4z2n › Citations

Integrated molecular mechanism directing nucleosome reorganization by human FACT.

Figure 1.
Figure 2.
Figure 3.
Tsunaka Y, Fujiwara Y, Oyama T, Hirose S, Morikawa K
OpenAccess logo Genes Dev 30 673-86 (2016)
Cited: 86 times
EuropePMC logo PMID: 26966247

Abstract

Facilitates chromatin transcription (FACT) plays essential roles in chromatin remodeling during DNA transcription, replication, and repair. Our structural and biochemical studies of human FACT-histone interactions present precise views of nucleosome reorganization, conducted by the FACT-SPT16 (suppressor of Ty 16) Mid domain and its adjacent acidic AID segment. AID accesses the H2B N-terminal basic region exposed by partial unwrapping of the nucleosomal DNA, thereby triggering the invasion of FACT into the nucleosome. The crystal structure of the Mid domain complexed with an H3-H4 tetramer exhibits two separate contact sites; the Mid domain forms a novel intermolecular β structure with H4. At the other site, the Mid-H2A steric collision on the H2A-docking surface of the H3-H4 tetramer within the nucleosome induces H2A-H2B displacement. This integrated mechanism results in disrupting the H3 αN helix, which is essential for retaining the nucleosomal DNA ends, and hence facilitates DNA stripping from histone.

Reviews - 4z2n mentioned but not cited (1)

  1. Structure-function relationship of H2A-H2B specific plant histone chaperones. Kumar A, Vasudevan D. Cell Stress Chaperones 25 1-17 (2020)

Articles - 4z2n mentioned but not cited (1)

  1. Integrated molecular mechanism directing nucleosome reorganization by human FACT. Tsunaka Y, Fujiwara Y, Oyama T, Hirose S, Morikawa K. Genes Dev 30 673-686 (2016)


Reviews citing this publication (24)

  1. Histone chaperone networks shaping chromatin function. Hammond CM, Strømme CB, Huang H, Patel DJ, Groth A. Nat Rev Mol Cell Biol 18 141-158 (2017)
  2. The roles of histone variants in fine-tuning chromatin organization and function. Martire S, Banaszynski LA. Nat Rev Mol Cell Biol 21 522-541 (2020)
  3. Chromatin replication and epigenetic cell memory. Stewart-Morgan KR, Petryk N, Groth A. Nat Cell Biol 22 361-371 (2020)
  4. Replication-Coupled Nucleosome Assembly in the Passage of Epigenetic Information and Cell Identity. Serra-Cardona A, Zhang Z. Trends Biochem Sci 43 136-148 (2018)
  5. H3-H4 Histone Chaperone Pathways. Grover P, Asa JS, Campos EI. Annu Rev Genet 52 109-130 (2018)
  6. The role of FACT in managing chromatin: disruption, assembly, or repair? Formosa T, Winston F. Nucleic Acids Res 48 11929-11941 (2020)
