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Annual Review of Chemical and Biomolecular Engineering

Volume 5, 2014

Toward the Directed Self-Assembly of Engineered Tissues

Abstract

Using scaffold-based approaches, tissue engineers have made bold steps toward creating replacement tissues in the laboratory. However, many of these engineered constructs do not fully match the functional properties of their native counterparts. This is partially due to our limited quantitative understanding of the growth and remodeling processes that alter the architecture of engineered tissues, both in culture and after implantation. Here, we consider the mechanisms by which physical cues direct this adaptive response. In particular, we highlight recent experimental and computational studies that characterize quantitatively the mechanics of growth and remodeling in tissue constructs. These advances, from fields as diverse as soft tissue biomechanics and developmental biology, can be used to design new tissue engineering approaches that direct the self-assembly of engineered tissues.

Keyword(s): biomechanics, computational modeling, development, embryo, growth and remodeling, tissue engineering
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2014-06-07
2024-04-18
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Literature Cited

  1. Langer R, Vacanti JP. 1.  1993. Tissue engineering. Science 260:920–26 [Google Scholar]
  2. Bonassar LJ, Vacanti CA. 2.  1998. Tissue engineering: the first decade and beyond. J. Cell. Biochem. Suppl. 30–31:297–303 [Google Scholar]
  3. Berthiaume F, Maguire TJ, Yarmush ML. 3.  2011. Tissue engineering and regenerative medicine: history, progress, and challenges. Annu. Rev. Chem. Biomol. Eng. 2:403–30 [Google Scholar]
  4. Langer R, Vacanti JP. 4.  1995. Artificial organs. Sci. Am. 273:130–33 [Google Scholar]
  5. Varner VD, Nelson CM. 5.  2013. Let's push things forward: disruptive technologies and the mechanics of tissue assembly. Integr. Biol. 5:1162–73 [Google Scholar]
  6. Gleghorn JP, Manivannan S, Nelson CM. 6.  2013. Quantitative approaches to uncover physical mechanisms of tissue morphogenesis. Curr. Opin. Biotechnol. 24:954–61 [Google Scholar]
  7. Wyczalkowski MA, Chen Z, Filas BA, Varner VD, Taber LA. 7.  2012. Computational models for mechanics of morphogenesis. Birth Defects Res. C Embryo Today 96:132–52 [Google Scholar]
  8. Ateshian GA, Humphrey JD. 8.  2012. Continuum mixture models of biological growth and remodeling: past successes and future opportunities. Annu. Rev. Biomed. Eng. 14:97–111 [Google Scholar]
  9. Elbert DL. 9.  2011. Bottom-up tissue engineering. Curr. Opin. Biotechnol. 22:674–80 [Google Scholar]
  10. Martin I, Wendt D, Heberer M. 10.  2004. The role of bioreactors in tissue engineering. Trends Biotechnol. 22:80–86 [Google Scholar]
  11. Drury JL, Mooney DJ. 11.  2003. Hydrogels for tissue engineering: scaffold design variables and applications. Biomaterials 24:4337–51 [Google Scholar]
  12. Lee KY, Mooney DJ. 12.  2001. Hydrogels for tissue engineering. Chem. Rev. 101:1869–79 [Google Scholar]
  13. Slaughter BV, Khurshid SS, Fisher OZ, Khademhosseini A, Peppas NA. 13.  2009. Hydrogels in regenerative medicine. Adv. Mater. 21:3307–29 [Google Scholar]
  14. Hern DL, Hubbell JA. 14.  1998. Incorporation of adhesion peptides into nonadhesive hydrogels useful for tissue resurfacing. J. Biomed. Mater. Res. 39:266–76 [Google Scholar]
  15. Lee KY, Peters MC, Anderson KW, Mooney DJ. 15.  2000. Controlled growth factor release from synthetic extracellular matrices. Nature 408:998–1000 [Google Scholar]
