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
Henikoff S
中科院分区:
生物学2区
文献类型:
--
作者:
Ooi SL;Priess JR;Henikoff S

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在生物体的生命周期中,生殖细胞染色质经历了涉及组蛋白变体的戏剧性重塑事件。一种通用的组蛋白变体H3.3在整个细胞周期的活性转录位点被掺入。H3.3在染色质中的存在表明组蛋白更新,这是能量依赖性地去除先前存在的组蛋白并替换为新的组蛋白。在果蝇精子原核的去凝聚过程中,H3.3也被掺入,表明在受精后的染色质重塑中起直接作用。在这里,我们提出了一个系统来监测组蛋白营业额和染色质重塑秀丽隐杆线虫的发展过程中,以下的发展动态H3.3。我们产生了表达绿色荧光蛋白或黄色荧光蛋白融合的组蛋白H3.3蛋白、HIS-71和HIS-72的蠕虫菌株。我们发现H3.3保留在成熟精子染色质中,这增加了它通过男性生殖系传递表观遗传信息的可能性。受精后,母体H3.3进入雄性和雌性原核,并被纳入父亲的染色质,显然在胚胎转录开始之前,这表明H3.3可以独立于转录。在早期胚胎中,H3.3从原始生殖细胞中特异性地耗尽。引人注目的是,X染色体在配子发生过程中缺乏H3.3,表明组蛋白周转水平较低。这些结果提出了这样的可能性,即在配子发生过程中,X染色体和常染色体之间的组蛋白周转不对称。H3.3模式与原始生殖细胞和配子发生期间X染色体上的H3K4甲基化模式相似,表明组蛋白更新和修饰是耦合过程。我们的演示动态H3.3纳入非分裂细胞提供了一个机制的基础,在生殖细胞发育过程中的染色质变化。生殖细胞将遗传信息从一代传递到下一代。它们在减数分裂过程中转化为配子,然后在受精卵中重新编程发育。配子产生和发育重编程涉及DNA包装的巨大变化,但人们对这些变化如何参与重新设定整个生物体的发育程序知之甚少。在精子发生中,DNA被剥离并重新包装成高度浓缩的染色质。受精后,精子DNA再次被重新包装,因为它显着地解压缩,与卵核融合。这些重新包装过程涉及四种核心组蛋白,它们将DNA紧紧包裹成核小体颗粒。组蛋白3的一种通用变体H3.3在所有研究的植物和动物的生殖细胞中含量丰富,并且已显示在各种体细胞中的活跃转录位点处翻转。作者表明,H3.3在线虫的整个生殖细胞发育过程中显示动态周转。H3.3在第一次生殖系干细胞分裂期间合并,继续通过减数分裂,并最终进入精子和卵子。引人注目的是,H3.3从原始生殖细胞中耗尽,并且减数分裂沉默的X染色体缺乏H3.3,这表明减数分裂和重编程期间的H3.3动力学传递表观遗传信息。
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.
DOI: 10.1016/s1097-2765(00)00059-9
发表时间: 2000-09-01
期刊: MOLECULAR CELL
影响因子: 16
作者:
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通讯作者: Kim, SK
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发表时间: 2004-11-23
影响因子: 11.1
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发表时间: 2002-05-01
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发表时间: 2005-10-01
期刊: NATURE GENETICS
影响因子: 30.8
作者:
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通讯作者: Henikoff, S
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期刊: CHROMOSOMA
影响因子: 1.6
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