Pancreatic beta-cell specific BAG3 knockout results in chronic hyperinsulinemia inducing insulin resistance.


Journal

Molecular metabolism
ISSN: 2212-8778
Titre abrégé: Mol Metab
Pays: Germany
ID NLM: 101605730

Informations de publication

Date de publication:
08 2023
Historique:
received: 09 02 2023
revised: 07 06 2023
accepted: 08 06 2023
medline: 18 7 2023
pubmed: 13 6 2023
entrez: 12 6 2023
Statut: ppublish

Résumé

Insulin, secreted from pancreatic islets of Langerhans, is of critical importance in regulating glucose homeostasis. Defective insulin secretion and/or the inability of tissues to respond to insulin results in insulin resistance and to several metabolic and organ alterations. We have previously demonstrated that BAG3 regulates insulin secretion. Herein we explored the consequences of beta-cells specific BAG3 deficiency in an animal model. We generated a beta-cells specific BAG3 knockout mouse model. Glucose and insulin tolerance tests, proteomics, metabolomics, and immunohistochemical analysis were used to investigate the role of BAG3 in regulating insulin secretion and the effects of chronic exposure to excessive insulin release in vivo. Beta-cells specific BAG3 knockout results in primary hyperinsulinism due to excessive insulin exocytosis finally leading to insulin resistance. We demonstrate that resistance is mainly muscle-dependent while the liver remains insulin sensitive. The chronically altered metabolic condition leads in time to histopathological alterations in different organs. We observe elevated glycogen and lipid accumulation in the liver reminiscent of non-alcoholic fatty liver disease as well as mesangial matrix expansion and thickening of the glomerular basement membrane, resembling the histology of chronic kidney disease. Altogether, this study shows that BAG3 plays a role in insulin secretion and provides a model for the study of hyperinsulinemia and insulin resistance.

Sections du résumé

BACKGROUND
Insulin, secreted from pancreatic islets of Langerhans, is of critical importance in regulating glucose homeostasis. Defective insulin secretion and/or the inability of tissues to respond to insulin results in insulin resistance and to several metabolic and organ alterations. We have previously demonstrated that BAG3 regulates insulin secretion. Herein we explored the consequences of beta-cells specific BAG3 deficiency in an animal model.
METHODS
We generated a beta-cells specific BAG3 knockout mouse model. Glucose and insulin tolerance tests, proteomics, metabolomics, and immunohistochemical analysis were used to investigate the role of BAG3 in regulating insulin secretion and the effects of chronic exposure to excessive insulin release in vivo.
RESULTS
Beta-cells specific BAG3 knockout results in primary hyperinsulinism due to excessive insulin exocytosis finally leading to insulin resistance. We demonstrate that resistance is mainly muscle-dependent while the liver remains insulin sensitive. The chronically altered metabolic condition leads in time to histopathological alterations in different organs. We observe elevated glycogen and lipid accumulation in the liver reminiscent of non-alcoholic fatty liver disease as well as mesangial matrix expansion and thickening of the glomerular basement membrane, resembling the histology of chronic kidney disease.
CONCLUSION
Altogether, this study shows that BAG3 plays a role in insulin secretion and provides a model for the study of hyperinsulinemia and insulin resistance.

Identifiants

pubmed: 37308077
pii: S2212-8778(23)00086-8
doi: 10.1016/j.molmet.2023.101752
pmc: PMC10333681
pii:
doi:

Substances chimiques

Insulin 0
Glucose IY9XDZ35W2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

101752

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier GmbH.. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Auteurs

Verena Damiani (V)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy.

Alessia Lamolinara (A)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Neurosciences, Imaging and Clinical Sciences, G. D'Annunzio University of Chieti-Pescara, 66100, Chieti, Italy.

Ilaria Cicalini (I)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy.

Maria Concetta Cufaro (MC)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy.

Francesco Del Pizzo (F)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy.

Federica Di Marco (F)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy.

Piero Del Boccio (P)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Pharmacy, University "G. d'Annunzio" of Chieti-Pescara, 66100, Chieti, Italy.

Beatrice Dufrusine (B)

Department of Bioscience and Technology for Food Agriculture and Environment, University of Teramo, 64100, Teramo, Italy.

Michael Hahne (M)

IGMM, CNRS, University of Montpellier, 34090, Montpellier, France.

Rossano Lattanzio (R)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy.

Damiana Pieragostino (D)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy.

Manuela Iezzi (M)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Neurosciences, Imaging and Clinical Sciences, G. D'Annunzio University of Chieti-Pescara, 66100, Chieti, Italy.

Massimo Federici (M)

Department of Systems Medicine, University of Rome Tor Vergata, 00133, Rome, Italy.

Maria Caterina Turco (MC)

Department of Medicine, Surgery and Dentistry, University of Salerno, 84081, Baronissi, Italy.

Arianna Maiorana (A)

Division of Metabolism, Department of Pediatrics Subspecialties, Ospedale Pediatrico Bambino Gesù, IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico), 00100, Rome, Italy.

Carlo Dionisi-Vici (C)

Division of Metabolism, Department of Pediatrics Subspecialties, Ospedale Pediatrico Bambino Gesù, IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico), 00100, Rome, Italy.

Vincenzo De Laurenzi (V)

Center for Advanced Studies and Technology (CAST), "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy; Department of Innovative Technologies in Medicine and Dentistry, "G. d'Annunzio" University of Chieti-Pescara, 66100, Chieti, Italy. Electronic address: delaurenzi@unich.it.

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