Macromolecular gelatin properties affect fibrin microarchitecture and tumor spheroid behavior in fibrin-gelatin gels

Dubbin, Karen; Robertson, Claire; Hinckley, Aubree; Alvarado, Javier A.; Gilmore, Sean F.; Hynes, William F.; Wheeler, Elizabeth K.; Moya, Monica L.

doi:10.1016/j.biomaterials.2020.120035

Title: Macromolecular gelatin properties affect fibrin microarchitecture and tumor spheroid behavior in fibrin-gelatin gels

Journal Article · Tue Apr 14 00:00:00 EDT 2020 · Biomaterials

DOI:https://doi.org/10.1016/j.biomaterials.2020.120035· OSTI ID:1650420

Dubbin, Karen ^[1]; Robertson, Claire ^[1]; Hinckley, Aubree ^[1]; Alvarado, Javier A. ^[1]; Gilmore, Sean F. ^[1]; Hynes, William F. ^[1]; Wheeler, Elizabeth K. ^[1]; Moya, Monica L. ^[1]

Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

The biophysical properties of extracellular matrices (ECM) are known to regulate cell behavior, however decoupling cell behavior changes due to the relative contributions of material microstructure versus biomechanics or nutrient permeability remains challenging, especially within complex, multi-material matrices. We developed four gelatin-fibrin interpenetrating network (IPN) formulations which are identical in composition but possess variable gelatin molecular weight distributions, and display differences in microstructure, biomechanics, and diffusivity. In this work we interrogate the response of multicellular tumor spheroids to these IPN formulations and found that a high stiffness, gelatin-network dominated IPNs impeded remodeling and invasion of multicellular tumor spheroids; whereas relatively lower stiffness, fibrin-network dominated IPNs permitted protease-dependent remodeling and spheroid invasion. Cell proliferation correlated to nutrient diffusivity across tested IPN formulations. These findings demonstrate the complexity of ECM IPNs, relative to single polymer matrices, and highlight that cell response does not derive from a single aspect of the ECM, but rather from the interplay of multiple biomechanical properties. The methodology developed in this study represents a framework for future studies which aim to characterize cellular phenotypic responses to biophysical cues present within complex, multi-material matrices.

View Accepted Manuscript (DOE)

View Accepted Manuscript (Publisher)

Cite

Export

Save

Research Organization:: Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Laboratory Directed Research and Development (LDRD) Program

Grant/Contract Number:: AC52-07NA27344; LDRD-19-SI-003; LDRD-18-ERD-062

OSTI ID:: 1650420

Alternate ID(s):: OSTI ID: 1692052

Report Number(s):: LLNL-JRNL-800043; 1003406

Journal Information:: Biomaterials, Vol. 250, Issue na; ISSN 0142-9612

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 2 works

Citation information provided by
Web of Science

References (77)

