Closing the loop: 3C versus DNA FISH

Genome Biology

Volumn 17, Issue 1, 2016, Pages

  Giorgetti, Luca ^a   Heard, Edith ^b,c  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b INSTITUT CURIE   (France)

^c l'alimentation et l'Environnement   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; CHROMATIN;

CHROMOSOME ANALYSIS; CHROMOSOME CONFORMATION CAPTURE; CHROMOSOME STRUCTURE; CONCEPTUAL FRAMEWORK; DNA CROSS LINKING; DNA PROBE; EXPERIMENTAL DESIGN; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC DISTANCE; HUMAN; INTERMETHOD COMPARISON; MEASUREMENT ERROR; NONHUMAN; PROCESS DESIGN; QUANTITATIVE ANALYSIS; REVIEW; STRUCTURE ANALYSIS; SYSTEMATIC ERROR; CHROMATIN; CHROMOSOME; GENETICS; THEORETICAL MODEL;

CHROMATIN; CHROMOSOMES; DNA; IN SITU HYBRIDIZATION, FLUORESCENCE; MODELS, THEORETICAL;

EID: 84992202526     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-016-1081-2     Document Type: Review

References (64)

1. Bouwman BA, de Laat W. Getting the genome in shape: the formation of loops, domains and compartments. Genome Biol. 2015;16:154.
2. Dekker J, Mirny L. The 3D genome as moderator of chromosomal communication. Cell. 2016;164:1110-21.
3. Spitz F. Gene regulation at a distance: from remote enhancers to 3D regulatory ensembles. Semin Cell Dev Biol. 2016;57:57-67.
4. Balázsi G, van Oudenaarden A, Collins JJ. Cellular decision making and biological noise: from microbes to mammals. Cell. 2011;144:910-25.
5. Belmont A. Dynamics of chromatin, proteins, and bodies within the cell nucleus. Curr Opin Cell Biol. 2003;15:304-10.
6. Bridger JM, Volpi EV. Fluorescence in situ hybridization (FISH): protocols and applications. Totowa: Humana Press; 2010. http://link.springer.com/10.1007/978-1-60761-789-1.
7. de Wit E, de Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 2012;26:11-24.
8. Cremer T, Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet. 2001;2:292-301.
9. Fraser J, Williamson I, Bickmore WA, Dostie J. An overview of genome organization and how we got there: from FISH to Hi-C. Microbiol Mol Biol Rev. 2015;79:347-72.
10. Rao SSP, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2015;162:687-8.
11. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature. 2012;485:381-5.
12. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485:376-80.
13. Hou C, Li L, Qin ZS, Corces VG. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol Cell. 2012;48:471-84.
14. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell. 2012;148:458-72.
15. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326:289-93.
16. Gibcus JH, Dekker J. The hierarchy of the 3D genome. Mol Cell. 2013;49:773-82.
17. Chaumeil J, Augui S, Chow JC, Heard E. Combined immunofluorescence, RNA fluorescent in situ hybridization, and DNA fluorescent in situ hybridization to study chromatin changes, transcriptional activity, nuclear organization, and X-chromosome inactivation. In: Hancock R, editor. The nucleus. Totowa: Humana Press; 2008. p. 297-308. http://link.springer.com/10.1007/978-1-59745-406-3_18.
18. Bickmore WA, Carothers AD. Factors affecting the timing and imprinting of replication on a mammalian chromosome. J Cell Sci. 1995;108:2801-9.
19. Garimberti E, Tosi S. Fluorescence in situ hybridization (FISH), basic principles and methodology. In: Bridger JM, Volpi EV, editors. Fluorescence in situ hybridization (FISH). Totowa: Humana Press; 2010. p. 3-20. http://dx.doi.org/10.1007/978-1-60761-789-1_1.
20. Cremer M, Müller S, Köhler D, Brero A, Solovei I. Cell preparation and multicolor FISH in 3D preserved cultured mammalian cells. Cold Spring Harb Protoc. 2007;2007:pdb.prot4723.
21. Sachs RK, van den Engh G, Trask B, Yokota H, Hearst JE. A random-walk/giant-loop model for interphase chromosomes. Proc Natl Acad Sci U S A. 1995;92:2710-4.
