Cells immersed in collagen matrices show a decrease in plasma membrane fluidity as the matrix stiffness increases

Biochimica et Biophysica Acta (BBA) - Biomembranes - Tập 1865 - Trang 184176 - 2023
Joao Aguilar1, Leonel Malacrida2,3, German Gunther4, Belén Torrado5, Viviana Torres6, Bruno F. Urbano1, Susana A. Sánchez1
1Laboratorio de Interacciones Macromoleculares (LIMM), Departamento de Polímeros, Facultad de Ciencias Químicas, Universidad de Concepción, Concepción, Chile
2Departamento de Fisiopatología, Hospital de Clínicas, Universidad de la República, Montevideo, Uruguay
3Advanced Bioimaging Unit, Institut Pasteur Montevideo, Universidad de la República, Montevideo, Uruguay
4Facultad de Ciencias Químicas y Farmacéuticas, Universidad de Chile, Santiago, Chile
5Biomedical Engineering Department, University of California at Irvine, California, USA
6Departamento de Bioquímica, Facultad de Ciencias Biológicas, Universidad de Concepción, Concepción, Chile

Tài liệu tham khảo

Fredriksson, 2006, Red blood cells increase secretion of matrix metalloproteinases from human lung fibroblasts in vitro, Am. J. Phys. Lung Cell., 290, L326, 10.1152/ajplung.00057.2005 Boutouyrie, 2002, Aortic stiffness is an independent predictor of primary coronary events in hypertensive patients - a longitudinal study, Hypertension, 39, 10, 10.1161/hy0102.099031 Schnider, 1980, Glucosylation of human collagen in aging and diabetes mellitus, J. Clin. Invest., 66, 1179, 10.1172/JCI109950 Harrison, 1907, Observations on the living developing nerve fiber, Anat. Rec., 1, 116, 10.1002/ar.1090010503 Conway, 2017, Three dimensional organotypic matrices from alternative collagen sources as pre-clinical models for cell biology, Sci. Rep., 7, 1, 10.1038/s41598-017-17177-5 Kato, 1999, Effects of high pressure on lipids and biomembranes for understanding high-pressure-induced biological phenomena, Biosci. Biotechnol. Biochem., 63, 1321, 10.1271/bbb.63.1321 Gasparski, 2015, Mechanoreception at the cell membrane: more than the integrins, Arch. Biochem. Biophys., 586, 20, 10.1016/j.abb.2015.07.017 Mitrossilis, 2010, Real-time single-cell response to stiffness, Proc. Natl. Acad. Sci. U. S. A., 107, 16518, 10.1073/pnas.1007940107 Handorf, 2015, Tissue stiffness dictates development, homeostasis, and disease progression, Organogenesis, 11, 1, 10.1080/15476278.2015.1019687 Watt, 2013, Role of the extracellular matrix in regulating stem cell fate, Nat. Rev. Mol. Cell Biol., 14, 467, 10.1038/nrm3620 Lv, 2015, Mechanism of regulation of stem cell differentiation by matrix stiffness, Stem Cell Res Ther, 6, 103, 10.1186/s13287-015-0083-4 Lo, 2000, Cell movement is guided by the rigidity of the substrate, Biophys. J., 79, 144, 10.1016/S0006-3495(00)76279-5 Muller, 2008, Calcium phosphate surfaces promote osteogenic differentiation of mesenchymal stem cells, J. Cell. Mol. Med., 12, 281, 10.1111/j.1582-4934.2007.00103.x Solon, 2007, Fibroblast adaptation and stiffness matching to soft elastic substrates, Biophys. J., 93, 4453, 10.1529/biophysj.106.101386 Saez, 2007, Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates, Proc. Natl. Acad. Sci. U. S. A., 104, 8281, 10.1073/pnas.0702259104 Mitrossilis, 2009, Single-cell response to stiffness exhibits muscle-like behavior, Proc. Natl. Acad. Sci. U. S. A., 106, 18243, 10.1073/pnas.0903994106 Brown, 2000, Structure and function of sphingolipid and cholesterol rich membrane rafts, J. Biol. Chem., 275, 17221, 10.1074/jbc.R000005200 Gomez-Mouton, 2001, Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization, Proc. Natl. Acad. Sci. U. S. A., 98, 9642, 10.1073/pnas.171160298 Jacobson, 2007, Lipid rafts: at a crossroad between cell biology and physics, Nat. Cell Biol., 9, 7, 10.1038/ncb0107-7 Sanchez, 2012, Laurdan generalized polarization fluctuations measures membrane packing micro-heterogeneity in vivo, Proc. Natl. Acad. Sci. U. S. A., 109, 7314, 10.1073/pnas.1118288109 Simons, 2002, Cholesterol, lipid rafts, and disease, J. Clin. Invest., 110, 597, 10.1172/JCI0216390 Simons, 2000, Lipid rafts and signal transduction, Nat. Rev. Mol. Cell Biol., 1, 31, 10.1038/35036052 Zajchowski, 2002, Lipid rafts and little caves - compartmentalized signalling in membrane microdomains, Eur. J. Biochem., 269, 737, 10.1046/j.0014-2956.2001.02715.x Tanaka, 2017, Turnover and flow of the cell membrane for cell migration, Sci. Rep., 7, 12970, 10.1038/s41598-017-13438-5 Noutsi, 2016, Assessment of membrane fluidity fluctuations during cellular development reveals time and cell type specificity, PLoS One, 30 Manes, 2003, From rafts to crafts: membrane asymmetry in moving cells, Trends Immunol., 24, 320, 10.1016/S1471-4906(03)00137-6 Ross, 2013, Integrins in mechanotransduction, Curr. Opin. Cell Biol., 25, 613, 10.1016/j.ceb.2013.05.006 Wang, 2010, A role for caveolin-1 in mechanotransduction of fetal type II epithelial cells, Am. J. Phys. Lung Cell. Mol. Phys., 298, L775 Isshiki, 2002, Sites of Ca2+ wave initiation move with caveolae to the trailing edge of migrating cells, J. Cell Sci., 115, 475, 10.1242/jcs.115.3.475 Yu, 2006, Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels, J. Clin. Invest., 116, 1284, 10.1172/JCI27100 Yeh, 2017, Mechanotransduction of matrix stiffness in regulation of focal adhesion size and number: reciprocal regulation of caveolin-1 and beta1 integrin, Sci. Rep., 7, 15008, 10.1038/s41598-017-14932-6 Roy, 2012, The role of membrane lipid rafts in osteoblastic sensing and propagation of mechanical forces: a microfluidic based single cell analysis study Petersen, 2016, Kinetic disruption of lipid rafts is a mechanosensor for phospholipase D, Nat. Commun., 7, 13873, 10.1038/ncomms13873 Zhao, 2002, Membrane lipids, EGF receptors, and intracellular signals colocalize and are polarized in epithelial cells moving directionally in a physiological electric field, FASEB J., 16, 857, 10.1096/fj.01-0811fje Lin, 2017, Lipid rafts sense and direct electric field-induced migration, Proc. Natl. Acad. Sci. U. S. A., 114, 8568, 10.1073/pnas.1702526114 Sinha, 2011, Cells respond to mechanical stress by rapid disassembly of caveolae, Cell, 144, 402, 10.1016/j.cell.2010.12.031 Yamamoto, 2020, Shear stress activates mitochondrial oxidative phosphorylation by reducing plasma membrane cholesterol in vascular endothelial cells, Proc. Natl. Acad. Sci. U. S. A., 117, 33660, 10.1073/pnas.2014029117 Yamamoto, 2015, Vascular endothelial cell membranes differentiate between stretch and shear stress through transitions in their lipid phases, Am. J. Physiol. Heart Circ. Physiol., 309, H1178, 10.1152/ajpheart.00241.2015 Yamamoto, 2018, Emerging role of plasma membranes in vascular endothelial mechanosensing, Circ. J., 82, 2691, 10.1253/circj.CJ-18-0052 Parasassi, 1998, Laurdan and Prodan as polarity-sensitive fluorescent membrane probes, J. Fluoresc., 8, 365, 10.1023/A:1020528716621 Günther, 2018, Study of rabbit erythrocytes membrane solubilization by sucrose monomyristate using laurdan and phasor analysis, Colloids Surf. B: Biointerfaces, 161, 375, 10.1016/j.colsurfb.2017.10.068 Gunther, 2021, LAURDAN since weber: the quest for visualizing membrane heterogeneity, Acc. Chem. Res., 54, 976, 10.1021/acs.accounts.0c00687 Golfetto, 2015, The Laurdan spectral phasor method to explore membrane micro-heterogeneity and lipid domains in live cells, Methods Mol. Biol., 1232, 273, 10.1007/978-1-4939-1752-5_19 Malacrida, 2015, Model-free methods to study membrane environmental probes: a comparison of the spectral phasor and generalized polarization approaches, Methods Appl. Fluoresc., 3, 10.1088/2050-6120/3/4/047001 Parasassi, 1993, Modulation and dynamics of phase properties in phospholipid mixtures detected by Laurdan fluorescence, Photochem. Photobiol., 57, 403, 10.1111/j.1751-1097.1993.tb02309.x Malacrida, 2017, A multidimensional phasor approach reveals LAURDAN photophysics in NIH-3T3 cell membranes, Sci. Rep., 7, 9215, 10.1038/s41598-017-08564-z Parasassi, 1991, Quantitation of lipid phases in phospholipid vesicles by the generalized polarization of LAURDAN fluorescence, Biophys. J., 60, 179, 10.1016/S0006-3495(91)82041-0 Parasassi, 1997, Two-photon fluorescence microscopy of laurdan generalized polarization domains in model and natural membranes, Biophys. J., 72, 2413, 10.1016/S0006-3495(97)78887-8 Parasassi, 1994, Influence of cholesterol on phospholipid bilayers phase domains as detected by Laurdan fluorescence, Biophys. J., 66, 120, 10.1016/S0006-3495(94)80763-5 Parasassi, 1995, Membrane lipid domains and dynamics as detected by Laurdan fluorescence, J. Fluoresc., 5, 59, 10.1007/BF00718783 Malacrida, 2018, LAURDAN fluorescence and phasor plots reveal the effects of a H2O2 bolus in NIH-3T3 fibroblast membranes dynamics and hydration, Free Radic. Biol. Med., 144, 10.1016/j.freeradbiomed.2018.06.004 Sameni, 2018, Alteration in fluidity of cell plasma membrane in Huntington disease revealed by spectral phasor analysis, Sci. Rep., 8, 734, 10.1038/s41598-018-19160-0 Rodriguez-Agudo, 2019, StarD5: an ER stress protein regulates plasma membrane and intracellular cholesterol homeostasis, J. Lipid Res., 60, 1087, 10.1194/jlr.M091967 Sena, 2017, Spectral phasor analysis reveals altered membrane order and function of root hair cells in Arabidopsis dry2/sqe1-5 drought hypersensitive mutant, Plant Physiol. Biochem., 119, 224, 10.1016/j.plaphy.2017.08.017 Bron, 2009, Rheological characterization of the nucleus pulposus and dense collagen scaffolds intended for functional replacement, J. Orthop. Res., 27, 620, 10.1002/jor.20789 Baradet, 1995, Three dimensional reconstruction of fibrin clot networks from stereoscopic intermediate voltage electron microscope images and analysis of branching, Biophys. J., 68, 1551, 10.1016/S0006-3495(95)80327-9 Dvornikov, 2019, The DIVER microscope for imaging in scattering media, Methods Protoc., 2, 53, 10.3390/mps2020053 Digman, 2008, The phasor approach to fluorescence lifetime imaging analysis, Biophys. J., 94, L14, 10.1529/biophysj.107.120154 Jameson, 1984, The measurement and analysis of heterogeneous emissions by multifrequency phase and modulation fluorometry, Appl. Spectrosc. Rev., 20, 55, 10.1080/05704928408081716 Redford, 2005, Polar plot representation for frequency-domain analysis of fluorescence lifetimes, J. Fluoresc., 15, 805, 10.1007/s10895-005-2990-8 James, 2011, Applications of phasor plots to in vitro protein studies, Anal. Biochem., 410, 70, 10.1016/j.ab.2010.11.011 Fereidouni, 2012, Spectral phasor analysis allows rapid and reliable unmixing of fluorescence microscopy spectral images, Opt. Express, 20, 12729, 10.1364/OE.20.012729 Chiu, 2013, Cell matrix remodeling ability shown by image spatial correlation, J. Biophys., 2013, 1, 10.1155/2013/532030 Osidak, 2019, Viscoll collagen solution as a novel bioink for direct 3D bioprinting, J. Mater. Sci. Mater. Med., 30, 31, 10.1007/s10856-019-6233-y Riedel, 2019, Design of biomimetic collagen matrices by reagent-free electron beam induced crosslinking: structure-property relationships and cellular response, Mater. Des., 168, 10.1016/j.matdes.2019.107606 Wang, 2016, Differences in cytocompatibility between collagen, gelatin and keratin, Mater. Sci. Eng. C Mater. Biol. Appl., 59, 30, 10.1016/j.msec.2015.09.093 Turker, 2019, Biomimetic hybrid scaffold consisting of co-electrospun collagen and PLLCL for 3D cell culture, Int. J. Biol. Macromol., 139, 1054, 10.1016/j.ijbiomac.2019.08.082 Engler, 2006, Matrix elasticity directs stem cell lineage specification, Cell, 126, 677, 10.1016/j.cell.2006.06.044 Kreger, 2010, Polymerization and matrix physical properties as important design considerations for soluble collagen formulations, Biopolymers, 93, 690, 10.1002/bip.21431 Raub, 2007, Noninvasive assessment of collagen gel microstructure and mechanics using multiphoton microscopy, Biophys. J., 92, 2212, 10.1529/biophysj.106.097998 Zhang, 2017, Systematic modulation of gelation dynamics of snakehead (Channa argus) skin collagen by environmental parameters, Macromol. Res., 25, 1105, 10.1007/s13233-017-5149-y Ranjit, 2016, Characterizing fibrosis in UUO mice model using multiparametric analysis of phasor distribution from FLIM images, Biomed. Opt. Express, 7, 3519, 10.1364/BOE.7.003519 Motte, 2013, Strain stiffening in collagen I networks, Biopolymers, 99, 35, 10.1002/bip.22133 Storm, 2005, Nonlinear elasticity in biological gels, Nature, 435, 191, 10.1038/nature03521 Kurniawan, 2012, Early stiffening and softening of collagen: interplay of deformation mechanisms in biopolymer networks, Biomacromolecules, 13, 691, 10.1021/bm2015812 Henson, 1995, Effect of gap on the viscosity of monodisperse polystyrene melts: slip effects, J. Rheol., 39, 359, 10.1122/1.550702 Burla, 2020, Connectivity and plasticity determine collagen network fracture, Proc. Natl. Acad. Sci. U. S. A., 117, 8326, 10.1073/pnas.1920062117 Vader, 2009, Strain-induced alignment in collagen gels, PLoS One, 4, 10.1371/journal.pone.0005902 Roeder, 2002, Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure, J. Biomech. Eng., 124, 214, 10.1115/1.1449904 Madhavan, 2010, Evaluation of composition and crosslinking effects on collagen-based composite constructs, Acta Biomater., 6, 1413, 10.1016/j.actbio.2009.09.028