1p3b › Citations

Crystal structures of histone Sin mutant nucleosomes reveal altered protein-DNA interactions.

Muthurajan UM, Bao Y, Forsberg LJ, Edayathumangalam RS, Dyer PN, White CL, Luger K
EMBO J 23 260-71 (2004)
Related entries: 1p34, 1p3a, 1p3f, 1p3g, 1p3i, 1p3k, 1p3l, 1p3m, 1p3o, 1p3p

Cited: 102 times
EuropePMC logo PMID: 14739929

Abstract

Here we describe 11 crystal structures of nucleosome core particles containing individual point mutations in the structured regions of histones H3 and H4. The mutated residues are located at the two protein-DNA interfaces flanking the nucleosomal dyad. Five of the mutations partially restore the in vivo effects of SWI/SNF inactivation in yeast. We find that even nonconservative mutations of these residues (which exhibit a distinct phenotype in vivo) have only moderate effects on global nucleosome structure. Rather, local protein-DNA interactions are disrupted and weakened in a subtle and complex manner. The number of lost protein-DNA interactions correlates directly with an increased propensity of the histone octamer to reposition with respect to the DNA, and with an overall destabilization of the nucleosome. Thus, the disruption of only two to six of the approximately 120 direct histone-DNA interactions within the nucleosome has a pronounced effect on nucleosome mobility and stability. This has implications for our understanding of how these structures are made accessible to the transcription and replication machinery in vivo.

Reviews - 1p3b mentioned but not cited (1)

  1. Histone structure and nucleosome stability. Mariño-Ramírez L, Kann MG, Shoemaker BA, Landsman D. Expert Rev Proteomics 2 719-729 (2005)

Articles - 1p3b mentioned but not cited (6)

  1. The expanding landscape of 'oncohistone' mutations in human cancers. Nacev BA, Feng L, Bagert JD, Lemiesz AE, Gao J, Soshnev AA, Kundra R, Schultz N, Muir TW, Allis CD. Nature 567 473-478 (2019)
  2. Crystal structures of histone Sin mutant nucleosomes reveal altered protein-DNA interactions. Muthurajan UM, Bao Y, Forsberg LJ, Edayathumangalam RS, Dyer PN, White CL, Luger K. EMBO J 23 260-271 (2004)
  3. An ensemble of B-DNA dinucleotide geometries lead to characteristic nucleosomal DNA structure and provide plasticity required for gene expression. Marathe A, Bansal M. BMC Struct Biol 11 1 (2011)
  4. DNA architecture, deformability, and nucleosome positioning. Xu F, Olson WK. J Biomol Struct Dyn 27 725-739 (2010)
  5. Matching protein surface structural patches for high-resolution blind peptide docking. Khramushin A, Ben-Aharon Z, Tsaban T, Varga JK, Avraham O, Schueler-Furman O. Proc Natl Acad Sci U S A 119 e2121153119 (2022)
  6. Statistical investigation of position-specific deformation pattern of nucleosome DNA based on multiple conformational properties. Yang X, Yan Y. Bioinformation 7 120-124 (2011)


Reviews citing this publication (21)

