From Engineered Tissues and Microfludics to Human Eyes-On-A-Chip

Meyer U. The history of tissue engineering and regenerative medicine in perspective. In: Mayer, U., Meyer, T., Handschel, J., Wiesmann, H.P. eds. Fundamentals of Tissue Engineering and Regenerative Medicine. Berlin Heidelberg: Springer; 2009; p. 5–12.

Kirkton R.D. , Santiago-Maysonet M. , Lawson J.H. , Tente W.E. , Dahl S.L.M. , Niklason L.E. , and Prichard H.L. Bioengineered human acellular vessels recellularize and evolve into living blood vessels after human implantation. Sci. Transl. Med. 11:pii: eaau6934, 2019.

Thavandiran N. , Dubois N. , Mikryukov A. , Masse S. , Beca B. , Simmons C.A. , Deshpande V.S. , McGarry J.P. , Chen C.S. , Nanthakumar K. , Keller G.M. , Radisic M. , and Zandstra P.W. Design and formulation of functional pluripotent stem cell-derived cardiac microtissues. Proc. Natl. Acad. Sci. U. S. A. 110:E4698–E4707, 2013.

Yodmuang S. , Gadjanski I. , Chao P.H. , and Vunjak-Novakovic G. Transient hypoxia improves matrix properties in tissue engineered cartilage. J. Orthop. Res. 31:544–553, 2013.

Bursac N. , Papadaki M. , Cohen R.J. , Schoen F.J. , Eisenberg S.R. , Carrier R. , Vunjak-Novakovic G. , and Freed L.E. Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am. J. Physiol. 277:H433–H444, 1999.

Levenberg S. , Rouwkema J. , Macdonald M. , Garfein E.S. , Kohane D.S. , Darland D.C. , Marini R. , van Blitterswijk C.A. , Mulligan R.C. , D'Amore P.A. , and Langer R. Engineering vascularized skeletal muscle tissue. Nat. Biotechnol. 23:879–884, 2005.

Iyer R.K. , Odedra D. , Chiu L.L. , Vunjak-Novakovic G. , and Radisic M. VEGF secretion by non-myocytes modulates Connexin-43 levels in cardiac organoids. Tissue Eng. Part A. 18:1771–1783, 2012.

Stevens K.R. , Kreutziger K.L. , Dupras S.K. , Korte F.S. , Regnier M. , Muskheli V. , Nourse M.B. , Bendixen K. , Reinecke H. , and Murry C.E. Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc. Natl. Acad. Sci. U. S. A. 106:16568–16573, 2009.

Bhana B. , Iyer R.K. , Chen W.L. , Zhao R. , Sider K.L. , Likhitpanichkul M. , Simmons C.A. , and Radisic M. Influence of substrate stiffness on the phenotype of heart cells. Biotechnol. Bioeng. 105:1148–1160, 2010.

Discher D.E. , Janmey P. , and Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science. 310:1139–1143, 2005.

Engler A.J. , Sen S. , Sweeney H.L. , and Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell. 126:677–689, 2006.

DeForest C.A. , and Anseth K.S. Cytocompatible click-based hydrogels with dynamically tunable properties through orthogonal photoconjugation and photocleavage reactions. Nat. Chem. 3:925–931, 2011.

Mann B.K. , Gobin A.S. , Tsai A.T. , Schmedlen R.H. , and West J.L. Smooth muscle cell growth in photopolymerized hydrogels with cell adhesive and proteolytically degradable domains: synthetic ECM analogs for tissue engineering. Biomaterials. 22:3045–3051, 2001.

Ehrbar M. , Rizzi S.C. , Schoenmakers R.G. , Miguel B.S. , Hubbell J.A. , Weber F.E. , and Lutolf M.P. Biomolecular hydrogels formed and degraded via site-specific enzymatic reactions. Biomacromolecules. 8:3000–3007, 2007.

Radisic M. , Malda J. , Epping E. , Geng W. , Langer R. , and Vunjak-Novakovic G. Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol. Bioeng. 93:332–343, 2006.

Duffy D.C. , McDonald J.C. , Schueller O.J. , and Whitesides G.M. Rapid prototyping of microfluidic systems in poly(dimethylsiloxane). Anal. Chem. 70:4974–4984, 1998.

Zhang B. , and Radisic M. Organ-on-a-chip devices advance to market. Lab Chip. 17:2395–2420, 2017.

