Anomalously diffusing and persistently migrating cells in 2D and 3D culture environments

APL Bioengineering - Tập 2 Số 2 - 2018
Igor D. Luzhansky1, Alyssa D. Schwartz1, Joshua D. Cohen2, John P. MacMunn1, Lauren E. Barney1, Lauren Jansen1, Shelly R. Peyton1
1Department of Chemical Engineering, University of Massachusetts Amherst 1 , Amherst, Massachusetts 01003, USA
2Department of Biomedical Engineering, The Johns Hopkins University School of Medicine 2 , Baltimore, Maryland 21205, USA

Tóm tắt

Appropriately chosen descriptive models of cell migration in biomaterials will allow researchers to characterize and ultimately predict the movement of cells in engineered systems for a variety of applications in tissue engineering. The persistent random walk (PRW) model accurately describes cell migration on two-dimensional (2D) substrates. However, this model inherently cannot describe subdiffusive cell movement, i.e., migration paths in which the root mean square displacement increases more slowly than the square root of the time interval. Subdiffusivity is a common characteristic of cells moving in confined environments, such as three-dimensional (3D) porous scaffolds, hydrogel networks, and in vivo tissues. We demonstrate that a generalized anomalous diffusion (AD) model, which uses a simple power law to relate the mean square displacement to time, more accurately captures individual cell migration paths across a range of engineered 2D and 3D environments than does the more commonly used PRW model. We used the AD model parameters to distinguish cell movement profiles on substrates with different chemokinetic factors, geometries (2D vs 3D), substrate adhesivities, and compliances. Although the two models performed with equal precision for superdiffusive cells, we suggest a simple AD model, in lieu of PRW, to describe cell trajectories in populations with a significant subdiffusive fraction, such as cells in confined, 3D environments.

Từ khóa


Tài liệu tham khảo

2005, Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion, J. Cell Physiol., 204, 198, 10.1002/jcp.20274

2014, Bioengineered 3D brain tumor model to elucidate the effects of matrix stiffness on glioblastoma cell behavior using PEG-based hydrogels, Mol. Pharm., 11, 2115, 10.1021/mp5000828

2011, Marrow-derived stem cell motility in 3D synthetic scaffold is governed by geometry along with adhesivity and stiffness, Biotechnol. Bioeng., 108, 1181, 10.1002/bit.23027

2006, Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis, Proc. Natl. Acad. Sci. U. S. A., 103, 10889, 10.1073/pnas.0604460103

2009, Guiding cell migration in 3D: A collagen matrix with graded directional stiffness, Cell Motil. Cytoskeleton, 66, 121, 10.1002/cm.20331

2009, Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength, Biophys. J., 97, 1313, 10.1016/j.bpj.2009.06.021

2014, A peptide functionalized poly(ethylene glycol) (PEG) hydrogel for investigating the influence of biochemical and biophysical matrix properties on tumor cell migration, Biomater. Sci., 2, 1024, 10.1039/c4bm00022f

2012, Independent regulation of tumor cell migration by matrix stiffness and confinement, Proc. Natl. Acad. Sci. U. S. A., 109, 10334, 10.1073/pnas.1118073109

2012, Bio-inspired materials for parsing matrix physicochemical control of cell migration: A review, Integr. Biol., 4, 37, 10.1039/C1IB00069A

2009, Model substrates for studies of cell mobility, Curr. Opin. Chem. Biol., 13, 697, 10.1016/j.cbpa.2009.10.001

1993, Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength, J. Cell Biol., 122, 729, 10.1083/jcb.122.3.729

1991, Migration of individual microvessel endothelial cells: Stochastic model and parameter measurement, J. Cell Sci., 99, 419

1992, Measurement of individual cell migration parameters for human tissue cells, AIChE J., 38, 1092, 10.1002/aic.690380712

2010, Persistent random motion: Uncovering cell migration dynamics, J. Theor. Biol., 267, 526, 10.1016/j.jtbi.2010.09.022

2015, Supramolecular hydrogels: Synthesis, properties and their biomedical applications, Biomater. Sci., 3, 937, 10.1039/C4BM00448E

2014, Extracellular matrix-mimetic poly (ethylene glycol) hydrogels engineered to regulate smooth muscle cell proliferation in 3D, Acta Biomater., 10, 5106, 10.1016/j.actbio.2014.08.025

2013, Hydrogels that mimic developmentally relevant matrix and N-cadherin interactions enhance MSC chondrogenesis, Proc. Natl. Acad. Sci. U. S. A., 110, 10117, 10.1073/pnas.1214100110

2010, Synthesis of photodegradable hydrogels as dynamically tunable cell culture platforms, Nat. Protoc., 5, 1867, 10.1038/nprot.2010.139

2018, Guiding 3D cell migration in deformed synthetic hydrogel microstructures, Soft Matter, 14, 2816, 10.1039/C8SM00018B

