The S-phase-induced lncRNA SUNO1 promotes cell proliferation by controlling YAP1/Hippo signaling pathway

Qinyu Hao; Xinying Zong; Qinyu Sun; Yo Chuen Lin; You Jin Song; Seyedsasan Hashemikhabir; Rosaline Y.C. Hsu; Mohammad Kamran; Ritu Chaudhary; Vidisha Tripathi; Deepak Kumar Singh; Arindam Chakraborty; Xiao Ling Li; Yoon Jung Kim; Arturo V. Orjalo; Maria Polycarpou-Schwarz; Branden S. Moriarity; Lisa M. Jenkins; Hans E. Johansson; Yuelin J. Zhu; Sven Diederichs; Anindya Bagchi; Tae Hoon Kim; Sarath C. Janga; Ashish Lal; Supriya G. Prasanth; Kannanganattu V. Prasanth

doi:10.7554/eLife.55102

The S-phase-induced lncRNA SUNO1 promotes cell proliferation by controlling YAP1/Hippo signaling pathway

Qinyu Hao, Xinying Zong, Qinyu Sun, Yo Chuen Lin, You Jin Song, Seyedsasan Hashemikhabir, Rosaline Y.C. Hsu, Mohammad Kamran, Ritu Chaudhary, Vidisha Tripathi, Deepak Kumar Singh, Arindam Chakraborty, Xiao Ling Li, Yoon Jung Kim, Arturo V. Orjalo, Maria Polycarpou-Schwarz, Branden S. Moriarity, Lisa M. Jenkins, Hans E. Johansson, Yuelin J. ZhuSven Diederichs, Anindya Bagchi, Tae Hoon Kim, Sarath C. Janga, Ashish Lal, Supriya G. Prasanth, Kannanganattu V. Prasanth

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

18 Scopus citations

Abstract

Cell cycle is a cellular process that is subject to stringent control. In contrast to the wealth of knowledge of proteins controlling the cell cycle, very little is known about the molecular role of lncRNAs (long noncoding RNAs) in cell-cycle progression. By performing genome-wide transcriptome analyses in cell-cycle-synchronized cells, we observed cell-cycle phase-specific induction of >2000 lncRNAs. Further, we demonstrate that an S-phase-upregulated lncRNA, SUNO1, facilitates cell-cycle progression by promoting YAP1-mediated gene expression. SUNO1 facilitates the cell-cycle-specific transcription of WTIP, a positive regulator of YAP1, by promoting the co-activator, DDX5-mediated stabilization of RNA polymerase II on chromatin. Finally, elevated SUNO1 levels are associated with poor cancer prognosis and tumorigenicity, implying its pro-survival role. Thus, we demonstrate the role of a S-phase up-regulated lncRNA in cell-cycle progression via modulating the expression of genes controlling cell proliferation.

Original language	English (US)
Article number	e55102
Pages (from-to)	1-33
Number of pages	33
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.55102
State	Published - Oct 2020
Externally published	Yes

ASJC Scopus subject areas

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

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.7554/eLife.55102

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Hao, Q., Zong, X., Sun, Q., Lin, Y. C., Song, Y. J., Hashemikhabir, S., Hsu, R. Y. C., Kamran, M., Chaudhary, R., Tripathi, V., Singh, D. K., Chakraborty, A., Li, X. L., Kim, Y. J., Orjalo, A. V., Polycarpou-Schwarz, M., Moriarity, B. S., Jenkins, L. M., Johansson, H. E., ... Prasanth, K. V. (2020). The S-phase-induced lncRNA SUNO1 promotes cell proliferation by controlling YAP1/Hippo signaling pathway. eLife, 9, 1-33. Article e55102. https://doi.org/10.7554/eLife.55102

Hao, Q, Zong, X, Sun, Q, Lin, YC, Song, YJ, Hashemikhabir, S, Hsu, RYC, Kamran, M, Chaudhary, R, Tripathi, V, Singh, DK, Chakraborty, A, Li, XL, Kim, YJ, Orjalo, AV, Polycarpou-Schwarz, M, Moriarity, BS, Jenkins, LM, Johansson, HE, Zhu, YJ, Diederichs, S, Bagchi, A, Kim, TH, Janga, SC, Lal, A, Prasanth, SG & Prasanth, KV 2020, 'The S-phase-induced lncRNA SUNO1 promotes cell proliferation by controlling YAP1/Hippo signaling pathway', eLife, vol. 9, e55102, pp. 1-33. https://doi.org/10.7554/eLife.55102

