Engineering functional epithelium for regenerative medicine and in vitro organ models: A review

Tissue Engineering - Part B: Reviews

Volumn 19, Issue 6, 2013, Pages 529-543

  Vrana, Nihal E ^a,b,c   Lavalle, Philippe ^a,d   Dokmeci, Mehmet R ^b,c   Dehghani, Fariba ^e   Ghaemmaghami, Amir M ^f   Khademhosseini, Ali ^b,c,g  

^a INSERM   (France)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e UNIVERSITY OF SYDNEY   (Australia)

^f UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOTTOM-UP FABRICATION; EMERGING APPLICATIONS; ENGINEERED TISSUES; EPITHELIAL BARRIER; EPITHELIAL CELL MIGRATION; OPTIMAL STRUCTURES; REGENERATIVE MEDICINE; TISSUE INTERACTIONS;

BIOMIMETICS; HISTOLOGY; MODELS; RESPIRATORY SYSTEM; STRUCTURAL OPTIMIZATION; TISSUE ENGINEERING;

TISSUE;

AGGRECAN; BIOMATERIAL; CHITOSAN; COLLAGEN; DIMETICONE; ELASTIN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; GELATIN; LAMININ; MATRIX METALLOPROTEINASE; MUCIN; POLYLACTIC ACID; POLYMER; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ARTIFICIAL CELL; ASTHMA; BASEMENT MEMBRANE; BASOLATERAL MEMBRANE; BIOMIMETICS; BLADDER; BLADDER RECONSTRUCTION; BRONCHUS CANCER; CELL CULTURE; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL RENEWAL; CELL THERAPY; CELL TYPE; CILIARY DYSKINESIA; COMPUTER ASSISTED TOMOGRAPHY; CORNEA; CYSTIC FIBROSIS; EPITHELIUM; EPITHELIUM CELL; EPITHELIZATION; ESOPHAGUS; EXTRACELLULAR MATRIX; HUMAN; HYDROGEL; IN VITRO STUDY; INFECTION RISK; INTESTINE EPITHELIUM; LAB ON A CHIP; LUNG DISEASE; LUNG TRANSPLANTATION; MESENCHYME CELL; MUCUS; NONHUMAN; ORGAN ON A CHIP; ORGAN SYSTEMS; PATHOGENESIS; PRIORITY JOURNAL; REGENERATIVE MEDICINE; REVIEW; SKIN; SKIN GRAFT; THORAX RADIOGRAPHY; TISSUE ENGINEERING; TISSUE GRAFT; TRACHEA; TRACHEA DISEASE; TRACHEA RECONSTRUCTION; URETHROPLASTY; WOUND HEALING;

ANIMALS; EPITHELIAL CELLS; EPITHELIUM; HUMANS; MODELS, BIOLOGICAL; ORGAN CULTURE TECHNIQUES; REGENERATIVE MEDICINE; TISSUE ENGINEERING;

EID: 84887893632     PISSN: 19373368     EISSN: 19373376     Source Type: Journal    
DOI: 10.1089/ten.teb.2012.0603     Document Type: Review

References (129)

1. Lindsay, M. Clinical experience and applications of drugeluting stents in the noncoronary vasculature, bile duct and esophagus. Adv Drug Deliv Rev 58, 447, 2006
2. Zhang, W., Ahluwalia, I.P., and Yelick, P.C. Three dimensional dental epithelial-mesenchymal constructs of predetermined size and shape for tooth regeneration. Biomaterials 31, 7995, 2010
3. Ardizzone, S., and Porro, G.B. Biologic therapy for inflammatory bowel disease. Drugs 65, 2253, 2005
4. Coraux, C., Hajj, R., Lesimple, P., and Puchelle, E. Repair and regeneration of the airway epithelium. Med Sci 21, 1063, 2005
5. Mangoni, M.L. Host-defense peptides: from biology to therapeutic strategies. Cell Mol Life Sci 68, 2157, 2011
6. Priya, S.G., Jungvid, H., and Kumar, A. Skin tissue engineering for tissue repair and regeneration. Tissue Eng Part B Rev 14, 105, 2008
7. Liu, P., Deng, Z.H., Han, S.F., Liu, T., Wen, N., Lu, W., et al. Tissue-engineered skin containing mesenchymal stem cells improves burn wounds. Artif Organs 32, 925, 2008
8. Oberpenning, F., Meng, J., Yoo, J.J., and Atala, A. De novo reconstitution of a functional mammalian urinary bladder by tissue engineering. Nat Biotechnol 17, 149, 1999
9. Omori, K., Nakamura, T., Kanemaru, S., Asato, R., Yamashita, M., Tanaka, S., et al. Regenerative medicine of the trachea: the first human case. Ann Otol Rhinol Laryngol 114, 429, 2005
10. Bianco, P., and Robey, P.G. Stem cells in tissue engineering. Nature 414, 118, 2001
11. Coraux, C., Nawrocki-Raby, B., Hinnrasky, J., Kileztky, C., Gaillard, D., Dani, C., et al. Embryonic stem cells generate airway epithelial tissue. Am J Respir Cell Mol Biol 32, 87, 2005
12. Yang, J., Yamato, M., Shimizu, T., Sekine, H., Ohashi, K., Kanzaki, M., et al. Reconstruction of functional tissues with cell sheet engineering. Biomaterials 28, 5033, 2007
13. Shier, D., Butler, J., and Lewis, R. Hole?s Human Anatomy and Physiology. New York: McGraw-Hill, 2007
14. Sell, S., Barnes, C., Smith, M., McClure, M., Madurantakam, P., Grant, J., et al. Extracellular matrix regenerated: tissue engineering via electrospun biomimetic nanofibers. Polym Int 56, 1349, 2007
15. Zilberman, M., and Eberhart, R.C. Drug-eluting bioresorbable stents for various applications. Annu Rev Biomed Eng 8, 153, 2006
16. Hong, K.U., Reynolds, S.D., Watkins, S., Fuchs, E., and Stripp, B.R. In vivo differentiation potential of tracheal basal cells: evidence for multipotent and unipotent subpopulations. Am J Physiol Lung Cell Mol Physiol 286, L643, 2004
17. Joo, N.S., Wu, J.V., Krouse, M.E., Saenz, Y., and Wine, J.J. Optical method for quantifying rates of mucus secretion from single submucosal glands. Am J Physiol Lung Cell Mol Physiol 281, L458, 2001
18. Sancho, E., Batlle, E., and Clevers, H. Live and let die in the intestinal epithelium. Curr Opin Cell Biol 15, 763, 2003
19. Powell, D.W., Adegboyega, P.A., Di Mari, J.F., and Mifflin, R.C. Epithelial cells and their neighbors, I. role of intestinal myofibroblasts in development, repair, and cancer. Am J Physiol Gastrointest Liver Physiol 289, G2, 2005
20. Proud, D., and Leigh, R. Epithelial cells and airway diseases. Immunol Rev 242, 186, 2011
21. Liu, J., Bian, Z., Kuijpers-Jagtman, A.M., and Von den Hoff, J.W. Skin and oral mucosa equivalents: construction and performance. Orthod Craniofac Res 13, 11, 2010
22. Dongari-Bagtzoglou, A., and Kashleva, H. Development of a highly reproducible three-dimensional organotypic model of the oral mucosa. Nat Protoc 1, 2012, 2006
23. Mooney, D.J., and Vandenburgh, H. Cell delivery mechanisms for tissue repair. Cell Stem Cell 2, 205, 2008
24. Yen, C.-M., Chan, C.-C., and Lin, S.-J. High-throughput reconstitution of epithelial-mesenchymal interaction in folliculoid microtissues by biomaterial-facilitated selfassembly of dissociated heterotypic adult cells. Biomaterials 31, 4341, 2010
25. Zhu, Y., Leong, M.F., Ong, W.F., Chan-Park, M.B., and Chian, K.S. Esophageal epithelium regeneration on fibronectin grafted poly(L-lactide-co- caprolactone) (PLLC) nanofiber scaffold. Biomaterials 28, 861, 2007
26. Kao, B., Kadomatsu, K., and Hosaka, Y. Construction of synthetic dermis and skin based on a self-assembled peptide hydrogel scaffold. Tissue Eng Part A 15, 2385, 2009
27. Vrana, N.E., Dupret-Bories, A., Bach, C., Chaubaroux, C., Coraux, C., Vautier, D., et al. Modification of macroporous titanium tracheal implants with biodegradable structures: Tracking in vivo integration for determination of optimal in situ epithelialization conditions. Biotechnol Bioeng 109, 2134, 2012
