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The Distribution and Possible Role of ERK8 in Mouse Oocyte Meiotic Maturation and Early Embryo Cleavage

Published online by Cambridge University Press:  28 January 2013

Shang-Wu Yang ,
Hao Huang ,
Chen Gao ,
Lei Chen ,
Shu-Tao Qi ,
Fei Lin ,
Jian-Xin Wang ,
Yi Hou ,
Fu-Qi Xing  and
Qing-Yuan Sun
Shang-Wu Yang
Affiliation:
Center for Reproductive Medicine, Department of Ob/Gy, Nanfang Hospital, Southern Medical University, Guangzhou City, Guangdong Province, China State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China Department of Ob/Gy, Nanhai People's Hospital, Foshan City, Guangdong Province, China
Hao Huang
Affiliation:
Department of Ob/Gy, Nanhai People's Hospital, Foshan City, Guangdong Province, China
Chen Gao
Affiliation:
State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Changbai Rd 155, Beijing, China
Lei Chen
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Shu-Tao Qi
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Fei Lin
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Jian-Xin Wang
Affiliation:
Department of Neurosurgery, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China
Yi Hou
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Fu-Qi Xing*
Affiliation:
Center for Reproductive Medicine, Department of Ob/Gy, Nanfang Hospital, Southern Medical University, Guangzhou City, Guangdong Province, China
Qing-Yuan Sun*
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
*
**Corresponding author: E-mail: [email protected]
*Corresponding author: E-mail: [email protected]
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Abstract

It is well known that extracellular signal-regulated kinase 8 (ERK8) plays pivotal roles in various mitotic events. But its physiological roles in oocyte meiotic maturation remain unclear. In this study, we found that although no specific ERK8 signal was detected in oocyte at the germinal vesicle stage, ERK8 began to migrate to the periphery of chromosomes shortly after germinal vesicle breakdown. At prometaphase I, metaphase I (MI), anaphase I, telophase I, and metaphase II (MII) stages, ERK8 was stably detected at the spindles. By taxol treatment, we clarified that the ERK8 signal was stained on the spindle fibers as well as microtubule asters in MI and MII oocytes. In fertilized eggs, the ERK8 signal was not observed in the two pronuclei stages. At prometaphase, metaphase, and anaphase of the first mitosis, ERK8 was detected on the mitotic spindle. ERK8 knock down by antibody microinjection and specific siRNA caused abnormal spindles, failed chromosome congression, and decreased first polar body extrusion. Taken together, our results suggest that ERK8 plays an important role in spindle organization during mouse oocyte meiotic maturation and early embryo cleavage.

Keywords

ERK8mouse oocyte meiosisMTOCspindleembryo
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 19 , Issue 1 , February 2013 , pp. 190 - 200
Copyright
Copyright © Microscopy Society of America 2013

