Molecular Biology

, Volume 52, Issue 5, pp 637–647 | Cite as

HMGB Proteins as DNA Chaperones That Modulate Chromatin Activity

  • A. L. Kozlova
  • M. E. Valieva
  • N. V. Maluchenko
  • V. M. Studitsky


HMGB proteins are involved in structural rearrangements caused by regulatory chromatin remodeling factors. Particular interest is attracted to a DNA chaperone mechanism, suggesting that the HMGB proteins introduce bends into the double helix, thus rendering DNA accessible to effector proteins and facilitating their activity. The review discusses the role that the HMBG proteins play in key intranuclear processes, including assembly of the preinitiation complex during transcription of ribosomal genes; transcription by RNA polymerases I, II, and III; recruitment of the SWI/SNF complex during transcription of nonribosomal genes; DNA repair; etc. The functions of the HMGB proteins are considered in detail with the examples of yeast HMO1 and NHP6. The two proteins possess unique features in adition to properties characteristic of the HMGB proteins. Thus, NHP6 stimulates a large-scale ATP-independent unwrapping of nucleosomal DNA by the FACT complex, while in its absence FACT stabilizes the nucleosome. HMO1 acts as an alternative linker histone. Both HMO1 and NHP6 are of applied interest primarly because they are homologs of human HMGB1, an important therapeutic target of anticancer and anti-inflammatory treatments.


chromatin nucleosome transcription transcription factors HMGB proteins HMO1 NHP6 HMGB1 SPT16 POB3 FACT 



This work was supported by the Russian Science Foundation (project no. 14-24-00031).


  1. 1.
    John E.W. 1985. The HMG Chromosomal Proteins. London: Academic.Google Scholar
  2. 2.
    Bustin M., Reeves R. 1996. HMG chromosomal proteins: Architectural components that facilitate chromatin function. Prog. Nucl. Acids Res. Mol. Biol. 54, 35–100.CrossRefGoogle Scholar
  3. 3.
    Aravind L., Landsman D. 1998. AT-hook motifs identified in a wide variety of DNA binding proteins. Nucleic Acids Res. 26, 4413.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bustin M. 2001. Chromatin unfolding and activation by HMGN chromosomal proteins. Trends Biochem. Sci. 26 (7), 431–437.CrossRefPubMedGoogle Scholar
  5. 5.
    Körner U., Bustin M., Scheer U., Hock R. 2003. Developmental role of HMGN proteins in Xenopus laevis. Mech. Dev. 120 (10), 1177–1192.CrossRefPubMedGoogle Scholar
  6. 6.
    Bradbury E.M. 2002. Chromatin structure and dynamics: State-of-the-art. Mol. Cell. 10 (1), 13–19.Google Scholar
  7. 7.
    Grosschedl R., Giese K., Pagel J. 1994. HMG domain proteins: Architectural elements in the assembly of nucleoprotein structures. Trends Genet. 10 (3), 94–100.CrossRefPubMedGoogle Scholar
  8. 8.
    Štros M. 2010. HMGB proteins: interactions with DNA and chromatin. Biochim. Biophys. Acta. 1799 (1), 101–113.Google Scholar
  9. 9.
    Joshi S.R., Sarpong Y.C., Peterson R.C., Scovell W.M. 2012. Nucleosome dynamics: HMGB1 relaxes canonical nucleosome structure to facilitate estrogen receptor binding. Nucleic Acids Res. 40 (20), 10 161–10 171.CrossRefGoogle Scholar
  10. 10.
    Phair R.D., Scaffidi P., Elbi C., Vecerová J., Dey A., Ozato K., Misteli T. 2004. Global nature of dynamic protein–chromatin interactions in vivo: Three-dimensional genome scanning and dynamic interaction networks of chromatin proteins. Mol. Cell. Biol. 24 (14), 6393–6402.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Reeves R. 2015. High mobility group (HMG. proteins: Modulators of chromatin structure and DNA repair in mammalian cells. DNA Repair (Amst.). 36, 122–136.CrossRefGoogle Scholar
  12. 12.
    Agresti A., Bianchi M.E. 2003. HMGB proteins and gene expression. Curr. Opin. Genet. Dev. 13 (2), 170–178.CrossRefPubMedGoogle Scholar
  13. 13.