  16. Khademhosseini A, Langer R, Borenstein J, Vacanti JP. 16.  2006. Microscale technologies for tissue engineering and biology. Proc. Natl. Acad. Sci. USA 103:2480–87 [Google Scholar]
  17. Bianco P, Robey PG. 17.  2001. Stem cells in tissue engineering. Nature 414:118–21 [Google Scholar]
  18. Hipp J, Atala A. 18.  2008. Sources of stem cells for regenerative medicine. Stem Cell Rev. 4:3–11 [Google Scholar]
  19. Willerth SM, Sakiyama-Elbert SE. 19.  2008. Cell therapy for spinal cord regeneration. Adv. Drug Deliv. Rev. 60:263–76 [Google Scholar]
  20. Wang A, Tang Z, Park IH, Zhu Y, Patel S. 20.  et al. 2011. Induced pluripotent stem cells for neural tissue engineering. Biomaterials 32:5023–32 [Google Scholar]
  21. de Peppo GM, Marcos-Campos I, Kahler DJ, Alsalman D, Shang L. 21.  et al. 2013. Engineering bone tissue substitutes from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. USA 110:8680–85 [Google Scholar]
  22. Robinton DA, Daley GQ. 22.  2012. The promise of induced pluripotent stem cells in research and therapy. Nature 481:295–305 [Google Scholar]
  23. Lutolf MP, Gilbert PM, Blau HM. 23.  2009. Designing materials to direct stem-cell fate. Nature 462:433–41 [Google Scholar]
  24. Nussbaum J, Minami E, Laflamme MA, Virag JA, Ware CB. 24.  et al. 2007. Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J. 21:1345–57 [Google Scholar]
  25. Place ES, Evans ND, Stevens MM. 25.  2009. Complexity in biomaterials for tissue engineering. Nat. Mater. 8:457–70 [Google Scholar]
  26. Macchiarini P, Jungebluth P, Go T, Asnaghi MA, Rees LE. 26.  et al. 2008. Clinical transplantation of a tissue-engineered airway. Lancet 372:2023–30 [Google Scholar]
  27. Badylak SF, Weiss DJ, Caplan A, Macchiarini P. 27.  2012. Engineered whole organs and complex tissues. Lancet 379:943–52 [Google Scholar]
  28. Jungebluth P, Alici E, Baiguera S, Le Blanc K, Blomberg P. 28.  et al. 2011. Tracheobronchial transplantation with a stem-cell-seeded bioartificial nanocomposite: a proof-of-concept study. Lancet 378:1997–2004 [Google Scholar]
  29. Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. 29.  2006. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet 367:1241–46 [Google Scholar]
  30. Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM. 30.  et al. 2008. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat. Med. 14:213–21 [Google Scholar]
  31. Petersen TH, Calle EA, Zhao L, Lee EJ, Gui L. 31.  et al. 2010. Tissue-engineered lungs for in vivo implantation. Science 329:538–41 [Google Scholar]
  32. Song JJ, Guyette JP, Gilpin SE, Gonzalez G, Vacanti JP, Ott HC. 32.  2013. Regeneration and experimental orthotopic transplantation of a bioengineered kidney. Nat. Med. 19:646–51 [Google Scholar]
  33. Hockaday LA, Kang KH, Colangelo NW, Cheung PY, Duan B. 33.  et al. 2012. Rapid 3D printing of anatomically accurate and mechanically heterogeneous aortic valve hydrogel scaffolds. Biofabrication 4:035005 [Google Scholar]
  34. Reiffel AJ, Kafka C, Hernandez KA, Popa S, Perez JL. 34.  et al. 2013. High-fidelity tissue engineering of patient-specific auricles for reconstruction of pediatric microtia and other auricular deformities. PLoS ONE 8:e56506 [Google Scholar]
  35. Xu T, Binder KW, Albanna MZ, Dice D, Zhao W. 35.  et al. 2013. Hybrid printing of mechanically and biologically improved constructs for cartilage tissue engineering applications. Biofabrication 5:015001 [Google Scholar]
  36. Fung YC. 36.  1993. Biomechanics: Mechanical Properties of Living Tissues New York: Springer-Verlag568
  37. Humphrey JD. 37.  2002. Cardiovascular Solid Mechanics: Cells, Tissues, and Organs New York: Springer757This book is a vast and indispensible resource for those interested in the continuum mechanical studies of the cardiovascular system.
  38. Weinberg CB, Bell E. 38.  1986. A blood vessel model constructed from collagen and cultured vascular cells. Science 231:397–400This pioneering paper presents the first attempt to construct tissue-engineered blood vessels in culture. [Google Scholar]
  39. Bell E, Ivarsson B, Merrill C. 39.  1979. Production of a tissue-like structure by contraction of collagen lattices by human fibroblasts of different proliferative potential in vitro. Proc. Natl. Acad. Sci. USA 76:1274–78 [Google Scholar]
  40. Harris AK, Stopak D, Wild P. 40.  1981. Fibroblast traction as a mechanism for collagen morphogenesis. Nature 290:249–51 [Google Scholar]
  41. Bell E, Ehrlich HP, Buttle DJ, Nakatsuji T. 41.  1981. Living tissue formed in vitro and accepted as skin-equivalent tissue of full thickness. Science 211:1052–54 [Google Scholar]
  42. Wagenseil JE, Mecham RP. 42.  2009. Vascular extracellular matrix and arterial mechanics. Physiol. Rev. 89:957–89 [Google Scholar]
  43. Wolinsky H, Glagov S. 43.  1964. Structural basis for the static mechanical properties of the aortic media. Circ. Res. 14:400–13 [Google Scholar]
  44. L'Heureux N, Germain L, Labbé R, Auger FA. 44.  1993. In vitro construction of a human blood vessel from cultured vascular cells: a morphologic study. J. Vasc. Surg. 17:499–509 [Google Scholar]
  45. Tranquillo RT, Girton TS, Bromberek BA, Triebes TG, Mooradian DL. 45.  1996. Magnetically orientated tissue-equivalent tubes: application to a circumferentially orientated media-equivalent. Biomaterials 17:349–57 [Google Scholar]
  46. Dickinson RB, Guido S, Tranquillo RT. 46.  1994. Biased cell migration of fibroblasts exhibiting contact guidance in oriented collagen gels. Ann. Biomed. Eng. 22:342–56 [Google Scholar]
  47. Barocas VH, Girton TS, Tranquillo RT. 47.  1998. Engineered alignment in media equivalents: magnetic prealignment and mandrel compaction. J. Biomech. Eng. 120:660–66 [Google Scholar]
  48. Barocas VH, Tranquillo RT. 48.  1997. An anisotropic biphasic theory of tissue-equivalent mechanics: the interplay among cell traction, fibrillar network deformation, fibril alignment, and cell contact guidance. J. Biomech. Eng. 119:137–45This excellent theoretical paper presents a biphasic theory for the mechanical behavior of engineered tissues. [Google Scholar]
  49. Barocas VH, Tranquillo RT. 49.  1997. A finite element solution for the anisotropic biphasic theory of tissue-equivalent mechanics: the effect of contact guidance on isometric cell traction measurement. J. Biomech. Eng. 119:261–68 [Google Scholar]
  50. Bellows CG, Melcher AH, Aubin JE. 50.  1982. Association between tension and orientation of periodontal ligament fibroblasts and exogenous collagen fibres in collagen gels in vitro. J. Cell Sci. 58:125–38 [Google Scholar]
  51. Huang D, Chang TR, Aggarwal A, Lee RC, Ehrlich HP. 51.  1993. Mechanisms and dynamics of mechanical strengthening in ligament-equivalent fibroblast-populated collagen matrices. Ann. Biomed. Eng. 21:289–305 [Google Scholar]
  52. Klebe RJ, Caldwell H, Milam S. 52.  1989. Cells transmit spatial information by orienting collagen fibers. Matrix 9:451–58 [Google Scholar]
