Везде

RAS BiologyБиофизика Biophysics

  • ISSN (Print) 0006-3029
  • ISSN (Online) 3034-5278

Identification of Potential SOX2 Binding Sites to Nucleosomes via Molecular Modeling

You can
PII
S30345278S0006302925030039-1
DOI
10.7868/S3034527825030039
Publication type
Article
Status
Published
Authors
T.A. Romanova
  • Affiliation: Lomonosov Moscow State University
D.M. Ryabov
  • Affiliation: Lomonosov Moscow State University
G.A. Komarova
  • Affiliation: Lomonosov Moscow State University
A.K. Shaytan
  • Affiliation: Lomonosov Moscow State University
G.A. Armeev
  • Affiliation: Lomonosov Moscow State University
Volume/ Edition
Volume 70 / Issue number 3
Pages
439-452
Abstract
The pioneer transcription factor SOX2 plays an important role in the regulation of gene expression by binding to condensed chromatin and inducing its decondensation. Experimental data on the preferred positions of SOX2 binding to DNA in the context of the nucleosome are contradictory: in some studies, binding to the inner segments of nucleosomal DNA is preferred, in others – to the edge segments. Within the framework of this work, all possible variants of SOX2 binding to nucleosomal DNA at different distances from the nucleosome center (determined by the superhelix position parameter – SHL) and different orientation of the binding site relative to the nucleosome center (determined by the SHL sign) were analyzed by molecular modeling. It was shown that on an intact nucleosome, binding is possible at positions SHL +2, SHL ±4 and SHL ±5, but if we assume a shift of nucleosomal DNA by one pair of nucleotides, binding becomes possible at positions corresponding to all integer values of SHL. This observation helps to explain part of the contradictions between the experimental data.
Keywords
хроматин нуклеосома пионерные транскрипционные факторы молекулярное моделирование
Date of publication
07.05.2025
Year of publication
2025
Number of purchasers
0
Views
46

