A detailed three-step protocol for live imaging of intracellular traffic in polarized primary porcine RPE monolayers

Experimental Eye Research

Volumn 124, Issue , 2014, Pages 74-85

  Toops, Kimberly A ^a,b   Tan, Li Xuan ^a   Lakkaraju, Aparna ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Age related macular degeneration; Culture protocol; Gene expression; Live imaging; Organelle traffic; Polarized monolayers; Retinal diseases; Retinal pigment epithelium

Indexed keywords

ADULT; ANIMAL TISSUE; CELL ACTIVITY; CELL POLARITY; CELL SUSPENSION; CLEARANCE; CLINICAL PROTOCOL; CONFOCAL MICROSCOPE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRIC RESISTANCE; EXPERIMENTAL PIG; FEMALE; FILTERS AND MEMBRANES; GENE EXPRESSION; GENETIC TRANSFECTION; IMAGE ANALYSIS; IMAGING AND DISPLAY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; INTRACELLULAR SPACE; INTRACELLULAR TRAFFIC; LIVE IMAGING; MALE; MORPHOGENESIS; NONHUMAN; PHAGOCYTOSIS; PHOTORECEPTOR OUTER SEGMENT; PIGMENT EPITHELIUM; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL DETECTION; SOLID STATE LASER; SUCROSE GRADIENT; TIGHT JUNCTION; TRANSGENE;

AGE-RELATED MACULAR DEGENERATION; CULTURE PROTOCOL; GENE EXPRESSION; LIVE IMAGING; ORGANELLE TRAFFIC; POLARIZED MONOLAYERS; RETINAL DISEASES; RETINAL PIGMENT EPITHELIUM;

ANIMALS; CELL DIFFERENTIATION; CELL POLARITY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; INTRACELLULAR FLUID; MALE; REPRODUCIBILITY OF RESULTS; RETINAL DEGENERATION; RETINAL PIGMENT EPITHELIUM; SWINE;

EID: 84901784613     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2014.05.003     Document Type: Short Survey

References (62)

