Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system
Identifieur interne : 002025 ( Pmc/Curation ); précédent : 002024; suivant : 002026Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system
Auteurs : Michael J. Workman [États-Unis] ; Maxime M. Mahe [États-Unis] ; Stephen Trisno [États-Unis] ; Holly M. Poling [États-Unis] ; Carey L. Watson [États-Unis] ; Nambirajan Sundaram [États-Unis] ; Ching-Fang Chang [États-Unis] ; Jacqueline Schiesser [États-Unis] ; Philippe Aubert [France] ; Edouard G. Stanley [Australie] ; Andrew G. Elefanty [Australie] ; Yuichiro Miyaoka [États-Unis] ; Mohammad A. Mandegar [États-Unis] ; Bruce R. Conklin [États-Unis] ; Michel Neunlist [France] ; Samantha A. Brugmann [États-Unis] ; Michael A. Helmrath [États-Unis] ; James M. Wells [États-Unis]Source :
- Nature medicine [ 1078-8956 ] ; 2016.
Abstract
The enteric nervous system (ENS) of the gastrointestinal tract controls many diverse functions, including motility and epithelial permeability. Perturbations in ENS development or function are common, yet there is no human model for studying ENS-intestinal biology and disease. We used a tissue-engineering approach with embryonic and induced pluripotent stem cells (PSCs) to generate human intestinal tissue containing a functional ENS. We recapitulated normal intestinal ENS development by combining human-PSC-derived neural crest cells (NCCs) and developing human intestinal organoids (HIOs). NCCs recombined with HIOs
Url:
DOI: 10.1038/nm.4233
PubMed: 27869805
PubMed Central: 5562951
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<affiliation wicri:level="1"><nlm:aff id="A6">Department of Pediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, Australia</nlm:aff>
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<author><name sortKey="Elefanty, Andrew G" sort="Elefanty, Andrew G" uniqKey="Elefanty A" first="Andrew G" last="Elefanty">Andrew G. Elefanty</name>
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<author><name sortKey="Watson, Carey L" sort="Watson, Carey L" uniqKey="Watson C" first="Carey L" last="Watson">Carey L. Watson</name>
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<author><name sortKey="Sundaram, Nambirajan" sort="Sundaram, Nambirajan" uniqKey="Sundaram N" first="Nambirajan" last="Sundaram">Nambirajan Sundaram</name>
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<country xml:lang="fr">France</country>
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<affiliation wicri:level="1"><nlm:aff id="A6">Department of Pediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Department of Pediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="A7">Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton, Victoria, Australia</nlm:aff>
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<wicri:regionArea>Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton, Victoria</wicri:regionArea>
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<author><name sortKey="Elefanty, Andrew G" sort="Elefanty, Andrew G" uniqKey="Elefanty A" first="Andrew G" last="Elefanty">Andrew G. Elefanty</name>
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<affiliation wicri:level="1"><nlm:aff id="A6">Department of Pediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Department of Pediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="A7">Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton, Victoria, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea>Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton, Victoria</wicri:regionArea>
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<author><name sortKey="Miyaoka, Yuichiro" sort="Miyaoka, Yuichiro" uniqKey="Miyaoka Y" first="Yuichiro" last="Miyaoka">Yuichiro Miyaoka</name>
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<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Gladstone Institutes, San Francisco, California</wicri:regionArea>
</affiliation>
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<author><name sortKey="Mandegar, Mohammad A" sort="Mandegar, Mohammad A" uniqKey="Mandegar M" first="Mohammad A" last="Mandegar">Mohammad A. Mandegar</name>
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<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Gladstone Institutes, San Francisco, California</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Conklin, Bruce R" sort="Conklin, Bruce R" uniqKey="Conklin B" first="Bruce R" last="Conklin">Bruce R. Conklin</name>
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<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Gladstone Institutes, San Francisco, California</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="A9">Departments of Medicine and Molecular and Cellular Pharmacology, University of California at San Francisco, San Francisco, California, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Departments of Medicine and Molecular and Cellular Pharmacology, University of California at San Francisco, San Francisco, California</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Neunlist, Michel" sort="Neunlist, Michel" uniqKey="Neunlist M" first="Michel" last="Neunlist">Michel Neunlist</name>
<affiliation wicri:level="1"><nlm:aff id="A4">INSERM UMR 913, University of Nantes, CHU de Nantes—Institut des Maladies de l'Appareil Digestif, Nantes, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>INSERM UMR 913, University of Nantes, CHU de Nantes—Institut des Maladies de l'Appareil Digestif, Nantes</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Brugmann, Samantha A" sort="Brugmann, Samantha A" uniqKey="Brugmann S" first="Samantha A" last="Brugmann">Samantha A. Brugmann</name>
<affiliation wicri:level="1"><nlm:aff id="A1">Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="A3">Division of Plastic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Division of Plastic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio</wicri:regionArea>
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</author>
<author><name sortKey="Helmrath, Michael A" sort="Helmrath, Michael A" uniqKey="Helmrath M" first="Michael A" last="Helmrath">Michael A. Helmrath</name>
<affiliation wicri:level="1"><nlm:aff id="A2">Division of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Division of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wells, James M" sort="Wells, James M" uniqKey="Wells J" first="James M" last="Wells">James M. Wells</name>
<affiliation wicri:level="1"><nlm:aff id="A1">Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="A10">Division of Endocrinology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</nlm:aff>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Division of Endocrinology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Nature medicine</title>
<idno type="ISSN">1078-8956</idno>
<idno type="eISSN">1546-170X</idno>
<imprint><date when="2016">2016</date>
</imprint>
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<front><div type="abstract" xml:lang="en"><p id="P1">The enteric nervous system (ENS) of the gastrointestinal tract controls many diverse functions, including motility and epithelial permeability. Perturbations in ENS development or function are common, yet there is no human model for studying ENS-intestinal biology and disease. We used a tissue-engineering approach with embryonic and induced pluripotent stem cells (PSCs) to generate human intestinal tissue containing a functional ENS. We recapitulated normal intestinal ENS development by combining human-PSC-derived neural crest cells (NCCs) and developing human intestinal organoids (HIOs). NCCs recombined with HIOs <italic>in vitro</italic>
migrated into the mesenchyme, differentiated into neurons and glial cells and showed neuronal activity, as measured by rhythmic waves of calcium transients. ENS-containing HIOs grown <italic>in vivo</italic>
formed neuroglial structures similar to a myenteric and submucosal plexus, had functional interstitial cells of Cajal and had an electromechanical coupling that regulated waves of propagating contraction. Finally, we used this system to investigate the cellular and molecular basis for Hirschsprung's disease caused by a mutation in the gene <italic>PHOX2B</italic>
. This is, to the best of our knowledge, the first demonstration of human-PSC-derived intestinal tissue with a functional ENS and how this system can be used to study motility disorders of the human gastrointestinal tract.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<pmc-dir>properties manuscript</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-journal-id">9502015</journal-id>
<journal-id journal-id-type="pubmed-jr-id">8791</journal-id>
<journal-id journal-id-type="nlm-ta">Nat Med</journal-id>
<journal-id journal-id-type="iso-abbrev">Nat. Med.</journal-id>
<journal-title-group><journal-title>Nature medicine</journal-title>
</journal-title-group>
<issn pub-type="ppub">1078-8956</issn>
<issn pub-type="epub">1546-170X</issn>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27869805</article-id>
<article-id pub-id-type="pmc">5562951</article-id>
<article-id pub-id-type="doi">10.1038/nm.4233</article-id>
<article-id pub-id-type="manuscript">NIHMS892701</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Workman</surname>
<given-names>Michael J</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref rid="FN2" ref-type="author-notes">11</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mahe</surname>
<given-names>Maxime M</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
<xref rid="FN2" ref-type="author-notes">11</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Trisno</surname>
<given-names>Stephen</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Poling</surname>
<given-names>Holly M</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Watson</surname>
<given-names>Carey L</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sundaram</surname>
<given-names>Nambirajan</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chang</surname>
<given-names>Ching-Fang</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Schiesser</surname>
<given-names>Jacqueline</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Aubert</surname>
<given-names>Philippe</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stanley</surname>
<given-names>Edouard G</given-names>
</name>
<xref ref-type="aff" rid="A5">5</xref>
<xref ref-type="aff" rid="A6">6</xref>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Elefanty</surname>
<given-names>Andrew G</given-names>
</name>
<xref ref-type="aff" rid="A5">5</xref>
<xref ref-type="aff" rid="A6">6</xref>
<xref ref-type="aff" rid="A7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Miyaoka</surname>
<given-names>Yuichiro</given-names>
</name>
<xref ref-type="aff" rid="A8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mandegar</surname>
<given-names>Mohammad A</given-names>
</name>
<xref ref-type="aff" rid="A8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Conklin</surname>
<given-names>Bruce R</given-names>
</name>
<xref ref-type="aff" rid="A8">8</xref>
<xref ref-type="aff" rid="A9">9</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Neunlist</surname>
<given-names>Michel</given-names>
</name>
<xref ref-type="aff" rid="A4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Brugmann</surname>
<given-names>Samantha A</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Helmrath</surname>
<given-names>Michael A</given-names>
</name>
<xref ref-type="aff" rid="A2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wells</surname>
<given-names>James M</given-names>
</name>
<xref ref-type="aff" rid="A1">1</xref>
<xref ref-type="aff" rid="A10">10</xref>
</contrib>
</contrib-group>
<aff id="A1"><label>1</label>
Division of Developmental Biology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</aff>
<aff id="A2"><label>2</label>
Division of Pediatric General and Thoracic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</aff>
<aff id="A3"><label>3</label>
Division of Plastic Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</aff>
<aff id="A4"><label>4</label>
INSERM UMR 913, University of Nantes, CHU de Nantes—Institut des Maladies de l'Appareil Digestif, Nantes, France</aff>
<aff id="A5"><label>5</label>
Murdoch Children's Research Institute, The Royal Children's Hospital, Parkville, Victoria, Australia</aff>
<aff id="A6"><label>6</label>
Department of Pediatrics, Faculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, Victoria, Australia</aff>
<aff id="A7"><label>7</label>
Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton, Victoria, Australia</aff>
<aff id="A8"><label>8</label>
Gladstone Institutes, San Francisco, California, USA</aff>
<aff id="A9"><label>9</label>
Departments of Medicine and Molecular and Cellular Pharmacology, University of California at San Francisco, San Francisco, California, USA</aff>
<aff id="A10"><label>10</label>
Division of Endocrinology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA</aff>
<author-notes><corresp id="FN1">Correspondence should be addressed to J.M.W. (<email>james.wells@cchmc.org</email>
) or M.A.H. (<email>michael.helmrath@cchmc.org</email>
)</corresp>
<fn id="FN2" fn-type="equal"><label>11</label>
<p>These authors contributed equally to this work.</p>
</fn>
</author-notes>
<pub-date pub-type="nihms-submitted"><day>15</day>
<month>7</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="epub"><day>21</day>
<month>11</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="ppub"><month>1</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>19</day>
<month>8</month>
<year>2017</year>
</pub-date>
<volume>23</volume>
<issue>1</issue>
<fpage>49</fpage>
<lpage>59</lpage>
<pmc-comment>elocation-id from pubmed: 10.1038/nm.4233</pmc-comment>
<abstract><p id="P1">The enteric nervous system (ENS) of the gastrointestinal tract controls many diverse functions, including motility and epithelial permeability. Perturbations in ENS development or function are common, yet there is no human model for studying ENS-intestinal biology and disease. We used a tissue-engineering approach with embryonic and induced pluripotent stem cells (PSCs) to generate human intestinal tissue containing a functional ENS. We recapitulated normal intestinal ENS development by combining human-PSC-derived neural crest cells (NCCs) and developing human intestinal organoids (HIOs). NCCs recombined with HIOs <italic>in vitro</italic>
migrated into the mesenchyme, differentiated into neurons and glial cells and showed neuronal activity, as measured by rhythmic waves of calcium transients. ENS-containing HIOs grown <italic>in vivo</italic>
formed neuroglial structures similar to a myenteric and submucosal plexus, had functional interstitial cells of Cajal and had an electromechanical coupling that regulated waves of propagating contraction. Finally, we used this system to investigate the cellular and molecular basis for Hirschsprung's disease caused by a mutation in the gene <italic>PHOX2B</italic>
. This is, to the best of our knowledge, the first demonstration of human-PSC-derived intestinal tissue with a functional ENS and how this system can be used to study motility disorders of the human gastrointestinal tract.</p>
</abstract>
</article-meta>
</front>
</pmc>
</record>
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