CCBE1 promotes tumor lymphangiogenesis and is negatively regulated by TGFβ signaling in colorectal cancer
Collagen and calcium-binding EGF domain-1 (CCBE1) is essential for lymphatic vascular development as it promotes vascular endothelial growth factor C (VEGFC) proteolysis. A recent study reported that CCBE1 was overexpressed in epithelial colorectal cancer (CRC) cells; however, the role of CCBE1 in t...
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| Veröffentlicht in: | Theranostics 2020-01, Vol.10 (5), p.2327-2341 |
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| creator | Song, Jinglue Chen, Wei Cui, Xuewei Huang, Zhenyu Wen, Dongpeng Yang, Yili Yu, Wei Cui, Long Liu, Chen-Ying |
| description | Collagen and calcium-binding EGF domain-1 (CCBE1) is essential for lymphatic vascular development as it promotes vascular endothelial growth factor C (VEGFC) proteolysis. A recent study reported that CCBE1 was overexpressed in epithelial colorectal cancer (CRC) cells; however, the role of CCBE1 in tumor lymphangiogenesis and the mechanism underlying dysregulated CCBE1 expression in CRC remain undefined.
The role of CCBE1 in tumor lymphangiogenesis and lymphatic metastasis was investigated using human lymphatic endothelial cells (HLECs) model
, and a hindfoot lymphatic metastasis model
. Immunochemistry analysis was performed to assess CCBE1 expression, prognostic value and correlation with clinicopathological characteristics in CRC. The biochemical function and transcriptional regulatory mechanism of CCBE1 were explored by western blot, qPCR, and chromatin immunoprecipitation.
: Cancer cell-derived CCBE1 enhances VEGFC proteolysis
, facilitates tube formation and migration of HLECs
, and promotes tumor lymphangiogenesis and lymphatic metastasis
. In addition to CRC cells, tumor stroma within CRC tissue shows high CCBE1 expression, which is associated with high lymphatic vessel density, increased lymph node metastasis and poor prognosis. Cancer-associated fibroblasts (CAFs) express and secret CCBE1, thereby contributing to VEGFC maturation and tumor lymphangiogenesis in CRC. Transforming growth factor beta (TGF-β) downregulates the transcription and lymphangiogenic function of CCBE1 in CAFs and CRC cells through direct binding of SMADs to CCBE1 gene locus. Inactivation of the TGF-β pathway correlates with increased CCBE1 expression in CRC.
: Our results demonstrate the protumorigenic role of CCBE1 in promoting lymphangiogenesis and lymphatic metastasis in CRC, revealing a new mechanism by which loss of TGF-β signaling promotes CRC metastasis. |
| doi_str_mv | 10.7150/thno.39740 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7019157</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2598254905</sourcerecordid><originalsourceid>FETCH-LOGICAL-c406t-d90e43a4112208dafeccd37936e52294316507f5462bd1fc94e3e4bf7fd602033</originalsourceid><addsrcrecordid>eNpdkctqHDEQRZsQExvHG39AEGQTAuPordEmkAx-BAze2GuhUVf3aFBLE0ltmN_Kh-SbIscPnNSmCurU5VK3604JPlNE4C91E9MZ04rjN90RWbLlQkmO376aD7uTUra4FcdUE_2uO2QUL9uJOOq2q9X3c4J2OU2pQkF1nlJGYT_tNjaOPo0QofiCbOxRaxFGW_09hD3KMM7BVujReo9uLy9-_0LFj9EGH0fkI3IppAyu2oCcjQ7y--5gsKHAyVM_7u4uzm9XV4vrm8sfq2_XC8exrIteY-DMckJoc9nbAZzrmdJMgqBUc0akwGoQXNJ1TwanOTDg60ENvcQUM3bcfX3U3c3rCXoHsWYbzC77yea9SdabfzfRb8yY7o3CRBOhmsCnJ4Gcfs5Qqpl8cRCCjZDmYiiTDAslJW3ox__QbZpze0KjhF5SwTUWjfr8SLmcSskwvJgh2DykaB5SNH9TbPCH1_Zf0OfM2B-jlJn6</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2598254905</pqid></control><display><type>article</type><title>CCBE1 promotes tumor lymphangiogenesis and is negatively regulated by TGFβ signaling in colorectal cancer</title><source>MEDLINE</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central Open Access</source><source>PubMed Central</source><creator>Song, Jinglue ; Chen, Wei ; Cui, Xuewei ; Huang, Zhenyu ; Wen, Dongpeng ; Yang, Yili ; Yu, Wei ; Cui, Long ; Liu, Chen-Ying</creator><creatorcontrib>Song, Jinglue ; Chen, Wei ; Cui, Xuewei ; Huang, Zhenyu ; Wen, Dongpeng ; Yang, Yili ; Yu, Wei ; Cui, Long ; Liu, Chen-Ying</creatorcontrib><description>Collagen and calcium-binding EGF domain-1 (CCBE1) is essential for lymphatic vascular development as it promotes vascular endothelial growth factor C (VEGFC) proteolysis. A recent study reported that CCBE1 was overexpressed in epithelial colorectal cancer (CRC) cells; however, the role of CCBE1 in tumor lymphangiogenesis and the mechanism underlying dysregulated CCBE1 expression in CRC remain undefined.
