p21-activated kinase 1 activity is required for histone H3 Ser10 phosphorylation and chromatin condensation in mouse oocyte meiosis
Nana Zhang A , Xiuhong Li B , Xiaoyun Liu A , Yan Cao A , Dandan Chen A , Xiaoyu Liu A , Qian Wang A , Juan Du A , Jing Weng C D and Wei Ma A D
+ Author Affiliations
- Author Affiliations
A Department of Histology and Embryology, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.
B Biospecimen and Clinical Data Repository, Beijing Friendship Hospital, Capital Medical University, Beijing, 100050, China.
C Experimental Center for Basic Medical Teaching, School of Basic Medical Sciences, Capital Medical University, Beijing, 100069, China.
D Corresponding authors. Emails: mawei1026@ccmu.edu.cn; wengjing@ccmu.edu.cn
Reproduction, Fertility and Development 29(7) 1287-1296 https://doi.org/10.1071/RD16026
Submitted: 13 January 2016 Accepted: 6 April 2016 Published: 11 May 2016
Abstract
p21-activated kinase 1 (Pak1) is essential for a variety of cellular events, including gene transcription, cytoskeletal organisation, cell proliferation and apoptosis. Pak1 is activated upon autophosphorylation on many amino residues; in particular, phosphorylation on Thr423 maintains maximal Pak1 activation. In the present study we investigated the protein expression, subcellular localisation and function of Pak1 phosphorylated on Thr423 (pPak1Thr423) in mouse oocytes. pPak1Thr423 was detected upon meiotic resumption and localised on the condensing chromatin. Thr423 phosphorylation was markedly suppressed by the Pak1 ATP-competitive inhibitor PF-3758309, but not by the allosteric inhibitors IPA-3 (2.5 μM and 10 μM) (1, 1′-dithiobis-2-naphthalenol) and TAT-PAK18 (10 μM), which prevent the binding of Pak1 to its upstream activators GTPase Cdc42/Rac and Pak-interacting exchange factor (PIX), respectively, implying that Pak1 activation may be independent of GTPase and PIX in oocyte meiosis. Inhibition of Pak1 activation concomitantly restrained histone H3 phosphorylation on Ser10 and consequently inhibited chromatin condensation; however, this phenotype was reversed by concomitant administration of the Pak1 activator FTY720. The changes in the pattern of expression of phosphorylated extracellular signal-regulated kinase 1/2 in response to PF-3758309 or FTY720 were the same as seen for pPak1Thr423. These results show that activated Pak1 regulates chromatin condensation by promoting H3 Ser10 phosphorylation in oocytes after the resumption of meiotic progression.
Additional keywords: Cdc42, chromosome separation, FTY720, germinal vesicle (GV), meiotic resumption, PF3758309, PIX.
References
Beeser, A., Jaffer, Z. M., Hofmann, C., and Chernoff, J. (2005). Role of group A p21-activated kinases in activation of extracellular-regulated kinase by growth factors. J. Biol. Chem. 280, 36 609–36 615.| Role of group A p21-activated kinases in activation of extracellular-regulated kinase by growth factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFKht7fN&md5=475e95275fa243b5428522b49e021dcdCAS |
Brown, M. C., West, K. A., and Turner, C. E. (2002). Paxillin-dependent paxillin kinase linker and p21-activated kinase localization to focal adhesions involves a multistep activation pathway. Mol. Biol. Cell 13, 1550–1565.
| Paxillin-dependent paxillin kinase linker and p21-activated kinase localization to focal adhesions involves a multistep activation pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktFyru70%3D&md5=5d5b0cbd887c0ae5c3de388e910c768fCAS | 12006652PubMed |
Bui, H. T., Yamaoka, E., and Miyano, T. (2004). Involvement of histone H3 (Ser10) phosphorylation in chromosome condensation without Cdc2 kinase and mitogen-activated protein kinase activation in pig oocytes. Biol. Reprod. 70, 1843–1851.
| Involvement of histone H3 (Ser10) phosphorylation in chromosome condensation without Cdc2 kinase and mitogen-activated protein kinase activation in pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmtLk%3D&md5=743bfe8fb881e4081c857a8433b607ddCAS | 14960481PubMed |
Bui, H. T., Thuan, N. V., Kishigami, S., Wakayama, S., Hikichi, T., Ohta, H., Mizutani, E., Yamaoka, E., Wakayama, W., and Miyano, T. (2007). Regulation of chromatin and chromosome morphology by histone H3 modifications in pig oocytes. Reproduction 133, 371–382.
| Regulation of chromatin and chromosome morphology by histone H3 modifications in pig oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVOjtrs%3D&md5=54c63549bb9289ebaa4e7b4d45612435CAS | 17307905PubMed |
Castellano-Pozo, M., Santos-Pereira, J. M., Rondón, A. G., Barroso, S., Andújar, E., Pérez-Alegre, M., García-Muse, T., and Aguilera, A. (2013). R loops are linked to histone H3 S10 phosphorylation and chromatin condensation. Mol. Cell 52, 583–590.
| R loops are linked to histone H3 S10 phosphorylation and chromatin condensation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCltLjJ&md5=f90709a9e7980998677ee176f991769fCAS | 24211264PubMed |
Chow, H. Y., Jubb, A. M., Koch, J. N., Jaffer, Z. M., Stepanova, D., Campbell, D. A., Duron, S. G., O’Farrell, M., Cai, Q., Klein, A. J., Gutkind, J. S., Hoeflich, K. P., and Chernoff, J. (2012). p21-activated kinase 1 is required for efficient tumor formation and progression in a Ras-mediated skin cancer model. Cancer Res. 72, 5966–5975.
| p21-activated kinase 1 is required for efficient tumor formation and progression in a Ras-mediated skin cancer model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1yntLzI&md5=7a382eefb31d2dfc091e2a13edf58654CAS | 22983922PubMed |
de la Barre, A. E., Angelov, D., Molla, A., and Dimitrov, S. (2001). The N-terminus of histone H2B, but not that of histone H3 or its phosphorylation, is essential for chromosome condensation. EMBO J. 20, 6383–6393.
| The N-terminus of histone H2B, but not that of histone H3 or its phosphorylation, is essential for chromosome condensation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovFOntLg%3D&md5=941be1bb7a4b0bb09a9e3606fe612f86CAS | 11707409PubMed |
Deacon, S. W., Beeser, A., Fukui, J. A., Rennefahrt, U. E. E., Myers, C., Chernoff, J., and Peterson, J. R. (2008). An isoform-selective, small-molecule inhibitor targets the autoregulatory mechanism of p21-activated kinase. Chem. Biol. 15, 322–331.
| An isoform-selective, small-molecule inhibitor targets the autoregulatory mechanism of p21-activated kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvFWqtr0%3D&md5=9342faa963b6e83f4862e5e984e5c4f6CAS | 18420139PubMed |
Ding, J., Swain, J. E., and Smith, G. D. (2011). Aurora kinase-A regulates microtubule organizing center (MTOC) localization, chromosome dynamics, and histone-H3 phosphorylation in mouse oocytes. Mol. Reprod. Dev. 78, 80–90.
| Aurora kinase-A regulates microtubule organizing center (MTOC) localization, chromosome dynamics, and histone-H3 phosphorylation in mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitVyltLw%3D&md5=ff6469d0d1491e5b498b194e976694d3CAS | 21274965PubMed |
Dummler, B., Ohshiro, K., Kumar, R., and Field, J. (2009). Pak protein kinases and their role in cancer. Cancer Metastasis Rev. 28, 51–63.
| Pak protein kinases and their role in cancer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVWntrY%3D&md5=de648a5f752cd3d61969325f4b8b2057CAS | 19165420PubMed |
Egom, E. E. A., Ke, Y., Musa, H., Mohamed, T. M. A., Wang, T., Cartwright, E., Solaro, R. J., and Lei, M. (2010). FTY720 prevents ischemia/reperfusion injury-associated arrhythmias in an ex vivo rat heart model via activation of Pak1/Akt signaling. J. Mol. Cell. Cardiol. 48, 406–414.
| FTY720 prevents ischemia/reperfusion injury-associated arrhythmias in an ex vivo rat heart model via activation of Pak1/Akt signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpslCgsQ%3D%3D&md5=73d7c060a7daefda5d5dfed1740bf52eCAS |
Fan, H. Y., and Sun, Q. Y. (2004). Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 70, 535–547.
| Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Chsro%3D&md5=0e3922fe1fa3d71454ba9a06a22ead6fCAS | 14613897PubMed |
Fuchs, J., Demidov, D., Houben, A., and Schubert, I. (2006). Chromosomal histone modification patterns: from conservation to diversity. Trends Plant Sci. 11, 199–208.
| Chromosomal histone modification patterns: from conservation to diversity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvVGnsLk%3D&md5=d8a6b2bfa19b4fd4c6fc6e08d858bdd0CAS | 16546438PubMed |
George, O., Johnston, M. A., and Shuster, C. B. (2006). Aurora B kinase maintains chromatin organization during the MI to MII transition in surf clam oocytes. Cell Cycle 5, 2648–2656.
| Aurora B kinase maintains chromatin organization during the MI to MII transition in surf clam oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhslyhsLg%3D&md5=0c4aad5d1e8960ca45fc06759f5f658aCAS | 17172833PubMed |
Giet, R., and Glover, D. M. (2001). Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152, 669–682.
| Drosophila Aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtlGmtrc%3D&md5=98b73e51ba61e00f9be9f35b0ac92683CAS | 11266459PubMed |
Gu, L., Wang, Q., and Sun, Q. Y. (2010). Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions. Cell Cycle 9, 1942–1950.
| Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht12kur7M&md5=e60d18a38c7835a0130142d6e7274af3CAS | 20436284PubMed |
Hashimoto, H., Sudo, T., Maruta, H., and Nishimural, R. (2010). The direct PAK1 inhibitor, TAT-PAK18, blocks preferentially the growth of human ovarian cancer cell lines in which PAK1 is abnormally activated by autophosphorylation at Thr 423. Drug Discov. Ther. 4, 1–4.
| 1:CAS:528:DC%2BC3cXmtFClurs%3D&md5=0641bcbc441fa6c6c95cf0427048511eCAS | 22491145PubMed |
Houben, A., Wako, T., Rieko, F. S., Presting, G., Kunzel, G., Schubert, I., and Fukui, K. (1999). The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. Plant J. 18, 675–679.
| The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsFGhtrw%3D&md5=5ec0a9d57717abd38b8033b22143a146CAS | 10417719PubMed |
Jelínková, L., and Kubelka, M. (2006). Neither Aurora B activity nor histone H3 phosphorylation is essential for chromosome condensation during meiotic maturation of porcine oocytes. Biol. Reprod. 74, 905–912.
| Neither Aurora B activity nor histone H3 phosphorylation is essential for chromosome condensation during meiotic maturation of porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 16452462PubMed |
Ji, J. H., Hwang, H. I., Lee, H. J., Hyun, S. Y., Kang, H. J., and Jang, Y. J. (2010). Purification and proteomic identification of putative upstream regulators of polo-like kinase-1 from mitotic cell extracts. FEBS Lett. 584, 4299–4305.
| Purification and proteomic identification of putative upstream regulators of polo-like kinase-1 from mitotic cell extracts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSmurbN&md5=07291f74209c94687dd995f38e4d217cCAS | 20869364PubMed |
King, C. C., Gardiner, E. M. M., Zenke, F. T., Bohl, B. P., Newtoni, A. C., Hemmings, B. A., and Bokoch, G. M. (2000). p21-activated kinase (Pak1) is phosphorylated and activated by 3-phosphoinositide-dependent kinase-1 (PDK1). J. Biol. Chem. 275, 41 201–41 209.
| p21-activated kinase (Pak1) is phosphorylated and activated by 3-phosphoinositide-dependent kinase-1 (PDK1).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsVKjsA%3D%3D&md5=5be7b53b4b6c3ad91fa7f782e43538f2CAS |
Li, F., Adam, L., Vadlamudi, R. K., Zhou, H., Sen, S., Chernoff, J., Mandal, M., and Kumar, R. (2002). p21-activated kinase 1 interacts with and phosphorylates histone H3 in breast cancer cells. EMBO Rep. 3, 767–773.
| p21-activated kinase 1 interacts with and phosphorylates histone H3 in breast cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVOgtL8%3D&md5=cb7bb76fde0741c9f2ee396d96722bc8CAS | 12151336PubMed |
Li, X., Zhu, Y. B., Cao, Y., Wang, Q., Du, J., Tian, J. H., Liang, Y. J., and Ma, W. (2016). LIM kinase activity is required for microtubule organising centre positioning in mouse oocyte meiosis. Reprod. Fertil. Dev. , .
| LIM kinase activity is required for microtubule organising centre positioning in mouse oocyte meiosis.Crossref | GoogleScholarGoogle Scholar | 26733281PubMed |
Lin, S. L., Qi, S. T., Sun, S. C., Wang, Y. P., Schatten, H., and Sun, Q. Y. (2010). PAK1 regulates spindle microtubule organization during oocyte meiotic maturation. Front. Biosci. (Elite Ed.) 2, 1254–1264.
