Skip to main content
Log in

Tandem 41-bp repeats in chicken and Japanese quail genomes: FISH mapping and transcription analysis on lampbrush chromosomes

  • Research Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

The chromosomal distribution of 41-bp repeats, known as CNM and PO41 repeats in the chicken genome and BglII repeats in the Japanese quail, was analyzed precisely using giant lampbrush chromosomes (LBC) from chicken, Japanese quail, and turkey growing oocytes. The PO41 repeat is conserved in all galliform species, whereas the other repeats are species specific. In chicken and quail, the centromere and subtelomere regions share homologous satellite sequences. RNA polymerase II transcribes the 41-bp repeats in both centromere and subtelomere regions. Ongoing transcription of these repeats was demonstrated by incorporation of BrUTP injected into oocytes at the lampbrush stage. RNA complementary to both strands of CNM and PO41 repeats is present on chicken LBC loops, whereas strand-specific G-rich transcripts are characteristic of BglII repeats in the Japanese quail. The RNA from 41-bp repeats does not undergo cotranscriptional U snRNP-dependent splicing. At the same time, the ribonucleoprotein matrix of transcription units with C-rich RNA of CNM and PO41 repeats was enriched with hnRNP protein K. Potential promoters for satellite transcription are discussed.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Almedia R, Allshire RC (2005) RNA silencing and genome regulation. Trends Cell Biol 5:251–258

    Article  Google Scholar 

  • Baldwin L, Macgregor HC (1985) Centromeric satellite in the newt Triturus cristatus karelinii and related species: its distribution and transcription on lampbrush chromosomes. Chromosoma 92:100–107

    Article  PubMed  CAS  Google Scholar 

  • Barsacchi-Pilone G, Batistoni R, Andronico F, Vitelli L, Nardi I (1986) Heterochromatic DNA in Triturus (Amphibia, Urodela). I. A satellite DNA component of the pericentric C-bands. Chromosoma 93:435–446

    Article  PubMed  CAS  Google Scholar 

  • Bomsztyk K, Denisenko O, Ostrowski J (2004) hnRNP K: one protein multiple processes. Bioessays 26:629–638

    Article  PubMed  CAS  Google Scholar 

  • Boyce-Jacino MT, Resnick R, Faras AJ (1989) Structural and functional characterization of the unusually short long terminal repeats and their adjacent regions of a novel endogenous avian retrovirus. Virology 173:157–166

    Article  PubMed  CAS  Google Scholar 

  • Christy RJ, Huang RCC (1988) Functional analysis of the long terminal repeats of intracisternal A-particle genes: sequences within the U3 region determine both the efficiency and direction of promoter activity. Mol Cell Biol 8:1093–1102

    PubMed  CAS  Google Scholar 

  • Diaz MO, Gall JG (1985) Giant readthrough transcription units at the histone loci on lampbrush chromosomes of the newt Notophthalmus. Chromosoma 92:243–253

    Article  PubMed  CAS  Google Scholar 

  • Diaz MO, Barsacchi-Pilone G, Mahon KA, Gall JG (1981) Transcripts from both strands of a satellite DNA occur on lampbrush chromosome loops of the newt Notophthalmus. Cell 24:649–659

    Article  PubMed  CAS  Google Scholar 

  • Dreyfuss G, Kim VN, Kataoka N (2002) Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3:195–205

    Article  PubMed  CAS  Google Scholar 

  • Dunn CA, Romanish MT, Gutierrez LE, van de Lagemaat LN, Mager DL (2006) Transcription of two human genes from a bi-directional endogenous retroviral promoter. Gene 366:335–342

    Article  PubMed  CAS  Google Scholar 

  • Epstein LM, Mahon KA, Gall JG (1986) Transcription of a satellite DNA in the newt. J Cell Biol 103:1137–1144

    Article  PubMed  CAS  Google Scholar 

  • Galkina S, Deryusheva S, Fillon V, Vignal A, Crooijmans R, Groenen M, Rodionov A, Gaginskaya E (2006) FISH on avian lampbrush chromosomes produces higher resolution gene mapping. Genetica 128:241–251

    Article  PubMed  CAS  Google Scholar 

  • Hori T, Suzuki Y, Solovei I, Saitoh Y, Hatchison N, Ikeda J-E, Macgregor H, Mizuno S (1996) Characterization of DNA sequence constituting the terminal heterochromatin of the chicken Z chromosome. Chromosome Res 4:411–426

    Article  PubMed  CAS  Google Scholar 

  • Jamrich M, Warrion R, Steele R, Gall JG (1983) Transcription of repetitive sequences on Xenopus lampbrush chromosomes. Proc Natl Acad Sci USA 80:3364–3367

