The conserved kinase SRPK regulates karyosome formation and spindle microtubule assembly in Drosophila oocytes

Journal of Cell Science

Volumn 125, Issue 19, 2012, Pages 4457-4462

  Loh, Benjamin J ^a   Cullen, C Fiona ^a   Vogt, Nina ^b,c   Ohkura, Hiroyuki ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c NEW YORK UNIVERSITY   (United States)

Author keywords

Drosophila; Kinase; Meiosis; Mitosis; Oocyte; Spindle; SRPK

Indexed keywords

PROTEIN KINASE; SR PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMOSOME MUTATION; CONTROLLED STUDY; CYTOLOGY; DNA REPAIR; DROSOPHILA; FEMALE; GENE CLUSTER; HETEROCHROMATIN; KARYOSOME; MEIOSIS; MICROTUBULE ASSEMBLY; MITOSIS; MOLECULAR CLONING; NONHUMAN; OOCYTE; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; RNA INTERFERENCE; SPINDLE CELL;

ANIMALS; CELL CYCLE CHECKPOINTS; CENTROMERE; CHROMOSOMES, INSECT; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MEIOSIS; MITOTIC SPINDLE APPARATUS; MUTATION; OOCYTES; PROTEIN-SERINE-THREONINE KINASES;

EID: 84872186357     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.107979     Document Type: Article

References (38)

