TRPV6 channel mediates alcohol-induced gut barrier dysfunction and systemic response
Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca2+. Here we identify TRPV6, a Ca2+-permeable channel, as...
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| Published in | Cell reports (Cambridge) Vol. 39; no. 11; p. 110937 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
14.06.2022
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2211-1247 2211-1247 |
| DOI | 10.1016/j.celrep.2022.110937 |
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| Abstract | Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca2+. Here we identify TRPV6, a Ca2+-permeable channel, as responsible for alcohol-induced elevation of intracellular Ca2+, intestinal barrier dysfunction, and systemic inflammation. Ethanol and acetaldehyde elicit TRPV6 ionic currents in Caco-2 cells. Studies in Caco-2 cell monolayers and mouse intestinal organoids show that TRPV6 deficiency or inhibition attenuates ethanol- and acetaldehyde-induced Ca2+ influx, tight junction disruption, and barrier dysfunction. Moreover, Trpv6−/− mice are resistant to alcohol-induced intestinal barrier dysfunction. Photoaffinity labeling of 3-azibutanol identifies a histidine as a potential alcohol-binding site in TRPV6. The substitution of this histidine, and a nearby arginine, reduces ethanol-activated currents. Our findings reveal that TRPV6 is required for alcohol-induced gut barrier dysfunction and inflammation. Molecules that decrease TRPV6 function have the potential to attenuate alcohol-associated tissue injury.
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•Ethanol and acetaldehyde elicit inward TRPV6 currents in intestinal epithelial cells•TRPV6 is required for alcohol-induced barrier dysfunction in the intestinal epithelium•TRPV6 null mice are resistant to alcohol-induced endotoxemia and systemic inflammation•H185 and R134 residues in the TRPV6 N terminus fine-tune channel response to ethanol
Meena et al. show that the mechanism of alcohol-induced gut permeability, endotoxemia, and systemic inflammation requires the TRPV6 channel. They show that ethanol activates TRPV6, induces calcium influx, and disrupts intestinal epithelial tight junctions. Furthermore, specific histidine and arginine residues at the N terminus fine-tune the alcohol-induced activation of TRPV6. |
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| AbstractList | Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca2+. Here we identify TRPV6, a Ca2+-permeable channel, as responsible for alcohol-induced elevation of intracellular Ca2+, intestinal barrier dysfunction, and systemic inflammation. Ethanol and acetaldehyde elicit TRPV6 ionic currents in Caco-2 cells. Studies in Caco-2 cell monolayers and mouse intestinal organoids show that TRPV6 deficiency or inhibition attenuates ethanol- and acetaldehyde-induced Ca2+ influx, tight junction disruption, and barrier dysfunction. Moreover, Trpv6−/− mice are resistant to alcohol-induced intestinal barrier dysfunction. Photoaffinity labeling of 3-azibutanol identifies a histidine as a potential alcohol-binding site in TRPV6. The substitution of this histidine, and a nearby arginine, reduces ethanol-activated currents. Our findings reveal that TRPV6 is required for alcohol-induced gut barrier dysfunction and inflammation. Molecules that decrease TRPV6 function have the potential to attenuate alcohol-associated tissue injury.
[Display omitted]
•Ethanol and acetaldehyde elicit inward TRPV6 currents in intestinal epithelial cells•TRPV6 is required for alcohol-induced barrier dysfunction in the intestinal epithelium•TRPV6 null mice are resistant to alcohol-induced endotoxemia and systemic inflammation•H185 and R134 residues in the TRPV6 N terminus fine-tune channel response to ethanol
Meena et al. show that the mechanism of alcohol-induced gut permeability, endotoxemia, and systemic inflammation requires the TRPV6 channel. They show that ethanol activates TRPV6, induces calcium influx, and disrupts intestinal epithelial tight junctions. Furthermore, specific histidine and arginine residues at the N terminus fine-tune the alcohol-induced activation of TRPV6. Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca . Here we identify TRPV6, a Ca -permeable channel, as responsible for alcohol-induced elevation of intracellular Ca , intestinal barrier dysfunction, and systemic inflammation. Ethanol and acetaldehyde elicit TRPV6 ionic currents in Caco-2 cells. Studies in Caco-2 cell monolayers and mouse intestinal organoids show that TRPV6 deficiency or inhibition attenuates ethanol- and acetaldehyde-induced Ca influx, tight junction disruption, and barrier dysfunction. Moreover, Trpv6 mice are resistant to alcohol-induced intestinal barrier dysfunction. Photoaffinity labeling of 3-azibutanol identifies a histidine as a potential alcohol-binding site in TRPV6. The substitution of this histidine, and a nearby arginine, reduces ethanol-activated currents. Our findings reveal that TRPV6 is required for alcohol-induced gut barrier dysfunction and inflammation. Molecules that decrease TRPV6 function have the potential to attenuate alcohol-associated tissue injury. Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca2+. Here we identify TRPV6, a Ca2+-permeable channel, as responsible for alcohol-induced elevation of intracellular Ca2+, intestinal barrier dysfunction, and systemic inflammation. Ethanol and acetaldehyde elicit TRPV6 ionic currents in Caco-2 cells. Studies in Caco-2 cell monolayers and mouse intestinal organoids show that TRPV6 deficiency or inhibition attenuates ethanol- and acetaldehyde-induced Ca2+ influx, tight junction disruption, and barrier dysfunction. Moreover, Trpv6-/- mice are resistant to alcohol-induced intestinal barrier dysfunction. Photoaffinity labeling of 3-azibutanol identifies a histidine as a potential alcohol-binding site in TRPV6. The substitution of this histidine, and a nearby arginine, reduces ethanol-activated currents. Our findings reveal that TRPV6 is required for alcohol-induced gut barrier dysfunction and inflammation. Molecules that decrease TRPV6 function have the potential to attenuate alcohol-associated tissue injury.Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca2+. Here we identify TRPV6, a Ca2+-permeable channel, as responsible for alcohol-induced elevation of intracellular Ca2+, intestinal barrier dysfunction, and systemic inflammation. Ethanol and acetaldehyde elicit TRPV6 ionic currents in Caco-2 cells. Studies in Caco-2 cell monolayers and mouse intestinal organoids show that TRPV6 deficiency or inhibition attenuates ethanol- and acetaldehyde-induced Ca2+ influx, tight junction disruption, and barrier dysfunction. Moreover, Trpv6-/- mice are resistant to alcohol-induced intestinal barrier dysfunction. Photoaffinity labeling of 3-azibutanol identifies a histidine as a potential alcohol-binding site in TRPV6. The substitution of this histidine, and a nearby arginine, reduces ethanol-activated currents. Our findings reveal that TRPV6 is required for alcohol-induced gut barrier dysfunction and inflammation. Molecules that decrease TRPV6 function have the potential to attenuate alcohol-associated tissue injury. Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca 2+ . Here we identify TRPV6, a Ca 2+ -permeable channel, as responsible for alcohol-induced elevation of intracellular Ca 2+ , intestinal barrier dysfunction, and systemic inflammation. Ethanol and acetaldehyde elicit TRPV6 ionic currents in Caco-2 cells. Studies in Caco-2 cell monolayers and mouse intestinal organoids show that TRPV6 deficiency or inhibition attenuates ethanol- and acetaldehyde-induced Ca 2+ influx, tight junction disruption, and barrier dysfunction. Moreover, Trpv6 −/− mice are resistant to alcohol-induced intestinal barrier dysfunction. Photoaffinity labeling of 3-azibutanol identifies a histidine as a potential alcohol-binding site in TRPV6. The substitution of this histidine, and a nearby arginine, reduces ethanol-activated currents. Our findings reveal that TRPV6 is required for alcohol-induced gut barrier dysfunction and inflammation. Molecules that decrease TRPV6 function have the potential to attenuate alcohol-associated tissue injury. Meena et al. show that the mechanism of alcohol-induced gut permeability, endotoxemia, and systemic inflammation requires the TRPV6 channel. They show that ethanol activates TRPV6, induces calcium influx, and disrupts intestinal epithelial tight junctions. Furthermore, specific histidine and arginine residues at the N terminus fine-tune the alcohol-induced activation of TRPV6. Intestinal epithelial tight junction disruption is a primary contributing factor in alcohol-associated endotoxemia, systemic inflammation, and multiple organ damage. Ethanol and acetaldehyde disrupt tight junctions by elevating intracellular Ca2+. Here we identify TRPV6, a Ca2+-permeable channel, as responsible for alcohol-induced elevation of intracellular Ca2+, intestinal barrier dysfunction, and systemic inflammation. Ethanol and acetaldehyde elicit TRPV6 ionic currents in Caco-2 cells. Studies in Caco-2 cell monolayers and mouse intestinal organoids show that TRPV6 deficiency or inhibition attenuates ethanol- and acetaldehyde-induced Ca2+ influx, tight junction disruption, and barrier dysfunction. Moreover, Trpv6−/− mice are resistant to alcohol-induced intestinal barrier dysfunction. Photoaffinity labeling of 3-azibutanol identifies a histidine as a potential alcohol-binding site in TRPV6. The substitution of this histidine, and a nearby arginine, reduces ethanol-activated currents. Our findings reveal that TRPV6 is required for alcohol-induced gut barrier dysfunction and inflammation. Molecules that decrease TRPV6 function have the potential to attenuate alcohol-associated tissue injury. |
| ArticleNumber | 110937 |
| Author | Shukla, Pradeep K. Bell, Briar Jaggar, Jonathan H. Makowski, Liza Radic, Marko Z. Aihara, Eitaro Fernández-Peña, Carlos Beranova, Sarka Neeli, Indira Montrose, Marshall H. Vásquez, Valeria Cordero-Morales, Julio F. Chaib, Mehdi Giorgianni, Francesco Rao, RadhaKrishna Meena, Avtar S. Caires, Rebeca |
| AuthorAffiliation | 5 Present address: Center for Cellular and Molecular Biology, CSIR, Hyderabad, India 6 Lead contact 4 These authors contributed equally 1 Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA 3 Memphis Veterans Affairs Medical Center, Memphis, TN 38104, USA 2 Department of Pharmacology and Systems Physiology, University of Cincinnati, Cincinnati, OH 45221, USA |
| AuthorAffiliation_xml | – name: 4 These authors contributed equally – name: 3 Memphis Veterans Affairs Medical Center, Memphis, TN 38104, USA – name: 5 Present address: Center for Cellular and Molecular Biology, CSIR, Hyderabad, India – name: 2 Department of Pharmacology and Systems Physiology, University of Cincinnati, Cincinnati, OH 45221, USA – name: 6 Lead contact – name: 1 Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA |
| Author_xml | – sequence: 1 givenname: Avtar S. surname: Meena fullname: Meena, Avtar S. organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 2 givenname: Pradeep K. surname: Shukla fullname: Shukla, Pradeep K. organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 3 givenname: Briar surname: Bell fullname: Bell, Briar organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 4 givenname: Francesco surname: Giorgianni fullname: Giorgianni, Francesco organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 5 givenname: Rebeca surname: Caires fullname: Caires, Rebeca organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 6 givenname: Carlos surname: Fernández-Peña fullname: Fernández-Peña, Carlos organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 7 givenname: Sarka surname: Beranova fullname: Beranova, Sarka organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 8 givenname: Eitaro surname: Aihara fullname: Aihara, Eitaro organization: Department of Pharmacology and Systems Physiology, University of Cincinnati, Cincinnati, OH 45221, USA – sequence: 9 givenname: Marshall H. surname: Montrose fullname: Montrose, Marshall H. organization: Department of Pharmacology and Systems Physiology, University of Cincinnati, Cincinnati, OH 45221, USA – sequence: 10 givenname: Mehdi surname: Chaib fullname: Chaib, Mehdi organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 11 givenname: Liza surname: Makowski fullname: Makowski, Liza organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 12 givenname: Indira surname: Neeli fullname: Neeli, Indira organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 13 givenname: Marko Z. surname: Radic fullname: Radic, Marko Z. organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 14 givenname: Valeria surname: Vásquez fullname: Vásquez, Valeria organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 15 givenname: Jonathan H. surname: Jaggar fullname: Jaggar, Jonathan H. organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 16 givenname: Julio F. surname: Cordero-Morales fullname: Cordero-Morales, Julio F. email: jcordero@uthsc.edu organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA – sequence: 17 givenname: RadhaKrishna surname: Rao fullname: Rao, RadhaKrishna email: rrao2@uthsc.edu organization: Departments of Physiology, Medicine, Molecular Biology Immunology & Biochemistry, and Pharmaceutical Sciences, University of Tennessee Health Science Center, Memphis, TN 38163, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35705057$$D View this record in MEDLINE/PubMed |
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| Keywords | alcohol alcohol-binding site CP: Immunology systemic inflammation calcium TRPV intestine CP: Cell biology liver neuroinflammation endotoxemia tight junction |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS A.S.M. performed experiments, processed data, and prepared figures; P.K.S. assisted in many of these experiments and processed data; B.B. performed electrophysiology; C.F.-P. conducted intracellular calcium measurements; R.C. performed electrophysiology in Caco-2 cells; F.G. and S.B. performed LC-MS/MS analysis; E.A. conducted some of the initial experiments in enteroids; M.H.M. designed initial enteroid experiments; M.C. and L.M. performed studies in macrophages; I.N. and M.Z.R. performed studies in neutrophils; V.V. contributed to the design of ionic current measurements and manuscript preparation; J.H.J. supervised C.F.-P. in performing intracellular calcium imaging and analyses; J.F.C.-M. was instrumental in designing electrophysiology, preparation and interpretation of data figures, and manuscript writing; R.R. was responsible for the central hypothesis, design, supervision, and execution of the experiments, data interpretation, and manuscript writing. |
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| SubjectTerms | alcohol alcohol-binding site calcium CP: Cell biology CP: Immunology endotoxemia intestine liver neuroinflammation systemic inflammation tight junction TRPV |
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| Title | TRPV6 channel mediates alcohol-induced gut barrier dysfunction and systemic response |
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