Asymmetric Division of
            <i>Drosophila</i>
            Male Germline Stem Cell Shows Asymmetric Histone Distribution

Tran, Vuong; Lim, Cindy; Xie, Jing; Chen, Xin

doi:10.1126/science.1226028

Cited by 168 publications

(212 citation statements)

References 31 publications

(22 reference statements)

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“…Further investigation is required to test these ideas. Intriguingly, a similar phenomenon was recently reported in the Drosophila male germ line (48,49), where the germ line stem cells (GSCs) undergo asymmetric cell division to generate one GSC and one differentiating daughter cell. Chen and coworkers (48) discovered that old/pre-existing canonical histone H3 but not H3.3 were selectively segregated to the daughter GSC.…”

Section: Mass Spectrometry Provides a Powerful Tool To Study Dynamicsmentioning

confidence: 91%

“…They further showed that H3T3ph was required for the asymmetric inheritance of H3, and they suggested it was required in a specific time window (prophase to metaphase) (49). The asymmetric cell division is only limited to Drosophila GSCs and is not seen in surrounding somatic tissues, so is the asymmetric distribution of H3T3ph and directional inheritance of histone H3 (48,49). However, the observations are highly similar to ours in this study that mitotic histone ph mark(s) is(are) enriched on the old histones in early mitosis, suggesting the underlying mechanism is conserved between Drosophila and humans.…”

Section: Mass Spectrometry Provides a Powerful Tool To Study Dynamicsmentioning

confidence: 99%

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Preferential Phosphorylation on Old Histones during Early Mitosis in Human Cells

Lin

Yuan

Han

et al. 2016

Journal of Biological Chemistry

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How histone post-translational modifications (PTMs) are inherited through the cell cycle remains poorly understood. Canonical histones are made in the S phase of the cell cycle. Combining mass spectrometry-based technologies and stable isotope labeling by amino acids in cell culture, we question the distribution of multiple histone PTMs on old versus new histones in synchronized human cells. We show that histone PTMs can be grouped into three categories according to their distributions. Most lysine mono-methylation and acetylation PTMs are either symmetrically distributed on old and new histones or are enriched on new histones. In contrast, most di-and tri-methylation PTMs are enriched on old histones, suggesting that the inheritance of different PTMs is regulated distinctly. Intriguingly, old and new histones are distinct in their phosphorylation status during early mitosis in the following three human cell types: HeLa, 293T, and human foreskin fibroblast cells. The mitotic hallmark H3S10ph is predominantly associated with old H3 at early mitosis and becomes symmetric with the progression of mitosis. This same distribution was observed with other mitotic phosphorylation marks, including H3T3/T6ph, H3.1/ 2S28ph, and H1.4S26ph but not S28/S31ph on the H3 variant H3.3. Although H3S10ph often associates with the neighboring Lys-9 di-or tri-methylations, they are not required for the asymmetric distribution of Ser-10 phosphorylation on the same H3 tail. Inhibition of the kinase Aurora B does not change the distribution despite significant reduction of H3S10ph levels. However, K9me2 abundance on the new H3 is significantly reduced after Aurora B inhibition, suggesting a cross-talk between H3S10ph and H3K9me2.In eukaryotes, histone proteins facilitate the packaging of DNA molecules. The DNA double helix wraps around histone octamers to form nucleosomes. A histone octamer contains two copies of each core histone H3, H4, H2A, and H2B. A 5th histone, histone H1, is associated with the linker DNA which lies between the nucleosomes. Canonical histone proteins are cell cycle-dependent and are produced in S phase (1, 2), whereas cell cycle-independent histone variants (e.g. H3.3) are synthesized throughout the cell cycle (3). Histone proteins carry numerous post-translational modifications (PTMs) 3 that are involved in multiple functions such as epigenetic regulation of transcription, DNA damage repair, and cell cycle progression (4, 5). To maintain lineage identity and to guide proper transcription, cells must replicate PTMs from old histones onto new histones at each cell division. Major efforts have been devoted to understanding how histones themselves are transmitted through the DNA replication fork in S phase (6). In principle, the newly deposited nucleosomes could contain entirely old or newly synthesized histone proteins, or a mixture of both. Accumulating evidence suggests that most H3/H4 tetramers remain intact, with the exception of some H3.3/H4 tetramers, indicating that nucleosomes should contain either new or ...

