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Protein Regulator of Cytokinesis 1 (PRC1) Regulates Chromosome Dynamics and Cytoplasmic Division During Mouse Oocyte Meiotic Maturation and Early Embryonic Development.
FEBS J. 2020 Jun 19 [Online ahead of print]FJ

Abstract

In contrast to the homeokinesis of mitosis, asymmetric division of cytoplasm is the conspicuous feature of meiosis in mammalian oocytes. Protein regulator of cytokinesis 1 (PRC1) is an important regulator during mitotic spindle assembly and cytoplasmic division, but its functions in oocyte meiosis and early embryo development have not been fully elucidated. In this study, we detected PRC1 expression and localization and revealed a nuclear, spindle midzone-related dynamic pattern throughout meiotic and mitotic progressions. Treatment of oocytes with the reagents taxol or nocodazole disturbed the distribution of PRC1 in metaphase II oocytes. Further, PRC1 depletion led to failure of first polar body (PB1) extrusion and spindle migration, aneuploidy, and defective kinetochore-microtubules (MT) attachment and spindle assembly. Overexpression of PRC1 resulted in PB1 extrusion failure, aneuploidy, and serious defects of spindle assembly. To investigate PRC1 function in early embryos, we injected Prc1 morpholino into zygotes and 2-cell stage embryos. Depletion of PRC1 in zygotes impaired 4-cell, morula, and blastocyst formation. Loss of PRC1 in single or double blastomeres in 2-cell stage embryos significantly impaired cell division, indicating its indispensable role in early embryo development. Co-immunoprecipitation showed that PRC1 interacts with polo-like kinase 1 (PLK1), and functional knockdown and rescue experiments demonstrated that PRC1 recruits PLK1 to the spindle midzone to regulate cytoplasmic division during meiosis. Finally, Kif4 knockdown down-regulates PRC1 expression and leads to PRC1 localization failure. Taken together, our data suggest PRC1 plays an important role during oocyte maturation and early embryonic development by regulating chromosome dynamics and cytoplasmic division.

Authors+Show Affiliations

State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070.State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070. Sichuan Key Laboratory of Conservation Biology for Endangered Wildlife, Chengdu Research Base of Giant Panda Breeding, Sichuan Province, Chengdu, People's Republic of China, 610000.State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070.State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070.State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070.State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070.State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070.State Key Laboratory of Reproductive Regulation & Breeding of Grassland Livestock, School of Life Science, Inner Mongolia University, Hohhot, Inner Mongolia, People's Republic of China, 010070.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

32562308

Citation

Zhou, Cheng-Jie, et al. "Protein Regulator of Cytokinesis 1 (PRC1) Regulates Chromosome Dynamics and Cytoplasmic Division During Mouse Oocyte Meiotic Maturation and Early Embryonic Development." The FEBS Journal, 2020.
Zhou CJ, Wang DH, Kong XW, et al. Protein Regulator of Cytokinesis 1 (PRC1) Regulates Chromosome Dynamics and Cytoplasmic Division During Mouse Oocyte Meiotic Maturation and Early Embryonic Development. FEBS J. 2020.
Zhou, C. J., Wang, D. H., Kong, X. W., Han, Z., Hao, X., Wang, X. Y., Wen, X., & Liang, C. G. (2020). Protein Regulator of Cytokinesis 1 (PRC1) Regulates Chromosome Dynamics and Cytoplasmic Division During Mouse Oocyte Meiotic Maturation and Early Embryonic Development. The FEBS Journal. https://doi.org/10.1111/febs.15458
Zhou CJ, et al. Protein Regulator of Cytokinesis 1 (PRC1) Regulates Chromosome Dynamics and Cytoplasmic Division During Mouse Oocyte Meiotic Maturation and Early Embryonic Development. FEBS J. 2020 Jun 19; PubMed PMID: 32562308.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Protein Regulator of Cytokinesis 1 (PRC1) Regulates Chromosome Dynamics and Cytoplasmic Division During Mouse Oocyte Meiotic Maturation and Early Embryonic Development. AU - Zhou,Cheng-Jie, AU - Wang,Dong-Hui, AU - Kong,Xiang-Wei, AU - Han,Zhe, AU - Hao,Xin, AU - Wang,Xing-Yue, AU - Wen,Xin, AU - Liang,Cheng-Guang, Y1 - 2020/06/19/ PY - 2019/11/26/received PY - 2020/06/01/revised PY - 2020/06/09/accepted PY - 2020/6/21/entrez KW - chromosome dynamics KW - cytoplasmic division KW - early embryo development KW - oocyte meiosis KW - protein regulator of cytokinesis 1 JF - The FEBS journal JO - FEBS J. N2 - In contrast to the homeokinesis of mitosis, asymmetric division of cytoplasm is the conspicuous feature of meiosis in mammalian oocytes. Protein regulator of cytokinesis 1 (PRC1) is an important regulator during mitotic spindle assembly and cytoplasmic division, but its functions in oocyte meiosis and early embryo development have not been fully elucidated. In this study, we detected PRC1 expression and localization and revealed a nuclear, spindle midzone-related dynamic pattern throughout meiotic and mitotic progressions. Treatment of oocytes with the reagents taxol or nocodazole disturbed the distribution of PRC1 in metaphase II oocytes. Further, PRC1 depletion led to failure of first polar body (PB1) extrusion and spindle migration, aneuploidy, and defective kinetochore-microtubules (MT) attachment and spindle assembly. Overexpression of PRC1 resulted in PB1 extrusion failure, aneuploidy, and serious defects of spindle assembly. To investigate PRC1 function in early embryos, we injected Prc1 morpholino into zygotes and 2-cell stage embryos. Depletion of PRC1 in zygotes impaired 4-cell, morula, and blastocyst formation. Loss of PRC1 in single or double blastomeres in 2-cell stage embryos significantly impaired cell division, indicating its indispensable role in early embryo development. Co-immunoprecipitation showed that PRC1 interacts with polo-like kinase 1 (PLK1), and functional knockdown and rescue experiments demonstrated that PRC1 recruits PLK1 to the spindle midzone to regulate cytoplasmic division during meiosis. Finally, Kif4 knockdown down-regulates PRC1 expression and leads to PRC1 localization failure. Taken together, our data suggest PRC1 plays an important role during oocyte maturation and early embryonic development by regulating chromosome dynamics and cytoplasmic division. SN - 1742-4658 UR - https://www.unboundmedicine.com/medline/citation/32562308/Protein_Regulator_of_Cytokinesis_1_(PRC1)_Regulates_Chromosome_Dynamics_and_Cytoplasmic_Division_During_Mouse_Oocyte_Meiotic_Maturation_and_Early_Embryonic_Development L2 - https://doi.org/10.1111/febs.15458 DB - PRIME DP - Unbound Medicine ER -
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