Gelatine Methacrylamide-Based Hydrogels: An Alternative Three-Dimensional Cancer Cell Culture System

Kaemmerer, Elke; Melchels, Ferry P.W.; Holzapfel, Boris M.; Meckel, Tobias; Hutmacher, Dietmar W.; Loessner, Daniela

doi:10.1016/j.actbio.2014.02.035

Cited by 219Hydrogels: synthesis, properties, applications3D Printing in Biomedical ResearchCellular Mechanics and Interactions

Gelatine Methacrylamide-Based Hydrogels: An Alternative Three-Dimensional Cancer Cell Culture System

Kaemmerer, Elke, Melchels, Ferry P.W., Holzapfel, Boris M., Meckel, Tobias, Hutmacher, Dietmar W., Loessner, Daniela·2014·Acta Biomaterialia

DOI 10.1016/j.actbio.2014.02.035

Open this paper in CoChat — free account

Abstract

Modern cancer research requires physiological, three-dimensional (3-D) cell culture platforms, wherein the physical and chemical characteristics of the extracellular matrix (ECM) can be modified. In this study, gelatine methacrylamide (GelMA)-based hydrogels were characterized and established as in vitro and in vivo spheroid-based models for ovarian cancer, reflecting the advanced disease stage of patients, with accumulation of multicellular spheroids in the tumour fluid (ascites). Polymer concentration (2.5-7% w/v) strongly influenced hydrogel stiffness (0.5±0.2kPa to 9.0±1.8kPa) but had little effect on solute diffusion. The diffusion coefficient of 70kDa fluorescein isothiocyanate (FITC)-labelled dextran in 7% GelMA-based hydrogels was only 2.3 times slower compared to water. Hydrogels of medium concentration (5% w/v GelMA) and stiffness (3.4kPa) allowed spheroid formation and high proliferation and metabolic rates. The inhibition of matrix metalloproteinases and consequently ECM degradability reduced spheroid formation and proliferation rates. The incorporation of the ECM components laminin-411 and hyaluronic acid further stimulated spheroid growth within GelMA-based hydrogels. The feasibility of pre-cultured GelMA-based hydrogels as spheroid carriers within an ovarian cancer animal model was proven and led to tumour development and metastasis. These tumours were sensitive to treatment with the anti-cancer drug paclitaxel, but not the integrin antagonist ATN-161. While paclitaxel and its combination with ATN-161 resulted in a treatment response of 33-37.8%, ATN-161 alone had no effect on tumour growth and peritoneal spread. The semi-synthetic biomaterial GelMA combines relevant natural cues with tunable properties, providing an alternative, bioengineered 3-D cancer cell culture in in vitro and in vivo model systems.

Integrity signals

Registry

Crossref · 10.1016/j.actbio.2014.02.035

Cites

74 of 74 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Addition of Laminin-411 and hyaluronic acid to GelMA hydrogels of 3.4 kPa stiffness enabled ovarian cancer spheroid formation, proliferation and chemoresistance to paclitaxel.
“Addition of Laminin-411 and hyaluronic acid to GelMA hydrogels of 3.4 kPa stiffness enabled ovarian cancer spheroid formation, proliferation and chemoresistance to paclitaxel (Kaemmerer et al., 2014).”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as Kaemmerer et al., 2014

Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Fabrication of novel biomaterials through molecular self-assembly
Zhang, S. (2003) · Nature Biotechnology · doi:10.1038/nbt874 · Cited by 3,353 · see citing works
The third dimension bridges the gap between cell culture and live tissue
Pampaloni, F., Reynaud, E. G., & Stelzer, E. H. K. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2236 · Cited by 2,817 · see citing works
Cell-laden microengineered gelatin methacrylate hydrogels
Nichol, J. W., Koshy, S. T., Bae, H., Hwang, C. M., Yamanlar, S., & Khademhosseini, A. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.03.064 · Cited by 2,377 · see citing works
Capturing complex 3D tissue physiology in vitro
Griffith, L. G., & Swartz, M. A. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1858 · Cited by 2,274 · see citing works
Determination of subcutaneous tumor size in athymic (nude) mice
Tomayko, M. M., & Reynolds, C. P. (1989) · Cancer Chemotherapy and Pharmacology · doi:10.1007/bf00300234 · Cited by 1,830 · see citing works
Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly.
Galis, Z. S., & Khatri, J. J. (2002) · PubMed · Cited by 1,787 · see citing works
Modeling Tissue Morphogenesis and Cancer in 3D
Yamada, K. M., & Cukierman, E. (2007) · Cell · doi:10.1016/j.cell.2007.08.006 · Cited by 1,751 · see citing works
Multicellular tumor spheroids: An underestimated tool is catching up again
Hirschhaeuser, F., Menne, H., Dittfeld, C., West, J., Mueller-Klieser, W., & Kunz-Schughart, L. A. (2010) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2010.01.012 · Cited by 1,674 · see citing works
Matrigel: Basement membrane matrix with biological activity
Kleinman, H. K., & Martin, G. R. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.05.004 · Cited by 1,673 · see citing works
Matrix Metalloproteinases in Vascular Remodeling and Atherogenesis
Galis, Z. S., & Khatri, J. J. (2002) · Circulation Research · doi:10.1161/res.90.3.251 · Cited by 1,550 · see citing works
Structural and Rheological Properties of Methacrylamide Modified Gelatin Hydrogels
Van Den Bulcke, A. I., Bogdanov, B., De Rooze, N., Schacht, E. H., Cornelissen, M., & Berghmans, H. (2000) · Biomacromolecules · doi:10.1021/bm990017d · Cited by 1,536 · see citing works
The physics of cancer: the role of physical interactions and mechanical forces in metastasis
Wirtz, D., Κωνσταντόπουλος, Κ., & Searson, P. C. (2011) · Nature reviews. Cancer · doi:10.1038/nrc3080 · Cited by 1,349 · see citing works
Three-dimensional culture models of normal and malignant breast epithelial cells
Lee, G. Y., Kenny, P. A., Lee, E. H., & Bissell, M. J. (2007) · Nature Methods · doi:10.1038/nmeth1015 · Cited by 1,336 · see citing works
Cell Encapsulation in Biodegradable Hydrogels for Tissue Engineering Applications
Nicodemus, G. D., & Bryant, S. J. (2008) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2007.0332 · Cited by 1,242 · see citing works
Ovarian cancer: strategies for overcoming resistance to chemotherapy
Agarwal, R., & Kaye, S. B. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1123 · Cited by 1,155 · see citing works
Three-Dimensional Cell Culture Matrices: State of the Art
Lee, J., Cuddihy, M. J., & Kotov, N. A. (2008) · Tissue Engineering Part B: Reviews · doi:10.1089/teb.2007.0150 · Cited by 1,047 · see citing works
Biochemistry and Molecular Biology of Gelatinase B or Matrix Metalloproteinase-9 (MMP-9)
den Steen, P. E. V., Dubois, B., Nelissen, I., Rudd, P., Dwek, R., & Opdenakker, G. (2002) · Critical reviews in biochemistry and molecular biology · doi:10.1080/10409230290771546 · Cited by 948 · see citing works
Physical models of diffusion for polymer solutions, gels and solids
Masaro, L., & Zhu, X. X. (1999) · Progress in Polymer Science · doi:10.1016/s0079-6700(99)00016-7 · Cited by 913 · see citing works
Variable cytocompatibility of six cell lines with photoinitiators used for polymerizing hydrogels and cell encapsulation
Williams, C. G., Malik, A. N., Kim, T. K., Manson, P. N., & Elisseeff, J. H. (2004) · Biomaterials · doi:10.1016/j.biomaterials.2004.04.024 · Cited by 903 · see citing works
Gelatin‐Methacrylamide Hydrogels as Potential Biomaterials for Fabrication of Tissue‐Engineered Cartilage Constructs
Schuurman, W., Levett, P. A., Pot, M. W., van Weeren, P. R., Dhert, W. J. A., Hutmacher, D. W., Melchels, F. P. W., Klein, T. J., & Malda, J. (2013) · Macromolecular Bioscience · doi:10.1002/mabi.201200471 · Cited by 791 · see citing works
Self-citation
Growth factors and wound healing: Biochemical properties of growth factors and their receptors
Bennett, N. T., & Schultz, G. S. (1993) · The American Journal of Surgery · doi:10.1016/s0002-9610(05)80797-4 · Cited by 658 · see citing works
Bioengineered 3D platform to explore cell–ECM interactions and drug resistance of epithelial ovarian cancer cells
Loessner, D., Stok, K. S., Lutolf, M. P., Hutmacher, D. W., Clements, J. A., & Rizzi, S. C. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.07.064 · Cited by 602 · see citing works
Self-citation
Hydrogel Cell Cultures
Cushing, M. C., & Anseth, K. S. (2007) · Science · doi:10.1126/science.1140171 · Cited by 520 · see citing works
Soft fibrin gels promote selection and growth of tumorigenic cells
Liu, J., Tan, Y., Zhang, H., Zhang, Y., Xu, P., Chen, J., Poh, Y., Tang, K., Wang, N., & Huang, B. (2012) · Nature Materials · doi:10.1038/nmat3361 · Cited by 469 · see citing works
Cell migration in 3D matrix
Even‐Ram, S., & Yamada, K. M. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.08.015 · Cited by 466 · see citing works
Mechanisms of mechanical signaling in development and disease
Janmey, P. A., & Miller, R. T. (2010) · Journal of Cell Science · doi:10.1242/jcs.071001 · Cited by 462 · see citing works
Quantum dots spectrally distinguish multiple species within the tumor milieu in vivo
Stroh, M., Zimmer, J. P., Duda, D. G., Levchenko, T. S., Cohen, K. S., Brown, E. B., Scadden, D. T., Torchilin, V. P., Bawendi, M. G., Fukumura, D., et al. (2005) · Nature Medicine · doi:10.1038/nm1247 · Cited by 433 · see citing works
Multicellular spheroids in ovarian cancer metastases: Biology and pathology
Shield, K., Ackland, M. L., Ahmed, N., & Rice, G. E. (2009) · Gynecologic Oncology · doi:10.1016/j.ygyno.2008.11.032 · Cited by 412 · see citing works
Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells ‘feel’ outside and in?
Buxboim, A., Ivanovska, I. L., & Discher, D. E. (2010) · Journal of Cell Science · doi:10.1242/jcs.041186 · Cited by 401 · see citing works
The influence of the microenvironment on the malignant phenotype
Park, C. C., Bissell, M. J., & Barcellos-Hoff, M. H. (2000) · Molecular Medicine Today · doi:10.1016/s1357-4310(00)01756-1 · Cited by 398 · see citing works
Biological hydrogels as selective diffusion barriers
Lieleg, O., & Ribbeck, K. (2011) · Trends in Cell Biology · doi:10.1016/j.tcb.2011.06.002 · Cited by 387 · cited 2× · see citing works
“Diffusion into and within a hydrogel directly influences the local cell microenvironment that supplies cells with nutrients, oxygen, growth factors, as well as the effectiveness of drug treatment [29– 31, 33 , 59 ].”
Background
A biomimetic extracellular matrix for cartilage tissue engineering centered on photocurable gelatin, hyaluronic acid and chondroitin sulfate
Levett, P. A., Melchels, F. P. W., Schrobback, K., Hutmacher, D. W., Malda, J., & Klein, T. J. (2013) · Acta Biomaterialia · doi:10.1016/j.actbio.2013.10.005 · Cited by 379 · see citing works
Self-citation
Increased expression of matrix metalloproteinases (MMP)-2, MMP-9, and the urokinase-type plasminogen activator is associated with progression from benign to advanced ovarian cancer.
Schmalfeldt, B., Prechtel, D., Härting, K., Späthe, K., Rutke, S., Konik, E., Fridman, R., Berger, U., Schmitt, M., Kuhn, W. C., et al. (2001) · PubMed · Cited by 334 · see citing works
High levels of stromal hyaluronan predict poor disease outcome in epithelial ovarian cancer.
Anttila, M., Tammi, R., Tammi, M., Syrjänen, K. J., Saarikoski, S., & Kosma, V. (2000) · PubMed · Cited by 327 · see citing works
Biomaterials offer cancer research the third dimension
Hutmacher, D. W. (2010) · Nature Materials · doi:10.1038/nmat2619 · Cited by 324 · see citing works
Self-citation
Preparation and properties of fluorescein-labelled dextrans
de Belder, A. N., & Granath, K. A. (1973) · Carbohydrate Research · doi:10.1016/s0008-6215(00)81824-8 · Cited by 321 · see citing works
Cancer cell angiogenic capability is regulated by 3D culture and integrin engagement
Fischbach, C., Kong, H. J., Hsiong, S. X., Evangelista, M. B., Yuen, W. W., & Mooney, D. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808932106 · Cited by 312 · see citing works
Selective Filtering of Particles by the Extracellular Matrix: An Electrostatic Bandpass
Lieleg, O., Baumgärtel, R. M., & Bausch, A. R. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2009.07.009 · Cited by 304 · see citing works