  53. Eastwood M, Mudera VC, McGrouther DA, Brown RA. 53.  1998. Effect of precise mechanical loading on fibroblast populated collagen lattices: morphological changes. Cell Motil. Cytoskelet. 40:13–21 [Google Scholar]
  54. Costa KD, Lee EJ, Holmes JW. 54.  2003. Creating alignment and anisotropy in engineered heart tissue: role of boundary conditions in a model three-dimensional culture system. Tissue Eng. 9:567–77 [Google Scholar]
  55. Girton TS, Oegema TR, Tranquillo RT. 55.  1999. Exploiting glycation to stiffen and strengthen tissue equivalents for tissue engineering. J. Biomed. Mater. Res. 46:87–92 [Google Scholar]
  56. Girton TS, Oegema TR, Grassl ED, Isenberg BC, Tranquillo RT. 56.  2000. Mechanisms of stiffening and strengthening in media-equivalents fabricated using glycation. J. Biomech. Eng. 122:216–23 [Google Scholar]
  57. Niklason LE, Gao J, Abbott WM, Hirschi KK, Houser S. 57.  et al. 1999. Functional arteries grown in vitro. Science 284:489–93 [Google Scholar]
  58. Dahl SL, Rhim C, Song YC, Niklason LE. 58.  2007. Mechanical properties and compositions of tissue engineered and native arteries. Ann. Biomed. Eng. 35:348–55 [Google Scholar]
  59. Kanda K, Matsuda T, Oka T. 59.  1993. In vitro reconstruction of hybrid vascular tissue. Hierarchic and oriented cell layers. ASAIO J. 39:M561–65 [Google Scholar]
  60. Kanda K, Matsuda T. 60.  1994. In vitro reconstruction of hybrid arterial media with molecular and cellular orientations. Cell Transplant. 3:537–45 [Google Scholar]
  61. Seliktar D, Black RA, Vito RP, Nerem RM. 61.  2000. Dynamic mechanical conditioning of collagen-gel blood vessel constructs induces remodeling in vitro. Ann. Biomed. Eng. 28:351–62 [Google Scholar]
  62. Seliktar D, Nerem RM, Galis ZS. 62.  2001. The role of matrix metalloproteinase-2 in the remodeling of cell-seeded vascular constructs subjected to cyclic strain. Ann. Biomed. Eng. 29:923–34 [Google Scholar]
  63. Kanda K, Matsuda T, Oka T. 63.  1993. Mechanical stress induced cellular orientation and phenotypic modulation of 3-D cultured smooth muscle cells. ASAIO J. 39:M686–90 [Google Scholar]
  64. Chamley-Campbell JH, Campbell GR, Ross R. 64.  1981. Phenotype-dependent response of cultured aortic smooth muscle to serum mitogens. J. Cell Biol. 89:379–83 [Google Scholar]
  65. Nerem RM, Seliktar D. 65.  2001. Vascular tissue engineering. Annu. Rev. Biomed. Eng. 3:225–43 [Google Scholar]
  66. Stegemann JP, Nerem RM. 66.  2003. Phenotype modulation in vascular tissue engineering using biochemical and mechanical stimulation. Ann. Biomed. Eng. 31:391–402 [Google Scholar]
  67. Isenberg BC, Tranquillo RT. 67.  2003. Long-term cyclic distention enhances the mechanical properties of collagen-based media-equivalents. Ann. Biomed. Eng. 31:937–49 [Google Scholar]
  68. Humphrey JD. 68.  2003. Continuum biomechanics of soft biological tissues. Proc. R. Soc. Lond. Ser. A 459:3–46 [Google Scholar]
  69. Taber LA. 69.  2004. Nonlinear Theory of Elasticity: Applications in Biomechanics River Edge, NJ: World Sci399
  70. Holzapfel GA, Ogden RW. 70.  2010. Constitutive modelling of arteries. Proc. R. Soc. Lond. Ser. A 466:1551–97 [Google Scholar]
