CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs

Désirée Schatton, David Pla-Martin, Marie-Charlotte Marx, Henriette Hansen, Arnaud Mourier, Ivan Nemazanyy, Alberto Pessia, Peter Zentis, Teresa Corona, Vangelis Kondylis, Esther Barth, Astrid C. Schauss, Vidya Velagapudi, Elena I. Rugarli

Forskningsoutput: TidskriftsbidragArtikelVetenskapligPeer review

Sammanfattning

Mitochondria are essential organelles that host crucial metabolic pathways and produce adenosine triphosphate. The mitochondrial proteome is heterogeneous among tissues and can dynamically change in response to different metabolic conditions. Although the transcriptional programs that govern mitochondrial biogenesis and respiratory function are well known, posttranscriptional regulatory mechanisms remain unclear. In this study, we show that the cytosolic RNA-binding protein clustered mitochondria homologue (CLUH) regulates the expression of a mitochondrial protein network supporting key metabolic programs required under nutrient deprivation. CLUH exerts its function by controlling the stability and translation of target messenger RNAs. In the absence of Cluh, mitochondria are severely depleted of crucial enzymes involved in catabolic energy-converting pathways. CLUH preserves oxidative mitochondrial function and glucose homeostasis, thus preventing death at the fetal–neonatal transition. In the adult liver, CLUH ensures maximal respiration capacity and the metabolic response to starvation. Our results shed new light on the posttranscriptional mechanisms controlling the expression of mitochondrial proteins and suggest novel strategies to tailor mitochondrial function to physiological and pathological conditions.
Originalspråkengelska
TidskriftJournal of Cell Biology
Volym216
Utgåva3
Sidor (från-till)675-693
Antal sidor19
ISSN0021-9525
DOI
StatusPublicerad - 6 mar 2017
MoE-publikationstypA1 Tidskriftsartikel-refererad

Vetenskapsgrenar

  • 1182 Biokemi, cell- och molekylärbiologi

Citera det här

Schatton, D., Pla-Martin, D., Marx, M-C., Hansen, H., Mourier, A., Nemazanyy, I., ... Rugarli, E. I. (2017). CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs. Journal of Cell Biology, 216(3), 675-693. https://doi.org/10.1083/jcb.201607019
Schatton, Désirée ; Pla-Martin, David ; Marx, Marie-Charlotte ; Hansen, Henriette ; Mourier, Arnaud ; Nemazanyy, Ivan ; Pessia, Alberto ; Zentis, Peter ; Corona, Teresa ; Kondylis, Vangelis ; Barth, Esther ; Schauss, Astrid C. ; Velagapudi, Vidya ; Rugarli, Elena I. / CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs. I: Journal of Cell Biology. 2017 ; Vol. 216, Nr. 3. s. 675-693.
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title = "CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs",
abstract = "Mitochondria are essential organelles that host crucial metabolic pathways and produce adenosine triphosphate. The mitochondrial proteome is heterogeneous among tissues and can dynamically change in response to different metabolic conditions. Although the transcriptional programs that govern mitochondrial biogenesis and respiratory function are well known, posttranscriptional regulatory mechanisms remain unclear. In this study, we show that the cytosolic RNA-binding protein clustered mitochondria homologue (CLUH) regulates the expression of a mitochondrial protein network supporting key metabolic programs required under nutrient deprivation. CLUH exerts its function by controlling the stability and translation of target messenger RNAs. In the absence of Cluh, mitochondria are severely depleted of crucial enzymes involved in catabolic energy-converting pathways. CLUH preserves oxidative mitochondrial function and glucose homeostasis, thus preventing death at the fetal–neonatal transition. In the adult liver, CLUH ensures maximal respiration capacity and the metabolic response to starvation. Our results shed new light on the posttranscriptional mechanisms controlling the expression of mitochondrial proteins and suggest novel strategies to tailor mitochondrial function to physiological and pathological conditions.",
keywords = "1182 Biochemistry, cell and molecular biology, METABOLOMICS, CLUH",
author = "D{\'e}sir{\'e}e Schatton and David Pla-Martin and Marie-Charlotte Marx and Henriette Hansen and Arnaud Mourier and Ivan Nemazanyy and Alberto Pessia and Peter Zentis and Teresa Corona and Vangelis Kondylis and Esther Barth and Schauss, {Astrid C.} and Vidya Velagapudi and Rugarli, {Elena I.}",
year = "2017",
month = "3",
day = "6",
doi = "10.1083/jcb.201607019",
language = "English",
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journal = "Journal of Cell Biology",
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Schatton, D, Pla-Martin, D, Marx, M-C, Hansen, H, Mourier, A, Nemazanyy, I, Pessia, A, Zentis, P, Corona, T, Kondylis, V, Barth, E, Schauss, AC, Velagapudi, V & Rugarli, EI 2017, 'CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs', Journal of Cell Biology, vol. 216, nr. 3, s. 675-693. https://doi.org/10.1083/jcb.201607019

CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs. / Schatton, Désirée; Pla-Martin, David; Marx, Marie-Charlotte; Hansen, Henriette; Mourier, Arnaud; Nemazanyy, Ivan; Pessia, Alberto; Zentis, Peter; Corona, Teresa; Kondylis, Vangelis; Barth, Esther; Schauss, Astrid C.; Velagapudi, Vidya; Rugarli, Elena I.

I: Journal of Cell Biology, Vol. 216, Nr. 3, 06.03.2017, s. 675-693.

Forskningsoutput: TidskriftsbidragArtikelVetenskapligPeer review

TY - JOUR

T1 - CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs

AU - Schatton, Désirée

AU - Pla-Martin, David

AU - Marx, Marie-Charlotte

AU - Hansen, Henriette

AU - Mourier, Arnaud

AU - Nemazanyy, Ivan

AU - Pessia, Alberto

AU - Zentis, Peter

AU - Corona, Teresa

AU - Kondylis, Vangelis

AU - Barth, Esther

AU - Schauss, Astrid C.

AU - Velagapudi, Vidya

AU - Rugarli, Elena I.

PY - 2017/3/6

Y1 - 2017/3/6

N2 - Mitochondria are essential organelles that host crucial metabolic pathways and produce adenosine triphosphate. The mitochondrial proteome is heterogeneous among tissues and can dynamically change in response to different metabolic conditions. Although the transcriptional programs that govern mitochondrial biogenesis and respiratory function are well known, posttranscriptional regulatory mechanisms remain unclear. In this study, we show that the cytosolic RNA-binding protein clustered mitochondria homologue (CLUH) regulates the expression of a mitochondrial protein network supporting key metabolic programs required under nutrient deprivation. CLUH exerts its function by controlling the stability and translation of target messenger RNAs. In the absence of Cluh, mitochondria are severely depleted of crucial enzymes involved in catabolic energy-converting pathways. CLUH preserves oxidative mitochondrial function and glucose homeostasis, thus preventing death at the fetal–neonatal transition. In the adult liver, CLUH ensures maximal respiration capacity and the metabolic response to starvation. Our results shed new light on the posttranscriptional mechanisms controlling the expression of mitochondrial proteins and suggest novel strategies to tailor mitochondrial function to physiological and pathological conditions.

AB - Mitochondria are essential organelles that host crucial metabolic pathways and produce adenosine triphosphate. The mitochondrial proteome is heterogeneous among tissues and can dynamically change in response to different metabolic conditions. Although the transcriptional programs that govern mitochondrial biogenesis and respiratory function are well known, posttranscriptional regulatory mechanisms remain unclear. In this study, we show that the cytosolic RNA-binding protein clustered mitochondria homologue (CLUH) regulates the expression of a mitochondrial protein network supporting key metabolic programs required under nutrient deprivation. CLUH exerts its function by controlling the stability and translation of target messenger RNAs. In the absence of Cluh, mitochondria are severely depleted of crucial enzymes involved in catabolic energy-converting pathways. CLUH preserves oxidative mitochondrial function and glucose homeostasis, thus preventing death at the fetal–neonatal transition. In the adult liver, CLUH ensures maximal respiration capacity and the metabolic response to starvation. Our results shed new light on the posttranscriptional mechanisms controlling the expression of mitochondrial proteins and suggest novel strategies to tailor mitochondrial function to physiological and pathological conditions.

KW - 1182 Biochemistry, cell and molecular biology

KW - METABOLOMICS

KW - CLUH

U2 - 10.1083/jcb.201607019

DO - 10.1083/jcb.201607019

M3 - Article

VL - 216

SP - 675

EP - 693

JO - Journal of Cell Biology

JF - Journal of Cell Biology

SN - 0021-9525

IS - 3

ER -

Schatton D, Pla-Martin D, Marx M-C, Hansen H, Mourier A, Nemazanyy I et al. CLUH regulates mitochondrial metabolism by controlling translation and decay of target mRNAs. Journal of Cell Biology. 2017 mar 6;216(3):675-693. https://doi.org/10.1083/jcb.201607019