Skip to main content

Advertisement

Log in

Re-localization of nuclear DNA helicase II during the growth period of bovine oocytes

  • Original paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Nuclear DNA helicase II (NDH II) is the bovine homolog of human RNA helicase A. The aim of this study was to compare NDH II localization between somatic cells (bovine embryonal fibroblasts) and female germ cells (oocytes), with the main focus on the dynamic changes in the redistribution of NDH II during the growth phase of the bovine oocytes. The fine granular staining of NDH II was spread in the whole nucleoplasm of fibroblasts, excluding the reticulated nucleoli. In contrast, the large reticulated nucleoli of the growing oocytes isolated from early antral follicles exhibited strong positivity for NDH II together with the immunostaining signals of upstream binding factor (UBF) and RNA polymerase I subunit (PAF53), documenting the high synthetic activity of these nucleoli. At the time of termination of oocyte growth, NDH II was preferentially located at the nucleolar periphery together with proteins of fibrillar centres. In fully grown oocytes, NDH II was still present in the thin periphery shell around the compact nucleolar core. The semiquantitative RT-PCR revealed that the average signal of NDH II mRNA in fully grown oocytes was only at 40% level in comparison with growing oocytes. Western blot analysis further confirmed that a 140 kD NDH II protein was abundant in growing oocytes, while the signal was substantially weaker in fully grown oocytes. The significant decrease in NDH II gene expression and in NDH II mRNA translation correlates with a termination of the oocyte growth. Altogether, the results demonstrate that NDH II expression parallels the activity of ribosomal RNA biosynthesis in the bovine growing oocytes.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anderson SF, Schlegel BP, Nakajima T, Wolpin ES, Parvin JD (1998) BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat Genet 19:254–256

    Article  PubMed  CAS  Google Scholar 

  • Aratani S, Fujii R, Fujita H, Fukamizu A, Nakajima T (2003) Aromatic residues are required for RNA helicase A mediated transactivation. Int J Mol Med 12:175–180

    PubMed  CAS  Google Scholar 

  • Baran V, Pavlok A, Bjerregaard B, Wrenzycki C, Hermann D, Philimonenko VV, Lapathitis G, Hozak P, Niemann H, Motlik J (2004) Immunolocalization of upstream binding factor (UBF) and pocket protein p130 during final stages of bovine oocyte growth. Biol Reprod 70:877–886

    Article  PubMed  CAS  Google Scholar 

  • Bell P, Mais C, McStay B, Scheer U (1997) Association of the nucleolar transcription factor UBF with the transcriptionally inactive rRNA genes of pronuclei and early Xenopus embryos. J Cell Sci 110:2053–2063

    PubMed  CAS  Google Scholar 

  • Bjerregaard B, Wrenzycki C, Philimonenko VV, Hozak P, Laurincik J, Niemann H, Motlik J, Maddox-Hyttel P (2004) Regulation of ribosomal RNA synthesis during the final phases of porcine oocyte growth. Biol Reprod 70:925–935

    Article  PubMed  CAS  Google Scholar 

  • Crozet N, Motlik J, Szolosi D (1981) Nucleolar fine structure and RNA synthesis in porcine oocytes during the early stage of antrum formation. Biol Cell 41:35–42

    CAS  Google Scholar 

  • Crozet N, Kanka J, Motlik J, Fulka J (1986) Nucleolar fine structure and RNA synthesis in bovine oocytes from antral follicles. Gamete Res 14:65–73

    Article  CAS  Google Scholar 

  • De Smedt V, Crozet N, Gall L (1994) Morphological and functional changes accompanying the acquisition of meiotic competence in ovarian goat oocyte. J Exp Zool 269:128–139

    Article  PubMed  Google Scholar 

  • Duguet M (1997) When helicase and topoisomerase meet! J Cell Sci 110:1345–1350

    PubMed  CAS  Google Scholar 

  • Dumont JN (1986) Oogenesis in Xenopus laevis (daudin) I stages of oocyte development in laboratory maintained animals. J Morphol 136:153–180

    Article  Google Scholar 

  • Fair T, Hyttel P (1997) Oocyte growth in cattle—ultrastructure, transcription and development competence. In: Motta (eds) Microscopy of reproduction and development: a dynamic approach. pp 109–118

  • Fair T, Hyttel P, Greve T, Bolard M (1996) Nucleus structure and transcriptional activity in relation to oocyte diameter in cattle. Mol Reprod Dev 43:503–512

    Article  PubMed  CAS  Google Scholar 

  • Fair T, Hulshof SCJ, Hyttel P, Greve T, Boland M (1997) Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Mol reprod Dev 46:208–215

    Article  PubMed  CAS  Google Scholar 

  • Fair T, Hyttel P, Lonergan P, Boland MP (2001) Immunolocalization of nuclear proteins during bovine oocyte growth, meiotic maturation, and fertilization. Biol Reprod 64:1516–1525

