Citation: Liu Sirui, Quan Hui, Tian Hao, Zhou Rui, Yang Lijiang, Gao Yiqin. 1D Sequence Based 3D Chromatin Phase Separation: Forces, Processes, and Functions[J]. Acta Physico-Chimica Sinica, ;2020, 36(1): 190701. doi: 10.3866/PKU.WHXB201907010 shu

1D Sequence Based 3D Chromatin Phase Separation: Forces, Processes, and Functions

Liu Sirui ¹ ,
Quan Hui ¹ ,
Tian Hao ¹ ,
Zhou Rui ² ,
Yang Lijiang ¹ ,
Gao Yiqin ^1,2,,

1.
College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, P. R. China
2.
Biomedical Pioneering Innovation Center, Peking University, Beijing 100871, P. R. China

Corresponding author: Gao Yiqin, gaoyq@pku.edu.cn
Received Date: 1 July 2019
Revised Date: 30 August 2019
Accepted Date: 30 August 2019
Available Online: 6 January 2019
Fund Project: The project was supported by the National Natural Science Foundation of China (21573006, 21821004, 21873007) and the National Key R & D Program of China (2017YFA0204702)the National Natural Science Foundation of China 21573006the National Natural Science Foundation of China 21821004the National Natural Science Foundation of China 21873007the National Key R & D Program of China 2017YFA0204702

The high-order chromatin structure plays a non-negligible role in gene regulation. The formation of chromatin structure and its regulatory mechanisms have been studied intensely. To analyze the high-order chromatin structures, both computational and physical models have been developed, including polymer physics models and molecular crowding models. Over the past few years, the phase separation theory has drawn a lot of research interest, and the effect of heterochromatin and transcriptional factors (TFs) on phase separation has attracted much attention. Existing phase separation models for chromatin focus on multivalent molecules or on epigenetic properties and does not adequately explore the dependence of chromatin structure organization and remodeling on DNA sequence. Genomes of a number of species are highly uneven at multiple scales. It can be divided purely based on sequential properties into two sequentially, epigenetically, and transcriptionally distinct regions, namely forest and prairie domains, demonstrating the intrinsic mosaicity in genome. Compared to prairies, forest domains are on average more gene-rich, accessible, transcriptionally active, higher in open-sea methylation level, and are enriched in RNA polymerase Ⅱ binding sites as well as active histone modifications. Moreover, different structural properties of these two types of sequential domains suggest that sequence may play a role in topologically associated domain (TAD) and compartment formation. The chromatin sequence-structural relationship and functional regulation in different cell types with almost identical sequences are discussed in this review. We try to describe the evolution of chromatin structure in multiple biological processes including early development, differentiation, and senescence in a unified framework. The forest and prairie domains with high and low CGI densities, respectively, show enhanced segregation from each other in development, differentiation, and senescence. Meanwhile the multiscale forest-prairie spatial intermingling is cell-type specific and increases upon differentiation, thereby helping to define cell identity. The consistency between chromatin structure and open-sea methylation level suggests that the latter is a promising indicator of structural segregation, deepening our understanding of epigenetic-structure relation. We further discuss the physical driving forces of phase separation as well as their biological implications. The phase separation of the uneven 1D sequence in 3D space serves as a potential driving force, and together with cell type specific epigenetic marks and transcription factors shapes the chromatin structure in different cell types. Transcriptional complex along with dynamic TFs and epigenetic marks may account for local structure formation and separation, regulating chromatin structure at a smaller spatial-temporal scale based on their sequential environment. Finally, role of physical factors like temperature and sequence unevenness in affecting chromatin structure have also been discussed.
