OPA1-Exon4b Binds to mtDNA D-Loop for Transcriptional and Metabolic Modulation, Independent of Mitochondrial Fusion
Optic Atrophy 1 (OPA1) has well-established roles in both mitochondrial fusion and apoptotic crista remodeling and is required for the maintenance and distribution of mitochondrial DNA (mtDNA), which are essential for energy metabolism. However, the relationship between OPA1 and mitochondrial metabo...
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| Published in | Frontiers in cell and developmental biology Vol. 8; p. 180 |
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| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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| Abstract | Optic Atrophy 1 (OPA1) has well-established roles in both mitochondrial fusion and apoptotic crista remodeling and is required for the maintenance and distribution of mitochondrial DNA (mtDNA), which are essential for energy metabolism. However, the relationship between OPA1 and mitochondrial metabolism and the underlying mechanisms remain unclear. Here, we show that OPA1-Exon4b modulates mitochondrial respiration and rescues inner mitochondrial membrane potential (Δψm), independent of mitochondrial fusion. OPA1-Exon4b is required for the maintenance of normal TFAM distribution and enhances mtDNA transcription by binding the D-loop of mtDNA. Finally, we show that mRNA levels of OPA1 isoforms containing Exon4b are specifically downregulated in hepatocellular carcinoma (HCC), leading to a reduction in Δψm. Thus, our study demonstrates a novel mitochondrial functional self-recovery pathway involving enhanced mtDNA transcription-mediated recovery of mitochondrial respiratory chain proteins. This mitochondrial fusion-independent pathway may contribute to mitochondrial multi-functional switches in tumorigenesis. |
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| AbstractList | Optic Atrophy 1 (OPA1) has well-established roles in both mitochondrial fusion and apoptotic crista remodeling and is required for the maintenance and distribution of mitochondrial DNA (mtDNA), which are essential for energy metabolism. However, the relationship between OPA1 and mitochondrial metabolism and the underlying mechanisms remain unclear. Here, we show that OPA1-Exon4b modulates mitochondrial respiration and rescues inner mitochondrial membrane potential (Δψm), independent of mitochondrial fusion. OPA1-Exon4b is required for the maintenance of normal TFAM distribution and enhances mtDNA transcription by binding the D-loop of mtDNA. Finally, we show that mRNA levels of OPA1 isoforms containing Exon4b are specifically downregulated in hepatocellular carcinoma (HCC), leading to a reduction in Δψm. Thus, our study demonstrates a novel mitochondrial functional self-recovery pathway involving enhanced mtDNA transcription-mediated recovery of mitochondrial respiratory chain proteins. This mitochondrial fusion-independent pathway may contribute to mitochondrial multi-functional switches in tumorigenesis.Optic Atrophy 1 (OPA1) has well-established roles in both mitochondrial fusion and apoptotic crista remodeling and is required for the maintenance and distribution of mitochondrial DNA (mtDNA), which are essential for energy metabolism. However, the relationship between OPA1 and mitochondrial metabolism and the underlying mechanisms remain unclear. Here, we show that OPA1-Exon4b modulates mitochondrial respiration and rescues inner mitochondrial membrane potential (Δψm), independent of mitochondrial fusion. OPA1-Exon4b is required for the maintenance of normal TFAM distribution and enhances mtDNA transcription by binding the D-loop of mtDNA. Finally, we show that mRNA levels of OPA1 isoforms containing Exon4b are specifically downregulated in hepatocellular carcinoma (HCC), leading to a reduction in Δψm. Thus, our study demonstrates a novel mitochondrial functional self-recovery pathway involving enhanced mtDNA transcription-mediated recovery of mitochondrial respiratory chain proteins. This mitochondrial fusion-independent pathway may contribute to mitochondrial multi-functional switches in tumorigenesis. Optic Atrophy 1 (OPA1) has well-established roles in both mitochondrial fusion and apoptotic crista remodeling and is required for the maintenance and distribution of mitochondrial DNA (mtDNA), which are essential for energy metabolism. However, the relationship between OPA1 and mitochondrial metabolism and the underlying mechanisms remain unclear. Here, we show that OPA1-Exon4b modulates mitochondrial respiration and rescues inner mitochondrial membrane potential (Δψm), independent of mitochondrial fusion. OPA1-Exon4b is required for the maintenance of normal TFAM distribution and enhances mtDNA transcription by binding the D-loop of mtDNA. Finally, we show that mRNA levels of OPA1 isoforms containing Exon4b are specifically downregulated in hepatocellular carcinoma (HCC), leading to a reduction in Δψm. Thus, our study demonstrates a novel mitochondrial functional self-recovery pathway involving enhanced mtDNA transcription-mediated recovery of mitochondrial respiratory chain proteins. This mitochondrial fusion-independent pathway may contribute to mitochondrial multi-functional switches in tumorigenesis. |
| Author | Pan, Yongzhang Zeng, Sheng Li, Yukun Jiang, Yiguo Xiang, Ge Yang, Liang Zhuang, Shi-Mei Tang, Haite Wu, Yi Lin, Yi-Fang Liu, Xingguo Lin, Xiaobing Song, Zhiyin |
| AuthorAffiliation | 5 Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University , Wuhan , China 6 State Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University , Guangzhou , China 1 CAS Key Laboratory of Regenerative Biology, Joint School of Life Sciences, Hefei Institute of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou Medical University , Guangzhou , China 2 Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, South China Institute for Stem Cell Biology and Regenerative Medicine, Institute for Stem Cell and Regeneration, Guangzhou Institutes of Biomedicine and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences , Guangzhou , China 4 MOE Key Laboratory of Gene Function and Regulation, School of Life Sciences, Collaborative Innovation Center for Can |
| AuthorAffiliation_xml | – name: 5 Hubei Key Laboratory of Cell Homeostasis, College of Life Sciences, Wuhan University , Wuhan , China – name: 4 MOE Key Laboratory of Gene Function and Regulation, School of Life Sciences, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University , Guangzhou , China – name: 1 CAS Key Laboratory of Regenerative Biology, Joint School of Life Sciences, Hefei Institute of Stem Cell and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou Medical University , Guangzhou , China – name: 6 State Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University , Guangzhou , China – name: 2 Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangdong Provincial Key Laboratory of Stem Cell and Regenerative Medicine, South China Institute for Stem Cell Biology and Regenerative Medicine, Institute for Stem Cell and Regeneration, Guangzhou Institutes of Biomedicine and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences , Guangzhou , China – name: 3 State Key Laboratory of Respiratory Disease, Guangzhou Regenerative Medicine and Health Guangdong Laboratory, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences , Guangzhou , China |
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| Copyright | Copyright © 2020 Yang, Tang, Lin, Wu, Zeng, Pan, Li, Xiang, Lin, Zhuang, Song, Jiang and Liu. Copyright © 2020 Yang, Tang, Lin, Wu, Zeng, Pan, Li, Xiang, Lin, Zhuang, Song, Jiang and Liu. 2020 Yang, Tang, Lin, Wu, Zeng, Pan, Li, Xiang, Lin, Zhuang, Song, Jiang and Liu |
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| Keywords | Optic Atrophy 1 (OPA1) mitochondrial fusion mitochondrial DNA hepatocellular carcinoma mtDNA D-loop |
| Language | English |
| License | Copyright © 2020 Yang, Tang, Lin, Wu, Zeng, Pan, Li, Xiang, Lin, Zhuang, Song, Jiang and Liu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Laura Lackner, Northwestern University, United States These authors have contributed equally to this work This article was submitted to Molecular Medicine, a section of the journal Frontiers in Cell and Developmental Biology Reviewed by: Ian Jame Holt, Biodonostia Health Research Institute (IIS Biodonostia), Spain; Ryan J. Mailloux, McGill University, Canada |
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| SubjectTerms | Cell and Developmental Biology hepatocellular carcinoma mitochondrial DNA mitochondrial fusion mtDNA D-loop Optic Atrophy 1 (OPA1) |
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| Title | OPA1-Exon4b Binds to mtDNA D-Loop for Transcriptional and Metabolic Modulation, Independent of Mitochondrial Fusion |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/32373606 https://www.proquest.com/docview/2399236912 https://pubmed.ncbi.nlm.nih.gov/PMC7179665 https://doaj.org/article/0d7372cd69674f4eba43e0a7c2063873 |
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