3D in vitro bioengineered tumors based on collagen I hydrogels
Szot, C. S., Buchanan, C. F., Freeman, J. W., & Rylander, M. N. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.07.001 · Cited by 304 · see citing works
A three-dimensional microenvironment alters protein expression and chemosensitivity of epithelial ovarian cancer cells in vitro
Lee, J. M., Mhawech-Fauceglia, P. Y., Lee, N., Parsanian, L. C., Lin, Y. G., Gayther, S. A., & Lawrenson, K. (2013) · Laboratory Investigation · doi:10.1038/labinvest.2013.41 · Cited by 302 · see citing works
Three-Dimensional Fluorescence Recovery after Photobleaching with the Confocal Scanning Laser Microscope
Braeckmans, K., Peeters, L., Sanders, N. N., Smedt, S. C. D., & Demeester, J. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74649-9 · Cited by 291 · see citing works
Unraveling the microenvironmental influences on the normal mammary gland and breast cancer
Weigelt, B., & Bissell, M. J. (2008) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2008.03.013 · Cited by 274 · see citing works
Principles of Tissue Engineering
Akter, F. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-805361-4.00002-3 · Cited by 264 · see citing works
Can tissue engineering concepts advance tumor biology research?
Hutmacher, D. W., Loessner, D., Rizzi, S. C., Kaplan, D. L., Mooney, D. J., & Clements, J. A. (2010) · Trends in biotechnology · doi:10.1016/j.tibtech.2009.12.001 · Cited by 237 · see citing works
Self-citation
Cell-matrix adhesions in 3D
Harunaga, J. S., & Yamada, K. M. (2011) · Matrix Biology · doi:10.1016/j.matbio.2011.06.001 · Cited by 225 · see citing works
A non–RGD-based integrin binding peptide (ATN-161) blocks breast cancer growth and metastasis in vivo
Khalili, P., Arakelian, A., Chen, G., Plunkett, M. L., Beck, I., Parry, G. C., Doñate, F., Shaw, D. E., Mazar, A. P., & Rabbani, S. A. (2006) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-06-0100 · Cited by 203 · see citing works
Hyaluronan promotes the malignant phenotype
Toole, B. P. (2002) · Glycobiology · doi:10.1093/glycob/12.3.37r · Cited by 200 · see citing works
Phase 1 trial of the antiangiogenic peptide ATN-161 (Ac-PHSCN-NH2), a beta integrin antagonist, in patients with solid tumours
Cianfrocca, M. E., Kimmel, K. A., Gallo, J. M., Cardoso, T., Brown, M. M., Hudes, G. R., Lewis, N. L., Weiner, L. M., Lam, G. N., Brown, S., et al. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6603171 · Cited by 182 · see citing works
Matrix metalloproteinase 9 is a mediator of epidermal growth factor-dependent e-cadherin loss in ovarian carcinoma cells.
Cowden-Dahl, K., Symowicz, J., Ning, Y., Gutierrez, E. T., Fishman, D., Adley, B., Stack, M., & Hudson, L. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5046 · Cited by 182 · see citing works
β1-Integrin: A Potential Therapeutic Target in the Battle against Cancer Recurrence
Barkan, D., & Chambers, A. F. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-0642 · Cited by 181 · see citing works
MMP-2 functions as an early response protein in ovarian cancer metastasis
Kenny, H. A., & Lengyel, E. R. (2009) · Cell Cycle · doi:10.4161/cc.8.5.7703 · Cited by 149 · see citing works
Enhanced macromolecule diffusion deep in tumors after enzymatic digestion of extracellular matrix collagen and its associated proteoglycan decorin
Magzoub, M. M., Jin, S., & Verkman, A. S. (2007) · The FASEB Journal · doi:10.1096/fj.07-9150com · Cited by 143 · see citing works
Mechanotransduction from the ECM to the genome: Are the pieces now in place?
Gieni, R. S., & Hendzel, M. J. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21364 · Cited by 143 · see citing works
Solute diffusion in hydrogels.
Amsden, B. G. (1998) · Polymer Gels and Networks · doi:10.1016/s0966-7822(97)00012-9 · Cited by 141 · see citing works
Role of Integrin Receptors for Fibronectin, Collagen and Laminin in the Regulation of Ovarian Carcinoma Functions in Response to a Matrix Microenvironment
Ahmed, N., Riley, C. B., Rice, G. E., & Quinn, M. A. (2005) · Clinical & Experimental Metastasis · doi:10.1007/s10585-005-1262-y · Cited by 140 · see citing works
Overexpression of alpha4 chain-containing laminins in human glial tumors identified by gene microarray analysis.
Ljubimova, J. Y., Lakhter, A. J., Loksh, A., Yong, W. H., Riedinger, M. S., Miner, J. H., Sorokin, L. M., Ljubimov, A. V., & Black, K. L. (2001) · PubMed · Cited by 118 · see citing works
Transforming Growth Factor-β1, Transforming Growth Factor-β2, and Transforming Growth Factor-β3 Enhance Ovarian Cancer Metastatic Potential by Inducing a Smad3-Dependent Epithelial-to-Mesenchymal Transition
Do, T.-V., Kubba, L. A., Du, H., Sturgis, C. D., & Woodruff, T. K. (2008) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-07-0294 · Cited by 112 · see citing works
Role of CD44 in tumour progression and strategies for targeting
Negi, L. M. S., Talegaonkar, S., Jaggi, M., Ahmad, F. J., Iqbal, Z., & Khar, R. K. (2012) · Journal of drug targeting · doi:10.3109/1061186x.2012.702767 · Cited by 109 · see citing works
Global gene expression analysis of early response to chemotherapy treatment in ovarian cancer spheroids
L'Espérance, S., Bachvarova, M., Tetu, B., Mes-Masson, A.-M., & Bachvarov, D. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-99 · Cited by 108 · see citing works
Hydrogels for in vivo‐like three‐dimensional cellular studies
DeVolder, R. J., & Kong, H. (2012) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1174 · Cited by 102 · see citing works
A 3D model of ovarian cancer cell lines on peptide nanofiber scaffold to explore the cell–scaffold interaction and chemotherapeutic resistance of anticancer drugs
Yang, Z., & Zhao, X. (2011) · International Journal of Nanomedicine · doi:10.2147/ijn.s15279 · Cited by 96 · see citing works
The effect of hyaluronic acid incorporation on fibroblast spreading and proliferation within PEG-diacrylate based semi-interpenetrating networks
Kutty, J. K., Cho, E., Lee, J. S., Vyavahare, N. R., & Webb, K. (2007) · Biomaterials · doi:10.1016/j.biomaterials.2007.08.007 · Cited by 95 · see citing works
Human ovarian tumour cells can bind hyaluronic acid via membrane CD44: a possible step in peritoneal metastasis
Gardner, M. J., Catterall, J., Jones, L. M., & Turner, G. A. (1996) · Clinical & Experimental Metastasis · doi:10.1007/bf00123391 · Cited by 93 · see citing works
Straightforward FRAP for quantitative diffusion measurements with a laser scanning microscope
Deschout, H. G., Hagman, J., Fransson, S., Jonasson, J. K., Rudemo, M., Lorén, N., & Braeckmans, K. (2010) · Optics Express · doi:10.1364/oe.18.022886 · Cited by 86 · see citing works
Laminin-8 (α4β1γ1) is synthesized by lymphoid cells, promotes lymphocyte migration and costimulates T cell proliferation
Geberhiwot, T., Assefa, D., Kortesmaa, J., Ingerpuu, S., Pedraza, C., Wondimu, Z., Charo, J., Kiessling, R. W., Virtanen, I., Tryggvason, K., et al. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.2.423 · Cited by 68 · see citing works
Reticulated hyaluronan hydrogels: a model for examining cancer cell invasion in 3D
David, L., Dulong, V., Cerf, D. L., Chauzy, C., Norris, V., Delpech, B., LAMACZ, M., & Vannier, J. (2004) · Matrix Biology · doi:10.1016/j.matbio.2004.05.005 · Cited by 59 · see citing works
A bioengineered 3D ovarian cancer model for the assessment of peptidase–mediated enhancement of spheroid growth and intraperitoneal spread
Loessner, D., Rizzi, S. C., Stok, K. S., Führmann, T., Hollier, B. G., Magdolen, V., Hutmacher, D. W., & Clements, J. A. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.06.009 · Cited by 58 · see citing works
Self-citation
Growth of confined cancer spheroids: a combined experimental and mathematical modelling approach
Loessner, D., Flegg, J. A., Byrne, H. M., Clements, J. A., & Hutmacher, D. W. (2013) · Integrative Biology · doi:10.1039/c3ib20252f · Cited by 47 · see citing works
Self-citation
Increased levels of laminin in ascitic fluid of patients with ovarian cancer
Byers, L. J., Osborne, J. L., Carson, L. F., Carter, J. R., Haney, A. F., Weinberg, J. B., & Ramakrishnan, S. (1995) · Cancer Letters · doi:10.1016/0304-3835(94)03625-s · Cited by 29 · see citing works
MMPs in Ovarian Cancer as Therapeutic Targets
Karam, A., & Dorigo, O. (2012) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/187152012802650174 · Cited by 27 · see citing works
MATRIX EFFECTS
Hubbell, J. A. (2000) · Elsevier eBooks · doi:10.1016/b978-012436630-5/50024-6 · Cited by 12 · see citing works
Growth factors and ovarian cancer
Langdon, S. P., & Smyth, J. F. (1998) · Endocrine Related Cancer · doi:10.1677/erc.0.0050283 · Cited by 5 · see citing works
Macromol. Biosci. 1/2013
Mandal, B. B., Gil, E. S., Panilaitis, B., & Kaplan, D. L. (2013) · Macromolecular Bioscience · doi:10.1002/mabi.201370001 · Cited by 1 · see citing works