The role of CCBE1 in tumor lymphangiogenesis and lymphatic metastasis was investigated using human lymphatic endothelial cells (HLECs) model
, and a hindfoot lymphatic metastasis model
. Immunochemistry analysis was performed to assess CCBE1 expression, prognostic value and correlation with clinicopathological characteristics in CRC. The biochemical function and transcriptional regulatory mechanism of CCBE1 were explored by western blot, qPCR, and chromatin immunoprecipitation.
: Cancer cell-derived CCBE1 enhances VEGFC proteolysis
, facilitates tube formation and migration of HLECs
, and promotes tumor lymphangiogenesis and lymphatic metastasis
. In addition to CRC cells, tumor stroma within CRC tissue shows high CCBE1 expression, which is associated with high lymphatic vessel density, increased lymph node metastasis and poor prognosis. Cancer-associated fibroblasts (CAFs) express and secret CCBE1, thereby contributing to VEGFC maturation and tumor lymphangiogenesis in CRC. Transforming growth factor beta (TGF-β) downregulates the transcription and lymphangiogenic function of CCBE1 in CAFs and CRC cells through direct binding of SMADs to CCBE1 gene locus. Inactivation of the TGF-β pathway correlates with increased CCBE1 expression in CRC.
: Our results demonstrate the protumorigenic role of CCBE1 in promoting lymphangiogenesis and lymphatic metastasis in CRC, revealing a new mechanism by which loss of TGF-β signaling promotes CRC metastasis.</description><identifier>ISSN: 1838-7640</identifier><identifier>EISSN: 1838-7640</identifier><identifier>DOI: 10.7150/thno.39740</identifier><identifier>PMID: 32089745</identifier><language>eng</language><publisher>Australia: Ivyspring International Publisher Pty Ltd</publisher><subject>Aged ; Animals ; Calcium-Binding Proteins - metabolism ; Cancer-Associated Fibroblasts - metabolism ; Colorectal cancer ; Colorectal Neoplasms - metabolism ; Colorectal Neoplasms - pathology ; Endothelial Cells - metabolism ; Female ; Growth factors ; HCT116 Cells ; Humans ; Lymphangiogenesis ; Lymphatic Metastasis - pathology ; Lymphatic system ; Male ; Medical prognosis ; Metastasis ; Mice ; Proteins ; Research Paper ; Signal Transduction ; Transforming Growth Factor beta - metabolism ; Tumor Suppressor Proteins - metabolism ; Tumors ; Vascular Endothelial Growth Factor C - metabolism</subject><ispartof>Theranostics, 2020-01, Vol.10 (5), p.2327-2341</ispartof><rights>The author(s).</rights><rights>2020. This work is published under https://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><rights>The author(s) 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c406t-d90e43a4112208dafeccd37936e52294316507f5462bd1fc94e3e4bf7fd602033</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7019157/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7019157/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,882,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32089745$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Song, Jinglue</creatorcontrib><creatorcontrib>Chen, Wei</creatorcontrib><creatorcontrib>Cui, Xuewei</creatorcontrib><creatorcontrib>Huang, Zhenyu</creatorcontrib><creatorcontrib>Wen, Dongpeng</creatorcontrib><creatorcontrib>Yang, Yili</creatorcontrib><creatorcontrib>Yu, Wei</creatorcontrib><creatorcontrib>Cui, Long</creatorcontrib><creatorcontrib>Liu, Chen-Ying</creatorcontrib><title>CCBE1 promotes tumor lymphangiogenesis and is negatively regulated by TGFβ signaling in colorectal cancer</title><title>Theranostics</title><addtitle>Theranostics</addtitle><description>Collagen and calcium-binding EGF domain-1 (CCBE1) is essential for lymphatic vascular development as it promotes vascular endothelial growth factor C (VEGFC) proteolysis. A recent study reported that CCBE1 was overexpressed in epithelial colorectal cancer (CRC) cells; however, the role of CCBE1 in tumor lymphangiogenesis and the mechanism underlying dysregulated CCBE1 expression in CRC remain undefined.
The role of CCBE1 in tumor lymphangiogenesis and lymphatic metastasis was investigated using human lymphatic endothelial cells (HLECs) model
, and a hindfoot lymphatic metastasis model
. Immunochemistry analysis was performed to assess CCBE1 expression, prognostic value and correlation with clinicopathological characteristics in CRC. The biochemical function and transcriptional regulatory mechanism of CCBE1 were explored by western blot, qPCR, and chromatin immunoprecipitation.
: Cancer cell-derived CCBE1 enhances VEGFC proteolysis
, facilitates tube formation and migration of HLECs
, and promotes tumor lymphangiogenesis and lymphatic metastasis
. In addition to CRC cells, tumor stroma within CRC tissue shows high CCBE1 expression, which is associated with high lymphatic vessel density, increased lymph node metastasis and poor prognosis. Cancer-associated fibroblasts (CAFs) express and secret CCBE1, thereby contributing to VEGFC maturation and tumor lymphangiogenesis in CRC. Transforming growth factor beta (TGF-β) downregulates the transcription and lymphangiogenic function of CCBE1 in CAFs and CRC cells through direct binding of SMADs to CCBE1 gene locus. Inactivation of the TGF-β pathway correlates with increased CCBE1 expression in CRC.
: Our results demonstrate the protumorigenic role of CCBE1 in promoting lymphangiogenesis and lymphatic metastasis in CRC, revealing a new mechanism by which loss of TGF-β signaling promotes CRC metastasis.</description><subject>Aged</subject><subject>Animals</subject><subject>Calcium-Binding Proteins - metabolism</subject><subject>Cancer-Associated Fibroblasts - metabolism</subject><subject>Colorectal cancer</subject><subject>Colorectal Neoplasms - metabolism</subject><subject>Colorectal Neoplasms - pathology</subject><subject>Endothelial Cells - metabolism</subject><subject>Female</subject><subject>Growth factors</subject><subject>HCT116 Cells</subject><subject>Humans</subject><subject>Lymphangiogenesis</subject><subject>Lymphatic Metastasis - pathology</subject><subject>Lymphatic system</subject><subject>Male</subject><subject>Medical prognosis</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Proteins</subject><subject>Research Paper</subject><subject>Signal Transduction</subject><subject>Transforming Growth Factor beta - metabolism</subject><subject>Tumor Suppressor Proteins - metabolism</subject><subject>Tumors</subject><subject>Vascular Endothelial Growth Factor C - metabolism</subject><issn>1838-7640</issn><issn>1838-7640</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</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><recordid>eNpdkctqHDEQRZsQExvHG39AEGQTAuPordEmkAx-BAze2GuhUVf3aFBLE0ltmN_Kh-SbIscPnNSmCurU5VK3604JPlNE4C91E9MZ04rjN90RWbLlQkmO376aD7uTUra4FcdUE_2uO2QUL9uJOOq2q9X3c4J2OU2pQkF1nlJGYT_tNjaOPo0QofiCbOxRaxFGW_09hD3KMM7BVujReo9uLy9-_0LFj9EGH0fkI3IppAyu2oCcjQ7y--5gsKHAyVM_7u4uzm9XV4vrm8sfq2_XC8exrIteY-DMckJoc9nbAZzrmdJMgqBUc0akwGoQXNJ1TwanOTDg60ENvcQUM3bcfX3U3c3rCXoHsWYbzC77yea9SdabfzfRb8yY7o3CRBOhmsCnJ4Gcfs5Qqpl8cRCCjZDmYiiTDAslJW3ox__QbZpze0KjhF5SwTUWjfr8SLmcSskwvJgh2DykaB5SNH9TbPCH1_Zf0OfM2B-jlJn6</recordid><startdate>20200101</startdate><enddate>20200101</enddate><creator>Song, Jinglue</creator><creator>Chen, Wei</creator><creator>Cui, Xuewei</creator><creator>Huang, Zhenyu</creator><creator>Wen, Dongpeng</creator><creator>Yang, Yili</creator><creator>Yu, Wei</creator><creator>Cui, Long</creator><creator>Liu, Chen-Ying</creator><general>Ivyspring International Publisher Pty Ltd</general><general>Ivyspring International Publisher</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20200101</creationdate><title>CCBE1 promotes tumor lymphangiogenesis and is negatively regulated by TGFβ signaling in colorectal cancer</title><author>Song, Jinglue ; Chen, Wei ; Cui, Xuewei ; Huang, Zhenyu ; Wen, Dongpeng ; Yang, Yili ; Yu, Wei ; Cui, Long ; Liu, Chen-Ying</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c406t-d90e43a4112208dafeccd37936e52294316507f5462bd1fc94e3e4bf7fd602033</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Aged</topic><topic>Animals</topic><topic>Calcium-Binding Proteins - metabolism</topic><topic>Cancer-Associated Fibroblasts - metabolism</topic><topic>Colorectal cancer</topic><topic>Colorectal Neoplasms - metabolism</topic><topic>Colorectal Neoplasms - pathology</topic><topic>Endothelial Cells - metabolism</topic><topic>Female</topic><topic>Growth factors</topic><topic>HCT116 Cells</topic><topic>Humans</topic><topic>Lymphangiogenesis</topic><topic>Lymphatic Metastasis - pathology</topic><topic>Lymphatic system</topic><topic>Male</topic><topic>Medical prognosis</topic><topic>Metastasis</topic><topic>Mice</topic><topic>Proteins</topic><topic>Research Paper</topic><topic>Signal Transduction</topic><topic>Transforming Growth Factor beta - metabolism</topic><topic>Tumor Suppressor Proteins - metabolism</topic><topic>Tumors</topic><topic>Vascular Endothelial Growth Factor C - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Song, Jinglue</creatorcontrib><creatorcontrib>Chen, Wei</creatorcontrib><creatorcontrib>Cui, Xuewei</creatorcontrib><creatorcontrib>Huang, Zhenyu</creatorcontrib><creatorcontrib>Wen, Dongpeng</creatorcontrib><creatorcontrib>Yang, Yili</creatorcontrib><creatorcontrib>Yu, Wei</creatorcontrib><creatorcontrib>Cui, Long</creatorcontrib><creatorcontrib>Liu, Chen-Ying</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</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 Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Theranostics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Song, Jinglue</au><au>Chen, Wei</au><au>Cui, Xuewei</au><au>Huang, Zhenyu</au><au>Wen, Dongpeng</au><au>Yang, Yili</au><au>Yu, Wei</au><au>Cui, Long</au><au>Liu, Chen-Ying</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>CCBE1 promotes tumor lymphangiogenesis and is negatively regulated by TGFβ signaling in colorectal cancer</atitle><jtitle>Theranostics</jtitle><addtitle>Theranostics</addtitle><date>2020-01-01</date><risdate>2020</risdate><volume>10</volume><issue>5</issue><spage>2327</spage><epage>2341</epage><pages>2327-2341</pages><issn>1838-7640</issn><eissn>1838-7640</eissn><abstract>Collagen and calcium-binding EGF domain-1 (CCBE1) is essential for lymphatic vascular development as it promotes vascular endothelial growth factor C (VEGFC) proteolysis. A recent study reported that CCBE1 was overexpressed in epithelial colorectal cancer (CRC) cells; however, the role of CCBE1 in tumor lymphangiogenesis and the mechanism underlying dysregulated CCBE1 expression in CRC remain undefined.
The role of CCBE1 in tumor lymphangiogenesis and lymphatic metastasis was investigated using human lymphatic endothelial cells (HLECs) model
, and a hindfoot lymphatic metastasis model
. Immunochemistry analysis was performed to assess CCBE1 expression, prognostic value and correlation with clinicopathological characteristics in CRC. The biochemical function and transcriptional regulatory mechanism of CCBE1 were explored by western blot, qPCR, and chromatin immunoprecipitation.
: Cancer cell-derived CCBE1 enhances VEGFC proteolysis
, facilitates tube formation and migration of HLECs
, and promotes tumor lymphangiogenesis and lymphatic metastasis
. In addition to CRC cells, tumor stroma within CRC tissue shows high CCBE1 expression, which is associated with high lymphatic vessel density, increased lymph node metastasis and poor prognosis. Cancer-associated fibroblasts (CAFs) express and secret CCBE1, thereby contributing to VEGFC maturation and tumor lymphangiogenesis in CRC. Transforming growth factor beta (TGF-β) downregulates the transcription and lymphangiogenic function of CCBE1 in CAFs and CRC cells through direct binding of SMADs to CCBE1 gene locus. Inactivation of the TGF-β pathway correlates with increased CCBE1 expression in CRC.
: Our results demonstrate the protumorigenic role of CCBE1 in promoting lymphangiogenesis and lymphatic metastasis in CRC, revealing a new mechanism by which loss of TGF-β signaling promotes CRC metastasis.</abstract><cop>Australia</cop><pub>Ivyspring International Publisher Pty Ltd</pub><pmid>32089745</pmid><doi>10.7150/thno.39740</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; PubMed Central |
| subjects | Aged Animals Calcium-Binding Proteins - metabolism Cancer-Associated Fibroblasts - metabolism Colorectal cancer Colorectal Neoplasms - metabolism Colorectal Neoplasms - pathology Endothelial Cells - metabolism Female Growth factors HCT116 Cells Humans Lymphangiogenesis Lymphatic Metastasis - pathology Lymphatic system Male Medical prognosis Metastasis Mice Proteins Research Paper Signal Transduction Transforming Growth Factor beta - metabolism Tumor Suppressor Proteins - metabolism Tumors Vascular Endothelial Growth Factor C - metabolism |
| title | CCBE1 promotes tumor lymphangiogenesis and is negatively regulated by TGFβ signaling in colorectal cancer |
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