Arginine methyltransferase Capsuléen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila

Development

Volumn 134, Issue 1, 2007, Pages 137-146

  Anne, Joël ^a,b   Ollo, Roger ^b   Ephrussi, Anne ^c   Mechler, Bernard M ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b Laboratoire de Biologie Moléculaire de la Drosophile   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Capsul en; Drosophila oogenesis; Nuage; Pole plasm; Protein arginine methyltransferase

Indexed keywords

ARGININE; CAPSULEEN; METHYLTRANSFERASE; PROTEIN SM; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN ARGININE METHYLTRANSFERASE; RNA BINDING PROTEIN;

ANIMAL CELL; ARTICLE; CATALYSIS; CELL MATURATION; CELL NUCLEUS; CONTROLLED STUDY; EMBRYO; GERM CELL; IMMUNOCYTOCHEMISTRY; METHYLATION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TARGETING; AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; CHEMISTRY; COMPARATIVE STUDY; CYTOLOGY; DROSOPHILA; ENZYMOLOGY; FEMALE; GENE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; METABOLISM; MOLECULAR GENETICS; OOCYTE; PHYSIOLOGY; PRENATAL DEVELOPMENT; RESTRICTION MAPPING; SEQUENCE HOMOLOGY; SPLICEOSOME; TRANSGENE; TRANSGENIC ANIMAL;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CONSERVED SEQUENCE; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FEMALE; GENES, INSECT; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; METHYLATION; MOLECULAR SEQUENCE DATA; OOCYTES; OOGENESIS; PROTEIN-ARGININE N-METHYLTRANSFERASE; RECOMBINANT FUSION PROTEINS; RESTRICTION MAPPING; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPLICEOSOMES; TRANSGENES;

EID: 33846517786     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02687     Document Type: Article

References (50)

