A protocol for the culture and differentiation of highly polarized human retinal pigment epithelial cells
Open accessAbstract
We provide our detailed, standardized in vitro protocol for the culture and differentiation of human retinal pigment epithelial (RPE) cells into a highly polarized and functional monolayer. Disruption of the polarized RPE function plays an important role in the pathogenesis of common blinding disorders of the retina. The availability of this polarized RPE monolayer allows for reproducible evaluation of RPE function, modeling of RPE dysfunction in retinal disease and in vitro evaluation of new therapies. The protocol, which takes approximately 6 weeks to complete, describes the culture of RPE from human fetal donor eyes, the differentiation of these cells into a polarized monolayer with high transepithelial resistance and morphologic characteristics that mimic the RPE monolayer in vivo. By modifying the procedure for initial isolation of pure RPE cells and the culture conditions used in existing protocols, we have established a standardized protocol that provides highly reproducible RPE monolayers from the same donor eye.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Human fetal RPE cultures have a high trans-epithelial electrical resistance (TER), from 500 to over 800 Ω cm2.
“These cultures also have a high trans-epithelial electrical resistance (TER), from 500 to over 800 Ω cm2 (Hu and Bok, 2001; Maminishkis et al., 2006; Sonoda et al., 2009).”
From The cell biology of the retinal pigment epithelium (2020) · cites this paper as Sonoda et al., 2009
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Stevenson, B. R., Siliciano, J. D., Mooseker, M. S., & Goodenough, D. A. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.103.3.755 · Cited by 1,640 · see citing works
ARPE-19, A Human Retinal Pigment Epithelial Cell Line with Differentiated Properties
Dunn, K. C., Aotaki-Keen, A. E., Putkey, F. R., & Hjelmeland, L. M. (1996) · Experimental Eye Research · doi:10.1006/exer.1996.0020 · Cited by 1,334 · see citing works
Morphogenesis of the Polarized Epithelial Cell Phenotype
Rodriguez-Boulan, E. J., & Nelson, W. J. (1989) · Science · doi:10.1126/science.2672330 · Cited by 1,085 · see citing works
Tight junctions and the molecular basis for regulation of paracellular permeability
Anderson, J. M., & Itallie, C. M. V. (1995) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1995.269.4.g467 · Cited by 844 · see citing works
Blaauwgeers, H. G. T., Holtkamp, G. M., Rutten, H., Witmer, A. N., Koolwijk, P., Partanen, T. A., Alitalo, K. K., Kroon, M. E., Kijlstra, A., van Hinsbergh, V. W. M., et al. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65138-3 · Cited by 520 · see citing works
Maminishkis, A., Chen, S., Jalickee, S., Banzon, T., Shi, G., Wang, F. E., Ehalt, T., Hammer, J. A., & Miller, S. S. (2006) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.05-1622 · Cited by 401 · see citing works
Ohno‐Matsui, K., Morita, I., Tombran‐Tink, J., Mrazek, D., Onodera, M., Uetama, T., Hayano, M., Murota, S., & Mochizuki, M. (2001) · Journal of Cellular Physiology · doi:10.1002/jcp.10026 · Cited by 261 · see citing works
Role of the retinal pigment epithelium in macular disease.
Hogan, M. J. (1972) · PubMed · Cited by 248 · see citing works
Hu, J. G., & Bok, D. (2001) · PubMed · Cited by 165 · see citing works
Philp, N. J., Wang, D., Yoon, H., & Hjelmeland, L. M. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.02-0287 · Cited by 163 · see citing works
The effect of metabolic inhibitors on retinal adhesion and subretinal fluid resorption.
Marmor, M. F., Abdul-Rahim, A. S., & Cohen, D. S. (1980) · PubMed · Cited by 147 · see citing works
Polarized secretion of IL-6 and IL-8 by human retinal pigment epithelial cells
Holtkamp, G. M., van Rossem, M., de Vos, A. F., Willekens, B., Peek, R., & Kijlstra, A. (1998) · Clinical & Experimental Immunology · doi:10.1046/j.1365-2249.1998.00560.x · Cited by 146 · see citing works
Polarity and the development of the outer blood-retinal barrier.
Rizzolo, L. J. (1997) · PubMed · Cited by 139 · see citing works
Ion transport mechanisms in native human retinal pigment epithelium.
