Changes in nuclear pore numbers control nuclear import and stress response of mouse hearts.


Journal

Developmental cell
ISSN: 1878-1551
Titre abrégé: Dev Cell
Pays: United States
ID NLM: 101120028

Informations de publication

Date de publication:
24 10 2022
Historique:
received: 19 10 2021
revised: 24 06 2022
accepted: 28 09 2022
entrez: 25 10 2022
pubmed: 26 10 2022
medline: 28 10 2022
Statut: ppublish

Résumé

Nuclear pores are essential for nuclear-cytoplasmic transport. Whether and how cells change nuclear pores to alter nuclear transport and cellular function is unknown. Here, we show that rat heart muscle cells (cardiomyocytes) undergo a 63% decrease in nuclear pore numbers during maturation, and this changes their responses to extracellular signals. The maturation-associated decline in nuclear pore numbers is associated with lower nuclear import of signaling proteins such as mitogen-activated protein kinase (MAPK). Experimental reduction of nuclear pore numbers decreased nuclear import of signaling proteins, resulting in decreased expression of immediate-early genes. In a mouse model of high blood pressure, reduction of nuclear pore numbers improved adverse heart remodeling and reduced progression to lethal heart failure. The decrease in nuclear pore numbers in cardiomyocyte maturation and resulting functional changes demonstrate how terminally differentiated cells permanently alter their handling of information flux across the nuclear envelope and, with that, their behavior.

Identifiants

pubmed: 36283391
pii: S1534-5807(22)00719-5
doi: 10.1016/j.devcel.2022.09.017
pmc: PMC9614572
mid: NIHMS1841489
pii:
doi:

Substances chimiques

Nuclear Pore Complex Proteins 0
Mitogen-Activated Protein Kinases EC 2.7.11.24

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

2397-2411.e9

Subventions

Organisme : NINDS NIH HHS
ID : R21 NS121706
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL151386
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL155597
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL129949
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR001857
Pays : United States
Organisme : NIBIB NIH HHS
ID : R21 EB023507
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL151415
Pays : United States
Organisme : NIH HHS
ID : S10 OD011967
Pays : United States

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Références

J Clin Invest. 1997 Jul 1;100(1):169-79
pubmed: 9202069
Dev Cell. 2021 Jun 21;56(12):1786-1803.e9
pubmed: 34129835
J Cell Biol. 1977 Jun;73(3):748-60
pubmed: 406262
Cell. 2016 Mar 10;164(6):1162-1171
pubmed: 26967283
Proc Natl Acad Sci U S A. 2003 Feb 4;100(3):981-5
pubmed: 12552102
Science. 1996 Sep 27;273(5283):1875-7
pubmed: 8791595
J Cell Sci. 2014 Feb 15;127(Pt 4):908-21
pubmed: 24363447
J Gen Physiol. 1999 Feb;113(2):239-48
pubmed: 9925822
Mol Biol Cell. 2011 Dec;22(23):4683-93
pubmed: 21976703
Bioinformatics. 2014 Apr 1;30(7):923-30
pubmed: 24227677
Am J Physiol Heart Circ Physiol. 2004 May;286(5):H1742-9
pubmed: 14693681
Cell. 2009 Jan 23;136(2):284-95
pubmed: 19167330
Nat Cell Biol. 2007 Oct;9(10):1160-6
pubmed: 17828249
Genes Dev. 2003 Oct 1;17(19):2362-7
pubmed: 12975322
Science. 2004 Nov 19;306(5700):1370-3
pubmed: 15550670
Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6668-73
pubmed: 11381115
Elife. 2020 Dec 21;9:
pubmed: 33346731
Sci Transl Med. 2019 Oct 9;11(513):
pubmed: 31597755
OMICS. 2012 May;16(5):284-7
pubmed: 22455463
Dev Cell. 2020 Apr 6;53(1):42-59.e11
pubmed: 32109383
Genome Biol. 2014;15(12):550
pubmed: 25516281
Nat Rev Mol Cell Biol. 2012 Nov;13(11):687-99
pubmed: 23090414
Cell Rep. 2018 Jul 24;24(4):873-882
pubmed: 30044984
Nat Rev Mol Cell Biol. 2006 Aug;7(8):589-600
pubmed: 16936699
Development. 2021 Jul 15;148(14):
pubmed: 34897388
EMBO J. 2012 Oct 17;31(20):4072-84
pubmed: 22960634
Am J Physiol Heart Circ Physiol. 2006 Jun;290(6):H2516-21
pubmed: 16415075
Circ Res. 1999 Jun 11;84(11):1292-301
pubmed: 10364567
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15545-50
pubmed: 16199517
J Cell Biol. 2010 Nov 1;191(3):505-21
pubmed: 20974814
Annu Rev Biochem. 2019 Jun 20;88:725-783
pubmed: 30883195
Proc Natl Acad Sci U S A. 1987 Nov;84(21):7552-6
pubmed: 3313397
Cardiovasc Res. 2015 Jan 1;105(1):31-43
pubmed: 25341891
Physiol Rev. 1991 Jul;71(3):909-49
pubmed: 1711701
Nat Commun. 2020 Apr 20;11(1):1899
pubmed: 32313005
Biophys J. 2017 May 23;112(10):2196-2208
pubmed: 28538156
J Biol Chem. 2001 Jun 8;276(23):20566-71
pubmed: 11283025
Nat Methods. 2006 Oct;3(10):793-5
pubmed: 16896339
Proc Natl Acad Sci U S A. 2012 Mar 27;109(13):4834-9
pubmed: 22411826