28. Neal, R.A., McClugage, S.G., Link, M.C., Sefcik, L.S., Ogle, R.C., and Botchwey, E.A. Laminin nanofiber meshes that mimic morphological properties and bioactivity of basement membranes. Tissue Eng Part C Methods 15, 11, 2009
29. Hayakawa, T., Yoshinari, M., Nitta, K., and Inoue, K. Collagen nanofiber on titanium or partially stabilized zirconia by electrospray deposition. J Hard Tissue Biol 19, 5, 2010
30. Hajicharalambous, C.S., Lichter, J., Hix, W.T., Swierczewska, M., Rubner, M.F., and Rajagopalan, P. Nano- and sub-micron porous polyelectrolyte multilayer assemblies: biomimetic surfaces for human corneal epithelial cells. Biomaterials 30, 4029, 2009
31. Tsai, R.J., Li, L.M., and Chen, J.K. Reconstruction of damaged corneas by transplantation of autologous limbal epithelial cells. New Engl J Med 343, 86, 2000
32. Kundu, A.K., Gelman, J., and Tyson, D.R. Composite thin film and electrospun biomaterials for urologic tissue reconstruction. Biotechnol Bioeng 108, 207, 2011
33. Noh, H.K., Lee, S.W., Kim, J.M., Oh, J.E., Kim, K.H., Chung, C.P., et al. Electrospinning of chitin nanofibers: Degradation behavior and cellular response to normal human keratinocytes and fibroblasts. Biomaterials 27, 3934, 2006
34. Vrana, N.E., Dupret, A., Coraux, C., Vautier, D., Debry, C., and Lavalle, P. Hybrid titanium/biodegradable polymer implants with an hierarchical pore structure as a means to control selective cell movement. Plos One 6, e20480 2011
35. Risbud, M., Endres, M., Ringe, J., Bhonde, R., and Sittinger, M. Biocompatible hydrogel supports the growth of respiratory epithelial cells: possibilities in tracheal tissue engineering. J Biomed Mater Res 56, 120, 2001
36. Kinikoglu, B., Carlos Rodriguez-Cabello, J., Damour, O., and Hasirci, V. The influence of elastin-like recombinant polymer on the self-renewing potential of a 3D tissue equivalent derived from human lamina propria fibroblasts and oral epithelial cells. Biomaterials 32, 5756, 2011
37. Rolli, C.G., Nakayama, H., Yamaguchi, K., Spatz, J.P., Kemkemer, R., and Nakanishi, J. Switchable adhesive substrates: revealing geometry dependence in collective cell behavior. Biomaterials 33, 2409, 2012
38. Nagpal, R., Patel, A., and Gibson, M.C. Epithelial topology. Bioessays 30, 260, 2008
39. Chistiakov, D.A. Endogenous and exogenous stem cells: a role in lung repair and use in airway tissue engineering and transplantation. J Biomed Sci 17, 92 2010
40. Agle, K.A., Vongsa, R.A., and Dwinell, M.B. Chemokine stimulation promotes enterocyte migration through laminin-specific integrins. Am J Physiol Gastrointest Liver Physiol 301, G968, 2011
41. Koshikawa, N., Giannelli, G., Cirulli, V., Miyazaki, K., and Quaranta, V. Role of cell surface Metalloprotease Mt1-Mmp in epithelial cell migration over Laminin-5. J Cell Biol 148, 615, 2000
42. Shastri, V.P. In vivo engineering of tissues: biological considerations, challenges, strategies, and future directions. Adv Mater 21, 3246, 2009
43. Mori, H., Gjorevski, N., Inman, J.L., Bissell, M.J., and Nelson, C.M. Self-organization of engineered epithelial tubules by differential cellular motility. Proc Natl Acad Sci U S A 106, 14890, 2009
