Peripheral neuronal activation shapes the microbiome and alters gut physiology
Summary: The gastrointestinal (GI) tract is innervated by intrinsic neurons of the enteric nervous system (ENS) and extrinsic neurons of the central nervous system and peripheral ganglia. The GI tract also harbors a diverse microbiome, but interactions between the ENS and the microbiome remain poorl...
| Main Authors: | , , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-04-01
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| Series: | Cell Reports |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S221112472400281X |
| _version_ | 1797249156301979648 |
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| author | Jessica A. Griffiths Bryan B. Yoo Peter Thuy-Boun Victor J. Cantu Kelly C. Weldon Collin Challis Michael J. Sweredoski Ken Y. Chan Taren M. Thron Gil Sharon Annie Moradian Gregory Humphrey Qiyun Zhu Justin P. Shaffer Dennis W. Wolan Pieter C. Dorrestein Rob Knight Viviana Gradinaru Sarkis K. Mazmanian |
| author_facet | Jessica A. Griffiths Bryan B. Yoo Peter Thuy-Boun Victor J. Cantu Kelly C. Weldon Collin Challis Michael J. Sweredoski Ken Y. Chan Taren M. Thron Gil Sharon Annie Moradian Gregory Humphrey Qiyun Zhu Justin P. Shaffer Dennis W. Wolan Pieter C. Dorrestein Rob Knight Viviana Gradinaru Sarkis K. Mazmanian |
| author_sort | Jessica A. Griffiths |
| collection | DOAJ |
| description | Summary: The gastrointestinal (GI) tract is innervated by intrinsic neurons of the enteric nervous system (ENS) and extrinsic neurons of the central nervous system and peripheral ganglia. The GI tract also harbors a diverse microbiome, but interactions between the ENS and the microbiome remain poorly understood. Here, we activate choline acetyltransferase (ChAT)-expressing or tyrosine hydroxylase (TH)-expressing gut-associated neurons in mice to determine effects on intestinal microbial communities and their metabolites as well as on host physiology. The resulting multi-omics datasets support broad roles for discrete peripheral neuronal subtypes in shaping microbiome structure, including modulating bile acid profiles and fungal colonization. Physiologically, activation of either ChAT+ or TH+ neurons increases fecal output, while only ChAT+ activation results in increased colonic contractility and diarrhea-like fluid secretion. These findings suggest that specific subsets of peripherally activated neurons differentially regulate the gut microbiome and GI physiology in mice without involvement of signals from the brain. |
| first_indexed | 2024-04-24T20:26:00Z |
| format | Article |
| id | doaj.art-8903257bb5ea472f893d149c894884a6 |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-24T20:26:00Z |
| publishDate | 2024-04-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-8903257bb5ea472f893d149c894884a62024-03-22T05:39:13ZengElsevierCell Reports2211-12472024-04-01434113953Peripheral neuronal activation shapes the microbiome and alters gut physiologyJessica A. Griffiths0Bryan B. Yoo1Peter Thuy-Boun2Victor J. Cantu3Kelly C. Weldon4Collin Challis5Michael J. Sweredoski6Ken Y. Chan7Taren M. Thron8Gil Sharon9Annie Moradian10Gregory Humphrey11Qiyun Zhu12Justin P. Shaffer13Dennis W. Wolan14Pieter C. Dorrestein15Rob Knight16Viviana Gradinaru17Sarkis K. Mazmanian18Division of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA; Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network, Chevy Chase, MD 20815, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADepartments of Molecular Medicine and Integrative Structural and Computational Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USADepartment of Pediatrics, University of California, San Diego, San Diego, CA, USACollaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, San Diego, CA, USA; UCSD Center for Microbiome Innovation, University of California, San Diego, San Diego, CA, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USADepartment of Pediatrics, University of California, San Diego, San Diego, CA, USADepartment of Pediatrics, University of California, San Diego, San Diego, CA, USADepartment of Pediatrics, University of California, San Diego, San Diego, CA, USADepartments of Molecular Medicine and Integrative Structural and Computational Biology, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USADepartment of Pediatrics, University of California, San Diego, San Diego, CA, USA; Collaborative Mass Spectrometry Innovation Center, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, San Diego, CA, USA; UCSD Center for Microbiome Innovation, University of California, San Diego, San Diego, CA, USADepartment of Pediatrics, University of California, San Diego, San Diego, CA, USA; UCSD Center for Microbiome Innovation, University of California, San Diego, San Diego, CA, USA; Department of Computer Science and Engineering, University of California, San Diego, San Diego, CA, USA; Shu Chien-Gene Lay Department of Engineering, University of California, San Diego, San Diego, CA, USA; Halıcıoğlu Data Science Institute, University of California, San Diego, San Diego, CA, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA; Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network, Chevy Chase, MD 20815, USADivision of Biology & Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA; Aligning Science Across Parkinson’s (ASAP) Collaborative Research Network, Chevy Chase, MD 20815, USA; Corresponding authorSummary: The gastrointestinal (GI) tract is innervated by intrinsic neurons of the enteric nervous system (ENS) and extrinsic neurons of the central nervous system and peripheral ganglia. The GI tract also harbors a diverse microbiome, but interactions between the ENS and the microbiome remain poorly understood. Here, we activate choline acetyltransferase (ChAT)-expressing or tyrosine hydroxylase (TH)-expressing gut-associated neurons in mice to determine effects on intestinal microbial communities and their metabolites as well as on host physiology. The resulting multi-omics datasets support broad roles for discrete peripheral neuronal subtypes in shaping microbiome structure, including modulating bile acid profiles and fungal colonization. Physiologically, activation of either ChAT+ or TH+ neurons increases fecal output, while only ChAT+ activation results in increased colonic contractility and diarrhea-like fluid secretion. These findings suggest that specific subsets of peripherally activated neurons differentially regulate the gut microbiome and GI physiology in mice without involvement of signals from the brain.http://www.sciencedirect.com/science/article/pii/S221112472400281XCP: MicrobiologyCP: Neuroscience |
| spellingShingle | Jessica A. Griffiths Bryan B. Yoo Peter Thuy-Boun Victor J. Cantu Kelly C. Weldon Collin Challis Michael J. Sweredoski Ken Y. Chan Taren M. Thron Gil Sharon Annie Moradian Gregory Humphrey Qiyun Zhu Justin P. Shaffer Dennis W. Wolan Pieter C. Dorrestein Rob Knight Viviana Gradinaru Sarkis K. Mazmanian Peripheral neuronal activation shapes the microbiome and alters gut physiology Cell Reports CP: Microbiology CP: Neuroscience |
| title | Peripheral neuronal activation shapes the microbiome and alters gut physiology |
| title_full | Peripheral neuronal activation shapes the microbiome and alters gut physiology |
| title_fullStr | Peripheral neuronal activation shapes the microbiome and alters gut physiology |
| title_full_unstemmed | Peripheral neuronal activation shapes the microbiome and alters gut physiology |
| title_short | Peripheral neuronal activation shapes the microbiome and alters gut physiology |
| title_sort | peripheral neuronal activation shapes the microbiome and alters gut physiology |
| topic | CP: Microbiology CP: Neuroscience |
| url | http://www.sciencedirect.com/science/article/pii/S221112472400281X |
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