Perfusion and endothelialization of engineered tissues with patterned vascular networks

Ian S. Kinstlinger, Gisele A. Calderon, Madison K. Royse, A. Kristen Means, Bagrat Grigoryan, Jordan S. Miller

Published: 2021-05-23 DOI: 10.1038/s41596-021-00533-1

tissue engineering

vascular networks

perfusion chambers

endothelialization

open-source protocol

AI 解读

Author Correction: Full-length sequencing of circular DNA viruses and extrachromosomal circular DNA using CIDER-Seq

Generation of heart-forming organoids from human pluripotent stem cells

Design and fabrication of wearable electronic textiles using twisted fiber-based threads

Activation of mechanoluminescent nanotransducers by focused ultrasound enables light delivery to deep-seated tissue in vivo

Chromatin accessibility profiling by ATAC-seq

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Author Correction: cfSNV: a software tool for the sensitive detection of somatic mutations from cell-free DNA

Human primordial germ cell-like cells specified from resetting precursors develop in human hindgut organoids

An inexpensive semi-automated sample processing pipeline for cell-free RNA extraction

Application of CHyMErA Cas9-Cas12a combinatorial genome-editing platform for genetic interaction mapping and gene fragment deletion screening

查看全部

Sections

Figures

References

As engineered tissues progress toward therapeutically relevant length scales and cell densities, it is critical to deliver oxygen and nutrients throughout the tissue volume via perfusion through vascular networks. Furthermore, seeding of endothelial cells
Introduction
Materials
Procedure
Troubleshooting
Timing
Anticipated results
References
ACKNOWLEDGMENTS
ACKNOWLEDGMENTS

