In vitro characterization of micropatterned PLGA-PHBV8 blend films as temporary scaffolds for photoreceptor cells

Journal of Biomedical Materials Research - Part A

Volumn 86, Issue 1, 2008, Pages 170-181

  Tezcaner, A ^a,b   Hicks, D ^b  

^a MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^b Institut des Neurosciences Cellulaires et Intégratives UPR3212   (France)

Author keywords

Micropatterning; Photoreceptors; Polymer; Scaffold; Tissue engineering

Indexed keywords

AGING POPULATION; ARRESTIN; BLEND FILMS; DEGRADATION RATES; DEVELOPED COUNTRIES; HYDROXYBUTYRATE (PHB); IN VITRO CHARACTERIZATION; L LACTIC ACID (PLLA); LAMININ; MICROPATTERNED; PARALLEL GROOVES; PHOTORECEPTOR CELLS; RETINAL DISEASES; RETINAL PIGMENT EPITHELIUM (RPE); RHODOPSIN (RHO); THIN AND THICK FILMS; WATER UPTAKE;

BIOLOGICAL MARKER; BIOMATERIAL; LAMININ; POLY(HYDOXYBUTYRATE CO HYDROXYVALERIC ACID); POLYGLACTIN; RETINA S ANTIGEN; RHODOPSIN; SCAFFOLD PROTEIN;

ANIMAL TISSUE; ARTICLE; BIODEGRADABLE IMPLANT; BIODEGRADATION; CELL CULTURE; CELL DIFFERENTIATION; CELL SURVIVAL; CELL VIABILITY; IN VITRO STUDY; INCUBATION TIME; MICROFILM; MUELLER CELL; NONHUMAN; PHOTORECEPTOR CELL; PIGMENT EPITHELIUM; PROTEIN DEGRADATION; PROTEIN EXPRESSION; RETINA CONE; RETINA ROD; STATISTICAL SIGNIFICANCE; SURVIVAL RATE; TISSUE ENGINEERING;

ANIMALS; BIOCOMPATIBLE MATERIALS; CELL SURVIVAL; CHEMISTRY; IMMUNOHISTOCHEMISTRY; LACTIC ACID; LAMININ; MATERIALS TESTING; NEUROGLIA; PHOTORECEPTORS; PIGMENT EPITHELIUM OF EYE; POLYESTERS; POLYGLYCOLIC ACID; RETINA; SWINE; TISSUE ENGINEERING;

EID: 44849129678     PISSN: 15493296     EISSN: 15524965     Source Type: Journal    
DOI: 10.1002/jbm.a.31600     Document Type: Article

References (76)

1. Delyfer MN, Léveillard T, Mohand-Saïd S, Hicks D, Picaud S, Sahel JA. Inherited retinal degenerations: Therapeutic prospects. Biol Cell 2004;96:261-269.
2. Bennett J, Zeng Y, Bajwa R, Klatt L, Li Y, Maguire AM. Adenovirus-mediated delivery of rhodopsin-promoted bcl-2 results in a delay in photoreceptor cell death in the rd/rd mouse. Gene Ther 1998;5:1156-1164.
3. Takashi M, Miyoshi H, Verma IM, Gage FH. Rescue from photoreceptor degeneration in the rd mouse by human immunodeficiency virus vector-mediated gene transfer. J Virol 1999;73:7812-7816.
4. D'Cruz PM, Yasumura D, Weir J, Matthes MT, Abderrahim H, La Vail MM, Vollrath D. Mutation of the receptor tyrosine kinase gene Mertk in the retinal dystrophic RCS rat. Hum Mol Genet 2000;9:645-651.
5. Laura H, Sanftner MG, Abel H, Hauswirth WW, Flannery JG. Glial cell line derived neurotrophic factor delays photoreceptor degeneration in a transgenic rat model of retinitis pigmentosa. Mol Ther 2001;4:622-629.
6. Sung CH, Schneider BG, Agarwal N, Papermaster DS, Nathans J. Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc Natl Acad Sci USA 1991;88:8840-8844.
7. Li T, Sandberg MA, Pawlyk BS, Rosner B, Hayes KC, Dryja TP, Berson EL. Effect of vitamin A supplementation on rhodopsin mutants threonine-17 → methionine and proline-347 → serine in transgenic mice and in cell cultures. Proc Natl Acad Sci USA 1998;95:11933-11938.
8. LaVail MM, Yasumura D, Matthes MT, Lau-Villacorta C, Unoki K, Sung CH, Steinberg RH. Protection of mouse photoreceptors by survival factors in retinal degenerations. Invest Ophthalmol Vis Sci 1998;39:592-602.
9. Frasson M, Picaud S, Leveillard T, Simonutti M, Mohand-Said S, Dreyfus H, Hicks D, Sahel J. Glial cell line-derived neurotrophic factor induces histologic and functional protection of rod photoreceptors in the rd/rd mouse. Invest Ophthalmol Vis Sci 1999;40:2724-2734.
10. Bok D, Yasumura D, Matthes MT, Ruiz A, Duncan JL, Chappelow AV, Zolutukhin S, Hauswirth W, LaVail MM. Effects of adeno-associated virus-vectored ciliary neurotrophic factor on retinal structure and function in mice with a P216L rds/peripherin mutation. Exp Eye Res 2002;74:719-735.
11. Kommonen B, Kylma T, Cohen RJ, Penn JS, Paulin L, Hurwitz M, Hurwitz RL. Elevation of cGMP with normal expression and activity of rod cGMP-PDE in photoreceptor degenerate labrador retrievers. Ophthalmic Res 1996;28:19-28.
12. Lee KS, Tsien RW. Mechanism of calcium channel blockade by verapamil, D600, diltiazem and nitrendipine in single dialysed heart cells. Nature 1983;302:790-794.
13. Frasson M, Sahel JA, Fabre M, Simonutti M, Dreyfus H, Picaud S. Retinitis pigmentosa: Rod photoreceptor rescue by a calcium-channel blocker in the rd mouse. Nat Med 1999;5:1183-1187.
14. Turner JE, Blair JR. Newborn rat retinal cells transplanted into a retinal lesion site in adult host eyes. Brain Res 1986;391:91-104.
15. Mohand Said S, Hicks D, Simonutti M, Tran-Minh D, Deudon-Combe A, Dreyfus H, Silverman MS, Ogilvie JM, Ten-kova T, Sahel J. Photoreceptor transplants increase host cone survival in the retinal degeneration (rd) mouse. Ophthalmic Res 1997;29:290-297.
16. Ahmad I, Dooley CM, Thoreson WB, Rogers JA, Afiat S. In vitro analysis of a mammalian retinal progenitor that gives rise to neurons and glia. Brain Res 1999;831:1-10.
17. Chacko DM, Rogers JA, Turner JE, Ahmad I. Survival and differentiation of cultured retinal progenitors transplanted in the subretinal space of the rat. Biochem Biophys Res Commun 2000;268:842-846.
18. Kicic A, Shen WY, Wilson AS, Constable IJ, Robertson T, Rakoczy PE. Differentiation of marrow stromal cells into photoreceptors in the rat eye. J Neurosci 2003;23:7742-7749.
19. Radtke ND, Aramant RB, Seiler M, Petry HM. Preliminary report: Indications of improved visual function after retinal sheet transplantation in retinitis pigmentosa patients. Am J Ophthalmol 1999;128:384-387.
20. Arai S, Thomas BB, Seiler MJ, Aramant RB, Qiu G, Mui C, de Juan E, Sadda SR. Restoration of visual responses following transplantation of intact retinal sheets in rd mice. Exp Eye Res 2004;79:331-341.
21. MacLaren RE, Pearson RA, Macneil A, Douglas RH, Salt TE, Akimoto M, Swaroop A, Sowden JC, Ali RR. Retinal repair by transplantation of photoreceptor precursors. Nature 2006;444:203-207.
22. Algvere PV, Berglin L, Gouras P, Sheng Y. Transplantation of fetal retinal pigment epithelium in age-related macular degeneration with subfoveal neovascularization. Graefe's Arch Clin Exp Ophthalmol 1994;232:707-716.
23. Aramant RB, Seiler MJ. Fiber and synaptic connections between embryonic retinal transplants and host retina. Exp Neurol 1995;133:244-255.
24. Laura H, Sanftner MG, Abel H., Hauswirth WW, Flannery JG. Glial cell line derived neurotrophic factor delays photoreceptor degeneration in a transgenic rat model of retinitis pigmentosa. Mol Ther 2001;4:622-629.
25. Lavail MM, Li L, Turner JE, Yasumura D. Retinal pigment epithelial cell transplantation in RCS rats: Normal metabolism in rescued photoreceptors. Exp Eye Res 1992;55:555-562.
26. Lawrence JM, Keegan DJ, Muir EM, Coffey PJ, Rogers JH, Wilby MJ, Fawcett JW, Lund RD. Transplantation of Schwann cell line clones secreting GDNF or BDNF into the retinas of dystrophic royal college of surgeons rats. Invest Ophthalmol Vis Sci 2004;45:267-274.
27. Nishida A, Takahashi M, Tanihara H, Nakano I, Takahashi JB, Mizoguchi A, Ide C, Honda Y. Incorporation and differentiation of hippocampus-derived neural stem cells transplanted in injured adult rat retina. Invest Ophthalmol Vis Sci 2000;41:4268-4274.
28. Tomita M, Adachi Y, Yamada H, Takahashi K, Kiuchi K, Oyaizu H, Ikebukuro K, Kaneda H, Matsumura M, Ikehara S. Bone marrow-derived stem cells can differentiate into retinal cells in injured rat retina. Stem Cells 2002;20:279-283
29. Lavik EB, Klassen H, Warfinge K, Langer R, Young MJ. Fabrication of degradable polymer scaffolds to direct the integration of retinal progenitors. Biomaterials 2005;26:3187-3196.
30. Tezcaner A, Hicks D, Bouldemais F, Sahel J, Schaaf P, Voegel JC, Lavalle P. Polyelectrolyte multilayer films as substrates for photoreceptor cells. Biomacromolecules 2006;7:86-94.
31. Tao W, Wen R, Goddard MB, Sherman SD, O'Rourke PJ, Stabila PF, Bell WJ, Dean BJ, Kauper KA, Budz VA, Tsiaras WG, Acland GM, Pearce-Kelling S, Laties AM, Aguirre GD. Encapsulated cell-based delivery of CNTF reduces photoreceptor degeneration in animal models of retinis pigmentosa. Invest Opthalmol Vis Sci 2002;43:3292-3298.
32. Sieving PA, Caruso RC, Tao W, Coleman HR, Thompson DJS, Fullmer KR, Bush RA. Ciliary neurotrophic factor (CNTF) for human retinal degeneration: Phase I trial of CNTF delivered by encapsulated cell intraocular implants. PNAS 2006;103:3896-3901.
33. Curtis A, Riehle M. Tissue engineering: The biophysical background. Phys Med Biol 2001;46:R47-R65.
34. Craighead HG, James CD, Turner AMP. Chemical and topographical patterning for directed cell attachment. Curr Opin Solid State Mater Sci 2001;5:177-184.
35. Clark P, Connolly P, Curtis ASG, Dow JAT, Wilkinson CDW. Cell guidance by an ultrafine topography in vitro. J Cell Sci 1991;99:73-77.
36. Matsuzaka K, Walboomers XF, Ruijter JE, Jansen JA. The effect of poly-L-lactic acid with parallel surface microgroove on osteoblast-like cells in vitro. Biomaterials 1999;20:1293-1301.
37. Miller C, Shanks H, Witt A, Rutkowski G, Mallapragada S. Oriented schwann cell growth on micropatterned biodegradable polymer substrates. Biomaterials 2001;22:1263-1269.
38. Miller C, Jeftinija S, Mallapragada S. Micropatterned Schwann cell-seeded biodegradable polymer substrates significantly enhance neurite alignment and outgrowth. Tissue Eng 2001;7:705-715.
39. Miller C, Jeftinija S, Mallapragada S. Synergistic effects of physical and chemical guidance cues on neurite alignment and outgrowth on biodegradable polymer substrates. Tissue Eng 2002;8:367-378.
40. Wilkinson CD, Riehle M, Wood M, Gallagher J, Curtis ASG. The use of materials patterned on a nano-and micro-metric scale in cellular engineering. Mater Sci Eng C 2002;19:263-269.
41. Dalby MJ, Riehle MO, Yardwood SJ, Wilkinson CDW, Curtis ASG. Nucleus alignment and cell signalling in fibroblasts: Response to microgrooved topography. Exp Cell Res 2003;284:274-282.
42. Ber S, Köse GT, Hasirci V. Bone tissue engineering on patterned collagen films: An in vitro study. Biomaterials 2005;26:1977-1986.
43. Kenar H, Köse GT, Hasirci V. Tissue engineering of bone on micropatterned biodegradable polyester films. Biomaterials 2006;27:885-895.
44. Zorlutuna P, Tezcaner A, Kiyat I, Aydinli A, Hasirci V. Cornea engineering on polyester carriers. J Biomed Mater Res 2006;79:104-113.
45. Recknor JB, Sakaguchi DS, Mallapragada SK. Directed growth and selective differentiation of neural progenitor cells on micropatterned polymer substrates. Biomaterials 2006;27:4098-4108.
46. Weiss P. Experiments on cell and axon orientation in vitro: The role of colloidal exudates in tissue organisation. J Exp Zool 1945;100:353-386.
47. Walboomers XF, Ginsei LA, Jansel JA. Early spreading events of fibroblasts on microgrooved substrates. J Biomed Mater Res 2000;51:529-534.
48. Brunette DM, Chehroudi B. The effect of the surface topography of micromachined titanium substrata on cellular behaviour in vitro and in vivo. J Biomech Eng 1999;121:49-57.
49. Walboomers XF, Croes HJE, Ginsel LA, Jansen JA. Contact guidance of rat fibroblasts on various implant materials. J Biomed Mater Res 1999;47:204-212.
50. Traverso V, Kinkl N, Grimm L, Sahel J, Hicks D. Basic fibroblast and EGF factors stimulate survival in adult porcine photoreceptor cell cultures. Invest Ophthalmol Vis Sci 2003;44:4550-4558.
51. Fintz AC, Audo I, Hicks D, Mohand-Said S, Léveillard T, Sahel J. Partial characterization of retina-derived cone neuroprotection in two culture models of photoreceptor degeneration. Invest Ophthalmol Vis Sci 2003;44:818-824.
52. Thomson RC, Giardano GG, Collier JH, Ishaug SL, Mikos AG, Lahiri-Munir D, Garcia CA. Manufacture and characterization of poly(α-hydroxy ester) thin films as temporary substrates for retinal pigment epithelium cells. Biomaterials 1996;17:321-327.
53. Lu L, Garcia CA, Mikos AG. Retinal pigment epithelium cell culture on thin biodegradable poly(DL-lactic-co-glycolic acid) films. Biomater Sci Polym Ed 1998;9:1187-1205.
54. Lu L, Yaszemski MJ, Mikos AG. Retinal pigment epithelium engineering using synthetic biodegradable polymers. Biomaterials 2000;22:3345-3355.
55. Lu L, Nyalakonda K, Kam L, Bizios R, Gopferich A, Mikos AG. Retinal pigment epithelial cell adhesion on novel micro-patterned surfaces fabricated from synthetic biodegradable polymers. Biomaterials 2001;22:291-297.
56. Tezcaner A, Bugra K, Hasirci V. Retinal pigment epithelium cultured on thin, biodegradable poly(hydroxybutyrate-co-hydroxyvalerate) films. Biomaterials 2003;24:4573-4583.
57. Lu L, Garcia CA, Mikos AG. In vitro degradation of thin poly (DL-lactic-co-glycolic acid) films. J Biomed Mater Res 1999;46:236-244.
