Mechanosensing in the Physiology and Pathology of the Gastrointestinal Tract
Abstract
:1. Introduction
2. The Role of Mechanotransduction in Normal Gastrointestinal Physiology
2.1. Mechanosensitive Cells
2.1.1. Enterochromaffin Cells
2.1.2. Enteric Neurons
2.1.3. Interstitial Cells of Cajal
2.1.4. Smooth Muscle Cells
2.1.5. Macrophages
3. Examples of Mechanical Signals in the Regulation of Gastrointestinal Motility
3.1. Adaptive Relaxation of the Stomach
3.2. Distension-Evoked Peristalsis
4. Dysregulation of Mechanosensing Mechanisms in Gastrointestinal Diseases
4.1. Ileus
4.2. Irritable Bowel Syndrome
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Mercado-Perez, A.; Beyder, A. Gut feelings: Mechanosensing in the gastrointestinal tract. Nat. Rev. Gastroenterol. Hepatol. 2022, 19, 283–296. [Google Scholar] [CrossRef]
- Bayliss, W.M.; Starling, E.H. The movements and innervation of the small intestine. J. Physiol. 1899, 24, 99–143. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.; Heo, G.; Kim, S.Y. Neural signalling of gut mechanosensation in ingestive and digestive processes. Nat. Rev. Neurosci. 2022, 23, 135–156. [Google Scholar] [CrossRef]
- Joshi, V.; Strege, P.R.; Farrugia, G.; Beyder, A. Mechanotransduction in gastrointestinal smooth muscle cells: Role of mechanosensitive ion channels. Am. J. Physiol. Gastrointest. Liver Physiol. 2021, 320, G897–G906. [Google Scholar] [CrossRef] [PubMed]
- Uray, I.P.; Uray, K. Mechanotransduction at the Plasma Membrane-Cytoskeleton Interface. Int. J. Mol. Sci. 2021, 22, 1566. [Google Scholar] [CrossRef] [PubMed]
- Wang, F.; Knutson, K.; Alcaino, C.; Linden, D.R.; Gibbons, S.J.; Kashyap, P.; Grover, M.; Oeckler, R.; Gottlieb, P.A.; Li, H.J.; et al. Mechanosensitive ion channel Piezo2 is important for enterochromaffin cell response to mechanical forces. J. Physiol. 2017, 595, 79–91. [Google Scholar] [CrossRef] [Green Version]
- Alcaino, C.; Knutson, K.R.; Treichel, A.J.; Yildiz, G.; Strege, P.R.; Linden, D.R.; Li, J.H.; Leiter, A.B.; Szurszewski, J.H.; Farrugia, G.; 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 2018, 115, E7632–E7641. [Google Scholar] [CrossRef] [Green Version]
- Treichel, A.J.; Finholm, I.; Knutson, K.R.; Alcaino, C.; Whiteman, S.T.; Brown, M.R.; Matveyenko, A.; Wegner, A.; Kacmaz, H.; Mercado-Perez, A.; et al. Specialized Mechanosensory Epithelial Cells in Mouse Gut Intrinsic Tactile Sensitivity. Gastroenterology 2022, 162, 535–547.e13. [Google Scholar] [CrossRef]
- Brierley, S.M.; Hughes, P.A.; Page, A.J.; Kwan, K.Y.; Martin, C.M.; O’Donnell, T.A.; Cooper, N.J.; Harrington, A.M.; Adam, B.; Liebregts, T.; et al. The ion channel TRPA1 is required for normal mechanosensation and is modulated by algesic stimuli. Gastroenterology 2009, 137, 2084–2095.e3. [Google Scholar] [CrossRef] [Green Version]
- Bielefeldt, K.; Davis, B.M. Differential effects of ASIC3 and TRPV1 deletion on gastroesophageal sensation in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294, G130–G138. [Google Scholar] [CrossRef]
- Kefauver, J.M.; Ward, A.B.; Patapoutian, A. Discoveries in structure and physiology of mechanically activated ion channels. Nature 2020, 587, 567–576. [Google Scholar] [CrossRef] [PubMed]
- Wang, W.; Huang, H.; Hou, D.; Liu, P.; Wei, H.; Fu, X.; Niu, W. Mechanosensitivity of STREX-lacking BKCa channels in the colonic smooth muscle of the mouse. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G1231–G1240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sanders, K.M.; Koh, S.D. Two-pore-domain potassium channels in smooth muscles: New components of myogenic regulation. J. Physiol. 2006, 570 Pt 1, 37–43. [Google Scholar] [CrossRef] [PubMed]
