Evolutionarily Conserved Principles Predict 3D Chromatin Organization

Molecular Cell

Volumn 67, Issue 5, 2017, Pages 837-852.e7

  Rowley, M Jordan ^a   Nichols, Michael H ^a   Lyu, Xiaowen ^a   Ando Kuri, Masami ^a   Rivera, I Sarahi M ^a   Hermetz, Karen ^a   Wang, Ping ^b   Ruan, Yijun ^b   Corces, Victor G ^a  

^a EMORY UNIVERSITY   (United States)

^b JACKSON LABORATORY   (United States)

Author keywords

compartment; CTCF; epigenetics; Hi C; insulator; loop; TAD; transcription

Indexed keywords

TRIPTOLIDE; ARABIDOPSIS PROTEIN; CAENORHABDITIS ELEGANS PROTEIN; CHROMATIN; DNA; DROSOPHILA PROTEIN; HISTONE; NONHISTONE PROTEIN; PLANT DNA;

ARABIDOPSIS THALIANA; ARTICLE; CAENORHABDITIS ELEGANS; CELL COMPARTMENTALIZATION; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME STRUCTURE; CLINICAL FEATURE; COMPUTER SIMULATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EUKARYOTE; GENE EXPRESSION; GENOME ANALYSIS; HISTONE MODIFICATION; HUMAN; HUMAN CELL; NONHUMAN; PHYLOGENETIC TREE; PRINCIPAL COMPONENT ANALYSIS; PROMOTER REGION; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; ANIMAL; ARABIDOPSIS; BIOLOGICAL MODEL; CHEMISTRY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONFORMATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOMAL PROTEINS, NON-HISTONE; COMPUTER SIMULATION; DNA; DNA, PLANT; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HISTONES; HUMANS; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION, GENETIC;

EID: 85027529210     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2017.07.022     Document Type: Article

References (48)

1. Andersson, R., Refsing Andersen, P., Valen, E., Core, L.J., Bornholdt, J., Boyd, M., Heick Jensen, T., Sandelin, A., Nuclear stability and transcriptional directionality separate functionally distinct RNA species. Nat. Commun., 5, 2014, 5336.
2. Ay, F., Bunnik, E.M., Varoquaux, N., Bol, S.M., Prudhomme, J., Vert, J.-P., Noble, W.S., Le Roch, K.G., Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression. Genome Res. 24 (2014), 974–988.
3. Corces, M.R., Buenrostro, J.D., Wu, B., Greenside, P.G., Chan, S.M., Koenig, J.L., Snyder, M.P., Pritchard, J.K., Kundaje, A., Greenleaf, W.J., et al. Lineage-specific and single-cell chromatin accessibility charts human hematopoiesis and leukemia evolution. Nat. Genet. 48 (2016), 1193–1203.
4. Core, L.J., Waterfall, J.J., Lis, J.T., Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322 (2008), 1845–1848.
5. Core, L.J., Waterfall, J.J., Gilchrist, D.A., Fargo, D.C., Kwak, H., Adelman, K., Lis, J.T., Defining the status of RNA polymerase at promoters. Cell Rep. 2 (2012), 1025–1035.
6. Core, L.J., Martins, A.L., Danko, C.G., Waters, C.T., Siepel, A., Lis, J.T., Analysis of nascent RNA identifies a unified architecture of initiation regions at mammalian promoters and enhancers. Nat. Genet. 46 (2014), 1311–1320.
7. Crane, E., Bian, Q., McCord, R.P., Lajoie, B.R., Wheeler, B.S., Ralston, E.J., Uzawa, S., Dekker, J., Meyer, B.J., Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523 (2015), 240–244.
8. Cubeñas-Potts, C., Rowley, M.J., Lyu, X., Li, G., Lei, E.P., Corces, V.G., Different enhancer classes in Drosophila bind distinct architectural proteins and mediate unique chromatin interactions and 3D architecture. Nucleic Acids Res. 45 (2017), 1714–1730.
9. Dixon, J.R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J.S., Ren, B., Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485 (2012), 376–380.
10. Durand, N.C., Shamim, M.S., Machol, I., Rao, S.S.P., Huntley, M.H., Lander, E.S., Aiden, E.L., Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 3 (2016), 95–98.
11. Durand, N.C., Robinson, J.T., Shamim, M.S., Machol, I., Mesirov, J.P., Lander, E.S., Aiden, E.L., Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. Cell Syst. 3 (2016), 99–101.
12. El-Sharnouby, S., Fischer, B., Magbanua, J.P., Umans, B., Flower, R., Choo, S.W., Russell, S., White, R., Regions of very low H3K27me3 partition the Drosophila genome into topological domains. PLoS ONE, 12, 2017, e0172725.
13. Galazka, J.M., Klocko, A.D., Uesaka, M., Honda, S., Selker, E.U., Freitag, M., Neurospora chromosomes are organized by blocks of importin alpha-dependent heterochromatin that are largely independent of H3K9me3. Genome Res. 26 (2016), 1069–1080.
14. Goh, Y., Fullwood, M.J., Poh, H.M., Peh, S.Q., Ong, C.T., Zhang, J., Ruan, X., Ruan, Y., Chromatin interaction analysis with paired-end tag sequencing (ChIA-PET) for mapping chromatin interactions and understanding transcription regulation. J. Vis. Exp., 2012, 2012, 3770.
15. Gómez-Marín, C., Tena, J.J., Acemel, R.D., López-Mayorga, M., Naranjo, S., de la Calle-Mustienes, E., Maeso, I., Beccari, L., Aneas, I., Vielmas, E., et al. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders. Proc. Natl. Acad. Sci. USA 112 (2015), 7542–7547.
16. Gonçalves, A.P., Hall, C., Kowbel, D.J., Glass, N.L., Videira, A., CZT-1 is a novel transcription factor controlling cell death and natural drug resistance in Neurospora crassa. G3 (Bethesda) 4 (2014), 1091–1102.
17. Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D.U., Jung, I., Wu, H., Zhai, Y., Tang, Y., et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162 (2015), 900–910.
18. He, C., Zhang, M.Q., Wang, X., MICC: an R package for identifying chromatin interactions from ChIA-PET data. Bioinformatics 31 (2015), 3832–3834.
19. Hillier, L.W., Reinke, V., Green, P., Hirst, M., Marra, M.A., Waterston, R.H., Massively parallel sequencing of the polyadenylated transcriptome of C. elegans. Genome Res. 19 (2009), 657–666.
20. Hou, C., Li, L., Qin, Z.S., Corces, V.G., Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 48 (2012), 471–484.
21. Hug, C.B., Grimaldi, A.G., Kruse, K., Vaquerizas, J.M., Chromatin architecture emerges during zygotic genome activation independent of transcription. Cell 169 (2017), 216–228.e19.
22. 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., A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503 (2013), 290–294.
23. Jung, Y.H., Sauria, M.E.G., Lyu, X., Cheema, M.S., Ausio, J., Taylor, J., Corces, V.G., Chromatin states in mouse sperm correlate with embryonic and adult regulatory landscapes. Cell Rep. 18 (2017), 1366–1382.
24. Kasowski, M., Kyriazopoulou-Panagiotopoulou, S., Grubert, F., Zaugg, J.B., Kundaje, A., Liu, Y., Boyle, A.P., Zhang, Q.C., Zakharia, F., Spacek, D.V., et al. Extensive variation in chromatin states across humans. Science 342 (2013), 750–752.
25. Kensche, P.R., Hoeijmakers, W.A.M., Toenhake, C.G., Bras, M., Chappell, L., Berriman, M., Bártfai, R., The nucleosome landscape of Plasmodium falciparum reveals chromatin architecture and dynamics of regulatory sequences. Nucleic Acids Res. 44 (2016), 2110–2124.
26. Kubo, N., Ishii, H., Gorkin, D., Meitinger, F., Xiong, X., Fang, R., Liu, T., Ye, Z., Li, B., Dixon, J., et al. Preservation of chromatin organization after acute loss of CTCF in mouse embryonic stem cells. bioRxiv, 2017, 10.1101/118737.
27. Kwak, H., Fuda, N.J., Core, L.J., Lis, J.T., Precise maps of RNA polymerase reveal how promoters direct initiation and pausing. Science 339 (2013), 950–953.
28. Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, 2009, R25.
29. Li, L., Lyu, X., Hou, C., Takenaka, N., Nguyen, H.Q., Ong, C.-T., Cubeñas-Potts, C., Hu, M., Lei, E.P., Bosco, G., et al. Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing. Mol. Cell 58 (2015), 216–231.
30. 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. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326 (2009), 289–293.
31. Moore, B.L., Aitken, S., Semple, C.A., Integrative modeling reveals the principles of multi-scale chromatin boundary formation in human nuclear organization. Genome Biol., 16, 2015, 110.
32. Mumbach, M.R., Rubin, A.J., Flynn, R.A., Dai, C., Khavari, P.A., Greenleaf, W.J., Chang, H.Y., HiChIP: efficient and sensitive analysis of protein-directed genome architecture. Nat. Methods 13 (2016), 919–922.
33. Nora, E.P., Goloborodko, A., Valton, A.-L., Gibcus, J.H., Uebersohn, A., Abdennur, N., Dekker, J., Mirny, L.A., Bruneau, B.G., Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169 (2017), 930–944.e22.
34. Pai, C.-Y., Lei, E.P., Ghosh, D., Corces, V.G., The centrosomal protein CP190 is a component of the gypsy chromatin insulator. Mol. Cell 16 (2004), 737–748.
35. Rao, S.S.P., 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., Aiden, E.L., A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159 (2014), 1665–1680.
36. Rowley, M.J., Corces, V.G., The three-dimensional genome: principles and roles of long-distance interactions. Curr. Opin. Cell Biol. 40 (2016), 8–14.
37. Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A., Cavalli, G., Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148 (2012), 458–472.
38. Shen, L., Shao, N., Liu, X., Nestler, E., ngs.plot: quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics, 15, 2014, 284.
39. Swaminathan, J., Baxter, E.M., Corces, V.G., The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev. 19 (2005), 65–76.
40. Ulianov, S.V., Khrameeva, E.E., Gavrilov, A.A., Flyamer, I.M., Kos, P., Mikhaleva, E.A., Penin, A.A., Logacheva, M.D., Imakaev, M.V., Chertovich, A., et al. Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res. 26 (2016), 70–84.
41. Van Bortle, K., Corces, V.G., The role of chromatin insulators in nuclear architecture and genome function. Curr. Opin. Genet. Dev. 23 (2013), 212–218.
42. Van Bortle, K., Ramos, E., Takenaka, N., Yang, J., Wahi, J.E., Corces, V.G., Drosophila CTCF tandemly aligns with other insulator proteins at the borders of H3K27me3 domains. Genome Res. 22 (2012), 2176–2187.
43. Van Bortle, K., Nichols, M.H., Li, L., Ong, C.-T., Takenaka, N., Qin, Z.S., Corces, V.G., Insulator function and topological domain border strength scale with architectural protein occupancy. Genome Biol., 15, 2014, R82.
44. Wang, C., Liu, C., Roqueiro, D., Grimm, D., Schwab, R., Becker, C., Lanz, C., Weigel, D., Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res. 25 (2015), 246–256.
45. Wirbelauer, C., Bell, O., Schübeler, D., Variant histone H3.3 is deposited at sites of nucleosomal displacement throughout transcribed genes while active histone modifications show a promoter-proximal bias. Genes Dev. 19 (2005), 1761–1766.
46. Yang, J., Sung, E., Donlin-Asp, P.G., Corces, V.G., A subset of Drosophila Myc sites remain associated with mitotic chromosomes colocalized with insulator proteins. Nat. Commun., 4, 2013, 1464.
47. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., Liu, X.S., Model-based analysis of ChIP-seq (MACS). Genome Biol., 9, 2008, R137.
48. Zhu, Y., Rowley, M.J., Böhmdorfer, G., Wierzbicki, A.T., A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing. Mol. Cell 49 (2013), 298–309.