Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus.
Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus.
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DOI：
10.1371/journal.ppat.1000343
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发表时间：
2009-03
期刊：
影响因子：
6.7
通讯作者：
Sullivan W
中科院分区：
文献类型：
--
作者：
Landmann F;Orsi GA;Loppin B;Sullivan W
沃尔巴克氏体是一种细菌内共生体，通过称为细胞质不相容性（CI）的机制快速感染昆虫种群。在CI中，Wolbachia感染的雄性和未感染的雌性之间的杂交在雄性原核中产生严重的细胞周期缺陷，导致早期胚胎致死。相反，当双亲都被感染时，就会产生有活力的后代（拯救杂交）。CI-拯救的一个重要后果是，受感染的女性比未感染的女性具有选择性优势，从而促进沃尔巴克氏体通过昆虫种群的快速传播。CI破坏了雄性原核中的一些前期和中期事件，包括Cdk 1激活，染色体凝聚和分离。在这里，我们表明，CI破坏早期间期细胞周期事件。具体地，Cl延迟了从雄性原核去除鱼精蛋白后立即发生的H3.3和H4沉积。此外，我们发现男性原核中的复制因子PCNA的延长保留到中期，表明不完全复制的DNA进入有丝分裂的进展。我们建议，这些CI诱导的间期缺陷从头核小体组装和复制的原因所观察到的有丝分裂凝聚和分离缺陷。此外，这些间期染色体缺陷可能会激活S期检查点，解释先前描述的Cdk 1激活延迟。这些结果对Rescue和其他Wolbachia诱导表型的机制具有重要意义。 沃尔巴克氏体是所有细胞内细菌中最成功的细菌之一，估计感染了65%的昆虫物种。沃尔巴克氏体也存在于丝虫线虫中，是非洲河盲症的原因。沃尔巴克氏体的成功部分是由于它能够诱导一种被称为细胞质不相容性（CI）的条件性不育形式，赋予受感染的雌性巨大的选择优势。CI导致未感染的雌性和沃尔巴克氏体感染的雄性之间杂交的后代严重减少。然而，感染沃尔巴克氏体的雌性可以与感染或未感染的雄性交配，而不会减少后代。CI可以驱动物种形成，并作为控制昆虫传播的人类疾病的一种手段而受到广泛关注。尽管其生物学和医学意义，CI的分子基础尚不清楚。我们利用新产生的染色质试剂来证明，在染色体凝聚和分离中的缺陷得到充分证明之前，CI在将复制独立的组蛋白H3.3/H4复合物招募到雄性原核中时产生延迟。由于组蛋白H3.3在转录和受精后精子染色质重塑中的普遍作用，因此对组蛋白H3.3有很大的兴趣。此外，这些发现可能会提供洞察其他沃尔巴克氏体宿主相互作用，如CI救援和男性杀戮。
Wolbachia is a bacteria endosymbiont that rapidly infects insect populations through a mechanism known as cytoplasmic incompatibility (CI). In CI, crosses between Wolbachia-infected males and uninfected females produce severe cell cycle defects in the male pronucleus resulting in early embryonic lethality. In contrast, viable progeny are produced when both parents are infected (the Rescue cross). An important consequence of CI–Rescue is that infected females have a selective advantage over uninfected females facilitating the rapid spread of Wolbachia through insect populations. CI disrupts a number of prophase and metaphase events in the male pronucleus, including Cdk1 activation, chromosome condensation, and segregation. Here, we demonstrate that CI disrupts earlier interphase cell cycle events. Specifically, CI delays the H3.3 and H4 deposition that occurs immediately after protamine removal from the male pronucleus. In addition, we find prolonged retention of the replication factor PCNA in the male pronucleus into metaphase, indicating progression into mitosis with incompletely replicated DNA. We propose that these CI-induced interphase defects in de novo nucleosome assembly and replication are the cause of the observed mitotic condensation and segregation defects. In addition, these interphase chromosome defects likely activate S-phase checkpoints, accounting for the previously described delays in Cdk1 activation. These results have important implications for the mechanism of Rescue and other Wolbachia-induced phenotypes. Wolbachia are among the most successful of all intracellular bacteria, infecting an estimated 65% of insect species. Wolbachia are also present in filarial nematodes and are the cause of African river blindness. Wolbachia's success is due in part to its ability to induce a conditional form of sterility known as cytoplasmic incompatibility (CI), endowing infected females with a tremendous selective advantage. CI results in the severe reduction in progeny from crosses between uninfected females and Wolbachia-infected males. However, Wolbachia-infected females can mate with either infected or uninfected males with no reduction in progeny. CI may drive speciation and is intensively being pursued as a means to control insect-borne human disease. In spite of its biological and medical significance, the molecular basis of CI is not understood. We take advantage of newly generated chromatin reagents to demonstrate that prior to the well-documented defects in chromosome condensation and segregation, CI produces a delay in recruiting the replication-independent histone H3.3/H4 complex to the male pronucleus. There is great interest in histone H3.3 because of its general role in transcription and in remodeling of the sperm chromatin following fertilization. In addition, these findings may provide insight into other Wolbachia–host interactions such as CI–Rescue and male-killing.
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