Tracing the cellular dynamics of sebaceous gland development in normal and perturbed states
The sebaceous gland (SG) is an essential component of the skin, and SG dysfunction is debilitating 1 , 2 . Yet, the cellular bases for its origin, development and subsequent maintenance remain poorly understood. Here, we apply large-scale quantitative fate mapping to define the patterns of cell fate...
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| Veröffentlicht in: | Nature cell biology 2019-08, Vol.21 (8), p.924-932 |
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| creator | Andersen, Marianne Stemann Hannezo, Edouard Ulyanchenko, Svetlana Estrach, Soline Antoku, Yasuko Pisano, Sabrina Boonekamp, Kim E. Sendrup, Sarah Maimets, Martti Pedersen, Marianne Terndrup Johansen, Jens V. Clement, Ditte L. Feral, Chloe C. Simons, Benjamin D. Jensen, Kim B. |
| description | The sebaceous gland (SG) is an essential component of the skin, and SG dysfunction is debilitating
1
,
2
. Yet, the cellular bases for its origin, development and subsequent maintenance remain poorly understood. Here, we apply large-scale quantitative fate mapping to define the patterns of cell fate behaviour during SG development and maintenance. We show that the SG develops from a defined number of lineage-restricted progenitors that undergo a programme of independent and stochastic cell fate decisions. Following an expansion phase, equipotent progenitors transition into a phase of homeostatic turnover, which is correlated with changes in the mechanical properties of the stroma and spatial restrictions on gland size. Expression of the oncogene KrasG12D results in a release from these constraints and unbridled gland expansion. Quantitative clonal fate analysis reveals that, during this phase, the primary effect of the
Kras
oncogene is to drive a constant fate bias with little effect on cell division rates. These findings provide insight into the developmental programme of the SG, as well as the mechanisms that drive tumour progression and gland dysfunction.
Andersen, Hannezo, Ulyanchenko et al. map cell behaviour and spatiotemporal dynamics of the sebaceous gland during homeostasis and oncogene-induced gland expansion, and show that all basal cells contribute to long-term gland maintenance. |
| doi_str_mv | 10.1038/s41556-019-0362-x |
| format | Article |
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1
,
2
. Yet, the cellular bases for its origin, development and subsequent maintenance remain poorly understood. Here, we apply large-scale quantitative fate mapping to define the patterns of cell fate behaviour during SG development and maintenance. We show that the SG develops from a defined number of lineage-restricted progenitors that undergo a programme of independent and stochastic cell fate decisions. Following an expansion phase, equipotent progenitors transition into a phase of homeostatic turnover, which is correlated with changes in the mechanical properties of the stroma and spatial restrictions on gland size. Expression of the oncogene KrasG12D results in a release from these constraints and unbridled gland expansion. Quantitative clonal fate analysis reveals that, during this phase, the primary effect of the
Kras
oncogene is to drive a constant fate bias with little effect on cell division rates. These findings provide insight into the developmental programme of the SG, as well as the mechanisms that drive tumour progression and gland dysfunction.
Andersen, Hannezo, Ulyanchenko et al. map cell behaviour and spatiotemporal dynamics of the sebaceous gland during homeostasis and oncogene-induced gland expansion, and show that all basal cells contribute to long-term gland maintenance.</description><identifier>ISSN: 1465-7392</identifier><identifier>EISSN: 1476-4679</identifier><identifier>DOI: 10.1038/s41556-019-0362-x</identifier><identifier>PMID: 31358966</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/100 ; 14/19 ; 631/136/1660/1986 ; 631/532/2118/2438 ; 631/532/2139 ; 631/67/395 ; 64/60 ; Animal biology ; Animals ; Biomedical and Life Sciences ; Cancer Research ; Cell Biology ; Cell division ; Cell fate ; Cell Proliferation - physiology ; Cell research ; Development Biology ; Developmental Biology ; Developmental cytology ; Disease Progression ; Fate maps ; Gene Expression Regulation, Developmental - immunology ; Health aspects ; Homeostasis - physiology ; Letter ; Life Sciences ; Mapping ; Mechanical properties ; Mice, Transgenic ; Molecular dynamics ; Morphogenesis ; Phase transitions ; Physiological aspects ; Sebaceous gland ; Sebaceous glands ; Skin ; Stem Cells ; Stem Cells - cytology ; Stochasticity ; Stroma ; Tumors ; Veterinary medicine and animal Health</subject><ispartof>Nature cell biology, 2019-08, Vol.21 (8), p.924-932</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2019</rights><rights>COPYRIGHT 2019 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Aug 2019</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c671t-d85a6d7457300ff065132350fce494793de31b4121f52cb1d892c168edad85053</citedby><cites>FETCH-LOGICAL-c671t-d85a6d7457300ff065132350fce494793de31b4121f52cb1d892c168edad85053</cites><orcidid>0000-0002-2452-4736 ; 0000-0001-9756-2082 ; 0000-0001-6005-1561 ; 0000-0001-7343-2769 ; 0000-0001-6569-1664 ; 0000-0003-2088-5988 ; 0000-0002-3875-7071 ; 0000-0001-6751-5453 ; 0000-0003-3124-9178</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31358966$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.univ-cotedazur.fr/hal-02526771$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Andersen, Marianne Stemann</creatorcontrib><creatorcontrib>Hannezo, Edouard</creatorcontrib><creatorcontrib>Ulyanchenko, Svetlana</creatorcontrib><creatorcontrib>Estrach, Soline</creatorcontrib><creatorcontrib>Antoku, Yasuko</creatorcontrib><creatorcontrib>Pisano, Sabrina</creatorcontrib><creatorcontrib>Boonekamp, Kim E.</creatorcontrib><creatorcontrib>Sendrup, Sarah</creatorcontrib><creatorcontrib>Maimets, Martti</creatorcontrib><creatorcontrib>Pedersen, Marianne Terndrup</creatorcontrib><creatorcontrib>Johansen, Jens V.</creatorcontrib><creatorcontrib>Clement, Ditte L.</creatorcontrib><creatorcontrib>Feral, Chloe C.</creatorcontrib><creatorcontrib>Simons, Benjamin D.</creatorcontrib><creatorcontrib>Jensen, Kim B.</creatorcontrib><title>Tracing the cellular dynamics of sebaceous gland development in normal and perturbed states</title><title>Nature cell biology</title><addtitle>Nat Cell Biol</addtitle><addtitle>Nat Cell Biol</addtitle><description>The sebaceous gland (SG) is an essential component of the skin, and SG dysfunction is debilitating
1
,
2
. Yet, the cellular bases for its origin, development and subsequent maintenance remain poorly understood. Here, we apply large-scale quantitative fate mapping to define the patterns of cell fate behaviour during SG development and maintenance. We show that the SG develops from a defined number of lineage-restricted progenitors that undergo a programme of independent and stochastic cell fate decisions. Following an expansion phase, equipotent progenitors transition into a phase of homeostatic turnover, which is correlated with changes in the mechanical properties of the stroma and spatial restrictions on gland size. Expression of the oncogene KrasG12D results in a release from these constraints and unbridled gland expansion. Quantitative clonal fate analysis reveals that, during this phase, the primary effect of the
Kras
oncogene is to drive a constant fate bias with little effect on cell division rates. These findings provide insight into the developmental programme of the SG, as well as the mechanisms that drive tumour progression and gland dysfunction.
Andersen, Hannezo, Ulyanchenko et al. map cell behaviour and spatiotemporal dynamics of the sebaceous gland during homeostasis and oncogene-induced gland expansion, and show that all basal cells contribute to long-term gland maintenance.</description><subject>13/100</subject><subject>14/19</subject><subject>631/136/1660/1986</subject><subject>631/532/2118/2438</subject><subject>631/532/2139</subject><subject>631/67/395</subject><subject>64/60</subject><subject>Animal biology</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Cancer Research</subject><subject>Cell Biology</subject><subject>Cell division</subject><subject>Cell fate</subject><subject>Cell Proliferation - physiology</subject><subject>Cell research</subject><subject>Development Biology</subject><subject>Developmental Biology</subject><subject>Developmental cytology</subject><subject>Disease Progression</subject><subject>Fate maps</subject><subject>Gene Expression Regulation, Developmental - immunology</subject><subject>Health aspects</subject><subject>Homeostasis - physiology</subject><subject>Letter</subject><subject>Life Sciences</subject><subject>Mapping</subject><subject>Mechanical properties</subject><subject>Mice, Transgenic</subject><subject>Molecular dynamics</subject><subject>Morphogenesis</subject><subject>Phase transitions</subject><subject>Physiological aspects</subject><subject>Sebaceous gland</subject><subject>Sebaceous glands</subject><subject>Skin</subject><subject>Stem Cells</subject><subject>Stem Cells - cytology</subject><subject>Stochasticity</subject><subject>Stroma</subject><subject>Tumors</subject><subject>Veterinary medicine and animal 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the cellular dynamics of sebaceous gland development in normal and perturbed states</title><author>Andersen, Marianne Stemann ; Hannezo, Edouard ; Ulyanchenko, Svetlana ; Estrach, Soline ; Antoku, Yasuko ; Pisano, Sabrina ; Boonekamp, Kim E. ; Sendrup, Sarah ; Maimets, Martti ; Pedersen, Marianne Terndrup ; Johansen, Jens V. ; Clement, Ditte L. ; Feral, Chloe C. ; Simons, Benjamin D. ; Jensen, Kim B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c671t-d85a6d7457300ff065132350fce494793de31b4121f52cb1d892c168edad85053</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>13/100</topic><topic>14/19</topic><topic>631/136/1660/1986</topic><topic>631/532/2118/2438</topic><topic>631/532/2139</topic><topic>631/67/395</topic><topic>64/60</topic><topic>Animal biology</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Cancer Research</topic><topic>Cell Biology</topic><topic>Cell division</topic><topic>Cell fate</topic><topic>Cell Proliferation - physiology</topic><topic>Cell research</topic><topic>Development Biology</topic><topic>Developmental Biology</topic><topic>Developmental cytology</topic><topic>Disease Progression</topic><topic>Fate maps</topic><topic>Gene Expression Regulation, Developmental - immunology</topic><topic>Health aspects</topic><topic>Homeostasis - physiology</topic><topic>Letter</topic><topic>Life Sciences</topic><topic>Mapping</topic><topic>Mechanical properties</topic><topic>Mice, Transgenic</topic><topic>Molecular dynamics</topic><topic>Morphogenesis</topic><topic>Phase transitions</topic><topic>Physiological aspects</topic><topic>Sebaceous gland</topic><topic>Sebaceous glands</topic><topic>Skin</topic><topic>Stem Cells</topic><topic>Stem Cells - cytology</topic><topic>Stochasticity</topic><topic>Stroma</topic><topic>Tumors</topic><topic>Veterinary medicine and animal 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titles)</collection><jtitle>Nature cell biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Andersen, Marianne Stemann</au><au>Hannezo, Edouard</au><au>Ulyanchenko, Svetlana</au><au>Estrach, Soline</au><au>Antoku, Yasuko</au><au>Pisano, Sabrina</au><au>Boonekamp, Kim E.</au><au>Sendrup, Sarah</au><au>Maimets, Martti</au><au>Pedersen, Marianne Terndrup</au><au>Johansen, Jens V.</au><au>Clement, Ditte L.</au><au>Feral, Chloe C.</au><au>Simons, Benjamin D.</au><au>Jensen, Kim B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tracing the cellular dynamics of sebaceous gland development in normal and perturbed states</atitle><jtitle>Nature cell biology</jtitle><stitle>Nat Cell Biol</stitle><addtitle>Nat Cell Biol</addtitle><date>2019-08-01</date><risdate>2019</risdate><volume>21</volume><issue>8</issue><spage>924</spage><epage>932</epage><pages>924-932</pages><issn>1465-7392</issn><eissn>1476-4679</eissn><abstract>The sebaceous gland (SG) is an essential component of the skin, and SG dysfunction is debilitating
1
,
2
. Yet, the cellular bases for its origin, development and subsequent maintenance remain poorly understood. Here, we apply large-scale quantitative fate mapping to define the patterns of cell fate behaviour during SG development and maintenance. We show that the SG develops from a defined number of lineage-restricted progenitors that undergo a programme of independent and stochastic cell fate decisions. Following an expansion phase, equipotent progenitors transition into a phase of homeostatic turnover, which is correlated with changes in the mechanical properties of the stroma and spatial restrictions on gland size. Expression of the oncogene KrasG12D results in a release from these constraints and unbridled gland expansion. Quantitative clonal fate analysis reveals that, during this phase, the primary effect of the
Kras
oncogene is to drive a constant fate bias with little effect on cell division rates. These findings provide insight into the developmental programme of the SG, as well as the mechanisms that drive tumour progression and gland dysfunction.
Andersen, Hannezo, Ulyanchenko et al. map cell behaviour and spatiotemporal dynamics of the sebaceous gland during homeostasis and oncogene-induced gland expansion, and show that all basal cells contribute to long-term gland maintenance.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31358966</pmid><doi>10.1038/s41556-019-0362-x</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-2452-4736</orcidid><orcidid>https://orcid.org/0000-0001-9756-2082</orcidid><orcidid>https://orcid.org/0000-0001-6005-1561</orcidid><orcidid>https://orcid.org/0000-0001-7343-2769</orcidid><orcidid>https://orcid.org/0000-0001-6569-1664</orcidid><orcidid>https://orcid.org/0000-0003-2088-5988</orcidid><orcidid>https://orcid.org/0000-0002-3875-7071</orcidid><orcidid>https://orcid.org/0000-0001-6751-5453</orcidid><orcidid>https://orcid.org/0000-0003-3124-9178</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1465-7392 |
| ispartof | Nature cell biology, 2019-08, Vol.21 (8), p.924-932 |
| issn | 1465-7392 1476-4679 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6978139 |
| source | MEDLINE; Nature; Alma/SFX Local Collection |
| subjects | 13/100 14/19 631/136/1660/1986 631/532/2118/2438 631/532/2139 631/67/395 64/60 Animal biology Animals Biomedical and Life Sciences Cancer Research Cell Biology Cell division Cell fate Cell Proliferation - physiology Cell research Development Biology Developmental Biology Developmental cytology Disease Progression Fate maps Gene Expression Regulation, Developmental - immunology Health aspects Homeostasis - physiology Letter Life Sciences Mapping Mechanical properties Mice, Transgenic Molecular dynamics Morphogenesis Phase transitions Physiological aspects Sebaceous gland Sebaceous glands Skin Stem Cells Stem Cells - cytology Stochasticity Stroma Tumors Veterinary medicine and animal Health |
| title | Tracing the cellular dynamics of sebaceous gland development in normal and perturbed states |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-29T12%3A58%3A24IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Tracing%20the%20cellular%20dynamics%20of%20sebaceous%20gland%20development%20in%20normal%20and%20perturbed%20states&rft.jtitle=Nature%20cell%20biology&rft.au=Andersen,%20Marianne%20Stemann&rft.date=2019-08-01&rft.volume=21&rft.issue=8&rft.spage=924&rft.epage=932&rft.pages=924-932&rft.issn=1465-7392&rft.eissn=1476-4679&rft_id=info:doi/10.1038/s41556-019-0362-x&rft_dat=%3Cgale_pubme%3EA595279339%3C/gale_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2267707335&rft_id=info:pmid/31358966&rft_galeid=A595279339&rfr_iscdi=true |