Silica bioreplication preserves three-dimensional spheroid structures of human pluripotent stem cells and HepG2 cells

Lou, Yan-Ru; Kanninen, Liisa; Kaehr, Bryan; Townson, Jason L.; Niklander, Johanna; Harjumäki, Riina; Jeffrey Brinker, C.; Yliperttula, Marjo

doi:10.1038/srep13635

Title: Silica bioreplication preserves three-dimensional spheroid structures of human pluripotent stem cells and HepG2 cells

Journal Article · Tue Sep 01 00:00:00 EDT 2015 · Scientific Reports

DOI:https://doi.org/10.1038/srep13635· OSTI ID:1261097

Lou, Yan-Ru ^[1]; Kanninen, Liisa ^[1]; Kaehr, Bryan ^[2]; Townson, Jason L. ^[3]; Niklander, Johanna ^[1]; Harjumäki, Riina ^[1]; Jeffrey Brinker, C. ^[2]; Yliperttula, Marjo ^[1]

Univ. of Helsinki (Finland). Centre for Drug Research
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States). Advanced Materials Lab.; Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Chemical and Biomolecular Engineering
Univ. of New Mexico, Albuquerque, NM (United States). Dept. of Internal Medicine; Univ. of New Mexico, Albuquerque, NM (United States). Center for Micro-Engineered Materials

Three-dimensional (3D) cell cultures produce more in vivo-like multicellular structures such as spheroids that cannot be obtained in two-dimensional (2D) cell cultures. Thus, they are increasingly employed as models for cancer and drug research, as well as tissue engineering. It has proven challenging to stabilize spheroid architectures for detailed morphological examination. Here we overcome this issue using a silica bioreplication (SBR) process employed on spheroids formed from human pluripotent stem cells (hPSCs) and hepatocellular carcinoma HepG2 cells cultured in the nanofibrillar cellulose (NFC) hydrogel. The cells in the spheroids are more round and tightly interacting with each other than those in 2D cultures, and they develop microvilli-like structures on the cell membranes as seen in 2D cultures. Furthermore, SBR preserves extracellular matrix-like materials and cellular proteins. In conclusion, these findings provide the first evidence of intact hPSC spheroid architectures and similar fine structures to 2D-cultured cells, providing a pathway to enable our understanding of morphogenesis in 3D cultures.

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Research Organization:: Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FA9550-14-1-0066; CBET-1344298

OSTI ID:: 1261097

Journal Information:: Scientific Reports, Vol. 5; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 27 works

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References (41)

