Remodelling of the fibre-aggregate structure of collagen gels by cancer-associated fibroblasts: a time-resolved grey-tone image analysis based on stochastic modelling
[en] Solid tumors consist of tumor cells associated with stromal and immune cells, secreted factors and extracellular matrix (ECM), that together constitute the tumor microenvironment. Among stromal cells, activated fibroblasts, known as cancer-associated fibroblasts (CAFs) are of particular interest. CAFs secrete a plethora of ECM components including collagen and modulate the architecture of the ECM, thereby influencing cancer cell migration. The characterization of the collagen fibre network and its space and time-dependent microstructural modifications is key to investigating the interactions between cells and the ECM. Developing image analysis tools for that purpose is still a challenge because the structural complexity of the collagen network calls for specific statistical descriptors. Moreover, the low signal-to-noise ratio of imaging techniques available for time-resolved studies rules out standard methods based on image segmentation. In this work, we develop a novel approach based on the stochastic modelling of the gel structure and on grey-tone image analysis. The method is then used to study the remodelling of a collagen matrix by migrating breast cancer-derived CAFs in a three-dimensional spheroid model of cellular invasion.
Specifically, the structure of the collagen at the scale of a few microns is found to consist in regions with high fibre density separated by depleted regions, which can be thought of as aggregates and pores. The approach we develop captures this two-scale structure with a clipped Gaussian field model to describe the aggregates-and-pores large-scale structure, and a homogeneous Boolean model to describe the small-scale fibre network within the aggregates. The model parameters are identified by fitting the grey-tone histograms and correlation functions of confocal microscopy images. The method applies to unprocessed grey-tone images, and it can therefore be used with low magnification, noisy time-lapse reflectance images. When applied to the spheroid time-resolved images, the method reveals different matrix densification mechanisms for the matrix in direct contact or far from the cells.
Blacher, Silvia ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire
Maquoi, Erik ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Language :
English
Title :
Remodelling of the fibre-aggregate structure of collagen gels by cancer-associated fibroblasts: a time-resolved grey-tone image analysis based on stochastic modelling
Publication date :
2023
Journal title :
Frontiers in Immunology
eISSN :
1664-3224
Publisher :
Frontiers Research Foundation, Lausanne, Switzerland
CJG and EM are grateful to the Funds for Scientific Research (F.R.S.-FNRS, Belgium) for Research Associate positions. This work was supported by FNRS-Televie grants 7.4589.16 and 7.6527.18.
scite shows how a scientific paper has been cited by providing the context of the citation, a classification describing whether it supports, mentions, or contrasts the cited claim, and a label indicating in which section the citation was made.
Bibliography
Hynes RO. The extracellular matrix: Not just pretty fibrils. Science (2009) 326:1216–9. doi: 10.1126/science.1176009
Hynes RO Naba A. Overview of the matrisome-an inventory of extracellular matrix constituents and functions. Cold Spring Harbor Perspect Biol (2012) 4. doi: 10.1101/cshperspect.a004903
Oskarsson T. Extracellular matrix components in breast cancer progression and metastasis. Breast (2013) 22:S66–72. doi: 10.1016/j.breast.2013.07.012