44. Diehl, K.A., Foley, J.D., Nealey, P.F., and Murphy, C.J. Nanoscale topography modulates corneal epithelial cell migration. J Biomed Mater Res Part A 75A, 603, 2005
45. Fong, E., Tzlil, S., and Tirrell, D.A. Boundary crossing in epithelial wound healing. Proc Natl Acad Sci U S A 107, 19302, 2010
46. Atala, A. Engineering organs. Curr Opin Biotechnol 20, 575, 2009
47. Cartwright, L., Farhat, W.A., Sherman, C., Chen, J., Babyn, P., Yeger, H., et al. Dynamic contrast-enhanced MRI to quantify VEGF-enhanced tissue-engineered bladder graft neovascularization: pilot study. J Biomed Mater Res Part A 77A, 390, 2006
48. Kirkpatrick, C.J., Fuchs, S., Hermanns, M.I., Peters, K., and Unger, R.E. Cell culture models of higher complexity in tissue engineering and regenerative medicine. Biomaterials 28, 5193, 2007
49. Zorlutuna, P., Jeong, J.H., Kong, H., and Bashir, R. Stereolithography- based hydrogel microenvironments to examine cellular interactions. Adv Funct Mater 21, 3642, 2011
50. Hofmann, A., Ritz, U., Verrier, S., Eglin, D., Alini, M., Fuchs, S., et al. The effect of human osteoblasts on proliferation and neo-vessel formation of human umbilical vein endothelial cells in a long-term 3D co-culture on polyurethane scaffolds. Biomaterials 29, 4217, 2008
51. Kirkpatrick, C.J., Fuchs, S., and Unger, R.E. Co-culture systems for vascularization - Learning from nature. Adv Drug Deliv Rev 63, 291, 2011
52. Zani, B.G., Kojima, K., Vacanti, C.A., and Edelman, E.R. Tissue-engineered endothelial and epithelial implants differentially and synergistically regulate airway repair. Proc Natl Acad Sci U S A 105, 7046, 2008
53. Honda, M.J., Tsuchiya, S., Sumita, Y., Sagara, H., and Ueda, M. The sequential seeding of epithelial and mesenchymal cells for tissue-engineered tooth regeneration. Biomaterials 28, 680, 2007
54. Honda, M.J., Shinohara, Y., Hata, K.I., and Ueda, M. Subcultured odontogenic epithelial cells in combination with dental mesenchymal cells produce enamel-dentin-like complex structures. Cell Transplant 16, 833, 2007
55. Mahjour, S.B., Ghaffarpasand, F., and Wang, H.J. Hair follicle regeneration in skin grafts: current concepts and future perspectives. Tissue Eng Part B Rev 18, 15, 2012
56. Pageau, S.C., Sazonova, O.V., Wong, J.Y., Soto, A.M., and Sonnenschein, C. The effect of stromal components on the modulation of the phenotype of human bronchial epithelial cells in 3D culture. Biomaterials 32, 7169, 2011
57. Gray, F.L., Turner, C.G., Ahmed, A., Calvert, C.E., Zurakowski, D., and Fauza, D.O. Prenatal tracheal reconstruction with a hybrid amniotic mesenchymal stem cells- engineered construct derived from decellularized airway. J Pediatr Surg 47, 1072, 2012
58. Green, N., Huang, Q., Khan, L., Battaglia, G., Corfe, B., MacNeil, S., et al. The development and characterization of an organotypic tissue-engineered human esophageal mucosal model. Tissue Eng Part A 16, 1053, 2010
59. Liu, J., Mao, J.J., and Chen, L. Epithelial-mesenchymal interactions as a working concept for oral mucosa regeneration. Tissue Eng Part B Rev 17, 25, 2011
