Skip to main content

The nme gene family in zebrafish oogenesis and early development

Naunyn-Schmiedeberg's Archives of Pharmacology volume 384, pages 439–449 (2011)Cite this article

Abstract

After the recent report of the expression of several nme genes in the zebrafish gonads, the present study aimed at further analyzing the expression of nme genes in the ovary with special attention for the nme transcripts that are maternally inherited and could thus participate in the determination of oocyte developmental competence. The expression levels of all groups I and II nme genes were characterized by QPCR in a panel of zebrafish tissues. The nme genes exhibiting an ovarian expression were subsequently monitored throughout oogenesis and early development, and their expression sites characterized using in situ hybridization. Here, we show that nme2b1, nme3, nme4, and nme6 are highly expressed in the ovary and present in the zebrafish oocyte throughout oogenesis. While the four transcripts are maternally inherited, nme3 and nme6 display a typical maternal profile and are detected in the zebrafish early embryo. In contrast to nme3, nme6, abundance exhibits a sharp decrease during early embryogenesis. After zygotic genome activation, we observed an increased expression of nme2b1, nme2b2, nme3, and nme6. The present study provides a comprehensive overview of the expression of nme family members during zebrafish oogenesis and early development. In addition, the maternal origin of two nme transcripts in the early embryo is reported here for the first time in any vertebrate species. Together, our observations suggest an important role of the nme family in oocyte and embryo development in vertebrates.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

Hpf:

Hour post-fertilization

BSA:

Bovine serum albumin

MZT:

Maternal-to-zygotic transition

MBT:

Mid-blastula transition

References

  • Abrams EW, Mullins MC (2009) Early zebrafish development: it's in the maternal genes. Curr Opin Genet Dev 19:396–403

    PubMed  Article  CAS  Google Scholar 

  • Aegerter S, Jalabert B, Bobe J (2005) Large scale real-time PCR analysis of mRNA abundance in rainbow trout eggs in relationship with egg quality and post-ovulatory ageing. Mol Reprod Dev 72:377–385

    PubMed  Article  CAS  Google Scholar 

  • Amrein L, Barraud P, Daniel JY, Perel Y, Landry M (2005) Expression patterns of nm23 genes during mouse organogenesis. Cell Tissue Res 322:365–378

    PubMed  Article  CAS  Google Scholar 

  • Bai JL, Solberg C, Fernandes JMO, Johnston IA (2007) Profiling of maternal and developmental-stage specific mRNA transcripts in Atlantic halibut Hippoglossus hippoglossus. Gene 386:202–210

    PubMed  Article  CAS  Google Scholar 

  • Barraud P, Amrein L, Dobremez E, Dabernat S, Masse K, Larou M, Daniel JY, Landry M (2002) Differential expression of nm23 genes in adult mouse dorsal root ganglia. J Comp Neurol 444:306–323

    PubMed  Article  CAS  Google Scholar 

  • Biggs J, Hersperger E, Steeg PS, Liotta LA, Shearn A (1990) A Drosophila gene that is homologous to a mammalian gene associated with tumor metastasis codes for a nucleoside diphosphate kinase. Cell 63:933–940

    PubMed  Article  CAS  Google Scholar 

  • Bilitou A, Watson J, Gartner A, Ohnuma SI (2009) The NM23 family in development. Mol Cell Biochem 329:17–33

    PubMed  Article  CAS  Google Scholar 

  • Bobe J, Labbe C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548

    PubMed  Article  CAS  Google Scholar 

  • Boissan M, Dabernat S, Peuchant E, Schlattner U, Lascu I, Lacombe ML (2009) The mammalian Nm23/NDPK family: from metastasis control to cilia movement. Mol Cell Biochem 329:51–62

    PubMed  Article  CAS  Google Scholar 

  • Carotenuto P, Marino N, Bello AM, D'Angelo A, Di Porzio U, Lombardi D, Zollo M (2006) PRUNE and NM23-M1 expression in embryonic and adult mouse brain. J Bioenerg Biomembr 38:233–246

    PubMed  Article  CAS  Google Scholar 

  • Crespel A, Rime H, Fraboulet E, Bobe J, Fauvel C (2008) Egg quality in domesticated and wild seabass (Dicentrarchus labrax): a proteomic analysis. Cybium 32(2):205

    Google Scholar 

  • Dabernat S, Larou M, Masse K, Hokfelt T, Mayer G, Daniel JY, Landry M (1999a) Cloning of a second nm23-M1 cDNA: expression in the central nervous system of adult mouse and comparison with nm23-M2 mRNA distribution. Brain Res Mol Brain Res 63:351–365

