DOI: 10.1093/genetics/152.4.1501. Genetic Control of Telomere Integrity in Schizosaccharomyces pombe: rad3+ and tel1+ Are Parts of Two Regulatory Networks Independent of the Downstream Protein Kinases chk1+ and cds1+

Genetic Control of Telomere Integrity in Schizosaccharomyces pombe: rad3+ and tel1+ Are Parts of Two Regulatory Networks Independent of the Downstream Protein Kinases chk1+ and cds1+

10.1093/genetics/152.4.1501

Crossref journal-article

Oxford University Press (OUP)

Genetics (286)

Abstract

Abstract The Schizosaccharomyces pombe checkpoint gene named rad3+ encodes an ATM-homologous protein kinase that shares a highly conserved motif with proteins involved in DNA metabolism. Previous studies have shown that Rad3 fulfills its function via the regulation of the Chk1 and Cds1 protein kinases. Here we describe a novel role for Rad3 in the control of telomere integrity. Mutations in the rad3+ gene alleviated telomeric silencing and produced shortened lengths in the telomere repeat tracts. Genetic analysis revealed that the other checkpoint rad mutations rad1, rad17, and rad26 belong to the same phenotypic class with rad3 with regard to control of the telomere length. Of these mutations, rad3 and rad26 have a drastic effect on telomere shortening. tel1+, another ATM homologue in S. pombe, carries out its telomere maintenance function in parallel with the checkpoint rad genes. Furthermore, either a single or double disruption of cds1+ and chk1+ caused no obvious changes in the telomeric DNA structure. Our results demonstrate a novel role of the S. pombe ATM homologues that is independent of chk1+ and cds1+.

Bibliography

Matsuura, A., Naito, T., & Ishikawa, F. (1999). Genetic Control of Telomere Integrity in Schizosaccharomyces pombe: rad3+ and tel1+ Are Parts of Two Regulatory Networks Independent of the Downstream Protein Kinases chk1+ and cds1+. Genetics, 152(4), 1501â1512.

Authors 3

Akira Matsuura (first)
Taku Naito (additional)
Fuyuki Ishikawa (additional)

