TOWARDS UNDERSTANDING THE MECHANISMS OF EPIGENETIC REGULATION: PART 1. AN EVOLUTIONAL INSIGHT INTO PCG-MEDIATED GENE REPRESSION



Cite item

Full Text

Abstract

The evolutionary conserved PcG proteins maintain stable transcriptional epigenetic repression, established earlier by transiently acting regulator proteins. The exact mechanism of PcG-mediated repression is not identified yet, and here we outline existing models of the repression mechanism. We also shortly summarize the current knowledge about PcG proteins and their role in various processes and present an insight into the evolution of PRC1 and PRC2 complexes.

About the authors

Elena M Fedorova

I.P. Pavlov Institute of Physiology, RAS, Saint-Petersburg, RF

Email: ellena_fedorova@yahoo.com

Alexander V Rodionov

V. L. Komarov Botanical Institute RAS, Saint-Petersburg, RF

Email: avrodionov@mail.ru

References

  1. Bannister A.J., Zegerman P., Partridge J.F. et al., 2001. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain//Nature. Vol. 410. P. 120-124.
  2. Bantignies F., Grimaud C., Lavrov S. et al., 2003. Inheritance of Polycomb-dependent chromosomal interactions in Drosophila//Genes Dev. Vol. 17. P. 2406-2420.
  3. Bienz M., Mutter J., 1995. Transcriptional silencing of homeotic genes in Drosophila//Bioessays. Vol. 17. P. 775-784.
  4. Birve A., Sengupta A.K, Beuchle D. et al., 2001. Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants//Development. Vol. 128. P. 3371-3379.
  5. Boudreault A.A., Cronier D., Selleck W. et al., 2003. Yeast enhancer of polycomb defines global Esal-dependent acetylation of chromatin//Genes Dev. Vol. 17. P. 1415-1428.
  6. Boyer L.A., Plath K., Zeitlinger J. et al., 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells//Nature. Vol. 441. R 349-353.
  7. Bracken A.P., Dietrich N., Pasini D., et al., 2006. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions//Genes Dev. Vol. 20. P. 1123-1136.
  8. Breiling A., Bonte E., Ferrari S. et al., 1999. The Drosophila polycomb protein interacts with nucleosomal core particles in vitro via its repression domain//Mol Cell Biol. Vol. 19. P. 8451-8460.
  9. Breiling A., Sessa L., Orlando V., 2007. Biology of polycomb and trithorax group proteins//Int. Rev. Cytol.Vol. 258. P. 83-136.
  10. Brown J.L., Mucci D., Whiteley M. et al., 1998. The Drosophila Polycomb group gene pleiohomeotic encodes a DNA binding protein with homology to the transcription factor YY1//Mol Cell. Vol. 1. P. 1057-1064.
  11. Buchenau P., Hodgson J., Strutt H., Arndt-Jovin D. J., 1998. The distribution of polycomb-group proteins during cell division and development in Drosophila embryos: impact on models for silencing//J. Cell. Biol. Vol. 141. P. 469-481.
  12. Busturia file:///2.Busturia A., Wightman C.D., Sakonju S., 1997. A silencer is required for maintenance of transcriptional repression throughout Drosophila development // Development. Vol. 124. P. 4343-4350.
  13. Casares F., Sanchez-Herrero E., 1995. Regulation of the infraabdominal regions of the bithorax complex of Drosophila by gap genes//Development. Vol. 121. P. 1855-1866.
  14. Cavalli G., Paro R., 1998. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis//Cell. Vol. 93. P. 505-518.
  15. Ceol C.J., Horvitz H.R., 2004. A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling//Dev. Cell. Vol. 6. P. 563-576.
  16. Czermin В., Melfi R., McCabe D. et al., 2002. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites//Cell. Vol. 111. P. 185-196.
  17. Fedorova E., Sadoni N., Dahlsveen I.К. et al., 2008. The nuclear organization of Polycomb/rithorax group response elements in larval tissues of Drosophila melanogaster//Chromosome Res: in presss.