References

  1. 1. McGinty R. K. and Tan S. Nucleosome structure and function. Chem Rev., 115 (6), 2255–2273 (2015). DOI: 10.1021/cr500373h
  2. 2. Luger K., Mäder A. W., Richmond R. K., Sargent D. F., and Richmond T. J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature, 389 (6648), 251–260 (1997). DOI: 10.1038/38444
  3. 3. Zaret K. S. Pioneer transcription factors initiating gene network changes. Annu. Rev. Genet., 54, 367–385 (2020). DOI: 10.1146/annurev-genet-030220-015007
  4. 4. Balsalobe A. and Drouin J. Pioneer factors as master regulators of the epigenome and cell fate. Nat. Rev. Mol. Cell Biol., 23 (7), 449–464 (2022). DOI: 10.1038/s41580-022-00464-z
  5. 5. Sunkel B. D. and Stanton B. Z. Pioneer factors in development and cancer. iScience, 24 (10), 103132 (2021). DOI: 10.1016/j.isci.2021.103132
  6. 6. Takahashi K. and Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell, 126 (4), 663 (2006). DOI: 10.1016/j.cell.2006.07.024
  7. 7. Reményi A., Lins K., Nissen L. J., Reinbold R., Schöler H. R., and Wilmanns M. Crystal structure of a POU/HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev., 17 (16), 2048–2059 (2003). DOI: 10.1101/gad.269303
  8. 8. Michael A. K., Grand R. S., Isbel L., Cavadini S., Kozicka Z., Kempf G., Bunker R. D., Schenk A. D., Graff-Meyer A., Pathare G. R., Weiss J., Matsumoto S., Burger L., Schübeler D., and Thornå N. H. Mechanisms of OCT4-SOX2 motif readout on nucleosomes. Science, 368 (6498), 1460–1465 (2020). DOI: 10.1126/science.abb0074
  9. 9. Malaga Gadea F. C. and Nikolova E. N. Structural plasticity of pioneer factor Sox2 and DNA bendability modulate nucleosome engagement and Sox2–Oct4 synergism. J. Mol. Biol., 435 (2), 167916 (2022). DOI: 10.1016/j.jmb.2022.167916
  10. 10. Zhu F., Fanning L., Kaasinen E., Sahu B., Yin Y., Wei B., Dodonova S. O., Nitta K. R., Morgunova E., Taipale M., Cramer P., and Taipale J. The interaction landscape between transcription factors and the nucleosome. Nature, 562 (7725), 76–81 (2018). DOI: 10.1038/s41586-018-0549-5
  11. 11. Tsompana M., Wilson P., Murugaiyan V., Handelmann Ch. R., and Buck M. J. Defining transcription factor nucleosome binding with Pioneer-seq. bioRxiv (2022). DOI: 10.1101/2022.11.11516133
  12. 12. Li S., Zheng E. B., Zhao L., and Liu S. Nonreciprocal and conditional cooperativity directs the pioneer activity of pluripotency transcription factors. Cell Rep., 28 (10), 2689–2703 (2019). DOI: 10.1016/j.celrep.2019.07.103
  13. 13. Hall M. A., Shundrovsky A., Bai L., Fulbright R. M., Lis J. T., and Wang M. D. High resolution dynamic mapping of histone-DNA interactions in a nucleosome. Nat. Struct. Mol. Biol., 16 (2), 124–129 (2009). DOI: 10.1038/nsmb.1526
  14. 14. Ozden B., Boopathi R., Barlas A. B., Lone I. N., Bednar J., Petosa C., Kale S., Hamiche A., Angelov D., Dimitrov S., and Karaca E. Molecular mechanism of nucleosome recognition by the pioneer transcription factor Sox. J. Chem. Inf. Model., 63 (12), 3839–3853 (2023). DOI: 10.1021/acs.jctm.2c01520
  15. 15. Dodonova S. O., Zhu F., Dienermann C., Taipale J., and Cramer P. Nucleosome-bound SOX2 and SOX11 structures elucidate pioneer factor function. Nature, 580, 669–672 (2020). DOI: 10.1038/s41586-020-2195-y
  16. 16. Marin-Gonzalez A., Vilhena J. G., Perez R., and Moreno-Herrero F. A molecular view of DNA flexibility. Q. Rev. Biophys., 54, 68 (2021). DOI: 10.1017/S0033583521000068
  17. 17. Tan C. and Takada S., Nucleosome allostery in pioneer transcription factor binding. Proc. Natl. Acad. Sci. USA, 117 (34), 20586–20596 (2020).
  18. 18. Nurk S., Koren S., Rhie A., Rautiainen M., Bzikadze A. V., Mikheenko A., Voliger M. R., Altemose N., Uralsky L., Gershman A., Aganezov S., Hoyt S. J., Diekhans M., Logsdon G. A., Alonge M., Antonarakis S. E., Borchers M., Bouffard G. G., Brooks S. Y., Caldas G. V., Chen N. C., Cheng H., Chin C. S., Chow W., de Lima L. G., Disluck P. C., Durbin R., Dvorkian T., Fiddes I. T., Formenti G., Fulton R. S., Fungiammasan A., Garrison E., Grady P. G. S., Graves-Lindsay T. A., Hall I. M., Hansen N. F., Hartley G. A., Haukmess M., Howe K., Hunkapiller M. W., Jain C., Jain M., Jarvis E. D., Kerpedjiev P., Kirsche M., Kolmogorov M., Korlach J., Kremitzki M., Li H., Maduro V. V., Marschall T., McCartney A. M., McDaniel J., Miller D. E., Mullikin J. C., Myers E. W., Olson N. D., Paten B., Peluso P., Pevzner P. A., Porubsky D., Potapova T., Rogev E. I., Rosenfeld J. A., Salzberg S. L., Schneider V. A., Sed-lazeck F. J., Shafir K., Shew C. J., Shumac A., Sims Y., Smit A. F. A., Soto D. C., Sovic I., Storer J. M., Streets A., Sullivan B. A., Thibaud-Nissen F., Torrance J., Wagner J., Walenz B. P., Wenger A., Wood J. M. D., Xiao C., Yan S. M., Young A. C., Zarate S., Surti U., McCoy R. C., Dennis M. Y., Alexandrov I. A., Gerton J. L., O'Neill R. J., Timp W., Zook J. M., Schatz M. C., Eichler E. E., Miga K. H., and Phillippy A. M. The complete sequence of a human genome. Science, 376 (6588), 44–53 (2022). DOI: 10.1126/science.aab6987