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References

Abe, M.K., Saelzler, M.P., Espinosa, R. 3rd, Kahle, K.T., Hershenson, M.B., Le Beau, M.M. & Rosner, M.R. (2002). ERK8, a new member of the mitogen-activated protein kinase family. J Biol Chem 277(19), 16733–16743.CrossRefGoogle ScholarPubMed
Ai, J.S., Wang, Q., Li, M., Shi, L.H., Ola, S.I., Xiong, B., Yin, S., Chen, D.Y. & Sun, Q.Y. (2008a). Roles of microtubules and microfilaments in spindle movements during rat oocyte meiosis. J Reprod Dev 54(5), 391–396.CrossRefGoogle ScholarPubMed
Ai, J.S., Wang, Q., Yin, S., Shi, L.H., Xiong, B., OuYang, Y.C., Hou, Y., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2008b). Regulation of peripheral spindle movement and spindle rotation during mouse oocyte meiosis: New perspectives. Microsc Microanal 14(4), 349–356.Google Scholar
Basto, R., Lau, J., Vinogradova, T., Gardiol, A., Woods, C.G., Khodjakov, A. & Raff, J.W. (2006). Flies without centrioles. Cell 125(7), 1375–1386.Google Scholar
Bogoyevitch, M.A. & Court, N.W. (2004). Counting on mitogen-activated protein kinases—ERKs 3, 4, 5, 6, 7 and 8. Cell Signal 16(12), 1345–1354.Google Scholar
Chen, L., Chao, S.B., Wang, Z.B., Qi, S.T., Zhu, X.L., Yang, S.W., Yang, C.R., Zhang, Q.H., Ouyang, Y.C., Hou, Y., Schatten, H. & Sun, Q.Y. (2012). Checkpoint kinase 1 is essential for meiotic cell cycle regulation in mouse oocytes. Cell Cycle 11(10), 1948–1955.Google Scholar
Compton, D.A. (2000). Spindle assembly in animal cells. Annu Rev Biochem 69, 95–114.Google Scholar
Fant, X., Merdes, A. & Haren, L. (2004). Cell and molecular biology of spindle poles and NuMA. Int Rev Cytol 238, 1–57.Google Scholar
Groehler, A.L. & Lannigan, D.A. (2010). A chromatin-bound kinase, ERK8, protects genomic integrity by inhibiting HDM2-mediated degradation of the DNA clamp PCNA. J Cell Biol 190(4), 575–586.CrossRefGoogle ScholarPubMed
Haren, L., Remy, M.H., Bazin, I., Callebaut, I., Wright, M. & Merdes, A. (2006). NEDD1-dependent recruitment of the gamma-tubulin ring complex to the centrosome is necessary for centriole duplication and spindle assembly. J Cell Biol 172(4), 505–515.CrossRefGoogle Scholar
Huang, X., Tong, J.S., Wang, Z.B., Yang, C.R., Qi, S.T., Guo, L., Ouyang, Y.C., Quan, S., Sun, Q.Y., Qi, Z.Q., Huang, R.X. & Wang, H.L. (2011). JNK2 participates in spindle assembly during mouse oocyte meiotic maturation. Microsc Microanal 17(2), 197–205.Google Scholar
Iavarone, C., Acunzo, M., Carlomagno, F., Catania, A., Melillo, R.M., Carlomagno, S.M., Santoro, M. & Chiariello, M. (2006). Activation of the Erk8 mitogen-activated protein (MAP) kinase by RET/PTC3, a constitutively active form of the RET proto-oncogene. J Biol Chem 281(15), 10567–10576.Google Scholar
Lewis, T.S., Shapiro, P.S. & Ahn, N.G. (1998). Signal transduction through MAP kinase cascades. Adv Cancer Res 74, 49–139.CrossRefGoogle ScholarPubMed
Li, M., Ai, J.S., Xu, B.Z., Xiong, B., Yin, S., Lin, S.L., Hou, Y., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2008). Testosterone potentially triggers meiotic resumption by activation of intraoocyte SRC and MAPK in porcine oocytes. Biol Reprod 79(5), 897–905.CrossRefGoogle ScholarPubMed
Liu, H.C., Tang, Y., He, Z. & Rosenwaks, Z. (2010). Dicer is a key player in oocyte maturation. J Assist Reprod Genet 27, 571–580.CrossRefGoogle ScholarPubMed
Ma, W., Baumann, C. & Viveiros, M.M. (2010). NEDD1 is crucial for meiotic spindle stability and accurate chromosome segregation in mammalian oocytes. Dev Biol 339(2), 439–450.Google Scholar
Mackey, Z.B., Koupparis, K., Nishino, M. & McKerrow, J.H. (2011). High-throughput analysis of an RNAi library identifies novel kinase targets in Trypanosoma brucei. Chem Biol Drug Des 78(3), 454–463.Google Scholar
Pearson, G., Robinson, F., Beers Gibson, T., Xu, B.E., Karandikar, M., Berman, K. & Cobb, M.H. (2001). Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr Rev 22(2), 153–183.Google Scholar
Quimby, B.B. & Dasso, M. (2003). The small GTPase Ran: Interpreting the signs. Curr Opin Cell Biol 15(3), 338–344.Google Scholar
Robinson, M.J. & Cobb, M.H. (1997). Mitogen-activated protein kinase pathways. Curr Opin Cell Biol 9(2), 180–186.Google Scholar
Schatten, H. (2008). The mammalian centrosome and its functional significance. Histochem Cell Biol 129(6), 667–686.Google Scholar
Schatten, H. & Sun, Q.Y. (2011a). Centrosome dynamics during mammalian oocyte maturation with a focus on meiotic spindle formation. Mol Reprod Dev 78(10-11), 757–768.Google Scholar
Schatten, H. & Sun, Q.Y. (2011b). The significant role of centrosomes in stem cell division and differentiation. Microsc Microanal 17(4), 506–512.Google Scholar
Schuh, M. & Ellenberg, J. (2007). Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130(3), 484–498.Google Scholar
Sun, S.C., Zhang, D.X., Lee, S.E., Xu, Y.N. & Kim, N.H. (2011). Ndc80 regulates meiotic spindle organization, chromosome alignment, and cell cycle progression in mouse oocytes. Microsc Microanal 17(3), 431–439.Google Scholar
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(2), 546–554.Google Scholar
Verlhac, M.H., de Pennart, H., Maro, B., Cobb, M.H. & Clarke, H.J. (1993). MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. Dev Biol 158(2), 330–340.Google Scholar
Wadsworth, P., Lee, W.L., Murata, T. & Baskin, T.I. (2011). Variations on theme: Spindle assembly in diverse cells. Protoplasma 248(3), 439–446.Google Scholar
Walczak, C.E. & Heald, R. (2008). Mechanisms of mitotic spindle assembly and function. Int Rev Cytol 265, 111–158.Google Scholar
Wang, Q., Racowsky, C. & Deng, M. (2011). Mechanism of the chromosome-induced polar body extrusion in mouse eggs. Cell Div 6, 17.Google Scholar
Wang, R., He, G., Nelman-Gonzalez, M., Ashorn, C.L., Gallick, G.E., Stukenberg, P.T., Kirschner, M.W. & Kuang, J. (2007). Regulation of Cdc25C by ERK-MAP kinases during the G2/M transition. Cell 128(6), 1119–1132.CrossRefGoogle ScholarPubMed
Waskiewicz, A.J. & Cooper, J.A. (1995). Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr Opin Cell Biol 7(6), 798–805.Google Scholar
Xiong, B., Li, S., Ai, J.S., Yin, S., Ouyang, Y.C., Sun, S.C., Chen, D.Y. & Sun, Q.Y. (2008). BRCA1 is required for meiotic spindle assembly and spindle assembly checkpoint activation in mouse oocytes. Biol Reprod 79(4), 718–726.Google Scholar
Xu, Y.M., Zhu, F., Cho, Y.Y., Carper, A., Peng, C., Zheng, D., Yao, K., Lau, A.T., Zykova, T.A., Kim, H.G., Bode, A.M. & Dong, Z. (2010). Extracellular signal-regulated kinase 8-mediated c-Jun phosphorylation increases tumorigenesis of human colon cancer. Cancer Res 70(8), 3218–3227.CrossRefGoogle ScholarPubMed
Yao, L.J., Zhong, Z.S., Zhang, L.S., Chen, D.Y., Schatten, H. & Sun, Q.Y. (2004). Aurora-A is a critical regulator of microtubule assembly and nuclear activity in mouse oocytes, fertilized eggs, and early embryos. Biol Reprod 70(5), 1392–1399.Google Scholar
Yuan, J., Li, M., Wei, L., Yin, S., Xiong, B., Li, S., Lin, S.L., Schatten, H. & Sun, Q.Y. (2009). Astrin regulates meiotic spindle organization, spindle pole tethering and cell cycle progression in mouse oocytes. Cell Cycle 8(20), 3384–3395.Google Scholar
Yuan, J., Xu, B.Z., Qi, S.T., Tong, J.S., Wei, L., Li, M., Ouyang, Y.C., Hou, Y., Schatten, H. & Sun, Q.Y. (2010). MAPK-activated protein kinase 2 is required for mouse meiotic spindle assembly and kinetochore-microtubule attachment. PLoS One 5(6), e11247. CrossRefGoogle ScholarPubMed
Zheng, K.G., Meng, X.Q., Yang, Y., Yu, Y.S., Liu, D.C. & Li, Y.L. (2007). Requirements of Src family kinase during meiotic maturation in mouse oocyte. Mol Reprod Dev 74(1), 125–130.Google Scholar
Zhu, J., Qi, S.T., Wang, Y.P., Wang, Z.B., Ouyang, Y.C., Hou, Y., Schatten, H. & Sun, Q.Y. (2011). Septin1 is required for spindle assembly and chromosome congression in mouse oocytes. Dev Dyn 240(10), 2281–2289.Google Scholar