Collagen vitrigel membranes for the in vitro reconstruction of separate corneal epithelial, stromal, and endothelial cell layers

Journal of Biomedical Materials Research - Part B Applied Biomaterials

Volumn 90 B, Issue 2, 2009, Pages 818-831

  Ambrose, Winnette McIntosh ^a   Salahuddin, Afrah ^a   So, Stephen ^a   Ng, Shengyong ^a   Márquez, Sara Ponce ^b   Takezawa, Toshiaki ^c   Schein, Oliver ^d   Elisseeff, Jennifer ^a  

^a Johns Hopkins University School of Medicine   (United States)

^b TECNALIA RESEARCH AND INNOVATION   (Spain)

^c NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Collagen; Cornea; Keratocytes; Limbus; Vitrigel

Indexed keywords

BIOASSAY; BIOMECHANICS; BLOOD VESSEL PROSTHESES; CELL CULTURE; CELL MEMBRANES; CHLORINE COMPOUNDS; COLLAGEN; ELECTRIC POTENTIAL; HYDRATES; MECHANICAL PROPERTIES; MONOLAYERS; REPAIR; SELF ASSEMBLY; SODIUM; SUBSTRATES; TENSILE STRENGTH; TENSILE TESTING; TISSUE; TISSUE CULTURE;

ADHESIVE STRUCTURE; BASAL LAMINA; CELL SHEET; CELLULAR LAYERS; CHLORIDE CHANNELS; COLLAGEN VITRIGEL; CORNEA; CRYSTALLIN; DENSE MONOLAYERS; EPITHELIAL SHEETS; IN-VITRO; INTERCELLULAR JUNCTION; KERATOCYTES; LIMBUS; PROTEOGLYCAN; SODIUM BICARBONATES; STEM CELL; SULPHATE; TISSUE CULTURE PLASTICS; TYPE I COLLAGEN; ULTIMATE TENSILE STRENGTH; UNIFORM CELLS; UP-REGULATION; VITRIGEL; VOLTAGE-DEPENDENT ANION CHANNELS;

ENDOTHELIAL CELLS;

CHLORIDE CHANNEL; COLLAGEN TYPE 1; KERATOCAN; PLASTIC; PROTEIN P63; VOLTAGE DEPENDENT ANION CHANNEL 2; VOLTAGE DEPENDENT ANION CHANNEL 3;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; CELL CULTURE; CELL SIZE; CELL STRUCTURE; COLLAGEN VITRIGEL; CONTROLLED STUDY; CORNEA CELL; CORNEA EPITHELIUM; DESCEMET MEMBRANE; DESMOSOME; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; EXPLANT; GEL; HEMIDESMOSOME; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDRATION; IN VITRO STUDY; MICROSCOPY; NONHUMAN; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERUM; STELLATE CELL; STROMA CELL; TENSILE STRENGTH; TIGHT JUNCTION; TISSUE CULTURE; UPREGULATION;

EID: 67749149026     PISSN: 15524973     EISSN: 15524981     Source Type: Journal    
DOI: 10.1002/jbm.b.31351     Document Type: Article

References (73)

