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Tissue engineering toward organ-specific regeneration and disease modeling

Published online by Cambridge University Press:  31 July 2017

Christian Mandrycky ,
Kiet Phong  and
Ying Zheng
Christian Mandrycky
Affiliation:
Departments of Bioengineering, Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, WA, USA
Kiet Phong
Affiliation:
Departments of Bioengineering, Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, WA, USA
Ying Zheng*
Affiliation:
Departments of Bioengineering, Institute for Stem Cell and Regenerative Medicine, University of Washington, Seattle, WA, USA
*
Address all correspondence to Ying Zheng at yingzy@uw.edu
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Abstract

Tissue engineering has been recognized as a translational approach to replace damaged tissue or whole organs. Engineering tissue, however, faces an outstanding knowledge gap in the challenge to fully recapitulate complex organ-specific features. Major components, such as cells, matrix, and architecture, must each be carefully controlled to engineer tissue-specific structure and function that mimics what is found in vivo. Here we review different methods to engineer tissue, and discuss critical challenges in recapitulating the unique features and functional units in four major organs—the kidney, liver, heart, and lung, which are also the top four candidates for organ transplantation in the USA. We highlight advances in tissue engineering approaches to enable the regeneration of complex tissue and organ substitutes, and provide tissue-specific models for drug testing and disease modeling. We discuss the current challenges and future perspectives toward engineering human tissue models.

Type
Biomaterials for 3D Cell Biology Prospective Articles
Information
MRS Communications , Volume 7 , Issue 3 , September 2017 , pp. 332 - 347
Copyright
Copyright © Materials Research Society 2017 

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References

1.MacNeil, S.: Progress and opportunities for tissue-engineered skin. Nature 445, 874 (2007).Google Scholar
2.Atala, A., Bauer, S.B., Soker, S., Yoo, J.J., and Retik, A.B.: Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 367, 1241 (2006).Google Scholar
3.Bhatia, S.N. and Ingber, D.E.: Microfluidic organs-on-chips. Nat. Biotechnol. 32, 760 (2014).Google Scholar
4.Wikswo, J.P.: The relevance and potential roles of microphysiological systems in biology and medicine. Exp. Biol. Med. (Maywood) 239, 1061 (2014).Google Scholar
5.Weber, E.J., Chapron, A., Chapron, B.D., Voellinger, J.L., Lidberg, K.A., Yeung, C.K., Wang, Z., Yamaura, Y., Hailey, D.W., Neumann, T., Shen, D.D., Thummel, K.E., Muczynski, K.A., Himmelfarb, J., and Kelly, E.J.: Development of a microphysiological model of human kidney proximal tubule function. Kidney Int. 90, 627 (2016).Google Scholar
6.Fernandez, C.E., Yen, R.W., Perez, S.M., Bedell, H.W., Povsic, T.J., Reichert, W.M., and Truskey, G.A.: Human vascular microphysiological system for in vitro drug screening. Sci. Rep. 6, 21579 (2016).Google Scholar
7.Mathur, A., Loskill, P., Shao, K., Huebsch, N., Hong, S., Marcus, S.G., Marks, N., Mandegar, M., Conklin, B.R., Lee, L.P., and Healy, K.E.: Human iPSC-based cardiac microphysiological system for drug screening applications. Sci. Rep. 5, 8883 (2015).Google Scholar
8.Atala, A., Kasper, F.K., and Mikos, A.G.: Engineering complex tissues. Sci Transl. Med. 4, 160rv12 (2012).Google Scholar
9.Mikos, A.G., Herring, S.W., Ochareon, P., Elisseeff, J., Lu, H.H., Kandel, R., Schoen, F.J., Toner, M., Mooney, D., Atala, A., Van Dyke, M.E., Kaplan, D., and Vunjak-Novakovic, G.: Engineering complex tissues. Tissue Eng. 12, 3307 (2006).Google Scholar
10.Kellar, C.A.: Solid organ transplantation overview and delection criteria. Am. J. Manag. Care 21, S4 (2015).Google Scholar
11.Magee, J.C., Barr, M.L., Basadonna, G.P., Johnson, M.R., Mahadevan, S., McBride, M.A., Schaubel, D.E., and Leichtman, A.B.: Repeat organ transplantation in the United States, 1996–2005. Am. J. Transplant. 7, 1424 (2007).Google Scholar
12.Pocock, G., Richards, C.D., and Richards, D.A.: Human Physiology (Oxford University Press, 2013).Google Scholar
13.Jen, K.-Y., Haragsim, L., and Laszik, Z.G.: Kidney microvasculature in health and disease. Exp. Model. Ren. Dis. Pathog. Diagn. 169, 51 (2011).Google Scholar
14.Basile, D.P.: The endothelial cell in ischemic acute kidney injury: implications for acute and chronic function. Kidney Int. 72, 151 (2007).Google Scholar