    Article  PubMed  CAS  Google Scholar 

  • Jolly C, Lakhotia SC (2006) Human sat III and Drosophila hsrω transcripts: a common paradigm for regulation of nuclear RNA processing in stressed cells. Nucleic Acids Res 34:5508–5514

    Article  PubMed  CAS  Google Scholar 

  • Kim VN (2005) Small RNAs: classification, biogenesis, and function. Mol Cells 19:1–15

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Hahm B, Kim YK, Choi M, Jang SK (2000) Protein–protein interaction among hnRNPs shuttling between nucleus and cytoplasm. J Mol Biol 298:395–405

    Article  PubMed  CAS  Google Scholar 

  • Klimek-Tomczak K, Mikula M, Dzwonek A, Paziewska A, Wyrwicz LS, Hennig EE, Ostrowski J (2006) Mitochondria-associated satellite I RNA binds to hnRNP K protein. Acta Biochim Pol 53:169–178

    PubMed  CAS  Google Scholar 

  • Krasikova A, Kulikova T, Saifitdinova A, Derjusheva S, Gaginskaya E (2004) Centromeric protein bodies on avian lampbrush chromosomes contain a protein detectable with an antibody against DNA topoisomerase II. Chromosoma 113:316–323

    Article  PubMed  CAS  Google Scholar 

  • Krasikova A, Barbero JL, Gaginskaya E (2005) Cohesion proteins are present in centromere protein bodies associated with avian lampbrush chromosomes. Chromosome Res 13:675–685

    Article  PubMed  CAS  Google Scholar 

  • Krasikova A, Deryusheva S, Galkina S, Kurganova A, Evteev A, Gaginskaya E (2006) On the positions of centromeres in chicken lampbrush chromosomes. Chromosome Res 14:777–789

    Article  PubMed  CAS  Google Scholar 

  • Laurent A-M, Puechberty J, Roizes G (1999) Hypothesis: for the worst and for the best, L1Hs retrotransposons actively participate in the evolution of the centromeric alphoid sequences. Chromosome Res 7:305–317

    Article  PubMed  CAS  Google Scholar 

  • Lerner EA, Lerner MR, Janeway CA, Steitz JA (1981) Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci USA 78:2737–2741

    Article  PubMed  CAS  Google Scholar 

  • Ma J, Jackson SA (2006) Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. Genome Res 16:251–259

    Article  PubMed  CAS  Google Scholar 

  • Masi T, Johnson AD (2003) Read-through histone transcripts containing 3′ adenylate tails are zygotically expressed in Xenopus embryos and undergo processing to mature transcripts when introduced into oocytes nuclei. Biochem Biophys Res Commun 304:612–618

    Article  PubMed  CAS  Google Scholar 

  • Matunis MJ, Michael WM, Dreyfuss G (1992) Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein. Mol Cell Biol 12:164–171

    PubMed  CAS  Google Scholar 

  • Matzke MA, Birchler JA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35

    Article  PubMed  CAS  Google Scholar 

  • Matzke MA, Varga F, Berger H, Schernthaner J, Schweizer D, Mayr B, Matzke AJM (1990) A 41-42 bp tandemly repeated sequence isolated from nuclear envelopes of chicken erythrocytes is located predominantly on microchromosomes. Chromosoma 99:131–137

    Article  PubMed  CAS  Google Scholar 

  • Matzke AJM, Varga F, Gruendler P, Unfried I, Berger H, Mayr B, Matzke MA (1992) Characterization of a new repetitive sequence that is enriched on microchromosomes of turkey. Chromosoma 102:9–14

    Article  PubMed  CAS  Google Scholar 

  • Pinol-Roma S, Swanson MS, Gall JG, Dreyfuss G (1989) A novel heterogeneous nuclear RNP protein with unique distribution on nascent transcripts. J Cell Biol 109:2575–2587

    Article  PubMed  CAS  Google Scholar 

  • Prades C, Laurent A-M, Puechberty J, Yurov Y, Roizes G (1996) SINE and LINE within human centromeres. J Mol Evol 42:37–43

    Article  PubMed  CAS  Google Scholar 

  • Prasanth KV, Spector D (2007) Eukaryotic regulatory RNAs: an answer to the ‘genome complexity’ conundrum. Genes Dev 21:11–42

    Article  PubMed  CAS  Google Scholar 

  • Prieto I, Tease C, Pezzi N, Buesa JM, Ortega S, Kremer L, Martinez A, Martinez-A C, Hulten MA, Barbero JL (2004) Cohesin component dynamics during meiotic prophase I in mammalian oocytes. Chromosome Res 12:197–213