Quantitative extracellular matrix proteomics to study mammary and liver tissue microenvironments Goddard, Erica T.; Hill, Ryan C.; Barrett, Alexander The International Journal of Biochemistry & Cell Biology, Vol. 81 https://doi.org/10.1016/j.biocel.2016.10.014	journal	December 2016
How does the extracellular matrix direct gene expression? Bissell, Mina J.; Hall, H. Glenn; Parry, Gordon Journal of Theoretical Biology, Vol. 99, Issue 1 https://doi.org/10.1016/0022-5193(82)90388-5	journal	November 1982
Targeting ECM Disrupts Cancer Progression Venning, Freja A.; Wullkopf, Lena; Erler, Janine T. Frontiers in Oncology, Vol. 5 https://doi.org/10.3389/fonc.2015.00224	journal	October 2015
A synthetic modular approach for modeling the role of the 3D microenvironment in tumor progression Singh, S. P.; Schwartz, M. P.; Tokuda, E. Y. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep17814	journal	December 2015
Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression Bissell, Mina J.; Hines, William C. Nature Medicine, Vol. 17, Issue 3 https://doi.org/10.1038/nm.2328	journal	March 2011
Deconstructing the third dimension – how 3D culture microenvironments alter cellular cues Baker, Brendon M.; Chen, Christopher S. Journal of Cell Science, Vol. 125, Issue 13 https://doi.org/10.1242/jcs.079509	journal	July 2012
Diffusion and Convection in Collagen Gels: Implications for Transport in the Tumor Interstitium Ramanujan, Saroja; Pluen, Alain; McKee, Trevor D. Biophysical Journal, Vol. 83, Issue 3 https://doi.org/10.1016/S0006-3495(02)73933-7	journal	September 2002
Diffusion Anisotropy in Collagen Gels and Tumors: The Effect of Fiber Network Orientation Stylianopoulos, Triantafyllos; Diop-Frimpong, Benjamin; Munn, Lance L. Biophysical Journal, Vol. 99, Issue 10 https://doi.org/10.1016/j.bpj.2010.08.065	journal	November 2010
Biophysical control of invasive tumor cell behavior by extracellular matrix microarchitecture Carey, Shawn P.; Kraning-Rush, Casey M.; Williams, Rebecca M. Biomaterials, Vol. 33, Issue 16 https://doi.org/10.1016/j.biomaterials.2012.02.029	journal	June 2012
Quantitative Analysis of the Effect of Cancer Invasiveness and Collagen Concentration on 3D Matrix Remodeling Harjanto, Dewi; Maffei, Joseph S.; Zaman, Muhammad H. PLoS ONE, Vol. 6, Issue 9 https://doi.org/10.1371/journal.pone.0024891	journal	September 2011
Controlling matrix stiffness and topography for the study of tumor cell migration Kraning-Rush, Casey M.; Reinhart-King, Cynthia A. Cell Adhesion & Migration, Vol. 6, Issue 3 https://doi.org/10.4161/cam.21076	journal	May 2012
Force Matters: Biomechanical Regulation of Cell Invasion and Migration in Disease Kai, FuiBoon; Laklai, Hanane; Weaver, Valerie M. Trends in Cell Biology, Vol. 26, Issue 7 https://doi.org/10.1016/j.tcb.2016.03.007	journal	July 2016
Decoupling the effects of stiffness and fiber density on cellular behaviors via an interpenetrating network of gelatin-methacrylate and collagen Berger, Anthony J.; Linsmeier, Kelsey M.; Kreeger, Pamela K. Biomaterials, Vol. 141 https://doi.org/10.1016/j.biomaterials.2017.06.039	journal	October 2017
Predicting bulk mechanical properties of cellularized collagen gels using multiphoton microscopy Raub, C. B.; Putnam, A. J.; Tromberg, B. J. Acta Biomaterialia, Vol. 6, Issue 12 https://doi.org/10.1016/j.actbio.2010.07.004	journal	December 2010
Noninvasive Assessment of Collagen Gel Microstructure and Mechanics Using Multiphoton Microscopy Raub, Christopher B.; Suresh, Vinod; Krasieva, Tatiana Biophysical Journal, Vol. 92, Issue 6 https://doi.org/10.1529/biophysj.106.097998	journal	March 2007
The microstructure of laminin-111 compensates for dystroglycan loss in mammary epithelial cells in downstream expression of milk proteins Kent, A. J.; Mayer, N.; Inman, J. L. Biomaterials, Vol. 218 https://doi.org/10.1016/j.biomaterials.2019.119337	journal	October 2019
Buffers Strongly Modulate Fibrin Self-Assembly into Fibrous Networks Kurniawan, Nicholas A.; van Kempen, Thomas H. S.; Sonneveld, Stijn Langmuir, Vol. 33, Issue 25 https://doi.org/10.1021/acs.langmuir.7b00527	journal	June 2017
Superfibronectin is a functionally distinct form of fibronectin Morla, Alex; Zhang, Zhuohua; Ruoslahti, Erkki Nature, Vol. 367, Issue 6459 https://doi.org/10.1038/367193a0	journal	January 1994
Overview of the Matrisome--An Inventory of Extracellular Matrix Constituents and Functions Hynes, R. O.; Naba, A. Cold Spring Harbor Perspectives in Biology, Vol. 4, Issue 1 https://doi.org/10.1101/cshperspect.a004903	journal	September 2011
