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Nutrients activate distinct patterns of small-intestinal enteric neurons

  • Bertrand, P. P. The cornucopia of intestinal chemosensory transduction. Front. Neurosci. 3, 48 (2009).

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Neunlist, M. & Schemann, M. Nutrient-induced changes in the phenotype and function of the enteric nervous system. J. Physiol. 592, 2959–2965 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fung, C. & Vanden Berghe, P. Functional circuits and signal processing in the enteric nervous system. Cell. Mol. Life Sci. 77, 4505–4522 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Furness, J. B. The enteric nervous system and neurogastroenterology. Nat. Rev. Gastroenterol. Hepatol. 9, 286–294 (2012).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Buchanan, K. L. et al. The preference for sugar over sweetener depends on a gut sensor cell. Nat. Neurosci. 25, 191–200 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao, Q. et al. A multidimensional coding architecture of the vagal interoceptive system. Nature 603, 878–884 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schemann, M. & Ehrlein, H. J. Postprandial patterns of canine jejunal motility and transit of luminal content. Gastroenterology 90, 991–1000 (1986).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Nocerino, A., Iafusco, M. & Guandalini, S. Cholera toxin-induced small intestinal secretion has a secretory effect on the colon of the rat. Gastroenterology 108, 34–39 (1995).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fung, C., Ellis, M. & Bornstein, J. C. Luminal cholera toxin alters motility in isolated guinea-pig jejunum via a pathway independent of 5-HT3 receptors. Front. Neurosci. 4, 162 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schneider, S., Wright, C. M. & Heuckeroth, R. O. Unexpected roles for the second brain: enteric nervous system as master regulator of bowel function. Annu. Rev. Physiol. 81, 235–259 (2019).

    Article 
    PubMed 

    Google Scholar
     

  • Spencer, N. J. & Hu, H. Enteric nervous system: sensory transduction, neural circuits and gastrointestinal motility. Nat. Rev. Gastroenterol. Hepatol. 17, 338–351 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mercado-Perez, A. & Beyder, A. Gut feelings: mechanosensing in the gastrointestinal tract. Nat. Rev. Gastroenterol. Hepatol. 19, 283–296 (2022).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Alcaino, C. et al. A population of gut epithelial enterochromaffin cells is mechanosensitive and requires Piezo2 to convert force into serotonin release. Proc. Natl Acad. Sci. USA 115, E7632–E7641 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Furness, J. B., Rivera, L. R., Cho, H.-J., Bravo, D. M. & Callaghan, B. The gut as a sensory organ. Nat. Rev. Gastroenterol. Hepatol. 10, 729 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Husted, A. S., Trauelsen, M., Rudenko, O., Hjorth, S. A. & Schwartz, T. W. GPCR-mediated signaling of metabolites. Cell Metab. 25, 777–796 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Worthington, J. J., Reimann, F. & Gribble, F. M. Enteroendocrine cells-sensory sentinels of the intestinal environment and orchestrators of mucosal immunity. Mucosal Immunol. 11, 3–20 (2018).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lasrado, R. et al. Lineage-dependent spatial and functional organization of the mammalian enteric nervous system. Science 356, 722–726 (2017).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Song, Z. M., Brookes, S. J. & Costa, M. Identification of myenteric neurons which project to the mucosa of the guinea-pig small intestine. Neurosci. Lett. 129, 294–298 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Song, Z. M., Brookes, S. J., Steele, P. A. & Costa, M. Projections and pathways of submucous neurons to the mucosa of the guinea-pig small intestine. Cell Tissue Res. 269, 87–98 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Martin, A. M. et al. The nutrient-sensing repertoires of mouse enterochromaffin cells differ between duodenum and colon. Neurogastroenterol. Motil. 29, e13046 (2017).

