Epidermal Snail expression drives skin cancer initiation and progression through enhanced cytoprotection, epidermal stem/progenitor cell expansion and enhanced metastatic potential
Expression of the EMT-inducing transcription factor Snail is enhanced in different human cancers. To investigate the in vivo role of Snail during progression of epithelial cancer, we used a mouse model with skin-specific overexpression of Snail. Snail transgenic mice spontaneously developed distinct...
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| Veröffentlicht in: | Cell death and differentiation 2014-02, Vol.21 (2), p.310-320 |
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| creator | De Craene, B Denecker, G Vermassen, P Taminau, J Mauch, C Derore, A Jonkers, J Fuchs, E Berx, G |
| description | Expression of the EMT-inducing transcription factor Snail is enhanced in different human cancers. To investigate the
in vivo
role of Snail during progression of epithelial cancer, we used a mouse model with skin-specific overexpression of Snail. Snail transgenic mice spontaneously developed distinct histological subtypes of skin cancer, such as basal cell carcinoma, squamous cell carcinoma and sebaceous gland carcinoma. Development of sebaceous gland carcinomas strongly correlated with the direct and complete repression of Blimp-1, a central regulator of sebocyte homeostasis. Snail expression in keratinocyte stem cells significantly promotes their proliferation associated with an activated FoxM1 gene expression signature, resulting in a larger pool of Mts24-marked progenitor cells. Furthermore, primary keratinocytes expressing Snail showed increased survival and strong resistance to genotoxic stress. Snail expression in a skin-specific p53-null background resulted in accelerated formation of spontaneous tumours and enhanced metastasis. Our data demonstrate that
in vivo
expression of Snail results in
de novo
epithelial carcinogenesis by allowing enhanced survival, expansion of the cancer stem cell pool with accumulated DNA damage, a block in terminal differentiation and increased proliferation rates of tumour-initiating cells. |
| doi_str_mv | 10.1038/cdd.2013.148 |
| format | Article |
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in vivo
role of Snail during progression of epithelial cancer, we used a mouse model with skin-specific overexpression of Snail. Snail transgenic mice spontaneously developed distinct histological subtypes of skin cancer, such as basal cell carcinoma, squamous cell carcinoma and sebaceous gland carcinoma. Development of sebaceous gland carcinomas strongly correlated with the direct and complete repression of Blimp-1, a central regulator of sebocyte homeostasis. Snail expression in keratinocyte stem cells significantly promotes their proliferation associated with an activated FoxM1 gene expression signature, resulting in a larger pool of Mts24-marked progenitor cells. Furthermore, primary keratinocytes expressing Snail showed increased survival and strong resistance to genotoxic stress. Snail expression in a skin-specific p53-null background resulted in accelerated formation of spontaneous tumours and enhanced metastasis. Our data demonstrate that
in vivo
expression of Snail results in
de novo
epithelial carcinogenesis by allowing enhanced survival, expansion of the cancer stem cell pool with accumulated DNA damage, a block in terminal differentiation and increased proliferation rates of tumour-initiating cells.</description><identifier>ISSN: 1350-9047</identifier><identifier>EISSN: 1476-5403</identifier><identifier>DOI: 10.1038/cdd.2013.148</identifier><identifier>PMID: 24162662</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/136/142 ; 631/67/1813 ; 631/67/322 ; 692/420/755 ; Animals ; Apoptosis ; Biochemistry ; Biomedical and Life Sciences ; Breast cancer ; Cell Biology ; Cell Cycle Analysis ; Cell death ; Cell Differentiation ; Cell Proliferation ; Disease Progression ; Humans ; Life Sciences ; Medical prognosis ; Metastasis ; Mice ; Mice, Transgenic ; Molecular biology ; Neoplasm Metastasis - genetics ; Neoplasm Metastasis - pathology ; Neoplastic Stem Cells - metabolism ; Neoplastic Stem Cells - pathology ; Oncology ; Original Paper ; Sebaceous Gland Neoplasms - genetics ; Sebaceous Gland Neoplasms - pathology ; Skin cancer ; Skin Neoplasms - genetics ; Skin Neoplasms - pathology ; Snail Family Transcription Factors ; Stem Cells ; Transcription factors ; Transcription Factors - genetics ; Transgenic animals ; Tumors</subject><ispartof>Cell death and differentiation, 2014-02, Vol.21 (2), p.310-320</ispartof><rights>Macmillan Publishers Limited 2014</rights><rights>Copyright Nature Publishing Group Feb 2014</rights><rights>Copyright © 2014 Macmillan Publishers Limited 2014 Macmillan Publishers Limited</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c450t-e6b6fa2578d581c243e2c0d45e8034459bf70ec430f06425577172ff8794b9853</citedby><cites>FETCH-LOGICAL-c450t-e6b6fa2578d581c243e2c0d45e8034459bf70ec430f06425577172ff8794b9853</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3890953/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3890953/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,41464,42533,51294,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24162662$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>De