  7. Structure and function of the histone chaperone FACT - Resolving FACTual issues. Gurova K, Chang HW, Valieva ME, Sandlesh P, Studitsky VM. Biochim Biophys Acta Gene Regul Mech S1874-9399(18)30159-7 (2018)
  8. The histone chaperoning pathway: from ribosome to nucleosome. Pardal AJ, Fernandes-Duarte F, Bowman AJ. Essays Biochem 63 29-43 (2019)
  9. A Molecular Prospective for HIRA Complex Assembly and H3.3-Specific Histone Chaperone Function. Ricketts MD, Marmorstein R. J Mol Biol 429 1924-1933 (2017)
  10. The architecture and function of the chromatin replication machinery. Miller TC, Costa A. Curr Opin Struct Biol 47 9-16 (2017)
  11. DNA replication through a chromatin environment. Bellush JM, Whitehouse I. Philos Trans R Soc Lond B Biol Sci 372 20160287 (2017)
  12. The Effects of Replication Stress on S Phase Histone Management and Epigenetic Memory. Šviković S, Sale JE. J Mol Biol 429 2011-2029 (2017)
  13. The replisome guides nucleosome assembly during DNA replication. Zhang W, Feng J, Li Q. Cell Biosci 10 37 (2020)
  14. Chromatin Stability as a Target for Cancer Treatment. Gurova KV. Bioessays 41 e1800141 (2019)
  15. Regulation of chromatin structure and function: insights into the histone chaperone FACT. Wang P, Yang W, Zhao S, Nashun B. Cell Cycle 20 465-479 (2021)
  16. Molecular recognition of nucleosomes by binding partners. Kale S, Goncearenco A, Markov Y, Landsman D, Panchenko AR. Curr Opin Struct Biol 56 164-170 (2019)
  17. Recognition of ubiquitinated nucleosomes. Morgan MT, Wolberger C. Curr Opin Struct Biol 42 75-82 (2017)
  18. The FACT Histone Chaperone: Tuning Gene Transcription in the Chromatin Context to Modulate Plant Growth and Development. Grasser KD. Front Plant Sci 11 85 (2020)
  19. Molecular basis for chromatin assembly and modification by multiprotein complexes. Ricketts MD, Han J, Szurgot MR, Marmorstein R. Protein Sci 28 329-343 (2019)
  20. The histone chaperone FACT: a guardian of chromatin structure integrity. Jeronimo C, Robert F. Transcription 13 16-38 (2022)
  21. Dynamic structures of intrinsically disordered proteins related to the general transcription factor TFIIH, nucleosomes, and histone chaperones. Okuda M, Tsunaka Y, Nishimura Y. Biophys Rev 14 1449-1472 (2022)
  22. 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)
  23. Opposing Roles of FACT for Euchromatin and Heterochromatin in Yeast. Takahata S, Murakami Y. Biomolecules 13 377 (2023)
  24. Structural Transition of the Nucleosome during Transcription Elongation. Kujirai T, Ehara H, Sekine SI, Kurumizaka H. Cells 12 1388 (2023)

