CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive decline

Summary: Emerging evidence suggests that immune receptors may participate in many aging-related processes such as energy metabolism, inflammation, and cognitive decline. CD300f, a TREM2-like lipid-sensing immune receptor, is an exceptional receptor as it integrates activating and inhibitory cell-sig...

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Main Authors: Frances Evans, Daniela Alí-Ruiz, Natalia Rego, María Luciana Negro-Demontel, Natalia Lago, Fabio Andrés Cawen, Bruno Pannunzio, Paula Sanchez-Molina, Laura Reyes, Andrea Paolino, Jorge Rodríguez-Duarte, Valentina Pérez-Torrado, Almudena Chicote-González, Celia Quijano, Inés Marmisolle, Ana Paula Mulet, Geraldine Schlapp, María Noel Meikle, Mariana Bresque, Martina Crispo, Eduardo Savio, Cristina Malagelada, Carlos Escande, Hugo Peluffo
Format: Article
Language:English
Published: Elsevier 2023-10-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723012810
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author Frances Evans
Daniela Alí-Ruiz
Natalia Rego
María Luciana Negro-Demontel
Natalia Lago
Fabio Andrés Cawen
Bruno Pannunzio
Paula Sanchez-Molina
Laura Reyes
Andrea Paolino
Jorge Rodríguez-Duarte
Valentina Pérez-Torrado
Almudena Chicote-González
Celia Quijano
Inés Marmisolle
Ana Paula Mulet
Geraldine Schlapp
María Noel Meikle
Mariana Bresque
Martina Crispo
Eduardo Savio
Cristina Malagelada
Carlos Escande
Hugo Peluffo
author_facet Frances Evans
Daniela Alí-Ruiz
Natalia Rego
María Luciana Negro-Demontel
Natalia Lago
Fabio Andrés Cawen
Bruno Pannunzio
Paula Sanchez-Molina
Laura Reyes
Andrea Paolino
Jorge Rodríguez-Duarte
Valentina Pérez-Torrado
Almudena Chicote-González
Celia Quijano
Inés Marmisolle
Ana Paula Mulet
Geraldine Schlapp
María Noel Meikle
Mariana Bresque
Martina Crispo
Eduardo Savio
Cristina Malagelada
Carlos Escande
Hugo Peluffo
author_sort Frances Evans
collection DOAJ
description Summary: Emerging evidence suggests that immune receptors may participate in many aging-related processes such as energy metabolism, inflammation, and cognitive decline. CD300f, a TREM2-like lipid-sensing immune receptor, is an exceptional receptor as it integrates activating and inhibitory cell-signaling pathways that modulate inflammation, efferocytosis, and microglial metabolic fitness. We hypothesize that CD300f can regulate systemic aging-related processes and ultimately healthy lifespan. We closely followed several cohorts of two strains of CD300f−/− and WT mice of both sexes for 30 months and observed an important reduction in lifespan and healthspan in knockout mice. This was associated with systemic inflammaging, increased cognitive decline, reduced brain glucose uptake observed by 18FDG PET scans, enrichment in microglial aging/neurodegeneration phenotypes, proteostasis alterations, senescence, increased frailty, and sex-dependent systemic metabolic changes. Moreover, the absence of CD300f altered macrophage immunometabolic phenotype. Taken together, we provide strong evidence suggesting that myeloid cell CD300f immune receptor contributes to healthy aging.
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spelling doaj.art-d519438bc10c484aad49f226011c5dfa2023-10-21T04:22:31ZengElsevierCell Reports2211-12472023-10-014210113269CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive declineFrances Evans0Daniela Alí-Ruiz1Natalia Rego2María Luciana Negro-Demontel3Natalia Lago4Fabio Andrés Cawen5Bruno Pannunzio6Paula Sanchez-Molina7Laura Reyes8Andrea Paolino9Jorge Rodríguez-Duarte10Valentina Pérez-Torrado11Almudena Chicote-González12Celia Quijano13Inés Marmisolle14Ana Paula Mulet15Geraldine Schlapp16María Noel Meikle17Mariana Bresque18Martina Crispo19Eduardo Savio20Cristina Malagelada21Carlos Escande22Hugo Peluffo23Department of Histology and Embryology, Faculty of Medicine, UDELAR, Montevideo, Uruguay; Neuroinflammation and Gene Therapy Laboratory, Institut Pasteur de Montevideo, Montevideo, UruguayNeuroinflammation and Gene Therapy Laboratory, Institut Pasteur de Montevideo, Montevideo, UruguayBioinformatics Unit, Institut Pasteur de Montevideo, Montevideo, Uruguay; Faculty of Sciences, UDELAR, Montevideo, UruguayDepartment of Histology and Embryology, Faculty of Medicine, UDELAR, Montevideo, Uruguay; Neuroinflammation and Gene Therapy Laboratory, Institut Pasteur de Montevideo, Montevideo, UruguayNeuroinflammation and Gene Therapy Laboratory, Institut Pasteur de Montevideo, Montevideo, UruguayNeuroinflammation and Gene Therapy Laboratory, Institut Pasteur de Montevideo, Montevideo, UruguayDepartment of Histology and Embryology, Faculty of Medicine, UDELAR, Montevideo, Uruguay; Neuroinflammation and Gene Therapy Laboratory, Institut Pasteur de Montevideo, Montevideo, UruguayDepartment of Cell Biology, Physiology and Immunology, and Institute of Neuroscience, Universitat Autònoma de Barcelona, Barcelona, SpainUruguayan Center for Molecular Imaging (CUDIM), Montevideo, UruguayUruguayan Center for Molecular Imaging (CUDIM), Montevideo, UruguayLaboratory of Vascular Biology and Drug Development, INDICYO Program, Institut Pasteur Montevideo, Montevideo, UruguayMetabolic Diseases and Aging Laboratory, INDICYO Program, Institut Pasteur de Montevideo, Montevideo, UruguayUnitat de Bioquímica i Biologia Molecular, Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona (UB), Barcelona, Spain; Institut de Neurociències, Universitat de Barcelona (UB), Barcelona, SpainDepartamento de Bioquímica y Centro de Investigaciones Biomédicas (CEINBIO), Facultad de Medicina, Universidad de la República, Montevideo, UruguayDepartamento de Bioquímica y Centro de Investigaciones Biomédicas (CEINBIO), Facultad de Medicina, Universidad de la República, Montevideo, UruguayUnidad de Biotecnología en Animales de Laboratorio, Institut Pasteur de Montevideo, Montevideo, UruguayUnidad de Biotecnología en Animales de Laboratorio, Institut Pasteur de Montevideo, Montevideo, UruguayUnidad de Biotecnología en Animales de Laboratorio, Institut Pasteur de Montevideo, Montevideo, UruguayMetabolic Diseases and Aging Laboratory, INDICYO Program, Institut Pasteur de Montevideo, Montevideo, UruguayUnidad de Biotecnología en Animales de Laboratorio, Institut Pasteur de Montevideo, Montevideo, UruguayUruguayan Center for Molecular Imaging (CUDIM), Montevideo, UruguayUnitat de Bioquímica i Biologia Molecular, Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona (UB), Barcelona, Spain; Institut de Neurociències, Universitat de Barcelona (UB), Barcelona, SpainMetabolic Diseases and Aging Laboratory, INDICYO Program, Institut Pasteur de Montevideo, Montevideo, UruguayDepartment of Histology and Embryology, Faculty of Medicine, UDELAR, Montevideo, Uruguay; Neuroinflammation and Gene Therapy Laboratory, Institut Pasteur de Montevideo, Montevideo, Uruguay; Unitat de Bioquímica i Biologia Molecular, Departament de Biomedicina, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona (UB), Barcelona, Spain; Institut de Neurociències, Universitat de Barcelona (UB), Barcelona, Spain; Corresponding authorSummary: Emerging evidence suggests that immune receptors may participate in many aging-related processes such as energy metabolism, inflammation, and cognitive decline. CD300f, a TREM2-like lipid-sensing immune receptor, is an exceptional receptor as it integrates activating and inhibitory cell-signaling pathways that modulate inflammation, efferocytosis, and microglial metabolic fitness. We hypothesize that CD300f can regulate systemic aging-related processes and ultimately healthy lifespan. We closely followed several cohorts of two strains of CD300f−/− and WT mice of both sexes for 30 months and observed an important reduction in lifespan and healthspan in knockout mice. This was associated with systemic inflammaging, increased cognitive decline, reduced brain glucose uptake observed by 18FDG PET scans, enrichment in microglial aging/neurodegeneration phenotypes, proteostasis alterations, senescence, increased frailty, and sex-dependent systemic metabolic changes. Moreover, the absence of CD300f altered macrophage immunometabolic phenotype. Taken together, we provide strong evidence suggesting that myeloid cell CD300f immune receptor contributes to healthy aging.http://www.sciencedirect.com/science/article/pii/S2211124723012810CP: ImmunologyCP: Metabolism
spellingShingle Frances Evans
Daniela Alí-Ruiz
Natalia Rego
María Luciana Negro-Demontel
Natalia Lago
Fabio Andrés Cawen
Bruno Pannunzio
Paula Sanchez-Molina
Laura Reyes
Andrea Paolino
Jorge Rodríguez-Duarte
Valentina Pérez-Torrado
Almudena Chicote-González
Celia Quijano
Inés Marmisolle
Ana Paula Mulet
Geraldine Schlapp
María Noel Meikle
Mariana Bresque
Martina Crispo
Eduardo Savio
Cristina Malagelada
Carlos Escande
Hugo Peluffo
CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive decline
Cell Reports
CP: Immunology
CP: Metabolism
title CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive decline
title_full CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive decline
title_fullStr CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive decline
title_full_unstemmed CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive decline
title_short CD300f immune receptor contributes to healthy aging by regulating inflammaging, metabolism, and cognitive decline
title_sort cd300f immune receptor contributes to healthy aging by regulating inflammaging metabolism and cognitive decline
topic CP: Immunology
CP: Metabolism
url http://www.sciencedirect.com/science/article/pii/S2211124723012810
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