Mechanically induced alterations in chromatin architecture guide the balance between cell plasticity and mechanical memory.

cellular plasticity chromatin epigenetics mechanical memory mechanotransduction

Journal

Frontiers in cell and developmental biology
ISSN: 2296-634X
Titre abrégé: Front Cell Dev Biol
Pays: Switzerland
ID NLM: 101630250

Informations de publication

Date de publication:
2023
Historique:
received: 30 10 2022
accepted: 07 04 2023
medline: 5 5 2023
pubmed: 5 5 2023
entrez: 5 5 2023
Statut: epublish

Résumé

Phenotypic plasticity, or adaptability, of a cell determines its ability to survive and function within changing cellular environments. Changes in the mechanical environment, ranging from stiffness of the extracellular matrix (ECM) to physical stress such as tension, compression, and shear, are critical environmental cues that influence phenotypic plasticity and stability. Furthermore, an exposure to a prior mechanical signal has been demonstrated to play a fundamental role in modulating phenotypic changes that persist even after the mechanical stimulus is removed, creating stable mechanical memories. In this mini review, our objective is to highlight how the mechanical environment alters both phenotypic plasticity and stable memories through changes in chromatin architecture, mainly focusing on examples in cardiac tissue. We first explore how cell phenotypic plasticity is modulated in response to changes in the mechanical environment, and then connect the changes in phenotypic plasticity to changes in chromatin architecture that reflect short-term and long-term memories. Finally, we discuss how elucidating the mechanisms behind mechanically induced chromatin architecture that lead to cell adaptations and retention of stable mechanical memories could uncover treatment methods to prevent mal-adaptive permanent disease states.

Identifiants

pubmed: 37143893
doi: 10.3389/fcell.2023.1084759
pii: 1084759
pmc: PMC10151697
doi:

Types de publication

Journal Article Review

Langues

eng

Pagination

1084759

Subventions

Organisme : NIAMS NIH HHS
ID : R01 AR063712
Pays : United States

Informations de copyright

Copyright © 2023 Scott, Rafuse and Neu.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Cell Rep. 2019 Apr 30;27(5):1607-1620.e4
pubmed: 31042484
ACS Appl Mater Interfaces. 2020 Jan 8;12(1):260-274
pubmed: 31800206
Biochem Soc Trans. 2011 Dec;39(6):1729-34
pubmed: 22103516
Biol Chem. 2019 May 27;400(6):687-698
pubmed: 30465711
Int J Biochem Cell Biol. 2021 Aug;137:106035
pubmed: 34242685
Nature. 2021 Nov;599(7886):684-691
pubmed: 34789882
Nucleic Acids Res. 2016 Jun 20;44(11):5148-60
pubmed: 26939888
Nat Rev Cardiol. 2019 Jun;16(6):361-378
pubmed: 30683889
Circ Res. 2020 Jan 31;126(3):e10-e26
pubmed: 31822208
Proc Natl Acad Sci U S A. 2020 Sep 1;117(35):21258-21266
pubmed: 32817542
J Mol Cell Cardiol. 2019 Mar;128:198-211
pubmed: 30742811
J Clin Invest. 2005 Mar;115(3):527-37
pubmed: 15765134
Proc Natl Acad Sci U S A. 2015 May 5;112(18):5720-5
pubmed: 25901323
J Cell Sci. 2021 Jan 27;134(2):
pubmed: 33310912
Cardiovasc Eng. 2007 Dec;7(4):140-55
pubmed: 18026835
Nat Rev Mol Cell Biol. 2017 Dec;18(12):717-727
pubmed: 29044247
J Appl Physiol (1985). 2001 Aug;91(2):645-53
pubmed: 11457776
Circ Res. 2015 Apr 10;116(8):1462-1476
pubmed: 25858069
Biophys J. 2018 May 22;114(10):2262-2270
pubmed: 29628210
Integr Biol (Camb). 2012 Apr;4(4):410-21
pubmed: 22410748
Mol Biol Cell. 2018 Dec 1;29(25):3039-3051
pubmed: 30256731
Biomech Model Mechanobiol. 2022 Aug;21(4):1267-1283
pubmed: 35668305
Biochem Soc Trans. 2013 Jun;41(3):789-96
pubmed: 23697939
Nat Rev Mol Cell Biol. 2009 Jan;10(1):63-73
pubmed: 19197333
Cell Mol Bioeng. 2016 Jun;9(2):268-276
pubmed: 28163791
Exp Mol Med. 2017 Apr 28;49(4):e322
pubmed: 28450738
Cell. 2009 Apr 17;137(2):356-68
pubmed: 19379699
J Mol Cell Cardiol. 2014 May;70:9-18
pubmed: 24189039
Adv Healthc Mater. 2016 Oct;5(19):2536-2544
pubmed: 27276521
Diseases. 2019 Sep 01;7(3):
pubmed: 31480510
Obesity (Silver Spring). 2012 Mar;20(3):605-11
pubmed: 21566562
J Biol Eng. 2019 Aug 7;13:68
pubmed: 31406505
Cell. 2020 May 14;181(4):800-817.e22
pubmed: 32302590
ACS Biomater Sci Eng. 2017 Nov 13;3(11):2798-2805
pubmed: 29276759
Nat Biomed Eng. 2021 Dec;5(12):1485-1499
pubmed: 33875841
Adv Healthc Mater. 2017 Mar;6(5):
pubmed: 28105774
J Am Coll Cardiol. 2013 Jun 25;61(25):2514-21
pubmed: 23623915
Nat Biomed Eng. 2023 Feb;7(2):177-191
pubmed: 35996026
J Clin Invest. 2004 Feb;113(3):370-8
pubmed: 14755334
Adv Sci (Weinh). 2018 Dec 10;6(3):1801483
pubmed: 30775233
Nature. 2011 Jun 08;474(7350):179-83
pubmed: 21654799
Circulation. 1989 Apr;79(4):744-55
pubmed: 2522356
Nat Rev Mol Cell Biol. 2009 Mar;10(3):192-206
pubmed: 19234478
Nat Mater. 2022 Oct;21(10):1191-1199
pubmed: 35927431
Adv Healthc Mater. 2020 Apr;9(8):e2000030
pubmed: 32285630
Science. 2010 Aug 27;329(5995):1078-81
pubmed: 20647425
Heart Lung Circ. 2013 May;22(5):373-82
pubmed: 23333051
Biophys J. 2022 Jan 4;121(1):131-141
pubmed: 34800469
Nat Biomed Eng. 2021 Dec;5(12):1500-1516
pubmed: 34857921
Nat Mater. 2014 Jun;13(6):645-52
pubmed: 24633344
Genes Dev. 2006 Sep 1;20(17):2355-60
pubmed: 16951252
Nat Mater. 2013 Dec;12(12):1154-62
pubmed: 24141451
Cell. 2007 Feb 23;128(4):635-8
pubmed: 17320500
J Cell Sci. 2017 Jul 15;130(14):2243-2250
pubmed: 28646093
Circ Res. 1998 Mar 9;82(4):430-7
pubmed: 9506703
Mol Biol Cell. 2017 Jul 7;28(14):1997-2009
pubmed: 28615317
Cell. 2006 Aug 25;126(4):677-89
pubmed: 16923388
Nat Rev Genet. 2022 Oct;23(10):624-643
pubmed: 35606569
Am J Physiol Heart Circ Physiol. 2003 Nov;285(5):H1871-81
pubmed: 12842814
Nat Cell Biol. 2016 Aug;18(8):864-75
pubmed: 27398909
N Engl J Med. 2008 Mar 27;358(13):1370-80
pubmed: 18367740
Curr Opin Genet Dev. 2021 Apr;67:130-141
pubmed: 33524904
Am J Cardiol. 2008 Dec 1;102(11):1530-4
pubmed: 19026309
Biophys J. 2023 Apr 18;122(8):1428-1444
pubmed: 36871159
J Biol Chem. 2011 Jul 29;286(30):26743-53
pubmed: 21652697
Nat Rev Mol Cell Biol. 2022 Sep;23(9):583-602
pubmed: 35513718
Clin Sci (Lond). 2009 Mar;116(5):377-89
pubmed: 19175356
Biomaterials. 2017 Nov;146:146-155
pubmed: 28918264
Trends Mol Med. 2022 Sep;28(9):710-725
pubmed: 35717527
Bioeng Transl Med. 2022 Aug 22;7(3):e10394
pubmed: 36176599
Sci Rep. 2015 Nov 23;5:16895
pubmed: 26592929
Circulation. 2020 Mar 10;141(10):869-871
pubmed: 32150467
Mol Cell. 2010 May 28;38(4):603-13
pubmed: 20513434
Cardiovasc Res. 2000 Jul;47(1):23-37
pubmed: 10869527
Glob Cardiol Sci Pract. 2014 Jun 18;2014(2):9-25
pubmed: 25405172
Nat Mater. 2017 Mar;16(3):379-389
pubmed: 27798620
J Biomech Eng. 2022 Aug 1;144(8):
pubmed: 35147160
Cell. 2002 Nov 1;111(3):285-91
pubmed: 12419240
Proc Natl Acad Sci U S A. 2019 Jul 2;116(27):13200-13209
pubmed: 31209017
Nat Cell Biol. 2018 Apr;20(4):373-381
pubmed: 29467443
Biomech Model Mechanobiol. 2020 Jun;19(3):1079-1089
pubmed: 31813071
Trends Cell Biol. 2021 Jun;31(6):457-472
pubmed: 33712293
Circulation. 1972 Feb;45(2):310-8
pubmed: 4257897
Annu Rev Neurosci. 2020 Jul 8;43:207-229
pubmed: 32084327
Nat Rev Mol Cell Biol. 2019 Sep;20(9):535-550
pubmed: 31197269
Cell Mol Bioeng. 2021 Oct 13;14(5):397-408
pubmed: 34777600
J Mol Cell Cardiol. 2016 Mar;92:206-13
pubmed: 26876451
Ann N Y Acad Sci. 2004 May;1015:53-70
pubmed: 15201149
Prog Biophys Mol Biol. 2011 Sep;106(3):517-24
pubmed: 21846479
Nat Mater. 2016 Dec;15(12):1287-1296
pubmed: 27548707
FASEB J. 2020 Sep;34(9):12976-12990
pubmed: 33411380
Front Physiol. 2021 Aug 02;12:710809
pubmed: 34408666
Am J Physiol Heart Circ Physiol. 2005 Jun;288(6):H2702-7
pubmed: 15665058
Front Physiol. 2018 Jul 05;9:824
pubmed: 30026699
J Surg Res. 2007 Oct;142(2):387-93
pubmed: 17574596
Cell. 2012 Jun 22;149(7):1447-60
pubmed: 22704655
Curr Biol. 2016 Jul 25;26(14):R644-8
pubmed: 27458904
Biophys J. 2016 Aug 23;111(4):864-874
pubmed: 27558729
BMC Syst Biol. 2017 May 16;11(1):55
pubmed: 28511648

Auteurs

Adrienne K Scott (AK)

Paul M. Rady Department of Mechanical Engineering, University of Colorado Boulder, Boulder, CO, United States.

Michael Rafuse (M)

Paul M. Rady Department of Mechanical Engineering, University of Colorado Boulder, Boulder, CO, United States.

Corey P Neu (CP)

Paul M. Rady Department of Mechanical Engineering, University of Colorado Boulder, Boulder, CO, United States.
Biomedical Engineering Program, University of Colorado Boulder, Boulder, CO, United States.
BioFrontiers Institute, University of Colorado Boulder, Boulder, CO, United States.

Classifications MeSH