5y0d › Citations

Cancer-associated mutations of histones H2B, H3.1 and H2A.Z.1 affect the structure and stability of the nucleosome.

Arimura Y, Ikura M, Fujita R, Noda M, Kobayashi W, Horikoshi N, Sun J, Shi L, Kusakabe M, Harata M, Ohkawa Y, Tashiro S, Kimura H, Ikura T, Kurumizaka H
Nucleic Acids Res 46 10007-10018 (2018)
Related entries: 5y0c, 5z30

Cited: 52 times
EuropePMC logo PMID: 30053102

Abstract

Mutations of the Glu76 residue of canonical histone H2B are frequently found in cancer cells. However, it is quite mysterious how a single amino acid substitution in one of the multiple H2B genes affects cell fate. Here we found that the H2B E76K mutation, in which Glu76 is replaced by Lys (E76K), distorted the interface between H2B and H4 in the nucleosome, as revealed by the crystal structure and induced nucleosome instability in vivo and in vitro. Exogenous production of the H2B E76K mutant robustly enhanced the colony formation ability of the expressing cells, indicating that the H2B E76K mutant has the potential to promote oncogenic transformation in the presence of wild-type H2B. We found that other cancer-associated mutations of histones, H3.1 E97K and H2A.Z.1 R80C, also induced nucleosome instability. Interestingly, like the H2B E76K mutant, the H3.1 E97K mutant was minimally incorporated into chromatin in cells, but it enhanced the colony formation ability. In contrast, the H2A.Z.1 R80C mutant was incorporated into chromatin in cells, and had minor effects on the colony formation ability of the cells. These characteristics of histones with cancer-associated mutations may provide important information toward understanding how the mutations promote cancer progression.

Reviews - 5y0d mentioned but not cited (1)

  1. Chromatin structure related to oncogenesis. Matsumoto S, Horikoshi N, Takizawa Y, Kurumizaka H. Cancer Sci 114 3068-3075 (2023)

Articles - 5y0d mentioned but not cited (3)

  1. Cancer-associated mutations of histones H2B, H3.1 and H2A.Z.1 affect the structure and stability of the nucleosome. Arimura Y, Ikura M, Fujita R, Noda M, Kobayashi W, Horikoshi N, Sun J, Shi L, Kusakabe M, Harata M, Ohkawa Y, Tashiro S, Kimura H, Ikura T, Kurumizaka H. Nucleic Acids Res 46 10007-10018 (2018)
  2. Letter Limitations of the iterative electron density reconstruction algorithm from solution scattering data. Konarev PV, Svergun DI. Nat Methods 18 244-245 (2021)
  3. Letter Reply to: Limitations of the iterative electron density reconstruction algorithm from solution scattering data. Grant TD. Nat Methods 18 246-248 (2021)


Reviews citing this publication (13)

  1. 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)
  2. The epigenomics of sarcoma. Nacev BA, Jones KB, Intlekofer AM, Yu JSE, Allis CD, Tap WD, Ladanyi M, Nielsen TO. Nat Rev Cancer 20 608-623 (2020)
  3. Histone Variants: Guardians of Genome Integrity. Ferrand J, Rondinelli B, Polo SE. Cells 9 E2424 (2020)
  4. Physical Nature of Chromatin in the Nucleus. Maeshima K, Iida S, Tamura S. Cold Spring Harb Perspect Biol 13 a040675 (2021)
  5. The dark side of histones: genomic organization and role of oncohistones in cancer. Amatori S, Tavolaro S, Gambardella S, Fanelli M. Clin Epigenetics 13 71 (2021)
  6. Oncohistone Mutations in Diffuse Intrinsic Pontine Glioma. Zhang X, Zhang Z. Trends Cancer 5 799-808 (2019)
  7. Histone H1 Mutations in Lymphoma: A Link(er) between Chromatin Organization, Developmental Reprogramming, and Cancer. Soshnev AA, Allis CD, Cesarman E, Melnick AM. Cancer Res 81 6061-6070 (2021)
  8. Oncohistones: Exposing the nuances and vulnerabilities of epigenetic regulation. Mitchener MM, Muir TW. Mol Cell 82 2925-2938 (2022)
  9. Histone H2B Mutations in Cancer. Wan YCE, Chan KM. Biomedicines 9 694 (2021)
  10. Histone variants: The unsung guardians of the genome. Phillips EON, Gunjan A. DNA Repair (Amst) 112 103301 (2022)
  11. Nucleosome proteostasis and histone turnover. Arrieta A, Vondriska TM. Front Mol Biosci 9 990006 (2022)
  12. Small round cell sarcomas. Cidre-Aranaz F, Watson S, Amatruda JF, Nakamura T, Delattre O, de Alava E, Dirksen U, Grünewald TGP. Nat Rev Dis Primers 8 66 (2022)
  13. (B)On(e)-cohistones and the epigenetic alterations at the root of bone cancer. Salomoni P, Flanagan AM, Cottone L. Cell Death Differ (2023)

