Enhancement of retinal pigment epithelial culture characteristics and subretinal space tolerance of scaffolds with 200 nm fiber topography

Biomaterials

Volumn 35, Issue 9, 2014, Pages 2837-2850

  Liu, Zengping ^a   Yu, Na ^b   Holz, Frank G ^a   Yang, Fang ^b   Stanzel, Boris V ^a  

^a UNIVERSITY OF BONN   (Germany)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Biocompatibility; Cell culture; Epithelium cell; Retina; Scaffold; Surface topography

Indexed keywords

BIOCOMPATIBILITY; CELL CULTURE; EPITHELIUM CELL; RETINA; SCAFFOLD; SURFACE TOPOGRAPHY;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELL ADHESION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; CELLS, CULTURED; EPITHELIAL CELLS; HUMANS; MATERIALS TESTING; NANOFIBERS; POLYESTERS; POLYETHYLENE TEREPHTHALATES; PROSTHESIS IMPLANTATION; RABBITS; RETINAL PIGMENT EPITHELIUM; TISSUE SCAFFOLDS;

EID: 84895001072     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.12.069     Document Type: Article

References (71)

1. Binder S., Stanzel B.V., Krebs I., Glittenberg C. Transplantation of the RPE in AMD. Prog Retin Eye Res 2007, 26:516-554.
2. da Cruz L., Chen F.K., Ahmado A., Greenwood J., Coffey P. RPE transplantation and its role in retinal disease. Prog Retin Eye Res 2007, 26:598-635.
3. Lim L.S., Mitchell P., Seddon J.M., Holz F.G., Wong T.Y. Age-related macular degeneration. Lancet 2012, 379:1728-1738.
4. Herrmann P., Holz F.G., Charbel Issa P. Etiology and pathogenesis of age-related macular degeneration. Ophthalmologe 2013, 110:377-387.
5. Singer M.A., Awh C.C., Sadda S., Freeman W.R., Antoszyk A.N., Wong P., et al. Horizon: an open-label extension trial of ranibizumab for choroidal neovascularization secondary to age-related macular degeneration. Ophthalmology 2012, 119:1175-1183.
6. Schwartz S.D., Hubschman J.P., Heilwell G., Franco-Cardenas V., Pan C.K., Ostrick R.M., et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 2012, 379:713-720.
7. Sugino I.K., Sun Q., Wang J., Nunes C.F., Cheewatrakoolpong N., Rapista A., et al. Comparison of FRPE and human embryonic stem cell-derived RPE behavior on aged human Bruch's membrane. Invest Ophthalmol Vis Sci 2011, 52:4979-4997.
8. Diniz B., Thomas P., Thomas B., Ribeiro R., Hu Y., Brant R., et al. Subretinal implantation of retinal pigment epithelial cells derived from human embryonic stem cells: improved survival when implanted as a monolayer. Invest Ophthalmol Vis Sci 2013, 54:5087-5096.
9. Lu L., Yaszemski M.J., Mikos A.G. Retinal pigment epithelium engineering using synthetic biodegradable polymers. Biomaterials 2001, 22:3345-3355.
10. Hynes S.R., Lavik E.B. Atissue-engineered approach towards retinal repair: scaffolds for cell transplantation to the subretinal space. Graefes Arch Clin Exp Ophthalmol 2010, 248:763-778.
11. Treharne A.J., Grossel M.C., Lotery A.J., Thomson H.A. The chemistry of retinal transplantation: the influence of polymer scaffold properties on retinal cell adhesion and control. Br J Ophthalmol 2011, 95:768-773.
12. McHugh K.J., Saint-Geniez M., Tao S.L. Topographical control of ocular cell types for tissue engineering. JBiomed Mater Res B Appl Biomater 2013, Available from URL:. http://www.ncbi.nlm.nih.gov/pubmed/23744715, 10.1002/jbm.b.32968.
13. Treharne A.J., Thomson H.A., Grossel M.C., Lotery A.J. Developing methacrylate-based copolymers as an artificial Bruch's membrane substitute. JBiomed Mater Res A 2012, 100:2358-2364.
14. Kearns V., Mistry A., Mason S., Krishna Y., Sheridan C., Short R., et al. Plasma polymer coatings to aid retinal pigment epithelial growth for transplantation in the treatment of age related macular degeneration. JMater Sci Mater Med 2012, 23:2013-2021.
