Towards development of the 4c-based method detecting interactions of plasmid dna with host genome

封面

如何引用文章

全文:

开放存取 开放存取
受限制的访问 ##reader.subscriptionAccessGranted##
受限制的访问 订阅存取

详细

Chromosome conformation capture techniques have revolutionized our understanding of chromatin architecture and dynamics at the genome-wide scale. In recent years, these methods have been applied to a diverse array of species, revealing fundamental principles of chromosomal organization. However, structural organization of the extrachromosomal entities, like viral genomes or plasmids, and their interactions with the host genome, remain relatively underexplored. In this work, we introduce an enhanced 4C-protocol tailored for probing plasmid DNA interactions. We design specific plasmid vector and optimize protocol to allow high detection rate of contacts between the plasmid and host DNA.

全文:

受限制的访问

作者简介

A. Yan

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

编辑信件的主要联系方式.
Email: a.yan@g.nsu.ru
俄罗斯联邦, Novosibirsk; Novosibirsk

P. Salnikov

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: a.yan@g.nsu.ru
俄罗斯联邦, Novosibirsk; Novosibirsk

M. Gridina

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: a.yan@g.nsu.ru
俄罗斯联邦, Novosibirsk; Novosibirsk

P. Belokopytova

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: a.yan@g.nsu.ru
俄罗斯联邦, Novosibirsk; Novosibirsk