Articles citing this publication (35)

  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. Distinct Structures and Dynamics of Chromatosomes with Different Human Linker Histone Isoforms. Zhou BR, Feng H, Kale S, Fox T, Khant H, de Val N, Ghirlando R, Panchenko AR, Bai Y. Mol Cell 81 166-182.e6 (2021)
  3. A Mutation in Histone H2B Represents a New Class of Oncogenic Driver. Bennett RL, Bele A, Small EC, Will CM, Nabet B, Oyer JA, Huang X, Ghosh RP, Ghosh RP, Grzybowski AT, Yu T, Zhang Q, Riva A, Lele TP, Schatz GC, Kelleher NL, Ruthenburg AJ, Liphardt J, Licht JD. Cancer Discov 9 1438-1451 (2019)
  4. Comprehensive nucleosome interactome screen establishes fundamental principles of nucleosome binding. Skrajna A, Goldfarb D, Kedziora KM, Cousins EM, Grant GD, Spangler CJ, Barbour EH, Yan X, Hathaway NA, Brown NG, Cook JG, Major MB, McGinty RK. Nucleic Acids Res 48 9415-9432 (2020)
  5. A basic motif anchoring ISWI to nucleosome acidic patch regulates nucleosome spacing. Dao HT, Dul BE, Dann GP, Liszczak GP, Muir TW. Nat Chem Biol 16 134-142 (2020)
  6. Oncohistone mutations enhance chromatin remodeling and alter cell fates. Bagert JD, Mitchener MM, Patriotis AL, Dul BE, Wojcik F, Nacev BA, Feng L, Allis CD, Muir TW. Nat Chem Biol 17 403-411 (2021)
  7. Bridging of nucleosome-proximal DNA double-strand breaks by PARP2 enhances its interaction with HPF1. Gaullier G, Roberts G, Muthurajan UM, Bowerman S, Rudolph J, Mahadevan J, Jha A, Rae PS, Luger K. PLoS One 15 e0240932 (2020)
  8. Short H2A histone variants are expressed in cancer. Chew GL, Bleakley M, Bradley RK, Malik HS, Henikoff S, Molaro A, Sarthy J. Nat Commun 12 490 (2021)
  9. Structural features of nucleosomes in interphase and metaphase chromosomes. Arimura Y, Shih RM, Froom R, Funabiki H. Mol Cell 81 4377-4397.e12 (2021)
  10. The CENP-A centromere targeting domain facilitates H4K20 monomethylation in the nucleosome by structural polymorphism. Arimura Y, Tachiwana H, Takagi H, Hori T, Kimura H, Fukagawa T, Kurumizaka H. Nat Commun 10 576 (2019)
  11. Letter Cancer-associated histone mutation H2BG53D disrupts DNA-histone octamer interaction and promotes oncogenic phenotypes. Wan YCE, Leung TCS, Ding D, Sun X, Liu J, Zhu L, Kang TZE, Yang D, Zhang Y, Zhang J, Qian C, Huen MSY, Li Q, Chow MZY, Zheng Z, Han J, Goel A, Wang X, Ishibashi T, Chan KM. Signal Transduct Target Ther 5 27 (2020)
  12. Histone variant H2A.B-H2B dimers are spontaneously exchanged with canonical H2A-H2B in the nucleosome. Hirano R, Arimura Y, Kujirai T, Shibata M, Okuda A, Morishima K, Inoue R, Sugiyama M, Kurumizaka H. Commun Biol 4 191 (2021)
  13. The elevated transcription of ADAM19 by the oncohistone H2BE76K contributes to oncogenic properties in breast cancer. Kang TZE, Zhu L, Yang D, Ding D, Zhu X, Wan YCE, Liu J, Ramakrishnan S, Chan LL, Chan SY, Wang X, Gan H, Han J, Ishibashi T, Li Q, Chan KM. J Biol Chem 296 100374 (2021)
  14. Evaluation of nucleosome concentrations in healthy dogs and dogs with cancer. Wilson-Robles H, Miller T, Jarvis J, Terrell J, Dewsbury N, Kelly T, Herzog M, Bygott T, Hardat N, Michel G. PLoS One 15 e0236228 (2020)
  15. Novel Classes and Evolutionary Turnover of Histone H2B Variants in the Mammalian Germline. Raman P, Rominger MC, Young JM, Molaro A, Tsukiyama T, Malik HS. Mol Biol Evol 39 msac019 (2022)
  16. Characterizing circulating nucleosomes in the plasma of dogs with hemangiosarcoma. Wilson-Robles H, Miller T, Jarvis J, Terrell J, Kelly TK, Bygott T, Bougoussa M. BMC Vet Res 17 231 (2021)
  17. Characterizing circulating nucleosomes in the plasma of dogs with lymphoma. Dolan C, Miller T, Jill J, Terrell J, Kelly TK, Bygott T, Wilson-Robles H. BMC Vet Res 17 276 (2021)
