Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre

Ezgi Hacisuleyman; Loyal A. Goff; Cole Trapnell; Adam Williams; Jorge Henao-Mejia; Lei Sun; Patrick McClanahan; David G. Hendrickson; Martin Sauvageau; David R. Kelley; Michael Morse; Jesse Engreitz; Eric S. Lander; Mitch Guttman; Harvey F. Lodish; Richard Flavell; Arjun Raj; John L. Rinn

doi:10.1038/nsmb.2764

Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre

Ezgi Hacisuleyman, Loyal A. Goff, Cole Trapnell, Adam Williams, Jorge Henao-Mejia, Lei Sun, Patrick McClanahan, David G. Hendrickson, Martin Sauvageau, David R. Kelley, Michael Morse, Jesse Engreitz, Eric S. Lander, Mitch Guttman, Harvey F. Lodish, Richard Flavell, Arjun Raj, John L. Rinn

Research output: Contribution to journal › Article › peer-review

366 Scopus citations

Abstract

RNA, including long noncoding RNA (lncRNA), is known to be an abundant and important structural component of the nuclear matrix. However, the molecular identities, functional roles and localization dynamics of lncRNAs that influence nuclear architecture remain poorly understood. Here, we describe one lncRNA, Firre, that interacts with the nuclear-matrix factor hnRNPU through a 156-bp repeating sequence and localizes across an ∼5-Mb domain on the X chromosome. We further observed Firre localization across five distinct trans-chromosomal loci, which reside in spatial proximity to the Firre genomic locus on the X chromosome. Both genetic deletion of the Firre locus and knockdown of hnRNPU resulted in loss of colocalization of these trans-chromosomal interacting loci. Thus, our data suggest a model in which lncRNAs such as Firre can interface with and modulate nuclear architecture across chromosomes.

Original language	English (US)
Pages (from-to)	198-206
Number of pages	9
Journal	Nature Structural and Molecular Biology
Volume	21
Issue number	2
DOIs	https://doi.org/10.1038/nsmb.2764
State	Published - Feb 2014
Externally published	Yes

ASJC Scopus subject areas

Structural Biology
Molecular Biology

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Hacisuleyman, E., Goff, L. A., Trapnell, C., Williams, A., Henao-Mejia, J., Sun, L., McClanahan, P., Hendrickson, D. G., Sauvageau, M., Kelley, D. R., Morse, M., Engreitz, J., Lander, E. S., Guttman, M., Lodish, H. F., Flavell, R., Raj, A., & Rinn, J. L. (2014). Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre. Nature Structural and Molecular Biology, 21(2), 198-206. https://doi.org/10.1038/nsmb.2764

Hacisuleyman, E, Goff, LA, Trapnell, C, Williams, A, Henao-Mejia, J, Sun, L, McClanahan, P, Hendrickson, DG, Sauvageau, M, Kelley, DR, Morse, M, Engreitz, J, Lander, ES, Guttman, M, Lodish, HF, Flavell, R, Raj, A & Rinn, JL 2014, 'Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre', Nature Structural and Molecular Biology, vol. 21, no. 2, pp. 198-206. https://doi.org/10.1038/nsmb.2764

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title = "Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre",

abstract = "RNA, including long noncoding RNA (lncRNA), is known to be an abundant and important structural component of the nuclear matrix. However, the molecular identities, functional roles and localization dynamics of lncRNAs that influence nuclear architecture remain poorly understood. Here, we describe one lncRNA, Firre, that interacts with the nuclear-matrix factor hnRNPU through a 156-bp repeating sequence and localizes across an ∼5-Mb domain on the X chromosome. We further observed Firre localization across five distinct trans-chromosomal loci, which reside in spatial proximity to the Firre genomic locus on the X chromosome. Both genetic deletion of the Firre locus and knockdown of hnRNPU resulted in loss of colocalization of these trans-chromosomal interacting loci. Thus, our data suggest a model in which lncRNAs such as Firre can interface with and modulate nuclear architecture across chromosomes.",

