Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-27T10:45:24.445Z Has data issue: false hasContentIssue false
  • English
  • Français

Regulation of Peripheral Spindle Movement and Spindle Rotation during Mouse Oocyte Meiosis: New Perspectives

Published online by Cambridge University Press:  04 July 2008

Jun-Shu Ai ,
Qiang Wang ,
Shen Yin ,
Li-Hong Shi ,
Bo Xiong ,
Ying-Chun OuYang ,
Yi Hou ,
Da-Yuan Chen ,
Heide Schatten  and
Qing-Yuan Sun
Jun-Shu Ai
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Graduate School, Chinese Academy of Sciences, Beijing 100101, China
Qiang Wang
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Graduate School, Chinese Academy of Sciences, Beijing 100101, China
Shen Yin
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Graduate School, Chinese Academy of Sciences, Beijing 100101, China
Li-Hong Shi
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Graduate School, Chinese Academy of Sciences, Beijing 100101, China
Bo Xiong
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Graduate School, Chinese Academy of Sciences, Beijing 100101, China
Ying-Chun OuYang
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Yi Hou
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Da-Yuan Chen
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Heide Schatten
Affiliation:
Department of Veterinary Pathobiology, University of Missouri-Columbia, Columbia, MO 65211, USA
Qing-Yuan Sun*
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
*
Corresponding author. E-mail: sunqy@ioz.ac.cn
Get access

Abstract

Spindle movement, including spindle migration during first meiosis and spindle rotation during second meiosis, is essential for asymmetric divisions in mouse oocytes. Previous studies by others and us have shown that microfilaments are required for both spindle migration and rotation. In the present study, we aimed to further investigate the mechanism controlling spindle movement during mouse oocyte meiosis. By employing drug treatment and immunofluorescence microscopy, we showed that dynamic microtubule assembly was involved in both spindle migration and rotation. Furthermore, we found that the calcium/CaM/CaMKII pathway was important for regulating spindle rotation.

Keywords

mouse oocytespindle migrationspindle rotationmicrotubulecalcium
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 14 , Issue 4 , August 2008 , pp. 349 - 356
Copyright
Copyright © Microscopy Society of America 2008