Frantz C Stewart KM Weaver VM. The extracellular matrix at a glance. J Cell Sci (2010) 123:4195–200. doi: 10.1242/jcs.023820
Theocharis AD Skandalis SS Gialeli C Karamanos NK. Extracellular matrix structure. Adv Drug Delivery Rev (2016) 97:4–27. doi: 10.1016/j.addr.2015.11.001
Leitinger B Hohenester E. Mammalian collagen receptors. Matrix Biol (2007) 26:146–55. doi: 10.1016/j.matbio.2006.10.007
Xian X Gopal S Couchman JR. Syndecans as receptors and organizers of the extracellular matrix. Cell Tissue Res (2010) 339:31–46. doi: 10.1007/s00441-009-0829-3
Doyle AD Wang FW Matsumoto K Yamada KM. One-dimensional topography underlies three-dimensional fi brillar cell migration. J Cell Biol (2009) 184:481–90. doi: 10.1083/jcb.200810041
Charras G Sahai E. Physical influences of the extracellular environment on cell migration. Nat Rev Mol Cell Biol (2014) 15:813–24. doi: 10.1038/nrm3897
Seo BR Chen X Ling L Song YH Shimpi AA Choi S et al. Collagen microarchitecture mechanically controls myofibroblast differentiation. Proc Natl Acad Sci U.S.A (2020) 117:11387–11398. doi: 10.1073/pnas.1919394117
Shieh AC Rozansky HA Hinz B Swartz MA. Tumor cell invasion is promoted by interstitial flow-induced matrix priming by stromal fibroblasts. Cancer Res (2011) 71:790–800. doi: 10.1158/0008-5472.CAN-10-1513
Yue B. Biology of the extracellular matrix: An overview. J Glaucoma (2014) 23:S20–3. doi: 10.1097/IJG.0000000000000108
Mouw JK Ou G Weaver VM. Extracellular matrix assembly: A multiscale deconstruction. Nat Rev Mol Cell Biol (2014) 15:771–85. doi: 10.1038/nrm3902
Bourgot I Primac I Louis T Noël A Maquoi E. Reciprocal interplay between fibrillar collagens and collagen-binding integrins: Implications in cancer progression and metastasis. Front Oncol (2020) 10. doi: 10.3389/fonc.2020.01488
Revell CK Jensen OE Shearer T Lu Y Holmes DF Kadler KE. Collagen fibril assembly: New approaches to unanswered questions. Matrix Biol Plus (2021) 12:100079. doi: 10.1016/j.mbplus.2021.100079
Provenzano P Inman D Eliceiri K Keely PJ. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene (2019) 28:4326–43. doi: 10.1038/onc.2009.299
Provenzano PP Inman DR Eliceiri KW Knittel JG Yan L Rueden CT et al. Collagen density promotes mammary tumor initiation and progression. BMC Med (2008) 6. doi: 10.1186/1741-7015-6-11
Buchmann B Engelbrecht LK Fernandez P et al. Mechanical plasticity of collagen directs branch elongation in human mammary gland organoids. Nat Commun (2021) 12:2759. doi: 10.1038/s41467-021-22988-2
Doyle AD Carvajal N Jin A Matsumoto K Yamada KM. Local 3d matrix microenvironment regulates cell migration through spatiotemporal dynamics of contractility-dependent adhesions. Nat Commun (2015) 6. doi: 10.1038/ncomms9720
Sun B. The mechanics of fibrillar collagen extracellular matrix. Cell Rep Phys Sci (2021) 2:100515. doi: 10.1016/j.xcrp.2021.100515
Lauffenburger DA Horwitz AF. Cell migration: A physically integrated molecular process. Cell (1996) 84:359–69. doi: 10.1016/S0092-8674(00)81280-5
Clark K Howe JD Pullar CE Green JA Artym VV Yamada KM et al. Tensin 2 modulates cell contractility in 3d collagen gels through the rhogap dlc1. J Cell Biochem (2010) 109:808–17. doi: 10.1002/jcb.22460
Provenzano PP Eliceiri KW Campbell JM Inman DR White JG Keely PJ. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med (2006) 4. doi: 10.1186/1741-7015-4-38
Conklin MW Eickhoff JC Riching KM Pehlke CA Eliceiri KW Provenzano PP et al. Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am J Pathol (2011) 178:1221–32. doi: 10.1016/j.ajpath.2010.11.076