58. Spenlehauer G, Vert M, Benoit JP, Boddaert A. In vitro and in vivo degradation of poly (D,L lactide/glycolide) type microspheres made by solvent evaporation method. Biomaterials 1989;10:557-563.
59. Park TG. Degradation of poly(D,L-lactic acid) microspheres: Effect of molecular weight. J Control Release 1994;30:161-173.
60. Grizzi I, Garreau H, Li S, Vert M. Hydrolytic degradation of devices based on poly(DL-lactic acid) size dependence. Biomaterials 1995;16:305-311.
61. Holy CE, Dang SM, Davies JE, Shoichet MS. In vitro degradation of a novel poly(lactide-co-glycolide) 75/25 foam. Biomaterials 1999;20:1177-1185.
62. Gogolewski S, Jovanovic M, Perren SM, Dillon JG, Hughes MK. The effect of melt processing on the degradation of selected poyhydroxyacids: Polylactides, polyhydroxybutyrate, and polyhydroxybutyrate-co-valerates. Polym Degrad Stab 1993;40:313-322.
63. Gogolewski S, Jovanovic M, Perren SM, Dillon JG, Hughes MK. Tissue response and in vivo degradationof selected polyhydroxyacids: Polylactides (PLA), Poly(3-hydroxybutyrate) (PHB), and poly(3-hydroxybutyrate-co-3- hydroxyvalerate) (PHB/VA). J Biomed Mater Res 1993;27:1135-1148.
64. Leenstra TS, Maltha JC, Kuijpers-Jagtman AM. Biodegradation of nonporous films after submucoperiosteal implantation on the palate of Beagle dogs. J Mater Sci: Mater Med 1995;6:445-450.
65. Holland SJ, Jolly AM, Yasin M, Tighe BJ. Polymers for biodegradable medical devices. II. Hydroxybutyrate-hydroxyvalerate copolymers hydrolytic degradation studies. Biomaterials 1987;8:289-295.
66. Doi Y, Kanesawa Y, Kuwaguchi Y, Kunioka M. Hydrolytic degradation of microbial poly(hydroxyalkanoates). Makromol Chem Rapid Commun 1989;10:227-230.
67. Majid MIA, Ismail J, Few LL, Tan CF. The degradation kinetics of poly(3-hydroxybutyrate) under non-aqueous and aqueous conditions. Eur Polym J 2002;38:837-839
68. Cao W, Wen R, Li F, Cheng T, Steinberg RH. Induction of basic fibroblast growth factor mRNA by basic fibroblast factor in Muller cells. Invest Ophthalmol Vis Sci 1997;38:1358-1366.
69. Gaur VP, Liu Y, Turner JE. RPE conditioned medium stimulates photoreceptor cell survival, neurite outgrowth and differentiation in vitro. Exp Eye Res 1992;54:645-659.
70. Sheedlo HJ, Nelson TH, Lin N, Rogers TA, Roque RS, Turner JE. RPE secreted proteins and antibody influence photoreceptor cell survival and maturation. Dev Brain Res 1998;107:57-69.
71. Bonnet D, Garcia M, Vecino E, Loerntz JG, Sahel J, Hicks D. Brain-derived neurotrophic factor signalling in adult pig retinal ganglion cell neurite regeneration in vitro. Brain Res 2004;1007:142-151
72. Tombran-Tink J, Chader GG, Johnson LV. PEDF: A pigment epithelium-derived factor with potent neuronal differentiative activity. Exp Eye Res 1991;53:411-414.
73. Jablonski MM, Tombran-Tink J, Mrazek DA, Iannaccone A. Pigment-epithelium derived factor supports normal development of photorecptor neurons and opsin expression after retinal pigment epithelium removal. J Neurosci 2000;20:7149-7157.
74. Mack AF, Uhlmann D, Germer A, Szel A, Enzmann V, Reichenbach A. Differentiation of cones in cultured rabbit retina: Effects of retinal pigment epithelial cell-conditioned medium. Neurosci Lett 2003;341:53-56.
75. Garcia M, Forster V, Hicks D, Vecino E. Effects of Muller glia on cell survival and neuritogenesis in adult porcine retina in vitro. Invest Ophthalmol Vis Sci 2002;43:3735-3743.
76. Leveillard T, Mohand-Said S, Fintz AC, Lambrou G, Sahel JA. The search for rod-dependent cone viability factors, secreted factors promoting cone viability. Novartis Found Symp 2004;255:117-127.