Correlation of Plasma Membrane Microviscosity and Cell Stiffness Revealed via Fluorescence-Lifetime Imaging and Atomic Force Microscopy.
actin cytoskeleton
atomic force microscopy (AFM)
cancer cell
fluorescence-lifetime imaging microscopy (FLIM)
microviscosity
molecular rotors
plasma membrane
time-of-flight secondary ion mass spectrometry (ToF-SIMS)
viscoelasticity
Journal
Cells
ISSN: 2073-4409
Titre abrégé: Cells
Pays: Switzerland
ID NLM: 101600052
Informations de publication
Date de publication:
06 Nov 2023
06 Nov 2023
Historique:
received:
17
09
2023
revised:
23
10
2023
accepted:
31
10
2023
medline:
13
11
2023
pubmed:
10
11
2023
entrez:
10
11
2023
Statut:
epublish
Résumé
The biophysical properties of cells described at the level of whole cells or their membranes have many consequences for their biological behavior. However, our understanding of the relationships between mechanical parameters at the level of cell (stiffness, viscoelasticity) and at the level of the plasma membrane (fluidity) remains quite limited, especially in the context of pathologies, such as cancer. Here, we investigated the correlations between cells' stiffness and viscoelastic parameters, mainly determined via the actin cortex, and plasma membrane microviscosity, mainly determined via its lipid profile, in cancer cells, as these are the keys to their migratory capacity. The mechanical properties of cells were assessed using atomic force microscopy (AFM). The microviscosity of membranes was visualized using fluorescence-lifetime imaging microscopy (FLIM) with the viscosity-sensitive probe BODIPY 2. Measurements were performed for five human colorectal cancer cell lines that have different migratory activity (HT29, Caco-2, HCT116, SW 837, and SW 480) and their chemoresistant counterparts. The actin cytoskeleton and the membrane lipid composition were also analyzed to verify the results. The cell stiffness (Young's modulus), measured via AFM, correlated well (Pearson r = 0.93) with membrane microviscosity, measured via FLIM, and both metrics were elevated in more motile cells. The associations between stiffness and microviscosity were preserved upon acquisition of chemoresistance to one of two chemotherapeutic drugs. These data clearly indicate that mechanical parameters, determined by two different cellular structures, are interconnected in cells and play a role in their intrinsic migratory potential.
Identifiants
pubmed: 37947661
pii: cells12212583
doi: 10.3390/cells12212583
pmc: PMC10650173
pii:
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Russian Science Foundation
ID : 23-74-00045
Organisme : the Ministry of Science and Higher Education of the Russian Federation
ID : framework of state support for the creation and development of World-Class Research Centers "Digital biodesign and personalized healthcare" №075-15-2022-304
Références
Biochim Biophys Acta. 2015 Nov;1853(11 Pt B):3117-25
pubmed: 25970206
Biophys J. 2011 Jul 6;101(1):43-52
pubmed: 21723813
Sci Rep. 2014 Dec 04;4:7307
pubmed: 25471686
Biophys Chem. 2022 Feb;281:106732
pubmed: 34844029
J Cell Biochem. 2000 Apr;77(4):517-28
pubmed: 10771509
Arch Biochem Biophys. 2007 Mar 1;459(1):98-106
pubmed: 17222386
Soft Matter. 2019 Jul 10;15(27):5455-5463
pubmed: 31231747
Biochem J. 2022 Sep 16;479(17):1825-1842
pubmed: 36094371
Biophys J. 2013 Mar 19;104(6):1248-56
pubmed: 23528084
Curr Opin Cell Biol. 2020 Oct;66:69-78
pubmed: 32580115
J Appl Physiol (1985). 2001 Sep;91(3):1152-9
pubmed: 11509510
Angew Chem Int Ed Engl. 2023 Oct 19;:e202311233
pubmed: 37856157
Neurochem Int. 2011 Feb;58(3):321-9
pubmed: 21184792
ACS Appl Mater Interfaces. 2022 Apr 27;14(16):18219-18232
pubmed: 35417121
PLoS One. 2012;7(10):e46609
pubmed: 23056368
Eur J Cell Biol. 2022 Jun-Aug;101(3):151241
pubmed: 35653881
Methods Appl Fluoresc. 2022 Aug 25;10(4):
pubmed: 35970177
Curr Top Membr. 2020;86:143-184
pubmed: 33837692
Phys Rev Lett. 2020 Aug 7;125(6):068101
pubmed: 32845697
Cell. 2011 Mar 4;144(5):646-74
pubmed: 21376230
J Cell Biol. 1998 Sep 21;142(6):1605-13
pubmed: 9744888
J Vis Exp. 2021 Jul 31;(173):
pubmed: 34398152
Int J Mol Sci. 2019 May 01;20(9):
pubmed: 31052427
Cancer Res. 2011 Aug 1;71(15):5075-80
pubmed: 21642375
Sci Rep. 2019 Apr 8;9(1):5757
pubmed: 30962474
Phys Chem Chem Phys. 2015 Jul 28;17(28):18393-402
pubmed: 26104504
Tohoku J Exp Med. 1982 Jul;137(3):325-8
pubmed: 6287670
Proc Natl Acad Sci U S A. 2013 Jun 4;110(23):9225-30
pubmed: 23690599
Cell Biochem Biophys. 2017 Dec;75(3-4):369-385
pubmed: 28417231
Methods Mol Biol. 2020;2169:167-174
pubmed: 32548828
Micron. 2012 Dec;43(12):1259-66
pubmed: 22436422
Cell Mol Bioeng. 2010 Mar 1;3(1):84-90
pubmed: 20368760
Am J Physiol Cell Physiol. 2023 Aug 1;325(2):C471-C482
pubmed: 37399498
J Clin Med. 2020 Apr 12;9(4):
pubmed: 32290558
Sci Rep. 2017 Jul 11;7(1):5117
pubmed: 28698636
J Bioenerg Biomembr. 2020 Oct;52(5):321-342
pubmed: 32715369
Int J Mol Sci. 2020 Oct 30;21(21):
pubmed: 33143259
Biophys J. 2018 Jun 19;114(12):2923-2932
pubmed: 29925028
Cancers (Basel). 2021 Dec 07;13(24):
pubmed: 34944789
Cancer Res. 2009 Mar 1;69(5):1951-7
pubmed: 19244128
Mol Cell Biochem. 2010 Aug;341(1-2):99-108
pubmed: 20336351
Br J Cancer. 2015 May 12;112(10):1675-86
pubmed: 25880005
Science. 2020 Jun 12;368(6496):1205-1210
pubmed: 32527825
Cell. 2018 Dec 13;175(7):1769-1779.e13
pubmed: 30392960
Nat Phys. 2018 Jul;14(7):648-652
pubmed: 31007706
Sci Rep. 2016 Jan 27;6:19686
pubmed: 26813872
Biochem Biophys Res Commun. 2011 May 27;409(1):1-6
pubmed: 21510920
Exp Cell Res. 2014 Mar 10;322(1):21-9
pubmed: 24412424
Soft Matter. 2012;8(32):8350-8360
pubmed: 23227105
Nanoscale. 2021 Oct 8;13(38):16339-16348
pubmed: 34581722
Exp Cell Res. 2017 Feb 15;351(2):173-181
pubmed: 28034672
Front Cell Dev Biol. 2020 Aug 05;8:684
pubmed: 32850810
Pathobiology. 2017;84(3):144-151
pubmed: 27832659
Sci Rep. 2017 Jan 30;7:41097
pubmed: 28134273
IEEE Trans Nanobioscience. 2017 Sep;16(6):523-540
pubmed: 28613180
Nat Rev Mol Cell Biol. 2001 May;2(5):392-6
pubmed: 11331914
J Cancer Res Clin Oncol. 2012 May;138(5):859-66
pubmed: 22297840
J Biomed Opt. 2020 Dec;25(12):
pubmed: 33331150
Adv Exp Med Biol. 2010;688:72-85
pubmed: 20919647
Curr Top Membr. 2020;86:83-141
pubmed: 33837699
Biol Cell. 2017 May;109(5):167-189
pubmed: 28244605
Chem Phys Lipids. 2007 Nov;150(1):66-81
pubmed: 17651712
Commun Biol. 2020 Oct 20;3(1):590
pubmed: 33082491
Sci Rep. 2020 Aug 20;10(1):14063
pubmed: 32820221
Biophys J. 2021 Feb 16;120(4):598-606
pubmed: 33460596
PLoS One. 2012;7(12):e50804
pubmed: 23251387
Biophys J. 2009 Mar 18;96(6):2457-65
pubmed: 19289070
Semin Cell Dev Biol. 2018 Jan;73:115-124
pubmed: 28694112
Proc Natl Acad Sci U S A. 1982 Sep;79(17):5327-31
pubmed: 6957866
Lipids Health Dis. 2021 Aug 4;20(1):85
pubmed: 34348720
Biophys J. 1999 Dec;77(6):3363-70
pubmed: 10585959
Trends Cell Biol. 2004 Apr;14(4):160-6
pubmed: 15066633
Oncotarget. 2015 Aug 28;6(25):20946-58
pubmed: 26189182
Anal Chem. 2023 May 9;95(18):7254-7261
pubmed: 37125920
J Membr Biol. 2022 Oct;255(4-5):385-405
pubmed: 36219221
World J Gastroenterol. 2002 Apr;8(2):243-6
pubmed: 11925600
Phys Rev E Stat Nonlin Soft Matter Phys. 2003 Oct;68(4 Pt 1):041914
pubmed: 14682980
Biophys J. 2017 Mar 14;112(5):831-833
pubmed: 28297642
PLoS One. 2013 Dec 05;8(12):e80068
pubmed: 24339870
Langmuir. 2020 May 19;36(19):5134-5144
pubmed: 32338922
Curr Opin Cell Biol. 2023 Apr;81:102173
pubmed: 37224683
Acta Biomater. 2023 Jul 15;165:140-152
pubmed: 36167239
Cell Mol Life Sci. 2020 Apr;77(7):1345-1355
pubmed: 31605149
Biochim Biophys Acta. 2013 Mar;1833(3):712-22
pubmed: 23178740
Front Cell Dev Biol. 2022 Sep 19;10:932510
pubmed: 36200037
Opt Express. 2021 Apr 12;29(8):11976-11986
pubmed: 33984967
Curr Opin Cell Biol. 2020 Oct;66:11-18
pubmed: 32416466
Front Cell Dev Biol. 2020 Nov 10;8:588801
pubmed: 33240887
Oncol Lett. 2018 Apr;15(4):4423-4426
pubmed: 29556289
Soft Matter. 2020 Jan 7;16(1):64-81
pubmed: 31720656
Dev Cell. 2019 Jan 7;48(1):15-16
pubmed: 30620900
Biochem Biophys Res Commun. 2008 Oct 3;374(4):609-13
pubmed: 18656442
Micromachines (Basel). 2018 Dec 11;9(12):
pubmed: 30544918
Cells. 2022 Apr 12;11(8):
pubmed: 35455986
Analyst. 2008 Nov;133(11):1498-500
pubmed: 18936825
Sci Rep. 2017 May 8;7(1):1541
pubmed: 28484282