lncRNA SNHG9 enhances liver cancer stem cell self-renewal and tumorigenicity by negatively regulating PTEN expression via recruiting EZH2

Liver cancer stem cell (CSC) self-renewal and tumorigenesis are important causes of hepatocellular carcinoma (HCC) recurrence. We purposed to investigate the function of long noncoding RNA small nucleolar RNA host gene 9 (SNHG9) in liver CSC self-renewal and tumorigenesis in this study. Flow cytomet...

Full description

Saved in:
Bibliographic Details
Published in:Cell and tissue research 2023-12, Vol.394 (3), p.441-453
Main Authors: Yang, Shouzhang, Ruan, Xiaojiao, Hu, Bingren, Tu, Jinfu, Cai, Huajie
Format: Article
Language:English
Subjects:
Analysis
Biomedical and Life Sciences
Biomedicine
Cell self-renewal
Chromatin
Colonies
Development and progression
Flow cytometry
Hepatocellular carcinoma
Hepatocytes
Human Genetics
Immunoprecipitation
Liver cancer
Molecular Medicine
Nucleoli
Proteomics
PTEN protein
Regular Article
RNA
snoRNA
Spheroids
Stem cells
Tumorigenesis
Tumorigenicity
Citations: Items that this one cites
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by
cites cdi_FETCH-LOGICAL-c401t-b1f404a8d0341555242d6190c759f5548b11f48d6e41e180e68a22c8711d062c3
container_end_page 453
container_issue 3
container_start_page 441
container_title Cell and tissue research
container_volume 394
creator Yang, Shouzhang
Ruan, Xiaojiao
Hu, Bingren
Tu, Jinfu
Cai, Huajie
description Liver cancer stem cell (CSC) self-renewal and tumorigenesis are important causes of hepatocellular carcinoma (HCC) recurrence. We purposed to investigate the function of long noncoding RNA small nucleolar RNA host gene 9 (SNHG9) in liver CSC self-renewal and tumorigenesis in this study. Flow cytometry was carried out to separate CD133 + Populations and CD133 − Populations from HCC cell lines. A combination of CD133 + cells and Matrigel matrix was subcutaneously injected to create the NOD-SCID mouse xenograft tumor model. Colony formation test and spheroids formation assay were carried out to clarify the impact of SNHG9 on the self-renewal of liver CSCs. RNA immunoprecipitation, RNA-pull down, and chromatin immunoprecipitation were performed on CD133 + cells to elucidate the mechanism of SNHG9 regulating PTEN expression. We found that SNHG9 was highly expressed in HCC clinical samples, HCC cells, and CD133 + cells. In vitro, interference with SNHG9 prevented the formation of colonies and spheroids in liver CSC cells and primary HCC cells. In vivo, interference with SNHG9 reduced the tumor volume and weight. SNHG9 could bind to EZH2, and SNHG9 interference suppressed EZH2 recruitment and H3K27me3 levels in the PTEN promoter region. In addition, SNHG9 inhibition promoted PTEN expression while having little impact on EZH2 levels. Interference with SNHG9 inhibited liver CSC self-renewal and tumorigenesis by up-regulating PTEN levels. In conclusion, by binding to EZH2, SNHG9 down-regulated PTEN levels, promoting liver CSC self-renewal and tumor formation, and exacerbating HCC progression.
doi_str_mv 10.1007/s00441-023-03834-x
format article
fullrecord <record><control><sourceid>gale_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_2878710827</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A775574414</galeid><sourcerecordid>A775574414</sourcerecordid><originalsourceid>FETCH-LOGICAL-c401t-b1f404a8d0341555242d6190c759f5548b11f48d6e41e180e68a22c8711d062c3</originalsourceid><addsrcrecordid>eNp9klFrFDEQxxdR8Kz9An0KCOLL1kk2u8k-HuXsCeUUbUH6EnLZ2b2UbPZMduvdR_Bbm-sJtSKShzCZ33-Ymfyz7IzCOQUQ7yMA5zQHVuRQyILnu2fZjPKC5SCFfJ7NoACWi6r69jJ7FeMdAOVVVc-yn86bL6s5-bpaXtYE_UZ7g5E4e4-BmEMQSByxJwadIxFdmwf0-EM7on1Dxqkfgu3QW2PHPVnvicdOj0nt9iRgN7kU-I58vl6sCO62AWO0gyf3Vqe0CZN9SC9ul-x19qLVLuLp7_sku_mwuL5Y5lefLj9ezK9yw4GO-Zq2HLiWDRSclmXJOGsqWoMRZd2WJZdrmgjZVMgpUglYSc2YkYLSBipmipPs3bHuNgzfJ4yj6m08TKc9DlNULC1MUJBMJPTNX-jdMAWfuktULWkp6qp4pDrtUFnfDmPQ5lBUzYUoS5F-hifq_B9UOg321gweW5venwje_iHYoHbjJg5uGtP-4lOQHUEThhgDtmobbK_DXlFQB3eooztUcod6cIfaJVFxFMUE-w7D42j_Uf0CS4y6sg</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2898157963</pqid></control><display><type>article</type><title>lncRNA SNHG9 enhances liver cancer stem cell self-renewal and tumorigenicity by negatively regulating PTEN expression via recruiting EZH2</title><source>Springer Nature</source><creator>Yang, Shouzhang ; Ruan, Xiaojiao ; Hu, Bingren ; Tu, Jinfu ; Cai, Huajie</creator><creatorcontrib>Yang, Shouzhang ; Ruan, Xiaojiao ; Hu, Bingren ; Tu, Jinfu ; Cai, Huajie</creatorcontrib><description>Liver cancer stem cell (CSC) self-renewal and tumorigenesis are important causes of hepatocellular carcinoma (HCC) recurrence. We purposed to investigate the function of long noncoding RNA small nucleolar RNA host gene 9 (SNHG9) in liver CSC self-renewal and tumorigenesis in this study. Flow cytometry was carried out to separate CD133 + Populations and CD133 − Populations from HCC cell lines. A combination of CD133 + cells and Matrigel matrix was subcutaneously injected to create the NOD-SCID mouse xenograft tumor model. Colony formation test and spheroids formation assay were carried out to clarify the impact of SNHG9 on the self-renewal of liver CSCs. RNA immunoprecipitation, RNA-pull down, and chromatin immunoprecipitation were performed on CD133 + cells to elucidate the mechanism of SNHG9 regulating PTEN expression. We found that SNHG9 was highly expressed in HCC clinical samples, HCC cells, and CD133 + cells. In vitro, interference with SNHG9 prevented the formation of colonies and spheroids in liver CSC cells and primary HCC cells. In vivo, interference with SNHG9 reduced the tumor volume and weight. SNHG9 could bind to EZH2, and SNHG9 interference suppressed EZH2 recruitment and H3K27me3 levels in the PTEN promoter region. In addition, SNHG9 inhibition promoted PTEN expression while having little impact on EZH2 levels. Interference with SNHG9 inhibited liver CSC self-renewal and tumorigenesis by up-regulating PTEN levels. In conclusion, by binding to EZH2, SNHG9 down-regulated PTEN levels, promoting liver CSC self-renewal and tumor formation, and exacerbating HCC progression.</description><identifier>ISSN: 0302-766X</identifier><identifier>EISSN: 1432-0878</identifier><identifier>DOI: 10.1007/s00441-023-03834-x</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Analysis ; Biomedical and Life Sciences ; Biomedicine ; Cell self-renewal ; Chromatin ; Colonies ; Development and progression ; Flow cytometry ; Hepatocellular carcinoma ; Hepatocytes ; Human Genetics ; Immunoprecipitation ; Liver cancer ; Molecular Medicine ; Nucleoli ; Proteomics ; PTEN protein ; Regular Article ; RNA ; snoRNA ; Spheroids ; Stem cells ; Tumorigenesis ; Tumorigenicity</subject><ispartof>Cell and tissue research, 2023-12, Vol.394 (3), p.441-453</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>COPYRIGHT 2023 Springer</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c401t-b1f404a8d0341555242d6190c759f5548b11f48d6e41e180e68a22c8711d062c3</cites><orcidid>0000-0003-1815-2064</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids></links><search><creatorcontrib>Yang, Shouzhang</creatorcontrib><creatorcontrib>Ruan, Xiaojiao</creatorcontrib><creatorcontrib>Hu, Bingren</creatorcontrib><creatorcontrib>Tu, Jinfu</creatorcontrib><creatorcontrib>Cai, Huajie</creatorcontrib><title>lncRNA SNHG9 enhances liver cancer stem cell self-renewal and tumorigenicity by negatively regulating PTEN expression via recruiting EZH2</title><title>Cell and tissue research</title><addtitle>Cell