title: Centriole Remodeling during Spermiogenesis in Drosophila.
abstract: 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.
authors.affiliation: Department of Biological Sciences, University of Toledo, 3050 W. Towerview Boulevard, Toledo, OH 43606, USA.
authors.forename: Atul
authors.initials: A
authors.lastname: Khire
authors.affiliation: Department of Biological Sciences, University of Toledo, 3050 W. Towerview Boulevard, Toledo, OH 43606, USA.
authors.forename: Kyoung H
authors.initials: KH
authors.lastname: Jo
authors.affiliation: Laboratory of Protein Dynamics and Signaling, Center for Cancer Research, National Cancer Institute, Frederick, MD 21702-1201, USA.
authors.forename: Dong
authors.initials: D
authors.lastname: Kong
authors.affiliation: Department of Biochemistry, Cell Biology Program, The Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, ON M5G 1X8, Canada.
authors.forename: Tara
authors.initials: T
authors.lastname: Akhshi
authors.affiliation: Hybrigenics Services, 3-5 Impasse Reille, 75014 Paris, France.
authors.forename: Stephanie
authors.initials: S
authors.lastname: Blachon
authors.affiliation: Department of Biological Sciences, University of Toledo, 3050 W. Towerview Boulevard, Toledo, OH 43606, USA.
authors.forename: Anthony R
authors.initials: AR
authors.lastname: Cekic
authors.affiliation: Department of Biological Sciences, University of Toledo, 3050 W. Towerview Boulevard, Toledo, OH 43606, USA.
authors.forename: Sarah
authors.initials: S
authors.lastname: Hynek
authors.affiliation: Department of Biological Sciences, University of Toledo, 3050 W. Towerview Boulevard, Toledo, OH 43606, USA.
authors.forename: Andrew
authors.initials: A
authors.lastname: Ha
authors.affiliation: Laboratory of Protein Dynamics and Signaling, Center for Cancer Research, National Cancer Institute, Frederick, MD 21702-1201, USA.
authors.forename: Jadranka
authors.initials: J
authors.lastname: Loncarek
authors.affiliation: Department of Biochemistry, Cell Biology Program, The Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, ON M5G 1X8, Canada.
authors.forename: Vito
authors.initials: V
authors.lastname: Mennella
authors.affiliation: Department of Biological Sciences, University of Toledo, 3050 W. Towerview Boulevard, Toledo, OH 43606, USA. Electronic address: tomer.avidorreiss@utoledo.edu.
authors.forename: Tomer
authors.initials: T
authors.lastname: Avidor-Reiss
mesh_terms: D000818:Animals; D002502:Centrioles / Q000502:physiology*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism; D004331:Drosophila melanogaster / Q000502:physiology*; D005786:Gene Expression Regulation / Q000502:physiology; D008297:Male; D013091:Spermatogenesis / Q000502:physiology*; D013094:Spermatozoa / Q000502:physiology
chemical_list: D029721:Drosophila Proteins
keywords: PCL; Poc1; centriole; centrosome; centrosome reaction; embryo; fertilization; giant centriole; sperm; zygote