- Phase separation,
- Sequence mosaicity,
- Forest and prairie domains,
- Development and differentiation,
- Aging and disease
1. [1]
  Helmut, S. J. Phys. Condens. Matter 2003, 15, R699. doi: 10.1088/0953-8984/27/6/060301 doi: 10.1088/0953-8984/27/6/060301
2. [2]
  Cortini, R.; Barbi, M.; Care, B. R.; Lavelle, C.; Lesne, A.; Mozziconacci, J.; Victor, J. M. Rev. Mod. Phys. 2016, 88, 025002. doi: 10.1103/Revmodphys.88.025002 doi: 10.1103/Revmodphys.88.025002
3. [3]
  Thoma, F.; Koller, T.; Klug, A. J. Cell Biol. 1979, 83, 403. doi: 10.1083/jcb.83.2.403 doi: 10.1083/jcb.83.2.403
4. [4]
  Finch, J. T.; Klug, A. Proc. Natl. Acad. Sci. U. S. A. 1976, 73, 1897. doi: 10.1073/pnas.73.6.1897 doi: 10.1073/pnas.73.6.1897
5. [5]
  Cremer, T.; Cremer, M. Cold Spring Harb. Perspect. Biol. 2010, 2, a003889. doi: 10.1101/cshperspect.a003889 doi: 10.1101/cshperspect.a003889
6. [6]
  Lieberman-Aiden, E.; van Berkum, N. L.; Williams, L.; Imakaev, M.; Ragoczy, T.; Telling, A.; Amit, I.; Lajoie, B. R.; Sabo, P. J.; Dorschner, M. O.; et al. Science 2009, 326, 289. doi: 10.1126/science.1181369 doi: 10.1126/science.1181369
7. [7]
  Fullwood, M. J.; Liu, M. H.; Pan, Y. F.; Liu, J.; Xu, H.; Mohamed, Y. B.; Orlov, Y. L.; Velkov, S.; Ho, A.; Mei, P. H.; et al. Nature 2009, 462, 58. doi: 10.1038/nature08497 doi: 10.1038/nature08497
8. [8]
  Dixon, J. R.; Selvaraj, S.; Yue, F.; Kim, A.; Li, Y.; Shen, Y.; Hu, M.; Liu, J. S.; Ren, B. Nature 2012, 485, 376. doi: 10.1038/nature11082 doi: 10.1038/nature11082
9. [9]
  Nora, E. P.; Lajoie, B. R.; Schulz, E. G.; Giorgetti, L.; Okamoto, I.; Servant, N.; Piolot, T.; van Berkum, N. L.; Meisig, J.; Sedat, J.; et al. Nature 2012, 485, 381. doi: 10.1038/nature11049 doi: 10.1038/nature11049
10. [10]
  Sexton, T.; Yaffe, E.; Kenigsberg, E.; Bantignies, F.; Leblanc, B.; Hoichman, M.; Parrinello, H.; Tanay, A.; Cavalli, G. Cell 2012, 148, 458. doi: 10.1016/j.cell.2012.01.010 doi: 10.1016/j.cell.2012.01.010
11. [11]
  Rao, S. S.; Huntley, M. H.; Durand, N. C.; Stamenova, E. K.; Bochkov, I. D.; Robinson, J. T.; Sanborn, A. L.; Machol, I.; Omer, A. D.; Lander, E. S.; et al. Cell 2014, 159, 1665. doi: 10.1016/j.cell.2014.11.021 doi: 10.1016/j.cell.2014.11.021
12. [12]
  Dixon, J. R.; Jung, I.; Selvaraj, S.; Shen, Y.; Antosiewicz-Bourget, J. E.; Lee, A. Y.; Ye, Z.; Kim, A.; Rajagopal, N.; Xie, W.; et al. Nature 2015, 518, 331. doi: 10.1038/nature14222 doi: 10.1038/nature14222
13. [13]
  Schmitt, A. D.; Hu, M.; Jung, I.; Xu, Z.; Qiu, Y.; Tan, C. L.; Li, Y.; Lin, S.; Lin, Y.; Barr, C. L.; et al. Cell Rep. 2016, 17, 2042. doi: 10.1016/j.celrep.2016.10.061 doi: 10.1016/j.celrep.2016.10.061
14. [14]
  Boettiger, A. N.; Bintu, B.; Moffitt, J. R.; Wang, S.; Beliveau, B. J.; Fudenberg, G.; Imakaev, M.; Mirny, L. A.; Wu, C. T.; Zhuang, X. Nature 2016, 529, 418. doi: 10.1038/nature16496 doi: 10.1038/nature16496
15. [15]
  Zuin, J.; Dixon, J. R.; van der Reijden, M. I.; Ye, Z.; Kolovos, P.; Brouwer, R. W.; van de Corput, M. P.; van de Werken, H. J.; Knoch, T. A.; van IJcken, W. F.; et al. Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 996. doi: 10.1073/pnas.1317788111 doi: 10.1073/pnas.1317788111
16. [16]
  Jabbari, K.; Bernardi, G. PloS One 2017, 12, e0168023. doi: 10.1371/journal.pone.0168023 doi: 10.1371/journal.pone.0168023
17. [17]
  Lesne, A.; Riposo, J.; Roger, P.; Cournac, A.; Mozziconacci, J. Nat. Methods 2014, 11, 1141. doi: 10.1038/Nmeth.3104 doi: 10.1038/Nmeth.3104
18. [18]
  Huet, S.; Lavelle, C.; Ranchon, H.; Carrivain, P.; Victor, J. M.; Bancaud, A. In.t Rev. Cell. Mol. Biol. 2014, 307, 443. doi: 10.1016/B978-0-12-800046-5.00013-8 doi: 10.1016/B978-0-12-800046-5.00013-8
19. [19]
  Wong, H.; Marie-Nelly, H.; Herbert, S.; Carrivain, P.; Blanc, H.; Koszul, R.; Fabre, E.; Zimmer, C. Curr. Biol. 2012, 22, 1881. doi: 10.1016/j.cub.2012.07.069 doi: 10.1016/j.cub.2012.07.069
20. [20]
  Jost, D.; Carrivain, P.; Cavalli, G.; Vaillant, C. Nucleic Acids Res. 2014, 42, 9553. doi: 10.1093/nar/gku698 doi: 10.1093/nar/gku698
21. [21]
  Filion, G. J.; van Bemmel, J. G.; Braunschweig, U.; Talhout, W.; Kind, J.; Ward, L. D.; Brugman, W.; de Castro, I. J.; Kerkhoven, R. M.; Bussemaker, H. J.; et al. Cell 2010, 143, 212. doi: 10.1016/j.cell.2010.09.009 doi: 10.1016/j.cell.2010.09.009
22. [22]
  Zhu, Y.; Chen, Z.; Zhang, K.; Wang, M. C.; Medovoy, D.; Whitaker, J. W.; Ding, B.; Li, N.; Zheng, L. N.; Wang, W. Nat. Commun. 2016, 7, 10812. doi: 10.1038/Ncomms10812 doi: 10.1038/Ncomms10812
23. [23]
  Huang, J. L.; Marco, E.; Pinello, L.; Yuan, G. C. Genome Biol. 2015, 16, 162. doi: 10.1186/S13059-015-0740-Z doi: 10.1186/S13059-015-0740-Z
24. [24]
  Fortin, J. P.; Hansen, K. D. Genome Biol. 2015, 16, 180. doi: 10.1186/s13059-015-0741-y doi: 10.1186/s13059-015-0741-y
25. [25]
  Mirny, L. A. Chromosome Res. 2011, 19, 37. doi: 10.1007/s10577-010-9177-0 doi: 10.1007/s10577-010-9177-0
26. [26]
  Scolari, V. F.; Sclavi, B.; Cosentino Lagomarsino, M. Front. Microbiol. 2015, 6, 424. doi: 10.3389/fmicb.2015.00424 doi: 10.3389/fmicb.2015.00424
27. [27]
  Falk, M.; Feodorova, Y.; Naumova, N.; Imakaev, M.; Lajoie, B. R.; Leonhardt, H.; Joffe, B.; Dekker, J.; Fudenberg, G.; Solovei, I.; et al. Nature 2019, 570, 395. doi: 10.1038/s41586-019-1275-3 doi: 10.1038/s41586-019-1275-3
28. [28]
  Di Pierro, M.; Zhang, B.; Aiden, E. L.; Wolynes, P. G.; Onuchic, J. N. Proc. Natl. Acad. Sci. U. S. A. 2016, 113, 12168. doi: 10.1073/pnas.1613607113 doi: 10.1073/pnas.1613607113
29. [29]
  Zhang, B.; Wolynes, P. G. Phys. Rev. Lett. 2016, 116, 248101. doi: 10.1103/PhysRevLett.116.248101 doi: 10.1103/PhysRevLett.116.248101
30. [30]
  Xie, W. J.; Meng, L.; Liu, S.; Zhang, L.; Cai, X.; Gao, Y. Q. Sci. Rep. 2017, 7, 2818. doi: 10.1038/s41598-017-02923-6 doi: 10.1038/s41598-017-02923-6
31. [31]
  Ellis, R. J. Trends. Biochem. Sci. 2001, 26, 597. doi: 10.1016/S0968-0004(01)01938-7 doi: 10.1016/S0968-0004(01)01938-7
32. [32]
  Hyman, A. A.; Brangwynne, C. P. Dev. Cell 2011, 21, 14. doi: 10.1016/j.devcel.2011.06.013 doi: 10.1016/j.devcel.2011.06.013
33. [33]
  Rivas, G.; Minton, A. P. Trends. Biochem. Sci. 2016, 41, 970. doi: 10.1016/j.tibs.2016.08.013 doi: 10.1016/j.tibs.2016.08.013
34. [34]
  Zimmerman, S. B.; Minton, A. P. Annu. Rev. Biophys. Biom. Struct. 1993, 22, 27. doi: 10.1146/annurev.bb.22.060193.000331 doi: 10.1146/annurev.bb.22.060193.000331
35. [35]
  Schnell, S.; Turner, T. E. Prog. Biophys. Mol. Biol. 2004, 85, 235. doi: 10.1016/j.pbiomolbio.2004.01.012 doi: 10.1016/j.pbiomolbio.2004.01.012
36. [36]
  Wang, J.; Yang, L.; Zhu, T.; Wang, S.; Chen, Z. Acta Phys. -Chim. Sin. 2016, 32, 2027. doi: 10.3866/PKU.WHXB201605033