Tien, J. Microfluidic approaches for engineering vasculature. Curr. Opin. Chem. Eng. 3, 36–41 (2014).
Kinstlinger, I. S. & Miller, J. S. 3D-printed fluidic networks as vasculature for engineered tissue. Lab Chip 16, 2025–2043 (2016).
Miller, J. S. The billion cell construct: will three-dimensional printing get us there? PLoS Biol. 12, e1001882 (2014).
Zhang, B. & Radisic, M. Organ-level vascularization: the Mars mission of bioengineering. J. Thorac. Cardiovasc. Surg. 159, 2003–2007 (2020).
Xie, R., Zheng, W., Guan, L., Ai, Y. & Liang, Q. Engineering of hydrogel materials with perfusable microchannels for building vascularized tissues. Small 16, e1902838 (2019).
Grigoryan, B. et al. Multivascular networks and functional intravascular topologies within biocompatible hydrogels. Science 364, 458–464 (2019).
Kinstlinger, I. S. et al. Generation of model tissues with dendritic vascular networks via sacrificial laser-sintered carbohydrate templates. Nat. Biomed. Eng. 4, 916–932 (2020).
Kolesky, D. B., Homan, K. A., Skylar-Scott, M. A. & Lewis, J. A. Three-dimensional bioprinting of thick vascularized tissues. Proc. Natl Acad. Sci. USA 113, 3179–3184 (2016).
Skylar-Scott, M. A. et al. Biomanufacturing of organ-specific tissues with high cellular density and embedded vascular channels. Sci. Adv. 5, eaaw2459 (2019).
Kang, H.-W. et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat. Biotechnol. 34, 312–319 (2016).
Lee, A. et al. 3D bioprinting of collagen to rebuild components of the human heart. Science 365, 482–487 (2019).
Mori, N., Akagi, Y., Imai, Y., Takayama, Y. & Kida, Y. S. Fabrication of perfusable vascular channels and capillaries in 3D liver-like tissue. Sci. Rep. 10, 5646 (2020).
Galie, P. A. et al. Fluid shear stress threshold regulates angiogenic sprouting. Proc. Natl Acad. Sci. USA 111, 7968–7973 (2014).
Polacheck, W. J. et al. A non-canonical Notch complex regulates adherens junctions and vascular barrier function. Nature 552, 258–262 (2017).
Davies, P. F. Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat. Clin. Pract. Cardiovasc. Med 6, 16–26 (2009).
Chrobak, K. M., Potter, D. R. & Tien, J. Formation of perfused, functional microvascular tubes in vitro. Microvasc. Res 71, 185–196 (2006).
Zheng, Y. et al. In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl Acad. Sci. USA 109, 9342–9347 (2012).
Mandrycky, C., Hadland, B. & Zheng, Y. 3D curvature-instructed endothelial flow response and tissue vascularization. Sci. Adv. 6, eabb3629 (2020).
Temiz, Y., Lovchik, R. D., Kaigala, G. V. & Delamarche, E. Lab-on-a-chip devices: how to close and plug the lab? Microelectron. Eng. 132, 156–175 (2015).
Maoz, B. M. et al. A linked organ-on-chip model of the human neurovascular unit reveals the metabolic coupling of endothelial and neuronal cells. Nat. Biotechnol. 36, 865–877 (2018).
Skardal, A. et al. Multi-tissue interactions in an integrated three-tissue organ-on-a-chip platform. Sci. Rep. 7, 8837 (2017).
Gray, B. L. et al. Novel interconnection technologies for integrated microfluidic systems. Sens. Actuators A Phys 77, 57–65 (1999).
Chen, C. F. et al. High-pressure needle interface for thermoplastic microfluidics. Lab Chip 9, 50–55 (2009).
Zhang, R. & Larsen, N. B. Stereolithographic hydrogel printing of 3D culture chips with biofunctionalized complex 3D perfusion networks. Lab Chip 17, 4273–4282 (2017).
Anandakrishnan, N. et al. Fast stereolithography printing of large-scale biocompatible hydrogel models. Adv. Healthc. Mater. https://doi.org/10.1002/adhm.202002103 (2021).
Ouyang, L., Armstrong, J. P. K., Chen, Q., Lin, Y. & Stevens, M. M. Void-free 3D bioprinting for in situ endothelialization and microfluidic perfusion. Adv. Funct. Mater. https://doi.org/10.1002/adfm.201908349 (2019).
Song, K. H., Highley, C. B., Rouff, A. & Burdick, J. A. Complex 3D-printed microchannels within cell-degradable hydrogels. Adv. Funct. Mater. https://doi.org/10.1002/adfm.201801331 (2018).
Brandenberg, N. & Lutolf, M. P. In situ patterning of microfluidic networks in 3D cell-laden hydrogels. Adv. Mater. 28, 7450–7456 (2016).
Tocchio, A. et al. Versatile fabrication of vascularizable scaffolds for large tissue engineering in bioreactor. Biomaterials 45, 124–131 (2015).
Lee, V. K. et al. Creating perfused functional vascular channels using 3D bio-printing technology. Biomaterials 35, 8092–8102 (2014).
Sawyer, S. W., Zhang, K., Horton, J. A. & Soman, P. Perfusion-based co-culture model system for bone tissue engineering. AIMS Bioeng. 7, 91–105 (2020).
Mao, M. et al. Human-on-leaf-chip: a biomimetic vascular system integrated with chamber-specific organs. Small 16, e2000546 (2020).
Homan, K. A. et al. Flow-enhanced vascularization and maturation of kidney organoids in vitro. Nat. Methods. 16, 255–262 (2019).
Qiu, Y. et al. Microvasculature-on-a-chip for the long-term study of endothelial barrier dysfunction and microvascular obstruction in disease. Nat. Biomed. Eng 2, 453–463 (2018).
Udan, R. S., Vadakkan, T. J. & Dickinson, M. E. Dynamic responses of endothelial cells to changes in blood flow during vascular remodeling of the mouse yolk sac. Development 140, 4041–4050 (2013).
Koike, N. et al. Tissue engineering: creation of long-lasting blood vessels. Nature 428, 138–139 (2004).
Miller, J. S. et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11, 768–774 (2012).
Moon, J. J. et al. Biomimetic hydrogels with pro-angiogenic properties. Biomaterials 31, 3840–3847 (2010).
Moya, M. L., Hsu, Y.-H., Lee, A. P., Hughes, C. C. W. & George, S. C. In vitro perfused human capillary networks. Tissue Eng. Part C Methods 19, 730–737 (2013).
Kolesky, D. B. et al. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26, 3124–3130 (2014).
Chen, Y. Y., Kingston, B. R. & Chan, W. C. W. Transcribing in vivo blood vessel networks into in vitro perfusable microfluidic devices. Adv. Mater. Technol. 5, 2000103 (2020).
Radisic, M. et al. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol. Bioeng. 93, 332–343 (2006).
Brown, D. A. et al. Analysis of oxygen transport in a diffusion-limited model of engineered heart tissue. Biotechnol. Bioeng. 97, 962–975 (2007).
Cheema, U., Brown, R. A., Alp, B. & MacRobert, A. J. Spatially defined oxygen gradients and vascular endothelial growth factor expression in an engineered 3D cell model. Cell Mol. Life Sci. 65, 177–186 (2008).
Lewis, M. C., MacArthur, B. D., Malda, J., Pettet, G. & Please, C. P. Heterogeneous proliferation within engineered cartilaginous tissue: the role of oxygen tension. Biotechnol. Bioeng. 91, 607–615 (2005).
Demol, J., Lambrechts, D., Geris, L., Schrooten, J. & Van Oosterwyck, H. Towards a quantitative understanding of oxygen tension and cell density evolution in fibrin hydrogels. Biomaterials 32, 107–118 (2011).
Hillebrandt, K. H. et al. Strategies based on organ decellularization and recellularization. Transpl. Int. 32, 571–585 (2019).
Guyette, J. P. et al. Perfusion decellularization of whole organs. Nat. Protoc. 9, 1451–1468 (2014).
Zheng, Y., Chen, J. & López, J. A. Microvascular platforms for the study of platelet-vessel wall interactions. Thromb. Res. 133, 525–531 (2014).
Arakawa, C. et al. Biophysical and biomolecular interactions of malaria-infected erythrocytes in engineered human capillaries. Sci. Adv. 6, eayy7243 (2020).
Zhang, B. & Radisic, M. Organ-on-a-chip devices advance to market. Lab Chip 17, 2395–2420 (2017).
Sontheimer-Phelps, A., Hassell, B. A. & Ingber, D. E. Modelling cancer in microfluidic human organs-on-chips. Nat. Rev. Cancer 19, 65–81 (2019).
Cybulski, O., Garstecki, P. & Grzybowski, B. A. Oscillating droplet trains in microfluidic networks and their suppression in blood flow. Nat. Phys. 15, 706–713 (2019).
Peel, S. et al. Introducing an automated high content confocal imaging approach for Organs-on-Chips. Lab Chip 19, 410–421 (2019).
Ewart, L. et al. Application of microphysiological systems to enhance safety assessment in drug discovery. Annu. Rev. Pharmacol. Toxicol 58, 65–82 (2018).
Novak, R. et al. Robotic fluidic coupling and interrogation of multiple vascularized organ chips. Nat. Biomed. Eng. 4, 407–420 (2020).
Herland, A. et al. Quantitative prediction of human pharmacokinetic responses to drugs via fluidically coupled vascularized organ chips. Nat. Biomed. Eng 4, 421–436 (2020).
Marquis, K. et al. Vascularized polymers spatially control bacterial cells on surfaces. Adv. Biosyst. 4, 1900216 (2020).
Miller, J. S. et al. Bioactive hydrogels made from step-growth derived PEG-peptide macromers. Biomaterials 31, 3736–3743 (2010).
Gholipourmalekabadi, M., Zhao, S., Harrison, B. S., Mozafari, M. & Seifalian, A. M. Oxygen-generating biomaterials: a new, viable paradigm for tissue engineering? Trends Biotechnol. 34, 1010–1021 (2016).
Erdem, A. et al. 3D bioprinting of oxygenated cell-laden gelatin methacryloyl constructs. Adv Healthc. Mater. 9, 1901794 (2020).
Zhu, W. et al. Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomaterials 124, 106–115 (2017).
Colosi, C., Costantini, M., Barbetta, A. & Dentini, M. Microfluidic bioprinting of heterogeneous 3D tissue constructs. Methods Mol. Biol. 1612, 369–380 (2017).
Noor, N. et al. 3D printing of personalized thick and perfusable cardiac patches and hearts. Adv. Sci. 6, 1900344 (2019).
Loessner, D. et al. Functionalization, preparation and use of cell-laden gelatin methacryloyl–based hydrogels as modular tissue culture platforms. Nat. Protoc. 11, 727–746 (2016).
Elbert, D. L. & Hubbell, J. A. Conjugate addition reactions combined with free-radical cross-linking for the design of materials for tissue engineering. Biomacromolecules 2, 430–441 (2001).
Fairbanks, B., Schwartz, M., Bowman, C. & Anseth, K. Photoinitiated polymerisation of PEG-diacrylate with lithium phenyl-2,4,6-trimethylbenzoylphosphinate: polymerisation rate ans cytocompatibility. Biomaterials 30, 6702–6707 (2009).
Miller, L. R. et al. Considering sex as a biological variable in preclinical research. FASEB J. 31, 29–34 (2017).
Marin, V., Kaplanski, G., Grès, S., Farnarier, C. & Bongrand, P. Endothelial cell culture: protocol to obtain and cultivate human umbilical endothelial cells. J. Immunol. Methods 254, 183–190 (2001).
Price, G. M. et al. Effect of mechanical factors on the function of engineered human blood microvessels in micro fluidic collagen gels. Biomaterials 31, 6182–6189 (2010).
Bertassoni, L. E. et al. Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 14, 2202–2211 (2014).
Song, H. H. G. et al. Transient support from fibroblasts is sufficient to drive functional vascularization in engineered tissues. Adv. Func. Mater. 30, 2003777 (2020).

Perfusion and endothelialization of engineered tissues with patterned vascular networks

Supplementary information

推荐阅读