Interpenetrating Collagen-Fibrin Composite Matrices with Varying Protein Contents and Ratios Rowe, Shaneen L.; Stegemann, Jan P. Biomacromolecules, Vol. 7, Issue 11 https://doi.org/10.1021/bm0602233	journal	November 2006
Properties of engineered vascular constructs made from collagen, fibrin, and collagen–fibrin mixtures Cummings, Christopher L.; Gawlitta, Debby; Nerem, Robert M. Biomaterials, Vol. 25, Issue 17 https://doi.org/10.1016/j.biomaterials.2003.10.073	journal	August 2004
Extracellular matrix stiffness and composition jointly regulate the induction of malignant phenotypes in mammary epithelium Chaudhuri, Ovijit; Koshy, Sandeep T.; Branco da Cunha, Cristiana Nature Materials, Vol. 13, Issue 10 https://doi.org/10.1038/nmat4009	journal	June 2014
A cell-instructive hydrogel to regulate malignancy of 3D tumor spheroids with matrix rigidity Liang, Youyun; Jeong, Jaehyun; DeVolder, Ross J. Biomaterials, Vol. 32, Issue 35 https://doi.org/10.1016/j.biomaterials.2011.08.045	journal	December 2011
Probing cellular mechanobiology in three-dimensional culture with collagen–agarose matrices Ulrich, Theresa A.; Jain, Amit; Tanner, Kandice Biomaterials, Vol. 31, Issue 7 https://doi.org/10.1016/j.biomaterials.2009.10.047	journal	March 2010
Magnitude and presentation of mechanical signals influence adult stem cell behavior in 3-dimensional macroporous hydrogels Marklein, Ross A.; Soranno, Danielle E.; Burdick, Jason A. Soft Matter, Vol. 8, Issue 31 https://doi.org/10.1039/c2sm25501d	journal	January 2012
Heparin-hyaluronic acid hydrogel in support of cellular activities of 3D encapsulated adipose derived stem cells Gwon, Kihak; Kim, Eunsol; Tae, Giyoong Acta Biomaterialia, Vol. 49 https://doi.org/10.1016/j.actbio.2016.12.001	journal	February 2017
Tuning three-dimensional collagen matrix stiffness independently of collagen concentration modulates endothelial cell behavior Mason, Brooke N.; Starchenko, Alina; Williams, Rebecca M. Acta Biomaterialia, Vol. 9, Issue 1 https://doi.org/10.1016/j.actbio.2012.08.007	journal	January 2013
Microstructural and mechanical differences between digested collagen–fibrin co-gels and pure collagen and fibrin gels Lai, Victor K.; Frey, Christina R.; Kerandi, Allan M. Acta Biomaterialia, Vol. 8, Issue 11 https://doi.org/10.1016/j.actbio.2012.07.010	journal	November 2012
Swelling of Collagen-Hyaluronic Acid Co-Gels: An In Vitro Residual Stress Model Lai, Victor K.; Nedrelow, David S.; Lake, Spencer P. Annals of Biomedical Engineering, Vol. 44, Issue 10 https://doi.org/10.1007/s10439-016-1636-0	journal	May 2016
Long-term stable fibrin gels for cartilage engineering Eyrich, Daniela; Brandl, Ferdinand; Appel, Bernhard Biomaterials, Vol. 28, Issue 1 https://doi.org/10.1016/j.biomaterials.2006.08.027	journal	January 2007
Fibrin: A Versatile Scaffold for Tissue Engineering Applications Ahmed, Tamer A. E.; Dare, Emma V.; Hincke, Max Tissue Engineering Part B: Reviews, Vol. 14, Issue 2 https://doi.org/10.1089/ten.teb.2007.0435	journal	June 2008
A fibrinogen-based precision microporous scaffold for tissue engineering Linnes, Michael P.; Ratner, Buddy D.; Giachelli, Cecilia M. Biomaterials, Vol. 28, Issue 35 https://doi.org/10.1016/j.biomaterials.2007.08.020	journal	December 2007
Hydrogels for Tissue Engineering Lee, Kuen Yong; Mooney, David J. Chemical Reviews, Vol. 101, Issue 7 https://doi.org/10.1021/cr000108x	journal	July 2001
Gelatin-Based Materials in Ocular Tissue Engineering Rose, James; Pacelli, Settimio; Haj, Alicia Materials, Vol. 7, Issue 4 https://doi.org/10.3390/ma7043106	journal	April 2014
Collagen Structure and Stability Shoulders, Matthew D.; Raines, Ronald T. Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.77.032207.120833	journal	June 2009
Three-dimensional bioprinting of thick vascularized tissues Kolesky, David B.; Homan, Kimberly A.; Skylar-Scott, Mark A. Proceedings of the National Academy of Sciences, Vol. 113, Issue 12 https://doi.org/10.1073/pnas.1521342113	journal	March 2016
Plasma fibrin D-dimer levels correlate with tumour volume, progression rate and survival in patients with metastatic breast cancer Dirix, L. Y.; Salgado, R.; Weytjens, R. British Journal of Cancer, Vol. 86, Issue 3 https://doi.org/10.1038/sj.bjc.6600069	journal	February 2002
Study of the degradation of gelatin in paper upon aging using aqueous size-exclusion chromatography Dupont, Anne-Laurence Journal of Chromatography A, Vol. 950, Issue 1-2 https://doi.org/10.1016/S0021-9673(02)00010-9	journal	March 2002
Multiscale analysis of collagen microstructure with generalized image correlation spectroscopy and the detection of tissue prestress Robertson, Claire; Ikemura, Kenji; Krasieva, Tatiana B. Biomaterials, Vol. 34, Issue 26 https://doi.org/10.1016/j.biomaterials.2013.04.019	journal	August 2013
Turbidimetric studies of the in vitro assembly and disassembly of porcine neurotubules Gaskin, Felicia; Cantor, Charles R.; Shelanski, Michael L. Journal of Molecular Biology, Vol. 89, Issue 4 https://doi.org/10.1016/0022-2836(74)90048-5	journal	November 1974
A Method Improving the Accuracy of Fluorescence Recovery after Photobleaching Analysis Jönsson, Peter; Jonsson, Magnus P.; Tegenfeldt, Jonas O. Biophysical Journal, Vol. 95, Issue 11 https://doi.org/10.1529/biophysj.108.134874	journal	December 2008
INSIDIA: A FIJI Macro Delivering High‐Throughput and High‐Content Spheroid Invasion Analysis Moriconi, Chiara; Palmieri, Valentina; Di Santo, Riccardo Biotechnology Journal, Vol. 12, Issue 10 https://doi.org/10.1002/biot.201700140	journal	September 2017
TASI: A software tool for spatial-temporal quantification of tumor spheroid dynamics Hou, Yue; Konen, Jessica; Brat, Daniel J. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-25337-4	journal	May 2018
IGF2 and cancer Livingstone, Callum Endocrine-Related Cancer, Vol. 20, Issue 6 https://doi.org/10.1530/ERC-13-0231	journal	September 2013
A Multiscale Model for Solute Diffusion in Hydrogels Axpe, Eneko; Chan, Doreen; Offeddu, Giovanni S. Macromolecules, Vol. 52, Issue 18 https://doi.org/10.1021/acs.macromol.9b00753	journal	August 2019
A spectrophotometer-based diffusivity assay reveals that diffusion hindrance of small molecules in extracellular matrix gels used in 3D cultures is dominated by viscous effects Galgoczy, Roland; Pastor, Isabel; Colom, Adai Colloids and Surfaces B: Biointerfaces, Vol. 120 https://doi.org/10.1016/j.colsurfb.2014.05.017	journal	August 2014
Nonlinear simulation of the effect of microenvironment on tumor growth Macklin, Paul; Lowengrub, John Journal of Theoretical Biology, Vol. 245, Issue 4 https://doi.org/10.1016/j.jtbi.2006.12.004	journal	April 2007
Soft fibrin gels promote selection and growth of tumorigenic cells Liu, Jing; Tan, Youhua; Zhang, Huafeng Nature Materials, Vol. 11, Issue 8 https://doi.org/10.1038/nmat3361	journal	July 2012
The extracellular matrix in breast cancer predicts prognosis through composition, splicing, and crosslinking Robertson, Claire Experimental Cell Research, Vol. 343, Issue 1 https://doi.org/10.1016/j.yexcr.2015.11.009	journal	April 2016
A guide to mechanobiology: Where biology and physics meet Jansen, Karin A.; Donato, Dominique M.; Balcioglu, Hayri E. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 11 https://doi.org/10.1016/j.bbamcr.2015.05.007	journal	November 2015
Tensional homeostasis and the malignant phenotype Paszek, Matthew J.; Zahir, Nastaran; Johnson, Kandice R. Cancer Cell, Vol. 8, Issue 3 https://doi.org/10.1016/j.ccr.2005.08.010	journal	September 2005
3D collagen architecture induces a conserved migratory and transcriptional response linked to vasculogenic mimicry Velez, D. O.; Tsui, B.; Goshia, T. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01556-7	journal	November 2017
Macromolecular crowding tunes 3D collagen architecture and cell morphogenesis Ranamukhaarachchi, S. K.; Modi, R. N.; Han, A. Biomaterials Science, Vol. 7, Issue 2 https://doi.org/10.1039/C8BM01188E	journal	January 2019
Multicellular spheroids as an in vitro tumor model Hamilton, Gerhard Cancer Letters, Vol. 131, Issue 1 https://doi.org/10.1016/S0304-3835(98)00198-0	journal	September 1998
In vitro three-dimensional (3D) models in cancer research: An update Kimlin, Lauren C.; Casagrande, Giovanna; Virador, Victoria M. Molecular Carcinogenesis, Vol. 52, Issue 3 https://doi.org/10.1002/mc.21844	journal	December 2011
The Mechanics of Single Cell and Collective Migration of Tumor Cells Lintz, Marianne; Muñoz, Adam; Reinhart-King, Cynthia A. Journal of Biomechanical Engineering, Vol. 139, Issue 2 https://doi.org/10.1115/1.4035121	journal	January 2017
ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium Nguyen-Ngoc, K. -V.; Cheung, K. J.; Brenot, A. Proceedings of the National Academy of Sciences, Vol. 109, Issue 39 https://doi.org/10.1073/pnas.1212834109	journal	August 2012
Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion Wolf, Katarina; Wu, Yi I.; Liu, Yueying Nature Cell Biology, Vol. 9, Issue 8 https://doi.org/10.1038/ncb1616	journal	July 2007
