Polo-mediated phosphorylation of maelstrom regulates oocyte determination during oogenesis in drosophila

Development (Cambridge)

Volumn 139, Issue 24, 2012, Pages 4505-4513

  Pek, Jun Wei ^a,b   Ng, Bing Fu ^a   Kai, Toshie ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b GEOPHYSICAL LABORATORY   (United States)

Author keywords

Drosophila; Germline; Maelstrom; Nuage; Pachytene checkpoint; Phosphorylation; Polo; Sir2

Indexed keywords

HIGH MOBILITY GROUP PROTEIN; MAELSTROM PROTEIN; MICRORNA; PIWI INTERACTING RNA; POLO LIKE KINASE; SILENT INFORMATION REGULATOR PROTEIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE CHECKPOINT; CELL DIFFERENTIATION; DROSOPHILA; FEMALE; GAMETOGENESIS; GERMLINE MICRONUCLEUS; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY; PACHYTENE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STEM CELL; WESTERN BLOTTING;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; DNA TRANSPOSABLE ELEMENTS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; GENE SILENCING; GERM CELLS; HISTONE DEACETYLASES; OOCYTES; OOGENESIS; OVARY; PACHYTENE STAGE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SIRTUINS;

EID: 84870014655     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.082867     Document Type: Article

References (56)

