A tale of two tissues: Stem cells in cartilage and corneal tissue engineering

Current Stem Cell Research and Therapy

Volumn 5, Issue 1, 2010, Pages 37-48

  Ambrose, Winnette McIntosh ^a   Schein, Oliver ^b   Elisseeff, Jennifer ^a,b  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Cartilage; Cornea; Differentiation; Scaffold; Stem cell; Tissue engineering

Indexed keywords

ADIPOSE TISSUE CELL; ADULT; CARTILAGE; CELL DIFFERENTIATION; CELL POPULATION; CELL REGENERATION; CELL THERAPY; CORNEA; CORNEA EPITHELIUM; CORNEA STROMA; EMBRYONIC STEM CELL; HUMAN; LIMBAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL; STEM CELL TRANSPLANTATION; TISSUE ENGINEERING;

ADULT STEM CELLS; ANIMALS; CARTILAGE; CELL DIFFERENTIATION; CORNEA; EMBRYONIC STEM CELLS; GUIDED TISSUE REGENERATION; HEMATOPOIETIC STEM CELL MOBILIZATION; HUMANS; MESENCHYMAL STEM CELLS; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 77949357348     PISSN: 1574888X     EISSN: None     Source Type: Journal    
DOI: 10.2174/157488810790442804     Document Type: Review

References (195)

1. Langer RS, Vacanti JP. Tissue engineering: The challenges ahead. Sci Am 1999; 280: 86-9.
2. Daar AS, Greenwood HL. A proposed definition of regenerative medicine. J Tissue Eng Regener Med 2007; 1: 179-84.
3. Meek KM, Boote C. The organization of collagen in the corneal stroma. Exp Eye Res 2004; 78: 503-12.
4. Meek KM, Fullwood NJ. Corneal and scleral collagens-a microscopist's perspective. Micron 2001; 32: 261-72.
5. Klintworth GK. The cornea - structure and macromolecules in health and disease. A review. Am J Pathol 1977; 89: 718-808.
6. Kurpakus WM, Kernacki KA, Hazlett LD. Corneal cell proteins and ocular surface pathology. Biotech Histochem 1999; 74: 146-59.
7. Darling EM, Athanasiou KA. Growth factor impact on articular cartilage subpopulations. Cell Tissue Res 2005; 322: 463-73.
8. Mizrahi J, Maroudas A, Lanir Y, Ziv I, Webber TJ. The "instantaneous" deformation of cartilage: Effects of collagen fiber orientation and osmotic stress. Biorheology 1986; 23: 311-30.
9. Kydd AS, Reno CR, Tsao HW, Hart DA. Impact of age, systemic glucocorticoids, and progressive knee arthritis on specific mRNA levels in different areas of the rabbit cornea. Cornea 2007; 26: 352-61.
10. Elisseeff J. Injectable cartilage tissue engineering. Expert Opin Biol Ther 2004; 4: 1849-59.
11. Marlovits S, Zeller P, Singer P, Resinger C, Vecsei V. Cartilage repair: generations of autologous chondrocyte transplantation. Eur J Radiol 2006; 57: 24-31.
12. Whitcher JP, Srinivasan M, Upadhyay MP. Corneal blindness: A global perspective. Bull World Health Organ 2001; 79: 214-21.
13. Darlington JK, Adrean SD, Schwab IR. Trends of penetrating keratoplasty in the United States from 1980 to 2004. Ophthalmology 2006; 113: 2171-5.
14. Moffatt SL, Cartwright VA, Stumpf TH. Centennial review of corneal transplantation. Clin Experiment Ophthalmol 2005; 33: 642-57.
15. Aquavella JV, Qian Y, McCormick GJ, Palakuru JR. Keratoprosthesis: Current techniques. Cornea 2006; 25: 656-62.
16. Chirila TV. An overview of the development of artificial corneas with porous skirts and the use of PHEMA for such an application. Biomaterials 2001; 22: 3311-7.
17. Hille K. Keratoprostheses. Clinical aspects. Ophthalmologe 2002; 99: 523-31.
18. Ilhan-Sarac O, Akpek EK. Current concepts and techniques in keratoprosthesis. Curr Opin Ophthalmol 2005; 16: 246-50.
19. Khan B, Dudenhoefer EJ, Dohlman CH. Keratoprosthesis: An update. Curr Opin Ophthalmol 2001; 12: 282-7.
20. Yaghouti F, Nouri M, Abad JC, Power WJ, Doane MG, Dohlman CH. Keratoprosthesis: Preoperative prognostic categories. Cornea 2001; 20: 19-23.
21. Cotsarelis G, Cheng SZ, Dong G, Sun TT, Lavker RM. Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: Implications on epithelial stem cells. Cell 1989; 57: 201-9.
22. Lindberg K, Brown ME, Chaves HV, Kenyon KR, Rheinwald JG. In vitro propagation of human ocular surface epithelial cells for transplantation. Invest Ophthalmol Vis Sci 1993; 34: 2672-9.
