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JNK2 Participates in Spindle Assembly during Mouse Oocyte Meiotic Maturation

Published online by Cambridge University Press:  31 January 2011

Xin Huang ,
Jing-Shan Tong ,
Zhen-Bo Wang ,
Cai-Rong Yang ,
Shu-Tao Qi ,
Lei Guo ,
Ying-Chun Ouyang ,
Song Quan ,
Qing-Yuan Sun  and
Zhong-Quan Qi
...Show all authors
Xin Huang
Affiliation:
Organ Transplantation Institute, Xiamen University, Xiamen City, Fujian Province, China State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Jing-Shan Tong
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Zhen-Bo Wang
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Cai-Rong Yang
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
Lei Guo
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Ying-Chun Ouyang
Affiliation:
State Key Laboratory of Reproductive Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China
Song Quan
Affiliation:
Department of OB/GY, 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
Zhong-Quan Qi
Affiliation:
Organ Transplantation Institute, Xiamen University, Xiamen City, Fujian Province, China
Ru-Xin Huang*
Affiliation:
Organ Transplantation Institute, Xiamen University, Xiamen City, Fujian Province, China Health Bureau of Xiamen, Xiamen City, Fujian Province, China
Hai-Long Wang*
Affiliation:
Organ Transplantation Institute, Xiamen University, Xiamen City, Fujian Province, China
*
Corresponding author. E-mail: [email protected]
Corresponding author. E-mail: [email protected]
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Abstract

It is well known that c-Jun N-terminal kinase (JNK) plays pivotal roles in various mitotic events, but its function in mammalian oocyte meiosis remains unknown. In this study, we found that no specific JNK2 signal was detected in germinal vesicle stage. JNK2 was associated with the spindles especially the spindle poles and cytoplasmic microtubule organizing centers at prometaphase I, metaphase I, and metaphase II stages. JNK2 became diffusely distributed and associated with the midbody at telophase I stage. Injection of myc-tagged JNK2α1 mRNA into oocytes also revealed its localization on spindle poles. The association of JNK2 with spindle poles was further confirmed by colocalization with the centrosomal proteins, γ-tubulin and Plk1. Nocodazole treatment showed that JNK2 may interact with Plk1 to regulate the spindle assembly. Then we investigated the possible function of JNK2 by JNK2 antibody microinjection and JNK specific inhibitor SP600125 treatment. These two manipulations caused abnormal spindle formation and decreased the rate of first polar body (PB1) extrusion. In addition, inhibition of JNK2 resulted in impaired localization of Plk1. Taken together, our results suggest that JNK2 plays an important role in spindle assembly and PB1 extrusion during mouse oocyte meiotic maturation.

Keywords

JNK2mouse oocytemeiosisMTOCspindle
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 17 , Issue 2 , April 2011 , pp. 197 - 205
Copyright
Copyright © Microscopy Society of America 2011

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References

REFERENCES

Bagowski, C.P., Xiong, W. & Ferrell, J.E. Jr. (2001). c-Jun N-terminal kinase activation in Xenopus laevis eggs and embryos. A possible non-genomic role for the JNK signaling pathway. J Biol Chem 276(2), 1459–1465.Google Scholar
Bode, A.M. & Dong, Z. (2007). The functional contrariety of JNK. Mol Carcinog 46(8), 591–598.CrossRefGoogle ScholarPubMed
Brennan, I.M., Peters, U., Kapoor, T.M. & Straight, A.F. (2007). Polo-like kinase controls vertebrate spindle elongation and cytokinesis. PLoS One 2(5), e409.Google Scholar
Chang, L., Jones, Y., Ellisman, M.H., Goldstein, L.S. & Karin, M. (2003). JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 4(4), 521–533.CrossRefGoogle ScholarPubMed
Dai, W., Wang, Q. & Traganos, F. (2002). Polo-like kinases and centrosome regulation. Oncogene 21(40), 6195–6200.CrossRefGoogle ScholarPubMed
Daire, V., Giustiniani, J., Leroy-Gori, I., Quesnoit, M., Drevensek, S., Dimitrov, A., Perez, F. & Pous, C. (2009). Kinesin-1 regulates microtubule dynamics via a c-Jun N-terminal kinase-dependent mechanism. J Biol Chem 284(46), 31992–32001.CrossRefGoogle Scholar
Gupta, S., Barrett, T., Whitmarsh, A.J., Cavanagh, J., Sluss, H.K., Derijard, B. & Davis, R.J. (1996). Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 15(11), 2760–2770.Google Scholar
Gutierrez, G.J., Tsuji, T., Cross, J.V., Davis, R.J., Templeton, D.J., Jiang, W. & Ronai, Z.A. (2010). JNK-mediated phosphorylation of Cdc25C regulates cell cycle entry and G(2)/M DNA damage checkpoint. J Biol Chem 285(19), 14217–14228.Google Scholar
Ho, C.Y. & Li, H.Y. (2010). DNA damage during mitosis invokes a JNK-mediated stress response that leads to cell death. J Cell Biochem 110(3), 725–731.Google Scholar
Horiuchi, D., Barkus, R.V., Pilling, A.D., Gassman, A. & Saxton, W.M. (2005). APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in Drosophila. Curr Biol 15(23), 2137–2141.CrossRefGoogle ScholarPubMed
Inamura, N., Enokido, Y. & Hatanaka, H. (2001). Involvement of c-Jun N-terminal kinase and caspase 3-like protease in DNA damage-induced, p53-mediated apoptosis of cultured mouse cerebellar granule neurons. Brain Res 904(2), 270–278.Google Scholar
Jacobs-Helber, S.M. & Sawyer, S.T. (2004). Jun N-terminal kinase promotes proliferation of immature erythroid cells and erythropoietin-dependent cell lines. Blood 104(3), 696–703.CrossRefGoogle ScholarPubMed
Karsenti, E. & Vernos, I. (2001). The mitotic spindle: A self-made machine. Science 294(5542), 543–547.CrossRefGoogle ScholarPubMed
Kawauchi, T., Chihama, K., Nabeshima, Y. & Hoshino, M. (2003). The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J 22(16), 4190–4201.CrossRefGoogle ScholarPubMed
Kyriakis, J.M. & Avruch, J. (2001). Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev 81(2), 807–869.CrossRefGoogle Scholar
LaRosa, C. & Downs, S.M. (2007). Meiotic induction by heat stress in mouse oocytes: Involvement of AMP-activated protein kinase and MAPK family members. Biol Reprod 76(3), 476–486.CrossRefGoogle ScholarPubMed
Levy, J.R. & Holzbaur, E.L. (2006). Cytoplasmic dynein/dynactin function and dysfunction in motor neurons. Int J Dev Neurosci 24(2–3), 103–111.Google Scholar
Li, C., Ge, B., Nicotra, M., Stern, J.N., Kopcow, H.D., Chen, X. & Strominger, J.L. (2008). JNK MAP kinase activation is required for MTOC and granule polarization in NKG2D-mediated NK cell cytotoxicity. Proc Natl Acad Sci USA 105(8), 3017–3022.Google Scholar
Li, S., Ou, X.H., Wang, Z.B., Xiong, B., Tong, J.S., Wei, L., Li, M., Yuan, J., Ouyang, Y.C., Hou, Y., Schatten, H. & Sun, Q.Y. (2010). ERK3 is required for metaphase-anaphase transition in mouse oocyte meiosis. PLoS One 5(9).Google ScholarPubMed
MacCorkle, R.A. & Tan, T.H. (2004). Inhibition of JNK2 disrupts anaphase and produces aneuploidy in mammalian cells. J Biol Chem 279(38), 40112–40121.CrossRefGoogle ScholarPubMed
MacCorkle-Chosnek, R.A., VanHooser, A., Goodrich, D.W., Brinkley, B.R. & Tan, T.H. (2001). Cell cycle regulation of c-Jun N-terminal kinase activity at the centrosomes. Biochem Biophys Res Commun 289(1), 173–180.CrossRefGoogle ScholarPubMed
Matsumura, S., Toyoshima, F. & Nishida, E. (2007). Polo-like kinase 1 facilitates chromosome alignment during prometaphase through BubR1. J Biol Chem 282(20), 15217–15227.CrossRefGoogle ScholarPubMed
Mingo-Sion, A.M., Marietta, P.M., Koller, E., Wolf, D.M. & Van Den Berg, C.L. (2004). Inhibition of JNK reduces G2/M transit independent of p53, leading to endoreduplication, decreased proliferation, and apoptosis in breast cancer cells. Oncogene 23(2), 596–604.Google Scholar
Mood, K., Bong, Y.S., Lee, H.S., Ishimura, A. & Daar, I.O. (2004). Contribution of JNK, Mek, Mos and PI-3K signaling to GVBD in Xenopus oocytes. Cell Signal 16(5), 631–642.CrossRefGoogle ScholarPubMed
Moon, D.O., Kim, M.O., Kang, C.H., Lee, J.D., Choi, Y.H. & Kim, G.Y. (2009). JNK inhibitor SP600125 promotes the formation of polymerized tubulin, leading to G2/M phase arrest, endoreduplication, and delayed apoptosis. Exp Mol Med 41(9), 665–677.Google Scholar
Nomachi, A., Nishita, M., Inaba, D., Enomoto, M., Hamasaki, M. & Minami, Y. (2008). Receptor tyrosine kinase Ror2 mediates Wnt5a-induced polarized cell migration by activating c-Jun N-terminal kinase via actin-binding protein filamin A. J Biol Chem 283(41), 27973–27981.Google Scholar
Sabapathy, K. & Wagner, E.F. (2004). JNK2: A negative regulator of cellular proliferation. Cell Cycle 3(12), 1520–1523.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Steigemann, P. & Gerlich, D.W. (2009). Cytokinetic abscission: Cellular dynamics at the midbody. Trends Cell Biol 19(11), 606–616.Google Scholar
Sun, Q.Y. & Schatten, H. (2006). Role of NuMA in vertebrate cells: Review of an intriguing multifunctional protein. Front Biosci 11, 1137–1146.CrossRefGoogle ScholarPubMed
Sun, S.C., Wei, L., Li, M., Lin, S.L., Xu, B.Z., Liang, X.W., Kim, N.H., Schatten, H., Lu, S.S. & Sun, Q.Y. (2009). Perturbation of survivin expression affects chromosome alignment and spindle checkpoint in mouse oocyte meiotic maturation. Cell Cycle 8(20), 3365–3372.Google Scholar
Teraishi, F., Wu, S., Sasaki, J., Zhang, L., Davis, J.J., Guo, W., Dong, F. & Fang, B. (2005). JNK1-dependent antimitotic activity of thiazolidin compounds in human non-small-cell lung and colon cancer cells. Cell Mol Life Sci 62(19–20), 2382–2389.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
Tseng, C.J., Wang, Y.J., Liang, Y.C., Jeng, J.H., Lee, W.S., Lin, J.K., Chen, C.H., Liu, I.C. & Ho, Y.S. (2002). Microtubule damaging agents induce apoptosis in HL 60 cells and G2/M cell cycle arrest in HT 29 cells. Toxicology 175(1–3), 123–142.Google Scholar
Ventura, J.J., Cogswell, P., Flavell, R.A., Baldwin, A.S. Jr. & Davis, R.J. (2004). JNK potentiates TNF-stimulated necrosis by increasing the production of cytotoxic reactive oxygen species. Genes Dev 18(23), 2905–2915.Google Scholar
Vogt, E., Kirsch-Volders, M., Parry, J. & Eichenlaub-Ritter, U. (2008). Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. Mutat Res 651(1–2), 14–29.CrossRefGoogle ScholarPubMed
Wang, I.C., Chen, Y.J., Hughes, D.E., Ackerson, T., Major, M.L., Kalinichenko, V.V., Costa, R.H., Raychaudhuri, P., Tyner, A.L. & Lau, L.F. (2008). FoxM1 regulates transcription of JNK1 to promote the G1/S transition and tumor cell invasiveness. J Biol Chem 283(30), 20770–20778.Google Scholar
Weston, C.R. & Davis, R.J. (2007). The JNK signal transduction pathway. Curr Opin Cell Biol 19(2), 142–149.Google Scholar
Xiao, D., Pinto, J.T., Soh, J.W., Deguchi, A., Gundersen, G.G., Palazzo, A.F., Yoon, J.T., Shirin, H. & Weinstein, I.B. (2003). Induction of apoptosis by the garlic-derived compound S-allylmercaptocysteine (SAMC) is associated with microtubule depolymerization and c-Jun NH(2)-terminal kinase 1 activation. Cancer Res 63(20), 6825–6837.Google Scholar
Xiong, B., Li, S., Ai, J.S., Yin, S., Ouyang, Y.C., Sun, S.C., Chen, D.Y. & Sun, Q.Y. (2008a). BRCA1 is required for meiotic spindle assembly and spindle assembly checkpoint activation in mouse oocytes. Biol Reprod 79(4), 718–726.Google Scholar
Xiong, B., Sun, S.C., Lin, S.L., Li, M., Xu, B.Z., OuYang, Y.C., Hou, Y., Chen, D.Y. & Sun, Q.Y. (2008b). Involvement of Polo-like kinase 1 in MEK1/2-regulated spindle formation during mouse oocyte meiosis. Cell Cycle 7(12), 1804–1809.Google Scholar
Xiong, B., Yu, L.Z., Wang, Q., Ai, J.S., Yin, S., Liu, J.H., OuYang, Y.C., Hou, Y., Chen, D.Y., Zou, H. & Sun, Q.Y. (2007). Regulation of intracellular MEK1/2 translocation in mouse oocytes: Cytoplasmic dynein/dynactin-mediated poleward transport and cyclin B degradation-dependent release from spindle poles. Cell Cycle 6(12), 1521–1527.Google Scholar
Yang, D.D., Conze, D., Whitmarsh, A.J., Barrett, T., Davis, R.J., Rincon, M. & Flavell, R.A. (1998). Differentiation of CD4+ T cells to Th1 cells requires MAP kinase JNK2. Immunity 9(4), 575–585.Google Scholar
Yu, L.Z., Xiong, B., Gao, W.X., Wang, C.M., Zhong, Z.S., Huo, L.J., Wang, Q., Hou, Y., Liu, K., Liu, X.J., Schatten, H., Chen, D.Y. & Sun, Q.Y. (2007). MEK1/2 regulates microtubule organization, spindle pole tethering and asymmetric division during mouse oocyte meiotic maturation. Cell Cycle 6(3), 330–338.CrossRefGoogle ScholarPubMed
Zhang, D., Yin, S., Jiang, M.X., Ma, W., Hou, Y., Liang, C.G., Yu, L.Z., Wang, W.H. & 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(4), 685–695.Google Scholar
Zhang, H., Shi, X., Zhang, Q.J., Hampong, M., Paddon, H., Wahyuningsih, D. & Pelech, S. (2002). Nocodazole-induced p53-dependent c-Jun N-terminal kinase activation reduces apoptosis in human colon carcinoma HCT116 cells. J Biol Chem 277(46), 43648–43658.Google Scholar