Craene, B</creatorcontrib><creatorcontrib>Denecker, G</creatorcontrib><creatorcontrib>Vermassen, P</creatorcontrib><creatorcontrib>Taminau, J</creatorcontrib><creatorcontrib>Mauch, C</creatorcontrib><creatorcontrib>Derore, A</creatorcontrib><creatorcontrib>Jonkers, J</creatorcontrib><creatorcontrib>Fuchs, E</creatorcontrib><creatorcontrib>Berx, G</creatorcontrib><title>Epidermal Snail expression drives skin cancer initiation and progression through enhanced cytoprotection, epidermal stem/progenitor cell expansion and enhanced metastatic potential</title><title>Cell death and differentiation</title><addtitle>Cell Death Differ</addtitle><addtitle>Cell Death Differ</addtitle><description>Expression of the EMT-inducing transcription factor Snail is enhanced in different human cancers. To investigate the
in vivo
role of Snail during progression of epithelial cancer, we used a mouse model with skin-specific overexpression of Snail. Snail transgenic mice spontaneously developed distinct histological subtypes of skin cancer, such as basal cell carcinoma, squamous cell carcinoma and sebaceous gland carcinoma. Development of sebaceous gland carcinomas strongly correlated with the direct and complete repression of Blimp-1, a central regulator of sebocyte homeostasis. Snail expression in keratinocyte stem cells significantly promotes their proliferation associated with an activated FoxM1 gene expression signature, resulting in a larger pool of Mts24-marked progenitor cells. Furthermore, primary keratinocytes expressing Snail showed increased survival and strong resistance to genotoxic stress. Snail expression in a skin-specific p53-null background resulted in accelerated formation of spontaneous tumours and enhanced metastasis. Our data demonstrate that
in vivo
expression of Snail results in
de novo
epithelial carcinogenesis by allowing enhanced survival, expansion of the cancer stem cell pool with accumulated DNA damage, a block in terminal differentiation and increased proliferation rates of tumour-initiating cells.</description><subject>631/136/142</subject><subject>631/67/1813</subject><subject>631/67/322</subject><subject>692/420/755</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Breast cancer</subject><subject>Cell Biology</subject><subject>Cell Cycle Analysis</subject><subject>Cell death</subject><subject>Cell Differentiation</subject><subject>Cell Proliferation</subject><subject>Disease Progression</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Medical prognosis</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Molecular biology</subject><subject>Neoplasm Metastasis - genetics</subject><subject>Neoplasm Metastasis - pathology</subject><subject>Neoplastic Stem Cells - metabolism</subject><subject>Neoplastic Stem Cells - pathology</subject><subject>Oncology</subject><subject>Original Paper</subject><subject>Sebaceous Gland Neoplasms - genetics</subject><subject>Sebaceous Gland Neoplasms - pathology</subject><subject>Skin cancer</subject><subject>Skin Neoplasms - genetics</subject><subject>Skin Neoplasms - pathology</subject><subject>Snail Family Transcription Factors</subject><subject>Stem Cells</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transgenic animals</subject><subject>Tumors</subject><issn>1350-9047</issn><issn>1476-5403</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNptkV1rFDEUhoMotlbvvJaAt51tMvmcG0FKtYWCF-p1yGbO7KbOJGOSLfZ_-QPNuN2lglcJnOc874EXobeUrChh-sL1_aollK0o18_QKeVKNoIT9rz-mSBNR7g6Qa9yviOESNXJl-ik5VS2Uran6PfV7HtIkx3x12D9iOHXnCBnHwPuk7-HjPMPH7CzwUHCPvjibVmmNvR4TnFzoMs2xd1miyFsF7bH7qHEChRwC3-O4ZiUC0wXyy5UXUzYwfg32IZ8MB8tExSbS410eK6uUOPH1-jFYMcMbx7fM_T909W3y-vm9svnm8uPt43jgpQG5FoOthVK90JT13IGrSM9F6AJ41x060ERcJyRgUjeCqEUVe0waNXxdacFO0Mf9t55t56gdzU92dHMyU82PZhovfl3EvzWbOK9YbojnWBV8P5RkOLPHeRi7uIuhXqzWXrSTHZ0iTnfUy7FnBMMxwRKzNKxqR2bpeO6pSv-7ulVR_hQagWaPZDrKGwgPUn9n_APN7C3WA</recordid><startdate>20140201</startdate><enddate>20140201</enddate><creator>De Craene, B</creator><creator>Denecker, G</creator><creator>Vermassen, P</creator><creator>Taminau, J</creator><creator>Mauch, C</creator><creator>Derore, A</creator><creator>Jonkers, J</creator><creator>Fuchs, E</creator><creator>Berx, G</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>7QP</scope><scope>7QR</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</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>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>5PM</scope></search><sort><creationdate>20140201</creationdate><title>Epidermal Snail expression drives skin cancer initiation and progression through enhanced cytoprotection, epidermal stem/progenitor cell expansion and enhanced metastatic potential</title><author>De Craene, B ; Denecker, G ; Vermassen, P ; Taminau, J ; Mauch, C ; Derore, A ; Jonkers, J ; Fuchs, E ; Berx, G</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c450t-e6b6fa2578d581c243e2c0d45e8034459bf70ec430f06425577172ff8794b9853</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>631/136/142</topic><topic>631/67/1813</topic><topic>631/67/322</topic><topic>692/420/755</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Biochemistry</topic><topic>Biomedical and Life Sciences</topic><topic>Breast cancer</topic><topic>Cell Biology</topic><topic>Cell Cycle Analysis</topic><topic>Cell death</topic><topic>Cell Differentiation</topic><topic>Cell Proliferation</topic><topic>Disease Progression</topic><topic>Humans</topic><topic>Life Sciences</topic><topic>Medical prognosis</topic><topic>Metastasis</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>Molecular biology</topic><topic>Neoplasm Metastasis - genetics</topic><topic>Neoplasm Metastasis - pathology</topic><topic>Neoplastic Stem Cells - metabolism</topic><topic>Neoplastic Stem Cells - pathology</topic><topic>Oncology</topic><topic>Original Paper</topic><topic>Sebaceous Gland Neoplasms - genetics</topic><topic>Sebaceous Gland Neoplasms - pathology</topic><topic>Skin cancer</topic><topic>Skin Neoplasms - genetics</topic><topic>Skin Neoplasms - pathology</topic><topic>Snail Family Transcription Factors</topic><topic>Stem Cells</topic><topic>Transcription factors</topic><topic>Transcription Factors - genetics</topic><topic>Transgenic animals</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>De Craene, B</creatorcontrib><creatorcontrib>Denecker, G</creatorcontrib><creatorcontrib>Vermassen, P</creatorcontrib><creatorcontrib>Taminau, J</creatorcontrib><creatorcontrib>Mauch, C</creatorcontrib><creatorcontrib>Derore, A</creatorcontrib><creatorcontrib>Jonkers, J</creatorcontrib><creatorcontrib>Fuchs, E</creatorcontrib><creatorcontrib>Berx, G</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>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</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>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</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>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell death and differentiation</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>De Craene, B</au><au>Denecker, G</au><au>Vermassen, P</au><au>Taminau, J</au><au>Mauch, C</au><au>Derore, A</au><au>Jonkers, J</au><au>Fuchs, E</au><au>Berx, G</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Epidermal Snail expression drives skin cancer initiation and progression through enhanced cytoprotection, epidermal stem/progenitor cell expansion and enhanced metastatic potential</atitle><jtitle>Cell death and differentiation</jtitle><stitle>Cell Death Differ</stitle><addtitle>Cell Death Differ</addtitle><date>2014-02-01</date><risdate>2014</risdate><volume>21</volume><issue>2</issue><spage>310</spage><epage>320</epage><pages>310-320</pages><issn>1350-9047</issn><eissn>1476-5403</eissn><abstract>Expression of the EMT-inducing transcription factor Snail is enhanced in different human cancers. To investigate the
in vivo
role of Snail during progression of epithelial cancer, we used a mouse model with skin-specific overexpression of Snail. Snail transgenic mice spontaneously developed distinct histological subtypes of skin cancer, such as basal cell carcinoma, squamous cell carcinoma and sebaceous gland carcinoma. Development of sebaceous gland carcinomas strongly correlated with the direct and complete repression of Blimp-1, a central regulator of sebocyte homeostasis. Snail expression in keratinocyte stem cells significantly promotes their proliferation associated with an activated FoxM1 gene expression signature, resulting in a larger pool of Mts24-marked progenitor cells. Furthermore, primary keratinocytes expressing Snail showed increased survival and strong resistance to genotoxic stress. Snail expression in a skin-specific p53-null background resulted in accelerated formation of spontaneous tumours and enhanced metastasis. Our data demonstrate that
in vivo
expression of Snail results in
de novo
epithelial carcinogenesis by allowing enhanced survival, expansion of the cancer stem cell pool with accumulated DNA damage, a block in terminal differentiation and increased proliferation rates of tumour-initiating cells.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>24162662</pmid><doi>10.1038/cdd.2013.148</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 631/136/142 631/67/1813 631/67/322 692/420/755 Animals Apoptosis Biochemistry Biomedical and Life Sciences Breast cancer Cell Biology Cell Cycle Analysis Cell death Cell Differentiation Cell Proliferation Disease Progression Humans Life Sciences Medical prognosis Metastasis Mice Mice, Transgenic Molecular biology Neoplasm Metastasis - genetics Neoplasm Metastasis - pathology Neoplastic Stem Cells - metabolism Neoplastic Stem Cells - pathology Oncology Original Paper Sebaceous Gland Neoplasms - genetics Sebaceous Gland Neoplasms - pathology Skin cancer Skin Neoplasms - genetics Skin Neoplasms - pathology Snail Family Transcription Factors Stem Cells Transcription factors Transcription Factors - genetics Transgenic animals Tumors |
| title | Epidermal Snail expression drives skin cancer initiation and progression through enhanced cytoprotection, epidermal stem/progenitor cell expansion and enhanced metastatic potential |
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