1. Amikura, R., Hanyu, K., Kashikawa, M. and Kobayashi, S. (2001). Tudor protein is essential for the localization of mitochondrial RNAs in polar granules of Drosophila embryos. Mech. Dev 107, 97-104.
2. Anne, J. and Mechler, B. M. (2005). Valois, a component of the nuage and pole plasm, is involved in assembly of these structures and binds to Tudor and the methyltransferase Capsuléen. Development 132, 2167-2177.
3. Arkov, A. L., Wang, J.-Y. S., Ramos, A. and Lehmann, R. (2006). The role of Tudor domains in germline development and polar granule architecture. Development 133, 4053-4062.
4. Bardsley, A., McDonald, K. and Boswell, R. E. (1993). Distribution of tudor protein in the Drosophila embryo suggests separation of functions based on site of localization. Development 119, 207-219.
5. Boisvert, F.-M., Côté, J., Boulanger, M.-C., Cléroux, P., Bachand, F., Autexier, C. and Richard, S. (2002). Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing. J. Cell Biol. 159, 957-969.
6. Boisvert, F.-M., Côté, J., Boulanger, M.-C. and Richard, S. (2003). A proteomic analysis of arginine-methylated protein complexes. Mol. Cell. Proteomics 2, 1319-1330.
7. Brahms, H., Meheus, L., de Brabandere, V., Fischer, U. and Luhrmann, R. (2001). Symmetrical dimethylation of arginine residues in spliceosomal Sm protein B/B′ and the Sm-like protein LSm4, and their interaction with the SMN protein. RNA 11, 1531-1542.
8. Branscombe, T. L., Frankel, A., Lee, J.-H., Cook, J. R., Yang, Z.-h., Pestka, S. and Clarke, S. (2001). PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J. Biol. Chem. 276, 32971-32976.
9. Breitwieser, W., Markussen, F.-H., Horstmann, H. and Ephrussi, A. (1996). Oskar protein interaction with Vasa represents an essential step in polar granule assembly Genes Dev 10, 2179-2188.
10. Cook, J. R., Lee, J. H., Yang, Z. H., Krause, C. D., Herth, N., Hoffmann, R. and Pestka, S. (2006). FBXO11/PRMT9, a new protein arginine methyltransferase, symmetrically dimethylates arginine residues. Biochem. Biophys. Res. Commun. 342, 472-481.
11. Côté, J. and Richard, S. (2005). Tudor domains bind symmetrical dimethylated arginines. J. Biol. Chem. 280, 28476-28483.
12. Eddy, E. M. (1975). Germ plasm and the differentiation of the germ cell line. Int Rev Cytol. 43, 229-280.
13. Ephrussi, A. and Lehmann, R. (1992). Induction of germ cell formation by oskar. Nature 358, 387-392.
14. Ephrussi, A., Dickinson, L. K. and Lehmann, R. (1991). oskar organizes the germ plasm and directs localization of the posterior determinant nanos. Cell 66, 37-50.
15. Findley, S. D., Tamanaha, M., Clegg, N. J. and Ruohola-Baker, H. (2003). Maelstrom, a Drosophila spindie-class gene, encodes a protein that colocalizes with Vasa and RDE1/AGO1 homolog, Aubergine, in nuage. Development 130, 859-871.
16. Friesen, W. J., Paushkin, S., Wyce, A., Massenet, S., Pesiridis, G. S., Van Duyne, G., Rappsilber, J., Mann, M. and Dreyfuss, G. (2001a). The methylosome, a 20S complex containing JBP1 and plCln, produces dimethylarginine-modified Sm proteins. Mol. Cell. Biol. 21, 8289-8300.
17. Friesen, W. J., Massenet, S., Paushkin, S., Wyce, A. and Dreyfuss, G. (2001b). SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets. Mol. Cell 7, 1111-1117.
18. Friesen, W. J., Wyce, A., Paushkin, S., Abel, L., Rappsilber, J., Mann, M. and Dreyfuss, G. (2002). A novel WD repeat protein component of the methylosome binds Sm proteins. J. Biol. Chem. 277, 8243-8247.
19. Golumbeski, G. S., Bardsley, A., Tax, F. and Boswell, R. E. (1991). tudor, a posterior-group gene of Drosophila melanograster, encodes a novel protein and an mRNA localized during mid-oogenesis. Genes Dev. 5, 2060-2070.
20. Gonsalvez, G. B., Rajendra, T. K., Tian, L. and Matera, A. G. (2006). The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance. Curr. Biol. 16, 1077-1089.
21. Hay, B., Ackerman, L., Barbel, S., Jan, L. Y. and Jan, Y. N. (1988). Identification of a component of Drosophila polar granules. Development 103, 625-640.
22. Hay, B., Jan, L. Y. and Jan, Y. N. (1990). Localization of vasa, a component of Drosophila polar granules, in maternal-effect mutants that alter embryonic anteroposterior polarity. Development 109, 425-433.
23. Illmensee, K. and Mahowald, A. P. (1974). Transplantation of posterior polar plasm in Drosophila. Induction of germ cells at the anterior pole of the egg. Proc. Natl. Acad. Sci. USA 71, 1016-1020.
24. Jongens, T A., Hay, B., Jan, L. Y. and Jan, Y. N. (1992). The germ cell-less gene product: a posteriorly localized component necessary for germ cell development in Drosophila. Cell 70, 569-584.
