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CRMP5 participates in oocyte meiosis by regulating spastin to correct microtubule–kinetochore misconnection

Published online by Cambridge University Press:  04 December 2023

Zhen Jin
Center for Reproductive Medicine, Department of Reproductive Endocrinology, Zhejiang Provincial People’s Hospital (Affiliated People’s Hospital), Hangzhou Medical College, Hangzhou, Zhejiang, 310014, China
Zhi-Cai Zhang
Department of Dispatching Management, Zibo Medical Emergency Command Center, Zibo, Shandong, 255030, China
Chen-Yu Xiao
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital (Affiliated People’s Hospital), Hangzhou Medical College, Hangzhou, Zhejiang, 310014, China
Mei-Qi Li
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital (Affiliated People’s Hospital), Hangzhou Medical College, Hangzhou, Zhejiang, 310014, China
Qian-Ru Li
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital (Affiliated People’s Hospital), Hangzhou Medical College, Hangzhou, Zhejiang, 310014, China
Lei-Lei Gao*
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital (Affiliated People’s Hospital), Hangzhou Medical College, Hangzhou, Zhejiang, 310014, China
Corresponding author: Lei-Lei Gao; Email:


Our previous studies have suggested that spastin, which aggregates on spindle microtubules in oocytes, may promote the assembly of mouse oocyte spindles by cutting microtubules. This action may be related to CRMP5, as knocking down CRMP5 results in reduced spindle microtubule density and maturation defects in oocytes. In this study, we found that, after knocking down CRMP5 in oocytes, spastin distribution shifted from the spindle to the spindle poles and errors in microtubule–kinetochore attachment appeared in oocyte spindles. However, CRMP5 did not interact with the other two microtubule-severing proteins, katanin-like-1 (KATNAL1) and fidgetin-like-1 (FIGNL1), which aggregate at the spindle poles. We speculate that, in oocytes, due to the reduction of spastin distribution on chromosomes after knocking down CRMP5, microtubule–kinetochore errors cannot be corrected through severing, resulting in meiotic division abnormalities and maturation defects in oocytes. This finding provides new insights into the regulatory mechanisms of spastin in oocytes and important opportunities for the study of meiotic division mechanisms.

