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Chromosome Research

, Volume 23, Issue 3, pp 495–503 | Cite as

Transcription of subtelomere tandemly repetitive DNA in chicken embryogenesis

  • Irina Trofimova
  • Darya Chervyakova
  • Alla Krasikova
Original Article

Abstract

Transcription of tandemly repetitive DNA in embryogenesis seems to be of special interest due to a crucial role of non-coding RNAs in many aspects of development. However, only a few data are available on tandem repeats transcription at subtelomere regions of chromosomes during vertebrate embryogenesis. To reduce this gap, we examined stage and tissue-specific pattern of subtelomeric PO41 (pattern of 41 bp) tandem repeat transcription during embryogenesis of chicken (Gallus gallus domesticus). Using whole-mount RNA fluorescent in situ hybridization and reverse transcription PCR with specific primers, we demonstrated that both strands of PO41 repeat are transcribed at each of the studied stages of chicken embryo development: from 7–8 HH to 20 HH stages. Subtelomere-derived transcripts localize in the nuclei of all cell types and throughout the all embryonic bodies: head, somites, tail, wings and buds. In embryo-dividing cells and cultured embryonic fibroblasts, PO41 RNAs envelop terminal regions of chromosomes. PO41-containing RNAs are predominantly single-stranded and can be polyadenylated, indicating appearance of non-nascent form of subtelomeric transcripts. PO41 repeat RNAs represent a rare example of ubiquitously transcribed non-coding RNAs, such as Xist/XIST RNA or telomere repeat-containing RNA. Distribution of PO41 repeat transcripts at different stages of embryo development and among cell types has extremely uniform pattern, indicating on possible universal functions of PO41 non-coding RNAs.

Keywords

Chicken Embryogenesis Mitosis Non-coding RNA Subtelomere Tandem repeat Transcription Whole-mount in situ hybridization 

Abbreviations

CEFs

Chicken embryonic fibroblasts

HH

Hamburger and Hamilton

DMEM

Dulbecco’s modified Eagle’s medium

PO41

Pattern of 41 bp

RNA FISH

RNA fluorescent in situ hybridization

RT-PCR

Reverse transcription polymerase chain reaction

WISH

Whole-mount in situ hybridization

Notes

Acknowledgments

We thank Antonina Maslova (St. Petersburg State University, Russia) for chicken embryonic fibroblasts collection and cultivation. This research was supported by Russian Science Foundation (grant #14-14-00131). The work was partially performed using experimental equipment of the Research Resource Centers ‘Chromas’ and ‘Molecular and cell technologies’ of St Petersburg State University.

Supplementary material

10577_2015_9487_MOESM1_ESM.pdf (3.3 mb)
ESM 1 (PDF 3367 kb)

