Coordination of mitochondrial and lysosomal homeostasis mitigates inflammation and muscle atrophy during aging


Por: Irazoki A, Martinez-Vicente M, Aparicio-García P, Aris C, Alibakhshi E, Rubio-Valera M, Castellanos J, Lores L, Palacín M, Gumá L, Zorzano A and Sebastián D

Publicada: 1 abr 2022 Ahead of Print: 1 mar 2022
Resumen:
Sarcopenia is one of the main factors contributing to the disability of aged people. Among the possible molecular determinants of sarcopenia, increasing evidences suggest that chronic inflammation contributes to its development. However, a key unresolved question is the nature of the factors that drive inflammation during aging and that participate in the development of sarcopenia. In this regard, mitochondrial dysfunction and alterations in mitophagy induce inflammatory responses in a wide range of cells and tissues. However, whether accumulation of damaged mitochondria (MIT) in muscle could trigger inflammation in the context of aging is still unknown. Here, we demonstrate that BCL2 interacting protein 3 (BNIP3) plays a key role in the control of mitochondrial and lysosomal homeostasis, and mitigates muscle inflammation and atrophy during aging. We show that muscle BNIP3 expression increases during aging in mice and in some humans. BNIP3 deficiency alters mitochondrial function, decreases mitophagic flux and, surprisingly, induces lysosomal dysfunction, leading to an upregulation of Toll-like receptor 9 (TLR9)-dependent inflammation and activation of the NLRP3 (nucleotide-binding oligomerization domain (NOD)-, leucine-rich repeat (LRR)-, and pyrin domain-containing protein 3) inflammasome in muscle cells and mouse muscle. Importantly, downregulation of muscle BNIP3 in aged mice exacerbates inflammation and muscle atrophy, and high BNIP3 expression in aged human subjects associates with a low inflammatory profile, suggesting a protective role for BNIP3 against age-induced muscle inflammation in mice and humans. Taken together, our data allow us to propose a new adaptive mechanism involving the mitophagy protein BNIP3, which links mitochondrial and lysosomal homeostasis with inflammation and is key to maintaining muscle health during aging.

Filiaciones:
Irazoki A:
 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain

 Departament de Bioquímica i Biomedicina Molecular, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

 Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto de Salud Carlos III, Barcelona, Spain

Martinez-Vicente M:
 Neurodegenerative Diseases Research Group, Vall d'Hebron Research Institute-Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), Barcelona, Spain

Aparicio-García P:
 Department of Orthopedic Surgery and Traumatology, Hospital General Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Barcelona, Spain

Aris C:
 Department of Family and Community Medicine, Hospital General Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Barcelona, Spain

Alibakhshi E:
 Pneumology Department, Hospital General Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Barcelona, Spain

 Physical Medicine and Rehabilitation Department, Clinical Research Development Unite, Baqyiatallah Hospital, Faculty of Medicine, Baqyiatallah University of Medical Science, Tehran, Iran

 Quantitative MR Imaging and Spectroscopy Group, Research Center for Molecular and Cellular Imaging, Advanced Medical Technologies and Equipment Institute, Tehran University of Medical Science, Tehran, Iran

Rubio-Valera M:
 Hospital General Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Barcelona, Spain

 The Biomedical Research Centre Network for Epidemiology and Public Health (CIBERESP), Madrid, Spain

Castellanos J:
 Department of Orthopedic Surgery and Traumatology, Hospital General Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Barcelona, Spain

Lores L:
 Pneumology Department, Hospital General Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Barcelona, Spain

Palacín M:
 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain

 Departament de Bioquímica i Biomedicina Molecular, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

 CIBER de Enfermedades Raras (CIBERER), Instituto de Salud Carlos III, Madrid, Spain

Gumá L:
 Departament de Bioquímica i Biomedicina Molecular, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

 Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto de Salud Carlos III, Barcelona, Spain

 Institute of Biomedicine of the University of Barcelona (IBUB), Barcelona, Spain

Zorzano A:
 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain

 Departament de Bioquímica i Biomedicina Molecular, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

 Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto de Salud Carlos III, Barcelona, Spain

Sebastián D:
 Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology, Barcelona, Spain

 Departament de Bioquímica i Biomedicina Molecular, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

 Centro de Investigación Biomédica en Red de Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM), Instituto de Salud Carlos III, Barcelona, Spain
ISSN: 14749718





AGING CELL
Editorial
WILEY, 111 RIVER ST, HOBOKEN 07030-5774, NJ, Reino Unido
Tipo de documento: Article
Volumen: 21 Número: 4
Páginas:
WOS Id: 000766271700001
ID de PubMed: 35263007
imagen Green Submitted, gold

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