    Bustin M., Catez F., Lim J.H. 2005. The dynamics of histone H1 function in chromatin. Mol. Cell. 17 (5), 617–620.CrossRefPubMedGoogle Scholar
  14. 14.
    Das D., Scovell W.M. 2001. The binding interaction of HMG-1 with the TATA-binding protein/TATA complex. J. Biol. Chem. 276 (35), 32 597–32 605.CrossRefGoogle Scholar
  15. 15.
    McKinney K., Prives C. 2002. Efficient specific DNA binding by p53 requires both its central and C-terminal domains as revealed by studies with high-mobility group 1 protein. Mol. Cell. Biol. 22 (19), 6797–6808.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Valieva M.E., Armeev G.A., Kudryashova K.S., Gerasimova  N.S., Shaytan A.K., Kulaeva O.I., McCullough L.L., Formosa T., Georgiev P.G., Kirpichnikov M.P., Studitsky V.M., Feofanov A.V. 2016. Large-scale ATP-independent nucleosome unfolding by a histone chaperone. Nat. Struct. Mol. Biol. 23, 1111–1116.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Valieva M.E., Gerasimova N.S., Kudryashova K.S., Kozlova A.L., Kirpichnikov M.P., Hu Q., Botuyan M.V., Mer G., Feofanov A.V., Studitsky V.M. 2017. Stabilization of nucleosomes by histone tails and by FACT revealed by spFRET microscopy. Cancers (Basel). 9 (1), 3.CrossRefPubMedCentralGoogle Scholar
  18. 18.
    Formosa T., Eriksson P., Wittmeyer J., Ginn J., Yu Y., Stillman D.J. 2001. Spt16-Pob3 and the HMG protein NHP6 combine to form the nucleosome-binding factor SPN. EMBO J. 20, 3506–3517.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Ruone S., Rhoades A.R., Formosa T. 2003. Multiple NHP6 molecules are required to recruit Spt16-Pob3 to form yFACT complexes and to reorganize nucleosomes. J. Biol. Chem. 278, 45 288–45 295.CrossRefGoogle Scholar
  20. 20.
    Erkina T.Y., Erkine A. 2015. ASF1 and the SWI/SNF complex interact functionally during nucleosome displacement, while FACT is required for nucleosome reassembly at yeast heat shock gene promoters during sustained stress. Cell. Stress Chaperones. 20 (2), 355–369.CrossRefPubMedGoogle Scholar
  21. 21.
    Kamau E., Bauerle K.T., Grove A. 2004. The Saccharomyces cerevisiae high mobility group box protein HMO1 contains two functional DNA binding domains. J. Biol. Chem. 279 (53), 55 234–55 240.CrossRefGoogle Scholar
  22. 22.
    Panday A., Grove A. 2016. Yeast HMO1: Linker histone reinvented. Microbiol. Mol. Biol. Rev. 81 (1), e00037-16.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Kulak N.A., Pichler G., Paron I., Nagaraj N., Mann M. 2014. Minimal, encapsulated proteomic-sample processing applied to copy-number estimation in eukaryotic cells. Nat. Methods. 11 (3), 319–324.CrossRefPubMedGoogle Scholar
  24. 24.
    Ghaemmaghami S., Huh W.K., Bower K., Howson R.W., Belle A., Dephoure N., O’Shea E.K., Weissman J.S. 2003. Global analysis of protein expression in yeast. Nature. 425 (6959), 737–741.CrossRefPubMedGoogle Scholar
  25. 25.
    Bauerle K.T., Kamau E., Grove A. 2006. Interactions between N- and C-terminal domains of the Saccharomyces cerevisiae high-mobility group protein HMO1 are required for DNA bending. Biochemistry. 45 (11), 3635–3645.CrossRefPubMedGoogle Scholar
  26. 26.
    Murugesapillai D., McCauley M.J., Huo R., Nelson Holte M.H., Stepanyants A., Maher L.J., Israeloff N.E., Williams M.C. 2014. DNA bridging and looping by HMO1 provides a mechanism for stabilizing nucleosome-free chromatin. Nucleic Acids Res. 42 (14), 8996–9004.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Xiao L., Williams A.M., Grove A. 2010. The C-terminal domain of yeast high mobility group protein HMO1 mediates lateral protein accretion and in-phase DNA bending. Biochemistry. 49 (19), 4051–4059.CrossRefPubMedGoogle Scholar
  28. 28.
