The Integrase Inhibitors Dolutegravir and Raltegravir Exert Proadipogenic and Profibrotic Effects and Induce Insulin Resistance in Human/Simian Adipose Tissue and Human Adipocytes.


Journal

Clinical infectious diseases : an official publication of the Infectious Diseases Society of America
ISSN: 1537-6591
Titre abrégé: Clin Infect Dis
Pays: United States
ID NLM: 9203213

Informations de publication

Date de publication:
17 12 2020
Historique:
received: 10 12 2019
accepted: 09 03 2020
pubmed: 14 3 2020
medline: 29 4 2021
entrez: 14 3 2020
Statut: ppublish

Résumé

Although some integrase strand transfer inhibitors (INSTIs) promote peripheral and central adipose tissue/weight gain in people with human immunodeficiency virus (PHIV), the underlying mechanism has not been identified. Here, we used human and simian models to assess the impact of INSTIs on adipose tissue phenotype and function. Adipocyte size and fibrosis were determined in biopsies of subcutaneous and visceral adipose tissue (SCAT and VAT, respectively) from 14 noninfected macaques and 19 PHIV treated or not treated with an INSTI. Fibrosis, adipogenesis, oxidative stress, mitochondrial function, and insulin sensitivity were assessed in human proliferating or adipocyte-differentiated adipose stem cells after long-term exposure to dolutegravir or raltegravir. We observed elevated fibrosis, adipocyte size, and adipogenic marker expression in SCAT and VAT from INSTI-treated noninfected macaques. Adiponectin expression was low in SCAT. Accordingly, SCAT and VAT samples from INSTI-exposed patients displayed higher levels of fibrosis than those from nonexposed patients. In vitro, dolutegravir and, to a lesser extent, raltegravir were associated with greater extracellular matrix production and lipid accumulation in adipose stem cells and/or adipocytes as observed in vivo. Despite the INSTIs' proadipogenic and prolipogenic effects, these drugs promoted oxidative stress, mitochondrial dysfunction, and insulin resistance. Dolutegravir and raltegravir can directly impact adipocytes and adipose tissue. These INSTIs induced adipogenesis, lipogenesis, oxidative stress, fibrosis, and insulin resistance. The present study is the first to shed light on the fat modifications observed in INSTI-treated PHIV.

Sections du résumé

BACKGROUND
Although some integrase strand transfer inhibitors (INSTIs) promote peripheral and central adipose tissue/weight gain in people with human immunodeficiency virus (PHIV), the underlying mechanism has not been identified. Here, we used human and simian models to assess the impact of INSTIs on adipose tissue phenotype and function.
METHODS
Adipocyte size and fibrosis were determined in biopsies of subcutaneous and visceral adipose tissue (SCAT and VAT, respectively) from 14 noninfected macaques and 19 PHIV treated or not treated with an INSTI. Fibrosis, adipogenesis, oxidative stress, mitochondrial function, and insulin sensitivity were assessed in human proliferating or adipocyte-differentiated adipose stem cells after long-term exposure to dolutegravir or raltegravir.
RESULTS
We observed elevated fibrosis, adipocyte size, and adipogenic marker expression in SCAT and VAT from INSTI-treated noninfected macaques. Adiponectin expression was low in SCAT. Accordingly, SCAT and VAT samples from INSTI-exposed patients displayed higher levels of fibrosis than those from nonexposed patients. In vitro, dolutegravir and, to a lesser extent, raltegravir were associated with greater extracellular matrix production and lipid accumulation in adipose stem cells and/or adipocytes as observed in vivo. Despite the INSTIs' proadipogenic and prolipogenic effects, these drugs promoted oxidative stress, mitochondrial dysfunction, and insulin resistance.
CONCLUSIONS
Dolutegravir and raltegravir can directly impact adipocytes and adipose tissue. These INSTIs induced adipogenesis, lipogenesis, oxidative stress, fibrosis, and insulin resistance. The present study is the first to shed light on the fat modifications observed in INSTI-treated PHIV.

Identifiants

pubmed: 32166319
pii: 5804258
doi: 10.1093/cid/ciaa259
doi:

Substances chimiques

HIV Integrase Inhibitors 0
Heterocyclic Compounds, 3-Ring 0
Integrase Inhibitors 0
Oxazines 0
Piperazines 0
Pyridones 0
Raltegravir Potassium 43Y000U234
dolutegravir DKO1W9H7M1

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e549-e560

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved. For permissions, e-mail: journals.permissions@oup.com.

Auteurs

Jennifer Gorwood (J)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.

Christine Bourgeois (C)

Commissariat à l'Energie Atomique, Université Paris Sud 11, Inserm U1184, Center for Immunology of Viral Infections and Autoimmune Diseases, Infectious Disease Models and Innovative Therapies Department, Fontenay-aux-Roses, France.

Valérie Pourcher (V)

Assistance publique-Hôpitaux de Paris, Sorbonne Université, Hôpital Pitié-Salpêtrière, Service de maladies infectieuses et tropicales, Paris, France.
Sorbonne Université-Inserm, Institut Pierre Louis d'Epidémiologie et de Santé Publique, Paris, France.

Guillaume Pourcher (G)

Obesity Center, Institut Mutualiste Montsouris, Paris Descartes University, Paris, France.

Frédéric Charlotte (F)

Assistance publique-Hôpitaux de Paris, Sorbonne Université, Hôpital Pitié-Salpêtrière, Service d'Anatomie Pathologique, Paris, France.

Matthieu Mantecon (M)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.

Cindy Rose (C)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.

Romain Morichon (R)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.

Michael Atlan (M)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.
Assistance publique-Hôpitaux de Paris, Hôpital Tenon, Service de Chirurgie Plastique et Esthétique, Paris, France.

Roger Le Grand (R)

Commissariat à l'Energie Atomique, Université Paris Sud 11, Inserm U1184, Center for Immunology of Viral Infections and Autoimmune Diseases, Infectious Disease Models and Innovative Therapies Department, Fontenay-aux-Roses, France.

Delphine Desjardins (D)

Commissariat à l'Energie Atomique, Université Paris Sud 11, Inserm U1184, Center for Immunology of Viral Infections and Autoimmune Diseases, Infectious Disease Models and Innovative Therapies Department, Fontenay-aux-Roses, France.

Christine Katlama (C)

Assistance publique-Hôpitaux de Paris, Sorbonne Université, Hôpital Pitié-Salpêtrière, Service de maladies infectieuses et tropicales, Paris, France.
Sorbonne Université-Inserm, Institut Pierre Louis d'Epidémiologie et de Santé Publique, Paris, France.

Bruno Fève (B)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.
Assistance publique-Hôpitaux de Paris, Hôpital Saint-Antoine, Pathologies de la Résistance à l'Insuline et de l'Insulino-Sensibilité, Service d'Endocrinologie, Diabétologie et Reproduction, Paris, France.

Olivier Lambotte (O)

Commissariat à l'Energie Atomique, Université Paris Sud 11, Inserm U1184, Center for Immunology of Viral Infections and Autoimmune Diseases, Infectious Disease Models and Innovative Therapies Department, Fontenay-aux-Roses, France.
Assistance publique-Hôpitaux de Paris, Hôpital Bicêtre, Service de Médecine Interne et Immunologie Clinique, Kremlin-Bicêtre, France.

Jacqueline Capeau (J)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.

Véronique Béréziat (V)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.

Claire Lagathu (C)

Sorbonne Université, Inserm Unité Mixte de Recherche S938, Centre de Recherche Saint-Antoine, Institut Hospitalo-Universitaire de Cardio-Métabolisme et Nutrition, Paris, France.

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