染色体间转录中心塑造了非洲锥虫的3D基因组结构-动脉网

Inter-chromosomal transcription hubs shape the 3D genome architecture of African trypanosomes

Nature 等信源发布 2024-12-23 02:05

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AbstractThe eukaryotic nucleus exhibits a highly organized 3D genome architecture, with RNA transcription and processing confined to specific nuclear structures. While intra-chromosomal interactions, such as promoter-enhancer dynamics, are well-studied, the role of inter-chromosomal interactions remains poorly understood.

摘要真核细胞核表现出高度组织化的3D基因组结构，RNA转录和加工仅限于特定的核结构。虽然染色体内相互作用（例如启动子-增强子动力学）得到了很好的研究，但染色体间相互作用的作用仍然知之甚少。

Investigating these interactions in mammalian cells is challenging due to large genome sizes and the need for deep sequencing. Additionally, transcription-dependent 3D topologies in mixed cell populations further complicate analyses. To address these challenges, we used high-resolution DNA-DNA contact mapping (Micro-C) in Trypanosoma brucei, a parasite with continuous RNA polymerase II (RNAPII) transcription and polycistronic transcription units (PTUs).

由于基因组大小较大且需要深度测序，因此研究哺乳动物细胞中的这些相互作用具有挑战性。此外，混合细胞群中依赖转录的3D拓扑结构进一步使分析复杂化。为了应对这些挑战，我们在布氏锥虫（一种具有连续RNA聚合酶II（RNAPII）转录和多顺反子转录单位（PTU）的寄生虫）中使用了高分辨率DNA-DNA接触作图（Micro-C）。

With approximately 300 transcription start sites (TSSs), this genome organization simplifies data interpretation. To minimize scaffolding artifacts, we also generated a highly contiguous phased genome assembly using ultra-long sequencing reads. Our Micro-C analysis revealed an intricate 3D genome organization.

该基因组组织具有大约300个转录起始位点（TSS），简化了数据解释。为了最大程度地减少支架伪影，我们还使用超长测序读数生成了高度连续的相控基因组组装。我们的Micro-C分析揭示了一个复杂的3D基因组组织。

While the T. brucei genome displays features resembling chromosome territories, its chromosomes are arranged around polymerase-specific transcription hubs. RNAPI-transcribed genes cluster, as expected from their localization to the nucleolus. However, we also found that RNAPII TSSs form distinct inter-chromosomal transcription hubs with other RNAPII TSSs.

虽然布鲁氏菌基因组显示出类似于染色体区域的特征，但其染色体排列在聚合酶特异性转录中心周围。RNAPI转录的基因簇，正如从它们定位到核仁所预期的那样。然而，我们还发现RNAPII TSS与其他RNAPII TSS形成不同的染色体间转录中心。

These findings highlight the evolutionary significance of inter-chromosomal transcription hubs and provide new insights into genome organization in T. brucei..

这些发现突出了染色体间转录中心的进化意义，并为布鲁氏菌的基因组组织提供了新的见解。。

IntroductionTo fit inside the nucleus of a cell, the long polymers of DNA that contain a cell’s genetic information must be tightly packaged1. Research over the past few decades has shown that DNA is not randomly packaged and that the 3D genome organization inside the nucleus regulates vital cellular processes, including gene expression and DNA repair2,3,4.

引言为了适合细胞核内，含有细胞遗传信息的DNA长聚合物必须紧密包装1。。

Chromosome conformation capture (3C)-based techniques, which measure the frequency of DNA-DNA contacts between any two DNA loci, have revealed a large number of distinct structures, collectively referred to as ‘contact domains’. Although it has long been recognized that contact domains vary in size and function, the terminology used to describe different contact domains has changed over time.

基于染色体构象捕获（3C）的技术测量了任何两个DNA基因座之间DNA-DNA接触的频率，揭示了大量不同的结构，统称为“接触域”。尽管人们早已认识到接触域的大小和功能各不相同，但用于描述不同接触域的术语随着时间的推移而发生了变化。

To reduce ambiguity, in our study we follow the definitions proposed by Beagan and Phillips-Cremins5. Here, ‘chromatin domains’ are defined as any triangle of enhanced contact frequency tiling the diagonal of a DNA-DNA contact matrix.At the largest scale, eukaryotic DNA is typically organized into active and inactive regions that segregate into A and B compartments6.

为了减少歧义，在我们的研究中，我们遵循Beagan和Phillips-Cremins5提出的定义。在这里，“染色质结构域”被定义为增强接触频率的任何三角形，平铺DNA-DNA接触基质的对角线。在最大规模上，真核DNA通常被组织成活性和非活性区域，分离成a和B区室6。

‘Compartment domains’ are thus defined as chromatin domains whose boundaries coincide with inflection points in the A/B compartmentalization signals, and compartment boundaries are identified by computing the eigenvectors of the interaction matrices7,8.At the intermediate scale, genomes can be organized into ‘topologically associating domains’ (TADs).

因此，“区室结构域”被定义为染色质结构域，其边界与A/B区室化信号中的拐点重合，并且通过计算相互作用矩阵的特征向量来识别区室边界7,8。在中间尺度上，基因组可以被组织成“拓扑关联域”（TAD）。

Beagan and Phillips-Cremins define TADs as contact domains whose formation is driven by cohesin-mediated loop extrusion5,9,10. These domains are flanked by CCCTC-binding factor (CTCF), a protein that restricts the movement of cohesin and thereby defines the boundaries of TADs11,12,13. TAD boundaries can be identified b.

Beagan和Phillips-Cremins将TAD定义为接触域，其形成由粘着蛋白介导的环挤出驱动5,9,10。这些结构域的两侧是CCCTC结合因子（CTCF），这是一种限制粘着蛋白运动的蛋白质，从而定义了TADs11,12,13的边界。TAD边界可以识别b。

Trypanosoma brucei cell culture and growthIn this study, two cell lines were used: T. brucei wildtype (WT) Lister 427 bloodstream form; and a double-selection T. brucei cell lines derived from the Lister 427 bloodstream-form MITat 1.2 isolate92. Both cell lines were grown in HMI-11 medium at 37 °C and 5% CO2.

布氏锥虫细胞培养和生长在这项研究中，使用了两种细胞系：布氏锥虫野生型（WT）Lister 427血流形式；。两种细胞系均在37℃和5%CO 2的HMI-11培养基中生长。

In the latter cell line, a neomycin resistance gene in bloodstream-form expression site (BES) 17 and a puromycin resistance gene in BES 1 allowed the selection for a homogenous cell population that expressed either VSG-2 from BES 1 or VSG-13 from BES 17. This cell line was grown in HMI-11 supplemented with either 20 μg/mL neomycin (also referred to as N50 cells) or 1 μg/mL puromycin (referred to as P10 cells).gDNA extraction for ONT sequencingFor nanopore sequencing, six sequencing libraries were obtained from P10 cells or T.

在后一种细胞系中，血流中的新霉素抗性基因形成表达位点（BES）17和BES 1中的嘌呤霉素抗性基因允许选择表达来自BES 1的VSG-2或来自BES 17的VSG-13的同质细胞群。该细胞系在补充有20g/mL新霉素（也称为N50细胞）或1的HMI-11中生长 μg/mL嘌呤霉素（称为P10细胞）。gDNA提取用于ONT测序对于纳米孔测序，从P10细胞或T获得六个测序文库。

brucei wildtype Lister 427 cells. For each library, gDNA extraction was performed using High Molecular Weight DNA Extraction Kit from Cells and Blood (NEB #T3050). The samples were sequenced using a GridION X5 or PromethION 24 platform on a FLO-PRO114M flowcell using MINKNOW software. Sequencing reports and details of each sequencing libraries are shown in Supplementary Table 1.Closing gaps and expanding repeats in the assemblyFirst, an assembly error in BES 2 of the previously fully phased version 10 of the T.

布鲁氏菌野生型Lister 427细胞。对于每个文库，使用来自细胞和血液的高分子量DNA提取试剂盒（NEB#T3050）进行gDNA提取。使用MINKNOW软件在FLO-PRO114M流通池上使用GridION X5或PromethION 24平台对样品进行测序。测序报告和每个测序文库的详细信息显示在补充表1中。在assemblyFirst中关闭缺口和扩展重复序列，这是先前完全分阶段的T版本10的BES 2中的组装错误。

brucei Lister 427 strain genome assembly51 was corrected and the contigs names were shortened to generate the version 11 of the assembly (Tb427v11). In order to close gaps and expand collapsed repeats in the Tb427v11 assembly, SAMBA93 was run with the ONT reads generated in this study (Supplementary Table 1) and the ONT reads from Girasol et al.94.

校正了布鲁氏菌Lister 427菌株基因组装配51，并缩短了重叠群名称以生成装配的版本11（Tb427v11）。为了缩小差距并扩大Tb427v11组件中折叠的重复序列，使用本研究中产生的ONT读数（补充表1）和Girasol等人94的ONT读数运行了SAMBA93。

It was confirmed that small contigs are not oriented the wrong way around, an error commo.

已经证实，小重叠群并没有方向错误，这是一个常见的错误。

Data availability

数据可用性

High-throughput sequencing Micro-C data and ultra-long ONT reads generated in this study have been deposited in the European Nucleotide Archive under primary accession number PRJEB76933 [https://www.ebi.ac.uk/ena/browser/view/PRJEB76933]. The resulting genome assembly is available at https://zenodo.org/doi/10.5281/zenodo.12683395.

本研究中产生的高通量测序Micro-C数据和超长ONT读数已保存在欧洲核苷酸档案馆，主要登录号为PRJEB76933[https://www.ebi.ac.uk/ena/browser/view/PRJEB76933]。由此产生的基因组组装可在https://zenodo.org/doi/10.5281/zenodo.12683395.

Previously published ChIP-seq and Hi-C data that were used in this study are publicly available at the European Nucleotide Archive or through GEO Series under accession numbers GSE98061 [https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE98061] (H2A.Z MNase-ChIP-seq55), GSE100896 [http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE100896] (SCC1 ChIP-seq48, samples GSM3357444 and GSM3357445), GSE150253 [https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE150253] (RNAPII ChIP-seq66, samples GSM5381488 and GSM5381492), PRJEB35632 [https://www.ebi.ac.uk/ena/data/view/PRJEB35632] and GSE100896 [http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE100896] (Hi-C datasets30,48, merged in this study)..

本研究中使用的先前发布的ChIP-seq和Hi-C数据可在欧洲核苷酸档案馆或通过GEO系列公开获得，登录号为GSE98061[https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE98061]（H2A.Z MNase-ChIP-seq55），GSE100896[http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE100896]（SCC1 ChIP-seq48，样品GSM3357444和GSM3357445），GSE150253[https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE150253]（RNAPII ChIP-seq66，样品GSM5381488和GSM5381492），PRJEB35632[https://www.ebi.ac.uk/ena/data/view/PRJEB35632]和GSE100896[http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE100896]（Hi-C数据集30,48，合并在本研究中）。。

Code availability

代码可用性

The code for the generation and quality control of the genome assembly has been deposited at Zenodo https://zenodo.org/doi/10.5281/zenodo.12683395. The code for the analysis of Micro-C and Hi-C data is available at https://zenodo.org/doi/10.5281/zenodo.12683439.

基因组组装的生成和质量控制代码已保存在Zenodohttps://zenodo.org/doi/10.5281/zenodo.12683395.Micro-C和Hi-C数据分析代码可在https://zenodo.org/doi/10.5281/zenodo.12683439.

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Oudelaar, I. Solovei and all members of the Siegel, Allshire, Ladurner, Meissner and Boshart laboratories for valuable discussions, T. Straub (Bioinformatics Core Facility, BMC) for providing server space, the Core Unit LAFUGA at the Gene Center Munich for next-generation sequencing and A. Thomae and S.

Oudelaar，I。Solovei和Siegel，Allshire，Ladurner，Meissner和Boshart实验室的所有成员进行了有价值的讨论，T.Straub（生物信息学核心设施，BMC）提供了服务器空间，慕尼黑基因中心的核心单元LAFUGA用于下一代测序，以及A.Thomae和S。

Dietzel (Bioimaging Core Facility, BMC) for providing microscopes. This work was funded by the German Research Foundation (SI 1610 / 2-2 and 213249687—SFB 1064 to T.N.S.), an ERC Starting Grant (3D_Tryps 715466) and an ERC Consolidator Grant (SwitchDecoding 101044320) awarded to T.N.S. P.Y. was supported by an MSCA ITN Cell2Cell (86067) fellowship.

