LncRNA SNHG1 facilitates colorectal cancer cells metastasis by recruiting HNRNPD protein to stabilize SERPINA3 mRNA

Metastasis continues to negatively impact individuals diagnosed with colorectal cancer (CRC). Research has revealed the important role of long noncoding RNAs (lncRNAs) in CRC metastasis, but the underlying mechanisms remain unclear. Here, we revealed that the lncRNA small nucleolar RNA host gene 1 (...

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Veröffentlicht in:Cancer letters 2024-11, Vol.604, p.217217, Article 217217
Hauptverfasser: Yang, Huan, Gong, Chunli, Wu, Yuyun, Xie, Xia, Chen, Yang, Li, Zhibin, Shi, Qiuyue, Liu, Jiao, Gao, Nannan, He, Bing, Wang, Chao, Liao, Qiushi, Bai, Jianying, Xiao, Yufeng
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container_title Cancer letters
container_volume 604
creator Yang, Huan
Gong, Chunli
Wu, Yuyun
Xie, Xia
Chen, Yang
Li, Zhibin
Shi, Qiuyue
Liu, Jiao
Gao, Nannan
He, Bing
Wang, Chao
Liao, Qiushi
Bai, Jianying
Xiao, Yufeng
description Metastasis continues to negatively impact individuals diagnosed with colorectal cancer (CRC). Research has revealed the important role of long noncoding RNAs (lncRNAs) in CRC metastasis, but the underlying mechanisms remain unclear. Here, we revealed that the lncRNA small nucleolar RNA host gene 1 (SNHG1) is expressed at higher levels in metastatic CRC tissues than in primary CRC tissues, and that high lncRNA SNHG1 expression indicates poor patient outcomes. We found that lncRNA SNHG1 promotes the migration and invasion of tumor cells both in vivo and in vitro. Moreover, lncRNA SNHG1 increases serpin family A member 3 (SERPINA3) mRNA stability by interacting with the heterogeneous nuclear ribonucleoprotein D (HNRNPD) protein, and subsequently upregulates SERPINA3 expression. Moreover, HNRNPD and SERPINA3 reversed the effects of lncRNA SNHG1 knockdown on CRC cell metastasis. In conclusion, we report that the lncRNA SNHG1 recruits HNRNPD, in turn upregulating SERPINA3 expression and ultimately facilitating CRC cell migration and invasion. Targeting the lncRNA SNHG1/HNRNPD/SERPINA3 signaling pathway might be a therapeutic option for preventing CRC metastasis. •Overexpression of lncRNA SNHG1 predicts a poor prognosis in CRC patients and promotes CRC cells metastasis.•LncRNA SNHG1 promotes CRC metastasis via SERPINA3 and upregulates SERPINA3 expression by enhancing its mRNA stability.•LncRNA SNHG1 interacts with HNRNPD protein without affecting HNRNPD expression.•HNRNPD binds to the 3′UTR of SERPINA3 mRNA and enhances SERPINA3 mRNA stability.•LncRNA SNHG1 binds to the 5′UTR of SERPINA3 mRNA and stabilizes SERPINA3 mRNA in a manner dependent on HNRNPD.
doi_str_mv 10.1016/j.canlet.2024.217217
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Research has revealed the important role of long noncoding RNAs (lncRNAs) in CRC metastasis, but the underlying mechanisms remain unclear. Here, we revealed that the lncRNA small nucleolar RNA host gene 1 (SNHG1) is expressed at higher levels in metastatic CRC tissues than in primary CRC tissues, and that high lncRNA SNHG1 expression indicates poor patient outcomes. We found that lncRNA SNHG1 promotes the migration and invasion of tumor cells both in vivo and in vitro. Moreover, lncRNA SNHG1 increases serpin family A member 3 (SERPINA3) mRNA stability by interacting with the heterogeneous nuclear ribonucleoprotein D (HNRNPD) protein, and subsequently upregulates SERPINA3 expression. Moreover, HNRNPD and SERPINA3 reversed the effects of lncRNA SNHG1 knockdown on CRC cell metastasis. In conclusion, we report that the lncRNA SNHG1 recruits HNRNPD, in turn upregulating SERPINA3 expression and ultimately facilitating CRC cell migration and invasion. Targeting the lncRNA SNHG1/HNRNPD/SERPINA3 signaling pathway might be a therapeutic option for preventing CRC metastasis. •Overexpression of lncRNA SNHG1 predicts a poor prognosis in CRC patients and promotes CRC cells metastasis.