1. Aravin, A. A., van der Heijden, G. W., Castañeda, J., Vagin, V. V., Hannon, G. J. and Bortvin, A. (2009). Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 5, e1000764.
2. Aström, S. U., Cline, T. W. and Rine, J. (2003). The Drosophila melanogaster sir2+ gene is nonessential and has only minor effects on position-effect variegation. Genetics 163, 931-937.
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. Blom, N., Gammeltoft, S. and Brunak, S. (1999). Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351- 1362.
5. Blower, M. D. and Karpen, G. H. (2001). The role of Drosophila CID in kinetochore formation, cell-cycle progression and heterochromatin interactions. Nat. Cell Biol. 3, 730-739.
6. Blumenstiel, J. P., Fu, R., Theurkauf, W. E. and Hawley, R. S. (2008). Components of the RNAi machinery that mediate long-distance chromosomal associations are dispensable for meiotic and early somatic homolog pairing in Drosophila melanogaster. Genetics 180, 1355-1365.
7. Byers, T. J., Dubreuil, R., Branton, D., Kiehart, D. P. and Goldstein, L. S. (1987). Drosophila spectrin. II. Conserved features of the alpha-subunit are revealed by analysis of cDNA clones and fusion proteins. J. Cell Biol. 105, 2103-2110.
8. Chen, C., Nott, T. J., Jin, J. and Pawson, T. (2011). Deciphering arginine methylation: Tudor tells the tale. Nat. Rev. Mol. Cell Biol. 12, 629-642.
9. Chen, Y., Pane, A. and Schüpbach, T. (2007). Cutoff and aubergine mutations result in retrotransposon upregulation and checkpoint activation in Drosophila. Curr. Biol. 17, 637-642.
10. Clarke, A. S., Tang, T. T.-L., Ooi, D. L.-Y. and Orr-Weaver, T. L. (2005). POLO kinase regulates the Drosophila centromere cohesion protein MEI-S332. Dev. Cell 8, 53-64.
11. Costa, Y., Speed, R. M., Gautier, P., Semple, C. A., Maratou, K., Turner, J. M. and Cooke, H. J. (2006). Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway? Hum. Mol. Genet. 15, 2324-2334.
12. de Cuevas, M. and Spradling, A. C. (1998). Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125, 2781- 2789.
13. Deák, P., Omar, M. M., Saunders, R. D., Pál, M., Komonyi, O., Szidonya, J., Maróy, P., Zhang, Y., Ashburner, M., Benos, P. et al. (1997). P-element insertion alleles of essential genes on the third chromosome of Drosophila melanogaster: correlation of physical and cytogenetic maps in chromosomal region 86E-87F. Genetics 147, 1697-1722.
14. Findley, S. D., Tamanaha, M., Clegg, N. J. and Ruohola-Baker, H. (2003). Maelstrom, a Drosophila spindle-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130, 859-871.
15. Gangaraju, V. K., Yin, H., Weiner, M. M., Wang, J., Huang, X. A. and Lin, H. (2011). Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nat. Genet. 43, 153-158.
16. Ghabrial, A. and Schüpbach, T. (1999). Activation of a meiotic checkpoint regulates translation of Gurken during Drosophila oogenesis. Nat. Cell Biol. 1, 354-357.
17. Huynh, J. R. and St Johnston, D. (2000). The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis to the Drosophila oocyte. Development 127, 2785-2794.
18. Joyce, E. F. and McKim, K. S. (2009). Drosophila PCH2 is required for a pachytene checkpoint that monitors double-strand-break-independent events leading to meiotic crossover formation. Genetics 181, 39-51.
19. Joyce, E. F. and McKim, K. S. (2010). Chromosome axis defects induce a checkpoint-mediated delay and interchromosomal effect on crossing over during Drosophila meiosis. PLoS Genet. 6, e1001059.
20. Joyce, E. F. and McKim, K. S. (2011). Meiotic checkpoints and the interchromosomal effect on crossing over in Drosophila females. Fly (Austin) 5, 134-140.
21. Khurana, J. S. and Theurkauf, W. (2010). piRNAs, transposon silencing, and Drosophila germline development. J. Cell Biol. 191, 905-913.
22. Kinoshita, E., Kinoshita-Kikuta, E., Takiyama, K. and Koike, T. (2006). Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5, 749-757.
23. Kirino, Y., Kim, N., de Planell-Saguer, M., Khandros, E., Chiorean, S., Klein, P. S., Rigoutsos, I., Jongens, T. A. and Mourelatos, Z. (2009). Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat. Cell Biol. 11, 652-658.
24. Kirino, Y., Vourekas, A., Kim, N., de Lima Alves, F., Rappsilber, J., Klein, P. S., Jongens, T. A. and Mourelatos, Z. (2010). Arginine methylation of vasa protein is conserved across phyla. J. Biol. Chem. 285, 8148-8154.
25. 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.
26. Klenov, M. S., Sokolova, O. A., Yakushev, E. Y., Stolyarenko, A. D., Mikhaleva, E. A., Lavrov, S. A. and Gvozdev, V. A. (2011). Separation of stem cell maintenance and transposon silencing functions of Piwi protein. Proc. Natl. Acad. Sci. USA 108, 18760-18765.
27. Lake, C. M. and Hawley, R. S. (2012). The molecular control of meiotic chromosomal behavior: events in early meiotic prophase in Drosophila oocytes. Annu. Rev. Physiol. 74, 425-451.
28. Lim, A. K. and Kai, T. (2007). Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 104, 6714-6719.
29. Llamazares, S., Moreira, A., Tavares, A., Girdham, C., Spruce, B. A., Gonzalez, C., Karess, R. E., Glover, D. M. and Sunkel, C. E. (1991). polo encodes a protein kinase homolog required for mitosis in Drosophila. Genes Dev. 5, 2153-2165.