Quinn, R. H., & Miller, S. S. (1992) · PubMed · Cited by 138 · see citing works
Kannan, R., Zhang, N., Sreekumar, P. G., Spee, C. K., Rodriguez, A., Barrón, E., & Hinton, D. R. (2006) · PubMed · Cited by 121 · see citing works
Self-citationHamel, C., Tsilou, E. T., Harris, E., Pfeffer, B. A., Hooks, J. J., Detrick, B., & Redmond, T. M. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490340406 · Cited by 117 · see citing works
Fluid transport across retinal pigment epithelium is inhibited by cyclic AMP.
Miller, S. S., Hughes, B. A., & Machen, T. E. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.6.2111 · Cited by 106 · see citing works
Control of Chemokine Gradients by the Retinal Pigment Epithelium
Shi, G., Maminishkis, A., Banzon, T., Jalickee, S., Li, R., Hammer, J., & Miller, S. S. (2008) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.08-1816 · Cited by 102 · see citing works
Regulation of RPE intercellular junction integrity and function by hepatocyte growth factor.
Jin, M., Barrón, E., He, S., Ryan, S. J., & Hinton, D. R. (2002) · PubMed · Cited by 88 · see citing works
Self-citationImproved uranyl acetate staining for electron microscopy
Tandler, B. (1990) · Journal of Electron Microscopy Technique · doi:10.1002/jemt.1060160110 · Cited by 80 · see citing works
Geisen, P., McColm, J. R., King, B., & Hartnett, M. E. (2006) · Current Eye Research · doi:10.1080/02713680600837408 · Cited by 74 · see citing works
Beta adrenergic receptors on cultured human retinal pigment epithelium.
Frambach, D. A., Fain, G., Farber, D. B., & Bok, D. (1990) · PubMed · Cited by 67 · see citing works
A culture model of development reveals multiple properties of RPE tight junctions.
Ban, Y., & Rizzolo, L. J. (1997) · PubMed · Cited by 60 · see citing works
Immunocytochemical localization of Na+,K(+)-ATPase in rat retinal pigment epithelial cells.
Okami, T., Yamamoto, A., Omori, K., Takada, T., Uyama, M., & Tashiro, Y. (1990) · Journal of Histochemistry & Cytochemistry · doi:10.1177/38.9.2167328 · Cited by 56 · see citing works
Characterization of Brimonidine Transport in Retinal Pigment Epithelium
Zhang, N., Kannan, R., Okamoto, C. T., Ryan, S. J., Lee, V. H. L., & Hinton, D. R. (2005) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.05-0189 · Cited by 46 · see citing works
Self-citationEffects of RPE-cell factors secreted from permselective fibers on retinal cells in vitro
Sheedlo, H. J., Li, L., & Turner, J. E. (1992) · Brain Research · doi:10.1016/0006-8993(92)91015-7 · Cited by 42 · see citing works
German, O. L., Buzzi, E. D., Rotstein, N. P., Rodríguez‐Boulan, E., & Politi, L. E. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21813 · Cited by 40 · see citing works
Cell Biology of the Retinal Pigment Epithelium
Thumann, G., Hoffmann, S., & Hinton, D. R. (2006) · Elsevier eBooks · doi:10.1016/b978-0-323-02598-0.50013-6 · Cited by 39 · see citing works
Self-citationN -(4-hydroxyphenyl) Retinamide Augments Laser-Induced Choroidal Neovascularization in Mice
Sreekumar, P. G., Zhou, J., Sohn, J., Spee, C. K., Ryan, S. J., Maurer, B. J., Kannan, R., & Hinton, D. R. (2008) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.07-0667 · Cited by 27 · see citing works
Self-citationSenanayake, P. D., Calabro, A. R., Nishiyama, K., Hu, J. G., Bok, D., & Hollyfield, J. G. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.1.199 · Cited by 26 · see citing works
Sonoda, S., Sreekumar, P. G., Spee, C., Ryan, S. J., Kannan, R., & Hinton, D. R. (2008) · Investigative Ophthalmology & Visual Science · Cited by 1 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Derivation of functional retinal pigmented epithelium from induced pluripotent stem cells
Buchholz, D. E., Hikita, S. T., Rowland, T. J., Friedrich, A. M., Hinman, C. R., Johnson, L. V., & Clegg, D. O. (2009) · Stem Cells · doi:10.1002/stem.189 · Cited by 417 · see citing works
