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PMID: 23446052 Published · epublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

The role of the nucleosome acidic patch in modulating higher order chromatin structure.

Journal of the Royal Society, Interface ·Vol. 10 ·No. 82 ·2013-05-06 ·Pages 20121022

Kalashnikova AA, Porter-Goff ME, Muthurajan UM, Luger K, Hansen JC

Abstract

Higher order folding of chromatin fibre is mediated by interactions of the histone H4 N-terminal tail domains with neighbouring nucleosomes. Mechanistically, the H4 tails of one nucleosome bind to the acidic patch region on the surface of adjacent nucleosomes, causing fibre compaction. The functionality of the chromatin fibre can be modified by proteins that interact with the nucleosome. The co-structures of five different proteins with the nucleosome (LANA, IL-33, RCC1, Sir3 and HMGN2) recently have been examined by experimental and computational studies. Interestingly, each of these proteins displays steric, ionic and hydrogen bond complementarity with the acidic patch, and therefore will compete with each other for binding to the nucleosome. We first review the molecular details of each interface, focusing on the key non-covalent interactions that stabilize the protein-acidic patch interactions. We then propose a model in which binding of proteins to the nucleosome disrupts interaction of the H4 tail domains with the acidic patch, preventing the intrinsic chromatin folding pathway and leading to assembly of alternative higher order chromatin structures with unique biological functions.

