Cytotechnology

, Volume 52, Issue 3, pp 159–170 | Cite as

YY1 binds to regulatory element of chicken lysozyme and ovalbumin promoters

  • Mahboob Morshed
  • Munetoshi Ando
  • Junko Yamamoto
  • Akitsu Hotta
  • Hidenori Kaneoka
  • Jun Kojima
  • Ken-ichi Nishijima
  • Masamichi Kamihira
  • Shinji Iijima
ORIGINAL PAPER

Abstract

Chicken lysozyme is highly expressed in the oviduct. The 5′ regulatory region of this gene contains a negative element that represses transcription. To assess the molecular basis underlying the regulation of lysozyme gene expression, we investigated the binding protein to this region. Sequence motif analysis suggested the existence of putative YY1 binding sites in this regulatory region. Electrophoretic mobility shift assay showed the specific binding of YY1 to the negative element. In addition, chromatin immunoprecipitation assay indicated that YY1 specifically bound to the negative element in oviduct cells but not in erythrocytes. It was suggested by electrophoretic mobility shift assay and chromatin immunoprecipitation assay that YY1 also bound to the negative regulatory region in the promoter of the ovalbumin gene which also shows oviduct-specific expression. Western blot analysis showed that YY1 was expressed in relatively high levels in the oviduct and nucleus fractionation experiments showed that YY1 was localized both in chromosome and nuclear matrix fractions. These results suggest that there are some specific roles in the negative regulatory regions of these genes in relation to the multifunctional transcription factor YY1.

Keywords

Lysozyme Ovalbumin Oviduct Promoter YY1 

Abbreviations

ChIP

chromatin immunoprecipitation

DHS

DNase I-hypersensitive site

EMSA

electrophoretic mobility shift assay

NE

negative element

NRE

negative regulatory element

SDRE

steroid dependent regulatory element

Notes

Acknowledgements

This work was supported in part by a Grant-in-Aid for Young Scientists (B) (16760634) from the Ministry of Education, Science, Sports and Culture of Japan and a Grant-in-Aid for Scientific Research (17360396) from Japan Society for the Promotion of Science.