Auteurs

Lu Han (L)

Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children's Hospital of Pittsburgh, 4401 Penn Avenue, Pittsburgh, PA 15224, USA; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

Jocelyn D Mich-Basso (JD)

Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children's Hospital of Pittsburgh, 4401 Penn Avenue, Pittsburgh, PA 15224, USA; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

Yao Li (Y)

Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children's Hospital of Pittsburgh, 4401 Penn Avenue, Pittsburgh, PA 15224, USA; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

Niyatie Ammanamanchi (N)

Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children's Hospital of Pittsburgh, 4401 Penn Avenue, Pittsburgh, PA 15224, USA; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

Jianquan Xu (J)

Departments of Medicine and Bioengineering, University of Pittsburgh, Pittsburgh, PA 15213, USA.

Anita P Bargaje (AP)

Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children's Hospital of Pittsburgh, 4401 Penn Avenue, Pittsburgh, PA 15224, USA; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

Honghai Liu (H)

Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children's Hospital of Pittsburgh, 4401 Penn Avenue, Pittsburgh, PA 15224, USA; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

Liwen Wu (L)

Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA 15261, USA.

Jong-Hyeon Jeong (JH)

Department of Biostatistics, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA 15261, USA.

Jonathan Franks (J)

Center for Biologic Imaging, Department of Cell Biology, University of Pittsburgh, Pittsburgh, PA 15261, USA.

Donna B Stolz (DB)

Center for Biologic Imaging, Department of Cell Biology, University of Pittsburgh, Pittsburgh, PA 15261, USA.

Yijen L Wu (YL)

Department of Developmental Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15224, USA.

Dhivyaa Rajasundaram (D)

Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA.

Yang Liu (Y)

Departments of Medicine and Bioengineering, University of Pittsburgh, Pittsburgh, PA 15213, USA.

Bernhard Kühn (B)

Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children's Hospital of Pittsburgh, 4401 Penn Avenue, Pittsburgh, PA 15224, USA; Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA 15219, USA; McGowan Institute of Regenerative Medicine, University of Pittsburgh School of Medicine, 450 Technology Drive, Pittsburgh, PA 15219-3110, USA. Electronic address: Bernhard.kuhn2@CHP.edu.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH