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.
Similar content being viewed by others
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
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
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
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
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
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
Bilitou A, Watson J, Gartner A, Ohnuma SI (2009) The NM23 family in development. Mol Cell Biochem 329:17–33
Bobe J, Labbe C (2010) Egg and sperm quality in fish. Gen Comp Endocrinol 165:535–548
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
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
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
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
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
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
Desvignes T, Pontarotti P, Fauvel C, Bobe J (2009) Nme protein family evolutionary history, a vertebrate perspective. BMC Evol Biol 9:256
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
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
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
Kane DA, Kimmel CB (1993) The zebrafish midblastula transition. Development 119:447–456
Keyvanshokooh S, Vaziri B (2008) Proteome analysis of Persian sturgeon (Acipenser persicus) ova. Anim Reprod Sci 109:287–297
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310
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
Lakso M, Steeg PS, Westphal H (1992) Embryonic expression of Nm23 during mouse organogenesis. Cell Growth Differ 3:873–879
Lubzens E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how eggs are formed. Gen Comp Endocrinol 165:367–389
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
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
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
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
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
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
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
Pelegri F (2003) Maternal factors in zebrafish development. Dev Dyn 228:535–554
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
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
Selman K, Wallace RA, Sarka A, Qi X (1993) Stages of oocyte development in the zebrafish, Brachydanio rerio. J Morphol 218:203–224
Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042
Timmons L, Shearn A (2000) Role of AWD/nucleoside diphosphate kinase in Drosophila development. J Bioenerg Biomembr 32:293–300
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
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
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
Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298
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
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
Authors and Affiliations
Corresponding author
Rights 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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00210-011-0619-9