A novel Bruch's membrane-mimetic electrospun substrate scaffold for human retinal pigment epithelium cells

Biomaterials

Volumn 35, Issue 37, 2014, Pages 9777-9788

  Xiang, Ping ^a   Wu, Kun Chao ^a   Zhu, Ying ^b   Xiang, Lue ^a   Li, Chong ^c   Chen, Deng Long ^b   Chen, Feng ^a   Xu, Guotong ^c   Wang, Aijun ^d   Li, Min ^b   Jin, Zi Bing ^a  

^a EYE HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

^b FUJIAN NORMAL UNIVERSITY   (China)

^c TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bruch's membrane; Cytocompatibility; Electrospinning; Regenerated wild Antheraea pernyi silk fibroin; RPE

Indexed keywords

ALDEHYDES; BIOCOMPATIBILITY; CELL PROLIFERATION; CELLS; CYTOLOGY; ELECTROSPINNING; GROWTH RATE; MEMBRANES; MORPHOLOGY; NANOFIBERS; OPHTHALMOLOGY; SUBSTRATES;

ANTHERAEA PERNYI SILK FIBROINS; AVERAGE FIBER DIAMETERS; BRUCH'S MEMBRANE; CYTOCOMPATIBILITY; INFLAMMATORY MEDIATORS; LONG-TERM CULTIVATIONS; NANOFIBROUS MEMBRANES; RETINAL PIGMENT EPITHELIUM;

SCAFFOLDS (BIOLOGY);

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CILIARY NEUROTROPHIC FACTOR; GELATIN; MELANOCYTE PROTEIN PMEL 17; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MOLECULAR SCAFFOLD; NEUROTROPHIN; PIGMENT EPITHELIUM DERIVED FACTOR; POLYCAPROLACTONE; VASCULOTROPIN; BIOMIMETIC MATERIAL; FIBROIN; NANOFIBER; POLYESTER;

ADULT; ARTICLE; ARTIFICIAL MEMBRANE; BIOCOMPATIBILITY; BRUCH MEMBRANE; CELL ADHESION; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIFFERENTIATION; CELL GROWTH; CELL POPULATION; CELL PROLIFERATION; CELL SHAPE; CELL VIABILITY; COCULTURE; CONTACT ANGLE; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYDROPHILICITY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICROMORPHOLOGY; MICROVILLUS; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHOTORECEPTOR OUTER SEGMENT; PHYSICAL CHEMISTRY; PIGMENT CELL; PIGMENT EPITHELIUM; PIGMENTATION; POROSITY; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; THICKNESS; TIGHT JUNCTION; WETTABILITY; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; METABOLISM; MOTH; PIG; RABBIT; TISSUE SCAFFOLD; ULTRASTRUCTURE;

ADULT; ANIMALS; BIOMIMETIC MATERIALS; BRUCH MEMBRANE; CELLS, CULTURED; FIBROINS; GELATIN; HUMANS; MOTHS; NANOFIBERS; POLYESTERS; POROSITY; RABBITS; RETINAL PIGMENT EPITHELIUM; SWINE; TISSUE SCAFFOLDS;

EID: 84907270590     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.08.040     Document Type: Article

References (64)