37. [37]
  Zhang, Y.; Tang, Q.; Cao, H.; Zheng, X. Acta Phys. -Chim. Sin. 2013, 29, 1785. doi: 10.3866/PKU.WHXB201305271
38. [38]
  Zhou, H. X.; Rivas, G.; Minton, A. P. Annu. Rev. Biophys. 2008, 37, 375. doi: 10.1146/annurev.biophys.37.032807.125817 doi: 10.1146/annurev.biophys.37.032807.125817
39. [39]
  Zhou, B. R.; Zhou, Z.; Hu, Q. L.; Chen, J.; Liang, Y. Biochim. Biophys. Acta 2008, 1784, 472. doi: 10.1016/j.bbapap.2008.01.004 doi: 10.1016/j.bbapap.2008.01.004
40. [40]
  Monterroso, B.; Reija, B.; Jiménez, M.; Zorrilla, S.; Rivas, G. PloS One 2016, 11, e0149060. doi: 10.1371/journal.pone.0149060 doi: 10.1371/journal.pone.0149060
41. [41]
  Du, F.; Zhou, Z.; Mo, Z. Y.; Shi, J. Z.; Chen, J.; Liang, Y. J. Mol. Biol. 2006, 364, 469. doi: 10.1016/j.jmb.2006.09.018 doi: 10.1016/j.jmb.2006.09.018
42. [42]
  Bancaud, A.; Huet, S.; Daigle, N.; Mozziconacci, J.; Beaudouin, J.; Ellenberg, J. EMBO J. 2009, 28, 3785. doi: 10.1038/emboj.2009.340 doi: 10.1038/emboj.2009.340
43. [43]
  Kim, J. S.; Backman, V.; Szleifer, I. Phys. Rev. Lett. 2011, 106, 168102. doi: 10.1103/PhysRevLett.106.168102 doi: 10.1103/PhysRevLett.106.168102
44. [44]
  Wu, F.; Swain, P.; Kuijpers, L.; Zheng, X.; Felter, K.; Guurink, M.; Chaudhuri, D.; Mulder, B.; Dekker, C. bioRxiv 2018, 348052. doi: 10.1101/348052 doi: 10.1101/348052
45. [45]
  Walter, A.; Chapuis, C.; Huet, S.; Ellenberg, J. J. Struct. Biol. 2013, 184, 445. doi: 10.1016/j.jsb.2013.10.004 doi: 10.1016/j.jsb.2013.10.004
46. [46]
  Marenduzzo, D.; Micheletti, C.; Cook, P. R. Biophys. J. 2006, 90, 3712. doi: 10.1529/biophysj.105.077685 doi: 10.1529/biophysj.105.077685
47. [47]
  Junier, I.; Martin, O.; Kepes, F. PLoS Comput. Biol. 2010, 6, e1000678. doi: 10.1371/journal.pcbi.1000678 doi: 10.1371/journal.pcbi.1000678
48. [48]
  Barbieri, M.; Chotalia, M.; Fraser, J.; Lavitas, L. M.; Dostie, J.; Pombo, A.; Nicodemi, M. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 16173. doi: 10.1073/pnas.1204799109 doi: 10.1073/pnas.1204799109
49. [49]
  Scolari, V. F.; Cosentino Lagomarsino, M. Soft Matt. 2015, 11, 1677. doi: 10.1039/c4sm02434f doi: 10.1039/c4sm02434f
50. [50]
  Larson, A. G.; Elnatan, D.; Keenen, M. M.; Trnka, M. J.; Johnston, J. B.; Burlingame, A. L.; Agard, D. A.; Redding, S.; Narlikar, G. J. Nature 2017, 547, 236. doi: 10.1038/nature22822 doi: 10.1038/nature22822
51. [51]
  Strom, A. R.; Emelyanov, A. V.; Mir, M.; Fyodorov, D. V.; Darzacq, X.; Karpen, G. H. Nature 2017, 547, 241. doi: 10.1038/nature22989 doi: 10.1038/nature22989
52. [52]
  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.; et al. Cell 2018, 175, 1842. doi: 10.1016/j.cell.2018.10.042 doi: 10.1016/j.cell.2018.10.042
53. [53]
  Hnisz, D.; Shrinivas, K.; Young, R. A.; Chakraborty, A. K.; Sharp, P. A. Cell 2017, 169, 13. doi: 10.1016/j.cell.2017.02.007 doi: 10.1016/j.cell.2017.02.007
54. [54]
  Erdel, F.; Rippe, K. Biophys. J. 2018, 114, 2262. doi: 10.1016/j.bpj.2018.03.011 doi: 10.1016/j.bpj.2018.03.011
55. [55]
  Alipour, E.; Marko, J. F. Nucleic Acids Res. 2012, 40, 11202. doi: 10.1093/nar/gks925 doi: 10.1093/nar/gks925
56. [56]
  Sanborn, A. L.; Rao, S. S.; Huang, S. C.; Durand, N. C.; Huntley, M. H.; Jewett, A. I.; Bochkov, I. D.; Chinnappan, D.; Cutkosky, A.; Li, J.; et al. Proc. Natl. Acad. Sci. U. S. A. 2015, 112, E6456. doi: 10.1073/pnas.1518552112 doi: 10.1073/pnas.1518552112
