Genomic signatures of the unjamming transition in compressed human bronchial epithelial cells.


Journal

Science advances
ISSN: 2375-2548
Titre abrégé: Sci Adv
Pays: United States
ID NLM: 101653440

Informations de publication

Date de publication:
07 2021
Historique:
received: 05 10 2020
accepted: 07 06 2021
entrez: 24 7 2021
pubmed: 25 7 2021
medline: 9 4 2022
Statut: epublish

Résumé

Epithelial tissue can transition from a jammed, solid-like, quiescent phase to an unjammed, fluid-like, migratory phase, but the underlying molecular events of the unjamming transition (UJT) remain largely unexplored. Using primary human bronchial epithelial cells (HBECs) and one well-defined trigger of the UJT, compression mimicking the mechanical effects of bronchoconstriction, here, we combine RNA sequencing data with protein-protein interaction networks to provide the first genome-wide analysis of the UJT. Our results show that compression induces an early transcriptional activation of the membrane and actomyosin network and a delayed activation of the extracellular matrix (ECM) and cell-matrix networks. This response is associated with a signaling cascade that promotes actin polymerization and cellular motility through the coordinated interplay of downstream pathways including ERK, JNK, integrin signaling, and energy metabolism. Moreover, in nonasthmatic versus asthmatic HBECs, common genomic patterns associated with ECM remodeling suggest a molecular connection between airway remodeling, bronchoconstriction, and the UJT.

Identifiants

pubmed: 34301595
pii: 7/30/eabf1088
doi: 10.1126/sciadv.abf1088
pmc: PMC8302128
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NHLBI NIH HHS
ID : R01 HL148152
Pays : United States
Organisme : NHLBI NIH HHS
ID : K25 HL133599
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL120839
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL007118
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA202123
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK065988
Pays : United States
Organisme : NIEHS NIH HHS
ID : P30 ES000002
Pays : United States
Organisme : NCATS NIH HHS
ID : UL1 TR002541
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL132825
Pays : United States
Organisme : NIH HHS
ID : UH3 OD023268
Pays : United States