23. Majo F, Rochat A, Nicolas M, Jaoude GA, Barrandon Y. Oligopotent stem cells are distributed throughout the mammalian ocular surface. Nature 2008.
24. Dowthwaite GP, Bishop JC, Redman SN, et al. The surface of articular cartilage contains a progenitor cell population. J Cell Sci 2004; 117: 889-97.
25. Martin JM, Smith M, Al-Rubeai M. Cryopreservation and in vitro expansion of chondroprogenitor cells isolated from the superficial zone of articular cartilage. Biotechnol Prog 2005; 21: 168-177.
26. Johnstone B, Hering TM, Caplan AI, Goldberg VM, Yoo JU. In vitro chondrogenesis of bone marrow-derived mesenchymal progenitor cells. Exp Cell Res 1998; 238: 265-72.
27. Williams CG, Kim TK, Taboas A, Malik A, Manson P, Elisseeff J. In vitro chondrogenesis of bone marrow-derived mesenchymal stem cells in a photopolymerizing hydrogel. Tissue Eng 2003; 9: 679-88.
28. Sharma B, Williams CG, Khan M, Manson P, Elisseeff JH. In vivo chondrogenesis of mesenchymal stem cells in a photopolymerized hydrogel. Plast Reconstr Surg 2007; 119: 112-20.
29. Hwang NS, Varghese S, Puleo C, Zhang Z, Elisseeff J. Morphogenetic signals from chondrocytes promote chondrogenic and osteogenic differentiation of mesenchymal stem cells. J Cell Physiol 2007; 212: 281-4.
30. Ahmed N, Dreier R, Gopferich A, Grifka J, Grassel S. Soluble signalling factors derived from differentiated cartilage tissue affect chondrogenic differentiation of rat adult marrow stromal cells. Cell Physiol Biochem 2007; 20: 665-78.
31. Coleman RM, Case ND, Guldberg RE. Hydrogel effects on bone marrow stromal cell response to chondrogenic growth factors. Biomaterials 2007; 28: 2077-86.
32. Xu J, Wang W, Ludeman M, et al. Chondrogenic differentiation of human mesenchymal stem cells in three-dimensional alginate gels. Tissue Eng Part A 2008; 14(5): 667-80.
33. Mauck RL, Yuan X, Tuan RS. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture. Osteoarthritis Cartilage 2006; 14: 179-89.
34. Huang CY, Reuben PM, D'Ippolito G, Schiller PC, Cheung HS. Chondrogenesis of human bone marrow-derived mesenchymal stem cells in agarose culture. Anat Rec A Discov Mol Cell Evol Biol 2004; 278: 428-36.
35. Pang Y, Cui P, Chen W, Gao P, Zhang H. Quantitative study of tissue-engineered cartilage with human bone marrow mesenchymal stem cells. Arch Facial Plast Surg 2005; 7: 7-11.
36. Chen G, Liu D, Tadokoro M, et al. Chondrogenic differentiation of human mesenchymal stem cells cultured in a cobweb-like biodegradable scaffold. Biochem Biophys Res Commun 2004; 322: 50-5.
37. Fan H, Hu Y, Zhang C, et al. Cartilage regeneration using mesenchymal stem cells and a PLGA-gelatin/chondroitin/hyaluronate hybrid scaffold. Biomaterials 2006; 27: 4573-80.
38. Fan H, Hu Y, Qin L, Li X, Wu H, Lv R. Porous gelatin-chondroitin- hyaluronate tri-copolymer scaffold containing microspheres loaded with TGF-beta1 induces differentiation of mesenchymal stem cells in vivo for enhancing cartilage repair. J Biomed Mater Res A 2006; 77: 785-94.
39. Li WJ, Tuli R, Okafor C, et al. A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 2005; 26: 599-609.
40. Huang CY, Reuben PM, Cheung HS. Temporal expression patterns and corresponding protein inductions of early responsive genes in rabbit bone marrow-derived mesenchymal stem cells under cyclic compressive loading. Stem Cells 2005; 23: 1113-21.
41. Mauck RL, Byers BA, Yuan X, Tuan RS. Regulation of cartilaginous ECM gene transcription by chondrocytes and MSCs in 3D culture in response to dynamic loading. Biomech Model Mechanobiol 2007; 6: 113-25.
42. Miyanishi K, Trindade MC, Lindsey DP, et al. Effects of hydrostatic pressure and transforming growth factor-beta 3 on adult human mesenchymal stem cell chondrogenesis in vitro. Tissue Eng 2006; 12: 1419-28.
43. Miyanishi K, Trindade MC, Lindsey DP, et al. Dose- and timedependent effects of cyclic hydrostatic pressure on transforming growth factor-beta3-induced chondrogenesis by adult human mesenchymal stem cells in vitro. Tissue Eng 2006; 12: 2253-62.
44. Freed LE, Hollander AP, Martin I, Barry JR, Langer R, Vunjak-Novakovic G. Chondrogenesis in a cell-polymer-bioreactor system. Exp Cell Res 1998; 240: 58-65.