22. Davies JOJ, Telenius JM, McGowan SJ, Roberts NA, Taylor S, Higgs DR, et al. Multiplexed analysis of chromosome conformation at vastly improved sensitivity. Nat Methods. 2016;13:74-80.
23. Martin P, McGovern A, Orozco G, Duffus K, Yarwood A, Schoenfelder S, et al. Capture Hi-C reveals novel candidate genes and complex long-range interactions with related autoimmune risk loci. Nat Commun. 2015;6:10069.
24. Belton J-M, McCord RP, Gibcus JH, Naumova N, Zhan Y, Dekker J. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods. 2012;58:268-76.
25. Rosa A, Becker NB, Everaers R. Looping probabilities in model interphase chromosomes. Biophys J. 2010;98:2410-9.
26. Hakim O, Sung M-H, Voss TC, Splinter E, John S, Sabo PJ, et al. Diverse gene reprogramming events occur in the same spatial clusters of distal regulatory elements. Genome Res. 2011;21:697-706.
27. Crane E, Bian Q, McCord RP, Lajoie BR, Wheeler BS, Ralston EJ, et al. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature. 2015;523:240-4.
28. Giorgetti L, Galupa R, Nora EP, Piolot T, Lam F, Dekker J, et al. Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell. 2014;157:950-63.
29. Giorgetti L, Lajoie BR, Carter AC, Attia M, Zhan Y, Xu J, et al. Structural organization of the inactive X chromosome in the mouse. Nature. 2016;535:575-9.
30. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, et al. A three-dimensional model of the yeast genome. Nature. 2010;465:363-7.
31. Baù D, Sanyal A, Lajoie BR, Capriotti E, Byron M, Lawrence JB, et al. The three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules. Nat Struct Mol Biol. 2011;18:107-14.
32. Marbouty M, Le Gall A, Cattoni DI, Cournac A, Koh A, Fiche J-B, et al. Condensin- and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolution imaging. Mol Cell. 2015;59:588-602.
33. Lesne A, Riposo J, Roger P, Cournac A, Mozziconacci J. 3D genome reconstruction from chromosomal contacts. Nat Methods. 2014;11:1141-3.
34. Brackley CA, Brown JM, Waithe D, Babbs C, Davies J, Hughes JR, et al. Predicting the three-dimensional folding of cis-regulatory regions in mammalian genomes using bioinformatic data and polymer models. Genome Biol. 2016;17:59.
35. Lu K, Ye W, Zhou L, Collins LB, Chen X, Gold A, et al. Structural characterization of formaldehyde-induced cross-links between amino acids and deoxynucleosides and their oligomers. J Am Chem Soc. 2010;132:3388-99.
36. Toews J, Rogalski JC, Clark TJ, Kast J. Mass spectrometric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal Chim Acta. 2008;618:168-83.
37. Sutherland BW, Toews J, Kast J. Utility of formaldehyde cross-linking and mass spectrometry in the study of protein-protein interactions. J Mass Spectrom. 2008;43:699-715.
38. Gavrilov A, Razin SV, Cavalli G. In vivo formaldehyde cross-linking: it is time for black box analysis. Brief Funct Genomics. 2015;14:163-5.
39. Belmont AS. Large-scale chromatin organization: the good, the surprising, and the still perplexing. Curr Opin Cell Biol. 2014;26:69-78.
40. Solovei I, Cremer M. 3D-FISH on cultured cells combined with immunostaining. In: Bridger JM, Volpi EV, editors. Fluorescence in situ hybridization (FISH). Totowa: Humana Press; 2010. p. 117-26. http://dx.doi.org/10.1007/978-1-60761-789-1_8.
41. Markaki Y, Smeets D, Cremer M, Schermelleh L. Fluorescence in situ hybridization applications for super-resolution 3D structured illumination microscopy. In: Sousa AA, Kruhlak MJ, editors. Nanoimaging. New York City: Humana Press; 2013. p. 43-64. http://dx.doi.org/10.1007/978-1-62703-137-0_4.
42. Xie SQ, Lavitas L-M, Pombo A. CryoFISH: fluorescence in situ hybridization on ultrathin cryosections. In: Bridger JM, Volpi EV, editors. Fluorescence in situ hybridization (FISH). Totowa: Humana Press; 2010. p. 219-30. http://link.springer.com/10.1007/978-1-60761-789-1_15.