References

  1. Bagchi M, Ansari SA, Lindenmuth DM, van Wijnen AJ, Lian J, Stein JL, Stein GS (1998) Nuclear matrix associated DNA-binding proteins of ocular lens epithelial cells. Mol Biol Rep 25:13–19CrossRefGoogle Scholar
  2. Baniahmad A, Steiner C, Köhne AC, Renkawitz R (1990) Modular structure of a chicken lysozyme silencer: Involvement of an unusual thyroid hormone receptor binding site. Cell 61:505–514CrossRefGoogle Scholar
  3. Bode J, Goetze S, Heng H, Krawetz SA, Benham C (2003) From DNA structure to gene expression: mediators of nuclear compartmentalization and dynamics. Chromosome Res 11:435–445CrossRefGoogle Scholar
  4. Bonifer C, Jägle U, Huber MC (1997) The chicken lysozyme locus as a paradigm for the complex developmental regulation of eukaryotic gene loci. J Biol Chem 272:26075–26078CrossRefGoogle Scholar
  5. Burcin M, Arnold R, Lutz M, Kaiser B, Runge D, Lottspeich F, Filippova GN, Lobanenkov VV, Renkawitz R (1997) Negative protein 1, which is required for function of the chicken lysozyme gene silencer in conjunction with hormone receptors, is identical to the multivalent zinc finger repressor CTCF. Mol Cell Biol 17:1281–1288Google Scholar
  6. Chamberlain EM, Sanders MM (1999) Identification of the novel players δEF1 in estrogen transcriptional cascades. Mol Cell Biol 19:3600–3606Google Scholar
  7. Ciejek EM, Tsai M-J, O’Malley W (1983) Actively transcribed genes are associated with nuclear matrix. Nature 306:607–609CrossRefGoogle Scholar
  8. Dillner NB, Sanders MM (2000) Hormone response units: the ovalbumin model. In: Pandalai SG (eds) Recent research developments in molecular & cellular biology, vol. 1, Kelara, India, pp 93–108Google Scholar
  9. Dillner NB, Sanders MM (2002) The zinc finger/homeodomain protein δEF1 mediates estrogen-specific induction of the ovalbumin gene. Mol Cell Endocrinol 192:85–91CrossRefGoogle Scholar
  10. Ehlen Haecker SA, Muramatsu T, Sensenbaugh KR, Sanders MM (1995) Repression of the ovalbumin gene involves multiple negative elements including a ubiquitous transcriptional silencer. Mol Endocrinol 9:1113–1126CrossRefGoogle Scholar
  11. Fritton HP, Igo-Kemenes T, Nowock J, Strech-Jurk U, Theisen M, Sippel AE (1984) Alternative sets of DNase I-hypersensitive sites characterize the various functional states of the chicken lysozyme gene. Nature 311:163–165CrossRefGoogle Scholar
  12. Fritton HP, Igo-Kemenes T, Nowock J, Strech-Jurk U, Theisen M, Sippel AE (1987) DNase I-hypersensitive sites in the chromatin structure of the lysozyme gene in steroid hormone target and non-target tissues. Biol Chem Hoppe-Seyler 368:111–119Google Scholar
  13. Guo B, Odgren PR, van Wijnen AJ, Last TJ, Nickerson J, Penman S, Lian JB, Stein JL, Stein GS (1995) The nuclear matrix protein NMP-1 is the transcription factor YY1. Proc Natl Acad Sci USA 92:10526–10530CrossRefGoogle Scholar
  14. Hyde-DeRuyscher RP, Jebbubgs E, Shenk T (1995) DNA binding sites for the transcriptional activator/repressor YY1. Nucl Acids Res 23:4457–4465CrossRefGoogle Scholar
  15. Inayoshi Y, Kaneoka H, Machida Y, Terajima M, Dohda T, Miyake K, Iijima S (2005) Repression of GR-mediated expression of the tryptophan oxygenase gene by the SWI/SNF complex during liver development. J Biochem 138:457–465CrossRefGoogle Scholar
  16. Kaye JS, Pratt-Kaye S, Bellard M, Dretzen G, Bellard F, Chambon P (1986) Steroid hormone dependence of four DNase I-hypersensitive regions located within the 7000-bp 5′-flanking segment of the ovalbumin gene. EMBO J 5:277–285Google Scholar
  17. Muramatsu T, Sanders MM (1995) Regulation of ovalbumin gene expression. Poult Avian Biol Rev 6:107–123Google Scholar
  18. Nishijima K, Ando M, Sano S, Hayashi-Ozawa A, Kinoshita Y, Iijima S (2005) Costimulation of T cell proliferation by anti-L-selectin antibody is associated with the reduction of a cdk inhibitor p27. Immunology 116:347–353CrossRefGoogle Scholar
  19. Pasqualini C, Guivarc’h D, Barnier J-V, Guibert B, Vincent J-D, Vernier P (2001) Differential subcellular distribution and transcriptional activity of ΣE3, ΣE4, and ΣE3–4 isoforms of the rat estrogen receptor-α. Mol Endrocrinol 15:894–908CrossRefGoogle Scholar
  20. Phi-Van L, Strätling WH (1988) The matrix attachment regions of the chicken lysozyme gene co-map with the boundaries of the chromatin domain. EMBO J 7:655–664Google Scholar
  21. Sanders MM, McKnight GS (1985) Chicken egg white genes: multihormonal regulation in a primary cell culture system. Mol Endocrinol 116:398–405Google Scholar
  22. Sanders MM, McKnight GS (1988) Positive and negative regulatory elements control the steroid-responsive ovalbumin promoter. Biochemistry 27:6550–6557CrossRefGoogle Scholar
  23. Shi Y, Lee J-S, Galvin KM (1997) Everything you have ever wanted to know about Yin Yang 1. Biochim Biophys Acta 1332:F49–F66Google Scholar
  24. Short ML, Nickel J, Schmitz A, Renkawitz R (1996) Lysozyme gene expression and regulation. EXS 75:243–257Google Scholar
  25. Spelsberg TC, Knowler JT, Moses HL (1974) Specific methods for the isolation of nuclei from chick oviduct. Methods Enzymol 31:263–279CrossRefGoogle Scholar
  26. Steiner C, Muller M, Baniahmad A, Renkawitz R (1987) Lysozyme gene activity in chicken macrophages is controlled by positive and negative regulatory elements. Nucl Acids Res 15:4163–4178CrossRefGoogle Scholar
  27. Sui G, Affar EB, Shi Y, Brignone C, Wall NR, Yin P, Donohoe M, Luke MP, Calvo D, Grossman SR, Shi Y (2004) Yin Yang 1 is a negative regulator of p53. Cell 117:859–872CrossRefGoogle Scholar
  28. Thomas MJ, Seto E (1999) Unlocking the mechanisms of transcription factor YY1: are chromatin modifying enzymes the key? Gene 236:197–208CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, B.V. 2006

Authors and Affiliations

  • Mahboob Morshed
    • 1
  • Munetoshi Ando
    • 1
  • Junko Yamamoto
    • 1
  • Akitsu Hotta
    • 1
  • Hidenori Kaneoka
    • 1
  • Jun Kojima
    • 1
  • Ken-ichi Nishijima
    • 1
  • Masamichi Kamihira
    • 2
  • Shinji Iijima
    • 1
  1. 1.Department of Biotechnology, Graduate School of EngineeringNagoya UniversityFuro-cho, Chikusa-kuJapan
  2. 2.Department of Chemical Engineering, Faculty of EngineeringKyushu UniversityMotooka, Nishi-kuJapan

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