Generation of model tissues with dendritic vascular networks via sacrificial laser-sintered carbohydrate templates.
Journal
Nature biomedical engineering
ISSN: 2157-846X
Titre abrégé: Nat Biomed Eng
Pays: England
ID NLM: 101696896
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
27
09
2018
accepted:
01
05
2020
pubmed:
1
7
2020
medline:
18
11
2020
entrez:
1
7
2020
Statut:
ppublish
Résumé
Sacrificial templates for patterning perfusable vascular networks in engineered tissues have been constrained in architectural complexity, owing to the limitations of extrusion-based 3D printing techniques. Here, we show that cell-laden hydrogels can be patterned with algorithmically generated dendritic vessel networks and other complex hierarchical networks by using sacrificial templates made from laser-sintered carbohydrate powders. We quantified and modulated gradients of cell proliferation and cell metabolism emerging in response to fluid convection through these networks and to diffusion of oxygen and metabolites out of them. We also show scalable strategies for the fabrication, perfusion culture and volumetric analysis of large tissue-like constructs with complex and heterogeneous internal vascular architectures. Perfusable dendritic networks in cell-laden hydrogels may help sustain thick and densely cellularized engineered tissues, and assist interrogations of the interplay between mass transport and tissue function.
Identifiants
pubmed: 32601395
doi: 10.1038/s41551-020-0566-1
pii: 10.1038/s41551-020-0566-1
doi:
Substances chimiques
Carbohydrates
0
Hydrogels
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
916-932Subventions
Organisme : NIDDK NIH HHS
ID : R01 DK115461
Pays : United States
Organisme : NHLBI NIH HHS
ID : F31 HL140905
Pays : United States
Organisme : NHLBI NIH HHS
ID : DP2 HL137188
Pays : United States
Organisme : NIBIB NIH HHS
ID : T32 EB001650
Pays : United States
Commentaires et corrections
Type : ErratumIn
Références
Zamir, M. Fractal dimensions and multifractility in vascular branching. J. Theor. Biol. 212, 183–190 (2001).
pubmed: 11531384
West, G. B., Brown, J. H. & Enquist, B. J. A general model for the origin of allometric scaling laws in biology. Science 276, 122–126 (1997).
West, G. B., Brown, J. H. & Enquist, B. J. A general model for ontogenetic growth. Nature 413, 628–631 (2001).
pubmed: 11675785
Monahan-Earley, R., Dvorak, A. M. & Aird, W. C. Evolutionary origins of the blood vascular system and endothelium. J. Thromb. Haemost. 11, 46–66 (2013).
pubmed: 23809110
pmcid: 5378490
Novosel, E. C., Kleinhans, C. & Kluger, P. J. Vascularization is the key challenge in tissue engineering. Adv. Drug Deliv. Rev. 63, 300–311 (2011).
pubmed: 21396416
Kinstlinger, I. S. & Miller, J. S. 3D-printed fluidic networks as vasculature for engineered tissue. Lab Chip 16, 2025–2043 (2016).
pubmed: 27173478
Cabodi, M. et al. A microfluidic biomaterial. J. Am. Chem. Soc. 127, 13788–13789 (2005).
pubmed: 16201789
Chrobak, K. M., Potter, D. R. & Tien, J. Formation of perfused, functional microvascular tubes in vitro. Microvasc. Res. 71, 185–196 (2006).
pubmed: 16600313
Zhang, B. et al. Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat. Mater. 15, 669–678 (2016).
pubmed: 26950595
pmcid: 4879054
Miller, J. S. The billion cell construct: will three-dimensional printing get us there? PLoS Biol. 12, e1001882 (2014).
pubmed: 24937565
pmcid: 4061004
Luo, Y., Lode, A. & Gelinsky, M. Direct plotting of three-dimensional hollow fiber scaffolds based on concentrated alginate pastes for tissue engineering. Adv. Healthc. Mater. 2, 777–783 (2013).