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

REFERENCES

Abbott, A.L., Fissore, R.A. & Ducibella, T. (1999). Incompetence of preovulatory mouse oocytes to undergo cortical granule exocytosis following induced calcium oscillations. Dev Biol 207, 38–48.CrossRefGoogle ScholarPubMed
Brunet, S., Maria, A.S., Guillaud, P., Dujardin, D., Kubiak, J.Z. & Maro, B. (1999). Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J Cell Biol 146, 1–12.CrossRefGoogle Scholar
Calarco, P.G. (2005). The role of microfilaments in early meiotic maturation of mouse oocytes. Microsc Microanal 11, 146–153.CrossRefGoogle ScholarPubMed
Chatot, C.L., Ziomek, C.A., Bavister, B.D., Lewis, J.L. & Torres, I. (1989). An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J Reprod Fertil 86, 679–688.CrossRefGoogle ScholarPubMed
Cheung, W.Y. (1980). Calmodulin plays a pivotal role in cellular regulation. Science 207, 19–27.CrossRefGoogle Scholar
Ducibella, T., Huneau, D., Angelichio, E., Xu, Z., Schultz, R.M., Kopf, G.S., Fissore, R., Madoux, S. & Ozil, J.P. (2002). Egg-to-embryo transition is driven by differential responses to Ca(2+) oscillation number. Dev Biol 250, 280–291.CrossRefGoogle Scholar
Dumont, J., Million, K., Sunderland, K., Rassinier, P., Lim, H., Leader, B. & Verlhac, M.H. (2007). Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Dev Biol 301, 254–265.CrossRefGoogle ScholarPubMed
Fan, H.Y., Huo, L.J., Meng, X.Q., Zhong, Z.S., Hou, Y., Chen, D.Y. & Sun, Q.Y. (2003). Involvement of calcium/calmodulin-dependent protein kinase II (CaMKII) in meiotic maturation and activation of pig oocytes. Biol Reprod 69, 1552–1564.CrossRefGoogle ScholarPubMed
Gonczy, P. (2002). Mechanisms of spindle positioning: Focus on flies and worms. Trends Cell Biol 12, 332–339.CrossRefGoogle ScholarPubMed
Grill, S.W., Gonczy, P., Stelzer, E.H. & Hyman, A.A. (2001). Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409, 630–633.CrossRefGoogle ScholarPubMed
Hyman, A.A. (1989). Centrosome movement in the early divisions of Caenorhabditis elegans: A cortical site determining centrosome position. J Cell Biol 109, 1185–1193.CrossRefGoogle ScholarPubMed
Ibanez, E., Albertini, D.F. & Overstrom, E.W. (2003). Demecolcine-induced oocyte enucleation for somatic cell cloning: Coordination between cell-cycle egress, kinetics of cortical cytoskeletal interactions, and second polar body extrusion. Biol Reprod 68, 1249–1258.CrossRefGoogle ScholarPubMed
Ibanez, E., Albertini, D.F. & Overstrom, E.W. (2005). Effect of genetic background and activating stimulus on the timing of meiotic cell cycle progression in parthenogenetically activated mouse oocytes. Reproduction 129, 27–38.CrossRefGoogle ScholarPubMed
Johnson, J., Bierle, B.M., Gallicano, G.I. & Capco, D.G. (1998). Calcium/calmodulin-dependent protein kinase II and calmodulin: Regulators of the meiotic spindle in mouse eggs. Dev Biol 204, 464–477.CrossRefGoogle ScholarPubMed
Klee, C.B., Crouch, T.H. & Richman, P.G. (1980). Calmodulin. Annu Rev Biochem 49, 489–515.CrossRefGoogle ScholarPubMed
Kline, D. & Kline, J.T. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev Biol 149, 80–89.CrossRefGoogle ScholarPubMed
Leader, B., Lim, H., Carabatsos, M.J., Harrington, A., Ecsedy, J., Pellman, D., Maas, R. & Leder, P. (2002). Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4, 921–928.CrossRefGoogle ScholarPubMed
Liu, L., Trimarchi, J.R., Oldenbourg, R. & Keefe, D.L. (2000). Increased birefringence in the meiotic spindle provides a new marker for the onset of activation in living oocytes. Biol Reprod 63, 251–258.CrossRefGoogle ScholarPubMed
Longo, F.J. & Chen, D.Y. (1985). Development of cortical polarity in mouse eggs: Involvement of the meiotic apparatus. Dev Biol 107, 382–394.CrossRefGoogle ScholarPubMed
Lorca, T., Cruzalegui, F.H., Fesquet, D., Cavadore, J.C., Mery, J., Means, A. & Doree, M. (1993). Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature 366, 270–273.CrossRefGoogle ScholarPubMed
Markoulaki, S., Matson, S., Abbott, A.L. & Ducibella, T. (2003). Oscillatory CaMKII activity in mouse egg activation. Dev Biol 258, 464–474.CrossRefGoogle ScholarPubMed
Markoulaki, S., Matson, S. & Ducibella, T. (2004). Fertilization stimulates long-lasting oscillations of CaMKII activity in mouse eggs. Dev Biol 272, 15–25.CrossRefGoogle ScholarPubMed
Maro, B., Howlett, S.K. & Webb, M. (1985). Non-spindle microtubule organizing centers in metaphase II-arrested mouse oocytes. J Cell Biol 101, 1665–1672.CrossRefGoogle ScholarPubMed