  18. Felsenfeld G., 1996. Chromatin unfolds//Cell. Vol. 86. P. 13-19.
  19. Ficz file:///9.Ficz G., Heintzmann R., Arndt-Jovin D.J., 2005. Polycomb group protein complexes exchange rapidly in living Drosophila // Development. Vol. 132. P. 3963-3976.
  20. Fischle W., Wang Y., Jacobs S. A. et al., 2003. Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains//Genes Dev. Vol. 17. P. 1870-1881.
  21. Francis N.J., Kingston R.E., 2001. Mechanisms of transcriptional memory//Nat Rev Mol Cell Biol. Vol. 2. P. 409-421.
  22. Francis N.J., Saurin A.J., Shao Z., Kingston R.E., 2001. Reconstitution of a functional core polycomb repressive complex//Mol Cell. Vol. 8. P. 545-556.
  23. Franke A., DeCamillis M., link D. et al., 1992. Polycomb and polyhomeotic are constituents of a multimeric protein complex in chromatin of Drosophila melanogaster//Embo J. Vol. 11. P. 2941 -2950.
  24. Glockner G., Eichinger E., Szafranski К. et al., 2002. Sequence and analysis of chromosome 2 of Dictyostelium discoideum//Nature. Vol.418. P. 79-85.
  25. Grimaud C., Bantignies F., Pal-Bhadra M. et al., 2006. RNAi components are required for nuclear clustering of Polycomb group response elements//Cell. Vol. 124. P. 957-971.
  26. Ingham P.W., Martinez Arias A., 1992. Boundaries and fields in early embryos//Cell. Vol. 68. P. 221-235.
  27. IsonoK., Fujimura Y., ShingaJ. et al., 2005. Mammalian polyhomeotic homologues Phc2 and Phc 1 act in synergy to mediate polycomb repression of Hox genes//Mol. Cell. Biol. Vol. 25. P. 6694-6706.
  28. Jacobs J.J., van Lohuizen M., 2002. Polycomb repression: from cellular memory to cellular proliferation and cancer//Biochim Biophys Acta. Vol. 1602. P. 151-161.
  29. Keeling P.J., Burger G., Durnford D.G. et al., 2005. The tree of eukaryotes//Trends Ecol Evol. Vol. 20. P. 670-676.
  30. Ketel C.S., Andersen E.F., Vargas M.L. et al., 2005. Subunit contributions to histone methyltransferase activities of fly and worm polycomb group complexes//Mol Cell Biol. Vol. 25. P. 6857-6868.
  31. Klymenko Т., Рарр В., Fischle W. et al., 2006. A Polycomb group protein complex with sequence-specific DNA-binding and selective methyl-lysine-binding activities//Genes Dev. Vol. 20. P. 1110-1122.
  32. Koonin E.V., Zhou S., Lucchesi J.C., 1995. The chromo superfamily: new members, duplication of the chromo domain and possible role in delivering transcription regulators to chromatin//Nucleic Acids Res. Vol. 23. P. 4229-4233.
  33. Korf I., Fan Y., Strome S., 1998. The Polycomb group in Caenorhabditis elegans and maternal control of germline development//Development. Vol. 125. P. 2469-2478.
  34. Kuzmichev A., Margueron R., Vaquero A. et al., 2005. Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation//Proc Natl Acad Sci USA. Vol. 102. P. 1859-1864.
  35. Lachner M., O'Carroll D., Rea S. et al., 2001. Methylation of histone H3 lysine 9 creates a binding site for HP 1 proteins//Nature. Vol. 410. P. 116-120.
  36. Lee T.I., Jenner R.G., Boyer E.A. et al., 2006. Control of developmental regulators by Polycomb in human embryonic stem cells//Cell. Vol. 125. P. 301-313.
  37. Levine S.S., Weiss A., Erdjument-Bromage H. et al., 2002. The core of the polycomb repressive complex is compositionally and functionally conserved in flies and humans//Mol Cell Biol. Vol. 22. P. 6070-6078.
  38. Liu Y., Taverna S.D., Muratore T.L. et al., 2007. RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena//Genes Dev. Vol. 21. P. 1530-1545.
  39. Eoftus B.J., Fung E., Roncaglia P. et al., 2005. The genome of the basidiomycetous yeast and human pathogen Cryptococcus neoformans//Science. Vol. 307. P. 1321-1324.