43. Solovei I, Cavallo A, Schermelleh L, Jaunin F, Scasselati C, Cmarko D, et al. Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp Cell Res. 2002;276:10-23.
44. Kim I-H, Nagel J, Otten S, Knerr B, Eils R, Rohr K, et al. Quantitative comparison of DNA detection by GFP-lac repressor tagging, fluorescence in situ hybridization and immunostaining. BMC Biotechnol. 2007;7:92.
45. Deng W, Shi X, Tjian R, Lionnet T, Singer RH. CASFISH: CRISPR/Cas9-mediated in situ labeling of genomic loci in fixed cells. Proc Natl Acad Sci U S A. 2015;112:11870-5.
46. Giorgetti L, Piolot T, Heard E. High-resolution 3D DNA FISH using plasmid probes and computational correction of optical aberrations to study chromatin structure at the sub-megabase scale. In: Nakagawa S, Hirose T, editors. Nuclear bodies and noncoding RNAs. Springer: New York; 2015. p. 37-53. http://dx.doi.org/ 10.1007/978-1-4939-2253-6_3.
47. Sorzano COS, Thevenaz P, Unser M. Elastic registration of biological images using vector-spline regularization. IEEE Trans Biomed Eng. 2005;52:652-63.
48. Wang C-W, Ka S-M, Chen A. Robust image registration of biological microscopic images. Sci Rep. 2014;4:6050.
49. Yaffe E, Tanay A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat Genet. 2011;43:1059-65.
50. Nagano T, Várnai C, Schoenfelder S, Javierre B-M, Wingett SW, Fraser P. Comparison of Hi-C results using in-solution versus in-nucleus ligation. Genome Biol. 2015;16:175.
51. Williamson I, Berlivet S, Eskeland R, Boyle S, Illingworth RS, Paquette D, et al. Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev. 2014;28:2778-91.
52. Splinter E, de Wit E, Nora EP, Klous P, van de Werken HJG, Zhu Y, et al. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev. 2011;25:1371-83.
53. Chaumeil J, Micsinai M, Ntziachristos P, Roth DB, Aifantis I, Kluger Y, et al. The RAG2 C-terminus and ATM protect genome integrity by controlling antigen receptor gene cleavage. Nat Commun. 2013;4:2231.
54. Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat Biotechnol. 2012;30:90-8.
55. Fabre PJ, Benke A, Joye E, Huynh THN, Manley S, Duboule D. Nanoscale spatial organization of the HoxD gene cluster in distinct transcriptional states. Proc Natl Acad Sci U S A. 2015;112:13964-9.
56. Naumova N, Imakaev M, Fudenberg G, Zhan Y, Lajoie BR, Mirny LA, et al. Organization of the mitotic chromosome. Science. 2013;342:948-53.
57. Boettiger AN, Bintu B, Moffitt JR, Wang S, Beliveau BJ, Fudenberg G, et al. Super-resolution imaging reveals distinct chromatin folding for different epigenetic states. Nature. 2016;529:418-22.
58. Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E, Dean W, et al. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature. 2013;502:59-64.
59. Masui O, Bonnet I, Le Baccon P, Brito I, Pollex T, Murphy N, et al. Live-cell chromosome dynamics and outcome of X chromosome pairing events during ES cell differentiation. Cell. 2011;145:447-58.
60. Sternberg SH, Doudna JA. Expanding the biologist's toolkit with CRISPR-Cas9. Mol Cell. 2015;58:568-74.
61. Flemr M, Bühler M. Single-step generation of conditional knockout mouse embryonic stem cells. Cell Rep. 2015;12:709-16.
62. Saad H, Gallardo F, Dalvai M, Tanguy-le-Gac N, Lane D, Bystricky K. DNA dynamics during early double-strand break processing revealed by non-intrusive imaging of living cells. PLoS Genet. 2014;10:e1004187.
63. Chen B, Gilbert LA, Cimini BA, Schnitzbauer J, Zhang W, Li G-W, et al. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell. 2013;155:1479-91.
64. Melnik S, Deng B, Papantonis A, Baboo S, Carr IM, Cook PR. The proteomes of transcription factories containing RNA polymerases I,II or III. Nat Methods. 2011;8:963-8.