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. Adijanto J., Philp N.J. Cultured primary human fetal retinal pigment epithelium (hfRPE) as a model for evaluating RPE metabolism. Exp. Eye Res. 2014 Jan 28, pii: S0014-4835(14)00030-X., (Epub ahead of print) Review. http://dx.doi.org/10.1016/j.exer.2014.01.015.
4. Ambati J., Atkinson J.P., Gelfand B.D. Immunology of age-related macular degeneration. Nat. Rev. Immunol. 2013, 13:438-451.
5. Ambati J., Fowler B.J. Mechanisms of age-related macular degeneration. Neuron 2012, 75:26-39.
6. Ames A., Li Y.Y., Heher E.C., Kimble C.R. Energy metabolism of rabbit retina as related to function: high cost of Na+ transport. J.Neurosci. 1992, 12:840-853.
7. 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.
8. Bok D. The retinal pigment epithelium: a versatile partner in vision. J.Cell Sci. Suppl. 1993, 17:189-195.
9. Bok D. Evidence for an inflammatory process in age-related macular degeneration gains new support. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:7053-7054.
10. Bonilha V.L. Retinal pigment epithelium (RPE) cytoskeleton invivo and invitro. Exp. Eye Res. 2013 Sep 30, pii: S0014-4835(13)00281-9., (Epub ahead of print). http://dx.doi.org/10.1016/j.exer.2013.09.015.
11. Chang C., Wang X., Caldwell R.B. Serum opens tight junctions and reduces ZO-1 protein in retinal epithelial cells. J.Neurochem. 1997, 69:859-867.
12. Chang C.W., Ye L., Defoe D.M., Caldwell R.B. Serum inhibits tight junction formation in cultured pigment epithelial cells. Investig. Ophthalmol. Vis. Sci. 1997, 38:1082-1093.
13. Chew E.C., Liew C.T., Chew S.B., Lee J.C., Hou H.J., Yam H.F., Ho P.C., Ip S.M. The growth and behaviour of pig retinal pigment epithelial cells in culture. Invivo 1993, 7:425-429.
14. Diemer T., Gibbs D., Williams D.S. Analysis of the rate of disk membrane digestion by cultured RPE cells. Adv. Exp. Med. Biol. 2008, 613:321-326.
15. Dintelmann T.S., Heimann K., Kayatz P., Schraermeyer U. Comparative study of ROS degradation by IPE and RPE cells invitro. Graefes Arch. Clin. Exp. Ophthalmol. 1999, 237:830-839.
16. Dithmer M., Fuchs S., Shi Y., Schmidt H., Richert E., Roider J., Klettner A. Fucoidan reduces secretion and expression of vascular endothelial growth factor in the retinal pigment epithelium and reduces angiogenesis invitro. PLoS One 2014, 9:e89150.
17. Drexler H.G., Uphoff C.C. Mycoplasma contamination of cell cultures: incidence, sources, effects, detection, elimination, prevention. Cytotechnology 2002, 39:75-90.
18. Finnemann S.C., Bonilha V.L., Marmorstein A.D., Rodriguez-Boulan E. Phagocytosis of rod outer segments by retinal pigment epithelial cells requires alpha(v)beta5 integrin for binding but not for internalization. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:12932-12937.
19. Finnemann S.C., Leung L.W., Rodriguez-Boulan E. The lipofuscin component A2E selectively inhibits phagolysosomal degradation of photoreceptor phospholipid by the retinal pigment epithelium. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:3842-3847.
20. Francis P.J., Appukuttan B., Simmons E., Landauer N., Stoddard J., Hamon S., Ott J., Ferguson B., Klein M., Stout J.T., Neuringer M. Rhesus monkeys and humans share common susceptibility genes for age-related macular disease. Hum. Mol. Genet. 2008, 17:2673-2680.
21. Fuhrmann S., Zou C., Levine E.M. Retinal pigment epithelium development, plasticity, and tissue homeostasis. Exp. Eye Res. 2013.
22. 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.
23. Gibbs D., Kitamoto J., Williams D.S. Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6481-6486.
24. Gordiyenko N.V., Fariss R.N., Zhi C., MacDonald I.M. Silencing of the CHM gene alters phagocytic and secretory pathways in the retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 2010, 51:1143-1150.