  40. Makarevich G., Leroy O., Akinci U. et al., 2006. Different Polycomb group complexes regulate common target genes in Arabidopsis//EMBO Rep. Vol. 7. P. 947-952.
  41. Martinez A.M., Cavalli G., 2006. The role of polycomb group proteins in cell cycle regulation during development//Cell. Cycle. Vol. 5. P. 1189-1197.
  42. Messmer file:///2.Messmer S., Franke A., Paro R., 1992. Analysis of the functional role of the Polycomb chromo domain in Drosophila melanogaster // Genes Dev. Vol. 6. P. 1241-1254.
  43. Muller J., Hart C.M., Francis N.J. et al., 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex//Cell. Vol. 111. P. 197-208.
  44. Muller J., Kassis J.A., 2006. Polycomb response elements and targeting of Polycomb group proteins in Drosophila//Curr. Opin. Genet. Dev. Vol. 16. P. 476-484.
  45. Nekrasov M., Wild В., Muller J., 2005. Nucleosome binding and histone methyltransferase activity of Drosophila PRC2//EMBO Rep. Vol. 6. P. 348-353.
  46. Ng J., Hart C.M., Morgan K., Simon J.A., 2000. A Drosophila ESC-E(Z) protein complex is distinct from other polycomb group complexes and contains covalently modified ESC//Mol. Cell Biol. Vol. 20. P. 3069-3078.
  47. Orlando V., 2003. Polycomb, epigenomes and control of cell identity//Cell. Vol. 112. P. 599-606.
  48. Paro R., Harte P.J., 1996. The role of Polycomb group and trithorax group chromatin complexes in the maintenance of determined cell states//Epigenetic Mechanisms of Gene Regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.-Y. P. 507-528.
  49. Paro R., Hogness D.S., 1991. The Polycomb protein shares a homologous domain with a heterochromatin-associated protein of Drosophila//Proc. Natl. Acad. Sci. USA. Vol. 88. P. 263-267.
  50. Petrino T.R., Lin Y.-W.P., Packed G.R. et al., 2001. Cloning and Sequencing of Zebrafish (Danio rerio) Polycomb Gene. Unpublished.
  51. Pirrotta V., 1995. Chromatin complexes regulating gene expression in Drosophila//Curr. Opin. Genet. Dev. Vol. 5. P. 466-472.
  52. Pirrotta V., 1998. Polycombing the genome: PcG, trxG, and chromatin silencing//Cell. Vol. 93. P. 333-336.
  53. Rastelli L., Chan C.S., Pirrotta V., 1993. Related chromosome binding sites for zeste, suppressors of zeste and Polycomb group proteins in Drosophila and their dependence on Enhancer of zeste function//EmboJ.Vol. 12. P. 1513-1522.
  54. Ringrose L., Paro R., 2004. Epigenetic regulation of cellular memory by the Polycomb and Trithorax group proteins//Annu. Rev. Genet. Vol. 38. P. 413-443.
  55. Ringrose L., Paro R., 2007. Polycomb/Trithorax response elements and epigenetic memory of cell identity//Development. Vol. 134. P. 223-232.
  56. Ringrose L., Rehmsmeier M., Dura J.M., Paro R., 2003. Genome-wide prediction of Polycomb/Trithorax response elements in Drosophila melanogaster//Dev. Cell. Vol. 5. P. 759-771.
  57. Roger A.J., Hug L.A., 2006. The origin and diversification of eukaryotes: problems with molecular phyogenetics and molecular clock estimation//Philos. Trans. R. Soc. Lond. B. Biol. Sci. Vol. 361. P. 1039-1054.
  58. Rybakina E., 2006. Nuclear positioning and functional regulation of endogenous genes and transgenes in the fruit fly Drosophila melanogaster and in mammalian cells//Fakultat fur Biologie LMU Munchen, Munchen. 176 p.
  59. Saleh A., Al-Abdallat A., Ndamukong I. et al., 2007. The Arabidopsis homologs of trithorax (ATX1) and enhancer of zeste (CLF) establish 'bivalent chromatin marks' at the silent AGAMOUS locus//Nucleic Acids Res. Vol. 35. P. 6290-6296.
  60. Satijn D.P., Hamer К.M., den Blaauwen J., Otte A.P., 2001. The polycomb group protein EED interacts with YY1, and both proteins induce neural tissue in Xenopus embryos//Mol. Cell Biol. Vol. 21. P. 1360-1369.