References

  1. Byron M, Hall LL, Lawrence JB (2013) A multifaceted FISH approach to study endogenous RNAs and DNAs in native nuclear and cell structures. Curr Protoc Hum Genet 76:4.15.1–4.15.21CrossRefGoogle Scholar
  2. Clemson CM, McNeil JA, Willard HF, Lawrence JB (1996) XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear chromosome structure. J Cell Biol 132:259–275CrossRefPubMedGoogle Scholar
  3. Darnell DK, Kaur S, Stanislaw S et al (2007) GEISHA: an in situ hybridization gene expression resource for the chicken embryo. Cytogenet Genome Res 117:30–35CrossRefPubMedGoogle Scholar
  4. Deng Z, Wang Z, Xiang C et al (2012) Formation of telomeric repeat-containing RNA (TERRA) foci in highly proliferating mouse cerebellar neuronal progenitors and medulloblastoma. J Cell Sci 125:4383–4394PubMedCentralCrossRefPubMedGoogle Scholar
  5. Deryusheva S, Krasikova A, Kulikova T, Gaginskaya E (2007) Tandem 41-bp repeats in chicken and Japanese quail genomes: FISH mapping and transcription analysis on lampbrush chromosomes. Chromosoma 116:519–530CrossRefPubMedGoogle Scholar
  6. Duthie SM, Nesterova TB, Formstone EJ et al (1999) Xist RNA exhibits a banded localization on the inactive X chromosome and is excluded from autosomal material in cis. Hum Mol Genet 8:195–204CrossRefPubMedGoogle Scholar
  7. Enukashvily NI, Ponomartsev NV (2013) Mammalian satellite DNA: a speaking dumb. In: Donev R, eds. Organisation of chromosomes. Adv Protein Chem Struct Biol 90. Academic Press, pp 31–65Google Scholar
  8. Enukashvily NI, Donev R, Waisertreiger IS, Podgornaya OI (2007) Human chromosome 1 satellite 3 DNA is decondensed, demethylated and transcribed in senescent cells and in A431 epithelial carcinoma cells. Cytogenet Genome Res 118:42–54CrossRefPubMedGoogle Scholar
  9. Eymery А, Callanan М, Vourc’h С (2009a) The secret message of heterochromatin: new insights into the mechanisms and function of centromeric and pericentric repeat sequence transcription. Dev Biol 53:259–268Google Scholar
  10. Eymery A, Horard B, Atifi-Borel M et al (2009b) A transcriptomic analysis of human centromeric and pericentric sequences in normal and tumor cells. Nucleic Acids Res 37:6340–6354PubMedCentralCrossRefPubMedGoogle Scholar
  11. Fukagawa T, Nogami M, Yoshikawa M et al (2004) Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat Cell Biol 6:784–791CrossRefPubMedGoogle Scholar
  12. Hall LL, Carone DM, Gomez AV et al (2014) Stable C0T-1 repeat RNA is abundant and is associated with euchromatic interphase chromosomes. Cell 156:907–919PubMedCentralCrossRefPubMedGoogle Scholar
  13. Hamburger V, Hamilton H (1951) A series of normal stages in the development of the chick embryo. Dev Dyn 195:231–272CrossRefGoogle Scholar
  14. Kuznetzova TV, Enukashvily NI, Trofimova IL, Gorbunova AV, Vashukova ES, Baranov VS (2012) Localisation and transcription of human chromosome 1 pericentromeric heterochromatin in embryonic and extraembryonic tissues. Med Genetics 11:19–24Google Scholar
  15. Lee H-R, Neumann P, Macas J, Jiang J (2006) Transcription and evolutionary dynamics of the centromeric satellite repeat CentO in rice. Mol Biol Evol 23:2505–2520CrossRefPubMedGoogle Scholar
  16. Lopez-Flores I, Garrido-Ramos MA (2012) The repetitive DNA content of eukaryotic genomes. In: Garrido-Ramos MA (ed) Genome Dynamics 7. Karger, Basel, pp 1–28Google Scholar
  17. Luke B, Lingner J (2009) TERRA: telomeric repeat-containing RNA. EMBO J 28:2503–2510PubMedCentralCrossRefPubMedGoogle Scholar
  18. May BP, Lippman ZB, Fang Y, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet 1:0705–0714CrossRefGoogle Scholar
  19. Pauli A, Rinn JL, Schier AF (2011) Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12:136–149PubMedCentralCrossRefPubMedGoogle Scholar
  20. Pizard A, Haramis A, Carrasco AE, Franco P, López S, Paganelli A (2004) Whole-mount in situ hybridization and detection of RNAs in vertebrate embryos and isolated organs. In: Ausubel FM (ed) Current Protocols in Molecular Biology. Greene Pub. Associates, Wiley-Interscience, New York, pp 14.9.1–14.9.24Google Scholar
  21. Probst AV, Almouzni G (2008) Pericentric heterochromatin: dynamic organization during early development in mammals. Differentiation 76:15–23CrossRefPubMedGoogle Scholar
  22. Probst AV, Almouzni G (2011) Heterochromatin establishment in the context of genome-wide epigenetic reprogramming. Trends Genet 27:177–185CrossRefPubMedGoogle Scholar
  23. Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G (2010) A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell 19:625–638CrossRefPubMedGoogle Scholar
  24. Riethman H, Ambrosini A, Paul S (2005) Human subtelomere structure and variation. Chromosome Res 13:505–515CrossRefPubMedGoogle Scholar
  25. Roeszler KN, Itman C, Sinclair AH, Smith CA (2012) The long non-coding RNA, MHM, plays a role in chicken embryonic development, including gonadogenesis. Dev Biol 366:317–326CrossRefPubMedGoogle Scholar
  26. Rudert F, Bronner S, Garnier JM, Dolle P (1995) Transcripts from opposite strands of gamma satellite DNA are differentially expressed during mouse development. Mamm Genome 6:76–83CrossRefPubMedGoogle Scholar
  27. Rychlik MP, Chon H, Cerritelli SM, Klimek P, Crouch RJ, Nowotny M (2010) Crystal structures of RNase H2 in complex with nucleic acid reveal the mechanism of RNA-DNA junction recognition and cleavage. Mol Cell 40:658–670PubMedCentralCrossRefPubMedGoogle Scholar
  28. Schoeftner S, Blasco MA (2008) Developmentally regulated transcription of mammalian telomeres by DNA-dependent RNA polymerase II. Nat Cell Biol 10:228–236CrossRefPubMedGoogle Scholar
  29. Shao P, Liaoa J-Y, Guana D-G et al (2012) Drastic expression change of transposon-derived piRNA-like RNAs and microRNAs in early stages of chicken embryos implies a role in gastrulation. RNA Biol 9:212–227CrossRefPubMedGoogle Scholar
  30. Sone M, Hayashi T, Tarui H, Agata K, Takeichi M, Nakagawa S (2007) The mRNA-like noncoding RNA Gomafu constitutes a novel nuclear domain in a subset of neurons. J Cell Sci 120:2498–2506CrossRefPubMedGoogle Scholar
  31. Teranishi M, Shimada Y, Hori T et al (2001) Transcripts of the MHM region on the chicken Z chromosome accumulate as non-coding RNA in the nucleus of female cells adjacent to the DMRT1 locus. Chromosome Res 9:147–165CrossRefPubMedGoogle Scholar
  32. Trofimova I, Popova D, Vasilevskaya E, Krasikova A (2014) Non-coding RNA derived from a conservative subtelomeric tandem repeat in chicken and Japanese quail somatic cells. Mol Cytogenet 7:1–13CrossRefGoogle Scholar
  33. Ugarkovic D (2005) Functional elements residing within satellite DNAs. EMBO Rep 6:1035–1039PubMedCentralCrossRefPubMedGoogle Scholar
  34. Vourc’h C, Biamonti G (2011) Transcription of satellite DNAs in mammals. In: Ugarkovic D (ed) Long non-coding RNAs, progress in molecular and subcellular biology. Springer-Verlag, New York, pp 95–118Google Scholar
  35. Wicker T, Robertson JS, Schulze SR et al (2005) The repetitive landscape of the chicken genome. Genome Res 15:126–136PubMedCentralCrossRefPubMedGoogle Scholar
  36. Zheng R, Shen Z, Tripathi V et al (2010) Polypurine-repeat-containing RNAs: a novel class of long non-coding RNA in mammalian cells. J Cell Sci 123:3734–3744PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Irina Trofimova
    • 1
  • Darya Chervyakova
    • 1
  • Alla Krasikova
    • 1
  1. 1.Saint-Petersburg State UniversitySaint-PetersburgRussia

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