Developing bioimaging and quantitative methods to study 3D genome
Juntao Gao, Xusan Yang, Mohamed Nadhir Djekidel, Yang Wang, Peng Xi, Michael Q. Zhang
Developing bioimaging and quantitative methods to study 3D genome
The recent advances in chromosome configuration capture (3C)-based series molecular methods and optical super-resolution (SR) techniques offer powerful tools to investigate three dimensional (3D) genomic structure in prokaryotic and eukaryotic cell nucleus. In this review, we focus on the progress during the last decade in this exciting field. Here we at first introduce briefly genome organization at chromosome, domain and sub-domain level, respectively; then we provide a short introduction to various super-resolution microscopy techniques which can be employed to detect genome 3D structure. We also reviewed the progress of quantitative and visualization tools to evaluate and visualize chromatin interactions in 3D genome derived from Hi-C data. We end up with the discussion that imaging methods and 3C-based molecular methods are not mutually exclusive - - - - actually they are complemental to each other and can be combined together to study 3D genome organization.
3D Genome / quantitative methods / bioimaging / super resolution
[1] |
Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P. (2002). Molecular Biology of the Cell New. 4th Ed., York: Garland Science
|
[2] |
Luger, K., Mäder, A. W., Richmond, R. K., Sargent, D. F. and Richmond, T. J. (1997) Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature, 389, 251–260
CrossRef
Google scholar
|
[3] |
Li, G. and Reinberg, D. (2011) Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev., 21, 175–186
CrossRef
Google scholar
|
[4] |
Thakar, A., Gupta, P., Ishibashi, T., Finn, R., Silva-Moreno, B., Uchiyama, S., Fukui, K., Tomschik, M., Ausio, J. and Zlatanova, J. (2009) H2A.Z and H3.3 histone variants affect nucleosome structure: biochemical and biophysical studies. Biochemistry (Mosc.), 48, 10852–10857
CrossRef
Google scholar
|
[5] |
Sahl, S. J. and Moerner, W. E. (2013) Super-resolution fluorescence imaging with single molecules. Curr. Opin. Struct. Biol., 23, 778–787
CrossRef
Google scholar
|
[6] |
Yamanaka, M., Smith, N. I. and Fujita, K. (2014) Introduction to super-resolution microscopy. Microscopy, 63, 177–192
CrossRef
Google scholar
|
[7] |
Doksani, Y., Wu, J. Y., de Lange, T. and Zhuang, X. (2013) Super-resolution fluorescence imaging of telomeres reveals TRF2-dependent t-loop formation. Cell, 155, 345–356
CrossRef
Google scholar
|
[8] |
Dekker, J., Rippe, K., Dekker, M. and Kleckner, N. (2002) Capturing chromosome conformation. Science, 295, 1306–1311
CrossRef
Google scholar
|
[9] |
Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S. and Ren, B. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature, 485, 376–380
CrossRef
Google scholar
|
[10] |
Kalhor, R., Tjong, H., Jayathilaka, N., Alber, F. and Chen, L. (2012) Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol., 30, 90–98
CrossRef
Google scholar
|
[11] |
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.,
CrossRef
Google scholar
|
[12] |