V. Fishman

Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State University

Email: a.yan@g.nsu.ru
俄罗斯联邦, Novosibirsk; Novosibirsk

参考

  1. Kabirova, E., Nurislamov, A., Shadskiy, A., Smirnov, A., Popov, A., Salnikov, P., Battulin, N., and Fishman, V. (2023) Function and evolution of the loop extrusion machinery in animals, Int. J. Mol. Sci., 24, 5017, https://doi.org/10.3390/ijms24055017.
  2. Nuebler, J., Fudenberg, G., Imakaev, M., Abdennur, N., and Mirny, L. A. (2018) Chromatin organization by an interplay of loop extrusion and compartmental segregation, Proc. Natl. Acad. Sci. USA, 115, E6697-E6706, https:// doi.org/10.1073/pnas.1717730115.
  3. Fishman, V., Battulin, N., Nuriddinov, M., Maslova, A., Zlotina, A., Strunov, A., Chervyakova, D., Korablev, A., Serov, O., and Krasikova, A. (2019) 3D organization of chicken genome demonstrates evolutionary conservation of topologically associated domains and highlights unique architecture of erythrocytes’ chromatin, Nucleic Acids Res., 47, 648-665, https://doi.org/10.1093/nar/gky1103.
  4. Ryzhkova, A., Taskina, A., Khabarova, A., Fishman, V., and Battulin, N. (2021) Erythrocytes 3D genome organization in vertebrates, Sci. Rep., 11, 4414, https://doi.org/10.1038/s41598-021-83903-9.
  5. Razin, S. V., and Gavrilov, A. A. (2020) The role of liquid-liquid phase separation in the compartmentalization of cell nucleus and spatial genome organization, Biochemistry (Moscow), 85, 643-650, https://doi.org/10.1134/S0006297920060012.
  6. Kantidze, O. L., and Razin, S. V. (2020) Weak interactions in higher-order chromatin organization, Nucleic Acids Res., 48, 4614-4626, https://doi.org/10.1093/nar/gkaa261.
  7. Nuriddinov, M., and Fishman, V. (2019) C-InterSecture-a computational tool for interspecies comparison of genome architecture, Bioinformatics (Oxford, England), 35, 4912-4921, https://doi.org/10.1093/bioinformatics/btz415.
  8. Lukyanchikova, V., Nuriddinov, M., Belokopytova, P., Taskina, A., Liang, J., Reijnders, J. M. F., Ruzzante, L., Feron, R., Waterhouse, R. M., Wu, Y., Mao, C., Tu, Z., and Sharakhov, I. V. (2022) Anopheles mosquitoes reveal new principles of 3D genome organization in insects, Nat. Commun., 13, 1960, https://doi.org/10.1038/s41467-022-29599-5.
  9. Dias, J. D., Sarica, N., Cournac, A., Koszul, R., and Neuveut, C. (2022) Crosstalk between hepatitis B virus and the 3D genome structure, Viruses, 14, 445, https://doi.org/10.3390/v14020445.
  10. Tang, D., Zhao, H., Wu, Y., Peng, B., Gao, Z., Sun, Y., Duan, J., Qi, Y., Li, Y., Zhou, Z., Guo, G., Zhang, Y., Li, C., Sui, J., and Li, W. (2021) Transcriptionally inactive hepatitis B virus episome DNA preferentially resides in the vicinity of chromosome 19 in 3D host genome upon infection, Cell Rep., 35, 109288, https://doi.org/10.1016/j.celrep.2021.109288.
  11. Sokol, M., Wabl, M., Ruiz, I. R., and Pedersen, F. S. (2014) Novel principles of gamma-retroviral insertional transcription activation in murine leukemia virus-induced end-stage tumors, Retrovirology, 11, 36, https://doi.org/ 10.1186/1742-4690-11-36.
  12. Razin, S. V., Gavrilov, A. A., and Iarovaia, O. V. (2020) Modification of nuclear compartments and the 3D genome in the course of a viral infection, Acta Naturae, 12, 34-46, https://doi.org/10.32607/actanaturae.11041.
  13. Everett, R. D. (2013) The spatial organization of DNA virus genomes in the nucleus, PLoS Pathog., 9, e1003386, https://doi.org/10.1371/journal.ppat.1003386.
  14. Corpet, A., Kleijwegt, C., Roubille, S., Juillard, F., Jacquet, K., Texier, P., and Lomonte, P. (2020) PML nuclear bodies and chromatin dynamics: catch me if you can! Nucleic Acids Res., 48, 11890-11912, https://doi.org/10.1093/nar/gkaa828.
  15. Rai, T. S., Glass, M., Cole, J. J., Rather, M. I., Marsden, M., Neilson, M., Brock, C., Humphreys, I., Everett, R., and Adams, P. (2017) Histone chaperone HIRA deposits histone H3.3 onto foreign viral DNA and contributes to anti-viral intrinsic immunity, Nucleic Acids Res., 45, 11673-11683, https://doi.org/10.1093/nar/gkx771.
  16. Schmid, M., Speiseder, T., Dobner, T., and Gonzalez, R. A. (2014) DNA virus replication compartments, J. Virol., 88, 1404-1420, https://doi.org/10.1128/JVI.02046-13.
  17. Charman, M., and Weitzman, M. D. (2020) Replication compartments of DNA viruses in the nucleus: location, location, location, Viruses, 12, 151, https://doi.org/10.3390/v12020151.