  19. 19. Khan A., Fornes O., Stigliani A., Gheorghe M., Castro-Mondragon J. A., van der Lee R., Bessy A., Cheney J., Kulkarni S. R., Tan G., Baranasic D., Arenillas D. J., Sandelin A., Vandepoek K., Lenhard B., Ballester B., Wasserman W. W., Parcy F., and Mathelier A. JASPAR 2018: update of the open-access database of transcription factor binding profiles and its web framework. Nucl. Acids Res., 46 (D1), D260–D266 (2018). DOI: 10.1093/nar/gkx1126. Erratum in: Nucl. Acids Res., 46 (D1), D1284 (2018). DOI: 10.1093/nar/gkx1188
  20. 20. Ambrosini G., Groux R., and Bucher P. PWMScan: a fast tool for scanning entire genomes with a position-specific weight matrix. Bioinformatics, 34 (14), 2483–2484 (2018). DOI: 10.1093/bioinformatics/bty127
  21. 21. Quinlan A. R. and Hall I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26 (6), 841–842 (2010). DOI: 10.1093/bioinformatics/btd033
  22. 22. Lu X.-J. and Olson W. K. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res., 31 (17), 5108–5121 (2003). DOI: 10.1093/nar/gkg680
  23. 23. Webb B. and Sali A. Comparative protein structure modeling using MODELLER. Curr. Protoe. Bioinform., 54, 5.6.1–5.6.37 (2016). DOI: 10.1002/cpbi.3
  24. 24. Abraham M. J., Muriola T., Schulz R., Páll S., Smith J. C., Hess B., and Lindahl E. GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25 (2015). DOI: 10.1016/j.softx.2015.06.001
  25. 25. Maier J. A., Martinez C., Kasavajhala K., Wickstrom L., Hauser K. E., and Simmerling C. ff148B: Improving the accuracy of protein side chain and backbone parameters from ff998B. J. Chem. Theory Comput., 11 (8), 3696–3713 (2015). DOI: 10.1021/acs.jctc.5b00255
  26. 26. Yoo J. and Aksimentiev A. New tricks for old dogs: improving the accuracy of biomolecular force fields by pair-specific corrections to non-bonded interactions. Phys. Chem. Chem. Phys., 20 (13), 8432–8449 (2018). DOI: 10.1039/C7CP08185E
  27. 27. Ivani I., Dans P. D., Noy A., Perez A., Faustino I., Hospital A., Walther J., Andrio P., Gorli R., Balaccanu A., Portella G., Battistini F., Gelpi J. L., Gonzalez C., Ventruscolo M., Laughton Ch. A., Harris S. A., Case D. A., and Orozco M. Parmbsci: a refined force field for DNA simulations. Nat. Methods, 13, 55–58 (2016). DOI: 10.1038/nmeth.3658
  28. 28. Bussi G., Donadio D., and Parrinello M. Canonical sampling through velocity rescaling. J. Chem. Phys., 126 (1), 014101 (2007). DOI: 10.1063/1.2408420
  29. 29. Parrinello M. and Rahman A. Polymorphic transitions in single crystals: A new molecular dynamics method. J. Appl. Phys., 52, 7182–7190 (1981). DOI: 10.1063/1.328693
  30. 30. Armeey G. A., Kniazeva A. S., Komarova G. A., Kirpichnikov M. P., and Shaytan A. K. Histone dynamics mediate DNA unwrapping and sliding in nucleosomes. Nat. Commun., 12 (1), 2387 (2021). DOI: 10.1038/s41467-021-22636-9
  31. 31. Efron B. Bootstrap methods: Another look at the jackknife. Ann. Stat., 7 (1), 1–26 (1979). DOI: 10.1214/aos/1176344552
  32. 32. Armeev G. A., Gribkova A. K., and Shaytan A. K. Nucleosome DB - a database of 3D nucleosome structures and their complexes with comparative analysis toolkit. bioRxiv (2023). DOI: 10.1101/2023.04.17.537230
  33. 33. Adams P. D., Afonine P. V., Bunkozzi G., Chen V. B., Davis I. W., Echols N., Headd J. J., Hung L. W., Kapral G. J., Grosse-Kunstleve R. W., McCoy A. J., Moriarty N. W., Geffner R., Read C. RJ., Richardson D. C., Richardson J. S., Terwilliger T. C., and Zwart P. H. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D – Biol. Crystallogr., 66 (Pt 2), 213–221 (2010). DOI: 10.1107/S0907444909052925
  34. 34. Ong M. S., Richmond T. J., and Davey C. A. DNA stretching and extreme kinking in the nucleosome core. J. Mol. Biol., 368 (4), 1067–1074 (2007). DOI: 10.1016/j.jmb.2007.02.062
  35. 35. Pranckwicene E., Hosid S., Liang N., and Ioshikhes I. Nucleosome positioning sequence patterns as packing or regulatory. PLoS Comput. Biol., 16 (1), e1007365 (2020). DOI: 10.1371/journal.pcbi.1007365
  36. 36. Armeev G. A., Moiseenko A. V., Motorin N. A., Afonin D. A., Zhao L., Vasilev V. A., Oleinikov P. D., Glukhov G. S., Peters G. S., Studitsky V. M., Feofanov A. V., Shaytan A. K., Shi X., and Sokolova O. S. Structure and dynamics of a nucleosome core particle based on Widom 603 DNA sequence. Structure, 33 (5), 948–959 (2025). DOI: 10.1016/j.str.2025.02.007
  37. 37. Nishimura M., Fujii T., Tanaka H., Maehara K., Morishima K., Shimizu M., Kobayashi Yu., Nozawa K., Takizawa Y., Sugiyama M., Ohkawa Ya., and Kurumizaka H. Genome-wide mapping and cryo-EM structural analyses of the overlapping tri-nucleosome composed of hexasome-hexasome-octasome moieties. Commun. Biol., 7, 61 (2024). DOI: 10.1038/s42003-023-05694-1
  38. 38. Cui F. and Zhurkin V. B. Structure-based analysis of DNA sequence patterns guiding nucleosome positioning. J. Biomol. Struct. Dyn., 27 (6), 821–841 (2010). DOI: 10.1080/073911010010524947
QR
Translate

Индексирование

Scopus

Scopus

Scopus

Crossref

Scopus

Higher Attestation Commission

At the Ministry of Education and Science of the Russian Federation

Scopus

Scientific Electronic Library