15.Basile, D.P., Friedrich, J.L., Spahic, J., Knipe, N., Mang, H., Leonard, E.C., Changizi-Ashtiyani, S., Bacallao, R.L., Molitoris, B.A., and Sutton, T.A.: Impaired endothelial proliferation and mesenchymal transition contribute to vascular rarefaction following acute kidney injury. Am. J. Physiol. Physiol. 300, F721 (2011).Google Scholar
16.Basile, D.P.: Rarefaction of peritubular capillaries following ischemic acute renal failure: a potential factor predisposing to progressive nephropathy. Curr. Opin. Nephrol. Hypertens. 13, 1 (2004).Google Scholar
17.Chawla, L.S., Eggers, P.W., Star, R.A., and Kimmel, P.L.: Acute kidney injury and chronic kidney disease as interconnected syndromes. N. Engl. J. Med. 371, 58 (2014).Google Scholar
18.Bussolati, B. and Camussi, G.: Therapeutic use of human renal progenitor cells for kidney regeneration. Nat. Rev. Nephrol. 11, 695 (2015).Google Scholar
19.Gordillo, M., Evans, T., and Gouon-Evans, V.: Orchestrating liver development. Development 142, 2094 (2015).Google Scholar
20.Laizzo, P.A.: Handbook of Cardiac Anatomy, Physiology, and Devices (Springer International Publishing, 2009).Google Scholar
21.Desai, T.J., Brownfield, D.G., and Krasnow, M.A.: Alveolar progenitor and stem cells in lung development, renewal and cancer. Nature 507, 190 (2014).Google Scholar
22.Bulger, R.E. and Dobyan, D.C.: Recent structure-function relationships in normal and injured mammalian kidneys. Anat. Rec. 205, 1 (1983).Google Scholar
23.Furriols, M., Chillarón, J., Mora, C., Castelló, A., Bertran, J., Camps, M., Testar, X., Vilaró, S., Zorzano, A., and Palacín, M.: rBAT, related to L-cysteine transport, is localized to the microvilli of proximal straight tubules, and its expression is regulated in kidney by development. J. Biol. Chem. 268, 27060 (1993).Google Scholar
24.Greka, A. and Mundel, P.: Cell biology and pathology of podocytes. Annu. Rev. Physiol. 74, 299 (2012).Google Scholar
25.Pavenstädt, H.: Roles of the podocyte in glomerular function. Am. J. Physiol. Renal Physiol. 278, F173 (2000).Google Scholar
26.Salmon, A.H.J., Neal, C.R., and Harper, S.J.: New aspects of glomerular filtration barrier structure and function: five layers (at least) not three. Curr. Opin. Nephrol. Hypertens. 18, 197 (2009).Google Scholar
27.Shirato, I., Tomino, Y., Koide, H., and Sakai, T.: Fine structure of the glomerular basement membrane of the rat kidney visualized by high-resolution scanning electron microscopy. Cell Tissue Res. 266, 1 (1991).Google Scholar
28.Cortes, P., Méndez, M., Riser, B.L., Guérin, C.J., Rodríguez-Barbero, A., Hassett, C., and Yee, J.: F-actin fiber distribution in glomerular cells: structural and functional implications. Kidney Int. 58, 2452 (2000).Google Scholar
29.Hui, E.E. and Bhatia, S.N.: Micromechanical control of cell–cell interactions. Proc. Natl. Acad. Sci. U. S. A. 104, 5722 (2007).Google Scholar
30.Albrecht, D.R., Underhill, G.H., Wassermann, T.B., Sah, R.L., and Bhatia, S.N.: Probing the role of multicellular organization in three-dimensional microenvironments. Nat. Methods 3, 369 (2006).Google Scholar
31.Bhatia, S.N., Underhill, G.H., Zaret, K.S., and Fox, I.J.: Cell and tissue engineering for liver disease. Sci. Transl. Med. 6, 245sr2 (2014).Google Scholar
32.Stevens, K.R., Ungrin, M.D., Schwartz, R.E., Ng, S., Carvalho, B., Christine, K.S., Chaturvedi, R.R., Li, C.Y., Zandstra, P.W., Chen, C.S., and Bhatia, S.N.: InVERT molding for scalable control of tissue microarchitecture. Nat. Commun. 4, 1847 (2013).Google Scholar
33.Shan, J., Logan, D.J., Root, D.E., Carpenter, A.E., and Bhatia, S.N.: High-throughput platform for identifying molecular factors involved in phenotypic stabilization of primary human hepatocytes in vitro. J. Biomol. Screen. 21, 897 (2016).Google Scholar
34.Krishna, M.: Microscopic anatomy of the liver. Clin. Liver Dis. 2, S4 (2013).Google Scholar
35.Rappaport, A.M., Borowy, Z.J., Lougheed, W.M., and Lotto, W.N.: Subdivision of hexagonal liver lobules into a structural and functional unit. Role in hepatic physiology and pathology. Anat. Rec. 119, 11 (1954).Google Scholar
36.Wisse, E., Braet, F., Dianzhong Luo, D., De Zanger, R., Jans, D., Crabbe, E., and Vermoesen, A.: Structure and function of sinusoidal lining cells in the liver. Toxicol. Pathol. 24, 100 (1996).Google Scholar
