Engineering a blood-retinal barrier with human embryonic stem cell-derived retinal pigment epithelium: Transcriptome and functional analysis

Stem Cells Translational Medicine

Volumn 2, Issue 7, 2013, Pages 534-544

  Peng, Shaomin ^a,b   Gan, Geliang ^a   Qiu, Caihong ^a   Zhong, Mei ^a   An, Hongyan ^a   Adelman, Ron A ^a   Rizzolo, Lawrence J ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b THE SECOND AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Blood retinal barrier; Claudins; Embryonic stem cells; Retinal pigmented epithelium

Indexed keywords

CLAUDIN; CLAUDIN 19; CLAUDIN 3; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ARTICLE; BLOOD RETINA BARRIER; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; PERMEABILITY; PHOTORECEPTOR; PIGMENT EPITHELIUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; TIGHT JUNCTION; TISSUE ENGINEERING;

ANIMALIA;

EID: 84879719538     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.5966/sctm.2012-0134     Document Type: Article

References (45)

1. Barishak YR. Embryology of the Eye and Its Adnexa. 2nd rev. ed. Basel, Switzerland: Karger, 2001.
2. Stroeva OG, Mitashov VI. Retinal pigment epithelium: Proliferation and differentiation during development and regeneration. Int Rev Cytol 1983;83:221-293.
3. Rizzolo LJ, Peng S, Luo Y et al. Integration of tight junctions and claudins with the barrier functions of the retinal pigment epithelium. Prog Retin Eye Res 2011;30:296-323.
4. Kiser PD, Golczak M, Maeda A et al. Key enzymes of the retinoid (visual) cycle in vertebrate retina. Biochim Biophys Acta 2012;1821:137-151.
5. Kevany BM, Palczewski K. Phagocytosis of retinal rod and cone photoreceptors. Physiology 2010;25:8-15.
6. Marmor MF, Wolfensberger TJ. The Retinal Pigment Epithelium: Function and Disease. New York, NY: Oxford University Press, 1998.
7. Schwartz SD, Hubschman JP, Heilwell G et al. Embryonic stem cell trials for macular degeneration: A preliminary report. Lancet 2012; 379:713-720.
8. Liao J-L, Yu J, Huang K et al. Molecular signature of primary retinal pigment epithelium and stem-cell-derived RPE cells. Hum Mol Genet 2010;19:4229-4238.
9. Strunnikova NV, Maminishkis A, Barb JJ et al. Transcriptome analysis and molecular signature of human retinal pigment epithelium. Hum Mol Genet 2010;19:2468-2486.
10. Bharti K, Miller SS, Arnheiter H. The new paradigm: Retinal pigment epithelium cells generated from embryonic or induced pluripotent stem cells. Pigment Cell Melanoma Res 2011;24:21-34.
11. Vugler A, Carr AJ, Lawrence J et al. Elucidating the phenomenon of hESC-derived RPE: Anatomy of cell genesis, expansion and retinal transplantation. Exp Neurol 2008;214:347-361.
12. Carr AJ, Vugler A, Lawrence J et al. Molecular characterization and functional analysis of phagocytosis by human embryonic stem cell-derived RPE cells using a novel human retinal assay. Mol Vis 2009;15:283-295.
13. Carr A-J, Vugler AA, Hikita ST et al. Protective effects of human iPS-derived retinal pigment epithelium cell transplantation in the retinal dystrophic rat. PLoS One 2009;4:e8152.
14. Peng S, Adelman RA, Rizzolo LJ. Minimal effects of VEGF and anti-VEGF drugs on the permeability or selectivity of RPE tight junctions. Invest Ophthalmol Vis Sci 2010;51:3216-3225.
15. Peng S, Rao VS, Adelman RA et al. Claudin-19 and the barrier properties of the human retinal pigment epithelium. Invest Ophthalmol Vis Sci 2011;52:1392-1403.
16. Peng S, Gan G, Rao VS et al. Effects of proinflammatory cytokines on the claudin-19 rich tight junctions of human retinal pigment epithelium. Invest Ophthalmol Vis Sci 2012;53: 5016-5028.
17. Cereijido M, Contreras RG, Shoshani L et al. Tight junction and polarity interaction in the transporting epithelial phenotype. Biochim Biophys Acta 2008;1778:770-793.
18. Elkouby-Naor L, Ben-Yosef T. Functions of claudin tight junction proteins and their complex interactions in various physiological systems. Int Rev Cell Mol Biol 2010;279:1-32.
19. Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu Rev Physiol 2006;68:403-429.