15. Lim J.Y., Donahue H.J. Cell sensing and response to micro- and nanostructured surfaces produced by chemical and topographic patterning. Tissue Eng 2007, 13:1879-1891.
16. Stanzel B.V., Englander M., Strick D.J., Sanislo S.S., Huie P., Blumenkranz M.S., et al. Perspektive: tissue engineering bei RPE-transplantation in AMD. Spektrum der Augenheilkunde 2007, 21:212-217.
17. Thieltges F., Stanzel B.V., Liu Z., Holz F.G. Ananofibrillar surface promotes superior growth characteristics in cultured human retinal pigment epithelium. Ophthalmic Res 2011, 46:133-140.
18. Li Y., Tang L. Comparison of growth of human fetal RPE cells on electrospun nanofibers and etched pore polyester membranes. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2012, 37:433-440.
19. Warnke P.H., Alamein M., Skabo S., Stephens S., Bourke R., Heiner P., et al. Primordium of an artificial Bruch's membrane made of nanofibers for engineering of retinal pigment epithelium cell monolayers. Acta Biomater 2013, 9:9411-9422.
20. Pham Q.P., Sharma U., Mikos A.G. Electrospinning of polymeric nanofibers for tissue engineering applications: a review. Tissue Eng 2006, 12:1197-1211.
21. Kumbar S.G., Nair L.S., Bhattacharyya S., Laurencin C.T. Polymeric nanofibers as novel carriers for the delivery of therapeutic molecules. JNanosci Nanotechnol 2006, 6:2591-2607.
22. Christopherson G.T., Song H., Mao H.Q. The influence of fiber diameter of electrospun substrates on neural stem cell differentiation and proliferation. Biomaterials 2009, 30:556-564.
23. Yang F., Murugan R., Wang S., Ramakrishna S. Electrospinning of nano/micro scale poly(l-lactic acid) aligned fibers and their potential in neural tissue engineering. Biomaterials 2005, 26:2603-2610.
24. Chen M., Patra P.K., Warner S.B., Bhowmick S. Role of fiber diameter in adhesion and proliferation of NIH 3T3 fibroblast on electrospun polycaprolactone scaffolds. Tissue Eng 2007, 13:579-587.
25. Ediriwickrema L.S., Peng S., Kristofik N., van Zyl T.A., Gan G., Li L., et al. Reconstructing an outer retina using electrospun polycaprolactone (PCL) and human embryonic stem cell-derived retinal progenitor cells. Invest Ophthalmol Vis Sci 2012, 53. E-Abstract 337. Available from URL:. http://abstracts.iovs.org//cgi/content/abstract/53/6/337.
26. Regatieri C.V., Baranov P., Carvalho A., Ko C., Tao S., Young M.J. Pre differentiated human retinal progenitor cells integrate and express mature markers on the host retina. Invest Ophthalmol Vis Sci 2012, 53. E-Abstract 1128. Available from URL:. http://abstracts.iovs.org//cgi/content/abstract/53/6/1128.
27. Williams D.F. On the mechanisms of biocompatibility. Biomaterials 2008, 29:2941-2953.
28. Schwahn H.N., Gekeler F., Kohler K., Kobuch K., Sachs H.G., Schulmeyer F., et al. Studies on the feasibility of a subretinal visual prosthesis: data from Yucatan micropig and rabbit. Graefes Arch Clin Exp Ophthalmol 2001, 239:961-967.
29. Zrenner E., Bartz-Schmidt K.U., Benav H., Besch D., Bruckmann A., Gabel V.P., et al. Subretinal electronic chips allow blind patients to read letters and combine them to words. Proc Biol Sci 2011, 278:1489-1497.
30. Montezuma S.R., Loewenstein J., Scholz C., Rizzo J.F. Biocompatibility of materials implanted into the subretinal space of Yucatan pigs. Invest Ophthalmol Vis Sci 2006, 47:3514-3522.
31. Kiilgaard J.F., Wiencke A.K., Scherfig E., Prause J.U., la Cour M. Transplantation of allogenic anterior lens capsule to the subretinal space in pigs. Acta Ophthalmol Scand 2002, 80:76-81.
32. Stanzel B.V., Liu Z., Brinken R., Braun N., Holz F.G., Eter N. Subretinal delivery of ultrathin rigid-elastic cell carriers using a metallic shooter instrument and biodegradable hydrogel encapsulation. Invest Ophthalmol Vis Sci 2012, 53:490-500.
33. Shang S., Yang F., Cheng X., Walboomers X.F., Jansen J.A. The effect of electrospun fibre alignment on the behaviour of rat periodontal ligament cells. Eur Cells Mater 2010, 19:180-192.