pubmed: 23184455
Christensen, K. et al. Freeform inkjet printing of cellular structures with bifurcations. Biotechnol. Bioeng. 112, 1047–1055 (2015).
pubmed: 25421556
Hinton, T. J. et al. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci. Adv. 1, e1500758 (2015).
pubmed: 26601312
pmcid: 4646826
Lee, A. et al. 3D bioprinting of collagen to rebuild components of the human heart. Science 365, 482–487 (2019).
pubmed: 31371612
Zhang, R. & Larsen, N. B. Stereolithographic hydrogel printing of 3D culture chips with biofunctionalized complex 3D perfusion networks. Lab Chip 17, 4273–4282 (2017).
pubmed: 29116271
Meyer, W. et al. Soft polymers for building up small and smallest blood supplying systems by stereolithography. J. Funct. Biomater. 3, 257–268 (2012).
pubmed: 24955530
pmcid: 4047929
Brandenberg, N. & Lutolf, M. P. In situ patterning of microfluidic networks in 3D cell-laden hydrogels. Adv. Mater. 28, 7450–7456 (2016).
pubmed: 27334545
Heintz, K. A. et al. Fabrication of 3D biomimetic microfluidic networks in hydrogels. Adv. Healthc. Mater. 5, 2153–2160 (2016).
pubmed: 27239785
pmcid: 5014628
Arakawa, C. K., Badeau, B. A., Zheng, Y. & DeForest, C. A. Multicellular vascularized engineered tissues through user-programmable biomaterial photodegradation. Adv. Mat. 29, 1703156 (2017).
Grigoryan, B. et al. Functional intravascular topologies and multivascular networks within biocompatible hydrogels. Science 364, 458–464 (2019).
pubmed: 31048486
pmcid: 7769170
Golden, A. P. & Tien, J. Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip 7, 720–725 (2007).
pubmed: 17538713
Miller, J. S. et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11, 768–774 (2012).
pubmed: 22751181
pmcid: 3586565
Bégin-Drolet, A. et al. Design of a 3D printer head for additive manufacturing of sugar glass for tissue engineering applications. Addit. Manuf. 15, 29–39 (2017).
Gelber, M. K., Hurst, G., Comi, T. J. & Bhargava, R. Model-guided design and characterization of a high-precision 3D printing process for carbohydrate glass. Addit. Manuf. 22, 38–50 (2018).
Homan, K. A. et al. Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci. Rep. 6, 34845 (2016).
pubmed: 27725720
pmcid: 5057112
Kolesky, D. B. et al. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv. Mater. 26, 3124–3130 (2014).
pubmed: 24550124
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).
pubmed: 26951646
pmcid: 4812707
Skylar-Scott, M. A. et al. Biomanufacturing of organ-specific tissues with high cellular density and embedded vascular channels. Sci. Adv. 5, eaaw2459 (2019).
pubmed: 31523707
pmcid: 6731072
Wu, W., Deconinck, A. & Lewis, J. A. Omnidirectional printing of 3D microvascular networks. Adv. Mater. 23, H178–H183 (2011).
pubmed: 21438034
Song, K. H., Highley, C. B., Rouff, A. & Burdick, J. A. Complex 3D-printed microchannels within cell-degradable hydrogels. Adv. Funct. Mater. 28, 1801331 (2018).
Pimentel, C. R. et al. Three-dimensional fabrication of thick and densely populated soft constructs with complex and actively perfused channel network. Acta Biomater. 65, 174–184 (2018).
Kinstlinger, I. S. et al. Open-source selective laser sintering (OpenSLS) of nylon and biocompatible polycaprolactone. PLoS ONE 11, e0147399 (2016).
pubmed: 26841023
pmcid: 4739701
Roszelle, B. N. et al. Flow diverter effect on cerebral aneurysm hemodynamics: An in vitro comparison of telescoping stents and the Pipeline. Neuroradiology 55, 751–758 (2013).
pubmed: 23515661
Saggiomo, V. & Velders, A. H. Simple 3D printed scaffold-removal method for the fabrication of intricate microfluidic devices. Adv. Sci. 2, 1500125 (2015).
Nguyen, L. H. et al. Vascularized bone tissue engineering: approaches for potential improvement. Tissue Eng. Part B 18, 363–382 (2012).
Nguyen, Q. T., Hwang, Y., Chen, A. C., Varghese, S. & Sah, R. L. Cartilage-like mechanical properties of poly (ethylene glycol)-diacrylate hydrogels. Biomaterials 33, 6682–6690 (2012).
pubmed: 22749448
pmcid: 3572364
Partlow, B. P. et al. Highly tunable elastomeric silk biomaterials. Adv. Funct. Mater. 24, 4615–4624 (2014).
pubmed: 25395921
pmcid: 4225629
Mooney, R., Tawil, B. & Mahoney, M. Specific fibrinogen and thrombin concentrations promote neuronal rather than glial growth when primary neural cells are seeded within plasma-derived fibrin gels. Tissue Eng. Part A 16, 1607–1619 (2010).
pubmed: 20028220
Duong, H., Wu, B. & Tawil, B. Modulation of 3D fibrin matrix stiffness by intrinsic fibrinogen–thrombin compositions and by extrinsic cellular activity. Tissue Eng. Part A 15, 1865–1876 (2009).
pubmed: 19309239
pmcid: 2749875
Subhash, G., Liu, Q., Moore, D. F., Ifju, P. G. & Haile, M. A. Concentration dependence of tensile behavior in agarose gel using digital image correlation. Exp. Mech. 51, 255–262 (2011).
Feugier, F. G., Mochizuki, A. & Iwasa, Y. Self-organization of the vascular system in plant leaves: inter-dependent dynamics of auxin flux and carrier proteins. J. Theor. Biol. 236, 366–375 (2005).
pubmed: 15899502
Fujita, H. & Mochizuki, A. The origin of the diversity of leaf venation pattern. Dev. Dyn. 235, 2710–2721 (2006).
pubmed: 16894601
Runions, A., Lane, B. & Prusinkiewicz, P. Modeling trees with a space colonization algorithm. In Proc. 3rd Eurographics Conference on Natural Phenomena (Eds Ebert, D. & Mérillou, S.) 63–70 (Eurographics Association, 2007).
Murray, C. D. The physiological principle of minimum work applied to the angle of branching of arteries. J. Gen. Physiol. 9, 835–841 (1926).
pubmed: 19872299
pmcid: 2140901
Miguel, A. F. Dendritic design as an archetype for growth patterns in nature: fractal and constructal views. Front. Phys. 2, 9 (2014).
Moon, J. J. et al. Biomimetic hydrogels with pro-angiogenic properties. Biomaterials 31, 3840–3847 (2010).
pubmed: 20185173
pmcid: 2839536
Calderon, G. et al. Tubulogenesis of co-cultured human iPS-derived endothelial cells and human mesenchymal stem cells in fibrin and gelatin methacrylate gels. Biomater. Sci. 5, 1652–1660 (2017).
pubmed: 28661522
Eskin, S. G., Ives, C., McIntire, L. & Navarro, L. Response of cultured endothelial cells to steady flow. Microvasc. Res. 28, 87–94 (1984).
pubmed: 6748961
Yang, P. J. & Temenoff, J. S. Engineering orthopedic tissue interfaces. Tissue Eng. Part B 15, 127–141 (2009).
