Cited by 284Mitochondrial Function and PathologyAutophagy in Disease and TherapyATP Synthase and ATPases Research

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Cellular ATP demand creates metabolically distinct subpopulations of mitochondria

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Ryu, Keun Woo, Fung, Tak Shun, Baker, Daphne C., Saoi, Michelle, Park, Jinsung, Febres-Aldana, Christopher A., Aly, Rania G., Cui, Ruobing, Sharma, Anurag, Fu, Yi, Jones, Olivia L., Cai, Xin, Pasolli, H. Amalia, Cross, Justin R., Rudin, Charles M., Thompson, Craig B.·2024·Nature

DOI 10.1038/s41586-024-08146-wPMC PMC11869630

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Abstract

Mitochondria serve a crucial role in cell growth and proliferation by supporting both ATP synthesis and the production of macromolecular precursors. Whereas oxidative phosphorylation (OXPHOS) depends mainly on the oxidation of intermediates from the tricarboxylic acid cycle, the mitochondrial production of proline and ornithine relies on reductive synthesis 1. How these competing metabolic pathways take place in the same organelle is not clear. Here we show that when cellular dependence on OXPHOS increases, pyrroline-5-carboxylate synthase (P5CS)-the rate-limiting enzyme in the reductive synthesis of proline and ornithine-becomes sequestered in a subset of mitochondria that lack cristae and ATP synthase. This sequestration is driven by both the intrinsic ability of P5CS to form filaments and the mitochondrial fusion and fission cycle. Disruption of mitochondrial dynamics, by impeding mitofusin-mediated fusion or dynamin-like-protein-1-mediated fission, impairs the separation of P5CS-containing mitochondria from mitochondria that are enriched in cristae and ATP synthase. Failure to segregate these metabolic pathways through mitochondrial fusion and fission results in cells either sacrificing the capacity for OXPHOS while sustaining the reductive synthesis of proline, or foregoing proline synthesis while preserving adaptive OXPHOS. These findings provide evidence of the key role of mitochondrial fission and fusion in maintaining both oxidative and reductive biosyntheses in response to changing nutrient availability and bioenergetic demand.

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“Arecent study by Ryu et al. has reported that subpopulations of mitochondria are induced by energy demand (Ryu et al., 2024).”
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“The number, size, and genetic material (mtDNA) of individual mitochondrial structures have a well-established connection to the metabolic function of mitochondria and their ability to produce ATP (6–10).”
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Total flavonoids isolated from Fructus Mume (Prunus mume Sieb. et Zucc.) mitigate Parkinson's disease progression by promoting neuronal mitophagy via activation of the CaMKKβ/AMPK signaling pathway
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“When mitochondrial function is compromised, ATP generation declines, leading to energy insufficiency that can impair essential cellular processes [57].”
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Influential
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Authors: Ryu, K. W., Fung, T. S., Baker, D. C., Saoi, M., Park, J., Febres-Aldana, C. A., Aly, R. G., Cui, R., Sharma, A., Fu, Y., Jones, O. L., Cai, X., Pasolli, H. A., Cross, J. R., Rudin, C. M., & Thompson, C. B.
Affiliations: Memorial Sloan Kettering Cancer Center (US)
Rockefeller University (US)
Corresponding author: Thompson, Craig B.
ORCID: Ryu, Keun Woo
Fung, Tak Shun
Baker, Daphne C.
Saoi, Michelle
Febres-Aldana, Christopher A.
Aly, Rania G.
Sharma, Anurag
Fu, Yi
Jones, Olivia L.
Cai, Xin
Pasolli, H. Amalia
Cross, Justin R.
Rudin, Charles M.
Thompson, Craig B.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2024-11-06
Volume: 635
Issue: 8039
Pages: 746-754
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-024-08146-w
PMC: PMC11869630
OpenAlex: W4404105362
Cited by: 284
References: 43
Citations by year: 2026: 125 · 2025: 154 · 2024: 5
FWCI: 38.66
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Memorial Sloan-Kettering Cancer Center (CA008748, P30 CA008748)
National Cancer Institute (K99CA256505, CA008748, CA263816, P30CA008748, R35CA283988, R35CA263816)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › ATP Synthase and ATPases Research
Keywords: mitochondrial heterogeneity, mitochondrial subpopulations, pyrroline-5-carboxylate synthase, proline biosynthesis, ornithine biosynthesis, oxidative phosphorylation, ATP synthase, mitochondrial fusion, mitochondrial fission, mitofusins, Drp1, mitochondrial cristae, ATP demand, metabolic compartmentation
MeSH terms: Adenosine Triphosphate, Animals, Cell Line, Humans, Mitochondria, Ornithine, Ornithine-Oxo-Acid Transaminase, Oxidative Phosphorylation, Proline, Carbon-Nitrogen Ligases, GTP Phosphohydrolases, Mitochondrial Proteins, Mitochondrial Proton-Translocating ATPases, Dynamins, Mice, Mitochondrial Dynamics

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Cellular ATP demand creates metabolically distinct subpopulations of mitochondria

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