Zhang, Y., McCord, R. P., Ho, Y.-J., Lajoie, B. R., Hildebrand, D. G., Simon, A. C., Becker, M. S., Alt, F. W. and Dekker, J. (2012) Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell, 148, 908–921
CrossRef
Google scholar
|
[13] |
Cremer, T. and Cremer, C. (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet., 2, 292–301
CrossRef
Google scholar
|
[14] |
Funabiki, H., Hagan, I., Uzawa, S. and Yanagida, M. (1993) Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast. J. Cell Biol., 121, 961–976
CrossRef
Google scholar
|
[15] |
Mizuguchi, T., Barrowman, J. and Grewal, S. I. S. (2015) Chromosome domain architecture and dynamic organization of the fission yeast genome. FEBS Lett., 589, 2975–2986
CrossRef
Google scholar
|
[16] |
Rabl, C. (1885) Über Zelltheilung. Morphol. Jahrb., 10, 214–330
|
[17] |
Jin, Q.-W., Fuchs, J. and Loidl, J. (2000) Centromere clustering is a major determinant of yeast interphase nuclear organization. J. Cell Sci., 113, 1903–1912
|
[18] |
Cremer, T. (2013) Von der Zellenlehre zur Chromosomentheorie: Naturwissenschaftliche Erkenntnis und Theorienwechsel in der frühen Zell- und Vererbungsforschung. Berlin: Springer-Verlag
|
[19] |
Hochstrasser, M., Mathog, D., Gruenbaum, Y., Saumweber, H. and Sedat, J. W. (1986) Spatial organization of chromosomes in the salivary gland nuclei of Drosophila melanogaster. J. Cell Biol., 102, 112–123
CrossRef
Google scholar
|
[20] |
Zickler, D. and Kleckner, N. (1998) The leptotene-zygotene transition of meiosis. Annu. Rev. Genet., 32, 619–697
CrossRef
Google scholar
|
[21] |
Jin, Q., Trelles-Sticken, E., Scherthan, H. and Loidl, J. (1998) Yeast nuclei display prominent centromere clustering that is reduced in nondividing cells and in meiotic prophase. J. Cell Biol., 141, 21–29
CrossRef
Google scholar
|
[22] |
Noguchi, J. and Fukui, K. (1995) Chromatin arrangements in intact interphase nuclei examined by laser confocal microscopy. J. Plant Res., 108, 209–216
CrossRef
Google scholar
|
[23] |
Wilkie, G. S., Shermoen, A. W., O’Farrell, P. H. and Davis, I. (1999) Transcribed genes are localized according to chromosomal position within polarized Drosophila embryonic nuclei. Curr. Biol., 9, 1263–1266
CrossRef
Google scholar
|
[24] |
Bolzer, A., Kreth, G., Solovei, I., Koehler, D., Saracoglu, K., Fauth, C., Müller, S., Eils, R., Cremer, C., Speicher, M. R.,
CrossRef
Google scholar
|
[25] |
Boyle, S., Gilchrist, S., Bridger, J. M., Mahy, N. L., Ellis, J. A. and Bickmore, W. A. (2001) The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum. Mol. Genet., 10, 211–219
CrossRef
Google scholar
|
[26] |
Küpper, K., Kölbl, A., Biener, D., Dittrich, S., von Hase, J., Thormeyer, T., FieglerH., Carter, N. P., Speicher, M. R., Cremer, T.,
CrossRef
Google scholar
|
[27] |
Croft, J. A., Bridger, J. M., Boyle, S., Perry, P., Teague, P. and Bickmore, W. A. (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J. Cell Biol., 145, 1119–1131
CrossRef
Google scholar
|
[28] |
Fraser, J., Williamson, I., Bickmore, W. A. and Dostie, J. (2015) An overview of genome organization and how we got there: from FISH to Hi-C. Microbiol. Mol. Biol. Rev., 79, 347–372
CrossRef
Google scholar
|
[29] |
