Loss of heat shock factor initiates intracellular lipid surveillance by actin destabilization.

Animals Caenorhabditis elegans Proteins / metabolism Actins / metabolism Caenorhabditis elegans / metabolism Heat-Shock Response Transcription Factors / metabolism Receptors, Cytoplasmic and Nuclear / metabolism Lipids rab GTP-Binding Proteins / metabolism
CP: Cell biology NHR-49 Rab GTPase absorption actin cytoskeleton geranylgeranylation heat shock factor lipid sensing lipid surveillance nuclear hormone receptor protein homeostasis

Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
18 10 2022
Historique:
received: 31 03 2022
revised: 19 08 2022
accepted: 21 09 2022
entrez: 19 10 2022
pubmed: 20 10 2022
medline: 22 10 2022
Statut: ppublish

Résumé

Cells sense stress and initiate response pathways to maintain lipid and protein homeostasis. However, the interplay between these adaptive mechanisms is unclear. Herein, we demonstrate how imbalances in cytosolic protein homeostasis affect intracellular lipid surveillance. Independent of its ancient thermo-protective properties, the heat shock factor, HSF-1, modulates lipid metabolism and age regulation through the metazoan-specific nuclear hormone receptor, NHR-49. Reduced hsf-1 expression destabilizes the Caenorhabditis elegans enteric actin network, subsequently disrupting Rab GTPase-mediated trafficking and cell-surface residency of nutrient transporters. The ensuing malabsorption limits lipid availability, thereby activating the intracellular lipid surveillance response through vesicular release and nuclear translocation of NHR-49 to both increase nutrient absorption and restore lipid homeostasis. Overall, cooperation between these regulators of cytosolic protein homeostasis and lipid surveillance ensures metabolic health and age progression through actin integrity, endocytic recycling, and lipid sensing.

Identifiants

DOI: 10.1016/j.celrep.2022.111493 PMID: 36261024 PMC: PMC9642076
pubmed: 36261024
pii: S2211-1247(22)01343-2
doi: 10.1016/j.celrep.2022.111493
pmc: PMC9642076
mid: NIHMS1843692
pii:
doi:

Substances chimiques

Caenorhabditis elegans Proteins 0
Actins 0
Transcription Factors 0
Receptors, Cytoplasmic and Nuclear 0
Lipids 0
rab GTP-Binding Proteins EC 3.6.5.2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

111493

Subventions

Organisme : NIA NIH HHS
ID : R01 AG061338
Pays : United States
Organisme : NIA NIH HHS
ID : R01 AG076529
Pays : United States
Organisme : NIA NIH HHS
ID : R56 AG070167
Pays : United States

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

Références

Nature. 2010 Mar 25;464(7288):504-12
pubmed: 20336132
J Biol Chem. 2001 Nov 9;276(45):41748-54
pubmed: 11535595
Nat Cell Biol. 2012 May 27;14(7):666-76
pubmed: 22634595
Nature. 2022 May;605(7911):736-740
pubmed: 35585236
Nature. 2020 Feb;578(7796):621-626
pubmed: 32051585
Sci Adv. 2020 Jul 15;6(29):eabb9614
pubmed: 32832649
Genetics. 1974 May;77(1):71-94
pubmed: 4366476
Genes Dev. 2016 Sep 15;30(18):2062-2075
pubmed: 27688402
Aging Cell. 2021 Jul;20(7):e13413
pubmed: 34156142
Ann N Y Acad Sci. 1998 May 15;839:143-6
pubmed: 9629140
EMBO Rep. 2017 Nov;18(11):1905-1921
pubmed: 29074503
Cell. 2011 Jan 7;144(1):67-78
pubmed: 21215370
Mol Biol Cell. 2013 Mar;24(5):643-58
pubmed: 23283983
Proc Natl Acad Sci U S A. 2013 Mar 19;110(12):4628-33
pubmed: 23487760
Elife. 2018 Feb 02;7:
pubmed: 29393852
J Chem Biol. 2008 Nov;1(1-4):63-77
pubmed: 19568799
Cell. 2015 Feb 26;160(5):842-855
pubmed: 25723162
Science. 2008 Jun 13;320(5882):1492-6
pubmed: 18556558
Oncotarget. 2017 Apr 7;8(33):54149-54159
pubmed: 28903330
PLoS Genet. 2014 Dec 04;10(12):e1004829
pubmed: 25474470
Cell Microbiol. 2016 Jan;18(1):30-45
pubmed: 26147591
Nature. 2006 Mar 23;440(7083):551-5
pubmed: 16554822
Nat Methods. 2008 Aug;5(8):711-8
pubmed: 18622397
Nat Protoc. 2009;4(1):44-57
pubmed: 19131956
PLoS Biol. 2005 Feb;3(2):e53
pubmed: 15719061
Cell. 1984 Sep;38(2):371-81
pubmed: 6380764
Nature. 2003 Jan 16;421(6920):268-72
pubmed: 12529643
Mol Genet Genomics. 2001 Apr;265(2):258-63
pubmed: 11361336
Nat Commun. 2021 Mar 5;12(1):1484
pubmed: 33674585
Nat Commun. 2020 Mar 12;11(1):1339
pubmed: 32165635
Proc Natl Acad Sci U S A. 1974 Feb;71(2):522-5
pubmed: 4360948
Cardiovasc Res. 2016 Jul 1;111(1):74-83
pubmed: 27131506
Science. 2014 Oct 17;346(6207):360-3
pubmed: 25324391
Nat Rev Mol Cell Biol. 2010 Aug;11(8):545-55
pubmed: 20628411
Cell. 1997 May 2;89(3):331-40
pubmed: 9150132
Mol Biol Cell. 2004 Feb;15(2):657-64
pubmed: 14668486
Cell. 2016 Jan 28;164(3):433-46
pubmed: 26824656
Nat Rev Mol Cell Biol. 2009 Apr;10(4):255-64
pubmed: 19305415
Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):14914-9
pubmed: 19706382
Cell Rep. 2015 Aug 18;12(7):1196-1204
pubmed: 26257177
Annu Rev Biochem. 2012;81:687-714
pubmed: 22524315
Z Naturforsch C J Biosci. 1989 Jul-Aug;44(7-8):698-704
pubmed: 2775410
Annu Rev Nutr. 2001;21:193-230
pubmed: 11375435
Mol Biol Cell. 2011 Sep;22(18):3520-32
pubmed: 21775630
Acta Neuropathol. 2015 Sep;130(3):315-31
pubmed: 26210990
Science. 2011 Nov 25;334(6059):1081-6
pubmed: 22116877
J Cell Biol. 2012 Jun 25;197(7):857-67
pubmed: 22733998
Nucleic Acids Res. 2009 Jan;37(1):1-13
pubmed: 19033363
Mol Cell Endocrinol. 2011 Mar 1;334(1-2):3-13
pubmed: 20615454
J Clin Invest. 2011 Jun;121(6):2102-10
pubmed: 21633178
Dev Cell. 2019 Dec 2;51(5):587-601.e7
pubmed: 31794717
Mol Cell. 2019 Nov 21;76(4):546-561.e8
pubmed: 31561952
Annu Rev Biochem. 2012;81:661-86
pubmed: 22663081
Cell. 2016 Sep 8;166(6):1539-1552.e16
pubmed: 27610574
Mol Cell. 2018 Aug 2;71(3):458-467
pubmed: 30075144
BMC Genomics. 2016 Aug 05;17:559
pubmed: 27496166
PLoS Genet. 2012;8(4):e1002645
pubmed: 22511885
Cell. 2003 Nov 14;115(4):475-87
pubmed: 14622601
Trends Cell Biol. 2014 Jul;24(7):407-15
pubmed: 24675420
Front Mol Neurosci. 2018 Jan 23;11:10
pubmed: 29410613
Cancers (Basel). 2019 Sep 13;11(9):
pubmed: 31540279
Nat Rev Mol Cell Biol. 2018 Feb;19(2):109-120
pubmed: 29165426
Nat Rev Mol Cell Biol. 2009 Aug;10(8):513-25
pubmed: 19603039
J Lipid Res. 2011 Dec;52(12):2111-2135
pubmed: 21976778
Genes Dev. 1992 Jul;6(7):1153-64
pubmed: 1628823
J Biol Chem. 1992 Nov 5;267(31):21987-90
pubmed: 1429548
Genome Res. 2004 Oct;14(10B):2162-8
pubmed: 15489339
Mol Cell Biol. 2001 Feb;21(4):1393-403
pubmed: 11158324
Science. 2003 May 16;300(5622):1142-5
pubmed: 12750521
Cell. 2013 Jun 20;153(7):1435-47
pubmed: 23791175
Cell. 1984 Sep;38(2):383-90
pubmed: 6380765
Proc Natl Acad Sci U S A. 2005 Sep 20;102(38):13496-501
pubmed: 16157872

Auteurs

Abigail Watterson (A)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Sonja L B Arneaud (SLB)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Naureen Wajahat (N)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Jordan M Wall (JM)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Lexus Tatge (L)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Shaghayegh T Beheshti (ST)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Melina Mihelakis (M)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Nicholas Y Cheatwood (NY)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Jacob McClendon (J)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Atossa Ghorashi (A)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Ishmael Dehghan (I)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Chase D Corley (CD)

Center for Human Nutrition, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Jeffrey G McDonald (JG)

Center for Human Nutrition, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Department of Molecular Genetics, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA.

Peter M Douglas (PM)

Department of Molecular Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390, USA; Hamon Center for Regenerative Science and Medicine, UT Southwestern Medical Center, Dallas, TX 75390, USA. Electronic address: peter.douglas@utsouthwestern.edu.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Loss of heat shock factor initiates...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines d'helminthes › Protéines de Caenorhabditis elegans › Loss of heat shock factor initiates...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines du cytosquelette › Protéines des microfilaments › Actines › Loss of heat shock factor initiates...
questionsmedicales.fr › Eucaryotes › Animaux › Invertébrés › Helminthes › Nematoda › Chromadorea › Rhabditida › Rhabditoidea › Caenorhabditis › Caenorhabditis elegans › Loss of heat shock factor initiates...
questionsmedicales.fr › Phénomènes physiologiques › Stress physiologique › Réaction de choc thermique › Loss of heat shock factor initiates...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Loss of heat shock factor initiates...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Récepteurs cytoplasmiques et nucléaires › Loss of heat shock factor initiates...
questionsmedicales.fr › Lipides › Loss of heat shock factor initiates...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines et peptides de signalisation intracellulaire › Protéines G › Protéines G monomériques › Protéines G rab › Loss of heat shock factor initiates...