Targeting of eIF6-driven translation induces a metabolic rewiring that reduces NAFLD and the consequent evolution to hepatocellular carcinoma.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
12 08 2021
Historique:
received: 08 07 2020
accepted: 24 07 2021
entrez: 13 8 2021
pubmed: 14 8 2021
medline: 31 8 2021
Statut: epublish

Résumé

A postprandial increase of translation mediated by eukaryotic Initiation Factor 6 (eIF6) occurs in the liver. Its contribution to steatosis and disease is unknown. In this study we address whether eIF6-driven translation contributes to disease progression. eIF6 levels increase throughout the progression from Non-Alcoholic Fatty Liver Disease (NAFLD) to hepatocellular carcinoma. Reduction of eIF6 levels protects the liver from disease progression. eIF6 depletion blunts lipid accumulation, increases fatty acid oxidation (FAO) and reduces oncogenic transformation in vitro. In addition, eIF6 depletion delays the progression from NAFLD to hepatocellular carcinoma, in vivo. Mechanistically, eIF6 depletion reduces the translation of transcription factor C/EBPβ, leading to a drop in biomarkers associated with NAFLD progression to hepatocellular carcinoma and preserves mitochondrial respiration due to the maintenance of an alternative mTORC1-eIF4F translational branch that increases the expression of transcription factor YY1. We provide proof-of-concept that in vitro pharmacological inhibition of eIF6 activity recapitulates the protective effects of eIF6 depletion. We hypothesize the existence of a targetable, evolutionarily conserved translation circuit optimized for lipid accumulation and tumor progression.

Identifiants

pubmed: 34385447
doi: 10.1038/s41467-021-25195-1
pii: 10.1038/s41467-021-25195-1
pmc: PMC8361022
doi:

Substances chimiques

CCAAT-Enhancer-Binding Protein-beta 0
Peptide Initiation Factors 0
eIF-6 0
Clofazimine D959AE5USF

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

4878

Informations de copyright

© 2021. The Author(s).

Références

Cancer Res. 2018 Oct 15;78(20):5741-5753
pubmed: 30072395
Nature. 2008 Oct 2;455(7213):684-8
pubmed: 18784653
Eur J Cancer. 2017 Sep;83:56-70
pubmed: 28715695
Cell Metab. 2013 Aug 6;18(2):296-302
pubmed: 23931760
Nature. 2019 Nov;575(7783):512-518
pubmed: 31597160
Nucleic Acids Res. 2014 Jan;42(Database issue):D148-55
pubmed: 24214955
Cell Metab. 2018 Dec 4;28(6):895-906.e5
pubmed: 30197303
Dev Comp Immunol. 2017 Dec;77:69-76
pubmed: 28743432
Mol Cell Biol. 2018 May 29;38(12):
pubmed: 29610153
Biochem Soc Trans. 2006 Apr;34(Pt 2):213-6
pubmed: 16545079
Nat Med. 2018 Jul;24(7):908-922
pubmed: 29967350
Mol Cell. 2017 Sep 21;67(6):922-935.e5
pubmed: 28918902
Commun Biol. 2019 Jun 14;2:208
pubmed: 31240246
Bioinformatics. 2015 May 15;31(10):1686-8
pubmed: 25600944
Head Neck. 2004 May;26(5):408-17
pubmed: 15122657
Nature. 2003 Dec 4;426(6966):579-84
pubmed: 14654845
Database (Oxford). 2020 Jan 1;2020:
pubmed: 32147717
Gut. 2020 Oct;69(10):1855-1866
pubmed: 32001554
J Cell Sci. 2019 Jun 19;132(12):
pubmed: 31118235
Cell Metab. 2019 Jan 8;29(1):174-182.e5
pubmed: 30244972
Nat Rev Gastroenterol Hepatol. 2019 Jul;16(7):411-428
pubmed: 31028350
Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15712-7
pubmed: 14660788
Nat Med. 2003 Apr;9(4):416-23
pubmed: 12640447
J Hepatol. 2018 Aug;69(2):385-395
pubmed: 29572095
Hepatology. 2005 Jun;41(6):1313-21
pubmed: 15915461
Nat Med. 2015 Aug;21(8):938-945
pubmed: 26193342
Trends Genet. 2020 Feb;36(2):71-80
pubmed: 31822355
Cold Spring Harb Perspect Biol. 2013 Feb 01;5(2):
pubmed: 22767671
Cell Metab. 2012 Apr 4;15(4):505-17
pubmed: 22482732
Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):850-5
pubmed: 12525691
Proc Natl Acad Sci U S A. 2014 May 27;111(21):7695-700
pubmed: 24821761
Nucleic Acids Res. 2016 Jan 4;44(D1):D110-5
pubmed: 26531826
Curr Opin Genet Dev. 2018 Feb;48:75-81
pubmed: 29153483
Nat Genet. 2014 Oct;46(10):1051-9
pubmed: 25151356
Nat Commun. 2015 Sep 18;6:8261
pubmed: 26383020
Oncogene. 2014 Apr 24;33(17):2145-56
pubmed: 23644661
Nature. 1999 Feb 4;397(6718):441-6
pubmed: 9989411
Biochem Soc Trans. 2016 Dec 15;44(6):1667-1673
pubmed: 27913676
Science. 2017 Aug 18;357(6352):
pubmed: 28818916
Int J Dev Neurosci. 1987;5(1):39-42
pubmed: 3503487
Cell. 2004 Feb 6;116(3):467-79
pubmed: 15016380
Science. 2016 Jun 17;352(6292):1413-6
pubmed: 27313038
Nat Metab. 2021 Feb;3(2):244-257
pubmed: 33619378
Int J Mol Sci. 2019 Nov 08;20(22):
pubmed: 31717414
Proc Natl Acad Sci U S A. 1985 Dec;82(24):8681-5
pubmed: 3909149
Cancer Cell. 2011 Jun 14;19(6):765-75
pubmed: 21665150
Hepatology. 2018 Jan;67(1):123-133
pubmed: 28802062
Nature. 2007 Nov 29;450(7170):736-40
pubmed: 18046414
PLoS Genet. 2017 Jan 5;13(1):e1006552
pubmed: 28056084
Am J Clin Nutr. 1971 Jul;24(7):770-6
pubmed: 5091520
Cells. 2020 Jan 10;9(1):
pubmed: 31936702
EMBO Rep. 2009 May;10(5):459-65
pubmed: 19373251
J Biol Chem. 1997 Nov 28;272(48):30314-21
pubmed: 9374518
Brain Res. 1990 Oct 1;528(2):353-7
pubmed: 1980226

