Gut enterochromaffin cells drive visceral pain and anxiety.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
06
04
2022
accepted:
10
02
2023
medline:
7
4
2023
pubmed:
24
3
2023
entrez:
23
3
2023
Statut:
ppublish
Résumé
Gastrointestinal (GI) discomfort is a hallmark of most gut disorders and represents an important component of chronic visceral pain
Identifiants
pubmed: 36949192
doi: 10.1038/s41586-023-05829-8
pii: 10.1038/s41586-023-05829-8
doi:
Substances chimiques
Serotonin
333DO1RDJY
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
137-142Subventions
Organisme : NIA NIH HHS
ID : R01 AG062331
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK063592
Pays : United States
Organisme : NIDDK NIH HHS
ID : T32 DK007762
Pays : United States
Organisme : NINDS NIH HHS
ID : U01 NS113869
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS105038
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK121657
Pays : United States
Organisme : NIDDK NIH HHS
ID : R03 DK121061
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK128346
Pays : United States
Commentaires et corrections
Type : CommentIn
Type : CommentIn
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Enck, P. et al. Irritable bowel syndrome. Nat. Rev. Dis. Primers 2, 16014 (2016).
pubmed: 27159638
pmcid: 5001845
doi: 10.1038/nrdp.2016.14
Grundy, L., Erickson, A. & Brierley, S. M. Visceral pain. Annu. Rev. Physiol. 81, 261–284 (2019).
pubmed: 30379615
doi: 10.1146/annurev-physiol-020518-114525
Bellono, N. W. et al. Enterochromaffin cells are gut chemosensors that couple to sensory neural pathways. Cell 170, 185–198 (2017).
pubmed: 28648659
pmcid: 5839326
doi: 10.1016/j.cell.2017.05.034
Racke, K. & Schworer, H. Characterization of the role of calcium and sodium channels in the stimulus secretion coupling of 5-hydroxytryptamine release from porcine enterochromaffin cells. Naunyn Schmiedebergs Arch. Pharmacol. 347, 1–8 (1993).
pubmed: 7680436
doi: 10.1007/BF00168764
Strege, P. R. et al. Sodium channel Na
pubmed: 29142310
pmcid: 5688111
doi: 10.1038/s41598-017-15834-3
Gershon, M. D. Serotonin is a sword and a shield of the bowel: serotonin plays offense and defense. Trans. Am. Clin. Climatol. Assoc. 123, 268–280 (2012).
pubmed: 23303993
pmcid: 3540639
Koh, A., De Vadder, F., Kovatcheva-Datchary, P. & Bäckhed, F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell 165, 1332–1345 (2016).
pubmed: 27259147
doi: 10.1016/j.cell.2016.05.041
Farup, P. G., Rudi, K. & Hestad, K. Faecal short-chain fatty acids—a diagnostic biomarker for irritable bowel syndrome? BMC Gastroenterol. 16, 51 (2016).
pubmed: 27121286
pmcid: 4847229
doi: 10.1186/s12876-016-0446-z
Gribble, F. M. & Reimann, F. Enteroendocrine cells: chemosensors in the intestinal epithelium. Annu. Rev. Physiol. 78, 277–299 (2016).
pubmed: 26442437
doi: 10.1146/annurev-physiol-021115-105439
Gribble, F. M. & Reimann, F. Function and mechanisms of enteroendocrine cells and gut hormones in metabolism. Nat. Rev. Endocrinol. 15, 226–237 (2019).
pubmed: 30760847
doi: 10.1038/s41574-019-0168-8
Liddle, R. A. Neuropods. Cell Mol. Gastroenterol. Hepatol. 7, 739–747 (2019).
pubmed: 30710726
pmcid: 6463090
doi: 10.1016/j.jcmgh.2019.01.006
Kaelberer, M. M. et al. A gut–brain neural circuit for nutrient sensory transduction. Science 361, eaat5236 (2018).
pubmed: 30237325
pmcid: 6417812
doi: 10.1126/science.aat5236
Treichel, A. J. et al. Specialized mechanosensory epithelial cells in mouse gut intrinsic tactile sensitivity. Gastroenterology 162, 535–547 (2022).
Nozawa, K. et al. TRPA1 regulates gastrointestinal motility through serotonin release from enterochromaffin cells. Proc. Natl Acad. Sci. USA 106, 3408–3413 (2009).
pubmed: 19211797
pmcid: 2651261
doi: 10.1073/pnas.0805323106
Mawe, G. M. & Hoffman, J. M. Serotonin signalling in the gut—functions, dysfunctions and therapeutic targets. Nat. Rev. Gastroenterol. Hepatol. 10, 473–486 (2013).
pubmed: 23797870
pmcid: 4048923
doi: 10.1038/nrgastro.2013.105
Osteen, J. D. et al. Selective spider toxins reveal a role for the Na
pubmed: 27281198
pmcid: 4919188
doi: 10.1038/nature17976
Sadeghi, M. et al. Contribution of membrane receptor signalling to chronic visceral pain. Int. J. Biochem. Cell Biol. 98, 10–23 (2018).