1. Whitcher JP, Srinivasan M, Upadhyay MP. Corneal blindness: A global perspective. Bull World Health Organ 2001;79:214-221.
2. Moffatt SL, Cartwright VA, Stumpf TH. Centennial review of corneal transplantation. Clin Exp Ophthalmol 2005;33:642-657.
3. Darlington JK, Adrean SD, Schwab IR. Trends of penetrating keratoplasty in the United States from 1980 to 2004. Ophthalmology 2006;113:2171-2175.
4. Aquavella JV, Qian Y, McCormick GJ, Palakuru JR. Keratoprosthesis: Current techniques. Cornea 2006;25:656-662.
5. Chirila TV. An overview of the development of artificial corneas with porous skirts and the use of PHEMA for such an application. Biomaterials 2001;22:3311-3317.
6. Hille K. Keratoprostheses. Clinical aspects. Ophthalmologe 2002;99:523-531.
7. Ilhan-Sarac O, Akpek EK. Current concepts and techniques in keratoprosthesis. Curr Opin Ophthalmol 2005;16:246-250.
8. Khan B, Dudenhoefer EJ, Dohlman CH. Keratoprosthesis: An update. Curr Opin Ophthalmol 2001;12:282-287.
9. Yaghouti F, Nouri M, Abad JC, Power WJ, Doane MG, Dohlman CH. Keratoprosthesis: Preoperative prognostic categories. Cornea 2001;20:19-23.
10. Griffith M, Osborne R, Munger R, Xiong X, Doillon CJ, Laycock NL, Hakim M, Song Y, Watsky MA. Functional human corneal equivalents constructed from cell lines. Science 1999; 286:2169-2172. (Pubitemid 129516294)
11. Zieske JD, Mason VS, Wasson ME, Meunier SF, Nolte CJ, Fukai N, Olsen BR, Parenteau NL. Basement membrane assembly and differentiation of cultured corneal cells: Importance of culture environment and endothelial cell interaction. Exp Cell Res 1994;214:621-633. (Pubitemid 24310821)
12. Alaminos M, Del Carmen Sanchez-Quevedo M, Munoz- Avila JI, Serrano D, Medialdea S, Carreras I, Campos A. Construction of a complete rabbit cornea substitute using a fibrin-agarose scaffold. Invest Ophthalmol Vis Sci 2006;47: 3311-3317. (Pubitemid 351639691)
13. 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;57:201-209. (Pubitemid 19112360)
14. 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;34:1983-1990. (Pubitemid 23148634)
15. 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: 2672-2679.
16. 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.
17. Schwab IR. Cultured corneal epithelia for ocular surface disease. Trans Am Ophthalmol Soc 1999;97:891-986. (Pubitemid 30106658)
18. Azuara-Blanco A, Pillai CT, Dua HS. Amniotic membrane transplantation for ocular surface reconstruction. Br J Ophthalmol 1999;83:399-402. (Pubitemid 29161178)
19. Gomes JA, Romano A, Santos MS, Dua HS. Amniotic membrane use in ophthalmology. Curr Opin Ophthalmol 2005;16: 233-240.
20. Kim JC, Tseng SC. Transplantation of preserved human amniotic membrane for surface reconstruction in severely damaged rabbit corneas. Cornea 1995;14:473-484.
21. 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;48:631-646. (Pubitemid 37386280)
22. Kanyshkova TG, Buneva VN, Nevinsky GA. Lactoferrin and its biological functions. Biochemistry (Mosc) 2001;66: 1-7.
23. 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.
24. Higa K, Shimmura S, Shimazaki J, Tsubota K. Hyaluronic acid-CD44 interaction mediates the adhesion of lymphocytes by amniotic membrane stroma. Cornea 2005;24:206-212. (Pubitemid 40283833)
25. Li H, Niederkorn JY, Neelam S, Mayhew E, Word RA, McCulley JP, Alizadeh H. Immunosuppressive factors secreted by human amniotic epithelial cells. Invest Ophthalmol Vis Sci 2005;46:900-907. (Pubitemid 41321026)