37.Wisse, E., Braet, F., Luo, D., Vermijlen, D., Eddouks, M., Konstandoulaki, M., Empsen, C., and de Zanger, R.B.: Endothelial cells of the hepatic sinusoids: a review. In Liver Diseases and Hepatic Sinusoidal Cells, edited by Tanikawa, K. and Ueno, T. (Springer, Tokyo, Japan, 1999), pp. 17–53.Google Scholar
38.Bilzer, M., Roggel, F., and Gerbes, A.L.: Role of Kupffer cells in host defense and liver disease. Liver Int. 26, 1175 (2006).Google Scholar
39.Puche, J.E., Saiman, Y., and Friedman, S.L.: Hepatic stellate cells and liver fibrosis. Compr. Physiol. 3, 1473 (2013).Google Scholar
40.Malarkey, D.E., Johnson, K., Ryan, L., Boorman, G., and Maronpot, R.R.: New insights into functional aspects of liver morphology. Toxicol. Pathol. 33, 27 (2005).Google Scholar
41.Buckberg, G., Hoffman, J.I.E., Mahajan, A., Saleh, S., and Coghlan, C.: Cardiac mechanics revisited: the relationship of cardiac architecture to ventricular function. Circulation 118, 2571 (2008).Google Scholar
42.Young, A.A. and Cowan, B.R.: Evaluation of left ventricular torsion by cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 14, 49 (2012).Google Scholar
43.Poveda, F., Gil, D., Martí, E., Andaluz, A., Ballester, M., and Carreras, F.: Helical structure of the cardiac ventricular anatomy assessed by diffusion tensor magnetic resonance imaging with multiresolution tractography. Rev. Española Cardiol. Engl. Ed. 66, 782 (2013).Google Scholar
44.Kocica, M.J., Corno, A.F., Carreras-Costa, F., Ballester-Rodes, M., Moghbel, M.C., Cueva, C.N.C., Lackovic, V., Kanjuh, V.I., and Torrent-Guasp, F.: The helical ventricular myocardial band: global, three-dimensional, functional architecture of the ventricular myocardium. Eur. J. Cardio-Thorac. Surg. 29, S21 (2006).Google Scholar
45.Korecky, B., Hai, C.M., and Rakusan, K.: Functional capillary density in normal and transplanted rat hearts. Can. J. Physiol. Pharmacol. 60, 23 (1982).Google Scholar
46.Cheung, D.Y., Duan, B., and Butcher, J.T.: Current progress in tissue engineering of heart valves: multiscale problems, multiscale solutions. Expert Opin. Biol. Ther. 15, 1155 (2015).Google Scholar
47.Schoen, F.J. and Levy, R.J.: Tissue heart valves: current challenges and future research perspectives. J. Biomed. Mater. Res. 47, 439 (1999).Google Scholar
48.McNulty, W. and Usmani, O.S.: Techniques of assessing small airways dysfunction. Eur. Clin. Respir. J. 1, 25898 (2014).Google Scholar
49.Hsia, C.C.W., Hyde, D.M., and Weibel, E.R.: Lung structure and the intrinsic challenges of gas exchange. Compr. Physiol. 6, 827 (2016).Google Scholar
50.Mercer, R.R., Russell, M.L., and Crapo, J.D.: Alveolar septal structure in different species. J. Appl. Physiol. 77, 1060 (1994).Google Scholar
51.Itoh, H., Nishino, M., and Hatabu, H.: Architecture of the lung: morphology and function. J. Thorac. Imaging 19, 221 (2004).Google Scholar
52.Weibel, E.R. and Knight, B.W.: A morphometric study on the thickness of the pulmonary air-blood barrier. J. Cell Biol. 21, 367 (1964).Google Scholar
53.West, J.B.: Comparative physiology of the pulmonary blood-gas barrier: the unique avian solution. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, R1625 (2009).Google Scholar
54.Roberts, M.A., Tran, D., Coulombe, K.L.K., Razumova, M., Regnier, M., Murry, C.E., and Zheng, Y.: Stromal cells in dense collagen promote cardiomyocyte and microvascular patterning in engineered human heart tissue. Tissue Eng. A 22, 633 (2016).Google Scholar
55.Nunes, S.S., Miklas, J.W., Liu, J., Aschar-Sobbi, R., Xiao, Y., Zhang, B., Jiang, J., Massé, S., Gagliardi, M., Hsieh, A., Thavandiran, N., Laflamme, M.A., Nanthakumar, K., Gross, G.J., Backx, P.H., Keller, G., and Radisic, M.: Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes. Nat. Methods 10, 781 (2013).Google Scholar
56.Badylak, S.F., Taylor, D., and Uygun, K.: Whole-organ tissue engineering: decellularization and recellularization of three-dimensional matrix scaffolds. Annu. Rev. Biomed. Eng. 13, 27 (2011).Google Scholar
57.Scarritt, M.E., Pashos, N.C., and Bunnell, B.A.: A review of cellularization strategies for tissue engineering of whole organs. Front. Bioeng. Biotechnol. 3, 43 (2015).Google Scholar
58.Ott, H.C., Matthiesen, T.S., Goh, S.-K., Black, L.D., Kren, S.M., Netoff, T.I., and Taylor, D.A.: Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14, 213 (2008).Google Scholar
59.Ott, H.C., Clippinger, B., Conrad, C., Schuetz, C., Pomerantseva, I., Ikonomou, L., Kotton, D., and Vacanti, J.P.: Regeneration and orthotopic transplantation of a bioartificial lung. Nat. Med. 16, 927 (2010).Google Scholar