Articles citing this publication (60)

  1. FACT caught in the act of manipulating the nucleosome. Liu Y, Zhou K, Zhang N, Wei H, Tan YZ, Zhang Z, Carragher B, Potter CS, D'Arcy S, Luger K. Nature 577 426-431 (2020)
  2. FACT is a sensor of DNA torsional stress in eukaryotic cells. Safina A, Cheney P, Pal M, Brodsky L, Ivanov A, Kirsanov K, Lesovaya E, Naberezhnov D, Nesher E, Koman I, Wang D, Wang J, Yakubovskaya M, Winkler D, Gurova K. Nucleic Acids Res 45 1925-1945 (2017)
  3. Large-scale ATP-independent nucleosome unfolding by a histone chaperone. Valieva ME, Armeev GA, Kudryashova KS, Gerasimova NS, Shaytan AK, Kulaeva OI, McCullough LL, Formosa T, Georgiev PG, Kirpichnikov MP, Studitsky VM, Feofanov AV. Nat Struct Mol Biol 23 1111-1116 (2016)
  4. The histone chaperone FACT modulates nucleosome structure by tethering its components. Wang T, Liu Y, Edwards G, Krzizike D, Scherman H, Luger K. Life Sci Alliance 1 e201800107 (2018)
  5. Transcription-driven chromatin repression of Intragenic transcription start sites. Nielsen M, Ard R, Leng X, Ivanov M, Kindgren P, Pelechano V, Marquardt S. PLoS Genet 15 e1007969 (2019)
  6. Histone H2A-H2B binding by Pol α in the eukaryotic replisome contributes to the maintenance of repressive chromatin. Evrin C, Maman JD, Diamante A, Pellegrini L, Labib K. EMBO J 37 e99021 (2018)
  7. Role of Chromatin Damage and Chromatin Trapping of FACT in Mediating the Anticancer Cytotoxicity of DNA-Binding Small-Molecule Drugs. Nesher E, Safina A, Aljahdali I, Portwood S, Wang ES, Koman I, Wang J, Gurova KV. Cancer Res 78 1431-1443 (2018)
  8. The elongation factor Spt4/5 regulates RNA polymerase II transcription through the nucleosome. Crickard JB, Lee J, Lee TH, Reese JC. Nucleic Acids Res 45 6362-6374 (2017)
  9. Functional roles of the DNA-binding HMGB domain in the histone chaperone FACT in nucleosome reorganization. McCullough LL, Connell Z, Xin H, Studitsky VM, Feofanov AV, Valieva ME, Formosa T. J Biol Chem 293 6121-6133 (2018)
  10. The CENP-T/-W complex is a binding partner of the histone chaperone FACT. Prendergast L, Müller S, Liu Y, Huang H, Dingli F, Loew D, Vassias I, Patel DJ, Sullivan KF, Almouzni G. Genes Dev 30 1313-1326 (2016)
  11. Transcription Promotes the Interaction of the FAcilitates Chromatin Transactions (FACT) Complex with Nucleosomes in Saccharomyces cerevisiae. Martin BJE, Chruscicki AT, Howe LJ. Genetics 210 869-881 (2018)
  12. Mechanism of FACT removal from transcribed genes by anticancer drugs curaxins. Chang HW, Valieva ME, Safina A, Chereji RV, Wang J, Kulaeva OI, Morozov AV, Kirpichnikov MP, Feofanov AV, Gurova KV, Studitsky VM. Sci Adv 4 eaav2131 (2018)
  13. The Chaperone FACT and Histone H2B Ubiquitination Maintain S. pombe Genome Architecture through Genic and Subtelomeric Functions. Murawska M, Schauer T, Matsuda A, Wilson MD, Pysik T, Wojcik F, Muir TW, Hiraoka Y, Straub T, Ladurner AG. Mol Cell 77 501-513.e7 (2020)
  14. The Modifier of Transcription 1 (Mot1) ATPase and Spt16 Histone Chaperone Co-regulate Transcription through Preinitiation Complex Assembly and Nucleosome Organization. True JD, Muldoon JJ, Carver MN, Poorey K, Shetty SJ, Bekiranov S, Auble DT. J Biol Chem 291 15307-15319 (2016)
  15. Structural visualization of key steps in nucleosome reorganization by human FACT. Mayanagi K, Saikusa K, Miyazaki N, Akashi S, Iwasaki K, Nishimura Y, Morikawa K, Tsunaka Y. Sci Rep 9 10183 (2019)
