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Recycling Endosomes in Mature Epithelia Restrain Tumorigenic Signaling
The effects of polarized membrane trafficking in mature epithelial tissue on cell growth and cancer progression have not been fully explored . A majority of colorectal cancers have reduced and mislocalized Rab11, a small GTPase dedicated to trafficking of recycling endosomes. Patients with low Rab11...
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| Published in: | Cancer research (Chicago, Ill.) Ill.), 2019-08, Vol.79 (16), p.4099-4112 |
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| creator | D'Agostino, Luca Nie, Yingchao Goswami, Sayantani Tong, Kevin Yu, Shiyan Bandyopadhyay, Sheila Flores, Juan Zhang, Xiao Balasubramanian, Iyshwarya Joseph, Ivor Sakamori, Ryotaro Farrell, Victoria Li, Qi Yang, Chung S Gao, Bin Ferraris, Ronaldo P Yehia, Ghassan Bonder, Edward M Goldenring, James R Verzi, Michael P Zhang, Lanjing Ip, Y Tony Gao, Nan |
| description | The effects of polarized membrane trafficking in mature epithelial tissue on cell growth and cancer progression have not been fully explored
. A majority of colorectal cancers have reduced and mislocalized Rab11, a small GTPase dedicated to trafficking of recycling endosomes. Patients with low Rab11 protein expression have poor survival rates. Using genetic models across species, we show that intact recycling endosome function restrains aberrant epithelial growth elicited by APC or RAS mutations. Loss of Rab11 protein led to epithelial dysplasia in early animal development and synergized with oncogenic pathways to accelerate tumor progression initiated by carcinogen, genetic mutation, or aging. Transcriptomic analysis uncovered an immediate expansion of the intestinal stem cell pool along with cell-autonomous Yki/Yap activation following disruption of Rab11a-mediated recycling endosomes. Intestinal tumors lacking Rab11a traffic exhibited marked elevation of nuclear Yap, upd3/IL6-Stat3, and amphiregulin-MAPK signaling, whereas suppression of Yki/Yap or upd3/IL6 reduced gut epithelial dysplasia and hyperplasia. Examination of Rab11a function in enteroids or cultured cell lines suggested that this endosome unit is required for suppression of the Yap pathway by Hippo kinases. Thus, recycling endosomes in mature epithelia constitute key tumor suppressors, loss of which accelerates carcinogenesis. SIGNIFICANCE: Recycling endosome traffic in mature epithelia constitutes a novel tumor suppressing mechanism. |
| doi_str_mv | 10.1158/0008-5472.can-18-4075 |
| format | article |
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. A majority of colorectal cancers have reduced and mislocalized Rab11, a small GTPase dedicated to trafficking of recycling endosomes. Patients with low Rab11 protein expression have poor survival rates. Using genetic models across species, we show that intact recycling endosome function restrains aberrant epithelial growth elicited by APC or RAS mutations. Loss of Rab11 protein led to epithelial dysplasia in early animal development and synergized with oncogenic pathways to accelerate tumor progression initiated by carcinogen, genetic mutation, or aging. Transcriptomic analysis uncovered an immediate expansion of the intestinal stem cell pool along with cell-autonomous Yki/Yap activation following disruption of Rab11a-mediated recycling endosomes. Intestinal tumors lacking Rab11a traffic exhibited marked elevation of nuclear Yap, upd3/IL6-Stat3, and amphiregulin-MAPK signaling, whereas suppression of Yki/Yap or upd3/IL6 reduced gut epithelial dysplasia and hyperplasia. Examination of Rab11a function in enteroids or cultured cell lines suggested that this endosome unit is required for suppression of the Yap pathway by Hippo kinases. Thus, recycling endosomes in mature epithelia constitute key tumor suppressors, loss of which accelerates carcinogenesis. SIGNIFICANCE: Recycling endosome traffic in mature epithelia constitutes a novel tumor suppressing mechanism.</description><identifier>ISSN: 0008-5472</identifier><identifier>EISSN: 1538-7445</identifier><identifier>DOI: 10.1158/0008-5472.can-18-4075</identifier><identifier>PMID: 31239271</identifier><language>eng</language><publisher>United States</publisher><subject>Adenomatous Polyposis Coli Protein - genetics ; Animals ; Animals, Genetically Modified ; Colorectal Neoplasms - metabolism ; Colorectal Neoplasms - mortality ; Colorectal Neoplasms - pathology ; Endosomes - metabolism ; Epithelial Cells - metabolism ; Epithelial Cells - pathology ; Humans ; Mice, Knockout ; Protein-Serine-Threonine Kinases - metabolism ; rab GTP-Binding Proteins - genetics ; rab GTP-Binding Proteins - metabolism ; Stem Cells - metabolism ; Stem Cells - pathology</subject><ispartof>Cancer research (Chicago, Ill.), 2019-08, Vol.79 (16), p.4099-4112</ispartof><rights>2019 American Association for Cancer Research.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c477t-33803e1f8b55f4fa3894977c03d243a978dba6ed5b634e50e8b150155e3c81133</citedby><cites>FETCH-LOGICAL-c477t-33803e1f8b55f4fa3894977c03d243a978dba6ed5b634e50e8b150155e3c81133</cites><orcidid>0000-0002-7833-2940 ; 0000-0002-1580-607X ; 0000-0001-6713-4837 ; 0000-0001-5436-887X ; 0000-0002-8213-6686 ; 0000-0002-9834-6012 ; 0000-0001-6151-0811</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31239271$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>D'Agostino, Luca</creatorcontrib><creatorcontrib>Nie, Yingchao</creatorcontrib><creatorcontrib>Goswami, Sayantani</creatorcontrib><creatorcontrib>Tong, Kevin</creatorcontrib><creatorcontrib>Yu, Shiyan</creatorcontrib><creatorcontrib>Bandyopadhyay, Sheila</creatorcontrib><creatorcontrib>Flores, Juan</creatorcontrib><creatorcontrib>Zhang, Xiao</creatorcontrib><creatorcontrib>Balasubramanian, Iyshwarya</creatorcontrib><creatorcontrib>Joseph, Ivor</creatorcontrib><creatorcontrib>Sakamori, Ryotaro</creatorcontrib><creatorcontrib>Farrell, Victoria</creatorcontrib><creatorcontrib>Li, Qi</creatorcontrib><creatorcontrib>Yang, Chung S</creatorcontrib><creatorcontrib>Gao, Bin</creatorcontrib><creatorcontrib>Ferraris, Ronaldo P</creatorcontrib><creatorcontrib>Yehia, Ghassan</creatorcontrib><creatorcontrib>Bonder, Edward M</creatorcontrib><creatorcontrib>Goldenring, James R</creatorcontrib><creatorcontrib>Verzi, Michael P</creatorcontrib><creatorcontrib>Zhang, Lanjing</creatorcontrib><creatorcontrib>Ip, Y Tony</creatorcontrib><creatorcontrib>Gao, Nan</creatorcontrib><title>Recycling Endosomes in Mature Epithelia Restrain Tumorigenic Signaling</title><title>Cancer research (Chicago, Ill.)</title><addtitle>Cancer Res</addtitle><description>The effects of polarized membrane trafficking in mature epithelial tissue on cell growth and cancer progression have not been fully explored
. A majority of colorectal cancers have reduced and mislocalized Rab11, a small GTPase dedicated to trafficking of recycling endosomes. Patients with low Rab11 protein expression have poor survival rates. Using genetic models across species, we show that intact recycling endosome function restrains aberrant epithelial growth elicited by APC or RAS mutations. Loss of Rab11 protein led to epithelial dysplasia in early animal development and synergized with oncogenic pathways to accelerate tumor progression initiated by carcinogen, genetic mutation, or aging. Transcriptomic analysis uncovered an immediate expansion of the intestinal stem cell pool along with cell-autonomous Yki/Yap activation following disruption of Rab11a-mediated recycling endosomes. Intestinal tumors lacking Rab11a traffic exhibited marked elevation of nuclear Yap, upd3/IL6-Stat3, and amphiregulin-MAPK signaling, whereas suppression of Yki/Yap or upd3/IL6 reduced gut epithelial dysplasia and hyperplasia. Examination of Rab11a function in enteroids or cultured cell lines suggested that this endosome unit is required for suppression of the Yap pathway by Hippo kinases. Thus, recycling endosomes in mature epithelia constitute key tumor suppressors, loss of which accelerates carcinogenesis. SIGNIFICANCE: Recycling endosome traffic in mature epithelia constitutes a novel tumor suppressing mechanism.</description><subject>Adenomatous Polyposis Coli Protein - genetics</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Colorectal Neoplasms - metabolism</subject><subject>Colorectal Neoplasms - mortality</subject><subject>Colorectal Neoplasms - pathology</subject><subject>Endosomes - metabolism</subject><subject>Epithelial Cells - metabolism</subject><subject>Epithelial Cells - pathology</subject><subject>Humans</subject><subject>Mice, Knockout</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>rab GTP-Binding Proteins - genetics</subject><subject>rab GTP-Binding Proteins - metabolism</subject><subject>Stem Cells - metabolism</subject><subject>Stem Cells - pathology</subject><issn>0008-5472</issn><issn>1538-7445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><recordid>eNpVkGFLwzAQhoMobk5_gtI_kJlrkib9IoyxqTAV5vwc0jTtIm06mk7Yv7dlOvTTcdw97x0PQrdApgBc3hNCJOZMxFOjPQaJGRH8DI2BU4kFY_wcjU87I3QVwmffciD8Eo0oxDSNBYzRcm3NwVTOl9HC501oahsi56MX3e1bGy12rtvayulobUPX6n6y2ddN60rrnYneXen1AF-ji0JXwd781An6WC428ye8ent8ns9W2DAhOkypJNRCITPOC1ZoKlOWCmEIzWNGdSpknunE5jxLKLOcWJkBJ8C5pUYCUDpBD8fc3T6rbW6s75-q1K51tW4PqtFO_Z94t1Vl86USEScsZX0APwaYtgmhtcWJBaIGsWqQpgZpaj57VSDVILbn7v4ePlG_Juk3MqF1nw</recordid><startdate>20190815</startdate><enddate>20190815</enddate><creator>D'Agostino, Luca</creator><creator>Nie, Yingchao</creator><creator>Goswami, Sayantani</creator><creator>Tong, Kevin</creator><creator>Yu, Shiyan</creator><creator>Bandyopadhyay, Sheila</creator><creator>Flores, Juan</creator><creator>Zhang, Xiao</creator><creator>Balasubramanian, Iyshwarya</creator><creator>Joseph, Ivor</creator><creator>Sakamori, Ryotaro</creator><creator>Farrell, Victoria</creator><creator>Li, Qi</creator><creator>Yang, Chung S</creator><creator>Gao, Bin</creator><creator>Ferraris, Ronaldo P</creator><creator>Yehia, Ghassan</creator><creator>Bonder, Edward M</creator><creator>Goldenring, James R</creator><creator>Verzi, Michael P</creator><creator>Zhang, Lanjing</creator><creator>Ip, Y Tony</creator><creator>Gao, Nan</creator><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>5PM</scope><orcidid>https://orcid.org/0000-0002-7833-2940</orcidid><orcidid>https://orcid.org/0000-0002-1580-607X</orcidid><orcidid>https://orcid.org/0000-0001-6713-4837</orcidid><orcidid>https://orcid.org/0000-0001-5436-887X</orcidid><orcidid>https://orcid.org/0000-0002-8213-6686</orcidid><orcidid>https://orcid.org/0000-0002-9834-6012</orcidid><orcidid>https://orcid.org/0000-0001-6151-0811</orcidid></search><sort><creationdate>20190815</creationdate><title>Recycling Endosomes in Mature Epithelia Restrain Tumorigenic Signaling</title><author>D'Agostino, Luca ; 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. A majority of colorectal cancers have reduced and mislocalized Rab11, a small GTPase dedicated to trafficking of recycling endosomes. Patients with low Rab11 protein expression have poor survival rates. Using genetic models across species, we show that intact recycling endosome function restrains aberrant epithelial growth elicited by APC or RAS mutations. Loss of Rab11 protein led to epithelial dysplasia in early animal development and synergized with oncogenic pathways to accelerate tumor progression initiated by carcinogen, genetic mutation, or aging. Transcriptomic analysis uncovered an immediate expansion of the intestinal stem cell pool along with cell-autonomous Yki/Yap activation following disruption of Rab11a-mediated recycling endosomes. Intestinal tumors lacking Rab11a traffic exhibited marked elevation of nuclear Yap, upd3/IL6-Stat3, and amphiregulin-MAPK signaling, whereas suppression of Yki/Yap or upd3/IL6 reduced gut epithelial dysplasia and hyperplasia. Examination of Rab11a function in enteroids or cultured cell lines suggested that this endosome unit is required for suppression of the Yap pathway by Hippo kinases. Thus, recycling endosomes in mature epithelia constitute key tumor suppressors, loss of which accelerates carcinogenesis. SIGNIFICANCE: Recycling endosome traffic in mature epithelia constitutes a novel tumor suppressing mechanism.</abstract><cop>United States</cop><pmid>31239271</pmid><doi>10.1158/0008-5472.can-18-4075</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-7833-2940</orcidid><orcidid>https://orcid.org/0000-0002-1580-607X</orcidid><orcidid>https://orcid.org/0000-0001-6713-4837</orcidid><orcidid>https://orcid.org/0000-0001-5436-887X</orcidid><orcidid>https://orcid.org/0000-0002-8213-6686</orcidid><orcidid>https://orcid.org/0000-0002-9834-6012</orcidid><orcidid>https://orcid.org/0000-0001-6151-0811</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Cancer research (Chicago, Ill.), 2019-08, Vol.79 (16), p.4099-4112 |
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| subjects | Adenomatous Polyposis Coli Protein - genetics Animals Animals, Genetically Modified Colorectal Neoplasms - metabolism Colorectal Neoplasms - mortality Colorectal Neoplasms - pathology Endosomes - metabolism Epithelial Cells - metabolism Epithelial Cells - pathology Humans Mice, Knockout Protein-Serine-Threonine Kinases - metabolism rab GTP-Binding Proteins - genetics rab GTP-Binding Proteins - metabolism Stem Cells - metabolism Stem Cells - pathology |
| title | Recycling Endosomes in Mature Epithelia Restrain Tumorigenic Signaling |
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