Flagged first, then by citations

1 of the 75 references couldn’t be matched to a known paper.

Sorted by citations

Synthesis, properties, and biomedical applications of gelatin methacryloyl (GelMA) hydrogels
Yue, K., Trujillo-de Santiago, G., Alvarez, M. M., Tamayol, A., Annabi, N., & Khademhosseini, A. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.08.045 · Cited by 3,146 · see citing works
“gelatin [14], or gelatin methacrylamide [15-18] in literature by different authors.”
BackgroundInfluential
Hydrogels for Biomedical Applications: Their Characteristics and the Mechanisms behind Them
Chai, Q., Jiao, Y., & Yu, X. (2017) · Gels · doi:10.3390/gels3010006 · Cited by 1,076 · see citing works
Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip
Zhang, Y. S., Arneri, A., Bersini, S., Shin, S.-R., Zhu, K., Goli-Malekabadi, Z., Aleman, J., Colosi, C., Busignani, F., Dell’Erba, V., et al. (2016) · Biomaterials · doi:10.1016/j.biomaterials.2016.09.003 · Cited by 957 · see citing works
Functionalization, preparation and use of cell-laden gelatin methacryloyl–based hydrogels as modular tissue culture platforms
Loessner, D., Meinert, C., Kaemmerer, E., Martine, L. C., Yue, K., Levett, P. A., Klein, T. J., Melchels, F. P. W., Khademhosseini, A., & Hutmacher, D. W. (2016) · Nature Protocols · doi:10.1038/nprot.2016.037 · Cited by 868 · see citing works
Self-citation
Hydrogels as Drug Delivery Systems: A Review of Current Characterization and Evaluation Techniques
Vigata, M., Meinert, C., Hutmacher, D. W., & Bock, N. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12121188 · Cited by 557 · see citing works
Self-citation
Gelatin methacryloyl and its hydrogels with an exceptional degree of controllability and batch-to-batch consistency
Zhu, M., Wang, Y., Ferracci, G., Zheng, J., Cho, N., & Lee, B. H. (2019) · Scientific Reports · doi:10.1038/s41598-019-42186-x · Cited by 488 · see citing works
Next-generation cancer organoids
LeSavage, B. L., Suhar, R. A., Broguière, N., Lütolf, M. P., & Heilshorn, S. C. (2021) · Nature Materials · doi:10.1038/s41563-021-01057-5 · Cited by 462 · see citing works
Gelatin-Methacryloyl (GelMA) Hydrogels with Defined Degree of Functionalization as a Versatile Toolkit for 3D Cell Culture and Extrusion Bioprinting
Pepelanova, I., Kruppa, K., Scheper, T. H., & Lavrentieva, A. V. (2018) · Bioengineering · doi:10.3390/bioengineering5030055 · Cited by 415 · see citing works
Hydrogels for tissue engineering and regenerative medicine
Hunt, J. A., Chen, R., van Veen, T., & Bryan, N. (2014) · Journal of Materials Chemistry B · doi:10.1039/c4tb00775a · Cited by 378 · see citing works
Nanoengineered Ionic–Covalent Entanglement (NICE) Bioinks for 3D Bioprinting
Chimene, D., Peak, C. W., Gentry, J. L., Carrow, J. K., Cross, L., Mondragón, E., Cardoso, G. B. C., Kaunas, R. R., & Gaharwar, A. K. (2018) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.7b19808 · Cited by 249 · see citing works
Structural analysis of photocrosslinkable methacryloyl-modified protein derivatives
Yue, K., Li, X., Schrobback, K., Sheikhi, A., Annabi, N., Leijten, J., Zhang, W., Zhang, Y. S., Hutmacher, D. W., Klein, T. J., et al. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.04.050 · Cited by 211 · see citing works
Self-citation
The Tumor-on-Chip: Recent Advances in the Development of Microfluidic Systems to Recapitulate the Physiology of Solid Tumors
Trujillo-de Santiago, G., Flores-Garza, B. G., Tavares-Negrete, J. A., Lara-Mayorga, I. M., González-Gamboa, I., Zhang, Y. S., Rojas-Martínez, A., Ortiz-López, R., & Álvarez, M. M. (2019) · Materials · doi:10.3390/ma12182945 · Cited by 184 · see citing works
“Several techniques also involve the use of semi-synthetic polymers, such as gelatin methacryloyl (GelMA) [166] based hydrogels [135,167], or self-assembling peptides, such as RADA16-I, Q11, and bQ13, that can form gels under specific conditions (e.”
Background
Click‐Crosslinked Injectable Gelatin Hydrogels
Koshy, S. T., Desai, R. M., Joly, P., Li, J., Bagrodia, R. K., Lewin, S. A., Joshi, N. S., & Mooney, D. J. (2016) · Advanced Healthcare Materials · doi:10.1002/adhm.201500757 · Cited by 173 · see citing works
Efficient and controllable synthesis of highly substituted gelatin methacrylamide for mechanically stiff hydrogels
Lee, B. H., Shirahama, H., Cho, N., & Tan, L. P. (2015) · RSC Advances · doi:10.1039/c5ra22028a · Cited by 170 · see citing works
Biohybrid methacrylated gelatin/polyacrylamide hydrogels for cartilage repair
Han, L., Xu, J., Lu, X., Gan, D., Wang, Z., Wang, K., Zhang, H., Yuan, H., & Weng, J. (2016) · Journal of Materials Chemistry B · doi:10.1039/c6tb02348g · Cited by 169 · see citing works
Microfluidic Spinning of Cell‐Responsive Grooved Microfibers
Shi, X., Ostrovidov, S., Zhao, Y., Liang, X., Kasuya, M., Kurihara, K., Nakajima, K., Bae, H., Wu, H., & Khademhosseini, A. (2015) · Advanced Functional Materials · doi:10.1002/adfm.201404531 · Cited by 163 · see citing works
Cranial Suture Regeneration Mitigates Skull and Neurocognitive Defects in Craniosynostosis
Yu, M., Ma, L., Yuan, Y., Ye, X., Montagne, A., He, J., Ho, T., Wu, Y., Zhao, Z., Maria, N. S. S., et al. (2021) · Cell · doi:10.1016/j.cell.2020.11.037 · Cited by 160 · see citing works
3D bioprinting: improving<i>in vitro</i>models of metastasis with heterogeneous tumor microenvironments
Albritton, J. L., & Miller, J. S. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.025049 · Cited by 154 · see citing works
Bioprinting of 3D breast epithelial spheroids for human cancer models
Swaminathan, S., Hamid, Q., Sun, W., & Clyne, A. M. (2019) · Biofabrication · doi:10.1088/1758-5090/aafc49 · Cited by 154 · see citing works
A three dimensional micropatterned tumor model for breast cancer cell migration studies
Peela, N., Sam, F. S., Christenson, W., Truong, D. D., Watson, A., Mouneimne, G., Ros, R., & Nikkhah, M. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.11.039 · Cited by 147 · see citing works
An engineered tumor-on-a-chip device with breast cancer–immune cell interactions for assessing T-cell recruitment
Aung, A., Kumar, V., Theprungsirikul, J., Davey, S. K., & Varghese, S. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-0342 · Cited by 146 · see citing works
Permeability mapping of gelatin methacryloyl hydrogels
Miri, A. K., Hosseinabadi, H. G., Çeçen, B., Hassan, S., & Zhang, Y. S. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.07.006 · Cited by 133 · see citing works
Designer Self‐Assembling Peptide Hydrogels to Engineer 3D Cell Microenvironments for Cell Constructs Formation and Precise Oncology Remodeling in Ovarian Cancer
Yang, Z., Xu, H., & Zhao, X. (2020) · Advanced Science · doi:10.1002/advs.201903718 · Cited by 120 · see citing works
Tumor microenvironment triple-responsive nanoparticles enable enhanced tumor penetration and synergetic chemo-photodynamic therapy
Shu, M., Tang, J., Chen, L., Zeng, Q., Li, C., Xiao, S., Jiang, Z., & Liu, J. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120574 · Cited by 118 · see citing works
Concise Review: Humanized Models of Tumor Immunology in the 21st Century: Convergence of Cancer Research and Tissue Engineering
Holzapfel, B. M., Wagner, F., Thibaudeau, L., Lévesque, J.-P., & Hutmacher, D. W. (2015) · Stem Cells · doi:10.1002/stem.1978 · Cited by 116 · see citing works
Self-citation
In Situ “Clickable” Zwitterionic Starch-Based Hydrogel for 3D Cell Encapsulation
Dong, D., Li, J., Cui, M., Wang, J., Zhou, Y., Luo, L., Wei, Y., Ye, L., Sun, H. C., & Yao, F. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5b12141 · Cited by 113 · see citing works
Engineering Hydrogels for the Development of Three-Dimensional In Vitro Models
Maji, S., & Lee, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052662 · Cited by 111 · see citing works
Polymer Hydrogels to Guide Organotypic and Organoid Cultures
Magno, V., Meinhardt, A., & Werner, C. (2020) · Advanced Functional Materials · doi:10.1002/adfm.202000097 · Cited by 106 · see citing works
Superabsorbent polymers: a state-of-art review on their classification, synthesis, physicochemical properties, and applications
Venkatachalam, D., & Subramanian, K. G. (2021) · Reviews in Chemical Engineering · doi:10.1515/revce-2020-0102 · Cited by 104 · see citing works
Three-dimensional printed multiphasic scaffolds with stratified cell-laden gelatin methacrylate hydrogels for biomimetic tendon-to-bone interface engineering
Cao, Y. L., Yang, S., Zhao, D., Li, Y., Cheong, S., Han, D., & Li, Q. (2020) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2020.01.004 · Cited by 98 · see citing works
In vivo therapeutic applications of cell spheroids
Ong, C. S., Zhou, X. J., Han, J., Huang, C., Nashed, A., Khatri, S., Mattson, G., Fukunishi, T., Zhang, H., & Hibino, N. (2018) · Biotechnology Advances · doi:10.1016/j.biotechadv.2018.02.003 · Cited by 94 · see citing works
Gelatin Methacryloyl (GelMA)-Based Biomaterial Inks: Process Science for 3D/4D Printing and Current Status
Das, S., Jegadeesan, J. T., & Basu, B. (2024) · Biomacromolecules · doi:10.1021/acs.biomac.3c01271 · Cited by 102 · see citing works
Synthesis and characterization of a photocrosslinkable chitosan–gelatin hydrogel aimed for tissue regeneration
Saraiva, S. M., Miguel, S. P., Ribeiro, M. P., Coutinho, P., & Correia, I. J. (2015) · RSC Advances · doi:10.1039/c5ra10638a · Cited by 94 · see citing works
