Cell-deposited matrix improves retinal pigment epithelium survival on aged submacular human Bruch's membrane

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 3, 2011, Pages 1345-1358

  Sugino, Ilene K ^a   Gullapalli, Vamsi K ^a   Sun, Qian ^a   Wang, Jianqiu ^a   Nunes, Celia F ^a   Cheewatrakoolpong, Noounanong ^a   Johnson, Adam C ^a   Degner, Benjamin C ^a   Hua, Jianyuan ^a   Liu, Tong ^b   Chen, Wei ^b   Li, Hong ^b   Zarbin, Marco A ^a  

^a INSTITUTE OF OPHTHALMOLOGY AND VISUAL SCIENCE   (United States)

^b The State University of New Jersey   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BESTROPHIN; CELL MEMBRANE PROTEIN; CELL PROTEIN; MESSENGER RNA; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ADULT; AFRICAN AMERICAN; AGED; ANIMAL CELL; ARTICLE; BRUCH MEMBRANE; CAUCASIAN; CELL DEPOSITED EXTRACELLULAR MATRIX; CELL NUCLEUS; CELL SURVIVAL; CONTROLLED STUDY; CORNEA ENDOTHELIUM; COW; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FETUS; HUMAN; HUMAN TISSUE; MASS SPECTROMETRY; NONHUMAN; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RACE DIFFERENCE; SCANNING ELECTRON MICROSCOPY;

ADULT; AGED; AGED, 80 AND OVER; AGING; ANIMALS; BRUCH MEMBRANE; CARRIER PROTEINS; CATTLE; CELL COUNT; CELL CULTURE TECHNIQUES; CELL SURVIVAL; CHLORIDE CHANNELS; COCULTURE TECHNIQUES; ENDOTHELIUM, CORNEAL; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; EYE PROTEINS; FEMALE; HUMANS; MALE; MASS SPECTROMETRY; MICROSCOPY, ELECTRON, SCANNING; MIDDLE AGED; ORGAN CULTURE TECHNIQUES; RETINAL PIGMENT EPITHELIUM; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 79955936252     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6112     Document Type: Article

References (91)

1. Friedman DS, O'Colmain BJ, Munoz B, et al. Prevalence of agerelated macular degeneration in the United States. Arch Ophthalmol. 2004;122:564-572.
2. Brown DM, Kaiser PK, Michels M, et al. Ranibizumab versus verteporfin for neovascular age-related macular degeneration. N Engl J Med. 2006;355:1432-1444.
3. Rosenfeld PJ, Brown DM, Heier JS, et al. Ranibizumab for neovascular age-related macular degeneration. N Engl J Med. 2006;355: 1419-1431.
4. A randomized, placebo-controlled, clinical trial of high-dose supplementation with vitamins C and E, beta carotene, and zinc for age-related macular degeneration and vision loss: AREDS report no. 8. Arch Ophthalmol. 2001;119:1417-1436.
5. Kanuga N, Winton HL, Beauchene L, et al. Characterization of genetically modified human retinal pigment epithelial cells developed for in vitro and transplantation studies. Invest Ophthalmol Vis Sci. 2002;43:546-555.
6. Becerra SP, Fariss RN, Wu YQ, Montuenga LM, Wong P, Pfeffer BA. Pigment epithelium-derived factor in the monkey retinal pigment epithelium and interphotoreceptor matrix: apical secretion and distribution. Exp Eye Res. 2004;78:223-234.
7. Marneros AG, Fan J, Yokoyama Y, et al. Vascular endothelial growth factor expression in the retinal pigment epithelium is essential for choriocapillaris development and visual. Am J Pathol. 2005;167:1451-1459.
8. Bost LM, Aotaki-Keen A, Hjelmeland LM. Coexpression of FGF5 and bFGF by the retinal pigment epithelium in vitro. Exp Eye Res. 1992;55:727-734.
9. Hackett SF, Schoenfeld CL, Freund J, Gotsch JD, Bhargave S, Campochiaro PA. Neurotrophic factors, cytokines and stress increase expression of basic fibroblast growth factor in retinal pigmented epithelial cells. Exp Eye Res. 1997;64:865-874.
10. Faktorovich EG, Steinberg RH, Yasumura D, Matthes MT, LaVail MM. Photoreceptor degeneration in inherited retinal dystrophy delayed by basic fibroblast growth factor. Nature. 1990;347:83-86.
11. Martin G, Schlunck G, Hansen LL, Agostini HT. Differential expression of angioregulatory factors in normal and CNV-derived human retinal pigment epithelium. Graefes Arch Clin Exp Ophthalmol. 2004;242:321-326.
12. Gullapalli VK, Khodair M, Wang H, Sugino IK, Madreperla S, Zarbin MA. Retinal pigment epithelium and photoreceptor transplantation frontiers. In: Ryan SJ, ed. Retina. 4th ed. Philadelphia: Elsevier Mosby, Inc.; 2006:2597-2613.
13. Li L, Turner JE. Optimal conditions for long-term photoreceptor cell rescue in RCS rats: the necessity for healthy RPE transplants. Exp Eye Res. 1991;52:669-679.
14. Coffey PJ, Girman S, Wang SM, et al. Long-term preservation of cortically dependent visual function in RCS rats by transplantation. Nat Neurosci. 2002;5:53-56.
15. Gouras P, Kong J, Tsang SH. Retinal degeneration and RPE transplantation in Rpe65(_/_) mice. Invest Ophthalmol Vis Sci. 2002; 43:3307-3311.
16. Wang NK, Tosi J, Kasanuki JM, et al. Transplantation of reprogrammed embryonic stem cells improves visual function in a mouse model for retinitis pigmentosa. Transplantation. 2010;89: 911-919.
17. Lu B, Malcuit C, Wang S, et al. Long-term safety and function of RPE from human embryonic stem cells in preclinical models of macular degeneration. Stem Cells. 2009;27:2126-2135.
18. Nozaki M, Raisler BJ, Sakurai E, et al. Drusen complement components C3a and C5a promote choroidal neovascularization. Proc Natl Acad Sci U S A. 2006;103:2328-2333.
19. Hageman GS, Anderson DH, Johnson LV, et al. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci U S A. 2005;102:7227-7232.
20. Klein RJ, Zeiss C, Chew EY, et al. Complement factor H polymorphism in age-related macular degeneration. Science. 2005;308: 385-389.
21. Edwards AO, Ritter R 3rd, Abel KJ, Manning A, Panhuysen C, Farrer LA. Complement factor H polymorphism and age-related maculardegeneration. Science. 2005;308:421-424.
22. Haines JL, Hauser MA, Schmidt S, et al. Complement factor H variant increases the risk of age-related macular degeneration. Science. 2005;308:419-421.
23. Hughes AE, Orr N, Esfandiary H Diaz-Torres M, Goodship T, Chakravarthy U. A common CFH haplotype, with deletion of CFHR1 and CFHR3, is associated with lower risk of age-related macular degeneration. Nat Genet. 2006;38:1173-1177.
24. Skerka C, Lauer N, Weinberger AA, et al. Defective complement control of factor H (Y402H) and FHL-1 in age-related macular degeneration. Mol Immunol. 2007;44:3398-3406.
25. Gold B, Merriam JE, Zernant J, et al. Variation in factor B (BF) and complement component 2 (C2) genes is associated with agerelated macular degeneration. Nat Genet. 2006;38:458-462.
26. Yates JR, Sepp T, Matharu BK, et al. Complement C3 variant and the risk of age-related macular degeneration. N Engl J Med. 2007; 357:553-561.
27. He X, Hahn P, Iacovelli J, et al. Iron homeostasis and toxicity in retinal degeneration. Prog Retin Eye Res. 2007;26:649-673.
28. Dewan A, Liu M, Hartman S, et al. HTRA1 promoter polymorphism in wet age-related macular degeneration. Science. 2006;314:989-992.
29. Rivera A, Fisher SA, Fritsche LG, et al. Hypothetical LOC387715 is a second major susceptibility gene for age-related macular degeneration, contributing independently of complement factor H to disease risk. Hum Mol Genet. 2005;14:3227-3236.
30. Jakobsdottir J, Conley YP, Weeks DE, Mah TS, Ferrell RE, Gorin MB. Susceptibility genes for age-related maculopathy on chromosome 10q26. Am J Hum Genet. 2005;77:389-407.
31. Schmidt S, Hauser MA, Scott WK, et al. Cigarette smoking strongly modifies the association of LOC387715 and age-related macular degeneration. Am J Hum Genet. 2006;78:852-864.
32. Conley YP, Jakobsdottir J, Mah T, et al. CFH, ELOVL4, PLEKHA1 and LOC387715 genes and susceptibility to age-related maculopathy: AREDS and CHS cohorts and meta-analyses. Hum Mol Genet. 2006; 15:3206-3218.
33. Shastry BS. Further support for the common variants in complement factor H (Y402H) and LOC387715 (A69S) genes as major risk factors for the exudative age-related macular degeneration. Ophthalmologica. 2006;220:291-295.
34. Kanda A, Chen W, Othman M, et al. A variant of mitochondrial protein LOC387715/ARMS2, not HTRA1, is strongly associated with age-related macular degeneration. Proc Natl Acad Sci U S A. 2007;104:16227-16232.
35. Zarbin MA. Current concepts in the pathogenesis of age-related macular degeneration. Arch Ophthalmol. 2004;122:598-614.
36. Zhou J, Jang YP, Kim SR, Sparrow JR. Complement activation by photooxidation products of A2E, a lipofuscin constituent of the retinal pigment epithelium. Proc Natl Acad Sci U S A. 2006;103: 16182-16187.
37. Donoso LA, Kim D, Frost A, Callahan A, Hageman G. The role of inflammation in the pathogenesis of age-related macular degeneration. Surv Ophthalmol. 2006;51:137-152.
38. Shen JK, Dong A, Hackett SF, Bell WR, Green WR, Campochiaro PA. Oxidative damage in age-related macular degeneration. Histol Histopathol. 2007;22:1301-1308.
39. Li LX, Turner JE. Inherited retinal dystrophy in the RCS rat: prevention of photoreceptor degeneration by pigment epithelial cell transplantation. Exp Eye Res. 1988;47:911-917.
40. Pinilla I, Cuenca N, Sauve Y, Wang S, Lund RD. Preservation of outer retina and its synaptic connectivity following subretinal injections of human RPE cells in the Royal College of Surgeons rat.Exp Eye Res. 2007;85:381-392.
41. Algvere PV, Gouras P, Dafgard Kopp E. Long-term outcome of RPE allografts in non-immunosuppressed patients with AMD. Eur J Ophthalmol. 1999;9:217-230.
42. Binder S, Krebs I, Hilgers RD, et al. Outcome of transplantation of autologous retinal pigment epithelium in age-related macular degeneration: a prospective trial. Invest Ophthalmol Vis Sci. 2004; 45:4151-4160.
43. Tezel TH, Del Priore LV, Berger AS, Kaplan HJ. Adult retinal pigment epithelial transplantation in exudative age-related macular degeneration. Am J Ophthalmol. 2007;143:584-595.
44. da Cruz L, Chen FK, Ahmado A, Greenwood J, Coffey P. RPE transplantation and its role in retinal disease. Prog Retin Eye Res. 2007;26:598-635.
45. Joussen AM, Joeres S, Fawzy N, et al. Autologous translocation of the choroid and retinal pigment epithelium in patients with geographic atrophy. Ophthalmology. 2007;114:551-560.
46. Joussen AM, Heussen FM, Joeres S, et al. Autlogous translocation of the choroid and retinal pigment epithelium in age-related macular degeneration. Am J Ophthalmol. 2006;142:17-30.
47. Tsukahara I, Ninomiya S, Castellarin A, Yagi F, Sugino IK, Zarbin MA. Early attachment of uncultured retinal pigment epithelium from aged donors onto Bruch's membrane explants. Exp Eye Res. 2002;74:255-266.
48. Gullapalli VK, Sugino IK, Van Patten Y, Shah S, Zarbin MA. Impaired RPE survival on aged submacular human Bruch's membrane. Exp Eye Res. 2005;80:235-248.
49. Booij JC, Baas DC, Beisekeeva J, Gorgels TG, Bergen AA. The dynamic nature of Bruch's membrane. Prog Retin Eye Res. 2010; 29:1-18.
50. Pauleikhoff D, Wojteki S, Muller D, Bornfeld N, Heiligenhaus A. Adhesive properties of basal membranes of Bruch's membrane: immunohistochemical studies of age-dependent changes in adhesive molecules and lipid deposits (in German). Ophthalmologe. 2000;97:243-250.
51. Del Priore LV, Geng L, Tezel TH, Kaplan HJ. Extracellular matrix ligands promote RPE attachment to inner Bruch's membrane. Curr Eye Res. 2002;25:79-89.
52. Tezel TH, Del Priore LV, Kaplan HJ. Reengineering of aged Bruch's membrane to enhance retinal pigment epithelium repopulation. Invest Ophthalmol Vis Sci. 2004;45:3337-3348.
53. Wang H, Van Patten Y, Sugino IK, Zarbin MA. Migration and proliferation of retinal pigment epithelium on extracellular matrix ligands. J Rehabil Res Devel. 2006;43:713-722.
54. Song MK, Lui GM. Propagation of fetal human RPE cells: preservation of original culture morphology after serial passage. J Cell Physiol. 1990;143:196-203.
55. Castellarin AA, Sugino IK, Vargas JA, Parolini B, Lui GM, Zarbin MA. In vitro transplantation of fetal human retinal pigment epithelial cells onto human cadaver Bruch's membrane. Exp Eye Res. 1998;66:49-67.
56. Zarbin MA. Analysis of retinal pigment epithelium integrin expression and adhesion to aged submacular human Bruch's membrane. Trans Am Ophthalmol Soc. 2003;101:499-520.
57. Gullapalli VK, Sugino IK, Van Patten Y, Shah S, Zarbin MA. Retinal pigment epithelium resurfacing of aged submacular human Bruch's membrane. Trans Am Ophthalmol Soc. 2004;102:123-137. discussion 137-128.
58. Sarks S, Cherepanoff S, Killingsworth M, Sarks J. Relationship of Basal laminar deposit and membranous debris to the clinical presentation of early age-related macular degeneration. Invest Ophthalmol Vis Sci. 2007;48:968-977.
59. Zheng X, Baker H, Hancock WS, Fawaz F, McCaman M, Pungor E Jr. Proteomic analysis for the assessment of different lots of fetal bovine serum as a raw material for cell culture, Part IV: application of proteomics to the manufacture of biological drugs. Biotechnol Prog. 2006;22:1294-1300.
60. Itaya H, Gullapalli V, Sugino IK, Tamai M, Zarbin MA. Iris pigment epithelium attachment to aged submacular human Bruch's membrane. Invest Ophthalmol Vis Sci. 2004;45:4520-4528.
61. Gullapalli VK, Sugino IK, Zarbin MA. Culture-induced increase in alpha integrin subunit expression in retinal pigment epithelium is important for improved resurfacing of aged human Bruch's membrane. Exp Eye Res. 2008;86:189-200.
62. Leonard DS, Sugino IK, Zhang XG, et al. Ultrastructural analysis of hydraulic and abrasive retinal pigment epithelial cell debridements. Exp Eye Res. 2003;76:473-491.
63. Underwood PA, Bennett FA. The effect of extracellular matrix molecules on the in vitro behavior of bovine endothelial cells. Exp Cell Res. 1993;205:311-319.
64. Gamm DM, Wang S, Lu B, et al. Protection of visual functions by human neural progenitors in a rat model of retinal disease. PLoS ONE. 2007;2:e338.
65. Lund RD, Wang S, Klimanskaya I, et al. Human embryonic stem cell-derived cells rescue visual function in dystrophic RCS rats. Cloning Stem Cells. 2006;8:189-199.
66. Lund RD, Wang S, Lu B, et al. Cells isolated from umbilical cord tissue rescue photoreceptors and visual functions in a rodent model of retinal disease. Stem Cells. 2007;25:602-611.
67. Lawrence JM, Keegan DJ, Muir EM, et al. 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.
68. Schraermeyer U, Kociok N, Heimann K. Rescue effects of IPE transplants in RCS rats: short-term results. Invest Ophthalmol Vis Sci. 1999;40:1545-1556.
69. Schraermeyer U, Kayatz P, Thumann G, et al. Transplantation of iris pigment epithelium into the choroid slows down the degeneration of photoreceptors in the RCS rat. Graefes Arch Clin Exp Ophthalmol. 2000;238:979-984.
70. Campochiaro PA, Hackett SF. Corneal endothelial cell matrix promotes expression of differentiated features of retinal pigmented epithelial cells: implication of laminin and basic fibroblast growth factor as active components. Exp Eye Res. 1993;57:539-547.
71. Kamei M, Kawasaki A, Tano Y. Analysis of extracellular matrix synthesis during wound healing of retinal pigment epithelial cells. Microsc Res Tech. 1998;42:311-316.
72. Campochiaro PA, Jerdon JA, Glaser BM The extracellular matrix of human retinal pigment epithelial cells in vivo and its synthesis in vitro. Invest Ophthalmol Vis Sci. 1986;27:1615-1621.
73. Newsome DA, Pfeffer BA, Hewitt AT, Robey PG, Hassell JR. Detection of extracellular matrix molecules synthesized in vitro by monkey and human retinal pigment epithelium: influence of donor age and multiple passages. Exp Eye Res. 1988;46:305-321.
74. Liu X, Ye X, Yanoff M, Li W. Extracellular matrix of retinal pigment epithelium regulates choriocapillaris endothelial survival in vitro. Exp Eye Res. 1997;65:117-126.
75. An E, Lu X, Flippin J, et al. Secreted proteome profiling in human RPE cell cultures derived from donors with age related maculardegeneration and age matched healthy donors. J Proteome Res. 2006;5:2599-2610.
76. An E, Sen S, Park SK, Gordish-Dressman H, Hathout Y. Identification of novel substrates for the serine protease HTRA1 in the human RPE secretome. Invest Ophthalmol Vis Sci. 2010;51:3379-3386.
77. Martini B, Pandey R, Ogden TE, Ryan SJ. Cultures of human retinal pigment epithelium. Modulation of extracellular matrix. Invest Ophthalmol Vis Sci. 1992;33:516-521.
78. Tseng SC, Savion N, Gospodarowicz D, Stern R. Characterization of collagens synthesized by cultured bovine corneal endothelial cells. J Biol Chem. 1981;256:3361-3365.
79. Kay EP, Oh S. Modulation of type III collagen synthesis in bovine corneal endothelial cells. Invest Ophthalmol Vis Sci. 1988;29:200-207.
80. Plenz GA, Deng MC, Robenek H, Volker W. Vascular collagens: spotlight on the role of type VIII collagen in atherogenesis. Atherosclerosis. 2003;166:1-11.
81. Sawada H, Konomi H, Hirosawa K. Characterization of the collagen in the hexagonal lattice of Descemet's membrane: its relation to type VIII collagen. J Cell Biol. 1990;110:219-227.
82. Levy SG, Moss J, Sawada H, Dopping-Hepenstal PJ, McCartney AC. The composition of wide-spaced collagen in normal and diseased Descemet's membrane. Curr Eye Res. 1996;15:45-52.
83. Thumann G, Schraermeyer U, Bartz-Schmidt KU, Heimann K. Descemet's membrane as membranous support in RPE/IPE transplantation. Curr Eye Res. 1997;16:1236-1238.
84. Shaw LM, Olsen BR. FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci. 1991;16:191-194.
85. Sawada H, Furthmayr H, Konomi H, Nagai Y. Immunoelectronmicroscopic localization of extracellular matrix components produced by bovine corneal endothelial cells in vitro. Exp Cell Res. 1987;171:94-109.
86. Klein R, Knudtson MD, Klein BE, et al. Inflammation, complement factor h, and age-related macular degeneration the multiethnic study of atherosclerosis. Ophthalmology. 2008;115: 1742-1749.
87. Klein R. Overview of progress in the epidemiology of age-related macular degeneration. Ophthalmic Epidemiol. 2007;14:184-187.
88. Klein R, Klein BE, Knudtson MD, et al. Prevalence of age-related macular degeneration in 4 racial/ethnic groups in the multi-ethnicstudy of atherosclerosis. Ophthalmology. 2006;113:373-380.
89. Chang MA, Bressler SB, Munoz B, West SK. Racial differences and other risk factors for incidence and progression of age-related macular degeneration: Salisbury Eye Evaluation (SEE) Project. Invest Ophthalmol Vis Sci. 2008;49:2395-2402.
90. Friedman DS, Katz J, Bressler NM, Rahmani B, Tielsch JM. Racial differences in the prevalence of age-related macular degeneration: the Baltimore Eye Survey. Ophthalmology. 1999; 106:1049-1055.
91. Bressler SB, Munoz B, Solomon SD, West SK. Racial differences in the prevalence of age-related macular degeneration: the Salisbury Eye Evaluation (SEE) Project. Arch Ophthalmol. 2008;126:241-245.