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Current Protein & Peptide Science

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ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

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Review Article

Phase Separation of Chromatin Structure-related Biomolecules: A Driving Force for Epigenetic Regulations

Author(s): Jiao Wang, Yuchen Chen*, Zixuan Xiao, Xikai Liu, Chengyu Liu, Kun Huang and Hong Chen*

Volume 25, Issue 7, 2024

Published on: 27 March, 2024

Page: [553 - 566] Pages: 14

DOI: 10.2174/0113892037296216240301074253

Price: $65

Abstract

Intracellularly, membrane-less organelles are formed by spontaneous fusion and fission of macro-molecules in a process called phase separation, which plays an essential role in cellular activities. In certain disease states, such as cancers and neurodegenerative diseases, aberrant phase separations take place and participate in disease progression. Chromatin structure-related proteins, based on their characteristics and upon external stimuli, phase separate to exert functions like genome assembly, transcription regulation, and signal transduction. Moreover, many chromatin structure-related proteins, such as histones, histone-modifying enzymes, DNA-modifying enzymes, and DNA methylation binding proteins, are involved in epigenetic regulations through phase separation. This review introduces phase separation and how phase separation affects epigenetics with a focus on chromatin structure-related molecules.

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[1]
Pantoja, C.F.; Zweckstetter, M.; Rezaei-Ghaleh, N. Dynamical component exchange in a model phase separating system: An NMR-based approach. Phys. Chem. Chem. Phys., 2022, 24(10), 6169-6175.
[http://dx.doi.org/10.1039/D2CP00042C] [PMID: 35229098]
[2]
Mudogo, C.N.; Falke, S.; Brognaro, H.; Duszenko, M.; Betzel, C. Protein phase separation and determinants of in cell crystallization. Traffic, 2020, 21(2), 220-230.
[http://dx.doi.org/10.1111/tra.12711] [PMID: 31664760]
[3]
Bloom, K.; Kolbin, D. Mechanisms of DNA mobilization and sequestration. Genes, 2022, 13(2), 352.
[http://dx.doi.org/10.3390/genes13020352] [PMID: 35205396]
[4]
Comert, F.; Dubin, P.L. Liquid-liquid and liquid-solid phase separation in protein-polyelectrolyte systems. Adv. Colloid Interface Sci., 2017, 239, 213-217.
[http://dx.doi.org/10.1016/j.cis.2016.08.005] [PMID: 27773339]
[5]
Rippe, K. Liquid–liquid phase separation in chromatin. Cold Spring Harb. Perspect. Biol., 2022, 14(2), a040683.
[http://dx.doi.org/10.1101/cshperspect.a040683] [PMID: 34127447]
[6]
Lei, Z.; Wang, L.; Kim, E.Y.; Cho, J. Phase separation of chromatin and small RNA pathways in plants. Plant J., 2021, 108(5), 1256-1265.
[http://dx.doi.org/10.1111/tpj.15517] [PMID: 34585805]
[7]
Nsengimana, B.; Khan, F.A.; Awan, U.A.; Wang, D.; Fang, N.; Wei, W.; Zhang, W.; Ji, S. Pseudogenes and liquid phase separation in epigenetic expression. Front. Oncol., 2022, 12, 912282.
[http://dx.doi.org/10.3389/fonc.2022.912282] [PMID: 35875144]
[8]
Lee, D.S.W.; Strom, A.R.; Brangwynne, C.P. The mechanobiology of nuclear phase separation. APL Bioeng., 2022, 6(2), 021503.
[http://dx.doi.org/10.1063/5.0083286] [PMID: 35540725]
[9]
Li, X.; An, Z.; Zhang, W.; Li, F. Phase separation: Direct and indirect driving force for high-order chromatin organization. Genes, 2023, 14(2), 499.
[http://dx.doi.org/10.3390/genes14020499] [PMID: 36833426]
[10]
Aguzzi, A.; Altmeyer, M. Phase separation: Linking cellular compartmentalization to disease. Trends Cell Biol., 2016, 26(7), 547-558.
[http://dx.doi.org/10.1016/j.tcb.2016.03.004] [PMID: 27051975]
[11]
Shen, C.; Li, R.; Negro, R.; Cheng, J.; Vora, S.M.; Fu, T.M.; Wang, A.; He, K.; Andreeva, L.; Gao, P.; Tian, Z.; Flavell, R.A.; Zhu, S.; Wu, H. Phase separation drives RNA virus-induced activation of the NLRP6 inflammasome. Cell, 2021, 184(23), 5759-5774.e20.
[http://dx.doi.org/10.1016/j.cell.2021.09.032] [PMID: 34678144]
[12]
Alberti, S.; Hyman, A.A. Biomolecular condensates at the nexus of cellular stress, protein aggregation disease and ageing. Nat. Rev. Mol. Cell Biol., 2021, 22(3), 196-213.
[http://dx.doi.org/10.1038/s41580-020-00326-6] [PMID: 33510441]
[13]
Liu, Z.; Qin, Z.; Liu, Y.; Xia, X.; He, L.; Chen, N.; Hu, X.; Peng, X. Liquid‒liquid phase separation: Roles and implications in future cancer treatment. Int. J. Biol. Sci., 2023, 19(13), 4139-4156.
[http://dx.doi.org/10.7150/ijbs.81521] [PMID: 37705755]
[14]
Bhat, P.; Honson, D.; Guttman, M. Nuclear compartmentalization as a mechanism of quantitative control of gene expression. Nat. Rev. Mol. Cell Biol., 2021, 22(10), 653-670.
[http://dx.doi.org/10.1038/s41580-021-00387-1] [PMID: 34341548]
[15]
Li, J.; Gao, J.; Wang, R. Control of chromatin organization and chromosome behavior during the cell cycle through phase separation. Int. J. Mol. Sci., 2021, 22(22), 12271.
[http://dx.doi.org/10.3390/ijms222212271] [PMID: 34830152]
[16]
Pessina, F.; Gioia, U.; Brandi, O.; Farina, S.; Ceccon, M.; Francia, S.; d’Adda di Fagagna, F. DNA damage triggers a new phase in neurodegeneration. Trends Genet., 2021, 37(4), 337-354.
[http://dx.doi.org/10.1016/j.tig.2020.09.006] [PMID: 33020022]
[17]
Zhang, Y.; Kutateladze, T.G. Liquid–liquid phase separation is an intrinsic physicochemical property of chromatin. Nat. Struct. Mol. Biol., 2019, 26(12), 1085-1086.
[http://dx.doi.org/10.1038/s41594-019-0333-8] [PMID: 31695191]
[18]
Ling, X.; Liu, X.; Jiang, S.; Fan, L.; Ding, J. The dynamics of three-dimensional chromatin organization and phase separation in cell fate transitions and diseases. Cell Regen., 2022, 11(1), 42.