60.Petersen, T.H., Calle, E.A., Zhao, L., Lee, E.J., Gui, L., Raredon, M.B., Gavrilov, K., Yi, T., Zhuang, Z.W., Breuer, C., Herzog, E., and Niklason, L.E.: Tissue-engineered lungs for in vivo implantation. Science 329, 538 (2010).Google Scholar
61.Song, J.J., Guyette, J.P., Gilpin, S.E., Gonzalez, G., Vacanti, J.P., and Ott, H.C.: Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat. Med. 19, 646 (2013).Google Scholar
62.Hasan, A., Paul, A., Vrana, N.E., Zhao, X., Memic, A., Hwang, Y.-S., Dokmeci, M.R., and Khademhosseini, A.: Microfluidic techniques for development of 3D vascularized tissue. Biomaterials 35, 7308 (2014).Google Scholar
63.Fatehullah, A., Tan, S.H., and Barker, N.: Organoids as an in vitro model of human development and disease. Nat. Cell Biol. 18, 246 (2016).Google Scholar
64.Keane, T.J., Swinehart, I.T., and Badylak, S.F.: Methods of tissue decellularization used for preparation of biologic scaffolds and in vivo relevance. Methods 84, 25 (2015).Google Scholar
65.Nakayama, K.H., Batchelder, C.A., Lee, C.I., and Tarantal, A.F.: Decellularized rhesus monkey kidney as a Three-Dimensional Scaffold for Renal Tissue Engineering. Tissue Eng. A 16, 2207 (2010).Google Scholar
66.Crapo, P.M., Gilbert, T.W., and Badylak, S.F.: An overview of tissue and whole organ decellularization processes. Biomaterials 32, 3233 (2011).Google Scholar
67.Wu, Q., Bao, J., Zhou, Y., Wang, Y., Du, Z., Shi, Y., Li, L., and Bu, H.: Optimizing perfusion-decellularization methods of porcine livers for clinical-scale whole-organ bioengineering. Biomed. Res. Int. 2015, 785474 (2015).Google Scholar
68.Malik, N. and Rao, M.S.: A review of the methods for human iPSC derivation. Methods Mol. Biol. 997, 23 (2013).Google Scholar
69.Shi, Y., Inoue, H., Wu, J.C., and Yamanaka, S.: Induced pluripotent stem cell technology: a decade of progress. Nat. Rev. Drug Discov. 16, 115 (2016).Google Scholar
70.Ren, X., Moser, P.T., Gilpin, S.E., Okamoto, T., Wu, T., Tapias, L.F., Mercier, F.E., Xiong, L., Ghawi, R., Scadden, D.T., Mathisen, D.J., and Ott, H.C.: Engineering pulmonary vasculature in decellularized rat and human lungs. Nat. Biotechnol. 33, 1097 (2015).Google Scholar
71.Huang, S.X.L., Islam, M.N., O'Neill, J., Hu, Z., Yang, Y.-G., Chen, Y.-W., Mumau, M., Green, M.D., Vunjak-Novakovic, G., Bhattacharya, J., and Snoeck, H.-W.: Efficient generation of lung and airway epithelial cells from human pluripotent stem cells. Nat. Biotechnol. 32, 84 (2013).Google Scholar
72.Lu, T.-Y., Lin, B., Kim, J., Sullivan, M., Tobita, K., Salama, G., and Yang, L.: Repopulation of decellularized mouse heart with human induced pluripotent stem cell-derived cardiovascular progenitor cells. Nat. Commun. 4, 2307 (2013).Google Scholar
73.Sutherland, M.L., Fabre, K.M., and Tagle, D.A.: The National Institutes of Health Microphysiological Systems Program focuses on a critical challenge in the drug discovery pipeline. Stem Cell Res. Ther. 4(Suppl. 1), I1 (2013).Google Scholar
74.Stokes, C.L., Cirit, M., and Lauffenburger, D.A.: Physiome-on-a-chip: the challenge of ‘scaling’ in design, operation, and translation of microphysiological systems. CPT Pharmacometrics Syst. Pharmacol. 4, 559 (2015).Google Scholar
75.Marx, U., Andersson, T.B., Bahinski, A., Beilmann, M., Beken, S., Cassee, F.R., Cirit, M., Daneshian, M., Fitzpatrick, S., Frey, O., Gaertner, C., Giese, C., Griffith, L., Hartung, T., Heringa, M.B., Hoeng, J., de Jong, W.H., Kojima, H., Kuehnl, J., Leist, M., Luch, A., Maschmeyer, I., Sakharov, D., Sips, A.J.A.M., Steger-Hartmann, T., Tagle, D.A., Tonevitsky, A., Tralau, T., Tsyb, S., van de Stolpe, A., Vandebriel, R., Vulto, P., Wang, J., Wiest, J., Rodenburg, M., and Roth, A.: Biology-inspired microphysiological system approaches to solve the prediction dilemma of substance testing. ALTEX 33, 272 (2016).Google Scholar
76.Vernetti, L., Gough, A., Baetz, N., Blutt, S., Broughman, J.R., Brown, J.A., Foulke-Abel, J., Hasan, N., In, J., Kelly, E., Kovbasnjuk, O., Repper, J., Senutovitch, N., Stabb, J., Yeung, C., Zachos, N.C., Donowitz, M., Estes, M., Himmelfarb, J., Truskey, G., Wikswo, J.P., and Taylor, D.L.: Functional coupling of human microphysiology systems: intestine, liver, kidney proximal tubule, blood-brain barrier and skeletal muscle. Sci. Rep. 7, 42296 (2017).Google Scholar
77.Miller, P.G. and Shuler, M.L.: Design and demonstration of a pumpless 14 compartment microphysiological system. Biotechnol. Bioeng. 113, 2213 (2016).Google Scholar