    Article  PubMed  CAS  Google Scholar 

  • Rudert F, Bronner S, Garnier J-M, Dolle P (1995) Transcripts from opposite strands of γ satellite DNA are differentially expressed during mouse development. Mamm Genome 6:76–83

    Article  PubMed  CAS  Google Scholar 

  • Schmid M, Nanda I, Hoehn H, Schartl M, Haaf T, Buerstedde J-M, Arakawa H, Caldwell RB, Weigend S, Burt DW, Smith J, Griffin DK, Masabanda JS, Groenen MAM, Crooijmans RPMA, Vignal A, Fillon V, Morisson M, Pitel F, Vignoles M, Garrigues A, Gellin J, Rodionov AV, Galkina SA, Lukina NA, Ben-Ari G, Blum S, Hillel J, Twito T, Lavi U, David L, Feldman MW, Delany ME, Conley CA, Fowler VM, Hedges SB, Godbout R, Katyal S, Smith C, Hudson Q, Sinclair A, Mizuno S (2005) Second report on chicken genes and chromosomes. Cytogenet Genome Res 109:415–479

    Article  PubMed  CAS  Google Scholar 

  • Solovei I, Gaginskaya ER, Macgregor HC (1994) The arrangement and transcription of telomere DNA sequences at the ends of lampbrush chromosomes of birds. Chromosome Res 2:460–470

    Article  PubMed  CAS  Google Scholar 

  • Solovei I, Macgregor H, Gaginskaya E (1995) Single stranded nucleic acid binding structures on chicken lampbrush chromosomes. J Cell Sci 108:1391–1396

    PubMed  CAS  Google Scholar 

  • Solovei I, Joffe BI, Gaginskaya ER, Macgregor HC (1996) Transcription on lampbrush chromosomes of a centromerically localized highly repeated DNA in pigeon (Columba) relates to sequence arrangement. Chromosome Res 4:588–603

    Article  PubMed  CAS  Google Scholar 

  • Sun X, Le HD, Wahlstrom JM, Karpen GH (2003) Sequence analysis of a functional Drosophila centromere. Genome Res 13:182–194

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Suzuki T, Nojiri T, Yamagata T, Namikawa T, Matsuda Y (2000) Characterization and chromosomal distribution of a novel satellite DNA sequence of Japanese quail (Coturnix coturnix japonica). J Hered 91:412–415

    Article  PubMed  CAS  Google Scholar 

  • Topp CN, Zhong CX, Dawe RK (2004) Centromere-encoded RNAs are integral components of the maize kinetochore. Proc Natl Acad Sci USA 101:15986–15991

    Article  PubMed  CAS  Google Scholar 

  • Varley JM, Macgregor HC, Erba HP (1980) Satellite DNA is transcribed on lampbrush chromosomes. Nature 283:686–688

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Li J, Leung FC (2002) Partially inverted tandem repeat isolated from pericentric region of chicken chromosome 8. Chromosome Res 10:73–82

    Article  PubMed  CAS  Google Scholar 

  • Wicker T, Robertson JS, Schulze SR, Feltus FA, Magrini V, Morrison JA, Mardis ER, Wilson RK, Peterson DG, Paterson AH, Ivarie R (2005) The repetitive landscape of the chicken genome. Genome Res 15:126–136

    Article  PubMed  Google Scholar 

  • Yamada K, Shibusawa M, Tsudzuki M, Matsuda Y (2002) Molecular cloning and characterization of novel centromeric repetitive DNA sequences in the blue-breasted quail (Coturnix chinensis, Galliformes). Cytogenet Genome Res 98:255–261

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the following people for providing antibodies: J. L. Barbero (Centro Nacional de Biotecnologia, Madrid, Spain), M. V. Filatov (Saint-Petersburg Institute of Nuclear Physics, Russia), J. G. Gall (Carnegie Institution of Washington, Baltimore, MD, USA), and U. Scheer and R. Hock (University of Wuerzburg, Germany). We are grateful to J. G. Gall for the critical reading and careful editing of the manuscript. We would like to thank our former graduate student A. Kurganova for her assistance in some experiments. This work was supported by the Russian Foundation for Basic Research (grant 05-04-48252). We used the equipment of the Core Facility “CHROMAS” (Biological Institute, Saint-Petersburg State University).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elena Gaginskaya.

Additional information

Communicated by M. Matzke

Rights and permissions

Reprints and permissions

About this article

Cite this article

Deryusheva, S., Krasikova, A., Kulikova, T. et al. Tandem 41-bp repeats in chicken and Japanese quail genomes: FISH mapping and transcription analysis on lampbrush chromosomes. Chromosoma 116, 519–530 (2007). https://doi.org/10.1007/s00412-007-0117-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-007-0117-5

Keywords

Navigation