57. [57]
  Fudenberg, G.; Imakaev, M.; Lu, C.; Goloborodko, A.; Abdennur, N.; Mirny, L. A. Cell Rep. 2016, 15, 2038. doi: 10.1016/j.celrep.2016.04.085 doi: 10.1016/j.celrep.2016.04.085
58. [58]
  Weintraub, A. S.; Li, C. H.; Zamudio, A. V.; Sigova, A. A.; Hannett, N. M.; Day, D. S.; Abraham, B. J.; Cohen, M. A.; Nabet, B.; Buckley, D. L.; et al. Cell 2017, 171, 1573. doi: 10.1016/j.cell.2017.11.008 doi: 10.1016/j.cell.2017.11.008
59. [59]
  Banani, S. F.; Lee, H. O.; Hyman, A. A.; Rosen, M. K. Nat. Rev. Mol. Cell Biol. 2017, 18, 285. doi: 10.1038/nrm.2017.7 doi: 10.1038/nrm.2017.7
60. [60]
  Brangwynne, C. P.; Tompa, P.; Pappu, R. V. Nat. Phys. 2015, 11, 899. doi: 10.1038/nphys3532 doi: 10.1038/nphys3532
61. [61]
  Bernardi, G.; Olofsson, B.; Filipski, J.; Zerial, M.; Salinas, J.; Cuny, G.; Meunier-Rotival, M.; Rodier, F. Science 1985, 228, 953. doi: 10.1126/science.4001930 doi: 10.1126/science.4001930
62. [62]
  Costantini, M.; Clay, O.; Auletta, F.; Bernardi, G. Genome Res. 2006, 16, 536. doi: 10.1101/gr.4910606 doi: 10.1101/gr.4910606
63. [63]
  Quante, T.; Bird, A. Nat. Rev. Mol. Cell Biol. 2016, 17, 257. doi: 10.1038/nrm.2015.31 doi: 10.1038/nrm.2015.31
64. [64]
  Deaton, A. M.; Bird, A. Genes Dev. 2011, 25, 1010. doi: 10.1101/gad.2037511 doi: 10.1101/gad.2037511
65. [65]
  Schneider, R.; Grosschedl, R. Genes Dev. 2007, 21, 3027. doi: 10.1101/gad.1604607 doi: 10.1101/gad.1604607
66. [66]
  Clauset, A.; Shalizi, C. R.; Newman, M. E. J. Siam. Rev. 2009, 51, 661. doi: 10.1137/070710111 doi: 10.1137/070710111
67. [67]
  Li, W. Phys. Rev. A 1991, 43, 5240. doi: 10.1103/physreva.43.5240 doi: 10.1103/physreva.43.5240
68. [68]
  Azbel, M. Y. Phys. Rev. Lett. 1973, 31, 589. doi: 10.1103/PhysRevLett.31.589 doi: 10.1103/PhysRevLett.31.589
69. [69]
  Azbel, M. Y.; Kantor, Y.; Verkh, L.; Vilenkin, A. Biopolymers 1982, 21, 1687. doi: 10.1002/bip.360210816 doi: 10.1002/bip.360210816
70. [70]
  Azbel, M. Y. Phys. Rev. Lett. 1995, 75, 168. doi: 10.1103/PhysRevLett.75.168 doi: 10.1103/PhysRevLett.75.168
71. [71]
  Grosberg, A.; Rabin, Y.; Havlin, S.; Neer, A. Europhys. Lett. 1993, 23, 373. doi: 10.1209/0295-5075/23/5/012 doi: 10.1209/0295-5075/23/5/012
72. [72]
  Liu, S.; Zhang, L.; Quan, H.; Tian, H.; Meng, L.; Yang, L.; Feng, H.; Gao, Y. Q. Nucleic Acids Res. 2018, doi: 10.1093/nar/gky633 doi: 10.1093/nar/gky633
73. [73]
  Du, Z.; Zheng, H.; Huang, B.; Ma, R.; Wu, J.; Zhang, X.; He, J.; Xiang, Y.; Wang, Q.; Li, Y.; et al. Nature 2017, 547, 232. doi: 10.1038/nature23263 doi: 10.1038/nature23263
74. [74]
  Ke, Y.; Xu, Y.; Chen, X.; Feng, S.; Liu, Z.; Sun, Y.; Yao, X.; Li, F.; Zhu, W.; Gao, L.; et al. Cell 2017, 170, 367. doi: 10.1016/j.cell.2017.06.029 doi: 10.1016/j.cell.2017.06.029
75. [75]
  Lu, F.; Liu, Y.; Inoue, A.; Suzuki, T.; Zhao, K.; Zhang, Y. Cell 2016, 165, 1375. doi: 10.1016/j.cell.2016.05.050 doi: 10.1016/j.cell.2016.05.050
76. [76]
  Flyamer, I. M.; Gassler, J.; Imakaev, M.; Brandao, H. B.; Ulianov, S. V.; Abdennur, N.; Razin, S. V.; Mirny, L. A.; Tachibana-Konwalski, K. Nature 2017, 544, 110. doi: 10.1038/nature21711 doi: 10.1038/nature21711
77. [77]
  Quan, H.; Liu, S.; Zhang, Y.; Xie, W.; Gao, Y. Q. bioRxiv 2019, 521401v1. doi: 10.1101/521401 doi: 10.1101/521401