  1. Regulated nucleosome mobility and the histone code. Cosgrove MS, Boeke JD, Wolberger C. Nat Struct Mol Biol 11 1037-1043 (2004)
  2. Post-translational modifications of histones that influence nucleosome dynamics. Bowman GD, Poirier MG. Chem Rev 115 2274-2295 (2015)
  3. Nucleosome structure(s) and stability: variations on a theme. Andrews AJ, Luger K. Annu Rev Biophys 40 99-117 (2011)
  4. Mechanisms for ATP-dependent chromatin remodelling: farewell to the tuna-can octamer? Flaus A, Owen-Hughes T. Curr Opin Genet Dev 14 165-173 (2004)
  5. Dynamic nucleosomes. Luger K. Chromosome Res 14 5-16 (2006)
  6. How does the histone code work? Cosgrove MS, Wolberger C. Biochem Cell Biol 83 468-476 (2005)
  7. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Mersfelder EL, Parthun MR. Nucleic Acids Res 34 2653-2662 (2006)
  8. Chromatin architecture. Woodcock CL. Curr Opin Struct Biol 16 213-220 (2006)
  9. Nucleosome structural studies. Tan S, Davey CA. Curr Opin Struct Biol 21 128-136 (2011)
  10. Mechanism of transcription through a nucleosome by RNA polymerase II. Kulaeva OI, Hsieh FK, Chang HW, Luse DS, Studitsky VM. Biochim Biophys Acta 1829 76-83 (2013)
  11. Mechanisms of ATP-dependent nucleosome sliding. Bowman GD. Curr Opin Struct Biol 20 73-81 (2010)
  12. Histone exchange and histone modifications during transcription and aging. Das C, Tyler JK. Biochim Biophys Acta 1819 332-342 (2013)
  13. Histone proteomics and the epigenetic regulation of nucleosome mobility. Cosgrove MS. Expert Rev Proteomics 4 465-478 (2007)
  14. Repair of UV lesions in nucleosomes--intrinsic properties and remodeling. Thoma F. DNA Repair (Amst) 4 855-869 (2005)
  15. Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Korolev N, Vorontsova OV, Nordenskiöld L. Prog Biophys Mol Biol 95 23-49 (2007)
  16. Structure and dynamic properties of nucleosome core particles. Chakravarthy S, Park YJ, Chodaparambil J, Edayathumangalam RS, Luger K. FEBS Lett 579 895-898 (2005)
  17. Molecular traffic jams on DNA. Finkelstein IJ, Greene EC. Annu Rev Biophys 42 241-263 (2013)
  18. Current progress on structural studies of nucleosomes containing histone H3 variants. Kurumizaka H, Horikoshi N, Tachiwana H, Kagawa W. Curr Opin Struct Biol 23 109-115 (2013)
  19. Histone H2B Mutations in Cancer. Wan YCE, Chan KM. Biomedicines 9 694 (2021)
  20. Histone 3.3-related chromatinopathy: missense variants throughout H3-3A and H3-3B cause a range of functional consequences across species. Bryant L, Sangree A, Clark K, Bhoj E. Hum Genet (2023)
  21. Structural studies of functional nucleosome complexes with transacting factors. Kurumizaka H. Proc Jpn Acad Ser B Phys Biol Sci 98 1-14 (2022)

Articles citing this publication (74)

