Expansion of Ovarian Cancer Stem-like Cells in Poly(ethylene glycol)-Cross-Linked Poly(methyl vinyl ether-alt-maleic acid) and Alginate Double-Network Hydrogels
Abstract
A better understanding of cancer stem cells (CSCs) is essential for research on cancer therapy and drug resistance. Currently, increasingly more investigations are focused on obtaining CSCs to study the mechanism of their enhanced malignancy. In this work, three kinds of double-network hydrogels (PEMM/alginate), consisting of poly(ethylene glycol) (PEG) covalently cross-linked poly(methyl vinyl ether- alt -maleic acid) (P(MVE- alt -MA)) (network 1, denoted as PEMM) and Sr 2+ (or Ca 2+, Fe 3+ ) ionically cross-linked alginates (network 2, denoted as SrAlg, CaAlg, or FeAlg), were prepared. The stiffness, morphology, and components of the PEMM/alginate hydrogels were systematically investigated to understand their effects on CSC enrichment. Only the PEMM/FeAlg hydrogels could support the long-term growth, proliferation, and spheroid formation of SK-OV-3 cells. The expression of CSC-related markers was evaluated with the levels of protein and gene at different stages. The cell spheroids cultured in the PEMM/FeAlg hydrogels acquired certain CSC-like properties, thus drug resistance was enhanced, especially in the PEMM-1/FeAlg hydrogel. In vivo tumorigenicity experiments also confirmed the presence of more CSCs in the PEMM-1/FeAlg hydrogel. The results suggest that matrix stiffness, morphology, and cations act synergistically on the regulation of the epithelial–mesenchymal transition (EMT), interleukin-6 (IL-6), and Wnt pathways, affecting the invasiveness of ovarian cancer and the conversion of the non-CSCs into CSCs. The PEMM-1/FeAlg hydrogel with lower elastic modulus, a more macroporous morphology, and higher swelling rate can significantly enhance the stemness, malignancy, and tumorigenicity of SK-OV-3 cells.
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A double network of alginate and polyethylene glycol (PEG)-based hydrogels was shown to increase doxorubicin resistance and CSC markers in SK-OV-3 cells compared to 2D cultures.
“A double network of alginate and polyethylene glycol (PEG)-based hydrogels was shown to increase doxorubicin resistance and CSC markers in SK-OV-3 cells compared to 2D cultures (Zhou et al., 2020).”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as Zhou et al., 2020
PEG-crosslinked poly(methyl vinyl ether-alt-maleic acid) or PEMM/alginate network hydrogels induced EMT, a CSC-like phenotype and chemoresistance in encapsulated SK-OV-3 spheroids, driven by hydrogel stiffness, porosity and cation of choice for crosslinking.
“PEG-crosslinked poly(methyl vinyl ether-alt-maleic acid) or PEMM/alginate network hydrogels induced EMT, a CSC-like phenotype and chemoresistance in encapsulated SK-OV-3 spheroids, driven by hydrogel stiffness, porosity and cation of choice for crosslinking (Zhou et al., 2020).”