    Hepp M.I., Alarcon V., Dutta A., Workman J.L., Gu-tiérrez J.L. 2014. Nucleosome remodeling by the SWI/SNF complex is enhanced by yeast High Mobility Group Box (HMGB) proteins. Biochim. Biophys. Acta. 1839 (9), 764–772.Google Scholar
  29. 29.
    Stillman D.J. 2010. NHP6: A small but powerful effector of chromatin structure in Saccharomyces cerevisiae. Biochim. Biophys. Acta. 1799 (1–2), 175–180.Google Scholar
  30. 30.
    Kuehl L., Salmond B., Tran L. 1984. Concentrations of high-mobility-group proteins in the nucleus and cytoplasm of several rat tissues. J. Cell. Biol. 99, 648–654.CrossRefPubMedGoogle Scholar
  31. 31.
    Masse J.E., Wong B., Yen Y.M., Allain F.H.T., Johnson R.C., Feigon J. 2002. The S. cerevisiae architectural HMGB protein NHP6A complexed with DNA: DNA and protein conformational changes upon binding. J. Mol. Biol. 323 (2), 263–284.CrossRefPubMedGoogle Scholar
  32. 32.
    Yen Y.M., Roberts P.M., Johnson R.C. 2001. Nuclear localization of the Saccharomyces cerevisiae HMG protein NHP6A occurs by a Ran-independent nonclassical pathway. Traffic. 2 (7), 449–464.CrossRefPubMedGoogle Scholar
  33. 33.
    Kotani T., Miyake T., Tsukihashi Y., Hinnebusch A.G., Nakatani Y., Kawaichi M., Kokubo T. 1998. Identification of highly conserved amino-terminal segments of dTAFII230 and yTAFII145 that are functionally interchangeable for inhibiting TBP–DNA interactions in vitro and in promoting yeast cell growth in vivo. J. Biol. Chem. 273 (48), 32 254–32 264.CrossRefGoogle Scholar
  34. 34.
    Kasahara K., Ohyama Y., Kokubo T. 2011. Hmo1 directs pre-initiation complex assembly to an appropriate site on its target gene promoters by masking a nucleosome-free region. Nucleic Acids Res. 39 (10), 4136–4150.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Kasahara K., Ki S., Aoyama K., Takahashi H., Kokubo T. 2008. Saccharomyces cerevisiae HMO1 interacts with TFIID and participates in start site selection by RNA polymerase II. Nucleic Acids Res. 36 (4), 1343–1357.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Panday A., Xiao L., Grove A. 2015. Yeast high mobility group protein HMO1 stabilizes chromatin and is evicted during repair of DNA double strand breaks. Nucleic Acids Res. 43 (12), 5759–5770.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Hepp M.I., Smolle M., Gidi C., Amigo R., Valenzuela N., Arriagada A., Marureira A., Gogol MM., Torrejon M., Workman JL., Gutiérrez JL. 2017. Role of NHP6 and Hmo1 in SWI/SNF occupancy and nucleosome landscape at gene regulatory regions. Biochim. Biophys. Acta. 1860 (3), 316–326.Google Scholar
  38. 38.
    Hsieh F.K., Kulaeva O.I., Studitsky V.M. 2015. Experimental analysis of hFACT action during Pol II transcription in vitro. Methods Mol. Biol. 1276, 315–326.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Singer R.A., Johnston G.C. 2004. The FACT chromatin modulator: Genetic and structure/function relationships. Biochem. Cell. Biol. 82 (4), 419–427.CrossRefPubMedGoogle Scholar
  40. 40.
    Szerlong H., Saha A., Cairns B.R. 2003. The nuclear actin-related proteins Arp7 and Arp9: A dimeric module that cooperates with architectural proteins for chromatin remodeling. EMBO J. 22 (12), 3175–3187.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Hsieh F.K., Kozlova A.L., Gerasimova N.S., Kotova E.U., Formosa T., Studitsky V.M. 2017. Role of the Nhp6 protein in in vitro transcription through the nucleosome. Moscow Univ. Biol. Sci. Bull. 72 (4), 253–257.CrossRefGoogle Scholar
  42. 42.
