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Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus

BACKGROUND: Acrosome formation and nuclear shaping are the main events in spermatogenesis. During spermiogenesis in Exopalaemon modestus, a unique microtubular structure called the acroframosome (AFS) forms in spermatids. The AFS links to a temporary organelle called the lamellar complex (LCx) leadi...

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Autores principales: Hou, Cong-Cong, Yang, Wan-Xi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3786892/
https://www.ncbi.nlm.nih.gov/pubmed/24098763
http://dx.doi.org/10.1371/journal.pone.0076065
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author Hou, Cong-Cong
Yang, Wan-Xi
author_facet Hou, Cong-Cong
Yang, Wan-Xi
author_sort Hou, Cong-Cong
collection PubMed
description BACKGROUND: Acrosome formation and nuclear shaping are the main events in spermatogenesis. During spermiogenesis in Exopalaemon modestus, a unique microtubular structure called the acroframosome (AFS) forms in spermatids. The AFS links to a temporary organelle called the lamellar complex (LCx) leading to the formation of an everted umbrella-shaped acrosome and a dish-shaped nucleus in the mature sperm. These morphological changes require complex cell motility in which the C-terminal kinesin motor protein called KIFC1 is involved. In this study, we demonstrate that KIFC1 moves along the AFS and plays an important role in acrosome formation and nuclear shaping during spermatogenesis in E. modestus. METHODOLOGY/PRINCIPAL FINDINGS: We cloned a 3125 bp complete cDNA of kifc1 from the testis of E. modestus by PCR. The predicted secondary and tertiary structures of E. modestus KIFC1 contain three domains: a) the C-terminus, b) the stalk region, and the c) N-terminusl. Semi-quantitative RT-PCR detected the expression of kifc1 mRNA in different tissues of E. modestus. In situ hybridization demonstrated the temporal and spatial expression profile of kifc1 during spermiogenesis. Western blot identified the expression of KIFC1 in different tissues of E. modestus, including the testis. Immunofluorescence localized KIFC1, tubulin, GM130, and mitochondria in order to elucidate their role during spermiogenesis in E. modestus. CONCLUSION/SIGNIFICANCE: Our results indicate that KIFC1 transports the Golgi complex, mitochondria, and other cellular components that results in acrosome formation and nuclear shaping in E. modestus. The KIFC1 transport function depends upon the microtubular structure called the acroframosome (AFS). This study describes some of the molecular mechanisms involved in the acrosome formation and nuclear shaping in E. modestus. In addition, this study may provide a model for studying the molecular mechanisms involved in spermatogenesis in other crustacean species and lead to a better understanding of the fertilization process in crustaceans.
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spelling pubmed-37868922013-10-04 Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus Hou, Cong-Cong Yang, Wan-Xi PLoS One Research Article BACKGROUND: Acrosome formation and nuclear shaping are the main events in spermatogenesis. During spermiogenesis in Exopalaemon modestus, a unique microtubular structure called the acroframosome (AFS) forms in spermatids. The AFS links to a temporary organelle called the lamellar complex (LCx) leading to the formation of an everted umbrella-shaped acrosome and a dish-shaped nucleus in the mature sperm. These morphological changes require complex cell motility in which the C-terminal kinesin motor protein called KIFC1 is involved. In this study, we demonstrate that KIFC1 moves along the AFS and plays an important role in acrosome formation and nuclear shaping during spermatogenesis in E. modestus. METHODOLOGY/PRINCIPAL FINDINGS: We cloned a 3125 bp complete cDNA of kifc1 from the testis of E. modestus by PCR. The predicted secondary and tertiary structures of E. modestus KIFC1 contain three domains: a) the C-terminus, b) the stalk region, and the c) N-terminusl. Semi-quantitative RT-PCR detected the expression of kifc1 mRNA in different tissues of E. modestus. In situ hybridization demonstrated the temporal and spatial expression profile of kifc1 during spermiogenesis. Western blot identified the expression of KIFC1 in different tissues of E. modestus, including the testis. Immunofluorescence localized KIFC1, tubulin, GM130, and mitochondria in order to elucidate their role during spermiogenesis in E. modestus. CONCLUSION/SIGNIFICANCE: Our results indicate that KIFC1 transports the Golgi complex, mitochondria, and other cellular components that results in acrosome formation and nuclear shaping in E. modestus. The KIFC1 transport function depends upon the microtubular structure called the acroframosome (AFS). This study describes some of the molecular mechanisms involved in the acrosome formation and nuclear shaping in E. modestus. In addition, this study may provide a model for studying the molecular mechanisms involved in spermatogenesis in other crustacean species and lead to a better understanding of the fertilization process in crustaceans. Public Library of Science 2013-09-30 /pmc/articles/PMC3786892/ /pubmed/24098763 http://dx.doi.org/10.1371/journal.pone.0076065 Text en © 2013 Hou, Yang http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Hou, Cong-Cong
Yang, Wan-Xi
Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus
title Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus
title_full Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus
title_fullStr Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus
title_full_unstemmed Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus
title_short Acroframosome-Dependent KIFC1 Facilitates Acrosome Formation during Spermatogenesis in the Caridean Shrimp Exopalaemon modestus
title_sort acroframosome-dependent kifc1 facilitates acrosome formation during spermatogenesis in the caridean shrimp exopalaemon modestus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3786892/
https://www.ncbi.nlm.nih.gov/pubmed/24098763
http://dx.doi.org/10.1371/journal.pone.0076065
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