Kreth, G., Finsterle, J., von Hase, J., Cremer, M. and Cremer, C. (2004) Radial arrangement of chromosome territories in human cell nuclei: a computer model approach based on gene density indicates a probabilistic global positioning code. Biophys. J., 86, 2803–2812
CrossRef
Google scholar
|
[30] |
Bridger, J. M., Boyle, S., Kill, I. R. and Bickmore, W. A. (2000) Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts. Curr. Biol., 10, 149–152
CrossRef
Google scholar
|
[31] |
Mehta, I. S., Amira, M., Harvey, A. J. and Bridger, J. M. (2010) Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biol., 11, R5
CrossRef
Google scholar
|
[32] |
Nagele, R., Freeman, T., McMorrow, L. and Lee, H. Y. (1995) Precise spatial positioning of chromosomes during prometaphase: evidence for chromosomal order. Science, 270, 1831–1835
CrossRef
Google scholar
|
[33] |
Nagele, R. G., Freeman, T., Fazekas, J., Lee, K. M., Thomson, Z. and Lee, H. Y. (1998) Chromosome spatial order in human cells: evidence for early origin and faithful propagation. Chromosoma, 107, 330–338
CrossRef
Google scholar
|
[34] |
Bickmore, W. A. (2013) The spatial organization of the human genome. Annu. Rev. Genomics Hum. Genet., 14, 67–84
CrossRef
Google scholar
|
[35] |
Habermann, F. A., CremerM., Walter, J., Kreth, G., von Hase, J., Bauer, K., Wienberg, J., Cremer, C., Cremer, T. and Solovei, I. (2001) Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res., 9, 569–584
CrossRef
Google scholar
|
[36] |
Sun, H. B. and Yokota, H. (1999) Correlated positioning of homologous chromosomes in daughter fibroblast cells. Chromosome Res., 7, 603–610
CrossRef
Google scholar
|
[37] |
Gerlich, D., Beaudouin, J., Kalbfuss, B., Daigle, N., Eils, R. and Ellenberg, J. (2003) Global chromosome positions are transmitted through mitosis in mammalian cells. Cell, 112, 751–764
CrossRef
Google scholar
|
[38] |
Manders, E. M., Kimura, H. and Cook, P. R. (1999) Direct imaging of DNA in living cells reveals the dynamics of chromosome formation. J. Cell Biol., 144, 813–821
CrossRef
Google scholar
|
[39] |
Allison, D. C. and Nestor, A. L. (1999) Evidence for a relatively random array of human chromosomes on the mitotic ring. J. Cell Biol., 145, 1–14
CrossRef
Google scholar
|
[40] |
Walter, J., Schermelleh, L., Cremer, M., Tashiro, S. and Cremer, T. (2003) Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. J. Cell Biol., 160, 685–697
CrossRef
Google scholar
|
[41] |
Strickfaden, H., Zunhammer, A., van Koningsbruggen, S., Köhler, D. and Cremer, T. (2010) 4D chromatin dynamics in cycling cells: Theodor Boveri’s hypotheses revisited. Nucleus, 1, 284–297
|
[42] |
Umbarger, M. A., Toro, E., Wright, M. A., Porreca, G. J., Baù, D., Hong, S.-H., Fero, M. J., Zhu, L. J., Marti-Renom, M. A., McAdams, H. H.,
CrossRef
Google scholar
|
[43] |
Duan, Z., Andronescu, M., Schutz, K., McIlwain, S., Kim, Y. J., Lee, C., Shendure, J., Fields, S., Blau, C. A. and Noble, W. S. (2010) A three-dimensional model of the yeast genome. Nature, 465, 363–367
CrossRef
Google scholar
|
[44] |
Feng, S., Cokus, S. J., Schubert, V., Zhai, J., Pellegrini, M. and Jacobsen, S. E. (2014) Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol. Cell, 55, 694–707
CrossRef
Google scholar
|
[45] |
