MIR100 host gene-encoded lncRNAs regulate cell cycle by modulating the interaction between HuR and its target mRNAs

Qinyu Sun; Vidisha Tripathi; Je Hyun Yoon; Deepak K. Singh; Qinyu Hao; Kyung Won Min; Sylvia Davila; Richard W. Zealy; Xiao Ling Li; Maria Polycarpou-Schwarz; Elin Lehrmann; Yongqing Zhang; Kevin G. Becker; Susan M. Freier; Yuelin Zhu; Sven Diederichs; Supriya G. Prasanth; Ashish Lal; Myriam Gorospe; Kannanganattu V. Prasanth

doi:10.1093/nar/gky696

MIR100 host gene-encoded lncRNAs regulate cell cycle by modulating the interaction between HuR and its target mRNAs

Qinyu Sun, Vidisha Tripathi, Je Hyun Yoon, Deepak K. Singh, Qinyu Hao, Kyung Won Min, Sylvia Davila, Richard W. Zealy, Xiao Ling Li, Maria Polycarpou-Schwarz, Elin Lehrmann, Yongqing Zhang, Kevin G. Becker, Susan M. Freier, Yuelin Zhu, Sven Diederichs, Supriya G. Prasanth, Ashish Lal, Myriam Gorospe, Kannanganattu V. Prasanth

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

59 Scopus citations

Abstract

Long non-coding RNAs (lncRNAs) regulate vital biological processes, including cell proliferation, differentiation and development. A subclass of lncRNAs is synthesized from microRNA (miRNA) host genes (MIRHGs) due to pre-miRNA processing, and are categorized as miRNA-host gene lncRNAs (lnc-miRHGs). Presently, the cellular function of most lnc-miRHGs is not well understood. We demonstrate a miRNA-independent role for a nuclear-enriched lnc-miRHG in cell cycle progression. MIR100HG produces spliced and stable lncRNAs that display elevated levels during the G1 phase of the cell cycle. Depletion of MIR100HG-encoded lncRNAs in human cells results in aberrant cell cycle progression without altering the levels of miRNA encoded within MIR100HG. Notably, MIR100HG interacts with HuR/ELAVL1 as well as with several HuR-target mRNAs. Further, MIR100HG-depleted cells show reduced interaction between HuR and three of its target mRNAs, indicating that MIR100HG facilitates interaction between HuR and target mRNAs. Our studies have unearthed novel roles played by a MIRHG-encoded lncRNA in regulating RNA binding protein activity, thereby underscoring the importance of determining the function of several hundreds of lnc-miRHGs that are present in human genome.

Original language	English (US)
Pages (from-to)	10405-10416
Number of pages	12
Journal	Nucleic acids research
Volume	46
Issue number	19
DOIs	https://doi.org/10.1093/nar/gky696
State	Published - Nov 2 2018
Externally published	Yes

ASJC Scopus subject areas

Genetics

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Sun, Q., Tripathi, V., Yoon, J. H., Singh, D. K., Hao, Q., Min, K. W., Davila, S., Zealy, R. W., Li, X. L., Polycarpou-Schwarz, M., Lehrmann, E., Zhang, Y., Becker, K. G., Freier, S. M., Zhu, Y., Diederichs, S., Prasanth, S. G., Lal, A., Gorospe, M., & Prasanth, K. V. (2018). MIR100 host gene-encoded lncRNAs regulate cell cycle by modulating the interaction between HuR and its target mRNAs. Nucleic acids research, 46(19), 10405-10416. https://doi.org/10.1093/nar/gky696

Sun, Q, Tripathi, V, Yoon, JH, Singh, DK, Hao, Q, Min, KW, Davila, S, Zealy, RW, Li, XL, Polycarpou-Schwarz, M, Lehrmann, E, Zhang, Y, Becker, KG, Freier, SM, Zhu, Y, Diederichs, S, Prasanth, SG, Lal, A, Gorospe, M & Prasanth, KV 2018, 'MIR100 host gene-encoded lncRNAs regulate cell cycle by modulating the interaction between HuR and its target mRNAs', Nucleic acids research, vol. 46, no. 19, pp. 10405-10416. https://doi.org/10.1093/nar/gky696

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title = "MIR100 host gene-encoded lncRNAs regulate cell cycle by modulating the interaction between HuR and its target mRNAs",

abstract = "Long non-coding RNAs (lncRNAs) regulate vital biological processes, including cell proliferation, differentiation and development. A subclass of lncRNAs is synthesized from microRNA (miRNA) host genes (MIRHGs) due to pre-miRNA processing, and are categorized as miRNA-host gene lncRNAs (lnc-miRHGs). Presently, the cellular function of most lnc-miRHGs is not well understood. We demonstrate a miRNA-independent role for a nuclear-enriched lnc-miRHG in cell cycle progression. MIR100HG produces spliced and stable lncRNAs that display elevated levels during the G1 phase of the cell cycle. Depletion of MIR100HG-encoded lncRNAs in human cells results in aberrant cell cycle progression without altering the levels of miRNA encoded within MIR100HG. Notably, MIR100HG interacts with HuR/ELAVL1 as well as with several HuR-target mRNAs. Further, MIR100HG-depleted cells show reduced interaction between HuR and three of its target mRNAs, indicating that MIR100HG facilitates interaction between HuR and target mRNAs. Our studies have unearthed novel roles played by a MIRHG-encoded lncRNA in regulating RNA binding protein activity, thereby underscoring the importance of determining the function of several hundreds of lnc-miRHGs that are present in human genome.",

