Dynamics of microtubules, motor proteins and 20S proteasomes during bovine oocyte IVM
S. E. Racedo A C , M. C. Branzini B , D. Salamone A , C. Wójcik D , V. Y. Rawe B and H. Niemann C EA Laboratorio de Biotecnología Animal, Facultad de Agronomía, Universidad de Buenos Aires, Av. San Martin 4453 (C1417DSE), Buenos Aires, Argentina.
B Centro de Estudios en Ginecología y Reproducción, CEGyR, Viamonte 1432 (C1055ABB), Buenos Aires, Argentina.
C Department of Biotechnology, Institute of Farm Animal Genetics (FLI), Mariensee, 31535 Neustadt, Germany.
D Department of Anatomy and Cell Biology, Indiana University School of Medicine-Evansville, 8600 University Boulevard, Evansville, IN 47712, USA.
E Corresponding author. Email: heiner.niemann@fli.bund.de
Reproduction, Fertility and Development 21(2) 304-312 https://doi.org/10.1071/RD08111
Submitted: 20 May 2008 Accepted: 15 August 2008 Published: 27 January 2009
Abstract
The present study investigated the distribution of cytoplasmic dynein, dynactin and 20S proteasomes in oocytes isolated from small (<2 mm) and large (2–8 mm) follicles during IVM. Immediately after chromatin condensation (germinal vesicle (GV) breakdown), dynactin was closely associated with the chromatin and interacted with tubulin at the MI and MII spindles in oocytes recovered from large follicles. Dynactin showed perinuclear concentration. Dynein was homogeneously distributed in the cytoplasm of GV oocytes in both groups and was associated with the chromatin at the MI and MII spindle. The 20S proteasomes were found predominantly in the nucleus at the GV stage and were associated with the chromatin up to the MII stage in both groups of oocytes. The use of sodium orthovanadate, an inhibitor or phosphatase and ATPase activity, and nocodazole, a known disruptor of microtubules, affected the localisation of proteasomes in the meiotic stages. The results demonstrate the distinct dynamics of molecular motors and proteasomes during bovine oocyte IVM, their possible relationship with the developmental competence of the oocyte and the link between microtubules, their associated molecular motors and the transport of proteasomes during bovine female meiosis.
Additional keywords: developmental competence, follicle size, molecular motors.
Acknowledgements
The technical assistance of Sabine Klein, Dieter Bunke, Miguel Velazquez, Khursheed Iqbal, Cristian Alvarez Sedó, Paolo Catalano and Roberto Fernandez is gratefully acknowledged. The authors acknowledge the gift of anti-β5 proteasomal antibodies from Dr George N. DeMartino (UT South-western, Dallas, TX, USA). This work was supported, in part, by CEGyR Foundation. SER was fellow from the National Research Council of Argentina (CONICET).
Beaudouin, J. , Gerlich, D. , Daigle, N. , Eils, R. , and Ellenberg, J. (2002). Nuclear envelope breakdown proceeds by microtubules-induced tearing of the lamina. Cell 108, 83–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Blangy, A. , Arnaud, L. , and Nigg, E. A. (1997). Phosphorylation by p34cdc2 protein kinase regulates binding of the kinesin-related protein HsEg5 to the dynactin subunit p150. J. Biol. Chem. 272, 19 418–19 424.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Brevini, T. A. , Cillo, F. , Francisci, C. , Antonini, S. , Toselli, V. , and Gandolfi, F. (2007). Temporal and spatial control of gene expression in early embryos of farm animals. Reprod. Fertil. Dev. 19, 35–42.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Carabatsos, M. J. , Combelles, C. M. , Messinger, S. M. , and Albertini, D. F. (2000). Sorting and reorganization of centrosomes during oocyte maturation in the mouse. Microsc. Res. Tech. 49, 435–444.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Coux, O. , Tanaka, K. , and Goldberg, A. L. (1996). Structure and functions of the 20S and 26S proteasomes. Annu. Rev. Biochem. 65, 801–847.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Deacon, S. W. , Serpinskaya, A. S. , Vaugham, P. S. , Lopez Fanarraga, M. , Vernos, I. , Vaughan, K. T. , and Gelfand, V. I. (2003). Dynactin is required for bidirectional organelle transport. J. Cell Biol. 160, 297–301.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Demartino, G. N. , and Gillette, T. G. (2007). Proteasomes: machines for all reasons. Cell 129, 659–662.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
FitzHarris, G. , Marangos, P. , and Carroll, J. (2007). Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. Dev. Biol. 305, 133–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Goldberg, A. L. (1995). Functions of the proteasome: the lysis at the end of the tunnel. Science 268, 522–523.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hershko, A. (2005). The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle. Cell Death Differ. 12, 1191–1197.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Höök, P. , and Vallee, R. B. (2006). The dynein family at a glance. J. Cell Sci. 119, 4369–4371.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Huang, C. Y. , Chang, C. P. , Huang, C. L. , and Ferrell, J. E. (1999). M phase phosphorylation of cytoplasmic dynein intermediate chain and p150Glued. J. Biol. Chem. 274, 14 262–14 269.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Huo, L. J. , Fan, H. Y. , Liang, C. G. , Yu, L. Z. , Zhong, Z. S. , Chen, D. Y. , and Sun, Q. Y. (2004). Regulation of ubiquitin–proteasome pathway on pig oocyte meiotic maturation and fertilization. Biol. Reprod. 71, 853–862.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Hyttel, P. , Fair, T. , Callesen, H. , and Greve, T. (1997). Ooocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
| Crossref | GoogleScholarGoogle Scholar |
