The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth muscles
The gut undergoes peristaltic movements regulated by intricate cellular interactions. How these interactions emerge in the developing gut remains poorly explored due to a lack of model system. We here developed a novel contractile organoid that is derived from the muscle layer of chicken embryonic h...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2025-08-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/97860 |
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| author | Rei Yagasaki Ryo Nakamura Yuuki Shikaya Ryosuke Tadokoro Ruolin Hao Zhe Wang Mototsugu Eiraku Masafumi Inaba Yoshiko Takahashi |
| author_facet | Rei Yagasaki Ryo Nakamura Yuuki Shikaya Ryosuke Tadokoro Ruolin Hao Zhe Wang Mototsugu Eiraku Masafumi Inaba Yoshiko Takahashi |
| author_sort | Rei Yagasaki |
| collection | DOAJ |
| description | The gut undergoes peristaltic movements regulated by intricate cellular interactions. How these interactions emerge in the developing gut remains poorly explored due to a lack of model system. We here developed a novel contractile organoid that is derived from the muscle layer of chicken embryonic hindgut. The organoid contained smooth muscle cells (SMCs) and interstitial cells of Cajal (ICCs; pacemaker) with few enteric neurons and underwent periodic contractions. The organoid was formed by self-organization with morphological arrangements of ICCs (internal) and SMCs (peripheral), allowing identification of these cells in live. GCaMP-Ca2+ imaging analyses revealed that Ca2+ transients between ICC-ICC, SMC-SMC, or SMC-ICC were markedly coordinated. Pharmacological studies further suggested a role of gap junctions in ICC-to-SMC signaling, and also possible mechanical feedback from SMC’s contraction to ICC’s pace-making activities. In addition, two organoids with different rhythms became synchronized when mediated by SMCs, unveiling a novel contribution of SMCs to ICC’s pace-making. The gut contractile organoid developed in this study offers a useful model to understand how the rhythm coordination between/among ICCs and SMCs is regulated and maintained during gut development. |
| format | Article |
| id | doaj-art-7020b2219dfb437ba7b0dd36e037cd66 |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-08-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-7020b2219dfb437ba7b0dd36e037cd662025-08-22T09:35:25ZengeLife Sciences Publications LtdeLife2050-084X2025-08-011310.7554/eLife.97860The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth musclesRei Yagasaki0https://orcid.org/0009-0005-7830-4391Ryo Nakamura1https://orcid.org/0000-0002-0761-0704Yuuki Shikaya2https://orcid.org/0009-0009-3544-9725Ryosuke Tadokoro3https://orcid.org/0000-0001-7556-4263Ruolin Hao4Zhe Wang5Mototsugu Eiraku6https://orcid.org/0000-0002-9433-9085Masafumi Inaba7https://orcid.org/0000-0001-6896-5819Yoshiko Takahashi8https://orcid.org/0000-0002-1596-7527Department of Zoology, Graduate School of Science, Kyoto University Sakyo-ku, Kyoto, JapanDepartment of Zoology, Graduate School of Science, Kyoto University Sakyo-ku, Kyoto, JapanDepartment of Zoology, Graduate School of Science, Kyoto University Sakyo-ku, Kyoto, JapanDepartment of Zoology, Graduate School of Science, Kyoto University Sakyo-ku, Kyoto, JapanInstitute for Life and Medical Sciences, Kyoto University, Sakyo-ku, Kyoto, Japan; Department of Polymer Chemistry, Graduate School of Engineering, Kyoto University, Kyoto, JapanInstitute for Life and Medical Sciences, Kyoto University, Sakyo-ku, Kyoto, Japan; Department of Polymer Chemistry, Graduate School of Engineering, Kyoto University, Kyoto, JapanInstitute for Life and Medical Sciences, Kyoto University, Sakyo-ku, Kyoto, Japan; Department of Polymer Chemistry, Graduate School of Engineering, Kyoto University, Kyoto, JapanDepartment of Zoology, Graduate School of Science, Kyoto University Sakyo-ku, Kyoto, JapanDepartment of Zoology, Graduate School of Science, Kyoto University Sakyo-ku, Kyoto, JapanThe gut undergoes peristaltic movements regulated by intricate cellular interactions. How these interactions emerge in the developing gut remains poorly explored due to a lack of model system. We here developed a novel contractile organoid that is derived from the muscle layer of chicken embryonic hindgut. The organoid contained smooth muscle cells (SMCs) and interstitial cells of Cajal (ICCs; pacemaker) with few enteric neurons and underwent periodic contractions. The organoid was formed by self-organization with morphological arrangements of ICCs (internal) and SMCs (peripheral), allowing identification of these cells in live. GCaMP-Ca2+ imaging analyses revealed that Ca2+ transients between ICC-ICC, SMC-SMC, or SMC-ICC were markedly coordinated. Pharmacological studies further suggested a role of gap junctions in ICC-to-SMC signaling, and also possible mechanical feedback from SMC’s contraction to ICC’s pace-making activities. In addition, two organoids with different rhythms became synchronized when mediated by SMCs, unveiling a novel contribution of SMCs to ICC’s pace-making. The gut contractile organoid developed in this study offers a useful model to understand how the rhythm coordination between/among ICCs and SMCs is regulated and maintained during gut development.https://elifesciences.org/articles/97860gut peristalsisOrganoidoscillationinterstitial cells of cajalsmooth muscle cellsGCaMP |
| spellingShingle | Rei Yagasaki Ryo Nakamura Yuuki Shikaya Ryosuke Tadokoro Ruolin Hao Zhe Wang Mototsugu Eiraku Masafumi Inaba Yoshiko Takahashi The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth muscles eLife gut peristalsis Organoid oscillation interstitial cells of cajal smooth muscle cells GCaMP |
| title | The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth muscles |
| title_full | The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth muscles |
| title_fullStr | The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth muscles |
| title_full_unstemmed | The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth muscles |
| title_short | The gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of Cajal and smooth muscles |
| title_sort | gut contractile organoid for studying the gut motility regulated by coordinating signals between interstitial cells of cajal and smooth muscles |
| topic | gut peristalsis Organoid oscillation interstitial cells of cajal smooth muscle cells GCaMP |
| url | https://elifesciences.org/articles/97860 |
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