From Three-dimensional modelling of ovarian cancer: from cell lines to organoids for discovery and personalized medicine (2022) · cites this paper as Zhou et al., 2020
Cites
Role of YAP/TAZ in mechanotransduction
Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., et al. (2011) · Nature · doi:10.1038/nature10137 · Cited by 5,979 · see citing works
Identification and Characterization of Ovarian Cancer-Initiating Cells from Primary Human Tumors
Zhang, S., Balch, C., Chan, M. W. Y., Lai, H., Matei, D. E., Schilder, J. M., Yan, P. S., Huang, T. H. ‐., & Nephew, K. P. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0364 · Cited by 1,295 · see citing works
PEG Hydrogels for the Controlled Release of Biomolecules in Regenerative Medicine
Lin, C., & Anseth, K. S. (2008) · Pharmaceutical Research · doi:10.1007/s11095-008-9801-2 · Cited by 1,067 · see citing works
Effect of Ca 2+ , Ba 2+ , and Sr 2+ on Alginate Microbeads
Mørch, Y. A., Donati, I., Strand, B. L., & Skjåk‐Bræk, G. (2006) · Biomacromolecules · doi:10.1021/bm060010d · Cited by 864 · see citing works
Strengthening Alginate/Polyacrylamide Hydrogels Using Various Multivalent Cations
Yang, C. H., Wang, M. X., Haider, H., Yang, J., Sun, J., Chen, Y. M., Zhou, J., & Suo, Z. (2013) · ACS Applied Materials & Interfaces · doi:10.1021/am403966x · Cited by 649 · see citing works
Preparation methods of alginate nanoparticles
Paques, J. P., van der Linden, E., van Rijn, C. J. M., & Sagis, L. M. C. (2014) · Advances in Colloid and Interface Science · doi:10.1016/j.cis.2014.03.009 · Cited by 480 · see citing works
Iron addiction: a novel therapeutic target in ovarian cancer
Basuli, D., Tesfay, L., Deng, Z., Paul, B., Yamamoto, Y., Ning, G., Xian, W., McKeon, F., Lynch, M. L., Crum, C. P., et al. (2017) · Oncogene · doi:10.1038/onc.2017.11 · Cited by 469 · see citing works
The Wnt/β-catenin pathway in ovarian cancer: A review
Arend, R. C., Londoño-Joshi, A. I., Straughn, J. M., & Buchsbaum, D. J. (2013) · Gynecologic Oncology · doi:10.1016/j.ygyno.2013.09.034 · Cited by 458 · see citing works
Role of YAP/TAZ in cell-matrix adhesion-mediated signalling and mechanotransduction
Dupont, S. (2016) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.10.034 · Cited by 449 · see citing works
Preferential Iron Trafficking Characterizes Glioblastoma Stem-like Cells
Schonberg, D. L., Miller, T. E., Wu, Q., Flavahan, W. A., Das, N. K., Hale, J. S., Hubert, C. G., Mack, S. C., Jarrar, A., Karl, R. T., et al. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.09.002 · Cited by 347 · see citing works
Chowdhury, F., Li, Y., Poh, Y., Yokohama‐Tamaki, T., Wang, N., & Tanaka, T. S. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015655 · Cited by 341 · see citing works
Xu, Q., Sigen, A., Gao, Y., Guo, L., Creagh-Flynn, J., Zhou, D., Greiser, U., Dong, Y., Wang, F., Tai, H., et al. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.05.039 · Cited by 300 · see citing works
Kim, S. Y., Kang, J. W., Song, X., Kim, B. K., Yoo, Y. D., Kwon, Y. T., & Lee, Y. J. (2013) · Cellular Signalling · doi:10.1016/j.cellsig.2013.01.007 · Cited by 297 · see citing works
Expression of aldehyde dehydrogenase and CD133 defines ovarian cancer stem cells
Kryczek, I., Liu, S., Roh, M. H., Vatan, L., Szeliga, W., Wei, S., Banerjee, M., Mao, Y., Kotarski, J., Wicha, M. S., et al. (2011) · International Journal of Cancer · doi:10.1002/ijc.25967 · Cited by 266 · see citing works
Three-dimensional biomaterials for the study of human pluripotent stem cells
Kraehenbuehl, T. P., Langer, R., & Ferreira, L. (2011) · Nature Methods · doi:10.1038/nmeth.1671 · Cited by 226 · see citing works
Brus, J., Urbanová, M., Czernek, J., Pavelková, M., Kubová, K., Vysloužil, J., Abbrent, S., Konefał, R., Horský, J., Vetchý, D., et al. (2017) · Biomacromolecules · doi:10.1021/acs.biomac.7b00627 · Cited by 213 · see citing works
