zbMATH — the first resource for mathematics

Using sacrificial cell spheroids for the bioprinting of perfusable 3D tissue and organ constructs: a computational study. (English) Zbl 1423.92110
Summary: A long-standing problem in tissue engineering is the biofabrication of perfusable tissue constructs that can be readily connected to the patient’s vasculature. It was partially solved by three-dimensional (3D) printing of sacrificial material (e.g., hydrogel) strands: upon incorporation in another cell-laden hydrogel, the strands were removed, leaving behind perfusable channels. Their complexity, however, did not match that of the native vasculature. Here, we propose to use multicellular spheroids as a sacrificial material and investigate their potential benefits in the context of 3D bioprinting of cell aggregates and/or cell-laden hydrogels. Our study is based on computer simulations of postprinting cellular rearrangements. The computational model of the biological system is built on a cubic lattice, whereas its evolution is simulated using the Metropolis Monte Carlo algorithm. The simulations describe structural changes in three types of tissue constructs: a tube made of a single cell type, a tube made of two cell types, and a cell-laden hydrogel slab that incorporates a branching tube. In all three constructs, the lumen is obtained after the elimination of the sacrificial cell population. Our study suggests that sacrificial cell spheroids (sacrospheres) enable one to print tissue constructs outfitted with a finer and more complex network of channels than the ones obtained so far. Moreover, cellular interactions might give rise to a tissue microarchitecture that lies beyond the bioprinter’s resolution. Although more expensive than inert materials, sacrificial cells have the potential to bring further progress towards the biofabrication of fully vascularized tissue substitutes.
92C50 Medical applications (general)
Full Text: DOI
[1] Khademhosseini, A.; Langer, R., A decade of progress in tissue engineering, Nature Protocols, 11, 10, 1775-1781, (2016)
[2] Rouwkema, J.; Khademhosseini, A., Vascularization and angiogenesis in tissue engineering: beyond creating static networks, Trends in Biotechnology, 34, 9, 733-745, (2016)
[3] Visconti, R. P.; Kasyanov, V.; Gentile, C.; Zhang, J.; Markwald, R. R.; Mironov, V., Towards organ printing: engineering an intra-organ branched vascular tree, Expert Opinion on Biological Therapy, 10, 3, 409-420, (2010)
[4] Miller, J. S.; Stevens, K. R.; Yang, M. T., Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues, Nature Materials, 11, 9, 768-774, (2012)
[5] Kolesky, D. B.; Homan, K. A.; Skylar-Scott, M. A.; Lewis, J. A., Three-dimensional bioprinting of thick vascularized tissues, Proceedings of the National Academy of Sciences, 113, 12, 3179-3184, (2016)
[6] Kolesky, D. B.; Truby, R. L.; Gladman, A. S.; Busbee, T. A.; Homan, K. A.; Lewis, J. A., 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs, Advanced Materials, 26, 19, 3124-3130, (2014)
[7] Tamarov, K. P.; Osminkina, L. A.; Zinovyev, S. V., Radio frequency radiation-induced hyperthermia using Si nanoparticle-based sensitizers for mild cancer therapy, Scientific Reports, 4, 1, 7034, (2014)
[8] Park, J.-H.; Gu, L.; von Maltzahn, G.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J., Biodegradable luminescent porous silicon nanoparticles for in vivo applications, Nature Materials, 8, 4, 331-336, (2009)
[9] Jang, B.; Park, J.-Y.; Tung, C.-H.; Kim, I.-H.; Choi, Y., Gold nanorod−photosensitizer complex for near-infrared fluorescence imaging and photodynamic/photothermal therapy in vivo, ACS Nano, 5, 2, 1086-1094, (2011)
[10] Moan, J.; Berg, K., The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen, Photochemistry and Photobiology, 53, 4, 549-553, (1991)
[11] Davies, J. A.; Cachat, E., Synthetic biology meets tissue engineering, Biochemical Society Transactions, 44, 3, 696-701, (2016)
[12] Cachat, E.; Liu, W.; Hohenstein, P.; Davies, J. A., A library of mammalian effector modules for synthetic morphology, Journal of Biological Engineering, 8, 1, 26, (2014)
[13] Amar, J. G., The Monte Carlo method in science and engineering, Computing in Science & Engineering, 8, 2, 9-19, (2006)
[14] Robu, A.; Aldea, R.; Munteanu, O.; Neagu, M.; Stoicu-Tivadar, L.; Neagu, A., Computer simulations of in vitro morphogenesis, Biosystems, 109, 3, 430-443, (2012)
[15] Jakab, K.; Neagu, A.; Mironov, V.; Markwald, R. R.; Forgacs, G., Engineering biological structures of prescribed shape using self-assembling multicellular systems, Proceedings of the National Academy of Sciences, 101, 9, 2864-2869, (2004)
[16] Neagu, A.; Jakab, K.; Jamison, R.; Forgacs, G., Role of physical mechanisms in biological self-organization, Physical Review Letters, 95, 17, (2005)
[17] Steinberg, M. S., Differential adhesion in morphogenesis: a modern view, Current Opinion in Genetics & Development, 17, 4, 281-286, (2007)
[18] Shafiee, A.; McCune, M.; Forgacs, G.; Kosztin, I., Post-deposition bioink self-assembly: a quantitative study, Biofabrication, 7, 4, (2015)
[19] Thomas, G. L.; Mironov, V.; Nagy-Mehez, A.; Mombach, J. C. M., Dynamics of cell aggregates fusion: experiments and simulations, Physica A: Statistical Mechanics and its Applications, 395, 247-254, (2014)
[20] Norotte, C.; Marga, F. S.; Niklason, L. E.; Forgacs, G., Scaffold-free vascular tissue engineering using bioprinting, Biomaterials, 30, 30, 5910-5917, (2009)
[21] Robu, A.; Stoicu-Tivadar, L., SIMMMC—an informatic application for modeling and simulating the evolution of multicellular systems in the vicinity of biomaterials, Romanian Journal of Biophysics, 26, 3, 145-162, (2016)
[22] Neagu, A., Role of computer simulation to predict the outcome of 3D bioprinting, Journal of 3D Printing in Medicine, 1, 2, 103-121, (2017)
[23] Beysens, D. A.; Forgacs, G.; Glazier, J. A., Cell sorting is analogous to phase ordering in fluids, Proceedings of the National Academy of Sciences, 97, 17, 9467-9471, (2000)
[24] Robu, A.; Robu, N.; Neagu, A., New software tools for hydrogel-based bioprinting, Proceedings of the 2018 IEEE 12th International Symposium on Applied Computational Intelligence and Informatics (SACI)
[25] Humphrey, W.; Dalke, A.; Schulten, K., VMD: visual molecular dynamics, Journal of Molecular Graphics, 14, 1, 33-38, (1996)
[26] De Moor, L.; Merovci, I.; Baetens, S., High-throughput fabrication of vascularized spheroids for bioprinting, Biofabrication, 10, 3, (2018)
[27] Murphy, S. V.; Atala, A., 3D bioprinting of tissues and organs, Nature Biotechnology, 32, 8, 773-785, (2014)
[28] Mekhileri, N. V.; Lim, K. S.; Brown, G. C. J., Automated 3D bioassembly of micro-tissues for biofabrication of hybrid tissue engineered constructs, Biofabrication, 10, 2, (2018)
[29] Moldovan, N. I.; Hibino, N.; Nakayama, K., Principles of the Kenzan method for robotic cell spheroid-based three-dimensional bioprinting, Tissue Engineering Part B: Reviews, 23, 3, 237-244, (2017)
[30] Tseng, T. C.; Wong, C. W.; Hsieh, F. Y.; Hsu, S. H., Biomaterial substrate-mediated multicellular spheroid formation and their applications in tissue engineering, Biotechnology Journal, 12, 12, (2017)
[31] Mironov, V.; Visconti, R. P.; Kasyanov, V.; Forgacs, G.; Drake, C. J.; Markwald, R. R., Organ printing: tissue spheroids as building blocks, Biomaterials, 30, 12, 2164-2174, (2009)
[32] Rezende, R. A.; Pereira, F. D. A. S.; Kasyanov, V., Scalable biofabrication of tissue spheroids for organ printing, Procedia CIRP, 5, 276-281, (2013)
[33] Dechristé, G.; Fehrenbach, J.; Griseti, E.; Lobjois, V.; Poignard, C., Viscoelastic modeling of the fusion of multicellular tumor spheroids in growth phase, Journal of Theoretical Biology, 454, 102-109, (2018) · Zbl 1406.92291
[34] Yang, X.; Mironov, V.; Wang, Q., Modeling fusion of cellular aggregates in biofabrication using phase field theories, Journal of Theoretical Biology, 303, 110-118, (2012) · Zbl 1337.92050
[35] Shafiee, A.; McCune, M.; Kosztin, I.; Forgacs, G., Shape evolution of multicellular systems; application to tissue engineering, Biophysical Journal, 106, 2, 618, (2014)
[36] Yu, Z.; Yang, L.; Shuangshuang, M.; Wei, S.; Rui, Y., The influence of printing parameters on cell survival rate and printability in microextrusion-based 3D cell printing technology, Biofabrication, 7, 4, (2015)
[37] Pereira, F. D. A. S.; Parfenov, V.; Khesuani, Y. D.; Ovsianikov, A.; Mironov, V.; Ovsianikov, A.; Yoo, J.; Mironov, V., Commercial 3D bioprinters, 3D Printing and Biofabrication. Reference Series in Biomedical Engineering, (2018), Springer, Cham, Switzerland
[38] Itoh, M.; Nakayama, K.; Noguchi, R., Scaffold-free tubular tissues created by a bio-3D printer undergo remodeling and endothelialization when implanted in rat aortae, PLoS One, 10, 9, (2015)
[39] Tertemiz, F.; Kayisli, U. A.; Arici, A.; Demir, R., Apoptosis contributes to vascular lumen formation and vascular branching in human placental vasculogenesis, Biology of Reproduction, 72, 3, 727-735, (2005)
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. It attempts to reflect the references listed in the original paper as accurately as possible without claiming the completeness or perfect precision of the matching.