author = "Ezgi Hacisuleyman and Goff, {Loyal A.} and Cole Trapnell and Adam Williams and Jorge Henao-Mejia and Lei Sun and Patrick McClanahan and Hendrickson, {David G.} and Martin Sauvageau and Kelley, {David R.} and Michael Morse and Jesse Engreitz and Lander, {Eric S.} and Mitch Guttman and Lodish, {Harvey F.} and Richard Flavell and Arjun Raj and Rinn, {John L.}",

note = "Funding Information: We thank Biosearch, especially M. Beal, H. Johansson, A. Orjalo, S. Coassin and R. Cook, for materials, advice and help with FISH experiments. We are grateful to the entire Rinn and Raj laboratories for generous help with experiments, bioinformatics and preparation of the manuscript. This work was supported by US National Institutes of Health grants 1DP2OD00667 (J.L.R.), P01GM099117 (J.L.R.), 1DP20D008514 (A.R.) and P50HG006193-01 (J.L.R.) and by the Howard Hughes Medical Institute (R.F.).",

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AU - Trapnell, Cole

AU - Williams, Adam

AU - Henao-Mejia, Jorge

AU - Sun, Lei

AU - McClanahan, Patrick

AU - Hendrickson, David G.

AU - Sauvageau, Martin

AU - Kelley, David R.

AU - Morse, Michael

AU - Engreitz, Jesse

AU - Lander, Eric S.

AU - Guttman, Mitch

AU - Lodish, Harvey F.

AU - Flavell, Richard

AU - Raj, Arjun

AU - Rinn, John L.

N1 - Funding Information: We thank Biosearch, especially M. Beal, H. Johansson, A. Orjalo, S. Coassin and R. Cook, for materials, advice and help with FISH experiments. We are grateful to the entire Rinn and Raj laboratories for generous help with experiments, bioinformatics and preparation of the manuscript. This work was supported by US National Institutes of Health grants 1DP2OD00667 (J.L.R.), P01GM099117 (J.L.R.), 1DP20D008514 (A.R.) and P50HG006193-01 (J.L.R.) and by the Howard Hughes Medical Institute (R.F.).

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N2 - RNA, including long noncoding RNA (lncRNA), is known to be an abundant and important structural component of the nuclear matrix. However, the molecular identities, functional roles and localization dynamics of lncRNAs that influence nuclear architecture remain poorly understood. Here, we describe one lncRNA, Firre, that interacts with the nuclear-matrix factor hnRNPU through a 156-bp repeating sequence and localizes across an ∼5-Mb domain on the X chromosome. We further observed Firre localization across five distinct trans-chromosomal loci, which reside in spatial proximity to the Firre genomic locus on the X chromosome. Both genetic deletion of the Firre locus and knockdown of hnRNPU resulted in loss of colocalization of these trans-chromosomal interacting loci. Thus, our data suggest a model in which lncRNAs such as Firre can interface with and modulate nuclear architecture across chromosomes.

AB - RNA, including long noncoding RNA (lncRNA), is known to be an abundant and important structural component of the nuclear matrix. However, the molecular identities, functional roles and localization dynamics of lncRNAs that influence nuclear architecture remain poorly understood. Here, we describe one lncRNA, Firre, that interacts with the nuclear-matrix factor hnRNPU through a 156-bp repeating sequence and localizes across an ∼5-Mb domain on the X chromosome. We further observed Firre localization across five distinct trans-chromosomal loci, which reside in spatial proximity to the Firre genomic locus on the X chromosome. Both genetic deletion of the Firre locus and knockdown of hnRNPU resulted in loss of colocalization of these trans-chromosomal interacting loci. Thus, our data suggest a model in which lncRNAs such as Firre can interface with and modulate nuclear architecture across chromosomes.

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Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre

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