25. Groenen M.A., Archibald A.L., Uenishi H., Tuggle C.K., Takeuchi Y., Rothschild M.F., Rogel-Gaillard C., Park C., Milan D., Megens H.J., Li S., Larkin D.M., Kim H., Frantz L.A., Caccamo M., Ahn H., Aken B.L., Anselmo A., Anthon C., Auvil L., Badaoui B., Beattie C.W., Bendixen C., Berman D., Blecha F., Blomberg J., Bolund L., Bosse M., Botti S., Bujie Z., Bystrom M., Capitanu B., Carvalho-Silva D., Chardon P., Chen C., Cheng R., Choi S.H., Chow W., Clark R.C., Clee C., Crooijmans R.P., Dawson H.D., Dehais P., De Sapio F., Dibbits B., Drou N., Du Z.Q., Eversole K., Fadista J., Fairley S., Faraut T., Faulkner G.J., Fowler K.E., Fredholm M., Fritz E., Gilbert J.G., Giuffra E., Gorodkin J., Griffin D.K., Harrow J.L., Hayward A., Howe K., Hu Z.L., Humphray S.J., Hunt T., Hornshoj H., Jeon J.T., Jern P., Jones M., Jurka J., Kanamori H., Kapetanovic R., Kim J., Kim J.H., Kim K.W., Kim T.H., Larson G., Lee K., Lee K.T., Leggett R., Lewin H.A., Li Y., Liu W., Loveland J.E., Lu Y., Lunney J.K., Ma J., Madsen O., Mann K., Matthews L., McLaren S., Morozumi T., Murtaugh M.P., Narayan J., Nguyen D.T., Ni P., Oh S.J., Onteru S., Panitz F., Park E.W., Park H.S., Pascal G., Paudel Y., Perez-Enciso M., Ramirez-Gonzalez R., Reecy J.M., Rodriguez-Zas S., Rohrer G.A., Rund L., Sang Y., Schachtschneider K., Schraiber J.G., Schwartz J., Scobie L., Scott C., Searle S., Servin B., Southey B.R., Sperber G., Stadler P., Sweedler J.V., Tafer H., Thomsen B., Wali R., Wang J., Wang J., White S., Xu X., Yerle M., Zhang G., Zhang J., Zhang J., Zhao S., Rogers J., Churcher C., Schook L.B. Analyses of pig genomes provide insight into porcine demography and evolution. Nature 2012, 491:393-398.
26. 2O in porcine retinal pigment epithelial cells. Exp. Eye Res. 2003, 76:493-504.
27. Hamel C.P., Tsilou E., Pfeffer B.A., Hooks J.J., Detrick B., Redmond T.M. Molecular cloning and expression of RPE65, a novel retinal pigment epithelium-specific microsomal protein that is post-transcriptionally regulated invitro. J.Biol. Chem. 1993, 268:15751-15757.
28. Hammer M., Richter S., Guehrs K.H., Schweitzer D. Retinal pigment epithelium cell damage by A2-E and its photo-derivatives. Mol. Vis. 2006, 12:1348-1354.
29. 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.
30. Joffre C., Leclere L., Buteau B., Martine L., Cabaret S., Malvitte L., Acar N., Lizard G., Bron A., Creuzot-Garcher C., Bretillon L. Oxysterols induced inflammation and oxidation in primary porcine retinal pigment epithelial cells. Curr. Eye Res. 2007, 32:271-280.
31. Kaida M., Cao F., Skumatz C.M., Irving P.E., Burke J.M. Time at confluence for human RPE cells: effects on the adherens junction and invitro wound closure. Investig. Ophthalmol. Vis. Sci. 2000, 41:3215-3224.
32. Keene C.D., Cudaback E., Li X., Montine K.S., Montine T.J. Apolipoprotein E isoforms and regulation of the innate immune response in brain of patients with Alzheimer's disease. Curr. Opin. Neurobiol. 2011, 21:920-928.
33. Kennedy C.J., Rakoczy P.E., Robertson T.A., Papadimitriou J.M., Constable I.J. Kinetic studies on phagocytosis and lysosomal digestion of rod outer segments by human retinal pigment epithelial cells invitro. Exp. Cell Res. 1994, 210:209-214.
34. Kevany B.M., Palczewski K. Phagocytosis of retinal rod and cone photoreceptors. Physiology (Bethesda) 2010, 25:8-15.
35. Klettner A., Westhues D., Lassen J., Bartsch S., Roider J. Regulation of constitutive vascular endothelial growth factor secretion in retinal pigment epithelium/choroid organ cultures: p38, nuclear factor kappaB, and the vascular endothelial growth factor receptor-2/phosphatidylinositol 3 kinase pathway. Mol. Vis. 2013, 19:281-291.
36. Lakkaraju A. Endo-lysosome function in the retinal pigment epithelium in health and disease. Adv. Exp. Med. Biol. 2012, 723:723-729.
37. Lakkaraju A., Finnemann S.C., Rodriguez-Boulan E. The lipofuscin fluorophore A2E perturbs cholesterol metabolism in retinal pigment epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:11026-11031.
38. Lassota N., Kiilgaard J.F., Prause J.U., Qvortrup K., Scherfig E., la Cour M. Surgical induction of choroidal neovascularization in a porcine model. Graefes Arch. Clin. Exp. Ophthalmol. 2007, 245:1189-1198.
39. Madara J.L. Regulation of the movement of solutes across tight junctions. Annu. Rev. Physiol. 1998, 60:143-159.
40. Mair K.H., Sedlak C., Kaser T., Pasternak A., Levast B., Gerner W., Saalmuller A., Summerfield A., Gerdts V., Wilson H.L., Meurens F. The porcine innate immune system: an update. Dev. Comp. Immunol. 2014.