1. Strauss O. The retinal pigment epithelium in visual function. Physiol Rev 2005, 85:845-881.
2. Kokkinaki M., Sahibzada N., Golestaneh N. Human induced pluripotent stem-derived retinal pigment epithelium (RPE) cells exhibit ion transport, membrane potential, polarized vascular endothelial growth factor secretion, and gene expression pattern similar to native RPE. Stem Cells 2011, 29:825-835.
3. Ming M., Li X., Fan X., Yang D., Li L., Chen S., et al. Retinal pigment epithelial cells secrete neurotrophic factors and synthesize dopamine: possible contribution to therapeutic effects of RPE cell transplantation in Parkinson's disease. J Transl Med 2009, 7:53.
4. Zhu D., Deng X., Spee C., Sonoda S., Hsieh C.L., Barron E., et al. Polarized secretion of PEDF from human embryonic stem cell-derived RPE promotes retinal progenitor cell survival. Invest Ophthalmol Vis Sci 2011, 52:1573-1585.
5. Rowland T.J., Buchholz D.E., Clegg D.O. Pluripotent human stem cells for the treatment of retinal disease. J Cell Physiol 2012, 227:457-466.
6. Wang H., Yagi F., Cheewatrakoolpong N., Sugino I.K., Zarbin M.A. Short-term study of retinal pigment epithelium sheet transplants onto Bruch's membrane. Exp Eye Res 2004, 78:53-65.
7. Seiler M.J., Aramant R.B. Cell replacement and visual restoration by retinal sheet transplants. Prog Retin Eye Res 2012, 31:661-687.
8. Lewallen M., Xie T. Cell-based therapies for retinal degenerative diseases: a thousand strategies. J Glaucoma 2013, 22(Suppl. 5):S42-S45.
9. 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.
10. Lamba D.A., Karl M.O., Reh T.A. Strategies for retinal repair: cell replacement and regeneration. Prog Brain Res 2009, 175:23-31.
11. Gouras P., Kong J., Tsang S.H. Retinal degeneration and RPE transplantation in Rpe65(-/-) mice. Invest Ophthalmol Vis Sci 2002, 43:3307-3311.
12. Xiang P., Li M., Zhang C.-y., Chen D.-l., Zhou Z.-h. Cytocompatibility of electrospun nanofiber tubular scaffolds for small diameter tissue engineering blood vessels. Int J Biol Macromol 2011, 49:281-288.
13. Li Y., Tsai Y.T., Hsu C.W., Erol D., Yang J., Wu W.H., et al. Long-term safety and efficacy of human-induced pluripotent stem cell (iPS) grafts in a preclinical model of retinitis pigmentosa. Mol Med 2012, 18:1312-1319.
14. Engelhardt M., Tosha C., Lopes V.S., Chen B., Nguyen L., Nusinowitz S., et al. Functional and morphological analysis of the subretinal injection of retinal pigment epithelium cells. Vis Neurosci 2012, 29:83-93.
15. Schwartz SD, Hubschman J-P, Heilwell G, Franco-Cardenas V, Pan CK, Ostrick RM, et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet;379:713-720.
16. Tezel T.H., Del Priore L.V., Berger A.S., Kaplan H.J. Adult retinal pigment epithelial transplantation in exudative age-related macular degeneration. Am J Ophthalmol 2007, 143:584-595.
17. Del Priore L.V., Kaplan H.J., Tezel T.H., Hayashi N., Berger A.S., Green W.R. Retinal pigment epithelial cell transplantation after subfoveal membranectomy in age-related macular degeneration: clinicopathologic correlation. Am J Ophthalmol 2001, 131:472-480.
18. Lu J.T., Lee C.J., Bent S.F., Fishman H.A., Sabelman E.E. Thin collagen film scaffolds for retinal epithelial cell culture. Biomaterials 2007, 28:1486-1494.
19. Thumann G., Viethen A., Gaebler A., Walter P., Kaempf S., Johnen S., et al. The in vitro and in vivo behaviour of retinal pigment epithelial cells cultured on ultrathin collagen membranes. Biomaterials 2009, 30:287-294.
20. Thumann G., Hueber A., Dinslage S., Schaefer F., Yasukawa T., Kirchhof B., et al. Characteristics of iris and retinal pigment epithelial cells cultured on collagen type I membranes. Curr Eye Res 2006, 31:241-249.
21. Shadforth A.M., George K.A., Kwan A.S., Chirila T.V., Harkin D.G. The cultivation of human retinal pigment epithelial cells on Bombyx mori silk fibroin. Biomaterials 2012, 33:4110-4117.