    PubMed  Article  CAS  Google Scholar 

  • Dabernat S, Larou M, Masse K, Dobremez E, Landry M, Mathieu C, Daniel JY (1999b) Organization and expression of mouse nm23-M1 gene. Comparison with nm23-M2 expression. Gene 236:221–230

    PubMed  Article  CAS  Google Scholar 

  • Desvignes T, Pontarotti P, Bobe J (2010) Nme gene family evolutionary history reveals pre-metazoan origins and high conservation between humans and the sea anemone, Nematostella vectensis. PLoS ONE 5:e15506

    PubMed  Article  Google Scholar 

  • Desvignes T, Pontarotti P, Fauvel C, Bobe J (2009) Nme protein family evolutionary history, a vertebrate perspective. BMC Evol Biol 9:256

    PubMed  Article  Google Scholar 

  • Dosch R, Wagner DS, Mintzer KA, Runke G, Wiemelt AP, Mullins MC (2004) Maternal control of vertebrate development before the midblastula transition: mutants from the zebrafish I. Dev Cell 6:771–780

    PubMed  Article  CAS  Google Scholar 

  • Hippe HJ, Wolf NM, Abu-Taha I, Mehringer R, Just S, Lutz S, Niroomand F, Postel EH, Katus HA, Rottbauer W, Wieland T (2009) The interaction of nucleoside diphosphate kinase B with Gbetagamma dimers controls heterotrimeric G protein function. Proc Natl Acad Sci 106:16269–16274

    PubMed  Article  CAS  Google Scholar 

  • Hwang KC, Ok DW, Hong JC, Kim MO, Kim JH (2003) Cloning, sequencing, and characterization of the murine nm23-M5 gene during mouse spermatogenesis and spermiogenesis. Biochem Biophys Res Commun 306:198–207

    PubMed  Article  CAS  Google Scholar 

  • Kane DA, Kimmel CB (1993) The zebrafish midblastula transition. Development 119:447–456

    PubMed  CAS  Google Scholar 

  • Keyvanshokooh S, Vaziri B (2008) Proteome analysis of Persian sturgeon (Acipenser persicus) ova. Anim Reprod Sci 109:287–297

    PubMed  Article  CAS  Google Scholar 

  • Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310

    PubMed  Article  CAS  Google Scholar 

  • Kimura N, Shimada N, Nomura K, Watanabe K (1990) Isolation and characterization of a cDNA clone encoding rat nucleoside diphosphate kinase. J Biol Chem 265:15744–15749

    PubMed  CAS  Google Scholar 

  • Lakso M, Steeg PS, Westphal H (1992) Embryonic expression of Nm23 during mouse organogenesis. Cell Growth Differ 3:873–879

    PubMed  CAS  Google Scholar 

  • Lubzens E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how eggs are formed. Gen Comp Endocrinol 165:367–389

    PubMed  Article  CAS  Google Scholar 

  • Masse K, Dabernat S, Bourbon PM, Larou M, Amrein L, Barraud P, Perel Y, Camara M, Landry M, Lacombe ML, Daniel JY (2002) Characterization of the nm23-M2, nm23-M3 and nm23-M4 mouse genes: comparison with their human orthologs. Gene 296:87–97

    PubMed  Article  CAS  Google Scholar 

  • Mathavan S, Lee SG, Mak A, Miller LD, Murthy KR, Govindarajan KR, Tong Y, Wu YL, Lam SH, Yang H, Ruan Y, Korzh V, Gong Z, Liu ET, Lufkin T (2005) Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genet 1:260–276

    PubMed  Article  CAS  Google Scholar 

  • Mehus JG, Deloukas P, Lambeth DO (1999) NME6: a new member of the nm23/nucleoside diphosphate kinase gene family located on human chromosome 3p21.3. Hum Genet 104:454–459

    PubMed  Article  CAS  Google Scholar 

  • Miranda-Vizuete A, Tsang K, Yu Y, Jimenez A, Pelto-Huikko M, Flickinger CJ, Sutovsky P, Oko R (2003) Cloning and developmental analysis of murid spermatid-specific thioredoxin-2 (SPTRX-2), a novel sperm fibrous sheath protein and autoantigen. J Biol Chem 278:44874–44885

    PubMed  Article  CAS  Google Scholar 

  • Munier A, Feral C, Milon L, Pinon VPB, Gyapay G, Capeau J, Guellaen G, Lacombe ML (1998) A new human nm23 homologue (nm23-H5) specifically expressed in testis germinal cells. FEBS Lett 434:289–294

