Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-25T15:58:18.940Z Has data issue: false hasContentIssue false

Spastin interacts with CRMP5 to promote spindle organization in mouse oocytes by severing microtubules

Published online by Cambridge University Press:  26 May 2021

Zhen Jin
Affiliation:
Department of Reproductive Endocrinology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China
Hua-Feng Shou
Affiliation:
Department of Gynaecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China
Jin-Wei Liu
Affiliation:
Department of Gynaecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China
Shan-Shan Jiang
Affiliation:
Department of Gynaecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China
Yan Shen
Affiliation:
Department of Gynaecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China
Wei-Ye Cheng
Affiliation:
Department of Gynaecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China
Lei-Lei Gao*
Affiliation:
Department of Gynaecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China
*
Author for correspondence: Lei-Lei Gao. Department of Gynaecology, Zhejiang Provincial People’s Hospital, People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang310014, China. Email: [email protected]

Abstract

Microtubule-severing protein (MTSP) is critical for the survival of both mitotic and postmitotic cells. However, the study of MTSP during meiosis of mammalian oocytes has not been reported. We found that spastin, a member of the MTSP family, was highly expressed in oocytes and aggregated in spindle microtubules. After knocking down spastin by specific siRNA, the spindle microtubule density of meiotic oocytes decreased significantly. When the oocytes were cultured in vitro, the oocytes lacking spastin showed an obvious maturation disorder. Considering the microtubule-severing activity of spastin, we speculate that spastin on spindles may increase the number of microtubule broken ends by severing the microtubules, therefore playing a nucleating role, promoting spindle assembly and ensuring normal meiosis. In addition, we found the colocalization and interaction of collapsin response mediator protein 5 (CRMP5) and spastin in oocytes. CRMP5 can provide structural support and promote microtubule aggregation, creating transportation routes, and can interact with spastin in the microtubule activity of nerve cells (30). Knocking down CRMP5 may lead to spindle abnormalities and developmental disorders in oocytes. Overexpression of spastin may reverse the abnormal phenotype caused by the deletion of CRMP5. In summary, our data support a model in which the interaction between spastin and CRMP5 promotes the assembly of spindle microtubules in oocytes by controlling microtubule dynamics, therefore ensuring normal meiosis.

Type
Research Article
Copyright
© The Author(s), 2021. 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

