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Comparison of Hi-C results using in-solution versus in-nucleus ligation
Open accessAbstract
BACKGROUND: Chromosome conformation capture and various derivative methods such as 4C, 5C and Hi-C have emerged as standard tools to analyze the three-dimensional organization of the genome in the nucleus. These methods employ ligation of diluted cross-linked chromatin complexes, intended to favor proximity-dependent, intra-complex ligation. During development of single-cell Hi-C, we devised an alternative Hi-C protocol with ligation in preserved nuclei rather than in solution. Here we directly compare Hi-C methods employing in-nucleus ligation with the standard in-solution ligation. RESULTS: We show in-nucleus ligation results in consistently lower levels of inter-chromosomal contacts. Through chromatin mixing experiments we show that a significantly large fraction of inter-chromosomal contacts are the result of spurious ligation events formed during in-solution ligation. In-nucleus ligation significantly reduces this source of experimental noise, and results in improved reproducibility between replicates. We also find that in-nucleus ligation eliminates restriction fragment length bias found with in-solution ligation. These improvements result in greater reproducibility of long-range intra-chromosomal and inter-chromosomal contacts, as well as enhanced detection of structural features such as topologically associated domain boundaries. CONCLUSIONS: We conclude that in-nucleus ligation captures chromatin interactions more consistently over a wider range of distances, and significantly reduces both experimental noise and bias. In-nucleus ligation creates higher quality Hi-C libraries while simplifying the experimental procedure. We suggest that the entire range of 3C applications are likely to show similar benefits from in-nucleus ligation.
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![Fig. 4 Experimental GC content bias. The mouse in-solution (ISL), in-nucleus (INL) and random (RL) ligations are compared for GC content-related bias matrices, calculated using the Hi-C matrix correction [21], employing a 100-kb bin resolution](/paper-figures/9c61dc5c67814f31a784965c1bacc69d/comparison-of-hi-c-results-using-in-solution-versus-in-nucleus-ligation-figure-4.jpg)
![Fig. 5 Experimental fragment length bias. The mouse and human in-solution (ISL), in-nucleus (INL) and TCC ligation datasets are compared for fragment length bias matrices, calculated using the Hi-C matrix correction [21], employing a 100-kb bin resolution. a Mouse foetal liver. b Human ES cells. c GM12878 human lymphoblastoid cells [4]](/paper-figures/50fdc2ed8d3445e08eb107038730c3d2/comparison-of-hi-c-results-using-in-solution-versus-in-nucleus-ligation-figure-5.jpg)
![Fig. 6 Normalized Hi-C matrices with compartments. Normalized matrices for mouse chromosome 9 from the indicated datasets with the first principal component indicated A and B compartments (defined by Lieberman-Aiden et al. [15]), at the top and left of each map. INL in-nucleus ligation, ISL in-solution ligation, RL random ligation](/paper-figures/9e952d1cfc1341abad17831c4ddf54b9/comparison-of-hi-c-results-using-in-solution-versus-in-nucleus-ligation-figure-6.jpg)
![Fig. 7 Reproducibility of the corrected Hi-C matrices. Element-wise comparison of coverage-corrected (a–f) and coverage- and distance-corrected (g–l) Hi-C matrices as indicated. The scatter plots show the log2-corrected counts in one dataset against the corresponding count values in the second dataset, for all cis-chromosomal (blue to green color varying with genomic distance) and trans-chromosomal (red) bin interaction counts. The correction of Imakaev et al. [22] was applied, using a bin resolution of 10 Mb. INL in-nucleus ligation, ISL in-solution ligation, RL random ligation](/paper-figures/f8d4baa101a84cae981bb57f74802baa/comparison-of-hi-c-results-using-in-solution-versus-in-nucleus-ligation-figure-7.jpg)
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Metadata
- Authors
- Nagano, T., Várnai, C., Schoenfelder, S., Javierre, B.-M., Wingett, S. W., & Fraser, P.
- Affiliations
- Babraham Institute (GB)
- Corresponding author
- Nagano, Takashi
- Fraser, Peter
- ORCID
- Venue
- Genome Biology
- Published
- 2015-08-26
- Volume
- 16
- Issue
- 1
- Pages
- 175-175
- ISSN
- 1465-6906 (ISSN-L)
- 1474-760X
- PMC
- PMC4580221
- OpenAlex
- W2116261028
- Cited by
- 166
- References
- 26
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 8 · 2023: 8 · 2022: 11 · 2021: 20 · 2020: 17 · 2019: 23 · 2018: 25 · 2017: 27 · 2016: 12 · 2015: 5
- FWCI
- 9.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Genome biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- European Research Council (111608)
- BBSRC (BBS/E/B/000C0405)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
- Keywords
- Hi-C, chromosome conformation capture, 3D genome organization, topologically associating domains, single-cell Hi-C
- MeSH terms
- Animals, Cell Nucleus, Cells, Cultured, Chromatin, Humans, Mice, Inbred C57BL, Genomics, Mice
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