    Article 
    ADS 

    Google Scholar
     

  • Martin, A. M. et al. Regional differences in nutrient‐induced secretion of gut serotonin. Physiol. Rep. 5, e13199 (2017).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gribble, F. M. & Reimann, F. Function and mechanisms of enteroendocrine cells and gut hormones in metabolism. Nat. Rev. Endocrinol. 15, 226–237 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rogers, G. J. et al. Electrical activity-triggered glucagon-like peptide-1 secretion from primary murine L-cells. J. Physiol. 589, 1081–1093 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bellono, N. W. et al. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 170, 185–198 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mongardi Fantaguzzi, C., Thacker, M., Chiocchetti, R. & Furness, J. B. Identification of neuron types in the submucosal ganglia of the mouse ileum. Cell Tissue Res. 336, 179–189 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Qu, Z. D. et al. Immunohistochemical ***ysis of neuron types in the mouse small intestine. Cell Tissue Res. 334, 147–161 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Morarach, K. et al. Diversification of molecularly defined myenteric neuron cl***es revealed by single-cell RNA sequencing. Nat. Neurosci. 24, 34–46 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liu, M., Seino, S. & Kirchgessner, A. L. Identification and characterization of glucoresponsive neurons in the enteric nervous system. J. Neurosci. 19, 10305 (1999).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hao, M. M. et al. Development of the intrinsic innervation of the small bowel mucosa and villi. Am. J. Physiol. Gastrointest. Liver Physiol. 318, G53–G65 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fung, C. et al. Luminal short chain fatty acids and 5-HT acutely activate myenteric neurons in the mouse proximal colon. Neurogastroenterol. Motil. 33, e14186 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Haber, A. L. et al. A single-cell survey of the small intestinal epithelium. Nature 551, 333–339 (2017).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Drokhlyansky, E. et al. The human and mouse enteric nervous system at single-cell resolution. Cell 182, 1606–1622 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Inoue, T. et al. Mizagliflozin, a novel selective SGLT1 inhibitor, exhibits potential in the amelioration of chronic constipation. Eur. J. Pharmacol. 806, 25–31 (2017).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Akalestou, E. et al. Intravital imaging of islet Ca2+ dynamics reveals enhanced β cell connectivity after bariatric surgery in mice. Nat. Commun. 12, 5165 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, T., Perkins, M. H., Chang, H., Han, W. & de Araujo, I. E. An inter-organ neural circuit for appetite suppression. Cell 185, 2478–2494 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gershon, M. D. & Tack, J. The serotonin signaling system: from basic understanding to drug development for functional gi disorders. Gastroenterology 132, 397–414 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bertrand, P. P., Kunze, W. A., Bornstein, J. C., Furness, J. B. & Smith, M. L. Analysis of the responses of myenteric neurons in the small intestine to chemical stimulation of the mucosa. Am. J. Physiol. 273, G422–G435 (1997).

    CAS 
    PubMed 

    Google Scholar
     

  • Bertrand, P. P., Kunze, W. A., Furness, J. B. & Bornstein, J. C. The terminals of myenteric intrinsic primary afferent neurons of the guinea-pig ileum are excited by 5-hydroxytryptamine acting at 5-hydroxytryptamine-3 receptors. Neuroscience 101, 459–469 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cooke, H. J., Wunderlich, J. & Christofi, F. L. ‘The force be with you’: ATP in gut mechanosensory transduction. News Physiol. Sci. 18, 43–49 (2003).

    CAS 
    PubMed 

    Google Scholar
     

  • Bertrand, P. P. & Bornstein, J. C. ATP as a putative sensory mediator: activation of intrinsic sensory neurons of the myenteric plexus via P2X receptors. Neuroscience 22, 4767–4775 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vanden Berghe, P. et al. Neurochemical coding of myenteric neurons in the guinea-pig antrum. Cell Tissue Res. 297, 81–90 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pan, H. & Gershon, M. D. Activation of intrinsic afferent pathways in submucosal ganglia of the guinea pig small intestine. J. Neurosci. 20, 3295–3309 (2000).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mazzuoli-Weber, G. & Schemann, M. Mechanosensitivity in the enteric nervous system. Front. Cell. Neurosci. 9, 408 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gershon, M. D. in The Enteric Nervous System II (eds Spencer, N. J. et al.) 307–318 (Springer, 2022).

