Upregulation of miR-96 enhances cellular proliferation of prostate cancer cells through FOXO1
Aberrant expression of miR-96 in prostate cancer has previously been reported. However, the role and mechanism of action of miR-96 in prostate cancer has not been determined. In this study, the diagnostic and prognostic properties of miR-96 expression levels were investigated by qRT-PCR in two well...
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| description | Aberrant expression of miR-96 in prostate cancer has previously been reported. However, the role and mechanism of action of miR-96 in prostate cancer has not been determined. In this study, the diagnostic and prognostic properties of miR-96 expression levels were investigated by qRT-PCR in two well documented prostate cancer cohorts. The miR-96 expression was found to be significantly higher in prostate cancer patients and correlate with WHO grade, and decreased overall survival time; patients with low levels of miR-96 lived 1.5 years longer than patients with high miR-96 levels. The therapeutic potential was further investigated in vitro, showing that ectopic levels of miR-96 enhances growth and cellular proliferation in prostate cancer cells, implying that miR-96 has oncogenic properties in this setting. We demonstrate that miR-96 expression decreases the transcript and protein levels of FOXO1 by binding to one of two predicted binding sites in the FOXO1 3'UTR sequence. Blocking this binding site completely inhibited the growth enhancement conveyed by miR-96. This finding was corroborated in a large external prostate cancer patient cohort where miR-96 expression inversely correlated to FOXO1 expression. Taken together these findings indicate that miR-96 plays a key role in prostate cancer cellular proliferation and can enhance prostate cancer progression. This knowledge might be utilized for the development of novel therapeutic tools for prostate cancer. |
| doi_str_mv | 10.1371/journal.pone.0072400 |
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However, the role and mechanism of action of miR-96 in prostate cancer has not been determined. In this study, the diagnostic and prognostic properties of miR-96 expression levels were investigated by qRT-PCR in two well documented prostate cancer cohorts. The miR-96 expression was found to be significantly higher in prostate cancer patients and correlate with WHO grade, and decreased overall survival time; patients with low levels of miR-96 lived 1.5 years longer than patients with high miR-96 levels. The therapeutic potential was further investigated in vitro, showing that ectopic levels of miR-96 enhances growth and cellular proliferation in prostate cancer cells, implying that miR-96 has oncogenic properties in this setting. We demonstrate that miR-96 expression decreases the transcript and protein levels of FOXO1 by binding to one of two predicted binding sites in the FOXO1 3'UTR sequence. Blocking this binding site completely inhibited the growth enhancement conveyed by miR-96. This finding was corroborated in a large external prostate cancer patient cohort where miR-96 expression inversely correlated to FOXO1 expression. Taken together these findings indicate that miR-96 plays a key role in prostate cancer cellular proliferation and can enhance prostate cancer progression. This knowledge might be utilized for the development of novel therapeutic tools for prostate cancer.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0072400</identifier><identifier>PMID: 23951320</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>3' Untranslated Regions ; Aberration ; Androgens ; Base Pairing ; Base Sequence ; Basic Medicine ; Binding sites ; Cancer ; Cancer and Oncology ; Cancer cells ; Cancer och onkologi ; Cell growth ; Cell Line, Tumor ; Cell Proliferation ; Clinical Medicine ; Cohort Studies ; Diagnostic systems ; Ethics ; Forkhead Box Protein O1 ; Forkhead Transcription Factors - chemistry ; Forkhead Transcription Factors - genetics ; Forkhead Transcription Factors - metabolism ; FOXO1 protein ; Gene Expression Regulation, Neoplastic ; Health aspects ; Humans ; Kinases ; Klinisk medicin ; Läkemedelskemi ; Male ; Medical and Health Sciences ; Medicin och hälsovetenskap ; Medicinal Chemistry ; Medicinska och farmaceutiska grundvetenskaper ; MicroRNAs - chemistry ; MicroRNAs - genetics ; MicroRNAs - metabolism ; Patients ; Prostate cancer ; Prostatic Neoplasms - genetics ; Prostatic Neoplasms - metabolism ; Prostatic Neoplasms - mortality ; Prostatic Neoplasms - pathology ; Protein binding ; RNA Interference ; Transcription ; Urologi och njurmedicin ; Urology and Nephrology</subject><ispartof>PloS one, 2013-08, Vol.8 (8), p.e72400-e72400</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Haflidadóttir et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Haflidadóttir et al 2013 Haflidadóttir et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c827t-df1526d40fc2e90389efc220d3dd39743bd4a51f636ae0e7d129e25f6b89986b3</citedby><cites>FETCH-LOGICAL-c827t-df1526d40fc2e90389efc220d3dd39743bd4a51f636ae0e7d129e25f6b89986b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3741168/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3741168/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,550,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23951320$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://lup.lub.lu.se/record/4005580$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><contributor>Ling, Ming Tat</contributor><creatorcontrib>Haflidadóttir, Benedikta S</creatorcontrib><creatorcontrib>Larne, Olivia</creatorcontrib><creatorcontrib>Martin, Myriam</creatorcontrib><creatorcontrib>Persson, Margareta</creatorcontrib><creatorcontrib>Edsjö, Anders</creatorcontrib><creatorcontrib>Bjartell, Anders</creatorcontrib><creatorcontrib>Ceder, Yvonne</creatorcontrib><title>Upregulation of miR-96 enhances cellular proliferation of prostate cancer cells through FOXO1</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Aberrant expression of miR-96 in prostate cancer has previously been reported. However, the role and mechanism of action of miR-96 in prostate cancer has not been determined. In this study, the diagnostic and prognostic properties of miR-96 expression levels were investigated by qRT-PCR in two well documented prostate cancer cohorts. The miR-96 expression was found to be significantly higher in prostate cancer patients and correlate with WHO grade, and decreased overall survival time; patients with low levels of miR-96 lived 1.5 years longer than patients with high miR-96 levels. The therapeutic potential was further investigated in vitro, showing that ectopic levels of miR-96 enhances growth and cellular proliferation in prostate cancer cells, implying that miR-96 has oncogenic properties in this setting. We demonstrate that miR-96 expression decreases the transcript and protein levels of FOXO1 by binding to one of two predicted binding sites in the FOXO1 3'UTR sequence. Blocking this binding site completely inhibited the growth enhancement conveyed by miR-96. This finding was corroborated in a large external prostate cancer patient cohort where miR-96 expression inversely correlated to FOXO1 expression. Taken together these findings indicate that miR-96 plays a key role in prostate cancer cellular proliferation and can enhance prostate cancer progression. This knowledge might be utilized for the development of novel therapeutic tools for prostate cancer.</description><subject>3' Untranslated Regions</subject><subject>Aberration</subject><subject>Androgens</subject><subject>Base Pairing</subject><subject>Base Sequence</subject><subject>Basic Medicine</subject><subject>Binding sites</subject><subject>Cancer</subject><subject>Cancer and Oncology</subject><subject>Cancer cells</subject><subject>Cancer och onkologi</subject><subject>Cell growth</subject><subject>Cell Line, Tumor</subject><subject>Cell Proliferation</subject><subject>Clinical Medicine</subject><subject>Cohort Studies</subject><subject>Diagnostic systems</subject><subject>Ethics</subject><subject>Forkhead Box Protein O1</subject><subject>Forkhead Transcription Factors - chemistry</subject><subject>Forkhead Transcription Factors - genetics</subject><subject>Forkhead Transcription Factors - metabolism</subject><subject>FOXO1 protein</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Kinases</subject><subject>Klinisk medicin</subject><subject>Läkemedelskemi</subject><subject>Male</subject><subject>Medical and Health Sciences</subject><subject>Medicin och hälsovetenskap</subject><subject>Medicinal Chemistry</subject><subject>Medicinska och farmaceutiska grundvetenskaper</subject><subject>MicroRNAs - chemistry</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>Patients</subject><subject>Prostate cancer</subject><subject>Prostatic Neoplasms - genetics</subject><subject>Prostatic Neoplasms - metabolism</subject><subject>Prostatic Neoplasms - mortality</subject><subject>Prostatic Neoplasms - pathology</subject><subject>Protein binding</subject><subject>RNA Interference</subject><subject>Transcription</subject><subject>Urologi och njurmedicin</subject><subject>Urology and Nephrology</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>D8T</sourceid><sourceid>DOA</sourceid><recordid>eNqNk12L1DAUhoso7rr6D0QLgujFjPlom-ZGWBZXBwYGVle8kZAmJ50umaYmrR__3nSnO0xlL6SEhpPnvGnfc06SPMdoiSnD727c4Ftpl51rYYkQIxlCD5JTzClZFATRh0f7k-RJCDcI5bQsisfJCaE8x5Sg0-T7deehHqzsG9emzqS75mrBixTarWwVhFSBtfHYp513tjHgD2QMhF72kKqR9LdkSPutd0O9TS833zb4afLISBvg2fQ-S64vP3y5-LRYbz6uLs7XC1US1i-0wTkpdIaMIsARLTnEHUGaak05y2ilM5ljU9BCAgKmMeFAclNUJedlUdGz5OVet7MuiMmZIHBGUUYQYzwSqz2hnbwRnW920v8RTjbiNuB8LaTvG2VBoByxqKwUKVmmK1ZpRpRSGFVMZYzrqLXea4Vf0A3VTM0OXVxVXCKAkBUYpJERpCy1yGLZRBn_S4CUTOacK4PLKPd--vih2oFW0PZe2pnq_KRttqJ2PwVlGcbFKPBmEvDuxwChF7smjNWQLbhhtIEUCDNekIi--ge936yJqmX0o2mNi_eqUVScZ6ykGPESR2p5DxUfDbtGxa40TYzPEt7OEiLTw---lkMIYvX56v_Zzdc5-_qI3YK0_TY4O4yNGuZgtgdVbN3gwRxMxkiMQ3XnhhiHSkxDFdNeHBfokHQ3RfQvtdwbpg</recordid><startdate>20130812</startdate><enddate>20130812</enddate><creator>Haflidadóttir, Benedikta S</creator><creator>Larne, Olivia</creator><creator>Martin, Myriam</creator><creator>Persson, Margareta</creator><creator>Edsjö, Anders</creator><creator>Bjartell, Anders</creator><creator>Ceder, Yvonne</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AGCHP</scope><scope>AOWAS</scope><scope>D8T</scope><scope>D95</scope><scope>ZZAVC</scope><scope>DOA</scope></search><sort><creationdate>20130812</creationdate><title>Upregulation of miR-96 enhances cellular proliferation of prostate cancer cells through FOXO1</title><author>Haflidadóttir, Benedikta S ; Larne, Olivia ; Martin, Myriam ; Persson, Margareta ; Edsjö, Anders ; Bjartell, Anders ; Ceder, Yvonne</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c827t-df1526d40fc2e90389efc220d3dd39743bd4a51f636ae0e7d129e25f6b89986b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>3' Untranslated Regions</topic><topic>Aberration</topic><topic>Androgens</topic><topic>Base Pairing</topic><topic>Base Sequence</topic><topic>Basic Medicine</topic><topic>Binding sites</topic><topic>Cancer</topic><topic>Cancer and Oncology</topic><topic>Cancer cells</topic><topic>Cancer och onkologi</topic><topic>Cell growth</topic><topic>Cell Line, Tumor</topic><topic>Cell Proliferation</topic><topic>Clinical Medicine</topic><topic>Cohort Studies</topic><topic>Diagnostic systems</topic><topic>Ethics</topic><topic>Forkhead Box Protein O1</topic><topic>Forkhead Transcription Factors - 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However, the role and mechanism of action of miR-96 in prostate cancer has not been determined. In this study, the diagnostic and prognostic properties of miR-96 expression levels were investigated by qRT-PCR in two well documented prostate cancer cohorts. The miR-96 expression was found to be significantly higher in prostate cancer patients and correlate with WHO grade, and decreased overall survival time; patients with low levels of miR-96 lived 1.5 years longer than patients with high miR-96 levels. The therapeutic potential was further investigated in vitro, showing that ectopic levels of miR-96 enhances growth and cellular proliferation in prostate cancer cells, implying that miR-96 has oncogenic properties in this setting. We demonstrate that miR-96 expression decreases the transcript and protein levels of FOXO1 by binding to one of two predicted binding sites in the FOXO1 3'UTR sequence. Blocking this binding site completely inhibited the growth enhancement conveyed by miR-96. This finding was corroborated in a large external prostate cancer patient cohort where miR-96 expression inversely correlated to FOXO1 expression. Taken together these findings indicate that miR-96 plays a key role in prostate cancer cellular proliferation and can enhance prostate cancer progression. This knowledge might be utilized for the development of novel therapeutic tools for prostate cancer.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23951320</pmid><doi>10.1371/journal.pone.0072400</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-08, Vol.8 (8), p.e72400-e72400 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1430420779 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; SWEPUB Freely available online; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | 3' Untranslated Regions Aberration Androgens Base Pairing Base Sequence Basic Medicine Binding sites Cancer Cancer and Oncology Cancer cells Cancer och onkologi Cell growth Cell Line, Tumor Cell Proliferation Clinical Medicine Cohort Studies Diagnostic systems Ethics Forkhead Box Protein O1 Forkhead Transcription Factors - chemistry Forkhead Transcription Factors - genetics Forkhead Transcription Factors - metabolism FOXO1 protein Gene Expression Regulation, Neoplastic Health aspects Humans Kinases Klinisk medicin Läkemedelskemi Male Medical and Health Sciences Medicin och hälsovetenskap Medicinal Chemistry Medicinska och farmaceutiska grundvetenskaper MicroRNAs - chemistry MicroRNAs - genetics MicroRNAs - metabolism Patients Prostate cancer Prostatic Neoplasms - genetics Prostatic Neoplasms - metabolism Prostatic Neoplasms - mortality Prostatic Neoplasms - pathology Protein binding RNA Interference Transcription Urologi och njurmedicin Urology and Nephrology |
| title | Upregulation of miR-96 enhances cellular proliferation of prostate cancer cells through FOXO1 |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-24T08%3A14%3A35IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Upregulation%20of%20miR-96%20enhances%20cellular%20proliferation%20of%20prostate%20cancer%20cells%20through%20FOXO1&rft.jtitle=PloS%20one&rft.au=Haflidad%C3%B3ttir,%20Benedikta%20S&rft.date=2013-08-12&rft.volume=8&rft.issue=8&rft.spage=e72400&rft.epage=e72400&rft.pages=e72400-e72400&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0072400&rft_dat=%3Cgale_plos_%3EA478310981%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1430420779&rft_id=info:pmid/23951320&rft_galeid=A478310981&rft_doaj_id=oai_doaj_org_article_05076b8cc2874db7bd72ccc10b7c479d&rfr_iscdi=true |