1. Abdu, U., Brodsky, M. and Schüpbach, T. (2002). Activation of a meiotic checkpoint during Drosophila oogenesis regulates the translation of Gurken through Chk2/Mnk. Curr. Biol. 12, 1645-1651.
2. Ashburner, M., Golic, K. G. and Hawley, R. S. (2005). Drosophila: A Laboratory Handbook, New York, NY: Cold Spring Harbor Laboratory Press.
3. Barbosa, V., Kimm, N. and Lehmann, R. (2007). A maternal screen for genes regulating Drosophila oocyte polarity uncovers new steps in meiotic progression. Genetics 176, 1967-1977.
4. Bettencourt-Dias, M., Giet, R., Sinka, R., Mazumdar, A., Lock, W. G., Balloux, F., Zafiropoulos, P. J., Yamaguchi, S., Winter, S., Carthew, R. W. et al. (2004). Genome-wide survey of protein kinases required for cell cycle progression. Nature 432, 980-987.
5. Carazo-Salas, R. E., Guarguaglini, G., Gruss, O. J., Segref, A., Karsenti, E. and Mattaj, I. W. (1999). Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation. Nature 400, 178-181.
6. Cesario, J. and McKim, K. S. (2011). RanGTP is required for meiotic spindle organization and the initiation of embryonic development in Drosophila. J. Cell Sci. 124, 3797-3810.
7. Cullen, C. F. and Ohkura, H. (2001). Msps protein is localized to acentrosomal poles to ensure bipolarity of Drosophila meiotic spindles. Nat. Cell Biol. 3, 637-642.
8. Cullen, C. F., Brittle, A. L., Ito, T. and Ohkura, H. (2005). The conserved kinase NHK-1 is essential for mitotic progression and unifying acentrosomal meiotic spindles in Drosophila melanogaster. J. Cell Biol. 171, 593-602.
9. Dernburg, A. F., Sedat, J. W. and Hawley, R. S. (1996). Direct evidence of a role for heterochromatin in meiotic chromosome segregation. Cell 86, 135-146.
10. Dumont, J., Petri, S., Pellegrin, F., Terret, M. E., Bohnsack, M. T., Rassinier, P., Georget, V., Kalab, P., Gruss, O. J. and Verlhac, M. H. (2007). A centriole- and RanGTP-independent spindle assembly pathway in meiosis I of vertebrate oocytes. J. Cell Biol. 176, 295-305.
11. Dzhindzhev, N. S., Rogers, S. L., Vale, R. D. and Ohkura, H. (2005). Distinct mechanisms govern the localisation of Drosophila CLIP-190 to unattached kinetochores and microtubule plus-ends. J. Cell Sci. 118, 3781-3790.
12. Gergely, F., Kidd, D., Jeffers, K., Wakefield, J. G. and Raff, J. W. (2000). D-TACC: a novel centrosomal protein required for normal spindle function in the early Drosophila embryo. EMBO J. 19, 241-252.
13. Ghabrial, A., Ray, R. P. and Schüpbach, T. (1998). okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev. 12, 2711-2723.
14. Giannakouros, T., Nikolakaki, E., Mylonis, I. and Georgatsou, E. (2011). Serinearginine protein kinases: a small protein kinase family with a large cellular presence. FEBS J. 278, 570-586.
15. Gruss, O. J., Carazo-Salas, R. E., Schatz, C. A., Guarguaglini, G., Kast, J., Wilm, M., Le Bot, N., Vernos, I., Karsenti, E. and Mattaj, I. W. (2001). Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 104, 83-93.
16. Jang, J. K., Rahman, T. and McKim, K. S. (2005). The kinesinlike protein Subito contributes to central spindle assembly and organization of the meiotic spindle in Drosophila oocytes. Mol. Biol. Cell 16, 4684-4694.
17. Kalab, P., Weis, K. and Heald, R. (2002). Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 295, 2452-2456.
18. King, R. C. (1970). Ovarian Development in Drosophila melanogaster. New York, NY: Academic Press.
19. Klattenhoff, C., Bratu, D. P., McGinnis-Schultz, N., Koppetsch, B. S., Cook, H. A. and Theurkauf, W. E. (2007). Drosophila rasiRNA pathway mutations disrupt embryonic axis specification through activation of an ATR/Chk2 DNA damage response. Dev. Cell 12, 45-55.
20. Lancaster, O. M., Cullen, C. F. and Ohkura, H. (2007). NHK-1 phosphorylates BAF to allow karyosome formation in the Drosophila oocyte nucleus. J. Cell Biol. 179, 817-824.
21. Lancaster, O. M., Breuer, M., Cullen, C. F., Ito, T. and Ohkura, H. (2010). The meiotic recombination checkpoint suppresses NHK-1 kinase to prevent reorganisation of the oocyte nucleus in Drosophila. PLoS Genet. 6, e1001179.
22. Lindsley, D. L. and Zimm, G. G. (1992). The Genome of Drosophila melanogaster. San Diego, CA: Academic Press.
23. Loomis, R. J., Naoe, Y., Parker, J. B., Savic, V., Bozovsky, M. R., Macfarlan, T., Manley, J. L. and Chakravarti, D. (2009). Chromatin binding of SRp20 and ASF/ SF2 and dissociation from mitotic chromosomes is modulated by histone H3 serine 10 phosphorylation. Mol. Cell 33, 450-461.
24. McKim, K. S. and Hawley, R. S. (1995). Chromosomal control of meiotic cell division. Science 270, 1595-1601.
25. McQuilton, P., St Pierre, S. E., Thurmond, J. FlyBase Consortium (2012). FlyBase 101-the basics of navigating FlyBase. Nucleic Acids Res. 40, D706-D714.
26. Mehrotra, S. and McKim, K. S. (2006). Temporal analysis of meiotic DNA doublestrand break formation and repair in Drosophila females. PLoS Genet. 2, e200.
27. Meireles, A. M., Fisher, K. H., Colombié, N., Wakefield, J. G. and Ohkura, H. (2009). Wac: a new Augmin subunit required for chromosome alignment but not for acentrosomal microtubule assembly in female meiosis. J. Cell Biol. 184, 777-784.
28. Ohkura, H., Garcia, M. A. and Toda, T. (2001). Dis1/TOG universal microtubule adaptors - one MAP for all? J. Cell Sci. 114, 3805-3812.
29. Parfenov, V., Potchukalina, G., Dudina, L., Kostyuchek, D. and Gruzova, M. (1989). Human antral follicles: oocyte nucleus and the karyosphere formation (electron microscopic and autoradiographic data). Gamete Res. 22, 219-231.
30. Sampath, S. C., Ohi, R., Leismann, O., Salic, A., Pozniakovski, A. and Funabiki, H. (2004). The chromosomal passenger complex is required for chromatin-induced microtubule stabilization and spindle assembly. Cell 118, 187-202.
31. Staeva-Vieira, E., Yoo, S. and Lehmann, R. (2003). An essential role of DmRad51/ SpnA in DNA repair and meiotic checkpoint control. EMBO J. 22, 5863-5874.
32. Takeuchi, M. and Yanagida, M. (1993). A mitotic role for a novel fission yeast protein kinase dsk1 with cell cycle stage dependent phosphorylation and localization. Mol. Biol. Cell 4, 247-260.
33. Tournebize, R., Popov, A., Kinoshita, K., Ashford, A. J., Rybina, S., Pozniakovsky, A., Mayer, T. U., Walczak, C. E., Karsenti, E. and Hyman, A. A. (2000). Control of microtubule dynamics by the antagonistic activities of XMAP215 and XKCM1 in Xenopus egg extracts. Nat. Cell Biol. 2, 13-19.
34. Venken, K. J., Carlson, J. W., Schulze, K. L., Pan, H., He, Y., Spokony, R., Wan, K. H., Koriabine, M., de Jong, P. J., White, K. P., Bellen, H. J. and Hoskins, R. A. (2009). Versatile P[acman] BAC libraries for transgenesis studies in Drosophila melanogaster. Nat. Methods 6, 431-434.
35. Vogt, N., Koch, I., Schwarz, H., Schnorrer, F. and Nü sslein-Volhard, C. (2006). The gammaTuRC components Grip75 and Grip128 have an essential microtubuleanchoring function in the Drosophila germline. Development 133, 3963-3972.
36. Wilde, A. and Zheng, Y. (1999). Stimulation of microtubule aster formation and spindle assembly by the small GTPase Ran. Science 284, 1359-1362.
37. Zuccotti, M., Giorgi Rossi, P., Martinez, A., Garagna, S., Forabosco, A. and Redi, C. A. (1998). Meiotic and developmental competence of mouse antral oocytes. Biol. Reprod. 58, 700-704.
38. Zuccotti, M., Ponce, R. H., Boiani, M., Guizzardi, S., Govoni, P., Scandroglio, R., Garagna, S. and Redi, C. A. (2002). The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote 10, 73-78.