Retinal pigment epithelium (RPE) cytoskeleton invivo and invitro

Experimental Eye Research

Volumn 126, Issue , 2014, Pages 38-45

  Bonilha, Vera L ^a  

^a CLEVELAND CLINIC LERNER COLLEGE OF MEDICINE   (United States)

Author keywords

Cytoskeleton; Polarity; Retinal pigment epithelium

Indexed keywords

ALPHA ACTININ; MYOSIN; TROPOMYOSIN; VILLIN; VINCULIN;

ACTIN FILAMENT; CELL JUNCTION; CELL MOTILITY; CYTOSKELETON; EUKARYOTIC FLAGELLUM; IN VITRO STUDY; IN VIVO STUDY; MICROTUBULE; MICROVILLUS; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

CYTOSKELETON; POLARITY; RETINAL PIGMENT EPITHELIUM;

ACTINS; ANIMALS; CELL POLARITY; CELLS, CULTURED; CYTOSKELETON; HUMANS; MICROTUBULE PROTEINS; RETINAL PIGMENT EPITHELIUM;

EID: 84906502802     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2013.09.015     Document Type: Review

References (85)

1. Ablonczy Z., Crosson C.E. VEGF modulation of retinal pigment epithelium resistance. Exp. Eye Res. 2007, 85:762-771.
2. Ablonczy Z., Dahrouj M., Tang P.H., Liu Y., Sambamurti K., Marmorstein A.D., Crosson C.E. Human retinal pigment epithelium cells as functional models for the RPE invivo. Investig. Ophthalmol. Vis. Sci. 2011, 52:8614-8620.
3. Ahmado A., Carr A.J., Vugler A.A., Semo M., Gias C., Lawrence J.M., Chen L.L., Chen F.K., Turowski P., da Cruz L., Coffey P.J. Induction of differentiation by pyruvate and DMEM in the human retinal pigment epithelium cell line ARPE-19. Investig. Ophthalmol. Vis. Sci. 2011, 52:7148-7159.
4. Alge C.S., Hauck S.M., Priglinger S.G., Kampik A., Ueffing M. Differential protein profiling of primary versus immortalized human RPE cells identifies expression patterns associated with cytoskeletal remodeling and cell survival. J.Proteome Res. 2006, 5:862-878.
5. Alge C.S., Suppmann S., Priglinger S.G., Neubauer A.S., May C.A., Hauck S., Welge-Lussen U., Ueffing M., Kampik A. Comparative proteome analysis of native differentiated and cultured dedifferentiated human RPE cells. Investig. Ophthalmol. Vis. Sci. 2003, 44:3629-3641.
6. Allen R.A. Isolated cilia in inner retinal neurons and in retinal pigment epithelium. J.Ultrastruct. Res. 1965, 12:730-747.
7. Arikawa K., Williams D.S. Alpha-actinin and actin in the outer retina: a double immunoelectron microscopic study. Cell Motil. Cytoskelet. 1991, 18:15-25.
8. Bacallao R., Antony C., Dotti C., Karsenti E., Stelzer E.H., Simons K. The subcellular organization of Madin-Darby canine kidney cells during the formation of a polarized epithelium. J.Cell Biol. 1989, 109:2817-2832.
9. Blaauwgeers H.G., Holtkamp G.M., Rutten H., Witmer A.N., Koolwijk P., Partanen T.A., Alitalo K., Kroon M.E., Kijlstra A., van Hinsbergh V.W., Schlingemann R.O. Polarized vascular endothelial growth factor secretion by human retinal pigment epithelium and localization of vascular endothelial growth factor receptors on the inner choriocapillaris. Evidence for a trophic paracrine relation. Am. J. Pathol. 1999, 155:421-428.
10. Blenkinsop T.A., Salero E., Stern J.H., Temple S. The culture and maintenance of functional retinal pigment epithelial monolayers from adult human eye. Methods Mol. Biol. 2013, 945:45-65.
11. Bok D. Retinal photoreceptor-pigment epithelium interactions. Friedenwald lecture. Investig. Ophthalmol. Vis. Sci. 1985, 26:1659-1694.
12. Bonilha V.L., Bhattacharya S.K., West K.A., Sun J., Crabb J.W., Rayborn M.E., Hollyfield J.G. Proteomic characterization of isolated retinal pigment epithelium microvilli. Mol. Cell Proteomics 2004, 3:1119-1127.
13. Bonilha V.L., Finnemann S.C., Rodriguez-Boulan E. Ezrin promotes morphogenesis of apical microvilli and basal infoldings in retinal pigment epithelium. J.Cell Biol. 1999, 147:1533-1548.
14. Bonilha V.L., Marmorstein A.D., Cohen-Gould L., Rodriguez-Boulan E. Apical sorting of influenza hemagglutinin by transcytosis in retinal pigment epithelium. J.Cell Sci. 1997, 110:1717-1727.
15. Bonilha V.L., Rodriguez-Boulan E. Polarity and developmental regulation of two PDZ proteins in the retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 2001, 42:3274-3282.
16. Breckler J., Burnside B. Myosin-I in retinal pigment epithelial cells. Investig. Ophthalmol. Vis. Sci. 1994, 35:2489-2499.
17. Burke J.M., Cao F., Irving P.E. High levels of E-/P-cadherin: correlation with decreased apical polarity of Na/K ATPase in bovine RPE cells in situ. Investig. Ophthalmol. Vis. Sci. 2000, 41:1945-1952.
18. Burke J.M., Skumatz C.M., Irving P.E., McKay B.S. Phenotypic heterogeneity of retinal pigment epithelial cells invitro and in situ. Exp. Eye Res. 1996, 62:63-73.
19. Burnside B., Bost-Usinger L. The retinal pigment epithelium cytoskeleton. The Retinal Pigment Epithelium 1998, 41-67. Oxford University Press, New York. J.F. Marmor, T.J. Wolfensberger (Eds.).
20. Chen M., Muckersie E., Robertson M., Fraczek M., Forrester J.V., Xu H. Characterization of a spontaneous mouse retinal pigment epithelial cell line B6-RPE07. Investig. Ophthalmol. Vis. Sci. 2008, 49:3699-3706.
21. Daniele L.L., Adams R.H., Durante D.E., Pugh E.N., Philp N.J. Novel distribution of junctional adhesion molecule-C in the neural retina and retinal pigment epithelium. J.Comp. Neurol. 2007, 505:166-176.
22. Devaul N., Wang R., Sperry A.O. PPP1R42, a PP1 binding protein, regulates centrosome dynamics in ARPE-19 cells. Biol. Cell. 2013, 105:359-371.
23. Drenckhahn D., Wagner H.J. Relation of retinomotor responses and contractile proteins in vertebrate retinas. Eur. J. Cell Biol. 1985, 37:156-168.
24. Dunn K.C., Aotaki-Keen A.E., Putkey F.R., Hjelmeland L.M. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 1996, 62:155-169.
25. Dunn K.C., Marmorstein A.D., Bonilha V.L., Rodriguez-Boulan E., Giordano F., Hjelmeland L.M. Use of the ARPE-19 cell line as a model of RPE polarity: basolateral secretion of FGF5. Investig. Ophthalmol. Vis. Sci. 1998, 39:2744-2749.
26. Economopoulou M., Hammer J., Wang F., Fariss R., Maminishkis A., Miller S.S. Expression, localization, and function of junctional adhesion molecule-C (JAM-C) in human retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 2009, 50:1454-1463.
27. Esser P., Grisanti S., Kociok N., Abts H., Hueber A., Unfried K., Heimann K., Weller M. Expression and upregulation of microtubule-associated protein 1B in cultured retinal pigment epithelial cells. Investig. Ophthalmol. Vis. Sci. 1997, 38:2852-2856.
28. Fisher S.K., Steinberg R.H. Origin and organization of pigment epithelial apical projections to cones in cat retina. J. Comp. Neurol. 1982, 206:131-145.
29. Ford K.M., D'Amore P.A. Molecular regulation of vascular endothelial growth factor expression in the retinal pigment epithelium. Mol. Vis. 2012, 18:519-527.
30. Geisen P., McColm J.R., King B.M., Hartnett M.E. Characterization of barrier properties and inducible VEGF expression of several types of retinal pigment epithelium in medium-term culture. Curr. Eye Res. 2006, 31:739-748.