20. Rizzolo LJ, Chen X, Weitzman M et al. Analysis of the RPE transcriptome reveals dynamic changes during the development of the outer blood-retinal barrier. Mol Vis 2007;13: 1259-1273.
21. Sun R, Peng S, Chen X et al. Diffusible retinal secretions regulate the expression of tight junctions and other diverse functions of the retinal pigment epithelium. Mol Vis 2008; 14:2237-2262.
22. Konrad M, Schaller A, Seelow D et al. Mutations in the tight-junction gene claudin 19 (CLDN19) are associated with renal magnesium wasting, renal failure, and severe ocular involvement. Am J Hum Genet 2006;79:949-957.
23. Rizzolo LJ. Development and role of tight junctions in the retinal pigment epithelium. Int Rev Cytol 2007;258:195-234.
24. Gamm DM, Melvan JN, Shearer RL et al. A novel serum-free method for culturing human prenatal retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 2008;49: 788-799.
25. Gamm DM, Wright LS, Capowski EE et al. Regulation of prenatal human retinal neurosphere growth and cell fate potential by retinal pigment epithelium and Mash1. STEM CELLS 2008;26:3182-3193.
26. Maminishkis A, Chen S, Jalickee S et al. Confluent monolayers of cultured human fetal retinal pigment epithelium exhibit morphology and physiology of native tissue. Invest Ophthalmol Vis Sci 2006;47:3612-3624.
27. Idelson M, Alper R, Obolensky A et al. Directed differentiation of human embryonic stem cells into functional retinal pigment epithelium cells. Cell Stem Cell 2009;5:396-408.
28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T) method. Methods 2001;25:402-408.
29. Kimizuka H, Koketsu K. Ion transport through cell membrane. J Theor Biol 1964;6: 290-305.
30. Yu AS, Cheng MH, Angelow S et al. Molecular basis for cation selectivity in claudin-2-based paracellular pores: Identification of an electrostatic interaction site. J Gen Physiol 2009;133:111-127.
31. Quinn RH, Miller SS. Ion transport mechanisms in native human retinal pigment epithelium. Invest Ophthalmol Vis Sci 1992;33: 3513-3527.
32. Burke JM. Epithelial phenotype and the RPE: Is the answer blowing in the Wnt? Prog Retin Eye Res 2008;27:579-595.
33. Grunwald GB. Cadherin cell adhesion molecules in retinal development and pathology. Prog Retinal Eye Res 1996;15:363-392.
34. Powell DW. Barrier function of epithelia. Am J Physiol 1981;241:G275-G288.
35. Braekevelt CR, Hollenberg MJ. Development of the retinal pigment epithelium, choriocapillaris and Bruch's membrane in the albino rat. Exp Eye Res 1970;9:124-131.
36. Greiner JV, Weidman TA. Comparative histogenesis of Bruch's membrane (complexus basalis). Exp Eye Res 1991;53:47-54.
37. Lutty GA, Hasegawa T, Baba T et al. Development of the human choriocapillaris. Eye (Lond) 2010;24:408-415.
38. Gelse K, Poschl E, Aigner T. Collagens: Structure, function, and biosynthesis. Adv Drug Deliv Rev 2003;55:1531-1546.
39. Nguyen NM, Senior RM. Laminin isoforms and lung development: All isoforms are not equal. Dev Biol 2006;294:271-279.
40. Kim ST, Adair-Kirk TL, Senior RM et al. Functional consequences of cell type-restricted expression of laminin α5 in mouse placental labyrinth and kidney glomerular capillaries. PLoS One 2012;7:e41348.
41. Aisenbrey S, Zhang M, Bacher D et al. Retinal pigment epithelial cells synthesize laminins, including laminin 5, and adhere to them through α3-and α6-containing integrins. Invest Ophthalmol Vis Sci 2006;47: 5537-5544.
42. Rizzolo LJ. Basement membrane stimulates the polarized distribution of integrins but not the Na, K-ATPase in the retinal pigment epithelium. Cell Regul 1991;2:939-949.
43. Phillips MJ, Wallace KA, Dickerson SJ et al. Blood-derived human iPS cells generate optic vesicle-like structures with the capacity to form retinal laminae and develop synapses. Invest Ophthalmol Vis Sci 2012;53: 2007-2019.
44. Eiraku M, Takata N, Ishibashi H et al. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 2011; 472:51-56.
45. Kolomeyer AM, Sugino IK, Zarbin MA. Characterization of conditioned media collected from aged versus young human eye cups. Invest Ophthalmol Vis Sci 2011;52:5963-5972.