    Article  PubMed  CAS  Google Scholar 

  • Fuchsova B, Hozak P (2002) The localization of nuclear DNA helicase II in different nuclear compartments is linked to transcription. Exp Cell Res 279:260–270

    Article  PubMed  CAS  Google Scholar 

  • Fuchsova B, Novak P, Kafkova P, Hozak P (2002) Nuclear DNA helicase II is recruited to IFN-α-activated transcription sites at PML nuclear bodies. J Cell Biol 158:463–473

    Article  PubMed  CAS  Google Scholar 

  • Gorbalenya AE, Koonin EV, Donchenko AP, Blinov VM (1989) Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acid Res 17:4713–4730

    Article  PubMed  CAS  Google Scholar 

  • Grummt I (1999) Regulation of mammalian ribosomal gene transcription by RNA polymerase I. Prog Nucleic Acid Res Mol Biol 10:189–154

    Google Scholar 

  • Gururajan R, Mathews L, Longo FJ, Weeks DL (1994) An3 mRNA encodes an RNA helicase that colocalizes with nucleoli in Xenopus oocytes in a stage-specific manner. Proc Natl Acad Sci USA 91:2056–2260

    Article  PubMed  CAS  Google Scholar 

  • Hyttel P, Viuff D, Fair T, Laurincik J, Thomsen PD, Callesen H, Vos P, Hendrixen PJM, Dieleman SJ, Schelander K, Besenfelder U, Greve T (2001) Ribosomal RNA gene expression and chromosome aberration in bovine oocyte and preimplantation embryo. Reproduction 122:21–30

    Article  PubMed  CAS  Google Scholar 

  • Kafatos FC, Efstratiadis A, Forget BG, Weissman SM (1997) Molecular evolution of human and rabbit beta-globin mRNAs. Proc Natl Acad Sci USA 74:5618–5622

    Article  Google Scholar 

  • Kernan MJ, Kuroda MI, Kreber R, Baker BS, Ganetzky B (1991) napts, a mutation affecting sodium channel activity in Drosophila, is an allele of mle, a regulator of X chromosome transcription. Cell 66:949–959

    Article  PubMed  CAS  Google Scholar 

  • Kitagawa H, Yanagisawa J, Fuse H, Ogawa S, Yogiashi Y, Okuno A, Nagasawa H (2002) Ligand-selective potentiation of rat mineralcorticoid receptor activation function 1 by a CBP-containing histone acetyltransferase complex. Mol Cell Biol 22:3698–3706

    Article  PubMed  CAS  Google Scholar 

  • Kuroda MI, Kernan MJ, Kreber R, Ganetzky B, Baker BS (1991) The maleless protein associates with the X chromosome to regulate dosage compensation in Drosophila. Cell 66:935–947

    Article  PubMed  CAS  Google Scholar 

  • Lee CG, Hurwitz J (1992) A new RNA helicase isolated from HeLa cells that catalytical translocates in the 3` to 5` direction. J Biol Chem 267:4398–4407

    PubMed  CAS  Google Scholar 

  • Lee CG, Hurwitz J (1993) Human RNA helicase A is homologous to the maleless protein Drosophila. J Biol Chem 268:16822–16830

    PubMed  CAS  Google Scholar 

  • Lee CG, Eki T, Okumura K, da Costa Soares V, Hurwitz J (1998) Molecular analysis of the cDNA and genomic DNA encoding mouse RNA helicase A. Genomics 47:365–371

    Article  PubMed  CAS  Google Scholar 

  • Longo FJ, Mathews L, Gururajan R, Chen J, Weeks DL (1996) Changes in nuclear localization of An3, a RNA helicase, during oogenesis and embryogenesis in Xenopus laevis. Mol Reprod Dev 45:491–502

    Article  PubMed  CAS  Google Scholar 

  • Miyara F, Migne C, Hassan-Dumont M, LeMeur A, Cohen-Bacrie P, Aubriot FC, Glissant A, Nathan C, Douard S, Stanovici A, Debey P (2003) Chromatin configuration and transcriptional control in human and mouse oocytes. Mol Reprod Dev 64:458–470

    Article  PubMed  CAS  Google Scholar 

  • Myohanen S, Baylin SB (2001) Sequence-specific DNA binding activity of RNA helicase A to the p16Ink4a promoter. J Biol Chem 276:1634–1642

    Article  PubMed  CAS  Google Scholar 

  • Ochs RL, Lischwe MA, Sponn WM, Busch H (1985) Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell 54:123–134

    PubMed  CAS  Google Scholar 

  • Pavlok A, Lucas-Hahn A, Niemann H (2000) Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol Reprod Dev 31:63–69

    Article  Google Scholar 

  • Pellizzoni L, Charroux B, Rappsilber J, Mann M, Dreyfuss G (2001) A functional interaction between the survival motor neuron complex and RNA polymerase II. J Cell Biol 152:75–85