  71. Humphrey JD, Rajagopal KR. 71.  2003. A constrained mixture model for arterial adaptations to a sustained step change in blood flow. Biomech. Model Mechanobiol. 2:109–26 [Google Scholar]
  72. Isenberg BC, Williams C, Tranquillo RT. 72.  2006. Small-diameter artificial arteries engineered in vitro. Circ. Res. 98:25–35 [Google Scholar]
  73. Dahl SL, Vaughn ME, Hu JJ, Driessen NJ, Baaijens FP. 73.  et al. 2008. A microstructurally motivated model of the mechanical behavior of tissue engineered blood vessels. Ann. Biomed. Eng. 36:1782–92 [Google Scholar]
  74. Dahl SL, Vaughn ME, Niklason LE. 74.  2007. An ultrastructural analysis of collagen in tissue engineered arteries. Ann. Biomed. Eng. 35:1749–55 [Google Scholar]
  75. Lanir Y. 75.  1983. Constitutive equations for fibrous connective tissues. J. Biomech. 16:1–12 [Google Scholar]
  76. Niklason LE, Yeh AT, Calle EA, Bai Y, Valentin A, Humphrey JD. 76.  2010. Enabling tools for engineering collagenous tissues integrating bioreactors, intravital imaging, and biomechanical modeling. Proc. Natl. Acad. Sci. USA 107:3335–39This paper presents an integrated theoretical/experimental approach to the construction of the tissue-engineered blood vessels. [Google Scholar]
  77. Humphrey JD, Rajagopal KR. 77.  2002. A constrained mixture model for growth and remodeling of soft tissues. Math. Models Methods Appl. Sci. 12:407–30 [Google Scholar]
  78. Rodriguez EK, Hoger A, McCulloch AD. 78.  1994. Stress-dependent finite growth in soft elastic tissues. J. Biomech. 27:455–67 [Google Scholar]
  79. Taber LA, Humphrey JD. 79.  2001. Stress-modulated growth, residual stress, and vascular heterogeneity. J. Biomech. Eng. 123:528–35 [Google Scholar]
  80. Alford PW, Humphrey JD, Taber LA. 80.  2008. Growth and remodeling in a thick-walled artery model: effects of spatial variations in wall constituents. Biomech. Model Mechanobiol. 7:245–62 [Google Scholar]
  81. Raykin J, Rachev AI, Gleason RL Jr. 81.  2009. A phenomenological model for mechanically mediated growth, remodeling, damage, and plasticity of gel-derived tissue engineered blood vessels. J. Biomech. Eng. 131:101016 [Google Scholar]
  82. Fung YC. 82.  1991. What are the residual stresses doing in our blood vessels?. Ann. Biomed. Eng. 19:237–49 [Google Scholar]
  83. Chuong CJ, Fung YC. 83.  1986. On residual stresses in arteries. J. Biomech. Eng. 108:189–92 [Google Scholar]
  84. Zaucha MT, Gauvin R, Auger FA, Germain L, Gleason RL. 84.  2011. Biaxial biomechanical properties of self-assembly tissue-engineered blood vessels. J. R. Soc. Interface 8:244–56 [Google Scholar]
  85. Cowin SC. 85.  2004. Tissue growth and remodeling. Annu. Rev. Biomed. Eng. 6:77–107 [Google Scholar]
  86. Humphrey JD. 86.  2001. Stress, strain, and mechanotransduction in cells. J. Biomech. Eng. 123:638–41 [Google Scholar]
  87. Taber LA. 87.  1998. Biomechanical growth laws for muscle tissue. J. Theor. Biol. 193:201–13 [Google Scholar]
  88. Huang H, Kamm RD, Lee RT. 88.  2004. Cell mechanics and mechanotransduction: pathways, probes, and physiology. Cell Physiol. Am. J. Physiol. 287:C1–11 [Google Scholar]
  89. Hoffman BD, Crocker JC. 89.  2009. Cell mechanics: dissecting the physical responses of cells to force. Annu. Rev. Biomed. Eng. 11:259–88 [Google Scholar]
