Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans.
Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans.
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DOI：
10.1371/journal.pgen.1000611
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发表时间：
2009-08
期刊：
影响因子：
4.5
通讯作者：
Chu DS
中科院分区：
文献类型：
--
作者：
Shakes DC;Wu JC;Sadler PL;Laprade K;Moore LL;Noritake A;Chu DS
在大多数有性生殖的生物中，减数分裂的基本过程与两个分化程序同时进行，它们以不同的速率发生，产生不同的细胞类型，精子和卵母细胞。然而，关于减数分裂程序是如何受到这种对比发育程序的影响，我们所知甚少。在这里，我们展示了秀丽隐杆线虫精子发生过程中减数分裂后期前期的详细时间表，利用细胞学和分子标记来相互关联染色体动力学变化与生殖细胞细胞化、纺锤体形成和细胞周期转变。该分析扩展了我们对秀丽隐杆线虫精子发生的理解，因为它确定了减数分裂程序的多个精子发生特异性特征，并为比较研究提供了一个框架。精母细胞的粗线后染色质在组成和形态上都不同于卵母细胞。引人注目的是，秀丽隐杆线虫的精子发生包括一个先前未被描述的核体阶段，这是许多生物体减数分裂的一个常见但鲜为人知的特征。我们发现，染色体在完整的核膜内形成一个狭窄的团块，核小体的形成遵循失突触，涉及转录的全局下调，并可能支持多种激酶的顺序激活，这些激酶为精母细胞进行减数分裂做准备。在精母细胞中，中心粒的存在改变了减数分裂纺锤体组装的相对时间和最终结构。这些微管的差异伴随着连接微管和染色体的着丝点的差异。这里揭示的精子减数分裂的特异性特征阐明了减数分裂所需的潜在分子机制如何在两性中受到不同的调节。精子和卵母细胞为每个新生命提供了相同但独特的DNA补充。这两种类型的细胞都是由减数分裂产生的，这是一个多步骤的程序，在这个过程中，染色体复制、配对和重组，然后分裂产生单倍体配子。同时，每种细胞类型也通过不同的发育程序进行分化。精子发生迅速产生许多小的、活动的、染色质受到高度保护的精子，而卵子发生的速度较慢，产生较少的大的、不活动的、营养丰富的卵母细胞。我们对模式生物秀丽隐杆线虫精子发生的关键里程碑事件进行了详细的分子分析，并确定了精子发生的减数分裂特征。我们发现，在许多减数分裂程序中，秀丽隐杆线虫的精子发生包括染色体聚集或“核体”阶段。这个延长的阶段在减数分裂前为染色体和微管重塑提供了一段时间。我们的分析确定了减数分裂程序的几个配子特异性特征，这些特征可能有助于减数分裂进程的不同时间、速度和机制。我们的发现为理解分化如何影响减数分裂提供了基础，减数分裂是识别所有生物繁殖成功所需的普遍特征的重要步骤。
In most sexually reproducing organisms, the fundamental process of meiosis is implemented concurrently with two differentiation programs that occur at different rates and generate distinct cell types, sperm and oocytes. However, little is known about how the meiotic program is influenced by such contrasting developmental programs. Here we present a detailed timeline of late meiotic prophase during spermatogenesis in Caenorhabditis elegans using cytological and molecular landmarks to interrelate changes in chromosome dynamics with germ cell cellularization, spindle formation, and cell cycle transitions. This analysis expands our understanding C. elegans spermatogenesis, as it identifies multiple spermatogenesis-specific features of the meiotic program and provides a framework for comparative studies. Post-pachytene chromatin of spermatocytes is distinct from that of oocytes in both composition and morphology. Strikingly, C. elegans spermatogenesis includes a previously undescribed karyosome stage, a common but poorly understood feature of meiosis in many organisms. We find that karyosome formation, in which chromosomes form a constricted mass within an intact nuclear envelope, follows desynapsis, involves a global down-regulation of transcription, and may support the sequential activation of multiple kinases that prepare spermatocytes for meiotic divisions. In spermatocytes, the presence of centrioles alters both the relative timing of meiotic spindle assembly and its ultimate structure. These microtubule differences are accompanied by differences in kinetochores, which connect microtubules to chromosomes. The sperm-specific features of meiosis revealed here illuminate how the underlying molecular machinery required for meiosis is differentially regulated in each sex. Sperm and oocytes contribute equal but unique complements of DNA to each new life. Both types of cells arise from meiosis, a multi-step program during which chromosomes replicate, pair and recombine, then divide to generate haploid gametes. Simultaneously, each cell type also differentiates via distinct developmental programs. Spermatogenesis rapidly produces many small, motile sperm with highly protected chromatin, while oogenesis occurs at a slower rate to yield fewer large, immobile, nutrient-rich oocytes. We provide a detailed molecular analysis of key landmark events of spermatogenesis and identify spermatogenesis-specific features of meiosis in the model organism C. elegans. We find that, as in many meiotic programs, C. elegans spermatogenesis includes a chromosome aggregation or “karyosome” phase. This extended stage provides a period for chromosome and microtubule remodeling prior to the meiotic divisions. Our analysis identifies several gamete-specific features of the meiotic program that may contribute to the differential timing, pace, and mechanics of meiotic progression. Our findings provide a foundation for understanding how differentiation influences meiosis, which is an essential step in identifying universal features required for reproductive success in all organisms.
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