References 75 Referenced 54

10.1002/j.1460-2075.1992.tb05179.x / EMBO J. / DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe by al-Khodairy (1992)
10.1091/mbc.5.2.147 / Mol. Biol. Cell / Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast by al-Khodairy (1994)
{'volume-title': 'Experiments with Fission Yeast: A Laboratory Course Manual', 'year': '1993', 'author': 'Alfa', 'key': '2022011809363592700_R3'} / Experiments with Fission Yeast: A Laboratory Course Manual by Alfa (1993)
10.1101/gad.9.2.218 / Genes Dev. / Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation by Allshire (1995)
10.1016/0378-1119(93)90552-E / Gene / TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility by Basi (1993)
10.1002/j.1460-2075.1996.tb01054.x / EMBO J. / The Schizosaccharomyces pombe rad3 checkpoint gene by Bentley (1996)
{'volume-title': 'Telomeres', 'year': '1995', 'author': 'Blackburn', 'key': '2022011809363592700_R7'} / Telomeres by Blackburn (1995)
10.1126/science.280.5365.909 / Science / Replication checkpoint enforced by kinases Cds1 and Chk1 by Boddy (1998)
10.1093/emboj/17.6.1819 / EMBO J. / Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing by Boulton (1998)
10.1073/pnas.91.12.5695 / Proc. Natl. Acad. Sci. USA / Effective amplification of long targets from cloned inserts and human genomic DNA by Cheng (1994)
10.1083/jcb.129.4.909 / J. Cell Biol. / The carboxy termini of Sir4 and Rap1 affect Sir3 localization: evidence for a multicomponent complex required for yeast telomeric silencing by Cockell (1995)
10.1016/0092-8674(90)90140-A / Cell / RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability by Conrad (1990)
10.1038/385744a0 / Nature / Regulation of telomere length and function by a Myb-domain protein in fission yeast by Cooper (1997)
10.1091/mbc.9.3.611 / Mol. Biol. Cell / Regulation of telomere length by checkpoint genes in Schizosaccharomyces pombe by Dahlen (1998)
{'key': '2022011809363592700_R15', 'first-page': '69', 'article-title': 'Telomere proteins', 'volume-title': 'Telomeres', 'author': 'Fang', 'year': '1995'} / Telomeres / Telomere proteins by Fang (1995)
10.1128/MCB.15.11.6128 / Mol. Cell. Biol. / Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint by Garvik (1995)
10.1083/jcb.134.6.1349 / J. Cell Biol. / The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae by Gotta (1996)
10.1016/0092-8674(90)90141-Z / Cell / Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription by Gottschling (1990)
10.1016/0092-8674(95)90479-4 / Cell / TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene by Greenwell (1995)
{'key': '2022011809363592700_R20', 'first-page': '35', 'article-title': 'Telomerase biochemistry and regulation', 'volume-title': 'Telomeres', 'author': 'Greider', 'year': '1995'} / Telomeres / Telomerase biochemistry and regulation by Greider (1995)
10.1002/j.1460-2075.1995.tb00269.x / EMBO J. / Fission yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins by Griffiths (1995)
10.1101/gad.6.5.801 / Genes Dev. / A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation by Hardy (1992)
10.1016/0092-8674(95)90512-X / Cell / Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast by Hecht (1995)
{'key': '2022011809363592700_R24', 'first-page': '11', 'article-title': 'Telomere DNA structure', 'volume-title': 'Telomeres', 'author': 'Henderson', 'year': '1995'} / Telomeres / Telomere DNA structure by Henderson (1995)
10.1016/S0168-9525(98)01511-X / Trends Genet. / Splitting the ATM: distinct repair and checkpoint defects in ataxia-telangiectasia by Jeggo (1998)
{'volume-title': 'Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual', 'year': '1994', 'author': 'Kaiser', 'key': '2022011809363592700_R26'} / Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual by Kaiser (1994)
10.1101/gad.10.19.2423 / Genes Dev. / The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes by Keegan (1996)
10.1128/MCB.19.2.1136 / Mol. Cell. Biol. / Role of a complex containing Rad17, Mec3, and Ddc1 in the yeast DNA damage checkpoint pathway by Kondo (1999)
10.1093/emboj/17.7.2055 / EMBO J. / Hus1p, a conserved fission yeast checkpoint protein, interacts with Rad1p and is phosphorylated in response to DNA damage by Kostrub (1998)
{'key': '2022011809363592700_R30', 'first-page': '5159', 'article-title': 'C-terminal truncation of RAP1 results in the deregulation of telomere size, stability, and function in Saccharomyces cerevisiae', 'volume': '12', 'author': 'Kyrion', 'year': '1992', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / C-terminal truncation of RAP1 results in the deregulation of telomere size, stability, and function in Saccharomyces cerevisiae by Kyrion (1992)
10.1093/genetics/144.4.1399 / Genetics / Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes by Lendvay (1996)
10.1073/pnas.93.24.13760 / Proc. Natl. Acad. Sci. USA / The Saccharomyces CDC13 protein is a single-strand TG1-3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo by Lin (1996)
10.1101/gad.12.3.382 / Genes Dev. / S-phase-specific activation of Cds1kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe by Lindsay (1998)
10.1126/science.276.5312.561 / Science / Reverse transcriptase motifs in the catalytic subunit of telomerase by Lingner (1997)
10.1093/genetics/138.4.1025 / Genetics / Mutational analysis defines a C-terminal tail domain of RAP1 essential for telomeric silencing in Saccharomyces cerevisiae by Liu (1994)
10.1016/0378-1119(94)90250-X / Gene / The Schizosaccharomyces pombe rad1 gene consists of three exons and the cDNA sequence is partially homologous to the Ustilago maydis REC1 cDNA by Long (1994)
10.1007/BF00422108 / Curr. Genet. / A yeast telomere binding activity binds to two related telomere sequence motifs and is indistinguishable from RAP1 by Longtine (1989)