Eckes, B. et al. Fibroblast-matrix interactions in wound healing and fibrosis. Matrix Biol. 19, 325–332 (2000).
pubmed: 10963993
Lu, P., Weaver, V. M. & Werb, Z. The extracellular matrix: a dynamic niche in cancer progression. J. Cell Biol. 196, 395–406 (2012).
pubmed: 22351925
pmcid: 3283993
Radisic, M. et al. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol. Bioeng. 93, 332–343 (2006).
pubmed: 16270298
Tocchio, A. et al. Versatile fabrication of vascularizable scaffolds for large tissue engineering in bioreactor. Biomaterials 45, 124–131 (2015).
pubmed: 25662502
Tsang, V. L. et al. Fabrication of 3D hepatic tissues by additive photopatterning of cellular hydrogels. FASEB J. 21, 790–801 (2007).
Krogh, A. The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J. Physiol. 52, 409–415 (1919).
pubmed: 16993405
pmcid: 1402716
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).
pubmed: 16025534
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).
pubmed: 20880579
Gu, W. Y., Yao, H., Huang, C. Y. & Cheung, H. S. New insight into deformation-dependent hydraulic permeability of gels and cartilage, and dynamic behavior of agarose gels in confined compression. J. Biomech. 36, 593–598 (2003).
pubmed: 12600349
Chuppa, S. et al. Fermentor temperature as a tool for control of high-density perfusion cultures of mammalian cells. Biotechnol. Bioeng. 55, 328–338 (1997).
pubmed: 18636491
Ducommun, P., Ruffieux, P. A., Kadouri, A., Von Stockar, U. & Marison, I. W. Monitoring of temperature effects on animal cell metabolism in a packed bed process. Biotechnol. Bioeng. 77, 838–842 (2002).
pubmed: 11835145
Jorjani, P. & Ozturk, S. S. Effects of cell density and temperature on oxygen consumption rate for different mammalian cell lines. Biotechnol. Bioeng. 64, 349–356 (1999).
pubmed: 10397872
Xiang, C. et al. Long-term functional maintenance of primary human hepatocytes in vitro. Science 364, 399–402 (2019).
pubmed: 31023926
Bhatia, S. N., Balis, U. J., Yarmush, M. L. & Toner, M. Effect of cell–cell interactions in preservation of cellular phenotype: cocultivation of hepatocytes and nonparenchymal cells. FASEB J. 13, 1883–1900 (1999).
pubmed: 10544172
Stevens, K. R. et al. InVERT molding for scalable control of tissue microarchitecture. Nat. Commun. 4, 1847 (2013).
pubmed: 23673632
Stevens, K. R. et al. In situ expansion of engineered human liver tissue in a mouse model of chronic liver disease. Sci. Transl. Med. 9, eaah5505 (2017).
pubmed: 28724577
pmcid: 5896001
Khetani, S. R. & Bhatia, S. N. Microscale culture of human liver cells for drug development. Nat. Biotechnol. 26, 120–126 (2008).
pubmed: 18026090
Bhatia, S. N., Underhill, G. H., Zaret, K. S. & Fox, I. J. Cell and tissue engineering for liver disease. Sci. Transl. Med. 6, 245sr2 (2014).
pubmed: 25031271
pmcid: 4374645
Rafii, S., Butler, J. M. & Ding, B.-S. Angiocrine functions of organ-specific endothelial cells. Nature 529, 316–325 (2016).
pubmed: 4878406
pmcid: 4878406
Baranski, J. D. et al. Geometric control of vascular networks to enhance engineered tissue integration and function. Proc. Natl Acad. Sci USA 110, 7586–7591 (2013).
pubmed: 23610423
pmcid: 3651499
Mirabella, T. et al. 3D-printed vascular networks direct therapeutic angiogenesis in ischaemia. Nat. Biomed. Eng. 1, 0083 (2017).
pubmed: 29515935
pmcid: 5837070
Lindström, N. O. et al. Conserved and divergent molecular and anatomic features of human and mouse nephron patterning. J. Am. Soc. Nephrol. 29, 825–840 (2018).
pubmed: 29449451
pmcid: 5827611
Bosco, D. et al. Unique arrangement of α- and β-cells in human islets of Langerhans. 59, 1202–1210 (2010).
Wang, X.-N. et al. A three-dimensional atlas of human dermal leukocytes, lymphatics, and blood vessels. J. Invest. Dermatol. 134, 965–974 (2014).
pubmed: 24352044
Kang, H.-W. et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat. Biotechnol. 34, 312–319 (2016).
pubmed: 26878319
Shapiro, A. J. et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regime. N. Engl. J. Med. 343, 230–238 (2000).
pubmed: 10911004
Iansante, V., Mitry, R. R., Filippi, C., Fitzpatrick, E. & Dhawan, A. Human hepatocyte transplantation for liver disease: current status and future perspectives. Pediatr. Res. 83, 232–240 (2018).
pubmed: 29149103
Parker Ponder, K. et al. Mouse hepatocytes migrate to liver parenchyma and function indefinitely after intrasplenic transplantation. Proc. Natl Acad. Sci. USA 88, 1217–1221 (1991).
Truslow, J. G. & Tien, J. Perfusion systems that minimize vascular volume fraction in engineered tissues. Biomicrofluidics 5, 022201 (2011).
pmcid: 3145227
Ronellenfitsch, H. & Katifori, E. Global optimization, local adaptation, and the role of growth in distribution networks. Phys. Rev. Lett. 117, 138301 (2016).
pubmed: 27715085
Freeman, R. Measuring the flow properties of consolidated, conditioned and aerated powders—a comparative study using a powder rheometer and a rotational shear cell. Powder Technol. 174, 25–33 (2007).
Thadavirul, N., Pavasant, P. & Supaphol, P. Development of polycaprolactone porous scaffolds by combining solvent casting, particulate leaching, and polymer leaching techniques for bone tissue engineering. J. Biomed. Mater. Res. A 102, 3379–3392 (2013).
pubmed: 24132871
Miller, J. S. et al. Bioactive hydrogels made from step-growth derived PEG-peptide macromers. Biomaterials 31, 3736–3743 (2010).
pubmed: 20138664
pmcid: 2837100
Rockwood, D. N. et al. Materials fabrication from Bombyx mori silk fibroin. Nat. Protoc. 6, 1612–1631 (2011).
pubmed: 21959241
Li, W., Germain, R. N. & Gerner, M. Y. Multiplex, quantitative cellular analysis in large tissue volumes with clearing-enhanced 3D microscopy (C
pubmed: 5584454
pmcid: 5584454
Thielicke, W. & Stamhuis, E. J. PIVlab—towards user-friendly, affordable and accurate digital particle image velocimetry in MATLAB. J. Open Res. Softw. 2, e30 (2014).
Thielicke, W. The Flapping Flight of Birds—Analysis and Application. PhD thesis, Rijksuniversiteit Groningen (2014).
Thielicke, W. & Stamhuis, E. J. PIVlab—time-resolved digital particle image velocimetry tool for MATLAB https://doi.org/10.6084/M9.FIGSHARE.1092508.V5 (2014).
Cheng, N.-S. Formula for the viscosity of a glycerol–water mixture. Ind. Eng. Chem. Res. 47, 3285–3288 (2008).
Volk, A. & Kähler, C. J. Density model for aqueous glycerol solutions. Exp. Fluids 59, 75 (2018).
van de Loosdrecht, A. A., Beelen, R. H., Ossenkoppele, G. J., Broekhoven, M. G. & Langenhuijsen, M. M. A tetrazolium-based colorimetric MTT assay to quantitate human monocyte mediated cytotoxicity against leukemic cells from cell lines and patients with acute myeloid leukemia. J. Immunol. Methods 174, 311–320 (1994).
pubmed: 8083535
Ahrens, J., Geveci, B. & Law, C. in The Visualization Handbook (eds Hansen, C. D. & Johnson, C. R.) 717–731 (2005).