Chromosome Research

, Volume 14, Issue 7, pp 777–789 | Cite as

On the positions of centromeres in chicken lampbrush chromosomes

  • Alla Krasikova
  • Svetlana Deryusheva
  • Svetlana Galkina
  • Anna Kurganova
  • Andrei Evteev
  • Elena Gaginskaya
Article

Abstract

Using immunostaining with antibodies against cohesin subunits, we show here that cohesin-enriched structures analogous to the so-called centromere protein bodies (PB) are the characteristic of galliform lampbrush chromosomes. Their centromeric location was verified by FISH with certain DNA probes. PB-like structures were used as markers for centromere localization in chicken lampbrush chromosomes. The gap predicted to be centromeric in current chicken chromosome 3 sequence assembly was found to correspond to the non-centromeric cluster of CNM repeat on the q-arm of chromosome 3; the centromere is proposed to be placed at another position. The majority of chicken microchromosomes were found to be acrocentric, in contrast to Japanese quail microchromosomes which are biarmed. Centromere cohesin-enriched structures on chicken and quail lampbrush microchromosomes co-localize with pericentromeric CNM and BglII− repeats respectively. FISH to the nascent transcripts on chicken lampbrush chromosomes revealed numerous non-centromeric CNM clusters in addition to pericentromeric arrays. Complementary CNM transcripts from both C- and G-rich DNA strands were revealed during the lampbrush stage.