    PubMed  Article  CAS  Google Scholar 

  • Murphy M, Harte T, McInerney J, Smith TJ (2000) Molecular cloning of an Atlantic salmon nucleoside diphosphate kinase cDNA and its pattern of expression during embryogenesis. Gene 257:139–148

    PubMed  Article  CAS  Google Scholar 

  • Ouatas T, Selo M, Sadji Z, Hourdry J, Denis H, Mazabraud A (1998) Differential expression of nucleoside diphosphate kinases (NDPK/NM23) during Xenopus early development. Int J Dev Biol 42:43–52

    PubMed  CAS  Google Scholar 

  • Pelegri F (2003) Maternal factors in zebrafish development. Dev Dyn 228:535–554

    PubMed  Article  CAS  Google Scholar 

  • Postel EH, Zou X, Notterman DA, La Perle KM (2009) Double knockout Nme1/Nme2 mouse model suggests a critical role for NDP kinases in erythroid development. Mol Cell Biochem 329:45–50

    PubMed  Article  CAS  Google Scholar 

  • Sadek CM, Damdimopoulos AE, Pelto-Huikko M, Gustafsson JA, Spyrou G, Miranda-Vizuete A (2001) Sptrx-2, a fusion protein composed of one thioredoxin and three tandemly repeated NDP-kinase domains is expressed in human testis germ cells. Genes Cells 6:1077–1090

    PubMed  Article  CAS  Google Scholar 

  • Selman K, Wallace RA, Sarka A, Qi X (1993) Stages of oocyte development in the zebrafish, Brachydanio rerio. J Morphol 218:203–224

    Article  Google Scholar 

  • Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042

    PubMed  Article  CAS  Google Scholar 

  • Timmons L, Shearn A (2000) Role of AWD/nucleoside diphosphate kinase in Drosophila development. J Bioenerg Biomembr 32:293–300

    PubMed  Article  CAS  Google Scholar 

  • Tsuchiya B, Sato Y, Urano T, Baba H, Shiku H, Kameya T (1998) Immunohistochemical and semiquantitative immunoblot analyses of Nm23-H1 and H2 isoforms in normal human tissues. Acta Histochem Cytochem 31:411–418

    Article  CAS  Google Scholar 

  • Wagner DS, Dosch R, Mintzer KA, Wiemelt AP, Mullins MC (2004) Maternal control of development at the midblastula transition and beyond: mutants from the zebrafish II. Dev Cell 6:781–790

    PubMed  Article  CAS  Google Scholar 

  • Westerfield M (2000) The zebrafish book. A guide for the laboratory use of zebrafish (Danio rerio). Univ. of Oregon Press, Eugene

  • Woolworth JA, Nallamothu G, Hsu T (2009) The Drosophila metastasis suppressor gene Nm23 homolog, awd, regulates epithelial integrity during oogenesis. Mol Cell Biol 29:4679–4690

    PubMed  Article  CAS  Google Scholar 

  • Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298

    Article  Google Scholar 

  • Ziv T, Gattegno T, Chapovetsky V, Wolf H, Barnea E, Lubzens E, Admon A (2008) Comparative proteomics of the developing fish (zebrafish and gilthead seabream) oocytes. Comp Biochem Physiol Genom Proteonomics 3:12–35

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank the Singapore Genome Institute for providing bacterial clones, Thaovi Nguyen for technical assistance, INRA-SCRIBE histological platform, and Frederic Borel and Amélie Patinote for zebrafish care. This work was supported by the European Community's Seventh Framework Program (FP7/2007-2013) under grant agreement no. 222719-LIFECYCLE.

Author information

Affiliations

  1. INRA, UR1037 SCRIBE, Campus de Beaulieu, 35042, Rennes, France

    T. Desvignes & J. Bobe

  2. IFREMER, LALR, 34250, Palavas-Les-Flots, France

    T. Desvignes & C. Fauvel

Authors
  1. T. Desvignes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. Fauvel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Bobe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Bobe.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Desvignes, T., Fauvel, C. & Bobe, J. The nme gene family in zebrafish oogenesis and early development. Naunyn-Schmiedeberg's Arch Pharmacol 384, 439–449 (2011). https://doi.org/10.1007/s00210-011-0619-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00210-011-0619-9

Keywords

  • NDPK
  • Nm23
  • Oocyte
  • Maternal
  • Teleost
  • Vertebrate