[http://dx.doi.org/10.1186/s13619-022-00145-4] [PMID: 36539553]
[19]
Aulas, A.; Finetti, P.; Lyons, S.M.; Bertucci, F.; Birnbaum, D.; Acquaviva, C.; Mamessier, E. Revisiting the concept of stress in the prognosis of solid tumors: A role for stress granules proteins? Cancers, 2020, 12(9), 2470.
[http://dx.doi.org/10.3390/cancers12092470] [PMID: 32882814]
[20]
Wang, B.; Zhang, L.; Dai, T.; Qin, Z.; Lu, H.; Zhang, L.; Zhou, F. Liquid–liquid phase separation in human health and diseases. Signal Transduct. Target. Ther., 2021, 6(1), 290.
[http://dx.doi.org/10.1038/s41392-021-00678-1] [PMID: 34334791]
[21]
Alberti, S.; Gladfelter, A.; Mittag, T. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell, 2019, 176(3), 419-434.
[http://dx.doi.org/10.1016/j.cell.2018.12.035] [PMID: 30682370]
[22]
McSwiggen, D.T.; Mir, M.; Darzacq, X.; Tjian, R. Evaluating phase separation in live cells: Diagnosis, caveats, and functional consequences. Genes Dev., 2019, 33(23-24), 1619-1634.
[http://dx.doi.org/10.1101/gad.331520.119] [PMID: 31594803]
[23]
Liu, X.; Jiang, S.; Ma, L.; Qu, J.; Zhao, L.; Zhu, X.; Ding, J. Time-dependent effect of 1,6-hexanediol on biomolecular condensates and 3D chromatin organization. Genome Biol., 2021, 22(1), 230.
[http://dx.doi.org/10.1186/s13059-021-02455-3] [PMID: 34404453]
[24]
Bousios, A.; Gaut, B.S.; Darzentas, N. Considerations and complications of mapping small RNA high-throughput data to transposable elements. Mob. DNA, 2017, 8(1), 3.
[http://dx.doi.org/10.1186/s13100-017-0086-z] [PMID: 28228849]
[25]
Wang, J.; Choi, J.M.; Holehouse, A.S.; Lee, H.O.; Zhang, X.; Jahnel, M.; Maharana, S.; Lemaitre, R.; Pozniakovsky, A.; Drechsel, D.; Poser, I.; Pappu, R.V.; Alberti, S.; Hyman, A.A. A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins. Cell, 2018, 174(3), 688-699.
[http://dx.doi.org/10.1016/j.cell.2018.06.006] [PMID: 29961577]
[26]
Hazawa, M.; Amemori, S.; Nishiyama, Y.; Iga, Y.; Iwashima, Y.; Kobayashi, A.; Nagatani, H.; Mizuno, M.; Takahashi, K.; Wong, R.W. A light-switching pyrene probe to detect phase-separated biomolecules. iScience, 2021, 24(8), 102865.
[http://dx.doi.org/10.1016/j.isci.2021.102865] [PMID: 34386728]
[27]
Uversky, V.N. Analyzing IDPs in interactomes. Methods Mol. Biol., 2020, 2141, 895-945.
[http://dx.doi.org/10.1007/978-1-0716-0524-0_46] [PMID: 32696395]
[28]
Mészáros, B.; Erdős, G.; Szabó, B.; Schád, É.; Tantos, Á.; Abukhairan, R.; Horváth, T.; Murvai, N.; Kovács, O.P.; Kovács, M.; Tosatto, S.C.E.; Tompa, P.; Dosztányi, Z.; Pancsa, R. PhaSePro: The database of proteins driving liquid-liquid phase separation. Nucleic Acids Res., 2020, 48(D1), D360-D367.
[PMID: 31612960]
[29]
Li, Q.; Wang, X.; Dou, Z.; Yang, W.; Huang, B.; Lou, J.; Zhang, Z. Protein databases related to liquid–liquid phase separation. Int. J. Mol. Sci., 2020, 21(18), 6796.
[http://dx.doi.org/10.3390/ijms21186796] [PMID: 32947964]
[30]
Wang, X.; Niu, J.; Yang, Y.; Wang, Y.; Sun, Y. SMART FRAP: A robust and quantitative FRAP analysis method for phase separation. Chem. Commun., 2023, 59(16), 2307-2310.
[http://dx.doi.org/10.1039/D2CC06398K] [PMID: 36748184]
[31]
Chen, Q.; Zhao, L.; Soman, A.; Arkhipova, A.Y.; Li, J.; Li, H.; Chen, Y.; Shi, X.; Nordenskiöld, L. Chromatin liquid–liquid phase separation (LLPS) is regulated by ionic conditions and fiber length. Cells, 2022, 11(19), 3145.
[http://dx.doi.org/10.3390/cells11193145] [PMID: 36231107]
[32]
Mimura, M.; Tomita, S.; Sugai, H.; Shinkai, Y.; Ishihara, S.; Kurita, R. Uncharged components of single-stranded dna modulate liquid–liquid phase separation with cationic linker histone H1. Front. Cell Dev. Biol., 2021, 9, 710729.
[http://dx.doi.org/10.3389/fcell.2021.710729] [PMID: 34422830]
[33]
Hammonds, E.F.; Harwig, M.C.; Paintsil, E.A.; Tillison, E.A.; Hill, R.B.; Morrison, E.A. Histone H3 and H4 tails play an important role in nucleosome phase separation. Biophys. Chem., 2022, 283, 106767.
[http://dx.doi.org/10.1016/j.bpc.2022.106767] [PMID: 35158124]
[34]
Hagihara, Y.; Asada, S.; Maeda, T.; Nakano, T.; Yamaguchi, S. Tet1 regulates epigenetic remodeling of the pericentromeric heterochromatin and chromocenter organization in DNA hypomethylated cells. PLoS Genet., 2021, 17(6), e1009646.
[http://dx.doi.org/10.1371/journal.pgen.1009646] [PMID: 34166371]
[35]
Wang, L.; Hu, M.; Zuo, M.Q.; Zhao, J.; Wu, D.; Huang, L.; Wen, Y.; Li, Y.; Chen, P.; Bao, X.; Dong, M.Q.; Li, G.; Li, P. Rett syndrome-causing mutations compromise MeCP2-mediated liquid–liquid phase separation of chromatin. Cell Res., 2020, 30(5), 393-407.