  90. Wakatsuki T, Kolodney MS, Zahalak GI, Elson EL. 90.  2000. Cell mechanics studied by a reconstituted model tissue. Biophys. J. 79:2353–68 [Google Scholar]
  91. Zahalak GI, Wagenseil JE, Wakatsuki T, Elson EL. 91.  2000. A cell-based constitutive relation for bio-artificial tissues. Biophys. J. 79:2369–81 [Google Scholar]
  92. Pryse KM, Nekouzadeh A, Genin GM, Elson EL, Zahalak GI. 92.  2003. Incremental mechanics of collagen gels: new experiments and a new viscoelastic model. Ann. Biomed. Eng. 31:1287–96 [Google Scholar]
  93. Wagenseil JE, Wakatsuki T, Okamoto RJ, Zahalak GI, Elson EL. 93.  2003. One-dimensional viscoelastic behavior of fibroblast populated collagen matrices. J. Biomech. Eng. 125:719–25 [Google Scholar]
  94. Wagenseil JE, Elson EL, Okamoto RJ. 94.  2004. Cell orientation influences the biaxial mechanical properties of fibroblast populated collagen vessels. Ann. Biomed. Eng. 32:720–31 [Google Scholar]
  95. Wagenseil JE, Okamoto RJ. 95.  2007. Modeling cell and matrix anisotropy in fibroblast populated collagen vessels. Biomech. Model Mechanobiol. 6:151–62 [Google Scholar]
  96. Marquez JP, Genin GM, Zahalak GI, Elson EL. 96.  2005. Thin bio-artificial tissues in plane stress: the relationship between cell and tissue strain, and an improved constitutive model. Biophys. J. 88:765–77 [Google Scholar]
  97. Marquez JP, Genin GM, Zahalak GI, Elson EL. 97.  2005. The relationship between cell and tissue strain in three-dimensional bio-artificial tissues. Biophys. J. 88:778–89 [Google Scholar]
  98. Sander EA, Stylianopoulos T, Tranquillo RT, Barocas VH. 98.  2009. Image-based multiscale modeling predicts tissue-level and network-level fiber reorganization in stretched cell-compacted collagen gels. Proc. Natl. Acad. Sci. USA 106:17675–80 [Google Scholar]
  99. Chandran PL, Barocas VH. 99.  2006. Affine versus non-affine fibril kinematics in collagen networks: theoretical studies of network behavior. J. Biomech. Eng. 128:259–70 [Google Scholar]
  100. Nelson CM, Inman JL, Bissell MJ. 100.  2008. Three-dimensional lithographically defined organotypic tissue arrays for quantitative analysis of morphogenesis and neoplastic progression. Nat. Protoc. 3:674–78 [Google Scholar]
  101. Nelson CM, Vanduijn MM, Inman JL, Fletcher DA, Bissell MJ. 101.  2006. Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 314:298–300 [Google Scholar]
  102. Gjorevski N, Nelson CM. 102.  2012. Mapping of mechanical strains and stresses around quiescent engineered three-dimensional epithelial tissues. Biophys. J. 103:152–62 [Google Scholar]
  103. Gjorevski N, Nelson CM. 103.  2010. Endogenous patterns of mechanical stress are required for branching morphogenesis. Integr. Biol. 2:424–34This paper uses 3D micropatterning techniques to show that mechanical stresses pattern branch locations in engineered mammary tissues. [Google Scholar]
  104. Engler AJ, Sen S, Sweeney HL, Discher DE. 104.  2006. Matrix elasticity directs stem cell lineage specification. Cell 126:677–89 [Google Scholar]
  105. Reilly GC, Engler AJ. 105.  2010. Intrinsic extracellular matrix properties regulate stem cell differentiation. J. Biomech. 43:55–62 [Google Scholar]