26. 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;44:4230-4236. (Pubitemid 37186256)
27. 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;47:2381-2389. (Pubitemid 351639818)
28. Koizumi N, Rigby H, Fullwood NJ, Kawasaki S, Tanioka H, Koizumi K, Kociok N, Joussen AM, Kinoshita S. 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;245:123-134. (Pubitemid 46766738)
29. Rama P, Bonini S, Lambiase A, Golisano O, Paterna P, De Luca M, Pellegrini G. Autologous fibrin-cultured limbal stem cells permanently restore the corneal surface of patients with total limbal stem cell deficiency. Transplantation 2001;72: 1478-1485. (Pubitemid 33095504)
30. Higa K, Shimmura S, Kato N, Kawakita T, Miyashita H, Itabashi Y, Fukuda K, Shimazaki J, Tsubota K. Proliferation and differentiation of transplantable rabbit epithelial sheets engineered with or without an amniotic membrane carrier. Invest Ophthalmol Vis Sci 2007;48:597-604. (Pubitemid 351260690)
31. Vinciguerra P, Albe E, Rosetta P, Di Iorio E, Pellegrini G. Custom phototherapeutic keratectomy and autologous fibrincultured limbal stem cell autografting: A combined approach. J Refract Surg 2008;24:323-324. (Pubitemid 351543996)
32. Inatomi T, Nakamura T, Koizumi N, Sotozono C, Kinoshita S. Current concepts and challenges in ocular surface reconstruction using cultivated mucosal epithelial transplantation. Cornea 2005;24(8 Suppl):S32-S38. (Pubitemid 41688553)
33. Nishida K, Yamato M, Hayashida Y, Watanabe K, Yamamoto K, Adachi E, Nagai S, Kikuchi A, Maeda N, Watanabe H, Okano T, Tano Y. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. N Engl J Med 2004;351:1187-1196. (Pubitemid 39296306)
34. Kheirkhah A, Casas V, Raju VK, Tseng SC. Sutureless amniotic membrane transplantation for partial limbal stem cell deficiency. Am J Ophthalmol 2008;145:787-794.
35. Takezawa T, Ozaki K, Nitani A, Takabayashi C, Shimo-Oka T. Collagen vitrigel: A novel scaffold that can facilitate a three-dimensional culture for reconstructing organoids. Cell Transplant 2004;13:463-473. (Pubitemid 39163091)
36. Takushi E, Asato L, Nakada T. Edible eyeballs from fish. Nature 1990;345:298-299.
37. Wang PC, Takezawa T. Reconstruction of renal glomerular tissue using collagen vitrigel scaffold. J Biosci Bioeng 2005; 99:529-540.
38. Takezawa T, Nitani A, Shimo-Oka T, Takayama Y. A protein- permeable scaffold of a collagen vitrigel membrane useful for reconstructing crosstalk models between two different cell types. Cells Tissues Organs 2007;185:237-241. (Pubitemid 46956864)
39. Takezawa T, Ozaki K, Takabayashi C. Reconstruction of a hard connective tissue utilizing a pressed silk sheet and type-I collagen as the scaffold for fibroblasts. Tissue Eng 2007;13: 1357-1366. (Pubitemid 46986735)
40. Takezawa T, Takeuchi T, Nitani A, Takayama Y, Kino-Oka M, Taya M, Enosawa S. Collagen vitrigel membrane useful for paracrine assays in vitro and drug delivery systems in vivo. J Biotechnol 2007;131:76-83. (Pubitemid 47042936)
41. Koizumi N, Sakamoto Y, Okumura N, Okahara N, Tsuchiya H, Torii R, Cooper LJ, Ban Y, Tanioka H, Kinoshita S. Cultivated corneal endothelial cell sheet transplantation in a primate model. Invest Ophthalmol Vis Sci 2007;48:4519-4526. (Pubitemid 351260967)
