Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans.
Histone H3.3 variant dynamics in the germline of Caenorhabditis elegans.
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DOI:
10.1371/journal.pgen.0020097
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发表时间:
2006-06
期刊:
影响因子:
4.5
通讯作者:
Henikoff S
中科院分区:
文献类型:
--
作者:
Ooi SL;Priess JR;Henikoff S
Germline chromatin undergoes dramatic remodeling events involving histone variants during the life cycle of an organism. A universal histone variant, H3.3, is incorporated at sites of active transcription throughout the cell cycle. The presence of H3.3 in chromatin indicates histone turnover, which is the energy-dependent removal of preexisting histones and replacement with new histones. H3.3 is also incorporated during decondensation of the Drosophila sperm pronucleus, indicating a direct role in chromatin remodeling upon fertilization. Here we present a system to monitor histone turnover and chromatin remodeling during Caenorhabditis elegans development by following the developmental dynamics of H3.3. We generated worm strains expressing green fluorescent protein– or yellow fluorescent protein–fused histone H3.3 proteins, HIS-71 and HIS-72. We found that H3.3 is retained in mature sperm chromatin, raising the possibility that it transmits epigenetic information via the male germline. Upon fertilization, maternal H3.3 enters both male and female pronuclei and is incorporated into paternal chromatin, apparently before the onset of embryonic transcription, suggesting that H3.3 can be incorporated independent of transcription. In early embryos, H3.3 becomes specifically depleted from primordial germ cells. Strikingly, the X chromosome becomes deficient in H3.3 during gametogenesis, indicating a low level of histone turnover. These results raise the possibility that the asymmetry in histone turnover between the X chromosome and autosomes is established during gametogenesis. H3.3 patterns are similar to patterns of H3K4 methylation in the primordial germ cells and on the X chromosome during gametogenesis, suggesting that histone turnover and modification are coupled processes. Our demonstration of dynamic H3.3 incorporation in nondividing cells provides a mechanistic basis for chromatin changes during germ cell development. Germ cells carry genetic information from one generation to the next. They are converted to gametes during meiosis, which are then reprogrammed for development in the fertilized egg. Gamete production and developmental reprogramming involve dramatic changes in DNA packaging, but little is understood about how these changes are involved in resetting the developmental program for the whole organism. In spermatogenesis, DNA is stripped and repackaged into highly condensed chromatin. After fertilization, sperm DNA is again repackaged as it dramatically decondenses to fuse with the egg nucleus. These repackaging processes involve the four core histone proteins, which tightly wrap DNA into nucleosome particles. A universal variant form of histone 3, H3.3, is abundant in the germ cells of all plants and animals studied and has been shown to turn over at sites of active transcription in various somatic cells. The authors show that H3.3 displays dynamic turnover throughout germ cell development of the roundworm Caenorhabditis elegans. H3.3 incorporates during the first germline stem cell division, continues through meiosis, and ends up in sperm and eggs. Strikingly, H3.3 becomes depleted from primordial germ cells, and the meiotically silenced X chromosome is deficient in H3.3, which suggests that H3.3 dynamics during meiosis and reprogramming transmit epigenetic information.
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影响因子:
16
作者:
Reinke, V;Smith, HE;Kim, SK
通讯作者:
Kim, SK
DOI:
10.1073/pnas.0406325101
发表时间:
2004-11-23
影响因子:
11.1
作者:
Khalil, AM;Boyar, FZ;Driscoll, DJ
通讯作者:
Driscoll, DJ
影响因子:
2.7
作者:
Reuben, M;Lin, R
通讯作者:
Lin, R
影响因子:
30.8
作者:
Mito, Y;Henikoff, JG;Henikoff, S
通讯作者:
Henikoff, S
影响因子:
1.6
作者:
PALMER, DK;ODAY, K;MARGOLIS, RL
通讯作者:
MARGOLIS, RL