- Brierley, S.M.; Page, A.J.; Hughes, P.A.; Adam, B.; Liebregts, T.; Cooper, N.J.; Holtmann, G.; Liedtke, W.; Blackshaw, L.A. Selective role for TRPV4 ion channels in visceral sensory pathways. Gastroenterology 2008, 134, 2059–2069. [Google Scholar] [CrossRef] [Green Version]
- Lyford, G.L.; Farrugia, G. Ion channels in gastrointestinal smooth muscle and interstitial cells of Cajal. Curr. Opin. Pharmacol. 2003, 3, 583–587. [Google Scholar] [CrossRef]
- Lyford, G.L.; Strege, P.R.; Shepard, A.; Ou, Y.; Ermilov, L.; Miller, S.M.; Gibbons, S.J.; Rae, J.L.; Szurszewski, J.H.; Farrugia, G. alpha(1C) (Ca(V)1.2) L-type calcium channel mediates mechanosensitive calcium regulation. Am. J. Physiol. Cell Physiol. 2002, 283, C1001–C1008. [Google Scholar] [CrossRef]
- Strege, P.R.; Ou, Y.; Sha, L.; Rich, A.; Gibbons, S.J.; Szurszewski, J.H.; Sarr, M.G.; Farrugia, G. Sodium current in human intestinal interstitial cells of Cajal. Am. J. Physiol. Gastrointest. Liver Physiol. 2003, 285, G1111–G1121. [Google Scholar] [CrossRef] [Green Version]
- Farrugia, G.; Holm, A.N.; Rich, A.; Sarr, M.G.; Szurszewski, J.H.; Rae, J.L. A mechanosensitive calcium channel in human intestinal smooth muscle cells. Gastroenterology 1999, 117, 900–905. [Google Scholar] [CrossRef]
- Neshatian, L.; Strege, P.R.; Rhee, P.L.; Kraichely, R.E.; Mazzone, A.; Bernard, C.E.; Cima, R.R.; Larson, D.W.; Dozois, E.J.; Kline, C.F.; et al. Ranolazine inhibits voltage-gated mechanosensitive sodium channels in human colon circular smooth muscle cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, 309, G506–G512. [Google Scholar] [CrossRef] [Green Version]
- Koh, S.D.; Sanders, K.M. Stretch-dependent potassium channels in murine colonic smooth muscle cells. J. Physiol. 2001, 533 Pt 1, 155–163. [Google Scholar] [CrossRef]
- Goswami, R.; Merth, M.; Sharma, S.; Alharbi, M.O.; Aranda-Espinoza, H.; Zhu, X.; Rahaman, S.O. TRPV4 calcium-permeable channel is a novel regulator of oxidized LDL-induced macrophage foam cell formation. Free Radic. Biol. Med. 2017, 110, 142–150. [Google Scholar] [CrossRef] [PubMed]
- Bulbring, E.; Crema, A. The release of 5-hydroxytryptamine in relation to pressure exerted on the intestinal mucosa. J. Physiol. 1959, 146, 18–28. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bertrand, P.P. Real-time measurement of serotonin release and motility in guinea pig ileum. J. Physiol. 2006, 577 Pt 2, 689–704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patel, B.A.; Bian, X.; Quaiserova-Mocko, V.; Galligan, J.J.; Swain, G.M. In vitro continuous amperometric monitoring of 5-hydroxytryptamine release from enterochromaffin cells of the guinea pig ileum. Analyst 2007, 132, 41–47. [Google Scholar] [CrossRef] [PubMed]
- Linan-Rico, A.; Ochoa-Cortes, F.; Beyder, A.; Soghomonyan, S.; Zuleta-Alarcon, A.; Coppola, V.; Christofi, F.L. Mechanosensory Signaling in Enterochromaffin Cells and 5-HT Release: Potential Implications for Gut Inflammation. Front. Neurosci. 2016, 10, 564. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gershon, M.D.; Tack, J. The serotonin signaling system: From basic understanding to drug development for functional GI disorders. Gastroenterology 2007, 132, 397–414. [Google Scholar] [CrossRef]
- Heredia, D.J.; Dickson, E.J.; Bayguinov, P.O.; Hennig, G.W.; Smith, T.K. Localized release of serotonin (5-hydroxytryptamine) by a fecal pellet regulates migrating motor complexes in murine colon. Gastroenterology 2009, 136, 1328–1338. [Google Scholar] [CrossRef] [Green Version]
- Heredia, D.J.; Gershon, M.D.; Koh, S.D.; Corrigan, R.D.; Okamoto, T.; Smith, T.K. Important role of mucosal serotonin in colonic propulsion and peristaltic reflexes: In vitro analyses in mice lacking tryptophan hydroxylase 1. J. Physiol. 2013, 591, 5939–5957. [Google Scholar] [CrossRef]
- Beyder, A. In Pursuit of the Epithelial Mechanosensitivity Mechanisms. Front. Endocrinol. (Lausanne) 2018, 9, 804. [Google Scholar] [CrossRef]
- Cooke, H.J.; Wunderlich, J.; Christofi, F.L. “The force be with you”: ATP in gut mechanosensory transduction. News Physiol. Sci. 2003, 18, 43–49. [Google Scholar] [CrossRef]
- 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 2000, 101, 459–469. [Google Scholar] [CrossRef] [PubMed]
- Ranade, S.S.; Woo, S.H.; Dubin, A.E.; Moshourab, R.A.; Wetzel, C.; Petrus, M.; Mathur, J.; Begay, V.; Coste, B.; Mainquist, J.; et al. Piezo2 is the major transducer of mechanical forces for touch sensation in mice. Nature 2014, 516, 121–125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kugler, E.M.; Michel, K.; Zeller, F.; Demir, I.E.; Ceyhan, G.O.; Schemann, M.; Mazzuoli-Weber, G. Mechanical stress activates neurites and somata of myenteric neurons. Front. Cell Neurosci. 2015, 9, 342. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mazzuoli, G.; Schemann, M. Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine. PLoS ONE 2012, 7, e39887. [Google Scholar] [CrossRef] [PubMed]
- Mazzuoli-Weber, G.; Schemann, M. Mechanosensitive enteric neurons in the guinea pig gastric corpus. Front. Cell Neurosci. 2015, 9, 430. [Google Scholar] [CrossRef] [Green Version]
- Wood, J.D. Electrical activity from single neurons in Auerbach’s plexus. Am. J. Physiol. 1970, 219, 159–169. [Google Scholar] [CrossRef]
- Mao, Y.; Wang, B.; Kunze, W. Characterization of myenteric sensory neurons in the mouse small intestine. J. Neurophysiol. 2006, 96, 998–1010. [Google Scholar] [CrossRef]
- Mazzuoli, G.; Schemann, M. Multifunctional rapidly adapting mechanosensitive enteric neurons (RAMEN) in the myenteric plexus of the guinea pig ileum. J. Physiol. 2009, 587 Pt 19, 4681–4694. [Google Scholar] [CrossRef]
- Kugler, E.M.; Michel, K.; Kirchenbuchler, D.; Dreissen, G.; Csiszar, A.; Merkel, R.; Schemann, M.; Mazzuoli-Weber, G. Sensitivity to Strain and Shear Stress of Isolated Mechanosensitive Enteric Neurons. Neuroscience 2018, 372, 213–224. [Google Scholar] [CrossRef]
- Mazzuoli-Weber, G.; Schemann, M. Mechanosensitivity in the enteric nervous system. Front. Cell Neurosci. 2015, 9, 408. [Google Scholar] [CrossRef]
- Spencer, N.J.; Smith, C.B.; Smith, T.K. Role of muscle tone in peristalsis in guinea-pig small intestine. J. Physiol. 2001, 530 Pt 2, 295–306. [Google Scholar] [CrossRef] [PubMed]
- Mazzuoli-Weber, G.; Kugler, E.M.; Buhler, C.I.; Kreutz, F.; Demir, I.E.; Ceyhan, O.G.; Zeller, F.; Schemann, M. Piezo proteins: Incidence and abundance in the enteric nervous system. Is there a link with mechanosensitivity? Cell Tissue Res. 2019, 375, 605–618. [Google Scholar] [CrossRef] [PubMed]
- Li, Z.; Chalazonitis, A.; Huang, Y.Y.; Mann, J.J.; Margolis, K.G.; Yang, Q.M.; Kim, D.O.; Cote, F.; Mallet, J.; Gershon, M.D. Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons. J. Neurosci. 2011, 31, 8998–9009. [Google Scholar] [CrossRef]
- Yadav, V.K.; Balaji, S.; Suresh, P.S.; Liu, X.S.; Lu, X.; Li, Z.; Guo, X.E.; Mann, J.J.; Balapure, A.K.; Gershon, M.D.; et al. Pharmacological inhibition of gut-derived serotonin synthesis is a potential bone anabolic treatment for osteoporosis. Nat. Med. 2010, 16, 308–312. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Z.Y.; Han, Y.F.; Huang, X.; Zhao, P.; Lu, H.L.; Kim, Y.C.; Xu, W.X. Pacemaking activity is regulated by membrane stretch via the CICR pathway in cultured interstitial cells of Cajal from murine intestine. J. Biomech. 2010, 43, 2214–2220. [Google Scholar] [CrossRef] [PubMed]
- Won, K.J.; Sanders, K.M.; Ward, S.M. Interstitial cells of Cajal mediate mechanosensitive responses in the stomach. Proc. Natl. Acad. Sci. USA 2005, 102, 14913–14918. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huizinga, J.D.; Thuneberg, L.; Kluppel, M.; Malysz, J.; Mikkelsen, H.B.; Bernstein, A. W/kit gene required for interstitial cells of Cajal and for intestinal pacemaker activity. Nature 1995, 373, 347–349. [Google Scholar] [CrossRef] [PubMed]
- Kraichely, R.E.; Farrugia, G. Mechanosensitive ion channels in interstitial cells of Cajal and smooth muscle of the gastrointestinal tract. Neurogastroenterol. Motil. 2007, 19, 245–252. [Google Scholar] [CrossRef]
- Treichel, A.J.; Farrugia, G.; Beyder, A. The touchy business of gastrointestinal (GI) mechanosensitivity. Brain Res. 2018, 1693 Pt B, 197–200. [Google Scholar] [CrossRef]
- Beyder, A.; Farrugia, G. Targeting ion channels for the treatment of gastrointestinal motility disorders. Therap. Adv. Gastroenterol. 2012, 5, 5–21. [Google Scholar] [CrossRef]
- Kunze, W.A.; Clerc, N.; Bertrand, P.P.; Furness, J.B. Contractile activity in intestinal muscle evokes action potential discharge in guinea-pig myenteric neurons. J. Physiol. 1999, 517 Pt 2, 547–561. [Google Scholar] [CrossRef] [PubMed]
- Strege, P.R.; Holm, A.N.; Rich, A.; Miller, S.M.; Ou, Y.; Sarr, M.G.; Farrugia, G. Cytoskeletal modulation of sodium current in human jejunal circular smooth muscle cells. Am. J. Physiol. Cell Physiol. 2003, 284, C60–C66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsvilovskyy, V.V.; Zholos, A.V.; Aberle, T.; Philipp, S.E.; Dietrich, A.; Zhu, M.X.; Birnbaumer, L.; Freichel, M.; Flockerzi, V. Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo. Gastroenterology 2009, 137, 1415–1424. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Schepper, S.; Stakenborg, N.; Matteoli, G.; Verheijden, S.; Boeckxstaens, G.E. Muscularis macrophages: Key players in intestinal homeostasis and disease. Cell Immunol. 2018, 330, 142–150. [Google Scholar] [CrossRef] [PubMed]
- Kalff, J.C.; Schraut, W.H.; Simmons, R.L.; Bauer, A.J. Surgical manipulation of the gut elicits an intestinal muscularis inflammatory response resulting in postsurgical ileus. Ann. Surg. 1998, 228, 652–663. [Google Scholar] [CrossRef]
- Docsa, T.; Bhattarai, D.; Sipos, A.; Wade, C.E.; Cox, C.S., Jr.; Uray, K. CXCL1 is upregulated during the development of ileus resulting in decreased intestinal contractile activity. Neurogastroenterol. Motil. 2020, 32, e13757. [Google Scholar] [CrossRef] [Green Version]
- Kalff, J.C.; Turler, A.; Schwarz, N.T.; Schraut, W.H.; Lee, K.K.; Tweardy, D.J.; Billiar, T.R.; Simmons, R.L.; Bauer, A.J. Intra-abdominal activation of a local inflammatory response within the human muscularis externa during laparotomy. Ann. Surg. 2003, 237, 301–315. [Google Scholar] [CrossRef]
- Wehner, S.; Buchholz, B.M.; Schuchtrup, S.; Rocke, A.; Schaefer, N.; Lysson, M.; Hirner, A.; Kalff, J.C. Mechanical strain and TLR4 synergistically induce cell-specific inflammatory gene expression in intestinal smooth muscle cells and peritoneal macrophages. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G1187–G1197. [Google Scholar] [CrossRef] [Green Version]