  16. FACT is recruited to the +1 nucleosome of transcribed genes and spreads in a Chd1-dependent manner. Jeronimo C, Angel A, Nguyen VQ, Kim JM, Poitras C, Lambert E, Collin P, Mellor J, Wu C, Robert F. Mol Cell 81 3542-3559.e11 (2021)
  17. TRAIN (Transcription of Repeats Activates INterferon) in response to chromatin destabilization induced by small molecules in mammalian cells. Leonova K, Safina A, Nesher E, Sandlesh P, Pratt R, Burkhart C, Lipchick B, Gitlin I, Frangou C, Koman I, Wang J, Kirsanov K, Yakubovskaya MG, Gudkov AV, Gurova K. Elife 7 e30842 (2018)
  18. CENP-B creates alternative epigenetic chromatin states permissive for CENP-A or heterochromatin assembly. Otake K, Ohzeki JI, Shono N, Kugou K, Okazaki K, Nagase T, Yamakawa H, Kouprina N, Larionov V, Kimura H, Earnshaw WC, Masumoto H. J Cell Sci 133 jcs243303 (2020)
  19. FACT subunit Spt16 controls UVSSA recruitment to lesion-stalled RNA Pol II and stimulates TC-NER. Wienholz F, Zhou D, Turkyilmaz Y, Schwertman P, Tresini M, Pines A, van Toorn M, Bezstarosti K, Demmers JAA, Marteijn JA. Nucleic Acids Res 47 4011-4025 (2019)
  20. Stabilization of Nucleosomes by Histone Tails and by FACT Revealed by spFRET Microscopy. Valieva ME, Gerasimova NS, Kudryashova KS, Kozlova AL, Kirpichnikov MP, Hu Q, Botuyan MV, Mer G, Feofanov AV, Studitsky VM. Cancers (Basel) 9 E3 (2017)
  21. SSRP1 silencing inhibits the proliferation and malignancy of human glioma cells via the MAPK signaling pathway. Liao J, Tao X, Ding Q, Liu J, Yang X, Yuan FE, Yang JA, Liu B, Xiang GA, Chen Q. Oncol Rep 38 2667-2676 (2017)
  22. The nucleosome acidic patch directly interacts with subunits of the Paf1 and FACT complexes and controls chromatin architecture in vivo. Cucinotta CE, Hildreth AE, McShane BM, Shirra MK, Arndt KM. Nucleic Acids Res 47 8410-8423 (2019)
  23. Electron microscopy analysis of ATP-independent nucleosome unfolding by FACT. Sivkina AL, Karlova MG, Valieva ME, McCullough LL, Formosa T, Shaytan AK, Feofanov AV, Kirpichnikov MP, Sokolova OS, Studitsky VM. Commun Biol 5 2 (2022)
  24. Establishment and Maintenance of Chromatin Architecture Are Promoted Independently of Transcription by the Histone Chaperone FACT and H3-K56 Acetylation in Saccharomyces cerevisiae. McCullough LL, Pham TH, Parnell TJ, Connell Z, Chandrasekharan MB, Stillman DJ, Formosa T. Genetics 211 877-892 (2019)
  25. Histone chaperone FACT is essential to overcome replication stress in mammalian cells. Prendergast L, Hong E, Safina A, Poe D, Gurova K. Oncogene 39 5124-5137 (2020)
  26. Partial Replacement of Nucleosomal DNA with Human FACT Induces Dynamic Exposure and Acetylation of Histone H3 N-Terminal Tails. Tsunaka Y, Ohtomo H, Morikawa K, Nishimura Y. iScience 23 101641 (2020)
  27. Structure-specific recognition protein-1 (SSRP1) is an elongated homodimer that binds histones. Marcianò G, Da Vela S, Tria G, Svergun DI, Byron O, Huang DT. J Biol Chem 293 10071-10083 (2018)
  28. SSRP1 influences colorectal cancer cell growth and apoptosis via the AKT pathway. Wang Q, Jia S, Jiao Y, Xu L, Wang D, Chen X, Hu X, Liang H, Wen N, Zhang S, Guo B, Zhang L. Int J Med Sci 16 1573-1582 (2019)
  29. Histone Tail Dynamics in Partially Disassembled Nucleosomes During Chromatin Remodeling. Kameda T, Awazu A, Togashi Y. Front Mol Biosci 6 133 (2019)
