Skip to main content
SpringerLink
Log in

Joint locus of a/b-globin genes in Danio rerio is segregated into structural subdomains active at different stages of development

  • Cell Molecular Biology
  • Published:
Molecular Biology Aims and scope Submit manuscript

Abstract

In the domain model of eukaryotic genome organization, the functional unit of the genome, along with the relevant regulatory elements, is considered to be a gene or a gene family. In hot-blooded vertebrate animals, the domains of a- and b-globin genes are positioned at different chromosomes and are organized and regulated in different fashion. In cold-blooded animals, in particular in tropical fish Danio rerio, a- and b-globin genes are located in a common gene cluster. However, the joint a/b-globin gene cluster is subdivided into two development stage-specific subdomains, the adult one and the embryonic-larval one. In an attempt to find out whether this functional segregation correlates with structural segregation of the domain we compared the DNase I sensitivity and profiles of histone modifications of adult and embryonic-larval segments of the domain in cultured D. rerio fibroblasts. We have demonstrated that, in these nonerythroid cells, adult and embryonic-larval subdomains possess different DNase I sensitivities and different profiles of H3K27me3, a histone modification introduced by PRC2 complex. These observations suggest that joint a/b globin gene domain of Danio rerio is segregated into two structural subdomain harboring adult and embryonic-larval globin genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

MRE:

main regulatory element

LCR:

locus control region

NaBut:

sodium butyrate

PIC:

protease inhibitor cocktail

References

  1. Bodnar J.W. 1988. A domain model for eukaryotic DNA organization: A molecular basis for cell differentiation and chromosome evolution. J. Theor. Biol. 132, 479–507.

    Article  CAS  PubMed  Google Scholar 

  2. Razin S.V., Farrell C.M., Recillas-Targa F. 2003. Genomic domains and regulatory elements operating at the domain level. Int. Rev. Cytol. 226, 63–125.

    CAS  PubMed  Google Scholar 

  3. Razin S.V., Ulianov S.V., Ioudinkova E.S., Gushchanskaya E.S., Gavrilov A.A., Iarovaia O.V. 2012. Domains of alpha- and beta-globin genes in the context of the structural-functional organization of the eukaryotic genome. Biochemistry (Moscow). 77, 1409–1423.

    Article  CAS  PubMed  Google Scholar 

  4. Recillas-Targa F., Razin S.V. 2001. Chromatin domains and regulation of gene expression: Familiar and enigmatic clusters of chicken globin genes. Crit. Rev. Eukaryot. Gene Expr. 11, 227–242.

    CAS  PubMed  Google Scholar 

  5. Higgs D.R., Wood W.G., Jarman A.P., Sharpe J., Lida J., Pretorius I.-M., Ayyub H. 1990. A major positive regulatory region located far upstream of the human a-globin gene locus. Genes Dev. 4, 1588–1601.

    Article  CAS  PubMed  Google Scholar 

  6. Vyas P., Vickers M.A., Simmons D.L., Ayyub H., Craddoc C.F., Higgs D.R. 1992. cis-Acting sequences regulating expression of the human α-globin cluster lie within constitutively open chromatin. Cell. 69, 781–793.

    Article  CAS  PubMed  Google Scholar 

  7. Zhou G.L., Xin L., Song W., Di L.J., Liu G., Wu X.S., Li D.P., Liang C.C. 2006. Active chromatin hub of the mouse alpha-globin locus forms in a transcription factory of clustered housekeeping genes. Mol. Cell Biol. 26, 5096–5105.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Iudinkova E.S., Razin S.V. 2003. Regulatory systems of genome domains with vague boundaries. Russ. J. Genet. 39, 128–132.

    Article  Google Scholar 

  9. Craddock C.F., Vyas P., Sharpe J.A., Ayyub H., Wood W.G., Higgs D.R. 1995. Contrasting effects of alpha and beta globin regulatory elements on chromatin structure may be related to their different chromosomal environments. EMBO J. 14, 1718–1726.

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Forrester W.C., Epner E., Driscol, M.C., Enver T., Brice M., Papayannopoulou T., Groudin M. 1990. A deletion of the human β-globin locus activation region causes a major alteration in chromatin structure and replication across the entire β-globin locus. Genes Dev. 4, 1637–1649.

    Article  CAS  PubMed  Google Scholar 

  11. Bulger M., Bende, M.A., van Doorninck J.H., Wertman B., Farrell C.M., Felsenfel G., Groudine M., Hardison R.C. 2000. Comparative structural and functional analysis of the olfactory receptor genes flanking the human and mouse β-globin gene clusters. Proc. Natl. Acad. Sci. U. S. A. 97, 14560–14565.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Ulianov S.V., Gavrilov A.A., Razin S.V. 2012. Spatial organization of the chicken beta-globin gene domain in erythroid cells of embryonic and adult lineages. Epigenet. Chromatin. 5, 16.