78.Qin, D., Xia, Y., and Whitesides, G.M.: Soft lithography for micro- and nanoscale patterning. Nat. Protoc. 5, 491 (2010).Google Scholar
79.Sia, S.K. and Whitesides, G.M.: Microfluidic devices fabricated in Poly(dimethylsiloxane) for biological studies. Electrophoresis 24, 3563 (2003).Google Scholar
80.Berthier, E., Young, E.W.K., and Beebe, D.: Engineers are from PDMS-land, Biologists are from Polystyrenia. Lab Chip 12, 1224 (2012).Google Scholar
81.Xia, Y. and Whitesides, G.M.: Soft lithography. Annu. Rev. Mater. Sci. 28, 153 (1998).Google Scholar
82.Song, J.W., Gu, W., Futai, N., Warner, K.A., Nor, J.E., and Takayama, S.: Computer-controlled microcirculatory support system for endothelial cell culture and shearing. Anal. Chem. 77, 3993 (2005).Google Scholar
83.Zheng, C., Zhang, X., Li, C., Pang, Y., and Huang, Y.: Microfluidic device for studying controllable hydrodynamic flow induced cellular responses. Anal. Chem. 89, 3710 (2017).Google Scholar
84.Smith, Q. and Gerecht, S.: Going with the flow: microfluidic platforms in vascular tissue engineering. Curr. Opin. Chem. Eng. 3, 42 (2014).Google Scholar
85.Lee, S.A., Chung, S.E., Park, W., Lee, S.H., and Kwon, S.: Three-dimensional fabrication of heterogeneous microstructures using soft membrane deformation and optofluidic maskless lithography. Lab Chip 9, 1670 (2009).Google Scholar
86.Chueh, B., Huh, D., Kyrtsos, C.R., Houssin, T., Futai, N., and Takayama, S.: Leakage-free bonding of porous membranes into layered microfluidic array systems. Anal. Chem. 79, 3504 (2007).Google Scholar
87.Huh, D., Matthews, B.D., Mammoto, A., Montoya-Zavala, M., Hsin, H.Y., and Ingber, D.E.: Reconstituting organ-level lung functions on a chip. Science 328, 1662 (2010).Google Scholar
88.Kane, R.: Patterning proteins and cells using soft lithography. Biomaterials 20, 2363 (1999).Google Scholar
89.Dittrich, P.S. and Manz, A.: Lab-on-a-chip: microfluidics in drug discovery. Nat. Rev. Drug Discov. 5, 210 (2006).Google Scholar
90.Khademhosseini, A., Langer, R., Borenstein, J., and Vacanti, J.P.: Microscale technologies for tissue engineering and biology. Proc. Natl. Acad. Sci. U. S. A. 103, 2480 (2006).Google Scholar
91.Jang, K.-J., Mehr, A.P., Hamilton, G.A., McPartlin, L.A., Chung, S., Suh, K.-Y., and Ingber, D.E.: Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment. Integr. Biol. 5, 1119 (2013).Google Scholar
92.Kim, S., LesherPerez, S.C., Kim, B.C., Yamanishi, C., Labuz, J.M., Leung, B., and Takayama, S.: Pharmacokinetic profile that reduces nephrotoxicity of gentamicin in a perfused kidney-on-a-chip. Biofabrication 8, 15021 (2016).Google Scholar
93.Gori, M., Simonelli, M.C., Giannitelli, S.M., Businaro, L., Trombetta, M., and Rainer, A.: Investigating nonalcoholic fatty liver disease in a liver-on-a-chip microfluidic device. PLoS ONE 11, e0159729 (2016).Google Scholar
94.Benam, K.H., Villenave, R., Lucchesi, C., Varone, A., Hubeau, C., Lee, H.-H., Alves, S.E., Salmon, M., Ferrante, T.C., Weaver, J.C., Bahinski, A., Hamilton, G.A., and Ingber, D.E.: Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro. Nat. Methods 13, 151 (2015).Google Scholar
95.Lee, P.J., Hung, P.J., and Lee, L.P.: An artificial liver sinusoid with a microfluidic endothelial-like barrier for primary hepatocyte culture. Biotechnol. Bioeng. 97, 1340 (2007).Google Scholar
96.Legendre, A., Baudoin, R., Alberto, G., Paullier, P., Naudot, M., Bricks, T., Brocheton, J., Jacques, S., Cotton, J., and Leclerc, E.: Metabolic characterization of primary rat hepatocytes cultivated in parallel microfluidic biochips. J. Pharm. Sci. 102, 3264 (2013).Google Scholar
97.Kim, D.-H., Lipke, E.A., Kim, P., Cheong, R., Thompson, S., Delannoy, M., Suh, K.-Y., Tung, L., and Levchenko, A.: Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc. Natl. Acad. Sci. U. S. A. 107, 565 (2010).Google Scholar
98.Tanaka, Y., Sato, K., Shimizu, T., Yamato, M., Okano, T., Kitamori, T., Healy, K.E., Folch, A., and Okano, T.: A micro-spherical heart pump powered by cultured cardiomyocytes. Lab Chip 7, 207 (2007).Google Scholar
99.Carson, D., Hnilova, M., Yang, X., Nemeth, C.L., Tsui, J.H., Smith, A.S.T., Jiao, A., Regnier, M., Murry, C.E., Tamerler, C., and Kim, D.-H.: Nanotopography-induced structural anisotropy and sarcomere development in human cardiomyocytes derived from induced pluripotent stem cells. ACS Appl. Mater. Interfaces 8, 21923 (2016).Google Scholar