    Dowell N.L., Sperling A.S., Mason M.J., Johnson R.C. 2010. Chromatin-dependent binding of the S. cerevisiae HMGB protein NHP6A affects nucleosome dynamics and transcription. Genes Dev. 24 (18), 2031–2042.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Lu J., Kobayashi R., Brill S.J. 1996. Characterization of a high mobility group 1/2 homolog in yeast. J. Biol. Chem. 271 (52), 33 678–33 685.CrossRefGoogle Scholar
  44. 44.
    Gonzalez-Huici V., Szakal B., Urulangodi M., Psakhye I., Castellucci F., Menolfi D., Raiakumara E., Fumasoni M., Bermejo R., Jentsch S., Branzei D. 2014. DNA bending facilitates the error-free DNA damage tolerance pathway and upholds genome integrity. EMBO J. 33 (4), 327–340.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Panday A., Grove A. 2016. The high mobility group protein HMO1 functions as a linker histone in yeast. Epigenetics Chromatin. 9 (1), 13.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Usdin K., House N.C., Freudenreich C.H. 2015. Repeat instability during DNA repair: Insights from model systems. Crit. Rev. Biochem. Mol. Biol. 50, 142–167.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kim H., Livingston D.M. 2006). A high mobility group protein binds to long CAG repeat tracts and establishes their chromatin organization in Saccharomyces cerevisiae. J Biol Chem. 281, 15 735–15 740.CrossRefGoogle Scholar
  48. 48.
    Jackson S.P., Bartek J. 2009. The DNA-damage response in human biology and disease. Nature. 461 (7267), 1071–1078.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Alekseev S.Y., Kovaltsova S.V., Fedorova I.V., Gracheva L.M., Evstukhina T.A., Peshekhonov V.T., Korolev V.G. 2002. HSM2 (HMO1) gene participates in mutagenesis control in yeast Saccharomyces cerevisiae. DNA Repair (Amst.). 1 (4), 287–297.CrossRefGoogle Scholar
  50. 50.
    Biswas D., Imbalzano A.N., Eriksson P., Yu Y., Stillman D.J. 2004. Role for NHP6, Gcn5, and the SWI/SNF complex in stimulating formation of the TATA-binding protein–TFIIA–DNA complex. Mol. Cell. Biol. 24, 8312–8321.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Brewster N.K., Johnston G.C., Singer R.A. 1998. Characterization of the CP complex, an abundant dimer of Cdc68 and Pob3 proteins that regulates yeast transcriptional activation and chromatin repression. J. Biol. Chem. 273, 21 972–21 979.CrossRefGoogle Scholar
  52. 52.
    Yu Y., Eriksson P., Stillman D.J. 2000. Architectural transcription factors and the SAGA complex function in parallel pathways to activate transcription. Mol. Cell. Biol. 20, 2350–2357.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Celona B., Weiner A., Di Felice F., Mancuso F.M., Cesarini E., Rossi R.L., Gregory L., Baban D., Rossetti G., Pagani M., Bonaldi T., Ragoussis J., Friedman N., Camilloni G., Bianchi M.E., Agresti A. 2011. Substantial histone reduction modulates genome-wide nucleosomal occupancy and global transcriptional output. PLoS Biol. 9 (6), e1001086.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Hu P., Wang D., Cassidy M.J., Stanier S.A. 2014. Predicting the resistance profile of a spudcan penetrating sand overlying clay. Can. Geotech. J. 51 (10), 1151–1164.CrossRefGoogle Scholar
  55. 55.
    Feser J., Truong D., Das C., Carson J.J., Kieft J., Harkness T., Tyler J.K. 2010. Elevated histone expression promotes life span extension. Mol. Cell. 39 (5), 724–735.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Durano D., Lukacs A., Di Felice F., Micheli G., Camilloni G. 2017. A novel role for Nhp6 proteins in histone gene regulation in Saccharomyces cerevisiae. Int. J. Biochem. Cell Biol. 83, 76–83.CrossRefPubMedGoogle Scholar
  57. 57.
    Bajpai G., Jain I., Inamdar M.M., Das D., Padinhateeri R. 2017. Binding of DNA-bending non-histone proteins destabilizes regular 30-nm chromatin structure. PLoS Comput. Biol. 13 (1), e1005365.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Widom J., Klug A. 1985. Structure of the 3000 Å chromatin filament: X-ray diffraction from oriented samples. Cell. 43 (1), 207–213.CrossRefPubMedGoogle Scholar
  59. 59.