Auteurs

Alessandra Scagliola (A)

Istituto Nazionale di Genetica Molecolare, INGM, "Romeo ed Enrica Invernizzi", Milan, Italy.

Annarita Miluzio (A)

Istituto Nazionale di Genetica Molecolare, INGM, "Romeo ed Enrica Invernizzi", Milan, Italy.

Gabriele Ventura (G)

Department of Biosciences, University of Milan, Milan, Italy.

Stefania Oliveto (S)

Istituto Nazionale di Genetica Molecolare, INGM, "Romeo ed Enrica Invernizzi", Milan, Italy.

Chiara Cordiglieri (C)

Istituto Nazionale di Genetica Molecolare, INGM, "Romeo ed Enrica Invernizzi", Milan, Italy.

Nicola Manfrini (N)

Istituto Nazionale di Genetica Molecolare, INGM, "Romeo ed Enrica Invernizzi", Milan, Italy.
Department of Biosciences, University of Milan, Milan, Italy.

Delia Cirino (D)

Department of Biosciences, University of Milan, Milan, Italy.

Sara Ricciardi (S)

Istituto Nazionale di Genetica Molecolare, INGM, "Romeo ed Enrica Invernizzi", Milan, Italy.
Department of Biosciences, University of Milan, Milan, Italy.

Luca Valenti (L)

Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy.
Translational Medicine, Department of Transfusion Medicine and Hematology, Fondazione IRCCS Ca' Granda Ospedale Policlinico, Milan, Italy.

Guido Baselli (G)

Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy.

Roberta D'Ambrosio (R)

Department of Hepatology, Fondazione IRCCS Ca' Granda Granda Ospedale Policlinico, Milan, Italy.

Marco Maggioni (M)

Department of Pathology, Fondazione IRCCS Ca' Granda Ospedale Policlinico, Milan, Italy.

Daniela Brina (D)

Institute of Oncology Research, Oncology Institute of Southern Switzerland, Università della Svizzera Italiana, Bellinzona, Switzerland.

Alberto Bresciani (A)

Department of Translational and Discovery Research, IRBM S.p.A., Pomezia (Roma), Italy.

Stefano Biffo (S)

Istituto Nazionale di Genetica Molecolare, INGM, "Romeo ed Enrica Invernizzi", Milan, Italy. biffo@ingm.org.
Department of Biosciences, University of Milan, Milan, Italy. biffo@ingm.org.

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Classifications MeSH