Filippova, D., Patro, R., Duggal, G. and Kingsford, C. (2014) Identification of alternative topological domains in chromatin. Algorithms Mol. Biol., 9, 14
CrossRef
Google scholar
|
[46] |
Phillips-Cremins, J. E., Sauria, M. E. G., Sanyal, A., Gerasimova, T. I., Lajoie, B. R., Bell, J. S. K., Ong, C.-T., Hookway, T. A., Guo, C., Sun, Y.,
CrossRef
Google scholar
|
[47] |
Hell, S. W. and Wichmann, J. (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett., 19, 780
CrossRef
Google scholar
|
[48] |
Klar, T. A. and Hell, S. W. (1999) Subdiffraction resolution in far-field fluorescence microscopy. Opt. Lett., 24, 954
CrossRef
Google scholar
|
[49] |
Schermelleh, L., Carlton, P. M., Haase, S., Shao, L., Winoto, L., Kner, P., Burke, B., Cardoso, M. C., Agard, D. A., Gustafsson, M. G. L.,
CrossRef
Google scholar
|
[50] |
Hafi, N., Grunwald, M., van den Heuvel, L. S., Aspelmeier, T., Chen, J.-H., Zagrebelsky, M., Schütte, O. M., Steinem, C., Korte, M., Munk, A.,
CrossRef
Google scholar
|
[51] |
Cox, S., Rosten, E., Monypenny, J., Jovanovic-Talisman, T., Burnette, D. T., Lippincott-SchwartzJ., Jones, G. E. and Heintzmann, R. (2012) Bayesian localization microscopy reveals nanoscale podosome dynamics. Nat. Methods, 9, 195–200
CrossRef
Google scholar
|
[52] |
Zhu, L., Zhang, W., Elnatan, D. and Huang, B. (2012) Faster STORM using compressed sensing. Nat. Methods, 9, 721–723
CrossRef
Google scholar
|
[53] |
Jungmann, R., Avendaño, M. S., Woehrstein, J. B., Dai, M., Shih, W. M. and Yin, P. (2014) Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat. Methods, 11, 313–318
CrossRef
Google scholar
|
[54] |
Sharonov, A. and Hochstrasser, R. M. (2006) Wide-field subdiffraction imaging by accumulated binding of diffusing probes. Proc. Natl. Acad. Sci. USA, 103, 18911–18916
CrossRef
Google scholar
|
[55] |
Henriques, R., Lelek, M., Fornasiero, E. F., Valtorta, F., Zimmer, C. and Mhlanga, M. M. (2010) QuickPALM: 3D real-time photoactivation nanoscopy image processing in Image. J. Nat. Methods, 7, 339–340
CrossRef
Google scholar
|
[56] |
Schoen, I., Ries, J., Klotzsch, E., Ewers, H. and Vogel, V. (2011) Binding-activated localization microscopy of DNA structures. Nano Lett., 11, 4008–4011
CrossRef
Google scholar
|
[57] |
Geissbuehler, S., Bocchio, N. L., Dellagiacoma, C., Berclaz, C., Leutenegger, M. and Lasser, T. (2012) Mapping molecular statistics with balanced super-resolution optical fluctuation imaging (bSOFI). Opt. Nanoscopy, 1, 1–7
CrossRef
Google scholar
|
[58] |
Hu, Y. S., Nan, X., Sengupta, P., Lippincott-Schwartz, J. and Cang, H. (2013) Accelerating 3B single-molecule super-resolution microscopy with cloud computing. Nat. Methods, 10, 96–97
CrossRef
Google scholar
|
[59] |
Wang, Y., Fruhwirth, G., Cai, E., Ng, T. and Selvin, P. R. (2013) 3D super-resolution imaging with blinking quantum dots. Nano Lett., 13, 5233–5241
CrossRef
Google scholar
|
[60] |
Ribeiro, S. A., Vagnarelli, P., Dong, Y., Hori, T., McEwen, B. F., Fukagawa, T., Flors, C. and Earnshaw, W. C. (2010) A super-resolution map of the vertebrate kinetochore. Proc. Natl. Acad. Sci. USA, 107, 10484–10489
CrossRef
Google scholar
|
[61] |
Matsuda, A., Shao, L., Boulanger, J., Kervrann, C., Carlton, P. M., Kner, P., Agard, D. and Sedat, J. W. (2010) Condensed mitotic chromosome structure at nanometer resolution using PALM and EGFP- histones. PLoS One, 5, e12768
CrossRef
Google scholar
|
[62] |
Bohn, M., Diesinger, P., Kaufmann, R., Weiland, Y., Müller, P., Gunkel, M., von Ketteler, A., Lemmer, P., Hausmann, M., Heermann, D. W.,
CrossRef
Google scholar
|
[63] |
Gunkel, M., Erdel, F., Rippe, K., Lemmer, P., Kaufmann, R., Hörmann, C., Amberger, R. and Cremer, C. (2009) Dual color localization microscopy of cellular nanostructures. Biotechnol. J., 4, 927–938
CrossRef
Google scholar
|
[64] |
Ptacin, J. L., Lee, S. F., Garner, E. C., Toro, E., Eckart, M., Comolli, L. R., Moerner, W. E. and Shapiro, L. (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat. Cell Biol., 12, 791–798
CrossRef
Google scholar
|
[65] |
Lee, H. D., Lord, S. J., Iwanaga, S., Zhan, K., Xie, H., Williams, J. C., Wang, H., Bowman, G. R., Goley, E. D., Shapiro, L.,
CrossRef
Google scholar
|
[66] |
Wang, W., Li, G.-W., Chen, C., Xie, X. S. and Zhuang, X. (2011) Chromosome organization by a nucleoid-associated protein in live bacteria. Science, 333, 1445–1449
CrossRef
Google scholar
|
[67] |
Wombacher, R., Heidbreder, M., van de Linde, S., Sheetz, M. P., Heilemann, M., Cornish, V. W. and Sauer, M. (2010) Live-cell super-resolution imaging with trimethoprim conjugates. Nat. Methods, 7, 717–719
CrossRef
Google scholar
|
[68] |
Klein, T., Löschberger, A., Proppert, S., Wolter, S., van de Linde, S. and Sauer, M. (2011) Live-cell dSTORM with SNAP-tag fusion proteins. Nat. Methods, 8, 7–9
CrossRef
Google scholar
|
[69] |
Flors, C. (2010) Photoswitching of monomeric and dimeric DNA-intercalating cyanine dyes for super-resolution microscopy applications. Photochem. Photobiol. Sci., 9, 643–648
|
[70] |
Müller, P., Schmitt, E., Jacob, A., Hoheisel, J., Kaufmann, R., Cremer, C. and Hausmann, M. (2010) COMBO-FISH enables high precision localization microscopy as a prerequisite for nanostructure analysis of genome loci. Int. J. Mol. Sci., 11, 4094–4105
CrossRef
Google scholar
|
[71] |
Weiland, Y., Lemmer, P. and Cremer, C. (2011) Combining FISH with localisation microscopy: Super-resolution imaging of nuclear genome nanostructures. Chromosome Res., 19, 5–23
CrossRef
Google scholar
|
[72] |
Beliveau, B. J., Boettiger, A. N., Avendaño, M. S., Jungmann, R., McCole, R. B., Joyce, E. F., Kim-Kiselak, C., Bantignies, F., Fonseka, C. Y., Erceg, J.,
CrossRef
Google scholar
|
[73] |
Zhang, H., Chen, L., Yang, X., Wang, M., Jing, Z., Han, H., Zhang, M., Jin, D., Gao, J., and Xi, P. (2016) Orientation mapping super-resolution with polarization demodulation. Light Sci. Appl., (Accepted)
|
[74] |
Liu, Z., Legant, W. R., Chen, B.-C., Li, L., Grimm, J. B., Lavis, L. D., Betzig, E. and Tjian, R. (2014) 3D imaging of Sox2 enhancer clusters in embryonic stem cells. eLife, 3, e04236
CrossRef
Google scholar
|
[75] |
Smeets, D., Markaki, Y., Schmid, V. J., Kraus, F., Tattermusch, A., Cerase, A., Sterr, M., Fiedler, S., Demmerle, J., Popken, J.,
CrossRef
Google scholar
|
[76] |
Markaki, Y., Smeets, D., Fiedler, S., Schmid, V. J., Schermelleh, L., Cremer, T. and Cremer, M. (2012) The potential of 3D-FISH and super-resolution structured illumination microscopy for studies of 3D nuclear architecture: 3D structured illumination microscopy of defined chromosomal structures visualized by 3D (immuno)-FISH opens new perspectives for studies of nuclear architecture. BioEssays, 34, 412–426
|
[77] |
Patel, N. S., Rhinn, M., Semprich, C. I., Halley, P. A., Dollé, P., Bickmore, W. A. and Storey, K. G. (2013) FGF signalling regulates chromatin organisation during neural differentiation via mechanisms that can be uncoupled from transcription. PLoS Genet., 9, e1003614
CrossRef
Google scholar
|
[78] |
Harke, B., Ullal, C. K., Keller, J. and Hell, S. W. (2008) Three-dimensional nanoscopy of colloidal crystals. Nano Lett., 8, 1309–1313
CrossRef
Google scholar
|
[79] |
Yang, X., Tzeng, Y.-K., Zhu, Z., Huang, Z., Chen, X., Liu, Y., Chang, H.-C., Huang, L., Li, W.-D. and Xi, P. (2014) Sub-diffraction imaging of nitrogen-vacancy centers in diamond by stimulated emission depletion and structured illumination. RSC Advances, 4, 11305–11310
CrossRef
Google scholar
|
[80] |
Xie, H., Liu, Y., Jin, D., Santangelo, P. J. and Xi, P. (2013) Analytical description of high-aperture STED resolution with 0–2p vortex phase modulation. J. Opt. Soc. Am. A Opt. Image Sci. Vis., 30, 1640–1645
CrossRef
Google scholar
|
[81] |
Watanabe, S., Punge, A., Hollopeter, G., Willig, K. I., Hobson, R. J., Davis, M. W., Hell, S. W. and Jorgensen, E. M. (2011) Protein localization in electron micrographs using fluorescence nanoscopy. Nat. Methods, 8, 80–84
CrossRef
Google scholar
|
[82] |
Ascoli, C. A., Jacob, T., Crowe, S. and Heidemann, K. (2015) Localization of HDAC1 Using Super-Resolution STED Microscopy. Leica Sci.
|
[83] |
Hu, Y. S., Zhu, Q., Elkins, K., Tse, K., Li, Y., Fitzpatrick, J. A. J., Verma, I. M. and Cang, H. (2013) Light-sheet Bayesian microscopy enables deep-cell super-resolution imaging of heterochromatin in live human embryonic stem cells. Opt. Nanoscopy, 2, 7
CrossRef
Google scholar
|
[84] |
Gebhardt, J. C. M., Suter, D. M., Roy, R., Zhao, Z. W., Chapman, A. R., BasuS., Maniatis, T. and Xie, X. S. (2013) Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nat. Methods, 10, 421–426
CrossRef
Google scholar
|
[85] |
Zhao, Z. W., Roy, R., Gebhardt, J. C. M., Suter, D. M., Chapman, A. R. and Xie, X. S. (2014) Spatial organization of RNA polymerase II inside a mammalian cell nucleus revealed by reflected light-sheet superresolution microscopy. Proc. Natl. Acad. Sci. USA, 111, 681–686
CrossRef
Google scholar
|
[86] |
Chen, B.-C., Legant, W. R., Wang, K., Shao, L., Milkie, D. E., Davidson, M. W., Janetopoulos, C., Wu, X. S., Hammer, J. A., Liu, Z.,
CrossRef
Google scholar
|
[87] |
O’Sullivan, J. M., Tan-Wong, S. M., Morillon, A., Lee, B., Coles, J., Mellor, J. and Proudfoot, N. J. (2004) Gene loops juxtapose promoters and terminators in yeast. Nat. Genet., 36, 1014–1018
CrossRef
Google scholar
|
[88] |
Ansari, A. and Hampsey, M. (2005) A role for the CPF 3′-end processing machinery in RNAP II-dependent gene looping. Genes Dev., 19, 2969–2978
CrossRef
Google scholar
|
[89] |
Boyle, S., Rodesch, M. J., Halvensleben, H. A., Jeddeloh, J. A. and Bickmore, W. A. (2011) Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosome Res., 19, 901–909
CrossRef
Google scholar
|
[90] |
Lévy-Leduc, C., Delattre, M., Mary-Huard, T. and Robin, S. (2014) Two-dimensional segmentation for analyzing Hi-C data. Bioinformatics, 30, i386–i392
CrossRef
Google scholar
|
[91] |
Wang, Y., Li, Y., Gao, J. and Zhang, M. Q. (2015) A novel method to identify topological domains using Hi-C data. Quant. Biol., 3, 81–89
CrossRef
Google scholar
|
[92] |
Dostie, J., Richmond, T. A., Arnaout, R. A., Selzer, R. R., Lee, W. L., Honan, T. A., Rubio, E. D., Krumm, A., Lamb, J., Nusbaum, C.,
CrossRef
Google scholar
|
[93] |
Handoko, L., Xu, H., Li, G., Ngan, C. Y., Chew, E., Schnapp, M., LeeC. W. H., Ye, C., Ping, J. L. H., Mulawadi, F.,
CrossRef
Google scholar
|
[94] |
Duggal, G., Wang, H. and Kingsford, C. (2014) Higher-order chromatin domains link eQTLs with the expression of far-away genes. Nucleic Acids Res., 42, 87–96
CrossRef
Google scholar
|
[95] |
Jhunjhunwala, S., van Zelm, M. C., Peak, M. M., Cutchin, S., Riblet, R., van Dongen, J. J. M., Grosveld, F. G., Knoch, T. A. and Murre, C. (2008) The 3D structure of the immunoglobulin heavy-chain locus: implications for long-range genomic interactions. Cell, 133, 265–279
CrossRef
Google scholar
|
[96] |
Nagano, T., Lubling, Y., Stevens, T. J., Schoenfelder, S., Yaffe, E., Dean, W., Laue, E. D., Tanay, A. and Fraser, P. (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature, 502, 59–64
CrossRef
Google scholar
|
[97] |
Marti-Renom, M. and Mirny, L. (2011) Bridging the resolution gap in structural modeling of 3D genome organization. PLoS Comput. Biol., 7, e1002125
CrossRef
Google scholar
|
[98] |
Barbieri, M., Chotalia, M., Fraser, J., Lavitas, L.-M., Dostie, J., Pombo, A. and Nicodemi, M. (2012) Complexity of chromatin folding is captured by the strings and binders switch model. Proc. Natl. Acad. Sci. USA, 109, 16173–16178
CrossRef
Google scholar
|
[99] |
Dekker, J., Marti-Renom, M. and Mirny, L. A. (2013) Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat. Rev. Genet., 14, 390–403
CrossRef
Google scholar
|
[100] |
Barbieri, M., Scialdone, A., Piccolo, A., Chiariello, A. M., di Lanno, C., Prisco, A., Pombo, A. and Nicodemi, M. (2013) Polymer models of chromatin organization. Front. Genet., 4, 113
CrossRef
Google scholar
|
[101] |
Zhang, Z., Li, G., Toh, K.-C. and Sung, W.-K. (2013) 3D chromosome modeling with semi-definite programming and Hi-C data. J. Comput. Biol., 20, 831–846
CrossRef
Google scholar
|
[102] |
Varoquaux, N., Ay, F., Noble, W. S. and Vert, J.-P. (2014) A statistical approach for inferring the 3D structure of the genome. Bioinformatics, 30, i26–i33
CrossRef
Google scholar
|
[103] |
Rousseau, M., Fraser, J., Ferraiuolo, M. A., Dostie, J. and Blanchette, M. (2011) Three-dimensional modeling of chromatin structure from interaction frequency data using Markov chain Monte Carlo sampling. BMC Bioinformatics, 12, 414
CrossRef
Google scholar
|
[104] |
Lesne, A., Riposo, J., Roger, P., Cournac, A. and Mozziconacci, J. (2014) 3D genome reconstruction from chromosomal contacts. Nat. Methods, 11, 1141–1143
CrossRef
Google scholar
|
[105] |
Paulsen, J., Gramstad, O. and Collas, P. (2015) Manifold based optimization for single-cell 3D genome reconstruction. PLoS Comput. Biol., 11, e1004396
