Tissue-specific expression atlas of murine mitochondrial tRNAs

Qiufen He; Xiao He; Yun Xiao; Qiong Zhao; Zhenzhen Ye; Limei Cui; Ye Chen; Min-Xin Guan

doi:10.1016/j.jbc.2021.100960

Tissue-specific expression atlas of murine mitochondrial tRNAs

J Biol Chem. 2021 Aug;297(2):100960. doi: 10.1016/j.jbc.2021.100960. Epub 2021 Jul 13.

Authors

Qiufen He¹, Xiao He¹, Yun Xiao², Qiong Zhao², Zhenzhen Ye², Limei Cui², Ye Chen³, Min-Xin Guan⁴

Affiliations

¹ Division of Medical Genetics and Genomics, The Children's Hospital, Zhejiang University School of Medicine and National Clinical Research Center for Child Health, Hangzhou, Zhejiang, China; Institute of Genetics, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.
² Institute of Genetics, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.
³ Division of Medical Genetics and Genomics, The Children's Hospital, Zhejiang University School of Medicine and National Clinical Research Center for Child Health, Hangzhou, Zhejiang, China; Institute of Genetics, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China; Zhejiang Provincial Key Lab of Genetic and Developmental Disorders, Zhejiang Univrsity, Hangzhou, Zhejiang, China. Electronic address: yechency@zju.edu.cn.
⁴ Division of Medical Genetics and Genomics, The Children's Hospital, Zhejiang University School of Medicine and National Clinical Research Center for Child Health, Hangzhou, Zhejiang, China; Institute of Genetics, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China; Zhejiang Provincial Key Lab of Genetic and Developmental Disorders, Zhejiang Univrsity, Hangzhou, Zhejiang, China; Key Lab of Reproductive Genetics, Center for Mitochondrial Genetics, Ministry of Education of PRC, Zhejiang University, Hangzhou, Zhejiang, China; Division of Mitochondrial Biomedicine, Zhejiang University-University of Toronto Joint Institute of Genetics and Genome Medicine, Hangzhou, Zhejiang, China. Electronic address: gminxin88@zju.edu.cn.

Abstract

Mammalian mitochondrial tRNA (mt-tRNA) plays a central role in the synthesis of the 13 subunits of the oxidative phosphorylation complex system (OXPHOS). However, many aspects of the context-dependent expression of mt-tRNAs in mammals remain unknown. To investigate the tissue-specific effects of mt-tRNAs, we performed a comprehensive analysis of mitochondrial tRNA expression across five mice tissues (brain, heart, liver, skeletal muscle, and kidney) using Northern blot analysis. Striking differences in the tissue-specific expression of 22 mt-tRNAs were observed, in some cases differing by as much as tenfold from lowest to highest expression levels among these five tissues. Overall, the heart exhibited the highest levels of mt-tRNAs, while the liver displayed markedly lower levels. Variations in the levels of mt-tRNAs showed significant correlations with total mitochondrial DNA (mtDNA) contents in these tissues. However, there were no significant differences observed in the 2-thiouridylation levels of tRNA^Lys, tRNA^Glu, and tRNA^Gln among these tissues. A wide range of aminoacylation levels for 15 mt-tRNAs occurred among these five tissues, with skeletal muscle and kidneys most notably displaying the highest and lowest tRNA aminoacylation levels, respectively. Among these tissues, there was a negative correlation between variations in mt-tRNA aminoacylation levels and corresponding variations in mitochondrial tRNA synthetases (mt-aaRS) expression levels. Furthermore, the variable levels of OXPHOS subunits, as encoded by mtDNA or nuclear genes, may reflect differences in relative functional emphasis for mitochondria in each tissue. Our findings provide new insight into the mechanism of mt-tRNA tissue-specific effects on oxidative phosphorylation.

Keywords: mitochondrial tRNA; murine; oxidative phosphorylation; tissue specific expression; translation.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Cell Nucleus / metabolism
Mice
Mitochondria*
Organ Specificity
Oxidative Phosphorylation
RNA Processing, Post-Transcriptional
RNA, Transfer*

Substances

RNA, Transfer