2008, Epidermal growth factor-induced enhancement of glioblastoma cell migration in 3D arises from an intrinsic increase in speed but an extrinsic matrix- and proteolysis-dependent increase in persistence, Mol. Biol. Cell, 19, 4249, 10.1091/mbc.e08-05-0501

2007, Understanding the molecular basis for differential binding of integrins to collagen and gelatin, Biophys. J., 92, L17, 10.1529/biophysj.106.097519

2007, Understanding effects of matrix protease and matrix organization on directional persistence and translational speed in three-dimensional cell migration, Ann. Biomed. Eng., 35, 91, 10.1007/s10439-006-9205-6

2008, A Levy flight for light, Nature, 453, 495, 10.1038/nature06948

2010, Bacterial chromosomal loci move subdiffusively through a viscoelastic cytoplasm, Phys. Rev. Lett., 104, 238102, 10.1103/PhysRevLett.104.238102

1984, Anomalous diffusion of erythrocytes in the presence of polyvinylpyrrolidone, Biophys. J., 46, 219, 10.1016/S0006-3495(84)84015-1

2013, Anomalous transport in the crowded world of biological cells, Rep. Prog. Phys., 76, 046602, 10.1088/0034-4885/76/4/046602

1996, Anomalous diffusion due to binding: A Monte Carlo study, Biophys. J., 70, 1250, 10.1016/S0006-3495(96)79682-0

1994, Anomalous diffusion due to obstacles: A Monte Carlo study, Biophys. J., 66, 394, 10.1016/S0006-3495(94)80789-1

2012, Collective cell migration: Leadership, invasion and segregation, J. R. Soc. Interface, 9, 3268, 10.1098/rsif.2012.0448

2001, Anomalous diffusion and non-Gaussian velocity distribution of Hydra cells in cellular aggregates, Physica A, 293, 549, 10.1016/S0378-4371(01)00009-7

2008, Anomalous dynamics of cell migration, Proc. Natl. Acad. Sci. U. S. A., 105, 459, 10.1073/pnas.0707603105

2015, A cell-ECM screening method to predict breast cancer metastasis, Integr. Biol., 7, 198, 10.1039/C4IB00218K

2013, PEG-phosphorylcholine hydrogels as tunable and versatile platforms for mechanobiology, Biomacromolecules, 14, 2294, 10.1021/bm400418g

1983, Characterising a kinesis response: Time averaged measures of cell speed and directional persistence, Agents Actions Suppl., 12, 14

2014, Quantitative and unbiased analysis of directional persistence in cell migration, Nat. Protoc., 9, 1931, 10.1038/nprot.2014.131

1997, Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness, Nature, 385, 537, 10.1038/385537a0

2017, Biphasic dependence of glioma survival and cell migration on CD44 expression level, Cell Rep., 18, 23, 10.1016/j.celrep.2016.12.024

2009, The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells, Cancer Res., 69, 4167, 10.1158/0008-5472.CAN-08-4859

2008, Sampling the cell with anomalous diffusion - the discovery of slowness, Biophys. J., 94, 90, 10.1529/biophysj.107.117044

2018, Complementary, high-throughput methods for creating multi-dimensional, PEG-based biomaterials, ACS Biomater. Sci. Eng., 4, 707, 10.1021/acsbiomaterials.7b00737

2018, Control of thiol-maleimide reaction kinetics in PEG hydrogel networks, Acta Biomater., 70, 120, 10.1016/j.actbio.2018.01.043

2018, A biomaterial screening approach reveals microenvironmental mechanisms of drug resistance, Integr. Biol., 9, 912, 10.1039/C7IB00128B

2015, Actin flows mediate a universal coupling between cell speed and cell persistence, Cell, 161, 374, 10.1016/j.cell.2015.01.056

2016, Substrate engagement of integrins alpha5beta1 and alphavbeta3 is necessary, but not sufficient, for high directional persistence in migration on fibronectin, Sci. Rep., 6, 23258, 10.1038/srep23258

2005, Directional persistence of EGF-induced cell migration is associated with stabilization of lamellipodial protrusions, Biophys. J., 88, 1479, 10.1529/biophysj.104.047365

2004, Anomalous diffusion probes microstructure dynamics of entangled F-actin networks, Phys. Rev. Lett., 92, 178101, 10.1103/PhysRevLett.92.178101

2002, Properties of cage rearrangements observed near the colloidal glass transition, Phys. Rev. Lett., 89, 095704, 10.1103/PhysRevLett.89.095704

2017, Single and collective cell migration: The mechanics of adhesions, Mol. Biol. Cell, 28, 1833, 10.1091/mbc.e17-03-0134

2012, Generalized Levy walks and the role of chemokines in migration of effector CD8(+) T cells, Nature, 486, 545, 10.1038/nature11098

Thông tin
Thông tin xuất bản

APL Bioengineering

Tập 2 Số 2

Thông tin tác giả