3D tumor spheroids as in vitro models to mimic in vivo human solid tumors resistance to therapeutic drugs: NUNES et al. Nunes, Ana S.; Barros, Andreia S.; Costa, Elisabete C. Biotechnology and Bioengineering, Vol. 116, Issue 1 https://doi.org/10.1002/bit.26845	journal	October 2018
Immunocompetent mouse allograft models for development of therapies to target breast cancer metastasis Yang, Yuan; Yang, Howard H.; Hu, Ying Oncotarget, Vol. 8, Issue 19 https://doi.org/10.18632/oncotarget.15695	journal	February 2017
Classifying collective cancer cell invasion Friedl, Peter; Locker, Joseph; Sahai, Erik Nature Cell Biology, Vol. 14, Issue 8 https://doi.org/10.1038/ncb2548	journal	August 2012
Twist1-induced dissemination preserves epithelial identity and requires E-cadherin Shamir, Eliah R.; Pappalardo, Elisa; Jorgens, Danielle M. Journal of Cell Biology, Vol. 204, Issue 5 https://doi.org/10.1083/jcb.201306088	journal	March 2014
Aligned Collagen Is a Prognostic Signature for Survival in Human Breast Carcinoma Conklin, Matthew W.; Eickhoff, Jens C.; Riching, Kristin M. The American Journal of Pathology, Vol. 178, Issue 3 https://doi.org/10.1016/j.ajpath.2010.11.076	journal	March 2011
Collective cell migration over long time scales reveals distinct phenotypes Lee, R. M.; Stuelten, C. H.; Parent, C. A. Convergent Science Physical Oncology, Vol. 2, Issue 2 https://doi.org/10.1088/2057-1739/2/2/025001	journal	May 2016
Membrane Type I Matrix Metalloproteinase Usurps Tumor Growth Control Imposed by the Three-Dimensional Extracellular Matrix Hotary, Kevin B.; Allen, Edward D.; Brooks, Peter C. Cell, Vol. 114, Issue 1 https://doi.org/10.1016/S0092-8674(03)00513-0	journal	July 2003
Mechanisms of 3D cell migration Yamada, Kenneth M.; Sixt, Michael Nature Reviews Molecular Cell Biology, Vol. 20, Issue 12 https://doi.org/10.1038/s41580-019-0172-9	journal	October 2019
Hindered transport of large molecules in liquid-filled pores Deen, W. M. AIChE Journal, Vol. 33, Issue 9, p. 1409-1425 https://doi.org/10.1002/aic.690330902	journal	September 1987
A numerical calculation of the hydraulic permeability of three-dimensional disordered fibrous media Clague, David S.; Phillips, Ronald J. Physics of Fluids, Vol. 9, Issue 6 https://doi.org/10.1063/1.869278	journal	June 1997
Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis Zaman, M. H.; Trapani, L. M.; Sieminski, A. L. Proceedings of the National Academy of Sciences, Vol. 103, Issue 29 https://doi.org/10.1073/pnas.0604460103	journal	July 2006
Microarchitecture of Three-Dimensional Scaffolds Influences Cell Migration Behavior via Junction Interactions Harley, Brendan A. C.; Kim, Hyung-Do; Zaman, Muhammad H. Biophysical Journal, Vol. 95, Issue 8 https://doi.org/10.1529/biophysj.107.122598	journal	October 2008
Independent regulation of tumor cell migration by matrix stiffness and confinement Pathak, A.; Kumar, S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 26 https://doi.org/10.1073/pnas.1118073109	journal	June 2012
Marrow-Derived stem cell motility in 3D synthetic scaffold is governed by geometry along with adhesivity and stiffness Peyton, Shelly R.; Kalcioglu, Z. Ilke; Cohen, Joshua C. Biotechnology and Bioengineering, Vol. 108, Issue 5 https://doi.org/10.1002/bit.23027	journal	January 2011
Impact of the biophysical features of a 3D gelatin microenvironment on glioblastoma malignancy: GBM Cell Malignancy in 3D Microenvironments Pedron, S.; Harley, B. A. C. Journal of Biomedical Materials Research Part A, Vol. 101, Issue 12 https://doi.org/10.1002/jbm.a.34637	journal	April 2013
Hypoxia Induces a HIF-1-Dependent Transition from Collective-to-Amoeboid Dissemination in Epithelial Cancer Cells Lehmann, Steffi; te Boekhorst, Veronika; Odenthal, Julia Current Biology, Vol. 27, Issue 3 https://doi.org/10.1016/j.cub.2016.11.057	journal	February 2017
Overview of natural hydrogels for regenerative medicine applications Catoira, Marta Calvo; Fusaro, Luca; Di Francesco, Dalila Journal of Materials Science: Materials in Medicine, Vol. 30, Issue 10 https://doi.org/10.1007/s10856-019-6318-7	journal	October 2019
Functional Augmentation of Naturally-Derived Materials for Tissue Regeneration Allen, Ashley B.; Priddy, Lauren B.; Li, Mon-Tzu A. Annals of Biomedical Engineering, Vol. 43, Issue 3 https://doi.org/10.1007/s10439-014-1192-4	journal	November 2014
Natural–origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications Malafaya, Patrícia B.; Silva, Gabriela A.; Reis, Rui L. Advanced Drug Delivery Reviews, Vol. 59, Issue 4-5 https://doi.org/10.1016/j.addr.2007.03.012	journal	May 2007

