Monoallelically expressed noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression

Qinyu Hao; Minxue Liu; Swapna Vidhur Daulatabad; Saba Gaffari; You Jin Song; Rajneesh Srivastava; Shivang Bhaskar; Anurupa Moitra; Hazel Mangan; Elizabeth Tseng; Rachel B Gilmore; Susan M Frier; Xin Chen; Chengliang Wang; Sui Huang; Stormy Chamberlain; Hong Jin; Jonas Korlach; Brian McStay; Saurabh Sinha; Sarath Chandra Janga; Supriya G Prasanth; Kannanganattu V Prasanth

doi:10.7554/eLife.80684

Monoallelically expressed noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression

Qinyu Hao, Minxue Liu, Swapna Vidhur Daulatabad, Saba Gaffari, You Jin Song, Rajneesh Srivastava, Shivang Bhaskar, Anurupa Moitra, Hazel Mangan, Elizabeth Tseng, Rachel B Gilmore, Susan M Frier, Xin Chen, Chengliang Wang, Sui Huang, Stormy Chamberlain, Hong Jin, Jonas Korlach, Brian McStay, Saurabh SinhaSarath Chandra Janga, Supriya G Prasanth, Kannanganattu V Prasanth

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

Abstract

Out of the several hundred copies of rRNA genes arranged in the nucleolar organizing regions (NOR) of the five human acrocentric chromosomes, ~50% remain transcriptionally inactive. NOR-associated sequences and epigenetic modifications contribute to the differential expression of rRNAs. However, the mechanism(s) controlling the dosage of active versus inactive rRNA genes within each NOR in mammals is yet to be determined. We have discovered a family of ncRNAs, SNULs (Single NUcleolus Localized RNA), which form constrained sub-nucleolar territories on individual NORs and influence rRNA expression. Individual members of the SNULs monoallelically associate with specific NOR-containing chromosomes. SNULs share sequence similarity to pre-rRNA and localize in the sub-nucleolar compartment with pre-rRNA. Finally, SNULs control rRNA expression by influencing pre-rRNA sorting to the DFC compartment and pre-rRNA processing. Our study discovered a novel class of ncRNAs influencing rRNA expression by forming constrained nucleolar territories on individual NORs.

Original language	English (US)
Article number	e80684
Journal	eLife
Volume	13
DOIs	https://doi.org/10.7554/eLife.80684
State	Published - Feb 8 2024

Keywords

cell lines
chromosomes
gene expression
human
noncoding RNA
nucleolus

ASJC Scopus subject areas

General Neuroscience
General Biochemistry, Genetics and Molecular Biology
General Immunology and Microbiology

Online availability

10.7554/eLife.80684License: CC BY

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Hao, Q., Liu, M., Daulatabad, S. V., Gaffari, S., Song, Y. J., Srivastava, R., Bhaskar, S., Moitra, A., Mangan, H., Tseng, E., Gilmore, R. B., Frier, S. M., Chen, X., Wang, C., Huang, S., Chamberlain, S., Jin, H., Korlach, J., McStay, B., ... Prasanth, K. V. (2024). Monoallelically expressed noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression. eLife, 13, Article e80684. https://doi.org/10.7554/eLife.80684

Hao, Q, Liu, M, Daulatabad, SV, Gaffari, S, Song, YJ, Srivastava, R, Bhaskar, S, Moitra, A, Mangan, H, Tseng, E, Gilmore, RB, Frier, SM, Chen, X, Wang, C, Huang, S, Chamberlain, S, Jin, H, Korlach, J, McStay, B, Sinha, S, Janga, SC, Prasanth, SG & Prasanth, KV 2024, 'Monoallelically expressed noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression', eLife, vol. 13, e80684. https://doi.org/10.7554/eLife.80684

@article{e85655f142f84c92b8381e72e7432e4c,

title = "Monoallelically expressed noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression",

abstract = "Out of the several hundred copies of rRNA genes arranged in the nucleolar organizing regions (NOR) of the five human acrocentric chromosomes, ~50% remain transcriptionally inactive. NOR-associated sequences and epigenetic modifications contribute to the differential expression of rRNAs. However, the mechanism(s) controlling the dosage of active versus inactive rRNA genes within each NOR in mammals is yet to be determined. We have discovered a family of ncRNAs, SNULs (Single NUcleolus Localized RNA), which form constrained sub-nucleolar territories on individual NORs and influence rRNA expression. Individual members of the SNULs monoallelically associate with specific NOR-containing chromosomes. SNULs share sequence similarity to pre-rRNA and localize in the sub-nucleolar compartment with pre-rRNA. Finally, SNULs control rRNA expression by influencing pre-rRNA sorting to the DFC compartment and pre-rRNA processing. Our study discovered a novel class of ncRNAs influencing rRNA expression by forming constrained nucleolar territories on individual NORs.",

keywords = "cell lines, chromosomes, gene expression, human, noncoding RNA, nucleolus",

author = "Qinyu Hao and Minxue Liu and Daulatabad, {Swapna Vidhur} and Saba Gaffari and Song, {You Jin} and Rajneesh Srivastava and Shivang Bhaskar and Anurupa Moitra and Hazel Mangan and Elizabeth Tseng and Gilmore, {Rachel B} and Frier, {Susan M} and Xin Chen and Chengliang Wang and Sui Huang and Stormy Chamberlain and Hong Jin and Jonas Korlach and Brian McStay and Saurabh Sinha and Janga, {Sarath Chandra} and Prasanth, {Supriya G} and Prasanth, {Kannanganattu V}",

note = "This work was supported by National Institute of Health R21-AG065748 & R01-GM132458 to KVP, GM125196 to SGP, R35GM131819 to SS, R21AG065748 and R01GM123314 to SCJ, Cancer center at Illinois seed grants and Prairie Dragon Paddlers to KVP, National Science Foundation (NSF) to KVP [1723008 {EAGER}] & 2243257 {NSF center for quantitative cell biology}, SGP [1243372, 1818286, 2225264] and SCJ [1940422 &1908992]. HJ acknowledges support from the NIH (R01-GM120552). SMF is an employee of Ionis Inc, and ET and JK work for PACBIO and receive salary from the respective companies.",

year = "2024",

month = feb,

day = "8",

doi = "10.7554/eLife.80684",

language = "English (US)",

volume = "13",

journal = "eLife",

issn = "2050-084X",

publisher = "eLife Sciences Publications",

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TY - JOUR

T1 - Monoallelically expressed noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression

AU - Hao, Qinyu

AU - Liu, Minxue

AU - Daulatabad, Swapna Vidhur

AU - Gaffari, Saba

AU - Song, You Jin

AU - Srivastava, Rajneesh

AU - Bhaskar, Shivang

AU - Moitra, Anurupa

AU - Mangan, Hazel

AU - Tseng, Elizabeth

AU - Gilmore, Rachel B

AU - Frier, Susan M

AU - Chen, Xin

AU - Wang, Chengliang

AU - Huang, Sui

AU - Chamberlain, Stormy

AU - Jin, Hong

AU - Korlach, Jonas

AU - McStay, Brian

AU - Sinha, Saurabh

AU - Janga, Sarath Chandra

AU - Prasanth, Supriya G

AU - Prasanth, Kannanganattu V

N1 - This work was supported by National Institute of Health R21-AG065748 & R01-GM132458 to KVP, GM125196 to SGP, R35GM131819 to SS, R21AG065748 and R01GM123314 to SCJ, Cancer center at Illinois seed grants and Prairie Dragon Paddlers to KVP, National Science Foundation (NSF) to KVP [1723008 {EAGER}] & 2243257 {NSF center for quantitative cell biology}, SGP [1243372, 1818286, 2225264] and SCJ [1940422 &1908992]. HJ acknowledges support from the NIH (R01-GM120552). SMF is an employee of Ionis Inc, and ET and JK work for PACBIO and receive salary from the respective companies.

PY - 2024/2/8

Y1 - 2024/2/8

N2 - Out of the several hundred copies of rRNA genes arranged in the nucleolar organizing regions (NOR) of the five human acrocentric chromosomes, ~50% remain transcriptionally inactive. NOR-associated sequences and epigenetic modifications contribute to the differential expression of rRNAs. However, the mechanism(s) controlling the dosage of active versus inactive rRNA genes within each NOR in mammals is yet to be determined. We have discovered a family of ncRNAs, SNULs (Single NUcleolus Localized RNA), which form constrained sub-nucleolar territories on individual NORs and influence rRNA expression. Individual members of the SNULs monoallelically associate with specific NOR-containing chromosomes. SNULs share sequence similarity to pre-rRNA and localize in the sub-nucleolar compartment with pre-rRNA. Finally, SNULs control rRNA expression by influencing pre-rRNA sorting to the DFC compartment and pre-rRNA processing. Our study discovered a novel class of ncRNAs influencing rRNA expression by forming constrained nucleolar territories on individual NORs.

AB - Out of the several hundred copies of rRNA genes arranged in the nucleolar organizing regions (NOR) of the five human acrocentric chromosomes, ~50% remain transcriptionally inactive. NOR-associated sequences and epigenetic modifications contribute to the differential expression of rRNAs. However, the mechanism(s) controlling the dosage of active versus inactive rRNA genes within each NOR in mammals is yet to be determined. We have discovered a family of ncRNAs, SNULs (Single NUcleolus Localized RNA), which form constrained sub-nucleolar territories on individual NORs and influence rRNA expression. Individual members of the SNULs monoallelically associate with specific NOR-containing chromosomes. SNULs share sequence similarity to pre-rRNA and localize in the sub-nucleolar compartment with pre-rRNA. Finally, SNULs control rRNA expression by influencing pre-rRNA sorting to the DFC compartment and pre-rRNA processing. Our study discovered a novel class of ncRNAs influencing rRNA expression by forming constrained nucleolar territories on individual NORs.

KW - cell lines

KW - chromosomes

KW - gene expression

KW - human

KW - noncoding RNA

KW - nucleolus

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U2 - 10.7554/eLife.80684

DO - 10.7554/eLife.80684

M3 - Article

C2 - 38240312

SN - 2050-084X

VL - 13

JO - eLife

JF - eLife

M1 - e80684

ER -

Monoallelically expressed noncoding RNAs form nucleolar territories on NOR-containing chromosomes and regulate rRNA expression

Abstract

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