22. Subrizi A., Hiidenmaa H., Ilmarinen T., Nymark S., Dubruel P., Uusitalo H., et al. Generation of hESC-derived retinal pigment epithelium on biopolymer coated polyimide membranes. Biomaterials 2012, 33:8047-8054.
23. 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.
24. Thomson H.A., Treharne A.J., Walker P., Grossel M.C., Lotery A.J. Optimisation of polymer scaffolds for retinal pigment epithelium (RPE) cell transplantation. Br J Ophthalmol 2011, 95:563-568.
25. Williams R., Krishna Y., Dixon S., Haridas A., Grierson I., Sheridan C. Polyurethanes as potential substrates for sub-retinal retinal pigment epithelial cell transplantation. J Mater Sci Mater Med 2005, 16:1087-1092.
26. Harkin D.G., George K.A., Madden P.W., Schwab I.R., Hutmacher D.W., Chirila T.V. Silk fibroin in ocular tissue reconstruction. Biomaterials 2011, 32:2445-2458.
27. Ito A., Hibino E., Kobayashi C., Terasaki H., Kagami H., Ueda M., et al. Construction and delivery of tissue-engineered human retinal pigment epithelial cell sheets, using magnetite nanoparticles and magnetic force. Tissue Eng 2005, 11:489-496.
28. 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.
29. Dong Y., Yong T., Liao S., Chan C.K., Stevens M.M., Ramakrishna S. Distinctive degradation behaviors of electrospun polyglycolide, poly(DL-lactide-co-glycolide), and poly(L-lactide-co-epsilon-caprolactone) nanofibers cultured with/without porcine smooth muscle cells. Tissue Eng Part A 2010, 16:283-298.
30. Chen H., Fan X., Xia J., Chen P., Zhou X., Huang J., et al. Electrospun chitosan-graft-poly (varepsilon-caprolactone)/poly (varepsilon-caprolactone) nanofibrous scaffolds for retinal tissue engineering. Int J Nanomedicine 2011, 6:453-461.
31. Fon D., Zhou K., Ercole F., Fehr F., Marchesan S., Minter M.R., et al. Nanofibrous scaffolds releasing a small molecule BDNF-mimetic for the re-direction of endogenous neuroblast migration in the brain. Biomaterials 2014, 35:2692-2712.
32. Zhao W., Ju Y.M., Christ G., Atala A., Yoo J.J., Lee S.J. Diaphragmatic muscle reconstruction with an aligned electrospun poly(ε-caprolactone)/collagen hybrid scaffold. Biomaterials 2013, 34:8235-8240.
33. Lee J., Yoo J.J., Atala A., Lee S.J. The effect of controlled release of PDGF-BB from heparin-conjugated electrospun PCL/gelatin scaffolds on cellular bioactivity and infiltration. Biomaterials 2012, 33:6709-6720.
34. Woodruff M.A., Hutmacher D.W. The return of a forgotten polymer-polycaprolactone in the 21st century. Prog Polym Sci 2010, 35:1217-1256.
35. Christiansen A.T., Tao S.L., Smith M., Wnek G.E., Prause J.U., Young M.J., et al. Subretinal implantation of electrospun, short nanowire, and smooth poly(epsilon-caprolactone) scaffolds to the subretinal space of porcine eyes. Stem Cells Int 2012, 2012:454295.
36. Cai S., Smith M.E., Redenti S.M., Wnek G.E., Young M.J. Mouse retinal progenitor cell dynamics on electrospun poly(varepsilon-caprolactone). J Biomater Sci Polym Ed 2011, 23:1451-1465.
37. Pritchard C.D., Arner K.M., Langer R.S., Ghosh F.K. Retinal transplantation using surface modified poly(glycerol-co-sebacic acid) membranes. Biomaterials 2010, 31:7978-7984.
38. Li X., Zhang C., Wang L., Ma C., Yang W., Li M. Acylation modification of antheraea pernyi silk fibroin using succinic anhydride and its effects on enzymatic degradation behavior. J Chem 2013, 2013. 640913.
39. Ruoslahti E. RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 1996, 12:697-715.
40. Wu L., Li M., Zhao J., Chen D., Zhou Z. Preliminary study on polyvinyl alcohol/wild antheraea pernyi silk fibroin as nanofiber scaffolds for tissue engineered tendon. Zhongguo xiu fu chong jian wai ke za zhi = Zhongguo xiufu chongjian waike zazhi = Chin J Reparative Reconstr Surg 2011, 25:181-186.
41. Sonoda S., Spee C., Barron E., Ryan S.J., Kannan R., Hinton D.R. A protocol for the culture and differentiation of highly polarized human retinal pigment epithelial cells. Nat Protoc 2009, 4:662-673.