100.Macadangdang, J., Guan, X., Smith, A.S.T., Lucero, R., Czerniecki, S., Childers, M.K., Mack, D.L., and Kim, D.-H.: Nanopatterned human iPSC-based model of a dystrophin-null cardiomyopathic phenotype. Cell. Mol. Bioeng. 8, 320 (2015).Google Scholar
101.Slaughter, B.V., Khurshid, S.S., Fisher, O.Z., Khademhosseini, A., and Peppas, N.A.: Hydrogels in regenerative medicine. Adv. Mater. 21, 3307 (2009).Google Scholar
102.Griffith, L.G. and Swartz, M.A.: Capturing complex 3D tissue physiology in vitro. Nat. Rev. Mol. Cell Biol. 7, 211 (2006).Google Scholar
103.O'Brien, F.J.: Biomaterials & scaffolds for tissue engineering. Mater. Today 14, 88 (2011).Google Scholar
104.Tien, J.: Microfluidic approaches for engineering vasculature. Curr. Opin. Chem. Eng. 3, 36 (2014).Google Scholar
105.Chrobak, K.M., Potter, D.R., and Tien, J.: Formation of perfused, functional microvascular tubes in vitro. Microvasc. Res. 71, 185 (2006).Google Scholar
106.Wong, K.H.K., Truslow, J.G., Khankhel, A.H., Chan, K.L.S., and Tien, J.: Artificial lymphatic drainage systems for vascularized microfluidic scaffolds. J. Biomed. Mater. Res. A 101A, 2181 (2013).Google Scholar
107.Golden, A.P. and Tien, J.: Fabrication of microfluidic hydrogels using molded gelatin as a sacrificial element. Lab Chip 7, 720 (2007).Google Scholar
108.Miller, J.S., Stevens, K.R., Yang, M.T., Baker, B.M., Nguyen, D.-H.T., Cohen, D.M., Toro, E., Chen, A.A., Galie, P.A., Yu, X., Chaturvedi, R., Bhatia, S.N., and Chen, C.S.: Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11, 768 (2012).Google Scholar
109.Huling, J., Ko, I.K., Atala, A., and Yoo, J.J.: Fabrication of biomimetic vascular scaffolds for 3D tissue constructs using vascular corrosion casts. Acta Biomater. 32, 190 (2016).Google Scholar
110.Zheng, Y., Chen, J., Craven, M., Choi, N.W., Totorica, S., Diaz-Santana, A., Kermani, P., Hempstead, B., Fischbach-Teschl, C., López, J.A., and Stroock, A.D.: In vitro microvessels for the study of angiogenesis and thrombosis. Proc. Natl. Acad. Sci. U. S. A. 109, 9342 (2012).Google Scholar
111.Zhang, B., Montgomery, M., Chamberlain, M.D., Ogawa, S., Korolj, A., Pahnke, A., Wells, L.A., Massé, S., Kim, J., Reis, L., Momen, A., Nunes, S.S., Wheeler, A.R., Nanthakumar, K., Keller, G., Sefton, M.V., and Radisic, M.: Biodegradable scaffold with built-in vasculature for organ-on-a-chip engineering and direct surgical anastomosis. Nat. Mater. 15, 669 (2016).Google Scholar
112.Lee, E.J., Kim, D.E., Azeloglu, E.U., and Costa, K.D.: Engineered cardiac organoid chambers: toward a functional biological model ventricle. Tissue Eng. A 14, 215 (2008).Google Scholar
113.Bajaj, P., Schweller, R.M., Khademhosseini, A., West, J.L., and Bashir, R.: 3D biofabrication strategies for tissue engineering and regenerative medicine. Annu. Rev. Biomed. Eng. 16, 247 (2014).Google Scholar
114.Vernetti, L.A., Senutovitch, N., Boltz, R., DeBiasio, R., Ying Shun, T., Gough, A., and Taylor, D.L.: A human liver microphysiology platform for investigating physiology, drug safety, and disease models. Exp. Biol. Med. 241, 101 (2016).Google Scholar
115.Ligresti, G., Nagao, R.J., Xue, J., Choi, Y.J., Xu, J., Ren, S., Aburatani, T., Anderson, S.K., MacDonald, J.W., Bammler, T.K., Schwartz, S.M., Muczynski, K.A., Duffield, J.S., Himmelfarb, J., and Zheng, Y.: A Novel three-dimensional human peritubular microvascular system. J. Am. Soc. Nephrol. 27, 2370 (2016).Google Scholar
116.Chaturvedi, R.R., Stevens, K.R., Solorzano, R.D., Schwartz, R.E., Eyckmans, J., Baranski, J.D., Stapleton, S.C., Bhatia, S.N., and Chen, C.S.: Patterning vascular networks in vivo for tissue engineering applications. Tissue Eng. C Methods 21, 509 (2015).Google Scholar
117.Mihic, A., Li, J., Miyagi, Y., Gagliardi, M., Li, S.-H., Zu, J., Weisel, R.D., Keller, G., and Li, R.-K.: The effect of cyclic stretch on maturation and 3D tissue formation of human embryonic stem cell-derived cardiomyocytes. Biomaterials 35, 2798 (2014).Google Scholar
118.Tulloch, N.L., Muskheli, V., Razumova, M.V., Korte, F.S., Regnier, M., Hauch, K.D., Pabon, L., Reinecke, H., and Murry, C.E.: Growth of engineered human myocardium with mechanical loading and vascular coculture. Circ. Res. 109, 47 (2011).Google Scholar
119.Murphy, S.V., Skardal, A., and Atala, A.: Evaluation of hydrogels for bio-printing applications. J. Biomed. Mater. Res. A 101A, 272 (2013).Google Scholar
120.Skardal, A. and Atala, A.: Biomaterials for Integration with 3-D bioprinting. Ann. Biomed. Eng. 43, 730 (2014).Google Scholar
