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AGO1 in association with NEAT1 lncRNA contributes to nuclear and 3D chromatin architecture in human cells

Muhammad Shuaib, Krishna Mohan Parsi, Hideya Kawaji, Manjula Thimma, Sabir Abdu Adroub, Alexandre Fort, Yanal Ghosheh, Tomohiro Yamazaki, Taro Mannen, Loqmane Seridi, Bodor Fallatah, Waad Albawardi, Timothy Ravasi, Piero Carninci, Tetsuro Hirose, Valerio Orlando
doi: https://doi.org/10.1101/525527
Muhammad Shuaib
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Krishna Mohan Parsi
2IRCSS Fondazione Santa Lucia, Epigenetics and Genome Reprogramming, Rome, Italy.
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Hideya Kawaji
3RIKEN Center for Life Science Technologies, Division of Genomic Technologies, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan.
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Manjula Thimma
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Sabir Abdu Adroub
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Alexandre Fort
3RIKEN Center for Life Science Technologies, Division of Genomic Technologies, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan.
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Yanal Ghosheh
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Tomohiro Yamazaki
4Institute for Genetic Medicine, Hokkaido University, Sapporo 060-0815, Japan
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Taro Mannen
4Institute for Genetic Medicine, Hokkaido University, Sapporo 060-0815, Japan
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Loqmane Seridi
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Bodor Fallatah
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Waad Albawardi
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Timothy Ravasi
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
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Piero Carninci
3RIKEN Center for Life Science Technologies, Division of Genomic Technologies, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa 230-0045, Japan.
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Tetsuro Hirose
4Institute for Genetic Medicine, Hokkaido University, Sapporo 060-0815, Japan
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Valerio Orlando
1King Abdullah University of Science and Technology (KAUST), BESE Division, KAUST Environmental Epigenetics Program, Thuwal, 23955-6900, Saudi Arabia
2IRCSS Fondazione Santa Lucia, Epigenetics and Genome Reprogramming, Rome, Italy.
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  • For correspondence: valerio.orlando@kaust.edu.sa
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Abstract

Aside from their roles in the cytoplasm, RNA-interference components have been reported to localize also in the nucleus of human cells. In particular, AGO1 associates with active chromatin and appears to influence global gene expression. However, the mechanistic aspects remain elusive. Here, we identify AGO1 as a paraspeckle component that in combination with the NEAT1 lncRNA maintains 3D genome architecture. We demonstrate that AGO1 interacts with NEAT1 lncRNA and its depletion affects NEAT1 expression and the formation of paraspeckles. By Hi-C analysis in AGO1 knockdown cells, we observed global changes in chromatin organization, including TADs configuration, and A/B compartment mixing. Consistently, distinct groups of genes located within the differential interacting loci showed altered expression upon AGO1 depletion. NEAT1 knockout cells displayed similar changes in TADs and higher-order A/B compartmentalization. We propose that AGO1 in association with NEAT1 lncRNA can act as a scaffold that bridges chromatin and nuclear bodies to regulate genome organization and gene expression in human cells.

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Posted January 20, 2019.
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AGO1 in association with NEAT1 lncRNA contributes to nuclear and 3D chromatin architecture in human cells
Muhammad Shuaib, Krishna Mohan Parsi, Hideya Kawaji, Manjula Thimma, Sabir Abdu Adroub, Alexandre Fort, Yanal Ghosheh, Tomohiro Yamazaki, Taro Mannen, Loqmane Seridi, Bodor Fallatah, Waad Albawardi, Timothy Ravasi, Piero Carninci, Tetsuro Hirose, Valerio Orlando
bioRxiv 525527; doi: https://doi.org/10.1101/525527
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AGO1 in association with NEAT1 lncRNA contributes to nuclear and 3D chromatin architecture in human cells
Muhammad Shuaib, Krishna Mohan Parsi, Hideya Kawaji, Manjula Thimma, Sabir Abdu Adroub, Alexandre Fort, Yanal Ghosheh, Tomohiro Yamazaki, Taro Mannen, Loqmane Seridi, Bodor Fallatah, Waad Albawardi, Timothy Ravasi, Piero Carninci, Tetsuro Hirose, Valerio Orlando
bioRxiv 525527; doi: https://doi.org/10.1101/525527

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