  1. A unifying model for the selective regulation of inducible transcription by CpG islands and nucleosome remodeling. Ramirez-Carrozzi VR, Braas D, Bhatt DM, Cheng CS, Hong C, Doty KR, Black JC, Hoffmann A, Carey M, Smale ST. Cell 138 114-128 (2009)
  2. High-resolution dynamic mapping of histone-DNA interactions in a nucleosome. Hall MA, Shundrovsky A, Bai L, Fulbright RM, Lis JT, Wang MD. Nat Struct Mol Biol 16 124-129 (2009)
  3. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Hyland EM, Cosgrove MS, Molina H, Wang D, Pandey A, Cottee RJ, Boeke JD. Mol Cell Biol 25 10060-10070 (2005)
  4. A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nakanishi S, Sanderson BW, Delventhal KM, Bradford WD, Staehling-Hampton K, Shilatifard A. Nat Struct Mol Biol 15 881-888 (2008)
  5. Histone fold modifications control nucleosome unwrapping and disassembly. Simon M, North JA, Shimko JC, Forties RA, Ferdinand MB, Manohar M, Zhang M, Fishel R, Ottesen JJ, Poirier MG. Proc Natl Acad Sci U S A 108 12711-12716 (2011)
  6. Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA. Bao Y, Konesky K, Park YJ, Rosu S, Dyer PN, Rangasamy D, Tremethick DJ, Laybourn PJ, Luger K. EMBO J 23 3314-3324 (2004)
  7. Structural basis of instability of the nucleosome containing a testis-specific histone variant, human H3T. Tachiwana H, Kagawa W, Osakabe A, Kawaguchi K, Shiga T, Hayashi-Takanaka Y, Kimura H, Kurumizaka H. Proc Natl Acad Sci U S A 107 10454-10459 (2010)
  8. Nucleosomal elements that control the topography of the barrier to transcription. Bintu L, Ishibashi T, Dangkulwanich M, Wu YY, Lubkowska L, Kashlev M, Bustamante C. Cell 151 738-749 (2012)
  9. Acetylation of histone H3 at the nucleosome dyad alters DNA-histone binding. Manohar M, Mooney AM, North JA, Nakkula RJ, Picking JW, Edon A, Fishel R, Poirier MG, Ottesen JJ. J Biol Chem 284 23312-23321 (2009)
  10. DNA conformations and their sequence preferences. Svozil D, Kalina J, Omelka M, Schneider B. Nucleic Acids Res 36 3690-3706 (2008)
  11. Histone tails and the H3 alphaN helix regulate nucleosome mobility and stability. Ferreira H, Somers J, Webster R, Flaus A, Owen-Hughes T. Mol Cell Biol 27 4037-4048 (2007)
  12. Histone H3 K36 methylation is mediated by a trans-histone methylation pathway involving an interaction between Set2 and histone H4. Du HN, Fingerman IM, Briggs SD. Genes Dev 22 2786-2798 (2008)
  13. Scratching the (lateral) surface of chromatin regulation by histone modifications. Tropberger P, Schneider R. Nat Struct Mol Biol 20 657-661 (2013)
  14. Contribution of histone N-terminal tails to the structure and stability of nucleosomes. Iwasaki W, Miya Y, Horikoshi N, Osakabe A, Taguchi H, Tachiwana H, Shibata T, Kagawa W, Kurumizaka H. FEBS Open Bio 3 363-369 (2013)
  15. Nucleosome remodeling by hMSH2-hMSH6. Javaid S, Manohar M, Punja N, Mooney A, Ottesen JJ, Poirier MG, Fishel R. Mol Cell 36 1086-1094 (2009)
  16. Cluster analysis reveals differential transcript profiles associated with resistance training-induced human skeletal muscle hypertrophy. Thalacker-Mercer A, Stec M, Cui X, Cross J, Windham S, Bamman M. Physiol Genomics 45 499-507 (2013)
  17. Global analysis of functional surfaces of core histones with comprehensive point mutants. Matsubara K, Sano N, Umehara T, Horikoshi M. Genes Cells 12 13-33 (2007)
  18. Nucleosome formation with the testis-specific histone H3 variant, H3t, by human nucleosome assembly proteins in vitro. Tachiwana H, Osakabe A, Kimura H, Kurumizaka H. Nucleic Acids Res 36 2208-2218 (2008)
  19. Distortion of histone octamer core promotes nucleosome mobilization by a chromatin remodeler. Sinha KK, Gross JD, Narlikar GJ. Science 355 eaaa3761 (2017)
