MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BAT

Abstract Macrophages are key regulators of adipose tissue plasticity. Obesity impairs brown adipose tissue (BAT) function in humans, yet macrophage-mediated mechanisms remain elusive. Here, we introduce MACanalyzeR, a single-cell RNA sequencing (scRNAseq) tool designed for comprehensive monocyte/mac...

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Main Authors: Andrea Ninni, Fabio Zaccaria, Luca Verteramo, Francesca Sciarretta, Loreana Sanches Silveira, José Cesar Rosa-Neto, Simone Carotti, Lorenzo Nevi, Paolo Grumati, Satish Patel, Giulia Carrera, Alessandro Sgambato, Donatella Lucchetti, Filomena Colella, Ilenia Severi, Martina Senzacqua, Antonio Giordano, Sergio Bernardini, Claudia Di Biagio, Flavia Tortolici, Giuseppe Rizzo, Clement Cochain, Valerio Chiurchiù, Stoyan Ivanov, Beiyan Zhou, Jesse W. Williams, David B. Savage, Katia Aquilano, Daniele Lettieri-Barbato
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60295-2
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author Andrea Ninni
Fabio Zaccaria
Luca Verteramo
Francesca Sciarretta
Loreana Sanches Silveira
José Cesar Rosa-Neto
Simone Carotti
Lorenzo Nevi
Paolo Grumati
Satish Patel
Giulia Carrera
Alessandro Sgambato
Donatella Lucchetti
Filomena Colella
Ilenia Severi
Martina Senzacqua
Antonio Giordano
Sergio Bernardini
Claudia Di Biagio
Flavia Tortolici
Giuseppe Rizzo
Clement Cochain
Valerio Chiurchiù
Stoyan Ivanov
Beiyan Zhou
Jesse W. Williams
David B. Savage
Katia Aquilano
Daniele Lettieri-Barbato
author_facet Andrea Ninni
Fabio Zaccaria
Luca Verteramo
Francesca Sciarretta
Loreana Sanches Silveira
José Cesar Rosa-Neto
Simone Carotti
Lorenzo Nevi
Paolo Grumati
Satish Patel
Giulia Carrera
Alessandro Sgambato
Donatella Lucchetti
Filomena Colella
Ilenia Severi
Martina Senzacqua
Antonio Giordano
Sergio Bernardini
Claudia Di Biagio
Flavia Tortolici
Giuseppe Rizzo
Clement Cochain
Valerio Chiurchiù
Stoyan Ivanov
Beiyan Zhou
Jesse W. Williams
David B. Savage
Katia Aquilano
Daniele Lettieri-Barbato
author_sort Andrea Ninni
collection DOAJ
description Abstract Macrophages are key regulators of adipose tissue plasticity. Obesity impairs brown adipose tissue (BAT) function in humans, yet macrophage-mediated mechanisms remain elusive. Here, we introduce MACanalyzeR, a single-cell RNA sequencing (scRNAseq) tool designed for comprehensive monocyte/macrophage metabolic profiling. Applying MACanalyzeR to BAT from obese male murine models (db/db and HFD-fed mice), we identify lipid-associated macrophages (LAMs) with foamy characteristics. Unlike db/db BAT LAMs, those in HFD BAT correlate with thermogenic gene expression and PPAR signaling activation. A distinct PpargHIGH LAM subcluster progressively accumulates in thermogenically active BAT. Macrophage-specific Pparg depletion disrupts BAT thermogenesis, inducing a white-like phenotype and metabolic dysfunctions. Mechanistically, PpargHIGH LAMs secrete GDF15, a key regulator of BAT identity and lipid metabolism under high-energy demand. Our study establishes MACanalyzeR as a powerful tool for immunometabolic interrogation and identifies PpargHIGH LAMs as critical mediators of BAT homeostasis.
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spelling doaj-art-c222936de52b410e95c85af4adc0b7012025-08-20T02:00:03ZengNature PortfolioNature Communications2041-17232025-05-0116111610.1038/s41467-025-60295-2MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BATAndrea Ninni0Fabio Zaccaria1Luca Verteramo2Francesca Sciarretta3Loreana Sanches Silveira4José Cesar Rosa-Neto5Simone Carotti6Lorenzo Nevi7Paolo Grumati8Satish Patel9Giulia Carrera10Alessandro Sgambato11Donatella Lucchetti12Filomena Colella13Ilenia Severi14Martina Senzacqua15Antonio Giordano16Sergio Bernardini17Claudia Di Biagio18Flavia Tortolici19Giuseppe Rizzo20Clement Cochain21Valerio Chiurchiù22Stoyan Ivanov23Beiyan Zhou24Jesse W. Williams25David B. Savage26Katia Aquilano27Daniele Lettieri-Barbato28Department of Biology, University of Rome Tor VergataDepartment of Biology, University of Rome Tor VergataDepartment of Biology, University of Rome Tor VergataDepartment of Biology, University of Rome Tor VergataImmunometabolism Research Group, Department of Cell Biology and Development, Institute of Biomedical Sciences, University of São Paulo (ICB1-USP)Immunometabolism Research Group, Department of Cell Biology and Development, Institute of Biomedical Sciences, University of São Paulo (ICB1-USP)Microscopic and Ultrastructural Anatomy Research Unit, Department of Medicine and Surgery, Università Campus Bio-Medico di RomaMicroscopic and Ultrastructural Anatomy Research Unit, Department of Medicine and Surgery, Università Campus Bio-Medico di RomaTelethon Institute of Genetics and MedicineMetabolic Research Laboratories, Wellcome Trust-Medical Research Council Institute of Metabolic Science, University of CambridgeLaboratory of Resolution of Neuroinflammation, IRCCS Santa Lucia FoundationMultiplex Spatial Profiling Facility, Fondazione Policlinico Universitario ‘Agostino Gemelli’ IRCCSMultiplex Spatial Profiling Facility, Fondazione Policlinico Universitario ‘Agostino Gemelli’ IRCCSMultiplex Spatial Profiling Facility, Fondazione Policlinico Universitario ‘Agostino Gemelli’ IRCCSDepartment of Experimental and Clinical Medicine, Marche Polytechnic UniversityDepartment of Experimental and Clinical Medicine, Marche Polytechnic UniversityDepartment of Experimental and Clinical Medicine, Marche Polytechnic UniversityDepartment of Biology, University of Rome Tor VergataDepartment of Biology, University of Rome Tor VergataDepartment of Biology, University of Rome Tor VergataInstitute of Experimental Biomedicine, University Hospital Würzburg, D16Institute of Experimental Biomedicine, University Hospital Würzburg, D16Laboratory of Resolution of Neuroinflammation, IRCCS Santa Lucia FoundationUniversité Côte d’Azur, CNRSDepartment of Immunology, School of Medicine, University of ConnecticutCenter for Immunology, University of MinnesotaMetabolic Research Laboratories, Wellcome Trust-Medical Research Council Institute of Metabolic Science, University of CambridgeDepartment of Biology, University of Rome Tor VergataDepartment of Biology, University of Rome Tor VergataAbstract Macrophages are key regulators of adipose tissue plasticity. Obesity impairs brown adipose tissue (BAT) function in humans, yet macrophage-mediated mechanisms remain elusive. Here, we introduce MACanalyzeR, a single-cell RNA sequencing (scRNAseq) tool designed for comprehensive monocyte/macrophage metabolic profiling. Applying MACanalyzeR to BAT from obese male murine models (db/db and HFD-fed mice), we identify lipid-associated macrophages (LAMs) with foamy characteristics. Unlike db/db BAT LAMs, those in HFD BAT correlate with thermogenic gene expression and PPAR signaling activation. A distinct PpargHIGH LAM subcluster progressively accumulates in thermogenically active BAT. Macrophage-specific Pparg depletion disrupts BAT thermogenesis, inducing a white-like phenotype and metabolic dysfunctions. Mechanistically, PpargHIGH LAMs secrete GDF15, a key regulator of BAT identity and lipid metabolism under high-energy demand. Our study establishes MACanalyzeR as a powerful tool for immunometabolic interrogation and identifies PpargHIGH LAMs as critical mediators of BAT homeostasis.https://doi.org/10.1038/s41467-025-60295-2
spellingShingle Andrea Ninni
Fabio Zaccaria
Luca Verteramo
Francesca Sciarretta
Loreana Sanches Silveira
José Cesar Rosa-Neto
Simone Carotti
Lorenzo Nevi
Paolo Grumati
Satish Patel
Giulia Carrera
Alessandro Sgambato
Donatella Lucchetti
Filomena Colella
Ilenia Severi
Martina Senzacqua
Antonio Giordano
Sergio Bernardini
Claudia Di Biagio
Flavia Tortolici
Giuseppe Rizzo
Clement Cochain
Valerio Chiurchiù
Stoyan Ivanov
Beiyan Zhou
Jesse W. Williams
David B. Savage
Katia Aquilano
Daniele Lettieri-Barbato
MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BAT
Nature Communications
title MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BAT
title_full MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BAT
title_fullStr MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BAT
title_full_unstemmed MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BAT
title_short MACanalyzeR scRNAseq analysis tool reveals PPARγHIGH/GDF15HIGH lipid-associated macrophages facilitate thermogenic expansion in BAT
title_sort macanalyzer scrnaseq analysis tool reveals pparγhigh gdf15high lipid associated macrophages facilitate thermogenic expansion in bat
url https://doi.org/10.1038/s41467-025-60295-2
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