Abstract
Free full text
Role of Saccharomyces cerevisiae chromatin assembly factor-I in repair of ultraviolet radiation damage in vivo.
Abstract
In vitro, the protein complex Chromatin Assembly Factor-I (CAF-I) from human or yeast cells deposits histones onto DNA templates after replication. In Saccharomyces cerevisiae, the CAC1, CAC2, and CAC3 genes encode the three CAF-I subunits. Deletion of any of the three CAC genes reduces telomeric gene silencing and confers an increase in sensitivity to killing by ultraviolet (UV) radiation. We used double and triple mutants involving cac1Delta and yeast repair gene mutations to show that deletion of the CAC1 gene increases the UV sensitivity of cells mutant in genes from each of the known DNA repair epistasis groups. For example, double mutants involving cac1Delta and excision repair gene deletions rad1Delta or rad14Delta showed increased UV sensitivity, as did double mutants involving cac1Delta and deletions of members of the RAD51 recombinational repair group. cac1Delta also increased the UV sensitivity of strains with defects in either the error-prone (rev3Delta) or error-free (pol30-46) branches of RAD6-mediated postreplicative DNA repair but did not substantially increase the sensitivity of strains carrying null mutations in the RAD6 or RAD18 genes. Deletion of CAC1 also increased the UV sensitivity and rate of UV-induced mutagenesis in rad5Delta mutants, as has been observed for mutants defective in error-free postreplicative repair. Together, these data suggest that CAF-I has a role in error-free postreplicative damage repair and may also have an auxiliary role in other repair mechanisms. Like the CAC genes, RAD6 is also required for gene silencing at telomeres. We find an increased loss of telomeric gene silencing in rad6Delta cac1Delta and rad18Delta cac1Delta double mutants, suggesting that CAF-I and multiple factors in the postreplicative repair pathway influence chromosome structure.
Full Text
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Cox B, Game J. Repair systems in Saccharomyces. Mutat Res. 1974 Aug;26(4):257–264. [Abstract] [Google Scholar]
- di Caprio L, Cox BS. DNA synthesis in UV-irradiated yeast. Mutat Res. 1981 Jun;82(1):69–85. [Abstract] [Google Scholar]
- Dohmen RJ, Madura K, Bartel B, Varshavsky A. The N-end rule is mediated by the UBC2(RAD6) ubiquitin-conjugating enzyme. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7351–7355. [Europe PMC free article] [Abstract] [Google Scholar]
- Enomoto S, Berman J. Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci. Genes Dev. 1998 Jan 15;12(2):219–232. [Europe PMC free article] [Abstract] [Google Scholar]
- Enomoto S, McCune-Zierath PD, Gerami-Nejad M, Sanders MA, Berman J. RLF2, a subunit of yeast chromatin assembly factor-I, is required for telomeric chromatin function in vivo. Genes Dev. 1997 Feb 1;11(3):358–370. [Abstract] [Google Scholar]
- Fan HY, Cheng KK, Klein HL. Mutations in the RNA polymerase II transcription machinery suppress the hyperrecombination mutant hpr1 delta of Saccharomyces cerevisiae. Genetics. 1996 Mar;142(3):749–759. [Europe PMC free article] [Abstract] [Google Scholar]
- Gaillard PH, Martini EM, Kaufman PD, Stillman B, Moustacchi E, Almouzni G. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell. 1996 Sep 20;86(6):887–896. [Abstract] [Google Scholar]
- Game JC. DNA double-strand breaks and the RAD50-RAD57 genes in Saccharomyces. Semin Cancer Biol. 1993 Apr;4(2):73–83. [Abstract] [Google Scholar]
- Aboussekhra A, Biggerstaff M, Shivji MK, Vilpo JA, Moncollin V, Podust VN, Protić M, Hübscher U, Egly JM, Wood RD. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell. 1995 Mar 24;80(6):859–868. [Abstract] [Google Scholar]
- Game JC, Cox BS. Synergistic interactions between rad mutations in yeast. Mutat Res. 1973 Oct;20(1):35–44. [Abstract] [Google Scholar]
- Game JC, Zamb TJ, Braun RJ, Resnick M, Roth RM. The Role of Radiation (rad) Genes in Meiotic Recombination in Yeast. Genetics. 1980 Jan;94(1):51–68. [Europe PMC free article] [Abstract] [Google Scholar]
- Ahne F, Jha B, Eckardt-Schupp F. The RAD5 gene product is involved in the avoidance of non-homologous end-joining of DNA double strand breaks in the yeast Saccharomyces cerevisiae. Nucleic Acids Res. 1997 Feb 15;25(4):743–749. [Europe PMC free article] [Abstract] [Google Scholar]
- Gottschling DE, Aparicio OM, Billington BL, Zakian VA. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell. 1990 Nov 16;63(4):751–762. [Abstract] [Google Scholar]
- Alani E, Cao L, Kleckner N. 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):541–545. [Europe PMC free article] [Abstract] [Google Scholar]
- Guzder SN, Sung P, Prakash L, Prakash S. Yeast DNA-repair gene RAD14 encodes a zinc metalloprotein with affinity for ultraviolet-damaged DNA. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5433–5437. [Europe PMC free article] [Abstract] [Google Scholar]
- Armstrong JD, Chadee DN, Kunz BA. Roles for the yeast RAD18 and RAD52 DNA repair genes in UV mutagenesis. Mutat Res. 1994 Nov;315(3):281–293. [Abstract] [Google Scholar]
- Huang H, Kahana A, Gottschling DE, Prakash L, Liebman SW. The ubiquitin-conjugating enzyme Rad6 (Ubc2) is required for silencing in Saccharomyces cerevisiae. Mol Cell Biol. 1997 Nov;17(11):6693–6699. [Europe PMC free article] [Abstract] [Google Scholar]
- Ayyagari R, Impellizzeri KJ, Yoder BL, Gary SL, Burgers PM. A mutational analysis of the yeast proliferating cell nuclear antigen indicates distinct roles in DNA replication and DNA repair. Mol Cell Biol. 1995 Aug;15(8):4420–4429. [Europe PMC free article] [Abstract] [Google Scholar]
- Jentsch S, McGrath JP, Varshavsky A. The yeast DNA repair gene RAD6 encodes a ubiquitin-conjugating enzyme. Nature. 1987 Sep 10;329(6135):131–134. [Abstract] [Google Scholar]
- Bailly V, Lamb J, Sung P, Prakash S, Prakash L. Specific complex formation between yeast RAD6 and RAD18 proteins: a potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites. Genes Dev. 1994 Apr 1;8(7):811–820. [Abstract] [Google Scholar]
- Johnson RE, Henderson ST, Petes TD, Prakash S, Bankmann M, Prakash L. Saccharomyces cerevisiae RAD5-encoded DNA repair protein contains DNA helicase and zinc-binding sequence motifs and affects the stability of simple repetitive sequences in the genome. Mol Cell Biol. 1992 Sep;12(9):3807–3818. [Europe PMC free article] [Abstract] [Google Scholar]
- Bailly V, Lauder S, Prakash S, Prakash L. Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J Biol Chem. 1997 Sep 12;272(37):23360–23365. [Abstract] [Google Scholar]
- Bailly V, Prakash S, Prakash L. Domains required for dimerization of yeast Rad6 ubiquitin-conjugating enzyme and Rad18 DNA binding protein. Mol Cell Biol. 1997 Aug;17(8):4536–4543. [Europe PMC free article] [Abstract] [Google Scholar]
- Kamakaka RT, Bulger M, Kaufman PD, Stillman B, Kadonaga JT. Postreplicative chromatin assembly by Drosophila and human chromatin assembly factor 1. Mol Cell Biol. 1996 Mar;16(3):810–817. [Europe PMC free article] [Abstract] [Google Scholar]
- Bankmann M, Prakash L, Prakash S. Yeast RAD14 and human xeroderma pigmentosum group A DNA-repair genes encode homologous proteins. Nature. 1992 Feb 6;355(6360):555–558. [Abstract] [Google Scholar]
- Kaufman PD, Kobayashi R, Stillman B. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev. 1997 Feb 1;11(3):345–357. [Abstract] [Google Scholar]
- Bardwell AJ, Bardwell L, Tomkinson AE, Friedberg EC. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science. 1994 Sep 30;265(5181):2082–2085. [Abstract] [Google Scholar]
- Kaufman PD, Cohen JL, Osley MA. Hir proteins are required for position-dependent gene silencing in Saccharomyces cerevisiae in the absence of chromatin assembly factor I. Mol Cell Biol. 1998 Aug;18(8):4793–4806. [Europe PMC free article] [Abstract] [Google Scholar]
- Boeke JD, Trueheart J, Natsoulis G, Fink GR. 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 1987;154:164–175. [Abstract] [Google Scholar]
- Broomfield S, Chow BL, Xiao W. MMS2, encoding a ubiquitin-conjugating-enzyme-like protein, is a member of the yeast error-free postreplication repair pathway. Proc Natl Acad Sci U S A. 1998 May 12;95(10):5678–5683. [Europe PMC free article] [Abstract] [Google Scholar]
- Lawrence CW, Christensen R. UV mutagenesis in radiation-sensitive strains of yeast. Genetics. 1976 Feb;82(2):207–232. [Europe PMC free article] [Abstract] [Google Scholar]
- Bryk M, Banerjee M, Murphy M, Knudsen KE, Garfinkel DJ, Curcio MJ. Transcriptional silencing of Ty1 elements in the RDN1 locus of yeast. Genes Dev. 1997 Jan 15;11(2):255–269. [Abstract] [Google Scholar]
- Li B, Lustig AJ. A novel mechanism for telomere size control in Saccharomyces cerevisiae. Genes Dev. 1996 Jun 1;10(11):1310–1326. [Abstract] [Google Scholar]
- Cassier-Chauvat C, Fabre F. A similar defect in UV-induced mutagenesis conferred by the rad6 and rad18 mutations of Saccharomyces cerevisiae. Mutat Res. 1991 May;254(3):247–253. [Abstract] [Google Scholar]
- Markvart MB, Ankerfelt D, Kirpekar F, Gulløv K. The yeast Rad6 protein: a mediator of homologous recombination across the scaffold attached region at the replication origin ARS1. Yeast. 1996 Nov;12(14):1427–1438. [Abstract] [Google Scholar]
- Singh J, Goel V, Klar AJ. A novel function of the DNA repair gene rhp6 in mating-type silencing by chromatin remodeling in fission yeast. Mol Cell Biol. 1998 Sep;18(9):5511–5522. [Europe PMC free article] [Abstract] [Google Scholar]
- McDonald JP, Levine AS, Woodgate R. The Saccharomyces cerevisiae RAD30 gene, a homologue of Escherichia coli dinB and umuC, is DNA damage inducible and functions in a novel error-free postreplication repair mechanism. Genetics. 1997 Dec;147(4):1557–1568. [Europe PMC free article] [Abstract] [Google Scholar]
- Smith S, Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell. 1989 Jul 14;58(1):15–25. [Abstract] [Google Scholar]
- Sung P, Prakash S, Prakash L. The RAD6 protein of Saccharomyces cerevisiae polyubiquitinates histones, and its acidic domain mediates this activity. Genes Dev. 1988 Nov;2(11):1476–1485. [Abstract] [Google Scholar]
- Moazed D, Johnson D. A deubiquitinating enzyme interacts with SIR4 and regulates silencing in S. cerevisiae. Cell. 1996 Aug 23;86(4):667–677. [Abstract] [Google Scholar]
- Sung P, Prakash S, Prakash L. Mutation of cysteine-88 in the Saccharomyces cerevisiae RAD6 protein abolishes its ubiquitin-conjugating activity and its various biological functions. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2695–2699. [Europe PMC free article] [Abstract] [Google Scholar]
- Monson EK, de Bruin D, Zakian VA. The yeast Cac1 protein is required for the stable inheritance of transcriptionally repressed chromatin at telomeres. Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13081–13086. [Europe PMC free article] [Abstract] [Google Scholar]
- Sung P, Prakash S, Prakash L. Stable ester conjugate between the Saccharomyces cerevisiae RAD6 protein and ubiquitin has no biological activity. J Mol Biol. 1991 Oct 5;221(3):745–749. [Abstract] [Google Scholar]
- Nelson JR, Lawrence CW, Hinkle DC. Thymine-thymine dimer bypass by yeast DNA polymerase zeta. Science. 1996 Jun 14;272(5268):1646–1649. [Abstract] [Google Scholar]
- Swerdlow PS, Schuster T, Finley D. A conserved sequence in histone H2A which is a ubiquitination site in higher eucaryotes is not required for growth in Saccharomyces cerevisiae. Mol Cell Biol. 1990 Sep;10(9):4905–4911. [Europe PMC free article] [Abstract] [Google Scholar]
- Picologlou S, Brown N, Liebman SW. Mutations in RAD6, a yeast gene encoding a ubiquitin-conjugating enzyme, stimulate retrotransposition. Mol Cell Biol. 1990 Mar;10(3):1017–1022. [Europe PMC free article] [Abstract] [Google Scholar]
- Thomas BJ, Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell. 1989 Feb 24;56(4):619–630. [Abstract] [Google Scholar]
- Prakash L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol Gen Genet. 1981;184(3):471–478. [Abstract] [Google Scholar]
- Torres-Ramos CA, Yoder BL, Burgers PM, Prakash S, Prakash L. Requirement of proliferating cell nuclear antigen in RAD6-dependent postreplicational DNA repair. Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9676–9681. [Europe PMC free article] [Abstract] [Google Scholar]
- Prelich G, Tan CK, Kostura M, Mathews MB, So AG, Downey KM, Stillman B. Functional identity of proliferating cell nuclear antigen and a DNA polymerase-delta auxiliary protein. Nature. 1987 Apr 2;326(6112):517–520. [Abstract] [Google Scholar]
- Watkins JF, Sung P, Prakash S, Prakash L. The extremely conserved amino terminus of RAD6 ubiquitin-conjugating enzyme is essential for amino-end rule-dependent protein degradation. Genes Dev. 1993 Feb;7(2):250–261. [Abstract] [Google Scholar]
- Roest HP, van Klaveren J, de Wit J, van Gurp CG, Koken MH, Vermey M, van Roijen JH, Hoogerbrugge JW, Vreeburg JT, Baarends WM, et al. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell. 1996 Sep 6;86(5):799–810. [Abstract] [Google Scholar]
- Weinert TA, Hartwell LH. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science. 1988 Jul 15;241(4863):317–322. [Abstract] [Google Scholar]
- Rundlett SE, Carmen AA, Kobayashi R, Bavykin S, Turner BM, Grunstein M. HDA1 and RPD3 are members of distinct yeast histone deacetylase complexes that regulate silencing and transcription. Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14503–14508. [Europe PMC free article] [Abstract] [Google Scholar]
- Weinert TA, Kiser GL, Hartwell LH. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 1994 Mar 15;8(6):652–665. [Abstract] [Google Scholar]
- Sancar A. Mechanisms of DNA excision repair. Science. 1994 Dec 23;266(5193):1954–1956. [Abstract] [Google Scholar]
Articles from Genetics are provided here courtesy of Oxford University Press
Full text links
Read article at publisher's site: https://doi.org/10.1093/genetics/151.2.485
Read article for free, from open access legal sources, via Unpaywall: https://academic.oup.com/genetics/article-pdf/151/2/485/35113024/genetics0485.pdf
Free to read at intl.genetics.org
http://intl.genetics.org/cgi/content/abstract/151/2/485
Subscription required at intl.genetics.org
http://intl.genetics.org/cgi/content/full/151/2/485
Subscription required at intl.genetics.org
http://intl.genetics.org/cgi/reprint/151/2/485.pdf
Citations & impact
Impact metrics
Citations of article over time
Article citations
RebL1 is required for macronuclear structure stability and gametogenesis in Tetrahymena thermophila.
Mar Life Sci Technol, 6(2):183-197, 26 Mar 2024
Cited by: 0 articles | PMID: 38827131 | PMCID: PMC11136921
CAF-1 and Rtt101p function within the replication-coupled chromatin assembly network to promote H4 K16ac, preventing ectopic silencing.
PLoS Genet, 16(12):e1009226, 07 Dec 2020
Cited by: 2 articles | PMID: 33284793 | PMCID: PMC7746308
Cac1 WHD and PIP domains have distinct roles in replisome progression and genomic stability.
Curr Genet, 67(1):129-139, 06 Oct 2020
Cited by: 6 articles | PMID: 33025160
A genome-wide screen identifies genes that suppress the accumulation of spontaneous mutations in young and aged yeast cells.
Aging Cell, 19(2):e13084, 18 Dec 2019
Cited by: 10 articles | PMID: 31854076 | PMCID: PMC6996960
Modulation of Gene Silencing by Cdc7p via H4 K16 Acetylation and Phosphorylation of Chromatin Assembly Factor CAF-1 in Saccharomyces cerevisiae.
Genetics, 211(4):1219-1237, 06 Feb 2019
Cited by: 4 articles | PMID: 30728156 | PMCID: PMC6456304
Go to all (50) article citations
Data
Similar Articles
To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.
Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I.
Genes Dev, 11(3):345-357, 01 Feb 1997
Cited by: 270 articles | PMID: 9030687
A role for histone H2B during repair of UV-induced DNA damage in Saccharomyces cerevisiae.
Genetics, 160(4):1375-1387, 01 Apr 2002
Cited by: 18 articles | PMID: 11973294 | PMCID: PMC1462056
Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci.
Genes Dev, 12(2):219-232, 01 Jan 1998
Cited by: 142 articles | PMID: 9436982 | PMCID: PMC316446
The structure and function of RAD6 and RAD18 DNA repair genes of Saccharomyces cerevisiae.
Genome, 31(2):597-600, 01 Jan 1989
Cited by: 15 articles | PMID: 2698834
Review