Case A Brisson BK Durham AC Rosen S Monslow J Buza E et al. Identification of prognostic collagen signatures and potential therapeutic stromal targets in canine mammary gland carcinoma. PloS One (2017) 12. doi: 10.1371/journal.pone.0180448
Dickinson RB Guido S Tranquillo RT. Biased cell migration of fibroblasts exhibiting contact guidance in oriented collagen gels. Ann Biomed Eng (1994) 22:342–56. doi: 10.1007/BF02368241
Ray A Provenzano PP. Aligned forces: Origins and mechanisms of cancer dissemination guided by extracellular matrix architecture. Curr Opin Cell Biol (2021) 72:63–71. doi: 10.1016/j.ceb.2021.05.004
Ray A Callaway MK Rodríguez-Merced NJ Crampton AL Carlson M Emme KB et al. Stromal architecture directs early dissemination in pancreatic ductal adenocarcinoma. JCI Insight (2022) 7. doi: 10.1172/jci.insight.150330
Lu P Weaver VM Werb Z. The extracellular matrix: A dynamic niche in cancer progression. J Cell Biol (2012) 196:395–406. doi: 10.1083/jcb.201102147
Stylianopoulos T Poh M-Z Insin N Bawendi MG Fukumura D Munn LL et al. Diffusion of particles in the extracellular matrix: The effect of repulsive electrostatic interactions. Biophys J (2010) 99:1342–9. doi: 10.1016/j.bpj.2010.06.016
Gomez D Natan S Shokef Y Lesman A. Mechanical interaction between cells facilitates molecular transport. Adv Biosys (2019) 3:1900192. Gomez:2019. doi: 10.1002/adbi.201900192
Gieniec KA Butler LM Worthley DL Woods SL. Cancer-associated fibroblasts–heroes or villains? Br J Cancer (2019) 121:293–302. doi: 10.1038/s41416-019-0509-3
Barbazán J Vignjevic DM. Cancer associated fibroblasts: is the force the path to the dark side? Curr Opin Cell Biol (2019) 56:71–9. doi: 10.1016/j.ceb.2018.09.002
Kalluri R. The biology and function of fibroblasts in cancer. Nat Rev Cancer (2016) 16:582–98. doi: 10.1038/nrc.2016.73
Biffi G Tuveson DA. Diversity and biology of cancer-associated fibroblasts. Physiol Rev (2021) 101:147–76. doi: 10.1152/physrev.00048.2019
Sahai E Astsaturov I Cukierman E DeNardo DG Egeblad M Evans RM et al. A framework for advancing our understanding of cancer-associated fibroblasts. Nat Rev Cancer (2020) 20:174–86. doi: 10.1038/s41568-019-0238-1
Attieh Y Vignjevic DM. The hallmarks of CAFs in cancer invasion. Eur J Cell Biol (2016) 95:493–502. doi: 10.1016/j.ejcb.2016.07.004
Boulter L Bullock E Mabruk Z Brunton VG. The fibrotic and immune microenvironments as targetable drivers of metastasis. Br J Cancer (2020) 124:27–36. doi: 10.1038/s41416-020-01172-1
D’Arcangelo E Wu NC Cadavid JL McGuigan AP. The life cycle of cancer-associated fibroblasts within the tumour stroma and its importance in disease outcome. Br J Cancer (2020) 122:931–42. doi: 10.1038/s41416-019-0705-1
Faouzi S Bail BL Neaud V Boussarie L Saric J Bioulac-Sage P et al. Myofibroblasts are responsible for collagen synthesis in the stroma of human hepatocellular carcinoma: an in vivo and in vitro study. J Hepatol (1999) 30:275–84. doi: 10.1016/S0168-8278(99)80074-9
Papanicolaou M Parker AL Yam M Filipe EC Wu SZ Chitty JL et al. Temporal profiling of the breast tumour microenvironment reveals collagen XII as a driver of metastasis. Nat Comm (2022) 13. doi: 10.1038/s41467-022-32255-7
Brichkina A Bertero T Loh HM Nguyen NTM Emelyanov A Rigade S et al. p38mapk builds a hyaluronan cancer niche to drive lung tumorigenesis. Genes Dev (2016) 30:2623–36. Brichkina:2016. doi: 10.1101/gad.290346.116
Kim BG An HJ Kang S Choi YP Gao M-Q Park H et al. Laminin-332-rich tumor microenvironment for tumor invasion in the interface zone of breast cancer. Am J Pathol (2011) 178:373–81. doi: 10.1016/j.ajpath.2010.11.028
Attieh Y Clark AG Grass C Richon S Pocard M Mariani P et al. Cancer-associated fibroblasts lead tumor invasion through integrin-β3-dependent fibronectin assembly. J Cell Biol (2017) 216:3509–20. doi: 10.1083/jcb.201702033
