Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function
Background and aims As the importance of gut–brain interactions increases, understanding how specific gut microbes interact with the enteric nervous system (ENS), which is the first point of neuronal exposure becomes critical. Our aim was to understand how the dominant human gut bacterium Bacteroide...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2020-11-01
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| Series: | Gut Microbes |
| Subjects: | |
| Online Access: | http://dx.doi.org/10.1080/19490976.2020.1766936 |
| _version_ | 1818844618620403712 |
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| author | Rubina Aktar Nabil Parkar Regis Stentz Lucas Baumard Aimee Parker Andrew Goldson Arlaine Brion Simon Carding Ashley Blackshaw Madusha Peiris |
| author_facet | Rubina Aktar Nabil Parkar Regis Stentz Lucas Baumard Aimee Parker Andrew Goldson Arlaine Brion Simon Carding Ashley Blackshaw Madusha Peiris |
| author_sort | Rubina Aktar |
| collection | DOAJ |
| description | Background and aims As the importance of gut–brain interactions increases, understanding how specific gut microbes interact with the enteric nervous system (ENS), which is the first point of neuronal exposure becomes critical. Our aim was to understand how the dominant human gut bacterium Bacteroides thetaiotaomicron (Bt) regulates anatomical and functional characteristics of the ENS. Methods Neuronal cell populations, as well as enteroendocrine cells, were assessed in proximal colonic sections using fluorescent immunohistochemistry in specific pathogen-free (SPF), germ-free (GF) and Bt conventionalized-germ-free mice (Bt-CONV). RNA expression of tight junction proteins and toll-like receptors (TLR) were measured using qPCR. Colonic motility was analyzed using in vitro colonic manometry. Results Decreased neuronal and vagal afferent innervation observed in GF mice was normalized by Bt-CONV with increased neuronal staining in mucosa and myenteric plexus. Bt-CONV also restored expression of nitric oxide synthase expressing inhibitory neurons and of choline acetyltransferase and substance P expressing excitatory motor neurons comparable to those of SPF mice. Neurite outgrowth and glial cells were upregulated by Bt-CONV. RNA expression of tight junction protein claudin 3 was downregulated while TLR2 was upregulated by Bt-CONV. The enteroendocrine cell subtypes L-cells and enterochromaffin cells were reduced in GF mice, with Bt-CONV restoring L-cell numbers. Motility as measured by colonic migrating motor complexes (CMMCs) increased in GF and Bt-CONV. Conclusion Bt, common gut bacteria, is critical in regulating enteric neuronal and enteroendocrine cell populations, and neurogenic colonic activity. This highlights the potential use of this resident gut bacteria for maintaining healthy gut function. |
| first_indexed | 2024-12-19T05:16:38Z |
| format | Article |
| id | doaj.art-0a442b32ef8b4be1bc82cd908bbc88d6 |
| institution | Directory Open Access Journal |
| issn | 1949-0976 1949-0984 |
| language | English |
| last_indexed | 2024-12-19T05:16:38Z |
| publishDate | 2020-11-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj.art-0a442b32ef8b4be1bc82cd908bbc88d62022-12-21T20:34:38ZengTaylor & Francis GroupGut Microbes1949-09761949-09842020-11-011161745175710.1080/19490976.2020.17669361766936Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic functionRubina Aktar0Nabil Parkar1Regis Stentz2Lucas Baumard3Aimee Parker4Andrew Goldson5Arlaine Brion6Simon Carding7Ashley Blackshaw8Madusha Peiris9Queen Mary University of LondonQueen Mary University of LondonQuadram Institute BioscienceQueen Mary University of LondonQuadram Institute BioscienceQuadram Institute BioscienceQuadram Institute BioscienceQuadram Institute BioscienceQueen Mary University of LondonQueen Mary University of LondonBackground and aims As the importance of gut–brain interactions increases, understanding how specific gut microbes interact with the enteric nervous system (ENS), which is the first point of neuronal exposure becomes critical. Our aim was to understand how the dominant human gut bacterium Bacteroides thetaiotaomicron (Bt) regulates anatomical and functional characteristics of the ENS. Methods Neuronal cell populations, as well as enteroendocrine cells, were assessed in proximal colonic sections using fluorescent immunohistochemistry in specific pathogen-free (SPF), germ-free (GF) and Bt conventionalized-germ-free mice (Bt-CONV). RNA expression of tight junction proteins and toll-like receptors (TLR) were measured using qPCR. Colonic motility was analyzed using in vitro colonic manometry. Results Decreased neuronal and vagal afferent innervation observed in GF mice was normalized by Bt-CONV with increased neuronal staining in mucosa and myenteric plexus. Bt-CONV also restored expression of nitric oxide synthase expressing inhibitory neurons and of choline acetyltransferase and substance P expressing excitatory motor neurons comparable to those of SPF mice. Neurite outgrowth and glial cells were upregulated by Bt-CONV. RNA expression of tight junction protein claudin 3 was downregulated while TLR2 was upregulated by Bt-CONV. The enteroendocrine cell subtypes L-cells and enterochromaffin cells were reduced in GF mice, with Bt-CONV restoring L-cell numbers. Motility as measured by colonic migrating motor complexes (CMMCs) increased in GF and Bt-CONV. Conclusion Bt, common gut bacteria, is critical in regulating enteric neuronal and enteroendocrine cell populations, and neurogenic colonic activity. This highlights the potential use of this resident gut bacteria for maintaining healthy gut function.http://dx.doi.org/10.1080/19490976.2020.1766936bacteroides thetaiotaomicrongut microbiomeenteric nervous systemneuronal plasticitycolonic motility |
| spellingShingle | Rubina Aktar Nabil Parkar Regis Stentz Lucas Baumard Aimee Parker Andrew Goldson Arlaine Brion Simon Carding Ashley Blackshaw Madusha Peiris Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function Gut Microbes bacteroides thetaiotaomicron gut microbiome enteric nervous system neuronal plasticity colonic motility |
| title | Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function |
| title_full | Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function |
| title_fullStr | Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function |
| title_full_unstemmed | Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function |
| title_short | Human resident gut microbe Bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function |
| title_sort | human resident gut microbe bacteroides thetaiotaomicron regulates colonic neuronal innervation and neurogenic function |
| topic | bacteroides thetaiotaomicron gut microbiome enteric nervous system neuronal plasticity colonic motility |
| url | http://dx.doi.org/10.1080/19490976.2020.1766936 |
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