Self-Assembling Peptides as Building Blocks of Functional Materials for Biomedical Applications
Fukunaga, K., Tsutsumi, H., & Mihara, H. (2018) · Bulletin of the Chemical Society of Japan · doi:10.1246/bcsj.20180293 · Cited by 92 · see citing works
Advanced biomaterials and microengineering technologies to recapitulate the stepwise process of cancer metastasis
Peela, N., Truong, D. D., Saini, H., Chu, H., Mashaghi, S., Ham, S. L., Singh, S. K., Tavana, H., Mosadegh, B., & Nikkhah, M. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.04.017 · Cited by 91 · see citing works
Development of a 3D Printed, Bioengineered Placenta Model to Evaluate the Role of Trophoblast Migration in Preeclampsia
Kuo, C., Eranki, A., Placone, J. K., Rhodes, K. R., Aranda‐Espinoza, H., Fernandes, R., Fisher, J. P., & Kim, P. C. W. (2016) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.6b00031 · Cited by 90 · see citing works
Deciphering the Molecular Mechanism of Water Interaction with Gelatin Methacryloyl Hydrogels: Role of Ionic Strength, pH, Drug Loading and Hydrogel Network Characteristics
Vigata, M., Meinert, C., Bock, N., Dargaville, B. L., & Hutmacher, D. W. (2021) · Biomedicines · doi:10.3390/biomedicines9050574 · Cited by 94 · see citing works
Self-citation
Engineering a biomimetic three-dimensional nanostructured bone model for breast cancer bone metastasis study
Zhu, W., Wang, M., Fu, Y., Castro, N. J., Fu, S. W., & Zhang, L. G. (2014) · Acta Biomaterialia · doi:10.1016/j.actbio.2014.12.008 · Cited by 85 · see citing works
Bioinspired Hydrogels to Engineer Cancer Microenvironments
Park, K. M., Lewis, D. M., & Gerecht, S. (2017) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071516-044619 · Cited by 83 · see citing works
An Overview of Hydrogel-Based Bioinks for 3D Bioprinting of Soft Tissues
Das, S., & Basu, B. (2019) · Journal of the Indian Institute of Science · doi:10.1007/s41745-019-00129-5 · Cited by 83 · see citing works
Integrated cancer tissue engineering models for precision medicine
Bregenzer, M. E., Horst, E. N., Mehta, P., Novak, C. M., Raghavan, S. A., Snyder, C. S., & Mehta, G. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216564 · Cited by 83 · see citing works
A 3D View of Colorectal Cancer Models in Predicting Therapeutic Responses and Resistance
Reidy, E., Leonard, N. A., Treacy, O., & Ryan, A. E. (2021) · Cancers · doi:10.3390/cancers13020227 · Cited by 81 · see citing works
Proteinaceous Hydrogels for Bioengineering Advanced 3D Tumor Models
Blanco‐Fernandez, B., Gaspar, V. M., Engel, E., & Mano, J. F. (2021) · Advanced Science · doi:10.1002/advs.202003129 · Cited by 78 · see citing works
Coaxial Extrusion of Tubular Tissue Constructs Using a Gelatin/GelMA Blend Bioink
Wang, Y., Kankala, R. K., Zhu, K., Wang, S., Zhang, Y. S., & Chen, A. (2019) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.9b00926 · Cited by 77 · see citing works
Peptide-protein Coassembling Matrices as a Biomimetic 3D Model of Ovarian Cancer
Hedegaard, C. L., Redondo-Gómez, C., Tan, B. Y., Ng, K. W., Loessner, D., & Mata, A. (2020) · Science Advances · doi:10.1126/sciadv.abb3298 · Cited by 76 · see citing works
Self-citation
Dual-degradable and injectable hyaluronic acid hydrogel mimicking extracellular matrix for 3D culture of breast cancer MCF-7 cells
Suo, A., Xu, W., Wang, Y., Sun, T., Ji, L., & Qian, J. (2019) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2019.01.115 · Cited by 77 · see citing works
Addressing Patient Specificity in the Engineering of Tumor Models
Bray, L. J., Hutmacher, D. W., & Bock, N. (2019) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2019.00217 · Cited by 76 · see citing works
Self-citation
Decellularized ECM hydrogels: prior use considerations, applications, and opportunities in tissue engineering and biofabrication
Kort-Mascort, J., Flores-Torres, S., Peza-Chavez, O., Jang, J. H., Pardo, L. A., Tran, S. D., & Kinsella, J. M. (2022) · Biomaterials Science · doi:10.1039/d2bm01273a · Cited by 76 · see citing works
Endosteal-like extracellular matrix expression on melt electrospun written scaffolds
Muerza-Cascante, M. L., Shokoohmand, A., Khosrotehrani, K., Haylock, D. N., Dalton, P. D., Hutmacher, D. W., & Loessner, D. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.12.040 · Cited by 75 · see citing works
Self-citation
Patterning of Structurally Anisotropic Composite Hydrogel Sheets
Prince, E., Alizadehgiashi, M., Campbell, M., Khuu, N., Albulescu, A., France, K. J. D., Ratkov, D., Li, Y., Hoare, T. R., & Kumacheva, E. (2018) · Biomacromolecules · doi:10.1021/acs.biomac.8b00100 · Cited by 75 · see citing works
Engineered cell-degradable poly(2-alkyl-2-oxazoline) hydrogel for epicardial placement of mesenchymal stem cells for myocardial repair
You, Y., Kobayashi, K., Colak, B., Luo, P., Cozens, E. J., Fields, L., Suzuki, K., & Gautrot, J. E. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120356 · Cited by 73 · see citing works
GelMA, Click-Chemistry Gelatin and Bioprinted Polyethylene Glycol-Based Hydrogels as 3D Ex Vivo Drug Testing Platforms for Patient-Derived Breast Cancer Organoids
Bock, N., Forouz, F., Hipwood, L., Clegg, J., Jeffery, P. L., Gough, M., van Wyngaard, T., Pyke, C., Adams, M. N., Bray, L. J., et al. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15010261 · Cited by 73 · see citing works
Nonswelling Click-Cross-Linked Gelatin and PEG Hydrogels with Tunable Properties Using Pluronic Linkers
Truong, V. X., Tsang, K., & Forsythe, J. S. (2017) · Biomacromolecules · doi:10.1021/acs.biomac.6b01601 · Cited by 72 · see citing works
Modular Cross-Linking of Gelatin-Based Thiol–Norbornene Hydrogels for in Vitro 3D Culture of Hepatocellular Carcinoma Cells
Greene, T., & Lin, C. (2015) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.5b00436 · Cited by 70 · see citing works
Bioprinting a 3D vascular construct for engineering a vessel-on-a-chip
Abudupataer, M., Chen, N., Yan, S., Alam, M. F., Shi, Y., Wang, L., Lai, H., Li, J., Zhu, K., & Wang, C. (2019) · Biomedical Microdevices · doi:10.1007/s10544-019-0460-3 · Cited by 69 · see citing works
Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine
Yee, C., Dickson, K.-A., Muntasir, M. N., Ma, Y., & Marsh, D. J. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.836984 · Cited by 66 · see citing works
Gelatin-Methacryloyl (GelMA) Formulated with Human Platelet Lysate Supports Mesenchymal Stem Cell Proliferation and Differentiation and Enhances the Hydrogel’s Mechanical Properties
Kirsch, M., Birnstein, L., Pepelanova, I., Handke, W., Rach, J., Seltsam, A. W., Scheper, T. H., & Lavrentieva, A. V. (2019) · Bioengineering · doi:10.3390/bioengineering6030076 · Cited by 66 · see citing works
Injectable and photocurable CAR-T cell formulation enhances the anti-tumor activity to melanoma in mice
Zhou, W., Lei, S., Liu, M., Li, D., Huang, Y., Hu, X., Yang, J., Li, J., Fu, M., Zhang, M., et al. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121872 · Cited by 65 · see citing works
Chitosan promotes cancer progression and stem cell properties in association with Wnt signaling in colon and hepatocellular carcinoma cells
Chang, P.-H., Sekine, K., Chao, H., Hsu, S., & Chern, E. (2017) · Scientific Reports · doi:10.1038/srep45751 · Cited by 59 · see citing works
Gelatin Methacryloyl Hydrogels in the Absence of a Crosslinker as 3D Glioblastoma Multiforme (GBM)‐Mimetic Microenvironment
Erkoc, P., Seker-Polat, F., Onder, T. B., & Kızılel, S. (2018) · Macromolecular Bioscience · doi:10.1002/mabi.201700369 · Cited by 59 · see citing works
Engineered microenvironments provide new insights into ovarian and prostate cancer progression and drug responses
Loessner, D., Holzapfel, B. M., & Clements, J. A. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.06.001 · Cited by 57 · see citing works
Self-citation
An In Vitro and Ex Vivo Analysis of the Potential of GelMA Hydrogels as a Therapeutic Platform for Preclinical Spinal Cord Injury
Walsh, C. M., Wychowaniec, J. K., Costello, L., Brougham, D. F., & Dooley, D. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202300951 · Cited by 56 · see citing works
Epithelial-mesenchymal transition of cancer cells using bioengineered hybrid scaffold composed of hydrogel/3D-fibrous framework
Pal, M., Chen, H., Lee, B. H., Lee, J. Y. H., Yip, Y. S., Tan, N. S., & Tan, L. P. (2019) · Scientific Reports · doi:10.1038/s41598-019-45384-9 · Cited by 53 · see citing works
Inflammation-triggered dual release of nitroxide radical and growth factor from heparin mimicking hydrogel-tissue composite as cardiovascular implants for anti-coagulation, endothelialization, anti-inflammation, and anti-calcification
Yang, F., Guo, G., & Wang, Y. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121761 · Cited by 52 · see citing works
Highly Methacrylated Gelatin Bioink for Bone Tissue Engineering
Irmak, G., Demirtaş, T. T., & Gümüşderelı́oğlu, M. (2018) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.8b00778 · Cited by 51 · see citing works
Chemotaxis-driven assembly of endothelial barrier in a tumor-on-a-chip platform
Aung, A., Theprungsirikul, J., Lim, H. L., & Varghese, S. (2016) · Lab on a Chip · doi:10.1039/c6lc00184j · Cited by 50 · see citing works
Photocrosslinkable liver extracellular matrix hydrogels for the generation of 3D liver microenvironment models
Ravichandran, A., Murekatete, B., Moedder, D., Meinert, C., & Bray, L. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-94990-z · Cited by 49 · see citing works
The bone marrow niche in support of breast cancer dormancy
Walker, N. D., Patel, J. S., Munoz, J. L., Hu, M. D., Guiro, K., Sinha, G., & Rameshwar, P. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.10.033 · Cited by 47 · see citing works
Hydrogel-Based Cell Therapies for Kidney Regeneration: Current Trends in Biofabrication and In Vivo Repair
Jansen, K., Schuurmans, C. C. L., Jansen, J., Masereeuw, R., & Vermonden, T. (2017) · Current Pharmaceutical Design · doi:10.2174/1381612823666170710155726 · Cited by 48 · see citing works
Modulating Three-Dimensional Microenvironment with Hyaluronan of Different Molecular Weights Alters Breast Cancer Cell Invasion Behavior
Zhao, Y., Qiao, S., Shi, S., Yao, L., Hou, X., Li, C., Lin, F., Guo, K., Acharya, A., Chen, D., et al. (2017) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.6b15187 · Cited by 47 · see citing works
Addressing the tumour microenvironment in early drug discovery: a strategy to overcome drug resistance and identify novel targets for cancer therapy
Kaemmerer, E., Loessner, D., & Avery, V. M. (2020) · Drug Discovery Today · doi:10.1016/j.drudis.2020.11.030 · Cited by 46 · see citing works
Self-citation
Encapsulation and recovery of murine hematopoietic stem and progenitor cells in a thiol-crosslinked maleimide-functionalized gelatin hydrogel
Gilchrist, A. E., Serrano, J. F., Ngo, M. T., Hrnjak, Z., Kim, S., & Harley, B. A. C. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.06.028 · Cited by 46 · see citing works
Chitosan-hyaluronan based 3D co-culture platform for studying the crosstalk of lung cancer cells and mesenchymal stem cells
Han, H., & Hsu, S. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.06.014 · Cited by 45 · see citing works
Hydrogel co-networks of gelatine methacrylate and poly(ethylene glycol) diacrylate sustain 3D functional in vitro models of intestinal mucosa
Vila, A., Torras, N., Castaño, A. G., García-Díaz, M., Comelles, J., Pérez, T., Corregidor, C., Castaño, Ó., Engel, E., Fernández‐Majada, V., et al. (2019) · Biofabrication · doi:10.1088/1758-5090/ab5f50 · Cited by 44 · see citing works
3D printing of reduced glutathione grafted gelatine methacrylate hydrogel scaffold promotes diabetic bone regeneration by activating PI3K/Akt signaling pathway
Wang, L., Shen, M., Hou, Q., Wu, Z., Xu, J., & Wang, L. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.09.236 · Cited by 45 · see citing works
Injectable alendronate-functionalized GelMA hydrogels for mineralization and osteogenesis
Liu, L., Li, X., Shi, X., & Wang, Y. (2018) · RSC Advances · doi:10.1039/c8ra03550d · Cited by 44 · see citing works
Hydrolytic Stability of Methacrylamide and Methacrylate in Gelatin Methacryloyl and Decoupling of Gelatin Methacrylamide from Gelatin Methacryloyl through Hydrolysis
Zheng, J., Zhu, M., Ferracci, G., Cho, N., & Lee, B. H. (2018) · Macromolecular Chemistry and Physics · doi:10.1002/macp.201800266 · Cited by 44 · see citing works
3D in vitro hydrogel models to study the human lung extracellular matrix and fibroblast function
Phogat, S., Thiam, F., Yazeedi, S. A., Abokor, F. A., & Osei, E. T. (2023) · Respiratory Research · doi:10.1186/s12931-023-02548-6 · Cited by 45 · see citing works
Polymeric Hydrogels for In Vitro 3D Ovarian Cancer Modeling
Braccini, S., Tacchini, C., Chiellini, E., & Puppi, D. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063265 · Cited by 42 · see citing works
Unexpected Switching of the Photogelation Chemistry When Cross-Linking Poly(2-oxazoline) Copolymers
Dargaville, T. R., Lava, K., Verbraeken, B., & Hoogenboom, R. (2016) · Macromolecules · doi:10.1021/acs.macromol.6b00167 · Cited by 41 · see citing works
An oxygen-releasing device to improve the survival of mesenchymal stem cells in tissue engineering
Lu, Z., Jiang, X., Chen, M., Feng, L., & Kang, Y. J. (2019) · Biofabrication · doi:10.1088/1758-5090/ab332a · Cited by 41 · see citing works
3D scaffold-free microlivers with drug metabolic function generated by lineage-reprogrammed hepatocytes from human fibroblasts
Lu, Z., Rajan, S. A. P., Song, Q., Zhao, Y., Wan, M., Aleman, J., Skardal, A., Bishop, C. E., Atala, A., & Lu, B. (2021) · Biomaterials · doi:10.1016/j.biomaterials.2021.120668 · Cited by 40 · see citing works
Gelatin Methacryloyl Hydrogels for Musculoskeletal Tissue Regeneration
Kim, Y., Dawson, J. I., Oreffo, R. O. C., Tabata, Y., Kumar, D., Aparicio, C., & Mutreja, I. (2022) · Bioengineering · doi:10.3390/bioengineering9070332 · Cited by 40 · see citing works
Reproducible Dendronized PEG Hydrogels via SPAAC Cross-Linking
Hodgson, S. M., McNelles, S. A., Abdullahu, L., Marozas, I. A., Anseth, K. S., & Adronov, A. (2017) · Biomacromolecules · doi:10.1021/acs.biomac.7b01115 · Cited by 40 · see citing works
Hybrid Hydrogels Based on Methacrylate-Functionalized Gelatin (GelMA) and Synthetic Polymers
Liang, J., Dijkstra, P. J., Poot, A. A., & Grijpma, D. W. (2022) · Biomedical Materials & Devices · doi:10.1007/s44174-022-00023-2 · Cited by 40 · see citing works
A versatile GelMA composite hydrogel: Designing principles, delivery forms and biomedical applications
Zhang, Y., Lv, J., Zhao, J., Ling, G., & Zhang, P. (2023) · European Polymer Journal · doi:10.1016/j.eurpolymj.2023.112370 · Cited by 38 · see citing works
Sacrificial Bioprinting of a Mammary Ductal Carcinoma Model
Duchamp, M., Liu, T., van Genderen, A. M., Kappings, V., Öklü, R., Ellisen, L. W., & Zhang, Y. S. (2019) · Biotechnology Journal · doi:10.1002/biot.201700703 · Cited by 38 · see citing works
Histone deacetylase 4 increases progressive epithelial ovarian cancer cells via repression of p21 on fibrillar collagen matrices
Shen, Y., WEI, A.-M., Kou, Q., Zhu, Q., & Zhang, L. (2015) · Oncology Reports · doi:10.3892/or.2015.4423 · Cited by 36 · see citing works
A review on 3D printing functional brain model
Samanipour, R., Tahmooressi, H., Nejad, H. R., Hirano, M., Shin, S. R., & Hoorfar, M. (2022) · Biomicrofluidics · doi:10.1063/5.0074631 · Cited by 34 · see citing works
Biomechanical forces in tissue engineered tumor models
Chim, L. K., & Mikos, A. G. (2018) · Current Opinion in Biomedical Engineering · doi:10.1016/j.cobme.2018.03.004 · Cited by 32 · see citing works
In Vitro Anticancer Efficacy of Six Different Clinically Approved Types of Liquids Exposed to Physical Plasma
Freund, E., Liedtke, K. R., Gebbe, R., Heidecke, A., Partecke, L.-I., & Bekeschus, S. (2019) · IEEE Transactions on Radiation and Plasma Medical Sciences · doi:10.1109/trpms.2019.2902015 · Cited by 34 · see citing works
Combined Molybdenum Gelatine Methacrylate Injectable Nano-Hydrogel Effective Against Diabetic Bone Regeneration
Liao, X., Shen, M., Li, T., Li, F., Zhao, L., Shi, G., Pei, G., & Cai, X. (2023) · International Journal of Nanomedicine · doi:10.2147/ijn.s428429 · Cited by 34 · see citing works
Gelatin methacrylate hydrogels culture model for glioblastoma cells enriches for mesenchymal-like state and models interactions with immune cells
Shah, N., Hallur, P. M., Ganesh, R. A., Sonpatki, P., Naik, D., Chandrachari, K. P., Puchalski, R. B., & Chaubey, A. (2021) · Scientific Reports · doi:10.1038/s41598-021-97059-z · Cited by 34 · see citing works
GelMA and Biomimetic Culture Allow the Engineering of Mineralized, Adipose, and Tumor Tissue Human Microenvironments for the Study of Advanced Prostate Cancer In Vitro and In Vivo
Bessot, A., Gunter, J. H., Waugh, D. J. J., Clements, J. A., Hutmacher, D. W., McGovern, J., & Bock, N. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202201701 · Cited by 32 · see citing works
Self-citation
Tissue-Engineered Injectable Gelatin–Methacryloyl Hydrogel-Based Adjunctive Therapy for Intervertebral Disc Degeneration
Li, P., Zhang, M., Chen, Z., Tian, B., & Kang, X. (2023) · ACS Omega · doi:10.1021/acsomega.3c00211 · Cited by 31 · see citing works
ATN-161 reduces virus proliferation in PHEV-infected mice by inhibiting the integrin α5β1-FAK signaling pathway
Lv, X., Li, Z., Guan, J., Zhang, J., Xu, B., He, W., Lan, Y., Zhao, K., Lu, H., Song, D., et al. (2019) · Veterinary Microbiology · doi:10.1016/j.vetmic.2019.04.029 · Cited by 30 · see citing works
3D Printing of Diatomite Incorporated Composite Scaffolds for Skin Repair of Deep Burn Wounds
Ma, J., Wu, J., Zhang, H., Du, L., Zhuang, H., Zhang, Z., Ma, B., Chang, J., & Wu, C. (2022) · International Journal of Bioprinting · doi:10.18063/ijb.v8i3.580 · Cited by 30 · see citing works
3D-bioprinted cholangiocarcinoma-on-a-chip model for evaluating drug responses
Liu, Q., Mille, L. S., Villalobos, C., Anaya, I., Vostatek, M., Yi, S., Li, W., Liao, J., Wu, H., Song, Y., et al. (2023) · Bio-Design and Manufacturing · doi:10.1007/s42242-022-00229-9 · Cited by 30 · see citing works
Three‐dimensional cryogel matrix for spheroid formation and anti‐cancer drug screening
Singh, A. K., & Tayalia, P. (2019) · Journal of Biomedical Materials Research Part A · doi:10.1002/jbm.a.36822 · Cited by 30 · see citing works
In vivo gene editing of T-cells in lymph nodes for enhanced cancer immunotherapy
Qu, J., Wang, Y., Xiong, C., Wang, M., He, X., Jia, W., Li, C. Y., Zhang, T., Wang, Z., Li, W., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54292-0 · Cited by 31 · see citing works