[http://dx.doi.org/10.1038/s41422-020-0288-7] [PMID: 32111972]
[36]
Jiang, Y.; Fu, X.; Zhang, Y.; Wang, S.F.; Zhu, H.; Wang, W.K.; Zhang, L.; Wu, P.; Wong, C.C.L.; Li, J.; Ma, J.; Guan, J.S.; Huang, Y.; Hui, J. Rett syndrome linked to defects in forming the MeCP2/Rbfox/LASR complex in mouse models. Nat. Commun., 2021, 12(1), 5767.
[http://dx.doi.org/10.1038/s41467-021-26084-3] [PMID: 34599184]
[37]
Jiang, S.; Fagman, J.B.; Chen, C.; Alberti, S.; Liu, B. Protein phase separation and its role in tumorigenesis. eLife, 2020, 9, e60264.
[http://dx.doi.org/10.7554/eLife.60264] [PMID: 33138914]
[38]
Egan, G.; Schimmer, A.D. Contribution of metabolic abnormalities to acute myeloid leukemia pathogenesis. Trends Cell Biol., 2023, 33(6), 455-462.
[http://dx.doi.org/10.1016/j.tcb.2022.11.004] [PMID: 36481232]
[39]
Gonskikh, Y.; Stoute, J.; Shen, H.; Budinich, K.; Pingul, B.; Schultz, K.; Elashal, H.; Marmorstein, R.; Shi, J.; Liu, K.F. Noncatalytic regulation of 18 S rRNA methyltransferase DIMT1 in acute myeloid leukemia. Genes Dev., 2023, 37(7-8), 321-335.
[http://dx.doi.org/10.1101/gad.350298.122] [PMID: 37024283]
[40]
Papageorgiou, S.; Pashley, S.L.; O’Regan, L.; Khan, S.; Bayliss, R.; Fry, A.M. Alternative treatment options to ALK inhibitor monotherapy for eml4-alk-driven lung cancer. Cancers, 2022, 14(14), 3452.
[http://dx.doi.org/10.3390/cancers14143452] [PMID: 35884511]
[41]
Qin, Z.; Sun, H.; Yue, M.; Pan, X.; Chen, L.; Feng, X.; Yan, X.; Zhu, X.; Ji, H. Phase separation of EML4–ALK in firing downstream signaling and promoting lung tumorigenesis. Cell Discov., 2021, 7(1), 33.
[http://dx.doi.org/10.1038/s41421-021-00270-5] [PMID: 33976114]
[42]
Zois, C.E.; Favaro, E.; Harris, A.L. Glycogen metabolism in cancer. Biochem. Pharmacol., 2014, 92(1), 3-11.
[http://dx.doi.org/10.1016/j.bcp.2014.09.001] [PMID: 25219323]
[43]
Liu, Q.; Li, J.; Zhang, W.; Xiao, C.; Zhang, S.; Nian, C.; Li, J.; Su, D.; Chen, L.; Zhao, Q.; Shao, H.; Zhao, H.; Chen, Q.; Li, Y.; Geng, J.; Hong, L.; Lin, S.; Wu, Q.; Deng, X.; Ke, R.; Ding, J.; Johnson, R.L.; Liu, X.; Chen, L.; Zhou, D. Glycogen accumulation and phase separation drives liver tumor initiation. Cell, 2021, 184(22), 5559-5576.e19.
[http://dx.doi.org/10.1016/j.cell.2021.10.001] [PMID: 34678143]
[44]
Hindson, J. Glycogen phase separation and liver cancer. Nat. Rev. Gastroenterol. Hepatol., 2021, 18(12), 831.
[http://dx.doi.org/10.1038/s41575-021-00548-9] [PMID: 34728820]
[45]
Zbinden, A.; Pérez-Berlanga, M.; De Rossi, P.; Polymenidou, M. Phase separation and neurodegenerative diseases: A disturbance in the force. Dev. Cell, 2020, 55(1), 45-68.
[http://dx.doi.org/10.1016/j.devcel.2020.09.014] [PMID: 33049211]
[46]
Wang, S.; Zheng, J.; Ma, L.; Petersen, R.B.; Xu, L.; Huang, K. Inhibiting protein aggregation with nanomaterials: The underlying mechanisms and impact factors. Biochim. Biophys. Acta, Gen. Subj., 2022, 1866(2), 130061.
[http://dx.doi.org/10.1016/j.bbagen.2021.130061] [PMID: 34822925]
[47]
Cheng, B.; Gong, H.; Xiao, H.; Petersen, R.B.; Zheng, L.; Huang, K. Inhibiting toxic aggregation of amyloidogenic proteins: A therapeutic strategy for protein misfolding diseases. Biochim. Biophys. Acta, Gen. Subj., 2013, 1830(10), 4860-4871.
[http://dx.doi.org/10.1016/j.bbagen.2013.06.029] [PMID: 23820032]
[48]
Ma, L.; Yang, C.; Zhang, X.; Li, Y.; Wang, S.; Zheng, L.; Huang, K. C-terminal truncation exacerbates the aggregation and cytotoxicity of α-Synuclein: A vicious cycle in Parkinson’s disease. Biochim. Biophys. Acta Mol. Basis Dis., 2018, 1864(12), 3714-3725.
[http://dx.doi.org/10.1016/j.bbadis.2018.10.003] [PMID: 30290273]
[49]
Babinchak, W.M.; Haider, R.; Dumm, B.K.; Sarkar, P.; Surewicz, K.; Choi, J.K.; Surewicz, W.K. The role of liquid–liquid phase separation in aggregation of the TDP-43 low-complexity domain. J. Biol. Chem., 2019, 294(16), 6306-6317.
[http://dx.doi.org/10.1074/jbc.RA118.007222] [PMID: 30814253]
[50]
Yu, H.; Lu, S.; Gasior, K.; Singh, D.; Vazquez-Sanchez, S.; Tapia, O.; Toprani, D.; Beccari, M.S.; Yates, J.R., III; Da Cruz, S.; Newby, J.M.; Lafarga, M.; Gladfelter, A.S.; Villa, E.; Cleveland, D.W. HSP70 chaperones RNA-free TDP-43 into anisotropic intranuclear liquid spherical shells. Science, 2021, 371(6529), eabb4309.
[http://dx.doi.org/10.1126/science.abb4309] [PMID: 33335017]
[51]
Xiang, L.; Wang, Y.; Liu, S.; Liu, B.; Jin, X.; Cao, X. Targeting protein aggregates with natural products: An optional strategy for neurodegenerative diseases. Int. J. Mol. Sci., 2023, 24(14), 11275.
[http://dx.doi.org/10.3390/ijms241411275] [PMID: 37511037]
[52]
Yoshizawa, T.; Ali, R.; Jiou, J.; Fung, H.Y.J.; Burke, K.A.; Kim, S.J.; Lin, Y.; Peeples, W.B.; Saltzberg, D.; Soniat, M.; Baumhardt, J.M.; Oldenbourg, R.; Sali, A.; Fawzi, N.L.; Rosen, M.K.; Chook, Y.M. Nuclear import receptor inhibits phase separation of fus through binding to multiple sites. Cell, 2018, 173(3), 693-705.
[http://dx.doi.org/10.1016/j.cell.2018.03.003] [PMID: 29677513]
[53]
Hofweber, M.; Hutten, S.; Bourgeois, B.; Spreitzer, E.; Niedner-Boblenz, A.; Schifferer, M.; Ruepp, M.D.; Simons, M.; Niessing, D.; Madl, T.; Dormann, D. Phase separation of FUS is suppressed by its nuclear import receptor and arginine methylation. Cell, 2018, 173(3), 706-719.e13.
[http://dx.doi.org/10.1016/j.cell.2018.03.004] [PMID: 29677514]
[54]
Ma, L.; Zheng, J.; Chen, H.; Zeng, X.; Wang, S.; Yang, C.; Li, X.; Xiao, Y.; Zheng, L.; Chen, H.; Huang, K. A systematic screening of traditional chinese medicine identifies two novel inhibitors against the cytotoxic aggregation of amyloid beta. Front. Pharmacol., 2021, 12, 637766.
[http://dx.doi.org/10.3389/fphar.2021.637766] [PMID: 33897425]
[55]
Wegmann, S.; Eftekharzadeh, B.; Tepper, K.; Zoltowska, K.M.; Bennett, R.E.; Dujardin, S.; Laskowski, P.R.; MacKenzie, D.; Kamath, T.; Commins, C.; Vanderburg, C.; Roe, A.D.; Fan, Z.; Molliex, A.M.; Hernandez-Vega, A.; Muller, D.; Hyman, A.A.; Mandelkow, E.; Taylor, J.P.; Hyman, B.T. Tau protein liquid–liquid phase separation can initiate tau aggregation. EMBO J., 2018, 37(7), e98049.
[http://dx.doi.org/10.15252/embj.201798049] [PMID: 29472250]
[56]
Hnisz, D.; Shrinivas, K.; Young, R.A.; Chakraborty, A.K.; Sharp, P.A. A phase separation model for transcriptional control. Cell, 2017, 169(1), 13-23.
[http://dx.doi.org/10.1016/j.cell.2017.02.007] [PMID: 28340338]
[57]
Hazawa, M.; Ikliptikawati, D. K.; Iwashima, Y.; Lin, D. C.; Jiang, Y.; Qiu, Y.; Makiyama, K.; Matsumoto, K.; Kobayashi, A.; Nishide, G.; Keesiang, L.; Yoshino, H.; Minamoto, T.; Suzuki, T.; Kobayashi, I.; Meguro-Horike, M.; Jiang, Y. Y.; Nishiuchi, T.; Konno, H.; Koeffler, H. P.; Hosomichi, K.; Tajima, A.; Horike, S. I.; Wong, R. W. Super-enhancer trapping by the nuclear pore via intrinsically disordered regions of proteins in squamous cell carcinoma cells. Cell Chem. Biol., 2023, 23, 2451-9456.
[http://dx.doi.org/10.1016/j.chembiol.2023.10.005]
[58]
Lu, Y.; Wu, T.; Gutman, O.; Lu, H.; Zhou, Q.; Henis, Y.I.; Luo, K. Phase separation of TAZ compartmentalizes the transcription machinery to promote gene expression. Nat. Cell Biol., 2020, 22(4), 453-464.
[http://dx.doi.org/10.1038/s41556-020-0485-0] [PMID: 32203417]
[59]
Cai, D.; Feliciano, D.; Dong, P.; Flores, E.; Gruebele, M.; Porat-Shliom, N.; Sukenik, S.; Liu, Z.; Lippincott-Schwartz, J. Phase separation of YAP reorganizes genome topology for long-term YAP target gene expression. Nat. Cell Biol., 2019, 21(12), 1578-1589.
[http://dx.doi.org/10.1038/s41556-019-0433-z] [PMID: 31792379]
[60]
Boija, A.; Klein, I.A.; Sabari, B.R.; Dall’Agnese, A.; Coffey, E.L.; Zamudio, A.V.; Li, C.H.; Shrinivas, K.; Manteiga, J.C.; Hannett, N.M.; Abraham, B.J.; Afeyan, L.K.; Guo, Y.E.; Rimel, J.K.; Fant, C.B.; Schuijers, J.; Lee, T.I.; Taatjes, D.J.; Young, R.A. Transcription factors activate genes through the phase-separation capacity of their activation domains. Cell, 2018, 175(7), 1842-1855.
[http://dx.doi.org/10.1016/j.cell.2018.10.042] [PMID: 30449618]
[61]
Cho, W.K.; Spille, J.H.; Hecht, M.; Lee, C.; Li, C.; Grube, V.; Cisse, I.I. Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science, 2018, 361(6400), 412-415.
[http://dx.doi.org/10.1126/science.aar4199] [PMID: 29930094]
[62]
Chen, Y.; Yang, D.; Cheng, B.; Chen, J.; Peng, A.; Yang, C.; Liu, C.; Xiong, M.; Deng, A.; Zhang, Y.; Zheng, L.; Huang, K. Clinical characteristics and outcomes of patients with diabetes and COVID-19 in association with glucose-lowering medication. Diabetes Care, 2020, 43(7), 1399-1407.
[http://dx.doi.org/10.2337/dc20-0660] [PMID: 32409498]
[63]
Gibson, B.A.; Doolittle, L.K.; Schneider, M.W.G.; Jensen, L.E.; Gamarra, N.; Henry, L.; Gerlich, D.W.; Redding, S.; Rosen, M.K. Organization of chromatin by intrinsic and regulated phase separation. Cell, 2019, 179(2), 470-484.
[http://dx.doi.org/10.1016/j.cell.2019.08.037] [PMID: 31543265]
[64]
Wagh, K.; Garcia, D.A.; Upadhyaya, A. Phase separation in transcription factor dynamics and chromatin organization. Curr. Opin. Struct. Biol., 2021, 71, 148-155.
[http://dx.doi.org/10.1016/j.sbi.2021.06.009] [PMID: 34303933]
[65]
Zhang, H.; Qin, W.; Romero, H.; Leonhardt, H.; Cardoso, M.C. Heterochromatin organization and phase separation. Nucleus, 2023, 14(1), 2159142.
[http://dx.doi.org/10.1080/19491034.2022.2159142] [PMID: 36710442]
[66]
Chen, W.; Zhu, Q.; Liu, Y.; Zhang, Q. Chromatin remodeling and plant immunity. Adv. Protein Chem. Struct. Biol., 2017, 106, 243-260.
[http://dx.doi.org/10.1016/bs.apcsb.2016.08.006] [PMID: 28057214]
[67]
Kumar, V.C.; Pai, R. Genes of the month: H3.3 histone genes: H3F3A and H3F3B. J. Clin. Pathol., 2021, 74(12), 753-758.
[http://dx.doi.org/10.1136/jclinpath-2021-207857] [PMID: 34667098]
[68]
Yuan, Y.; Fan, Y.; Zhou, Y.; Qiu, R.; Kang, W.; Liu, Y.; Chen, Y.; Wang, C.; Shi, J.; Liu, C.; Li, Y.; Wu, M.; Huang, K.; Liu, Y.; Zheng, L. Linker histone variant H1.2 is a brake on white adipose tissue browning. Nat. Commun., 2023, 14(1), 3982.
[http://dx.doi.org/10.1038/s41467-023-39713-w] [PMID: 37414781]
[69]
Wang, Q.; Chen, Y.; Xie, Y.; Yang, D.; Sun, Y.; Yuan, Y.; Chen, H.; Zhang, Y.; Huang, K.; Zheng, L. Histone H1.2 promotes hepatocarcinogenesis by regulating signal transducer and activator of transcription 3 signaling. Cancer Sci., 2022, 113(5), 1679-1692.
[http://dx.doi.org/10.1111/cas.15336] [PMID: 35294987]
[70]
Chen, Y.; Shi, J.; Wang, X.; Zhou, L.; Wang, Q.; Xie, Y.; Peng, C.; Kuang, L.; Yang, D.; Yang, J.; Yang, C.; Li, X.; Yuan, Y.; Zhou, Y.; Peng, A.; Zhang, Y.; Chen, H.; Liu, X.; Zheng, L.; Huang, K.; Li, Y. An antioxidant feedforward cycle coordinated by linker histone variant H1.2 and NRF2 that drives nonsmall cell lung cancer progression. Proc. Natl. Acad. Sci., 2023, 120(39), e2306288120.
[http://dx.doi.org/10.1073/pnas.2306288120] [PMID: 37729198]
[71]
Chen, H.; Liu, C.; Wang, Q.; Xiong, M.; Zeng, X.; Yang, D.; Xie, Y.; Su, H.; Zhang, Y.; Huang, Y.; Chen, Y.; Yue, J.; Liu, C.; Wang, S.; Huang, K.; Zheng, L. Renal UTX-PHGDH-serine axis regulates metabolic disorders in the kidney and liver. Nat. Commun., 2022, 13(1), 3835.
[http://dx.doi.org/10.1038/s41467-022-31476-0] [PMID: 35788583]
[72]
Yang, D.; Fan, Y.; Xiong, M.; Chen, Y.; Zhou, Y.; Liu, X.; Yuan, Y.; Wang, Q.; Zhang, Y.; Petersen, R.B.; Su, H.; Yue, J.; Zhang, C.; Chen, H.; Huang, K.; Zheng, L. Loss of renal tubular G9a benefits acute kidney injury by lowering focal lipid accumulation via CES1. EMBO Rep., 2023, 24(6), e56128.
[http://dx.doi.org/10.15252/embr.202256128] [PMID: 37042626]
[73]
Shakya, A.; Park, S.; Rana, N.; King, J.T. Liquid-liquid phase separation of histone proteins in cells: Role in chromatin organization. Biophys. J., 2020, 118(3), 753-764.
[http://dx.doi.org/10.1016/j.bpj.2019.12.022] [PMID: 31952807]
[74]
Wang, W.; Wang, Q.; Wan, D.; Sun, Y.; Wang, L.; Chen, H.; Liu, C.; Petersen, R.B.; Li, J.; Xue, W.; Zheng, L.; Huang, K. Histone HIST1H1C/H1.2 regulates autophagy in the development of diabetic retinopathy. Autophagy, 2017, 13(5), 941-954.
[http://dx.doi.org/10.1080/15548627.2017.1293768] [PMID: 28409999]
[75]
Turner, A.L.; Watson, M.; Wilkins, O.G.; Cato, L.; Travers, A.; Thomas, J.O.; Stott, K. Highly disordered histone H1−DNA model complexes and their condensates. Proc. Natl. Acad. Sci., 2018, 115(47), 11964-11969.
[http://dx.doi.org/10.1073/pnas.1805943115] [PMID: 30301810]
[76]
Mimura, M.; Tomita, S.; Shinkai, Y.; Hosokai, T.; Kumeta, H.; Saio, T.; Shiraki, K.; Kurita, R. Quadruplex folding promotes the condensation of linker histones and dnas via liquid–liquid phase separation. J. Am. Chem. Soc., 2021, 143(26), 9849-9857.
[http://dx.doi.org/10.1021/jacs.1c03447] [PMID: 34152774]
[77]
Buttress, T.; He, S.; Wang, L.; Zhou, S.; Saalbach, G.; Vickers, M.; Li, G.; Li, P.; Feng, X. Histone H2B.8 compacts flowering plant sperm through chromatin phase separation. Nature, 2022, 611(7936), 614-622.
[http://dx.doi.org/10.1038/s41586-022-05386-6] [PMID: 36323776]
[78]
Bi, X. Heterochromatin structure: Lessons from the budding yeast. IUBMB Life, 2014, 66(10), 657-666.
[http://dx.doi.org/10.1002/iub.1322] [PMID: 25355678]
[79]
Maeda, R.; Tachibana, M. HP1 maintains protein stability of H3K9 methyltransferases and demethylases. EMBO Rep., 2022, 23(4), e53581.
[http://dx.doi.org/10.15252/embr.202153581] [PMID: 35166421]
[80]
Strom, A.R.; Emelyanov, A.V.; Mir, M.; Fyodorov, D.V.; Darzacq, X.; Karpen, G.H. Phase separation drives heterochromatin domain formation. Nature, 2017, 547(7662), 241-245.
[http://dx.doi.org/10.1038/nature22989] [PMID: 28636597]
[81]
Qin, W.; Stengl, A.; Ugur, E.; Leidescher, S.; Ryan, J.; Cardoso, M.C.; Leonhardt, H. HP1β carries an acidic linker domain and requires H3K9me3 for phase separation. Nucleus, 2021, 12(1), 44-57.
[http://dx.doi.org/10.1080/19491034.2021.1889858] [PMID: 33660589]
[82]
Huo, X.; Ji, L.; Zhang, Y.; Lv, P.; Cao, X.; Wang, Q.; Yan, Z.; Dong, S.; Du, D.; Zhang, F.; Wei, G.; Liu, Y.; Wen, B. The nuclear matrix protein SAFB cooperates with major satellite rnas to stabilize heterochromatin architecture partially through phase separation. Mol. Cell, 2020, 77(2), 368-383.