•LncRNA SNHG1 promotes CRC metastasis via SERPINA3 and upregulates SERPINA3 expression by enhancing its mRNA stability.•LncRNA SNHG1 interacts with HNRNPD protein without affecting HNRNPD expression.•HNRNPD binds to the 3′UTR of SERPINA3 mRNA and enhances SERPINA3 mRNA stability.•LncRNA SNHG1 binds to the 5′UTR of SERPINA3 mRNA and stabilizes SERPINA3 mRNA in a manner dependent on HNRNPD.</description><identifier>ISSN: 0304-3835</identifier><identifier>ISSN: 1872-7980</identifier><identifier>EISSN: 1872-7980</identifier><identifier>DOI: 10.1016/j.canlet.2024.217217</identifier><identifier>PMID: 39233042</identifier><language>eng</language><publisher>Ireland: Elsevier B.V</publisher><subject>Animals ; Cell Line, Tumor ; Cell Movement ; Colorectal Neoplasms - genetics ; Colorectal Neoplasms - metabolism ; Colorectal Neoplasms - pathology ; Female ; Gene Expression Regulation, Neoplastic ; HCT116 Cells ; Humans ; Long noncoding RNA ; Male ; Metastasis ; Mice ; Mice, Inbred BALB C ; Mice, Nude ; Middle Aged ; mRNA stability ; Neoplasm Invasiveness ; Posttranscriptional modification ; RNA Stability ; RNA, Long Noncoding - genetics ; RNA, Long Noncoding - metabolism ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; RNA-Binding protein ; Serpins - genetics ; Serpins - metabolism ; Up-Regulation</subject><ispartof>Cancer letters, 2024-11, Vol.604, p.217217, Article 217217</ispartof><rights>2024</rights><rights>Copyright © 2024. Published by Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c241t-7461484d0b4c16f7ad10aa21f1c33759025cfea78c916065f9e635ce603cc1b33</cites><orcidid>0009-0006-8096-5452</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0304383524006128$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39233042$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Huan</creatorcontrib><creatorcontrib>Gong, Chunli</creatorcontrib><creatorcontrib>Wu, Yuyun</creatorcontrib><creatorcontrib>Xie, Xia</creatorcontrib><creatorcontrib>Chen, Yang</creatorcontrib><creatorcontrib>Li, Zhibin</creatorcontrib><creatorcontrib>Shi, Qiuyue</creatorcontrib><creatorcontrib>Liu, Jiao</creatorcontrib><creatorcontrib>Gao, Nannan</creatorcontrib><creatorcontrib>He, Bing</creatorcontrib><creatorcontrib>Wang, Chao</creatorcontrib><creatorcontrib>Liao, Qiushi</creatorcontrib><creatorcontrib>Bai, Jianying</creatorcontrib><creatorcontrib>Xiao, Yufeng</creatorcontrib><title>LncRNA SNHG1 facilitates colorectal cancer cells metastasis by recruiting HNRNPD protein to stabilize SERPINA3 mRNA</title><title>Cancer letters</title><addtitle>Cancer Lett</addtitle><description>Metastasis continues to negatively impact individuals diagnosed with colorectal cancer (CRC). Research has revealed the important role of long noncoding RNAs (lncRNAs) in CRC metastasis, but the underlying mechanisms remain unclear. Here, we revealed that the lncRNA small nucleolar RNA host gene 1 (SNHG1) is expressed at higher levels in metastatic CRC tissues than in primary CRC tissues, and that high lncRNA SNHG1 expression indicates poor patient outcomes. We found that lncRNA SNHG1 promotes the migration and invasion of tumor cells both in vivo and in vitro. Moreover, lncRNA SNHG1 increases serpin family A member 3 (SERPINA3) mRNA stability by interacting with the heterogeneous nuclear ribonucleoprotein D (HNRNPD) protein, and subsequently upregulates SERPINA3 expression. Moreover, HNRNPD and SERPINA3 reversed the effects of lncRNA SNHG1 knockdown on CRC cell metastasis. In conclusion, we report that the lncRNA SNHG1 recruits HNRNPD, in turn upregulating SERPINA3 expression and ultimately facilitating CRC cell migration and invasion. Targeting the lncRNA SNHG1/HNRNPD/SERPINA3 signaling pathway might be a therapeutic option for preventing CRC metastasis. •Overexpression of lncRNA SNHG1 predicts a poor prognosis in CRC patients and promotes CRC cells metastasis.•LncRNA SNHG1 promotes CRC metastasis via SERPINA3 and upregulates SERPINA3 expression by enhancing its mRNA stability.•LncRNA SNHG1 interacts with HNRNPD protein without affecting HNRNPD expression.•HNRNPD binds to the 3′UTR of SERPINA3 mRNA and enhances SERPINA3 mRNA stability.•LncRNA SNHG1 binds to the 5′UTR of SERPINA3 mRNA and stabilizes SERPINA3 mRNA in a manner dependent on HNRNPD.</description><subject>Animals</subject><subject>Cell Line, Tumor</subject><subject>Cell Movement</subject><subject>Colorectal Neoplasms - genetics</subject><subject>Colorectal Neoplasms - metabolism</subject><subject>Colorectal Neoplasms - pathology</subject><subject>Female</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>HCT116 Cells</subject><subject>Humans</subject><subject>Long noncoding RNA</subject><subject>Male</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Mice, Nude</subject><subject>Middle Aged</subject><subject>mRNA stability</subject><subject>Neoplasm Invasiveness</subject><subject>Posttranscriptional modification</subject><subject>RNA Stability</subject><subject>RNA, Long Noncoding - genetics</subject><subject>RNA, Long Noncoding - metabolism</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA-Binding protein</subject><subject>Serpins - genetics</subject><subject>Serpins - metabolism</subject><subject>Up-Regulation</subject><issn>0304-3835</issn><issn>1872-7980</issn><issn>1872-7980</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1rGzEQhkVpaNw0_6AUHXtZd_SxX5eCSdI4YDbBac5COztbZPYjleRC-usrs2mPhQEd9My8Mw9jHwWsBYjiy2GNdhooriVIvZaiTPWGrURVyqysK3jLVqBAZ6pS-Tl7H8IBAHJd5u_YuaqlSn9yxcJuwn2z4Y_N9lbw3qIbXLSRAsd5mD1htANPQUieIw1D4CNFG1K5wNsXngh_dNFNP_i22TcP1_zZz5HcxOPME9ameb-JP97sH-6ajeJjCvvAzno7BLp8fS_Y07eb71fbbHd_e3e12WUotYhZqQuhK91Bq1EUfWk7AdZK0QtUqsxrkDn2ZMsKa1FAkfc1FSpHKkAhilapC_Z5mZtW-nmkEM3owukIO9F8DEYJgNSqCp1QvaDo5xA89ebZu9H6FyPAnHSbg1l0m5Nus-hObZ9eE47tSN2_pr9-E_B1ASjd-cuRNwEdJZudO7k13ez-n_AHIzWRJg</recordid><startdate>20241101</startdate><enddate>20241101</enddate><creator>Yang, Huan</creator><creator>Gong, Chunli</creator><creator>Wu, Yuyun</creator><creator>Xie, Xia</creator><creator>Chen, Yang</creator><creator>Li, Zhibin</creator><creator>Shi, Qiuyue</creator><creator>Liu, Jiao</creator><creator>Gao, Nannan</creator><creator>He, Bing</creator><creator>Wang, Chao</creator><creator>Liao, Qiushi</creator><creator>Bai, Jianying</creator><creator>Xiao, Yufeng</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0009-0006-8096-5452</orcidid></search><sort><creationdate>20241101</creationdate><title>LncRNA SNHG1 facilitates colorectal cancer cells metastasis by recruiting HNRNPD protein to stabilize SERPINA3 mRNA</title><author>Yang, Huan ; Gong, Chunli ; Wu, Yuyun ; Xie, Xia ; Chen, Yang ; Li, Zhibin ; Shi, Qiuyue ; Liu, Jiao ; Gao, Nannan ; He, Bing ; Wang, Chao ; Liao, Qiushi ; Bai, Jianying ; Xiao, Yufeng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c241t-7461484d0b4c16f7ad10aa21f1c33759025cfea78c916065f9e635ce603cc1b33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Cell Line, Tumor</topic><topic>Cell Movement</topic><topic>Colorectal Neoplasms - genetics</topic><topic>Colorectal Neoplasms - metabolism</topic><topic>Colorectal Neoplasms - pathology</topic><topic>Female</topic><topic>Gene Expression Regulation, Neoplastic</topic><topic>HCT116 Cells</topic><topic>Humans</topic><topic>Long noncoding RNA</topic><topic>Male</topic><topic>Metastasis</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Mice, Nude</topic><topic>Middle Aged</topic><topic>mRNA stability</topic><topic>Neoplasm Invasiveness</topic><topic>Posttranscriptional modification</topic><topic>RNA Stability</topic><topic>RNA, Long Noncoding - genetics</topic><topic>RNA, Long Noncoding - metabolism</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA-Binding protein</topic><topic>Serpins - genetics</topic><topic>Serpins - metabolism</topic><topic>Up-Regulation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Huan</creatorcontrib><creatorcontrib>Gong, Chunli</creatorcontrib><creatorcontrib>Wu, Yuyun</creatorcontrib><creatorcontrib>Xie, Xia</creatorcontrib><creatorcontrib>Chen, Yang</creatorcontrib><creatorcontrib>Li, Zhibin</creatorcontrib><creatorcontrib>Shi, Qiuyue</creatorcontrib><creatorcontrib>Liu, Jiao</creatorcontrib><creatorcontrib>Gao, Nannan</creatorcontrib><creatorcontrib>He, Bing</creatorcontrib><creatorcontrib>Wang, Chao</creatorcontrib><creatorcontrib>Liao, Qiushi</creatorcontrib><creatorcontrib>Bai, Jianying</creatorcontrib><creatorcontrib>Xiao, Yufeng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Cancer letters</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Huan</au><au>Gong, Chunli</au><au>Wu, Yuyun</au><au>Xie, Xia</au><au>Chen, Yang</au><au>Li, Zhibin</au><au>Shi, Qiuyue</au><au>Liu, Jiao</au><au>Gao, Nannan</au><au>He, Bing</au><au>Wang, Chao</au><au>Liao, Qiushi</au><au>Bai, Jianying</au><au>Xiao, Yufeng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>LncRNA SNHG1 facilitates colorectal cancer cells metastasis by recruiting HNRNPD protein to stabilize SERPINA3 mRNA</atitle><jtitle>Cancer letters</jtitle><addtitle>Cancer Lett</addtitle><date>2024-11-01</date><risdate>2024</risdate><volume>604</volume><spage>217217</spage><pages>217217-</pages><artnum>217217</artnum><issn>0304-3835</issn><issn>1872-7980</issn><eissn>1872-7980</eissn><abstract>Metastasis continues to negatively impact individuals diagnosed with colorectal cancer (CRC). Research has revealed the important role of long noncoding RNAs (lncRNAs) in CRC metastasis, but the underlying mechanisms remain unclear. Here, we revealed that the lncRNA small nucleolar RNA host gene 1 (SNHG1) is expressed at higher levels in metastatic CRC tissues than in primary CRC tissues, and that high lncRNA SNHG1 expression indicates poor patient outcomes. We found that lncRNA SNHG1 promotes the migration and invasion of tumor cells both in vivo and in vitro. Moreover, lncRNA SNHG1 increases serpin family A member 3 (SERPINA3) mRNA stability by interacting with the heterogeneous nuclear ribonucleoprotein D (HNRNPD) protein, and subsequently upregulates SERPINA3 expression. Moreover, HNRNPD and SERPINA3 reversed the effects of lncRNA SNHG1 knockdown on CRC cell metastasis. In conclusion, we report that the lncRNA SNHG1 recruits HNRNPD, in turn upregulating SERPINA3 expression and ultimately facilitating CRC cell migration and invasion. Targeting the lncRNA SNHG1/HNRNPD/SERPINA3 signaling pathway might be a therapeutic option for preventing CRC metastasis. •Overexpression of lncRNA SNHG1 predicts a poor prognosis in CRC patients and promotes CRC cells metastasis.•LncRNA SNHG1 promotes CRC metastasis via SERPINA3 and upregulates SERPINA3 expression by enhancing its mRNA stability.•LncRNA SNHG1 interacts with HNRNPD protein without affecting HNRNPD expression.•HNRNPD binds to the 3′UTR of SERPINA3 mRNA and enhances SERPINA3 mRNA stability.•LncRNA SNHG1 binds to the 5′UTR of SERPINA3 mRNA and stabilizes SERPINA3 mRNA in a manner dependent on HNRNPD.</abstract><cop>Ireland</cop><pub>Elsevier B.V</pub><pmid>39233042</pmid><doi>10.1016/j.canlet.2024.217217</doi><orcidid>https://orcid.org/0009-0006-8096-5452</orcidid></addata></record>
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subjects Animals
Cell Line, Tumor
Cell Movement
Colorectal Neoplasms - genetics
Colorectal Neoplasms - metabolism
Colorectal Neoplasms - pathology
Female
Gene Expression Regulation, Neoplastic
HCT116 Cells
Humans
Long noncoding RNA
Male
Metastasis
Mice
Mice, Inbred BALB C
Mice, Nude
Middle Aged
mRNA stability
Neoplasm Invasiveness
Posttranscriptional modification
RNA Stability
RNA, Long Noncoding - genetics
RNA, Long Noncoding - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA-Binding protein
Serpins - genetics
Serpins - metabolism
Up-Regulation
title LncRNA SNHG1 facilitates colorectal cancer cells metastasis by recruiting HNRNPD protein to stabilize SERPINA3 mRNA
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