pubmed: 29477359
doi: 10.1016/j.biocel.2018.02.017
Lu, V. B., Gribble, F. M. & Reimann, F. Free fatty acid receptors in enteroendocrine cells. Endocrinology 159, 2826–2835 (2018).
pubmed: 29688303
doi: 10.1210/en.2018-00261
Mars, R. A. T. et al. Longitudinal multi-omics reveals subset-specific mechanisms underlying irritable bowel syndrome. Cell 182, 1460–1473 (2020).
pubmed: 32916129
pmcid: 8109273
doi: 10.1016/j.cell.2020.08.007
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).
pubmed: 30037999
pmcid: 6094143
doi: 10.1073/pnas.1804938115
Wang, F. et al. Mechanosensitive ion channel Piezo2 is important for enterochromaffin cell response to mechanical forces. J. Physiol. 595, 79–91 (2017).
pubmed: 27392819
doi: 10.1113/JP272718
Brierley, S. M., Jones, R. C. 3rd, Gebhart, G. F. & Blackshaw, L. A. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127, 166–178 (2004).
pubmed: 15236183
doi: 10.1053/j.gastro.2004.04.008
Daou, I. et al. Remote optogenetic activation and sensitization of pain pathways in freely moving mice. J. Neurosci. 33, 18631–18640 (2013).
pubmed: 24259584
pmcid: 6618811
doi: 10.1523/JNEUROSCI.2424-13.2013
Kim, J. C. et al. Linking genetically defined neurons to behavior through a broadly applicable silencing allele. Neuron 63, 305–315 (2009).
pubmed: 19679071
pmcid: 2814245
doi: 10.1016/j.neuron.2009.07.010
Jensen, P. et al. Redefining the serotonergic system by genetic lineage. Nat. Neurosci. 11, 417–419 (2008).
pubmed: 18344997
pmcid: 2897136
doi: 10.1038/nn2050
Erspamer, V. & Asero, B. Identification of enteramine, the specific hormone of the enterochromaffin cell system, as 5-hydroxytryptamine. Nature 169, 800–801 (1952).
pubmed: 14941051
doi: 10.1038/169800b0
Spohn, S. N. & Mawe, G. M. Non-conventional features of peripheral serotonin signalling—the gut and beyond. Nat. Rev. Gastroenterol. Hepatol. 14, 412–420 (2017).
pubmed: 28487547
pmcid: 5672796
doi: 10.1038/nrgastro.2017.51
Brierley, S. M., Hibberd, T. J. & Spencer, N. J. Spinal afferent innervation of the colon and rectum. Front. Cell Neurosci. 12, 467 (2018).
pubmed: 30564102
pmcid: 6288476
doi: 10.3389/fncel.2018.00467
Uhlig, F. et al. Identification of a quorum sensing-dependent communication pathway mediating bacteria–gut–brain cross talk. iScience 23, 101695 (2020).
pubmed: 33163947
pmcid: 7607502
doi: 10.1016/j.isci.2020.101695
Makadia, P. A. et al. Optogenetic activation of colon epithelium of the mouse produces high-frequency bursting in extrinsic colon afferents and engages visceromotor responses. J. Neurosci. 38, 5788–5798 (2018).
pubmed: 29789376
pmcid: 6010562
doi: 10.1523/JNEUROSCI.0837-18.2018
Grundy, L. et al. Chronic linaclotide treatment reduces colitis-induced neuroplasticity and reverses persistent bladder dysfunction. JCI Insight 3, e121841 (2018).
pubmed: 30282832
pmcid: 6237488
doi: 10.1172/jci.insight.121841
Najjar, S. A. et al. Optogenetic inhibition of the colon epithelium reduces hypersensitivity in a mouse model of inflammatory bowel disease. Pain 162, 1126–1134 (2021).
pubmed: 33048854
pmcid: 7969374
doi: 10.1097/j.pain.0000000000002110
Jones, R. C. 3rd, Xu, L. & Gebhart, G. F. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J. Neurosci. 25, 10981–10989 (2005).
pubmed: 16306411
pmcid: 6725875
doi: 10.1523/JNEUROSCI.0703-05.2005
Castro, J. et al. Activation of pruritogenic TGR5, MrgprA3, and MrgprC11 on colon-innervating afferents induces visceral hypersensitivity. JCI Insight 4, e131712 (2019).
pubmed: 31536477
pmcid: 6824308
doi: 10.1172/jci.insight.131712
Fothergill, L. J. & Furness, J. B. Diversity of enteroendocrine cells investigated at cellular and subcellular levels: the need for a new classification scheme. Histochem. Cell Biol. 150, 693–702 (2018).
pubmed: 30357510
pmcid: 6447040
doi: 10.1007/s00418-018-1746-x
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).
pubmed: 33608804
doi: 10.1007/s00418-021-01972-3
Lumsden, A. L. et al. Sugar responses of human enterochromaffin cells depend on gut region, sex, and body mass. Nutrients 11, 234 (2019).
pubmed: 30678223
pmcid: 6412251
doi: 10.3390/nu11020234
Bohórquez, D. V. et al. Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J. Clin. Invest. 125, 782–786 (2015).
pubmed: 25555217
pmcid: 4319442
doi: 10.1172/JCI78361
Brenner, D. M. & Sayuk, G. S. Current US Food and Drug Administration-approved pharmacologic therapies for the treatment of irritable bowel syndrome with diarrhea. Adv. Ther. 37, 83–96 (2020).
pubmed: 31707713
doi: 10.1007/s12325-019-01116-z
Bradesi, S. et al. Dual role of 5-HT
pubmed: 17161536
doi: 10.1016/j.pain.2006.10.028
Miranda, A., Peles, S., McLean, P. G. & Sengupta, J. N. Effects of the 5-HT
pubmed: 16844296
doi: 10.1016/j.pain.2006.06.014
El-Ayache, N. & Galligan, J. J. 5-HT
pubmed: 30359082
doi: 10.1152/ajpgi.00131.2018
Hicks, G. A. et al. Excitation of rat colonic afferent fibres by 5-HT(3) receptors. J. Physiol. 544, 861–869 (2002).
pubmed: 12411529
pmcid: 2290619
doi: 10.1113/jphysiol.2002.025452
Ji, Y., Tang, B. & Traub, R. J. The visceromotor response to colorectal distention fluctuates with the estrous cycle in rats. Neuroscience 154, 1562–1567 (2008).
pubmed: 18550290
doi: 10.1016/j.neuroscience.2008.04.070
Gustafsson, J. K. & Greenwood-Van Meerveld, B. Amygdala activation by corticosterone alters visceral and somatic pain in cycling female rats. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G1080–G1085 (2011).
pubmed: 21454447
doi: 10.1152/ajpgi.00349.2010
Ji, Y., Murphy, A. Z. & Traub, R. J. Estrogen modulates the visceromotor reflex and responses of spinal dorsal horn neurons to colorectal stimulation in the rat. J. Neurosci. 23, 3908–3915 (2003).
pubmed: 12736360
pmcid: 6742189
doi: 10.1523/JNEUROSCI.23-09-03908.2003
Balasuriya, G. K., Hill-Yardin, E. L., Gershon, M. D. & Bornstein, J. C. A sexually dimorphic effect of cholera toxin: rapid changes in colonic motility mediated via a 5-HT
pubmed: 26990461
pmcid: 4967745
doi: 10.1113/JP272071
Törnblom, H. & Drossman, D. A. Psychopharmacologic therapies for irritable bowel syndrome. Gastroenterol. Clin. North Am. 50, 655–669 (2021).
pubmed: 34304793
doi: 10.1016/j.gtc.2021.04.005
Galligan, J. J. et al. Visceral hypersensitivity in female but not in male serotonin transporter knockout rats. Neurogastroenterol. Motil. 25, e373–e381 (2013).
pubmed: 23594365
doi: 10.1111/nmo.12133
Wang, Y. C. et al. The ETS oncogene family transcription factor FEV identifies serotonin-producing cells in normal and neoplastic small intestine. Endocr. Relat. Cancer 17, 283–291 (2010).
pubmed: 20048018
doi: 10.1677/ERC-09-0243
Hennessy, M. L. et al. Activity of Tachykinin1-expressing Pet1 raphe neurons modulates the respiratory chemoreflex. J. Neurosci. 37, 1807–1819 (2017).
pubmed: 28073937
pmcid: 5320611
doi: 10.1523/JNEUROSCI.2316-16.2016
Madison, B. B. et al. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J. Biol. Chem. 277, 33275–33283 (2002).
pubmed: 12065599
doi: 10.1074/jbc.M204935200
Salvatierra, J. et al. NaV1.1 inhibition can reduce visceral hypersensitivity. JCI Insight 3, e121000 (2018).
pubmed: 29875317
pmcid: 6124407
doi: 10.1172/jci.insight.121000
Hockley, J. R. F. et al. Single-cell RNAseq reveals seven classes of colonic sensory neuron. Gut 68, 633–644 (2019).
pubmed: 29483303
doi: 10.1136/gutjnl-2017-315631
Cantu, D. A. et al. EZcalcium: open-source toolbox for analysis of calcium imaging data. Front. Neural Circuits 14, 25 (2020).
pubmed: 32499682
pmcid: 7244005
doi: 10.3389/fncir.2020.00025
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Sato, T. et al. Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche. Nature 459, 262–265 (2009).
pubmed: 19329995
doi: 10.1038/nature07935
Becker, L. et al. Age-dependent shift in macrophage polarisation causes inflammation-mediated degeneration of enteric nervous system. Gut 67, 827–836 (2018).
pubmed: 28228489
doi: 10.1136/gutjnl-2016-312940
Li, Z. S., Schmauss, C., Cuenca, A., Ratcliffe, E. & Gershon, M. D. Physiological modulation of intestinal motility by enteric dopaminergic neurons and the D2 receptor: analysis of dopamine receptor expression, location, development, and function in wild-type and knock-out mice. J. Neurosci. 26, 2798–2807 (2006).
pubmed: 16525059
pmcid: 6675162
doi: 10.1523/JNEUROSCI.4720-05.2006