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Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport

The ability to absorb ingested nutrients is an essential function of all metazoans and utilizes a wide array of nutrient transporters found on the absorptive enterocytes of the small intestine. A unique population of patients has previously been identified with severe congenital malabsorptive diarrh...

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Autores principales: McCauley, Heather A., Matthis, Andrea L., Enriquez, Jacob R., Nichol, Jonah T., Sanchez, J. Guillermo, Stone, William J., Sundaram, Nambirajan, Helmrath, Michael A., Montrose, Marshall H., Aihara, Eitaro, Wells, James M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7508945/
https://www.ncbi.nlm.nih.gov/pubmed/32963229
http://dx.doi.org/10.1038/s41467-020-18536-z
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author McCauley, Heather A.
Matthis, Andrea L.
Enriquez, Jacob R.
Nichol, Jonah T.
Sanchez, J. Guillermo
Stone, William J.
Sundaram, Nambirajan
Helmrath, Michael A.
Montrose, Marshall H.
Aihara, Eitaro
Wells, James M.
author_facet McCauley, Heather A.
Matthis, Andrea L.
Enriquez, Jacob R.
Nichol, Jonah T.
Sanchez, J. Guillermo
Stone, William J.
Sundaram, Nambirajan
Helmrath, Michael A.
Montrose, Marshall H.
Aihara, Eitaro
Wells, James M.
author_sort McCauley, Heather A.
collection PubMed
description The ability to absorb ingested nutrients is an essential function of all metazoans and utilizes a wide array of nutrient transporters found on the absorptive enterocytes of the small intestine. A unique population of patients has previously been identified with severe congenital malabsorptive diarrhea upon ingestion of any enteral nutrition. The intestines of these patients are macroscopically normal, but lack enteroendocrine cells (EECs), suggesting an essential role for this rare population of nutrient-sensing cells in regulating macronutrient absorption. Here, we use human and mouse models of EEC deficiency to identify an unappreciated role for the EEC hormone peptide YY in regulating ion-coupled absorption of glucose and dipeptides. We find that peptide YY is required in the small intestine to maintain normal electrophysiology in the presence of vasoactive intestinal polypeptide, a potent stimulator of ion secretion classically produced by enteric neurons. Administration of peptide YY to EEC-deficient mice restores normal electrophysiology, improves glucose and peptide absorption, diminishes diarrhea and rescues postnatal survival. These data suggest that peptide YY is a key regulator of macronutrient absorption in the small intestine and may be a viable therapeutic option to treat patients with electrolyte imbalance and nutrient malabsorption.
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spelling pubmed-75089452020-10-08 Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport McCauley, Heather A. Matthis, Andrea L. Enriquez, Jacob R. Nichol, Jonah T. Sanchez, J. Guillermo Stone, William J. Sundaram, Nambirajan Helmrath, Michael A. Montrose, Marshall H. Aihara, Eitaro Wells, James M. Nat Commun Article The ability to absorb ingested nutrients is an essential function of all metazoans and utilizes a wide array of nutrient transporters found on the absorptive enterocytes of the small intestine. A unique population of patients has previously been identified with severe congenital malabsorptive diarrhea upon ingestion of any enteral nutrition. The intestines of these patients are macroscopically normal, but lack enteroendocrine cells (EECs), suggesting an essential role for this rare population of nutrient-sensing cells in regulating macronutrient absorption. Here, we use human and mouse models of EEC deficiency to identify an unappreciated role for the EEC hormone peptide YY in regulating ion-coupled absorption of glucose and dipeptides. We find that peptide YY is required in the small intestine to maintain normal electrophysiology in the presence of vasoactive intestinal polypeptide, a potent stimulator of ion secretion classically produced by enteric neurons. Administration of peptide YY to EEC-deficient mice restores normal electrophysiology, improves glucose and peptide absorption, diminishes diarrhea and rescues postnatal survival. These data suggest that peptide YY is a key regulator of macronutrient absorption in the small intestine and may be a viable therapeutic option to treat patients with electrolyte imbalance and nutrient malabsorption. Nature Publishing Group UK 2020-09-22 /pmc/articles/PMC7508945/ /pubmed/32963229 http://dx.doi.org/10.1038/s41467-020-18536-z Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
McCauley, Heather A.
Matthis, Andrea L.
Enriquez, Jacob R.
Nichol, Jonah T.
Sanchez, J. Guillermo
Stone, William J.
Sundaram, Nambirajan
Helmrath, Michael A.
Montrose, Marshall H.
Aihara, Eitaro
Wells, James M.
Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport
title Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport
title_full Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport
title_fullStr Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport
title_full_unstemmed Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport
title_short Enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport
title_sort enteroendocrine cells couple nutrient sensing to nutrient absorption by regulating ion transport
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7508945/
https://www.ncbi.nlm.nih.gov/pubmed/32963229
http://dx.doi.org/10.1038/s41467-020-18536-z
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