The cell biology of the retinal pigment epithelium
Lakkaraju, A., Umapathy, A., Tan, L. X., Daniele, L., Philp, N. J., Boesze-Battaglia, K., & Williams, D. S. (2020) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100846 · Cited by 422 · see citing works
The oil spill in ageing Bruch membrane
Curcio, C. A., Johnson, M. F., Rudolf, M., & Huang, J.-D. (2011) · British Journal of Ophthalmology · doi:10.1136/bjophthalmol-2011-300344 · Cited by 392 · see citing works
Achberger, K., Probst, C., Haderspeck, J., Bolz, S., Rogal, J., Chuchuy, J., Nikolova, M., Cora, V., Antkowiak, L., Haq, W., et al. (2019) · eLife · doi:10.7554/elife.46188 · Cited by 380 · see citing works
Kanow, M. A., Giarmarco, M. M., Jankowski, C. S., Tsantilas, K., Engel, A. L., Du, J., Linton, J. D., Farnsworth, C. C., Sloat, S. R., Rountree, A., et al. (2017) · eLife · doi:10.7554/elife.28899 · Cited by 377 · see citing works
Soft Drusen in Age-Related Macular Degeneration: Biology and Targeting Via the Oil Spill Strategies
Curcio, C. A. (2018) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.18-24882 · Cited by 319 · see citing works
EMT and EndMT: Emerging Roles in Age-Related Macular Degeneration
Shu, D. Y., Butcher, E. R., & Saint‐Geniez, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124271 · Cited by 293 · see citing works
Cholesterol in the retina: The best is yet to come
Pikuleva, I. A., & Curcio, C. A. (2014) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2014.03.002 · Cited by 282 · see citing works
Understanding photoreceptor outer segment phagocytosis: use and utility of RPE cells in culture
Mazzoni, F., Safa, H., & Finnemann, S. C. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.01.010 · Cited by 221 · see citing works
Singh, R., Shen, W., Kuai, D., Martin, J., Guo, X., Smith, M. A., Perez, E. T., Phillips, M., Simonett, J. M., Wallace, K., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/dds469 · Cited by 221 · see citing works
Sreekumar, P. G., Kannan, R., Kitamura, M., Spee, C. K., Barrón, E., Ryan, S. J., & Hinton, D. R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012578 · Cited by 207 · see citing works
Self-citationStem cell based therapies for age-related macular degeneration: The promises and the challenges
Nazari, H. K., Zhang, L., Zhu, D., Chader, G. J., Falabella, P., Stefanini, F. R., Rowland, T. J., Clegg, D., Kashani, A. H., Hinton, D. R., et al. (2015) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2015.06.004 · Cited by 207 · see citing works
Self-citationFerrington, D. A., Ebeling, M. C., Kapphahn, R. J., Terluk, M. R., Fisher, C. R., Polanco, J. R., Roehrich, H., Leary, M. M., Geng, Z., Dutton, J. R., et al. (2017) · Redox Biology · doi:10.1016/j.redox.2017.05.015 · Cited by 182 · see citing works
Sreekumar, P. G., Ishikawa, K., Spee, C., Mehta, H. H., Wan, J., Yen, K., Cohen, P., Kannan, R., & Hinton, D. R. (2016) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.15-17053 · Cited by 179 · see citing works
Self-citationRole of epithelial–mesenchymal transition in proliferative vitreoretinopathy
Tamiya, S., & Kaplan, H. J. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.02.008 · Cited by 160 · see citing works
Vaajasaari, H., Ilmarinen, T., Juuti‐Uusitalo, K., Rajala, K. M., Onnela, N., Narkilahti, S., Suuronen, R., Hyttinen, J., Uusitalo, H. M. T., & Skottman, H. (2011) · PubMed Central · Cited by 152 · see citing works
Xiang, P., Wu, K., Zhu, Y., Xiang, L., Li, C., Chen, D.-L., Chen, F., Xu, G., Wang, A., Li, M., et al. (2014) · Biomaterials · doi:10.1016/j.biomaterials.2014.08.040 · Cited by 143 · see citing works
Functional Analysis of Serially Expanded Human iPS Cell-Derived RPE Cultures
Singh, R., Phillips, M. J., Kuai, D., Meyer, J., Martin, J. M., Smith, M. A., Perez, E. T., Shen, W., Wallace, K. A., Capowski, E. E., et al. (2013) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.13-11943 · Cited by 136 · see citing works