@article{47cd4b7330f34b0494c1c9c5c7b5b653,

title = "The S-phase-induced lncRNA SUNO1 promotes cell proliferation by controlling YAP1/Hippo signaling pathway",

abstract = "Cell cycle is a cellular process that is subject to stringent control. In contrast to the wealth of knowledge of proteins controlling the cell cycle, very little is known about the molecular role of lncRNAs (long noncoding RNAs) in cell-cycle progression. By performing genome-wide transcriptome analyses in cell-cycle-synchronized cells, we observed cell-cycle phase-specific induction of >2000 lncRNAs. Further, we demonstrate that an S-phase-upregulated lncRNA, SUNO1, facilitates cell-cycle progression by promoting YAP1-mediated gene expression. SUNO1 facilitates the cell-cycle-specific transcription of WTIP, a positive regulator of YAP1, by promoting the co-activator, DDX5-mediated stabilization of RNA polymerase II on chromatin. Finally, elevated SUNO1 levels are associated with poor cancer prognosis and tumorigenicity, implying its pro-survival role. Thus, we demonstrate the role of a S-phase up-regulated lncRNA in cell-cycle progression via modulating the expression of genes controlling cell proliferation.",

author = "Qinyu Hao and Xinying Zong and Qinyu Sun and Lin, {Yo Chuen} and Song, {You Jin} and Seyedsasan Hashemikhabir and Hsu, {Rosaline Y.C.} and Mohammad Kamran and Ritu Chaudhary and Vidisha Tripathi and Singh, {Deepak Kumar} and Arindam Chakraborty and Li, {Xiao Ling} and Kim, {Yoon Jung} and Orjalo, {Arturo V.} and Maria Polycarpou-Schwarz and Moriarity, {Branden S.} and Jenkins, {Lisa M.} and Johansson, {Hans E.} and Zhu, {Yuelin J.} and Sven Diederichs and Anindya Bagchi and Kim, {Tae Hoon} and Janga, {Sarath C.} and Ashish Lal and Prasanth, {Supriya G.} and Prasanth, {Kannanganattu V.}",

year = "2020",

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doi = "10.7554/eLife.55102",

language = "English (US)",

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AU - Hao, Qinyu

AU - Zong, Xinying

AU - Sun, Qinyu

AU - Lin, Yo Chuen

AU - Song, You Jin

AU - Hashemikhabir, Seyedsasan

AU - Hsu, Rosaline Y.C.

AU - Kamran, Mohammad

AU - Chaudhary, Ritu

AU - Tripathi, Vidisha

AU - Singh, Deepak Kumar

AU - Chakraborty, Arindam

AU - Li, Xiao Ling

AU - Kim, Yoon Jung

AU - Orjalo, Arturo V.

AU - Polycarpou-Schwarz, Maria

AU - Moriarity, Branden S.

AU - Jenkins, Lisa M.

AU - Johansson, Hans E.

AU - Zhu, Yuelin J.

AU - Diederichs, Sven

AU - Bagchi, Anindya

AU - Kim, Tae Hoon

AU - Janga, Sarath C.

AU - Lal, Ashish

AU - Prasanth, Supriya G.

AU - Prasanth, Kannanganattu V.

PY - 2020/10

Y1 - 2020/10

N2 - Cell cycle is a cellular process that is subject to stringent control. In contrast to the wealth of knowledge of proteins controlling the cell cycle, very little is known about the molecular role of lncRNAs (long noncoding RNAs) in cell-cycle progression. By performing genome-wide transcriptome analyses in cell-cycle-synchronized cells, we observed cell-cycle phase-specific induction of >2000 lncRNAs. Further, we demonstrate that an S-phase-upregulated lncRNA, SUNO1, facilitates cell-cycle progression by promoting YAP1-mediated gene expression. SUNO1 facilitates the cell-cycle-specific transcription of WTIP, a positive regulator of YAP1, by promoting the co-activator, DDX5-mediated stabilization of RNA polymerase II on chromatin. Finally, elevated SUNO1 levels are associated with poor cancer prognosis and tumorigenicity, implying its pro-survival role. Thus, we demonstrate the role of a S-phase up-regulated lncRNA in cell-cycle progression via modulating the expression of genes controlling cell proliferation.

AB - Cell cycle is a cellular process that is subject to stringent control. In contrast to the wealth of knowledge of proteins controlling the cell cycle, very little is known about the molecular role of lncRNAs (long noncoding RNAs) in cell-cycle progression. By performing genome-wide transcriptome analyses in cell-cycle-synchronized cells, we observed cell-cycle phase-specific induction of >2000 lncRNAs. Further, we demonstrate that an S-phase-upregulated lncRNA, SUNO1, facilitates cell-cycle progression by promoting YAP1-mediated gene expression. SUNO1 facilitates the cell-cycle-specific transcription of WTIP, a positive regulator of YAP1, by promoting the co-activator, DDX5-mediated stabilization of RNA polymerase II on chromatin. Finally, elevated SUNO1 levels are associated with poor cancer prognosis and tumorigenicity, implying its pro-survival role. Thus, we demonstrate the role of a S-phase up-regulated lncRNA in cell-cycle progression via modulating the expression of genes controlling cell proliferation.

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The S-phase-induced lncRNA SUNO1 promotes cell proliferation by controlling YAP1/Hippo signaling pathway

Abstract

ASJC Scopus subject areas

UN SDGs

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