31. Ghossoub R., Hu Q., Failler M., Rouyez M.C., Spitzbarth B., Mostowy S., Wolfrum U., Saunier S., Cossart P., Jamesnelson W., Benmerah A. Septins 2, 7 and 9 and MAP4 colocalize along the axoneme in the primary cilium and control ciliary length. J.Cell Sci. 2013, 126:2583-2594.
32. Gibbs D., Azarian S.M., Lillo C., Kitamoto J., Klomp A.E., Steel K.P., Libby R.T., Williams D.S. Role of myosin VIIa and Rab27a in the motility and localization of RPE melanosomes. J.Cell Sci. 2004, 117:6473-6483.
33. Gibbs D., Diemer T., Khanobdee K., Hu J., Bok D., Williams D.S. Function of MYO7A in the human RPE and the validity of shaker1 mice as a model for Usher syndrome 1B. Investig. Ophthalmol. Vis. Sci. 2010, 51:1130-1135.
34. Goncalves J., Nolasco S., Nascimento R., Lopez Fanarraga M., Zabala J.C., Soares H. TBCCD1, a new centrosomal protein, is required for centrosome and golgi apparatus positioning. Embo Rep. 2010, 11:194-200.
35. Grisanti S., Guidry C. Transdifferentiation of retinal pigment epithelial cells from epithelial to mesenchymal phenotype. Investig. Ophthalmol. Vis. Sci. 1995, 36:391-405.
36. Gu X., Neric N.J., Crabb J.S., Crabb J.W., Bhattacharya S.K., Rayborn M.E., Hollyfield J.G., Bonilha V.L. Age-related changes in the retinal pigment epithelium (RPE). PLoS One 2012, 7:e38673.
37. Gundersen D., Orlowski J., Rodriguez-Boulan E. Apical polarity of Na, K-ATPase in retinal pigment epithelium is linked to a reversal of the ankyrin-fodrin submembrane cytoskeleton. J.Cell Biol. 1991, 112:863-872.
38. Holtkamp G.M., Van Rossem M., de Vos A.F., Willekens B., Peek R., Kijlstra A. Polarized secretion of IL-6 and IL-8 by human retinal pigment epithelial cells. Clin. Exp. Immunol. 1998, 112:34-43.
39. 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.
40. Hunt R.C., Davis A.A. Altered expression of keratin and vimentin in human retinal pigment epithelial cells invivo and invitro. J.Cell Physiol. 1990, 145:187-199.
41. Irons M.J., Kalnins V.I. Distribution of microtubules in cultured RPE cells from normal and dystrophic RCS rats. Investig. Ophthalmol. Vis. Sci. 1984, 25:434-439.
42. Kivela T., Jaaskelainen J., Vaheri A., Carpen O. Ezrin, a membrane-organizing protein, as a polarization marker of the retinal pigment epithelium in vertebrates. Cell Tissue Res. 2000, 301:217-223.
43. Kivela T., Uusitalo M. Structure, development and function of cytoskeletal elements in non-neuronal cells of the human eye. Prog. Retin. Eye Res. 1998, 17:385-428.
44. Klomp A.E., Teofilo K., Legacki E., Williams D.S. Analysis of the linkage of MYRIP and MYO7A to melanosomes by RAB27A in retinal pigment epithelial cells. Cell Motil. Cytoskelet. 2007, 64:474-487.
45. Kreitzer G., Marmorstein A., Okamoto P., Vallee R., Rodriguez-Boulan E. Kinesin and dynamin are required for post-Golgi transport of a plasma-membrane protein. Nat. Cell Biol. 2000, 2:125-127.
46. Kreitzer G., Schmoranzer J., Low S.H., Li X., Gan Y., Weimbs T., Simon S.M., Rodriguez-Boulan E. Three-dimensional analysis of post-Golgi carrier exocytosis in epithelial cells. Nat. Cell Biol. 2003, 5:126-136.
47. Lin-Jones J., Sohlberg L., Dose A., Breckler J., Hillman D.W., Burnside B. Identification and localization of myosin superfamily members in fish retina and retinal pigmented epithelium. J.Comp. Neurol. 2009, 513:209-223.
48. Liu X., Vansant G., Udovichenko I.P., Wolfrum U., Williams D.S. Myosin VIIa, the product of the Usher 1B syndrome gene, is concentrated in the connecting cilia of photoreceptor cells. Cell Motil. Cytoskelet. 1997, 37:240-252.