  106. Davies JA. 106.  2005. Mechanisms of Morphogenesis Amsterdam/Boston: Elsevier Acad374
  107. Gilbert SF. 107.  2010. Developmental Biology Sunderland, Mass.: Sinauer Assoc711
  108. Thompson DAW. 108.  1942. On Growth and Form Cambridge: Camb. Univ. Press1,116
  109. Trinkaus JP. 109.  1969. Cells into Organs: The Forces That Shape the Embryo Englewood Cliffs, NJ: Prentice-Hall237
  110. Patten BM. 110.  1951. Early Embryology of the Chick Philadelphia: Blakiston244
  111. Balfour FM. 111.  1880. A Treatise on Comparative Embryology London: Macmillan and Co.
  112. Lillie FR. 112.  1908. The Development of the Chick: An Introduction to Embryology New York: Holt472
  113. Taber LA. 113.  1995. Biomechanics of growth, remodeling, and morphogenesis. Appl. Mech. Rev. 48:1–59This excellent review paper provides a comprehensive discussion of theoretical and experimental studies of the mechanics of growth and remodeling. [Google Scholar]
  114. Koehl MAR. 114.  1990. Biomechanical approaches to morphogenesis. Semin. Dev. Biol. 1:367–78 [Google Scholar]
  115. Davidson L, von Dassow M, Zhou J. 115.  2009. Multi-scale mechanics from molecules to morphogenesis. Int. J. Biochem. Cell Biol. 41:2147–62 [Google Scholar]
  116. Taber LA. 116.  2006. Biophysical mechanisms of cardiac looping. Int. J. Dev. Biol. 50:323–32 [Google Scholar]
  117. Nerurkar NL, Ramasubramanian A, Taber LA. 117.  2006. Morphogenetic adaptation of the looping embryonic heart to altered mechanical loads. Dev. Dyn. 235:1822–29 [Google Scholar]
  118. Ramasubramanian A, Nerurkar NL, Achtien KH, Filas BA, Voronov DA, Taber LA. 118.  2008. On modeling morphogenesis of the looping heart following mechanical perturbations. J. Biomech. Eng. 130:061018 [Google Scholar]
  119. Hove JR, Koster RW, Forouhar AS, Acevedo-Bolton G, Fraser SE, Gharib M. 119.  2003. Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis. Nature 421:172–77 [Google Scholar]
  120. Wagenseil JE. 120.  2011. A constrained mixture model for developing mouse aorta. Biomech. Model Mechanobiol. 10:671–87 [Google Scholar]
  121. Nelson CM, Gleghorn JP. 121.  2012. Sculpting organs: mechanical regulation of tissue development. Annu. Rev. Biomed. Eng. 14:129–54 [Google Scholar]
  122. Schittny JC, Miserocchi G, Sparrow MP. 122.  2000. Spontaneous peristaltic airway contractions propel lung liquid through the bronchial tree of intact and fetal lung explants. Am. J. Respir. Cell Mol. Biol. 23:11–18 [Google Scholar]
  123. Jesudason EC, Smith NP, Connell MG, Spiller DG, White MR. 123.  et al. 2005. Developing rat lung has a sided pacemaker region for morphogenesis-related airway peristalsis. Am. J. Respir. Cell Mol. Biol. 32:118–27 [Google Scholar]
  124. Miller AA, Hooper SB, Harding R. 124.  1993. Role of fetal breathing movements in control of fetal lung distension. J. Appl. Physiol. 75:2711–17 [Google Scholar]
  125. Nelson CM, Jean RP, Tan JL, Liu WF, Sniadecki NJ. 125.  et al. 2005. Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. USA 102:11594–99 [Google Scholar]
  126. Fu J, Wang YK, Yang MT, Desai RA, Yu X. 126.  et al. 2010. Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Methods 7:733–36 [Google Scholar]
  127. Lui C, Lee K, Nelson CM. 127.  2012. Matrix compliance and RhoA direct the differentiation of mammary progenitor cells. Biomech. Model Mechanobiol. 11:1241–49 [Google Scholar]
  128. Lee K, Chen QK, Lui C, Cichon MA, Radisky DC, Nelson CM. 128.  2012. Matrix compliance regulates Rac1b localization, NADPH oxidase assembly, and epithelial-mesenchymal transition. Mol. Biol. Cell 23:4097–108 [Google Scholar]
  129. Gomez EW, Chen QK, Gjorevski N, Nelson CM. 129.  2010. Tissue geometry patterns epithelial-mesenchymal transition via intercellular mechanotransduction. J. Cell. Biochem. 110:44–51 [Google Scholar]