Agulhon, P., Markova, V. K., Robitzer, M., Quignard, F., & Mineva, T. (2012) · Biomacromolecules · doi:10.1021/bm300420z · Cited by 208 · see citing works
Aldehyde dehydrogenases and cancer stem cells
Xu, X., Chai, S., Wang, P., Zhang, C., Yang, Y., Yang, Y., & Wang, K. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.08.018 · Cited by 205 · see citing works
Controlled delivery of VEGF via modulation of alginate microparticle ionic crosslinking
Jay, S. M., & Saltzman, W. M. (2008) · Journal of Controlled Release · doi:10.1016/j.jconrel.2008.10.019 · Cited by 195 · see citing works
Long-term human pluripotent stem cell self-renewal on synthetic polymer surfaces
Brafman, D. A., Chang, C., Fernandez-Perez, A., Willert, K., Varghese, S., & Chien, S. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.08.007 · Cited by 178 · see citing works
A promising new approach to cancer therapy: Targeting iron metabolism in cancer stem cells
El-Hout, M., Santos, L. D., Hamaï, A., & Mehrpour, M. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.07.009 · Cited by 170 · see citing works
Cancer stem cells (CSCs), cervical CSCs and targeted therapies
Huang, R., & Rofstad, E. K. (2016) · Oncotarget · doi:10.18632/oncotarget.10169 · Cited by 162 · see citing works
Luo, L., Zeng, J., Liang, B., Zhao, Z., Sun, L., Cao, D., Yang, J., & Shen, K. (2011) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2011.06.005 · Cited by 153 · see citing works
The cancer stem-cell signaling network and resistance to therapy
Carnero, A., Garcia‐Mayea, Y., Mir, C., Lorente, J., Rubio, I. T., & LLeonart, M. E. (2016) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2016.07.001 · Cited by 153 · see citing works
Li, Z., Gong, Y., Sun, S., Du, Y. M., Lü, D., Liu, X., & Long, M. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.06.059 · Cited by 150 · see citing works
Singh, T. R. R., McCarron, P. A., Woolfson, A. D., & Donnelly, R. F. (2008) · European Polymer Journal · doi:10.1016/j.eurpolymj.2008.12.019 · Cited by 143 · see citing works
Lignin-based hydrogels with “super-swelling” capacities for dye removal
Domínguez‐Robles, J., Peresin, M. S., Tamminen, T., Rodríguez, A., Larrañeta, E., & Jääskeläinen, A.-S. (2018) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2018.04.044 · Cited by 140 · see citing works
Kievit, F. M., Florczyk, S. J., Leung, M. C., Wang, K., Wu, J. D., Silber, J. R., Ellenbogen, R. G., Lee, J. S. H., & Zhang, M. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.07.037 · Cited by 124 · see citing works
Matrix stiffness-mediated effects on stemness characteristics occurring in HCC cells
You, Y., Zheng, Q., Dong, Y., Xie, X., Wang, Y., Wu, S., Zhang, L., Wang, Y., Xue, T., Wang, Z., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.8515 · Cited by 119 · see citing works
Dong, Y., Xie, X., Wang, Z., Hu, C., Zheng, Q., Wang, Y., Chen, R., Xue, T., Chen, J., Gao, D., et al. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.01.079 · Cited by 110 · see citing works
Dysregulation of iron metabolism in cancer stem cells
Recalcati, S., Gammella, E., & Cairo, G. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.07.015 · Cited by 107 · see citing works
A tunable silk–alginate hydrogel scaffold for stem cell culture and transplantation
Ziv, K., Nuhn, H., Ben-Haim, Y., Sasportas, L. S., Kempen, P. J., Niedringhaus, T. P., Hrynyk, M., Sinclair, R., Barron, A. E., & Gambhir, S. S. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.01.029 · Cited by 100 · see citing works
Zhang, Y., Wei, L., Chang, J., Miron, R. J., Shi, B., Yi, S., & Wu, C. (2013) · Journal of Materials Chemistry B · doi:10.1039/c3tb21047b · Cited by 100 · see citing works
Bruchet, M., & Melman, A. (2015) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2015.05.021 · Cited by 98 · see citing works
Hansen, E. L., Sozer, E. B., Romeo, S., Frandsen, S. K., Vernier, P. T., & Gehl, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122973 · Cited by 98 · see citing works
Lin, Z., Wu, M., He, H., Liang, Q., Hu, C., Zeng, Z., Cheng, D., Wang, G., Chen, D., Pan, H., et al. (2019) · Advanced Functional Materials · doi:10.1002/adfm.201808439 · Cited by 97 · see citing works
Rao, W., Zhao, S., Yu, J., Lu, X., Zynger, D. L., & He, X. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.06.011 · Cited by 96 · see citing works
Identification of cancer stem cell-like cells from human epithelial ovarian carcinoma cell line
Shi, M., Jiao, J., Lü, W., Ye, F., Ma, D., Dong, Q., & Xie, X. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0420-9 · Cited by 94 · see citing works
Pei, M., Jia, X., Zhao, X., Li, J., & Liu, P. (2017) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2017.12.013 · Cited by 91 · see citing works
3D porous chitosan–alginate scaffolds promote proliferation and enrichment of cancer stem-like cells
Florczyk, S. J., Kievit, F. M., Wang, K., Erickson, A. E., Ellenbogen, R. G., & Zhang, M. (2016) · Journal of Materials Chemistry B · doi:10.1039/c6tb01713d · Cited by 88 · see citing works
Expansion of breast cancer stem cells with fibrous scaffolds
Feng, S., Duan, X., Lo, P., Liu, S., Liu, X., Chen, H., & Wang, Q. (2013) · Integrative Biology · doi:10.1039/c3ib20255k · Cited by 82 · see citing works
Demir, Y. K., Metin, A. Ü., Şatıroğlu, B., Solmaz, M. E., Kayser, V., & Mäder, K. (2017) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2017.04.018 · Cited by 82 · see citing works
Yang, X., Sarvestani, S. K., Moeinzadeh, S., He, X., & Jabbari, E. (2012) · Tissue Engineering Part A · doi:10.1089/ten.tea.2012.0333 · Cited by 80 · see citing works
Huang, Y.-J., & Hsu, S. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.09.010 · Cited by 77 · see citing works
Angiogenesis and cancer stem cells: New perspectives on therapy of ovarian cancer
Markowska, A., Sajdak, S., Markowska, J., & Huczyński, A. (2017) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2017.06.030 · Cited by 77 · see citing works
Ahearne, M., & Kelly, D. J. (2013) · Biomedical Materials · doi:10.1088/1748-6041/8/3/035004 · Cited by 76 · see citing works
Iron induces cancer stem cells and aggressive phenotypes in human lung cancer cells
Pithi Chanvorachote, B., & Luanpitpong, S. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00322.2015 · Cited by 76 · see citing works
Ning, Y., Cui, Y., Li, X., Cao, X., Chen, A., Xu, C., Cao, J., & Luo, X. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.04.022 · Cited by 75 · see citing works
Chen, B., Wright, B., Sahoo, R., & Connon, C. J. (2012) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2012.0489 · Cited by 73 · see citing works
Menakbi, C., Quignard, F., & Mineva, T. (2016) · The Journal of Physical Chemistry B · doi:10.1021/acs.jpcb.6b00472 · Cited by 70 · see citing works
Bae, D., Moon, S., Park, B. G., Park, S., Jung, T., Kim, J. S., Lee, K. B., & Chung, H. (2013) · Biomaterials · doi:10.1016/j.biomaterials.2013.10.031 · Cited by 68 · see citing works
Characterization of primary ovarian cancer cells in different culture systems
Lai (2010) · Oncology Reports · doi:10.3892/or_00000761 · Cited by 62 · see citing works
Therapy‐induced enrichment of putative lung cancer stem‐like cells
Freitas, D. P., Teixeira, C. A., Santos‐Silva, F., Vasconcelos, M. H., & Almeida, G. M. (2013) · International Journal of Cancer · doi:10.1002/ijc.28478 · Cited by 61 · see citing works
Yang, X., Sarvestani, S. K., Moeinzadeh, S., He, X., & Jabbari, E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059147 · Cited by 60 · see citing works
Lipocalin-2 and iron trafficking in the tumor microenvironment
