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Differential analysis of histopathological and genetic markers of cancer aggressiveness, and survival difference in EBV-positive and EBV-negative prostate carcinoma
Several studies have shown an association between prostate carcinoma (PCa) and Epstein-Barr virus (EBV); however, none of the studies so far have identified the histopathological and genetic markers of cancer aggressiveness associated with EBV in PCa tissues. In this study, we used previously charac...
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| Published in: | Scientific reports 2024-05, Vol.14 (1), p.10315-10315, Article 10315 |
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| creator | Ahmed, Khalid Sheikh, Alisalman Fatima, Saira Ghulam, Tahira Haider, Ghulam Abbas, Farhat Sarria-Santamera, Antonio Ghias, Kulsoom Mughal, Nouman Abidi, Syed Hani |
| description | Several studies have shown an association between prostate carcinoma (PCa) and Epstein-Barr virus (EBV); however, none of the studies so far have identified the histopathological and genetic markers of cancer aggressiveness associated with EBV in PCa tissues. In this study, we used previously characterized EBV-PCR-positive (n = 39) and EBV-negative (n = 60) PCa tissues to perform an IHC-based assessment of key histopathological and molecular markers of PCa aggressiveness (EMT markers, AR expression, perineural invasion, and lymphocytic infiltration characterization). Additionally, we investigated the differential expression of key oncogenes, EMT-associated genes, and PCa-specific oncomiRs, in EBV-positive and -negative tissues, using the qPCR array. Finally, survival benefit analysis was also performed in EBV-positive and EBV-negative PCa patients. The EBV-positive PCa exhibited a higher percentage (80%) of perineural invasion (PNI) compared to EBV-negative PCa (67.3%) samples. Similarly, a higher lymphocytic infiltration was observed in EBV-LMP1-positive PCa samples. The subset characterization of T and B cell lymphocytic infiltration showed a trend of higher intratumoral and tumor stromal lymphocytic infiltration in EBV-negative tissues compared with EBV-positive tissues. The logistic regression analysis showed that EBV-positive status was associated with decreased odds (OR = 0.07;
p
-value |
| doi_str_mv | 10.1038/s41598-024-60538-0 |
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p
-value < 0.019) of CD3 intratumoral lymphocytic infiltration in PCa tissues. The analysis of IHC-based expression patterns of EMT markers showed comparable expression of all EMT markers, except vimentin, which showed higher expression in EBV-positive PCa tissues compared to EBV-negative PCa tissues. Furthermore, gene expression analysis showed a statistically significant difference (
p
< 0.05) in the expression of
CDH1, AR, CHEK-2, CDKN-1B
, and
CDC-20
and oncomiRs
miR-126, miR-152-3p, miR-452, miR-145-3p, miR-196a, miR-183-3p
, and
miR-146b
in EBV-positive PCa tissues compared to EBV-negative PCa tissues. Overall, the survival proportion was comparable in both groups. The presence of EBV in the PCa tissues results in an increased expression of certain oncogenes, oncomiRs, and EMT marker (vimentin) and a decrease in CD3 ITL, which may be associated with the aggressive forms of PCa.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-024-60538-0</identifier><identifier>PMID: 38705879</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/326 ; 631/67 ; Aged ; Biomarkers, Tumor - genetics ; CD3 antigen ; E-cadherin ; EBV ; Epithelial-Mesenchymal Transition - genetics ; Epstein-Barr virus ; Epstein-Barr Virus Infections - complications ; Epstein-Barr Virus Infections - genetics ; Epstein-Barr Virus Infections - pathology ; Epstein-Barr Virus Infections - virology ; Gene expression ; Gene Expression Regulation, Neoplastic ; Genetic Markers ; Gleason scores ; Herpesvirus 4, Human - genetics ; Humanities and Social Sciences ; Humans ; Infiltration ; LMP1 ; Lymphocytes, Tumor-Infiltrating - immunology ; Male ; Metastases ; Middle Aged ; multidisciplinary ; Neoplasm Invasiveness ; Oncogenes ; Prostate ; Prostate cancer ; Prostate carcinoma ; Prostatic Neoplasms - genetics ; Prostatic Neoplasms - metabolism ; Prostatic Neoplasms - mortality ; Prostatic Neoplasms - pathology ; Prostatic Neoplasms - virology ; Regression analysis ; Science ; Science (multidisciplinary) ; Statistical analysis ; Survival analysis ; Tissues ; Tumor grade ; Vimentin</subject><ispartof>Scientific reports, 2024-05, Vol.14 (1), p.10315-10315, Article 10315</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4432-876c17a778a8ca5e79015483ed5caf6a512793e338fdb23d8f84b4bc699b5f2e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/3050754479/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3050754479?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25752,27923,27924,37011,37012,44589,53790,53792,74897</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38705879$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ahmed, Khalid</creatorcontrib><creatorcontrib>Sheikh, Alisalman</creatorcontrib><creatorcontrib>Fatima, Saira</creatorcontrib><creatorcontrib>Ghulam, Tahira</creatorcontrib><creatorcontrib>Haider, Ghulam</creatorcontrib><creatorcontrib>Abbas, Farhat</creatorcontrib><creatorcontrib>Sarria-Santamera, Antonio</creatorcontrib><creatorcontrib>Ghias, Kulsoom</creatorcontrib><creatorcontrib>Mughal, Nouman</creatorcontrib><creatorcontrib>Abidi, Syed Hani</creatorcontrib><title>Differential analysis of histopathological and genetic markers of cancer aggressiveness, and survival difference in EBV-positive and EBV-negative prostate carcinoma</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>Several studies have shown an association between prostate carcinoma (PCa) and Epstein-Barr virus (EBV); however, none of the studies so far have identified the histopathological and genetic markers of cancer aggressiveness associated with EBV in PCa tissues. In this study, we used previously characterized EBV-PCR-positive (n = 39) and EBV-negative (n = 60) PCa tissues to perform an IHC-based assessment of key histopathological and molecular markers of PCa aggressiveness (EMT markers, AR expression, perineural invasion, and lymphocytic infiltration characterization). Additionally, we investigated the differential expression of key oncogenes, EMT-associated genes, and PCa-specific oncomiRs, in EBV-positive and -negative tissues, using the qPCR array. Finally, survival benefit analysis was also performed in EBV-positive and EBV-negative PCa patients. The EBV-positive PCa exhibited a higher percentage (80%) of perineural invasion (PNI) compared to EBV-negative PCa (67.3%) samples. Similarly, a higher lymphocytic infiltration was observed in EBV-LMP1-positive PCa samples. The subset characterization of T and B cell lymphocytic infiltration showed a trend of higher intratumoral and tumor stromal lymphocytic infiltration in EBV-negative tissues compared with EBV-positive tissues. The logistic regression analysis showed that EBV-positive status was associated with decreased odds (OR = 0.07;
p
-value < 0.019) of CD3 intratumoral lymphocytic infiltration in PCa tissues. The analysis of IHC-based expression patterns of EMT markers showed comparable expression of all EMT markers, except vimentin, which showed higher expression in EBV-positive PCa tissues compared to EBV-negative PCa tissues. Furthermore, gene expression analysis showed a statistically significant difference (
p
< 0.05) in the expression of
CDH1, AR, CHEK-2, CDKN-1B
, and
CDC-20
and oncomiRs
miR-126, miR-152-3p, miR-452, miR-145-3p, miR-196a, miR-183-3p
, and
miR-146b
in EBV-positive PCa tissues compared to EBV-negative PCa tissues. Overall, the survival proportion was comparable in both groups. The presence of EBV in the PCa tissues results in an increased expression of certain oncogenes, oncomiRs, and EMT marker (vimentin) and a decrease in CD3 ITL, which may be associated with the aggressive forms of PCa.</description><subject>631/326</subject><subject>631/67</subject><subject>Aged</subject><subject>Biomarkers, Tumor - genetics</subject><subject>CD3 antigen</subject><subject>E-cadherin</subject><subject>EBV</subject><subject>Epithelial-Mesenchymal Transition - genetics</subject><subject>Epstein-Barr virus</subject><subject>Epstein-Barr Virus Infections - complications</subject><subject>Epstein-Barr Virus Infections - genetics</subject><subject>Epstein-Barr Virus Infections - pathology</subject><subject>Epstein-Barr Virus Infections - virology</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Genetic Markers</subject><subject>Gleason scores</subject><subject>Herpesvirus 4, Human - genetics</subject><subject>Humanities and Social Sciences</subject><subject>Humans</subject><subject>Infiltration</subject><subject>LMP1</subject><subject>Lymphocytes, Tumor-Infiltrating - immunology</subject><subject>Male</subject><subject>Metastases</subject><subject>Middle Aged</subject><subject>multidisciplinary</subject><subject>Neoplasm Invasiveness</subject><subject>Oncogenes</subject><subject>Prostate</subject><subject>Prostate cancer</subject><subject>Prostate carcinoma</subject><subject>Prostatic Neoplasms - genetics</subject><subject>Prostatic Neoplasms - metabolism</subject><subject>Prostatic Neoplasms - mortality</subject><subject>Prostatic Neoplasms - pathology</subject><subject>Prostatic Neoplasms - virology</subject><subject>Regression analysis</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Statistical analysis</subject><subject>Survival analysis</subject><subject>Tissues</subject><subject>Tumor grade</subject><subject>Vimentin</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9ks9u1DAQxiMEotXSF-CAInHhQMB_Y-eEaClQqRIX4GpNnEnWSzYOdrJS34cHxU2W0nLAF1szv_nGY39Z9pySN5Rw_TYKKitdECaKkkieTo-yU0aELBhn7PG980l2FuOOpCVZJWj1NDvhWhGpVXWa_frg2hYDDpODPocB-pvoYu7bfOvi5EeYtr73nbNLtsk7HHByNt9D-IFhAS0MFkMOXRcwRndIRIyvFzrO4eAOqbQ5drGYuyG_PP9ejD66KcELdxsYsIMlMAYfJ5gwCQfrBr-HZ9mTFvqIZ8d9k337ePn14nNx_eXT1cX768IKwVmhVWmpAqU0aAsSVUWoFJpjIy20JUjKVMWRc902NeONbrWoRW3Lqqply5BvsqtVt_GwM2Nwacob48GZJeBDZyCk6Xs0vJZCydoyrkrB6laDZEQppnVNVcVs0nq3ao1zvcfGphcO0D8QfZgZ3NZ0_mAoJYoIJpLCq6NC8D9njJPZu2ix72FAP0fDiaSCSSZkQl_-g-78HNJnLhRRUog0-SZjK2XTC8eA7d1tKDG3pjKrqUwylVlMZUgqenF_jruSPxZKAF-BmFJDh-Fv7__I_gZg09oa</recordid><startdate>20240505</startdate><enddate>20240505</enddate><creator>Ahmed, Khalid</creator><creator>Sheikh, Alisalman</creator><creator>Fatima, Saira</creator><creator>Ghulam, Tahira</creator><creator>Haider, Ghulam</creator><creator>Abbas, Farhat</creator><creator>Sarria-Santamera, Antonio</creator><creator>Ghias, Kulsoom</creator><creator>Mughal, Nouman</creator><creator>Abidi, Syed Hani</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><general>Nature Portfolio</general><scope>C6C</scope><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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20240505</creationdate><title>Differential analysis of histopathological and genetic markers of cancer aggressiveness, and survival difference in EBV-positive and EBV-negative prostate carcinoma</title><author>Ahmed, Khalid ; Sheikh, Alisalman ; Fatima, Saira ; Ghulam, Tahira ; Haider, Ghulam ; Abbas, Farhat ; Sarria-Santamera, Antonio ; Ghias, Kulsoom ; Mughal, Nouman ; Abidi, Syed Hani</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4432-876c17a778a8ca5e79015483ed5caf6a512793e338fdb23d8f84b4bc699b5f2e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>631/326</topic><topic>631/67</topic><topic>Aged</topic><topic>Biomarkers, Tumor - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Scientific reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ahmed, Khalid</au><au>Sheikh, Alisalman</au><au>Fatima, Saira</au><au>Ghulam, Tahira</au><au>Haider, Ghulam</au><au>Abbas, Farhat</au><au>Sarria-Santamera, Antonio</au><au>Ghias, Kulsoom</au><au>Mughal, Nouman</au><au>Abidi, Syed Hani</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Differential analysis of histopathological and genetic markers of cancer aggressiveness, and survival difference in EBV-positive and EBV-negative prostate carcinoma</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2024-05-05</date><risdate>2024</risdate><volume>14</volume><issue>1</issue><spage>10315</spage><epage>10315</epage><pages>10315-10315</pages><artnum>10315</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>Several studies have shown an association between prostate carcinoma (PCa) and Epstein-Barr virus (EBV); however, none of the studies so far have identified the histopathological and genetic markers of cancer aggressiveness associated with EBV in PCa tissues. In this study, we used previously characterized EBV-PCR-positive (n = 39) and EBV-negative (n = 60) PCa tissues to perform an IHC-based assessment of key histopathological and molecular markers of PCa aggressiveness (EMT markers, AR expression, perineural invasion, and lymphocytic infiltration characterization). Additionally, we investigated the differential expression of key oncogenes, EMT-associated genes, and PCa-specific oncomiRs, in EBV-positive and -negative tissues, using the qPCR array. Finally, survival benefit analysis was also performed in EBV-positive and EBV-negative PCa patients. The EBV-positive PCa exhibited a higher percentage (80%) of perineural invasion (PNI) compared to EBV-negative PCa (67.3%) samples. Similarly, a higher lymphocytic infiltration was observed in EBV-LMP1-positive PCa samples. The subset characterization of T and B cell lymphocytic infiltration showed a trend of higher intratumoral and tumor stromal lymphocytic infiltration in EBV-negative tissues compared with EBV-positive tissues. The logistic regression analysis showed that EBV-positive status was associated with decreased odds (OR = 0.07;
p
-value < 0.019) of CD3 intratumoral lymphocytic infiltration in PCa tissues. The analysis of IHC-based expression patterns of EMT markers showed comparable expression of all EMT markers, except vimentin, which showed higher expression in EBV-positive PCa tissues compared to EBV-negative PCa tissues. Furthermore, gene expression analysis showed a statistically significant difference (
p
< 0.05) in the expression of
CDH1, AR, CHEK-2, CDKN-1B
, and
CDC-20
and oncomiRs
miR-126, miR-152-3p, miR-452, miR-145-3p, miR-196a, miR-183-3p
, and
miR-146b
in EBV-positive PCa tissues compared to EBV-negative PCa tissues. Overall, the survival proportion was comparable in both groups. The presence of EBV in the PCa tissues results in an increased expression of certain oncogenes, oncomiRs, and EMT marker (vimentin) and a decrease in CD3 ITL, which may be associated with the aggressive forms of PCa.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>38705879</pmid><doi>10.1038/s41598-024-60538-0</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | Scientific reports, 2024-05, Vol.14 (1), p.10315-10315, Article 10315 |
| issn | 2045-2322 2045-2322 |
| language | eng |
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| source | Open Access: PubMed Central; Publicly Available Content Database; Full-Text Journals in Chemistry (Open access); Springer Nature - nature.com Journals - Fully Open Access |
| subjects | 631/326 631/67 Aged Biomarkers, Tumor - genetics CD3 antigen E-cadherin EBV Epithelial-Mesenchymal Transition - genetics Epstein-Barr virus Epstein-Barr Virus Infections - complications Epstein-Barr Virus Infections - genetics Epstein-Barr Virus Infections - pathology Epstein-Barr Virus Infections - virology Gene expression Gene Expression Regulation, Neoplastic Genetic Markers Gleason scores Herpesvirus 4, Human - genetics Humanities and Social Sciences Humans Infiltration LMP1 Lymphocytes, Tumor-Infiltrating - immunology Male Metastases Middle Aged multidisciplinary Neoplasm Invasiveness Oncogenes Prostate Prostate cancer Prostate carcinoma Prostatic Neoplasms - genetics Prostatic Neoplasms - metabolism Prostatic Neoplasms - mortality Prostatic Neoplasms - pathology Prostatic Neoplasms - virology Regression analysis Science Science (multidisciplinary) Statistical analysis Survival analysis Tissues Tumor grade Vimentin |
| title | Differential analysis of histopathological and genetic markers of cancer aggressiveness, and survival difference in EBV-positive and EBV-negative prostate carcinoma |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-12T23%3A36%3A22IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Differential%20analysis%20of%20histopathological%20and%20genetic%20markers%20of%20cancer%20aggressiveness,%20and%20survival%20difference%20in%20EBV-positive%20and%20EBV-negative%20prostate%20carcinoma&rft.jtitle=Scientific%20reports&rft.au=Ahmed,%20Khalid&rft.date=2024-05-05&rft.volume=14&rft.issue=1&rft.spage=10315&rft.epage=10315&rft.pages=10315-10315&rft.artnum=10315&rft.issn=2045-2322&rft.eissn=2045-2322&rft_id=info:doi/10.1038/s41598-024-60538-0&rft_dat=%3Cproquest_doaj_%3E3050754479%3C/proquest_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c4432-876c17a778a8ca5e79015483ed5caf6a512793e338fdb23d8f84b4bc699b5f2e3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=3050754479&rft_id=info:pmid/38705879&rfr_iscdi=true |