Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T13:30:51.006Z Has data issue: false hasContentIssue false
  • English
  • Français

Microtubule-severing protein Fidgetin-like 1 promotes spindle organization during meiosis of mouse oocytes

Published online by Cambridge University Press:  23 September 2022

Hua-Feng Shou ,
Zhen Jin ,
Yan Yu ,
Yu-Cheng Lai ,
Qing Wu  and
Lei-Lei Gao Open the ORCID record for Lei-Lei Gao [Opens in a new window]
Hua-Feng Shou
Affiliation:
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital, (Affiliated People’s Hospital, Hangzhou Medical College), Hangzhou, Zhejiang310014, China
Zhen Jin
Affiliation:
Center for Reproductive Medicine, Department of Reproductive Endocrinology, Zhejiang Provincial People’s Hospital, (Affiliated People’s Hospital, Hangzhou Medical College), Hangzhou, Zhejiang310014, China
Yan Yu
Affiliation:
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital, (Affiliated People’s Hospital, Hangzhou Medical College), Hangzhou, Zhejiang310014, China
Yu-Cheng Lai
Affiliation:
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital, (Affiliated People’s Hospital, Hangzhou Medical College), Hangzhou, Zhejiang310014, China
Qing Wu
Affiliation:
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital, (Affiliated People’s Hospital, Hangzhou Medical College), Hangzhou, Zhejiang310014, China
Lei-Lei Gao*
Affiliation:
Center for Reproductive Medicine, Department of Gynecology, Zhejiang Provincial People’s Hospital, (Affiliated People’s Hospital, Hangzhou Medical College), Hangzhou, Zhejiang310014, China
*
Author for correspondence: Lei-Lei Gao. Department of Gynecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Microtubule-severing proteins (MTSPs) play important roles in mitosis and interphase. However, to the best of our knowledge, no previous studies have evaluated the role of MTSPs in female meiosis in mammals. It was found that FIGNL1, a member of MTSPs, was predominantly expressed in mouse oocytes and distributed at the spindle poles during meiosis in the present study. FIGNL1 was co-localized and interacted with γ-tubulin, an important component of the microtubule tissue centre (MTOC). Fignl1 knockdown by specific small interfering RNA caused spindle defects characterized by an abnormal length:width ratio and decreased microtubule density, which consequently led to aberrant chromosome arrangement, oocyte maturation and fertilization obstacles. In conclusion, the present results suggested that FIGNL1 may be an essential factor in oocyte maturation by influencing the meiosis process via the formation of spindles.

Keywords

MeiosisMicrotubuleMicrotubule-severing proteinsOocyteSpindle
Type
Research Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 872 - 881
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Beard, S. M., Smit, R. B., Chan, B. G. and Mains, P. E. (2016). Regulation of the MEI-1/MEI-2 microtubule-severing katanin complex in early Caenorhabditis elegans development. G3, 6 (10), 3257–3268. doi: 10.1534/g3.116.031666 CrossRefGoogle ScholarPubMed
Brouhard, G. J. (2015). Dynamic instability 30 years later: Complexities in microtubule growth and catastrophe. Molecular Biology of the Cell, 26(7), 1207–1210. doi: 10.1091/mbc.E13-10-0594 CrossRefGoogle ScholarPubMed
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), 1083–1092. doi: 10.1242/jcs.115.5.1083 CrossRefGoogle ScholarPubMed
Caburet, S., Arboleda, V. A., Llano, E., Overbeek, P. A., Barbero, J. L., Oka, K., Harrison, W., Vaiman, D., Ben-Neriah, Z., García-Tuñón, I., Fellous, M., Pendás, A. M., Veitia, R. A. and Vilain, E. (2014). Mutant cohesin in premature ovarian failure. New England Journal of Medicine, 370(10), 943–949. doi: 10.1056/NEJMoa1309635 CrossRefGoogle ScholarPubMed