34. Ma Z., Kotaki M., Yong T., He W., Ramakrishna S. Surface engineering of electrospun polyethylene terephthalate (PET) nanofibers towards development of a new material for blood vessel engineering. Biomaterials 2005, 26:2527-2536.
35. Hu J., Bok D. Acell culture medium that supports the differentiation of human retinal pigment epithelium into functionally polarized monolayers. Mol Vis 2001, 7:14-19.
36. Yang F., Both S.K., Yang X., Walboomers X.F., Jansen J.A. Development of an electrospun nano-apatite/PCL composite membrane for GTR/GBR application. Acta Biomater 2009, 5:3295-3304.
37. Drexler W., Fujimoto J.G. State-of-the-art retinal optical coherence tomography. Prog Retin Eye Res 2008, 27:45-88.
38. Tezcaner A., Bugra K., Hasirci V. Retinal pigment epithelium cell culture on surface modified poly(hydroxybutyrate-co-hydroxyvalerate) thin films. Biomaterials 2003, 24:4573-4583.
39. Lim J.-M., Byun S., Chung S., Park T.H., Seo J.-M., Joo C.-K., et al. Retinal pigment epithelial cell behavior is modulated by alterations in focal cell-substrate contacts. Invest Ophthalmol Vis Sci 2004, 45:4210-4216.
40. Zajicova A., Pokorna K., Lencova A., Krulova M., Svobodova E., Kubinova S., et al. Treatment of ocular surface injuries by limbal and mesenchymal stem cells growing on nanofiber scaffolds. Cell Transpl 2010, 19:1281-1290.
41. Babaeijandaghi F., Shabani I., Seyedjafari E., Naraghi Z.S., Vasei M., Haddadi-Asl V., et al. Accelerated epidermal regeneration and improved dermal reconstruction achieved by polyethersulfone nanofibers. Tissue Eng Part A 2010, 16:3527-3536.
42. Schindler M., Ahmed I., Kamal J., Nur E.K.A., Grafe T.H., Young Chung H., et al. Asynthetic nanofibrillar matrix promotes invivo-like organization and morphogenesis for cells in culture. Biomaterials 2005, 26:5624-5631.
43. Sharma S., Mohanty S., Gupta D., Jassal M., Agrawal A.K., Tandon R. Cellular response of limbal epithelial cells on electrospun poly-epsilon-caprolactone nanofibrous scaffolds for ocular surface bioengineering: a preliminary invitro study. Mol Vis 2011, 17:2898-2910.
44. Tezel T.H., Del Priore L.V. Repopulation of different layers of host human Bruch's membrane by retinal pigment epithelial cell grafts. Invest Ophthalmol Vis Sci 1999, 40:767-774.
45. Rak D.J., Hardy K.M., Jaffe G.J., McKay B.S. Ca++-switch induction of RPE differentiation. Exp Eye Res 2006, 82:648-656.
46. Engelmann K., Valtink M. RPE cell cultivation. Graefes Arch Clin Exp Ophthalmol 2004, 242:65-67.
47. Buttafoco L., Kolkman N.G., Engbers-Buijtenhuijs P., Poot A.A., Dijkstra P.J., Vermes I., et al. Electrospinning of collagen and elastin for tissue engineering applications. Biomaterials 2006, 27:724-734.
48. Burke J.M. Epithelial phenotype and the RPE: is the answer blowing in the Wnt?. Prog Retin Eye Res 2008, 27:579-595.
49. Salero E., Blenkinsop T.A., Corneo B., Harris A., Rabin D., Stern J.H., et al. Adult human RPE can be activated into a multipotent stem cell that produces mesenchymal derivatives. Cell Stem Cell 2012, 10:88-95.
50. Booij J.C., Baas D.C., Beisekeeva J., Gorgels T.G., Bergen A.A. The dynamic nature of Bruch's membrane. Prog Retin Eye Res 2010, 29:1-18.
51. Tezel T.H., Del Priore L.V., Kaplan H.J. Reengineering of aged Bruch's membrane to enhance retinal pigment epithelium repopulation. Invest Ophthalmol Vis Sci 2004, 45:3337-3348.
52. Wang H., Ninomiya Y., Sugino I.K., Zarbin M.A. Retinal pigment epithelium wound healing in human Bruch's membrane explants. Invest Ophthalmol Vis Sci 2003, 44:2199-2210.
53. Cranford S.W., de Boer J., van Blitterswijk C., Buehler M.J. Materiomics: an -omics approach to biomaterials research. Adv Mater 2013, 25:802-824.