  18. Gene Expression Signature of BRAF Inhibitor Resistant Melanoma Spheroids. Koroknai V, Patel V, Szász I, Ádány R, Balazs M. Pathol Oncol Res 26 2557-2566 (2020)
  19. Structural basis for p53 binding to its nucleosomal target DNA sequence. Nishimura M, Takizawa Y, Nozawa K, Kurumizaka H. PNAS Nexus 1 pgac177 (2022)
  20. Evaluation of plasma nucleosome concentrations in dogs with a variety of common cancers and in healthy dogs. Wilson-Robles HM, Bygott T, Kelly TK, Miller TM, Miller P, Matsushita M, Terrell J, Bougoussa M, Butera T. BMC Vet Res 18 329 (2022)
  21. Inhibition of histone H3-H4 chaperone pathways rescues C. elegans sterility by H2B loss. Zhao R, Zhu Z, Geng R, Jiang X, Li W, Ou G. PLoS Genet 18 e1010223 (2022)
  22. Structural basis of paralog-specific KDM2A/B nucleosome recognition. Spangler CJ, Skrajna A, Foley CA, Nguyen A, Budziszewski GR, Azzam DN, Arteaga EC, Simmons HC, Smith CB, Wesley NA, Wilkerson EM, McPherson JE, Kireev D, James LI, Frye SV, Goldfarb D, McGinty RK. Nat Chem Biol 19 624-632 (2023)
  23. Analysis of histone variant constraint and tissue expression suggests five potential novel human disease genes: H2AFY2, H2AFZ, H2AFY, H2AFV, H1F0. Lubin E, Bryant L, Aicher J, Li D, Bhoj E. Hum Genet 141 1409-1421 (2022)
  24. Deform-nu: A DNA Deformation Energy-Based Predictor for Nucleosome Positioning. Liu G, Zhao H, Meng H, Xing Y, Yang H, Lin H. Front Cell Dev Biol 8 596341 (2020)
  25. Placental proteome in late‑onset of fetal growth restriction. Gęca T, Stupak A, Nawrot R, Goździcka-Józefiak A, Kwaśniewska A, Kwaśniewski W. Mol Med Rep 26 356 (2022)
  26. Aclarubicin stimulates RNA polymerase II elongation at closely spaced divergent promoters. Wooten M, Takushi B, Ahmad K, Henikoff S. Sci Adv 9 eadg3257 (2023)
  27. Competitive Chemical Reaction Kinetic Model of Nucleosome Assembly Using the Histone Variant H2A.Z and H2A In Vitro. Zhao H, Shao X, Guo M, Xing Y, Wang J, Luo L, Cai L. Int J Mol Sci 24 15846 (2023)
  28. Systematic Review Contribution of histone variants to aneuploidy: a cancer perspective. Ragusa D, Vagnarelli P. Front Genet 14 1290903 (2023)
  29. Genome-wide mapping and cryo-EM structural analyses of the overlapping tri-nucleosome composed of hexasome-hexasome-octasome moieties. Nishimura M, Fujii T, Tanaka H, Maehara K, Morishima K, Shimizu M, Kobayashi Y, Nozawa K, Takizawa Y, Sugiyama M, Ohkawa Y, Kurumizaka H. Commun Biol 7 61 (2024)
  30. Histone mutations in cancer. Espinoza Pereira KN, Shan J, Licht JD, Bennett RL. Biochem Soc Trans 51 1749-1763 (2023)
  31. Leveraging Gene Redundancy to Find New Histone Drivers in Cancer. Ostroverkhova D, Espiritu D, Aristizabal MJ, Panchenko AR. Cancers (Basel) 15 3437 (2023)
  32. Monitoring plasma nucleosome concentrations to measure disease response and progression in dogs with hematopoietic malignancies. Wilson-Robles H, Warry E, Miller T, Jarvis J, Matsushita M, Miller P, Herzog M, Turatsinze JV, Kelly TK, Butera ST, Michel G. PLoS One 18 e0281796 (2023)
  33. Nucleosome Assembly and Disassembly in vitro Are Governed by Chemical Kinetic Principles. Zhao H, Guo M, Zhang F, Shao X, Liu G, Xing Y, Zhao X, Luo L, Cai L. Front Cell Dev Biol 9 762571 (2021)
  34. Pan-cancer atlas of somatic core and linker histone mutations. Bonner ER, Dawood A, Gordish-Dressman H, Eze A, Bhattacharya S, Yadavilli S, Mueller S, Waszak SM, Nazarian J. NPJ Genom Med 8 23 (2023)
  35. Stochastic nucleosome disassembly mediated by remodelers and histone fragmentation. Li X, Chou T. J Chem Phys 159 204107 (2023)


Quick links