Matrix Effects
Hubbell, J. A. (2007) · Elsevier eBooks · doi:10.1016/b978-012370615-7/50025-1 · Cited by 4 · see citing works
Gelatin Methacrylate Hydrogels as Biomimetic Three-Dimensional Matrixes for Modeling Breast Cancer Invasion and Chemoresponse in Vitro
Arya, A. D., Hallur, P. M., Karkisaval, A. G., Gudipati, A., Rajendiran, S., Dhavale, V., Ramachandran, B., Aravindakshan, J., Gundiah, N., & Chaubey, A. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.6b06309 · Cited by 98 · see citing works
Influence of the extracellular matrix oncellular behaviour – Development andapplication of a bioengineered 3D cellculture system for cancer research and highresolution microscopy
Kämmerer, E. (2014)
Bioengineered 3D platform to explore cell–ECM interactions and drug resistance of epithelial ovarian cancer cells
Loessner, D., Stok, K. S., Lutolf, M. P., Hutmacher, D. W., Clements, J. A., & Rizzi, S. C. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.07.064 · Cited by 602 · see citing works
Self-citation
Poly(ethylene glycol)-cross linked poly(methyl vinyl ether-co-maleic acid)hydrogels for three-dimensional human ovarian cancer cell culture
Zhang, T., Chen, J. S., Zhang, Q., Dou, J., & Gu, N. (2013) · Colloids and Surfaces A Physicochemical and Engineering Aspects · doi:10.1016/j.colsurfa.2013.01.030 · Cited by 26 · see citing works