60. Vrana, N.E., Builles, N., Justin, V., Bednarz, J., Pellegrini, G., Ferrari, B., et al. Development of a reconstructed cornea from collagen-chondroitin sulfate foams and human cell cultures. Invest Ophthalmol Vis Sci 49, 5325, 2008
61. Rainer, C., Wechselberger, G., Bauer, T., Neumeister, M.W., Lille, S., Mowlavi, A., et al. Transplantation of tracheal epithelial cells onto a prefabricated capsule pouch with fibrin glue as a delivery vehicle. J Thorac Cardiovasc Surg 121, 1187, 2001
62. Li, Y.W., Liu, W.H., Hayward, S.W., Cunha, G.R., and Baskin, L.S. Plasticity of the urothelial phenotype: Effects of gastro-intestinal mesenchyme/stroma and implications for urinary tract reconstruction. Differentiation 66, 126, 2000
63. Koo, J.P., Kim, C.-H., Lee, J.-G., Kim, K.-S., and Yoon, J.-H. Airway reconstruction with carrier-free cell sheets composed of autologous nasal squamous epithelium. Laryngoscope 117, 1750, 2007
64. Tan, Q., Steiner, R., Yang, L., Welti, M., Neuenschwander, P., Hillinger, S., et al. Accelerated angiogenesis by continuous medium flow with vascular endothelial growth factor inside tissue-engineered trachea. Eur J Cardiothorac Surg 31, 806, 2007
65. Kanzaki, M., Yamato, M., Hatakeyama, H., Kohno, C., Yang, J., Umemoto, T., et al. Tissue engineered epithelial cell sheets for the creation of a bioartificial trachea. Tissue Eng 12, 1275, 2006
66. Nishida, K., Yamato, M., Hayashida, Y., Watanabe, K., Yamamoto, K., Adachi, E., et al. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. New Engl J Med 351, 1187, 2004
67. Bader, A., and Macchiarini, P. Moving towards in situ tracheal regeneration: the bionic tissue engineered transplantation approach. J Cell Mol Med 14, 1877, 2010
68. Kunisaki, S.M., Freedman, D.A., and Fauza, D.O. Fetal tracheal reconstruction with cartilaginous grafts engineered from mesenchymal amniocytes. J Pediatr Surg 41, 675, 2006
69. Donnenberg, V.S., Zimmerlin, L., Rubin, J.P., and Donnenberg, A.D. Regenerative therapy after cancer: what are the risks? Tissue Eng Part B Rev 16, 567, 2010
70. Park, K.S., Wells, J.M., Zorn, A.M., Wert, S.E., Laubach, V.E., Fernandez, L.G., et al. Transdifferentiation of ciliated cells during repair of the respiratory epithelium. Am J Respir Cell Mol Biol 34, 151, 2006
71. Wendt, M., Tian, M., and Schiemann, W. Deconstructing the mechanisms and consequences of TGF-b-induced EMT during cancer progression. Cell Tissue Res 347, 85, 2012
72. Mani, S.A., Guo, W., Liao, M.-J., Eaton, E.N., Ayyanan, A., Zhou, A.Y., et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704, 2008
73. Lutolf, M.P., and Hubbell, J.A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23, 47, 2005
74. Macchiarini, P., Jungebluth, P., Go, T., Asnaghi, M.A., Rees, L.E., Cogan, T.A., et al. Clinical transplantation of a tissueengineered airway. Lancet 372, 2023, 2008
75. Dupuit, F., Gaillard, D., Hinnrasky, J., Mongodin, E., De Bentzmann, S., Copreni, E., et al. Differentiated and functional human airway epithelium regeneration in tracheal xenografts. Am J Physiol Lung Cell Mol Physiol 278, L165, 2000
76. Shieh, S.J., and Vacanti, J.P. State-of-the-art tissue engineering: From tissue engineering to organ building. Surgery 137, 1, 2005
77. Lee, K.H. Tissue-engineered human living skin substitutes: development and clinical application. Yonsei Med J 41, 774, 2000