45. Janjanin S, Li WJ, Morgan MT, Shanti RM, Tuan RS. Mold-Shaped, nanofiber scaffold-based cartilage engineering using human mesenchymal stem cells and bioreactor. J Surg Res 2008; 149(1): 47-56.
46. Lee DK, Choi KB, Oh IS, et al. Continuous transforming growth factor beta1 secretion by cell-mediated gene therapy maintains chondrocyte redifferentiation. Tissue Eng 2005; 11: 310-8.
47. Guo CA, Liu XG, Huo JZ, Jiang C, Wen XJ, Chen ZR. Novel gene-modified-tissue engineering of cartilage using stable transforming growth factor-beta1-transfected mesenchymal stem cells grown on chitosan scaffolds. J Biosci Bioeng 2007; 103: 547-56.
48. Mierisch CM, Cohen SB, Jordan LC, Robertson PG, Balian G, Diduch DR. Transforming growth factor-beta in calcium alginate beads for the treatment of articular cartilage defects in the rabbit. Arthroscopy 2002; 18: 892-900.
49. Cui JH, Park SR, Park K, Choi BH, Min BH. Preconditioning of mesenchymal stem cells with low-intensity ultrasound for cartilage formation in vivo. Tissue Eng 2007; 13: 351-60.
50. Kayakabe M, Tsutsumi S, Watanabe H, Kato Y, Takagishi K. Transplantation of autologous rabbit BM-derived mesenchymal stromal cells embedded in hyaluronic acid gel sponge into osteochondral defects of the knee. Cytotherapy 2006; 8: 343-53.
51. Tatebe M, Nakamura R, Kagami H, Okada K, Ueda M. Differentiation of transplanted mesenchymal stem cells in a large osteochondral defect in rabbit. Cytotherapy 2005; 7: 520-30.
52. OsirisTherapeutics. Inc. Osiris therapeutics announces positive one year data from chondrogen trial for knee repair. Columbia, Maryland 2007.
53. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007; 213: 341-7.
54. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006; 98: 1076-84.
55. Zuk PA, Zhu M, Mizuno H, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7: 211-28.
56. Zuk PA, Zhu M, Ashjian P, et al. Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 2002; 13: 4279-95.
57. Erickson GR, Gimble JM, Franklin DM, Rice HE, Awad H, Guilak F. Chondrogenic potential of adipose tissue-derived stromal cells in vitro and in vivo. Biochem Biophys Res Commun 2002; 290: 763-9.
58. Gonda K, Shigeura T, Sato T, et al. Preserved proliferative capacity and multipotency of human adipose-derived stem cells after long-term cryopreservation. Plast Reconstr Surg 2008; 121: 401-10.
59. Huang JI, Zuk PA, Jones NF, et al. Chondrogenic potential of multipotential cells from human adipose tissue. Plast Reconstr Surg 2004; 113: 585-94.
60. Huang JI, Kazmi N, Durbhakula MM, Hering TM, Yoo JU, Johnstone B. Chondrogenic potential of progenitor cells derived from human bone marrow and adipose tissue: A patient-matched comparison. J Orthop Res 2005; 23: 1383-9.
61. Im GI, Shin YW, Lee KB. Do adipose tissue-derived mesenchymal stem cells have the same osteogenic and chondrogenic potential as bone marrow-derived cells? Osteoarthritis Cartilage 2005; 13: 845-53.
62. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source. Arthritis Rheum 2005; 52: 2521-9.
63. Chiou M, Xu Y, Longaker MT. Mitogenic and chondrogenic effects of fibroblast growth factor-2 in adipose-derived mesenchymal cells. Biochem Biophys Res Commun 2006; 343: 644-52.
64. Xu Y, Balooch G, Chiou M, Bekerman E, Ritchie RO, Longaker MT. Analysis of the material properties of early chondrogenic differentiated adipose-derived stromal cells (ASC) using an in vitro three-dimensional micromass culture system. Biochem Biophys Res Commun 2007; 359: 311-6.
65. Awad HA, Wickham MQ, Leddy HA, Gimble JM, Guilak F. Chondrogenic differentiation of adipose-derived adult stem cells in agarose, alginate, and gelatin scaffolds. Biomaterials 2004; 25: 3211-22.
66. Lin Y, Luo E, Chen X, et al. Molecular and cellular characterization during chondrogenic differentiation of adipose tissue-derived stromal cells in vitro and cartilage formation in vivo. J Cell Mol Med 2005; 9: 929-39.
67. Estes BT, Wu AW, Guilak F. Potent induction of chondrocytic differentiation of human adipose-derived adult stem cells by bone morphogenetic protein 6. Arthritis Rheum 2006; 54: 1222-32.
68. Jin X, Sun Y, Zhang K, et al. Ectopic neocartilage formation from predifferentiated human adipose derived stem cells induced by adenoviral-mediated transfer of hTGF beta2. Biomaterials 2007; 28: 2994-3003.
69. Jin XB, Sun YS, Zhang K, Wang J, Ju XD, Lou SQ. Neocartilage formation from predifferentiated human adipose derived stem cells in vivo. Acta Pharmacol Sin 2007; 28: 663-71.