42. Koizumi N, Sakamoto Y, Okumura N, Tsuchiya H, Torii R, Cooper LJ, Ban Y, Tanioka H, Kinoshita S. Cultivated corneal endothelial transplantation in a primate: Possible future clinical application in corneal endothelial regenerative medicine. Cornea 2008;27 (Suppl 1):S48-S55.
43. Tseng SC, Prabhasawat P, Barton K, Gray T, Meller D. Amniotic membrane transplantation with or without limbal allografts for corneal surface reconstruction in patients with limbal stem cell deficiency. Arch Ophthalmol 1998;116:431-441. (Pubitemid 28169742)
44. Dua HS, Gomes JA, King AJ, Maharajan VS. The amniotic membrane in ophthalmology. Surv Ophthalmol 2004;49:51-77.
45. Garagorri N, Fermanian S, Thibault R, Ambrose WM, Schein OD, Chakravarti S, Elisseeff J. Keratocyte behavior in threedimensional photopolymerizable poly(ethylene glycol) hydrogels. Acta Biomater 2008;4:1139-1147.
46. Beales MP, Funderburgh JL, Jester JV, Hassell JR. Proteoglycan synthesis by bovine keratocytes and corneal fibroblasts: Maintenance of the keratocyte phenotype in culture. Invest Ophthalmol Vis Sci 1999;40:1658-1663.
47. Chen KH, Azar D, Joyce NC. Transplantation of adult human corneal endothelium ex vivo: A morphologic study. Cornea 2001;20:731-737. (Pubitemid 34506472)
48. Zhu C, Joyce NC. Proliferative response of corneal endothelial cells from young and older donors. Invest Ophthalmol Vis Sci 2004;45:1743-1751. (Pubitemid 38868967)
49. Joyce NC, Zhu CC. Human corneal endothelial cell proliferation: Potential for use in regenerative medicine. Cornea 2004;23(8 Suppl):S8-S19.
50. Long CJ, Roth MR, Tasheva ES, Funderburgh M, Smit R, Conrad GW, Funderburgh JL. Fibroblast growth factor-2 promotes keratan sulfate proteoglycan expression by keratocytes in vitro. J Biol Chem 2000;275:13918-13923. (Pubitemid 30257468)
51. McCaffery JM, Farquhar MG. Localization of GTPases by indirect immunofluorescence and immunoelectron microscopy. Methods Enzymol 1995;257:259-279.
52. Doughty MJ, Seabert W, Bergmanson JP, Blocker Y. A descriptive and quantitative study of the keratocytes of the corneal stroma of albino rabbits using transmission electron microscopy. Tissue Cell 2001;33:408-422. (Pubitemid 32755115)
53. Szaflik JP. Comparison of in vivo confocal microscopy of human cornea by white light scanning slit and laser scanning systems. Cornea 2007;26:438-445. (Pubitemid 46684385)
54. Shanmuganathan VA, Foster T, Kulkarni BB, Hopkinson A, Gray T, Powe DG, Lowe J, Dua HS. Morphological characteristics of the limbal epithelial crypt. Br J Ophthalmol 2007;91:514-519. (Pubitemid 46623688)
55. Nishida K, Yamato M, Hayashida Y, Watanabe K, Maeda N, Watanabe H, Yamamoto K, Nagai S, Kikuchi A, Tano Y, Okano T. Functional bioengineered corneal epithelial sheet grafts from corneal stem cells expanded ex vivo on a temperature- responsive cell culture surface. Transplantation 2004;77: 379-385. (Pubitemid 38209736)
56. Harkin DG, Barnard Z, Gillies P, Ainscough SL, Apel AJ. Analysis of p63 and cytokeratin expression in a cultivated limbal autograft used in the treatment of limbal stem cell defi- ciency. Br J Ophthalmol 2004;88:1154-1158. (Pubitemid 39144408)
57. Wang DY, Hsueh YJ, Yang VC, Chen JK. Propagation and phenotypic preservation of rabbit limbal epithelial cells on amniotic membrane. Invest Ophthalmol Vis Sci 2003;44: 4698-4704. (Pubitemid 37315281)
58. Kao WW, Liu CY. Roles of lumican and keratocan on corneal transparency. Glycoconj J 2002;19:275-285.
59. Abedinia M, Pain T, Algar EM, Holmes RS. Bovine corneal aldehyde dehydrogenase: The major soluble corneal protein with a possible dual protective role for the eye. Exp Eye Res 1990;51:419-426. (Pubitemid 20315319)
60. Espana EM, He H, Kawakita T, Di Pascuale MA, Raju VK, Liu CY, Tseng SC. Human keratocytes cultured on amniotic membrane stroma preserve morphology and express keratocan. Invest Ophthalmol Vis Sci 2003;44: 5136-5141. (Pubitemid 37475381)
61. Funderburgh JL, Funderburgh ML, Mann MM, Corpuz L, Roth MR. Proteoglycan expression during transforming growth factor beta-induced keratocyte- myofibroblast transdifferentiation. J Biol Chem 2001;276:44173-44178. (Pubitemid 37383990)
62. Funderburgh JL, Hevelone ND, Roth MR, Funderburgh ML, Rodrigues MR, Nirankari VS, Conrad GW. Decorin and biglycan of normal and pathologic human corneas. Invest Ophthalmol Vis Sci 1998;39:1957-1964.
63. Ishino Y, Sano Y, Nakamura T, Connon CJ, Rigby H, Fullwood NJ, Kinoshita S. Amniotic membrane as a carrier for cultivated human corneal endothelial cell transplantation. Invest Ophthalmol Vis Sci 2004;45:800-806. (Pubitemid 38868373)
64. Sumide T, Nishida K, Yamato M, Ide T, Hayashida Y, Watanabe K, Yang J, Kohno C, Kikuchi A, Maeda N, Wantanabe H, Okano T, et al. Functional human corneal endothelial cell sheets harvested from temperature-responsive culture surfaces. Faseb J 2006;20:392-394. (Pubitemid 46671182)
65. Ihanamaki T, Pelliniemi LJ, Vuorio E. Collagens and collagen- related matrix components in the human and mouse eye. Prog Retin Eye Res 2004;23:403-434. (Pubitemid 38829450)
66. Griffith M, Hakim M, Shimmura S, Watsky MA, Li F, Carlsson D, Doillon CJ, Nakamura M, Suuronen E, Shinozaki N, Nakata K, Sheardown H. Artificial human corneas: Scaffolds for transplantation and host regeneration. Cornea 2002;21(7 Suppl):S54-S61.
67. Doillon CJ, Watsky MA, Hakim M, Wang J, Munger R, Laycock N, Osborne R, Griffith M. A collagen-based scaffold for a tissue engineered human cornea: Physical and physiological properties. Int J Artif Organs 2003;26:764-773. (Pubitemid 37236036)
68. Li F, Carlsson D, Lohmann C, Suuronen E, Vascotto S, Kobuch K, Sheardown H, Munger R, Nakamura M, Griffith M. Cellular and nerve regeneration within a biosynthetic extracellular matrix for corneal transplantation. Proc Natl Acad Sci USA 2003;100:15346-15351. (Pubitemid 38020992)
69. Shimmura S, Doillon CJ, Griffith M, Nakamura M, Gagnon E, Usui A, Shinozaki N, Tsubota K. Collagen-poly(N-isopropylacrylamide)- based membranes for corneal stroma scaffolds. Cornea 2003;22(7 Suppl):S81-S88. (Pubitemid 37169609)
70. Li F, Griffith M, Li Z, Tanodekaew S, Sheardown H, Hakim M, Carlsson DJ. Recruitment of multiple cell lines by collagen- synthetic copolymer matrices in corneal regeneration. Biomaterials 2005;26:3093-3104. (Pubitemid 39647244)
71. Liu Y, Gan L, Carlsson DJ, Fagerholm P, Lagali N, Watsky MA, Munger R, Hodge WG, Priest D, Griffith M. A simple, cross-linked collagen tissue substitute for corneal implantation. Invest Ophthalmol Vis Sci 2006;47:1869-1875. (Pubitemid 46768266)
72. 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. (Pubitemid 44427909)
73. Kim JS, Kim JC, Na BK, Jeong JM, Song CY. Amniotic membrane patching promotes healing and inhibits proteinase activity on wound healing following acute corneal alkali burn. Exp Eye Res 2000;70:329-337