Ahmad, FJ, Yu, W, McNally, FJ and Baas, PW (1999). An essential role for katanin in severing microtubules in the neuron. J Cell Biol 145, 305–15.CrossRefGoogle ScholarPubMed
Banks, G, Lassi, G, Hoerder-Suabedissen, A, Tinarelli, F, Simon, MM and Wilcox, A (2018). A missense mutation in Katnal1 underlies behavioural, neurological and ciliary anomalies. Mol Psychiatry 23, 713–22.CrossRefGoogle ScholarPubMed
Beard, SM, Smit, RB, Chan, BG and Mains, PE (2016). Regulation of the MEI-1/MEI-2 microtubule-severing katanin complex in early Caenorhabditis elegans development. G3 (Bethesda) 6, 3257–68.CrossRefGoogle ScholarPubMed
Brouhard, GJ (2015). Dynamic instability 30 years later: complexities in microtubule growth and catastrophe. Mol Biol Cell 26, 1207–10.CrossRefGoogle ScholarPubMed
Buster, D, McNally, K and McNally, FJ (2002). Katanin inhibition prevents the redistribution of gamma-tubulin at mitosis. J Cell Sci 115, 1083–92.CrossRefGoogle ScholarPubMed
Clark-Maguire, S and Mains, PE (1994). Localization of the mei-1 gene product of Caenorhaditis elegans, a meiotic-specific spindle component. J Cell Biol 126, 199209.CrossRefGoogle ScholarPubMed
Eckert, T, Le, DT, Link, S, Friedmann, L and Woehlke, G (2012). Spastin’s microtubule-binding properties and comparison to katanin. PLoS One 7, e50161.CrossRefGoogle ScholarPubMed
Errico, A, Ballabio, A and Rugarli, EI (2002). Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet 11, 153–63.CrossRefGoogle ScholarPubMed
Errico, A, Claudiani, P, D’Addio, M and Rugarli, EI (2004). Spastin interacts with the centrosomal protein NA14, and is enriched in the spindle pole, the midbody and the distal axon. Hum Mol Genet 13, 2121–32.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, Shi, H, Wang, H, Feng, Y, Shao, R, Chai, R, Li, Q, Xing, Q, Zhang, R, Nogales, E, Jin, L, He, L, Gupta, ML Jr, Cowan, NJ and Wang, L (2016). Mutations in TUBB8 and human oocyte meiotic arrest. N Engl J Med 374, 223–32.CrossRefGoogle ScholarPubMed
Filges, I, Manokhina, I, Peñaherrera, MS, McFadden, DE, Louie, K, Nosova, E, Friedman, JM and Robinson, WP (2015). Recurrent triploidy due to a failure to complete maternal meiosis II: whole-exome sequencing reveals candidate variants. Mol Hum Reprod 21, 339–46.CrossRefGoogle ScholarPubMed
Frickey, T and Lupas, AN (2004). Phylogenetic analysis of AAA proteins. J Struct Biol 146, 210.CrossRefGoogle ScholarPubMed
Friel, CT and Howard, J (2011). The kinesin-13 MCAK has an unconventional ATPase cycle adapted for microtubule depolymerization. EMBO J 30, 3928–39.CrossRefGoogle ScholarPubMed
Gardner, MK, Zanic, M and Howard, J (2013). Microtubule catastrophe and rescue. Curr Opin Cell Biol 25, 1422.CrossRefGoogle ScholarPubMed
Han, X, Wen, H, Ju, X, Chen, X, Ke, G, Zhou, Y, Li, J, Xia, L, Tang, J and Liang, S (2017). Predictive factors of para-aortic lymph nodes metastasis in cervical cancer patients: a retrospective analysis based on 723 para-aortic lymphadenectomy cases. Oncotarget 8, 51840–7.CrossRefGoogle ScholarPubMed
Hartman, JJ, Mahr, J, McNally, K, Okawa, K, Iwamatsu, A, Thomas, S, Cheesman, S, Heuser, J, Vale, RD and McNally, FJ (1998). Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell 93, 277–87.CrossRefGoogle Scholar
Hazan, J, Fonknechten, N, Mavel, D, Paternotte, C, Samson, D, Artiguenave, F, Davoine, CS, Cruaud, C, Dürr, A, Wincker, P, Brottier, P, Cattolico, L, Barbe, V, Burgunder, JM, Prud’homme, JF, 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. Nat Genet 23, 296303.CrossRefGoogle ScholarPubMed
Howard, J and Hyman, AA (2007). Microtubule polymerases and depolymerases. Curr Opin Cell Biol 19, 31–5.CrossRefGoogle ScholarPubMed
Ji, Z, Zhang, G, Chen, L and Guo, G (2018). Spastin interacts with CRMP5 to promote neurite outgrowth by controlling microtubule dynamics. Dev Neurobiol 12, 1191–205.CrossRefGoogle Scholar
Jin, ZL, Suk, N and Kim, NH (2019). TP53BP1 regulates chromosome alignment and spindle bipolarity in mouse oocytes. Mol Reprod Dev 86, 1126–37.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. J Biol Chem 290, 11762–70.CrossRefGoogle ScholarPubMed
Joly, N, Martino, L, Gigant, E and Pintard, L (2016). Microtubule-severing activity of the AAA+ ATPase katanin is essential for female meiotic spindle assembly. Development 143, 3604–14.Google ScholarPubMed
Karabay, A, Yu, W, Solowska, JM, Baird, DH and Baas, PW (2004). Axonal growth is sensitive to the levels of katanin, a protein that severs microtubules. J Neurosci 24, 5778–88.CrossRefGoogle Scholar
Kelle, D, Kırımtay, K, Selçuk, E and Karabay, A (2019). Elk1 affects katanin and spastin proteins via differential transcriptional and post-transcriptional regulations. PLoS One 14, e0212518.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. J Hum Genet 55, 293–9.CrossRefGoogle ScholarPubMed
Lee, H (2014). How chromosome mis-segregation leads to cancer: lessons from BubR1 mouse models. Mol Cell 37, 713–8.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. J Cell Sci 120, 3179–87.CrossRefGoogle ScholarPubMed
Mao, CX, Xiong, Y, Xiong, Z, Wang, Q, Zhang, YQ and Jin, S (2014). Microtubule-severing protein Katanin regulates neuromuscular junction development and dendritic elaboration in Drosophila . Development 141, 1064–74.CrossRefGoogle ScholarPubMed
McNally, K, Berg, E, Cortes, DB and McNally, FJ (2014). Katanin maintains meiotic metaphase chromosome alignment and spindle structure in vivo and has multiple effects on microtubules in vitro . Mol Biol Cell 25, 1037–49.CrossRefGoogle ScholarPubMed
Meraldi, P, Honda, R and Nigg, EA (2004). Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr Opin Genet Dev 14, 2936.CrossRefGoogle ScholarPubMed
Mishra-Gorur, K, Caglayan, AO, Schaffer, AE, Chabu, C, Henegariu, O and Vonhoff, F (2014). Mutations in KATNB1 cause complex cerebral malformations by disrupting asymmetrically dividing neural progenitors. Neuron 84, 1226–39.CrossRefGoogle ScholarPubMed
Monroe, N and Hill, CP (2016). Meiotic clade AAA ATPases: protein polymer disassembly machines. J Mol Biol 428, 1897–911.CrossRefGoogle ScholarPubMed
Mukherjee, S, Diaz Valencia, JD, Stewman, S, Metz, J, Monnier, S, Rath, U, Asenjo, AB, Charafeddine, RA, Sosa, HJ, Ross, JL, Ma, A and Sharp, DJ (2012). Human fidgetin is a microtubule severing the enzyme and minus-end depolymerase that regulates mitosis. Cell Cycle 11, 2359–66.CrossRefGoogle ScholarPubMed
Nogales, E and Wang, HW (2006). Structural intermediates in microtubule assembly and disassembly: how and why? Curr Opin Cell Biol 18, 179–84.CrossRefGoogle ScholarPubMed
Qiang, L, Yu, W, Andreadis, A, Luo, M and Baas, PW (2006). Tau protects microtubules in the axon from severing by katanin. J Neurosci 26, 3120–9.CrossRefGoogle ScholarPubMed
Roll-Mecak, A and McNally, FJ (2010). Microtubule-severing enzymes. Curr Opin Cell Biol 22, 96103.CrossRefGoogle ScholarPubMed
Roll-Mecak, A and Vale, RD (2008). Structural basis of microtubule severing by the hereditary spastic paraplegia protein spastin. Nature 451, 363–7.CrossRefGoogle ScholarPubMed
Sharp, DJ and Ross, JL (2012). Microtubule-severing enzymes at the cutting edge. J Cell Sci 125, 2561–9.Google ScholarPubMed
Sonbuchner, TM, Rath, U and Sharp, DJ (2010). KL1 is a novel microtubule severing enzyme that regulates mitotic spindle architecture. Cell Cycle 9, 24032411.CrossRefGoogle ScholarPubMed
Srayko, M, Buster, DW, Bazirgan, OA and Mains, PE (2000). MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev 14, 1072–84.CrossRefGoogle ScholarPubMed
Srayko, M, O’Toole, ET, Hyman, AA and Müller-Reichert, T (2006). Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr Biol 16, 1944–9.CrossRefGoogle ScholarPubMed
Tanenbaum, ME, Macurek, L, van der Vaart, B, Galli, M, Akhmanova, A and Medema, RH (2011). A complex of Kif18b and MCAK promotes microtubule depolymerization and is negatively regulated by Aurora kinases. Curr Biol 21, 1356–65.CrossRefGoogle ScholarPubMed
Vale, RD (2000). AAA proteins. Lords of the ring. J Cell Biol 150, F1319.CrossRefGoogle Scholar
Ververis, A, Christodoulou, A, Christoforou, M, Kamilari, C, Lederer, CW 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. Cell Mol Life Sci 73, 163–84.CrossRefGoogle Scholar
Wordeman, L (2005). Microtubule-depolymerizing kinesins. Curr Opin Cell Biol 17, 8288.CrossRefGoogle ScholarPubMed
Yu, W, Qiang, L, Solowska, JM, Karabay, A, Korulu, S and Baas, PW (2008). The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol Biol Cell 19, 1485–98.CrossRefGoogle ScholarPubMed
Zhang, D, Rogers, GC, Buster, DW and Sharp, DJ (2007). Three microtubule severing enzymes contribute to the ‘Pacman-flux’ machinery that moves chromosomes. J Cell Biol 177, 231–42.CrossRefGoogle Scholar
Supplementary material: File

Jin et al. supplementary material

Figure S1

Download Jin et al. supplementary material(File)
File 941.3 KB