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Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells
Open accessAbstract
Satiety and other core physiological functions are modulated by sensory signals arising from the surface of the gut. Luminal nutrients and bacteria stimulate epithelial biosensors called enteroendocrine cells. Despite being electrically excitable, enteroendocrine cells are generally thought to communicate indirectly with nerves through hormone secretion and not through direct cell-nerve contact. However, we recently uncovered in intestinal enteroendocrine cells a cytoplasmic process that we named neuropod. Here, we determined that neuropods provide a direct connection between enteroendocrine cells and neurons innervating the small intestine and colon. Using cell-specific transgenic mice to study neural circuits, we found that enteroendocrine cells have the necessary elements for neurotransmission, including expression of genes that encode pre-, post-, and transsynaptic proteins. This neuroepithelial circuit was reconstituted in vitro by coculturing single enteroendocrine cells with sensory neurons. We used a monosynaptic rabies virus to define the circuit's functional connectivity in vivo and determined that delivery of this neurotropic virus into the colon lumen resulted in the infection of mucosal nerves through enteroendocrine cells. This neuroepithelial circuit can serve as both a sensory conduit for food and gut microbes to interact with the nervous system and a portal for viruses to enter the enteric and central nervous systems.
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“A basolateral cytoplasmic process of the L cells -the neuropod -was shown to establish a functional synaptic contact with the enteric glia and vagal afferents.”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Bohorquez et al., 2015
Experimental — accuracy not yet measuredIn the citing paper
“Enteroendocrine and enterochromaffin cells (ECCs) form close synaptic connections with certain vagal afferent fibers through cell extensions called neuropods [25, 26].”
From Role of diet and its effects on the gut microbiome in the pathophysiology of mental disorders (2022) · cites this paper as [26]
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Alway, E., Reicher, N., & Bohórquez, D. V. (2024) · Genes & Development · doi:10.1101/gad.352279.124 · Cited by 2
“These cells detect signals within the gut lumen and instantly transmit them to the brain via the vagus nerve, influencing our food choices in real time (Bohórquez et al. 2015; Kael-berer et al. 2018; Buchanan et al. 2022).”
BackgroundSelf-citationChilders, L., Park, J., Wang, S., Liu, R., Barry, R. J., Watts, S. A., Rawls, J. F., & Bagnat, M. (2025) · eLife · doi:10.7554/elife.100611.2 · Cited by 3
The interactions between gut and brain in psychiatric and neurological disorders
Shin, C., & Kim, Y. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821927-0.00010-3 · Cited by 1
Salazar, V., Bolaños, P., & del Castillo, J. R. (2023) · Journal of Histochemistry & Cytochemistry · doi:10.1369/00221554231203038 · Cited by 1
“Recently Bohórquez et al. 53 identified synaptic links between epithelial sensory cells and nerves in the colon, using co-culture of cholecystokinin-green fluorescent protein (CCK-GFP) cells purified by cell sorting and sensory neurons dissociated from sensory ganglia by enzymatic digestion.”
BackgroundEndocrine Properties of Microbiota
Sobol, K. V. (2024) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093024070019 · Cited by 2
“EECs are integrated into the host nervous network through both the pro(cid:2) duction of active substances and synaptic communi(cid:2) cation with ENS efferent and afferent fibers [126] (Fig.”
The gut and heart’s role in reward processing
Arinel, M., & Abdelaal, K. (2025) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2025.1479923 · Cited by 3
A neurobiotic sense curbs feeding: a new frontier in gut–brain communication
Singh, R. (2025) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-025-01126-z · Cited by 1
Iba, K., Kitano, R., & Iwasaki, Y. (2025) · Physiological Reports · doi:10.14814/phy2.70636 · Cited by 2
Hartenstein, V., Sprecher, S., & Martinez, P. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00043-9 · Cited by 1
The brain–gut–joint axis in arthritis: crosstalk, treatment, and future perspectives
Zhong, S., Li, F., Li, D., Cheng, Y., Wang, X., Gao, Y., & Xie, X. (2026) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2025.101045 · Cited by 3
The Neuroepithelial Landscape of Enterochromaffin Cells Varies Across Gastrointestinal Location
Jones, L. A., Coleman, R., Allman, C., Humenick, A., Martin, A. M., Thorpe, D. W., Eyre, N. S., & Keating, D. J. (2026) · Neurogastroenterology & Motility · doi:10.1111/nmo.70221 · Cited by 1
“Since the discovery of EEC projections, they have been termed “basal processes” [12], “pseudopod-like basal cellular” processes [13], and most recently “neuropods” [7, 8, 14].”
InfluentialRakhat, Y., Banno, S., Zhantleu, D., Tsunekawa, S., Yabe, D., Seino, Y., Iwasaki, Y., & Yada, T. (2026) · Nutrients · doi:10.3390/nu18040707 · Cited by 2
Enteric nervous system in exercise physiology: a microbiota-neural interface
Chen, H.-L., Huang, J.-T., Guo, J.-J., & Wang, L.-S. (2026) · npj Metabolic Health and Disease · doi:10.1038/s44324-026-00106-4 · Cited by 1
Jia, X., Simo, L., Rosenfeld, S., Li, F., Zhou, Y., Ding, Y., & Geng, X. (2026) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2026.1735569 · Cited by 1
Barros, H. D. D. F. Q., Casagrande, B. P., Araújo, D. D., Mutran, T. A. J., Telles, M. M., Estadella, D., & Pisani, L. P. (2026) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-026-10038-5 · Cited by 3
“Through specialized synapse-like structures called neuropods, EECs form direct contact with vagal afferent fibers, enabling rapid transmission of gut-derived signals to the brainstem [70, 71, 123].”
D’Alessio, D. A., & Campbell, J. E. (2026) · Diabetes Obesity and Metabolism · doi:10.1111/dom.70894 · Cited by 1
Ngoumou, G. B., Schepanski, S. N., Nejati, F., Diedering, A., Cassagnau, N., Beyrow, C., Wicaksono, W. A., Berg, G., & Seifert, G. (2026) · Frontiers in Nutrition · doi:10.3389/fnut.2026.1903488 · Cited by 1
Clinical and Pre-Clinical Evidence for Enteric α-Synuclein Involvement in Parkinson's Disease
Kochman, E. M., Akhtar, K., Ali, A., & Shin Damian, S. (2021) · International Journal of Neurodegenerative Disorders · doi:10.23937/2643-4539/1710019 · Cited by 2
Spreading of alpha-synuclein pathology from the gut to the brain in Parkinson's disease
Jevans, B., & Monte, D. A. D. (2021) · International review of movement disorders · doi:10.1016/bs.irmvd.2021.08.004 · Cited by 1
Epithelial-Neuronal Communication in Visceral Pain
Najjar, S. A. (2023) · Springer eBooks · doi:10.1007/978-3-031-25702-5_9 · Cited by 1
Crop Responses to Metal Toxicity
Muhammad, S., Ashraf, S., Mukhtiar, M., Ul‐Allah, S., Hasan, Z., Azeem, A., Shah, J. M., Gull, R., & Javed, I. (2023) · Springer eBooks · doi:10.1007/978-3-031-37424-1_10 · Cited by 1
Enteroendocrine Cells Sense Sucrose and Alter Enteric Neuron Excitability via Insulin Signaling
Snyder, J. R., Ahmed, M., Bhave, S. M., Hotta, R., Koppes, R. A., Goldstein, A. M., & Koppes, A. N. (2024) · Advanced Biology · doi:10.1002/adbi.202300566 · Cited by 1
Enterochromaffin cells and gastrointestinal diseases
Zhu, M.-J., Yang, Z., Wang, F., Di, Z.-S., Wang, Y.-X., Li, L., & Xu, J. (2019) · World Chinese Journal of Digestology · doi:10.11569/wcjd.v27.i2.117 · Cited by 1
Self-citationAndrews, P. L. R., Li, S., Meli, F., Vinson, P., Broening, H. W., & Nash, J. F. (2020) · Food and Chemical Toxicology · doi:10.1016/j.fct.2020.111553 · Cited by 1
Functional morphology of the glandular esophageal pouches of chitons (Mollusca, Polyplacophora)
Lobo‐da‐Cunha, A., Alves, Â., Oliveira, E., & Calado, G. (2020) · Journal of Morphology · doi:10.1002/jmor.21309 · Cited by 1
“…and nerve terminals that were observed in the esophageal pouches of chitons, and in other animals (Alba et al., 1988; García-Arrarás et al., 2019), are part of a neuroepithelial circuit that provides an interaction between digestive tract content and the nervous system (Bohórquez et al., 2015).”
BackgroundThe Role of Vagal Afferent Nerves in Feeding Regulation
Ohbayashi, K., Nohmi, T., & Iwasaki, Y. (2023) · Nippon Eiyo Shokuryo Gakkaishi · doi:10.4327/jsnfs.76.95 · Cited by 1
Functional amyloids in the microbiomes of a rat Parkinson’s disease model and wild-type ratsPreprint
Christensen, L. F. B., Alijanvand, S. H., Burdukiewicz, M. J., Herbst, F., Kjeldal, H., Dueholm, M. S., & Otzen, D. E. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.03.31.438001 · Cited by 1
“Enteric nerve fibers extend through the different layers of the GI tract and have been shown to connect directly with enteroendocrine cells (EECs) [15].”
BackgroundNeto, D. P. A., Bosque, B. P., de Godoy, J. V. P., Rodrigues, P. V., Meneses, D. D., Tostes, K., Tonoli, C. C. C., González-Billault, C. E., & Fonseca, M. D. C. (2021) · Research Square · doi:10.21203/rs.3.rs-696660/v1 · Cited by 1
Metadata
- Authors
- Bohórquez, D. V., Shahid, R. A., Erdmann, A., Kreger, A. M., Wang, Y., Calakos, N., Wang, F., & Liddle, R. A.
- Affiliations
- Duke Medical Center (US)
- Durham VA Medical Center (US)
- Venue
- Journal of Clinical Investigation
- Published
- 2015-01-02
- Volume
- 125
- Issue
- 2
- Pages
- 782-786
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC4319442
- OpenAlex
- W2119429325
- Cited by
- 484
- References
- 28
- Citations by year
- 2026: 42 · 2025: 51 · 2024: 45 · 2023: 45 · 2022: 47 · 2021: 60 · 2020: 47 · 2019: 38 · 2018: 41 · 2017: 22 · 2016: 29 · 2015: 17
- FWCI
- 38.12
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DukeSpace (Duke University) (submittedVersion)
- DukeSpace (Duke University) (submittedVersion, cc-by-nc-nd)
- Funders
- U.S. Department of Veterans Affairs (I01 BX002230)
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (F32DK094704, R01DK098796, R01DK091946, K01DK103832)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- enteroendocrine cells, sensory neurons, enteric nervous system, neurotransmission, gut-brain signaling, satiety, rabies virus, small intestine
- MeSH terms
- Animals, Cell Communication, Cells, Cultured, Colon, Intestine, Small, Coculture Techniques, Enteroendocrine Cells, Neuroepithelial Cells, Mice
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