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Microprotein SMIM26 drives oxidative metabolism via serine-responsive mitochondrial translation

Microprotein SMIM26 drives oxidative metabolism via serine-responsive mitochondrial translation
Microprotein SMIM26 drives oxidative metabolism via serine-responsive mitochondrial translation

Mitochondrial small open reading frame (ORF)-encoded microproteins (SEPs) are key regulators and components of the electron transport chain (ETC). Although ETC complex I assembly is tightly coupled to nutrient availability, including serine, the coordinating mechanism remains unknown. A genome-wide CRISPR screen targeting SEPs revealed that deletion of the LINC00493-encoded microprotein SMIM26 sensitizes cells to one-carbon restriction. SMIM26 interacts with mitochondrial serine transporters SFXN1/2 and the mitoribosome, forming a functional triad that facilitates translation of the complex I subunit mt-ND5. SMIM26 loss impairs serine import, reduces folate intermediates, and disrupts key mitochondrial tRNA modifications (τm 5U and τm 5s²U), resulting in ND5 translation failure and complex I deficiency. SMIM26 deletion is embryonic lethal in mice and impedes tumor growth in a xenograft model of folate-dependent acute myeloid leukemia. These findings define SMIM26 as a critical integrator of one-carbon flux and complex I biogenesis and establish a paradigm for localized mitochondrial translation through transporter-ribosome interactions.

complex I, electron transport chain, micropeptides, mitochondria, mitochondrial translation, one-carbon pathway, oxidative phosphorylation, small ORF-encoded peptides
1097-2765
2759-2775.e12
Nah, Jiemin
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Mahendran, Sreya
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Kerouanton, Baptiste
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Cui, Liang
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Hock, Daniella H.
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Cabrera-Orefice, Alfredo
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Dunlap, Kyle
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Robinson, David
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Tung, Desmond W.H.
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Leong, Sze huey
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Tan, Kiat-Yi
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Chothani, Sonia P.
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Sun, Jingjing
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Dziegowska, Agnieszka
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Leszczynska, Grazyna
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Rackham, Owen J.L.
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Wittig, Ilka
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Dedon, Peter
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Ducker, Gregory S.
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Stroud, David A.
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Ho, Lena
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Nah, Jiemin
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Mahendran, Sreya
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Kerouanton, Baptiste
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Cui, Liang
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Hock, Daniella H.
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Cabrera-Orefice, Alfredo
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Dunlap, Kyle
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Robinson, David
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Tung, Desmond W.H.
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Leong, Sze huey
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Tan, Kiat-Yi
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Chothani, Sonia P.
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Sun, Jingjing
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Dziegowska, Agnieszka
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Leszczynska, Grazyna
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Rackham, Owen J.L.
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Wittig, Ilka
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Dedon, Peter
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Ducker, Gregory S.
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Stroud, David A.
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Ho, Lena
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Nah, Jiemin, Mahendran, Sreya, Kerouanton, Baptiste, Cui, Liang, Hock, Daniella H., Cabrera-Orefice, Alfredo, Dunlap, Kyle, Robinson, David, Tung, Desmond W.H., Leong, Sze huey, Tan, Kiat-Yi, Chothani, Sonia P., Sun, Jingjing, Dziegowska, Agnieszka, Leszczynska, Grazyna, Rackham, Owen J.L., Wittig, Ilka, Dedon, Peter, Ducker, Gregory S., Stroud, David A. and Ho, Lena (2025) Microprotein SMIM26 drives oxidative metabolism via serine-responsive mitochondrial translation. Molecular Cell, 85 (14), 2759-2775.e12. (doi:10.1016/j.molcel.2025.05.033).

Record type: Article

Abstract

Mitochondrial small open reading frame (ORF)-encoded microproteins (SEPs) are key regulators and components of the electron transport chain (ETC). Although ETC complex I assembly is tightly coupled to nutrient availability, including serine, the coordinating mechanism remains unknown. A genome-wide CRISPR screen targeting SEPs revealed that deletion of the LINC00493-encoded microprotein SMIM26 sensitizes cells to one-carbon restriction. SMIM26 interacts with mitochondrial serine transporters SFXN1/2 and the mitoribosome, forming a functional triad that facilitates translation of the complex I subunit mt-ND5. SMIM26 loss impairs serine import, reduces folate intermediates, and disrupts key mitochondrial tRNA modifications (τm 5U and τm 5s²U), resulting in ND5 translation failure and complex I deficiency. SMIM26 deletion is embryonic lethal in mice and impedes tumor growth in a xenograft model of folate-dependent acute myeloid leukemia. These findings define SMIM26 as a critical integrator of one-carbon flux and complex I biogenesis and establish a paradigm for localized mitochondrial translation through transporter-ribosome interactions.

Text
MOLECULAR-CELL - Accepted Manuscript
Restricted to Repository staff only until 26 September 2026.
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More information

Accepted/In Press date: 29 May 2025
Published date: 26 June 2025
Keywords: complex I, electron transport chain, micropeptides, mitochondria, mitochondrial translation, one-carbon pathway, oxidative phosphorylation, small ORF-encoded peptides

Identifiers

Local EPrints ID: 505134
URI: http://eprints.soton.ac.uk/id/eprint/505134
ISSN: 1097-2765
PURE UUID: 6c06b2ae-9542-4b43-ab3d-d3f9f34f6518
ORCID for Owen J.L. Rackham: ORCID iD orcid.org/0000-0002-4390-0872

Catalogue record

Date deposited: 30 Sep 2025 16:43
Last modified: 01 Oct 2025 02:05

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Contributors

Author: Jiemin Nah
Author: Sreya Mahendran
Author: Baptiste Kerouanton
Author: Liang Cui
Author: Daniella H. Hock
Author: Alfredo Cabrera-Orefice
Author: Kyle Dunlap
Author: David Robinson
Author: Desmond W.H. Tung
Author: Sze huey Leong
Author: Kiat-Yi Tan
Author: Sonia P. Chothani
Author: Jingjing Sun
Author: Agnieszka Dziegowska
Author: Grazyna Leszczynska
Author: Ilka Wittig
Author: Peter Dedon
Author: Gregory S. Ducker
Author: David A. Stroud
Author: Lena Ho

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