78. Guerra, L., Dellambra, E., Panacchia, L., and Paionni, E. Tissue engineering for damaged surface and lining epithelia: stem cells, current clinical applications, and available engineered tissues. Tissue Eng Part B Rev 15, 91, 2009
79. Badylak, S.F., Weiss, D.J., Caplan, A., and Macchiarini, P. Engineered whole organs and complex tissues. Lancet 379, 943
80. Bhargava, S., Patterson, J.M., Inman, R.D., MacNeil, S., and Chapple, C.R. Tissue-engineered buccal mucosa urethroplasty - Clinical outcomes. Eur Urol 53, 1263, 2008
81. 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
82. Lauer, G., and Schimming, R. Tissue-engineered mucosa graft for reconstruction of the intraoral lining after freeing of the tongue: a clinical and immunohistologic study. J Oral Maxillofac Surg 59, 169, 2001
83. Wang, S.H., and Nagrath, D. Liver tissue engineering. In: Burdick, J.A., Mauck, R.L., eds. Biomaterials for Tissue Engineering Applications: A Review of the Past and Future Trends. NY: Springer, 2011, pp. 389-419
84. Lange, P., Fishman, J.M., Elliott, M.J., De Coppi, P., and Birchall, M.A. What can regenerative medicine offer for infants with laryngotracheal agenesis? Otolaryngol Head Neck Surg 145, 544, 2011
85. Ott, L.M., Weatherly, R.A., and Detamore, M.S. Overview of tracheal tissue engineering: clinical need drives the laboratory approach. Ann Biomed Eng 39, 2091, 2011
86. Omori, K., Tada, Y., Suzuki, T., Nomoto, Y., Matsuzuka, T., Kobayashi, K., et al. Clinical application of in situ tissue engineering using a scaffolding technique for reconstruction of the larynx and trachea. Ann Otol Rhinol Laryngol 117, 673, 2008
87. Go, T., Jungebluth, P., Baiguero, S., Asnaghi, A., Martorell, J., Ostertag, H., et al. Both epithelial cells and mesenchymal stem cell-derived chondrocytes contribute to the survival of tissue-engineered airway transplants in pigs. J Thorac Cardiovasc Surg 139, 437, 2010
88. Schultz, P., Vautier, D., Richert, L., Jessel, N., Haikel, Y., Schaaf, P., et al. Polyelectrolyte multilayers functionalized by a synthetic analogue of an anti-inflammatory peptide, alpha-MSH, for coating a tracheal prosthesis. Biomaterials 26, 2621, 2005
89. Martinod, E., Radu, D.M., Chouahnia, K., Seguin, A., Fialaire- Legendre, A., Brillet, P.-Y., et al. Human transplantation of a biologic airway substitute in conservative lung cancer surgery. Ann Thorac Surg 91, 837, 2011
90. Roomans, G.M. Tissue engineering and the use of stem/ progenitor cells for airway epithelium repair. Eur Cell Mater 19, 284, 2010
91. Endres, M., Leinhase, I., Kaps, C., Wentges, M., Unger, M., Olze, H., et al. Changes in the gene expression pattern of cytokeratins in human respiratory epithelial cells during culture. Eur Arch Otorhinolaryngol 262, 390, 2005
92. Widdicombe, J.H., Sachs, L.A., Morrow, J.L., and Finkbeiner, W.E. Expansion of cultures of human tracheal epithelium with maintenance of differentiated structure and function. Biotechniques 39, 249, 2005
93. Pezzulo, A.A., Starner, T.D., Scheetz, T.E., Traver, G.L., Tilley, A.E., Harvey, B.-G., et al. The air-liquid interface and use of primary cell cultures are important to recapitulate the transcriptional profile of in vivo airway epithelia. Am J Physiol Lung Cell Mol Physiol 300, L25, 2011
94. Wang, Y., Wong, L.B., and Mao, H. Induction of ciliated cells from avian embryonic stem cells using threedimensional matrix. Tissue Eng Part C Methods 16, 929, 2010
95. Huang, T.W., Chan, Y.H., Cheng, P.W., Young, Y.H., Lou, P.J., and Young, T.H. Increased mucociliary differentiation of human respiratory epithelial cells on hyaluronan-derivative membranes. Acta Biomater 6, 1191, 2010
96. Bukowy, Z., Zietkiewicz, E., and Witt, M. In vitro culturing of ciliary respiratory cells-a model for studies of genetic diseases. J Appl Genet 52, 39, 2011
97. Grillo, H.C. Tracheal replacement: a critical review. Ann Thorac Surg 73, 1995, 2002
98. Asnaghi, M.A., Jungebluth, P., Raimondi, M.T., Dickinson, S.C., Rees, L.E., Go, T., et al. A double-chamber rotating bioreactor for the development of tissue-engineered hollow organs: from concept to clinical trial. Biomaterials 30, 5260, 2009
99. Gauvin, R., and Khademhosseini, A. Microscale technologies and modular approaches for tissue engineering: moving toward the fabrication of complex functional structures. Acs Nano 5, 4258, 2011
100. Fernandez, J.G., and Khademhosseini, A. Micro-masonry: construction of 3D structures by microscale self-assembly. Adv Mater 22, 2538, 2010
101. Yanagawa, F., Kaji, H., Jang, Y.H., Bae, H., Du, Y.A., Fukuda, J., et al. Directed assembly of cell-laden microgels for building porous three-dimensional tissue constructs. J Biomed Mater Res Part A 97A, 93, 2011
102. Swiston, A.J., Gilbert, J.B., Irvine, D.J., Cohen, R.E., and Rubner, M.F. Freely suspended cellular 'Backpacks' lead to cell aggregate self-assembly. Biomacromolecules 11, 1826, 2010
103. Duan, X., and Sheardown, H. Dendrimer crosslinked collagen as a corneal tissue engineering scaffold: Mechanical properties and corneal epithelial cell interactions. Biomaterials 27, 4608, 2006
104. Kocgozlu, L., Lavalle, P., Koenig, G., Senger, B., Haikel, Y., Schaaf, P., et al. Selective and uncoupled role of substrate elasticity in the regulation of replication and transcription in epithelial cells. J Cell Sci 123, 29, 2010
105. Rosso, F., Giordano, A., Barbarisi, M., and Barbarisi, A. From cell-ECM interactions to tissue engineering. J Cell Physiol 199, 174, 2004
106. Castillon, N., Avril-Delplanque, A., Coraux, C., Delenda, C., Peault, B., Danos, O., et al. Regeneration of a welldifferentiated human airway surface epithelium by spheroid and lentivirus vector-transduced airway cells. J Gene Med 6, 846, 2004
107. Higa, K., Shimmura, S., Kato, N., Kawakita, T., Miyashita, H., Itabashi, Y., et al. Proliferation and differentiation of transplantable rabbit epithelial sheets engineered with or without an amniotic membrane carrier. Invest Ophthalmol Vis Sci 48, 597, 2007
108. Lai, J.-Y., Lu, P.-L., Chen, K.-H., Tabata, Y., and Hsiue, G.-H. Effect of charge and molecular weight on the functionality of gelatin carriers for corneal endothelial cell therapy. Biomacromolecules 7, 1836, 2006
109. Peppas, N.A., and Sahlin, J.J. Hydrogels as mucoadhesive and bioadhesive materials: a review. Biomaterials 17, 1553, 1996
110. Yang, T.-L. Chitin-based materials in tissue engineering: applications in soft tissue and epithelial organ. Int J Mol Sci 12, 1936, 2011