- Jetten, N.; Verbruggen, S.; Gijbels, M.J.; Post, M.J.; De Winther, M.P.; Donners, M.M. Anti-inflammatory M2, but not pro-inflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 2014, 17, 109–118. [Google Scholar] [CrossRef]
- Ballotta, V.; Driessen-Mol, A.; Bouten, C.V.; Baaijens, F.P. Strain-dependent modulation of macrophage polarization within scaffolds. Biomaterials 2014, 35, 4919–4928. [Google Scholar] [CrossRef]
- Atcha, H.; Jairaman, A.; Holt, J.R.; Meli, V.S.; Nagalla, R.R.; Veerasubramanian, P.K.; Brumm, K.T.; Lim, H.E.; Othy, S.; Cahalan, M.D.; et al. Mechanically activated ion channel Piezo1 modulates macrophage polarization and stiffness sensing. Nat. Commun. 2021, 12, 3256. [Google Scholar] [CrossRef] [PubMed]
- McWhorter, F.Y.; Davis, C.T.; Liu, W.F. Physical and mechanical regulation of macrophage phenotype and function. Cell Mol. Life Sci. 2015, 72, 1303–1316. [Google Scholar] [CrossRef] [Green Version]
- Schubert, M.L.; Makhlouf, G.M. Gastrin secretion induced by distention is mediated by gastric cholinergic and vasoactive intestinal peptide neurons in rats. Gastroenterology 1993, 104, 834–839. [Google Scholar] [CrossRef] [PubMed]
- Dixit, D.; Zarate, N.; Liu, L.W.; Boreham, D.R.; Huizinga, J.D. Interstitial cells of Cajal and adaptive relaxation in the mouse stomach. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 291, G1129–G1136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lang, K.; Breer, H.; Frick, C. Mechanosensitive ion channel Piezo1 is expressed in antral G cells of murine stomach. Cell Tissue Res. 2018, 371, 251–260. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mihara, H.; Suzuki, N.; Yamawaki, H.; Tominaga, M.; Sugiyama, T. TRPV2 ion channels expressed in inhibitory motor neurons of gastric myenteric plexus contribute to gastric adaptive relaxation and gastric emptying in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 304, G235–G240. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Seerden, T.C.; Lammers, W.J.; De Winter, B.Y.; De Man, J.G.; Pelckmans, P.A. Spatiotemporal electrical and motility mapping of distension-induced propagating oscillations in the murine small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289, G1043–G1051. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Huizinga, J.D.; McKay, C.M.; White, E.J. The many facets of intestinal peristalsis. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290, G1347–G1349, author reply G1348–G1349. [Google Scholar] [CrossRef]
- Spencer, N.J.; Hennig, G.W.; Smith, T.K. A rhythmic motor pattern activated by circumferential stretch in guinea-pig distal colon. J. Physiol. 2002, 545, 629–648. [Google Scholar] [CrossRef]
- Liu, Y.L.; Chen, Y.; Fan, W.T.; Cao, P.; Yan, J.; Zhao, X.Z.; Dong, W.G.; Huang, W.H. Mechanical Distension Induces Serotonin Release from Intestine as Revealed by Stretchable Electrochemical Sensing. Angew. Chem. Int. Ed. Engl. 2020, 59, 4075–4081. [Google Scholar] [CrossRef]
- Spencer, N.J.; Nicholas, S.J.; Robinson, L.; Kyloh, M.; Flack, N.; Brookes, S.J.; Zagorodnyuk, V.P.; Keating, D.J. Mechanisms underlying distension-evoked peristalsis in guinea pig distal colon: Is there a role for enterochromaffin cells? Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301, G519–G527. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tsuji, S.; Anglade, P.; Ozaki, T.; Sazi, T.; Yokoyama, S. Peristaltic movement evoked in intestinal tube devoid of mucosa and submucosa. Jpn. J. Physiol. 1992, 42, 363–375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sia, T.C.; Flack, N.; Robinson, L.; Kyloh, M.; Nicholas, S.J.; Brookes, S.J.; Wattchow, D.A.; Dinning, P.; Oliver, J.; Spencer, N.J. Is serotonin in enteric nerves required for distension-evoked peristalsis and propulsion of content in guinea-pig distal colon? Neuroscience 2013, 240, 325–335. [Google Scholar] [CrossRef]
