Sustained Elongation of Sperm Tail Promoted by Local Remodeling of Giant Mitochondria in Drosophila

Sustained Elongation of Sperm Tail Promoted by Local Remodeling of Giant Mitochondria in Drosophila
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DOI:
10.1016/j.cub.2011.04.016
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发表时间:
2011-05-24
期刊:
影响因子:
9.2
通讯作者:
Hayashi, Shigeo
Hayashi, Shigeo
中科院分区:
生物学1区
文献类型:
--
作者:
Noguchi, Tatsuhiko;Koizumi, Michiko;Hayashi, Shigeo

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背景:由于进化选择,果蝇科的精子长度从几百微米到6厘米不等。在交配后的竞争中,较长的精子在头部靠近卵子的位置上具有优势。精子细胞的伸长可以在没有轴丝的情况下进行,这表明除了鞭毛内运输外还出现了一种机制来维持它。结果:在这里,我们报告了果蝇精子的伸长是由巨大的线粒体和微管阵列的相互依赖的延伸驱动的,这些微管阵列形成在线粒体表面周围。在原代培养的伸长精子细胞,我们证明了线粒体的完整性和微管在尾尖区域的局部动力学是必不可少的单轴伸长的精子尾部。线粒体-微管连接蛋白米尔顿聚集在尾尖附近的线粒体上,是微管滑动运动所必需的。破坏米尔顿和它的相关蛋白dMiro,以及潜在的微管交联剂Nebbish和Fascetto,引起强烈的伸长缺陷,表明精子细胞尾部伸长需要微管-微管结合和微管交联。线粒体通过为微管重组提供结构平台以支持尖端发生的强劲伸长,在果蝇精子尾部伸长中发挥着意想不到的作用很长的精子尾巴。线粒体作为细胞骨架动力学的组织者的鉴定扩展了我们对细胞形态发生机制的理解。
Background: Sperm length in Drosophilidae varies from a few hundred microns to 6 cm as a result of evolutionary selection. In postcopulatory competition, longer sperm have an advantage in positioning their head closer to the egg. Sperm cell elongation can proceed in the absence of an axoneme, suggesting that a mechanism besides intraflagellar transport emerged to sustain it.Results: Here we report that sperm elongation in Drosophila melanogaster is driven by the interdependent extension of giant mitochondria and microtubule array that is formed around the mitochondrial surface. In primary cultures of elongating spermatids, we demonstrated that the mitochondrial integrity and local dynamics of microtubules at the tail tip region are essential for uniaxial elongation of the sperm tail. Mitochondria-microtubule linker protein Milton accumulated on mitochondria near the tail tip and is required for the sliding movement of microtubules. Disruption of Milton and its associated protein dMiro, and of potential microtubule crosslinkers Nebbish and Fascetto, caused strong elongation defects, indicating that mitochondria-microtubule association and microtubule crosslinking are required for spermatid tail elongation.Conclusions: Mitochondria play unexpected roles in sperm tail elongation in Drosophila by providing a structural platform for microtubule reorganization to support the robust elongation taking place at the tip of the very long sperm tail. The identification of mitochondria as an organizer of cytoskeletal dynamics extends our understanding of mechanisms of cell morphogenesis.