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Cited by 8Mitochondrial Function and PathologyGenomics and Chromatin DynamicsAutophagy in Disease and Therapy

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A transcription network underlies the dual genomic coordination of mitochondrial biogenesis

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Zhang, Fan, Lee, Annie, Freitas, Anna V, Herb, Jake T, Wang, Zong-Heng, Gupta, Snigdha, Chen, Zhe, Xu, Hong·2024·eLife
DOI 10.7554/elife.96536.3PMC PMC10896348

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Abstract

Mitochondrial biogenesis requires the expression of genes encoded by both the nuclear and mitochondrial genomes. However, aside from a handful transcription factors regulating specific subsets of mitochondrial genes, the overall architecture of the transcriptional control of mitochondrial biogenesis remains to be elucidated. The mechanisms coordinating these two genomes are largely unknown. We performed a targeted RNAi screen in developing eyes with reduced mitochondrial DNA content, anticipating a synergistic disruption of tissue development due to impaired mitochondrial biogenesis and mitochondrial DNA (mtDNA) deficiency. Among 638 transcription factors annotated in the Drosophila genome, 77 were identified as potential regulators of mitochondrial biogenesis. Utilizing published ChIP-seq data of positive hits, we constructed a regulatory network revealing the logic of the transcription regulation of mitochondrial biogenesis. Multiple transcription factors in core layers had extensive connections, collectively governing the expression of nearly all mitochondrial genes, whereas factors sitting on the top layer may respond to cellular cues to modulate mitochondrial biogenesis through the underlying network. CG1603, a core component of the network, was found to be indispensable for the expression of most nuclear mitochondrial genes, including those required for mtDNA maintenance and gene expression, thus coordinating nuclear genome and mtDNA activities in mitochondrial biogenesis. Additional genetic analyses validated YL-1, a transcription factor upstream of CG1603 in the network, as a regulator controlling CG1603 expression and mitochondrial biogenesis.

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Metadata

Authors
Zhang, F., Lee, A., Freitas, A. V., Herb, J. T., Wang, Z.-H., Gupta, S., Chen, Z., & Xu, H.
Affiliations
  • National Institutes of Health (US)
  • National Heart, Lung, and Blood Institute, National Institutes of Health
Corresponding author
Xu, Hong
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2024-12-27
Volume
13
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.96536.3
PMC
PMC10896348
OpenAlex
W4405830359
Cited by
8
References
2
Citations by year
2026: 3 · 2025: 5
FWCI
1.09
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
Funders
National Heart, Lung, and Blood Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Keywords
mitochondrial biogenesis, transcriptional regulation, transcriptional regulatory networks, mitochondrial DNA maintenance, Drosophila eye development, RNAi screen, transcription factors

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