10.1016/0092-8674(89)90132-3 / Cell / A mutant with a defect in telomere elongation leads to senescence in yeast by Lundblad (1989)
10.1073/pnas.83.5.1398 / Proc. Natl. Acad. Sci. USA / Identification of yeast mutants with altered telomere structure by Lustig (1986)
10.1126/science.275.5302.986 / Science / A protein-counting mechanism for telomere length regulation in yeast by Marcand (1997)
10.1093/emboj/17.24.7239 / EMBO J. / Analysis of Rad3 and Chk1 protein kinases defines different checkpoint responses by Martinho (1998)
10.1016/0378-1119(93)90551-D / Gene / Thiamine-repressible expression vectors pREP and pRIP for fission yeast by Maundrell (1993)
10.1038/ng0796-350 / Nat. Genet. / Accelerated telomere shortening in ataxia telangiectasia by Metcalfe (1996)
10.1101/gad.8.19.2257 / Genes Dev. / Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1 by Moretti (1994)
10.1016/0092-8674(95)90480-8 / Cell / TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1 by Morrow (1995)
10.1038/374817a0 / Nature / A kinase from fission yeast responsible for blocking mitosis in S phase by Murakami (1995)
10.1038/2517 / Nat. Genet. / Circular chromosome formation in a fission yeast mutant defective in two ATM-homologues by Naito (1998)
10.1002/j.1460-2075.1994.tb06691.x / EMBO J. / Telomere-associated chromosome breakage in fission yeast results in variegated expression of adjacent genes by Nimmo (1994)
10.1002/j.1460-2075.1989.tb08455.x / EMBO J. / Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their centromere by Niwa (1989)
10.1101/gad.12.8.1073 / Genes Dev. / The telomerase reverse transcriptase: components and regulation by Nugent (1998)
10.1126/science.274.5285.249 / Science / Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance by Nugent (1996)
10.1093/emboj/17.14.4199 / EMBO J. / Mec1p is essential for phosphorylation of the yeast DNA damage checkpoint protein Ddc1p, which physically interacts with Mec3p by Paciotti (1998)
10.1016/0092-8674(93)90388-7 / Cell / SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres by Palladino (1993)
{'key': '2022011809363592700_R54', 'first-page': '339', 'article-title': 'Drosophila telomeres: another way to end it all', 'volume-title': 'Telomeres', 'author': 'Pardue', 'year': '1995'} / Telomeres / Drosophila telomeres: another way to end it all by Pardue (1995)
10.1002/j.1460-2075.1992.tb05178.x / EMBO J. / Checkpoint controls in Schizosaccharomyces pombe: rad1 by Rowley (1992)
{'volume-title': 'Molecular Cloning, A Laboratory Manual', 'year': '1989', 'author': 'Sambrook', 'key': '2022011809363592700_R56'} / Molecular Cloning, A Laboratory Manual by Sambrook (1989)
10.1126/science.7792600 / Science / A single ataxia telangiectasia gene with a product similar to PI-3 kinase by Savitsky (1995)
10.1016/0168-9525(94)90058-2 / Trends Genet. / RAP1: a protean regulator in yeast by Shore (1994)
10.1126/science.7545955 / Science / TLC1: template RNA component of Saccharomyces cerevisiae telomerase by Singer (1994)
10.1038/sj.onc.1201449 / Oncogene / Influence of ATM function on telomere metabolism by Smilenov (1997)
Sugawara N , 1989DNA sequences at the telomeres of the fission yeast S. pombe. Ph.D. thesis. Harvard University, Cambridge, MA.
{'key': '2022011809363592700_R62', 'first-page': '3750', 'article-title': 'Cloning and analysis of a gene involved in DNA repair and recombination, the rad1 gene of Schizosaccharomyces pombe', 'volume': '10', 'author': 'Sunnerhagen', 'year': '1990', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / Cloning and analysis of a gene involved in DNA repair and recombination, the rad1 gene of Schizosaccharomyces pombe by Sunnerhagen (1990)
10.1073/pnas.88.17.7749 / Proc. Natl. Acad. Sci. USA / Separation of transcriptional activation and silencing functions of the RAP1-encoded repressor/activator protein 1: isolation of viable mutants affecting both silencing and telomere length by Sussel (1991)
10.1016/0022-2836(88)90051-4 / J. Mol. Biol. / DNA sequence analysis of the ade6 gene of Schizosaccharomyces pombe. Wild-type and mutant alleles including the recombination host spot allele ade6-M26 by Szankasi (1988)
10.1101/gad.13.2.152 / Genes Dev. / A role for ATR in the DNA damage-induced phosphorylation of p53 by Tibbetts (1999)
10.1128/MCB.17.6.3103 / Mol. Cell. Biol. / A novel mutant allele of Schizosaccharomyces pombe rad26 defective in monitoring S-phase progression to prevent premature mitosis by Uchiyama (1997)
10.1038/385740a0 / Nature / Control of telomere length by the human telomeric protein TRF1 by van Steensel (1997)
10.1093/emboj/16.19.6018 / EMBO J. / ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase by Vaziri (1997)
10.1101/gad.10.24.3094 / Genes Dev. / Est1 has the properties of a single-stranded telomere end-binding protein by Virta-Pearlman (1996)
10.1126/science.271.5247.353 / Science / rad-dependent response of the chk1-encoded protein kinase at the DNA damage checkpoint by Walworth (1996)
10.1038/363368a0 / Nature / Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2 by Walworth (1993)
10.1016/S0092-8674(00)81597-4 / Cell / DNA damage and checkpoint pathways: molecular anatomy and interactions with repair by Weinert (1998)
10.1101/gad.11.6.748 / Genes Dev. / A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae by Wotton (1997)
10.1093/nar/23.9.1454 / Nucleic Acids Res. / Protein-DNA interactions in soluble telosomes from Saccharomyces cerevisiae by Wright (1995)
{'key': '2022011809363592700_R75', 'first-page': '107', 'article-title': 'Saccharomyces telomeres: function, structure, and regulation', 'volume-title': 'Telomeres', 'author': 'Zakian', 'year': '1995'} / Telomeres / Saccharomyces telomeres: function, structure, and regulation by Zakian (1995)

Dates

Type	When
Created	4 years, 4 months ago (April 27, 2021, 11:06 p.m.)
Deposited	3 years, 7 months ago (Jan. 18, 2022, 5:25 a.m.)
Indexed	1 month, 3 weeks ago (July 2, 2025, 3:11 p.m.)
Issued	26 years ago (Aug. 1, 1999)
Published	26 years ago (Aug. 1, 1999)
Published Online	26 years ago (Aug. 1, 1999)
Published Print	26 years ago (Aug. 1, 1999)

Funders 0

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BibTeX

@article{Matsuura_1999, title={Genetic Control of Telomere Integrity in Schizosaccharomyces pombe: rad3+ and tel1+ Are Parts of Two Regulatory Networks Independent of the Downstream Protein Kinases chk1+ and cds1+}, volume={152}, ISSN={1943-2631}, url={http://dx.doi.org/10.1093/genetics/152.4.1501}, DOI={10.1093/genetics/152.4.1501}, number={4}, journal={Genetics}, publisher={Oxford University Press (OUP)}, author={Matsuura, Akira and Naito, Taku and Ishikawa, Fuyuki}, year={1999}, month=aug, pages={1501–1512} }

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  "abstract": "<jats:title>Abstract</jats:title>\n               <jats:p>The Schizosaccharomyces pombe checkpoint gene named rad3+ encodes an ATM-homologous protein kinase that shares a highly conserved motif with proteins involved in DNA metabolism. Previous studies have shown that Rad3 fulfills its function via the regulation of the Chk1 and Cds1 protein kinases. Here we describe a novel role for Rad3 in the control of telomere integrity. Mutations in the rad3+ gene alleviated telomeric silencing and produced shortened lengths in the telomere repeat tracts. Genetic analysis revealed that the other checkpoint rad mutations rad1, rad17, and rad26 belong to the same phenotypic class with rad3 with regard to control of the telomere length. Of these mutations, rad3 and rad26 have a drastic effect on telomere shortening. tel1+, another ATM homologue in S. pombe, carries out its telomere maintenance function in parallel with the checkpoint rad genes. Furthermore, either a single or double disruption of cds1+ and chk1+ caused no obvious changes in the telomeric DNA structure. Our results demonstrate a novel role of the S. pombe ATM homologues that is independent of chk1+ and cds1+.</jats:p>",
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      "first-page": "1343",
      "DOI": "10.1002/j.1460-2075.1992.tb05179.x",
      "article-title": "DNA repair mutants defining G2 checkpoint pathways in Schizosaccharomyces pombe",
      "volume": "11",
      "author": "al-Khodairy",
      "year": "1992",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R2",
      "doi-asserted-by": "crossref",
      "first-page": "147",
      "DOI": "10.1091/mbc.5.2.147",
      "article-title": "Identification and characterization of new elements involved in checkpoint and feedback controls in fission yeast",
      "volume": "5",
      "author": "al-Khodairy",
      "year": "1994",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "volume-title": "Experiments with Fission Yeast: A Laboratory Course Manual",
      "year": "1993",
      "author": "Alfa",
      "key": "2022011809363592700_R3"
    },
    {
      "key": "2022011809363592700_R4",
      "doi-asserted-by": "crossref",
      "first-page": "218",
      "DOI": "10.1101/gad.9.2.218",
      "article-title": "Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation",
      "volume": "9",
      "author": "Allshire",
      "year": "1995",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R5",
      "doi-asserted-by": "crossref",
      "first-page": "131",
      "DOI": "10.1016/0378-1119(93)90552-E",
      "article-title": "TATA box mutations in the Schizosaccharomyces pombe nmt1 promoter affect transcription efficiency but not the transcription start point or thiamine repressibility",
      "volume": "123",
      "author": "Basi",
      "year": "1993",
      "journal-title": "Gene"
    },
    {
      "key": "2022011809363592700_R6",
      "doi-asserted-by": "crossref",
      "first-page": "6641",
      "DOI": "10.1002/j.1460-2075.1996.tb01054.x",
      "article-title": "The Schizosaccharomyces pombe rad3 checkpoint gene",
      "volume": "15",
      "author": "Bentley",
      "year": "1996",
      "journal-title": "EMBO J."
    },
    {
      "volume-title": "Telomeres",
      "year": "1995",
      "author": "Blackburn",
      "key": "2022011809363592700_R7"
    },
    {
      "key": "2022011809363592700_R8",
      "doi-asserted-by": "crossref",
      "first-page": "909",
      "DOI": "10.1126/science.280.5365.909",
      "article-title": "Replication checkpoint enforced by kinases Cds1 and Chk1",
      "volume": "280",
      "author": "Boddy",
      "year": "1998",
      "journal-title": "Science"
    },
    {
      "key": "2022011809363592700_R9",
      "doi-asserted-by": "crossref",
      "first-page": "1819",
      "DOI": "10.1093/emboj/17.6.1819",
      "article-title": "Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing",
      "volume": "17",
      "author": "Boulton",
      "year": "1998",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R10",
      "doi-asserted-by": "crossref",
      "first-page": "5695",
      "DOI": "10.1073/pnas.91.12.5695",
      "article-title": "Effective amplification of long targets from cloned inserts and human genomic DNA",
      "volume": "91",
      "author": "Cheng",
      "year": "1994",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022011809363592700_R11",
