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The cohesin loader NIPBL interacts with pre-ribosomal RNA and treacle to regulate ribosomal RNA synthesis

Xiangduo Kong, Yen-Yun Chen, View ORCID ProfileJianhuang Lin, Ebony Flowers, Eric Van Nostrand, View ORCID ProfileSteven M. Blue, Jonathan Chau, Christopher I-Hsing Ma, Isaiah Mohr, Ryan Thai, Chengguo Yao, Alexander R. Ball Jr., Richard Chien, Shimako Kawauchi, Rosaysela Santos, Anne L. Calof, Arthur D. Lander, Yongsheng Shi, Mitsuru Okuwaki, Gene W. Yeo, View ORCID ProfileKyoko Yokomori
doi: https://doi.org/10.1101/658492
Xiangduo Kong
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Yen-Yun Chen
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Jianhuang Lin
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
2PhD Program in Human Biology, School of Integrative and Global Majors and Faculty of Medicine, University of Tsukuba, Japan
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Ebony Flowers
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
3California State University Long Beach, CA 90840, USA
8UT Southwestern Medical Center 5323 Harry Hines Blvd, NA8.124 Dallas, TX 75390
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Eric Van Nostrand
4Department of Cellular & Molecular Medicine and Institute for Genomic Medicine, University of California, San Diego, La Jolla, CA 92093, USA
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Steven M. Blue
4Department of Cellular & Molecular Medicine and Institute for Genomic Medicine, University of California, San Diego, La Jolla, CA 92093, USA
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Jonathan Chau
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Christopher I-Hsing Ma
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Isaiah Mohr
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Ryan Thai
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Chengguo Yao
5Department of Microbiology & Molecular Genetics, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Alexander R. Ball Jr.
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Richard Chien
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Shimako Kawauchi
6Department of Anatomy & Neurobiology, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Rosaysela Santos
6Department of Anatomy & Neurobiology, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
9Department of Pathology, Anatomy, and Laboratory Medicine, West Virginia University, School of Medicine, Morgantown, WV 26506-9128
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Anne L. Calof
6Department of Anatomy & Neurobiology, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Arthur D. Lander
7Department of Developmental & Cell Biology, School of Biological Sciences, University of California, Irvine, CA 92697, U.S.A.
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Yongsheng Shi
5Department of Microbiology & Molecular Genetics, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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Mitsuru Okuwaki
2PhD Program in Human Biology, School of Integrative and Global Majors and Faculty of Medicine, University of Tsukuba, Japan
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Gene W. Yeo
4Department of Cellular & Molecular Medicine and Institute for Genomic Medicine, University of California, San Diego, La Jolla, CA 92093, USA
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Kyoko Yokomori
1Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, U.S.A.
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  • ORCID record for Kyoko Yokomori
  • For correspondence: kyokomor@uci.edu
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Abstract

NIPBL is an essential loader of cohesin to mediate sister chromatid cohesion and chromatin loop organization. NIPBL mutations cause Cornelia de Lange Syndrome. How NIPBL’s genomic localization is specified is not fully understood. We found that NIPBL localizes to the nucleolus in an RNA-dependent manner and binds directly to ribosomal RNA (rRNA). We identified two RNA binding domains in NIPBL in vitro, both of which are required for efficient rRNA binding in vivo. NIPBL binds to ribosomal DNA (rDNA) in an RNA-stimulated manner, recruits PAF1 and promotes pre-rRNA transcription. Stress that inhibits rRNA synthesis displaces NIPBL from the nucleolus and rDNA. Interestingly, treacle, mutated in Treacher Collins syndrome, tightly binds to and recruits NIPBL to the nucleolus, nucleolar organizer regions, and the stress-induced nucleolar cap. The results reveal that a subpopulation of NIPBL is recruited to the nucleolus through its interaction with RNA and treacle and regulates pre-rRNA transcription.

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Posted June 04, 2019.
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The cohesin loader NIPBL interacts with pre-ribosomal RNA and treacle to regulate ribosomal RNA synthesis
Xiangduo Kong, Yen-Yun Chen, Jianhuang Lin, Ebony Flowers, Eric Van Nostrand, Steven M. Blue, Jonathan Chau, Christopher I-Hsing Ma, Isaiah Mohr, Ryan Thai, Chengguo Yao, Alexander R. Ball Jr., Richard Chien, Shimako Kawauchi, Rosaysela Santos, Anne L. Calof, Arthur D. Lander, Yongsheng Shi, Mitsuru Okuwaki, Gene W. Yeo, Kyoko Yokomori
bioRxiv 658492; doi: https://doi.org/10.1101/658492
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The cohesin loader NIPBL interacts with pre-ribosomal RNA and treacle to regulate ribosomal RNA synthesis
Xiangduo Kong, Yen-Yun Chen, Jianhuang Lin, Ebony Flowers, Eric Van Nostrand, Steven M. Blue, Jonathan Chau, Christopher I-Hsing Ma, Isaiah Mohr, Ryan Thai, Chengguo Yao, Alexander R. Ball Jr., Richard Chien, Shimako Kawauchi, Rosaysela Santos, Anne L. Calof, Arthur D. Lander, Yongsheng Shi, Mitsuru Okuwaki, Gene W. Yeo, Kyoko Yokomori
bioRxiv 658492; doi: https://doi.org/10.1101/658492

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