121.Pati, F., Jang, J., Ha, D.-H., Won Kim, S., Rhie, J.-W., Shim, J.-H., Kim, D.-H., and Cho, D.-W.: Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat. Commun. 5, 3935 (2014).Google Scholar
122.He, Y., Yang, F., Zhao, H., Gao, Q., Xia, B., and Fu, J.: Research on the printability of hydrogels in 3D bioprinting. Sci. Rep. 6, 29977 (2016).Google Scholar
123.Ahmed, E.M.: Hydrogel: preparation, characterization, and applications: a review. J. Adv. Res. 6, 105 (2015).Google Scholar
124.Rutz, A.L., Hyland, K.E., Jakus, A.E., Burghardt, W.R., and Shah, R.N.: A multimaterial bioink method for 3D printing tunable, cell-compatible hydrogels. Adv. Mater. 27, 1607 (2015).Google Scholar
125.Skardal, A., Devarasetty, M., Kang, H.-W., Mead, I., Bishop, C., Shupe, T., Lee, S.J., Jackson, J., Yoo, J., Soker, S., and Atala, A.: A hydrogel bioink toolkit for mimicking native tissue biochemical and mechanical properties in bioprinted tissue constructs. Acta Biomater. 25, 24 (2015).Google Scholar
126.Mandrycky, C., Wang, Z., Kim, K., and Kim, D.-H.: 3D bioprinting for engineering complex tissues. Biotechnol. Adv. 34, 422 (2016).Google Scholar
127.Ozbolat, I.T. and Hospodiuk, M.: Current advances and future perspectives in extrusion-based bioprinting. Biomaterials 76, 321 (2016).Google Scholar
128.Raman, R. and Bashir, R.: Chapter 6—stereolithographic 3D bioprinting for biomedical applications. In Essentials of 3D Biofabrication and Translation, edited by A. Atala and J.J. Yoo (Academic Press, 2015), pp. 89–121.Google Scholar
129.Homan, K.A., Kolesky, D.B., Skylar-Scott, M.A., Herrmann, J., Obuobi, H., Moisan, A., and Lewis, J.A.: Bioprinting of 3D convoluted renal proximal tubules on perfusable chips. Sci. Rep. 6, 34845 (2016).Google Scholar
130.Ma, X., Qu, X., Zhu, W., Li, Y.-S., Yuan, S., Zhang, H., Liu, J., Wang, P., Lai, C.S.E., Zanella, F., Feng, G.-S., Sheikh, F., Chien, S., and Chen, S.: Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc. Natl. Acad. Sci. U. S. A. 113, 2206 (2016).Google Scholar
131.Horváth, L., Umehara, Y., Jud, C., Blank, F., Petri-Fink, A., and Rothen-Rutishauser, B.: Engineering an in vitro air-blood barrier by 3D bioprinting. Sci. Rep. 5, 7974 (2015).Google Scholar
132.Faulkner-Jones, A., Fyfe, C., Cornelissen, D.-J., Gardner, J., King, J., Courtney, A., and Shu, W.: Bioprinting of human pluripotent stem cells and their directed differentiation into hepatocyte-like cells for the generation of mini-livers in 3D. Biofabrication 7, 44102 (2015).Google Scholar
133.Nguyen, D.G., Funk, J., Robbins, J.B., Crogan-Grundy, C., Presnell, S.C., Singer, T., and Roth, A.B.: Bioprinted 3D primary liver tissues allow assessment of organ-level response to clinical drug induced toxicity in vitro. PLoS ONE 11, e0158674 (2016).Google Scholar
134.Bhise, N.S., Manoharan, V., Massa, S., Tamayol, A., Ghaderi, M., Miscuglio, M., Lang, Q., Shrike Zhang, Y., Shin, S.R., Calzone, G., Annabi, N., Shupe, T.D., Bishop, C.E., Atala, A., Dokmeci, M.R., and Khademhosseini, A.: A liver-on-a-chip platform with bioprinted hepatic spheroids. Biofabrication 8, 14101 (2016).Google Scholar
135.Gaetani, R., Doevendans, P.A., Metz, C.H.G., Alblas, J., Messina, E., Giacomello, A., and Sluijter, J.P.G.: Cardiac tissue engineering using tissue printing technology and human cardiac progenitor cells. Biomaterials 33, 1782 (2012).Google Scholar
136.Gaetani, R., Feyen, D.A.M., Verhage, V., Slaats, R., Messina, E., Christman, K.L., Giacomello, A., Doevendans, P.A.F.M., and Sluijter, J.P.G.: Epicardial application of cardiac progenitor cells in a 3D-printed gelatin/hyaluronic acid patch preserves cardiac function after myocardial infarction. Biomaterials 61, 339 (2015).Google Scholar
137.Zhang, Y.S., Arneri, A., Bersini, S., Shin, S.-R., Zhu, K., Goli-Malekabadi, Z., Aleman, J., Colosi, C., Busignani, F., Dell'Erba, V., Bishop, C., Shupe, T., Demarchi, D., Moretti, M., Rasponi, M., Dokmeci, M.R., Atala, A., and Khademhosseini, A.: Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials 110, 45 (2016).Google Scholar
138.Takasato, M., Er, P.X., Chiu, H.S., Maier, B., Baillie, G.J., Ferguson, C., Parton, R.G., Wolvetang, E.J., Roost, M.S., Chuva de Sousa Lopes, S.M., and Little, M.H.: Kidney organoids from human iPS cells contain multiple lineages and model human nephrogenesis. Nature 526, 564 (2015).Google Scholar
139.Morizane, R., Lam, A.Q., Freedman, B.S., Kishi, S., Valerius, M.T., and Bonventre, J.V.: Nephron organoids derived from human pluripotent stem cells model kidney development and injury. Nat. Biotechnol. 33, 1193 (2015).Google Scholar