Jung, M., Mertens, C., Bauer, R., Rehwald, C., & Brüne, B. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.03.018 · Cited by 60 · see citing works
Tan, F., Huang, Y., Pei, Q., Liu, H., Pei, H., & Zhu, H. (2018) · Journal of Cellular Biochemistry · doi:10.1002/jcb.27532 · Cited by 60 · see citing works
Schulz, A., Katsen‐Globa, A., Huber, E. J., Mueller, S. C., Kreiner, A., Pütz, N., Gepp, M. M., Fischer, B., Stracke, F., von Briesen, H., et al. (2018) · Journal of Materials Science Materials in Medicine · doi:10.1007/s10856-018-6113-x · Cited by 56 · see citing works
In vitroadhesion of human dermal fibroblasts on iron cross-linked alginate films
Machida‐Sano, I., Matsuda, Y., & Namiki, H. (2009) · Biomedical Materials · doi:10.1088/1748-6041/4/2/025008 · Cited by 55 · see citing works
An alginate-based platform for cancer stem cell research
Qiao, S., Zhao, Y., Li, C., Yin, Y., Meng, Q., Lin, F., Liu, Y., Hou, X., Guo, K. X., Chen, D., et al. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.04.032 · Cited by 54 · see citing works
Integrin Regulation of β-Catenin Signaling in Ovarian Carcinoma
Burkhalter, R. J., Symowicz, J., Hudson, L. G., Gottardi, C. J., & Stack, M. S. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.199539 · Cited by 51 · see citing works
Dou, J., Huang, Q., Huang, H., Gan, D., Chen, J., Deng, F., Wen, Y., Zhu, X., Zhang, X., & Wei, Y. (2018) · Journal of Colloid and Interface Science · doi:10.1016/j.jcis.2018.08.064 · Cited by 51 · see citing works
Shahbazi, M., Almeida, P. V., Mäkilä, E. M., Correia, A., Ferreira, M. P. A., Kaasalainen, M. H., Salonen, J., Hirvonen, J. J., & Santos, H. A. (2014) · Macromolecular Rapid Communications · doi:10.1002/marc.201300868 · Cited by 48 · see citing works
Nina, K. L., Lim, J. K., Leong, M. F., Sandanaraj, E., Ang, B. T., Tang, C., & Wan, A. C. A. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.11.031 · Cited by 46 · see citing works
Stankevičius, V., Kunigenas, L., Stankunas, E., Kuodyte, K., Strainienė, E., Cicenas, J., Samalavičius, N. E., & Sužiedėlis, K. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.01.111 · Cited by 46 · see citing works
Novel dendritic structure of alginate hybrid nanoparticles for effective anti-viral drug delivery
Joshy, K. S., George, A., Jose, J., Kalarikkal, N., Pothen, L. A., & Thomas, S. (2017) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2017.05.094 · Cited by 45 · see citing works
Hale, J. S., Li, M., & Lathia, J. D. (2012) · Cell Adhesion & Migration · doi:10.4161/cam.21294 · Cited by 42 · see citing works
Enrichment of cancer stem cell-like cells by culture in alginate gel beads
Xu, X., Liu, C. X., Yang, L., Li, Y., Li, N., Guo, X. W., Sun, G., & Ma, X. (2014) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2014.02.016 · Cited by 42 · see citing works
Self-citationAval, S. F., Lotfi, H., Sheervalilou, R., & Zarghami, N. (2017) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2017.05.020 · Cited by 42 · see citing works
Singh, T. R. R., Garland, M. J., Migalska, K., Caffarel–Salvador, E., Shaikh, R., McCarthy, H. O., Woolfson, A. D., & Donnelly, R. F. (2012) · Journal of Applied Polymer Science · doi:10.1002/app.36524 · Cited by 41 · see citing works
Lin, L., Marchant, R. E., Zhu, J., & Kottke‐Marchant, K. (2014) · Acta Biomaterialia · doi:10.1016/j.actbio.2014.08.025 · Cited by 38 · see citing works
Machida‐Sano, I., Ogawa, S., Ueda, H., Kimura, Y., Satoh, N., & Namiki, H. (2012) · International Journal of Biomaterials · doi:10.1155/2012/820513 · Cited by 37 · see citing works
Saadin, K., & White, I. M. (2012) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.12.117 · Cited by 33 · see citing works
Jones, D. S., Laverty, T. P., Caoimhe, M., & Andrews, G. P. (2016) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2016.03.008 · Cited by 33 · see citing works
Sun, W., Chen, G., Wang, F., Qin, Y., Wang, Z., Nie, J., & Ma, G. (2017) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2017.10.068 · Cited by 33 · see citing works
Qian, X., Villa-Diaz, L. G., Kumar, R., Lahann, J., & Krebsbach, P. H. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.08.015 · Cited by 32 · see citing works
Iron participated in breast cancer chemoresistance by reinforcing IL-6 paracrine loop
Li, J., He, K., Liu, P., & Xu, L. X. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.05.064 · Cited by 32 · see citing works
Cell viability modulation through changes of Ca2+-dependent signalling pathways
Wójcik‐Piotrowicz, K., Kaszuba-Zwoińska, J., Rokita, E., & Thor, P. J. (2016) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2016.01.004 · Cited by 29 · see citing works
Yu, F., Sim, A. C. N., Li, C., Li, Y., Zhao, X., Wang, D. Y., & Loh, K. S. (2013) · The Laryngoscope · doi:10.1002/lary.24003 · Cited by 27 · see citing works
Yu, H., Cauchois, G., Schmitt, J.-F., Louvet, N., Six, J., Chen, Y., Rahouadj, R., & Huselstein, C. (2017) · Journal of the mechanical behavior of biomedical materials/Journal of mechanical behavior of biomedical materials · doi:10.1016/j.jmbbm.2017.01.038 · Cited by 23 · see citing works
Oh, Y., Cha, J., Kang, S., & Kim, P. (2016) · Journal of Industrial and Engineering Chemistry · doi:10.1016/j.jiec.2016.05.012 · Cited by 22 · see citing works
Cancer stem cell markers in lung cancer
Miyata, T., Yoshimatsu, T., So, T., Oyama, T., Uramoto, H., Osaki, T., Nakanishi, R., Tanaka, F., Nagaya, H., & Gotoh, A. (2015) · Personalized Medicine Universe · doi:10.1016/j.pmu.2015.03.007 · Cited by 18 · see citing works
Saha, S., Lo, P., Duan, X., Chen, H., & Wang, Q. (2012) · Integrative Biology · doi:10.1039/c2ib20034a · Cited by 18 · see citing works
TRRAP stimulates the tumorigenic potential of ovarian cancer stem cells
Kang, K. T., Kwon, Y. W., Kim, D. K., Lee, S. I., Kim, K., Suh, D., & Kim, J. H. (2018) · BMB Reports · doi:10.5483/bmbrep.2018.51.10.042 · Cited by 18 · see citing works
Chang, H.-J., Chou, C.-T., Chang, H.-T., Liang, W.-Z., Hung, T.-Y., Li, Y. C., Fang, Y.-C., Kuo, C.-C., Kuo, D.-H., Shieh, P., et al. (2014) · Human & Experimental Toxicology · doi:10.1177/0960327114537536 · Cited by 15 · see citing works
Zhou, N., Ma, X., Zhang, T., Chen, X., Guo, Z., Ma, D., & Gu, N. (2016) · Journal of Nanoscience and Nanotechnology · doi:10.1166/jnn.2016.13768 · Cited by 6 · see citing works
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Advances in hydrogel-based vascularized tissues for tissue repair and drug screening
Wang, Y., Kankala, R. K., Ou, C., Chen, A., & Yang, Z. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.07.005 · Cited by 159 · see citing works
Double network hydrogels for energy/environmental applications: challenges and opportunities
Li, L., Wu, P., Yu, F., & Ma, J. (2022) · Journal of Materials Chemistry A · doi:10.1039/d2ta00540a · Cited by 133 · see citing works
Liu, H., Pan, B., Wang, Q., Niu, Y., Tai, Y., Du, X., & Zhang, K. (2020) · Chemosphere · doi:10.1016/j.chemosphere.2020.128240 · Cited by 93 · see citing works
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
Shaheen, A., Maswal, M., & Dar, A. A. (2021) · Colloids and Surfaces A Physicochemical and Engineering Aspects · doi:10.1016/j.colsurfa.2021.127223 · Cited by 63 · see citing works
Zhang, R., Yu, B., Tian, Y., Pang, L., Xu, T., Cong, H., & Shen, Y. (2022) · Applied Materials Today · doi:10.1016/j.apmt.2022.101396 · Cited by 53 · see citing works
Innovative approaches in skin therapy: bionanocomposites for skin tissue repair and regeneration
Bal‐Öztürk, A., Alarçın, E., Yaşayan, G., Avci‐Adali, M., Khosravi, A., Zarepour, A., Iravani, S., & Zarrabi, A. (2024) · Materials Advances · doi:10.1039/d4ma00384e · 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
