Khire Atul, Jo Kyoung H, Kong Dong, Akhshi Tara, Blachon Stephanie, Cekic Anthony R, Hynek Sarah, Ha Andrew, Loncarek Jadranka, Mennella Vito, Avidor-Reiss Tomer
Department of Biological Sciences, University of Toledo, 3050 W. Towerview Boulevard, Toledo, OH 43606, USA.
Laboratory of Protein Dynamics and Signaling, Center for Cancer Research, National Cancer Institute, Frederick, MD 21702-1201, USA.
Curr Biol. 2016 Dec 5;26(23):3183-3189. doi: 10.1016/j.cub.2016.07.006. Epub 2016 Oct 27.
The first cell of an animal (zygote) requires centrosomes that are assembled from paternally inherited centrioles and maternally inherited pericentriolar material (PCM) [1]. In some animals, sperm centrioles with typical ultrastructure are the origin of the first centrosomes in the zygote [2-4]. In other animals, however, sperm centrioles lose their proteins and are thought to be degenerated and non-functional during spermiogenesis [5, 6]. Here, we show that the two sperm centrioles (the giant centriole [GC] and the proximal centriole-like structure [PCL]) in Drosophila melanogaster are remodeled during spermiogenesis through protein enrichment and ultrastructure modification in parallel to previously described centrosomal reduction [7]. We found that the ultrastructure of the matured sperm (spermatozoa) centrioles is modified dramatically and that the PCL does not resemble a typical centriole. We also describe a new phenomenon of Poc1 enrichment of the atypical centrioles in the spermatozoa. Using various mutants, protein expression during spermiogenesis, and RNAi knockdown of paternal Poc1, we found that paternal Poc1 enrichment is essential for the formation of centrioles during spermiogenesis and for the formation of centrosomes after fertilization in the zygote. Altogether, these findings demonstrate that the sperm centrioles are remodeled both in their protein composition and in ultrastructure, yet they are functional and are essential for normal embryogenesis in Drosophila.
动物的第一个细胞（受精卵）需要由父本遗传的中心粒和母本遗传的中心粒外周物质（PCM）组装而成的中心体[1]。在一些动物中，具有典型超微结构的精子中心粒是受精卵中第一个中心体的起源[2-4]。然而，在其他动物中，精子中心粒会丢失其蛋白质，并且在精子发生过程中被认为会退化且失去功能[5,6]。在此，我们表明，果蝇的两个精子中心粒（巨型中心粒[GC]和近端中心粒样结构[PCL]）在精子发生过程中通过蛋白质富集和超微结构修饰进行重塑，这与之前描述的中心体减少过程并行[7]。我们发现，成熟精子（精子）中心粒的超微结构发生了显著改变，并且PCL与典型中心粒不同。我们还描述了精子中异常中心粒的Poc1富集这一新现象。通过使用各种突变体、精子发生过程中的蛋白质表达以及对父本Poc1进行RNA干扰敲低，我们发现父本Poc1富集对于精子发生过程中中心粒的形成以及受精卵受精后中心体的形成至关重要。总之，这些发现表明，精子中心粒在其蛋白质组成和超微结构方面都进行了重塑，但它们具有功能，并且对于果蝇的正常胚胎发育至关重要。