Authors: Kaemmerer, E., Melchels, F. P. W., Holzapfel, B. M., Meckel, T., Hutmacher, D. W., & Loessner, D.
Affiliations: Queensland University of Technology (AU)
Technische Universität Darmstadt (DE)
Corresponding author: Loessner, Daniela
ORCID: Melchels, Ferry P.W.
Holzapfel, Boris M.
Meckel, Tobias
Hutmacher, Dietmar W.
Loessner, Daniela
Venue: Acta Biomaterialia
Publisher: Elsevier BV
Published: 2014-06
Volume: 10
Issue: 6
Pages: 2551-2562
ISSN: 1742-7061 (ISSN-L)
DOI: 10.1016/j.actbio.2014.02.035
OpenAlex: W2091262660
Cited by: 219
References: 75
Citations by year: 2026: 8 · 2025: 16 · 2024: 17 · 2023: 24 · 2022: 26 · 2021: 18 · 2020: 15 · 2019: 24 · 2018: 15 · 2017: 18 · 2016: 19 · 2015: 13 · 2014: 5 · 2013: 1
FWCI: 8.39
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Acta Biomaterialia (publishedVersion)
PubMed (publishedVersion)
Griffith Research Online (submittedVersion)
Funders: Australian Research Council
the Cancer Council Queensland (PIOF-GA-2010-272286, HO 5068/1-1)
Cells and Tissue Domain Collaborative Research Development
Institute of Health and Biomedical Innovation
Queensland University of Technology, Australia
Marie Curie Fellowship
German Research Foundation
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Keywords: hydrogels, ovarian cancer, tumor spheroids, ascites, hydrogel stiffness, solute diffusion, extracellular matrix, matrix metalloproteinases, laminin-411, hyaluronic acid, paclitaxel, integrin antagonists, peritoneal carcinomatosis, biomaterials
MeSH terms: Acrylamides, Cell Division, Cells, Cultured, Extracellular Matrix, Gelatin, Humans, Hydrogels, Matrix Metalloproteinases, Cell Line, Tumor

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Gelatine Methacrylamide-Based Hydrogels: An Alternative Three-Dimensional Cancer Cell Culture System

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks