Chemotactic behavior of egg mitochondria in response to sperm fusion in mice

Mitochondria are the powerhouses of eukaryotic cells and their positioning contributes to fertilization and early developmental processes. We report that sperm fusion triggers Ca2+ oscillations and mitochondrial movement toward fused sperm (mitochondrial chemotaxis) in mouse eggs. Mitochondria funct...

Full description

Bibliographic Details
Main Authors: Maki Iwai, Yuichirou Harada, Rinako Miyabayashi, Woojin Kang, Akihiro Nakamura, Natsuko Kawano, Yoshitaka Miyamoto, Mitsutoshi Yamada, Toshio Hamatani, Mami Miyado, Keiichi Yoshida, Hidekazu Saito, Mamoru Tanaka, Akihiro Umezawa, Kenji Miyado
Format: Article
Language:English
Published: Elsevier 2018-11-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2405844018304304
_version_ 1818773146439778304
author Maki Iwai
Yuichirou Harada
Rinako Miyabayashi
Woojin Kang
Akihiro Nakamura
Natsuko Kawano
Yoshitaka Miyamoto
Mitsutoshi Yamada
Toshio Hamatani
Mami Miyado
Keiichi Yoshida
Hidekazu Saito
Mamoru Tanaka
Akihiro Umezawa
Kenji Miyado
author_facet Maki Iwai
Yuichirou Harada
Rinako Miyabayashi
Woojin Kang
Akihiro Nakamura
Natsuko Kawano
Yoshitaka Miyamoto
Mitsutoshi Yamada
Toshio Hamatani
Mami Miyado
Keiichi Yoshida
Hidekazu Saito
Mamoru Tanaka
Akihiro Umezawa
Kenji Miyado
author_sort Maki Iwai
collection DOAJ
description Mitochondria are the powerhouses of eukaryotic cells and their positioning contributes to fertilization and early developmental processes. We report that sperm fusion triggers Ca2+ oscillations and mitochondrial movement toward fused sperm (mitochondrial chemotaxis) in mouse eggs. Mitochondria functioned in Ca2+ storage and were colocalized with endoplasmic reticulum (ER) during Ca2+ oscillations. Mitochondria then moved toward the fused sperm. Sperm extracts lacking nuclei induced Ca2+ oscillations, but did not promote mitochondrial chemotaxis. Our results suggest that sperm fusion motivates Ca2+ oscillation-independent mitochondrial chemotaxis. This phenomenon indicates that egg mitochondria interact with sperm materials, presumably nuclear substances, and their network tethers egg and sperm nuclei at the early stage of zygote formation.
first_indexed 2024-12-18T10:20:37Z
format Article
id doaj.art-d7e0604cc1f345c0a65740e5133163d1
institution Directory Open Access Journal
issn 2405-8440
language English
last_indexed 2024-12-18T10:20:37Z
publishDate 2018-11-01
publisher Elsevier
record_format Article
series Heliyon
spelling doaj.art-d7e0604cc1f345c0a65740e5133163d12022-12-21T21:11:10ZengElsevierHeliyon2405-84402018-11-01411e00944Chemotactic behavior of egg mitochondria in response to sperm fusion in miceMaki Iwai0Yuichirou Harada1Rinako Miyabayashi2Woojin Kang3Akihiro Nakamura4Natsuko Kawano5Yoshitaka Miyamoto6Mitsutoshi Yamada7Toshio Hamatani8Mami Miyado9Keiichi Yoshida10Hidekazu Saito11Mamoru Tanaka12Akihiro Umezawa13Kenji Miyado14Department of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, Japan; Department of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanDepartment of Molecular Pathology, Tokyo Medical University, 6-1-1 Shinjuku, Shinjuku, Tokyo 192-0397, Japan; Corresponding author.Shinbashi YUME Clinic, 2-5-1 Shinbashi, Miyato, Tokyo 105-0004, JapanDepartment of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, Japan; Department of Perinatal Medicine and Oocyte Care, National Center for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanDepartment of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, Japan; Department of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanDepartment of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, Japan; Department of Life Sciences, School of Agriculture, Meiji University, 1-1-1 Higashimita, Tama, Kawasaki, Kanagawa 214-8571, JapanDepartment of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanDepartment of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, JapanDepartment of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, JapanDepartment of Molecular Endocrinology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanAdvanced Medicine, Innovation and Clinical Research Center, Tottori University Hospital, 36-1 Nishicho, Yonago, Tottori 683-8504, JapanDepartment of Perinatal Medicine and Oocyte Care, National Center for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanDepartment of Obstetrics and Gynecology, Keio University School of Medicine, 35 Shinanomachi, Shinjuku, Tokyo 160-8582, JapanDepartment of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, JapanDepartment of Reproductive Biology, National Research Institute for Child Health and Development, 2-10-1 Okura, Setagaya, Tokyo 157-8535, Japan; Corresponding author.Mitochondria are the powerhouses of eukaryotic cells and their positioning contributes to fertilization and early developmental processes. We report that sperm fusion triggers Ca2+ oscillations and mitochondrial movement toward fused sperm (mitochondrial chemotaxis) in mouse eggs. Mitochondria functioned in Ca2+ storage and were colocalized with endoplasmic reticulum (ER) during Ca2+ oscillations. Mitochondria then moved toward the fused sperm. Sperm extracts lacking nuclei induced Ca2+ oscillations, but did not promote mitochondrial chemotaxis. Our results suggest that sperm fusion motivates Ca2+ oscillation-independent mitochondrial chemotaxis. This phenomenon indicates that egg mitochondria interact with sperm materials, presumably nuclear substances, and their network tethers egg and sperm nuclei at the early stage of zygote formation.http://www.sciencedirect.com/science/article/pii/S2405844018304304Cell biologyDevelopmental biologyMolecular biologyZoology
spellingShingle Maki Iwai
Yuichirou Harada
Rinako Miyabayashi
Woojin Kang
Akihiro Nakamura
Natsuko Kawano
Yoshitaka Miyamoto
Mitsutoshi Yamada
Toshio Hamatani
Mami Miyado
Keiichi Yoshida
Hidekazu Saito
Mamoru Tanaka
Akihiro Umezawa
Kenji Miyado
Chemotactic behavior of egg mitochondria in response to sperm fusion in mice
Heliyon
Cell biology
Developmental biology
Molecular biology
Zoology
title Chemotactic behavior of egg mitochondria in response to sperm fusion in mice
title_full Chemotactic behavior of egg mitochondria in response to sperm fusion in mice
title_fullStr Chemotactic behavior of egg mitochondria in response to sperm fusion in mice
title_full_unstemmed Chemotactic behavior of egg mitochondria in response to sperm fusion in mice
title_short Chemotactic behavior of egg mitochondria in response to sperm fusion in mice
title_sort chemotactic behavior of egg mitochondria in response to sperm fusion in mice
topic Cell biology
Developmental biology
Molecular biology
Zoology
url http://www.sciencedirect.com/science/article/pii/S2405844018304304
work_keys_str_mv AT makiiwai chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT yuichirouharada chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT rinakomiyabayashi chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT woojinkang chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT akihironakamura chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT natsukokawano chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT yoshitakamiyamoto chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT mitsutoshiyamada chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT toshiohamatani chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT mamimiyado chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT keiichiyoshida chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT hidekazusaito chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT mamorutanaka chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT akihiroumezawa chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice
AT kenjimiyado chemotacticbehaviorofeggmitochondriainresponsetospermfusioninmice