Golestaneh, N., Chu, Y., Cheng, S. K., Cao, H., Poliakov, E., & Berinstein, D. M. (2016) · Journal of Translational Medicine · doi:10.1186/s12967-016-1101-8 · Cited by 127 · see citing works
Plasma membrane protein polarity and trafficking in RPE cells: past, present and future
Lehmann, G. L., Benedicto, I., Philp, N. J., & Rodriguez-Boulan, E. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.04.021 · Cited by 122 · see citing works
Zhu, D., Deng, X., Spee, C. K., Sonoda, S., Hsieh, C., Barrón, E., Pera, M. F., & Hinton, D. R. (2010) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.10-6413 · Cited by 119 · see citing works
Self-citationImplications of melanin binding in ocular drug delivery
Rimpelä, A., Reinisalo, M., Hellinen, L., Grazhdankin, E., Kidron, H., Urtti, A. O., & del Amo, E. M. (2017) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2017.12.008 · Cited by 119 · see citing works
Reductive carboxylation is a major metabolic pathway in the retinal pigment epithelium
Du, J., Yanagida, A., Knight, K., Engel, A. L., Vo, A. H., Jankowski, C. S. R., Sadı́lek, M., Tran, V., Manson, M. A., Ramakrishnan, A., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604572113 · Cited by 113 · see citing works
Isolation, culture and characterization of primary mouse RPE cells
Fernández‐Godino, R., Garland, D. L., & Pierce, E. A. (2016) · Nature Protocols · doi:10.1038/nprot.2016.065 · Cited by 106 · see citing works
Succinate Can Shuttle Reducing Power from the Hypoxic Retina to the O2-Rich Pigment Epithelium
Bisbach, C. M., Hass, D. T., Robbings, B. M., Rountree, A. M., Sadı́lek, M., Sweet, I. R., & Hurley, J. B. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107606 · Cited by 103 · see citing works
Miyagishima, K. J., Wan, Q., Corneo, B., Sharma, R., Lotfi, M., Boles, N. C., Hua, F., Maminishkis, A., Zhang, C., Blenkinsop, T. A., et al. (2016) · Stem Cells Translational Medicine · doi:10.5966/sctm.2016-0037 · Cited by 102 · see citing works
Glutathione Metabolism and the Novel Role of Mitochondrial GSH in Retinal Degeneration
Sreekumar, P. G., Ferrington, D. A., & Kannan, R. (2021) · Antioxidants · doi:10.3390/antiox10050661 · Cited by 103 · see citing works
Self-citationAhmado, 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., et al. (2011) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.10-6374 · Cited by 100 · see citing works
Thaker, S. K., Chapa, T. J., Garcia, G., Gong, D., Schmid, E. W., Arumugaswami, V., Sun, R., & Christofk, H. R. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.01.024 · Cited by 97 · see citing works
The culture and maintenance of functional retinal pigment epithelial monolayers from adult human eye
Blenkinsop, T. A., Salero, E., Stern, J. H., & Temple, S. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-125-7_4 · Cited by 96 · see citing works
Ghosh, S., Shang, P., Terasaki, H., Stepicheva, N. A., Hose, S., Yazdankhah, M., Weiss, J., Sakamoto, T., Bhutto, I. A., Xia, S., et al. (2018) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.18-24132 · Cited by 96 · see citing works
Self-citationChao, J. R., Knight, K., Engel, A. L., Jankowski, C. S. R., Wang, Y., Manson, M. A., Gu, H., Djukovic, D., Raftery, D., Hurley, J. B., et al. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.788422 · Cited by 93 · see citing works
Bharti, K., den Hollander, A. I., Lakkaraju, A., Sinha, D., Williams, D. S., Finnemann, S. C., Rickman, C. B., Malek, G., & D'Amore, P. A. (2022) · Experimental Eye Research · doi:10.1016/j.exer.2022.109170 · Cited by 92 · see citing works
Sonoda, S., Sreekumar, P. G., Kase, S., Spee, C. K., Ryan, S. J., Kannan, R., & Hinton, D. R. (2009) · Aging · doi:10.18632/aging.100111 · Cited by 92 · see citing works