CrossRef
Google scholar
|
[106] |
Hu, M., Deng, K., Qin, Z., Dixon, J., Selvaraj, S., Fang, J., Ren, B. and Liu, J. S. (2013a) Bayesian inference of spatial organizations of chromosomes. PLoS Comput. Biol., 9, e1002893
CrossRef
Google scholar
|
[107] |
Baù, D., Sanyal, A., Lajoie, B. R., Capriotti, E., Byron, M., Lawrence, J. B., Dekker, J. and Marti-Renom, M. (2011) The three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules. Nat. Struct. Mol. Biol., 18, 107–114
CrossRef
Google scholar
|
[108] |
Wang, S., Xu, J. and Zeng, J. (2015) Inferential modeling of 3D chromatin structure. Nucleic Acids Res., 43, e54
CrossRef
Google scholar
|
[109] |
DeLano, W. L., Ultsch, M. H., De, A. M., Vos,
|
[110] |
Nowotny, J., Wells, A., Xu, L., Cao, R., Trieu, T., He, C., and Cheng, J. (2015). GMOL: An Interactive Tool for 3D Genome Structure Visualization. ArXiv150706383
|
[111] |
Asbury, T. M., Mitman, M., Tang, J. and Zheng, W. J. (2010) Genome3D: A viewer-model framework for integrating and visualizing multi-scale epigenomic information within a three-dimensional genome. BMC Bioinformatics, 11, 444
CrossRef
Google scholar
|
[112] |
Cremer, T. and Cremer, M. (2010) Chromosome territories. Cold Spring Harb. Perspect. Biol., 2, a003889
CrossRef
Google scholar
|
[113] |
Li, G.-W. and Xie, X. S. (2011) Central dogma at the single-molecule level in living cells. Nature, 475, 308–315
CrossRef
Google scholar
|
[114] |
Schmied, J. J., Forthmann, C., Pibiri, E., Lalkens, B., Nickels, P., Liedl, T. and Tinnefeld, P. (2013) DNA origami nanopillars as standards for three-dimensional superresolution microscopy. Nano Lett., 13, 781–785
CrossRef
Google scholar
|
[115] |
Lu, Y., Zhao, J., Zhang, R., Liu, Y., Liu, D., Goldys, E. M., Yang, X., Xi, P., Sunna, A., Lu, J.,
CrossRef
Google scholar
|
[116] |
Sternberg, S. H. and Doudna, J. A. (2015) Expanding the biologist’s toolkit with CRISPR-Cas9. Mol. Cell, 58, 568–574
CrossRef
Google scholar
|
[117] |
Lomvardas, S., Barnea, G., Pisapia, D. J., Mendelsohn, M., Kirkland, J. and Axel, R. (2006) Interchromosomal interactions and olfactory receptor choice. Cell, 126, 403–413
CrossRef
Google scholar
|
[118] |
Chen, B., Gilbert, L. A., Cimini, B. A., Schnitzbauer, J., Zhang, W., Li, G.-W., Park, J., Blackburn, E. H., Weissman, J. S., Qi, L. S.,
CrossRef
Google scholar
|
[119] |
Li, J., Shou, J., Guo, Y., Tang, Y., Wu, Y., Jia, Z., Zhai, Y., Chen, Z., Xu, Q. and Wu, Q. (2015) Efficient inversions and duplications of mammalian regulatory DNA elements and gene clusters by CRISPR/Cas9. J. Mol. Cell Biol., 7, 284–298
CrossRef
Google scholar
|
[120] |
Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D. U., Jung, I., Wu, H., Zhai, Y., Tang, Y.,
CrossRef
Google scholar
|
[121] |
Ma, H., Naseri, A., Reyes-Gutierrez, P., Wolfe, S.A., Zhang, S., and Pederson, T. (2015) Multicolor CRISPR labeling of chromosomal loci in human cells. Proc. Natl. Acad. Sci. USA. 112, 3002–3007
|
[122] |
Ma, H., Tu, L.-C., Naseri, A., Huisman, M., Zhang, S., Grunwald, D., and Pederson, T. (2016) Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow. Nat. Biotechnol. Advance online publication,
CrossRef
Google scholar
|
/
〈 | 〉 |