  • Koo, A., Fothergill, L. J., Kuramoto, H. & Furness, J. B. 5-HT containing enteroendocrine cells characterised by morphologies, patterns of hormone co-expression, and relationships with nerve fibres in the mouse gastrointestinal tract. Histochem. Cell Biol. 155, 623–636 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Touhara, K. K. et al. Topological segregation of stress sensors along the gut crypt–villus axis. Nature 640, 732–742 (2025).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Su, C. Y., Menuz, K. & Carlson, J. R. Olfactory perception: receptors, cells, and circuits. Cell 139, 45–59 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Furness, J. B., Jones, C., Nurgali, K. & Clerc, N. Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog. Neurobiol. 72, 143–164 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • de Souza Melo, C. G. et al. Identification of intrinsic primary afferent neurons in mouse jejunum. Neurogastroenterol. Motil. 32, e13989 (2020).

    Article 
    PubMed Central 

    Google Scholar
     

  • Moore, B. A. & Vanner, S. Properties of synaptic inputs from myenteric neurons innervating submucosal S neurons in guinea pig ileum. Am. J. Physiol. Gastrointest. Liver Physiol. 278, G273–G280 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Monro, R. L., Bornstein, J. C. & Bertrand, P. P. Synaptic transmission from the submucosal plexus to the myenteric plexus in guinea-pig ileum. Neurogastroenterol. Motil. 20, 1165–1173 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vanden Berghe, P. & Fung, C. in The Enteric Nervous System II (eds Spencer, N. J. et al) 71–79 (Springer, 2022).

  • Heanue, T. A., Shepherd, I. T. & Burns, A. J. Enteric nervous system development in avian and zebrafish models. Dev. Biol. 417, 129–138 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zariwala, H. A. et al. A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J. Neurosci. 32, 3131–3141 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. & McMahon, A. P. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 8, 1323–1326 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • el Marjou, F. et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39, 186–193 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Vanden Berghe, P., Kenyon, J. L. & Smith, T. K. Mitochondrial Ca2+ uptake regulates the excitability of myenteric neurons. J. Neurosci. 22, 6962–6971 (2002).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Furness, J. B., Koopmans, H. S., Robbins, H. L. & Lin, H. C. Identification of intestinofugal neurons projecting to the coeliac and superior mesenteric ganglia in the rat. Auton. Neurosci. 83, 81–85 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tan, L. L., Bornstein, J. C. & Anderson, C. R. The neurochemistry and innervation patterns of extrinsic sensory and sympathetic nerves in the myenteric plexus of the C57Bl6 mouse jejunum. Neuroscience 166, 564–579 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Timmermans, J.-P. et al. Occurrence, distribution and neurochemical features of small intestinal neurons projecting to the cranial mesenteric ganglion in the pig. Cell Tissue Res. 272, 49–58 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • T***icker, B. C., Hennig, G. W., Costa, M. & Brookes, S. J. H. Rapid anterograde and retrograde tracing from mesenteric nerve trunks to the guinea-pig small intestine in vitro. Cell Tissue Res. 295, 437–452 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Preibisch, S., Saalfeld, S., Schindelin, J. & Tomancak, P. Software for bead-based registration of selective plane illumination microscopy data. Nat. Methods 7, 418–419 (2010).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ventura, E. E., Davis, J. N. & Goran, M. I. Sugar content of popular sweetened beverages based on objective laboratory ***ysis: focus on fructose content. Obesity 19, 868–874 (2011).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Akiba, Y. et al. Short-chain fatty acid sensing in rat duodenum. J. Physiol. 593, 585–599 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Reitelseder, S. et al. Phenylalanine stable isotope tracer labeling of cow milk and meat and human experimental applications to study dietary protein-derived amino acid availability. Clin. Nutr. 39, 3652–3662 (2020).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li, Z. et al. Regional complexity in enteric neuron wiring reflects diversity of motility patterns in the mouse large intestine. eLife 8, e42914 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wang, Y. et al. Accurate quantification of astrocyte and neurotransmitter fluorescence dynamics for single-cell and population-level physiology. Nat. Neurosci. 22, 1936–1944 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

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