Omental cancer‐associated fibroblast‐derived exosomes with low microRNA‐29c‐3p promote ovarian cancer peritoneal metastasis
Ovarian cancer (OC) is characterized by frequent widespread peritoneal metastasis. Cancer‐associated fibroblasts (CAFs) represent a critical stromal component of metastatic niche and promote omentum metastasis in OC patients. However, the role of exosomes derived from omental CAFs in metastasis rema...
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| Veröffentlicht in: | Cancer science 2023-05, Vol.114 (5), p.1929-1942 |
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| creator | Han, Qing Tan, Shuran Gong, Lanqing Li, Guoqing Wu, Qiulei Chen, Le Du, Shi Li, Wenhan Liu, Xiaoli Cai, Jing Wang, Zehua |
| description | Ovarian cancer (OC) is characterized by frequent widespread peritoneal metastasis. Cancer‐associated fibroblasts (CAFs) represent a critical stromal component of metastatic niche and promote omentum metastasis in OC patients. However, the role of exosomes derived from omental CAFs in metastasis remains unclear. We isolated exosomes from primary omental normal fibroblasts (NFs) and CAFs from OC patients (NF‐Exo and CAF‐Exo, respectively) and assessed their effect on metastasis. In mice bearing orthotopic OC xenografts, CAF‐Exo treatment led to more rapid intraperitoneal tumor dissemination and shorter animal survival. Similar results were observed in mice undergoing intraperitoneal injection of tumor cells. Among the miRNAs downregulated in CAF‐Exo, miR‐29c‐3p in OC tissues was associated with metastasis and survival in patients. Moreover, increasing miR‐29c‐3p in CAF‐Exo significantly weakened the metastasis‐promoting effect of CAF‐Exo. Based on RNA sequencing, expression assays, and luciferase assays, matrix metalloproteinase 2 (MMP2) was identified as a direct target of miR‐29c‐3p. These results verify the significant contribution of exosomes from omental CAFs to OC peritoneal metastasis, which could be partially due to the relief of MMP2 expression inhibition mediated by low exosomal miR‐29c‐3p.
The conversion from NFs to CAFs causes a reduction of miR‐29c‐3p. Subsequently, the low level of miR‐29c‐3p in the CAF‐derived exosomes contributes to the derepression of MMP2, which promotes the aggression of OC cells. |
| doi_str_mv | 10.1111/cas.15726 |
| format | Article |
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The conversion from NFs to CAFs causes a reduction of miR‐29c‐3p. Subsequently, the low level of miR‐29c‐3p in the CAF‐derived exosomes contributes to the derepression of MMP2, which promotes the aggression of OC cells.</description><identifier>ISSN: 1347-9032</identifier><identifier>EISSN: 1349-7006</identifier><identifier>DOI: 10.1111/cas.15726</identifier><identifier>PMID: 36644823</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Animals ; Breast cancer ; Cancer-Associated Fibroblasts - metabolism ; Cell Line, Tumor ; Cell Proliferation ; Cytokines ; exosome ; Exosomes ; Exosomes - metabolism ; Female ; Fibroblasts ; Gelatinase A ; Gene Expression Regulation, Neoplastic ; Humans ; Matrix metalloproteinase ; Matrix Metalloproteinase 2 - genetics ; Matrix Metalloproteinase 2 - metabolism ; Medical prognosis ; Metalloproteinase ; Metastases ; Metastasis ; Mice ; MicroRNAs ; MicroRNAs - genetics ; MicroRNAs - metabolism ; miRNA ; miR‐29c‐3p ; myofibroblast ; Omentum ; Omentum - metabolism ; Omentum - pathology ; Original ; Ovarian cancer ; Ovarian Neoplasms - pathology ; ovarian tumor ; Peritoneal Neoplasms - pathology ; Peritoneum ; Smooth muscle ; Tumor cells ; Tumors</subject><ispartof>Cancer science, 2023-05, Vol.114 (5), p.1929-1942</ispartof><rights>2023 The Authors. published by John Wiley & Sons Australia, Ltd on behalf of Japanese Cancer Association.</rights><rights>2023 The Authors. Cancer Science published by John Wiley & Sons Australia, Ltd on behalf of Japanese Cancer Association.</rights><rights>2023. This work is published under http://creativecommons.org/licenses/by-nc-nd/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><citedby>FETCH-LOGICAL-c4686-93509e667b7de05dad86ddf8411cb92b0ee515c94b9a652736ff39c8c3377e543</citedby><cites>FETCH-LOGICAL-c4686-93509e667b7de05dad86ddf8411cb92b0ee515c94b9a652736ff39c8c3377e543</cites><orcidid>0000-0001-6423-8219</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10154903/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10154903/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,1411,11543,27903,27904,45553,45554,46030,46454,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36644823$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Han, Qing</creatorcontrib><creatorcontrib>Tan, Shuran</creatorcontrib><creatorcontrib>Gong, Lanqing</creatorcontrib><creatorcontrib>Li, Guoqing</creatorcontrib><creatorcontrib>Wu, Qiulei</creatorcontrib><creatorcontrib>Chen, Le</creatorcontrib><creatorcontrib>Du, Shi</creatorcontrib><creatorcontrib>Li, Wenhan</creatorcontrib><creatorcontrib>Liu, Xiaoli</creatorcontrib><creatorcontrib>Cai, Jing</creatorcontrib><creatorcontrib>Wang, Zehua</creatorcontrib><title>Omental cancer‐associated fibroblast‐derived exosomes with low microRNA‐29c‐3p promote ovarian cancer peritoneal metastasis</title><title>Cancer science</title><addtitle>Cancer Sci</addtitle><description>Ovarian cancer (OC) is characterized by frequent widespread peritoneal metastasis. Cancer‐associated fibroblasts (CAFs) represent a critical stromal component of metastatic niche and promote omentum metastasis in OC patients. However, the role of exosomes derived from omental CAFs in metastasis remains unclear. We isolated exosomes from primary omental normal fibroblasts (NFs) and CAFs from OC patients (NF‐Exo and CAF‐Exo, respectively) and assessed their effect on metastasis. In mice bearing orthotopic OC xenografts, CAF‐Exo treatment led to more rapid intraperitoneal tumor dissemination and shorter animal survival. Similar results were observed in mice undergoing intraperitoneal injection of tumor cells. Among the miRNAs downregulated in CAF‐Exo, miR‐29c‐3p in OC tissues was associated with metastasis and survival in patients. Moreover, increasing miR‐29c‐3p in CAF‐Exo significantly weakened the metastasis‐promoting effect of CAF‐Exo. Based on RNA sequencing, expression assays, and luciferase assays, matrix metalloproteinase 2 (MMP2) was identified as a direct target of miR‐29c‐3p. These results verify the significant contribution of exosomes from omental CAFs to OC peritoneal metastasis, which could be partially due to the relief of MMP2 expression inhibition mediated by low exosomal miR‐29c‐3p.
The conversion from NFs to CAFs causes a reduction of miR‐29c‐3p. Subsequently, the low level of miR‐29c‐3p in the CAF‐derived exosomes contributes to the derepression of MMP2, which promotes the aggression of OC cells.</description><subject>Animals</subject><subject>Breast cancer</subject><subject>Cancer-Associated Fibroblasts - metabolism</subject><subject>Cell Line, Tumor</subject><subject>Cell Proliferation</subject><subject>Cytokines</subject><subject>exosome</subject><subject>Exosomes</subject><subject>Exosomes - metabolism</subject><subject>Female</subject><subject>Fibroblasts</subject><subject>Gelatinase A</subject><subject>Gene Expression Regulation, Neoplastic</subject><subject>Humans</subject><subject>Matrix metalloproteinase</subject><subject>Matrix Metalloproteinase 2 - genetics</subject><subject>Matrix Metalloproteinase 2 - metabolism</subject><subject>Medical prognosis</subject><subject>Metalloproteinase</subject><subject>Metastases</subject><subject>Metastasis</subject><subject>Mice</subject><subject>MicroRNAs</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - metabolism</subject><subject>miRNA</subject><subject>miR‐29c‐3p</subject><subject>myofibroblast</subject><subject>Omentum</subject><subject>Omentum - metabolism</subject><subject>Omentum - pathology</subject><subject>Original</subject><subject>Ovarian cancer</subject><subject>Ovarian Neoplasms - pathology</subject><subject>ovarian tumor</subject><subject>Peritoneal Neoplasms - pathology</subject><subject>Peritoneum</subject><subject>Smooth muscle</subject><subject>Tumor cells</subject><subject>Tumors</subject><issn>1347-9032</issn><issn>1349-7006</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNp1kc1O3DAURq2qVaHQRV-gitRNWQTs2LHjFRqNyo-EitTSteU4N8UoiYOdmSm7Sn0BnpEn4cJMUUGqF7Z1fXTs64-QD4zuMxwHzqZ9VqpCviLbjAudK0rl68e9yjXlxRZ5l9IVpVwKLd6SLS6lEFXBt8mf8x6GyXaZs4ODePf71qYUnLcTNFnr6xjqzqYJ6w1Ev8Qi_Aop9JCylZ8usy6sst67GL59nSFUaIczH7Mxhj5MkIWljd4OG302omQKA-CFPUwotsmnXfKmtV2C95t1h_w4-nIxP8nPzo9P57Oz3AlZyVzzkmqQUtWqAVo2tqlk07SVYMzVuqgpQMlKp0WtrSwLxWXbcu0qx7lSUAq-Qw7X3nFR99A4bDzazozR9zbemGC9eX4y-EvzMywNo6wU-I9o-LwxxHC9gDSZ3icHXWcHCItkCiUllYLqh8s-vUCvwiIO2J8pKloJDEJUSO2tKfzBlCK0T69h1DxkazBb85gtsh__ff4T-TdMBA7WwMp3cPN_k5nPvq-V9zQ4tIE</recordid><startdate>202305</startdate><enddate>202305</enddate><creator>Han, Qing</creator><creator>Tan, Shuran</creator><creator>Gong, Lanqing</creator><creator>Li, Guoqing</creator><creator>Wu, Qiulei</creator><creator>Chen, Le</creator><creator>Du, Shi</creator><creator>Li, Wenhan</creator><creator>Liu, Xiaoli</creator><creator>Cai, Jing</creator><creator>Wang, Zehua</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</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>8FE</scope><scope>8FH</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>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6423-8219</orcidid></search><sort><creationdate>202305</creationdate><title>Omental cancer‐associated fibroblast‐derived exosomes with low microRNA‐29c‐3p promote ovarian cancer peritoneal metastasis</title><author>Han, Qing ; 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Cancer‐associated fibroblasts (CAFs) represent a critical stromal component of metastatic niche and promote omentum metastasis in OC patients. However, the role of exosomes derived from omental CAFs in metastasis remains unclear. We isolated exosomes from primary omental normal fibroblasts (NFs) and CAFs from OC patients (NF‐Exo and CAF‐Exo, respectively) and assessed their effect on metastasis. In mice bearing orthotopic OC xenografts, CAF‐Exo treatment led to more rapid intraperitoneal tumor dissemination and shorter animal survival. Similar results were observed in mice undergoing intraperitoneal injection of tumor cells. Among the miRNAs downregulated in CAF‐Exo, miR‐29c‐3p in OC tissues was associated with metastasis and survival in patients. Moreover, increasing miR‐29c‐3p in CAF‐Exo significantly weakened the metastasis‐promoting effect of CAF‐Exo. Based on RNA sequencing, expression assays, and luciferase assays, matrix metalloproteinase 2 (MMP2) was identified as a direct target of miR‐29c‐3p. These results verify the significant contribution of exosomes from omental CAFs to OC peritoneal metastasis, which could be partially due to the relief of MMP2 expression inhibition mediated by low exosomal miR‐29c‐3p.
The conversion from NFs to CAFs causes a reduction of miR‐29c‐3p. Subsequently, the low level of miR‐29c‐3p in the CAF‐derived exosomes contributes to the derepression of MMP2, which promotes the aggression of OC cells.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>36644823</pmid><doi>10.1111/cas.15726</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-6423-8219</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Breast cancer Cancer-Associated Fibroblasts - metabolism Cell Line, Tumor Cell Proliferation Cytokines exosome Exosomes Exosomes - metabolism Female Fibroblasts Gelatinase A Gene Expression Regulation, Neoplastic Humans Matrix metalloproteinase Matrix Metalloproteinase 2 - genetics Matrix Metalloproteinase 2 - metabolism Medical prognosis Metalloproteinase Metastases Metastasis Mice MicroRNAs MicroRNAs - genetics MicroRNAs - metabolism miRNA miR‐29c‐3p myofibroblast Omentum Omentum - metabolism Omentum - pathology Original Ovarian cancer Ovarian Neoplasms - pathology ovarian tumor Peritoneal Neoplasms - pathology Peritoneum Smooth muscle Tumor cells Tumors |
| title | Omental cancer‐associated fibroblast‐derived exosomes with low microRNA‐29c‐3p promote ovarian cancer peritoneal metastasis |
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