30. Logarinho, E. and Sunkel, C. E. (1998). The Drosophila POLO kinase localises to multiple compartments of the mitotic apparatus and is required for the phosphorylation of MPM2 reactive epitopes. J. Cell Sci. 111, 2897-2909.
31. MacQueen, A. J. and Hochwagen, A. (2011). Checkpoint mechanisms: the puppet masters of meiotic prophase. Trends Cell Biol. 21, 393-400.
32. Manheim, E. A. and McKim, K. S. (2003). The Synaptonemal complex component C(2)M regulates meiotic crossing over in Drosophila. Curr. Biol. 13, 276-285.
33. Mirouse, V., Formstecher, E. and Couderc, J. L. (2006). Interaction between Polo and BicD proteins links oocyte determination and meiosis control in Drosophila. Development 133, 4005-4013.
34. Moutinho-Santos, T., Sampaio, P., Amorim, I., Costa, M. and Sunkel, C. E. (1999). In vivo localisation of the mitotic POLO kinase shows a highly dynamic association with the mitotic apparatus during early embryogenesis in Drosophila. Biol. Cell 91, 585-596.
35. Nagamori, I., Cruickshank, V. A. and Sassone-Corsi, P. (2011). Regulation of an RNA granule during spermatogenesis: acetylation of MVH in the chromatoid body of germ cells. J. Cell Sci. 124, 4346-4355.
36. Nakajima, H., Toyoshima-Morimoto, F., Taniguchi, E. and Nishida, E. (2003). Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J. Biol. Chem. 278, 25277-25280.
37. Nakamura, A., Sato, K. and Hanyu-Nakamura, K. (2004). Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 6, 69-78.
38. Nishida, K. M., Okada, T. N., Kawamura, T., Mituyama, T., Kawamura, Y., Inagaki, S., Huang, H., Chen, D., Kodama, T., Siomi, H. et al. (2009). Functional involvement of Tudor and dPRMT5 in the piRNA processing pathway in Drosophila germlines. EMBO J. 28, 3820-3831.
39. Patil, V. S. and Kai, T. (2010). Repression of retroelements in Drosophila germline via piRNA pathway by the Tudor domain protein Tejas. Curr. Biol. 20, 724-730.
40. Pek, J. W. and Kai, T. (2011a). DEAD-box RNA helicase Belle/DDX3 and the RNA interference pathway promote mitotic chromosome segregation. Proc. Natl. Acad. Sci. USA 108, 12007-12012.
41. Pek, J. W. and Kai, T. (2011b). A role for vasa in regulating mitotic chromosome condensation in Drosophila. Curr. Biol. 21, 39-44.
42. Pek, J. W., Lim, A. K. and Kai, T. (2009). Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev. Cell 17, 417-424.
43. Pek, J. W., Patil, V. S. and Kai, T. (2012a). piRNA pathway and the potential processing site, the nuage, in the Drosophila germline. Dev. Growth Differ. 54, 66-77.
44. Pek, J. W., Anand, A. and Kai, T. (2012b). Tudor domain proteins in development. Development 139, 2255-2266.
45. Rubin, G. M. and Spradling, A. C. (1982). Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353.
46. Sato, K., Nishida, K. M., Shibuya, A., Siomi, M. C. and Siomi, H. (2011). Maelstrom coordinates microtubule organization during Drosophila oogenesis through interaction with components of the MTOC. Genes Dev. 25, 2361-2373.
47. Senti, K. A. and Brennecke, J. (2010). The piRNA pathway: a fly's perspective on the guardian of the genome. Trends Genet. 26, 499-509.
48. Siomi, M. C., Sato, K., Pezic, D. and Aravin, A. A. (2011). PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12, 246-258.
49. Snee, M. J. and Macdonald, P. M. (2004). Live imaging of nuage and polar granules: evidence against a precursor-product relationship and a novel role for Oskar in stabilization of polar granule components. J. Cell Sci. 117, 2109-2120.
50. Soper, S. F., van der Heijden, G. W., Hardiman, T. C., Goodheart, M., Martin, S. L., de Boer, P. and Bortvin, A. (2008). Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev. Cell 15, 285-297.
51. Takeo, S., Lake, C. M., Morais-de-Sá, E., Sunkel, C. E. and Hawley, R. S. (2011). Synaptonemal complex-dependent centromeric clustering and the initiation of synapsis in Drosophila oocytes. Curr. Biol. 21, 1845-1851.
52. Tanneti, N. S., Landy, K., Joyce, E. F. and McKim, K. S. (2011). A pathway for synapsis initiation during zygotene in Drosophila oocytes. Curr. Biol. 21, 1852- 1857.
53. Tavares, A. A., Glover, D. M. and Sunkel, C. E. (1996). The conserved mitotic kinase polo is regulated by phosphorylation and has preferred microtubuleassociated substrates in Drosophila embryo extracts. EMBO J. 15, 4873-4883.
54. Voronina, E., Seydoux, G., Sassone-Corsi, P. and Nagamori, I. (2011). RNA granules in germ cells. Cold Spring Harb. Perspect. Biol. 3, a002774.
55. Xiang, Y., Takeo, S., Florens, L., Hughes, S. E., Huo, L. J., Gilliland, W. D., Swanson, S. K., Teeter, K., Schwartz, J. W., Washburn, M. P. et al. (2007). The inhibition of polo kinase by matrimony maintains G2 arrest in the meiotic cell cycle. PLoS Biol. 5, e323.
56. Zhang, D., Xiong, H., Shan, J., Xia, X. and Trudeau, V. L. (2008). Functional insight into Maelstrom in the germline piRNA pathway: a unique domain homologous to the DnaQ-H 3'-5' exonuclease, its lineage-specific expansion/loss and evolutionarily active site switch. Biol. Direct 3, 48.