Concise Review: Organ Engineering: Design, Technology, and Integration

Stem Cells

Volumn 35, Issue 1, 2017, Pages 51-60

  Kaushik, Gaurav ^a,b   Leijten, Jeroen ^a,b,c   Khademhosseini, Ali ^a,b,d,e  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF TWENTE   (Netherlands)

^d KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

^e Konkuk University   (South Korea)

Author keywords

Developmental biology; Microfluidics; Organ engineering; Three dimensional printing; Tissue engineering

Indexed keywords

BIOMATERIAL;

CELL FUNCTION; CELL INTERACTION; CYTOPLASM; DISEASE COURSE; HUMAN; MICROTECHNOLOGY; ORGAN SYSTEMS; REVIEW; STRUCTURE ACTIVITY RELATION; TISSUE ENGINEERING; ANIMAL; CHEMISTRY; PROCEDURES; SIGNAL TRANSDUCTION; TECHNOLOGY; TISSUE SCAFFOLD;

ANIMALS; HUMANS; SIGNAL TRANSDUCTION; TECHNOLOGY; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 85007079674     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2502     Document Type: Review

References (118)

1. Costantini F, Kopan R. Patterning a complex organ: Branching morphogenesis and nephron segmentation in kidney development. Dev Cell 2010;18:698–712.
2. Nelson CM. Geometric control of tissue morphogenesis. Biochim Biophys Acta 2009;1793:903–910.
3. Marvin MJ, Di Rocco G, Gardiner A et al. Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev 2001;15:316–327.
4. Leijten J, Georgi N, Moreira Teixeira L et al. Metabolic programming of mesenchymal stromal cells by oxygen tension directs chondrogenic cell fate. Proc Natl Acad Sci USA 2014;84:30–44.
5. Avorn J. The $2.6 billion pill–methodologic and policy considerations. New Engl J Med 2015;372:1877–1879.
6. Hay M, Thomas DW, Craighead JL et al. Clinical development success rates for investigational drugs. Nat Biotechnol 2014;32:40–51.
7. Selimovic S, Dokmeci MR, Khademhosseini A. Organs-on-a-chip for drug discovery. Curr Opin Pharmacol 2013;13:829–833.
8. Polini A, Prodanov L, Bhise NS et al. Organs-on-a-chip: A new tool for drug discovery. Expert Opin Drug Discov 2014;9:335–352.
9. Kang L, Chung BG, Langer R et al. Microfluidics for drug discovery and development: From target selection to product lifecycle management. Drug Discov Today 2008;13:1–13.
10. Sullivan KE, Black LD. The role of cardiac fibroblasts in extracellular matrix-mediated signaling during normal and pathological cardiac development. J Biomech Eng 2013;135:71001.
11. Brandi ML. Microarchitecture, the key to bone quality. Rheumatology 2009;48:iv3–iv8.
12. Viswanathan MC, Kaushik G, Engler AJ et al. A Drosophila melanogaster model of diastolic dysfunction and cardiomyopathy based on impaired troponin-T function. Circ Res 2014;114:e6–17.
13. Mezzano V, Sheikh F. Cell-cell junction remodeling in the heart: Possible role in cardiac conduction system function and arrhythmias? Life Sci 2012;90:313–321.
14. Unger RE, Sartoris A, Peters K et al. Tissue-like self-assembly in cocultures of endothelial cells and osteoblasts and the formation of microcapillary-like structures on three-dimensional porous biomaterials. Biomaterials 2007;28:3965–3976.
15. Zhang S. Fabrication of novel biomaterials through molecular self-assembly. Nat Biotechnol 2003;21:1171–1178.
16. Leijten J, Khademhosseini A. From nano to macro: Multiscale materials for improved stem cell culturing and analysis. Cell Stem Cell 2016;18:20–24.
17. Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol 2014;32:773–785.
18. Leijten J, Chai YC, Papantoniou I et al. Cell based advanced therapeutic medicinal products for bone repair: Keep it simple? Adv Drug Deliv Rev 2015;84:30–44.
19. Koch L, Deiwick A, Schlie S et al. Skin tissue generation by laser cell printing. Biotechnol Bioeng 2012;109:1855–1863.
20. Rimann M, Bono E, Annaheim H et al. Standardized 3D bioprinting of soft tissue models with human primary cells. J Lab Autom 2015.
21. Algzlan H, Varada S. Three-dimensional printing of the skin. JAMA Dermatol 2015;151:496–509.
22. Liu P, Deng Z, Han S et al. Tissue-engineered skin containing mesenchymal stem cells improves burn wounds. Artif Organs 2008;32:925–931.
23. Atala A, Bauer SB, Soker S et al. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 2006;367:1241–1246.
24. Gutman DA, Cobb J, Somanna D et al. Cancer digital slide archive: An informatics resource to support integrated in silico analysis of TCGA pathology data. J Am Med Inform Assoc 2013;20:1091–1098.
25. Epp JR, Niibori Y, Liz Hsiang HL et al. Optimization of CLARITY for Clearing Whole-Brain and Other Intact Organs(1,2,3). eNeuro 2015;2. pii: ENEURO.0022-15.2015.
26. Chung K, Wallace J, Kim SY et al. Structural and molecular interrogation of intact biological systems. Nature 2013;497:332–337.
27. Chen F, Tillberg PW, Boyden ES. Optical imaging. Expansion microscopy. Science 2015;347:543–548.
28. Tomer R, Ye L, Hsueh B et al. Advanced CLARITY for rapid and high-resolution imaging of intact tissues. Nat Protoc 2014;9:1682–1697.
29. Crowder SW, Leonardo V, Whittaker T et al. Material cues as potent regulators of epigenetics and stem cell function. Cell Stem Cell 2016;18:39–52.
30. Murphy WL, McDevitt TC, Engler AJ. Materials as stem cell regulators. Nat Mater 2014;13:547–557.
31. Spanjaard E, de Rooij J. Mechanotransduction: Vinculin provides stability when tension rises. Curr Biol 2013;23:R159–R161.
32. Holle AW, Tang X, Vijayraghavan D et al. In situ mechanotransduction via vinculin regulates stem cell differentiation. Stem Cells 2013;31:2467–2477.
33. Kaushik G, Fuhrmann A, Cammarato A et al. In situ mechanical analysis of myofibrillar perturbation and aging on soft, bilayered Drosophila myocardium. Biophys J 2011;101:2629–2637.
34. Kaushik G, Zambon AC, Fuhrmann A et al. Measuring passive myocardial stiffness in Drosophila melanogaster to investigate diastolic dysfunction. J Cell Mol Med 2012;16:1656–1662.
35. Kaushik G, Spenlehauer A, Sessions AO et al. Vinculin network-mediated cytoskeletal remodeling regulates contractile function in the aging heart. Sci Transl Med 2015;7:292ra299.
36. Huveneers S, de Rooij J. Mechanosensitive systems at the cadherin-F-actin interface. J Cell Sci 2013;126:403–413.
37. Orr AW, Helmke BP, Blackman BR et al. Mechanisms of mechanotransduction. Dev Cell 2006;10:11–20.
38. Holle AW, Engler AJ. More than a feeling: Discovering, understanding, and influencing mechanosensing pathways. Curr Opin Biotechnol 2011;22:648–654.
39. Engler AJ, Sen S, Sweeney HL et al. Matrix elasticity directs stem cell lineage specification. Cell 2006;126:677–689.
40. Guvendiren M, Burdick JA. Stiffening hydrogels to probe short- and long-term cellular responses to dynamic mechanics. Nat Commun 2012;3:792.
41. Young JL, Kretchmer K, Ondeck MG et al. Mechanosensitive kinases regulate stiffness-induced cardiomyocyte maturation. Sci Rep 2014;4:6425.
42. Weisbrod RM, Shiang T, Al Sayah L et al. Arterial stiffening precedes systolic hypertension in diet-induced obesity. Hypertension 2013;62:1105–1110.
43. Viswanathan P, Ondeck MG, Chirasatitsin S et al. 3D surface topology guides stem cell adhesion and differentiation. Biomaterials 2015;52:140–147.
44. Phadke A, Zhang C, Arman B et al. Rapid self-healing hydrogels. Proc Natl Acad Sci USA 2012;109:4383–4388.
45. Phadke A, Zhang C, Hwang Y et al. Templated mineralization of synthetic hydrogels for bone-like composite materials: Role of matrix hydrophobicity. Biomacromolecules 2010;11:2060–2068.
46. Fuhrmann A, Engler AJ. The cytoskeleton regulates cell attachment strength. Biophys J 2015;109:57–65.
47. Jahed Z, Shams H, Mehrbod M et al. Mechanotransduction pathways linking the extracellular matrix to the nucleus. Int Rev Cell Mol Biol 2014;310:171–220.
48. Oakes PW, Banerjee S, Marchetti MC et al. Geometry regulates traction stresses in adherent cells. Biophys J 2014;107:825–833.
49. Huebsch N, Arany PR, Mao AS et al. Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 2010;9:518–526.
50. Inoue Y, Tsuda S, Nakagawa K et al. Modeling myosin-dependent rearrangement and force generation in an actomyosin network. J Theor Biol 2011;281:65–73.
51. Taylor-Weiner H, Ravi N, Engler AJ. Traction forces mediated by integrin signaling are necessary for definitive endoderm specification. J Cell Sci 2015;128:1961–1968.
52. Wen JH, Vincent LG, Fuhrmann A et al. Interplay of matrix stiffness and protein tethering in stem cell differentiation. Nat Mater 2014;13:979–987.
53. Duband JL, Thiery JP. Spatio-temporal distribution of the adherens junction-associated molecules vinculin and talin in the early avian embryo. Cell Differ Dev 1990;30:55–76.
54. Farge E. Mechanical induction of twist in the Drosophila foregut/stomodeal primordium. Curr Biol 2003;13:1365–1377.
55. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA 1999;282:2035–2042.
56. Fuhrmann A, Engler AJ. Acute shear stress direction dictates adherent cell remodeling and verifies shear profile of spinning disk assays. Phys Biol 2015;12:016011.
57. Sinha B, Koster D, Ruez R et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 2011;144:402–413.
58. Rangamani P, Lipshtat A, Azeloglu EU et al. Decoding information in cell shape. Cell 2013;154:1356–1369.
59. Qiu H, Zhu Y, Sun Z et al. Short communication: vascular smooth muscle cell stiffness as a mechanism for increased aortic stiffness with aging. Circ Res 2010;107:615–619.
60. Humphrey JD, Harrison DG, Figueroa CA et al. Central artery stiffness in hypertension and aging: A problem with cause and consequence. Circ Res 2016;118:379–381.
61. Lauffenburger DA, Horwitz AF. Cell migration: A physically integrated molecular process. Cell 1996;84:359–369.
62. Barleon B, Sozzani S, Zhou D et al. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood 1996;87:3336–3343.
63. Brizzi MF, Tarone G, Defilippi P. Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Curr Opin Cell Biol 2012;24:645–651.
64. Moreira Teixeira LS, Leijten JC, Wennink JW et al. The effect of platelet lysate supplementation of a dextran-based hydrogel on cartilage formation. Biomaterials 2012;33:3651–3661.
65. Lian X, Hsiao C, Wilson G et al. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc Natl Acad Sci USA 2012;109:E1848–E1857.
66. Zlotorynski E. Circadian rhythms: Translating the clock. Nat Rev Mol Cell Biols 2015;16:390.
67. Costa MJ, So AY, Kaasik K et al. Circadian rhythm gene period 3 is an inhibitor of the adipocyte cell fate. J Biol Chem 2011;286:9063–9070.
68. Kawai M, Green CB, Lecka-Czernik B et al. A circadian-regulated gene, Nocturnin, promotes adipogenesis by stimulating PPAR-gamma nuclear translocation. Proc Natl Acad Sci USA 2010;107:10508–10513.
69. Guo B, Chatterjee S, Li L et al. The clock gene, brain and muscle Arnt-like 1, regulates adipogenesis via Wnt signaling pathway. FASEB J 2012;26:3453–3463.
70. Chatterjee S, Nam D, Guo B et al. Brain and muscle Arnt-like 1 is a key regulator of myogenesis. J Cell Sci 2013;126:2213–2224.