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Section: Mass Spectrometry Provides a Powerful Tool To Study Dynamicsmentioning

confidence: 91%

Section: Mass Spectrometry Provides a Powerful Tool To Study Dynamicsmentioning

confidence: 99%

Preferential Phosphorylation on Old Histones during Early Mitosis in Human Cells

Lin

Yuan

Han

et al. 2016

Journal of Biological Chemistry

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“…By labeling the budding yeast Saccharomyces cerevisiae genome for one cell cycle by incorporating 5-bromo-deoxyuridine nucleotide analog, then analyzing chromosomes of mother cells separated from those of daughter cells, it was recently reported that there is no mother-daughter bias in segregation of specific strands of any chromosome (Keyes et al 2102). In contrast, it was recently reported that preexisting histones are selectively retained in Drosophila male germline stem cells, while newly synthesized histones are enriched in the differentiating daughter cell (Tran et al 2012). Thus, an active area of research is aimed at determining the strand segregation pattern and exploring their significance in biology at large.…”

Section: Discussionmentioning

confidence: 99%

Unbiased segregation of fission yeast chromosome 2 strands to daughter cells

Klar

Bonaduce

2013

Chromosome Res

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The base complementarity feature (Watson and Crick in Nature 171(4356): [737][738] 1953) and the rule of semi-conservative mode of DNA replication (Messelson and Stahl in Proc Natl Acad Sci U S A 44: [671][672][673][674][675][676][677][678][679][680][681][682] 1958) dictate that two identical replicas of the parental chromosome are produced during replication. In principle, the inherent strand sequence differences could generate nonequivalent daughter chromosome replicas if one of the two strands were epigenetically imprinted during replication to effect silencing/expression of developmentally important genes. Indeed, inheritance of such a strand-and sitespecific imprint confers developmental asymmetry to fission yeast sister cells by a phenomenon called mating/cell-type switching. Curiously, location of DNA strands with respect to each other at the centromere is fixed, and as a result, their selected segregation to specific sister chromatid copies occurs in eukaryotic cells. The yeast system provides a unique opportunity to determine the significance of such biased strand distribution to sister chromatids. We determined whether the cylindrical-shaped yeast cell distributes the specific chromosomal strand to the same cellular pole in successive cycles of cell division. By observing the pattern of recurrent mating-type switching in progenies of individual cells by microscopic analyses, we found that chromosome 2 strands are distributed by the random mode in successive cell divisions. We also exploited unusual "hotspot" recombination features of this system to investigate whether there is selective segregation of strands such that oldest Watsoncontaining strands co-segregate in the diploid cell at mitosis. Our data suggests that chromosome 2 strands are segregated independently to those of the homologous chromosome.

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“…In addition, parental nucleosomes have been shown to be located within B400 bp of their original positions after the completion of the cell cycle 7,35,39 , close to the most probable loop size. DNA loop formation may also be facilitated by the configuration 40 of nascent dsDNA strands as they emerge from the replisome, which would contribute to the partitioning 19,41 of nucleosomes between the two daughter strands by coordinating nucleosome transfer with DNA synthesis 42 .…”

Section: Discussionmentioning

confidence: 99%

DNA Looping Mediates Nucleosome Transfer

Brennan

Forties²,

Patel

et al. 2017

Biophysical Journal

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Proper cell function requires preservation of the spatial organization of chromatin modifications. Maintenance of this epigenetic landscape necessitates the transfer of parental nucleosomes to newly replicated DNA, a process that is stringently regulated and intrinsically linked to replication fork dynamics. This creates a formidable setting from which to isolate the central mechanism of transfer. Here we utilized a minimal experimental system to track the fate of a single nucleosome following its displacement, and examined whether DNA mechanics itself, in the absence of any chaperones or assembly factors, may serve as a platform for the transfer process. We found that the nucleosome is passively transferred to available dsDNA as predicted by a simple physical model of DNA loop formation. These results demonstrate a fundamental role for DNA mechanics in mediating nucleosome transfer and preserving epigenetic integrity during replication.

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Asymmetric Division of Drosophila Male Germline Stem Cell Shows Asymmetric Histone Distribution

Cited by 168 publications

References 31 publications

Preferential Phosphorylation on Old Histones during Early Mitosis in Human Cells

Preferential Phosphorylation on Old Histones during Early Mitosis in Human Cells

Unbiased segregation of fission yeast chromosome 2 strands to daughter cells

DNA Looping Mediates Nucleosome Transfer

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