- Spencer, N.J.; Dickson, E.J.; Hennig, G.W.; Smith, T.K. Sensory elements within the circular muscle are essential for mechanotransduction of ongoing peristaltic reflex activity in guinea-pig distal colon. J. Physiol. 2006, 576 Pt 2, 519–531. [Google Scholar] [CrossRef] [PubMed]
- Lomax, A.E.; Sharkey, K.A.; Bertrand, P.P.; Low, A.M.; Bornstein, J.C.; Furness, J.B. Correlation of morphology, electrophysiology and chemistry of neurons in the myenteric plexus of the guinea-pig distal colon. J. Auton. Nerv. Syst. 1999, 76, 45–61. [Google Scholar] [CrossRef]
- Moriggi, M.; Pastorelli, L.; Torretta, E.; Tontini, G.E.; Capitanio, D.; Bogetto, S.F.; Vecchi, M.; Gelfi, C. Contribution of Extracellular Matrix and Signal Mechanotransduction to Epithelial Cell Damage in Inflammatory Bowel Disease Patients: A Proteomic Study. Proteomics 2017, 17, 1700164. [Google Scholar] [CrossRef] [PubMed]
- Page, A.J.; Li, H. Meal-Sensing Signaling Pathways in Functional Dyspepsia. Front. Syst. Neurosci. 2018, 12, 10. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Cheng, G.; Miao, Y.; Qiu, F.; Bai, L.; Gao, Z.; Huang, Y.; Dong, L.; Niu, X.; Wang, X.; et al. Piezo type mechanosensitive ion channel component 1 facilitates gastric cancer omentum metastasis. J. Cell Mol. Med. 2021, 25, 2238–2253. [Google Scholar] [CrossRef]
- Zhang, J.; Zhou, Y.; Tang, P.M.K.; Cheng, A.S.L.; Yu, J.; To, K.F.; Kang, W. Mechanotransduction and Cytoskeleton Remodeling Shaping YAP1 in Gastric Tumorigenesis. Int. J. Mol. Sci. 2019, 20, 1576. [Google Scholar] [CrossRef] [Green Version]
- Virani, F.R.; Peery, T.; Rivas, O.; Tomasek, J.; Huerta, R.; Wade, C.E.; Lee, J.; Holcomb, J.B.; Uray, K. Incidence and Effects of Feeding Intolerance in Trauma Patients. Jpen. J. Parenter. Enteral. Nutr. 2019, 43, 742–749. [Google Scholar] [CrossRef]
- Venara, A.; Neunlist, M.; Slim, K.; Barbieux, J.; Colas, P.A.; Hamy, A.; Meurette, G. Postoperative ileus: Pathophysiology, incidence, and prevention. J. Visc. Surg. 2016, 153, 439–446. [Google Scholar] [CrossRef] [PubMed]
- Caddell, K.A.; Martindale, R.; McClave, S.A.; Miller, K. Can the intestinal dysmotility of critical illness be differentiated from postoperative ileus? Curr. Gastroenterol. Rep. 2011, 13, 358–367. [Google Scholar] [CrossRef] [PubMed]
- Sperber, A.D. Epidemiology and Burden of Irritable Bowel Syndrome: An International Perspective. Gastroenterol. Clin. North Am. 2021, 50, 489–503. [Google Scholar] [CrossRef] [PubMed]
- Cox, C.S., Jr.; Radhakrishnan, R.; Villarrubia, L.; Xue, H.; Uray, K.; Gill, B.S.; Stewart, R.H.; Laine, G.A. Hypertonic saline modulation of intestinal tissue stress and fluid balance. Shock 2008, 29, 598–602. [Google Scholar] [CrossRef] [PubMed]
- Uray, K.S.; Laine, G.A.; Xue, H.; Allen, S.J.; Cox, C.S., Jr. Intestinal edema decreases intestinal contractile activity via decreased myosin light chain phosphorylation. Crit. Care Med. 2006, 34, 2630–2637. [Google Scholar] [CrossRef] [PubMed]
- Chu, J.; Miller, C.T.; Kislitsyna, K.; Laine, G.A.; Stewart, R.H.; Cox, C.S.; Uray, K.S. Decreased myosin phosphatase target subunit 1(MYPT1) phosphorylation via attenuated rho kinase and zipper-interacting kinase activities in edematous intestinal smooth muscle. Neurogastroenterol. Motil. 2012, 24, 257–266.e109. [Google Scholar] [CrossRef] [Green Version]
- Chu, J.; Pham, N.T.; Olate, N.; Kislitsyna, K.; Day, M.C.; LeTourneau, P.A.; Kots, A.; Stewart, R.H.; Laine, G.A.; Cox, C.S., Jr.; et al. Biphasic regulation of myosin light chain phosphorylation by p21-activated kinase modulates intestinal smooth muscle contractility. J. Biol. Chem. 2013, 288, 1200–1213. [Google Scholar] [CrossRef] [Green Version]
- Uray, K.S.; Laine, G.A.; Xue, H.; Allen, S.J.; Cox, C.S., Jr. Edema-induced intestinal dysfunction is mediated by STAT3 activation. Shock 2007, 28, 239–244. [Google Scholar] [CrossRef]
- Uray, K.S.; Wright, Z.; Kislitsyna, K.; Xue, H.; Cox, C.S., Jr. Nuclear factor-kappaB activation by edema inhibits intestinal contractile activity. Crit. Care Med. 2010, 38, 861–870. [Google Scholar] [CrossRef]
- Schwarz, N.T.; Kalff, J.C.; Turler, A.; Speidel, N.; Grandis, J.R.; Billiar, T.R.; Bauer, A.J. Selective jejunal manipulation causes postoperative pan-enteric inflammation and dysmotility. Gastroenterology 2004, 126, 159–169. [Google Scholar] [CrossRef]
- Mikkelsen, H.B. Interstitial cells of Cajal, macrophages and mast cells in the gut musculature: Morphology, distribution, spatial and possible functional interactions. J. Cell Mol. Med. 2010, 14, 818–832. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boeckxstaens, G.E.; de Jonge, W.J. Neuroimmune mechanisms in postoperative ileus. Gut 2009, 58, 1300–1311. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wehner, S.; Behrendt, F.F.; Lyutenski, B.N.; Lysson, M.; Bauer, A.J.; Hirner, A.; Kalff, J.C. Inhibition of macrophage function prevents intestinal inflammation and postoperative ileus in rodents. Gut 2007, 56, 176–185. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Michalick, L.; Kuebler, W.M. TRPV4-A Missing Link Between Mechanosensation and Immunity. Front. Immunol. 2020, 11, 413. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Matsumoto, K.; Kawanaka, H.; Hori, M.; Kusamori, K.; Utsumi, D.; Tsukahara, T.; Amagase, K.; Horie, S.; Yamamoto, A.; Ozaki, H.; et al. Role of transient receptor potential melastatin 2 in surgical inflammation and dysmotility in a mouse model of postoperative ileus. Am. J. Physiol. Gastrointest. Liver Physiol. 2018, 315, G104–G116. [Google Scholar] [CrossRef] [PubMed]
- Fukudo, S.; Kanazawa, M.; Kano, M.; Sagami, Y.; Endo, Y.; Utsumi, A.; Nomura, T.; Hongo, M. Exaggerated motility of the descending colon with repetitive distention of the sigmoid colon in patients with irritable bowel syndrome. J. Gastroenterol. 2002, 37 (Suppl. 14), 145–150. [Google Scholar] [CrossRef] [PubMed]
- Ritchie, J. Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut 1973, 14, 125–132. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Coates, M.D.; Mahoney, C.R.; Linden, D.R.; Sampson, J.E.; Chen, J.; Blaszyk, H.; Crowell, M.D.; Sharkey, K.A.; Gershon, M.D.; Mawe, G.M.; et al. Molecular defects in mucosal serotonin content and decreased serotonin reuptake transporter in ulcerative colitis and irritable bowel syndrome. Gastroenterology 2004, 126, 1657–1664. [Google Scholar] [CrossRef]
- Spigset, O. Adverse reactions of selective serotonin reuptake inhibitors: Reports from a spontaneous reporting system. Drug. Saf. 1999, 20, 277–287. [Google Scholar] [CrossRef]
- Naliboff, B.D.; Munakata, J.; Fullerton, S.; Gracely, R.H.; Kodner, A.; Harraf, F.; Mayer, E.A. Evidence for two distinct perceptual alterations in irritable bowel syndrome. Gut 1997, 41, 505–512. [Google Scholar] [CrossRef]
- Yang, H.; Hou, C.; Xiao, W.; Qiu, Y. The role of mechanosensitive ion channels in the gastrointestinal tract. Front. Physiol. 2022, 13, 904203. [Google Scholar] [CrossRef] [PubMed]
- Yang, J.; Zhang, J.; Yang, H.; Li, K.; Lei, X.; Xu, C. The potential role of Piezo2 in the mediation of visceral sensation. Neurosci. Lett. 2016, 630, 158–163. [Google Scholar] [CrossRef] [PubMed]
- Balemans, D.; Boeckxstaens, G.E.; Talavera, K.; Wouters, M.M. Transient receptor potential ion channel function in sensory transduction and cellular signaling cascades underlying visceral hypersensitivity. Am. J. Physiol. Gastrointest. Liver Physiol. 2017, 312, G635–G648. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Winston, J.; Shenoy, M.; Medley, D.; Naniwadekar, A.; Pasricha, P.J. The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats. Gastroenterology 2007, 132, 615–627. [Google Scholar] [CrossRef]
- Yiangou, Y.; Facer, P.; Chessell, I.P.; Bountra, C.; Chan, C.; Fertleman, C.; Smith, V.; Anand, P. Voltage-gated ion channel Nav1.7 innervation in patients with idiopathic rectal hypersensitivity and paroxysmal extreme pain disorder (familial rectal pain). Neurosci. Lett. 2007, 427, 77–82. [Google Scholar] [CrossRef] [PubMed]
- Strege, P.R.; Mazzone, A.; Bernard, C.E.; Neshatian, L.; Gibbons, S.J.; Saito, Y.A.; Tester, D.J.; Calvert, M.L.; Mayer, E.A.; Chang, L.; et al. Irritable bowel syndrome patients have SCN5A channelopathies that lead to decreased NaV1.5 current and mechanosensitivity. Am. J. Physiol. Gastrointest. Liver Physiol. 2018, 314, G494–G503. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Strege, P.R.; Mercado-Perez, A.; Mazzone, A.; Saito, Y.A.; Bernard, C.E.; Farrugia, G.; Beyder, A. SCN5A mutation G615E results in NaV1.5 voltage-gated sodium channels with normal voltage-dependent function yet loss of mechanosensitivity. Channels 2019, 13, 287–298. [Google Scholar] [CrossRef]
Cell Type | Mechanosensor | Stimuli * | Effect | References |
---|---|---|---|---|
Enterochromaffin cells | Piezo2 | Pressure; distension; luminal signals; shear stress | Ca2+ influx; serotonin release | [6,7,8] |
Enteric neurons | TRPA1 | Distension | Spike discharges | [9,10] |
BKCa | Stretch | Cell hyperpolarization | [11,12] | |
K2P (TREK2 and TRAAK) | Shear stress; negative membrane pressure; stretch | Hyperpolarization; regulate resting membrane potential | [13] | |
TRPV4 | Distension | Spike discharges | [14] | |
Interstitial cells of Cajal | L-Type Ca channel | Shear stress; membrane tension; pressure | Increased inward current; faster activation | [15,16] |
Nav1.5 | Stretch | Increases slow-wave frequency | [17] | |
Smooth muscle cells | L-Type Ca channel | Shear stress; membrane tension; pressure | Increased inward current; faster activation | [16,18] |
BK channels | Stretch | Regulation of excitability | [12] | |
Nav1.5 | Shear stress | Increased excitability | [19] | |
K2P (TREK1) | Stretch | Hyperpolarization | [13,20] | |
Macrophages | TRPV4 | Stretch | Spike discharges | [21] |
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Kola, J.B.; Docsa, T.; Uray, K. Mechanosensing in the Physiology and Pathology of the Gastrointestinal Tract. Int. J. Mol. Sci. 2023, 24, 177. https://doi.org/10.3390/ijms24010177
Kola JB, Docsa T, Uray K. Mechanosensing in the Physiology and Pathology of the Gastrointestinal Tract. International Journal of Molecular Sciences. 2023; 24(1):177. https://doi.org/10.3390/ijms24010177
Chicago/Turabian StyleKola, Job Baffin, Tibor Docsa, and Karen Uray. 2023. "Mechanosensing in the Physiology and Pathology of the Gastrointestinal Tract" International Journal of Molecular Sciences 24, no. 1: 177. https://doi.org/10.3390/ijms24010177