      "doi-asserted-by": "crossref",
      "first-page": "909",
      "DOI": "10.1083/jcb.129.4.909",
      "article-title": "The carboxy termini of Sir4 and Rap1 affect Sir3 localization: evidence for a multicomponent complex required for yeast telomeric silencing",
      "volume": "129",
      "author": "Cockell",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2022011809363592700_R12",
      "doi-asserted-by": "crossref",
      "first-page": "739",
      "DOI": "10.1016/0092-8674(90)90140-A",
      "article-title": "RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability",
      "volume": "63",
      "author": "Conrad",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R13",
      "doi-asserted-by": "crossref",
      "first-page": "744",
      "DOI": "10.1038/385744a0",
      "article-title": "Regulation of telomere length and function by a Myb-domain protein in fission yeast",
      "volume": "385",
      "author": "Cooper",
      "year": "1997",
      "journal-title": "Nature"
    },
    {
      "key": "2022011809363592700_R14",
      "doi-asserted-by": "crossref",
      "first-page": "611",
      "DOI": "10.1091/mbc.9.3.611",
      "article-title": "Regulation of telomere length by checkpoint genes in Schizosaccharomyces pombe",
      "volume": "9",
      "author": "Dahlen",
      "year": "1998",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "key": "2022011809363592700_R15",
      "first-page": "69",
      "article-title": "Telomere proteins",
      "volume-title": "Telomeres",
      "author": "Fang",
      "year": "1995"
    },
    {
      "key": "2022011809363592700_R16",
      "doi-asserted-by": "crossref",
      "first-page": "6128",
      "DOI": "10.1128/MCB.15.11.6128",
      "article-title": "Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint",
      "volume": "15",
      "author": "Garvik",
      "year": "1995",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022011809363592700_R17",
      "doi-asserted-by": "crossref",
      "first-page": "1349",
      "DOI": "10.1083/jcb.134.6.1349",
      "article-title": "The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae",
      "volume": "134",
      "author": "Gotta",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2022011809363592700_R18",
      "doi-asserted-by": "crossref",
      "first-page": "751",
      "DOI": "10.1016/0092-8674(90)90141-Z",
      "article-title": "Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription",
      "volume": "63",
      "author": "Gottschling",
      "year": "1990",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R19",
      "doi-asserted-by": "crossref",
      "first-page": "823",
      "DOI": "10.1016/0092-8674(95)90479-4",
      "article-title": "TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene",
      "volume": "82",
      "author": "Greenwell",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R20",
      "first-page": "35",
      "article-title": "Telomerase biochemistry and regulation",
      "volume-title": "Telomeres",
      "author": "Greider",
      "year": "1995"
    },
    {
      "key": "2022011809363592700_R21",
      "doi-asserted-by": "crossref",
      "first-page": "5812",
      "DOI": "10.1002/j.1460-2075.1995.tb00269.x",
      "article-title": "Fission yeast rad17: a homologue of budding yeast RAD24 that shares regions of sequence similarity with DNA polymerase accessory proteins",
      "volume": "14",
      "author": "Griffiths",
      "year": "1995",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R22",
      "doi-asserted-by": "crossref",
      "first-page": "801",
      "DOI": "10.1101/gad.6.5.801",
      "article-title": "A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation",
      "volume": "6",
      "author": "Hardy",
      "year": "1992",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R23",
      "doi-asserted-by": "crossref",
      "first-page": "583",
      "DOI": "10.1016/0092-8674(95)90512-X",
      "article-title": "Histone H3 and H4 N-termini interact with SIR3 and SIR4 proteins: a molecular model for the formation of heterochromatin in yeast",
      "volume": "80",
      "author": "Hecht",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R24",
      "first-page": "11",
      "article-title": "Telomere DNA structure",
      "volume-title": "Telomeres",
      "author": "Henderson",
      "year": "1995"
    },
    {
      "key": "2022011809363592700_R25",
      "doi-asserted-by": "crossref",
      "first-page": "312",
      "DOI": "10.1016/S0168-9525(98)01511-X",
      "article-title": "Splitting the ATM: distinct repair and checkpoint defects in ataxia-telangiectasia",
      "volume": "14",
      "author": "Jeggo",
      "year": "1998",
      "journal-title": "Trends Genet."
    },
    {
      "volume-title": "Methods in Yeast Genetics: A Cold Spring Harbor Laboratory Course Manual",
      "year": "1994",
      "author": "Kaiser",
      "key": "2022011809363592700_R26"
    },
    {
      "key": "2022011809363592700_R27",
      "doi-asserted-by": "crossref",
      "first-page": "2423",
      "DOI": "10.1101/gad.10.19.2423",
      "article-title": "The Atr and Atm protein kinases associate with different sites along meiotically pairing chromosomes",
      "volume": "10",
      "author": "Keegan",
      "year": "1996",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R28",