Maro, B., Johnson, M.H., Pickering, S.J. & Flach, G. (1984). Changes in actin distribution during fertilization of the mouse egg. J Embryol Exp Morphol 81, 211–237.Google ScholarPubMed
Maro, B., Johnson, M.H., Webb, M. & Flach, G. (1986). Mechanism of polar body formation in the mouse oocyte: An interaction between the chromosomes, the cytoskeleton and the plasma membrane. J Embryol Exp Morphol 92, 11–32.Google ScholarPubMed
Maro, B. & Verlhac, M.H. (2002). Polar body formation: New rules for asymmetric divisions. Nat Cell Biol 4, E281–E283.CrossRefGoogle ScholarPubMed
Matson, S., Markoulaki, S. & Ducibella, T. (2006). Antagonists of myosin light chain kinase and of myosin II inhibit specific events of egg activation in fertilized mouse eggs. Biol Reprod 74, 169–176.CrossRefGoogle ScholarPubMed
Navarro, P.A., Liu, L., Trimarchi, J.R., Ferriani, R.A. & Keefe, D.L. (2005). Noninvasive imaging of spindle dynamics during mammalian oocyte activation. Fertil Steril 83(Suppl 1), 1197–1205.CrossRefGoogle ScholarPubMed
Petronczki, M., Siomos, M.F. & Nasmyth, K. (2003). Un menage a quatre: The molecular biology of chromosome segregation in meiosis. Cell 112, 423–440.CrossRefGoogle Scholar
Roth, Z. & Hansen, P.J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129, 235–244.CrossRefGoogle ScholarPubMed
Schultz, R.M. & Kopf, G.S. (1995). Molecular basis of mammalian egg activation. Curr Top Dev Biol 30, 21–62.CrossRefGoogle ScholarPubMed
Su, Y.Q. & Eppig, J.J. (2002). Evidence that multifunctional calcium/calmodulin-dependent protein kinase II (CaM KII) participates in the meiotic maturation of mouse oocytes. Mol Reprod Dev 61, 560–569.CrossRefGoogle ScholarPubMed
Sun, Q.Y. & Schatten, H. (2006). Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 131, 193–205.CrossRefGoogle ScholarPubMed
Swann, K. & Ozil, J.P. (1994). Dynamics of the calcium signal that triggers mammalian egg activation. Int Rev Cytol 152, 183–222.CrossRefGoogle ScholarPubMed
Szollosi, D., Calarco, P. & Donahue, R.P. (1972). Absence of centrioles in the first and second meiotic spindles of mouse oocytes. J Cell Sci 11, 521–541.CrossRefGoogle ScholarPubMed
Tatone, C., Delle Monache, S., Iorio, R., Caserta, D., Di Cola, M. & Colonna, R. (2002). Possible role for Ca(2+) calmodulin-dependent protein kinase II as an effector of the fertilization Ca(2+) signal in mouse oocyte activation. Mol Hum Reprod 8, 750–757.CrossRefGoogle ScholarPubMed
Tatone, C., Iorio, R., Francione, A., Gioia, L. & Colonna, R. (1999). Biochemical and biological effects of KN-93, an inhibitor of calmodulin-dependent protein kinase II, on the initial events of mouse egg activation induced by ethanol. J Reprod Fertil 115, 151–157.CrossRefGoogle ScholarPubMed
Tong, C., Fan, H.Y., Lian, L., Li, S.W., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2002). Polo-like kinase-1 is a pivotal regulator of microtubule assembly during mouse oocyte meiotic maturation, fertilization, and early embryonic mitosis. Biol Reprod 67, 546–554.CrossRefGoogle ScholarPubMed
Verlhac, M.H., Lefebvre, C., Guillaud, P., Rassinier, P. & Maro, B. (2000). Asymmetric division in mouse oocytes: With or without Mos. Curr Biol 10, 1303–1306.CrossRefGoogle ScholarPubMed
Winston, N.J. & Maro, B. (1995). Calmodulin-dependent protein kinase II is activated transiently in ethanol-stimulated mouse oocytes. Dev Biol 170, 350–352.CrossRefGoogle ScholarPubMed
Yarm, F., Sagot, I. & Pellman, D. (2001). The social life of actin and microtubules: Interaction versus cooperation. Curr Opin Microbiol 4, 696–702.CrossRefGoogle ScholarPubMed
Yin, S., Wang, Q., Liu, J.H., Ai, J.S., Liang, C.G., Hou, Y., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2006). Bub1 prevents chromosome misalignment and precocious anaphase during mouse oocyte meiosis. Cell Cycle 5, 2130–2137.CrossRefGoogle ScholarPubMed
Zhong, Z.S., Huo, L.J., Liang, C.G., Chen, D.Y. & Sun, Q.Y. (2005). Small GTPase RhoA is required for ooplasmic segregation and spindle rotation, but not for spindle organization and chromosome separation during mouse oocyte maturation, fertilization, and early cleavage. Mol Reprod Dev 71, 256–261.CrossRefGoogle Scholar
Zhu, Z.Y., Chen, D.Y., Li, J.S., Lian, L., Lei, L., Han, Z.M. & Sun, Q.Y. (2003). Rotation of meiotic spindle is controlled by microfilaments in mouse oocytes. Biol Reprod 68, 943–946.CrossRefGoogle ScholarPubMed