Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesis

The SLC25A20 gene encodes carnitine-acylcarnitine translocase (CACT), facilitating the transport of long-chain acylcarnitine required for energy production via β-oxidation into the mitochondria. Loss-of-function mutations in this gene lead to CACT deficiency, a rare autosomal recessive disorder of f...

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Main Authors: Ryuichi Hishida, Kohei Ishiguro, Tomoyuki Yamanaka, Shinya Toyokuni, Hideaki Matsui
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Molecular Genetics and Metabolism Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2214426924001186
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author Ryuichi Hishida
Kohei Ishiguro
Tomoyuki Yamanaka
Shinya Toyokuni
Hideaki Matsui
author_facet Ryuichi Hishida
Kohei Ishiguro
Tomoyuki Yamanaka
Shinya Toyokuni
Hideaki Matsui
author_sort Ryuichi Hishida
collection DOAJ
description The SLC25A20 gene encodes carnitine-acylcarnitine translocase (CACT), facilitating the transport of long-chain acylcarnitine required for energy production via β-oxidation into the mitochondria. Loss-of-function mutations in this gene lead to CACT deficiency, a rare autosomal recessive disorder of fatty acid metabolism characterized by severe symptoms including cardiomyopathy, hepatic dysfunction, rhabdomyolysis, hypoketotic hypoglycemia, and hyperammonemia, often resulting in neonatal mortality. Here, we utilized CRISPR/Cas9 gene editing to isolate slc25a20 mutant zebrafish. Homozygous mutants displayed significant lethality, with the majority succumbing before reaching maturity. However, we identified a notably rare homozygous individual that survived into adulthood, prompting a histological examination. Firstly, we observed adipose tissue accumulation at various sites in the homozygous mutant. The mutant heart exhibited hypertrophy, along with degenerated myocardial and muscle cells containing numerous eosinophilic nuclei. Additionally, we found no large oil droplet vacuoles in the mutant liver; however, the hepatocytes displayed numerous small vacuoles resembling lipid droplets. Iron deposition was evident in the spleen and parts of the liver. Overall, our slc25a20 zebrafish mutant displayed tissue pathologies analogous to human CACT deficiency, suggesting its potential as a pathological model contributing to the elucidation of pathogenesis and the improvement/development of therapies for CACT deficiency.
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publishDate 2024-12-01
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spelling doaj-art-d8a1a34b4db045d497cb085f1306aaee2025-08-20T02:49:25ZengElsevierMolecular Genetics and Metabolism Reports2214-42692024-12-014110116510.1016/j.ymgmr.2024.101165Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesisRyuichi Hishida0Kohei Ishiguro1Tomoyuki Yamanaka2Shinya Toyokuni3Hideaki Matsui4Department of Neuroscience of Disease, Brain Research Institute, Niigata University, Niigata 951-8585, JapanDepartment of Neuroscience of Disease, Brain Research Institute, Niigata University, Niigata 951-8585, JapanDepartment of Neuroscience of Disease, Brain Research Institute, Niigata University, Niigata 951-8585, JapanDepartment of Pathology and Biological Responses, Nagoya University Graduate School of Medicine, Nagoya 466-8550, Japan; Center for Low-temperature Plasma Sciences, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8603, JapanDepartment of Neuroscience of Disease, Brain Research Institute, Niigata University, Niigata 951-8585, Japan; Corresponding author at: Department of Neuroscience of Disease, Brain Research Institute, Niigata University, 1-757, Asahimachidori, Niigata 951-8585, Japan.The SLC25A20 gene encodes carnitine-acylcarnitine translocase (CACT), facilitating the transport of long-chain acylcarnitine required for energy production via β-oxidation into the mitochondria. Loss-of-function mutations in this gene lead to CACT deficiency, a rare autosomal recessive disorder of fatty acid metabolism characterized by severe symptoms including cardiomyopathy, hepatic dysfunction, rhabdomyolysis, hypoketotic hypoglycemia, and hyperammonemia, often resulting in neonatal mortality. Here, we utilized CRISPR/Cas9 gene editing to isolate slc25a20 mutant zebrafish. Homozygous mutants displayed significant lethality, with the majority succumbing before reaching maturity. However, we identified a notably rare homozygous individual that survived into adulthood, prompting a histological examination. Firstly, we observed adipose tissue accumulation at various sites in the homozygous mutant. The mutant heart exhibited hypertrophy, along with degenerated myocardial and muscle cells containing numerous eosinophilic nuclei. Additionally, we found no large oil droplet vacuoles in the mutant liver; however, the hepatocytes displayed numerous small vacuoles resembling lipid droplets. Iron deposition was evident in the spleen and parts of the liver. Overall, our slc25a20 zebrafish mutant displayed tissue pathologies analogous to human CACT deficiency, suggesting its potential as a pathological model contributing to the elucidation of pathogenesis and the improvement/development of therapies for CACT deficiency.http://www.sciencedirect.com/science/article/pii/S2214426924001186Zebrafishslc25a20Carnitine-acylcarnitine translocase deficiencyHypertrophiedLipid storage myopathyFatty liver
spellingShingle Ryuichi Hishida
Kohei Ishiguro
Tomoyuki Yamanaka
Shinya Toyokuni
Hideaki Matsui
Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesis
Molecular Genetics and Metabolism Reports
Zebrafish
slc25a20
Carnitine-acylcarnitine translocase deficiency
Hypertrophied
Lipid storage myopathy
Fatty liver
title Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesis
title_full Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesis
title_fullStr Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesis
title_full_unstemmed Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesis
title_short Homozygous slc25a20 zebrafish mutant reveals insights into carnitine-acylcarnitine translocase deficiency pathogenesis
title_sort homozygous slc25a20 zebrafish mutant reveals insights into carnitine acylcarnitine translocase deficiency pathogenesis
topic Zebrafish
slc25a20
Carnitine-acylcarnitine translocase deficiency
Hypertrophied
Lipid storage myopathy
Fatty liver
url http://www.sciencedirect.com/science/article/pii/S2214426924001186
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