Chen, B., Zhang, Z., Sun, X., Kuang, Y., Mao, X., Wang, X., Yan, Z., Li, B., Xu, Y., Yu, M., Fu, J., Mu, J., Zhou, Z., Li, Q., Jin, L., He, L., Sang, Q. and Wang, L. (2017). Biallelic mutations in PATL2 cause female infertility characterized by oocyte maturation arrest. American Journal of Human Genetics, 101(4), 609–615. doi: 10.1016/j.ajhg.2017.08.018 CrossRefGoogle ScholarPubMed
Connolly, A. A., Osterberg, V., Christensen, S., Price, M., Lu, C., Chicas-Cruz, K., Lockery, S., Mains, P. E. and Bowerman, B. (2014). Caenorhabditis elegans oocyte meiotic spindle pole assembly requires microtubule severing and the calponin homology domain protein ASPM-1. Molecular Biology of the Cell, 25(8), 1298–1311. doi: 10.1091/mbc.E13-11-0687 CrossRefGoogle ScholarPubMed
Coralie, F., Amélie, F., Laïla, G., Christian, D., Daniel, T. M., Stéphanie, D. G., Monica, T., Christophe, B., Philippe, M., Céline, R., Leticia, P., Susanne, B., Sylvie, S. M., Corinne, H., Fatiha, N., Jean-Christophe, L., Annie, A. and Jamilé, H. (2018). Motor axon navigation relies on Fidgetin-like 1-driven microtubule plus end dynamics. Journal of Cell Biology, 5, 1719–1738 Google Scholar
Cox, G. A., Mahaffey, C. L., Nystuen, A., Letts, V. A. and Frankel, W. N. (2000). The mouse fidgetin gene defines a new role for AAA family proteins in mammalian development. Nature Genetics, 26(2), 198–202. doi: 10.1038/79923 CrossRefGoogle ScholarPubMed
Edlinger, B. and Schlögelhofer, P. (2011). Have a break: Determinants of meiotic DNA double strand break (DSB) formation and processing in plants. Journal of Experimental Botany, 62(5), 1545–1563. doi: 10.1093/jxb/erq421 CrossRefGoogle ScholarPubMed
Eot-Houllier, G., Venoux, M., Vidal-Eychenié, S., Hoang, M. T., Giorgi, D. and Rouquier, S. (2010). Plk1 regulates both ASAP localization and its role in spindle pole integrity. Journal of Biological Chemistry, 285(38), 29556–29568. doi: 10.1074/jbc.M110.144220 CrossRefGoogle ScholarPubMed
Errico, A., Ballabio, A. and Rugarli, E. I. (2002). Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia is involved in microtubule dynamics. Human Molecular Genetics, 11(2), 153–163. doi: 10.1093/hmg/11.2.153 CrossRefGoogle ScholarPubMed
Errico, A., Claudiani, P., D’Addio, M. and Rugarli, E. I. (2004). Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. Human Molecular Genetics, 13(18), 2121–2132. doi: 10.1093/hmg/ddh223 CrossRefGoogle ScholarPubMed
Feng, R., Sang, Q., Kuang, Y., Sun, X., Yan, Z., Zhang, S., Shi, J., Tian, G., Luchniak, A., Fukuda, Y., Li, B., Yu, M., Chen, J., Xu, Y., Guo, L., Qu, R., Wang, X., Sun, Z., Liu, M., et al. (2006). Mutations in TUBB8 and human oocyte meiotic arrest. New England Journal of Medicine, 3, 223–232 Google Scholar
Filges, I., Manokhina, I., Peñaherrera, M. S., McFadden, D. E., Louie, K., Nosova, E., Friedman, J. M. and Robinson, W. P. (2015). Recurrent triploidy due to a failure to complete maternal meiosis II: whole-exome sequencing reveals candidate variants. Molecular Human Reproduction, 21(4), 339–346. doi: 10.1093/molehr/gau112 CrossRefGoogle ScholarPubMed
Friel, C. T. and Howard, J. (2011). The kinesin-13 MCAK has an unconventional ATPase cycle adapted for microtubule depolymerization. EMBO Journal, 30(19), 3928–3939. doi: 10.1038/emboj.2011.290 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), 3573–3582. doi: 10.3892/mmr.2019.10605 Google Scholar
Gardner, M. K., Zanic, M. and Howard, J. (2013). Microtubule catastrophe and rescue. Current Opinion in Cell Biology, 25(1), 14–22. doi: 10.1016/j.ceb.2012.09.006 CrossRefGoogle ScholarPubMed
Govindaraj, V. and Rao, A. J. (2015). Comparative proteomic analysis of primordial follicles from ovaries of immature and aged rats. Systems Biology in Reproductive Medicine, 61(6), 367–375. doi: 10.3109/19396368.2015.1077903 CrossRefGoogle ScholarPubMed