70. Masuoka K, Asazuma T, Hattori H, et al. Tissue engineering of articular cartilage with autologous cultured adipose tissue-derived stromal cells using atelocollagen honeycomb-shaped scaffold with a membrane sealing in rabbits. J Biomed Mater Res B Appl Biomater 2006; 79: 25-34.
71. Betre H, Ong SR, Guilak F, Chilkoti A, Fermor B, Setton LA. Chondrocytic differentiation of human adipose-derived adult stem cells in elastin-like polypeptide. Biomaterials 2006; 27: 91-9.
72. Afizah H, Yang Z, Hui JH, Ouyang HW, Lee EH. A comparison between the chondrogenic potential of human bone marrow stem cells (BMSCs) and adipose-derived stem cells (ADSCs) taken from the same donors. Tissue Eng 2007; 13: 659-66.
73. Hennig T, Lorenz H, Thiel A, et al. Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profile and is overcome by BMP-6. J Cell Physiol 2007; 211: 682-91.
74. Ham AW. A histological study of the early phases of bone repair. J Bone Joint Surg 1930; 12: 827-44.
75. Nakata K, Nakahara H, Kimura T, et al. Collagen gene expression during chondrogenesis from chick periosteum-derived cells. FEBS Lett 1992; 299: 278-82.
76. Fukumoto T, Sperling JW, Sanyal A, et al.Combined effects of insulin-like growth factor-1 and transforming growth factor-beta1 on periosteal mesenchymal cells during chondrogenesis in vitro. Osteoarthritis Cartilage 2003; 11: 55-64.
77. Choi YS, Lim SM, Shin HC, Lee CW, Kim SL, Kim DI. Chondrogenesis of human periosteum-derived progenitor cells in atelocollagen. Biotechnol Lett 2007; 29: 323-9.
78. Park Y, Sugimoto M, Watrin A, Chiquet M, Hunziker EB. BMP-2 induces the expression of chondrocyte-specific genes in bovine synovium-derived progenitor cells cultured in three-dimensional alginate hydrogel. Osteoarthritis Cartilage 2005; 13: 527-36.
79. Yokoyama A, Sekiya I, Miyazaki K, Ichinose S, Hata Y, Muneta T. In vitro cartilage formation of composites of synovium-derived mesenchymal stem cells with collagen gel. Cell Tissue Res 2005; 322: 289-98.
80. Nawata M, Wakitani S, Nakaya H, et al. Use of bone morphogenetic protein 2 and diffusion chambers to engineer cartilage tissue for the repair of defects in articular cartilage. Arthritis Rheum 2005; 52: 155-63.
81. Adachi N, Sato K, Usas A, et al. Muscle derived, cell based ex vivo gene therapy for treatment of full thickness articular cartilage defects. J Rheumatol 2002; 29: 1920-30.
82. Yoshimura H, Muneta T, Nimura A, Yokoyama A, Koga H, Sekiya I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle. Cell Tissue Res 2007; 327: 449-62.
83. Koga H, Muneta T, Nagase T, et al. Comparison of mesenchymal tissues-derived stem cells for in vivo chondrogenesis: suitable conditions for cell therapy of cartilage defects in rabbit. Cell Tissue Res 2008.
84. Fehrer C, Lepperdinger G. Mesenchymal stem cell aging. Exp Gerontol 2005; 40: 926-30.
85. Stolzing A, Scutt A. Age-related impairment of mesenchymal progenitor cell function. Aging Cell 2006; 5: 213-24.
86. Hegert C, Kramer J, Hargus G, et al. Differentiation plasticity of chondrocytes derived from mouse embryonic stem cells. J Cell Sci 2002; 115: 4617-28.
87. Nakayama N, Duryea D, Manoukian R, Chow G, Han CY. Macroscopic cartilage formation with embryonic stem-cell-derived mesodermal progenitor cells. J Cell Sci 2003; 116: 2015-28.
88. Barberi T, Willis LM, Socci ND, Studer L. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2005; 2: e161.
89. Barberi T, Studer L. Mesenchymal cells. Methods Enzymol 2006; 418: 194-208.
90. Hopfl G, Gassmann M, Desbaillets I. Differentiating embryonic stem cells into embryoid bodies. Methods Mol Biol 2004; 254: 79-98.
91. Itskovitz-Eldor J, Schuldiner M, Karsenti D, et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med 2000; 6: 88-95.
92. Kramer J, Hegert C, Guan K, Wobus AM, Muller PK, Rohwedel J. Embryonic stem cell-derived chondrogenic differentiation in vitro: Activation by BMP-2 and BMP-4. Mech Dev 2000; 92: 193-205.
93. Hwang NS, Kim MS, Sampattavanich S, Baek JH, Zhang Z, Elisseeff J. Effects of three-dimensional culture and growth factors on the chondrogenic differentiation of murine embryonic stem cells. Stem Cells 2006; 24: 284-91.
94. Hwang NS, Varghese S, Zhang Z, Elisseeff J. Chondrogenic differentiation of human embryonic stem cell-derived cells in arginine-glycine-aspartate- modified hydrogels. Tissue Eng 2006; 12: 2695-706.
95. Kramer J, Hegert C, Hargus G, Rohwedel J. Mouse ES cell lines show a variable degree of chondrogenic differentiation in vitro. Cell Biol Int 2005; 29: 139-46.
96. Terraciano V, Hwang N, Moroni L, et al. Differential response of adult and embryonic mesenchymal progenitor cells to mechanical compression in hydrogels. Stem Cells 2007; 25: 2730-8.
97. Vats A, Bielby RC, Tolley N, et al. Chondrogenic differentiation of human embryonic stem cells: The effect of the micro-environment. Tissue Eng 2006; 12: 1687-97.
98. Takahashi K, Okita K, Nakagawa M, Yamanaka S. Induction of pluripotent stem cells from fibroblast cultures. Nat Protoc 2007; 2: 3081-9.
99. Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131: 861-72.
100. Yamanaka S. Strategies and new developments in the generation of patient-specific pluripotent stem cells. Cell Stem Cell 2007; 1: 39-49.
101. Germain L, Auger FA, Grandbois E, et al. Reconstructed human cornea produced in vitro by tissue engineering. Pathobiology 1999; 67: 140-7.
102. Griffith M, Osborne R, Munger R, et al. Functional human corneal equivalents constructed from cell lines. Science 1999; 286: 2169-72.
103. Kenyon KR, Tseng SC. Limbal autograft transplantation for ocular surface disorders. Ophthalmology 1989; 96: 709-22; discussion 722-3.
104. Lauweryns B, van den Oord JJ, De Vos R, Missotten L. A new epithelial cell type in the human cornea. Invest Ophthalmol Vis Sci 1993; 34: 1983-90.
105. Dua HS, Shanmuganathan VA, Powell-Richards AO, Tighe PJ, Joseph A. Limbal epithelial crypts: A novel anatomical structure and a putative limbal stem cell niche. Br J Ophthalmol 2005; 89: 529-32.
106. Budak MT, Alpdogan OS, Zhou M, Lavker RM, Akinci MA, Wolosin JM. Ocular surface epithelia contain ABCG2-dependent side population cells exhibiting features associated with stem cells. J Cell Sci 2005; 118: 1715-24.
107. Pellegrini G, Dellambra E, Golisano O, et al. p63 identifies keratinocyte stem cells. Proc Natl Acad Sci USA 2001; 98: 3156-61.
108. Schermer A, Galvin S, Sun TT. Differentiation-related expression of a major 64K corneal keratin in vivo and in culture suggests limbal location of corneal epithelial stem cells. J Cell Biol 1986; 103: 49-62.
109. Matic M, Petrov IN, Chen S, Wang C, Dimitrijevich SD, Wolosin JM. Stem cells of the corneal epithelium lack connexins and metabolite transfer capacity. Differentiation 1997; 61: 251-60.
110. Schofield R. The stem cell system. Biomed Pharmacother 1983; 37: 375-80.
111. Zumkeller W, Orth U, Gal A. Three novel PAX6 mutations in patients with aniridia. Mol Pathol 2003; 56: 180-3.
112. Puangsricharern V, Tseng SC. Cytologic evidence of corneal diseases with limbal stem cell deficiency. Ophthalmology 1995; 102: 1476-85.
113. Dua HS. The conjunctiva in corneal epithelial wound healing. Br J Ophthalmol 1998; 82: 1407-11.
114. Limb GA, Daniels JT, Cambrey AD, et al. Current prospects for adult stem cell-based therapies in ocular repair and regeneration. Curr Eye Res 2006; 31: 381-90.
115. Tseng SC, Hirst LW, Farazdaghi M, Green WR. Goblet cell density and vascularization during conjunctival transdifferentiation. Invest Ophthalmol Vis Sci 1984; 25: 1168-76.
116. Pellegrini G, Traverso CE, Franzi AT, Zingirian M, Cancedda R, De Luca M. Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet 1997; 349: 990-3.
117. Tsai RJ, Li LM, Chen JK. Reconstruction of damaged corneas by transplantation of autologous limbal epithelial cells. N Engl J Med 2000; 343: 86-93.
118. Schwab IR. Cultured corneal epithelia for ocular surface disease. Trans Am Ophthalmol Soc 1999; 97: 891-986.
119. Azuara-Blanco A, Pillai CT, Dua HS. Amniotic membrane transplantation for ocular surface reconstruction. Br J Ophthalmol 1999; 83: 399-402.
120. Gomes JA, Romano A, Santos MS, Dua HS. Amniotic membrane use in ophthalmology. Curr Opin Ophthalmol 2005; 16: 233-40.
121. Kim JC, Tseng SC. Transplantation of preserved human amniotic membrane for surface reconstruction in severely damaged rabbit corneas. Cornea 1995; 14: 473-84.
122. Grueterich M, Espana EM, Tseng SC. Ex vivo expansion of limbal epithelial stem cells: amniotic membrane serving as a stem cell niche. Surv Ophthalmol 2003; 48: 631-46.
123. Kanyshkova TG, Buneva VN, Nevinsky GA. Lactoferrin and its biological functions. Biochemistry (Mosc) 2001; 66: 1-7.
124. Keelan JA, Zhou RL, Mitchell MD. Activin A exerts both pro- and anti-inflammatory effects on human term gestational tissues. Placenta 2000; 21: 38-43.
125. Higa K, Shimmura S, Shimazaki J, Tsubota K. Hyaluronic acid-CD44 interaction mediates the adhesion of lymphocytes by amniotic membrane stroma. Cornea 2005; 24: 206-12.
126. Li H, Niederkorn JY, Neelam S, et al. Immunosuppressive factors secreted by human amniotic epithelial cells. Invest Ophthalmol Vis Sci 2005; 46: 900-7.
127. Grueterich M, Espana EM, Tseng SC. Modulation of keratin and connexin expression in limbal epithelium expanded on denuded amniotic membrane with and without a 3T3 fibroblast feeder layer. Invest Ophthalmol Vis Sci 2003; 44: 4230-6.
128. Li W, He H, Kuo CL, Gao Y, Kawakita T, Tseng SC. Basement membrane dissolution and reassembly by limbal corneal epithelial cells expanded on amniotic membrane. Invest Ophthalmol Vis Sci 2006; 47: 2381-9.
129. Koizumi N, Rigby H, Fullwood NJ, et al. Comparison of intact and denuded amniotic membrane as a substrate for cell-suspension culture of human limbal epithelial cells. Graefes Arch Clin Exp Ophthalmol 2007; 245: 123-34.
130. Kheirkhah A, Casas V, Raju VK, Tseng SC. Sutureless amniotic membrane transplantation for partial limbal stem cell deficiency. Am J Ophthalmol 2008; 145: 787-94.
131. Rama P, Bonini S, Lambiase A, et al. Autologous fibrin-cultured limbal stem cells permanently restore the corneal surface of patients with total limbal stem cell deficiency. Transplantation 2001; 72: 1478-85.
132. Higa K, Shimmura S, Kato N, et al. Proliferation and differentiation of transplantable rabbit epithelial sheets engineered with or without an amniotic membrane carrier. Invest Ophthalmol Vis Sci 2007; 48: 597-604.
133. Vinciguerra P, Albe E, Rosetta P, Di Iorio E, Pellegrini G. Custom phototherapeutic keratectomy and autologous fibrin-cultured limbal stem cell autografting: A combined approach. J Refract Surg 2008; 24: 323-4.
134. Ahmad S, Stewart R, Yung S, et al. Differentiation of human embryonic stem cells into corneal epithelial-like cells by in vitro replication of the corneal epithelial stem cell niche. Stem Cells 2007; 25: 1145-55.
135. McIntosh Ambrose W, Salahuddin A, So S, et al. Collagen vitrigel membranes for the in vitro reconstruction of separate corneal epithelial, stromal, and endothelial cell layers. J Biomed Mater Res B Appl Biomater 2009; 90(2): 818-31.
136. Nishida K, Yamato M, Hayashida Y, et al. Functional bioengineered corneal epithelial sheet grafts from corneal stem cells expanded ex vivo on a temperature-responsive cell culture surface. Transplantation 2004; 77: 379-85.
137. Hayashida Y, Nishida K, Yamato M, et al. Ocular surface reconstruction using autologous rabbit oral mucosal epithelial sheets fabricated ex vivo on a temperature-responsive culture surface. Invest Ophthalmol Vis Sci 2005; 46: 1632-9.
138. Nishida K, Yamato M, Hayashida Y, et al. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. N Engl J Med 2004; 351: 1187-96.
139. Sumide T, Nishida K, Yamato M, et al. Functional human corneal endothelial cell sheets harvested from temperature-responsive culture surfaces. FASEB J 2006; 20: 392-4.
140. Lai JY, Chen KH, Hsu WM, Hsiue GH, Lee YH. Bioengineered human corneal endothelium for transplantation. Arch Ophthalmol 2006; 124: 1441-8.
141. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 1975; 6: 331-43.
142. Barrandon Y, Green H. Cell size as a determinant of the clone-forming ability of human keratinocytes. Proc Natl Acad Sci USA 1985; 82: 5390-4.
143. Smola H, Thiekotter G, Fusenig NE. Mutual induction of growth factor gene expression by epidermal-dermal cell interaction. J Cell Biol 1993; 122: 417-29.
144. Fu B, Quintero J, Baker CC. Keratinocyte growth conditions modulate telomerase expression, senescence, and immortalization by human papillomavirus type 16 E6 and E7 oncogenes. Cancer Res 2003; 63: 7815-24.
145. Masson-Gadais B, Fugere C, Paquet C, et al. The feeder layer-mediated extended lifetime of cultured human skin keratinocytes is associated with altered levels of the transcription factors Sp1 and Sp3. J Cell Physiol 2006; 206: 831-42.
146. Miyashita H, Shimmura S, Higa K, et al. A Novel NIH/3T3 Duplex Feeder System to Engineer Corneal Epithelial Sheets with Enhanced Cytokeratin 15-Positive Progenitor Populations. Tissue Eng Part A 2008; 14(7): 1275-82.
147. Chen YT, Li W, Hayashida Y, et al. Human Amniotic Epithelial Cells as Novel Feeder Layers for Promoting Ex vivo Expansion of Limbal Epithelial Progenitor Cells. Stem Cells 2007; 25(8): 1995-2005. Epub 2007
148. Notara M, Haddow DB, MacNeil S, Daniels JT. A xenobiotic-free culture system for human limbal epithelial stem cells. Regener Med 2007; 2: 919-27.
149. Dravida S, Gaddipati S, Griffith M, et al. A biomimetic scaffold for culturing limbal stem cells: a promising alternative for clinical transplantation. J Tissue Eng Regener Med 2008; 2: 263-71.
150. Shortt AJ, Secker GA, Rajan MS, et al. Ex vivo Expansion and Transplantation of Limbal Epithelial Stem Cells. Ophthalmology 2008; 115(11): 1989-97. Epub 2008
151. Ye J, Lee SY, Kook KH, Yao K. Bone marrow-derived progenitor cells promote corneal wound healing following alkali injury. Graefes Arch Clin Exp Ophthalmol 2008; 246: 217-22.
152. Ye J, Yao K, Kim JC. Mesenchymal stem cell transplantation in a rabbit corneal alkali burn model: Engraftment and involvement in wound healing. Eye 2006; 20: 482-90.
153. Ma Y, Xu Y, Xiao Z, et al. Reconstruction of chemically burned rat corneal surface by bone marrow-derived human mesenchymal stem cells. Stem Cells 2006; 24: 315-21.
154. Homma R, Yoshikawa H, Takeno M, et al. Induction of epithelial progenitors in vitro from mouse embryonic stem cells and application for reconstruction of damaged cornea in mice. Invest Ophthalmol Vis Sci 2004; 45: 4320-6.
155. Carlson EC, Wang IJ, Liu CY, Brannan P, Kao CW, Kao WW. Altered KSPG expression by keratocytes following corneal injury. Mol Vis 2003; 9: 615-23.
156. Fini ME. Keratocyte and fibroblast phenotypes in the repairing cornea. Prog Retin Eye Res 1999; 18: 529-51.
157. Jester JV, Petroll WM, Cavanagh HD. Corneal stromal wound healing in refractive surgery: The role of myofibroblasts. Prog Retin Eye Res 1999; 18: 311-56.
158. Senoo T, Joyce NC. Cell cycle kinetics in corneal endothelium from old and young donors. Invest Ophthalmol Vis Sci 2000; 41: 660-7.
159. Zhu C, Joyce NC. Proliferative response of corneal endothelial cells from young and older donors. Invest Ophthalmol Vis Sci 2004; 45: 1743-51.
160. Engelmann K, Bohnke M, Friedl P. Isolation and long-term cultivation of human corneal endothelial cells. Invest Ophthalmol Vis Sci 1988; 29: 1656-62.
161. Miyata K, Drake J, Osakabe Y, et al. Effect of donor age on morphologic variation of cultured human corneal endothelial cells. Cornea 2001; 20: 59-63.
162. Melles GR, Lander F, van Dooren BT, Pels E, Beekhuis WH. Preliminary clinical results of posterior lamellar keratoplasty through a sclerocorneal pocket incision. Ophthalmology 2000; 107: 1850-56; discussion 1857.
163. Price FW, Jr., Price MO. Descemet's stripping with endothelial keratoplasty in 50 eyes: a refractive neutral corneal transplant. J Refract Surg 2005; 21: 339-45.
164. Terry MA, Ousley PJ. Deep lamellar endothelial keratoplasty in the first United States patients: early clinical results. Cornea 2001; 20: 239-43.
165. Doillon CJ, Watsky MA, Hakim M, et al. A collagen-based scaffold for a tissue engineered human cornea: physical and physiological properties. Int J Artif Organs 2003; 26: 764-73.
166. Duan X, McLaughlin C, Griffith M, Sheardown H. Biofunctionalization of collagen for improved biological response: scaffolds for corneal tissue engineering. Biomaterials 2007; 28: 78-88.
167. Li F, Carlsson D, Lohmann C, et al. Cellular and nerve regeneration within a biosynthetic extracellular matrix for corneal transplantation. Proc Natl Acad Sci USA 2003; 100: 15346-51.
168. Liu Y, Gan L, Carlsson DJ, et al. A simple, cross-linked collagen tissue substitute for corneal implantation. Invest Ophthalmol Vis Sci 2006; 47: 1869-75.
169. Liu Y, Griffith M, Watsky MA, et al. Properties of porcine and recombinant human collagen matrices for optically clear tissue engineering applications. Biomacromolecules 2006; 7: 1819-28.
170. Merrett K, Griffith CM, Deslandes Y, Pleizier G, Dube MA, Sheardown H. Interactions of corneal cells with transforming growth factor beta 2-modified poly dimethyl siloxane surfaces. J Biomed Mater Res A 2003; 67: 981-93.