Gonzalez LO Corte MD Junquera S Gonzalez-Fernndez R del Casar JM Garcia C et al. Expression and prognostic significance of metalloproteases and their inhibitors in luminal a and basal-like phenotypes of breast carcinoma. Hum Pathol (2009) 40:1224–33. doi: 10.1016/j.humpath.2008.12.022
Thorseth M-L Carretta M Jensen C Molgaard K Jurgensen HJ Engelholm LH et al. Uncovering mediators of collagen degradation in the tumor microenvironment. Matrix Biol Plus (2022) 13:100101. doi: 10.1016/j.mbplus.2022.100101
Yazdani S Bansal R Prakash J. Drug targeting to myofibroblasts: Implications for fibrosis and cancer. Advanced Drug Delivery Rev (2017) 121:101–16. doi: 10.1016/j.addr.2017.07.010
Gaggioli C Hooper S Hidalgo-Carcedo C Grosse R Marshall JF Harrington K et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for rhogtpases in leading and following cells. Nat Cell Biol (2007) 9:1392–400. doi: 10.1038/ncb1658
Feng B Wu J Shen B Jiang F Feng J. Cancer-associated fibroblasts and resistance to anticancer therapies: status, mechanisms, and countermeasures. Cancer Cell Int (2022) 22. doi: 10.1186/s12935-022-02599-7
Cohen IJ Blasberg R. Impact of the tumor microenvironment on tumor-infiltrating lymphocytes: Focus on breast cancer. Breast Cancer: Basic Clin Res (2017) 11:117822341773156. doi: 10.1177/1178223417731565
Salmon H Franciszkiewicz K Damotte D Dieu-Nosjean M-C Validire P Trautmann A et al. Matrix architecture defines the preferential localization and migration of t cells into the stroma of human lung tumors. J Clin Investig (2012) 122:899–910. doi: 10.1172/JCI45817
Grout JA Sirven P Leader AM Maskey S Hector E Puisieux I et al. Spatial positioning and matrix programs of cancer-associated fibroblasts promote t cell exclusion in human lung tumors. Cancer Discovery (2022) 12(11):2606–2625. doi: 10.1101/2022.01.20.476763
Rømer AMA Thorseth M-L Madsen DH. Immune modulatory properties of collagen in cancer. Front Immunol (2021) 12. doi: 10.3389/fimmu.2021.791453
Tsujino T Seshimo I Yamamoto H Ngan CY Ezumi K Takemasa I et al. Stromal myofibroblasts predict disease recurrence for colorectal cancer. Clin Cancer Res (2007) 13:2082–90. doi: 10.1158/1078-0432.CCR-06-2191
Paulsson J Micke P. Prognostic relevance of cancer-associated fibroblasts in human cancer. Semin Cancer Biol (2014) 25:61–8. doi: 10.1016/j.semcancer.2014.02.006
Galbo PM Zang X Zheng D. Molecular features of cancer-associated fibroblast subtypes and their implication on cancer pathogenesis, prognosis, and immunotherapy resistance. Clin Cancer Res (2021) 27:2636–47. doi: 10.1158/1078-0432.CCR-20-4226
Bell E Ivarsson B Merrill C. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc Natl Acad Sci USA (1979) 76:1274–8. doi: 10.1073/pnas.76.3.1274
Dallon JC Ehrlich HP. A review of fibroblast-populated collagen lattices. Wound Repair Regen (2008) 16:472–9. doi: 10.1111/j.1524-475X.2008.00392.x
Mikami Y Matsuzaki H Takeshima H Makita K Yamauchi Y Nagase T. Development of an in vitro assay to evaluate contractile function of mesenchymal cells that underwent epithelial-mesenchymal transition. J Visualized Exp (2016) 112:53974. doi: 10.3791/53974
Steinwachs J Metzner C Skodzek K Lang N Thievessen I Mark C et al. Three-dimensional force microscopy of cells in biopolymer networks. Nat Methods (2015) 13:171–6. doi: 10.1038/nmeth.3685
Hall MS Long R Feng X Huang Y Hui C-Y Wu M. Toward single cell traction microscopy within 3d collagen matrices. Exp Cell Res (2013) 319:2396–408. doi: 10.1016/j.yexcr.2013.06.009
Pakshir P Alizadehgiashi M Wong B Coelho NM Chen X Gong Z et al. Dynamic fibroblast contractions attract remote macrophages in fibrillar collagen matrix. Nat Commun (2019) 10. doi: 10.1038/s41467-019-09709-6
Mark C Grundy TJ Strissel PL Böhringer D Grummel N Gerum R et al. Collective forces of tumor spheroids in three-dimensional biopolymer networks. Elife (2020) 9. doi: 10.7554/eLife.59538
Frye M Taddei A Dierkes C Martinez-Corral I Fielden M Ortsäter H et al. Matrix stiffness controls lymphatic vessel formation through regulation of a GATA2-dependent transcriptional program. Nat Commun (2018) 9. doi: 10.1038/s41467-018-03959-6
Brightman AO Rajwa BP Sturgis JE McCallister ME Robinson JP Voytik-Harbin SL. Time-lapse confocal reflection microscopy of collagen fibrillogenesis and extracellular matrix assembly in vitro. Biopolymers (2000) 54:222–34. doi: 10.1002/1097-0282(200009)54:3<222::AID-BIP80>3.0.CO;2-K
Friedl P. Dynamic imaging of cellular interactions with extracellular matrix. Histochem Cell Biol (2004) 122:183–90. doi: 10.1007/s00418-004-0682-0
Friedl P Bröcker E. The biology of cell locomotion within three-dimensional extracellular matrix. Cell Mol Life Sci (2000) 57:41–64. doi: 10.1007/s000180050498
Wolf K Wu YI Liu Y Geiger J Tam E Overall C et al. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol (2007) 9:893–904. doi: 10.1038/ncb1616
Yang Y Leone LM Kaufman LJ. Elastic moduli of collagen gels can be predicted from two-dimensional confocal microscopy. Biophys J (2009) 97:2051–60. doi: 10.1016/j.bpj.2009.07.035
Lang NR Münster S Metzner C Krauss P Schürmann S Lange J et al. Estimating the 3d pore size distribution of biopolymer networks from directionally biased data. Biophys J (2013) 105:1967–75. doi: 10.1016/j.bpj.2013.09.038
Bayan C Levitt JM Miller E Kaplan D Georgakoudi I. Fully automated, quantitative, noninvasive assessment of collagen fiber content and organization in thick collagen gels. J Appl Phys (2009) 105. doi: 10.1063/1.3116626
Bredfeldt JS Liu Y Pehlke CA Conklin MW Szulczewski JM Inman DR et al. Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer. J Biomed Opt (2014) 19. doi: 10.1117/1.JBO.19.1.016007
Liu Z Speroni L Quinn KP Alonzo C Pouli D Zhang Y et al. 3d organizational mapping of collagen fibers elucidates matrix remodeling in a hormone-sensitive 3d breast tissue model. Biomaterials (2018) 179:96–108. doi: 10.1016/j.biomaterials.2018.06.036
Boudaoud A Burian A Borowska-Wykret D Uyttewaal M Wrzalik R Kwiatkowska D et al. FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat Protoc (2014) 9:457–63. doi: 10.1038/nprot.2014.024
Pijanka JK Markov PP Midgett D Paterson NG White N Blain EJ et al. Quantification of collagen fiber structure using second harmonic generation imaging and two-dimensional discrete fourier transform analysis: Application to the human optic nerve head. J Biophotonics (2019) 12. doi: 10.1002/jbio.201800376
Altendorf H Decenciere E Jeulin D Peixoto PDS Deniset-Besseau A Angelini E et al. Imaging and 3d morphological analysis of collagen fibrils. J Microscopy (2012) 247:161–75. doi: 10.1111/j.1365-2818.2012.03629.x
Wu PC Hsieh TY Tsai ZU Liu TM. In vivo quantification of the structural changes of collagens in a melanoma microenvironment with second and third harmonic generation microscopy. Sci Rep (2015) 5. doi: 10.1038/srep08879
Malandrino A Mak M Kamm RD Moeendarbary E. Complex mechanics of the heterogeneous extracellular matrix in cancer. Extreme Mechanics Lett (2018) 21:25–34. doi: 10.1016/j.eml.2018.02.003
Zhuo S Chen J Wu G Xie S Zheng L Jiang X et al. Quantitatively linking collagen alteration and epithelial tumor progression by second harmonic generation microscopy. Appl Phys Lett (2010) 96:213704. doi: 10.1063/1.3441337
Hu W Zhao G Wang C Zhang J Fu L. Nonlinear optical microscopy for histology of fresh normal and cancerous pancreatic tissues. PloS One (2012) 7. doi: 10.1371/journal.pone.0037962
Del Amo C Olivares V Cóndor M Blanco A Santolaria J Asín J et al. Matrix architecture plays a pivotal role in 3d osteoblast migration: The effect of interstitial fluid flow. J Mech Behav Biomed Mater (2018) 83:52–62. doi: 10.1016/j.jmbbm.2018.04.007
Geraldo S Simon A Elkhatib N Louvard D Fetler L Vignjevic DM. Do cancer cells have distinct adhesions in 3d collagen matrices and in vivo? Eur J Cell Biol (2012) 91:930–7. doi: 10.1016/j.ejcb.2012.07.005
Primac I Maquoi E Blacher S Heljasvaara R Deun JV Smeland HY et al. Stromal integrin α11 regulates PDGFRβ signaling and promotes breast cancer progression. J Clin Invest (2019) 129:4609–28. doi: 10.1172/JCI125890
Emi N Friedmann T Yee JK. Pseudotype formation of murine leukemia virus with the g protein of vesicular stomatitis virus. J Virol (1991) 65:1202–7. doi: 10.1128/jvi.65.3.1202-1207.1991
Christiansen DL Huang EK Silver FH. Assembly of type i collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol (2000) 19:409–20. doi: 10.1016/S0945-053X(00)00089-5
Lai VK Frey CR Kerandi AM Lake SP Tranquillo RT Barocas VH. Microstructural and mechanical differences between digested collagen–fibrin co-gels and pure collagen and fibrin gels. Acta Biomater (2012) 8:4031–42. doi: 10.1016/j.actbio.2012.07.010
Hall MS Alisafaei F Ban E Feng X Hui C-Y Shenoy VB et al. Fibrous nonlinear elasticity enables positive mechanical feedback between cells and ECMs. Proc Nat Sci USA (2016) 113:14043–8. doi: 10.1073/pnas.1613058113
Yang Y-l Motte S Kaufman LJ. Pore size variable type i collagen gels and their interaction with glioma cells. Biomaterials (2010) 31:5678–88. doi: 10.1016/j.biomaterials.2010.03.039
Serra J. Image analysis and mathematical morphology Vol. 1. London: Academic Press (1982). Serra:1982.
Lantuéjoul C. Geostatistical simulations. Berlin: Springer (2002).
Torquato S. Random heterogeneous materials. New York: Springer (2002).
Jeulin D. Morphological models of random structures. Cham, Switzerland: Springer (2021).
Aubert A Jeulin D. Estimation of the influence of second- and third-order moments on random sets reconstructions. Patt Rec (2000) 33:1083–104. doi: 10.1016/S0031-3203(99)00166-1
Jiao Y Stillinger FH Torquato S. A superior descriptor of random textures and its predictive capacity. Proc Natl Acad Sci USA (2009) 106:17634–9. doi: 10.1073/pnas.0905919106
Gommes CJ Jiao Y Torquato S. Microstructural degeneracy associated with a two-point correlation function and its information content. Phys Rev E (2012) 85. doi: 10.1103/PhysRevE.85.051140
Jeulin D. Random texture models for material structures. Stat Comput (2000) 10:121–32. doi: 10.1023/A:1008942325749
Gommes CJ. Stochastic models of disordered mesoporous materials for small-angle scattering analysis and more. Microp Mesop Mater (2018) 257:62–78. doi: 10.1016/j.micromeso.2017.08.009
Quiblier JA. A new three-dimensional modeling technique for studying porous media. J Coll Interf Sci (1984) 98:84–102. doi: 10.1016/0021-9797(84)90481-8
Berk N. Scattering properties of a model bicontinuous structure with a well defined length scale. Phys Rev Lett (1987) 58:2718–21. doi: 10.1103/PhysRevLett.58.2718
Jiao Y Berman H Kiehl T Torquato S. Spatial organization and correlations of cell nuclei in brain tumors. PloS One (2011) 6. doi: 10.1371/journal.pone.0027323
Balcioglu HE van de Water B Danen EHJ. Tumor-induced remote ECM network orientation steers angiogenesis. Sci Rep (2016) 6:22580. doi: 10.1038/srep22580
Kopanska KS Alcheikh Y Staneva R Vignjevic D Betz T. Tensile forces originating from cancer spheroids facilitate tumor invasion. PloS One (2016) 11:e0156442. doi: 10.1371/journal.pone.0156442
Piotrowski-Daspit AS Nerger BA Wolf AE Sundaresan S Nelson CM. Dynamics of tissue-induced alignment of fibrous extracellular matrix. Biophys J (2017) 113:702–13. doi: 10.1016/j.bpj.2017.06.046
Winkler J Abisoye-Ogunniyan A Metcalf KJ Werb Z. Concepts of extracellular matrix remodelling in tumour progression and metastasis. Nat Commun (2020) 11:5120. doi: 10.1038/s41467-020-18794-x
Doyle AD Sykora DJ Pacheco GG Kutys ML Yamada KM. 3d mesenchymal cell migration is driven by anterior cellular contraction that generates an extracellular matrix prestrain. Dev Cell (2021) 56:826–841.e4. doi: 10.1016/j.devcel.2021.02.017
Chen Y-Q Kuo J-C Wei M-T Chen Y-C Yang M-H Chiou A. Early stage mechanical remodeling of collagen surrounding head and neck squamous cell carcinoma spheroids correlates strongly with their invasion capability. Acta Biomater (2019) 84:280–92. doi: 10.1016/j.actbio.2018.11.046
Gullberg D Tingström A Thuresson A-C Olsson L Terracio L Borg TK et al. β1 integrin-mediated collagen gel contraction is stimulated by PDGF. Exp Cell Res (1990) 186:264–72. doi: 10.1016/0014-4827(90)90305-T
Reyhani V Tsioumpekou M van Wieringen T Rask L Lennartsson J Rubin K. PDGF-BB enhances collagen gel contraction through a PI3K-PLCγ-PKC-cofilin pathway. Sci Rep (2017) 7:8924. doi: 10.1038/s41598-017-08411-1
SenGupta S Parent CA Bear JE. The principles of directed cell migration. Nat Rev Mol Cell Biol (2021) 22:529–47. doi: 10.1038/s41580-021-00366-6
Lo C-M Wang H-B Dembo M li Wang Y. Cell movement is guided by the rigidity of the substrate. Biophys J (2000) 79:144–52. doi: 10.1016/S0006-3495(00)76279-5
DuChez BJ Doyle AD Dimitriadis EK Yamada KM. Durotaxis by human cancer cells. Biophys J (2019) 116:670–83. doi: 10.1016/j.bpj.2019.01.009
Artym VV Swatkoski S Matsumoto K Campbell CB Petrie RJ Dimitriadis EK et al. Dense fibrillar collagen is a potent inducer of invadopodia via a specific signaling network. J Cell Biol (2015) 208:331–50. doi: 10.1083/jcb.201405099
Jawerth LM Münster S Vader DA Fabry B Weitz DA. A blind spot in confocal reflection microscopy: The dependence of fiber brightness on fiber orientation in imaging biopolymer networks. Biophys J (2010) 98:L1–3. doi: 10.1016/j.bpj.2009.09.065
Similar publications
Sorry the service is unavailable at the moment. Please try again later.
This website uses cookies to improve user experience. Read more
Save & Close
Accept all
Decline all
Show detailsHide details
Cookie declaration
About cookies
Strictly necessary
Performance
Strictly necessary cookies allow core website functionality such as user login and account management. The website cannot be used properly without strictly necessary cookies.
This cookie is used by Cookie-Script.com service to remember visitor cookie consent preferences. It is necessary for Cookie-Script.com cookie banner to work properly.
Performance cookies are used to see how visitors use the website, eg. analytics cookies. Those cookies cannot be used to directly identify a certain visitor.
Used to store the attribution information, the referrer initially used to visit the website
Cookies are small text files that are placed on your computer by websites that you visit. Websites use cookies to help users navigate efficiently and perform certain functions. Cookies that are required for the website to operate properly are allowed to be set without your permission. All other cookies need to be approved before they can be set in the browser.
You can change your consent to cookie usage at any time on our Privacy Policy page.
