MicroRNA-214 controls skin and hair follicle development by modulating the activity of the Wnt pathway
Skin development is governed by complex programs of gene activation and silencing, including microRNA-dependent modulation of gene expression. Here, we show that miR-214 regulates skin morphogenesis and hair follicle (HF) cycling by targeting β-catenin, a key component of the Wnt signaling pathway....
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| Veröffentlicht in: | The Journal of cell biology 2014-11, Vol.207 (4), p.549-567 |
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| container_title | The Journal of cell biology |
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| creator | Ahmed, Mohammed I Alam, Majid Emelianov, Vladimir U Poterlowicz, Krzysztof Patel, Ankit Sharov, Andrey A Mardaryev, Andrei N Botchkareva, Natalia V |
| description | Skin development is governed by complex programs of gene activation and silencing, including microRNA-dependent modulation of gene expression. Here, we show that miR-214 regulates skin morphogenesis and hair follicle (HF) cycling by targeting β-catenin, a key component of the Wnt signaling pathway. miR-214 exhibits differential expression patterns in the skin epithelium, and its inducible overexpression in keratinocytes inhibited proliferation, which resulted in formation of fewer HFs with decreased hair bulb size and thinner hair production. The inhibitory effects of miR-214 on HF development and cycling were associated with altered activities of multiple signaling pathways, including decreased expression of key Wnt signaling mediators β-catenin and Lef-1, and were rescued by treatment with pharmacological Wnt activators. Finally, we identify β-catenin as one of the conserved miR-214 targets in keratinocytes. These data provide an important foundation for further analyses of miR-214 as a key regulator of Wnt pathway activity and stem cell functions during normal tissue homeostasis, regeneration, and aging. |
| doi_str_mv | 10.1083/jcb.201404001 |
| format | Article |
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Here, we show that miR-214 regulates skin morphogenesis and hair follicle (HF) cycling by targeting β-catenin, a key component of the Wnt signaling pathway. miR-214 exhibits differential expression patterns in the skin epithelium, and its inducible overexpression in keratinocytes inhibited proliferation, which resulted in formation of fewer HFs with decreased hair bulb size and thinner hair production. The inhibitory effects of miR-214 on HF development and cycling were associated with altered activities of multiple signaling pathways, including decreased expression of key Wnt signaling mediators β-catenin and Lef-1, and were rescued by treatment with pharmacological Wnt activators. Finally, we identify β-catenin as one of the conserved miR-214 targets in keratinocytes. These data provide an important foundation for further analyses of miR-214 as a key regulator of Wnt pathway activity and stem cell functions during normal tissue homeostasis, regeneration, and aging.</description><identifier>ISSN: 0021-9525</identifier><identifier>EISSN: 1540-8140</identifier><identifier>DOI: 10.1083/jcb.201404001</identifier><identifier>PMID: 25422376</identifier><identifier>CODEN: JCLBA3</identifier><language>eng</language><publisher>United States: Rockefeller University Press</publisher><subject>Animals ; beta Catenin - biosynthesis ; beta Catenin - genetics ; Cell Differentiation - physiology ; Cells, Cultured ; Cellular Senescence - genetics ; Genotype ; Hair ; Hair Follicle - growth & development ; Hair Follicle - metabolism ; Homeostasis ; Keratin-10 - biosynthesis ; Keratin-14 - biosynthesis ; Keratinocytes - cytology ; Lymphoid Enhancer-Binding Factor 1 - biosynthesis ; Lymphoid Enhancer-Binding Factor 1 - genetics ; Membrane Proteins - biosynthesis ; Mice ; Mice, Transgenic ; MicroRNAs ; MicroRNAs - genetics ; MicroRNAs - physiology ; Morphogenesis ; Protein expression ; Regeneration - genetics ; Signal transduction ; Skin ; Skin - growth & development ; Skin - metabolism ; Wnt Proteins - genetics ; Wnt Proteins - metabolism ; Wnt Signaling Pathway</subject><ispartof>The Journal of cell biology, 2014-11, Vol.207 (4), p.549-567</ispartof><rights>2014 Ahmed et al.</rights><rights>Copyright Rockefeller University Press Nov 24, 2014</rights><rights>2014 Ahmed et al. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c481t-43abce548d087e406d485c30378022f2e0698dd7acd1965385db76e717729c13</citedby><cites>FETCH-LOGICAL-c481t-43abce548d087e406d485c30378022f2e0698dd7acd1965385db76e717729c13</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25422376$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ahmed, Mohammed I</creatorcontrib><creatorcontrib>Alam, Majid</creatorcontrib><creatorcontrib>Emelianov, Vladimir U</creatorcontrib><creatorcontrib>Poterlowicz, Krzysztof</creatorcontrib><creatorcontrib>Patel, Ankit</creatorcontrib><creatorcontrib>Sharov, Andrey A</creatorcontrib><creatorcontrib>Mardaryev, Andrei N</creatorcontrib><creatorcontrib>Botchkareva, Natalia V</creatorcontrib><title>MicroRNA-214 controls skin and hair follicle development by modulating the activity of the Wnt pathway</title><title>The Journal of cell biology</title><addtitle>J Cell Biol</addtitle><description>Skin development is governed by complex programs of gene activation and silencing, including microRNA-dependent modulation of gene expression. Here, we show that miR-214 regulates skin morphogenesis and hair follicle (HF) cycling by targeting β-catenin, a key component of the Wnt signaling pathway. miR-214 exhibits differential expression patterns in the skin epithelium, and its inducible overexpression in keratinocytes inhibited proliferation, which resulted in formation of fewer HFs with decreased hair bulb size and thinner hair production. The inhibitory effects of miR-214 on HF development and cycling were associated with altered activities of multiple signaling pathways, including decreased expression of key Wnt signaling mediators β-catenin and Lef-1, and were rescued by treatment with pharmacological Wnt activators. Finally, we identify β-catenin as one of the conserved miR-214 targets in keratinocytes. These data provide an important foundation for further analyses of miR-214 as a key regulator of Wnt pathway activity and stem cell functions during normal tissue homeostasis, regeneration, and aging.</description><subject>Animals</subject><subject>beta Catenin - biosynthesis</subject><subject>beta Catenin - genetics</subject><subject>Cell Differentiation - physiology</subject><subject>Cells, Cultured</subject><subject>Cellular Senescence - genetics</subject><subject>Genotype</subject><subject>Hair</subject><subject>Hair Follicle - growth & development</subject><subject>Hair Follicle - metabolism</subject><subject>Homeostasis</subject><subject>Keratin-10 - biosynthesis</subject><subject>Keratin-14 - biosynthesis</subject><subject>Keratinocytes - cytology</subject><subject>Lymphoid Enhancer-Binding Factor 1 - biosynthesis</subject><subject>Lymphoid Enhancer-Binding Factor 1 - genetics</subject><subject>Membrane Proteins - biosynthesis</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>MicroRNAs</subject><subject>MicroRNAs - genetics</subject><subject>MicroRNAs - physiology</subject><subject>Morphogenesis</subject><subject>Protein expression</subject><subject>Regeneration - genetics</subject><subject>Signal transduction</subject><subject>Skin</subject><subject>Skin - growth & development</subject><subject>Skin - metabolism</subject><subject>Wnt Proteins - genetics</subject><subject>Wnt Proteins - metabolism</subject><subject>Wnt Signaling Pathway</subject><issn>0021-9525</issn><issn>1540-8140</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkd9rFDEQx4Mo9jx99FUCvviydfJjN9kXoRSrQm1BCj6GbJLt5cxuziR75f57U1sP9WkY5sN85ztfhF4TOCUg2futGU4pEA4cgDxBK9JyaGTtn6IVACVN39L2BL3IeQsAXHD2HJ3QllPKRLdC41dvUvx2ddZQwrGJc0kxZJx_-Bnr2eKN9gmPMQRvgsPW7V2Iu8nNBQ8HPEW7BF38fIvLxmFtit_7csBx_N1_r9ROl82dPrxEz0Ydsnv1WNfo5uLjzfnn5vL605fzs8vGcElKw5kejGu5tCCF49BZLlvDgAkJlI7UQddLa4U2lvRdy2RrB9E5QYSgvSFsjT48rN0tw-SsqXcmHdQu-Umng4raq38ns9-o27hXnHIqq84avXtckOLPxeWiJp-NC0HPLi5ZkY5Kynoi77Xe_odu45Lm6q5STMpeAu8q1TxQ9cs5JzcejyGg7gNUNUB1DLDyb_52cKT_JMZ-AaAYlh8</recordid><startdate>20141124</startdate><enddate>20141124</enddate><creator>Ahmed, Mohammed I</creator><creator>Alam, Majid</creator><creator>Emelianov, Vladimir U</creator><creator>Poterlowicz, Krzysztof</creator><creator>Patel, Ankit</creator><creator>Sharov, Andrey A</creator><creator>Mardaryev, Andrei N</creator><creator>Botchkareva, Natalia V</creator><general>Rockefeller University Press</general><general>The Rockefeller University Press</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20141124</creationdate><title>MicroRNA-214 controls skin and hair follicle development by modulating the activity of the Wnt