    Article  PubMed  CAS  Google Scholar 

  • Seither P, Zatsepina O, Hoffmann M, Grummt I (1997) Constitutive and strong association of PAF53 with RNA polymerase I. Chromosoma 106:216–225

    Article  PubMed  CAS  Google Scholar 

  • Roussel P, Andrate C, Gerand G, Hernandez-Verdun D (1993) Localization of the RNA polymerase I transcription factor hUBF during the cell cycle. J Cell Sci 104:327–337

    PubMed  CAS  Google Scholar 

  • Scheer U, Weisenberger D (1994) The nucleolus. Curr Opin Cell Biol 6:354–359

    Article  PubMed  CAS  Google Scholar 

  • Scheer U, Hock R (1999) Structure and function of the nucleolus. Curr Opin Cell Biol 11:385–390

    Article  PubMed  CAS  Google Scholar 

  • Tang H, Gaietta GM, Fischer WH, Ellisman MH, Wong-Staal F (1997) A cellular cofactor for the constitutive transport element of type D retrovirus. Science 276:1412–1415

    Article  PubMed  CAS  Google Scholar 

  • Traut W, Endl E, Scholzen T, Gerdes J, Wiking H (2002) The temporal and spatial distribution of the proliferation associated Ki-67 protein during female and male meiosis. Chromosoma 111:156–164

    Article  PubMed  CAS  Google Scholar 

  • Voit R, Grummt I (2001) Phosphorylation of UBF at serine 388 is required for interaction with RNA. Proc Natl Acad Sci USA 98:13631–13636

    Article  PubMed  CAS  Google Scholar 

  • Zatsepina O, Voit R, Grummt I, Spring H, Semenov MV, Trendelenburg MF (1993) The RNA polymerase I-specific transcription initiation factor UBF is associated with transcriptionally active and inactive ribosomal genes. Chromosoma 102:599–611

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Grosse R (1991) Purification and characterization of two DNA helicases from calf thymus nuclei. J Biol Chem 266:20483–20490

    Google Scholar 

  • Zhang S, Grosse R (1994) Nuclear DNA helicase II unwinds both DNA and RNA. Biochemistry 33:3906–3912

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Grosse F (2004) Multiple functions of nuclear DNA helicase II (RNA helicase A) in nucleic acid metabolism. Acta Biochem Biophys Sinica 36:177–183

    Article  CAS  Google Scholar 

  • Zhang S, Maacke H, Grosse F (1995) Molecular cloning of the gene encoding nuclear DNA helicase II A bovine homologue of human RNA helicase A and Drosophila MLE protein. J Biol Chem 270:16422–16427

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Herrmann C, Grosse F (1999a) Pre-mRNA and mRNA binding of human nuclear DNA helicase II (RNA helicase A). J Cell Sci 112:1055–1064

    PubMed  CAS  Google Scholar 

  • Zhang S, Herrmann C, Grosse F (1999b) Nucleolar localization of murine nuclear DNA helicase II (RNA helicase A). J Cell Sci 112:2693–2703

    PubMed  CAS  Google Scholar 

  • Zhang S, Kohler C, Hemmerich P, Grosse F (2004) Nuclear DNA helicase II (RNA helicase A) binds to an F-actin containing shell that surrounds the nucleolus. Exp Cell Res 293:248–258

    Article  PubMed  CAS  Google Scholar 

  • Zhou K, Choe KT, Zaidi Z, Wang Q, Mathews MB, Lee CG (2003) RNA helicase A interacts with dsDNA and topoisomerase II alfa. Nucleic Acids Res 31:2253–2260

    Article  PubMed  CAS  Google Scholar 

  • Zirwes RF, Eilbracht J, Kneissel S, Schimdt-Zachmann MS (2000) A novel helicase-type protein in the nucleolus: NOH61. Mol Biol Cell 11:1153–1167

    PubMed  CAS  Google Scholar 

  • Voit R, Grummt I (2001) Phosphorylation of UBF at serin 388 is required for interaction with RNA. Proc Natl Acad Sci USA 98:13631–13636

    Article  PubMed  CAS  Google Scholar 

  • Wilson R, Ainscough R, Anderson K, Bayes C, Berks M, Bonfield J, Burton G, Connell M, Copsey T, Cooper G (1994) 2.2 Mb of contiguous nucleotide sequence from chromosome III of C.elegans. Nature 368:32–38

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grant 523/03/0857 of Grant Agency of the Czech Republic and Slovak Academy of Sciences grant VEGA 2/3065/23

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jan Motlík.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baran, V., Kovářová, H., Klíma, J. et al. Re-localization of nuclear DNA helicase II during the growth period of bovine oocytes. Histochem Cell Biol 125, 155–164 (2006). https://doi.org/10.1007/s00418-005-0075-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-005-0075-z

Key words

Navigation