  20. Importance of electrostatic interactions in the association of intrinsically disordered histone chaperone Chz1 and histone H2A.Z-H2B. Chu X, Wang Y, Gan L, Bai Y, Han W, Wang E, Wang J. PLoS Comput Biol 8 e1002608 (2012)
  21. Phosphorylation of histone H3(T118) alters nucleosome dynamics and remodeling. North JA, Javaid S, Ferdinand MB, Chatterjee N, Picking JW, Shoffner M, Nakkula RJ, Bartholomew B, Ottesen JJ, Fishel R, Poirier MG. Nucleic Acids Res 39 6465-6474 (2011)
  22. Probing the (H3-H4)2 histone tetramer structure using pulsed EPR spectroscopy combined with site-directed spin labelling. Bowman A, Ward R, El-Mkami H, Owen-Hughes T, Norman DG. Nucleic Acids Res 38 695-707 (2010)
  23. Heterochromatin protein Sir3 induces contacts between the amino terminus of histone H4 and nucleosomal DNA. Wang F, Li G, Altaf M, Lu C, Currie MA, Johnson A, Moazed D. Proc Natl Acad Sci U S A 110 8495-8500 (2013)
  24. The Drosophila boundary element-associated factors BEAF-32A and BEAF-32B affect chromatin structure. Gilbert MK, Tan YY, Hart CM. Genetics 173 1365-1375 (2006)
  25. DNA sequence-directed organization of chromatin: structure-based computational analysis of nucleosome-binding sequences. Balasubramanian S, Xu F, Olson WK. Biophys J 96 2245-2260 (2009)
  26. A gene-specific requirement for FACT during transcription is related to the chromatin organization of the transcribed region. Jimeno-González S, Gómez-Herreros F, Alepuz PM, Chávez S. Mol Cell Biol 26 8710-8721 (2006)
  27. Histone Sin mutations promote nucleosome traversal and histone displacement by RNA polymerase II. Hsieh FK, Fisher M, Ujvári A, Studitsky VM, Luse DS. EMBO Rep 11 705-710 (2010)
  28. Structural rearrangements of the histone octamer translocate DNA. Bilokapic S, Strauss M, Halic M. Nat Commun 9 1330 (2018)
  29. From crystal and NMR structures, footprints and cryo-electron-micrographs to large and soft structures: nanoscale modeling of the nucleosomal stem. Meyer S, Becker NB, Syed SH, Goutte-Gattat D, Shukla MS, Hayes JJ, Angelov D, Bednar J, Dimitrov S, Everaers R. Nucleic Acids Res 39 9139-9154 (2011)
  30. Comprehensive structural analysis of mutant nucleosomes containing lysine to glutamine (KQ) substitutions in the H3 and H4 histone-fold domains. Iwasaki W, Tachiwana H, Kawaguchi K, Shibata T, Kagawa W, Kurumizaka H. Biochemistry 50 7822-7832 (2011)
  31. Efficient and rapid nucleosome traversal by RNA polymerase II depends on a combination of transcript elongation factors. Luse DS, Spangler LC, Újvári A. J Biol Chem 286 6040-6048 (2011)
  32. Kinetics and thermodynamics of phenotype: unwinding and rewinding the nucleosome. Mack AH, Schlingman DJ, Ilagan RP, Regan L, Mochrie SG. J Mol Biol 423 687-701 (2012)
  33. Generation of a synthetic GlcNAcylated nucleosome reveals regulation of stability by H2A-Thr101 GlcNAcylation. Lercher L, Raj R, Patel NA, Price J, Mohammed S, Robinson CV, Schofield CJ, Davis BG. Nat Commun 6 7978 (2015)
  34. Identification of histone mutants that are defective for transcription-coupled nucleosome occupancy. Hainer SJ, Martens JA. Mol Cell Biol 31 3557-3568 (2011)
  35. The LRS and SIN domains: two structurally equivalent but functionally distinct nucleosomal surfaces required for transcriptional silencing. Fry CJ, Norris A, Cosgrove M, Boeke JD, Peterson CL. Mol Cell Biol 26 9045-9059 (2006)
  36. Altering the chromatin landscape for nucleotide excision repair. Nag R, Smerdon MJ. Mutat Res 682 13-20 (2009)
  37. Histone H3.5 forms an unstable nucleosome and accumulates around transcription start sites in human testis. Urahama T, Harada A, Maehara K, Horikoshi N, Sato K, Sato Y, Shiraishi K, Sugino N, Osakabe A, Tachiwana H, Kagawa W, Kimura H, Ohkawa Y, Kurumizaka H. Epigenetics Chromatin 9 2 (2016)
  38. In Vitro Chromatin Assembly: Strategies and Quality Control. Muthurajan U, Mattiroli F, Bergeron S, Zhou K, Gu Y, Chakravarthy S, Dyer P, Irving T, Luger K. Methods Enzymol 573 3-41 (2016)
  39. Geometry of the nucleosomal DNA superhelix. Bishop TC. Biophys J 95 1007-1017 (2008)
  40. Nucleosome architecture throughout the cell cycle. Deniz Ö, Flores O, Aldea M, Soler-López M, Orozco M. Sci Rep 6 19729 (2016)
  41. Histone Acetylation near the Nucleosome Dyad Axis Enhances Nucleosome Disassembly by RSC and SWI/SNF. Chatterjee N, North JA, Dechassa ML, Manohar M, Prasad R, Luger K, Ottesen JJ, Poirier MG, Bartholomew B. Mol Cell Biol 35 4083-4092 (2015)
  42. Histone H3 phosphorylation near the nucleosome dyad alters chromatin structure. North JA, Šimon M, Ferdinand MB, Shoffner MA, Picking JW, Howard CJ, Mooney AM, van Noort J, Poirier MG, Ottesen JJ. Nucleic Acids Res 42 4922-4933 (2014)
  43. Histone Sprocket Arginine Residues Are Important for Gene Expression, DNA Repair, and Cell Viability in Saccharomyces cerevisiae. Hodges AJ, Gallegos IJ, Laughery MF, Meas R, Tran L, Wyrick JJ. Genetics 200 795-806 (2015)
  44. Global analysis of mutual interaction surfaces of nucleosomes with comprehensive point mutants. Sakamoto M, Noguchi S, Kawashima S, Okada Y, Enomoto T, Seki M, Horikoshi M. Genes Cells 14 1271-1330 (2009)
  45. NDF, a nucleosome-destabilizing factor that facilitates transcription through nucleosomes. Fei J, Ishii H, Hoeksema MA, Meitinger F, Kassavetis GA, Glass CK, Ren B, Kadonaga JT. Genes Dev 32 682-694 (2018)
  46. A single amino acid change in histone H4 enhances UV survival and DNA repair in yeast. Nag R, Gong F, Fahy D, Smerdon MJ. Nucleic Acids Res 36 3857-3866 (2008)
  47. DNA nanomechanics in the nucleosome. Becker NB, Everaers R. Structure 17 579-589 (2009)
  48. Aurora-A mediated histone H3 phosphorylation of threonine 118 controls condensin I and cohesin occupancy in mitosis. Wike CL, Graves HK, Hawkins R, Gibson MD, Ferdinand MB, Zhang T, Chen Z, Hudson DF, Ottesen JJ, Poirier MG, Schumacher J, Tyler JK. Elife 5 e11402 (2016)
  49. Structural and functional analyses of nucleosome complexes with mouse histone variants TH2a and TH2b, involved in reprogramming. Padavattan S, Shinagawa T, Hasegawa K, Kumasaka T, Ishii S, Kumarevel T. Biochem Biophys Res Commun 464 929-935 (2015)
  50. Nucleosome dynamics during chromatin remodeling in vivo. Ramachandran S, Henikoff S. Nucleus 7 20-26 (2016)
  51. Role of chromatin accessibility in the occupancy and transcription of the insulin gene by the pancreatic and duodenal homeobox factor 1. Francis J, Babu DA, Deering TG, Chakrabarti SK, Garmey JC, Evans-Molina C, Taylor DG, Mirmira RG. Mol Endocrinol 20 3133-3145 (2006)
  52. The conformational flexibility of the C-terminus of histone H4 promotes histone octamer and nucleosome stability and yeast viability. Chavez MS, Scorgie JK, Dennehey BK, Noone S, Tyler JK, Churchill ME. Epigenetics Chromatin 5 5 (2012)
  53. Choosing where to look next in a mutation sequence space: Active Learning of informative p53 cancer rescue mutants. Danziger SA, Zeng J, Wang Y, Brachmann RK, Lathrop RH. Bioinformatics 23 i104-14 (2007)
  54. The mechanism of nucleosome traversal by RNA polymerase II: roles for template uncoiling and transcript elongation factors. Luse DS, Studitsky VM. RNA Biol 8 581-585 (2011)
  55. Thermodynamic stability of histone H3 is a necessary but not sufficient driving force for its evolutionary conservation. Ramachandran S, Vogel L, Strahl BD, Dokholyan NV. PLoS Comput Biol 7 e1001042 (2011)
  56. A zinc-finger like metal binding site in the nucleosome. Adamczyk M, Poznański J, Kopera E, Bal W. FEBS Lett 581 1409-1416 (2007)