  18. Kempfer, R., and Pombo, A. (2020) Methods for mapping 3D chromosome architecture, Nat. Rev. Genet., 21, 207-226, https://doi.org/10.1038/s41576-019-0195-2.
  19. Belaghzal, H., Dekker, J., and Gibcus, J. H. (2017) Hi-C 2.0: an optimized Hi-C procedure for high-resolution genome-wide mapping of chromosome conformation, Methods, 123, 56-65, https://doi.org/10.1016/j.ymeth.2017.04.004.
  20. Gridina, M., Mozheiko, E., Valeev, E., Nazarenko, L. P., Lopatkina, M. E., Markova, Z. G., Yablonskaya, M. I., Voinova, V. Y., Shilova, N. V., Lebedev, I. N., and Fishman, V. (2021) A cookbook for DNase Hi-C, Epigenet. Chromatin, 14, 15, https://doi.org/10.1186/s13072-021-00389-5.
  21. Gvritishvili, A. G., Leung, K. W., and Tombran-Tink, J. (2010) Codon preference optimization increases heterologous PEDF expression, PLoS One, 5, e15056, https://doi.org/10.1371/journal.pone.0015056.
  22. Prajapati, H. K., Kumar, D., Yang, X.-M., Ma, C.-H., Mittal, P., Jayaram, M., and Ghosh, S. (2020) Hitchhiking on condensed chromatin promotes plasmid persistence in yeast without perturbing chromosome function, bioRxiv, https://doi.org/10.1101/2020.06.08.139568.
  23. Gracey Maniar, L. E., Maniar, J. M., Chen, Z.-Y., Lu, J., Fire, A. Z., and Kay, M. A. (2013) Minicircle DNA vectors achieve sustained expression reflected by active chromatin and transcriptional level, Mol. Ther., 21, 131-138, https:// doi.org/10.1038/mt.2012.244.
  24. Dean, D. A. (1997) Import of plasmid DNA into the nucleus is sequence specific, Exp. Cell Res., 230, 293-302, https://doi.org/10.1006/excr.1996.3427.
  25. Mladenova, V., Mladenov, E., and Russev, G. (2009) Organization of plasmid DNA into nucleosome-like structures after transfection in eukaryotic cells, Biotechnol. Biotechnolog. Equip., 23, 1044-1047, https://doi.org/10.1080/ 13102818.2009.10817609.
  26. Hildebrand, E. M., and Dekker, J. (2020) Mechanisms and functions of chromosome compartmentalization, Trends Biochem. Sci., 45, 385-396, https://doi.org/10.1016/j.tibs.2020.01.002.
  27. Erdel, F., and Rippe, K. (2018) Formation of chromatin subcompartments by phase separation, Biophys. J., 114, 2262-2270, https://doi.org/10.1016/j.bpj.2018.03.011.
  28. Ogiyama, Y., Schuettengruber, B., Papadopoulos, G. L., Chang, J.-M., and Cavalli, G. (2018) Polycomb-dependent chromatin looping contributes to gene silencing during Drosophila development, Mol. Cell, 71, 73-88.e5, https:// doi.org/10.1016/j.molcel.2018.05.032.
  29. Mattei, A. L., Bailly, N., and Meissner, A. (2022) DNA methylation: a historical perspective, Trends Genet., 38, 676-707, https://doi.org/10.1016/j.tig.2022.03.010.
  30. Rountree, M. R., and Selker, E. U. (2010) DNA methylation and the formation of heterochromatin in Neurospora crassa, Heredity, 105, 38-44, https://doi.org/10.1038/hdy.2010.44.
  31. Phillips, J. E., and Corces, V. G. (2009) CTCF: master weaver of the genome, Cell, 137, 1194-1211, https:// doi.org/10.1016/j.cell.2009.06.001.
  32. Singatulina, A. S., Hamon, L., Sukhanova, M. V., Desforges, B., Joshi, V., Bouhss, A., Lavrik, O. V., and Pastre, D. (2019) PARP-1 activation directs FUS to DNA damage sites to form PARG-reversible compartments enriched in damaged DNA, Cell Rep., 27, 1809-1821, https://doi.org/10.1016/j.celrep.2019.04.031.

补充文件

附件文件
动作
1. JATS XML
下载
2. Fig. 1. Design of the 4C experiment with a plasmid vector. a – General design of the experiment (I–VI). b – Scheme of the arrangement of restriction sites of the plasmid vectors used in this work. The maps and sequences of the plasmids are presented in Fig. A1–A3 and in Text 2 in Appendix

下载 (1MB)
索引源数据
3. Fig. 2. Estimation of the proportion of “random” contacts. a – Experimental scheme: plasmid #1 was transfected into HEK293T cells (I), then spatial contacts of DNA and proteins in the nucleus were fixed with formaldehyde (II). Fixed Mus musculus fibroblasts (III), plasmid #2 (IV) were added to the resulting sample and a 4C experiment was performed. b – Plasmid #1 and plasmid #2 differ in the ratio of the number of contacts with the chromatin of H. sapiens and M. musculus. The diagrams show the percentage of plasmid contacts with the corresponding chromatin, averaged over three independent experiments. The results for individual replicates are presented in Fig. A4 in the Appendix. The total number of contacts is taken as 100%.

下载 (614KB)
索引源数据

版权所有 © Russian Academy of Sciences, 2024