  30. Prevention of Chromatin Destabilization by FACT Is Crucial for Malignant Transformation. Sandlesh P, Safina A, Goswami I, Prendergast L, Rosario S, Gomez EC, Wang J, Gurova KV. iScience 23 101177 (2020)
  31. The fork protection complex recruits FACT to reorganize nucleosomes during replication. Safaric B, Chacin E, Scherr MJ, Rajappa L, Gebhardt C, Kurat CF, Cordes T, Duderstadt KE. Nucleic Acids Res 50 1317-1334 (2022)
  32. FACT and Ash1 promote long-range and bidirectional nucleosome eviction at the HO promoter. Yu Y, Yarrington RM, Stillman DJ. Nucleic Acids Res 48 10877-10889 (2020)
  33. The Oligomerization Landscape of Histones. Zhao H, Winogradoff D, Dalal Y, Papoian GA. Biophys J 116 1845-1855 (2019)
  34. FACT complex gene duplicates exhibit redundant and non-redundant functions in C. elegans. Suggs BZ, Latham AL, Dawes AT, Chamberlin HM. Dev Biol 444 71-82 (2018)
  35. Histone Chaperone FACT and Curaxins: Effects on Genome Structure and Function. Chang HW, Nizovtseva EV, Razin SV, Formosa T, Gurova KV, Studitsky VM. J Cancer Metastasis Treat 5 78 (2019)
  36. NAP1-Related Protein 1 (NRP1) has multiple interaction modes for chaperoning histones H2A-H2B. Luo Q, Wang B, Wu Z, Jiang W, Wang Y, Du K, Zhou N, Zheng L, Gan J, Shen WH, Ma J, Dong A. Proc Natl Acad Sci U S A 117 30391-30399 (2020)
  37. Proteasomal Regulation of Mammalian SPT16 in Controlling Transcription. Kaja A, Adhikari A, Karmakar S, Zhang W, Rothschild G, Basu U, Batra SK, Davie JK, Bhaumik SR. Mol Cell Biol 41 e00452-20 (2021)
  38. Role of lncSLCO1C1 in gastric cancer progression and resistance to oxaliplatin therapy. Xiao YF, Li BS, Liu JJ, Wang SM, Liu J, Yang H, Hu YY, Gong CL, Li JL, Yang SM. Clin Transl Med 12 e691 (2022)
  39. Charged residues on the side of the nucleosome contribute to normal Spt16-gene interactions in budding yeast. Nyamugenda E, Cox AB, Pierce JB, Banning RC, Huynh ML, May C, Marshall S, Turkal CE, Duina AA. Epigenetics 13 1-7 (2018)
  40. H2A mono-ubiquitination differentiates FACT's functions in nucleosome assembly and disassembly. Wang YZ, Liu C, Zhao J, Yu J, Luo A, Xiao X, Dou SX, Ma L, Wang PY, Li M, Li G, Yan J, Chen P, Li W. Nucleic Acids Res 50 833-846 (2022)
  41. Phosphorylation of the FACT histone chaperone subunit SPT16 affects chromatin at RNA polymerase II transcriptional start sites in Arabidopsis. Michl-Holzinger P, Obermeyer S, Markusch H, Pfab A, Ettner A, Bruckmann A, Babl S, Längst G, Schwartz U, Tvardovskiy A, Jensen ON, Osakabe A, Berger F, Grasser KD. Nucleic Acids Res 50 5014-5028 (2022)
  42. Spt5 histone binding activity preserves chromatin during transcription by RNA polymerase II. Evrin C, Serra-Cardona A, Duan S, Mukherjee PP, Zhang Z, Labib KPM. EMBO J 41 e109783 (2022)
  43. Structural insights into the ability of nucleoplasmin to assemble and chaperone histone octamers for DNA deposition. Franco A, Arranz R, Fernández-Rivero N, Velázquez-Campoy A, Martín-Benito J, Segura J, Prado A, Valpuesta JM, Muga A. Sci Rep 9 9487 (2019)
  44. Chaperoning of the histone octamer by the acidic domain of DNA repair factor APLF. Corbeski I, Guo X, Eckhardt BV, Fasci D, Wiegant W, Graewert MA, Vreeken K, Wienk H, Svergun DI, Heck AJR, van Attikum H, Boelens R, Sixma TK, Mattiroli F, van Ingen H. Sci Adv 8 eabo0517 (2022)
  45. Chemical map-based prediction of nucleosome positioning using the Bioconductor package nuCpos. Kato H, Shimizu M, Urano T. BMC Bioinformatics 22 322 (2021)
  46. FACT maintains nucleosomes during transcription and stem cell viability in adult mice. Goswami I, Sandlesh P, Stablewski A, Toshkov I, Safina AF, Magnitov M, Wang J, Gurova K. EMBO Rep 23 e53684 (2022)
  47. The FACT complex facilitates expression of lysosomal and antioxidant genes through binding to TFEB and TFE3. Jeong E, Martina JA, Contreras PS, Lee J, Puertollano R. Autophagy 18 2333-2349 (2022)
  48. The Paramecium histone chaperone Spt16-1 is required for Pgm endonuclease function in programmed genome rearrangements. de Vanssay A, Touzeau A, Arnaiz O, Frapporti A, Phipps J, Duharcourt S. PLoS Genet 16 e1008949 (2020)
  49. Chromatin structure-dependent histone incorporation revealed by a genome-wide deposition assay. Tachiwana H, Dacher M, Maehara K, Harada A, Seto Y, Katayama R, Ohkawa Y, Kimura H, Kurumizaka H, Saitoh N. Elife 10 e66290 (2021)
  50. Parvovirus nonstructural protein 2 interacts with chromatin-regulating cellular proteins. Mattola S, Salokas K, Aho V, Mäntylä E, Salminen S, Hakanen S, Niskanen EA, Svirskaite J, Ihalainen TO, Airenne KJ, Kaikkonen-Määttä M, Parrish CR, Varjosalo M, Vihinen-Ranta M. PLoS Pathog 18 e1010353 (2022)
  51. Dominant effects of the histone mutant H3-L61R on Spt16-gene interactions in budding yeast. Pablo-Kaiser A, Tucker MG, Turner GA, Dilday EG, Olmstead AG, Tackett CL, Duina AA. Epigenetics 17 2347-2355 (2022)
  52. Evidence that dissociation of Spt16 from transcribed genes is partially dependent on RNA Polymerase II termination. Campbell JB, Edwards MJ, Ozersky SA, Duina AA. Transcription 10 195-206 (2019)
  53. FACT modulates the conformations of histone H2A and H2B N-terminal tails within nucleosomes. Tsunaka Y, Ohtomo H, Nishimura Y. Commun Biol 5 814 (2022)
  54. Histone tyrosine sulfation by SULT1B1 regulates H4R3me2a and gene transcription. Yu W, Zhou R, Li N, Lei ZC, Guo D, Peng F, Li Y, Bai X, Feng S, Wang Y, He J, Yin S, Zeng X, He L, Gao Y, Li M, Guo YR, Liu K, Wang Y. Nat Chem Biol 19 855-864 (2023)
  55. Human FACT subunits coordinate to catalyze both disassembly and reassembly of nucleosomes. McCauley MJ, Morse M, Becker N, Hu Q, Botuyan MV, Navarrete E, Huo R, Muthurajan UM, Rouzina I, Luger K, Mer G, Maher LJ, Williams MC. Cell Rep 41 111858 (2022)
  56. N-Terminal Tails of Histones H2A and H2B Differentially Affect Transcription by RNA Polymerase II In Vitro. Chang HW, Feofanov AV, Lyubitelev AV, Armeev GA, Kotova EY, Hsieh FK, Kirpichnikov MP, Shaytan AK, Studitsky VM. Cells 11 2475 (2022)
  57. SSRP1 affects the growth and apoptosis of gastric cancer cells through AKT pathway. Jin G, Zhao R, Zhang J, Cao T, Tang T. J Med Biochem 41 100-107 (2022)
  58. H2B ubiquitination recruits FACT to maintain a stable altered nucleosome state for transcriptional activation. Luo A, Kong J, Chen J, Xiao X, Lan J, Li X, Liu C, Wang PY, Li G, Li W, Chen P. Nat Commun 14 741 (2023)
  59. Mitotic Chromosome Assembly In Vitro: Functional Cross Talk between Nucleosomes and Condensins. Shintomi K, Hirano T. Cold Spring Harb Symp Quant Biol 82 157-164 (2017)
  60. Structure and Epigenetic Regulation of Chromatin Fibers. Chen P, Li G. Cold Spring Harb Symp Quant Biol 82 25-35 (2017)


Quick links