78. [78]
  Efroni, S.; Duttagupta, R.; Cheng, J.; Dehghani, H.; Hoeppner, D. J.; Dash, C.; Bazett-Jones, D. P.; Le Grice, S.; McKay, R. D.; Buetow, K. H.; et al. Cell Stem Cell 2008, 2, 437. doi: 10.1016/j.stem.2008.03.021 doi: 10.1016/j.stem.2008.03.021
79. [79]
  Park, S. H.; Park, S. H.; Kook, M. C.; Kim, E. Y.; Park, S.; Lim, J. H. Ultrastruct. Pathol. 2004, 28, 229. doi: 10.1080/01913120490515595 doi: 10.1080/01913120490515595
80. [80]
  Hawkins, R. D.; Hon, G. C.; Lee, L. K.; Ngo, Q.; Lister, R.; Pelizzola, M.; Edsall, L. E.; Kuan, S.; Luu, Y.; Klugman, S.; et al. Cell Stem Cell 2010, 6, 479. doi: 10.1016/j.stem.2010.03.018 doi: 10.1016/j.stem.2010.03.018
81. [81]
  Meshorer, E.; Yellajoshula, D.; George, E.; Scambler, P. J.; Brown, D. T.; Misteli, T. Dev. Cell 2006, 10, 105. doi: 10.1016/j.devcel.2005.10.017 doi: 10.1016/j.devcel.2005.10.017
82. [82]
  Bonev, B.; Mendelson Cohen, N.; Szabo, Q.; Fritsch, L.; Papadopoulos, G. L.; Lubling, Y.; Xu, X.; Lv, X.; Hugnot, J. P.; Tanay, A.; et al. Cell 2017, 171, 557. doi: 10.1016/j.cell.2017.09.043 doi: 10.1016/j.cell.2017.09.043
83. [83]
  Chandra, T.; Ewels, P. A.; Schoenfelder, S.; Furlan-Magaril, M.; Wingett, S. W.; Kirschner, K.; Thuret, J. Y.; Andrews, S.; Fraser, P.; Reik, W. Cell Rep. 2015, 10, 471. doi: 10.1016/j.celrep.2014.12.055 doi: 10.1016/j.celrep.2014.12.055
84. [84]
  Chandra, T.; Kirschner, K.; Thuret, J. Y.; Pope, B. D.; Ryba, T.; Newman, S.; Ahmed, K.; Samarajiwa, S. A.; Salama, R.; Carroll, T.; et al. Mol. Cell 2012, 47, 203. doi: 10.1016/j.molcel.2012.06.010 doi: 10.1016/j.molcel.2012.06.010
85. [85]
  Singhal, N.; Graumann, J.; Wu, G.; Arauzo-Bravo, M. J.; Han, D. W.; Greber, B.; Gentile, L.; Mann, M.; Scholer, H. R. Cell 2010, 141, 943. doi: 10.1016/j.cell.2010.04.037 doi: 10.1016/j.cell.2010.04.037
86. [86]
  Gaspar-Maia, A.; Alajem, A.; Polesso, F.; Sridharan, R.; Mason, M. J.; Heidersbach, A.; Ramalho-Santos, J.; McManus, M. T.; Plath, K.; Meshorer, E.; et al. Nature 2009, 460, 863. doi: 10.1038/nature08212 doi: 10.1038/nature08212
87. [87]
  Wang, L.; Du, Y.; Ward, J. M.; Shimbo, T.; Lackford, B.; Zheng, X.; Miao, Y. L.; Zhou, B.; Han, L.; Fargo, D. C.; et al. Cell Stem Cell 2014, 14, 575. doi: 10.1016/j.stem.2014.02.013 doi: 10.1016/j.stem.2014.02.013
88. [88]
  Barutcu, A. R.; Maass, P. G.; Lewandowski, J. P.; Weiner, C. L.; Rinn, J. L. Nat. Commun. 2018, 9, 1444. doi: 10.1038/s41467-018-03614-0 doi: 10.1038/s41467-018-03614-0
89. [89]
  Wang, F.; Higgins, J. M. Trends Cell Biol. 2013, 23, 175. doi: 10.1016/j.tcb.2012.11.005 doi: 10.1016/j.tcb.2012.11.005
90. [90]
  Thomson, I.; Gilchrist, S.; Bickmore, W. A.; Chubb, J. R. Curr. Biol. 2004, 14, 166. doi: 10.1016/j.cub.2003.12.024 doi: 10.1016/j.cub.2003.12.024
91. [91]
  Walter, J.; Schermelleh, L.; Cremer, M.; Tashiro, S.; Cremer, T. J. Cell Biol. 2003, 160, 685. doi: 10.1083/jcb.200211103 doi: 10.1083/jcb.200211103
92. [92]
  Nagano, T.; Lubling, Y.; Stevens, T. J.; Schoenfelder, S.; Yaffe, E.; Dean, W.; Laue, E. D.; Tanay, A.; Fraser, P. Nature 2013, 502, 59. doi: 10.1038/nature12593 doi: 10.1038/nature12593
93. [93]
  Egli, D.; Birkhoff, G.; Eggan, K. Nat. Rev. Mol. Cell Biol. 2008, 9, 505. doi: 10.1038/nrm2439 doi: 10.1038/nrm2439
94. [94]
  Sabari, B. R.; Dall'Agnese, A.; Boija, A.; Klein, I. A.; Coffey, E. L.; Shrinivas, K.; Abraham, B. J.; Hannett, N. M.; Zamudio, A. V.; Manteiga, J. C.; et al. Science 2018, 361, eaar3958. doi: 10.1126/science.aar3958 doi: 10.1126/science.aar3958
95. [95]
  Rademacher, A.; Erdel, F.; Trojanowski, J.; Schumacher, S.; Rippe, K. J. Cell Sci. 2017, 130, 4213. doi: 10.1242/jcs.205534 doi: 10.1242/jcs.205534
96. [96]
  Janicki, S. M.; Tsukamoto, T.; Salghetti, S. E.; Tansey, W. P.; Sachidanandam, R.; Prasanth, K. V.; Ried, T.; Shav-Tal, Y.; Bertrand, E.; Singer, R. H.; et al. Cell 2004, 116, 683. doi: 10.1016/S0092-8674(04)00171-0 doi: 10.1016/S0092-8674(04)00171-0
97. [97]
  Li, G.; Ruan, X.; Auerbach, R. K.; Sandhu, K. S.; Zheng, M.; Wang, P.; Poh, H. M.; Goh, Y.; Lim, J.; Zhang, J.; et al. Cell 2012, 148, 84. doi: 10.1016/j.cell.2011.12.014 doi: 10.1016/j.cell.2011.12.014
98. [98]
  Hsieh, T. H.; Weiner, A.; Lajoie, B.; Dekker, J.; Friedman, N.; Rando, O. J. Cell 2015, 162, 108. doi: 10.1016/j.cell.2015.05.048 doi: 10.1016/j.cell.2015.05.048
99. [99]
  Hsieh, T. H. S.; Fudenberg, G.; Goloborodko, A.; Rando, O. J. Nat. Methods 2016, 13, 1009. doi: 10.1038/nmeth.4025 doi: 10.1038/nmeth.4025
100. [100]
  Hsieh, T. H. S.; Slobodyanyuk, E.; Hansen, A. S.; Cattoglio, C.; Rando, O. J.; Tjian, R.; Darzacq, X. bioRxiv 2019, 638775. doi: 10.1101/638775 doi: 10.1101/638775
101. [101]
  Sexton, T.; Cavalli, G. Cell 2015, 160, 1049. doi: 10.1016/j.cell.2015.02.040 doi: 10.1016/j.cell.2015.02.040
102. [102]
  Barbieri, M.; Chotalia, M.; Fraser, J.; Lavitas, L. M.; Dostie, J.; Pombo, A.; Nicodemi, M. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 16173. doi: 10.1073/pnas.1204799109 doi: 10.1073/pnas.1204799109
103. [103]
  Jin, F.; Li, Y.; Dixon, J. R.; Selvaraj, S.; Ye, Z.; Lee, A. Y.; Yen, C. A.; Schmitt, A. D.; Espinoza, C. A.; Ren, B. Nature 2013, 503, 290. doi: 10.1038/nature12644 doi: 10.1038/nature12644
104. [104]
  Sanyal, A.; Lajoie, B. R.; Jain, G.; Dekker, J. Nature 2012, 489, 109. doi: 10.1038/nature11279 doi: 10.1038/nature11279
105. [105]
  Toth, K. F.; Knoch, T. A.; Wachsmuth, M.; Frank-Stohr, M.; Stohr, M.; Bacher, C. P.; Muller, G.; Rippe, K. J. Cell Sci. 2004, 117, 4277. doi: 10.1242/jcs.01293 doi: 10.1242/jcs.01293
106. [106]
  Hsu, J. Y.; Sun, Z. W.; Li, X.; Reuben, M.; Tatchell, K.; Bishop, D. K.; Grushcow, J. M.; Brame, C. J.; Caldwell, J. A.; Hunt, D. F.; et al. Cell 2000, 102, 279. doi: 10.1016/s0092-8674(00)00034-9 doi: 10.1016/s0092-8674(00)00034-9
107. [107]
  Crosio, C.; Fimia, G. M.; Loury, R.; Kimura, M.; Okano, Y.; Zhou, H.; Sen, S.; Allis, C. D.; Sassone-Corsi, P. Mol. Cell Biol. 2002, 22, 874. doi: 10.1128/mcb.22.3.874-885.2002 doi: 10.1128/mcb.22.3.874-885.2002
108. [108]
  Van Hooser, A.; Goodrich, D. W.; Allis, C. D.; Brinkley, B. R.; Mancini, M. A. J Cell Sci. 1998, 111 (Pt 23), 3497
109. [109]
  West, M. H.; Bonner, W. M. Nucleic Acids Res. 1980, 8, 4671. doi: 10.1093/nar/8.20.4671 doi: 10.1093/nar/8.20.4671
110. [110]
  Xiao, T.; Kao, C. F.; Krogan, N. J.; Sun, Z. W.; Greenblatt, J. F.; Osley, M. A.; Strahl, B. D. Mol. Cell Biol. 2005, 25, 637. doi: 10.1128/mcb.25.2.637-651.2005 doi: 10.1128/mcb.25.2.637-651.2005
111. [111]
  Fierz, B.; Chatterjee, C.; McGinty, R. K.; Bar-Dagan, M.; Raleigh, D. P.; Muir, T. W. Nat. Chem. Biol. 2011, 7, 113. doi: 10.1038/nchembio.501 doi: 10.1038/nchembio.501
112. [112]
  Kadauke, S.; Blobel, G. A. Epigenetics Chromatin 2013, 6, 6. doi: 10.1186/1756-8935-6-6 doi: 10.1186/1756-8935-6-6
113. [113]
  Naumova, N.; Imakaev, M.; Fudenberg, G.; Zhan, Y.; Lajoie, B. R.; Mirny, L. A.; Dekker, J. Science 2013, 342, 948. doi: 10.1126/science.1236083 doi: 10.1126/science.1236083
114. [114]
  Nagano, T.; Lubling, Y.; Varnai, C.; Dudley, C.; Leung, W.; Baran, Y.; Mendelson Cohen, N.; Wingett, S.; Fraser, P.; Tanay, A. Nature 2017, 547, 61. doi: 10.1038/nature23001 doi: 10.1038/nature23001
115. [115]
  Simonis, M.; Klous, P.; Splinter, E.; Moshkin, Y.; Willemsen, R.; de Wit, E.; van Steensel, B.; de Laat, W. Nat. Genet. 2006, 38, 1348. doi: 10.1038/ng1896 doi: 10.1038/ng1896
116. [116]
  Zhang, L.; Xie, W. J.; Liu, S.; Meng, L.; Gu, C.; Gao, Y. Q. Biophys. J. 2017, 113, 1395. doi: 10.1016/j.bpj.2017.08.019 doi: 10.1016/j.bpj.2017.08.019
117. [117]
  Graf, W.; Porje, I. G.; Allgoth, A. M. Gastroenterologia 1955, 83, 233. doi: 10.1159/000200143 doi: 10.1159/000200143
118. [118]
  Dewasmes, G.; Loos, N.; Delanaud, S.; Ramadan, W.; Dewasmes, D. Sleep 2003, 26, 948. doi: 10.1093/sleep/26.8.948 doi: 10.1093/sleep/26.8.948
119. [119]
  Liu, C.; Cheng, Y. J.; Wang, J. W.; Weigel, D. Nat. Plants 2017, 3, 742. doi: 10.1038/s41477-017-0005-9 doi: 10.1038/s41477-017-0005-9
120. [120]
  Xiao, H.; Run, X.; Cao, X.; Su, Y.; Sun, Z.; Tian, C.; Sun, S.; Liang, Z. Psychiatry Clin. Neurosci. 2013, 67, 493. doi: 10.1111/pcn.12091 doi: 10.1111/pcn.12091
121. [121]
  Ahmadian-Attari, M. M.; Dargahi, L.; Mosaddegh, M.; Kamalinejad, M.; Khallaghi, B.; Noorbala, F.; Ahmadiani, A. Neurotox. Res. 2015, 28, 95. doi: 10.1007/s12640-015-9525-0 doi: 10.1007/s12640-015-9525-0
122. [122]
  Lawson, R. N.; Chughtai, M. S. Can. Med. Assoc. J. 1963, 88, 68.
123. [123]
  Chandrasoma, P.; Taylor, C. R. Concise Pathology, 3rd ed.; Appleton & Lange: Stamford, Connecticut, US, 1998; p. 1040.
124. [124]
  Johnston, R. K.; Snell, T. W. Exp. Gerontol. 2016, 78, 12. doi: 10.1016/j.exger.2016.02.014 doi: 10.1016/j.exger.2016.02.014
125. [125]
  Conti, B.; Sanchez-Alavez, M.; Winsky-Sommerer, R.; Morale, M. C.; Lucero, J.; Brownell, S.; Fabre, V.; Huitron-Resendiz, S.; Henriksen, S.; Zorrilla, E. P.; et al. Science 2006, 314, 825. doi: 10.1126/science.1132191 doi: 10.1126/science.1132191
126. [126]
  Waalen, J.; Buxbaum, J. N. J. Gerontol. A-Biol. Sci. Med. Sci. 2011, 66, 487. doi: 10.1093/gerona/glr001 doi: 10.1093/gerona/glr001
127. [127]
  Bernardi, G. Gene 2000, 241, 3. doi: 10.1016/S0378-1119(99)00485-0 doi: 10.1016/S0378-1119(99)00485-0
128. [128]
  White, C. R.; Seymour, R. S. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 4046. doi: 10.1073/pnas.0436428100 doi: 10.1073/pnas.0436428100
129. [129]
  Brattstrom, B. H. Am. Midl. Nat. 1965, 73, 376. doi: 10.2307/2423461 doi: 10.2307/2423461
130. [130]
  Coulondre, C.; Miller, J. H.; Farabaugh, P. J.; Gilbert, W. Nature 1978, 274, 775. doi: 10.1038/274775a0 doi: 10.1038/274775a0
131. [131]
  Dudchenko, O.; Batra, S. S.; Omer, A. D.; Nyquist, S. K.; Hoeger, M.; Durand, N. C.; Shamim, M. S.; Machol, I.; Lander, E. S.; Aiden, A. P.; et al. Science 2017, 356, 92. doi: 10.1126/science.aal3327 doi: 10.1126/science.aal3327
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