Endonuclease G promotes hepatic mitochondrial respiration by selectively increasing mitochondrial tRNA <sup>Thr</sup> production

X Xihui Xu (Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH) R Rozhin Penjweini L Lóránt Székvölgyi (Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen) Z Zsolt Karányi (Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen) A Anne-Marie Heckel (UMR 7156 Génétique Moléculaire, Génomique, Microbiologie, Strasbourg University-CNRS) D Devikala Gurusamy (Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH) D Dóra Varga (Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen) S Shutong Yang (Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH) A Alexandra L. Brown (Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH) W Wenqi Cui (Liver and Energy Metabolism Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases) J Jinsung Park (Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH) D Dénes Nagy (Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen) M Maren C. Podszun (Liver and Energy Metabolism Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases) S Sarah Yang (DNA Sequencing and Genomics Core Facility, National Heart Lung and Blood Institute, NIH) K Komudi Singh (Bioinformatics Core Facility, National Heart Lung and Blood Institute, NIH) S Stephen P. Ashcroft (Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen) J Jeonghan Kim (Department of Biochemistry, College of Medicine, The Catholic University of Korea) M Myung K. Kim (Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH) I Ivan Tarassov (UMR 7156 Génétique Moléculaire, Génomique, Microbiologie, Strasbourg University-CNRS) J Jun Zhu (Wuxi EliTe Solar Co., Wuxi, China.) A Andrew Philp (Centre for Healthy Ageing, Centenary Institute, Royal Prince Alfred Hospital) Y Yaron Rotman J Jay R. Knutson N Nina Entelis (UMR 7156 Génétique Moléculaire, Génomique, Microbiologie, Strasbourg University-CNRS) J Jay H. Chung (Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH)

Abstract

Mitochondrial endonuclease G (EndoG) contributes to chromosomal degradation when it is released from mitochondria during apoptosis. It is presumed to also have a mitochondrial function because EndoG deficiency causes mitochondrial dysfunction. However, the mechanism by which EndoG regulates mitochondrial function is not known. Fat accumulation in metabolic dysfunction–associated steatotic liver disease (MASLD), which is more common in men, is caused in part by mitochondrial dysfunction. EndoG expression is reduced in MASLD liver, and EndoG deficiency causes MASLD in an obesity-independent manner but only in males. EndoG promotes mitochondrial respiration by resolving mitochondrial tRNA/DNA hybrids formed during mtDNA transcription by recruiting RNA helicase DHX30 to unwind them. EndoG also cleaves off the 3′-end of the H-strand transcript that can prevent mt-tRNA Thr precursor cloverleaf-folding, and processing, which increases mt-tRNA Thr production and mitochondrial translation. Using fluorescent lifetime imaging microscopy technology to visualize oxygen consumption at the individual mitochondrion level, we found that EndoG deficiency leads to the selective loss of a mitochondrial subpopulation with high-oxygen consumption. This defect was reversed with mt-tRNA Thr supplementation. Thus, EndoG promotes mitochondrial respiration by selectively regulating the production of mt-tRNA Thr in male mice.

Article Details

Volume / Issue Vol. 122, Issue 1
Published January 07, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (25)

X

Xihui Xu

Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH

R

Rozhin Penjweini

L

Lóránt Székvölgyi

Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen

Z

Zsolt Karányi

Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen

A

Anne-Marie Heckel

UMR 7156 Génétique Moléculaire, Génomique, Microbiologie, Strasbourg University-CNRS

D

Devikala Gurusamy

Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH

D

Dóra Varga

Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen

S

Shutong Yang

Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH

A

Alexandra L. Brown

Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH

W

Wenqi Cui

Liver and Energy Metabolism Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases

J

Jinsung Park

Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH

D

Dénes Nagy

Momentum Genome Architecture and Recombination Research Group, Department of Molecular and Nanopharmaceutics, Faculty of Pharmacy, University of Debrecen

M

Maren C. Podszun

Liver and Energy Metabolism Section, Liver Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases

S

Sarah Yang

DNA Sequencing and Genomics Core Facility, National Heart Lung and Blood Institute, NIH

K

Komudi Singh

Bioinformatics Core Facility, National Heart Lung and Blood Institute, NIH

S

Stephen P. Ashcroft

Novo Nordisk Foundation Center for Basic Metabolic Research, Faculty of Health and Medical Sciences, University of Copenhagen

J

Jeonghan Kim

Department of Biochemistry, College of Medicine, The Catholic University of Korea

M

Myung K. Kim

Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH

I

Ivan Tarassov

UMR 7156 Génétique Moléculaire, Génomique, Microbiologie, Strasbourg University-CNRS

J

Jun Zhu

Wuxi EliTe Solar Co., Wuxi, China.

A

Andrew Philp

Centre for Healthy Ageing, Centenary Institute, Royal Prince Alfred Hospital

Y

Yaron Rotman

J

Jay R. Knutson

N

Nina Entelis

UMR 7156 Génétique Moléculaire, Génomique, Microbiologie, Strasbourg University-CNRS

J

Jay H. Chung

Laboratory of Obesity and Aging Research, Cardiovascular Branch, National Heart Lung and Blood Institute, NIH