Intracellular energy controls dynamics of stress-induced ribonucleoprotein granules.

Amyotrophic Lateral Sclerosis / metabolism C9orf72 Protein / genetics Cytoplasmic Granules / metabolism Cytoplasmic Ribonucleoprotein Granules Eukaryotic Initiation Factor-4E / metabolism Eukaryotic Initiation Factor-4F / metabolism Frontotemporal Dementia / genetics Humans RNA / metabolism Ribonucleoproteins / genetics Stress, Physiological / physiology TOR Serine-Threonine Kinases / genetics

Journal

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

Informations de publication

Date de publication:
23 09 2022
Historique:
received: 08 12 2021
accepted: 26 08 2022
entrez: 23 9 2022
pubmed: 24 9 2022
medline: 28 9 2022
Statut: epublish

Résumé

Energy metabolism and membraneless organelles have been implicated in human diseases including neurodegeneration. How energy deficiency regulates ribonucleoprotein particles such as stress granules (SGs) is still unclear. Here we identified a unique type of granules induced by energy deficiency under physiological conditions and uncovered the mechanisms by which the dynamics of diverse stress-induced granules are regulated. Severe energy deficiency induced the rapid formation of energy deficiency-induced stress granules (eSGs) independently of eIF2α phosphorylation, whereas moderate energy deficiency delayed the clearance of conventional SGs. The formation of eSGs or the clearance of SGs was regulated by the mTOR-4EBP1-eIF4E pathway or eIF4A1, involving assembly of the eIF4F complex or RNA condensation, respectively. In neurons or brain organoids derived from patients carrying the C9orf72 repeat expansion associated with amyotrophic lateral sclerosis (ALS) and frontotemporal dementia (FTD), the eSG formation was enhanced, and the clearance of conventional SGs was impaired. These results reveal a critical role for intracellular energy in the regulation of diverse granules and suggest that disruptions in energy-controlled granule dynamics may contribute to the pathogenesis of relevant diseases.

Identifiants

DOI: 10.1038/s41467-022-33079-1 PMID: 36151083 PMC: PMC9508253
pubmed: 36151083
doi: 10.1038/s41467-022-33079-1
pii: 10.1038/s41467-022-33079-1
pmc: PMC9508253
doi:

Substances chimiques

C9orf72 Protein 0
Eukaryotic Initiation Factor-4E 0
Eukaryotic Initiation Factor-4F 0
Ribonucleoproteins 0
RNA 63231-63-0
TOR Serine-Threonine Kinases EC 2.7.11.1

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S. Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

5584

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS128494
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS074324
Pays : United States
Organisme : NIH HHS
ID : S10 OD021844
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS110098
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS089616
Pays : United States

Informations de copyright

© 2022. The Author(s).

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Auteurs

Tao Wang (T)

Department of Biochemistry and Molecular Biology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, 21205, USA. twangsh@hotmail.com.
Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA. twangsh@hotmail.com.
ORCID: 0000-0002-8177-0298

Xibin Tian (X)

Department of Biochemistry and Molecular Biology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, 21205, USA.
Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA.

Han Byeol Kim (HB)

Department of Neurology, Institute for Cell Engineering, School of Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA.

Yura Jang (Y)

Department of Neurology, Institute for Cell Engineering, School of Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA.
ORCID: 0000-0002-1338-4686

Zhiyuan Huang (Z)

Department of Biochemistry and Molecular Biology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, 21205, USA.
Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA.

Chan Hyun Na (CH)

Department of Neurology, Institute for Cell Engineering, School of Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA.
ORCID: 0000-0002-3622-2938

Jiou Wang (J)

Department of Biochemistry and Molecular Biology, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, 21205, USA. jiouw@jhmi.edu.
Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, 21205, USA. jiouw@jhmi.edu.
ORCID: 0000-0003-0204-8932

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Classifications MeSH

questionsmedicales.fr › Maladies métaboliques et nutritionnelles › Maladies métaboliques › Troubles de l'homéostasie des protéines › Protéinopathies TDP-43 › Sclérose latérale amyotrophique › Intracellular energy controls dynamics of...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Régulateurs des protéines G › Facteurs d'échange de nucléotides guanyliques › Protéine C9orf72 › Intracellular energy controls dynamics of...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Vésicules cytoplasmiques › Granulations cytoplasmiques › Intracellular energy controls dynamics of...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Vésicules cytoplasmiques › Granulations cytoplasmiques › Granules ribonucléoprotéiques cytoplasmiques › Intracellular energy controls dynamics of...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines ribosomiques › Facteurs initiation chaîne peptidique › Facteurs d'initiation eucaryotes › Facteur-4F d'initiation eucaryote › Facteur-4E d'initiation eucaryote › Intracellular energy controls dynamics of...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines ribosomiques › Facteurs initiation chaîne peptidique › Facteurs d'initiation eucaryotes › Facteur-4F d'initiation eucaryote › Intracellular energy controls dynamics of...
questionsmedicales.fr › Troubles mentaux › Troubles neurocognitifs › Démence › Dégénérescence lobaire frontotemporale › Démence frontotemporale › Intracellular energy controls dynamics of...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Intracellular energy controls dynamics of...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ARN › Intracellular energy controls dynamics of...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Protéines de liaison à l'ARN › Ribonucléoprotéines › Intracellular energy controls dynamics of...
questionsmedicales.fr › Phénomènes physiologiques › Stress physiologique › Intracellular energy controls dynamics of...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protein-Serine-Threonine Kinases › Sérine-thréonine kinases TOR › Intracellular energy controls dynamics of...