Phosphorylation of threonine 3 on histone H3 by haspin kinase is required for meiosis I in mouse oocytes

Journal of Cell Science

Volumn 127, Issue 23, 2014, Pages 5066-5078

  Nguyen, Alexandra L ^a   Gentilello, Amanda S ^a   Balboula, Ahmed Z ^a,b   Shrivastava, Vibha ^a   Ohring, Jacob ^a   Schindler, Karen ^a  

^a RUTGERS UNIVERSITY   (United States)

^b Mansoura University   (Egypt)

Author keywords

Aurora kinase; Haspin kinase; Histone phosphorylation; Meiosis I; Meiotic maturation; Oocyte

Indexed keywords

ACTIN; CONDENSIN; HASPIN KINASE; HISTONE H3; MESSENGER RNA; PHALLOIDIN; PHOSPHOTRANSFERASE; THREONINE; THREONINE 3; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; AURKC PROTEIN, MOUSE; AURORA C KINASE; DNA BINDING PROTEIN; GSG2 PROTEIN, MOUSE; HISTONE; MULTIPROTEIN COMPLEX; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE;

ANEUPLOIDY; ANIMAL CELL; ARTICLE; CELL MATURATION; CENTROMERE; CHROMOSOME ARM; CHROMOSOME NUMBER; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; HISTONE PHOSPHORYLATION; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; INTERPHASE; KINETOCHORE MICROTUBULE; MEIOSIS; METAPHASE; MITOSIS; MOUSE; NONHUMAN; OOCYTE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SISTER CHROMATID; SOMATIC CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; DRUG EFFECTS; ENZYMOLOGY; FEMALE; GENETIC TRANSFECTION; GENETICS; MEIOTIC PROPHASE I; METABOLISM; MICROTUBULE; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TIME;

ADENOSINE TRIPHOSPHATASES; ANEUPLOIDY; ANIMALS; AURORA KINASE C; CELLS, CULTURED; CHROMOSOME SEGREGATION; DNA-BINDING PROTEINS; FEMALE; HISTONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KINETOCHORES; MEIOTIC PROPHASE I; MICE; MICROTUBULES; MULTIPROTEIN COMPLEXES; OOCYTES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; THREONINE; TIME FACTORS; TRANSFECTION;

EID: 84914127377     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.158840     Document Type: Article

References (51)

