Abstract
DNA methylation is an important biochemical epigenetic determinant of gene expression in cells and therefore actively involved in gene regulation, chromosomal conformation, and protein activity. Protein arginine methyltransferases (PRMTs) play a major role in the methylation of proteins that have an arginine residue, catalyzing both the asymetric dimethylation of arginine (aDMA) and symetric dimethylation of arginine (sDMA). PRMT5, a type II PRMT which catalyzes sDMA, has been shown to have a pivotal role in pole plasm assembly and germ cell development in Drosophila and also to be an associate factor of Blimp1 for germ cell development in mouse. Here, we report a homolog of prmt5 identified in medaka, Oryzias latipes, which was detected in the brain, gill, muscle, heart, liver, spleen, intestine, testis and ovary of adult fish by reverse transcriptase-PCR. The expression of prmt5 in the gonads is restricted to oocytes of the ovary, spermatogonia, and spermatocytes of testis. The prmt5 transcripts were detected as early as the one-cell stage and in all the tissues of embryos during embryogenesis. In summary, prmt5 is a maternal determinant factor of embryogenesis of medaka, possibly playing an important role in oogenesis and spermatogenesis in adult medaka.
Similar content being viewed by others
Abbreviations
- aDMA:
-
asymmetric dimethylation of arginine
- CDD:
-
conserved domain database
- dpf:
-
days post-fertilization
- PGC:
-
primordial germ cell
- PRMT:
-
protein arginine methyltransferase
- sDMA:
-
symmetric dimethylation of arginine
- STAT:
-
signal transducer and activator of transcription
References
Abramovich C, Yakobson B, Chebath J, Revel M (1997) A protein arginine methyltransferase binds to the intracytoplasmic domain of the IFNAR1 chain in the type I interferon receptor. EMBO J 16: 260–266
Altschuler L, Wook JO, Gurari D, Chebath J, Revel M (1999) Involvement of receptor-bound protein methyltransferase PRMT1 in antiviral and antiproliferative effects of type I interferons. J Interferon Cytokine Res 19:189–195
Amente S, Napolitano G, Licciardo P, Monti M, Pucci P, Lania L et al (2005) Identification of proteins interacting with the RNAPII FCP1 phosphatase: FCP1 forms a complex with arginine methyltransferase PRMT5 and it is a substrate for PRMT5-mediated methylation. FEBS Lett 579: 683–689
Ancelin K, Lange UC, Hajkova P, Schneider R, Bannister AJ, Kouzarides T, Surani MA (2006) Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8: 623–630
Anne J, Ollo R, Ephrussi A, Mechler BM (2007) Arginine methyltransferase Capsuléen is essential for methylation of spliceosomal Sm proteins and germ cell formation in Drosophila. Development 134:137–146
Boisvert FM, Côté J, Boulanger MC, Richard S (2003) A proteomic analysis of arginine-methylated protein complexes. Mol Cell Proteomics 2:1319–1330
Dacwag CS, Ohkawa Y, Pal S, Sif S, Imbalzano AN (2007) The protein arginine methyltransferase Prmt5 is required for myogenesis because it facilitates ATP-dependent chromatin remodeling. Mol Cell Biol 27:384–394
Eddy EM (2006) Germ plasm and the molecular determinants of germ cell fate. Encycl Life Sci. doi:10.1038/npg.els.0005960
Friesen WJ, Massenet S, Paushkin S, Wyce A, Dreyfuss G (2001) SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets. Mol Cell 7:1111–1117
Gilbreth M, Yang P, Bartholomeusz G, Pimental RA, Kansra S, Gadiraju R et al (1998) Negative regulation of mitosis in fission yeast by the shk1 interacting protein skb1 and its human homolog, Skb1Hs. Proc Natl Acad Sci USA 95:14781–14786
Gonsalvez GB, Rajendra TK, Tian L, Matera AG (2006) The Sm-protein methyltransferase, Dart5, is essential for germ-cell specification and maintenance. Curr Biol 16:1077–1089
Herpin A, Rohr S, Riedel D, Kluever N, Raz E, Schartl M (2007) Specification of primordial germ cells in medaka (Oryzias latipes). BMC Dev Biol 7:3
Hung C-M, Li C (2004) Identification and phylogenetic analyses of the protein arginine methyltransferase gene family in fish and ascidians. Gene 340:179–187
Iwamatsu T (1994) Stages of normal development in the medaka Oryzias latipes. Zool Sci 11: 825–839
Johnson P, Harris CI, Perry SV (1967) 3-methylhistidine in actin and other muscle proteins. Biochem J 103:P79
Klotz AV, Thomas BA, Glazer AN, Blacher RW (1990) Detection of methylated asparagine and glutamine residues in polypeptides. Anal Biochem 186:95–100
Krause CD, Yang Z-H, Kim Y-S, Lee J-H, Cook JR, Pestka S (2007) Protein arginine methyltransferases: evolution and assessment of their pharmacological and therapeutic potential. Pharmacol Ther 113:50–87
Marchler-Bauer A, Anderson JB, Derbyshire MK, DeWeese-Scott C, Gonzales NR, Gwadz M et al. (2007) CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res 35:D237–D240
McGraw S, Vigneault C, Sirard M-A (2007) Temporal expression of factors involved in chromatin remodeling and in gene regulation during early bovine in vitro embryo development. Reproduction 133:597–608
Mowen KA, Tang J, Zhu W, Schurter BT, Shuai K, Herschman HR et al. (2001) Arginine methylation of STAT1 modulates IFNα/β-induced transcription. Cell 104:731–741
Ohinata Y, Payer B, O’Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA (2005) Blimp1 is a critical determinant of the germ cell lineage in mice. Nature 436:207–213
Paik WK, Kim S (1970) ω-N-methylarginine in protein. J Biol Chem 245:88–92
Pal S, Vishwanath SN, Erdjument-Bromage H, Tempst P, Sif S (2004) Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol Cell Biol 24:9630–9645
Pawlak MR, Scherer CA, Chen J, Roshon MJ, Ruley HE (2000) Arginine N-methyltransferase 1 is required for early postimplantation mouse development, but cells deficient in the enzyme are viable. Mol Cell Biol 20:4859–4869
Richard S, Morel M, Cléroux P (2005) Arginine methylation regulates IL-2 gene expression: a role for protein arginine methyltransferase 5 (PRMT5). Biochem J 388:379–386
Shinomiya A, Tanaka M, Kobayashi T, Nagahama Y, Hamaguchi S (2000) The vasa-like gene, olvas, identifies the migration path of primordial germ cells during embryonic body formation stage in the medaka, Oryzias latipes. Dev Growth Differ 42:317–326
Sprangers R, Groves MR, Sinning I, Sattler M (2003) High-resolution X-ray and NMR structures of the SMN Tudor domain: conformational variation in the binding site for symmetrically dimethylated arginine residues. J Mol Biol 327:507–520
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Ullah AH, Ordal GW (1981) Purification and characterization of methyl-accepting chemotaxis protein methyltransferase I in Bacillus subtilis. Biochem J 199:795–805
Acknowledgements
This work was supported by grants from the Scientific Research Foundation for the Returned Overseas Chinese Scholars, State Education Ministry of China (to HZ). The authors thank Dr. Li for suggestions on preparation of this paper.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chen, W., Cao, M., Yang, Y. et al. Expression pattern of prmt5 in adult fish and embryos of medaka, Oryzias latipes . Fish Physiol Biochem 35, 325–332 (2009). https://doi.org/10.1007/s10695-008-9233-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-008-9233-2