author = "Qinyu Sun and Vidisha Tripathi and Yoon, {Je Hyun} and Singh, {Deepak K.} and Qinyu Hao and Min, {Kyung Won} and Sylvia Davila and Zealy, {Richard W.} and Li, {Xiao Ling} and Maria Polycarpou-Schwarz and Elin Lehrmann and Yongqing Zhang and Becker, {Kevin G.} and Freier, {Susan M.} and Yuelin Zhu and Sven Diederichs and Prasanth, {Supriya G.} and Ashish Lal and Myriam Gorospe and Prasanth, {Kannanganattu V.}",

note = "Publisher Copyright: {\textcopyright} The Author(s)",

year = "2018",

month = nov,

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doi = "10.1093/nar/gky696",

language = "English (US)",

volume = "46",

pages = "10405--10416",

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T1 - MIR100 host gene-encoded lncRNAs regulate cell cycle by modulating the interaction between HuR and its target mRNAs

AU - Sun, Qinyu

AU - Tripathi, Vidisha

AU - Yoon, Je Hyun

AU - Singh, Deepak K.

AU - Hao, Qinyu

AU - Min, Kyung Won

AU - Davila, Sylvia

AU - Zealy, Richard W.

AU - Li, Xiao Ling

AU - Polycarpou-Schwarz, Maria

AU - Lehrmann, Elin

AU - Zhang, Yongqing

AU - Becker, Kevin G.

AU - Freier, Susan M.

AU - Zhu, Yuelin

AU - Diederichs, Sven

AU - Prasanth, Supriya G.

AU - Lal, Ashish

AU - Gorospe, Myriam

AU - Prasanth, Kannanganattu V.

PY - 2018/11/2

Y1 - 2018/11/2

N2 - Long non-coding RNAs (lncRNAs) regulate vital biological processes, including cell proliferation, differentiation and development. A subclass of lncRNAs is synthesized from microRNA (miRNA) host genes (MIRHGs) due to pre-miRNA processing, and are categorized as miRNA-host gene lncRNAs (lnc-miRHGs). Presently, the cellular function of most lnc-miRHGs is not well understood. We demonstrate a miRNA-independent role for a nuclear-enriched lnc-miRHG in cell cycle progression. MIR100HG produces spliced and stable lncRNAs that display elevated levels during the G1 phase of the cell cycle. Depletion of MIR100HG-encoded lncRNAs in human cells results in aberrant cell cycle progression without altering the levels of miRNA encoded within MIR100HG. Notably, MIR100HG interacts with HuR/ELAVL1 as well as with several HuR-target mRNAs. Further, MIR100HG-depleted cells show reduced interaction between HuR and three of its target mRNAs, indicating that MIR100HG facilitates interaction between HuR and target mRNAs. Our studies have unearthed novel roles played by a MIRHG-encoded lncRNA in regulating RNA binding protein activity, thereby underscoring the importance of determining the function of several hundreds of lnc-miRHGs that are present in human genome.

AB - Long non-coding RNAs (lncRNAs) regulate vital biological processes, including cell proliferation, differentiation and development. A subclass of lncRNAs is synthesized from microRNA (miRNA) host genes (MIRHGs) due to pre-miRNA processing, and are categorized as miRNA-host gene lncRNAs (lnc-miRHGs). Presently, the cellular function of most lnc-miRHGs is not well understood. We demonstrate a miRNA-independent role for a nuclear-enriched lnc-miRHG in cell cycle progression. MIR100HG produces spliced and stable lncRNAs that display elevated levels during the G1 phase of the cell cycle. Depletion of MIR100HG-encoded lncRNAs in human cells results in aberrant cell cycle progression without altering the levels of miRNA encoded within MIR100HG. Notably, MIR100HG interacts with HuR/ELAVL1 as well as with several HuR-target mRNAs. Further, MIR100HG-depleted cells show reduced interaction between HuR and three of its target mRNAs, indicating that MIR100HG facilitates interaction between HuR and target mRNAs. Our studies have unearthed novel roles played by a MIRHG-encoded lncRNA in regulating RNA binding protein activity, thereby underscoring the importance of determining the function of several hundreds of lnc-miRHGs that are present in human genome.

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JO - Nucleic acids research

JF - Nucleic acids research

IS - 19

ER -

MIR100 host gene-encoded lncRNAs regulate cell cycle by modulating the interaction between HuR and its target mRNAs

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