Extrachromosomal circular ribosomal DNA in the yeast Saccharomyces carlsbergensis

Meyerink, J.H.; Klootwijk, J.; Planta, R.J.; Vanderende, A; Vanbruggen, Efj

doi:10.1093/nar/7.1.69

Cited by 29 publications

(12 citation statements)

References 22 publications

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“…(iii) Strains monosomic for chromosome I have fewer rDNA units than diploids (11,12), and amplification of the rDNA back to the normal level occurs during vegetative growth (13)(14)(15). (iv) Circular extrachromosomal copies of rDNA, which are one or a few units in length, are found at low frequencies in vegetative yeast cells (16,17). Extrachromosomal circular rDNA molecules are found in many other systems, including Xenopus oocytes, where amplification of rDNA occurs by a rolling circle form of replication (18).…”

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confidence: 99%

Replication and meiotic transmission of yeast ribosomal RNA genes.

Brewer

Zakian

Fangman

1980

Proc. Natl. Acad. Sci. U.S.A.

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The yeast Saccharomyces cerevisiae has ap proximately 120 genes for the ribosomal RNAs (rDNA) which are organized in tandem within chromosomal DNA. These multiple-copy genes are homogeneous in sequence but can undergo changes in copy number and topology. To (ii) Electron microscopy of meiotic cells indicates that a portion of the parental nucleolus is excluded from the four haploid spores which independently generate new nucleoli (9, 10). A possible extrapolation from this observation is that rDNA units are discarded during meiosis and are replaced at a later time. (iii) Strains monosomic for chromosome I have fewer rDNA units than diploids (11,12), and amplification of the rDNA back to the normal level occurs during vegetative growth (13-15). (iv) Circular extrachromosomal copies of rDNA, which are one or a few units in length, are found at low frequencies in vegetative yeast cells (16,17). Extrachromosomal circular rDNA molecules are found in many other systems, including Xenopus oocytes, where amplification of rDNA occurs by a rolling circle form of replication (18). The circular rDNA molecules found in yeast may reflect a mode of replication that is responsible for the normal duplication of rDNA or for the amplification of rDNA units after meiosis. These observations imply a flexibility of number and topology for yeast rDNA, which may reflect important aspects of its replication and inheritance.The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in accordance with 18 U. S. C. §1734 solely to indicate this fact. 6739We have examined some features of rDNA metabolism in S. cerevisiae that are relevant to the replication and inheritance of the individual rDNA units. We find that all rDNA units are transmitted through meiosis to the haploid generation and that each unit serves as a template for one replication event in each S phase of the mitotic cell cycle.EXPERIMENTAL PROCEDURES Density Transfer Experiments. The strain used was a diploid uracil auxotroph, A364A D5 U-A+ (called D5). The 13C glucose/(15NH4)2S04 medium and the cell transfer and cell lysis procedures have been described (19). CsCl equilibrium centrifugation was carried out in a Spinco VTi65 rotor. Lysates (1.0 ml, about 3 X 108 cells) were added to 1.23 g of CsCl, and enough CsCl solution (1.23 g of CsCl per 1 ml of 10 mM Tris-HCI/100 mM EDTA, pH 8) was added to fill 5.3-ml VTi65 heat-seal tubes. Gradients were formed by centrifugation at 30,000 rpm for 60 hr and then collected by bottom puncture into microtiter plates with fractions of 0.11 ml. The distribution of total DNA in the gradients was determined by sampling each fraction for alkali-stable, acid-precipitable 3H cpm.Quantitative Spot Hybridization. The density distribution in CsCl gradients of the repeated rRNA genes was determined by hybridizing 32P-labeled, nick-translated cloned DNA fragments to samples of each gradient fraction that had been spotted on nitrocellulose sheets. A portion...

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confidence: 99%

Replication and meiotic transmission of yeast ribosomal RNA genes.

Brewer

Zakian

Fangman

1980

Proc. Natl. Acad. Sci. U.S.A.