      "doi-asserted-by": "crossref",
      "first-page": "1136",
      "DOI": "10.1128/MCB.19.2.1136",
      "article-title": "Role of a complex containing Rad17, Mec3, and Ddc1 in the yeast DNA damage checkpoint pathway",
      "volume": "19",
      "author": "Kondo",
      "year": "1999",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022011809363592700_R29",
      "doi-asserted-by": "crossref",
      "first-page": "2055",
      "DOI": "10.1093/emboj/17.7.2055",
      "article-title": "Hus1p, a conserved fission yeast checkpoint protein, interacts with Rad1p and is phosphorylated in response to DNA damage",
      "volume": "17",
      "author": "Kostrub",
      "year": "1998",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R30",
      "first-page": "5159",
      "article-title": "C-terminal truncation of RAP1 results in the deregulation of telomere size, stability, and function in Saccharomyces cerevisiae",
      "volume": "12",
      "author": "Kyrion",
      "year": "1992",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022011809363592700_R31",
      "doi-asserted-by": "crossref",
      "first-page": "1399",
      "DOI": "10.1093/genetics/144.4.1399",
      "article-title": "Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes",
      "volume": "144",
      "author": "Lendvay",
      "year": "1996",
      "journal-title": "Genetics"
    },
    {
      "key": "2022011809363592700_R32",
      "doi-asserted-by": "crossref",
      "first-page": "13760",
      "DOI": "10.1073/pnas.93.24.13760",
      "article-title": "The Saccharomyces CDC13 protein is a single-strand TG1-3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo",
      "volume": "93",
      "author": "Lin",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022011809363592700_R33",
      "doi-asserted-by": "crossref",
      "first-page": "382",
      "DOI": "10.1101/gad.12.3.382",
      "article-title": "S-phase-specific activation of Cds1kinase defines a subpathway of the checkpoint response in Schizosaccharomyces pombe",
      "volume": "12",
      "author": "Lindsay",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R34",
      "doi-asserted-by": "crossref",
      "first-page": "561",
      "DOI": "10.1126/science.276.5312.561",
      "article-title": "Reverse transcriptase motifs in the catalytic subunit of telomerase",
      "volume": "276",
      "author": "Lingner",
      "year": "1997",
      "journal-title": "Science"
    },
    {
      "key": "2022011809363592700_R35",
      "doi-asserted-by": "crossref",
      "first-page": "1025",
      "DOI": "10.1093/genetics/138.4.1025",
      "article-title": "Mutational analysis defines a C-terminal tail domain of RAP1 essential for telomeric silencing in Saccharomyces cerevisiae",
      "volume": "138",
      "author": "Liu",
      "year": "1994",
      "journal-title": "Genetics"
    },
    {
      "key": "2022011809363592700_R36",
      "doi-asserted-by": "crossref",
      "first-page": "155",
      "DOI": "10.1016/0378-1119(94)90250-X",
      "article-title": "The Schizosaccharomyces pombe rad1 gene consists of three exons and the cDNA sequence is partially homologous to the Ustilago maydis REC1 cDNA",
      "volume": "148",
      "author": "Long",
      "year": "1994",
      "journal-title": "Gene"
    },
    {
      "key": "2022011809363592700_R37",
      "doi-asserted-by": "crossref",
      "first-page": "225",
      "DOI": "10.1007/BF00422108",
      "article-title": "A yeast telomere binding activity binds to two related telomere sequence motifs and is indistinguishable from RAP1",
      "volume": "16",
      "author": "Longtine",
      "year": "1989",
      "journal-title": "Curr. Genet."
    },
    {
      "key": "2022011809363592700_R38",
      "doi-asserted-by": "crossref",
      "first-page": "633",
      "DOI": "10.1016/0092-8674(89)90132-3",
      "article-title": "A mutant with a defect in telomere elongation leads to senescence in yeast",
      "volume": "57",
      "author": "Lundblad",
      "year": "1989",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R39",
      "doi-asserted-by": "crossref",
      "first-page": "1398",
      "DOI": "10.1073/pnas.83.5.1398",
      "article-title": "Identification of yeast mutants with altered telomere structure",
      "volume": "83",
      "author": "Lustig",
      "year": "1986",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022011809363592700_R40",
      "doi-asserted-by": "crossref",
      "first-page": "986",
      "DOI": "10.1126/science.275.5302.986",
      "article-title": "A protein-counting mechanism for telomere length regulation in yeast",
      "volume": "275",
      "author": "Marcand",
      "year": "1997",
      "journal-title": "Science"
    },
    {
      "key": "2022011809363592700_R41",
      "doi-asserted-by": "crossref",
      "first-page": "7239",
      "DOI": "10.1093/emboj/17.24.7239",
      "article-title": "Analysis of Rad3 and Chk1 protein kinases defines different checkpoint responses",
      "volume": "17",
      "author": "Martinho",
      "year": "1998",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R42",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1016/0378-1119(93)90551-D",
      "article-title": "Thiamine-repressible expression vectors pREP and pRIP for fission yeast",
      "volume": "123",
      "author": "Maundrell",