Hartman, J. J., Mahr, J., McNally, K., Okawa, K., Iwamatsu, A., Thomas, S., Cheesman, S., Heuser, J., Vale, R. D. and McNally, F. J. (1998). Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell, 93(2), 277–287. doi: 10.1016/s0092-8674(00)81578-0 CrossRefGoogle Scholar
Hazan, J., Fonknechten, N., Mavel, D., Paternotte, C., Samson, D., Artiguenave, F., Davoine, C. S., Cruaud, C., Dürr, A., Wincker, P., Brottier, P., Cattolico, L., Barbe, V. and Burgunder, J. M., Prud’homme, J. F., Brice, A., Fontaine, B., Heilig, B. and Weissenbach, J. (1999) Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nature Genetics, 23(3), 296–303. doi: 10.1038/15472.CrossRefGoogle ScholarPubMed
Howard, J. and Hyman, A. A. (2007). Microtubule polymerases and depolymerases. Current Opinion in Cell Biology, 19(1), 31–35. doi: 10.1016/j.ceb.2006.12.009 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), 80–91. doi: 10.1017/S0967199421000344 CrossRefGoogle ScholarPubMed
Johjima, A., Noi, K., Nishikori, S., Ogi, H., Esaki, M. and Ogura, T. (2015). Microtubule severing by katanin p60 AAA+ ATPase requires the C-terminal acidic tails of both α- and β-tubulins and basic amino acid residues in the AAA+ ring pore. Journal of Biological Chemistry, 290(18), 11762–11770. doi: 10.1074/jbc.M114.614768 CrossRefGoogle ScholarPubMed
Joly, N., Martino, L., Gigant, E., Dumont, J. and Pintard, L. (2016). Microtubule-severing activity of the AAAþ ATPase katanin is essential for female meiotic spindle assembly. Development, 143(19), 3604–3614. doi: 10.1242/dev.140830 Google ScholarPubMed
Kim, K. P. and Mirkin, E. V. (2018). So similar yet so different: The two ends of a double strand break. Mutation Research, 809, 70–80. doi: 10.1016/j.mrfmmm.2017.06.007 CrossRefGoogle ScholarPubMed
Kim, J. S., Kim, E. J., Oh, J. S., Park, I. C. and Hwang, S. G. (2013). CIP2A modulates cell-cycle progression in human cancer cells by regulating the stability and activity of Plk1. Cancer Research, 73(22), 6667–6678. doi: 10.1158/0008-5472.CAN-13-0888 CrossRefGoogle ScholarPubMed
Kogo, H., Kowa-Sugiyama, H., Yamada, K., Bolor, H., Tsutsumi, M., Ohye, T., Inagaki, H., Taniguchi, M., Toda, T. and Kurahashi, H. (2010). Screening of genes involved in chromosome segregation during meiosis I: toward the identification of genes responsible for infertility in humans. Journal of Human Genetics, 55(5), 293–299. doi: 10.1038/jhg.2010.26 CrossRefGoogle ScholarPubMed
Lantzsch, I., Yu, C. H., Chen, Y. Z. and Redemann, S. (2021). Microtubule reorganization during female meiosis in C. elegans . eLife, 11, 10 Google Scholar
Lee, H. (2006). How chromosome mis-segregation leads to cancer: Lessons from BubR1 mouse models. Molecules and Cells, 10, 713–718 Google Scholar
L’Hôte, D., Vatin, M., Auer, J., Castille, J., Passet, B., Montagutelli, X., Serres, C. and Vaiman, D. (2011). Fidgetin-like1 is a strong candidate for a dynamic impairment of male meiosis leading to reduced testis weight in mice. PLOS ONE, 6(11), e27582. doi: 10.1371/journal.pone.0027582 CrossRefGoogle ScholarPubMed
Luke-Glaser, S., Pintard, L., Tyers, M. and Peter, M. (2007). The AAA-ATPase FIGL-1 controls mitotic progression, and its levels are regulated by the CUL-3MEL-26 E3 ligase in the C. elegans germ line. Journal of Cell Science, 120(18), 3179–3187. doi: 10.1242/jcs.015883 CrossRefGoogle ScholarPubMed
Ma, J., Li, J., Yao, X., Lin, S., Gu, Y., Xu, J., Deng, Z., Ma, W. and Zhang, H. (2017). FIGNL1 is overexpressed in small cell lung cancer patients and enhances NCI-H446 cell resistance to cisplatin and etoposide. Oncology Reports, 37(4), 1935–1942. doi: 10.3892/or.2017.5483 CrossRefGoogle ScholarPubMed
Matsuzaki, K., Kondo, S., Ishikawa, T. and Shinohara, A. (2019). Human RAD51 paralogue SWSAP1 fosters RAD51 filament by regulating the anti-recombinase FIGNL1 AAA+ ATPase. Nature Communications, 10(1), 1407. doi: 10.1038/s41467-019-09190-1 CrossRefGoogle ScholarPubMed