Self-citationNasonkin, I. O., Merbs, S. L., Lazo, K., Oliver, V. F., Brooks, M., Patel, K., Enke, R. A., Nellissery, J. K., Jamrich, M., Le, Y. Z., et al. (2013) · Development · doi:10.1242/dev.086603 · Cited by 90 · see citing works
Flores‐Bellver, M., Mighty, J., Aparicio‐Domingo, S., Li, K. V., Shi, C., Zhou, J., Cobb, H., McGrath, P. S., Michelis, G., Lenhart, P., et al. (2021) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12165 · Cited by 87 · see citing works
The cultivation of human retinal pigment epithelial cells on Bombyx mori silk fibroin
Shadforth, A. M. A., George, K. A., Kwan, A., Chirilă, T. V., & Harkin, D. G. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.02.040 · Cited by 90 · see citing works
Proline mediates metabolic communication between retinal pigment epithelial cells and the retina
Yam, M., Engel, A. L., Wang, Y., Zhu, S., Hauer, A., Zhang, R., Lohner, D., Huang, J., Dinterman, M., Zhao, C., et al. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.007983 · Cited by 89 · see citing works
Blenkinsop, T. A., Saini, J. S., Maminishkis, A., Bharti, K., Wan, Q., Banzon, T. M., Lotfi, M., Davis, J. A., Singh, D., Rizzolo, L. J., et al. (2015) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.14-16246 · Cited by 87 · see citing works
Li, Y., Wu, W.-H., Hsu, C.-W., Nguyen, H. V., Tsai, Y., Chan, L., Nagasaki, T., Maumenee, I. H., Yannuzzi, L. A., Hoang, Q. V., et al. (2014) · Molecular Therapy · doi:10.1038/mt.2014.100 · Cited by 84 · see citing works
A local complement response by RPE causes early-stage macular degeneration
Fernandez-Godino, R., Garland, D. L., & Pierce, E. A. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv287 · Cited by 73 · see citing works
Kay, P., Yang, Y. C., & Paraoan, L. (2013) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12070 · Cited by 81 · see citing works
Fronk, A., & Vargis, E. (2016) · Journal of Tissue Engineering · doi:10.1177/2041731416650838 · Cited by 81 · see citing works
Differentiation Therapy: Targeting Human Renal Cancer Stem Cells with Interleukin 15
Azzi, S., Bruno, S., Giron‐Michel, J., Clay, D., Devocelle, A., Croce, M., Ferrini, S., Chouaı̈b, S., Vázquez, A., Charpentier, B., et al. (2011) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djr451 · Cited by 79 · see citing works
Ishikawa, K., He, S., Terasaki, H., Nazari, H. K., Zhang, H., Spee, C. K., Kannan, R., & Hinton, D. R. (2015) · Scientific Reports · doi:10.1038/srep16386 · Cited by 79 · see citing works
Self-citationYe, F., Kaneko, H., Hayashi, Y., Takayama, K., Hwang, S.-J., Nishizawa, Y., Kimoto, R., Nagasaka, Y., Tsunekawa, T., Matsuura, T., et al. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.02.027 · Cited by 78 · see citing works
Protection of Retina by αB Crystallin in Sodium Iodate Induced Retinal Degeneration
Zhou, P., Kannan, R., Spee, C. K., Sreekumar, P. G., Dou, G., & Hinton, D. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098275 · Cited by 77 · see citing works
Self-citationCell Models to Study Regulation of Cell Transformation in Pathologies of Retinal Pigment Epithelium
Kuznetsova, A. V., Kurinov, A. M., & Aleksandrova, M. A. (2014) · Journal of Ophthalmology · doi:10.1155/2014/801787 · Cited by 77 · see citing works
Minasyan, L., Sreekumar, P. G., Hinton, D. R., & Kannan, R. (2017) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2017/1675230 · Cited by 77 · see citing works
Self-citationZahabi, A., Shahbazi, E., Ahmadieh, H., Hassani, S., Totonchi, M., Taei, A., Masoudi, N., Ebrahimi, M., Aghdami, N., Seifinejad, A., et al. (2011) · Stem Cells and Development · doi:10.1089/scd.2011.0599 · Cited by 74 · see citing works
Lee, J. G., & Kay, E. P. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.11-9102 · Cited by 74 · see citing works
Toops, K. A., Tan, L. X., & Lakkaraju, A. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.05.003 · Cited by 73 · see citing works
Adijanto, J., & Philp, N. J. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.01.015 · Cited by 73 · see citing works