      "year": "1993",
      "journal-title": "Gene"
    },
    {
      "key": "2022011809363592700_R43",
      "doi-asserted-by": "crossref",
      "first-page": "350",
      "DOI": "10.1038/ng0796-350",
      "article-title": "Accelerated telomere shortening in ataxia telangiectasia",
      "volume": "13",
      "author": "Metcalfe",
      "year": "1996",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "2022011809363592700_R44",
      "doi-asserted-by": "crossref",
      "first-page": "2257",
      "DOI": "10.1101/gad.8.19.2257",
      "article-title": "Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1",
      "volume": "8",
      "author": "Moretti",
      "year": "1994",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R45",
      "doi-asserted-by": "crossref",
      "first-page": "831",
      "DOI": "10.1016/0092-8674(95)90480-8",
      "article-title": "TEL1, an S. cerevisiae homolog of the human gene mutated in ataxia telangiectasia, is functionally related to the yeast checkpoint gene MEC1",
      "volume": "82",
      "author": "Morrow",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R46",
      "doi-asserted-by": "crossref",
      "first-page": "817",
      "DOI": "10.1038/374817a0",
      "article-title": "A kinase from fission yeast responsible for blocking mitosis in S phase",
      "volume": "374",
      "author": "Murakami",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2022011809363592700_R47",
      "doi-asserted-by": "crossref",
      "first-page": "203",
      "DOI": "10.1038/2517",
      "article-title": "Circular chromosome formation in a fission yeast mutant defective in two ATM-homologues",
      "volume": "20",
      "author": "Naito",
      "year": "1998",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "2022011809363592700_R48",
      "doi-asserted-by": "crossref",
      "first-page": "3801",
      "DOI": "10.1002/j.1460-2075.1994.tb06691.x",
      "article-title": "Telomere-associated chromosome breakage in fission yeast results in variegated expression of adjacent genes",
      "volume": "13",
      "author": "Nimmo",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R49",
      "doi-asserted-by": "crossref",
      "first-page": "3045",
      "DOI": "10.1002/j.1460-2075.1989.tb08455.x",
      "article-title": "Characterization of Schizosaccharomyces pombe minichromosome deletion derivatives and a functional allocation of their centromere",
      "volume": "8",
      "author": "Niwa",
      "year": "1989",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R50",
      "doi-asserted-by": "crossref",
      "first-page": "1073",
      "DOI": "10.1101/gad.12.8.1073",
      "article-title": "The telomerase reverse transcriptase: components and regulation",
      "volume": "12",
      "author": "Nugent",
      "year": "1998",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R51",
      "doi-asserted-by": "crossref",
      "first-page": "249",
      "DOI": "10.1126/science.274.5285.249",
      "article-title": "Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance",
      "volume": "274",
      "author": "Nugent",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "2022011809363592700_R52",
      "doi-asserted-by": "crossref",
      "first-page": "4199",
      "DOI": "10.1093/emboj/17.14.4199",
      "article-title": "Mec1p is essential for phosphorylation of the yeast DNA damage checkpoint protein Ddc1p, which physically interacts with Mec3p",
      "volume": "17",
      "author": "Paciotti",
      "year": "1998",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R53",
      "doi-asserted-by": "crossref",
      "first-page": "543",
      "DOI": "10.1016/0092-8674(93)90388-7",
      "article-title": "SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres",
      "volume": "75",
      "author": "Palladino",
      "year": "1993",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R54",
      "first-page": "339",
      "article-title": "Drosophila telomeres: another way to end it all",
      "volume-title": "Telomeres",
      "author": "Pardue",
      "year": "1995"
    },
    {
      "key": "2022011809363592700_R55",
      "doi-asserted-by": "crossref",
      "first-page": "1335",
      "DOI": "10.1002/j.1460-2075.1992.tb05178.x",
      "article-title": "Checkpoint controls in Schizosaccharomyces pombe: rad1",
      "volume": "11",
      "author": "Rowley",
      "year": "1992",
      "journal-title": "EMBO J."
    },
    {
      "volume-title": "Molecular Cloning, A Laboratory Manual",
      "year": "1989",
      "author": "Sambrook",
      "key": "2022011809363592700_R56"
    },
    {
      "key": "2022011809363592700_R57",
      "doi-asserted-by": "crossref",
      "first-page": "1749",
      "DOI": "10.1126/science.7792600",
      "article-title": "A single ataxia telangiectasia gene with a product similar to PI-3 kinase",
      "volume": "268",
      "author": "Savitsky",
      "year": "1995",
      "journal-title": "Science"
    },
    {
      "key": "2022011809363592700_R58",
      "doi-asserted-by": "crossref",
      "first-page": "408",
      "DOI": "10.1016/0168-9525(94)90058-2",
      "article-title": "RAP1: a protean regulator in yeast",
      "volume": "10",
      "author": "Shore",
      "year": "1994",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2022011809363592700_R59",
      "doi-asserted-by": "crossref",