MeSH Terms
Animals Chromatin Assembly and Disassembly/physiology Chromosomal Proteins, Non-Histone/chemistry,genetics,metabolism Humans Models, Molecular Nucleosomes/chemistry,genetics,metabolism
Chemicals
Chromosomal Proteins, Non-Histone Nucleosomes
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Kalashnikova Anna A
Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, CO 80523-1870, USA.
Porter-Goff Mary E
Muthurajan Uma M
Luger Karolin
Hansen Jeffrey C
References (57)
57 references, click to expand
  1. Spreading of transcriptional repressor SIR3 from telomeric heterochromatin.
    Nature. 1996 Sep 5;383(6595):92-6 PMID: 8779721
  2. High-mobility-group chromosomal proteins: architectural components that facilitate chromatin function.
    Prog Nucleic Acid Res Mol Biol. 1996;54:35-100 PMID: 8768072
  3. Stimulation of replication efficiency of a chromatin template by chromosomal protein HMG-17.
    J Biol Chem. 1998 Apr 17;273(16):9409-14 PMID: 9545265
  4. Reversible oligonucleosome self-association: dependence on divalent cations and core histone tail domains.
    Biochemistry. 1996 Apr 2;35(13):4009-15 PMID: 8672434
  5. Architecture of the high mobility group nucleosomal protein 2-nucleosome complex as revealed by methyl-based NMR.
    Proc Natl Acad Sci U S A. 2011 Jul 26;108(30):12283-8 PMID: 21730181
  6. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 Å resolution.
    Science. 2011 Nov 18;334(6058):977-82 PMID: 22096199
  7. Core histone tail domains mediate oligonucleosome folding and nucleosomal DNA organization through distinct molecular mechanisms.
    J Biol Chem. 1995 Oct 27;270(43):25359-62 PMID: 7592700
  8. Sir3-dependent assembly of supramolecular chromatin structures in vitro.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8584-9 PMID: 11447281
  9. Nucleosome arrays reveal the two-start organization of the chromatin fiber.
    Science. 2004 Nov 26;306(5701):1571-3 PMID: 15567867
  10. Sir3-nucleosome interactions in spreading of silent chromatin in Saccharomyces cerevisiae.
    Mol Cell Biol. 2008 Nov;28(22):6903-18 PMID: 18794362
  11. Histone H4-K16 acetylation controls chromatin structure and protein interactions.
    Science. 2006 Feb 10;311(5762):844-7 PMID: 16469925
  12. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae.
    Annu Rev Biochem. 2003;72:481-516 PMID: 12676793
  13. The nucleosomal surface as a docking station for Kaposi's sarcoma herpesvirus LANA.
    Science. 2006 Feb 10;311(5762):856-61 PMID: 16469929
  14. Efficient persistence of extrachromosomal KSHV DNA mediated by latency-associated nuclear antigen.
    Science. 1999 Apr 23;284(5414):641-4 PMID: 10213686
  15. Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions.
    Annu Rev Biophys Biomol Struct. 2002;31:361-92 PMID: 11988475
  16. Structure and function of the Saccharomyces cerevisiae Sir3 BAH domain.
    Mol Cell Biol. 2006 Apr;26(8):3256-65 PMID: 16581798
  17. Regulation of chromatin structure and function by HMGN proteins.
    Biochim Biophys Acta. 2010 Jan-Feb;1799(1-2):62-8 PMID: 19948260
  18. The silent information regulator 3 protein, SIR3p, binds to chromatin fibers and assembles a hypercondensed chromatin architecture in the presence of salt.
    Mol Cell Biol. 2008 Jun;28(11):3563-72 PMID: 18362167
  19. The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus.
    EMBO J. 1997 Nov 3;16(21):6535-47 PMID: 9351834
  20. Regulation of the H4 tail binding and folding landscapes via Lys-16 acetylation.
    Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):17857-62 PMID: 22988066
  21. Chromatin architectural proteins.
    Chromosome Res. 2006;14(1):39-51 PMID: 16506095
  22. Incorporation of chromosomal proteins HMG-14/HMG-17 into nascent nucleosomes induces an extended chromatin conformation and enhances the utilization of active transcription complexes.
    EMBO J. 1995 Apr 3;14(7):1478-89 PMID: 7729423
  23. H2A.Z alters the nucleosome surface to promote HP1alpha-mediated chromatin fiber folding.
    Mol Cell. 2004 Nov 19;16(4):655-61 PMID: 15546624
  24. Ordered nucleation and spreading of silenced chromatin in Saccharomyces cerevisiae.
    Mol Biol Cell. 2002 Jul;13(7):2207-22 PMID: 12134062
  25. Delineation of the protein module that anchors HMGN proteins to nucleosomes in the chromatin of living cells.
    Mol Cell Biol. 2008 May;28(9):2872-83 PMID: 18299391
  26. Compensatory interactions between Sir3p and the nucleosomal LRS surface imply their direct interaction.
    PLoS Genet. 2008 Dec;4(12):e1000301 PMID: 19079580
  27. Structure and binding of the H4 histone tail and the effects of lysine 16 acetylation.
    Phys Chem Chem Phys. 2011 Feb 21;13(7):2911-21 PMID: 21157623
  28. The core histone N-terminal tail domains function independently and additively during salt-dependent oligomerization of nucleosomal arrays.
    J Biol Chem. 2005 Oct 7;280(40):33701-6 PMID: 16033758
  29. The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association.
    Nucleic Acids Res. 2011 Mar;39(5):1680-91 PMID: 21047799
  30. The Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen 1 N terminus is essential for chromosome association, DNA replication, and episome persistence.
    J Virol. 2004 Jan;78(1):294-301 PMID: 14671111
  31. HMGNs, DNA repair and cancer.
    Biochim Biophys Acta. 2010 Jan-Feb;1799(1-2):80-5 PMID: 20004154
  32. Structure of the Sir3 protein bromo adjacent homology (BAH) domain from S. cerevisiae at 1.95 A resolution.
    Protein Sci. 2006 May;15(5):1182-6 PMID: 16641491
  33. The 1.7 A crystal structure of the regulator of chromosome condensation (RCC1) reveals a seven-bladed propeller.
    Nature. 1998 Mar 5;392(6671):97-101 PMID: 9510255
  34. Two classes of sir3 mutants enhance the sir1 mutant mating defect and abolish telomeric silencing in Saccharomyces cerevisiae.
    Genetics. 2000 Jun;155(2):509-22 PMID: 10835377
  35. SIR2 and SIR4 interactions differ in core and extended telomeric heterochromatin in yeast.
    Genes Dev. 1997 Jan 1;11(1):83-93 PMID: 9000052
  36. Spatial and temporal coordination of mitosis by Ran GTPase.
    Nat Rev Mol Cell Biol. 2008 Jun;9(6):464-77 PMID: 18478030
  37. RCC1 uses a conformationally diverse loop region to interact with the nucleosome: a model for the RCC1-nucleosome complex.
    J Mol Biol. 2010 May 14;398(4):518-29 PMID: 20347844
  38. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin.
    J Cell Biol. 1979 Nov;83(2 Pt 1):403-27 PMID: 387806
  39. IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo.
    Proc Natl Acad Sci U S A. 2007 Jan 2;104(1):282-7 PMID: 17185418
  40. 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction.
    J Mol Biol. 2008 Sep 12;381(4):816-25 PMID: 18653199
  41. Structure of RCC1 chromatin factor bound to the nucleosome core particle.
    Nature. 2010 Sep 30;467(7315):562-6 PMID: 20739938
  42. Energy landscape analyses of disordered histone tails reveal special organization of their conformational dynamics.
    J Am Chem Soc. 2011 May 18;133(19):7405-15 PMID: 21517079
  43. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins.
    Mol Cell Biol. 1999 Aug;19(8):5237-46 PMID: 10409715
  44. Cyclic adenosine 3',5'-monophosphate-dependent phosphorylation of HMG 14 inhibits its interactions with nucleosomes.
    Mol Endocrinol. 1991 Jan;5(1):42-50 PMID: 1850110
  45. Participation of core histone "tails" in the stabilization of the chromatin solenoid.
    J Cell Biol. 1982 May;93(2):285-97 PMID: 7096439
  46. Mitotic phosphorylation prevents the binding of HMGN proteins to chromatin.
    Mol Cell Biol. 2001 Aug;21(15):5169-78 PMID: 11438671
  47. Generation of GTP-bound Ran by RCC1 is required for chromatin-induced mitotic spindle formation.
    Nature. 1999 Jul 8;400(6740):178-81 PMID: 10408446
  48. Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 "tail" to DNA.
    J Biol Chem. 1993 Jan 5;268(1):305-14 PMID: 8416938
  49. Molecular mimicry between IL-33 and KSHV for attachment to chromatin through the H2A-H2B acidic pocket.
    EMBO Rep. 2008 Oct;9(10):1006-12 PMID: 18688256
  50. Chromatin fiber folding: requirement for the histone H4 N-terminal tail.
    J Mol Biol. 2003 Mar 14;327(1):85-96 PMID: 12614610
  51. Hybrid trypsinized nucleosomal arrays: identification of multiple functional roles of the H2A/H2B and H3/H4 N-termini in chromatin fiber compaction.
    Biochemistry. 1997 Sep 23;36(38):11381-8 PMID: 9298957
  52. Determinants of histone H4 N-terminal domain function during nucleosomal array oligomerization: roles of amino acid sequence, domain length, and charge density.
    J Biol Chem. 2009 Jun 19;284(25):16716-16722 PMID: 19395382
  53. Use of selectively trypsinized nucleosome core particles to analyze the role of the histone "tails" in the stabilization of the nucleosome.
    J Mol Biol. 1989 Apr 5;206(3):451-63 PMID: 2716057
  54. Crystal structure of the nucleosome core particle at 2.8 A resolution.
    Nature. 1997 Sep 18;389(6648):251-60 PMID: 9305837
  55. Close but distinct regions of human herpesvirus 8 latency-associated nuclear antigen 1 are responsible for nuclear targeting and binding to human mitotic chromosomes.
    J Virol. 2001 Apr;75(8):3948-59 PMID: 11264383
  56. The RanGTP gradient - a GPS for the mitotic spindle.
    J Cell Sci. 2008 May 15;121(Pt 10):1577-86 PMID: 18469014
  57. Domain organization and quaternary structure of the Saccharomyces cerevisiae silent information regulator 3 protein, Sir3p.
    Biochemistry. 2006 Dec 26;45(51):15941-8 PMID: 17176117
Article Info
Journal
Journal of the Royal Society, Interface
Abbr.
J R Soc Interface
ISSN
1742-5662
Published
2013-05-06
Epub
2013-00-27
Pages
20121022
Language
English
Region
England
NLM ID
101217269
PMCID
PMC3627075
Subset
IM
Grants
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · GM066834 · United States
NIGMS NIH HHS · P01 GM088409 · United States
NIGMS NIH HHS · GM088409 · United States
NIGMS NIH HHS · R01 GM045916 · United States
NIGMS NIH HHS · R01 GM066834 · United States
NIGMS NIH HHS · GM045916 · United States
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