    Finch J.T., Klug A. 1976. Solenoidal model for superstructure in chromatin. Proc. Natl. Acad. Sci. U. S. A. 73 (6), 1897–1901.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Robinson P.J., Fairall L., Huynh V.A., Rhodes D. 2006. EM measurements define the dimensions of the “30-nm” chromatin fiber: evidence for a compact, interdigitated structure. Proc. Natl. Acad. Sci. U. S. A. 103 (17), 6506–6511.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Gerchman S.E., Ramakrishnan V. 1987. Chromatin higher-order structure studied by neutron scattering and scanning transmission electron microscopy. Proc. Natl. Acad. Sci. U. S. A. 84 (22), 7802–7806.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Van Holde K., Zlatanova J. 1995. Chromatin higher order structure: Chasing a mirage? J. Biol. Chem. 270 (15), 8373–8376.CrossRefPubMedGoogle Scholar
  63. 63.
    Maeshima K., Hihara S., Eltsov M. 2010. Chromatin structure: Does the 30-nm fibre exist in vivo? Curr. Opin. Cell Biol. 22 (3), 291–297.CrossRefPubMedGoogle Scholar
  64. 64.
    Fussner E., Ching R.W., Bazett-Jones D.P. 2011. Living without 30 nm chromatin fibers. Trends Biochem. Sci. 36 (1), 1–6.CrossRefPubMedGoogle Scholar
  65. 65.
    Razin S.V., Gavrilov A.A. 2014. Chromatin without the 30-nm fiber: Constrained disorder instead of hierarchical folding. Epigenetics. 9 (5), 653–657.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Hall D.B., Wade J.T., Struhl K. 2006. An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae. Mol. Cell. Biol. 26 (9), 3672–3679.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Gadal O., Labarre S., Boschiero C., Thuriaux P. 2002. Hmo1, an HMG-box protein, belongs to the yeast ribosomal DNA transcription system. EMBO J. 21 (20), 5498–5507.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Albert B., Colleran C., Léger-Silvestre I., Berger A.B., Dez C., Normand C., Perez-Fernandes J., McStay B., Gadal O. 2013. Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human. Nucleic Acids Res. 41 (22), 10 135–10 149.CrossRefGoogle Scholar
  69. 69.
    Costigan C., Kolodrubetz D., Snyder M. 1994. NHP6A and NHP6B, which encode HMG1-like proteins, are candidates for downstream components of the yeast SLT2 mitogen-activated protein kinase pathway. Mol. Cell. Biol. 14, 2391–2403.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Wong B., Masse J.E., Yen Y.M., Giannikoupolous P., Feigon J., Johnson R.C. 2002. Binding to cisplatin-modified DNA by the Saccharomyces cerevisiae HMGB protein NHP6A. Biochemistry. 41 (17), 5404–5414.CrossRefPubMedGoogle Scholar
  71. 71.
    Brewster N.K., Johnston G.C., Singer R.A. 2001. A bipartite yeast SSRP1 analog comprised of Pob3 and NHP6 proteins modulates transcription. Mol. Cell. Biol. 21 (10), 3491–3502.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Formosa T. 2012. The role of FACT in making and breaking nucleosomes. Biochim. Biophys. Acta. 1819 (3), 247–255.Google Scholar
  73. 73.
    Hondele M., Ladurner A.G. 2013. Catch me if you can: How the histone chaperone FACT capitalizes on nucleosome breathing. Nucleus. 4 (6), 443–449.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Tsunaka Y., Fujiwara Y., Oyama T., Hirose S., Morikawa K. 2016. Integrated molecular mechanism directing nucleosome reorganization by human FACT. Genes Dev. 30 (6), 673–686.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Xin H., Takahata S., Blanksma M., McCullough L., Stillman DJ., Formosa T. 2009. yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol. Cell. 35, 365–376.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Rhoades A.R., Ruone S., Formosa T. 2004. Structural features of nucleosomes reorganized by yeast FACT and its HMG box component, NHP6. Mol. Cell. Biol. 24 (9), 3907–3917.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Hsieh F.K., Kulaeva O.I., Patel S.S., Dyer P.N, Luger K., Reinberg D., Studitsky V.M. 2013. Histone chaperone FACT action during transcription through chromatin by RNA polymerase II. Proc. Natl. Acad. Sci. U. S. A. 19, 7654–7659.CrossRefGoogle Scholar
  78. 78.