49. Maminishkis A., Chen S., Jalickee S., Banzon T., Shi G., Wang F.E., Ehalt T., Hammer J.A., Miller S.S. Confluent monolayers of cultured human fetal retinal pigment epithelium exhibit morphology and physiology of native tissue. Investig. Ophthalmol. Vis. Sci. 2006, 47:3612-3624.
50. Mannermaa E., Reinisalo M., Ranta V.P., Vellonen K.S., Kokki H., Saarikko A., Kaarniranta K., Urtti A. Filter-cultured ARPE-19 cells as outer blood-retinal barrier model. Eur. J. Pharm. Sci. 2010, 40:289-296.
51. McKay B.S., Burke J.M. Separation of phenotypically distinct subpopulations of cultured human retinal pigment epithelial cells. Exp. Cell Res. 1994, 213:85-92.
52. Meng W., Takeichi M. Adherens junction: molecular architecture and regulation. Cold Spring Harb. Perspect. Biol. 2009, 1:a002899.
53. Musch A., Cohen D., Kreitzer G., Rodriguez-Boulan E. cdc42 regulates the exit of apical and basolateral proteins from the trans-Golgi network. Embo J. 2001, 20:2171-2179.
54. Nabi I.R., Mathews A.P., Cohen-Gould L., Gundersen D., Rodriguez-Boulan E. Immortalization of polarized rat retinal pigment epithelium. J.Cell Sci. 1993, 104:37-49.
55. Nasonkin I.O., Merbs S.L., Lazo K., Oliver V.F., Brooks M., Patel K., Enke R.A., Nellissery J., Jamrich M., Le Y.Z., Bharti K., Fariss R.N., Rachel R.A., Zack D.J., Rodriguez-Boulan E.J., Swaroop A. Conditional knockdown of DNA methyltransferase 1 reveals a key role of retinal pigment epithelium integrity in photoreceptor outer segment morphogenesis. Development 2013, 140:1330-1341.
56. Nawrot M., West K., Huang J., Possin D.E., Bretscher A., Crabb J.W., Saari J.C. Cellular retinaldehyde-binding protein interacts with ERM-binding phosphoprotein 50 in retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 2004, 45:393-401.
57. Nishiyama K., Sakaguchi H., Hu J.G., Bok D., Hollyfield J.G. Claudin localization in cilia of the retinal pigment epithelium. Anat. Rec. 2002, 267:196-203.
58. Opas M. The focal adhesions of chick retinal pigmented epithelial cells. Can. J. Biochem. Cell Biol. 1985, 63:553-563.
59. Opas M. Expression of the differentiated phenotype by epithelial cells invitro is regulated by both biochemistry and mechanics of the substratum. Dev. Biol. 1989, 131:281-293.
60. Opas M. Substratum mechanics and cell differentiation. Int. Rev. Cytol. 1994, 150:119-137.
61. Opas M., Dziak E. Effects of substrata and method of tissue dissociation on adhesion, cytoskeleton, and growth of chick retinal pigmented epithelium invitro. InVitro Cell Dev. Biol. 1988, 24:885-892.
62. Owaribe K., Eguchi G. Increase in actin contents and elongation of apical projections in retinal pigmented epithelial cells during development of the chicken eye. J.Cell Biol. 1985, 101:590-596.
63. Owaribe K., Kartenbeck J., Rungger-Brandle E., Franke W.W. Cytoskeletons of retinal pigment epithelial cells: interspecies differences of expression patterns indicate independence of cell function from the specific complement of cytoskeletal proteins. Cell Tissue Res. 1988, 254:301-315.
64. Philp N.J., Nachmias V.T. Components of the cytoskeleton in the retinal pigmented epithelium of the chick. J.Cell Biol. 1985, 101:358-362.
65. Philp N.J., Wang D., Yoon H., Hjelmeland L.M. Polarized expression of monocarboxylate transporters in human retinal pigment epithelium and ARPE-19 cells. Investig. Ophthalmol. Vis. Sci. 2003, 44:1716-1721.