41. 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.
42. Miura Y., Klettner A., Roider J. VEGF antagonists decrease barrier function of retinal pigment epithelium invitro: possible participation of intracellular glutathione. Investig. Ophthalmol. Vis. Sci. 2010, 51:4848-4855.
43. Molday R.S., Hicks D., Molday L. Peripherin. A rim-specific membrane protein of rod outer segment discs. Investig. Ophthalmol. Vis. Sci. 1987, 28:50-61.
44. Muller C., Mas Gomez N., Ruth P., Strauss O. Ca1.3 L-type channels, maxiK Ca-dependent K channels and bestrophin-1 regulate rhythmic photoreceptor outer segment phagocytosis by retinal pigment epithelial cells. Cell. Signal. 2014, 26:968-978.
45. Nandrot E.F., Kim Y., Brodie S.E., Huang X., Sheppard D., Finnemann S.C. Loss of synchronized retinal phagocytosis and age-related blindness in mice lacking alphavbeta5 integrin. J.Exp. Med. 2004, 200:1539-1545.
46. 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.
47. Petters R.M., Alexander C.A., Wells K.D., Collins E.B., Sommer J.R., Blanton M.R., Rojas G., Hao Y., Flowers W.L., Banin E., Cideciyan A.V., Jacobson S.G., Wong F. Genetically engineered large animal model for studying cone photoreceptor survival and degeneration in retinitis pigmentosa. Nat. Biotechnol. 1997, 15:965-970.
48. Quinn R.H., Miller S.S. Ion transport mechanisms in native human retinal pigment epithelium. Investig. Ophthalmol. Vis. Sci. 1992, 33:3513-3527.
49. Rattner A., Nathans J. Macular degeneration: recent advances and therapeutic opportunities. Nat. Rev. Neurosci. 2006, 7:860-872.
50. Rizzolo L.J. The distribution of Na+,K(+)-ATPase in the retinal pigmented epithelium from chicken embryo is polarized invivo but not in primary cell culture. Exp. Eye Res. 1990, 51:435-446.
51. Rizzolo L.J. Barrier properties of cultured retinal pigment epithelium. Exp. Eye Res. 2014.
52. Ross J.W., Fernandez de Castro J.P., Zhao J., Samuel M., Walters E., Rios C., Bray-Ward P., Jones B.W., Marc R.E., Wang W., Zhou L., Noel J.M., McCall M.A., DeMarco P.J., Prather R.S., Kaplan H.J. Generation of an inbred miniature pig model of retinitis pigmentosa. Investig. Ophthalmol. Vis. Sci. 2012, 53:501-507.
53. Sanchez I., Martin R., Ussa F., Fernandez-Bueno I. The parameters of the porcine eyeball. Graefes Arch. Clin. Exp. Ophthalmol. 2011, 249:475-482.
54. Shaner N.C., Steinbach P.A., Tsien R.Y. Aguide to choosing fluorescent proteins. Nat. Methods 2005, 2:905-909.
55. Shirasawa M., Sonoda S., Terasaki H., Arimura N., Otsuka H., Yamashita T., Uchino E., Hisatomi T., Ishibashi T., Sakamoto T. TNF-alpha disrupts morphologic and functional barrier properties of polarized retinal pigment epithelium. Exp. Eye Res. 2013, 110:59-69.
56. Siliciano J.D., Goodenough D.A. Localization of the tight junction protein, ZO-1, is modulated by extracellular calcium and cell-cell contact in Madin-Darby canine kidney epithelial cells. J.Cell Biol. 1988, 107:2389-2399.
57. Sommer J.R., Estrada J.L., Collins E.B., Bedell M., Alexander C.A., Yang Z., Hughes G., Mir B., Gilger B.C., Grob S., Wei X., Piedrahita J.A., Shaw P.X., Petters R.M., Zhang K. Production of ELOVL4 transgenic pigs: a large animal model for Stargardt-like macular degeneration. Br. J. Ophthalmol. 2011, 95:1749-1754.
58. 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.
59. Strauss O. The retinal pigment epithelium in visual function. Physiol. Rev. 2005, 85:845-881.
60. Terasaki H., Kase S., Shirasawa M., Otsuka H., Hisatomi T., Sonoda S., Ishida S., Ishibashi T., Sakamoto T. TNF-alpha decreases VEGF secretion in highly polarized RPE cells but increases it in non-polarized RPE cells related to crosstalk between JNK and NF-kappaB pathways. PLoS One 2013, 8:e69994.
61. Tian J., Ishibashi K., Honda S., Boylan S.A., Hjelmeland L.M., Handa J.T. The expression of native and cultured human retinal pigment epithelial cells grown in different culture conditions. Br. J. Ophthalmol. 2005, 89:1510-1517.
62. Xu J., Toops K.A., Diaz F., Carvajal-Gonzalez J.M., Gravotta D., Mazzoni F., Schreiner R., Rodriguez-Boulan E., Lakkaraju A. Mechanism of polarized lysosome exocytosis in epithelial cells. J.Cell Sci. 2012, 125:5937-5943.