42. Ahmado A., Carr A.J., Vugler A.A., Semo M., Gias C., Lawrence J.M., et al. Induction of differentiation by pyruvate and DMEM in the human retinal pigment epithelium cell line ARPE-19. Invest Ophthalmol Vis Sci 2011, 52:7148-7159.
43. Finnemann S.C., Bonilha V.L., Marmorstein A.D., Rodriguez-Boulan E. Phagocytosis of rod outer segments by retinal pigment epithelial cells requires αvβ5 integrin for binding but not for internalization. Proc Natl Acad Sci 1997, 94:12932-12937.
44. Liu Z., Yu N., Holz F.G., Yang F., Stanzel B.V. Enhancement of retinal pigment epithelial culture characteristics and subretinal space tolerance of scaffolds with 200 nm fiber topography. Biomaterials 2014, 35:2837-2850.
45. 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.
46. Kevany B.M., Palczewski K. Phagocytosis of retinal rod and cone photoreceptors. Physiology 2010, 25:8-15.
47. Gonzalez-Cordero A., West E.L., Pearson R.A., Duran Y., Carvalho L.S., Chu C.J., et al. Photoreceptor precursors derived from three-dimensional embryonic stem cell cultures integrate and mature within adult degenerate retina. Nat Biotechnol 2013, 31:741-747.
48. Treharne A.J., Thomson H.A.J., Grossel M.C., Lotery A.J. Developing methacrylate-based copolymers as an artificial Bruch's membrane substitute. J Biomed Mater Res Part A 2012, 100A:2358-2364.
49. Binder S. Scaffolds for retinal pigment epithelium (RPE) replacement therapy. Br J Ophthalmol 2011, 95:441-442.
50. Rodrigues M.T., Martins A., Dias I.R., Viegas C.A., Neves N.M., Gomes M.E., et al. Synergistic effect of scaffold composition and dynamic culturing environment in multilayered systems for bone tissue engineering. J Tissue Eng Regen Med 2012, 6:e24-30.
51. 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.
52. Heth C.A., Yankauckas M.A., Adamian M., Edwards R.B. Characterization of retinal pigment epithelial cells cultured on microporous filters. Curr Eye Res 1987, 6:1007-1019.
53. Curcio C.A., Johnson M. Structure, function, and pathology of Bruch's membrane. Elastic 2012, 146:210-213.
54. Karampelas M., Sim D.A., Keane P.A., Papastefanou V.P., Sadda S.R., Tufail A., et al. Evaluation of retinal pigment epithelium-Bruch's membrane complex thickness in dry age-related macular degeneration using optical coherence tomography. Br J Ophthalmol 2013, 97:1256-1261.
55. Afshari F., Fawcett J. Improving RPE adhesion to Bruch's membrane. Eye 2009, 23:1890-1893.
56. Hersel U., Dahmen C., Kessler H. RGD modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 2003, 24:4385-4415.
57. Ma Z., He W., Yong T., Ramakrishna S. Grafting of gelatin on electrospun poly (caprolactone) nanofibers to improve endothelial cell spreading and proliferation and to control cell orientation. Tissue Eng 2005, 11:1149-1158.
58. Singh A.K., Srivastava G.K., Martin L., Alonso M., Pastor J.C. Bioactive substrates for human retinal pigment epithelial cell growth from elastin-like recombinamers. J Biomed Mater Res Part A 2014, 102:639-646.
59. Theisen C., Fuchs-Winkelmann S., Knappstein K., Efe T., Schmitt J., Paletta J., et al. Influence of nanofibers on growth and gene expression of human tendon derived fibroblast. Biomed Eng OnLine 2010, 9:1-12.
60. Ishihara K., Hirano T. IL-6 in autoimmune disease and chronic inflammatory proliferative disease. Cytokine Growth Factor Rev 2002, 13:357-368.
61. Nakazawa T., Hisatomi T., Nakazawa C., Noda K., Maruyama K., She H., et al. Monocyte chemoattractant protein 1 mediates retinal detachment-induced photoreceptor apoptosis. Proc Natl Acad Sci U S A 2007, 104:2425-2430.
62. Liu Y., Yang X., Utheim T.P., Guo C., Xiao M., Liu Y., et al. Correlation of cytokine levels and microglial cell infiltration during retinal degeneration in RCS rats. PLoS One 2013, 8:e82061.
63. Tombran-Tink J., Barnstable C.J. PEDF: a multifaceted neurotrophic factor. Nat Rev Neurosci 2003, 4:628-636.
64. Rezai K.A., Farrokh-Siar L., Godowski K., Patel S.C., Ernest J.T. A model for xenogenic immune response. Graefe's Archive Clin Exp Ophthalmol 2000, 238:352-358.