171. Shimmura S, Doillon CJ, Griffith M, et al. Collagen-poly(N- isopropylacrylamide)-based membranes for corneal stroma scaffolds. Cornea 2003; 22: S81-88.
172. Suuronen EJ, McLaughlin CR, Stys PK, Nakamura M, Munger R, Griffith M. Functional innervation in tissue engineered models for in vitro study and testing purposes. Toxicol Sci 2004; 82: 525-33.
173. Suuronen EJ, Nakamura M, Watsky MA, et al. Innervated human corneal equivalents as in vitro models for nerve-target cell interactions. FASEB J 2004; 18: 170-2.
174. Garagorri N, Fermanian S, Thibault R, et al. Keratocyte behavior in three-dimensional photopolymerizable poly(ethylene glycol) hydrogels. Acta Biomater 2008; 4: 1139-47.
175. Koizumi N, Sakamoto Y, Okumura N, et al. Cultivated corneal endothelial transplantation in a primate: possible future clinical application in corneal endothelial regenerative medicine. Cornea 2008; 27 (Suppl 1): S48-55.
176. Koizumi N, Sakamoto Y, Okumura N, et al. Cultivated corneal endothelial cell sheet transplantation in a primate model. Invest Ophthalmol Vis Sci 2007; 48: 4519-26.
177. Mimura T, Amano S, Yokoo S, Uchida S, Usui T, Yamagami S. Isolation and distribution of rabbit keratocyte precursors. Mol Vis 2008; 14: 197-203.
178. Mimura T, Yamagami S, Usui T, Seiichi, Honda N, Amano S. Necessary prone position time for human corneal endothelial pre-cursor transplantation in a rabbit endothelial deficiency model. Curr Eye Res 2007; 32: 617-23.
179. Mimura T, Yamagami S, Yokoo S, et al. Cultured human corneal endothelial cell transplantation with a collagen sheet in a rabbit model. Invest Ophthalmol Vis Sci 2004; 45: 2992-7.
180. Ishino Y, Sano Y, Nakamura T, et al. Amniotic membrane as a carrier for cultivated human corneal endothelial cell transplantation. Invest Ophthalmol Vis Sci 2004; 45: 800-6.
181. Whikehart DR, Parikh CH, Vaughn AV, Mishler K, Edelhauser HF. Evidence suggesting the existence of stem cells for the human corneal endothelium. Mol Vis 2005; 11: 816-24.
182. McGowan SL, Edelhauser HF, Pfister RR, Whikehart DR. Stem cell markers in the human posterior limbus and corneal endothelium of unwounded and wounded corneas. Mol Vis 2007; 13: 1984-2000.
183. Toma JG, Akhavan M, Fernandes KJ, et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 2001; 3: 778-84.
184. Mimura T, Yokoo S, Araie M, Amano S, Yamagami S. Treatment of rabbit bullous keratopathy with precursors derived from cultured human corneal endothelium. Invest Ophthalmol Vis Sci 2005; 46: 3637-44.
185. Yokoo S, Yamagami S, Yanagi Y, et al. Human corneal endothelial cell precursors isolated by sphere-forming assay. Invest Ophthalmol Vis Sci 2005; 46: 1626-31.
186. Mimura T, Yamagami S, Yokoo S, et al. Sphere therapy for corneal endothelium deficiency in a rabbit model. Invest Ophthalmol Vis Sci 2005; 46: 3128-35.
187. Mimura T, Yamagami S, Yokoo S, Araie M, Amano S. Comparison of rabbit corneal endothelial cell precursors in the central and peripheral cornea. Invest Ophthalmol Vis Sci 2005; 46: 3645-8.
188. Yamagami S, Mimura T, Yokoo S, Takato T, Amano S. Isolation of human corneal endothelial cell precursors and construction of cell sheets by precursors. Cornea 2006; 25: S90-92.
189. Du Y, Funderburgh ML, Mann MM, SundarRaj N, Funderburgh JL. Multipotent stem cells in human corneal stroma. Stem Cells 2005; 23: 1266-75.
190. Amano S, Yamagami S, Mimura T, Uchida S, Yokoo S. Corneal stromal and endothelial cell precursors. Cornea 2006; 25: S73-77.
191. Yamagami S, Yokoo S, Mimura T, Takato T, Araie M, Amano S. Distribution of precursors in human corneal stromal cells and endothelial cells. Ophthalmology 2007; 114: 433-9.
192. Thill M, Schlagner K, Altenahr S, et al. A novel population of repair cells identified in the stroma of the human cornea. Stem Cells Dev 2007; 16: 733-45.
193. Polisetty N, Fatima A, Madhira SL, Sangwan VS, Vemuganti GK. Mesenchymal cells from limbal stroma of human eye. Mol Vis 2008; 14: 431-42.
194. Choong PF, Mok PL, Cheong SK, Then KY. Mesenchymal stromal cell-like characteristics of corneal keratocytes. Cytotherapy 2007; 9: 252-8.
195. Arnalich-Montiel F, Pastor S, Blazquez-Martinez A, et al. Adipose-derived stem cells are a source for cell therapy of the corneal stroma. Stem Cells 2008; 26: 570-9.