McNally, F. J. and Vale, R. D. (1993). Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell, 75(3), 419–429. doi: 10.1016/0092-8674(93)90377-3 CrossRefGoogle ScholarPubMed
McNally, K., Berg, E., Cortes, D. B., Hernandez, V., Mains, P. E. and McNally, F. J. (2014). Katanin maintains meiotic metaphase chromosome alignment and spindle structure in vivo and has multiple effects on microtubules in vitro. Molecular Biology of the Cell, 25(7), 1037–1049. doi: 10.1091/mbc.E13-12-0764 CrossRefGoogle ScholarPubMed
Meraldi, P., Honda, R. and Nigg, E. A. (2004). Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Current Opinion in Genetics and Development, 14(1), 29–36. doi: 10.1016/j.gde.2003.11.006 CrossRefGoogle ScholarPubMed
Monroe, N. and Hill, C. P. (2016). Meiotic clade AAA ATPases: Protein polymer disassembly machines. Journal of Molecular Biology, 428(9 Pt B), 1897–1911. doi: 10.1016/j.jmb.2015.11.004 CrossRefGoogle ScholarPubMed
Mukherjee, S., Diaz Valencia, J. D., Stewman, S., Metz, J., Monnier, S., Rath, U., Asenjo, A. B., Charafeddine, R. A., Sosa, H. J., Ross, J. L., Ma, A. and Sharp, D. J. (2012). Human Fidgetin is a microtubule severing the enzyme and minus-end depolymerase that regulates mitosis. Cell Cycle, 11(12), 2359–2366. doi: 10.4161/cc.20849 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), 1064–1070. doi: 10.1038/ncb2110 CrossRefGoogle ScholarPubMed
Nguyen, A. L., Marin, D., Zhou, A., Gentilello, A. S., Smoak, E. M., Cao, Z., Fedick, A., Wang, Y., Taylor, D., Scott, R. T., Xing, J., Treff, N. and Schindler, K. (2017). Identification and characterization of Aurora kinase B and C variants associated with maternal aneuploidy. MHR: Basic Science of Reproductive Medicine, 23(6), 406–416. doi: 10.1093/molehr/gax018 Google Scholar
Nogales, E. and Wang, H. W. (2006). Structural intermediates in microtubule assembly and disassembly: How and why? Current Opinion in Cell Biology, 18(2), 179–184. doi: 10.1016/j.ceb.2006.02.009 CrossRefGoogle ScholarPubMed
Patel, H., Zich, J., Serrels, B., Rickman, C., Hardwick, K. G., Frame, M. C. and Brunton, V. G. (2013). Kindlin-1 regulates mitotic spindle formation by interacting with integrins and Plk-1. Nature Communications, 4, 2056. doi: 10.1038/ncomms3056 CrossRefGoogle ScholarPubMed
Pimenta-Marques, A., Bento, I., Lopes, C. A., Duarte, P., Jana, S. C. and Bettencourt-Dias, M. (2016). A mechanism for the elimination of the female gamete centrosome in Drosophila melanogaster . Science, 353(6294), aaf4866. doi: 10.1126/science.aaf4866 CrossRefGoogle ScholarPubMed
Rath, U. and Sharp, D. J. (2011). The molecular basis of anaphase A in animal cells. Chromosome Research, 19(3), 423–432. doi: 10.1007/s10577-011-9199-2 CrossRefGoogle ScholarPubMed
Rogers, G. C., Rogers, S. L., Schwimmer, T. A., Ems-McClung, S. C., Walczak, C. E., Vale, R. D., Scholey, J. M. and Sharp, D. J. (2004). Two mitotic kinesins cooperate to drive sister chromatid separation during anaphase. Nature, 427(6972), 364–370. doi: 10.1038/nature02256 CrossRefGoogle ScholarPubMed
Roll-Mecak, A. and McNally, F. J. (2010). Microtubule-severing enzymes. Current Opinion in Cell Biology, 22(1), 96–103. doi: 10.1016/j.ceb.2009.11.001 CrossRefGoogle ScholarPubMed
Roll-Mecak, A. and Vale, R. D. (2008). Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin. Nature, 451(7176), 363–367. doi: 10.1038/nature06482 CrossRefGoogle ScholarPubMed
Rose, L., Wilbur, J. D., McNally, F. J. and François, J. (2011). Nédélec, Rebecca Heald. Katanin contributes to interspecies spindle length scaling in Xenopus. Cell, 6, 1397–1407.Google Scholar
Schaedel, L., John, K., Gaillard, J., Nachury, M. V., Blanchoin, L. and Théry, M. (2015). Microtubules self-repair in response to mechanical stress. Nature Materials, 14(11), 1156–1163. doi: 10.1038/nmat4396 CrossRefGoogle ScholarPubMed