25. Khusial, P. R., Vaidya, K. and Zieve, G. W. (2005). The symmetrical dimethylarginine post-translational modification of the SmD3 protein is not required for snRNP assembly and nuclear transport. Biochem. Biophys. Res. Common. 337, 1119-1124.
26. Kim-Ha, J., Smith, J. L. and Macdonald, P. M. (1991). oskar mRINA is localized to the posterior pole of the Drosophila oocyte. Cell 66, 23-35.
27. Lasko, P. and Ashburner, M. (1990). Posterior localization of vasa protein correlates with, but is not sufficient for, pole cell development. Genes Dev. 4, 905-921.
28. Lee, J. H., Cook, J. R., Pollack, B. P., Kinzy, T. G., Norris, D. and Pestka, S. (2000). Hsl7p, the yeast homologue of human JBP1, is a protein methyltransferase. Biochem. Biophys. Res. Commun. 274, 105-11.
29. Lee, J. H., Cook, J. R., Yang, Z. H., Mirochnitchenko, O., Gunderson, S. I., Felix, A. M., Herth, N., Hoffmann, R. and Pestka, S. (2005). PRMT7, a new protein arginine methyltransferase that synthesizes symmetric dimethylarginine. J. Biol. Chem. 280, 3656-3664.
30. Liang, L., Diehl-Jones, W. and Lasko, P. (1994). Localization of vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 120, 1201-1211.
31. Ma, X.-J. (2000). Cell-cycle regulatory proteins Hsl7p/Skb1p belong to the protein methyltransferase superfamily. Trends Biochem. Sci. 25, 11-12.
32. Mahowald, A. P. (1968). Polar granules of Drosophila. II. Ultrastructural changes during early embryogenesis. J. Exp. Zool. 167, 237-262.
33. Mahowald, A. P. (1971). Polar granules of Drosophila. III. The continuity of polar granules during the life cycle of Drosophila. J. Exp. Zool. 176, 329-343.
34. Makarova, O., Kamberov, E. and Margolis, B. (2000). Generation of deletion and point mutations with one primer in, a single cloning step. BioTechniques 29 970-972.
35. Meister, G. and Fischer, U. (2002). Assisted RNP assembly: SMN aid PRMT5 complexes cooperate in the formation of spliceosomal UsnRNPs. EMBO J. 21, 5853-5863.
36. Meister, G., Eggert, C., Bühler, D., Brahms, H., Kambach, C. and Fischer U. (2001). Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor plCln. Curr. Biol. 11, 1990-1994.
37. Paterson, T., Beggs, J. D., Finnegan, D. J. and Lührmann, R. (1991). Polypeptide components of Drosophila small nuclear ribonucleoprotein particles. Nucleic Acids Res. 19, 5877-5882.
38. Pollack, B. R, Kotenko, S. V., He, W., Izotova, L. S., Barnoski, E. L. and Pestka, S. (1999). The human homologue of the yeast proteins Skb1 and Hls7p interacts with Jak kinases and contains protein methyltransferase activity. J. Biol. Chem. 274, 31531-31542.
39. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M., Mann, M. and Séraphin, B. (1999). A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol, 17, 1030-1032.
40. Sano, H., Nakamura, A. and Kobayashi, S. (2002). Identification of a transcriptional regulatory region for germline-specific expression of vasa gene in Drosophila melanogaster. Mech. Dev 112, 129-139.
41. Saxton, W. M., Hicks, J., Goldstein, L. S. B. and Raff, E. C. (199). Kinesin heavy chain is essential for viability and neuromuscular functions in Drosophila, but mutants show no defects in mitosis. Cell 64, 1093-1102.
42. Schenkel, H., Hanke, S., De Lorenzo, C., Schmitt, R. and Mechler, B. M. (2002). P elements inserted in the vicinity of or within the Drosophila snRNP SmD3 gene nested in the first intron of the Ornithine Decarboxylase Antizyme gene affect only the expression of SmD3. Genetics 161, 763-772.
43. Schüpbach, T. and Wieschaus, E. (1986). Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Roux's Arch. Dev. Biol. 195, 302-317.
44. Selenko, P., Sprangers, R., Stier, G., Bühler, D., Fischer, U. and Sattler, M. (2001). SMN Tudor domain structure and its interaction with the Sm proteins. Nat. Struct. Biol. 8, 27-31.
45. Smith, J. L., Wilson, J. E. and Macdonald, R M. (1992). Overexpression of oskar directs ectopic activation of nanos and presumptive pole cell formation in Drosophila embryos. Cell 70, 849-859.
46. 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.
47. Spradling, A. C. (1993). Developmental genetics of oogenesis. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 1-70. Cold Spring Harbor, NY. Cold Spring Harbor Laborator, Press.
48. Wang, C. and Lehmann, R. (1991). nanos is the localized posterior determinant in Drosophila. Cell 66, 637-647.
49. Wilsch-Bräuninger, M., Schwarz, H. and Nüsslein-Volhard, C. 1997). A sponge-like structure involved in the association and transport of maternal products during Drosophila oogenesis. J. Cell Biol. 139, 817-829.
50. Wylie, C. (1999). Germ cells. Cell 96, 165-174.