Using human induced pluripotent stem cells to treat retinal disease
Borooah, S., Phillips, M. J., Bilican, B., Wright, A. F., Wilmut, I., Chandran, S., Gamm, D. M., & Dhillon, B. (2013) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.09.002 · Cited by 71 · see citing works
Fernández‐Godino, R., Bujakowska, K. M., & Pierce, E. A. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx392 · Cited by 71 · see citing works
Alves, C. H., Fernandes, R., Santiago, A. R., & Ambrósio, A. F. (2020) · Cells · doi:10.3390/cells9051217 · Cited by 71 · see citing works
Cellular models and therapies for age-related macular degeneration
Forest, D. L., Johnson, L. V., & Clegg, D. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.017236 · Cited by 69 · see citing works
TNF-α disrupts morphologic and functional barrier properties of polarized retinal pigment epithelium
Shirasawa, M., Sonoda, S., Terasaki, H., Arimura, N., Otsuka, H., Yamashita, T., Uchino, E., Hisatomi, T., Ishibashi, T., & Sakamoto, T. (2013) · Experimental Eye Research · doi:10.1016/j.exer.2013.02.012 · Cited by 68 · see citing works
Self-citationHazim, R. A., Karumbayaram, S., Jiang, M., Dimashkie, A., Lopes, V. S., Li, D., Burgess, B. L., Vijayaraj, P., Alva-Ornelas, J. A., Zack, J. A., et al. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0652-9 · Cited by 66 · see citing works
Shiose, S., Chen, Y., Okano, K., Roy, S., Kohno, H., Tang, J. C. O., Pearlman, E. M., Maeda, T., Palczewski, K., & Maeda, A. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.228551 · Cited by 64 · see citing works
Zhang, C., Xie, H., Yang, Q., Yang, Y., Li, W., Tian, H., Lü, L., Wang, F., Xu, J., Gao, F., et al. (2019) · Clinical and Experimental Ophthalmology · doi:10.1111/ceo.13619 · Cited by 65 · see citing works
Hsiung, J., Zhu, D., & Hinton, D. R. (2014) · Stem Cells Translational Medicine · doi:10.5966/sctm.2014-0205 · Cited by 61 · see citing works
Self-citationαB-Crystallin Regulates Subretinal Fibrosis by Modulation of Epithelial-Mesenchymal Transition
Ishikawa, K., Sreekumar, P. G., Spee, C. K., Nazari, H. K., Zhu, D., Kannan, R., & Hinton, D. R. (2016) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.11.014 · Cited by 61 · see citing works
Self-citationAbnormal mTORC1 signaling leads to retinal pigment epithelium degeneration
Huang, J., Gu, S., Chen, M., Zhang, S., Jiang, Z., Chen, X., Jiang, C., Liu, G., Radu, R. A., Sun, X., et al. (2019) · Theranostics · doi:10.7150/thno.26281 · Cited by 60 · see citing works
Zou, H., Shan, C., Ma, L., Liu, J., Yang, N., & Zhao, J. (2020) · PeerJ · doi:10.7717/peerj.10136 · Cited by 59 · see citing works
Xu, J., Zhu, D., Sonoda, S., He, S., Spee, C. K., Ryan, S. J., & Hinton, D. R. (2012) · Angiogenesis · doi:10.1007/s10456-012-9254-4 · Cited by 55 · see citing works
Self-citationLi, Y., Zhang, Y., Xu, Y. H., Kittredge, A., Ward, N., Chen, S., Tsang, S. H., & Yang, T. (2017) · eLife · doi:10.7554/elife.29914 · Cited by 54 · see citing works
Sreekumar, P. G., Spee, C. K., Ryan, S. J., Cole, S. P. C., Kannan, R., & Hinton, D. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033420 · Cited by 54 · see citing works
Self-citationRetinal pigment epithelium (RPE) cytoskeleton in vivo and in vitro
Bonilha, V. L. (2013) · Experimental Eye Research · doi:10.1016/j.exer.2013.09.015 · Cited by 52 · see citing works
Wang, W., Sreekumar, P. G., Valluripalli, V., Shi, P., Wang, J., Lin, Y., Cui, H., Kannan, R., Hinton, D. R., & MacKay, J. A. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.04.028 · Cited by 52 · see citing works
Self-citationSreekumar, P. G., Li, Z., Wang, W., Spee, C. K., Hinton, D. R., Kannan, R., & MacKay, J. A. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.05.014 · Cited by 52 · see citing works
Self-citationInhibition of PVR with a Tyrosine Kinase Inhibitor, Dasatinib, in the Swine
