{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T09:56:20Z","timestamp":1790070980651,"version":"4.0.1"},"reference-count":40,"publisher":"Wiley","issue":"3","license":[{"start":{"date-parts":[[2019,5,14]],"date-time":"2019-05-14T00:00:00Z","timestamp":1557792000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["pathsocjournals.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["The Journal of Pathology"],"published-print":{"date-parts":[[2019,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    High grade serous ovarian carcinoma (HGSC) without identifiable serous tubal intraepithelial carcinoma (STIC) within the fallopian tube (FT) occurs in approximately 50% of patients. The objective of this study was to use a multisite tumor sampling approach to study HGSC with and without STIC. RNAseq analysis of HGSC samples collected from multiple sites e.g. ovary, FT and peritoneum, revealed moderate levels of intrapatient heterogeneity in gene expression that could influence molecular profiles. Mixed\u2010model ANOVA analysis of gene expression in tumor samples from patients with multiple tumor sites (\n                    <jats:italic>n<\/jats:italic>\n                    \u2009=\u200913) and patients with a single site tumor sample (\n                    <jats:italic>n<\/jats:italic>\n                    \u2009=\u200911) to compare HGSC\u2010STIC to HGSC\u2010NOSTIC identified neurotensin (\n                    <jats:italic>NTS<\/jats:italic>\n                    ) as significantly higher (&gt; two\u2010fold change, False Discovery Rate (FDR)\u2009&lt;\u20090.10) in HGSC\u2010STIC. This data was validated using publicly available RNA\u2010Seq datasets. Concordance between higher\n                    <jats:italic>NTS<\/jats:italic>\n                    gene expression and NTS peptide levels in HGSC\u2010STIC samples was demonstrated by immunohistochemistry. To determine the role of NTS in HGSC, five ovarian cancer (OvCa) cell lines were screened for expression of NTS and its receptors, NTSR1 and NTSR3. Increased expression of NTS and NSTR1 was observed in several of the OvCa cells, whereas the NTSR3 receptor was lower in all OvCa cells, compared to immortalized FT epithelial cells. Treatment with NTSR1 inhibitor (SR48692) decreased cell proliferation, but increased cell migration in OvCa cells. The effects of SR48692 were receptor mediated, since transient RNAi knockdown of NTSR1 mimicked the migratory effects and knockdown of NTSR3 mimicked the anti\u2010proliferative effects. Further, knockdown of NTSR1 or NTSR3 was associated with acquisition of distinct morphological phenotypes, epithelial or mesenchymal, respectively. Taken together, our results reveal a difference in a biologically active pathway between HGSC with and without STIC. Furthermore, we identify neurotensin signaling as an important pathway involved in cell proliferation and epithelial\u2013mesenchymal transition in HGSC\u2010STIC which warrants further study as a potential therapeutic target. \u00a9 2019 The Authors.\n                    <jats:italic>The Journal of Pathology<\/jats:italic>\n                    published by John Wiley &amp; Sons Ltd on behalf of Pathological Society of Great Britain and Ireland.\n                  <\/jats:p>","DOI":"10.1002\/path.5264","type":"journal-article","created":{"date-parts":[[2019,3,19]],"date-time":"2019-03-19T02:26:16Z","timestamp":1552962376000},"page":"352-362","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Increased expression of neurotensin in high grade serous ovarian carcinoma with evidence of serous tubal intraepithelial carcinoma"],"prefix":"10.1002","volume":"248","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9204-5235","authenticated-orcid":false,"given":"Eric J","family":"Norris","sequence":"first","affiliation":[{"name":"Levine Cancer Institute, Atrium Health  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qing","family":"Zhang","sequence":"additional","affiliation":[{"name":"Levine Cancer Institute, Atrium Health  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9676-5387","authenticated-orcid":false,"given":"Wendell D","family":"Jones","sequence":"additional","affiliation":[{"name":"Department of Bioinformatics and Clinical Systems, Q<sup>2<\/sup> Solutions \u2013 EA Genomics  Morrisville NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Darla","family":"DeStephanis","sequence":"additional","affiliation":[{"name":"Levine Cancer Institute, Atrium Health  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ashley P","family":"Sutker","sequence":"additional","affiliation":[{"name":"Levine Cancer Institute, Atrium Health  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chad A","family":"Livasy","sequence":"additional","affiliation":[{"name":"Carolinas Pathology Group  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ram N","family":"Ganapathi","sequence":"additional","affiliation":[{"name":"Levine Cancer Institute, Atrium Health  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David L","family":"Tait","sequence":"additional","affiliation":[{"name":"Levine Cancer Institute, Atrium Health  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mahrukh K","family":"Ganapathi","sequence":"additional","affiliation":[{"name":"Levine Cancer Institute, Atrium Health  Charlotte NC USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2019,5,14]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"publisher","DOI":"10.1038\/nrc2644"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ygyno.2017.04.011"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1097\/IGC.0000000000000946"},{"key":"e_1_2_7_5_1","doi-asserted-by":"publisher","DOI":"10.1097\/GCO.0000000000000340"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1111\/1471-0528.14543"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.1038\/modpathol.2016.238"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1002\/path.5145"},{"key":"e_1_2_7_9_1","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.CAN-15-1382"},{"key":"e_1_2_7_10_1","doi-asserted-by":"publisher","DOI":"10.1002\/path.4230"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.eururo.2018.06.047"},{"key":"e_1_2_7_12_1","doi-asserted-by":"publisher","DOI":"10.1158\/1078-0432.CCR-16-0032"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13058-016-0725-1"},{"key":"e_1_2_7_14_1","doi-asserted-by":"publisher","DOI":"10.1101\/gr.161026.113"},{"key":"e_1_2_7_15_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-017-01217-9"},{"key":"e_1_2_7_16_1","doi-asserted-by":"publisher","DOI":"10.1038\/nature10166"},{"key":"e_1_2_7_17_1","doi-asserted-by":"publisher","DOI":"10.1038\/nprot.2007.30"},{"key":"e_1_2_7_18_1","doi-asserted-by":"publisher","DOI":"10.1158\/1078-0432.CCR-08-0196"},{"key":"e_1_2_7_19_1","doi-asserted-by":"publisher","DOI":"10.1007\/s13277-014-1794-3"},{"key":"e_1_2_7_20_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.90.1.65"},{"key":"e_1_2_7_21_1","doi-asserted-by":"publisher","DOI":"10.1053\/gast.2002.36000"},{"key":"e_1_2_7_22_1","doi-asserted-by":"publisher","DOI":"10.1080\/2162402X.2018.1440166"},{"key":"e_1_2_7_23_1","doi-asserted-by":"publisher","DOI":"10.1002\/ijc.25494"},{"key":"e_1_2_7_24_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00018-012-1251-7"},{"key":"e_1_2_7_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2017.07.025"},{"key":"e_1_2_7_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1525-1438.2007.00908.x"},{"key":"e_1_2_7_27_1","doi-asserted-by":"publisher","DOI":"10.1158\/1078-0432.CCR-06-0357"},{"key":"e_1_2_7_28_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms14046571"},{"key":"e_1_2_7_29_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms12645"},{"key":"e_1_2_7_30_1","doi-asserted-by":"publisher","DOI":"10.1158\/1541-7786.MCR-16-0097"},{"key":"e_1_2_7_31_1","doi-asserted-by":"publisher","DOI":"10.1158\/1078-0432.CCR-07-4959"},{"key":"e_1_2_7_32_1","doi-asserted-by":"publisher","DOI":"10.1038\/modpathol.2012.32"},{"key":"e_1_2_7_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.neo.2017.11.012"},{"key":"e_1_2_7_34_1","doi-asserted-by":"publisher","DOI":"10.1158\/1078-0432.CCR-17-0861"},{"key":"e_1_2_7_35_1","doi-asserted-by":"publisher","DOI":"10.3892\/ijo.2017.3990"},{"key":"e_1_2_7_36_1","first-page":"169","article-title":"The effect of sortilin silencing on ovarian carcinoma cells","volume":"6","author":"Ghaemimanesh F","year":"2014","journal-title":"Avicenna J Med Biotechnol"},{"key":"e_1_2_7_37_1","first-page":"184","article-title":"Neurotensin and its high affinity receptor 1 as a potential pharmacological target in cancer therapy","volume":"3","author":"Wu Z","year":"2012","journal-title":"Front Endocrinol (Lausanne)"},{"key":"e_1_2_7_38_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0016186"},{"key":"e_1_2_7_39_1","doi-asserted-by":"publisher","DOI":"10.1159\/000484232"},{"key":"e_1_2_7_40_1","doi-asserted-by":"publisher","DOI":"10.1158\/0008-5472.CAN-17-1671"},{"key":"e_1_2_7_41_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cellsig.2014.08.027"}],"container-title":["The Journal of Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/path.5264","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/path.5264","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/pathsocjournals.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/path.5264","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,20]],"date-time":"2025-10-20T10:08:22Z","timestamp":1760954902000},"score":1,"resource":{"primary":{"URL":"https:\/\/pathsocjournals.onlinelibrary.wiley.com\/doi\/10.1002\/path.5264"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,5,14]]},"references-count":40,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2019,7]]}},"alternative-id":["10.1002\/path.5264"],"URL":"https:\/\/doi.org\/10.1002\/path.5264","archive":["Portico"],"relation":{},"ISSN":["0022-3417","1096-9896"],"issn-type":[{"value":"0022-3417","type":"print"},{"value":"1096-9896","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,5,14]]},"assertion":[{"value":"2018-09-26","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-03-13","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2019-05-14","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}