    Orphanides G., Wu W.H., Lane WS., Hampsey M., Reinberg D. 1999. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature. 400, 284–288.CrossRefPubMedGoogle Scholar
  79. 79.
    Belotserkovskaya R., Oh S., Bondarenko V.A., Orphanides G., Studitsky V.M., Reinberg D. 2003. FACT facilitates transcription-dependent nucleosome alteration. Science. 301, 1090–1093.CrossRefPubMedGoogle Scholar
  80. 80.
    Kurat C.F., Yeeles J.T., Patel H., Early A., Diffley J.F. 2017. Chromatin controls DNA replication origin selection, lagging-strand synthesis, and replication fork rates. Mol. Cell. 65 (1), 117–130.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Yang J., Zhang X., Feng J., Leng H., Li S., Xiao J., Lui S., Xu Z., Xu J., Li D., Li Q., Wang J., Wang, Z. 2016. The histone chaperone FACT contributes to DNA replication-coupled nucleosome assembly. Cell Rep. 14 (5), 1128–1141.CrossRefPubMedGoogle Scholar
  82. 82.
    Evans D.R., Brewster N.K., Xu Q., Rowley A., Altheim B.A., Johnston G.C., Singer R.A. 1998. The yeast protein complex containing cdc68 and pob3 mediates core-promoter repression through the cdc68 N-terminal domain. Genetics. 150 (4), 1393–1405.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Malone E.A., Clark C.D., Chiang A., Winston F.R.E.D. 1991. Mutations in SPT16/CDC68 suppress cis-and trans-acting mutations that affect promoter function in Saccharomyces cerevisiae. Mol. Cell. Biol. 11 (11), 5710–5717.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Schlesinger M.B., Formosa T. 2000. POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics. 155, 1593–1606.PubMedPubMedCentralGoogle Scholar
  85. 85.
    Hainer S.J., Pruneski J.A., Mitchell R.D., Monteverde R.M., Martens J.A. 2011. Intergenic transcription causes repression by directing nucleosome assembly. Genes Dev. 25, 29–40.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Jamai A., Puglisi A., Strubin M. 2009. Histone chaperone spt16 promotes redeposition of the original h3-h4 histones evicted by elongating RNA polymerase. Mol. Cell. 35, 377–383.CrossRefPubMedGoogle Scholar
  87. 87.
    Foltz D.R., Jansen L.E., Black B.E., Bailey A.O., Yates J.R., Cleveland D.W. 2006. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell. Biol. 8, 458–469.CrossRefPubMedGoogle Scholar
  88. 88.
    Prendergast L., Muller S., Liu Y., Huang H., Dingli F., Loew D., Vassias I., Patel D.J., Sullivan K.F., Almouzni G. 2016. The CENP-T/-W complex is a binding partner of the histone chaperone FACT. Genes Dev. 30, 1313–1326.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Wittmeyer J., Formosa T. 1997)The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein. Mol. Cell. Biol. 17, 4178–4190.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Bonaldi T., Langst G., Strohner R., Becker P.B., Bianchi M.E. 2002. The DNA chaperone HMGB1 facilitates ACF/CHRAC-dependent nucleosome sliding. EMBO J. 21, 6865–6873.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Travers A.A., Ner S.S., Churchill M.E. 1994. DNA chaperones: A solution to a persistence problem? Cell. 77, 167–169.CrossRefPubMedGoogle Scholar
  92. 92.
    Kolodrubetz D., Burgum A. 1990. Duplicated NHP6 genes of Saccharomyces cerevisiae encode proteins homologous to bovine high mobility group protein 1. J. Biol. Chem. 265, 3234–3239.PubMedGoogle Scholar
  93. 93.
    Chertkov O.V., Valieva M.E., Malyuchenko N.V., Feofanov A.V. 2017. Analysis of nucleosome structure in polyacrylamide gel by the Förster resonance energy transfer method Moscow Univ. Biol. Sci. Bull. 72, 196–200.CrossRefGoogle Scholar
  94. 94.
    Ugrinova I., Pasheva E. 2016. HMGB1 protein: A therapeutic target inside and outside the cell. Adv. Protein Chem. Struct. Biol. 107, 37–76.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  1. 1.Biological Faculty, Moscow State UniversityMoscowRussia
  2. 2.Cancer Epigenetics Program, Fox Chase Cancer CenterPhiladelphiaUSA

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