140.Freedman, B.S., Brooks, C.R., Lam, A.Q., Fu, H., Morizane, R., Agrawal, V., Saad, A.F., Li, M.K., Hughes, M.R., Vander Werff, R., Peters, D.T., Lu, J., Baccei, A., Siedlecki, A.M., Valerius, M.T., Musunuru, K., McNagny, K.M., Steinman, T.I., Zhou, J., Lerou, P.H., and Bonventre, J.V.: Modelling kidney disease with CRISPR-mutant kidney organoids derived from human pluripotent epiblast spheroids. Nat. Commun. 6, 8715 (2015).Google Scholar
141.Huch, M., Dorrell, C., Boj, S.F., van Es, J.H., Li, V.S.W., van de Wetering, M., Sato, T., Hamer, K., Sasaki, N., Finegold, M.J., Haft, A., Vries, R.R.G., Grompe, M., and Clevers, H.: In vitro expansion of single Lgr5+ liver stem cells induced by WNT-driven regeneration. Nature 494, 247 (2013).Google Scholar
142.Takebe, T., Sekine, K., Enomura, M., Koike, H., Kimura, M., Ogaeri, T., Zhang, R.-R., Ueno, Y., Zheng, Y.-W., Koike, N., Aoyama, S., Adachi, Y., and Taniguchi, H.: Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499, 481 (2013).Google Scholar
143.Khademhosseini, A., Eng, G., Yeh, J., Kucharczyk, P.A., Langer, R., Vunjak-Novakovic, G., and Radisic, M.: Microfluidic patterning for fabrication of contractile cardiac organoids. Biomed. Microdevices 9, 149 (2007).Google Scholar
144.Iyer, R.K., Chui, J., and Radisic, M.: Spatiotemporal tracking of cells in tissue-engineered cardiac organoids. J. Tissue Eng. Regen. Med. 3, 196 (2009).Google Scholar
145.Voges, H.K., Mills, R.J., Elliott, D.A., Parton, R.G., Porrello, E.R., and Hudson, J.E.: Development of a human cardiac organoid injury model reveals innate regenerative potential. Development 144, 1118 (2017).Google Scholar
146.Dye, B.R., Hill, D.R., Ferguson, M.A., Tsai, Y.-H., Nagy, M.S., Dyal, R., Wells, J.M., Mayhew, C.N., Nattiv, R., Klein, O.D., White, E.S., Deutsch, G.H., Spence, J.R., Shroyer, N., Wells, J., Helmrath, M., Kotton, D., Elefanty, A., Stanley, E., Chen, Q., Prabhakar, S., Weissman, I., and Lim, B.: In vitro generation of human pluripotent stem cell derived lung organoids. Elife 4, 327 (2015).Google Scholar
147.Dye, B.R., Dedhia, P.H., Miller, A.J., Nagy, M.S., White, E.S., Shea, L.D., Spence, J.R., Ellis, J., Rossant, J., Sun, Y., Grabowski, G., Finkbeiner, S., Spence, J., Shroyer, N., Wells, J., Helmrath, M., Mense, M., Rowe, S., Engelhardt, J., Hsu, Y., and Rajagopal, J.: A bioengineered niche promotes in vivo engraftment and maturation of pluripotent stem cell derived human lung organoids. Elife 5, 876 (2016).Google Scholar
148.Takahashi, H., Nakayama, M., Shimizu, T., Yamato, M., and Okano, T.: Anisotropic cell sheets for constructing three-dimensional tissue with well-organized cell orientation. Biomaterials 32, 8830 (2011).Google Scholar
149.Jiao, A., Trosper, N.E., Yang, H.S., Kim, J., Tsui, J.H., Frankel, S.D., Murry, C.E., and Kim, D.-H.: Thermoresponsive nanofabricated substratum for the engineering of three-dimensional tissues with layer-by-layer architectural control. ACS Nano 8, 4430 (2014).Google Scholar
150.Gupta, R., Van Rooijen, N., and Sefton, M.V.: Fate of endothelialized modular constructs implanted in an omental pouch in nude rats. Tissue Eng. A 15, 2875 (2009).Google Scholar
151.Rafii, S., Butler, J.M., and Ding, B.-S.: Angiocrine functions of organ-specific endothelial cells. Nature 529, 316 (2016).Google Scholar
152.Tabar, V. and Studer, L.: Pluripotent stem cells in regenerative medicine: challenges and recent progress. Nat. Rev. Genet. 15, 82 (2014).Google Scholar
153.Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E.: Matrix elasticity directs stem cell lineage specification. Cell 126, 677 (2006).Google Scholar
154.Briquez, P.S., Clegg, L.E., Martino, M.M., Mac Gabhann, F., and Hubbell, J.A.: Design principles for therapeutic angiogenic materials. Nat. Rev. Mater. 1, 15006 (2016).Google Scholar
155.Asti, A. and Gioglio, L.: Natural and synthetic biodegradable polymers: different scaffolds for cell expansion and tissue formation. Int. J. Artif. Organs 37, 187 (2014).Google Scholar
156.Gilpin, A. and Yang, Y.: Decellularization strategies for regenerative medicine: from processing techniques to applications. Biomed Res. Int. 2017, 1 (2017).Google Scholar
157.Saldin, L.T., Cramer, M.C., Velankar, S.S., White, L.J., and Badylak, S.F.: Extracellular matrix hydrogels from decellularized tissues: structure and function. Acta Biomater. 49, 1 (2017).Google Scholar