Key words

centromere chicken CNM cohesin lampbrush chromosome 

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References

  1. Almedia R, Allshire RC (2005) RNA silencing and genome regulation. Trends Cell Biol 5: 251–258.CrossRefGoogle Scholar
  2. Callan HG (1986) Lampbrush Chromosomes. Berlin: Springer Verlag.Google Scholar
  3. Chelysheva LA, Solovei IV, Rodionov AV, Iakovlev AF, Gaginskaya ER (1990) The lampbrush chromosomes of the chicken. Cytological maps of the macrobivalents. Tsitologiia 32: 303–316.PubMedGoogle Scholar
  4. Crooijmans RPMA, Vrebalov J, Dijkhof RJ et al. (2000) Two-dimensional screening of the Wageningen chicken BAC library. Mamm Genome 11: 360–363.PubMedCrossRefGoogle Scholar
  5. Derjusheva S, Kurganova A, Krasikova A, Saifitdinova A, Habermann FA, Gaginskaya E (2003) Precise identification of chicken chromosomes in the lampbrush form using chromosome painting probes. Chromosome Res 11: 749–757.PubMedCrossRefGoogle Scholar
  6. Gaginskaya ER (1972) Nuclear structures in oocytes of adult birds. II. Protein bodies and the karyosphere. Tsitologiia 14: 568–578.Google Scholar
  7. Gaginskaya ER, Gruzova MN (1969) Characteristics of oogenesis in the finch. Tsitologiia 11: 1241–1251.Google Scholar
  8. Galkina S, Lukina N, Zakharova K, Rodionov AV (2005) Interstitial (TTAGGG)(n) sequences are not hot spots of recombination in the chicken lampbrush macrochromosomes 1-3. Chromosome Res 13: 551–557.PubMedCrossRefGoogle Scholar
  9. Galkina S, Deryusheva S, Fillon V et al. (2006) FISH on avian lampbrush chromosomes produces higher resolution gene mapping. Genetica DOI http://dx.doi.org/10.1007/s10709-005-5776-7.
  10. Gall JG (1992) Organelle assembly and function in the amphibian germinal vesicle. Adv Dev Biol 1: 1–29.CrossRefGoogle Scholar
  11. Griffin DK, Habermann F, Masabanda J et al. (1999) Micro- and macrochromosome paints generated by flow cytometry and microdissection: tools for mapping chicken genome. Cytogenet Cell Genet 87: 278–281.PubMedCrossRefGoogle Scholar
  12. Handwerger KE, Gall JG (2006) Subnuclear organelles: new insights into form and function. Trends Cell Biol 16: 19–26.PubMedCrossRefGoogle Scholar
  13. Hori T, Suzuki Y, Solovei I et al. (1996) Characterization of DNA sequence constituting the terminal heterochromatin of the chicken Z chromosome. Chromosome Res 4: 411–426.PubMedCrossRefGoogle Scholar
  14. Hutchison N (1987) Lampbrush chromosomes of the chicken, Gallus domesticus. J Cell Biol 105: 1493–1500.PubMedCrossRefGoogle Scholar
  15. ICGSC (International Chicken Genome Sequencing Consortium) (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–716.CrossRefGoogle Scholar
  16. Itoh Y, Mizuno S (2002) Molecular and cytological characterization of SspI-family repetitive sequence on the chicken W chromosome. Chromosome Res 10: 499–511.PubMedCrossRefGoogle Scholar
  17. Kaelbling M, Fechheimer NS (1983) Synaptonemal complexes and the chromosome complement of domestic fowl, Gallus domesticus. Cytogenet Cell Genet 35: 87–92.PubMedGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. Kropotova EV, Gaginskaya ER (1984) Lampbrush chromosomes from the Japanese quail oocytes. Tsitologiia 26: 1008–1015.Google Scholar
  21. Macgregor HC (1986) The lampbrush chromosomes of animal oocytes. In Risley MS, ed., Chromosome Structure and Function. New York: Van Rostrand Reinhold, pp. 152–186.Google Scholar
  22. Macgregor HC (2002) Lampbrush Chromosomes. Retrieved from http://www.exeter.ac.uk/projects/lampbrush/.
  23. Masabanda JS, Burt DW, O’Brien PCM et al. (2004) Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics 166: 1367–1373.PubMedCrossRefGoogle Scholar
  24. Matera AG (1999) Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends Cell Biol 9: 302–309.PubMedCrossRefGoogle Scholar
  25. Matzke MA, Varga F, Berger H et al. (1990) A 41–42 bp tandemly repeated sequence isolated from nuclear envelopes of chicken erythrocytes is located predominantly on microchromosomes. Chromosoma 99: 131–137.PubMedCrossRefGoogle Scholar
  26. Morgan GT (2002) Lampbrush chromosomes and associated bodies: new insights into principles of nuclear structure and function. Chromosome Res 10: 177–200.PubMedCrossRefGoogle Scholar
  27. Myakoshina YuA, Rodionov AV (1994) Meiotic lampbrush chromosomes in turkey, Meleagris gallopavo (Galliformes: Meleagrididae). Genetika 30: 577–583.Google Scholar
  28. Nanda I, Schmid M (1994) Localization of the telomeric (TTAGGG)n sequence in chicken (Gallus domesticus) chromosomes. Cytogenet Cell Genet 65: 190–193.PubMedCrossRefGoogle Scholar
  29. Ogawa A, Solovei I, Hutchison N et al. (1997) Molecular characterization and cytological mapping of a non-repetitive DNA sequence region from the W chromosome of chicken and its use as a universal probe for sexing carinatae birds. Chromosome Res 5: 93–101.PubMedCrossRefGoogle Scholar
  30. Parra MT, Viera A, Gomez R et al. (2004) Involvement of the cohesin Rad21 and SCP3 in monopolar attachment of sister kinetochores during mouse meiosis I. J Cell Sci 117: 1221–1234.PubMedCrossRefGoogle Scholar
  31. Pichugin AM, Galkina SA, Potekhin AA, Punina EO, Rautian MS, Rodionov AV (2001) Determination of the minimum size of Gallus gallus domesticus chicken microchromosome by a pulse electrophoresis method. Genetika 37: 657–660.PubMedGoogle Scholar
  32. Prieto I, Tease C, Pezzi N et al. (2004) Cohesin component dynamics during meiotic prophase I in mammalian oocytes. Chromosome Res 12: 197–213.PubMedCrossRefGoogle Scholar
  33. Rodionov AV, Chechik MS (2002) Lampbrush chromosomes in the Japanese quail Coturnix coturnix japonica: cytological maps of macro chromosomes and meiotic crossover frequency in females. Genetika 38: 1246–1251.PubMedGoogle Scholar
  34. Romanov MN, Daniels LM, Dodgson JB, Delany ME (2005) Integration of the cytogenetic and physical maps of chicken chromosome 17. Chromosome Res 13: 215–22.PubMedCrossRefGoogle Scholar
  35. Saifitdinova A, Derjusheva S, Krasikova A, Gaginskaya E (2003) Lampbrush chromosomes of the chaffinch (Fringilla coelebs L.). Chromosome Res 11: 93–113.CrossRefGoogle Scholar
  36. Schmid M, Nanda I, Guttenbach M et al. (2000) First report on chicken genes and chromosomes. Cytogenet Cell Genet 90: 169–218.PubMedCrossRefGoogle Scholar
  37. Schmid M, Nanda I, Hoehn H et al. (2005) Second report on chicken genes and chromosomes. Cytogenet Genome Res 109: 415–479.PubMedCrossRefGoogle Scholar
  38. Solari AJ (1980) El cariotipado ultrastructural. Actas IV Congr. Latinoam. Genetica 2: 171–178.Google Scholar
  39. Solari AJ (1992) Equalization of Z and W axes in chicken and quail oocytes. Cytogenet Cell Genet 59: 52–56.PubMedGoogle Scholar
  40. Solari AJ, Dresser ME (1995) High-resolution cytological localization of the XhoI and EcoRI repeat sequences in the pachytene ZW bivalent of the chicken. Chromosome Res 3: 87–93.PubMedCrossRefGoogle Scholar
  41. Solovei I, Gaginskaya E, Hutchison N, Macgregor H (1993) Avian sex chromosomes in the lampbrush form: the ZW lampbrush bivalent from six species of bird. Chromosome Res 1: 153–166.PubMedCrossRefGoogle Scholar
  42. 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.PubMedCrossRefGoogle Scholar
  43. Solovei IV, 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.PubMedCrossRefGoogle Scholar
  44. Solovei I, Ogawa A, Naito M, Mizuno S, Macgregor H (1998) Specific chromomeres on the chicken W lampbrush chromosome contain specific repetitive DNA sequence families. Chromosome Res 6: 323–327.PubMedCrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. Wang X, Li J, Leung FC (2002) Partially inverted tandem repeat isolated from pericentric region of chicken chromosome 8. Chromosome Res 10: 73–82.PubMedCrossRefGoogle Scholar
  47. Wicker T, Robertson JS, Schulze SR et al. (2005) The repetitive landscape of the chicken genome. Genome Res 15: 126–136.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Alla Krasikova
    • 1
  • Svetlana Deryusheva
    • 1
  • Svetlana Galkina
    • 1
  • Anna Kurganova
    • 1
  • Andrei Evteev
    • 1
  • Elena Gaginskaya
    • 1
  1. 1.Biological Research InstituteSaint-Petersburg State UniversitySaint-PetersburgRussia

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