Johnston, J. A. , Illing, M. E. , and Kopito, R. R. (2002). Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell Motil. Cytoskeleton 53, 26–38.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Josefsberg, L. B. , Galiani, D. , Dantes, A. , Amsterdam, A. , and Dekel, N. (2000). The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. Biol. Reprod. 62, 1270–1277.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Karki, S. , and Holzbaur, E. L. F. (1995). Affinity chromatography demonstrates a direct binding between cytoplasmic dynein and the dynactin complex. J. Biol. Chem. 270, 28 806–28 811.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Karki, S. , and Holzbaur, E. L. (1999). Cytoplasmic dynein and dynactin in cell division and intracellular transport. Curr. Opin. Cell Biol. 11, 45–53.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Kim, H. , Ling, S. C. , Rogers, G. C. , Kural, C. , Selvin, P. R. , Rogers, S. L. , and Gelfand, V. I. (2007). Microtubule binding by dynactin is required for microtubules organization but not cargo transport. J. Cell Biol. 176, 641–651.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Kim, N. H. , Cho, S. K. , Choi, S. H. , Kim, E. Y. , Park, S. P. , and Lim, J. H. (2000). The distribution and requirements of microtubules and microfilaments in bovine oocytes during in vitro maturation. Zygote 8, 25–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lee, J. , Miyano, T. , and Moor, R. M. (2000). Spindle formation and dynamics of γ-tubulin and nuclear mitotic apparatus protein distribution during meiosis in pig and mouse oocytes. Biol. Reprod. 62, 1184–1192.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Lequarre, A. S. , Vigneron, C. , Ribaucour, F. , Holm, P. , Donnay, I. , Dalbies-Tran, R. , Callesen, H. , and Mermillod, P. (2005). Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology 63, 841–859.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Merdes, A. , Heald, R. , Samejimak, K. , Earnshaw, W. C. , and Cleveland, D. W. (2000). Formation of spindle poles by dynein/dynactin-dependent transport of NuMA. J. Cell Biol. 149, 851–862.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Niclas, J. , Allan, V. J. , and Vale, R. D. (1996). Cell cycle regulation of dynein association with membranes modulates microtubules-based organelle transport. J. Cell Biol. 133, 585–593.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Pavlok, A. , Lucas-Hahn, A. , and Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–67.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Payne, C. , Rawe, V. Y. , Ramalho-Santos, J. , Simerly, C. , and Schatten, G. (2003). Preferentially localized dynein and perinuclear dynactin associate with nuclear pore complex proteins to mediate genomic union during mammalian fertilization. J. Cell Sci. 116, 4727–4738.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Pfister, K. K. , Shahm, P. R. , Hummerich, H. , Russ, A. , Cotton, J. , Annuar, A. A. , King, S. M. , and Fisher, E. M. (2006). Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet. 2, e1.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Racedo, S. E. , Wrenzycki, C. , Herrmann, D. , Salamone, D. , and Niemann, H. (2008). Effects of follicle size and stages of maturation on mRNA expression in bovine in vitro matured oocytes. Mol. Reprod. Dev. 75, 17–25.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rawe, V. Y. , Payne, C. , Navara, C. , and Schatten, G. (2004). WAVE1 intranuclear trafficking is essential for genomic and cytoskeletal dynamics during fertilization: cell-cycle-dependent shuttling between M-phase and interphase nuclei. Dev. Biol. 276, 253–267.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ross, J. L. , Wallace, K. , Shuman, H. , Goldman, Y. E. , and Holzbaur, E. L. (2006). Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat. Cell Biol. 8, 562–570.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Salina, D. , Bodoor, K. , Eckley, D. M. , Schroer, T. A. , Rattner, J. B. , and Burke, B. (2002). Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108, 97–107.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sirard, M. A. , Florman, H. M. , Leibfried-Rutledge, M. L. , Barnes, M. L. , and First, N. L. (1989). Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Biol. Reprod. 40, 1257–1263.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sun, Q. Y. , and Schatten, H. (2006). Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 131, 193–205.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Vaughan, K. T. , and Vallee, R. B. (1995). Cytoplasmic dynein binds dynactin through a direct interaction between the intermediate chains and p150Glued. J. Cell Biol. 131, 1507–1516.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wang, X. M. , Huang, T. H. , Xie, Q. D. , Zhang, Q. J. , and Ruan, Y. (2004). Effect of dynein inhibitor on mouse oocyte in vitro maturation and its cyclin B1 mRNA level. Biomed. Environ. Sci. 17, 341–349.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wigley, W. C. , Fabunmi, R. P. , Lee, M. G. , Marino, C. R. , Muallem, S. , DeMartino, G. N. , and Thomas, P. J. (1999). Dynamic association of proteasomal machinery with the centrosome. J. Cell Biol. 145, 481–490.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Wójcik, C. , Schroeter, D. , Wilk, S. , Lamprecht, J. , and Paweletz, N. (1996). Ubiquitin-mediated proteolysis centers in HeLa cells: indication from studies of an inhibitor of the chymotrypsin-like activity of the proteasome. Eur. J. Cell Biol. 71, 311–318.
| PubMed |
Wojcik, C. , Benchaib, M. , Lornage, J. , Czyba, J. C. , and Guerin, J. F. (2000). Localization of proteasomes in human oocytes and preimplantation embryos. Mol. Hum. Reprod. 6, 331–336.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zhang, D. , Yin, S. , Jiang, M. X. , Ma, W. , Hou, Y. , Liang, C. G. , Yu, L. Z. , Wang, W. H. , and Sun, Q. Y. (2007). Cytoplasmic dynein participates in meiotic checkpoint inactivation in mouse oocytes by transporting cytoplasmic mitotic arrest-deficient (Mad) proteins from kinetochores to spindle poles. Reproduction 133, 685–695.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |