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Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes

Compromised function of insulin-secreting pancreatic β cells is central to the development and progression of Type 2 Diabetes (T2D). However, the mechanisms underlying β cell failure remain incompletely understood. Here, we report that metabolic stress markedly enhances macroautophagy-independent ly...

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Autores principales: Pasquier, Adrien, Vivot, Kevin, Erbs, Eric, Spiegelhalter, Coralie, Zhang, Zhirong, Aubert, Victor, Liu, Zengzhen, Senkara, Meryem, Maillard, Elisa, Pinget, Michel, Kerr-Conte, Julie, Pattou, François, Marciniak, Gilbert, Ganzhorn, Axel, Ronchi, Paolo, Schieber, Nicole L., Schwab, Yannick, Saftig, Paul, Goginashvili, Alexander, Ricci, Romeo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6658524/
https://www.ncbi.nlm.nih.gov/pubmed/31346174
http://dx.doi.org/10.1038/s41467-019-11170-4
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author Pasquier, Adrien
Vivot, Kevin
Erbs, Eric
Spiegelhalter, Coralie
Zhang, Zhirong
Aubert, Victor
Liu, Zengzhen
Senkara, Meryem
Maillard, Elisa
Pinget, Michel
Kerr-Conte, Julie
Pattou, François
Marciniak, Gilbert
Ganzhorn, Axel
Ronchi, Paolo
Schieber, Nicole L.
Schwab, Yannick
Saftig, Paul
Goginashvili, Alexander
Ricci, Romeo
author_facet Pasquier, Adrien
Vivot, Kevin
Erbs, Eric
Spiegelhalter, Coralie
Zhang, Zhirong
Aubert, Victor
Liu, Zengzhen
Senkara, Meryem
Maillard, Elisa
Pinget, Michel
Kerr-Conte, Julie
Pattou, François
Marciniak, Gilbert
Ganzhorn, Axel
Ronchi, Paolo
Schieber, Nicole L.
Schwab, Yannick
Saftig, Paul
Goginashvili, Alexander
Ricci, Romeo
author_sort Pasquier, Adrien
collection PubMed
description Compromised function of insulin-secreting pancreatic β cells is central to the development and progression of Type 2 Diabetes (T2D). However, the mechanisms underlying β cell failure remain incompletely understood. Here, we report that metabolic stress markedly enhances macroautophagy-independent lysosomal degradation of nascent insulin granules. In different model systems of diabetes including of human origin, stress-induced nascent granule degradation (SINGD) contributes to loss of insulin along with mammalian/mechanistic Target of Rapamycin (mTOR)-dependent suppression of macroautophagy. Expression of Protein Kinase D (PKD), a negative regulator of SINGD, is reduced in diabetic β cells. Pharmacological activation of PKD counters SINGD and delays the onset of T2D. Conversely, inhibition of PKD exacerbates SINGD, mitigates insulin secretion and accelerates diabetes. Finally, reduced levels of lysosomal tetraspanin CD63 prevent SINGD, leading to increased insulin secretion. Overall, our findings implicate aberrant SINGD in the pathogenesis of diabetes and suggest new therapeutic strategies to prevent β cell failure.
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spelling pubmed-66585242019-07-29 Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes Pasquier, Adrien Vivot, Kevin Erbs, Eric Spiegelhalter, Coralie Zhang, Zhirong Aubert, Victor Liu, Zengzhen Senkara, Meryem Maillard, Elisa Pinget, Michel Kerr-Conte, Julie Pattou, François Marciniak, Gilbert Ganzhorn, Axel Ronchi, Paolo Schieber, Nicole L. Schwab, Yannick Saftig, Paul Goginashvili, Alexander Ricci, Romeo Nat Commun Article Compromised function of insulin-secreting pancreatic β cells is central to the development and progression of Type 2 Diabetes (T2D). However, the mechanisms underlying β cell failure remain incompletely understood. Here, we report that metabolic stress markedly enhances macroautophagy-independent lysosomal degradation of nascent insulin granules. In different model systems of diabetes including of human origin, stress-induced nascent granule degradation (SINGD) contributes to loss of insulin along with mammalian/mechanistic Target of Rapamycin (mTOR)-dependent suppression of macroautophagy. Expression of Protein Kinase D (PKD), a negative regulator of SINGD, is reduced in diabetic β cells. Pharmacological activation of PKD counters SINGD and delays the onset of T2D. Conversely, inhibition of PKD exacerbates SINGD, mitigates insulin secretion and accelerates diabetes. Finally, reduced levels of lysosomal tetraspanin CD63 prevent SINGD, leading to increased insulin secretion. Overall, our findings implicate aberrant SINGD in the pathogenesis of diabetes and suggest new therapeutic strategies to prevent β cell failure. Nature Publishing Group UK 2019-07-25 /pmc/articles/PMC6658524/ /pubmed/31346174 http://dx.doi.org/10.1038/s41467-019-11170-4 Text en © The Author(s) 2019 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
Pasquier, Adrien
Vivot, Kevin
Erbs, Eric
Spiegelhalter, Coralie
Zhang, Zhirong
Aubert, Victor
Liu, Zengzhen
Senkara, Meryem
Maillard, Elisa
Pinget, Michel
Kerr-Conte, Julie
Pattou, François
Marciniak, Gilbert
Ganzhorn, Axel
Ronchi, Paolo
Schieber, Nicole L.
Schwab, Yannick
Saftig, Paul
Goginashvili, Alexander
Ricci, Romeo
Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes
title Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes
title_full Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes
title_fullStr Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes
title_full_unstemmed Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes
title_short Lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes
title_sort lysosomal degradation of newly formed insulin granules contributes to β cell failure in diabetes
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6658524/
https://www.ncbi.nlm.nih.gov/pubmed/31346174
http://dx.doi.org/10.1038/s41467-019-11170-4
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