pathway</title><author>Ahmed, Mohammed I ; Alam, Majid ; Emelianov, Vladimir U ; Poterlowicz, Krzysztof ; Patel, Ankit ; Sharov, Andrey A ; Mardaryev, Andrei N ; Botchkareva, Natalia V</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c481t-43abce548d087e406d485c30378022f2e0698dd7acd1965385db76e717729c13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>beta Catenin - biosynthesis</topic><topic>beta Catenin - genetics</topic><topic>Cell Differentiation - physiology</topic><topic>Cells, Cultured</topic><topic>Cellular Senescence - genetics</topic><topic>Genotype</topic><topic>Hair</topic><topic>Hair Follicle - growth & development</topic><topic>Hair Follicle - metabolism</topic><topic>Homeostasis</topic><topic>Keratin-10 - biosynthesis</topic><topic>Keratin-14 - biosynthesis</topic><topic>Keratinocytes - cytology</topic><topic>Lymphoid Enhancer-Binding Factor 1 - biosynthesis</topic><topic>Lymphoid Enhancer-Binding Factor 1 - genetics</topic><topic>Membrane Proteins - biosynthesis</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>MicroRNAs</topic><topic>MicroRNAs - genetics</topic><topic>MicroRNAs - physiology</topic><topic>Morphogenesis</topic><topic>Protein expression</topic><topic>Regeneration - genetics</topic><topic>Signal transduction</topic><topic>Skin</topic><topic>Skin - growth & development</topic><topic>Skin - metabolism</topic><topic>Wnt Proteins - genetics</topic><topic>Wnt Proteins - metabolism</topic><topic>Wnt Signaling Pathway</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ahmed, Mohammed I</creatorcontrib><creatorcontrib>Alam, Majid</creatorcontrib><creatorcontrib>Emelianov, Vladimir U</creatorcontrib><creatorcontrib>Poterlowicz, Krzysztof</creatorcontrib><creatorcontrib>Patel, Ankit</creatorcontrib><creatorcontrib>Sharov, Andrey A</creatorcontrib><creatorcontrib>Mardaryev, Andrei N</creatorcontrib><creatorcontrib>Botchkareva, Natalia V</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ahmed, Mohammed I</au><au>Alam, Majid</au><au>Emelianov, Vladimir U</au><au>Poterlowicz, Krzysztof</au><au>Patel, Ankit</au><au>Sharov, Andrey A</au><au>Mardaryev, Andrei N</au><au>Botchkareva, Natalia V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MicroRNA-214 controls skin and hair follicle development by modulating the activity of the Wnt pathway</atitle><jtitle>The Journal of cell biology</jtitle><addtitle>J Cell Biol</addtitle><date>2014-11-24</date><risdate>2014</risdate><volume>207</volume><issue>4</issue><spage>549</spage><epage>567</epage><pages>549-567</pages><issn>0021-9525</issn><eissn>1540-8140</eissn><coden>JCLBA3</coden><abstract>Skin development is governed by complex programs of gene activation and silencing, including microRNA-dependent modulation of gene expression. Here, we show that miR-214 regulates skin morphogenesis and hair follicle (HF) cycling by targeting β-catenin, a key component of the Wnt signaling pathway. miR-214 exhibits differential expression patterns in the skin epithelium, and its inducible overexpression in keratinocytes inhibited proliferation, which resulted in formation of fewer HFs with decreased hair bulb size and thinner hair production. The inhibitory effects of miR-214 on HF development and cycling were associated with altered activities of multiple signaling pathways, including decreased expression of key Wnt signaling mediators β-catenin and Lef-1, and were rescued by treatment with pharmacological Wnt activators. Finally, we identify β-catenin as one of the conserved miR-214 targets in keratinocytes. 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| subjects | Animals beta Catenin - biosynthesis beta Catenin - genetics Cell Differentiation - physiology Cells, Cultured Cellular Senescence - genetics Genotype Hair Hair Follicle - growth & development Hair Follicle - metabolism Homeostasis Keratin-10 - biosynthesis Keratin-14 - biosynthesis Keratinocytes - cytology Lymphoid Enhancer-Binding Factor 1 - biosynthesis Lymphoid Enhancer-Binding Factor 1 - genetics Membrane Proteins - biosynthesis Mice Mice, Transgenic MicroRNAs MicroRNAs - genetics MicroRNAs - physiology Morphogenesis Protein expression Regeneration - genetics Signal transduction Skin Skin - growth & development Skin - metabolism Wnt Proteins - genetics Wnt Proteins - metabolism Wnt Signaling Pathway |
| title | MicroRNA-214 controls skin and hair follicle development by modulating the activity of the Wnt pathway |
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