[http://dx.doi.org/10.1016/j.molcel.2019.10.001] [PMID: 31677973]
[83]
Jenuwein, T.; Allis, C.D. Translating the histone code. Science, 2001, 293(5532), 1074-1080.
[http://dx.doi.org/10.1126/science.1063127] [PMID: 11498575]
[84]
Wang, L.; Gao, Y.; Zheng, X.; Liu, C.; Dong, S.; Li, R.; Zhang, G.; Wei, Y.; Qu, H.; Li, Y.; Allis, C.D.; Li, G.; Li, H.; Li, P. Histone modifications regulate chromatin compartmentalization by contributing to a phase separation mechanism. Mol. Cell, 2019, 76(4), 646-659.
[http://dx.doi.org/10.1016/j.molcel.2019.08.019] [PMID: 31543422]
[85]
Zhang, P.; Zhang, M. Epigenetic alterations and advancement of treatment in peripheral T-cell lymphoma. Clin. Epigenetics, 2020, 12(1), 169.
[http://dx.doi.org/10.1186/s13148-020-00962-x] [PMID: 33160401]
[86]
Millán-Zambrano, G.; Burton, A.; Bannister, A.J.; Schneider, R. Histone post-translational modifications cause and consequence of genome function. Nat. Rev. Genet., 2022, 23(9), 563-580.
[http://dx.doi.org/10.1038/s41576-022-00468-7] [PMID: 35338361]
[87]
Xiong, M.; Chen, H.; Fan, Y.; Jin, M.; Yang, D.; Chen, Y.; Zhang, Y.; Petersen, R.B.; Su, H.; Peng, A.; Wang, C.; Zheng, L.; Huang, K. Tubular Elabela-APJ axis attenuates ischemia-reperfusion induced acute kidney injury and the following AKI-CKD transition by protecting renal microcirculation. Theranostics, 2023, 13(10), 3387-3401.
[http://dx.doi.org/10.7150/thno.84308] [PMID: 37351176]
[88]
Huang, J.; Wan, D.; Li, J.; Chen, H.; Huang, K.; Zheng, L. Histone acetyltransferase PCAF regulates inflammatory molecules in the development of renal injury. Epigenetics, 2015, 10(1), 62-71.
[http://dx.doi.org/10.4161/15592294.2014.990780] [PMID: 25496441]
[89]
Wan, D.; Liu, C.; Sun, Y.; Wang, W.; Huang, K.; Zheng, L. MacroH2A1.1 cooperates with EZH2 to promote adipogenesis by regulating Wnt signaling. J. Mol. Cell Biol., 2017, 9(4), 325-337.
[http://dx.doi.org/10.1093/jmcb/mjx027] [PMID: 28992292]
[90]
Xue, W.; Huang, J.; Chen, H.; Zhang, Y.; Zhu, X.; Li, J.; Zhang, W.; Yuan, Y.; Wang, Y.; Zheng, L.; Huang, K. Histone methyltransferase G9a modulates hepatic insulin signaling via regulating HMGA1. Biochim. Biophys. Acta Mol. Basis Dis., 2018, 1864(2), 338-346.
[http://dx.doi.org/10.1016/j.bbadis.2017.10.037] [PMID: 29101051]
[91]
Hess, J.L. MLL: A histone methyltransferase disrupted in leukemia. Trends Mol. Med., 2004, 10(10), 500-507.
[http://dx.doi.org/10.1016/j.molmed.2004.08.005] [PMID: 15464450]
[92]
Zhang, Y.; Xue, W.; Zhang, W.; Yuan, Y.; Zhu, X.; Wang, Q.; Wei, Y.; Yang, D.; Yang, C.; Chen, Y.; Sun, Y.; Wang, S.; Huang, K.; Zheng, L. Histone methyltransferase G9a protects against acute liver injury through GSTP1. Cell Death Differ., 2020, 27(4), 1243-1258.
[http://dx.doi.org/10.1038/s41418-019-0412-8] [PMID: 31515511]
[93]
Zhang, W.; Yang, D.; Yuan, Y.; Liu, C.; Chen, H.; Zhang, Y.; Wang, Q.; Petersen, R.B.; Huang, K.; Zheng, L. Muscular G9a regulates muscle-liver-fat axis by musclin under overnutrition in female mice. Diabetes, 2020, 69(12), 2642-2654.
[http://dx.doi.org/10.2337/db20-0437] [PMID: 32994276]
[94]
Tang, S.Y.; Zhou, P.J.; Meng, Y.; Zeng, F.R.; Deng, G.T. Gastric cancer: An epigenetic view. World J. Gastrointest. Oncol., 2022, 14(1), 90-109.
[http://dx.doi.org/10.4251/wjgo.v14.i1.90] [PMID: 35116105]
[95]
Jang, S.; Hwang, J.; Jeong, H.S. The role of histone acetylation in mesenchymal stem cell differentiation. Chonnam Med. J., 2022, 58(1), 6-12.
[http://dx.doi.org/10.4068/cmj.2022.58.1.6] [PMID: 35169553]
[96]
Quan, C.; Chen, Y.; Wang, X.; Yang, D.; Wang, Q.; Huang, Y.; Petersen, R.B.; Liu, X.; Zheng, L.; Li, Y.; Huang, K. Loss of histone lysine methyltransferase EZH2 confers resistance to tyrosine kinase inhibitors in non-small cell lung cancer. Cancer Lett., 2020, 495, 41-52.
[http://dx.doi.org/10.1016/j.canlet.2020.09.003] [PMID: 32920200]
[97]
Yang, C.; Xu, H.; Yang, D.; Xie, Y.; Xiong, M.; Fan, Y.; Liu, X.; Zhang, Y.; Xiao, Y.; Chen, Y.; Zhou, Y.; Song, L.; Wang, C.; Peng, A.; Petersen, R.B.; Chen, H.; Huang, K.; Zheng, L. A renal YY1-KIM1-DR5 axis regulates the progression of acute kidney injury. Nat. Commun., 2023, 14(1), 4261.
[http://dx.doi.org/10.1038/s41467-023-40036-z] [PMID: 37460623]
[98]
Krishnan, S.; Trievel, R.C. Purification, biochemical analysis, and structure determination of jmjc lysine demethylases. Methods Enzymol., 2016, 573, 279-301.
[http://dx.doi.org/10.1016/bs.mie.2016.01.023] [PMID: 27372758]
[99]
Ashok, A.; Pooranawattanakul, S.; Tai, W.L.; Cho, K.S.; Utheim, T.P.; Cestari, D.M.; Chen, D.F. Epigenetic regulation of optic nerve development, protection, and repair. Int. J. Mol. Sci., 2022, 23(16), 8927.
[http://dx.doi.org/10.3390/ijms23168927] [PMID: 36012190]
[100]
Wang, L.L.; Chen, H.; Huang, K.; Zheng, L. Elevated histone acetylations in Müller cell contribute to inflammation: A novel inhibitory effect of minocycline. Glia, 2012, 60(12), 1896-1905.
[http://dx.doi.org/10.1002/glia.22405] [PMID: 22915469]
[101]
Yang, Q.; Yang, Y.; Zhou, N.; Tang, K.; Lau, W.B.; Lau, B.; Wang, W.; Xu, L.; Yang, Z.; Huang, S.; Wang, X.; Yi, T.; Zhao, X.; Wei, Y.; Wang, H.; Zhao, L.; Zhou, S. Epigenetics in ovarian cancer: Premise, properties, and perspectives. Mol. Cancer, 2018, 17(1), 109.
[http://dx.doi.org/10.1186/s12943-018-0855-4] [PMID: 30064416]
[102]
Kadiyala, C.S.R.; Zheng, L.; Du, Y.; Yohannes, E.; Kao, H.Y.; Miyagi, M.; Kern, T.S. Acetylation of retinal histones in diabetes increases inflammatory proteins: effects of minocycline and manipulation of histone acetyltransferase (HAT) and histone deacetylase (HDAC). J. Biol. Chem., 2012, 287(31), 25869-25880.
[http://dx.doi.org/10.1074/jbc.M112.375204] [PMID: 22648458]
[103]
Yuan, H.; Han, Y.; Wang, X.; Li, N.; Liu, Q.; Yin, Y.; Wang, H.; Pan, L.; Li, L.; Song, K.; Qiu, T.; Pan, Q.; Chen, Q.; Zhang, G.; Zang, Y.; Tan, M.; Zhang, J.; Li, Q.; Wang, X.; Jiang, J.; Qin, J. SETD2 restricts prostate cancer metastasis by integrating EZH2 and AMPK signaling pathways. Cancer Cell, 2020, 38(3), 350-365.
[http://dx.doi.org/10.1016/j.ccell.2020.05.022] [PMID: 32619406]
[104]
Bhattacharya, S.; Lange, J.J.; Levy, M.; Florens, L.; Washburn, M.P.; Workman, J.L. The disordered regions of the methyltransferase SETD2 govern its function by regulating its proteolysis and phase separation. J. Biol. Chem., 2021, 297(3), 101075.
[http://dx.doi.org/10.1016/j.jbc.2021.101075] [PMID: 34391778]
[105]
Xie, G.; Lee, J.E.; Senft, A.D.; Park, Y.K.; Jang, Y.; Chakraborty, S.; Thompson, J.J.; McKernan, K.; Liu, C.; Macfarlan, T.S.; Rocha, P.P.; Peng, W.; Ge, K. MLL3/MLL4 methyltransferase activities control early embryonic development and embryonic stem cell differentiation in a lineage-selective manner. Nat. Genet., 2023, 55(4), 693-705.
[http://dx.doi.org/10.1038/s41588-023-01356-4] [PMID: 37012455]
[106]
Li, W.; Wu, L.; Jia, H.; Lin, Z.; Zhong, R.; Li, Y.; Jiang, C.; Liu, S.; Zhou, X.; Zhang, E. The low-complexity domains of the KMT2D protein regulate histone monomethylation transcription to facilitate pancreatic cancer progression. Cell. Mol. Biol. Lett., 2021, 26(1), 45.
[http://dx.doi.org/10.1186/s11658-021-00292-7] [PMID: 34758724]
[107]
Vicioso-Mantis, M.; Aguirre, S.; Martínez-Balbás, M.A.; Jmj, C. JmjC family of histone demethylases form nuclear condensates. Int. J. Mol. Sci., 2022, 23(14), 7664.
[http://dx.doi.org/10.3390/ijms23147664] [PMID: 35887017]
[108]
Huang, Y.; Xie, Y.; Yang, D.; Xiong, M.; Chen, X.; Wu, D.; Wang, Q.; Chen, H.; Zheng, L.; Huang, K. Histone demethylase UTX aggravates acetaminophen overdose induced hepatotoxicity through dual mechanisms. Pharmacol. Res., 2022, 175, 106021.
[http://dx.doi.org/10.1016/j.phrs.2021.106021] [PMID: 34883214]
[109]
Shi, B.; Li, W.; Song, Y.; Wang, Z.; Ju, R.; Ulman, A.; Hu, J.; Palomba, F.; Zhao, Y.; Le, J.P.; Jarrard, W.; Dimoff, D.; Digman, M.A.; Gratton, E.; Zang, C.; Jiang, H. UTX condensation underlies its tumour-suppressive activity. Nature, 2021, 597(7878), 726-731.
[http://dx.doi.org/10.1038/s41586-021-03903-7] [PMID: 34526716]
[110]
Chen, H.; Wang, L.; Wang, W.; Cheng, C.; Zhang, Y.; Zhou, Y.; Wang, C.; Miao, X.; Wang, J.; Wang, C.; Li, J.; Zheng, L.; Huang, K. ELABELA and an ELABELA fragment protect against AKI. J. Am. Soc. Nephrol., 2017, 28(9), 2694-2707.
[http://dx.doi.org/10.1681/ASN.2016111210] [PMID: 28583915]
[111]
Chen, H.; Huang, Y.; Zhu, X.; Liu, C.; Yuan, Y.; Su, H.; Zhang, C.; Liu, C.; Xiong, M.; Qu, Y.; Yun, P.; Zheng, L.; Huang, K. Histone demethylase UTX is a therapeutic target for diabetic kidney disease. J. Physiol., 2019, 597(6), 1643-1660.
[http://dx.doi.org/10.1113/JP277367] [PMID: 30516825]
[112]
Wang, Y.; Hong, Q.; Xia, Y.; Zhang, Z.; Wen, B. The lysine demethylase KDM7A regulates immediate early genes in neurons. Adv. Sci., 2023, 10(28), 2301367.
[http://dx.doi.org/10.1002/advs.202301367] [PMID: 37565374]
[113]
Ming, H.; Wang, Q.; Zhang, Y.; Ji, L.; Cheng, L.; Huo, X.; Yan, Z.; Liu, Z.; Dang, Y.; Wen, B. The nuclear bodies formed by histone demethylase KDM7A. Protein Cell, 2021, 12(4), 297-304.
[http://dx.doi.org/10.1007/s13238-020-00783-x] [PMID: 32935279]
[114]
Dmitriev, R.I.; Pestov, N.B.; Shakhparonov, M.I.; Okkelman, I.A. Two distinct nuclear localization signals in mammalian MSL1 regulate its function. J. Cell. Biochem., 2014, 115(11), n/a.
[http://dx.doi.org/10.1002/jcb.24868] [PMID: 24913909]
[115]
He, Y.; Wang, S.; Liu, S.; Qin, D.; Liu, Z.; Wang, L.; Chen, X.; Zhang, L. MSL1 promotes liver regeneration by driving phase separation of STAT3 and histone h4 and enhancing their acetylation. Adv. Sci., 2023, 10(23), 2301094.
[http://dx.doi.org/10.1002/advs.202301094] [PMID: 37279389]
[116]
Li, M.; Li, M.; Xia, Y.; Li, G.; Su, X.; Wang, D.; Ye, J.; Lu, F.; Sun, T.; Ji, C. HDAC1/3-dependent moderate liquid–liquid phase separation of YY1 promotes METTL3 expression and AML cell proliferation. Cell Death Dis., 2022, 13(11), 992.
[http://dx.doi.org/10.1038/s41419-022-05435-y] [PMID: 36424383]
[117]
Tahiliani, M.; Koh, K.P.; Shen, Y.; Pastor, W.A.; Bandukwala, H.; Brudno, Y.; Agarwal, S.; Iyer, L.M.; Liu, D.R.; Aravind, L.; Rao, A. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science, 2009, 324(5929), 930-935.
[http://dx.doi.org/10.1126/science.1170116] [PMID: 19372391]
[118]
Fan, Y.; Yuan, Y.; Xiong, M.; Jin, M.; Zhang, D.; Yang, D.; Liu, C.; Petersen, R.B.; Huang, K.; Peng, A.; Zheng, L. Tet1 deficiency exacerbates oxidative stress in acute kidney injury by regulating superoxide dismutase. Theranostics, 2023, 13(15), 5348-5364.
[http://dx.doi.org/10.7150/thno.87416] [PMID: 37908721]
[119]
Meng, H.; Cao, Y.; Qin, J.; Song, X.; Zhang, Q.; Shi, Y.; Cao, L. DNA methylation, its mediators and genome integrity. Int. J. Biol. Sci., 2015, 11(5), 604-617.
[http://dx.doi.org/10.7150/ijbs.11218] [PMID: 25892967]
[120]
Mahmoud, A.; Ali, M. Methyl donor micronutrients that modify dna methylation and cancer outcome. Nutrients, 2019, 11(3), 608.
[http://dx.doi.org/10.3390/nu11030608] [PMID: 30871166]
[121]
Yuan, Y.; Liu, C.; Chen, X.; Sun, Y.; Xiong, M.; Fan, Y.; Petersen, R.B.; Chen, H.; Huang, K.; Zheng, L.; Vitamin, C. Vitamin C inhibits the metabolic changes induced by tet1 insufficiency under high fat diet stress. Mol. Nutr. Food Res., 2021, 65(16), 2100417.
[http://dx.doi.org/10.1002/mnfr.202100417] [PMID: 34129274]
[122]
Illingworth, R.S. Chromatin folding and nuclear architecture: PRC1 function in 3D. Curr. Opin. Genet. Dev., 2019, 55, 82-90.
[http://dx.doi.org/10.1016/j.gde.2019.06.006] [PMID: 31323466]
[123]
Namitz, K.E.W.; Showalter, S.A.; Cosgrove, M.S. Phase separation promotes a highly active oligomeric scaffold of the MLL1 core complex for regulation of histone H3K4 methylation. J. Biol. Chem., 2023, 299(10), 105204.
[http://dx.doi.org/10.1016/j.jbc.2023.105204] [PMID: 37660926]
[124]
Moore, L.D.; Le, T.; Fan, G. DNA methylation and its basic function. Neuropsychopharmacology, 2013, 38(1), 23-38.
[http://dx.doi.org/10.1038/npp.2012.112] [PMID: 22781841]
[125]
Liu, C.; Wang, J.; Wei, Y.; Zhang, W.; Geng, M.; Yuan, Y.; Chen, Y.; Sun, Y.; Chen, H.; Zhang, Y.; Xiong, M.; Li, Y.; Zheng, L.; Huang, K. Fat-specific knockout of Mecp2 upregulates slpi to reduce obesity by enhancing browning. Diabetes, 2020, 69(1), 35-47.
[http://dx.doi.org/10.2337/db19-0502] [PMID: 31597640]
[126]
Wang, J.; Xiao, Y.; Liu, C.; Huang, Y.; Petersen, R.B.; Zheng, L.; Huang, K. Emerging physiological and pathological roles of MeCP2 in non-neurological systems. Arch. Biochem. Biophys., 2021, 700, 108768.
[http://dx.doi.org/10.1016/j.abb.2021.108768] [PMID: 33485848]
[127]
Wang, J.; Xiong, M.; Fan, Y.; Liu, C.; Wang, Q.; Yang, D.; Yuan, Y.; Huang, Y.; Wang, S.; Zhang, Y.; Niu, S.; Yue, J.; Su, H.; Zhang, C.; Chen, H.; Zheng, L.; Huang, K. Mecp2 protects kidney from ischemia-reperfusion injury through transcriptional repressing IL-6/STAT3 signaling. Theranostics, 2022, 12(8), 3896-3910.
[http://dx.doi.org/10.7150/thno.72515] [PMID: 35664078]
[128]
Kumar, A.; Kamboj, S.; Malone, B.M.; Kudo, S.; Twiss, J.L.; Czymmek, K.J.; LaSalle, J.M.; Schanen, N.C. Analysis of protein domains and Rett syndrome mutations indicate that multiple regions influence chromatin-binding dynamics of the chromatin-associated protein MECP2 in vivo. J. Cell Sci., 2008, 121(7), 1128-1137.
[http://dx.doi.org/10.1242/jcs.016865] [PMID: 18334558]
[129]
Fan, C.; Zhang, H.; Fu, L.; Li, Y.; Du, Y.; Qiu, Z.; Lu, F. Rett mutations attenuate phase separation of MeCP2. Cell Discov., 2020, 6(1), 38.
[http://dx.doi.org/10.1038/s41421-020-0172-0] [PMID: 32566246]
[130]
Zhang, H.; Romero, H.; Schmidt, A.; Gagova, K.; Qin, W.; Bertulat, B.; Lehmkuhl, A.; Milden, M.; Eck, M.; Meckel, T.; Leonhardt, H.; Cardoso, M.C. MeCP2-induced heterochromatin organization is driven by oligomerization-based liquid–liquid phase separation and restricted by DNA methylation. Nucleus, 2022, 13(1), 1-34.
[http://dx.doi.org/10.1080/19491034.2021.2024691] [PMID: 35156529]

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