1. Ashtiyani, R. K., Moghaddam, A. M., Schubert, V., Rutten, T., Fuchs, J., Demidov, D., Blattner, F. R. and Houben, A. (2011). AtHaspin phosphorylates histone H3 at threonine 3 during mitosis and contributes to embryonic patterning in Arabidopsis. Plant J. 68, 443-454.
2. Balboula, A. Z. and Schindler, K. (2014). Selective disruption of aurora C kinase reveals distinct functions from aurora B kinase during meiosis in mouse oocytes. PLoS Genet. 10, e1004194.
3. Balboula, A. Z., Stein, P., Schultz, R. M. and Schindler, K. (2014). Knockdown of RBBP7 unveils a requirement of histone deacetylation for CPC function in mouse oocytes. Cell Cycle 13, 600-611.
4. Bembenek, J. N., Verbrugghe, K. J., Khanikar, J., Csankovszki, G. and Chan, R. C. (2013). Condensin and the spindle midzone prevent cytokinesis failure induced by chromatin bridges in C. elegans embryos. Curr. Biol. 23, 937-946.
5. Carmena, M., Wheelock, M., Funabiki, H. and Earnshaw, W. C. (2012). The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nat. Rev. Mol. Cell Biol. 13, 789-803.
6. Chiang, T., Duncan, F. E., Schindler, K., Schultz, R. M. and Lampson, M. A. (2010). Evidence that weakened centromere cohesion is a leading cause of age-related aneuploidy in oocytes. Curr. Biol. 20, 1522-1528.
7. Collette, K. S., Petty, E. L., Golenberg, N., Bembenek, J. N. and Csankovszki, G. (2011). Different roles for Aurora B in condensin targeting during mitosis and meiosis. J. Cell Sci. 124, 3684-3694.
8. Dai, J. and Higgins, J. M. (2005). Haspin: a mitotic histone kinase required for metaphase chromosome alignment. Cell Cycle 4, 665-668.
9. Dai, J., Sultan, S., Taylor, S. S. and Higgins, J. M. (2005). The kinase haspin is required for mitotic histone H3 Thr 3 phosphorylation and normal metaphase chromosome alignment. Genes Dev. 19, 472-488.
10. Dai, J., Sullivan, B. A. and Higgins, J. M. (2006). Regulation of mitotic chromosome cohesion by Haspin and Aurora B. Dev. Cell 11, 741-750.
11. Dai, J., Kateneva, A. V. and Higgins, J. M. (2009). Studies of haspin-depleted cells reveal that spindle-pole integrity in mitosis requires chromosome cohesion. J. Cell Sci. 122, 4168-4176.
12. De Antoni, A., Maffini, S., Knapp, S., Musacchio, A. and Santaguida, S. (2012). A small-molecule inhibitor of Haspin alters the kinetochore functions of Aurora B. J. Cell Biol. 199, 269-284.
13. Duncan, F. E., Chiang, T., Schultz, R. M. and Lampson, M. A. (2009). Evidence that a defective spindle assembly checkpoint is not the primary cause of maternal age-associated aneuploidy in mouse eggs. Biol. Reprod. 81, 768-776.
14. Fernández-Miranda, G., Trakala, M., Martín, J., Escobar, B., González, A., Ghyselinck, N. B., Ortega, S., Cañamero, M., Pérez de Castro, I. and Malumbres, M. (2011). Genetic disruption of aurora B uncovers an essential role for aurora C during early mammalian development. Development 138, 2661-2672.
15. Higgins, J. M. (2003). Structure, function and evolution of haspin and haspinrelated proteins, a distinctive group of eukaryotic protein kinases. Cell. Mol. Life Sci. 60, 446-462.
16. Hirano, T. (2012). Chromosome territories meet a condensin. PLoS Genet. 8, e1002939.
17. Huertas, D., Soler, M., Moreto, J., Villanueva, A., Martinez, A., Vidal, A., Charlton, M., Moffat, D., Patel, S., McDermott, J. et al. (2012). Antitumor activity of a small-molecule inhibitor of the histone kinase Haspin. Oncogene 31, 1408-1418.
18. Hunt, P. A. and Hassold, T. J. (2002). Sex matters in meiosis. Science 296, 2181- 2183.
19. Igarashi, H., Knott, J. G., Schultz, R. M. and Williams, C. J. (2007). Alterations of PLCbeta1 in mouse eggs change calcium oscillatory behavior following fertilization. Dev. Biol. 312, 321-330.
20. Kelly, A. E. and Funabiki, H. (2009). Correcting aberrant kinetochore microtubule attachments: an Aurora B-centric view. Curr. Opin. Cell Biol. 21, 51-58.
21. Kelly, A. E., Ghenoiu, C., Xue, J. Z., Zierhut, C., Kimura, H. and Funabiki, H. (2010). Survivin reads phosphorylated histone H3 threonine 3 to activate the mitotic kinase Aurora B. Science 330, 235-239.
22. Kimura, K., Cuvier, O. and Hirano, T. (2001). Chromosome condensation by a human condensin complex in Xenopus egg extracts. J. Biol. Chem. 276, 5417- 5420.
23. Lampson, M. A. and Kapoor, T. M. (2005). The human mitotic checkpoint protein BubR1 regulates chromosome-spindle attachments. Nat. Cell Biol. 7, 93-98.
24. Lane, S. I., Yun, Y. and Jones, K. T. (2012). Timing of anaphase-promoting complex activation in mouse oocytes is predicted by microtubule-kinetochore attachment but not by bivalent alignment or tension. Development 139, 1947- 1955.
25. Lee, J., Kitajima, T. S., Tanno, Y., Yoshida, K., Morita, T., Miyano, T., Miyake, M. and Watanabe, Y. (2008). Unified mode of centromeric protection by shugoshin in mammalian oocytes and somatic cells. Nat. Cell Biol. 10, 42-52.
26. Lee, J., Ogushi, S., Saitou, M. and Hirano, T. (2011). Condensins I and II are essential for construction of bivalent chromosomes in mouse oocytes. Mol. Biol. Cell 22, 3465-3477.
27. Li, X., Sakashita, G., Matsuzaki, H., Sugimoto, K., Kimura, K., Hanaoka, F., Taniguchi, H., Furukawa, K. and Urano, T. (2004). Direct association with inner centromere protein (INCENP) activates the novel chromosomal passenger protein, Aurora-C. J. Biol. Chem. 279, 47201-47211.