  61. Saurin A.J., Shao Z., Erdjument-Bromage H. et al., 2001. A Drosophila Polycomb group complex includes Zeste and dTAFII proteins//Nature. Vol. 412. P. 655-660.
  62. Schubert D., Clarenz O., Goodrich J., 2005. Epigenetic control of plant development by Polycomb-group proteins//Curr Opin Plant Biol. Vol. 8. P. 553-561.
  63. Schwartz Y.В., Pirrotta V., 2007. Polycomb silencing mechanisms and the management of genomic programmes//Nat Rev Genet. Vol. 8. P. 9-22.
  64. Sengupta A.K., Kuhrs A., Muller J., 2004. General transcriptional silencing by a Polycomb response element in Drosophila//Development. Vol. 131. P. 1959-1965.
  65. Shao Z., Raible F., Mollaaghababa R. et al., 1999.Stabilization of chromatin structure by PRC1, a Polycomb complex//Cell. Vol. 98. P. 37-46.
  66. Shimono Y., Murakami H., Hasegawa Y., Takahashi M., 2000.RET finger protein is a transcriptional repressor and interacts with enhancer of polycomb that has dual transcriptional functions//J. Biol. Chem. Vol. 275. P. 39411-39419.
  67. Simon J.A., Tamkun J.W., 2002. Programming off and on states in chromatin: mechanisms of Polycomb and trithorax group complexes//Curr Opin Genet Dev. Vol. 12. P. 210-218.
  68. Stankunas K., Berger J., Ruse С. et al., 1998. The enhancer of polycomb gene of Drosophila encodes a chromatin protein conserved in yeast and mammals//Development. Vol. 125. P. 4055-4066.
  69. Strouboulis J., Damjanovski S., Vermaak D. et al., 1999. Transcriptional repression by XPcl, a new Polycomb homolog in Xenopus laevis embryos, is independent of histone deacetylase//Mol. Cell Biol. Vol. 19. P. 3958-3968.
  70. Sun Y.A.Z., 2005. A unified mode of epigenetic gene silencing//RNA Biology. Vol. 2. P. e8-e 10.
  71. Thakur J.K., Malik M.R., Bhatt V. et al., 2003. A POLYCOMB group gene of rice (Oryza sativa L. subspecies indica), OsiEZl, codes for a nuclear-localized protein expressed preferentially in young seedlings and during reproductive development//Gene. Vol. 314. P. 1-13.
  72. Tie F., Furuyama Т., Prasad-Sinha J. et al., 2001.The Drosophila Polycomb Group proteins ESC and E(Z) are present in a complex containing the histone-binding protein p55 and the histone deacetylase RPD3//Development. Vol. 128. P. 275-286.
  73. Vazquez J., Muller M., Pirrotta V., Sedat J.W., 2006. The Мер element mediates stable long-range chromosome-chromosome interactions in Drosophila//Mol. Biol. Cell. Vol. 17. P. 2158-2165.
  74. Wakimoto В.Т., 1998. Beyond the nucleosome: epigenetic aspects of position-effect variegation in Drosophila//Cell. Vol. 93. P. 321-324.
  75. Wang D., Tyson M.D., Jackson S.S., Yadegari R., 2006. Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in 73. 73. Arabidopsis//Proc. Natl. Acad. Sci. USA. Vol. 103. P. 13244-13249.
  76. Wang L., Brown J.L., Cao R. et al., 2004. Hierarchical recruitment of polycomb group silencing complexes//Mol. Cell. Vol. 14. P. 637-646.
  77. Whitcomb S.J., Basu A., Allis С.D., Bernstein E., 2007. Polycomb Group proteins: an evolutionary perspective//Trends Genet. Vol. 23. P. 494-502.
  78. Yang Y., Sun Y., Luo X. et al., 2007. Polycomb-like genes are necessary for specification of dopaminergic and serotonergic neurons in Caenorhabditis elegans//Proc. Natl. Acad. Sci. USA. Vol. 104. P. 852-857.
  79. link В., Раro R., 1989. In vivo binding pattern of a trans-regulator of homoeotic genes in Drosophila melanogaster//Nature. Vol. 337. P. 468-471.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2008 Fedorova E.M., Rodionov A.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 65617 от 04.05.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies