Tracing the origin of adult intestinal stem cells
Adult intestinal stem cells are located at the bottom of crypts of Lieberkühn, where they express markers such as LGR5 1 , 2 and fuel the constant replenishment of the intestinal epithelium 1 . Although fetal LGR5-expressing cells can give rise to adult intestinal stem cells 3 , 4 , it remains uncle...
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| Veröffentlicht in: | Nature (London) 2019-06, Vol.570 (7759), p.107-111 |
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| creator | Guiu, Jordi Hannezo, Edouard Yui, Shiro Demharter, Samuel Ulyanchenko, Svetlana Maimets, Martti Jørgensen, Anne Perlman, Signe Lundvall, Lene Mamsen, Linn Salto Larsen, Agnete Olesen, Rasmus H. Andersen, Claus Yding Thuesen, Lea Langhoff Hare, Kristine Juul Pers, Tune H. Khodosevich, Konstantin Simons, Benjamin D. Jensen, Kim B. |
| description | Adult intestinal stem cells are located at the bottom of crypts of Lieberkühn, where they express markers such as LGR5
1
,
2
and fuel the constant replenishment of the intestinal epithelium
1
. Although fetal LGR5-expressing cells can give rise to adult intestinal stem cells
3
,
4
, it remains unclear whether this population in the patterned epithelium represents unique intestinal stem-cell precursors. Here we show, using unbiased quantitative lineage-tracing approaches, biophysical modelling and intestinal transplantation, that all cells of the mouse intestinal epithelium—irrespective of their location and pattern of LGR5 expression in the fetal gut tube—contribute actively to the adult intestinal stem cell pool. Using 3D imaging, we find that during fetal development the villus undergoes gross remodelling and fission. This brings epithelial cells from the non-proliferative villus into the proliferative intervillus region, which enables them to contribute to the adult stem-cell niche. Our results demonstrate that large-scale remodelling of the intestinal wall and cell-fate specification are closely linked. Moreover, these findings provide a direct link between the observed plasticity and cellular reprogramming of differentiating cells in adult tissues following damage
5
–
9
, revealing that stem-cell identity is an induced rather than a hardwired property.
Lineage tracing, biophysical modelling and intestinal transplantation approaches are used to demonstrate that, in the mouse fetal intestinal epithelium, cells are highly plastic with respect to cellular identity and, independent of LGR5 expression and cell position, can contribute to the adult stem cell compartment. |
| doi_str_mv | 10.1038/s41586-019-1212-5 |
| format | Article |
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1
,
2
and fuel the constant replenishment of the intestinal epithelium
1
. Although fetal LGR5-expressing cells can give rise to adult intestinal stem cells
3
,
4
, it remains unclear whether this population in the patterned epithelium represents unique intestinal stem-cell precursors. Here we show, using unbiased quantitative lineage-tracing approaches, biophysical modelling and intestinal transplantation, that all cells of the mouse intestinal epithelium—irrespective of their location and pattern of LGR5 expression in the fetal gut tube—contribute actively to the adult intestinal stem cell pool. Using 3D imaging, we find that during fetal development the villus undergoes gross remodelling and fission. This brings epithelial cells from the non-proliferative villus into the proliferative intervillus region, which enables them to contribute to the adult stem-cell niche. Our results demonstrate that large-scale remodelling of the intestinal wall and cell-fate specification are closely linked. Moreover, these findings provide a direct link between the observed plasticity and cellular reprogramming of differentiating cells in adult tissues following damage
5
–
9
, revealing that stem-cell identity is an induced rather than a hardwired property.
Lineage tracing, biophysical modelling and intestinal transplantation approaches are used to demonstrate that, in the mouse fetal intestinal epithelium, cells are highly plastic with respect to cellular identity and, independent of LGR5 expression and cell position, can contribute to the adult stem cell compartment.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-019-1212-5</identifier><identifier>PMID: 31092921</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/1 ; 13/100 ; 14/19 ; 38/91 ; 631/532/2118 ; 631/532/2437 ; 64/60 ; Adults ; Animals ; Cell Differentiation ; Cell Lineage ; Cellular Reprogramming ; Cloning ; Crypts ; Embryos ; Epithelial cells ; Epithelium ; Female ; Fetus - cytology ; Fetuses ; Homeostasis ; Humanities and Social Sciences ; Intestinal Mucosa - cytology ; Intestinal Mucosa - metabolism ; Intestine ; Intestines ; Intestines - cytology ; Intestines - growth & development ; Letter ; Male ; Mice ; Microbiology ; multidisciplinary ; Origin ; Plastic foam ; Population ; Receptors, G-Protein-Coupled - metabolism ; Regeneration ; Replenishment ; Science ; Science (multidisciplinary) ; Small intestine ; Stem Cell Niche ; Stem cell transplantation ; Stem cells ; Stem Cells - cytology ; Transplantation ; Villus</subject><ispartof>Nature (London), 2019-06, Vol.570 (7759), p.107-111</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 Jun 6, 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c739t-a43c49c97f417ff17f7e149a0d5e68c8ffc57378361cf38e146527dab6445faf3</citedby><cites>FETCH-LOGICAL-c739t-a43c49c97f417ff17f7e149a0d5e68c8ffc57378361cf38e146527dab6445faf3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-019-1212-5$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-019-1212-5$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31092921$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Guiu, Jordi</creatorcontrib><creatorcontrib>Hannezo, Edouard</creatorcontrib><creatorcontrib>Yui, Shiro</creatorcontrib><creatorcontrib>Demharter, Samuel</creatorcontrib><creatorcontrib>Ulyanchenko, Svetlana</creatorcontrib><creatorcontrib>Maimets, Martti</creatorcontrib><creatorcontrib>Jørgensen, Anne</creatorcontrib><creatorcontrib>Perlman, Signe</creatorcontrib><creatorcontrib>Lundvall, Lene</creatorcontrib><creatorcontrib>Mamsen, Linn Salto</creatorcontrib><creatorcontrib>Larsen, Agnete</creatorcontrib><creatorcontrib>Olesen, Rasmus H.</creatorcontrib><creatorcontrib>Andersen, Claus Yding</creatorcontrib><creatorcontrib>Thuesen, Lea Langhoff</creatorcontrib><creatorcontrib>Hare, Kristine Juul</creatorcontrib><creatorcontrib>Pers, Tune H.</creatorcontrib><creatorcontrib>Khodosevich, Konstantin</creatorcontrib><creatorcontrib>Simons, Benjamin D.</creatorcontrib><creatorcontrib>Jensen, Kim B.</creatorcontrib><title>Tracing the origin of adult intestinal stem cells</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Adult intestinal stem cells are located at the bottom of crypts of Lieberkühn, where they express markers such as LGR5
1
,
2
and fuel the constant replenishment of the intestinal epithelium
1
. Although fetal LGR5-expressing cells can give rise to adult intestinal stem cells
3
,
4
, it remains unclear whether this population in the patterned epithelium represents unique intestinal stem-cell precursors. Here we show, using unbiased quantitative lineage-tracing approaches, biophysical modelling and intestinal transplantation, that all cells of the mouse intestinal epithelium—irrespective of their location and pattern of LGR5 expression in the fetal gut tube—contribute actively to the adult intestinal stem cell pool. Using 3D imaging, we find that during fetal development the villus undergoes gross remodelling and fission. This brings epithelial cells from the non-proliferative villus into the proliferative intervillus region, which enables them to contribute to the adult stem-cell niche. Our results demonstrate that large-scale remodelling of the intestinal wall and cell-fate specification are closely linked. Moreover, these findings provide a direct link between the observed plasticity and cellular reprogramming of differentiating cells in adult tissues following damage
5
–
9
, revealing that stem-cell identity is an induced rather than a hardwired property.
Lineage tracing, biophysical modelling and intestinal transplantation approaches are used to demonstrate that, in the mouse fetal intestinal epithelium, cells are highly plastic with respect to cellular identity and, independent of LGR5 expression and cell position, can contribute to the adult stem cell compartment.</description><subject>13/1</subject><subject>13/100</subject><subject>14/19</subject><subject>38/91</subject><subject>631/532/2118</subject><subject>631/532/2437</subject><subject>64/60</subject><subject>Adults</subject><subject>Animals</subject><subject>Cell Differentiation</subject><subject>Cell Lineage</subject><subject>Cellular Reprogramming</subject><subject>Cloning</subject><subject>Crypts</subject><subject>Embryos</subject><subject>Epithelial cells</subject><subject>Epithelium</subject><subject>Female</subject><subject>Fetus - cytology</subject><subject>Fetuses</subject><subject>Homeostasis</subject><subject>Humanities and Social Sciences</subject><subject>Intestinal Mucosa - cytology</subject><subject>Intestinal Mucosa - metabolism</subject><subject>Intestine</subject><subject>Intestines</subject><subject>Intestines - cytology</subject><subject>Intestines - growth & development</subject><subject>Letter</subject><subject>Male</subject><subject>Mice</subject><subject>Microbiology</subject><subject>multidisciplinary</subject><subject>Origin</subject><subject>Plastic foam</subject><subject>Population</subject><subject>Receptors, G-Protein-Coupled - metabolism</subject><subject>Regeneration</subject><subject>Replenishment</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Small intestine</subject><subject>Stem Cell Niche</subject><subject>Stem cell transplantation</subject><subject>Stem cells</subject><subject>Stem Cells - 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Salto</au><au>Larsen, Agnete</au><au>Olesen, Rasmus H.</au><au>Andersen, Claus Yding</au><au>Thuesen, Lea Langhoff</au><au>Hare, Kristine Juul</au><au>Pers, Tune H.</au><au>Khodosevich, Konstantin</au><au>Simons, Benjamin D.</au><au>Jensen, Kim B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tracing the origin of adult intestinal stem cells</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2019-06</date><risdate>2019</risdate><volume>570</volume><issue>7759</issue><spage>107</spage><epage>111</epage><pages>107-111</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><abstract>Adult intestinal stem cells are located at the bottom of crypts of Lieberkühn, where they express markers such as LGR5
1
,
2
and fuel the constant replenishment of the intestinal epithelium
1
. Although fetal LGR5-expressing cells can give rise to adult intestinal stem cells
3
,
4
, it remains unclear whether this population in the patterned epithelium represents unique intestinal stem-cell precursors. Here we show, using unbiased quantitative lineage-tracing approaches, biophysical modelling and intestinal transplantation, that all cells of the mouse intestinal epithelium—irrespective of their location and pattern of LGR5 expression in the fetal gut tube—contribute actively to the adult intestinal stem cell pool. Using 3D imaging, we find that during fetal development the villus undergoes gross remodelling and fission. This brings epithelial cells from the non-proliferative villus into the proliferative intervillus region, which enables them to contribute to the adult stem-cell niche. Our results demonstrate that large-scale remodelling of the intestinal wall and cell-fate specification are closely linked. Moreover, these findings provide a direct link between the observed plasticity and cellular reprogramming of differentiating cells in adult tissues following damage
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, revealing that stem-cell identity is an induced rather than a hardwired property.
Lineage tracing, biophysical modelling and intestinal transplantation approaches are used to demonstrate that, in the mouse fetal intestinal epithelium, cells are highly plastic with respect to cellular identity and, independent of LGR5 expression and cell position, can contribute to the adult stem cell compartment.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>31092921</pmid><doi>10.1038/s41586-019-1212-5</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0028-0836 |
| ispartof | Nature (London), 2019-06, Vol.570 (7759), p.107-111 |
| issn | 0028-0836 1476-4687 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6986928 |
| source | MEDLINE; SpringerLink Journals; Nature Journals Online |
| subjects | 13/1 13/100 14/19 38/91 631/532/2118 631/532/2437 64/60 Adults Animals Cell Differentiation Cell Lineage Cellular Reprogramming Cloning Crypts Embryos Epithelial cells Epithelium Female Fetus - cytology Fetuses Homeostasis Humanities and Social Sciences Intestinal Mucosa - cytology Intestinal Mucosa - metabolism Intestine Intestines Intestines - cytology Intestines - growth & development Letter Male Mice Microbiology multidisciplinary Origin Plastic foam Population Receptors, G-Protein-Coupled - metabolism Regeneration Replenishment Science Science (multidisciplinary) Small intestine Stem Cell Niche Stem cell transplantation Stem cells Stem Cells - cytology Transplantation Villus |
| title | Tracing the origin of adult intestinal stem cells |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-08T14%3A02%3A08IST&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%20origin%20of%20adult%20intestinal%20stem%20cells&rft.jtitle=Nature%20(London)&rft.au=Guiu,%20Jordi&rft.date=2019-06&rft.volume=570&rft.issue=7759&rft.spage=107&rft.epage=111&rft.pages=107-111&rft.issn=0028-0836&rft.eissn=1476-4687&rft_id=info:doi/10.1038/s41586-019-1212-5&rft_dat=%3Cgale_pubme%3EA602150277%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=2244553805&rft_id=info:pmid/31092921&rft_galeid=A602150277&rfr_iscdi=true |