66. Philp N.J., Yoon M.Y., Hock R.S. Identification and localization of talin in chick retinal pigment epithelial cells. Exp. Eye Res. 1990, 51:191-198.
67. ++-switch induction of RPE differentiation. Exp. Eye Res. 2006, 82:648-656.
68. Rizzolo L.J., Chen X., Weitzman M., Sun R., Zhang H. Analysis of the RPE transcriptome reveals dynamic changes during the development of the outer blood-retinal barrier. Mol. Vis. 2007, 13:1259-1273.
69. Rizzolo L.J., Joshi H.C. Apical orientation of the microtubule organizing center and associated gamma-tubulin during the polarization of the retinal pigment epithelium invivo. Dev. Biol. 1993, 157:147-156.
70. +, K(+)-ATPase and 5A11 antigen in apical microvilli of the retinal pigment epithelium is unrelated to alpha-spectrin. J.Cell Sci. 1995, 108(Pt 11):3623-3633.
71. Rodriguez-Boulan E., Kreitzer G., Musch A. Organization of vesicular trafficking in epithelia. Nat. Rev. Mol. Cell Biol. 2005, 6:233-247.
72. Rohlich P. The interphotoreceptor matrix: electron microscopic and histochemical observations on the vertebrate retina. Exp. Eye Res. 1970, 10:80-86.
73. Ruiz-Loredo A.Y., Lopez-Colome A.M. New insights into the regulation of myosin light chain phosphorylation in retinal pigment epithelial cells. Int. Rev. Cell Mol. Biol. 2012, 293:85-121.
74. Ryhanen T., Viiri J., Hyttinen J.M., Uusitalo H., Salminen A., Kaarniranta K. Influence of Hsp90 and HDAC inhibition and tubulin acetylation on perinuclear protein aggregation in human retinal pigment epithelial cells. J.Biomed. Biotechnol. 2011, 2011:1-8.
75. Slomiany M.G., Rosenzweig S.A. IGF-1-induced VEGF and IGFBP-3 secretion correlates with increased HIF-1 alpha expression and activity in retinal pigment epithelial cell line D407. Investig. Ophthalmol. Vis. Sci. 2004, 45:2838-2847.
76. Soni L.E., Warren C.M., Bucci C., Orten D.J., Hasson T. The unconventional myosin-VIIa associates with lysosomes. Cell Motil. Cytoskelet. 2005, 62:13-26.
77. Sonoda S., Spee C., Barron E., Ryan S.J., Kannan R., Hinton D.R. Aprotocol for the culture and differentiation of highly polarized human retinal pigment epithelial cells. Nat. Protoc. 2009, 4:662-673.
78. Sun R., Peng S., Chen X., Zhang H., Rizzolo L.J. Diffusible retinal secretions regulate the expression of tight junctions and other diverse functions of the retinal pigment epithelium. Mol. Vis. 2008, 14:2237-2262.
79. Topp K.S., Bisla K., Saks N.D., Lavail J.H. Centripetal transport of herpes simplex virus in human retinal pigment epithelial cells invitro. Neuroscience 1996, 71:1133-1144.
80. Tsukita S., Furuse M., Itoh M. Multifunctional strands in tight junctions. Nat. Rev. Mol. Cell Biol. 2001, 2:285-293.
81. Turksen K., Kalnins V.I. The cytoskeleton of chick retinal pigment epithelial cells in situ. Cell Tissue Res. 1987, 248:95-101.
82. Vaughan D.K., Fisher S.K. The distribution of F-actin in cells isolated from vertebrate retinas. Exp. Eye Res. 1987, 44:393-406.
83. Wheelock M.J., Knudsen K.A., Johnson K.R. Membrane-cytoskeleton interactions with cadherin cell adhesion proteins: roles of catenins as linker proteins. Curr. Top. Membr. 1996, 43:169-185.
84. Wittig D., Wang X., Walter C., Gerdes H.H., Funk R.H., Roehlecke C. Multi-level communication of human retinal pigment epithelial cells via tunneling nanotubes. PLoS One 2012, 7:e33195.
85. Zhang N., Kannan R., Okamoto C.T., Ryan S.J., Lee V.H., Hinton D.R. Characterization of brimonidine transport in retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 2006, 47:287-294.