    Article  CAS  Google Scholar 

  13. Grosveld F., van Assandelt G.B., Greave D.R., Kollias B. 1987. Position-independent, high-level expression of the human β-globin gene in transgenic mice. Cell. 51, 975–985.

    Article  CAS  PubMed  Google Scholar 

  14. Simon I., Tenzen T., Mostoslavsky R., Fibach E., Lande L., Milot E., Gribnau J., Grosveld F., Frazer P., Cedar H. 2001. Developmental regulation of DNA replication timing at the human β-globin locus. EMBO J. 20, 6150–6157.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Hardison R.S. 2005. Globin genes: Evolution. In: Encyclopedia of Life Sciences. Whichester: Wiley, pp. 1–7. www.els.net.

    Chapter  Google Scholar 

  16. Iarovaia O.V., Ioudinkova E.S., Petrova N.V., Dolgushin K.V., Kovina A.V., Nefedochkina A.V., Vassetzky Y.S., Razin S.V. 2014. Evolution of α and β globin genes and their regulatory systems in light of the hypothesis of domain organization of the genome. Biochemistry (Moscow). 79, 1141–1150.

    Article  CAS  PubMed  Google Scholar 

  17. Ioudinkova E.S., Petrova N.V., Bunina D.A., Vishniakova H.S., Sklyar I.V., Razin S.V., Iarovaia O.V. 2013. Chromatin structure of the joint α/β-globin gene locus of Danio rerio. Dokl Biochem Biophys. 448. 59–61.

    Article  CAS  PubMed  Google Scholar 

  18. Ganis J.J., Hsia N., Trompouki E., de Jong J.L., DiBiase A., Lambert J.S., Jia Z., Sabo P.J., Weaver M., Sandstrom R., Stamatoyannopoulos J.A., Zhou Y., Zon L.I. 2012. Zebrafish globin switching occurs in two developmental stages and is controlled by the LCR. Dev. Biol. 366, 185–194.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Krajewski W.A., Becker P.B. 1998. Reconstitution of hyperacetylated, DNase I-sensitive chromatin characterized by high conformational flexibility of nucleosomal DNA. Proc. Natl. Acad. Sci. U. S. A. 95, 1540–1545.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Litt M.D., Simpson M., Recillas-Targa F., Prioleau M.N., Felsenfeld G. 2001. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 20, 2224–2235.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Anguita E., Johnson C.A., Wood W.G., Turner B.M., Higgs D.R. 2001. Identification of a conserved erythroid specific domain of histone acetylation across the alpha-globin gene cluster. Proc. Natl. Acad. Sci. U. S. A. 98, 12114–12119.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Ebert A., Lein S., Schotta G., Reuter G. 2006. Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res. 14, 377–392.

    Article  CAS  PubMed  Google Scholar 

  23. Justin N., De Marco V., Aasland R., Gamblin S.J. 2010. Reading, writing and editing methylated lysines on histone tails: new insights from recent structural studies. Curr. Opin. Struct. Biol. 20, 730–738.

    Article  CAS  PubMed  Google Scholar 

  24. Martin C., Zhang Y. 2005. The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell Biol. 6, 838–849.

    Article  CAS  PubMed  Google Scholar 

  25. Schübeler D., Francastel C., Cimbora D.M., Reik A., Martin D.I., Groudine M. 2000. Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human betaglobin locus. Genes Dev. 15, 940–950.

    Google Scholar 

  26. Bian Q., Khanna N., Alvikas J., Belmont A.S. 2013. β-Globin cis-elements determine differential nuclear targeting through epigenetic modifications. J. Cell Biol. 203, 767–783.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Garrick D., De Gobbi M., Samara V., Rugless M., Holland M., Ayyub H., Lower K., Sloane-Stanley J., Gray N., Koch C., Dunham I., Higgs D.R. 2008. The role of the polycomb complex in silencing alpha-globin gene expression in nonerythroid cells. Blood. 112, 3889–3899.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Gene Biology, Russian Academy of Sciences, Moscow, 119334, Russia

    K. V. Dolgushin, E. S. Iudinkova, N. V. Petrova, S. V. Razin & O. V. Iarovaia

  2. Biology Department, Moscow State University, Moscow, 119991, Russia

    S. V. Razin

Authors
  1. K. V. Dolgushin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. S. Iudinkova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. V. Petrova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. V. Razin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. O. V. Iarovaia
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Iarovaia.

Additional information

Original Russian Text © K.V. Dolgushin, E.S. Iudinkova, N.V. Petrova, S.V. Razin, O.V. Iarovaia, 2015, published in Molekulyarnaya Biologiya, 2015, Vol. 49, No. 3, pp. 498–506.

These authors contributed equally to the work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dolgushin, K.V., Iudinkova, E.S., Petrova, N.V. et al. Joint locus of a/b-globin genes in Danio rerio is segregated into structural subdomains active at different stages of development. Mol Biol 49, 442–449 (2015). https://doi.org/10.1134/S0026893315030048

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026893315030048

Keywords

Search

Navigation