Paternal DNA strands segregate to both trophectoderm and inner cell mass of the developing mouse embryo.

Ito, Kenichi; McGhee, James D.; Schultz, Gilbert A.

doi:10.1101/gad.2.8.929

Cited by 21 publications

(16 citation statements)

References 21 publications

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“…Both the DSB and the ssDNA tail are obligatory intermediates in meiotic recombination (9,38). The DNA of all spermatogenic cell types was substituted with BrdUrd by feeding male mice with BrdUrd containing water (25,26). After denaturation of testicular cell preparations, the majority of premeiotic, meiotic, and postmeiotic cells showed strong overall BrdUrd labeling (Fig.…”

Section: Resultsmentioning

confidence: 99%

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Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage

Raderschall

Golub

Haaf

1999

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

315

312

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A sensitive and rapid in situ method was developed to visualize sites of single-stranded (ss) DNA in cultured cells and in experimental test animals. Anti-bromodeoxyuridine antibody recognizes the halogenated base analog incorporated into chromosomal DNA only when substituted DNA is in the single strand form. After treatment of cells with DNA-damaging agents or ␥ irradiation, ssDNA molecules form nuclear foci in a dose-dependent manner within 60 min. The mammalian recombination protein Rad51 and the replication protein A then accumulate at sites of ssDNA and form foci, suggesting that these are sites of recombinational DNA repair.Eukaryotic cells are endowed with multiple pathways to repair damaged DNA. One of the major pathways is nucleotide excision repair, which can remove a broad range of DNA lesions. Nucleotide excision repair excises oligonucleotides of 25-32 bp including the damaged DNA, filling in the single-stranded (ss) DNA gap (1). This process is very efficient and usually repairs most DNA lesions before the damaged region is replicated. However, if the replication fork meets unrepaired DNA damage, breaks may occur in one or both strands of the nascent DNA (2). Single-and double-strand breaks (DSBs) may also arise as a direct effect of many DNA-damaging agents such as ionizing radiation. Singlestrand breaks are efficiently repaired and do not represent a threat for cell survival. In contrast, DSBs are potentially lethal. DSBs may be repaired either by direct end-joining of the broken ends in a process that is mediated by the Mre11-Rad50 complex or by homologous recombination (3). In yeast, DSBs are mainly repaired by homologous recombination; genes of the Rad52 epistasis group are largely responsible for this pathway. Although mammalian cells are presumed to repair DSBs predominantly by nonhomologous end-joining (4, 5), accumulating experimental evidence suggests that homologous recombination also plays an essential role in mammalian DSB repair (6-8).DSB repair by homologous recombination starts with 5Ј to 3Ј-exonucleolytic digestion of one DNA strand, which leads to the formation of 3Ј-overhanging ssDNA tails. In Escherichia coli, this ssDNA associates with the RecA recombination enzyme, forming the ssDNA-RecA filament. This RecA-nucleoprotein filament promotes homology search by the single DNA strand and initiates the exchange between ssDNA and homologous double-stranded (ds) DNA (3, 9). Rad51 is a structural and functional eukaryotic homolog of E. coli RecA (10, 11). Similar to RecA, both yeast and mammalian Rad51 proteins form nucleoprotein filaments on ssDNA, mediating homologous pairing and strand-exchange reactions between ssDNA and homologous dsDNA (12-15). Homologous pairing and DNA-strand exchange mediated by Rad51 are facilitated in vitro by the ssDNA-binding protein, RPA (12,(16)(17)(18).In normal, cultured human cells, the HsRad51 protein is detected in multiple discrete foci in the nucleoplasm of a low number of cells by immunofluorescent antibodies. After DNA damage the percent...

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Section: Resultsmentioning

confidence: 99%

“…mately 5 weeks. To label DNA of all spermatogenic cell types with BrdUrd, male mice were supplied with drinking water containing 0.5 mg͞ml BrdUrd continuously for more than 6 weeks (25,26). Immediately after the BrdUrd-treated mouse was sacrificed, the testes and the cauda epididymis were removed and placed in PBS.…”

Section: Methodsmentioning

confidence: 99%

Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage

Raderschall

Golub

Haaf

1999

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

315

312

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“…Ito and colleagues treated male mice with the halogenated thymidine analog bromo-deoxyuridine (BrdU) in order to label sperm DNA (Ito et al, 1988). Mating with untreated females allowed them to distinguish parental genomes in the resulting embryos.…”

Section: Introductionmentioning

confidence: 99%

Live imaging reveals spatial separation of parental chromatin until the four-cell stage in Caenorhabditis elegans embryos

Bolková

Lanctôt²

2016

Int. J. Dev. Biol.

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The parental genomes are initially spatially separated in each pronucleus after fertilization. Here we have used green-to-red photoconversion of Dendra2-H2B-labeled pronuclei to distinguish maternal and paternal chromatin domains and to track their spatial distribution in living Caenorhabditis elegans embryos starting shortly after fertilization. Intermingling of the parental chromatin did not occur until after the division of the AB and P1 blastomeres, at the 4-cell stage. Unexpectedly, we observed that the intermingling of chromatin did not take place during mitosis or during chromatin decondensation, but rather ~3-5 minutes into the cell cycle. Furthermore, unlike what has been observed in mammalian cells, the relative spatial positioning of chromatin domains remained largely unchanged during prometaphase in the early C. elegans embryo. Live imaging of photoconverted chromatin also allowed us to detect a reproducible 180° rotation of the nuclei during cytokinesis of the one-cell embryo. Imaging of fluorescently-labeled P granules and polar bodies showed that the entire embryo rotates during the first cell division. To our knowledge, we report here the first live observation of the initial separation and subsequent mixing of parental chromatin domains during embryogenesis.

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“…For example, LRCs could not be demonstrated during Caenorhabditis elegans development following BrdU labelling of sperm or oocyte DNA (23) . Furthermore, when the fate of labelled paternal DNA strands was followed during early cell divisions of mouse embryogenesis, there was no evidence to suggest that the paternal DNA strands segregated together and segregation appeared to follow a random pattern (24) .…”

Section: Evidence and Arguments Against The Ishmentioning

confidence: 98%

The immortal strand hypothesis: still non-randomly segregating opinions

Wakeman

Hmadcha

Soria

et al. 2012

BioMolecular Concepts

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Cairns first suggested a mechanism for protecting the genomes of stem cells (SCs) from replicative errors some 40 years ago when he proposed the immortal strand hypothesis, which argued for the inheritance of a so-called immortal strand by an SC following asymmetric SC divisions. To date, the existence of immortal strands remains contentious with published evidence arguing in favour of and against the retention of an immortal strand by asymmetrically dividing SCs. The conflicting evidence is derived from a diverse array of studies on adult SC types and is predominantly based on following the fate of labelled DNA strands during asymmetric cell division events. Here, we review current data, highlighting limitations of such labelling techniques, and suggest how interpretation of such data may be improved in the future.

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Paternal DNA strands segregate to both trophectoderm and inner cell mass of the developing mouse embryo.

Cited by 21 publications

References 21 publications

Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage

Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage

Live imaging reveals spatial separation of parental chromatin until the four-cell stage in Caenorhabditis elegans embryos

The immortal strand hypothesis: still non-randomly segregating opinions

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