Sinad, K. V. G., Ebubechukwu, R. C., & Chu, C. K. (2023) · Journal of Materials Chemistry B · doi:10.1039/d3tb00773a · Cited by 42 · see citing works
Malik, S. A., Dar, A. A., & Banday, J. A. (2023) · Colloids and Surfaces A Physicochemical and Engineering Aspects · doi:10.1016/j.colsurfa.2023.131046 · Cited by 40 · see citing works
A Comprehensive Assessment on the Pivotal Role of Hydrogels in Scaffold-Based Bioprinting
Ratnamani, M. P. C., Zhang, X., & Wang, H. (2022) · Gels · doi:10.3390/gels8040239 · Cited by 25 · see citing works
Application of hydrogels for targeting cancer stem cells in cancer treatment
Li, F., Li, Z., Wei, C., Xu, L., Liang, Y., Yan, J., Li, Y., He, B., & Sun, C. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117486 · Cited by 15 · see citing works
Deciphering the “Rosetta Stone” of ovarian cancer stem cells: Opportunities and challenges
Tan, J., Zheng, B., & Zhou, S. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189346 · Cited by 8 · see citing works
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Xiao, M., Chen, S., Yang, Y., Hu, K., Song, Y., Hou, Z., Sun, S., & Yang, L. (2024) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2024.122946 · Cited by 7 · see citing works
Models of High-Grade Serous Ovarian CarcinomaPreprint
Pundel, O. J., & Neel, B. G. (2025) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041949 · Cited by 2 · see citing works
Zhang, T., Yang, L., Wang, Z., & Zhou, N. (2025) · ACS Omega · doi:10.1021/acsomega.4c10301 · Cited by 1 · see citing works
Self-citationYousuf, S., Shafi, A., Gulzar, S., Ahanger, G., & Nazir, N. (2026) · Colloids and Surfaces C Environmental Aspects · doi:10.1016/j.colsuc.2026.100096 · Cited by 1 · see citing works
Scrocciolani, C., Caserio, L., Grillo, S., Ottavi, F., Masi, I., Jacchetti, E., Vangosa, F. B., Raimondi, M. T., Colosimo, B. M., Rosanò, L., et al. (2026) · ACS Applied Bio Materials · doi:10.1021/acsabm.6c00299 · Cited by 1 · see citing works
Characterization of pMVEMA-PMAA copolymers for biomedical applications
Cué-Sampedro, R., & Sánchez-Fernández, J. A. (2020) · Materials Today Proceedings · doi:10.1016/j.matpr.2020.10.294 · Cited by 1 · see citing works
- Authors
- Zhou, N., Ma, X., Bernaerts, K. V., Ren, P., Hu, W., & Zhang, T.
- Affiliations
- State Key Laboratory of Digital Medical Engineering (CN)
- Maastricht University (NL)
- Corresponding author
- Zhang, Tianzhu
- Venue
- ACS Biomaterials Science & Engineering
- Publisher
- American Chemical Society (ACS)
- Published
- 2020-04-09
- Volume
- 6
- Issue
- 6
- Pages
- 3310-3326
- ISSN
- 2373-9878 (ISSN-L)
- OpenAlex
- W3015485718
- Cited by
- 19
- References
- 85
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 2 · 2022: 5 · 2021: 2 · 2020: 2
- FWCI
- 0.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- ACS Biomaterials Science & Engineering (publishedVersion)
- PubMed (publishedVersion)
- Research Publications (Maastricht University) (publishedVersion)
- Research Publications (Maastricht University) (submittedVersion)
- Funders
- Ministry of Education of the People's Republic of China
- Ministry of Science and Technology of the People's Republic of China (2011YQ03013403)
- National Natural Science Foundation of China (81600407)
- Jiangsu Key Laboratory of Advanced Functional Polymer Design and Application
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- double-network hydrogel, alginate, ionic crosslinking, extracellular matrix stiffness, cell spheroids, drug resistance, epithelial-mesenchymal transition, interleukin-6, Wnt signaling, tumorigenicity, SKOV3 cells, stemness
- MeSH terms
- Alginates, Female, Humans, Maleic Anhydrides, Ovarian Neoplasms, Polyethylene Glycols, Polyvinyls, Neoplastic Stem Cells, Hydrogels
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