Similar Records

The TLR4 agonist fibronectin extra domain A is cryptic, exposed by elastase-2; use in a fibrin matrix cancer vaccine

Journal Article · Tue Feb 24 00:00:00 EST 2015 · Scientific Reports · OSTI ID:1650420

Julier, Ziad; Martino, Mikaël M.; de Titta, Alexandre; +2 more

Wnt11 alters integrin and cadherin expression by ovarian cancer spheroids and inhibits tumorigenesis and metastasis

Journal Article · Wed Aug 15 00:00:00 EDT 2018 · Experimental Cell Research · OSTI ID:1650420

Azimian-Zavareh, Vajihe; Hossein, Ghamartaj; Ebrahimi, Marzieh; +1 more

An extracellular matrix (ECM) model at high malignant colorectal tumor increases chondroitin sulfate chains to promote epithelial-mesenchymal transition and chemoresistance acquisition

Journal Article · Sat Sep 15 00:00:00 EDT 2018 · Experimental Cell Research · OSTI ID:1650420

Hoshiba, Takashi

Related Subjects

36 MATERIALS SCIENCE
Hydrogel
Fibrin
Collagen
Extracellular matrices
Microstructure
Tumors

Title: Macromolecular gelatin properties affect fibrin microarchitecture and tumor spheroid behavior in fibrin-gelatin gels

Citation Formats

References (77)

Similar Records

Related Subjects