Schaedel, L., Triclin, S., Chrétien, D., Abrieu, A., Aumeier, C., Gaillard, J., Blanchoin, L., Théry, M. and John, K. (2019). Lattice defects induce microtubule self-renewal. Nature Physics, 15(8), 830–838. doi: 10.1038/s41567-019-0542-4 CrossRefGoogle ScholarPubMed
Sharma, N., Bryant, J., Wloga, D., Donaldson, R., Davis, R. C., Jerka-Dziadosz, M. and Gaertig, J. (2007). Katanin regulates dynamics of microtubules and biogenesis of motile cilia. Journal of Cell Biology, 178(6), 1065–1079. doi: 10.1083/jcb.200704021 CrossRefGoogle ScholarPubMed
Sharp, D. J. and Ross, J. L. (2012). Microtubule-severing enzymes at the cutting edge. Journal of Cell Science, 125(11), 2561–2569. doi: 10.1242/jcs.101139 Google ScholarPubMed
Smith, L. B., Milne, L., Nelson, N., Eddie, S., Brown, P., Atanassova, N., O’Bryan, M. K., O’Donnell, L., Rhodes, D., Wells, S., Napper, D., Nolan, P., Lalanne, Z., Cheeseman, M. and Peters, J. (2012). KATNAL1 regulation of Sertoli cell microtubule dynamics is essential for spermiogenesis and male fertility. PLOS Genetics, 8(5), e1002697. doi: 10.1371/journal.pgen.1002697 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), 2403–2411. 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), 1072–1084. 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), 1944–1949. doi: 10.1016/j.cub.2006.08.029 CrossRefGoogle ScholarPubMed
Tanenbaum, M. E., Macurek, L., van der Vaart, B., Galli, M., Akhmanova, A. and Medema, R. H. (2011). A complex of Kif18b and MCAK promotes microtubule depolymerization and is negatively regulated by Aurora kinases. Current Biology, 21(16), 1356–1365. doi: 10.1016/j.cub.2011.07.017 CrossRefGoogle ScholarPubMed
Vale, R. D. (2000). AAA proteins. Lords of the ring. Journal of Cell Biology, 150(1), F13–F19. doi: 10.1083/jcb.150.1.f13 CrossRefGoogle Scholar
Vemu, A., Szczesna, E., Zehr, E. A., Spector, J. O., Grigorieff, N., Deaconescu, A. M. and Roll-Mecak, A. (2018). Severing enzymes amplify microtubule arrays through lattice GTP-tubulin incorporation. Science, 361(6404), 1504. doi: 10.1126/science.aau1504 CrossRefGoogle ScholarPubMed
Ververis, A., Christodoulou, A., Christoforou, M., Kamilari, C., Lederer, C. W. and Santama, N. (2016). A novel family of katanin-like 2 protein isoforms (KATNAL2), interacting with nucleotide-binding proteins Nubp1 and Nubp2, are key regulators of different MT-based processes in mammalian cells. Cellular and Molecular Life Sciences, 73(1), 163–184. doi: 10.1007/s00018-015-1980-5 CrossRefGoogle Scholar
Walczak, C. E. and Heald, R. (2008). Mechanisms of mitotic spindle assembly and function. International Review of Cytology, 265, 111–158. doi: 10.1016/S0074-7696(07)65003-7 CrossRefGoogle ScholarPubMed
Wiese, C. and Zheng, Y. (2000). A new function for the gamma-tubulin ring com- plex as a microtubule minus-end cap. Nature Cell Biology, 2(6), 358–364. doi: 10.1038/35014051 CrossRefGoogle Scholar
Wordeman, L. (2005). Microtubule-depolymerizing kinesins. Current Opinion in Cell Biology, 17(1), 82–88. doi: 10.1016/j.ceb.2004.12.003 CrossRefGoogle ScholarPubMed
Yang, H. Y., McNally, K. and McNally, F. J. (2003). MEI-1/katanin is required for translocation of the meiosis I spindle to the oocyte cortex in C. elegans. Developmental Biology, 260(1), 245–259. doi: 10.1016/S0012-1606(03)00216-1 CrossRefGoogle Scholar
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), 231–242. doi: 10.1083/jcb.200612011 CrossRefGoogle Scholar
Zhao, X., Jin, M., Wang, M., Sun, L., Hong, X., Cao, Y. and Wang, C. (2016). Fidgetin-like 1 is a ciliogenesis-inhibitory centrosome protein. Cell Cycle, 15(17), 2367–2375. doi: 10.1080/15384101.2016.1204059 CrossRefGoogle ScholarPubMed
Supplementary material: File

Shou et al. supplementary material

Shou et al. supplementary material

Download Shou et al. supplementary material(File)
File 533 KB