Tissue Res</addtitle><description>Liver cancer stem cell (CSC) self-renewal and tumorigenesis are important causes of hepatocellular carcinoma (HCC) recurrence. We purposed to investigate the function of long noncoding RNA small nucleolar RNA host gene 9 (SNHG9) in liver CSC self-renewal and tumorigenesis in this study. Flow cytometry was carried out to separate CD133 + Populations and CD133 − Populations from HCC cell lines. A combination of CD133 + cells and Matrigel matrix was subcutaneously injected to create the NOD-SCID mouse xenograft tumor model. Colony formation test and spheroids formation assay were carried out to clarify the impact of SNHG9 on the self-renewal of liver CSCs. RNA immunoprecipitation, RNA-pull down, and chromatin immunoprecipitation were performed on CD133 + cells to elucidate the mechanism of SNHG9 regulating PTEN expression. We found that SNHG9 was highly expressed in HCC clinical samples, HCC cells, and CD133 + cells. In vitro, interference with SNHG9 prevented the formation of colonies and spheroids in liver CSC cells and primary HCC cells. In vivo, interference with SNHG9 reduced the tumor volume and weight. SNHG9 could bind to EZH2, and SNHG9 interference suppressed EZH2 recruitment and H3K27me3 levels in the PTEN promoter region. In addition, SNHG9 inhibition promoted PTEN expression while having little impact on EZH2 levels. Interference with SNHG9 inhibited liver CSC self-renewal and tumorigenesis by up-regulating PTEN levels. In conclusion, by binding to EZH2, SNHG9 down-regulated PTEN levels, promoting liver CSC self-renewal and tumor formation, and exacerbating HCC progression.</description><subject>Analysis</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cell self-renewal</subject><subject>Chromatin</subject><subject>Colonies</subject><subject>Development and progression</subject><subject>Flow cytometry</subject><subject>Hepatocellular carcinoma</subject><subject>Hepatocytes</subject><subject>Human Genetics</subject><subject>Immunoprecipitation</subject><subject>Liver cancer</subject><subject>Molecular Medicine</subject><subject>Nucleoli</subject><subject>Proteomics</subject><subject>PTEN protein</subject><subject>Regular Article</subject><subject>RNA</subject><subject>snoRNA</subject><subject>Spheroids</subject><subject>Stem cells</subject><subject>Tumorigenesis</subject><subject>Tumorigenicity</subject><issn>0302-766X</issn><issn>1432-0878</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp9klFrFDEQxxdR8Kz9An0KCOLL1kk2u8k-HuXsCeUUbUH6EnLZ2b2UbPZMduvdR_Bbm-sJtSKShzCZ33-Ymfyz7IzCOQUQ7yMA5zQHVuRQyILnu2fZjPKC5SCFfJ7NoACWi6r69jJ7FeMdAOVVVc-yn86bL6s5-bpaXtYE_UZ7g5E4e4-BmEMQSByxJwadIxFdmwf0-EM7on1Dxqkfgu3QW2PHPVnvicdOj0nt9iRgN7kU-I58vl6sCO62AWO0gyf3Vqe0CZN9SC9ul-x19qLVLuLp7_sku_mwuL5Y5lefLj9ezK9yw4GO-Zq2HLiWDRSclmXJOGsqWoMRZd2WJZdrmgjZVMgpUglYSc2YkYLSBipmipPs3bHuNgzfJ4yj6m08TKc9DlNULC1MUJBMJPTNX-jdMAWfuktULWkp6qp4pDrtUFnfDmPQ5lBUzYUoS5F-hifq_B9UOg321gweW5venwje_iHYoHbjJg5uGtP-4lOQHUEThhgDtmobbK_DXlFQB3eooztUcod6cIfaJVFxFMUE-w7D42j_Uf0CS4y6sg</recordid><startdate>20231201</startdate><enddate>20231201</enddate><creator>Yang, Shouzhang</creator><creator>Ruan, Xiaojiao</creator><creator>Hu, Bingren</creator><creator>Tu, Jinfu</creator><creator>Cai, Huajie</creator><general>Springer Berlin Heidelberg</general><general>Springer</general><general>Springer Nature B.V</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7RV</scope><scope>7SS</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-1815-2064</orcidid></search><sort><creationdate>20231201</creationdate><title>lncRNA SNHG9 enhances liver cancer stem cell self-renewal and tumorigenicity by negatively regulating PTEN expression via recruiting EZH2</title><author>Yang, Shouzhang ; Ruan, Xiaojiao ; Hu, Bingren ; Tu, Jinfu ; Cai, Huajie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c401t-b1f404a8d0341555242d6190c759f5548b11f48d6e41e180e68a22c8711d062c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Analysis</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cell self-renewal</topic><topic>Chromatin</topic><topic>Colonies</topic><topic>Development and progression</topic><topic>Flow cytometry</topic><topic>Hepatocellular carcinoma</topic><topic>Hepatocytes</topic><topic>Human Genetics</topic><topic>Immunoprecipitation</topic><topic>Liver cancer</topic><topic>Molecular Medicine</topic><topic>Nucleoli</topic><topic>Proteomics</topic><topic>PTEN protein</topic><topic>Regular Article</topic><topic>RNA</topic><topic>snoRNA</topic><topic>Spheroids</topic><topic>Stem cells</topic><topic>Tumorigenesis</topic><topic>Tumorigenicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Shouzhang</creatorcontrib><creatorcontrib>Ruan, Xiaojiao</creatorcontrib><creatorcontrib>Hu, Bingren</creatorcontrib><creatorcontrib>Tu, Jinfu</creatorcontrib><creatorcontrib>Cai, Huajie</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing &amp; Allied Health Database</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Cell and tissue research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Shouzhang</au><au>Ruan, Xiaojiao</au><au>Hu, Bingren</au><au>Tu, Jinfu</au><au>Cai, Huajie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>lncRNA SNHG9 enhances liver cancer stem cell self-renewal and tumorigenicity by negatively regulating PTEN expression via recruiting EZH2</atitle><jtitle>Cell and tissue research</jtitle><stitle>Cell Tissue Res</stitle><date>2023-12-01</date><risdate>2023</risdate><volume>394</volume><issue>3</issue><spage>441</spage><epage>453</epage><pages>441-453</pages><issn>0302-766X</issn><eissn>1432-0878</eissn><abstract>Liver cancer stem cell (CSC) self-renewal and tumorigenesis are important causes of hepatocellular carcinoma (HCC) recurrence. We purposed to investigate the function of long noncoding RNA small nucleolar RNA host gene 9 (SNHG9) in liver CSC self-renewal and tumorigenesis in this study. Flow cytometry was carried out to separate CD133 + Populations and CD133 − Populations from HCC cell lines. A combination of CD133 + cells and Matrigel matrix was subcutaneously injected to create the NOD-SCID mouse xenograft tumor model. Colony formation test and spheroids formation assay were carried out to clarify the impact of SNHG9 on the self-renewal of liver CSCs. RNA immunoprecipitation, RNA-pull down, and chromatin immunoprecipitation were performed on CD133 + cells to elucidate the mechanism of SNHG9 regulating PTEN expression. We found that SNHG9 was highly expressed in HCC clinical samples, HCC cells, and CD133 + cells. In vitro, interference with SNHG9 prevented the formation of colonies and spheroids in liver CSC cells and primary HCC cells. In vivo, interference with SNHG9 reduced the tumor volume and weight. SNHG9 could bind to EZH2, and SNHG9 interference suppressed EZH2 recruitment and H3K27me3 levels in the PTEN promoter region. In addition, SNHG9 inhibition promoted PTEN expression while having little impact on EZH2 levels. Interference with SNHG9 inhibited liver CSC self-renewal and tumorigenesis by up-regulating PTEN levels. In conclusion, by binding to EZH2, SNHG9 down-regulated PTEN levels, promoting liver CSC self-renewal and tumor formation, and exacerbating HCC progression.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><doi>10.1007/s00441-023-03834-x</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-1815-2064</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 0302-766X
ispartof Cell and tissue research, 2023-12, Vol.394 (3), p.441-453
issn 0302-766X
1432-0878
language eng
recordid cdi_proquest_miscellaneous_2878710827
source Springer Nature
subjects Analysis
Biomedical and Life Sciences
Biomedicine
Cell self-renewal
Chromatin
Colonies
Development and progression
Flow cytometry
Hepatocellular carcinoma
Hepatocytes
Human Genetics
Immunoprecipitation
Liver cancer
Molecular Medicine
Nucleoli
Proteomics
PTEN protein
Regular Article
RNA
snoRNA
Spheroids
Stem cells
Tumorigenesis
Tumorigenicity
title lncRNA SNHG9 enhances liver cancer stem cell self-renewal and tumorigenicity by negatively regulating PTEN expression via recruiting EZH2
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-30T20%3A50%3A10IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=lncRNA%20SNHG9%20enhances%20liver%20cancer%20stem%20cell%20self-renewal%20and%20tumorigenicity%20by%20negatively%20regulating%20PTEN%20expression%20via%20recruiting%20EZH2&rft.jtitle=Cell%20and%20tissue%20research&rft.au=Yang,%20Shouzhang&rft.date=2023-12-01&rft.volume=394&rft.issue=3&rft.spage=441&rft.epage=453&rft.pages=441-453&rft.issn=0302-766X&rft.eissn=1432-0878&rft_id=info:doi/10.1007/s00441-023-03834-x&rft_dat=%3Cgale_proqu%3EA775574414%3C/gale_proqu%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c401t-b1f404a8d0341555242d6190c759f5548b11f48d6e41e180e68a22c8711d062c3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2898157963&rft_id=info:pmid/&rft_galeid=A775574414&rfr_iscdi=true