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“…Circular monomers and head-to-tail multimers of the repeat unit of the genes coding for rRNA (rDNA) have been observed in approximately 3 to 5 copies per cell in several species of yeast (5,6,8,10,15,22). These circles may be derived by excision from the multiple tandem array of rDNA repeats present in the chromosome and, by analogy to the experiments we describe here, may integrate into the chromosome as well.…”

Section: Resultsmentioning

confidence: 60%

“…These circles may be derived by excision from the multiple tandem array of rDNA repeats present in the chromosome and, by analogy to the experiments we describe here, may integrate into the chromosome as well. Indeed, it has been suggested that integration and excision of circular rDNA molecules play a role in the regulation of rDNA gene dosage (15,22). However, no direct evidence for either excision or integration exists, nor has it been shown that these elements replicate autonomously.…”

Section: Resultsmentioning

confidence: 99%

Identification of autonomously replicating circular subtelomeric Y' elements in Saccharomyces cerevisiae.

Horowitz¹,

Haber²

1985

Mol. Cell. Biol.

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We marked a large number of yeast telomeres within their Y' regions by transforming strains with a fragment of Y' DNA into which the URA3 gene had been inserted. A few of the Ura+ transformants obtained were very unstable and were found to contain autonomously replicating URA3-marked circular Y' elements in high copy number. These marked extrachromosomal circles were capable of reintegrating into the chromosome at other telomeric locations. In contrast, most of the Ura+ transformants obtained were quite stable mitotically and were marked at bona fide chromosomal ends. These stable transformants gave rise to mitotically unstable URA3-marked circular Y' elements at a low frequency (up to 2.5%). The likelihood that such excisions and integrations represent a natural process in Saccharomyces cerevisiae is supported by our identification of putative Y' circles in untransformed strains. The transfer of Y' information among telomeres via a circular intermediate may be important for homogenizing the sequences at the ends of yeast chromosomes and for generating the frequent telomeric rearrangements that have been observed in S. cerevisiae.

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“…For example, using the budding yeast (Saccharomyces cerevisiae) as a model for elucidating signaling pathways that control life span, Sinclair and Guarente [5] showed, that increased activity of SIR2 (the yeast ortholog of mammalian SIRT1) suppresses the gradual accumulation of extra-chromosomal circular DNA (eccDNA). As its name implies, e cc D NA are circular molecules propagated extra-chromosomally from repetitive and non-repetitive genomic regions of various species including, humans [6][7][8][9].…”

Section: Introductionmentioning

confidence: 99%

A Novel Approach to Assess the Dynamics of Extra-Chromosomal Circular Ribosomal DNA in Human Cells

Leheste

Katz²,

Miceli³

et al. 2015

Gratis Journal of Biomedical Sciences

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Several nutrient-signaling pathways that extend life span have been described in model organisms. Thus, parallel and redundant signaling pathways that are similar across species might be subject to experimental manipulation. Here, we develop a PCR-based technique for testing the hypothesis that mitotic accumulation of extra-chromosomal ribosomal DNA circles might also determine life span in human cells. Using resveratrol, a phytochemical that counters age-related signs, we find treatment-dependent subcellular accumulations of extra-chromosomal 5S ribosomal DNA in human cell lines. These data suggest an association between DNA circles and intrinsic aging and demonstrate the utility of a PCR-based technique for studying the accumulation of dysfunctional molecules that promote senescence.

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Extrachromosomal circular ribosomal DNA in the yeast Saccharomyces carlsbergensis

Cited by 29 publications

References 22 publications

Replication and meiotic transmission of yeast ribosomal RNA genes.

Replication and meiotic transmission of yeast ribosomal RNA genes.

Identification of autonomously replicating circular subtelomeric Y' elements in Saccharomyces cerevisiae.

A Novel Approach to Assess the Dynamics of Extra-Chromosomal Circular Ribosomal DNA in Human Cells

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