Embryonic Stem Cell Lines Derived from Human Blastocysts Thomson, J. A. Science, Vol. 282, Issue 5391 https://doi.org/10.1126/science.282.5391.1145	journal	November 1998
Human embryonic stem cells express an immunogenic nonhuman sialic acid Martin, Maria J.; Muotri, Alysson; Gage, Fred Nature Medicine, Vol. 11, Issue 2 https://doi.org/10.1038/nm1181	journal	January 2005
Long-term human pluripotent stem cell self-renewal on synthetic polymer surfaces Brafman, David A.; Chang, Chien W.; Fernandez, Antonio Biomaterials, Vol. 31, Issue 34 https://doi.org/10.1016/j.biomaterials.2010.08.007	journal	December 2010
Engineered polymer-media interfaces for the long-term self-renewal of human embryonic stem cells Irwin, Elizabeth F.; Gupta, Rohini; Dashti, Derek C. Biomaterials, Vol. 32, Issue 29 https://doi.org/10.1016/j.biomaterials.2011.05.058	journal	October 2011
Synthetic polymer coatings for long-term growth of human embryonic stem cells Villa-Diaz, Luis G.; Nandivada, Himabindu; Ding, Jun Nature Biotechnology, Vol. 28, Issue 6 https://doi.org/10.1038/nbt.1631	journal	May 2010
High-Throughput Discovery of Synthetic Surfaces That Support Proliferation of Pluripotent Cells Derda, Ratmir; Musah, Samira; Orner, Brendan P. Journal of the American Chemical Society, Vol. 132, Issue 4 https://doi.org/10.1021/ja906089g	journal	February 2010
Long-term self-renewal of human pluripotent stem cells on human recombinant laminin-511 Rodin, Sergey; Domogatskaya, Anna; Ström, Susanne Nature Biotechnology, Vol. 28, Issue 6 https://doi.org/10.1038/nbt.1620	journal	May 2010
Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells Melkoumian, Zara; Weber, Jennifer L.; Weber, David M. Nature Biotechnology, Vol. 28, Issue 6 https://doi.org/10.1038/nbt.1629	journal	May 2010
Recombinant Vitronectin Is a Functionally Defined Substrate That Supports Human Embryonic Stem Cell Self-Renewal via αVβ5 Integrin Braam, Stefan R.; Zeinstra, Laura; Litjens, Sandy Stem Cells, Vol. 26, Issue 9 https://doi.org/10.1634/stemcells.2008-0291	journal	September 2008
Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells Gerecht, S.; Burdick, J. A.; Ferreira, L. S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 27 https://doi.org/10.1073/pnas.0703723104	journal	June 2007
Feeder-free self-renewal of human embryonic stem cells in 3D porous natural polymer scaffolds Li, Zhensheng; Leung, Matthew; Hopper, Richard Biomaterials, Vol. 31, Issue 3 https://doi.org/10.1016/j.biomaterials.2009.09.070	journal	January 2010
A 3D microfibrous scaffold for long-term human pluripotent stem cell self-renewal under chemically defined conditions Lu, Hong Fang; Narayanan, Karthikeyan; Lim, Sze-Xian Biomaterials, Vol. 33, Issue 8 https://doi.org/10.1016/j.biomaterials.2011.11.077	journal	March 2012
The benefit of human embryonic stem cell encapsulation for prolonged feeder-free maintenance Siti-Ismail, Norhayati; Bishop, Anne E.; Polak, Julia M. Biomaterials, Vol. 29, Issue 29 https://doi.org/10.1016/j.biomaterials.2008.04.027	journal	October 2008
The Use of Nanofibrillar Cellulose Hydrogel As a Flexible Three-Dimensional Model to Culture Human Pluripotent Stem Cells Lou, Yan-Ru; Kanninen, Liisa; Kuisma, Tytti Stem Cells and Development, Vol. 23, Issue 4 https://doi.org/10.1089/scd.2013.0314	journal	February 2014
Xeno-Free Production of Human Embryonic Stem Cells in Stirred Microcarrier Systems Using a Novel Animal/Human-Component-Free Medium Marinho, Paulo André Nobrega; Vareschini, Daniel Tait; Gomes, Ismael Carlos Tissue Engineering Part C: Methods, Vol. 19, Issue 2 https://doi.org/10.1089/ten.tec.2012.0141	journal	February 2013
Effective surface-based cryopreservation of human embryonic stem cells by vitrification Beier, A. F. J.; Schulz, J. C.; Dörr, D. Cryobiology, Vol. 63, Issue 3 https://doi.org/10.1016/j.cryobiol.2011.06.003	journal	December 2011
Cellular complexity captured in durable silica biocomposites Kaehr, B.; Townson, J. L.; Kalinich, R. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 43, p. 17336-17341 https://doi.org/10.1073/pnas.1205816109	journal	October 2012
Synthetic fossilization of soft biological tissues and their shape-preserving transformation into silica or electron-conductive replicas Townson, Jason L.; Lin, Yu-Shen; Chou, Stanley S. Nature Communications, Vol. 5, Article No. 5665 https://doi.org/10.1038/ncomms6665	journal	December 2014
Biomimetic synthesis of ordered silica structures mediated by block copolypeptides Cha, Jennifer N.; Stucky, Galen D.; Morse, Daniel E. Nature, Vol. 403, Issue 6767 https://doi.org/10.1038/35002038	journal	January 2000
Surface Patterning of Silica Nanostructures Using Bio-Inspired Templates and Directed Synthesis Coffman, Elizabeth A.; Melechko, Anatoli V.; Allison, David P. Langmuir, Vol. 20, Issue 20 https://doi.org/10.1021/la048907o	journal	September 2004
Hierarchical architectures by synergy between dynamical template self-assembly and biomineralization Pouget, Emilie; Dujardin, Erik; Cavalier, Annie Nature Materials, Vol. 6, Issue 6, p. 434-439 https://doi.org/10.1038/nmat1912	journal	May 2007
Protein-Directed Assembly of Arbitrary Three-Dimensional Nanoporous Silica Architectures Khripin, Constantine Y.; Pristinski, Denis; Dunphy, Darren R. ACS Nano, Vol. 5, Issue 2, p. 1401-1409 https://doi.org/10.1021/nn1031774	journal	January 2011
Cell-Directed Assembly of Lipid-Silica Nanostructures Providing Extended Cell Viability Baca, Helen K.; Ashley, Carlee; Carnes, Eric Science, Vol. 313, Issue 5785, p. 337-341 https://doi.org/10.1126/science.1126590	journal	July 2006
Cell-Directed Assembly of Bio/Nano Interfaces—A New Scheme for Cell Immobilization Baca, Helen K.; Carnes, Eric; Singh, Seema Accounts of Chemical Research, Vol. 40, Issue 9, p. 836-845 https://doi.org/10.1021/ar600027u	journal	September 2007
Cell-Directed Localization and Orientation of a Functional Foreign Transmembrane Protein within a Silica Nanostructure Carnes, Eric C.; Harper, Jason C.; Ashley, Carlee E. Journal of the American Chemical Society, Vol. 131, Issue 40 https://doi.org/10.1021/ja906055m	journal	October 2009
Cell-Directed Integration into Three-Dimensional Lipid−Silica Nanostructured Matrices Harper, Jason C.; Khirpin, Constantine Y.; Carnes, Eric C. ACS Nano, Vol. 4, Issue 10, p. 5539-5550 https://doi.org/10.1021/nn101793u	journal	September 2010
Mechanically Encoded Cellular Shapes for Synthesis of Anisotropic Mesoporous Particles Meyer, Kristin C.; Coker, Eric N.; Bolintineanu, Dan S. Journal of the American Chemical Society, Vol. 136, Issue 38, p. 13138-13141 https://doi.org/10.1021/ja506718z	journal	September 2014
Nanofibrillar cellulose hydrogel promotes three-dimensional liver cell culture Bhattacharya, Madhushree; Malinen, Melina M.; Lauren, Patrick Journal of Controlled Release, Vol. 164, Issue 3 https://doi.org/10.1016/j.jconrel.2012.06.039	journal	December 2012
Differentiation of liver progenitor cell line to functional organotypic cultures in 3D nanofibrillar cellulose and hyaluronan-gelatin hydrogels Malinen, Melina M.; Kanninen, Liisa K.; Corlu, Anne Biomaterials, Vol. 35, Issue 19 https://doi.org/10.1016/j.biomaterials.2014.03.020	journal	June 2014
Engineering liver tissue spheroids with inverted colloidal crystal scaffolds Lee, Jungwoo; Cuddihy, Meghan J.; Cater, George M. Biomaterials, Vol. 30, Issue 27 https://doi.org/10.1016/j.biomaterials.2009.05.024	journal	September 2009
Suspension Culture of Undifferentiated Human Embryonic and Induced Pluripotent Stem Cells Amit, Michal; Chebath, Judith; Margulets, Victoria Stem Cell Reviews and Reports, Vol. 6, Issue 2 https://doi.org/10.1007/s12015-010-9149-y	journal	April 2010
Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension Steiner, Debora; Khaner, Hanita; Cohen, Malkiel Nature Biotechnology, Vol. 28, Issue 4 https://doi.org/10.1038/nbt.1616	journal	March 2010
Method for generation of homogeneous multicellular tumor spheroids applicable to a wide variety of cell types Kelm, Jens M.; Timmins, Nicholas E.; Brown, Catherine J. Biotechnology and Bioengineering, Vol. 83, Issue 2 https://doi.org/10.1002/bit.10655	journal	May 2003
Spheroid Culture for Enhanced Differentiation of Human Embryonic Stem Cells to Hepatocyte-Like Cells Subramanian, Kartik; Owens, Derek Jason; Raju, Ravali Stem Cells and Development, Vol. 23, Issue 2 https://doi.org/10.1089/scd.2013.0097	journal	January 2014
Drying cells for SEM, AFM and TEM by hexamethyldisilazane: a study on hepatic endothelial cells Braet, F.; De Zanger, R.; Wisse, E. Journal of Microscopy, Vol. 186, Issue 1, p. 84-87 https://doi.org/10.1046/j.1365-2818.1997.1940755.x	journal	April 1997
Biomimetic Silicification of Demineralized Hierarchical Collagenous Tissues Niu, Li-na; Jiao, Kai; Ryou, Heonjune Biomacromolecules, Vol. 14, Issue 5 https://doi.org/10.1021/bm400316e	journal	April 2013
Cells made of silica Ying, Jackie Y. Nature Nanotechnology, Vol. 7, Issue 12 https://doi.org/10.1038/nnano.2012.215	journal	December 2012
Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells Yu, J.; Vodyanik, M. A.; Smuga-Otto, K. Science, Vol. 318, Issue 5858 https://doi.org/10.1126/science.1151526	journal	December 2007
Cell-Directed Assembly of Bio/Nano Interfaces — A New Scheme for Cell Immobilization Baca, Helen K.; Carnes, Eric; Singh, Seema ChemInform, Vol. 38, Issue 50 https://doi.org/10.1002/chin.200750255	journal	December 2007
Induced Pluripotent Stem Cell Lines Derived From Human Somatic Cells Yu, Junying; Vodyanik, Maxim A.; Smuga-Otto, Kim Obstetrical & Gynecological Survey, Vol. 63, Issue 3 https://doi.org/10.1097/01.ogx.0000305193.72586.39	journal	January 2008
Micro-scaffold array chip for upgrading cell-based high-throughput drug testing to 3D using benchtop equipment Li, Xiaokang; Zhang, Xinyong; Zhao, Shan Lab Chip, Vol. 14, Issue 3 https://doi.org/10.1039/c3lc51103k	journal	January 2014

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Composites of Polymer Hydrogels and Nanoparticulate Systems for Biomedical and Pharmaceutical Applications Zhao, Fuli; Yao, Dan; Guo, Ruiwei Nanomaterials, Vol. 5, Issue 4 https://doi.org/10.3390/nano5042054	journal	December 2015
Bioinspired Silicification Reveals Structural Detail in Self-Assembled Peptide Cages Galloway, Johanna M.; Senior, Laura; Fletcher, Jordan M. ACS Nano, Vol. 12, Issue 2 https://doi.org/10.1021/acsnano.7b07785	journal	December 2017
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