Knockdown of UCHL5IP causes abnormalities in γ-tubulin localisation, spindle organisation and chromosome alignment in mouse oocyte meiotic maturation
Ya-Peng Wang A B , Shu-Tao Qi A B , Yanchang Wei A , Zhao-Jia Ge A B , Lei Chen A B , Yi Hou A , Ying-Chun Ouyang A , Heide Schatten C , Jian-Guo Zhao A D and Qing-Yuan Sun A DA State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China.
B Graduate School, Chinese Academy of Sciences, Beijing, 100101, China.
C Department of Veterinary Pathobiology, University of Missouri, Columbia, MO 65203, USA.
D Corresponding authors. Emails: zhaojg@ioz.ac.cn; sunqy@ioz.ac.cn
Reproduction, Fertility and Development 25(3) 495-502 https://doi.org/10.1071/RD12300
Submitted: 20 April 2012 Accepted: 16 October 2012 Published: 27 November 2012
Abstract
UCHL5IP is one of the subunits of the haus complex, which is important for microtubule generation, spindle bipolarity and accurate chromosome segregation in Drosophila and human mitotic cells. In this study, the expression and localisation of UCHL5IP were explored, as well as its functions in mouse oocyte meiotic maturation. The results showed that the UCHL5IP protein level was consistent during oocyte maturation and it was localised to the meiotic spindle in MI and MII stages. Knockdown of UCHL5IP led to spindle defects, chromosome misalignment and disruption of γ-tubulin localisation in the spindle poles. These results suggest that UCHL5IP plays critical roles in spindle formation during mouse oocyte meiotic maturation.
Additional keywords: haus protein complex, meiosis.
References
Carazo-Salas, R. E., Guarguaglini, G., Gruss, O. J., Segref, A., Karsenti, E., and Mattaj, I. W. (1999). Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 400, 178–181.| Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXks1Khtrk%3D&md5=8c50032d4c6f47cefd2edae775fdd28bCAS | 10408446PubMed |
Goshima, G., and Kimura, A. (2010). New look inside the spindle: microtubule-dependent microtubule generation within the spindle. Curr. Opin. Cell Biol. 22, 44–49.
| New look inside the spindle: microtubule-dependent microtubule generation within the spindle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslWqsbg%3D&md5=36c73fb63d86bdc4be9e47a318e91592CAS | 20022736PubMed |
Goshima, G., Wollman, R., Goodwin, S. S., Zhang, N., Scholey, J. M., Vale, R. D., and Stuurman, N. (2007). Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316, 417–421.
| Genes required for mitotic spindle assembly in Drosophila S2 cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlSkurc%3D&md5=c52f6adda862ed3915226b57f444c0f7CAS | 17412918PubMed |
Goshima, G., Mayer, M., Zhang, N., Stuurman, N., and Vale, R. D. (2008). Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle. J. Cell Biol. 181, 421–429.
| Augmin: a protein complex required for centrosome-independent microtubule generation within the spindle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlsl2nu7g%3D&md5=96516a64c6b7497f42d3a91bb05b4763CAS | 18443220PubMed |
Kolano, A., Brunet, S., Silk, A. D., Cleveland, D. W., and Verlhac, M. H. (2012). Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension. Proc. Natl. Acad. Sci. USA 109, E1858–E1867.
| Error-prone mammalian female meiosis from silencing the spindle assembly checkpoint without normal interkinetochore tension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFChsbfL&md5=20fbff8ec0f42781fe20593d501a6ec2CAS | 22552228PubMed |
Kollman, J. M., Polka, J. K., Zelter, A., Davis, T. N., and Agard, D. A. (2010). Microtubule nucleating gamma-TuSC assembles structures with 13-fold microtubule-like symmetry. Nature 466, 879–882.
| Microtubule nucleating gamma-TuSC assembles structures with 13-fold microtubule-like symmetry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosl2rtLo%3D&md5=781646bbcb4126c9755aa6d28ecfd77aCAS | 20631709PubMed |
Lajoie-Mazenc, I., Tollon, Y., Detraves, C., Julian, M., Moisand, A., Gueth-Hallonet, C., Debec, A., Salles-Passador, I., Puget, A., Mazarguil, H., Raynaud-Messina, B., and Wright, M. (1994). Recruitment of antigenic gamma-tubulin during mitosis in animal cells: presence of gamma-tubulin in the mitotic spindle. J. Cell Sci. 107, 2825–2837.
| 1:CAS:528:DyaK2MXitVyns7c%3D&md5=3ed15cb1d399f5a9894a736ba6dc75a5CAS | 7876350PubMed |
Lane, S. I., Yun, Y., and Jones, K. T. (2012). Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule–kinetochore attachment but not by bivalent alignment or tension. Development 139, 1947–1955.
| Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule–kinetochore attachment but not by bivalent alignment or tension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVGlsLvP&md5=66d103dbaa4cca670dac790a962bb4e8CAS | 22513370PubMed |
Lawo, S., Bashkurov, M., Mullin, M., Ferreria, M. G., Kittler, R., Habermann, B., Tagliaferro, A., Poser, I., Hutchins, J. R., Hegemann, B., Pinchev, D., Buchholz, F., Peters, J. M., Hyman, A. A., Gingras, A. C., and Pelletier, L. (2009). HAUS, the 8-subunit human Augmin complex, regulates centrosome and spindle integrity. Curr. Biol. 19, 816–826.
| HAUS, the 8-subunit human Augmin complex, regulates centrosome and spindle integrity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmsVCgt7k%3D&md5=e9192e5b91c41cf98bb0761ac530c08bCAS | 19427217PubMed |
Li, M., Li, S., Yuan, J., Wang, Z. B., Sun, S. C., Schatten, H., and Sun, Q. Y. (2009). Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis. PLoS ONE 4, e7701.
| Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis.Crossref | GoogleScholarGoogle Scholar | 19888327PubMed |
Lüders, J., Patel, U. K., and Stearns, T. (2006). GCP-WD is a gamma-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation. Nat. Cell Biol. 8, 137–147.
| GCP-WD is a gamma-tubulin targeting factor required for centrosomal and chromatin-mediated microtubule nucleation.Crossref | GoogleScholarGoogle Scholar | 16378099PubMed |
Mahoney, N. M., Goshima, G., Douglass, A. D., and Vale, R. D. (2006). Making microtubules and mitotic spindles in cells without functional centrosomes. Curr. Biol. 16, 564–569.
| Making microtubules and mitotic spindles in cells without functional centrosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1ehtLo%3D&md5=90ee26ee565b6c5d8055fe9f102bc2a2CAS | 16546079PubMed |
Petry, S., Pugieux, C., Nedelec, F. J., and Vale, R. D. (2011). Augmin promotes meiotic spindle formation and bipolarity in Xenopus egg extracts. Proc. Natl. Acad. Sci. USA 108, 14 473–14 478.
| Augmin promotes meiotic spindle formation and bipolarity in Xenopus egg extracts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFCltbnO&md5=de2df466476fa23d46cfc4185203e3a1CAS |
Schuh, M., and Ellenberg, J. (2007). Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130, 484–498.
| Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptlyntbc%3D&md5=850d27e94cdf135e42ccf7ffa55e6d80CAS | 17693257PubMed |
Sun, Q. Y., and Schatten, H. (2006). Role of NuMA in vertebrate cells: review of an intriguing multifunctional protein. Front. Biosci. 11, 1137–1146.
| Role of NuMA in vertebrate cells: review of an intriguing multifunctional protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlSru77N&md5=d96b2288e47791178e2e9faee28d77bcCAS | 16146802PubMed |
Uehara, R., Nozawa, R. S., Tomioka, A., Petry, S., Vale, R. D., Obuse, C., and Goshima, G. (2009). The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells. Proc. Natl. Acad. Sci. USA 106, 6998–7003.
| The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFSgsbk%3D&md5=3364215e5419502228bcc70f59318577CAS | 19369198PubMed |
Wassmann, K., Niault, T., and Maro, B. (2003). Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes. Curr. Biol. 13, 1596–1608.
| Metaphase I arrest upon activation of the Mad2-dependent spindle checkpoint in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsVKrsr4%3D&md5=092d51fb6d96fc3114551a486d9ba16fCAS | 13678590PubMed |
Wei, L., Liang, X. W., Zhang, Q. H., Li, M., Yuan, J., Li, S., Sun, S. C., Ouyang, Y. C., Schatten, H., and Sun, Q. Y. (2010). BubR1 is a spindle assembly checkpoint protein regulating meiotic cell cycle progression of mouse oocytes. Cell Cycle 9, 1112–1121.
| BubR1 is a spindle assembly checkpoint protein regulating meiotic cell cycle progression of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12itr%2FJ&md5=7b737414127873b1ebedc5d4d4bd6754CAS | 20237433PubMed |
Wiese, C., and Zheng, Y. (2006). Microtubule nucleation: gamma-tubulin and beyond. J. Cell Sci. 119, 4143–4153.
| Microtubule nucleation: gamma-tubulin and beyond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1GksrnE&md5=93ab4e88c911f85702b6588e9c5ac153CAS | 17038541PubMed |
Yin, S., Sun, X. F., Schatten, H., and Sun, Q. Y. (2008). Molecular insights into mechanisms regulating faithful chromosome separation in female meiosis. Cell Cycle 7, 2997–3005.
| Molecular insights into mechanisms regulating faithful chromosome separation in female meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVOgsrrE&md5=70f8418646378a1930b0d6909f5c94e3CAS | 18802407PubMed |