Skip to main content
Log in

Expression of the avian gene cNOC2 encoding nucleolar complex associated protein 2 during embryonic development

  • Original Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Genetic information that directs a cell during different phases of embryogenesis is locked up in the genome. Therein is contained the road map for growth, proliferation, differentiation and morphogenesis. The cellular transportation machinery plays a major role to ensure that all the components for transcription and translation are available at the right place at the right time. Nucleolar complex associated protein2 (NOC2) has a highly conserved UPF0120 domain, and is an element involved in ribosome transportation from the nucleoplasm to the cytoplasm. However, its gene expression pattern is still unknown. We chose the developing chick embryo to investigate the possible involvement of avian NOC2 (cNOC2) in developmental processes, particularly neurogenesis and myogenesis. For this purpose, we constructed a fragment of chicken cNOC2, which contains the UPF0120 domain coding sequence, into pDrive vector, and performed in situ hybridization on chicken embryos of different stages with this gene probe. A dynamic expression pattern of cNOC2 transcripts can be seen beginning as early as from stage HH7 until stage HH32. Using in situ hybridization we could detect that cNOC2 transcripts were expressed ubiquitously, but prominent expression could be found in the neural tissue, the somites and in the developing limbs. Comparison of cNOC2 gene expression with the proliferation marker gene cPCNA, muscle specific marker genes cMyf5 and cMyoD in single or double in situ hybridisation show that cNOC2 is expressed in the myotome, similar to cMyf5 and cMyoD, but not like cPCNA, which is hardly detectable in the myotome. Our results suggest that cNOC2 is involved in the development of neural tissue, somites and limbs.

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

Similar content being viewed by others

References

  • Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N (2004) Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci USA 101:12792–12797

    Article  PubMed  CAS  Google Scholar 

  • Brent AE, Schweitzer R, Tabin CJ (2003) A somitic compartment of tendon progenitors. Cell 113(2):235–248

    Article  PubMed  CAS  Google Scholar 

  • Caldwell RB, Kierzek AM, Arakawa H, Bezzubov Y, Zaim J, Fiedler P, Kutter S, Blagodatski A, Kostovska D, Koter M, Plachy J, Carninci P, Hayashizaki Y, Buerstedde JM (2005) Full-length cDNAs from chicken bursal lymphocytes to facilitate gene function analysis. Genome Biol 6:R6

    Article  PubMed  Google Scholar 

  • Chae JH, Stein GH, Lee JE (2004) NeuroD: the predicted and the surprising. Mol Cells 18:271–288

    PubMed  CAS  Google Scholar 

  • Chen AE, Ginty DD, Fan CM (2005) Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433:317–322

    Article  PubMed  CAS  Google Scholar 

  • Christ B, Brand-Saberi B (2002) Limb muscle development. Int J Dev Biol 46:905–914

    PubMed  CAS  Google Scholar 

  • Delfini MC, Hirsinger E, Pourquie O, Duprez D (2000) Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. Development 127:5213–5224

    PubMed  CAS  Google Scholar 

  • Diaconu M, Kothe U, Schlunzen F, Fischer N, Harms JM, Tonevitsky AG, Stark H, Rodnina MV, Wahl MC (2005) Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation. Cell 121:991–1004

    Article  PubMed  CAS  Google Scholar 

  • Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274:546, 563–567

    Google Scholar 

  • Gros J, Scaal M, Marcelle C (2004) A two-step mechanism for myotome formation in chick. Dev Cell 6(6):875–882

    Article  PubMed  CAS  Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stage in the development of the chick embryo. J Morphol 88:49–92

    Article  Google Scholar 

  • Hedges J, West M, Johnson AW (2005) Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J 24:567–579

    Article  PubMed  CAS  Google Scholar 

  • Hublitz P, Kunowska N, Mayer UP, Muller JM, Heyne K, Yin N, Fritzsche C, Poli C, Miguet L, Schupp IW, van Grunsven LA, Potiers N, van Dorsselaer A, Metzger E, Roemer K, Schule R (2005) NIR is a novel INHAT repressor that modulates the transcriptional activity of p53. Genes Dev 19:2912–2924

