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Kinesin-7 CENP-E mediates chromosome alignment and spindle assembly checkpoint in meiosis I

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Abstract

In eukaryotes, meiosis is the genetic basis for sexual reproduction, which is important for chromosome stability and species evolution. The defects in meiosis usually lead to chromosome aneuploidy, reduced gamete number, and genetic diseases, but the pathogenic mechanisms are not well clarified. Kinesin-7 CENP-E is a key regulator in chromosome alignment and spindle assembly checkpoint in cell division. However, the functions and mechanisms of CENP-E in male meiosis remain largely unknown. In this study, we have revealed that the CENP-E gene was highly expressed in the rat testis. CENP-E inhibition influences chromosome alignment and spindle organization in metaphase I spermatocytes. We have found that a portion of misaligned homologous chromosomes is located at the spindle poles after CENP-E inhibition, which further activates the spindle assembly checkpoint during the metaphase-to-anaphase transition in rat spermatocytes. Furthermore, CENP-E depletion leads to abnormal spermatogenesis, reduced sperm count, and abnormal sperm head structure. Our findings have elucidated that CENP-E is essential for homologous chromosome alignment and spindle assembly checkpoint in spermatocytes, which further contribute to chromosome stability and sperm cell quality during spermatogenesis.

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All data generated or analyzed during this study are included in this published article. The data and materials are available on request.

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Acknowledgements

We thank all members of the Cytoskeleton Laboratory at Fujian Medical University for insightful discussions. We thank Lin-Ying Zhou, Xi Lin, and Min-Xia Wu at Public Technology Service Center, Fujian Medical University for their technical assistance. We thank Zhi-Hong Huang and Jun-Jin Lin at Public Technology Service Center, Fujian Medical University for their technical assistance in confocal microscopy and flow cytometry. We are grateful to Ying Lin, Si-Yi Zheng, and Qi Ke at the Experimental Teaching Center of Basic Medical Sciences at Fujian Medical University for their support.

Funding

This study was supported by the following grants: National Natural Science Foundation of China (grant number 82001608 and 82101678), Fujian Medical University high level talents scientific research start-up funding project (grant number XRCZX2017025) and Natural Science Foundation of Fujian Province, China (grant number 2023J01306 and 2019J05071).

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Zhen-Yu She: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Project administration, Resources, Supervision, Validation, Visualization, Roles/Writing - original draft, Writing - review and editing. Jing-Lian Zhang: Formal analysis, Investigation, Validation, Visualization, Roles/Writing - original draft. Meng-Fei Xu: Investigation, Validation, Visualization. Jie Chen: Investigation, Validation, Visualization. Ya-Lan Wei: Formal analysis, Validation, Roles/Writing - original draft, Writing - review and editing.

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Correspondence to Zhen-Yu She.

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All animal experiments were reviewed and approved by the Institutional Animal Care and Use Committee at Fujian Medical University, China (Protocol No. SYXK 2016-0007).

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The authors declare no competing interests.

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Zhang, JL., Xu, MF., Chen, J. et al. Kinesin-7 CENP-E mediates chromosome alignment and spindle assembly checkpoint in meiosis I. Chromosoma (2024). https://doi.org/10.1007/s00412-024-00818-w

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  • DOI: https://doi.org/10.1007/s00412-024-00818-w

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