      "first-page": "404",
      "DOI": "10.1126/science.7545955",
      "article-title": "TLC1: template RNA component of Saccharomyces cerevisiae telomerase",
      "volume": "266",
      "author": "Singer",
      "year": "1994",
      "journal-title": "Science"
    },
    {
      "key": "2022011809363592700_R60",
      "doi-asserted-by": "crossref",
      "first-page": "2659",
      "DOI": "10.1038/sj.onc.1201449",
      "article-title": "Influence of ATM function on telomere metabolism",
      "volume": "15",
      "author": "Smilenov",
      "year": "1997",
      "journal-title": "Oncogene"
    },
    {
      "key": "2022011809363592700_R61",
      "unstructured": "Sugawara\n              N\n            \n          , 1989DNA sequences at the telomeres of the fission yeast S. pombe. Ph.D. thesis. Harvard University, Cambridge, MA."
    },
    {
      "key": "2022011809363592700_R62",
      "first-page": "3750",
      "article-title": "Cloning and analysis of a gene involved in DNA repair and recombination, the rad1 gene of Schizosaccharomyces pombe",
      "volume": "10",
      "author": "Sunnerhagen",
      "year": "1990",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022011809363592700_R63",
      "doi-asserted-by": "crossref",
      "first-page": "7749",
      "DOI": "10.1073/pnas.88.17.7749",
      "article-title": "Separation of transcriptional activation and silencing functions of the RAP1-encoded repressor/activator protein 1: isolation of viable mutants affecting both silencing and telomere length",
      "volume": "88",
      "author": "Sussel",
      "year": "1991",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2022011809363592700_R64",
      "doi-asserted-by": "crossref",
      "first-page": "917",
      "DOI": "10.1016/0022-2836(88)90051-4",
      "article-title": "DNA sequence analysis of the ade6 gene of Schizosaccharomyces pombe. Wild-type and mutant alleles including the recombination host spot allele ade6-M26",
      "volume": "204",
      "author": "Szankasi",
      "year": "1988",
      "journal-title": "J. Mol. Biol."
    },
    {
      "key": "2022011809363592700_R65",
      "doi-asserted-by": "crossref",
      "first-page": "152",
      "DOI": "10.1101/gad.13.2.152",
      "article-title": "A role for ATR in the DNA damage-induced phosphorylation of p53",
      "volume": "13",
      "author": "Tibbetts",
      "year": "1999",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R66",
      "doi-asserted-by": "crossref",
      "first-page": "3103",
      "DOI": "10.1128/MCB.17.6.3103",
      "article-title": "A novel mutant allele of Schizosaccharomyces pombe rad26 defective in monitoring S-phase progression to prevent premature mitosis",
      "volume": "17",
      "author": "Uchiyama",
      "year": "1997",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2022011809363592700_R67",
      "doi-asserted-by": "crossref",
      "first-page": "740",
      "DOI": "10.1038/385740a0",
      "article-title": "Control of telomere length by the human telomeric protein TRF1",
      "volume": "385",
      "author": "van Steensel",
      "year": "1997",
      "journal-title": "Nature"
    },
    {
      "key": "2022011809363592700_R68",
      "doi-asserted-by": "crossref",
      "first-page": "6018",
      "DOI": "10.1093/emboj/16.19.6018",
      "article-title": "ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase",
      "volume": "16",
      "author": "Vaziri",
      "year": "1997",
      "journal-title": "EMBO J."
    },
    {
      "key": "2022011809363592700_R69",
      "doi-asserted-by": "crossref",
      "first-page": "3094",
      "DOI": "10.1101/gad.10.24.3094",
      "article-title": "Est1 has the properties of a single-stranded telomere end-binding protein",
      "volume": "10",
      "author": "Virta-Pearlman",
      "year": "1996",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R70",
      "doi-asserted-by": "crossref",
      "first-page": "353",
      "DOI": "10.1126/science.271.5247.353",
      "article-title": "rad-dependent response of the chk1-encoded protein kinase at the DNA damage checkpoint",
      "volume": "271",
      "author": "Walworth",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "2022011809363592700_R71",
      "doi-asserted-by": "crossref",
      "first-page": "368",
      "DOI": "10.1038/363368a0",
      "article-title": "Fission yeast chk1 protein kinase links the rad checkpoint pathway to cdc2",
      "volume": "363",
      "author": "Walworth",
      "year": "1993",
      "journal-title": "Nature"
    },
    {
      "key": "2022011809363592700_R72",
      "doi-asserted-by": "crossref",
      "first-page": "555",
      "DOI": "10.1016/S0092-8674(00)81597-4",
      "article-title": "DNA damage and checkpoint pathways: molecular anatomy and interactions with repair",
      "volume": "94",
      "author": "Weinert",
      "year": "1998",
      "journal-title": "Cell"
    },
    {
      "key": "2022011809363592700_R73",
      "doi-asserted-by": "crossref",
      "first-page": "748",
      "DOI": "10.1101/gad.11.6.748",
      "article-title": "A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae",
      "volume": "11",
      "author": "Wotton",
      "year": "1997",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2022011809363592700_R74",
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