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Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice

Intraflagellar transport (IFT) is a conserved mechanism believed to be essential for the assembly and maintenance of cilia and flagella. However, little is known about its role in mammalian sperm flagella formation. To fill this gap, we disrupted the Ift20 gene in male germ cells. Homozygous mutant...

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Autores principales: Zhang, Zhengang, Li, Wei, Zhang, Yong, Zhang, Ling, Teves, Maria E., Liu, Hong, Strauss, Jerome F., Pazour, Gregory J., Foster, James A., Hess, Rex A., Zhang, Zhibing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5170554/
https://www.ncbi.nlm.nih.gov/pubmed/27682589
http://dx.doi.org/10.1091/mbc.E16-05-0318
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author Zhang, Zhengang
Li, Wei
Zhang, Yong
Zhang, Ling
Teves, Maria E.
Liu, Hong
Strauss, Jerome F.
Pazour, Gregory J.
Foster, James A.
Hess, Rex A.
Zhang, Zhibing
author_facet Zhang, Zhengang
Li, Wei
Zhang, Yong
Zhang, Ling
Teves, Maria E.
Liu, Hong
Strauss, Jerome F.
Pazour, Gregory J.
Foster, James A.
Hess, Rex A.
Zhang, Zhibing
author_sort Zhang, Zhengang
collection PubMed
description Intraflagellar transport (IFT) is a conserved mechanism believed to be essential for the assembly and maintenance of cilia and flagella. However, little is known about its role in mammalian sperm flagella formation. To fill this gap, we disrupted the Ift20 gene in male germ cells. Homozygous mutant mice were infertile, with significantly reduced sperm counts and motility. In addition, abnormally shaped, elongating spermatid heads and bulbous, round spermatids were found in the lumen of the seminiferous tubules. Electron microscopy revealed increased cytoplasmic vesicles, fiber-like structures, abnormal accumulation of mitochondria, and a decrease in mature lysosomes. The few developed sperm had disrupted axonemes, and some retained cytoplasmic lobe components on the flagella. ODF2 and SPAG16L, two sperm flagella proteins, failed to be incorporated into sperm tails of the mutant mice, and in the germ cells, both were assembled into complexes with lighter density in the absence of IFT20. Disrupting IFT20 did not significantly change expression levels of IFT88, a component of the IFT-B complex, and IFT140, a component of the IFT-A complex. Even though the expression level of an autophagy core protein that associates with IFT20, ATG16, was reduced in the testis of the Ift20 mutant mice, expression levels of other major autophagy markers, including LC3 and ubiquitin, were not changed. Our studies suggest that IFT20 is essential for male fertility and spermiogenesis in mice, and its major function is to transport cargo proteins for sperm flagella formation. It also appears to be involved in removing excess cytoplasmic components.
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spelling pubmed-51705542017-01-30 Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice Zhang, Zhengang Li, Wei Zhang, Yong Zhang, Ling Teves, Maria E. Liu, Hong Strauss, Jerome F. Pazour, Gregory J. Foster, James A. Hess, Rex A. Zhang, Zhibing Mol Biol Cell Articles Intraflagellar transport (IFT) is a conserved mechanism believed to be essential for the assembly and maintenance of cilia and flagella. However, little is known about its role in mammalian sperm flagella formation. To fill this gap, we disrupted the Ift20 gene in male germ cells. Homozygous mutant mice were infertile, with significantly reduced sperm counts and motility. In addition, abnormally shaped, elongating spermatid heads and bulbous, round spermatids were found in the lumen of the seminiferous tubules. Electron microscopy revealed increased cytoplasmic vesicles, fiber-like structures, abnormal accumulation of mitochondria, and a decrease in mature lysosomes. The few developed sperm had disrupted axonemes, and some retained cytoplasmic lobe components on the flagella. ODF2 and SPAG16L, two sperm flagella proteins, failed to be incorporated into sperm tails of the mutant mice, and in the germ cells, both were assembled into complexes with lighter density in the absence of IFT20. Disrupting IFT20 did not significantly change expression levels of IFT88, a component of the IFT-B complex, and IFT140, a component of the IFT-A complex. Even though the expression level of an autophagy core protein that associates with IFT20, ATG16, was reduced in the testis of the Ift20 mutant mice, expression levels of other major autophagy markers, including LC3 and ubiquitin, were not changed. Our studies suggest that IFT20 is essential for male fertility and spermiogenesis in mice, and its major function is to transport cargo proteins for sperm flagella formation. It also appears to be involved in removing excess cytoplasmic components. The American Society for Cell Biology 2016-11-15 /pmc/articles/PMC5170554/ /pubmed/27682589 http://dx.doi.org/10.1091/mbc.E16-05-0318 Text en © 2016 Zhang et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
spellingShingle Articles
Zhang, Zhengang
Li, Wei
Zhang, Yong
Zhang, Ling
Teves, Maria E.
Liu, Hong
Strauss, Jerome F.
Pazour, Gregory J.
Foster, James A.
Hess, Rex A.
Zhang, Zhibing
Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice
title Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice
title_full Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice
title_fullStr Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice
title_full_unstemmed Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice
title_short Intraflagellar transport protein IFT20 is essential for male fertility and spermiogenesis in mice
title_sort intraflagellar transport protein ift20 is essential for male fertility and spermiogenesis in mice
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5170554/
https://www.ncbi.nlm.nih.gov/pubmed/27682589
http://dx.doi.org/10.1091/mbc.E16-05-0318
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