| PAK1 regulates spindle microtubule organization during oocyte meiotic maturation.Crossref | GoogleScholarGoogle Scholar | 20515799PubMed |
Liu, F., Jia, L., Thompson-Baine, A. M., Puglise, J. M., Terbeest, M. B., and Zegers, M. M. (2010). Cadherins and Pak1 control contact inhibition of proliferation by Pak1-betaPIX-GIT complex-dependent regulation of cell-matrix signaling. Mol. Cell. Biol. 30, 1971–1983.
| Cadherins and Pak1 control contact inhibition of proliferation by Pak1-betaPIX-GIT complex-dependent regulation of cell-matrix signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksFKqsrc%3D&md5=851cfbe83bb671d363c2d595598a159cCAS | 20154149PubMed |
MacCallum, D. E., Losada, A., Kobayashi, R., and Hirano, T. (2002). ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol. Biol. Cell 13, 25–39.
| ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvFCjsg%3D%3D&md5=58caa12db1f6476ed85fe71ab6b04993CAS | 11809820PubMed |
Manser, E., Chong, C., Zhao, Z. S., Leung, T., and Michael, G. (1995). Molecular cloning of a new member of the p21-Cdc42/Rac-activated kinase (PAK) Family. J. Biol. Chem. 270, 25 070–25 078.
| Molecular cloning of a new member of the p21-Cdc42/Rac-activated kinase (PAK) Family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFWmtr8%3D&md5=4d950aeb69165354e240931bc8d25ae8CAS |
Maroto, B., Ye, M. B., von Lohneysen, K., Schnelzer, A., and Knaus, U. G. (2008). P21-activated kinase is required for mitotic progression and regulates Plk1. Oncogene 27, 4900–4908.
| P21-activated kinase is required for mitotic progression and regulates Plk1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVWgu7fN&md5=594bfdc003bc19d79ab0a45615eedea5CAS | 18427546PubMed |
Molli, P. R., Li, D. Q., Brion, M., Rayala, S. K., Kumar, R., and Li, D. Q. (2009). PAK signaling in oncogenesis. Oncogene 28, 2545–2555.
| PAK signaling in oncogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtlars74%3D&md5=5bafd1f94889493840c47fd03f3232ebCAS | 19465939PubMed |
Murray, B. W., Guo, C. X., Piraino, J., Westwick, J. K., Zhang, C., Lamerdin, J., Dagostino, E., Knighton, D., Loi, C. M., Zager, M., Kraynov, E., Popoff, I., Christensen, J. G., Martinez, R., Kephart, S. E., Marakovits, J., Karlicek, S., Bergqvist, S., and Smeal, T. (2010). Small-molecule p21-activated kinase inhibitor PF-3758309 is a potent inhibitor of oncogenic signaling and tumor growth. Proc. Natl Acad. Sci. USA 107, 9446–9451.
| Small-molecule p21-activated kinase inhibitor PF-3758309 is a potent inhibitor of oncogenic signaling and tumor growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslWqtrw%3D&md5=e6c01847b9c2b17feb63aef6b24ee267CAS | 20439741PubMed |
Nayal, A., Webb, D. J., Brown, C. M., Schaefer, E. M., Vicente-Manzanares, M., and Horwitz, A. R. (2006). Paxillin phosphorylation at Ser273 localizes a GIT1-PIX-PAK complex and regulates adhesion and protrusion dynamics. J. Cell Biol. 173, 587–589.
| Paxillin phosphorylation at Ser273 localizes a GIT1-PIX-PAK complex and regulates adhesion and protrusion dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVaqtrw%3D&md5=c46097ac4de11d104a2c504944e7c603CAS | 16717130PubMed |
Parrini, M. C. (2012). Untangling the complexity of PAK1 dynamics: The future challenge. Cell. Logist. 2, 78–83.
| Untangling the complexity of PAK1 dynamics: The future challenge.Crossref | GoogleScholarGoogle Scholar | 23125950PubMed |
Parrini, M. C., and Matsuda, M. (2005). Spatiotemporal regulation of the Pak1 kinase. Biochem. Soc. Trans. 33, 646–648.
| Spatiotemporal regulation of the Pak1 kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvFSnurs%3D&md5=7c4c5c5a03f8167378943cba322530adCAS | 16042564PubMed |
Parrini, M. C., Camonis, J., Matsuda, M., and de Gunzburg, J. (2009). Dissecting activation of the PAK1 kinase at protrusions in living cells. J. Biol. Chem. 284, 24 133–24 143.