111. Wang, D.-A., Varghese, S., Sharma, B., Strehin, I., Fermanian, S., Gorham, J., et al. Multifunctional chondroitin sulphate for cartilage tissue-biomaterial integration. Nat Mater 6, 385, 2007
112. McDermott, M.K., Chen, T.H., Williams, C.M., Markley, K.M., and Payne, G.F. Mechanical properties of biomimetic tissue adhesive based on the microbial transglutaminasecatalyzed crosslinking of gelatin. Biomacromolecules 5, 1270, 2004
113. Kwak, M.K., Pang, C., Jeong, H.-E., Kim, H.-N., Yoon, H., Jung, H.-S., et al. Towards the next level of bioinspired dry adhesives: new designs and applications. Adv Funct Mater 21, 3606, 2011
114. Jiwoon, K., Eugene, C., Sukho, P., and Metin, S. Friction enhancement via micro-patterned wet elastomer adhesives on small intestinal surfaces. Biomed Mater 1, 216, 2006
115. Murphy, M.P., Kim, S., and Sitti, M. Enhanced adhesion by gecko-inspired hierarchical fibrillar adhesives. ACS Appl Mater Interfaces 1, 849, 2009
116. Kim, S., Sitti, M., Xie, T., and Xiao, X. Reversible dry microfibrillar adhesives with thermally controllable adhesion. Soft Matter 5, 3689, 2009
117. Zhang, C., Zhao, Z.Q., Rahim, N.A.A., van Noort, D., and Yu, H. Towards a human-on-chip: culturing multiple cell types on a chip with compartmentalized microenvironments. Lab Chip 9, 3185, 2009
118. 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
119. Torisawa, Y.-S., Mosadegh, B., Cavnar, S.P., Ho, M., and Takayama, S. Transwells with microstamped membranes produce micropatterned two-dimensional and threedimensional co-cultures. Tissue Eng Part C Methods 17, 61, 2011
120. Paz, A.C., Javaherian, S., and McGuigan, A.P. Tools for micropatterning epithelial cells into microcolonies on transwell filter substrates. Lab Chip 11, 3440, 2011
121. Nelson, C.M., Khauv, D., Bissell, M.J., and Radisky, D.C. Change in cell shape is required for matrix metalloproteinaseinduced epithelial-mesenchymal transition of mammary epithelial cells. J Cell Biochem 105, 25, 2008
122. Paguirigan, A., and Beebe, D.J. Gelatin based microfluidic devices for cell culture. Lab Chip 6, 407, 2006
123. Sun, T., Swindle, E.J., Collins, J.E., Holloway, J.A., Davies, D.E., and Morgan, H. On-chip epithelial barrier function assays using electrical impedance spectroscopy. Lab Chip 10, 1611, 2010
124. Terryn, C., Bonnomet, A., Cutrona, J., Coraux, C., Tournier, J.M., Nawrocki-Raby, B., et al. Video-microscopic imaging of cell spatio-temporal dispersion and migration. Crit Rev Oncol/Hematol 69, 144, 2009
125. Andreu, N., Zelmer, A., and Wiles, S. Noninvasive biophotonic imaging for studies of infectious disease. FEMS Microbiol Rev 35, 360, 2011
126. Huh, D., Hamilton, G.A., and Ingber, D.E. From 3D cell culture to organs-on-chips. Trends Cell Biol 21, 745, 2011
127. Moraes, C., Mehta, G., Lesher-Perez, S.C., and Takayama, S. Organs-on-a-chip: a focus on compartmentalized microdevices. Ann Biomed Eng 40, 1211, 2012
128. Kim, H.J., Huh, D., Hamilton, G., and Ingber, D.E. Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow. Lab Chip 12, 2165, 2012
129. Esch, M., Sung, J., Yang, J., Yu, C., Yu, J., March, J., et al. On chip porous polymer membranes for integration of gastrointestinal tract epithelium with microfluidic 'bodyon- a-chip' devices. Biomed Microdevices 14, 895, 2012.