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. 328:1662–1668, 2010.

Takayama S. , McDonald J.C. , Ostuni E. , Liang M.N. , Kenis P.J. , Ismagilov R.F. , and Whitesides G.M. Patterning cells and their environments using multiple laminar fluid flows in capillary networks. Proc. Natl. Acad. Sci. U. S. A. 96:5545–5548, 1999.

Hediger S. , Sayah A. , Horisberger J.D. , and Gijs M.A. Modular microsystem for epithelial cell culture and electrical characterisation. Biosens. Bioelectron. 16:689–694, 2001.

Zhao Y. , Rafatian N. , Feric N.T. , Cox B.J. , Aschar-Sobbi R. , Wang E.Y. , Aggarwal P. , Zhang B. , Conant G. , Ronaldson-Bouchard K. , Pahnke A. , Protze S. , Lee J.H. , Davenport Huyer L. , Jekic D. , Wickeler A. , Naguib H.E. , Keller G.M. , Vunjak-Novakovic G. , Broeckel U. , Backx P.H. , and Radisic M. A platform for generation of chamber-specific cardiac tissues and disease modeling. Cell. 176:913–927.e18, 2019.

Nunes S.S. , Miklas J.W. , Liu J. , Aschar-Sobbi R. , Xiao Y. , Zhang B. , Jiang J. , Masse 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. 10:781–787, 2013.

Takebe T. , Enomura M. , Yoshizawa E. , Kimura M. , Koike H. , Ueno Y. , Matsuzaki T. , Yamazaki T. , Toyohara T. , Osafune K. , Nakauchi H. , Yoshikawa H.Y. , and Taniguchi H. Vascularized and complex organ buds from diverse tissues via mesenchymal cell-driven condensation. Cell Stem Cell. 16:556–565, 2015.

Lancaster M.A. , Corsini N.S. , Wolfinger S. , Gustafson E.H. , Phillips A.W. , Burkard T.R. , Otani T. , Livesey F.J. , and Knoblich J.A. Guided self-organization and cortical plate formation in human brain organoids. Nat. Biotechnol. 35:659–666, 2017.

Clevers H. Modeling development and disease with organoids. Cell. 165:1586–1597, 2016.

Lancaster M.A. , and Knoblich J.A. Organogenesis in a dish: modeling development and disease using organoid technologies. Science. 345:1247125, 2014.

Takahashi K. , and Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 126:663–676, 2006.

Takahashi K. , Tanabe K. , Ohnuki M. , Narita M. , Ichisaka T. , Tomoda K. , and Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 131:861–872, 2007.

Lian X. , Hsiao C. , Wilson G. , Zhu K. , Hazeltine L.B. , Azarin S.M. , Raval K.K. , Zhang J. , Kamp T.J. , and Palecek S.P. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc. Natl. Acad. Sci. U. S. A. 109:E1848–E1857, 2012.

Ronaldson-Bouchard K. , Ma S.P. , Yeager K. , Chen T. , Song L. , Sirabella D. , Morikawa K. , Teles D. , Yazawa M. , and Vunjak-Novakovic G. Advanced maturation of human cardiac tissue grown from pluripotent stem cells. Nature. 556:239–243, 2018.

Takebe T. , Zhang B. , and Radisic M. Synergistic engineering: organoids meet organs-on-a-chip. Cell Stem Cell. 21:297–300, 2017.

Chung M. , Lee S. , Lee B.J. , Son K. , Jeon N.L. , and Kim J.H. Wet-AMD on a chip: modeling outer blood-retinal barrier in vitro. Adv. Healthc. Mater. 7:1–7, 2018.

Yeste J. , Garcia-Ramirez M. , Illa X. , Guimera A. , Hernandez C. , Simo R. , and Villa R. A compartmentalized microfluidic chip with crisscross microgrooves and electrophysiological electrodes for modeling the blood-retinal barrier. Lab Chip. 18:95–105, 2017.

Dodson K.H. , Echevarria F.D. , Li D. , Sappington R.M. , and Edd J.F. Retina-on-a-chip: a microfluidic platform for point access signaling studies. Biomed. Microdevices. 17:114, 2015.

Bennet D. , Estlack Z. , Reid T. , and Kim J. A microengineered human corneal epithelium-on-a-chip for eye drops mass transport evaluation. Lab Chip. 18:1539–1551, 2018.