  130. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE. 130.  1997. Geometric control of cell life and death. Science 276:1425–28 [Google Scholar]
  131. Townes PL, Holtfreter J. 131.  1955. Directed movements and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128:53–120 [Google Scholar]
  132. Foty RA, Steinberg MS. 132.  2005. The differential adhesion hypothesis: a direct evaluation. Dev. Biol. 278:255–63 [Google Scholar]
  133. Manning ML, Foty RA, Steinberg MS, Schoetz EM. 133.  2010. Coaction of intercellular adhesion and cortical tension specifies tissue surface tension. Proc. Natl. Acad. Sci. USA 107:12517–22 [Google Scholar]
  134. Krieg M, Arboleda-Estudillo Y, Puech PH, Käfer J, Graner F. 134.  et al. 2008. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 10:429–36 [Google Scholar]
  135. Nakao K, Morita R, Saji Y, Ishida K, Tomita Y. 135.  et al. 2007. The development of a bioengineered organ germ method. Nat. Methods 4:227–30 [Google Scholar]
  136. Ikeda E, Morita R, Nakao K, Ishida K, Nakamura T. 136.  et al. 2009. Fully functional bioengineered tooth replacement as an organ replacement therapy. Proc. Natl. Acad. Sci. USA 106:13475–80 [Google Scholar]
  137. Mammoto T, Mammoto A, Torisawa YS, Tat T, Gibbs A. 137.  et al. 2011. Mechanochemical control of mesenchymal condensation and embryonic tooth organ formation. Dev. Cell 21:758–69 [Google Scholar]
  138. Hogan BL. 138.  1999. Morphogenesis. Cell 96:225–33 [Google Scholar]
  139. Du Y, Lo E, Ali S, Khademhosseini A. 139.  2008. Directed assembly of cell-laden microgels for fabrication of 3D tissue constructs. Proc. Natl. Acad. Sci. USA 105:9522–27 [Google Scholar]
  140. Sasai Y. 140.  2013. Cytosystems dynamics in self-organization of tissue architecture. Nature 493:318–26 [Google Scholar]
  141. Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E. 141.  et al. 2011. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472:51–56This paper demonstrates that cultured stem cell aggregates can spontaneously recapitulate optic cup morphogenesis in 3D culture. [Google Scholar]
  142. Eiraku M, Adachi T, Sasai Y. 142.  2012. Relaxation-expansion model for self-driven retinal morphogenesis: a hypothesis from the perspective of biosystems dynamics at the multi-cellular level. Bioessays 34:17–25 [Google Scholar]
  143. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N. 143.  et al. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:262–65 [Google Scholar]
  144. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG. 144.  et al. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469:415–18 [Google Scholar]
  145. Shyer AE, Tallinen T, Nerurkar NL, Wei Z, Gil ES. 145.  et al. 2013. Villification: how the gut gets its villi. Science 342:212–18 [Google Scholar]
  146. Rhodin JAG. 146.  2011. Architecture of the vessel wall. Comprehensive Physiology1–31 Hoboken, NJ: John Wiley & Sons [Google Scholar]
  147. Skalak R, Dasgupta G, Moss M, Otten E, Dullumeijer P, Vilmann H. 147.  1982. Analytical description of growth. J. Theor. Biol. 94:555–77 [Google Scholar]
  148. Skalak R. 148.  1982. Growth as a finite displacement field. Proc. IUTAM Symp. Finite Elast., Bethleham, PA347–55 Dordrecht: Springer Neth. [Google Scholar]
  149. Skalak R, Zargaryan S, Jain RK, Netti PA, Hoger A. 149.  1996. Compatibility and the genesis of residual stress by volumetric growth. J. Math. Biol. 34:889–914 [Google Scholar]
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Toward the Directed Self-Assembly of Engineered Tissues
Annual Review of Chemical and Biomolecular Engineering 5, 507 (2014); https://doi.org/10.1146/annurev-chembioeng-060713-040016
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