Peripheral modulation of antidepressant targets MAO-B and GABAAR by harmol induces mitohormesis and delays aging in preclinical models

Authors

Luis Filipe Costa-Machado, IMDEA Food Institute
Esther Garcia-Dominguez, Hospital Clinico Universitario de Valencia
Rebecca L. McIntyre, Universiteit van Amsterdam
Jose Luis Lopez-Aceituno, IMDEA Food Institute
Álvaro Ballesteros-Gonzalez, Centro de Investigacion Principe Felipe
Andrea Tapia-Gonzalez, Centro de Investigacion Principe Felipe
David Fabregat-Safont, Hospital del Mar
Tobias Eisenberg, Universitat Graz
Jesús Gomez, Centro Nacional de Investigaciones Oncológicas
Adrian Plaza, IMDEA Food Institute
Aranzazu Sierra-Ramirez, IMDEA Food Institute
Manuel Perez, Centro Nacional de Investigaciones Oncológicas
David Villanueva-Bermejo, CSIC-UAM - Instituto de Investigacion en Ciencias de la Alimentacion (CIAL)
Tiziana Fornari, CSIC-UAM - Instituto de Investigacion en Ciencias de la Alimentacion (CIAL)
María Isabel Loza, Kaertor Foundation
Gonzalo Herradon, Universidad San Pablo-CEU
Sebastian J. Hofer, Universitat Graz
Christoph Magnes, Joanneum Research Forschungsgesellschaft mbH
Frank Madeo, Universitat Graz
Janet S. Duerr, Ohio University
Oscar J. Pozo, Hospital del Mar
Maximo Ibo Galindo, Centro de Investigacion Principe Felipe
Isabel del Pino, Centro de Investigacion Principe Felipe
Riekelt H. Houtkooper, Universiteit van Amsterdam
Diego Megias, Centro Nacional de Investigaciones Oncológicas
Jose Viña, Hospital Clinico Universitario de Valencia
Mari Carmen Gomez-Cabrera, Hospital Clinico Universitario de Valencia
Pablo J. Fernandez-Marcos, IMDEA Food Institute

Document Type

Article

Publication Date

12-1-2023

Abstract

Reversible and sub-lethal stresses to the mitochondria elicit a program of compensatory responses that ultimately improve mitochondrial function, a conserved anti-aging mechanism termed mitohormesis. Here, we show that harmol, a member of the beta-carbolines family with anti-depressant properties, improves mitochondrial function and metabolic parameters, and extends healthspan. Treatment with harmol induces a transient mitochondrial depolarization, a strong mitophagy response, and the AMPK compensatory pathway both in cultured C2C12 myotubes and in male mouse liver, brown adipose tissue and muscle, even though harmol crosses poorly the blood–brain barrier. Mechanistically, simultaneous modulation of the targets of harmol monoamine-oxidase B and GABA-A receptor reproduces harmol-induced mitochondrial improvements. Diet-induced pre-diabetic male mice improve their glucose tolerance, liver steatosis and insulin sensitivity after treatment with harmol. Harmol or a combination of monoamine oxidase B and GABA-A receptor modulators extend the lifespan of hermaphrodite Caenorhabditis elegans or female Drosophila melanogaster. Finally, two-year-old male and female mice treated with harmol exhibit delayed frailty onset with improved glycemia, exercise performance and strength. Our results reveal that peripheral targeting of monoamine oxidase B and GABA-A receptor, common antidepressant targets, extends healthspan through mitohormesis.

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