| Dissecting activation of the PAK1 kinase at protrusions in living cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGgsr7E&md5=4536dc4f48a80378ef27921e53ddb4c6CAS |
Rane, C. K., and Minden, A. (2014). P21 activated kinases: structure, regulation, and functions. Small GTPases 5, e28003.
| P21 activated kinases: structure, regulation, and functions.Crossref | GoogleScholarGoogle Scholar | 24658305PubMed |
Sells, M. A., Pfaff, A., and Chernoff, J. (2000). Temporal and spatial distribution of activated Pak1 in fibroblasts. J. Cell Biol. 151, 1449–1458.
| Temporal and spatial distribution of activated Pak1 in fibroblasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosleg&md5=80b5dc69efdbeaf5f25c26575e558709CAS | 11134074PubMed |
Swain, J. E., Ding, J., Brautigan, D. L., Emma, V. M., and Smith, G. D. (2007). Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity. Biol. Reprod. 76, 628–638.
| Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsFCnu7k%3D&md5=eaa8f053d05d8ba4428166d548cf94fcCAS | 17182892PubMed |
Van Hooser, A., Goodrich, D. W., Allis, C. D., Brinkley, B. R., and Mancini, M. A. (1998). Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J. Cell Sci. 111, 3497–3506.
| 1:CAS:528:DyaK1MXjvVeqtA%3D%3D&md5=ce29423b175590292cd0fbd16552c997CAS | 9811564PubMed |
Wang, B., Ma, W., Xu, X., Wang, C., Zhu, Y., An, N., An, L., Wu, Z., and Tian, J. (2013a). Phosphorylation of histone H3 on Ser10 by auto-phosphorylated PAK1 is not essential for chromatin condensation and meiotic progression in porcine oocytes. J. Anim. Sci. Biotechnol. 4, 13.
| Phosphorylation of histone H3 on Ser10 by auto-phosphorylated PAK1 is not essential for chromatin condensation and meiotic progression in porcine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXns1Orsro%3D&md5=7783e125a5ddb37f3939ce9ee9808639CAS | 23521812PubMed |
Wang, Z., Fu, M., Wang, L., Liu, J., Li, Y., Brakebusch, C., and Mei, Q. (2013b). p21-activated kinase 1 (PAK1) can promote ERK activation in a kinase-independent manner. J. Biol. Chem. 288, 20 093–20 099.
| p21-activated kinase 1 (PAK1) can promote ERK activation in a kinase-independent manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVKntLfL&md5=86ce4c43b9d245f2551325033b8cb076CAS |
Wang, Q., Wei, H. J., Du, J., Cao, Y., Zhang, N. N., Liu, X. Y., Liu, X. Y., Chen, D. D., and Ma, W. (2016). H3 Thr3 phosphorylation is crucial for meiotic resumption and anaphase onset in oocyte meiosis. Cell Cycle 15, 213–224.
| H3 Thr3 phosphorylation is crucial for meiotic resumption and anaphase onset in oocyte meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XktlehtA%3D%3D&md5=62389075061c81ca5ab85c0f22476218CAS | 26636626PubMed |
Wei, Y., Mizzen, C. A., Cook, R. G., Gorovsky, M. A., and Allise, C. D. (1998). Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc. Natl Acad. Sci. USA 95, 7480–7484.
| Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktFChtbg%3D&md5=b54b91258c99d30f92e86714a955f4ebCAS | 9636175PubMed |
Wei, Y., Yu, L., Bowen, J., Gorovsky, M. A., and Allis, C. D. (1999). Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97, 99–109.
| Phosphorylation of histone H3 is required for proper chromosome condensation and segregation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitlGmtLo%3D&md5=47dd29b2c949baa4bc42a5511a6af04cCAS | 10199406PubMed |
Wilkins, B. J., Rall, N. A., Ostwal, Y., Kruitwagen, T., Kyoko, H. H., Winkler, M., Barral, Y., Fishle, W., and Neumann, H. (2014). A cascade of histone modifications induces chromatin condensation in mitosis. Science 343, 77–80.
| A cascade of histone modifications induces chromatin condensation in mitosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkslOr&md5=63d0b515bdd3a26dadcd28121f6ff2e8CAS | 24385627PubMed |
Zhao, Z. S., Lim, J. P., Ng, Y. W., Lim, L., and Manser, Ed. (2005). The GIT-associated kinase PAK targets to the centrosome and regulates Aurora-A. Mol. Cell 20, 237–249.
| The GIT-associated kinase PAK targets to the centrosome and regulates Aurora-A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1SntrfM&md5=44addc4f403730e2caefa76f98986b27CAS | 16246726PubMed |
