Molecular Characterization of New FBXL4 Mutations in Patients With mtDNA Depletion Syndrome


Por: Emperador S, Garrido-Pérez N, Amezcua-Gil J, Gaudó P, Andrés-Sanz JA, Yubero-Siles D, Fernández-Marmiesse A, O'Callaghan-Gordo M, Ortigoza-Escobar JD, Iriondo-Sanz M, Ruiz-Pesini E, Garcia-Cazorla A, Gil-Campos M, Artuch-Iriberri R, Montoya C and Bayona-Bafaluy MP

Publicada: 8 ene 2020 Ahead of Print: 8 ene 2020
Resumen:
Encephalomyopathic mitochondrial DNA (mtDNA) depletion syndrome 13 (MTDPS13) is a rare genetic disorder caused by defects in F-box leucine-rich repeat protein 4 (FBXL4). Although FBXL4 is essential for the bioenergetic homeostasis of the cell, the precise role of the protein remains unknown. In this study, we report two cases of unrelated patients presenting in the neonatal period with hyperlactacidemia and generalized hypotonia. Severe mtDNA depletion was detected in muscle biopsy in both patients. Genetic analysis showed one patient as having in compound heterozygosis a splice site variant c.858+5G>C and a missense variant c.1510T>C (p.Cys504Arg) in FBXL4. The second patient harbored a frameshift novel variant c.851delC (p.Pro284LeufsTer7) in homozygosis. To validate the pathogenicity of these variants, molecular and biochemical analyses were performed using skin-derived fibroblasts. We observed that the mtDNA depletion was less severe in fibroblasts than in muscle. Interestingly, the cells harboring a nonsense variant in homozygosis showed normal mtDNA copy number. Both patient fibroblasts, however, demonstrated reduced mitochondrial transcript quantity leading to diminished steady state levels of respiratory complex subunits, decreased respiratory complex IV (CIV) activity, and finally, low mitochondrial ATP levels. Both patients also revealed citrate synthase deficiency. Genetic complementation assays established that the deficient phenotype was rescued by the canonical version of FBXL4, confirming the pathological nature of the variants. Further analysis of fibroblasts allowed to establish that increased mitochondrial mass, mitochondrial fragmentation, and augmented autophagy are associated with FBXL4 deficiency in cells, but are probably secondary to a primary metabolic defect affecting oxidative phosphorylation.

Filiaciones:
Emperador S:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

 Instituto de Investigación Sanitaria de Aragón (IIS-Aragón), Zaragoza, Spain

 Fundación ARAID, Universidad de Zaragoza, Zaragoza, Spain

Garrido-Pérez N:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

 Instituto de Investigación Sanitaria de Aragón (IIS-Aragón), Zaragoza, Spain

 Fundación ARAID, Universidad de Zaragoza, Zaragoza, Spain

Amezcua-Gil J:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

Gaudó P:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

Andrés-Sanz JA:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

Yubero-Siles D:
 Clinical Biochemistry, Genetics, Pediatric Neurology and Neonatalogy Departments, Institut de Recerca Sant Joan de Déu, Barcelona, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Fernández-Marmiesse A:
 Genomes&Disease Group, Molecular Medicine and Chronic Diseases Research Centre (CiMUS), Santiago de Compostela University-IDIS, Santiago de Compostela, Spain

O'Callaghan-Gordo M:
 Clinical Biochemistry, Genetics, Pediatric Neurology and Neonatalogy Departments, Institut de Recerca Sant Joan de Déu, Barcelona, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Ortigoza-Escobar JD:
 Clinical Biochemistry, Genetics, Pediatric Neurology and Neonatalogy Departments, Institut de Recerca Sant Joan de Déu, Barcelona, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Iriondo-Sanz M:
 Clinical Biochemistry, Genetics, Pediatric Neurology and Neonatalogy Departments, Institut de Recerca Sant Joan de Déu, Barcelona, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Ruiz-Pesini E:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

 Instituto de Investigación Sanitaria de Aragón (IIS-Aragón), Zaragoza, Spain

 Fundación ARAID, Universidad de Zaragoza, Zaragoza, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Garcia-Cazorla A:
 Clinical Biochemistry, Genetics, Pediatric Neurology and Neonatalogy Departments, Institut de Recerca Sant Joan de Déu, Barcelona, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Gil-Campos M:
 Metabolism Unit, Reina Sofia University Clinical Hospital, Institute Maimónides of Biomedicine Investigation of Córdoba (IMIBIC), University of Córdoba, Córdoba, Spain

 CIBEROBN (Physiopathology of Obesity and Nutrition CB12/03/30038), Madrid, Spain

Artuch-Iriberri R:
 Clinical Biochemistry, Genetics, Pediatric Neurology and Neonatalogy Departments, Institut de Recerca Sant Joan de Déu, Barcelona, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Montoya C:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

 Instituto de Investigación Sanitaria de Aragón (IIS-Aragón), Zaragoza, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain

Bayona-Bafaluy MP:
 Departamento de Bioquímica, Biología Molecular y Celular, Universidad de Zaragoza, Zaragoza, Spain

 Instituto de Investigación Sanitaria de Aragón (IIS-Aragón), Zaragoza, Spain

 Centro de Investigaciones Biomédicas en Red de Enfermedades Raras (CIBERER), Madrid, Spain
ISSN: 16648021





Frontiers in Genetics
Editorial
FRONTIERS MEDIA SA, AVENUE DU TRIBUNAL FEDERAL 34, LAUSANNE CH-1015, SWITZERLAND, Suiza
Tipo de documento: Article
Volumen: 10 Número:
Páginas: 1300-1300
WOS Id: 000509526800001
ID de PubMed: 31969900
imagen Green Submitted, gold

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