Skip to main content
Log in

Expression pattern of prmt5 in adult fish and embryos of medaka, Oryzias latipes

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Boisvert FM, Côté J, Boulanger MC, Richard S (2003) A proteomic analysis of arginine-methylated protein complexes. Mol Cell Proteomics 2:1319–1330

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Iwamatsu T (1994) Stages of normal development in the medaka Oryzias latipes. Zool Sci 11: 825–839

    Google Scholar 

  • Johnson P, Harris CI, Perry SV (1967) 3-methylhistidine in actin and other muscle proteins. Biochem J 103:P79

    Google Scholar 

  • Klotz AV, Thomas BA, Glazer AN, Blacher RW (1990) Detection of methylated asparagine and glutamine residues in polypeptides. Anal Biochem 186:95–100

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Paik WK, Kim S (1970) ω-N-methylarginine in protein. J Biol Chem 245:88–92

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ullah AH, Ordal GW (1981) Purification and characterization of methyl-accepting chemotaxis protein methyltransferase I in Bacillus subtilis. Biochem J 199:795–805

    PubMed  CAS  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to H. Zhao.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-008-9233-2

Keywords

Navigation