28. Lipp, J. J., Hirota, T., Poser, I. and Peters, J. M. (2007). Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes. J. Cell Sci. 120, 1245-1255.
29. Losada, A., Hirano, M. and Hirano, T. (2002). Cohesin release is required for sister chromatid resolution, but not for condensin-mediated compaction, at the onset of mitosis. Genes Dev. 16, 3004-3016.
30. Maiolica, A., de Medina-Redondo, M., Schoof, E. M., Chaikuad, A., Villa, F., Gatti, M., Jeganathan, S., Lou, H. J., Novy, K., Hauri, S. et al. (2014). Modulation of the chromatin phosphoproteome by the Haspin protein kinase. Mol. Cell. Proteomics 13, 1724-1740.
31. Markaki, Y., Christogianni, A., Politou, A. S. and Georgatos, S. D. (2009). Phosphorylation of histone H3 at Thr3 is part of a combinatorial pattern that marks and configures mitotic chromatin. J. Cell Sci. 122, 2809-2819.
32. Nakazawa, N., Mehrotra, R., Ebe, M. and Yanagida, M. (2011). Condensin phosphorylated by the Aurora-B-like kinase Ark1 is continuously required until telophase in a mode distinct from Top2. J. Cell Sci. 124, 1795-1807.
33. Niedzialkowska, E., Wang, F., Porebski, P. J., Minor, W., Higgins, J. M. and Stukenberg, P. T. (2012). Molecular basis for phosphospecific recognition of histone H3 tails by Survivin paralogues at inner centromeres. Mol. Biol. Cell 23, 1457-1466.
34. Ono, T., Losada, A., Hirano, M., Myers, M. P., Neuwald, A. F. and Hirano, T. (2003). Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115, 109-121.
35. Panigada, D., Grianti, P., Nespoli, A., Rotondo, G., Castro, D. G., Quadri, R., Piatti, S., Plevani, P. and Muzi-Falconi, M. (2013). Yeast haspin kinase regulates polarity cues necessary for mitotic spindle positioning and is required to tolerate mitotic arrest. Dev. Cell 26, 483-495.
36. Qian, J., Lesage, B., Beullens, M., Van Eynde, A. and Bollen, M. (2011). PP1/ Repo-man dephosphorylates mitotic histone H3 at T3 and regulates chromosomal aurora B targeting. Curr. Biol. 21, 766-773.
37. Rattani, A., Wolna, M., Ploquin, M., Helmhart, W., Morrone, S., Mayer, B., Godwin, J., Xu, W., Stemmann, O., Pendas, A. et al. (2013). Sgol2 provides a regulatory platform that coordinates essential cell cycle processes during meiosis I in oocytes. eLife 2, e01133.
38. Rieder, C. L. (1981). The structure of the cold-stable kinetochore fiber in metaphase PtK1 cells. Chromosoma 84, 145-158.
39. Sasai, K., Katayama, H., Stenoien, D. L., Fujii, S., Honda, R., Kimura, M., Okano, Y., Tatsuka, M., Suzuki, F., Nigg, E. A. et al. (2004). Aurora-C kinase is a novel chromosomal passenger protein that can complement Aurora-B kinase function in mitotic cells. Cell Motil. Cytoskeleton 59, 249-263.
40. Schindler, K., Davydenko, O., Fram, B., Lampson, M. A. and Schultz, R. M. (2012). Maternally recruited Aurora C kinase is more stable than Aurora B to support mouse oocyte maturation and early development. Proc. Natl. Acad. Sci. U. S. A. 109, E2215-E2222.
41. Sharif, B., Na, J., Lykke-Hartmann, K., McLaughlin, S. H., Laue, E., Glover, D. M. and Zernicka-Goetz, M. (2010). The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes. J. Cell Sci. 123, 4292-4300.
42. Shuda, K., Schindler, K., Ma, J., Schultz, R. M. and Donovan, P. J. (2009). Aurora kinase B modulates chromosome alignment in mouse oocytes. Mol. Reprod. Dev. 76, 1094-1105.
43. Slattery, S. D., Mancini, M. A., Brinkley, B. R. and Hall, R. M. (2009). Aurora-C kinase supports mitotic progression in the absence of Aurora-B. Cell Cycle 8, 2986-2997.
44. Stein, P. and Schindler, K. (2011). Mouse oocyte microinjection, maturation and ploidy assessment. J. Vis. Exp. 53, 2851.
45. Tanaka, H., Yoshimura, Y., Nozaki, M., Yomogida, K., Tsuchida, J., Tosaka, Y., Habu, T., Nakanishi, T., Okada, M., Nojima, H. et al. (1999). Identification and characterization of a haploid germ cell-specific nuclear protein kinase (Haspin) in spermatid nuclei and its effects on somatic cells. J. Biol. Chem. 274, 17049- 17057.
46. Tsafriri, A., Chun, S. Y., Zhang, R., Hsueh, A. J. and Conti, M. (1996). Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178, 393-402.
47. Tseng, T. C., Chen, S. H., Hsu, Y. P. and Tang, T. K. (1998). Protein kinase profile of sperm and eggs: cloning and characterization of two novel testis-specific protein kinases (AIE1, AIE2) related to yeast and fly chromosome segregation regulators. DNA Cell Biol. 17, 823-833.
48. Wang, F., Dai, J., Daum, J. R., Niedzialkowska, E., Banerjee, B., Stukenberg, P. T., Gorbsky, G. J. and Higgins, J. M. (2010). Histone H3 Thr-3 phosphorylation by Haspin positions Aurora B at centromeres in mitosis. Science 330, 231-235.
49. Wang, F., Ulyanova, N. P., van der Waal, M. S., Patnaik, D., Lens, S. M. and Higgins, J. M. (2011). A positive feedback loop involving Haspin and Aurora B promotes CPC accumulation at centromeres in mitosis. Curr. Biol. 21, 1061- 1069.
50. Wang, F., Ulyanova, N. P., Daum, J. R., Patnaik, D., Kateneva, A. V., Gorbsky, G. J. and Higgins, J. M. (2012). Haspin inhibitors reveal centromeric functions of Aurora B in chromosome segregation. J. Cell Biol. 199, 251-268.
51. Yamagishi, Y., Honda, T., Tanno, Y. and Watanabe, Y. (2010). Two histone marks establish the inner centromere and chromosome bi-orientation. Science 330, 239-243.