54. Quester R., Hermanns B., Klosterhalfen B., Schroder R., Klug N. Biocompatibility and healing process of polyester meshes in the brain: invivo examination in rats. Biomaterials 2003, 24:711-721.
55. Xie J., Han Z., Naito M., Maeyama A., Kim S.H., Kim Y.H., et al. Articular cartilage tissue engineering based on a mechano-active scaffold made of poly(l-lactide-co-epsilon-caprolactone): invivo performance in adult rabbits. JBiomed Mater Res B Appl Biomater 2010, 94:80-88.
56. Okuda T., Higashide T., Fukuhira Y., Sumi Y., Shimomura M., Sugiyama K. Athin honeycomb-patterned film as an adhesion barrier in an animal model of glaucoma filtration surgery. JGlaucoma 2009, 18:220-226.
57. Thumann G., Viethen A., Gaebler A., Walter P., Kaempf S., Johnen S., et al. The invitro and invivo behaviour of retinal pigment epithelial cells cultured on ultrathin collagen membranes. Biomaterials 2009, 30:287-294.
58. Nicolini J., Kiilgaard J.F., Wiencke A.K., Heegaard S., Scherfig E., Prause J.U., et al. The anterior lens capsule used as support material in RPE cell-transplantation. Acta Ophthalmol Scand 2000, 78:527-531.
59. Pritchard C.D., Arner K.M., Neal R.A., Neeley W.L., Bojo P., Bachelder E., et al. The use of surface modified poly(glycerol-co-sebacic acid) in retinal transplantation. Biomaterials 2010, 31:2153-2162.
60. Lu B., Zhu D., Hinton D., Humayun M.S., Tai Y.C. Mesh-supported submicron parylene-c membranes for culturing retinal pigment epithelial cells. Biomed Microdevices 2012, 14:659-667.
61. Seiler M.J., Aramant R.B. Intact sheets of fetal retina transplanted to restore damaged rat retinas. Invest Ophthalmol Vis Sci 1998, 39:2121-2131.
62. Cereda M.G., Parolini B., Bellesini E., Pertile G. Surgery for CNV and autologous choroidal RPE patch transplantation: exposing the submacular space. Graefes Arch Clin Exp Ophthalmol 2010, 248:37-47.
63. Fisher S.K., Lewis G.P., Linberg K.A., Verardo M.R. Cellular remodeling in mammalian retina: results from studies of experimental retinal detachment. Prog Retin Eye Res 2005, 24:395-431.
64. Anderson D.H., Stern W.H., Fisher S.K., Erickson P.A., Borgula G.A. The onset of pigment epithelial proliferation after retinal detachment. Invest Ophthalmol Vis Sci 1981, 21:10-16.
65. Lewis G.P., Chapin E.A., Luna G., Linberg K.A., Fisher S.K. The fate of Muller's glia following experimental retinal detachment: nuclear migration, cell division, and subretinal glial scar formation. Mol Vis 2010, 16:1361-1372.
66. Butterwick A., Huie P., Jones B.W., Marc R.E., Marmor M., Palanker D. Effect of shape and coating of a subretinal prosthesis on its integration with the retina. Exp Eye Res 2009, 88:22-29.
67. Szurman P., Roters S., Grisanti S., Aisenbrey S., Schraermeyer U., Luke M., et al. Ultrastructural changes after artificial retinal detachment with modified retinal adhesion. Invest Ophthalmol Vis Sci 2006, 47:4983-4989.
68. Berglin L., Algvere P.V., Seregard S. Photoreceptor decay over time and apoptosis in experimental retinal detachment. Graefes Arch Clin Exp Ophthalmol 1997, 235:306-312.
69. Ivert L., Kjeldbye H., Gouras P. Long-term effects of short-term retinal bleb detachments in rabbits. Graefes Arch Clin Exp Ophthalmol 2002, 240:232-237.
70. Liao J.L., Yu J., Huang K., Hu J., Diemer T., Ma Z., et al. Molecular signature of primary retinal pigment epithelium and stem-cell-derived RPE cells. Hum Mol Genet 2010, 19:4229-4238.
71. Stanzel B.V., Liu Z., Somboonthanakij S., Wongsawad W., Brinken R., Eter N., et al. Human RPE stem cells grown into polarized RPE monolayers on a polyester matrix are maintained after grafting into rabbit subretinal space. Stem Cell Reports 2014, 2:1-14. Available from URL: http://www.cell.com/stem-cell-reports/fulltext/S2213-6711(13)00130-6#. 10.1016/j.stemcr.2013.11.005.