Research Article
© The Author(s), 2023. Published by Cambridge University Press

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Buster, D., McNally, K. and McNally, F. J. (2002). Katanin inhibition prevents the redistribution of gamma-tubulin at mitosis. Journal of Cell Science, 115(5), 10831092. doi: 10.1242/jcs.115.5.1083 CrossRefGoogle ScholarPubMed
Casanova, M., Crobu, L., Blaineau, C., Bourgeois, N., Bastien, P. and Pagès, M. (2009). Microtubule-severing proteins are involved in flagellar length control and mitosis in trypanosomatids. Molecular Microbiology, 71(6), 13531370. doi: 10.1111/j.1365-2958.2009.06594.x CrossRefGoogle ScholarPubMed
Frickey, T. and Lupas, A. N. (2004). Phylogenetic analysis of AAA proteins. Journal of Structural Biology, 146(1–2), 210. doi: 10.1016/j.jsb.2003.11.020 CrossRefGoogle ScholarPubMed
Gao, L. L., Xu, F., Jin, Z., Ying, X. Y. and Liu, J. W. (2019). Microtubule–severing protein Katanin p60 ATPase–containing subunit A–like 1 is involved in pole–based spindle organization during mouse oocyte meiosis. Molecular Medicine Reports, 20(4), 35733582. doi: 10.3892/mmr.2019.10605 Google ScholarPubMed
He, L., Kooistra, R., Das, R., Oudejans, E., van Leen, E., Ziegler, J., Portegies, S., de Haan, B., van Regteren Altena, A., Stucchi, R., Altelaar, A. M., Wieser, S., Krieg, M., Hoogenraad, C. C. and Harterink, M. (2020). Cortical anchoring of the microtubule cytoskeleton is essential for neuron polarity. eLife, 9, 1. doi: 10.7554/eLife.55111 CrossRefGoogle ScholarPubMed
Ji, Z., Zhang, G., Chen, L., Li, J., Yang, Y., Cha, C., Zhang, J., Lin, H. and Guo, G. (2018). Spastin interacts with CRMP5 to promote neurite outgrowth by controlling the microtubule dynamics. Developmental Neurobiology, 78(12), 11911205. doi: 10.1002/dneu.22640 CrossRefGoogle ScholarPubMed
Jin, Z., Shou, H. F., Liu, J. W., Jiang, S. S., Shen, Y., Cheng, W. Y. and Gao, L. L. (2022). Spastin interacts with CRMP5 to promote spindle organization in mouse oocytes by severing microtubules. Zygote, 30(1), 8091. doi: 10.1017/S0967199421000344 CrossRefGoogle ScholarPubMed
Knowlton, A. L., Lan, W. and Stukenberg, P. T. (2006). Aurora B is enriched at merotelic attachment sites, where it regulates MCAK. Current Biology, 16(17), 17051710. doi: 10.1016/j.cub.2006.07.057 CrossRefGoogle ScholarPubMed
Loughlin, R., Wilbur, J. D., McNally, F. J., Nédélec, F. J. and Heald, R. (2011). Katanin contributes to interspecies spindle length scaling in Xenopus . Cell, 147(6), 13971407. doi: 10.1016/j.cell.2011.11.014 CrossRefGoogle ScholarPubMed
Nakamura, M. (2015). Microtubule nucleating and severing enzymes for modifying microtubule array organization and cell morphogenesis in response to environmental cues. New Phytologist, 205(3), 10221027. doi: 10.1111/nph.12932 CrossRefGoogle ScholarPubMed
Nakamura, M., Ehrhardt, D. W. and Hashimoto, T. (2010). Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nature Cell Biology, 12(11), 10641070. doi: 10.1038/ncb2110 CrossRefGoogle ScholarPubMed
Parra, M. T., Gómez, R., Viera, A., Page, J. A., Calvente, A., Wordeman, L., Rufas, J. S. and Suja, J. A. (2006). A perikinetochoric ring defined by MCAK and aurora-B as a novel centromere domain. PLOS Genetics, 2(6), e84. doi: 10.1371/journal.pgen.0020084 CrossRefGoogle ScholarPubMed
Pleuger, C., Fietz, D., Hartmann, K., Weidner, W., Kliesch, S., O’Bryan, M. K., Dorresteijn, A. and Bergmann, M. (2016). Expression of katanin p80 in human spermatogenesis. Fertility and Sterility, 106(7), 16831690.e1. doi: 10.1016/j.fertnstert.2016.08.043 CrossRefGoogle ScholarPubMed
Sharp, D. J. and Ross, J. L. (2012). Microtubule-severing enzymes at the cutting edge. Journal of Cell Science, 125(11), 25612569. doi: 10.1242/jcs.101139 Google ScholarPubMed
Shou, H. F., Jin, Z., Yu, Y., Lai, Y. C., Wu, Q. and Gao, L. L. (2022). Microtubule-severing protein Fidgetin-like 1 promotes spindle organization during meiosis of mouse oocytes. Zygote, 30(6), 872881. doi: 10.1017/S0967199422000417 CrossRefGoogle ScholarPubMed
Sonbuchner, T. M., Rath, U. and Sharp, D. J. (2010). KL1 is a novel microtubule severing enzyme that regulates mitotic spindle architecture. Cell Cycle, 9(12), 24032411. doi: 10.4161/cc.9.12.11916 CrossRefGoogle ScholarPubMed
Srayko, M., Buster, D. W., Bazirgan, O. A., McNally, F. J. and Mains, P. E. (2000). MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes and Development, 14(9), 10721084. doi: 10.1101/gad.14.9.1072 CrossRefGoogle ScholarPubMed
Srayko, M., O’Toole, E. T., Hyman, A. A. and Müller-Reichert, T. (2006). Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Current Biology, 16(19), 19441949. doi: 10.1016/j.cub.2006.08.029 CrossRefGoogle ScholarPubMed
Thomas, C., Cavazza, T. and Schuh, M. (2021). Aneuploidy in human eggs: Contributions of the meiotic spindle. Biochemical Society Transactions, 49(1), 107118. doi: 10.1042/BST20200043 CrossRefGoogle ScholarPubMed
Vale, R. D. (2000). AAA proteins. Lords of the ring. Journal of Cell Biology, 150(1), F13F19. doi: 10.1083/jcb.150.1.f13 CrossRefGoogle ScholarPubMed
Vietri, M., Schink, K. O., Campsteijn, C., Wegner, C. S., Schultz, S. W., Christ, L., Thoresen, S. B., Brech, A., Raiborg, C. and Stenmark, H. (2015). Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature, 522(7555), 231235. doi: 10.1038/nature14408 CrossRefGoogle ScholarPubMed
Webster, A. and Schuh, M. (2017). Mechanisms of aneuploidy in human eggs. Trends in Cell Biology, 27(1), 5568. doi: 10.1016/j.tcb.2016.09.002 CrossRefGoogle ScholarPubMed
Wu, Y., Li, M. and Yang, M. (2021). Post-translational modifications in oocyte maturation and embryo development. Frontiers in Cell and Developmental Biology, 9, 645318. doi: 10.3389/fcell.2021.645318 CrossRefGoogle ScholarPubMed
Zhang, D., Rogers, G. C., Buster, D. W. and Sharp, D. J. (2007). Three microtubule severing enzymes contribute to the “PacMan-flux” machinery that moves chromosomes. Journal of Cell Biology, 177(2), 231242. doi: 10.1083/jcb.200612011 CrossRefGoogle Scholar
Zhang, D., Grode, K. D., Stewman, S. F., Diaz-Valencia, J. D., Liebling, E., Rath, U., Riera, T., Currie, J. D., Buster, D. W., Asenjo, A. B., Sosa, H. J., Ross, J. L., Ma, A., Rogers, S. L. and Sharp, D. J. (2011). Drosophila katanin is a microtubule depolymerase that regulates cortical-microtubule plus-end interactions and cell migration. Nature Cell Biology, 13(4), 361370. doi: 10.1038/ncb2206 CrossRefGoogle ScholarPubMed