Non-canonical Cajal bodies form in the nucleus of late stage avian oocytes lacking functional nucleolus

Abstract

In the somatic cell nucleus, there are several universal domains such as nucleolus, SC35-domains, Cajal bodies (CBs) and histone locus bodies (HLBs). Among them, CBs were described more than 100 years ago; however, we still do not have a final understanding of their nature and biological significance. The giant nucleus of avian and amphibian growing oocytes represents an advantageous model for analysis of functions and biogenesis of various nuclear domains. Nevertheless, in large-sized avian oocytes that contain transcriptionally active lampbrush chromosomes, CB-like organelles have not been identified yet. Here we demonstrate that in the pigeon (Columba livia) oocyte nucleus, characterized by absence of any functional nucleoli, extrachromosomal spherical bodies contain TMG-capped spliceosomal snRNAs, core proteins of Sm snRNPs and the protein coilin typical for CBs, but not splicing factor SC35 nor the histone pre-mRNA 3′-end processing factor symplekin. The results establish that coilin-rich nuclear organelles in pigeon late-stage oocyte are not the equivalents of HLBs but belong to a group of CBs. At the same time, they do not contain the snoRNP/scaRNP protein fibrillarin involved in 2′-O-methylation of snoRNAs and snRNAs. Thus, the nucleus of late-stage pigeon oocytes houses CB-like organelles that have an unusual molecular composition and are implicated in the snRNP biogenesis pathway. These data demonstrate that snRNP-rich non-canonical CBs can form in the absence of nucleolus. We argue that pigeon oocytes represent a new promising model to investigate CB modular organization, functions and formation mechanism.

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Acknowledgments

We are grateful to J.G. Gall (Carnegie Institution for Science, Department of Embryology, Baltimore, USA) for mAb against symplekin (BD Transduction Laboratories). The authors thank anonymous reviewers for helpful comments and suggestions. This investigation was supported by research Grant of the President of Russian Federation (project # 3299.2010.4) and Federal Grant-in-Aid Program "Human Capital for Science and Education in Innovative Russia" (Governmental Contracts ## P1367 and 14.740.11.1189). The authors acknowledge Saint-Petersburg State University for a research Grant No. 1.40.703.2011 and the Core Facility ‘CHROMAS’ (Saint-Petersburg State University) for technical support.

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Correspondence to Alla Krasikova.

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Khodyuchenko, T., Gaginskaya, E. & Krasikova, A. Non-canonical Cajal bodies form in the nucleus of late stage avian oocytes lacking functional nucleolus. Histochem Cell Biol 138, 57–73 (2012). https://doi.org/10.1007/s00418-012-0938-z

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Keywords

  • Avian oogenesis
  • Cajal body
  • Coilin
  • Germinal vesicle
  • Histone locus body
  • Nuclear bodies
  • Nuclear compartments
  • Nucleolus
  • Nucleus
  • Oocyte
  • Splicing factors