995 Dec 1;14(23):5812-23 PMID: 8846774
  15. Purification, gene cloning, and reconstitution of the heterotrimeric single-stranded DNA-binding protein from Schizosaccharomyces pombe.
    J Biol Chem. 1996 Aug 23;271(34):20868-78 PMID: 8702843
  16. Recovery, repair, and mutagenesis in Schizosaccharomyces pombe.
    Adv Genet. 1985;23:1-72 PMID: 3887858
  17. Simian virus 40 DNA replication in vitro: study of events preceding elongation of chains.
    Proc Natl Acad Sci U S A. 1986 Jul;83(13):4612-6 PMID: 2425351
  18. Replication of simian virus 40 origin-containing DNA in vitro with purified proteins.
    Proc Natl Acad Sci U S A. 1987 Apr;84(7):1834-8 PMID: 3031654
  19. Purification and characterization of replication protein A, a cellular protein required for in vitro replication of simian virus 40 DNA.
    Proc Natl Acad Sci U S A. 1988 Apr;85(8):2523-7 PMID: 2833742
  20. Cellular factors required for multiple stages of SV40 DNA replication in vitro.
    EMBO J. 1988 Apr;7(4):1211-8 PMID: 2841119
  21. Yeast replication factor-A functions in the unwinding of the SV40 origin of DNA replication.
    Nature. 1989 Nov 2;342(6245):92-5 PMID: 2554144
  22. The role of human single-stranded DNA binding protein and its individual subunits in simian virus 40 DNA replication.
    J Biol Chem. 1990 May 5;265(13):7693-700 PMID: 2159011
  23. An essential Saccharomyces cerevisiae single-stranded DNA binding protein is homologous to the large subunit of human RP-A.
    EMBO J. 1990 Jul;9(7):2321-9 PMID: 2192864
  24. Cell-cycle-regulated phosphorylation of DNA replication factor A from human and yeast cells.
    Genes Dev. 1990 Jun;4(6):968-77 PMID: 2200738
  25. Requirement for the replication protein SSB in human DNA excision repair.
    Nature. 1991 Feb 7;349(6309):538-41 PMID: 1992355
  26. Mitochondrial growth and DNA synthesis occur in the absence of nuclear DNA replication in fission yeast.
    J Cell Sci. 1990 Nov;97 ( Pt 3):509-16 PMID: 2074269
  27. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2.
    Cell. 1991 Mar 22;64(6):1111-22 PMID: 1706223
  28. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1991;194:795-823 PMID: 2005825
  29. Effects of T antigen and replication protein A on the initiation of DNA synthesis by DNA polymerase alpha-primase.
    Mol Cell Biol. 1991 Apr;11(4):2108-15 PMID: 1848671
  30. Characterization of a cDNA encoding the 70-kDa single-stranded DNA-binding subunit of human replication protein A and the role of the protein in DNA replication.
    J Biol Chem. 1991 Jun 25;266(18):12090-8 PMID: 2050703
  31. Replication factor-A from Saccharomyces cerevisiae is encoded by three essential genes coordinately expressed at S phase.
    Genes Dev. 1991 Sep;5(9):1589-600 PMID: 1885001
  32. The human homologous pairing protein HPP-1 is specifically stimulated by the cognate single-stranded binding protein hRP-A.
    Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9067-71 PMID: 1924369
  33. Control of DNA synthesis genes in fission yeast by the cell-cycle gene cdc10+.
    Nature. 1992 Jan 30;355(6359):449-53 PMID: 1734281
  34. Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen.
    EMBO J. 1992 Feb;11(2):769-76 PMID: 1311258
  35. Checkpoint controls in Schizosaccharomyces pombe: rad1.
    EMBO J. 1992 Apr;11(4):1335-42 PMID: 1563349
  36. DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe.
    EMBO J. 1992 Apr;11(4):1343-50 PMID: 1563350
  37. Parallel pathways of cell cycle-regulated gene expression.
    Trends Genet. 1992 Mar;8(3):79-81 PMID: 1579990
  38. Identification of nuclear pre-replication centers poised for DNA synthesis in Xenopus egg extracts: immunolocalization study of replication protein A.
    J Cell Biol. 1992 Oct;119(1):1-15 PMID: 1527163
  39. Creative blocks: cell-cycle checkpoints and feedback controls.
    Nature. 1992 Oct 15;359(6396):599-604 PMID: 1406993
  40. Fission yeast genes involved in coupling mitosis to completion of DNA replication.
    Genes Dev. 1992 Nov;6(11):2035-46 PMID: 1427071
  41. An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication.
    J Biol Chem. 1993 Feb 15;268(5):3389-95 PMID: 8381428
  42. High resolution cosmid and P1 maps spanning the 14 Mb genome of the fission yeast S. pombe.
    Cell. 1993 Apr 9;73(1):109-20 PMID: 8462094
  43. A 13 kb resolution cosmid map of the 14 Mb fission yeast genome by nonrandom sequence-tagged site mapping.
    Cell. 1993 Apr 9;73(1):121-32 PMID: 8462095
  44. Complete coverage of the Schizosaccharomyces pombe genome in yeast artificial chromosomes.
    Nat Genet. 1992 Jul;1(4):273-7 PMID: 1302023
  45. Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2.
    Nature. 1993 May 27;363(6427):368-71 PMID: 8497322
  46. Exercising self-restraint: discouraging illicit acts of S and M in eukaryotes.
    Cell. 1993 Jul 30;74(2):223-6 PMID: 8343950
  47. The fission yeast cdc18+ gene product couples S phase to START and mitosis.
    Cell. 1993 Jul 30;74(2):371-82 PMID: 7916658
  48. Fission yeast wee1 protein kinase is not required for DNA damage-dependent mitotic arrest.
    Nature. 1993 Aug 26;364(6440):824-7 PMID: 8355807
  49. Fission yeast with DNA polymerase delta temperature-sensitive alleles exhibits cell division cycle phenotype.
    Nucleic Acids Res. 1993 Aug 11;21(16):3821-8 PMID: 8367300
  50. cdt1 is an essential target of the Cdc10/Sct1 transcription factor: requirement for DNA replication and inhibition of mitosis.
    EMBO J. 1994 Jan 15;13(2):425-34 PMID: 8313888
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1997-05-00
Pages
2381-90
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC232087
Subset
IM
Databases
GENBANK
U75446
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: product@genelibs.com