  57. Mutations that prevent or mimic persistent post-translational modifications of the histone H3 globular domain cause lethality and growth defects in Drosophila. Graves HK, Wang P, Lagarde M, Chen Z, Tyler JK. Epigenetics Chromatin 9 9 (2016)
  58. Dispersed mutations in histone H3 that affect transcriptional repression and chromatin structure of the CHA1 promoter in Saccharomyces cerevisiae. He Q, Yu C, Morse RH. Eukaryot Cell 7 1649-1660 (2008)
  59. Mechanism of cohesin loading onto chromosomes: a conformational dynamics study. Kurkcuoglu O, Bates PA. Biophys J 99 1212-1220 (2010)
  60. Structural analyses of the nucleosome complexes with human testis-specific histone variants, hTh2a and hTh2b. Padavattan S, Thiruselvam V, Shinagawa T, Hasegawa K, Kumasaka T, Ishii S, Kumarevel T. Biophys Chem 221 41-48 (2017)
  61. Global analysis of functional relationships between histone point mutations and the effects of histone deacetylase inhibitors. Sato L, Noguchi S, Hayashi Y, Sakamoto M, Horikoshi M. Genes Cells 15 553-594 (2010)
  62. Long-range effects of histone point mutations on DNA remodeling revealed from computational analyses of SIN-mutant nucleosome structures. Xu F, Colasanti AV, Li Y, Olson WK. Nucleic Acids Res 38 6872-6882 (2010)
  63. Unwinding and rewinding the nucleosome inner turn: force dependence of the kinetic rate constants. Mochrie SG, Mack AH, Schlingman DJ, Collins R, Kamenetska M, Regan L. Phys Rev E Stat Nonlin Soft Matter Phys 87 012710 (2013)
  64. Surprising Twists in Nucleosomal DNA with Implication for Higher-order Folding. Todolli S, Young RT, Watkins AS, Bu Sha A, Yager J, Olson WK. J Mol Biol 433 167121 (2021)
  65. The electronic structure of the four nucleotide bases in DNA, of their stacks, and of their homopolynucleotides in the absence and presence of water. Ladik J, Bende A, Bogár F. J Chem Phys 128 105101 (2008)
  66. TGM2-mediated histone transglutamination is dictated by steric accessibility. Lukasak BJ, Mitchener MM, Kong L, Dul BE, Lazarus CD, Ramakrishnan A, Ni J, Shen L, Maze I, Muir TW. Proc Natl Acad Sci U S A 119 e2208672119 (2022)
  67. Excess free histone H3 localizes to centrosomes for proteasome-mediated degradation during mitosis in metazoans. Wike CL, Graves HK, Wason A, Hawkins R, Gopalakrishnan J, Schumacher J, Tyler JK. Cell Cycle 15 2216-2225 (2016)
  68. SMOG 2 and OpenSMOG: Extending the limits of structure-based models. de Oliveira AB, Contessoto VG, Hassan A, Byju S, Wang A, Wang Y, Dodero-Rojas E, Mohanty U, Noel JK, Onuchic JN, Whitford PC. Protein Sci 31 158-172 (2022)
  69. Calculation of the hole mobilities of the three homopolynucleotides, poly(guanilic acid), poly(adenilic acid), and polythymidine in the presence of water and Na+ ions. Bende A, Bogár F, Beleznay F, Ladik J. Phys Rev E Stat Nonlin Soft Matter Phys 78 061923 (2008)
  70. Histone mutations in cancer. Espinoza Pereira KN, Shan J, Licht JD, Bennett RL. Biochem Soc Trans 51 1749-1763 (2023)
  71. Micromechanical Study of Hyperacetylated Nucleosomes Using Single Molecule Transverse Magnetic Tweezers. Gaire S, Fabian RL, Adhikari R, Tuma PL, Pegg IL, Sarkar A. Int J Mol Sci 24 6188 (2023)
  72. Nucleosomes and their complexes in the cryoEM era: Trends and limitations. Armeev GA, Gribkova AK, Shaytan AK. Front Mol Biosci 9 1070489 (2022)
  73. Simulations of SIN Mutations and Histone Variants in Human Nucleosomes Reveal Altered Protein-DNA and Core Histone Interactions. Vijayalakshmi M, Shivashankar GV, Sowdhamini R. J Biomol Struct Dyn 25 207-218 (2007)
  74. Simulations of SIN mutations and histone variants in human nucleosomes reveal altered protein-DNA and core histone interactions. Vijayalakshmi M, Shivashankar GV, Sowdhamini R. J Biomol Struct Dyn 25 207-218 (2007)


Quick links