Dietzel（生物成像核心设施，BMC）提供显微镜。这项工作由德国研究基金会（SI 1610/2-2和213249687-SFB 1064授予T.N.S.）资助，ERC启动补助金（3D\U Tryps 715466）和ERC整合者补助金（SwitchDecoding 101044320）授予T.N.S.P.Y。并得到了MSCA ITN Cell2Cell（86067）奖学金的支持。

The Medical Research Council (UK) supported this research through funding to R.C.A. and K.R.M. (MR/T04702X/1), along with Wellcome Trust funding to R.C.A. (106144 and 225237) and K.R.M. (221717) and to the Discovery Research Platform for Hidden Cell Biology (226791, Bioinformatics core).FundingOpen Access funding enabled and organized by Projekt DEAL.Author informationAuthors and AffiliationsDivision of Experimental Parasitology, Faculty of Veterinary Medicine, Ludwig-Maximilians-Universität München, 82152, Planegg-Martinsried, GermanyClaudia Rabuffo, Markus R.

医学研究委员会（英国）通过资助R.C.A.和K.R.M.（MR/T04702X/1），以及惠康信托基金资助R.C.A.（106144和225237）和K.R.M.（221717）以及发现隐藏细胞生物学研究平台（226791，生物信息学核心）来支持这项研究。资金开放获取资金由Projekt交易启用和组织。作者信息作者和附属机构慕尼黑路德维希·马克西米利安大学兽医学院实验寄生虫学系，82152，Planegg Martinsried，GermanyClaudia Rabuffo，Markus R。

Schmidt, Prateek Yadav, Anna Barcons-Simon, Raúl O. Cosentino & T. Nicolai SiegelBiomedical Center Munich, Division of Physiological Chemistry, Ludwig-Maximilians-Universität München, 82152, Planegg-Martinsried, GermanyClaudia Rabuffo, Markus R. Schmidt, Prateek Yadav, Ann.

施密特（Schmidt），普拉提克·亚达夫（Prateek Yadav），安娜·巴康斯·西蒙（Anna Barcons Simon），劳尔·科森蒂诺（RaúO.Cosentino＆T）。慕尼黑路德维希·马克西米利安大学生理化学系Nicolai SiegelBiomedical Center慕尼黑，82152，Planegg Martinsried，GermanyClaudia Rabuffo，Markus R.Schmidt，Pratek Yadav，Ann。

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PubMed Google ScholarContributionsThe experiments were designed by C.R. and T.N.S. and carried out by C.R. unless otherwise indicated. Genomic DNA extraction for ONT sequencing was carried out by A.B.S., R.C. and S.K. Assembly of the new genome reference and quality controls were performed by M.R.S.

PubMed谷歌学术贡献除非另有说明，否则实验由C.R.和T.N.S.设计并由C.R.进行。用于ONT测序的基因组DNA提取由A.B.S.，R.C.和S.K.进行。新基因组参考的组装和质量控制由M.R.S.进行。

with the contribution of R.O.C. Annotation of the new reference genome was performed by M.R.S. and P.T. under the supervision of R.C.A. and K.R.M. Micro-C data were analyzed by C.R. and M.R.S. ChIP-seq data analysis was performed by C.R. and P.T. FISH experiments were performed and analyzed by P.Y. The work was supervised by T.N.S.

在R.O.C.的贡献下，新参考基因组的注释由M.R.S.和P.T.在R.C.A.和K.R.M.的监督下进行。Micro-C数据由C.R.和M.R.S.ChIP-seq数据分析由C.R.和P.T.进行。FISH实验由P.Y.进行和分析。工作由T.N.S.监督。

The manuscript was written by C.R. and T.N.S. and edited by all co-authors. All authors contributed to the data interpretation and development of a model. Figures were generated by M.R.S. and C.R.Corresponding authorCorrespondence to.

手稿由C.R.和T.N.S.撰写，并由所有合著者编辑。。数字由M.R.S.和C.R.相应的作者产生。

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Nature Communications thanks Peter Myler, and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. A peer review file is available.

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Reprints and permissionsAbout this articleCite this articleRabuffo, C., Schmidt, M.R., Yadav, P. et al. Inter-chromosomal transcription hubs shape the 3D genome architecture of African trypanosomes.

转载和许可本文引用本文Rabuffo，C.，Schmidt，M.R.，Yadav，P。等人。染色体间转录中心塑造了非洲锥虫的3D基因组结构。

Nat Commun 15, 10716 (2024). https://doi.org/10.1038/s41467-024-55285-9Download citationReceived: 10 July 2024Accepted: 06 December 2024Published: 23 December 2024DOI: https://doi.org/10.1038/s41467-024-55285-9Share this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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