    Article  PubMed  CAS  Google Scholar 

  • Kahane N, Cinnamon Y, Kalcheim C (1998) The origin and fate of pioneer myotomal cells in the avian embryo. Mech Dev 74:59–73

    Article  PubMed  CAS  Google Scholar 

  • Kalcheim C, Ben-Yair R (2005) Cell rearrangements during development of the somite and its derivatives. Curr Opin Genet Dev 15(4):371–380

    Article  PubMed  CAS  Google Scholar 

  • Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, Gotta M, Kanapin A, Le Bot N, Moreno S, Sohrmann M, Welchman DP, Zipperlen P, Ahringer J (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231–237

    Article  PubMed  CAS  Google Scholar 

  • Köhler T, Pröls F, Brand-Saberi B (2005) PCNA in situ hybridization: a novel and reliable tool for detection of dynamic changes in proliferative activity. Histochem Cell Biol 123:315–327

    Article  PubMed  Google Scholar 

  • Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H (1995) Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 68:836–844

    Article  Google Scholar 

  • Linker C, Lesbros C, Stark MR, Marcelle C (2003) Intrinsic signals regulate the initial steps of myogenesis in vertebrates. Development 130:4797–4807

    Article  PubMed  CAS  Google Scholar 

  • Milkereit P, Gadal O, Podtelejnikov A, Trumtel S, Gas N, Petfalski E, Tollervey D, Mann M, Hurt E, Tschochner H. (2001) Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 105:499–509

    Article  PubMed  CAS  Google Scholar 

  • Molkentin JD, Olson EN. (1996) Combinatorial control of muscle development by basic helix-loop-helix and MADS-box transcription factors. Proc Natl Acad Sci USA 93(18):9366–73

    Article  PubMed  CAS  Google Scholar 

  • Nieto MA, Patel K, Wilkinson DG (1996) In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219–235

    Article  PubMed  CAS  Google Scholar 

  • Nissan TA, Bassler J, Petfalski E, Tollervey D, Hurt E (2002) 60S pre-ribosome formation viewed from assembly in the nucleolus until export to the cytoplasm. EMBO J 21:5539–5547

    Article  PubMed  CAS  Google Scholar 

  • Oeffinger M, Dlakic M, Tollervey D (2004) A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev 18:196–209

    Article  PubMed  CAS  Google Scholar 

  • Ordahl CP, Berdougo E, Venters SJ, Denetclaw WF Jr (2001) The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. Development 128(10):1731–1744

    PubMed  CAS  Google Scholar 

  • Scaal M, Christ B (2004) Formation and differentiation of the avian dermomyotome. Anat Embryol (Berl) 208(6):411–424

    Google Scholar 

  • Solnica-Krezel L (2005) Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol 15:R213–R228

    Article  PubMed  CAS  Google Scholar 

  • Weintraub H, Dwarki VJ, Verma I, Davis R, Hollenberg S, Snider L, Lassar A, Tapscott SJ (1991) Muscle-specific transcriptional activation by MyoD. Genes Dev 5(8):1377–1386

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Ordahl CP (2006) The pattern of MyoD and contractile protein localization in primary epaxial myotome reflects the dynamic progression of nascent myoblast differentiation. Dev Dyn 235:382–394

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ulrike Pein, Ellen Gimbel for the excellent technical assistances, Dr. Philip Hublitz for providing reagents and support. The authors appreciate helpful discussion with Anton J Gamel.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Beate Brand-Saberi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, X., Dai, F., Weise, C. et al. Expression of the avian gene cNOC2 encoding nucleolar complex associated protein 2 during embryonic development. Anat Embryol 211, 649–657 (2006). https://doi.org/10.1007/s00429-006-0115-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-006-0115-z

Keywords

Navigation