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FBXL4 – Encephalomyopathic Mitochondrial DNA Depletion Syndrome 13

FBXL4 encodes an F-box and leucine-rich repeat protein critical for mitochondrial DNA (mtDNA) maintenance. Biallelic pathogenic variants in FBXL4 cause encephalomyopathic mitochondrial DNA depletion syndrome 13 (MTDPS13), an autosomal recessive disorder characterized by infantile onset hypotonia, failure to thrive, global developmental delay, encephalopathy, brain atrophy, and persistent lactic acidosis. Diagnostic sequencing of FBXL4 is recommended in patients presenting with these features even if mitochondrial respiratory chain enzyme activities are normal.

1. Clinical Validity

The association between FBXL4 and Encephalomyopathic Mitochondrial DNA Depletion Syndrome 13 is classified as Definitive by ClinGen criteria. Over 100 probands worldwide have been reported with biallelic FBXL4 variants and consistent autosomal recessive inheritance ([PMID:30804983]). Multiple unrelated kindreds, including consanguineous families, demonstrate the same genotype–phenotype correlation. Functional complementation and animal model studies further confirm causality.

2. Genetic Evidence

Inheritance is strictly autosomal recessive. Segregation data include at least 2 additional affected relatives in consanguineous families with homozygous FBXL4 variants. Case series describe 94 unrelated patients with MTDPS13 across diverse ethnicities, including a possible Arab founder variant ([PMID:30804983]). The variant spectrum comprises missense, nonsense, frameshift, and splice-site mutations. A representative pathogenic variant is c.1442T>C (p.Leu481Pro) identified in a Norwegian proband ([PMID:27182039]).

3. Functional Evidence

Loss-of-function and splice mutations in FBXL4 result in severe mtDNA depletion, mitochondrial respiratory chain deficiency, reduced membrane potential, and disrupted mitochondrial network dynamics in patient fibroblasts. Expression of wild-type FBXL4 fully rescued mtDNA copy number and biochemical deficits in cell lines ([PMID:23993193]). Mouse models harboring patient-derived FBXL4 mutations exhibit perinatal lethality, hyperactive mitophagy, and accumulation of BNIP3/BNIP3L, implicating excessive mitophagy in pathogenesis ([PMID:37568009]; [PMID:36896912]).

4. Mechanism and Therapeutic Insights

Mechanistic studies reveal that FBXL4 functions as a substrate adaptor for the SCF-Cullin1 ubiquitin ligase complex, targeting mitophagy receptors BNIP3 and BNIP3L for degradation. FBXL4 deficiency leads to uncontrolled mitophagy, mtDNA depletion, and energy failure. Dichloroacetate treatment mitigated lactic acidosis in patients and partially corrected acidification in fibroblasts, suggesting potential metabolic therapy.

5. Integration and Key Take-Home

Collectively, the genetic and experimental evidence provides a robust, definitive link between FBXL4 loss-of-function and MTDPS13. Clinical genetic testing for FBXL4 variants enables early diagnosis, informs management of metabolic crises, guides family counseling, and facilitates potential therapeutic interventions.

Key Take-home: Biallelic FBXL4 variants cause a definitive autosomal recessive encephalomyopathic mitochondrial DNA depletion syndrome, diagnosable by sequencing and supported by functional rescue and animal model data.

References

  • American Journal of Human Genetics • 2013 • Mutations in FBXL4 cause mitochondrial encephalopathy and a disorder of mitochondrial DNA maintenance. PMID:23993193
  • European Journal of Medical Genetics • 2016 • A novel mutation in FBXL4 in a Norwegian child with encephalomyopathic mitochondrial DNA depletion syndrome 13. PMID:27182039
  • Frontiers in Genetics • 2019 • FBXL4-Related Mitochondrial DNA Depletion Syndrome 13 (MTDPS13): A Case Report With a Comprehensive Mutation Review. PMID:30804983
  • Cell Death and Differentiation • 2023 • FBXL4 mutations cause excessive mitophagy via BNIP3/BNIP3L accumulation leading to mitochondrial DNA depletion syndrome. PMID:37568009
  • The EMBO Journal • 2023 • A mitochondrial SCF-FBXL4 ubiquitin E3 ligase complex degrades BNIP3 and NIX to restrain mitophagy and prevent mitochondrial disease. PMID:36896912

Evidence Based Scoring (AI generated)

Gene–Disease Association

Definitive

Over 100 probands across multiple unrelated families with consistent autosomal recessive inheritance and concordant functional studies

Genetic Evidence

Strong

94 unrelated patients with biallelic FBXL4 variants in autosomal recessive inheritance; genetic evidence cap reached

Functional Evidence

Strong

Multiple in vitro complementation assays and animal models demonstrating restoration of mtDNA copy number and reversal of mitochondrial dysfunction