71. Erickson IE, Kestle SR, Zellars KH et al. High mesenchymal stem cell seeding densities in hyaluronic acid hydrogels produce engineered cartilage with native tissue properties. Acta Biomater 2012;8:3027–3034.
72. Parker KK, Tan J, Chen CS et al. Myofibrillar architecture in engineered cardiac myocytes. Circ Res 2008;103:340–342.
73. Pfeiffer ER, Wright AT, Edwards AG et al. Caveolae in ventricular myocytes are required for stretch-dependent conduction slowing. J Mol Cell Cardiol 2014;76:265–274.
74. Ott HC, Matthiesen TS, Goh SK et al. Perfusion-decellularized matrix: Using nature's platform to engineer a bioartificial heart. Nat Med 2008;14:213–221.
75. Bao J, Shi Y, Sun H et al. Construction of a portal implantable functional tissue-engineered liver using perfusion-decellularized matrix and hepatocytes in rats. Cell Transplant 2011;20:753–766.
76. Badylak SF, Taylor D, Uygun K. Whole-organ tissue engineering: Decellularization and recellularization of three-dimensional matrix scaffolds. Annu Rev Biomed Eng 2011;13:27–53.
77. Lancaster MA, Renner M, Martin CA et al. Cerebral organoids model human brain development and microcephaly. Nature 2013;501:373–379.
78. Shin SR, Aghaei-Ghareh-Bolagh B, Dang TT et al. Cell-laden microengineered and mechanically tunable hybrid hydrogels of gelatin and graphene oxide. Adv Mater 2013;25:6385–6391.
79. Young JL Engler AJ. Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro. Biomaterials 2011;32:1002–1009.
80. Wang H, Liu K, Chen KJ et al. A rapid pathway toward a superb gene delivery system: Programming structural and functional diversity into a supramolecular nanoparticle library. ACS Nano 2010;4:6235–6243.
81. Hardin JO, Ober TJ, Valentine AD et al. Microfluidic printheads for multimaterial 3D printing of viscoelastic inks. Adv Mater 2015;27:3279–3284.
82. Kolesky DB, Truby RL, Gladman AS et al. 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 2014;26:3124–3130.
83. Zhu W, Li J, Leong YJ et al. 3D-printed artificial microfish. Adv Mater 2015. doi:10.1002/adma.201501372. [Epub ahead of print]
84. Bae H, Chu H, Edalat F et al. Development of functional biomaterials with micro- and nanoscale technologies for tissue engineering and drug delivery applications. J Tissue Eng Regen Med 2014;8:1–14.
85. Camci-Unal G, Alemdar N, Annabi N et al. Oxygen releasing biomaterials for tissue engineering. Polym Int 2013;62:843–848.
86. Khademhosseini A, Peppas NA. Micro- and nanoengineering of biomaterials for healthcare applications. Adv Healthcare Mater 2013;2:10–12.
87. Cha C, Liechty WB, Khademhosseini A et al. Designing biomaterials to direct stem cell fate. ACS Nano 2012;6:9353–9358.
88. Zorlutuna P, Annabi N, Camci-Unal G et al. Microfabricated biomaterials for engineering 3D tissues. Adv Mater 2012;24:1782–1804.
89. Thery M. Micropatterning as a tool to decipher cell morphogenesis and functions. Jo Cell Sci 2010;123:4201–4213.
90. Jackman RJ, Wilbur JL, Whitesides GM. Fabrication of submicrometer features on curved substrates by microcontact printing. Science 1995;269:664–666.
91. McCain ML, Parker KK. Mechanotransduction: The role of mechanical stress, myocyte shape, and cytoskeletal architecture on cardiac function. Pflugers Archiv 2011;462:89–104.
92. Downing TL, Soto J, Morez C et al. Biophysical regulation of epigenetic state and cell reprogramming. Nat Mater 2013;12:1154–1162.
93. Tumbleston JR, Shirvanyants D, Ermoshkin N et al. Additive manufacturing. Continuous liquid interface production of 3D objects. Science 2015;347:1349–1352.
94. Gaharwar AK, Avery RK, Assmann A et al. Shear-thinning nanocomposite hydrogels for the treatment of hemorrhage. ACS Nano 2014;8:9833–9842.
95. Yan C, Altunbas A, Yucel T et al. Injectable solid hydrogel: Mechanism of shear-thinning and immediate recovery of injectable beta-hairpin peptide hydrogels. Soft Matter 2010;6:5143–5156.
96. Rodell CB, Kaminski AL, Burdick JA. Rational design of network properties in guest-host assembled and shear-thinning hyaluronic acid hydrogels. Biomacromolecules 2013;14:4125–4134.
97. Peppas NA, Hilt JZ, Khademhosseini A et al. Hydrogels in biology and medicine: From molecular principles to bionanotechnology. Adv Mater 2006;18:1345–1360.
98. Mosiewicz KA, Kolb L, van der Vlies AJ et al. In situ cell manipulation through enzymatic hydrogel photopatterning. Nat Mater 2013;12:1072–1078.
99. Yan B, Boyer JC, Habault D et al. Near infrared light triggered release of biomacromolecules from hydrogels loaded with upconversion nanoparticles. J Am Chem Soc 2012;134:16558–16561.
100. Huh D, Matthews BD, Mammoto A et al. Reconstituting organ-level lung functions on a chip. Science 2010;328:1662–1668.
101. Huh D, Hamilton GA, Ingber DE. From 3D cell culture to organs-on-chips. Trends Cell Biol 2011;21:745–754.
102. Antonica F, Kasprzyk DF, Opitz R et al. Generation of functional thyroid from embryonic stem cells. Nature 2012;491:66–71.
103. Scannell JW, Blanckley A, Boldon H et al. Diagnosing the decline in pharmaceutical R&D efficiency. Nat Rev Drug Discov 2012;11:191–200.
104. Bhatia SN, Ingber DE. Microfluidic organs-on-chips. Nat Biotechnol 2014;32:760–772.
105. Grueter CE, van Rooij E, Johnson BA et al. A cardiac microRNA governs systemic energy homeostasis by regulation of MED13. Cell 2012;149:671–683.
106. Ulgherait M, Rana A, Rera M et al. AMPK modulates tissue and organismal aging in a non-cell-autonomous manner. Cell Rep 2014;8:1767–1780.
107. Bland ML, Lee RJ, Magallanes JM et al. AMPK supports growth in Drosophila by regulating muscle activity and nutrient uptake in the gut. Dev Biol 2010;344:293–303.
108. Park BK, Boobis A, Clarke S et al. Managing the challenge of chemically reactive metabolites in drug development. Nat Rev Drug Discov 2011;10:292–306.
109. Tacar O, Sriamornsak P, Dass CR. Doxorubicin: An update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol 2013;65:157–170.
110. Khademhosseini A, Bettinger C, Karp JM et al. Interplay of biomaterials and micro-scale technologies for advancing biomedical applications. J Biomater Sci Polym Ed 2006;17:1221–1240.
111. Sasai Y. Next-generation regenerative medicine: Organogenesis from stem cells in 3D culture. Cell Stem Cell 2013;12:520–530.
112. Moreira Teixeira LS, Leijten JC, Sobral J et al. High throughput generated micro-aggregates of chondrocytes stimulate cartilage formation in vitro and in vivo. Eur Cell Mater 2012;23:387–399.
113. Khademhosseini A, Eng G, Yeh J et al. Microfluidic patterning for fabrication of contractile cardiac organoids. Biomed Microdevices 2007;9:149–157.
114. Madden L, Juhas M, Kraus WE et al. Bioengineered human myobundles mimic clinical responses of skeletal muscle to drugs. eLife 2015;4:e04885.
115. Romacho T, Elsen M, Rohrborn D et al. Adipose tissue and its role in organ crosstalk. Acta Phys 2014;210:733–753.
116. Wang G, McCain ML, Yang L et al. Modeling the mitochondrial cardiomyopathy of Barth syndrome with induced pluripotent stem cell and heart-on-chip technologies. Nat Med 2014:616–623.
117. McCain ML, Sheehy SP, Grosberg A et al. Recapitulating maladaptive, multiscale remodeling of failing myocardium on a chip. Proc Natl Acad Sci USA 2013;110:9770–9775.
118. Hinton J, Jallerat Q, Palchesko Q et al. Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci Adv 2015;1:10.