KIF2C is essential for meiosis and manchette dynamics in male mice

In gametogenesis, microtubules undergo dramatic changes known as microtubule dynamics, and which is important for fertility both male and female. In spermatogenesis, spindle microtubule dynamics occur during meiosis and manchette microtubule dynamics occur in elongated spermatids. In oogenesis, spin...

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Main Authors: Ryua Harima, Mayu Kishinami, Kenshiro Hara, Kentaro Tanemura
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-03-01
Series:Frontiers in Cell and Developmental Biology
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Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2025.1523593/full
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author Ryua Harima
Mayu Kishinami
Kenshiro Hara
Kentaro Tanemura
Kentaro Tanemura
author_facet Ryua Harima
Mayu Kishinami
Kenshiro Hara
Kentaro Tanemura
Kentaro Tanemura
author_sort Ryua Harima
collection DOAJ
description In gametogenesis, microtubules undergo dramatic changes known as microtubule dynamics, and which is important for fertility both male and female. In spermatogenesis, spindle microtubule dynamics occur during meiosis and manchette microtubule dynamics occur in elongated spermatids. In oogenesis, spindle microtubule dynamics occur during meiosis. The microtubule depolymerization protein kinesin-13 family (KIF2A, KIF2B, and KIF2C) plays an important role in microtubule dynamics, and KIF2C is a well-known microtubule depolymerization factor in mitosis. Although the function of KIF2C in mitosis has been extensively studied, its role in meiosis remains unclear. Additionally, the role of microtubule dynamics in manchette formation remains unclear. We generated germ cell-specific Kif2c conditional knockout (Kif2c cKO) mice to elucidate KIF2C function in germ cells. Kif2c cKO male mice showed chromosomal misalignment at meiotic metaphase, abnormal manchette morphology and delayed manchette disassembly, which led to a significant increase in apoptosis. Furthermore, Kif2c cKO male mice were completely infertile. Therefore, KIF2C plays an important role in chromosomal alignment in male meiosis and in manchette dynamics in elongated spermatids. In contrast, Kif2c cKO female mice were sufficiently fertile, and only minor defects were observed in chromosome alignment in meiosis. This study demonstrates, for the first time, that KIF2C is important for microtubule dynamics of spermatogenesis to achieve male fertility, but not for female fertility.
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spelling doaj-art-9215dd03768e4a6c99c56d29ff78b3ec2025-08-20T03:42:02ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2025-03-011310.3389/fcell.2025.15235931523593KIF2C is essential for meiosis and manchette dynamics in male miceRyua Harima0Mayu Kishinami1Kenshiro Hara2Kentaro Tanemura3Kentaro Tanemura4Laboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi, JapanLaboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi, JapanLaboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi, JapanLaboratory of Animal Reproduction and Development, Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi, JapanLaboratory of Reproductive Technology (Repro-SOLEIL), Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi, JapanIn gametogenesis, microtubules undergo dramatic changes known as microtubule dynamics, and which is important for fertility both male and female. In spermatogenesis, spindle microtubule dynamics occur during meiosis and manchette microtubule dynamics occur in elongated spermatids. In oogenesis, spindle microtubule dynamics occur during meiosis. The microtubule depolymerization protein kinesin-13 family (KIF2A, KIF2B, and KIF2C) plays an important role in microtubule dynamics, and KIF2C is a well-known microtubule depolymerization factor in mitosis. Although the function of KIF2C in mitosis has been extensively studied, its role in meiosis remains unclear. Additionally, the role of microtubule dynamics in manchette formation remains unclear. We generated germ cell-specific Kif2c conditional knockout (Kif2c cKO) mice to elucidate KIF2C function in germ cells. Kif2c cKO male mice showed chromosomal misalignment at meiotic metaphase, abnormal manchette morphology and delayed manchette disassembly, which led to a significant increase in apoptosis. Furthermore, Kif2c cKO male mice were completely infertile. Therefore, KIF2C plays an important role in chromosomal alignment in male meiosis and in manchette dynamics in elongated spermatids. In contrast, Kif2c cKO female mice were sufficiently fertile, and only minor defects were observed in chromosome alignment in meiosis. This study demonstrates, for the first time, that KIF2C is important for microtubule dynamics of spermatogenesis to achieve male fertility, but not for female fertility.https://www.frontiersin.org/articles/10.3389/fcell.2025.1523593/fullKIF2C (MCAK)microtubule dynamicsmeiosischromosome alignmentmanchettemale infertility
spellingShingle Ryua Harima
Mayu Kishinami
Kenshiro Hara
Kentaro Tanemura
Kentaro Tanemura
KIF2C is essential for meiosis and manchette dynamics in male mice
Frontiers in Cell and Developmental Biology
KIF2C (MCAK)
microtubule dynamics
meiosis
chromosome alignment
manchette
male infertility
title KIF2C is essential for meiosis and manchette dynamics in male mice
title_full KIF2C is essential for meiosis and manchette dynamics in male mice
title_fullStr KIF2C is essential for meiosis and manchette dynamics in male mice
title_full_unstemmed KIF2C is essential for meiosis and manchette dynamics in male mice
title_short KIF2C is essential for meiosis and manchette dynamics in male mice
title_sort kif2c is essential for meiosis and manchette dynamics in male mice
topic KIF2C (MCAK)
microtubule dynamics
meiosis
chromosome alignment
manchette
male infertility
url https://www.frontiersin.org/articles/10.3389/fcell.2025.1523593/full
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