Disrupted Mitochondrial and Metabolic Plasticity Underlie Comorbidity between Age-Related and Degenerative Disorders as Parkinson Disease and Type 2 Diabetes Mellitus
Diana Luz Juárez-Flores,
Mario Ezquerra,
ïngrid Gonzàlez-Casacuberta,
Aida Ormazabal,
Constanza Morén,
Eduardo Tolosa,
Raquel Fucho,
Mariona Guitart-Mampel,
Mercedes Casado,
Francesc Valldeoriola,
Joan de la Torre-Lara,
Esteban Muñoz,
Ester Tobías,
Yaroslau Compta,
Francesc Josep García-García,
Carmen García-Ruiz,
Jose Carlos Fernandez-Checa,
Maria José Martí,
Josep Maria Grau,
Francesc Cardellach,
Rafael Artuch,
Rubén Fernández-Santiago,
Glòria Garrabou
Affiliations
Diana Luz Juárez-Flores
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Mario Ezquerra
Laboratory of Parkinson Disease and Other Neurodegenerative Movement Disorders, IDIBAPS, Institut de Neurociències, UB, 08036 Barcelona, Spain
ïngrid Gonzàlez-Casacuberta
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Aida Ormazabal
Centro de Investigación Biomédica en Red (CIBER) de Enfermedades Raras (CIBERER), 28029 Madrid, Spain
Constanza Morén
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Eduardo Tolosa
Laboratory of Parkinson Disease and Other Neurodegenerative Movement Disorders, IDIBAPS, Institut de Neurociències, UB, 08036 Barcelona, Spain
Raquel Fucho
Department of Cell Death and Proliferation, Instituto de Investigaciones Biomédicas de Barcelona (IIBB), Consejo Superior Investigaciones Científicas (CSIC), 08001 Barcelona, Spain
Mariona Guitart-Mampel
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Mercedes Casado
Centro de Investigación Biomédica en Red (CIBER) de Enfermedades Raras (CIBERER), 28029 Madrid, Spain
Francesc Valldeoriola
Laboratory of Parkinson Disease and Other Neurodegenerative Movement Disorders, IDIBAPS, Institut de Neurociències, UB, 08036 Barcelona, Spain
Joan de la Torre-Lara
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Esteban Muñoz
Laboratory of Parkinson Disease and Other Neurodegenerative Movement Disorders, IDIBAPS, Institut de Neurociències, UB, 08036 Barcelona, Spain
Ester Tobías
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Yaroslau Compta
Laboratory of Parkinson Disease and Other Neurodegenerative Movement Disorders, IDIBAPS, Institut de Neurociències, UB, 08036 Barcelona, Spain
Francesc Josep García-García
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Carmen García-Ruiz
Department of Cell Death and Proliferation, Instituto de Investigaciones Biomédicas de Barcelona (IIBB), Consejo Superior Investigaciones Científicas (CSIC), 08001 Barcelona, Spain
Jose Carlos Fernandez-Checa
Department of Cell Death and Proliferation, Instituto de Investigaciones Biomédicas de Barcelona (IIBB), Consejo Superior Investigaciones Científicas (CSIC), 08001 Barcelona, Spain
Maria José Martí
Laboratory of Parkinson Disease and Other Neurodegenerative Movement Disorders, IDIBAPS, Institut de Neurociències, UB, 08036 Barcelona, Spain
Josep Maria Grau
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Francesc Cardellach
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Rafael Artuch
Centro de Investigación Biomédica en Red (CIBER) de Enfermedades Raras (CIBERER), 28029 Madrid, Spain
Rubén Fernández-Santiago
Laboratory of Parkinson Disease and Other Neurodegenerative Movement Disorders, IDIBAPS, Institut de Neurociències, UB, 08036 Barcelona, Spain
Glòria Garrabou
Laboratory of Muscle Research and Mitochondrial Function, Department of Internal Medicine-Hospital Clínic of Barcelona (HCB), Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Faculty of Medicine and Health Science, University of Barcelona (UB), 08036 Barcelona, Spain
Idiopathic Parkinson’s disease (iPD) and type 2 diabetes mellitus (T2DM) are chronic, multisystemic, and degenerative diseases associated with aging, with eventual epidemiological co-morbidity and overlap in molecular basis. This study aims to explore if metabolic and mitochondrial alterations underlie the previously reported epidemiologic and clinical co-morbidity from a molecular level. To evaluate the adaptation of iPD to a simulated pre-diabetogenic state, we exposed primary cultured fibroblasts from iPD patients and controls to standard (5 mM) and high (25 mM) glucose concentrations to further characterize metabolic and mitochondrial resilience. iPD fibroblasts showed increased organic and amino acid levels related to mitochondrial metabolism with respect to controls, and these differences were enhanced in high glucose conditions (citric, suberic, and sebacic acids levels increased, as well as alanine, glutamate, aspartate, arginine, and ornithine amino acids; p-values between 0.001 and 0.05). The accumulation of metabolites in iPD fibroblasts was associated with (and probably due to) the concomitant mitochondrial dysfunction observed at enzymatic, oxidative, respiratory, and morphologic level. Metabolic and mitochondrial plasticity of controls was not observed in iPD fibroblasts, which were unable to adapt to different glucose conditions. Impaired metabolism and mitochondrial activity in iPD may limit energy supply for cell survival. Moreover, reduced capacity to adapt to disrupted glucose balance characteristic of T2DM may underlay the co-morbidity between both diseases. Conclusions: Fibroblasts from iPD patients showed mitochondrial impairment, resulting in the accumulation of organic and amino acids related to mitochondrial metabolism, especially when exposed to high glucose. Mitochondrial and metabolic defects down warding cell plasticity to adapt to changing glucose bioavailability may explain the comorbidity between iPD and T2DM.