Informations de copyright

Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

Références

Bioinformatics. 2015 Jan 15;31(2):166-9
pubmed: 25260700
Am J Respir Cell Mol Biol. 2016 Apr;54(4):524-31
pubmed: 26407210
Am J Physiol Lung Cell Mol Physiol. 2002 May;282(5):L904-11
pubmed: 11943653
Bioinformatics. 2013 Jan 1;29(1):15-21
pubmed: 23104886
Nat Commun. 2020 Oct 7;11(1):5053
pubmed: 33028821
Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3614-9
pubmed: 24550493
Nature. 2018 Sep;561(7723):401-405
pubmed: 30185907
Nat Commun. 2015 Jul 22;6:7866
pubmed: 26198319
Cell Metab. 2013 Dec 3;18(6):792-801
pubmed: 24055102
Nature. 2004 May 6;429(6987):83-6
pubmed: 15103386
N Engl J Med. 2011 May 26;364(21):2006-15
pubmed: 21612469
Nat Mater. 2017 May;16(5):587-596
pubmed: 28135264
Nat Commun. 2018 Jul 12;9(1):2691
pubmed: 30002366
Biochim Biophys Acta. 2014 Aug;1840(8):2386-95
pubmed: 24721714
EMBO J. 2000 Nov 15;19(22):6020-9
pubmed: 11080149
Cell Mol Life Sci. 2013 Mar;70(6):1123-33
pubmed: 23124190
Bioinformatics. 2011 Apr 1;27(7):1017-8
pubmed: 21330290
Nat Mater. 2019 Nov;18(11):1252-1263
pubmed: 31332337
Cell Rep. 2020 Mar 17;30(11):3875-3888.e3
pubmed: 32187556
Clin Biochem. 2013 Oct;46(15):1339-52
pubmed: 23680095
J Cell Physiol. 2007 Jun;211(3):736-47
pubmed: 17299801
FEBS J. 2013 Jan;280(2):489-504
pubmed: 22812510
OMICS. 2012 May;16(5):284-7
pubmed: 22455463
Nature. 2008 May 15;453(7193):314-21
pubmed: 18480812
Genome Biol. 2014;15(12):550
pubmed: 25516281
J Phys D Appl Phys. 2017 Oct 27;50(48):483001
pubmed: 29628530
EMBO Rep. 2013 Jun;14(6):509-19
pubmed: 23681438
BMC Bioinformatics. 2014 Jun 12;15:182
pubmed: 24925680
Curr Opin Cell Biol. 2009 Dec;21(6):864-70
pubmed: 19740640
Mol Cell Biol. 1999 Nov;19(11):7420-7
pubmed: 10523630
Ann Am Thorac Soc. 2016 Mar;13 Suppl 1:S64-7
pubmed: 27027955
Nat Mater. 2015 Oct;14(10):1040-8
pubmed: 26237129
Exp Cell Res. 2016 Apr 10;343(1):54-59
pubmed: 26546401
Phys Rev X. 2016 Apr-Jun;6(2):
pubmed: 28966874
Cold Spring Harb Perspect Biol. 2011 Dec 01;3(12):
pubmed: 21917992
Nat Mater. 2013 Sep;12(9):856-63
pubmed: 23793160
Open Biol. 2020 Dec;10(12):200254
pubmed: 33259745
Front Cell Dev Biol. 2020 Feb 11;8:21
pubmed: 32117962
Eur Respir Rev. 2020 Aug 4;29(157):
pubmed: 32759373
Dev Cell. 2020 Jun 22;53(6):646-660.e8
pubmed: 32497487
Sci Rep. 2020 Oct 27;10(1):18302
pubmed: 33110128
Differentiation. 2013 Oct;86(3):121-5
pubmed: 23791490
Am J Respir Cell Mol Biol. 2003 Feb;28(2):142-9
pubmed: 12540481
Cell. 2011 Mar 18;144(6):986-98
pubmed: 21414488
Nucleic Acids Res. 2020 Jan 8;48(D1):D498-D503
pubmed: 31691815
Nat Cell Biol. 2004 Feb;6(2):154-61
pubmed: 14743221
Nat Cell Biol. 2020 Sep;22(9):1103-1115
pubmed: 32839548
Sci Rep. 2020 Jan 22;10(1):966
pubmed: 31969610
Nat Rev Genet. 2009 Jan;10(1):57-63
pubmed: 19015660
J Biol Chem. 2010 Sep 24;285(39):29817-25
pubmed: 20650887
Trends Cell Biol. 2004 Feb;14(2):94-101
pubmed: 15102441
Proc Natl Acad Sci U S A. 2015 Dec 15;112(50):15314-9
pubmed: 26627719
Proc Natl Acad Sci U S A. 2011 Mar 22;108(12):4714-9
pubmed: 21321233
J Cell Sci. 2011 Dec 1;124(Pt 23):3923-7
pubmed: 22194302
Genome Res. 2002 Jun;12(6):996-1006
pubmed: 12045153
Nat Rev Mol Cell Biol. 2010 May;11(5):353-65
pubmed: 20414257
FASEB J. 2010 May;24(5):1604-15
pubmed: 20056713
J Allergy Clin Immunol. 2012 Dec;130(6):1375-83
pubmed: 22828416
Science. 2004 Nov 26;306(5701):1506-7
pubmed: 15567848
Mol Med Rep. 2015 Nov;12(5):6415-21
pubmed: 26324022
J Cell Sci. 2016 Sep 15;129(18):3375-83
pubmed: 27550520
Annu Rev Cell Biol. 1994;10:251-337
pubmed: 7888178
Nucleic Acids Res. 2019 Jan 8;47(D1):D330-D338
pubmed: 30395331
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Nat Commun. 2020 Feb 10;11(1):811
pubmed: 32041952
J Biol Chem. 2005 Apr 29;280(17):16546-9
pubmed: 15760908
Onco Targets Ther. 2017 Feb 20;10:711-724
pubmed: 28260916
Proc Natl Acad Sci U S A. 2001 May 22;98(11):6180-5
pubmed: 11353845
Nat Rev Mol Cell Biol. 2019 Aug;20(8):457-473
pubmed: 31182865
Nucleic Acids Res. 2009 Jul;37(Web Server issue):W202-8
pubmed: 19458158
BMC Syst Biol. 2018 Dec 31;12(Suppl 9):120
pubmed: 30598083
Nat Phys. 2018 Jun;14:613-620
pubmed: 30151030

Auteurs

Margherita De Marzio (M)

Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA. scott.weiss@channing.harvard.edu nhmdm@channing.harvard.edu.
Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Ayşe Kılıç (A)

Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.

Enrico Maiorino (E)

Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.

Jennifer A Mitchel (JA)

Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Chimwemwe Mwase (C)

Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Michael J O'Sullivan (MJ)

Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Maureen McGill (M)

Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Robert Chase (R)

Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.

Jeffrey J Fredberg (JJ)

Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Jin-Ah Park (JA)

Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Kimberly Glass (K)

Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
Department of Biostatistics, Harvard TH Chan School of Public Health, Boston, MA, USA.

Scott T Weiss (ST)

Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA. scott.weiss@channing.harvard.edu nhmdm@channing.harvard.edu.
Department of Environmental Health, Harvard TH Chan School of Public Health, Boston, MA, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH