Plasma membrane remodeling determines adipocyte expansion and mechanical adaptability

María C. M. Aboy-Pardal, Marta C. Guadamillas, Carlos R. Guerrero, Mauro Català-Montoro, Mónica Toledano-Donado, Sara Terrés-Domínguez, Dácil M. Pavón, Víctor Jiménez-Jiménez, Daniel Jimenez-Carretero, Moreno Zamai, Cintia Folgueira, Ana Cerezo, Fidel-Nicolás Lolo, Rubén Nogueiras, Guadalupe Sabio, Miguel Sánchez-Álvarez, Asier Echarri, Ricardo Garcia and Miguel A. Pozo ()
Additional contact information
María C. M. Aboy-Pardal: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Marta C. Guadamillas: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Carlos R. Guerrero: CSIC
Mauro Català-Montoro: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Mónica Toledano-Donado: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Sara Terrés-Domínguez: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Dácil M. Pavón: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Víctor Jiménez-Jiménez: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Daniel Jimenez-Carretero: Cell and Developmental Biology Area. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Moreno Zamai: Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Cintia Folgueira: Centro de Investigación en Medicina Molecular y Enfermedades Crónicas CIMUS
Ana Cerezo: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Fidel-Nicolás Lolo: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Rubén Nogueiras: Centro de Investigación en Medicina Molecular y Enfermedades Crónicas CIMUS
Guadalupe Sabio: Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Miguel Sánchez-Álvarez: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Asier Echarri: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)
Ricardo Garcia: CSIC
Miguel A. Pozo: Novel mechanisms in atherosclerosis program. Centro Nacional de Investigaciones Cardiovasculares (CNIC)

Nature Communications, 2024, vol. 15, issue 1, 1-27

Abstract: Abstract Adipocytes expand massively to accommodate excess energy stores and protect the organism from lipotoxicity. Adipose tissue expandability is at the center of disorders such as obesity and lipodystrophy; however, little is known about the relevance of adipocyte biomechanics on the etiology of these conditions. Here, we show in male mice in vivo that the adipocyte plasma membrane undergoes caveolar domain reorganization upon lipid droplet expansion. As the lipid droplet grows, caveolae disassemble to release their membrane reservoir and increase cell surface area, and transfer specific caveolar components to the LD surface. Adipose tissue null for caveolae is stiffer, shows compromised deformability, and is prone to rupture under mechanical compression. Mechanistically, phosphoacceptor Cav1 Tyr14 is required for caveolae disassembly: adipocytes bearing a Tyr14Phe mutation at this residue are stiffer and smaller, leading to decreased adiposity in vivo; exhibit deficient transfer of Cav1 and EHD2 to the LD surface, and show distinct Cav1 molecular dynamics and tension adaptation. These results indicate that Cav1 phosphoregulation modulates caveolar dynamics as a relevant component of the homeostatic mechanoadaptation of the differentiated adipocyte.

Date: 2024
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DOI: 10.1038/s41467-024-54224-y

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