Umazume, K., Liu, L., Scott, P. A., de Castro, J. P. F., McDonald, K., Kaplan, H. J., & Tamiya, S. (2013) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-10418 · Cited by 51 · see citing works
Foltz, L. P., & Clegg, D. (2017) · Journal of Visualized Experiments · doi:10.3791/56274 · Cited by 51 · see citing works
Terasaki, H., Kase, S., Shirasawa, M., Otsuka, H., Hisatomi, T., Sonoda, S., Ishida, S., Ishibashi, T., & Sakamoto, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0069994 · Cited by 50 · see citing works
Self-citationGonçalves, S., Rodrigues, I. P., Padrão, J., Silva, J. P., Sencadas, V., Lanceros-Méndez, S., Girão, H., Gama, M., Dourado, F. O. Q., & Rodrigues, L. R. (2015) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2015.11.051 · Cited by 50 · see citing works
Pelkonen, L., Sato, K., Reinisalo, M., Kidron, H., Tachikawa, M., Watanabe, M., Uchida, Y., Urtti, A. O., & Terasaki, T. (2017) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.6b00782 · Cited by 50 · see citing works
Replication ofMycobacterium Tuberculosisin Retinal Pigment Epithelium
Nazari, H. K., Karakousis, P. C., & Rao, N. A. (2014) · JAMA Ophthalmology · doi:10.1001/jamaophthalmol.2014.270 · Cited by 49 · see citing works
Villarroel, M., García‐Ramírez, M., Corraliza, L., Hernández, C., & Simó, R. (2011) · Diabetologia · doi:10.1007/s00125-011-2089-5 · Cited by 47 · see citing works
Liu, Y., Zhang, D., Yong-pei, W., & Ji, B. (2014) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2014.07.016 · Cited by 47 · see citing works
A TGF-β receptor 1 inhibitor for prevention of proliferative vitreoretinopathy
Nassar, K., Grisanti, S., Tura, A., Lüke, J., Lüke, M., Soliman, M. M., & Grisanti, S. (2014) · Experimental Eye Research · doi:10.1016/j.exer.2014.04.006 · Cited by 45 · see citing works
Wang, S., Du, S., Wu, Q., Hu, J., & Li, T. (2015) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.14-15874 · Cited by 44 · see citing works
Shadforth, A. M. A., Suzuki, S., Theodoropoulos, C., Richardson, N. A., Chirilă, T. V., & Harkin, D. G. (2015) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2089 · Cited by 44 · see citing works
TGF-β2 secretion from RPE decreases with polarization and becomes apically oriented
Hirsch, L., Nazari, H. K., Sreekumar, P. G., Kannan, R., Dustin, L., Zhu, D., Barrón, E., & Hinton, D. R. (2014) · Cytokine · doi:10.1016/j.cyto.2014.11.014 · Cited by 43 · see citing works
Self-citationChen, C.-Y., Melo, E., Jakob, P., Friedlein, A., Elsässer, B., Goettig, P., Küppers, V., Delobel, F., Stucki, C., Dunkley, T. P. J., et al. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.03.013 · Cited by 43 · see citing works
Zhu, D., Sreekumar, P. G., Hinton, D. R., & Kannan, R. (2009) · Vision Research · doi:10.1016/j.visres.2009.09.002 · Cited by 41 · see citing works
Self-citationProliferative Vitreoretinopathy in the Swine–A New Model
Umazume, K., Barak, Y., McDonald, K., Liu, L., Kaplan, H. J., & Tamiya, S. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-9768 · Cited by 42 · see citing works
Emri, E., Körtvely, E., Dammeier, S., Klose, F., Simpson, D. A. C., den Hollander, A. I., Ueffing, M., & Lengyel, I. (2020) · Nutrients · doi:10.3390/nu12103051 · Cited by 41 · see citing works
Sreekumar, P. G., Reddy, S. T., Hinton, D. R., & Kannan, R. (2022) · Experimental Eye Research · doi:10.1016/j.exer.2021.108918 · Cited by 41 · see citing works
Self-citationSonoporation Enhances Chemotherapeutic Efficacy in Retinoblastoma Cells In Vitro
Lee, N. G., Berry, J. L., Lee, T. C., Wang, A. T., Honowitz, S., Murphree, A. L., Varshney, N., Hinton, D. R., & Fawzi, A. A. (2011) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.10-6501 · Cited by 40 · see citing works
Self-citationHashida, N., & Nishida, K. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.114870 · Cited by 37 · see citing works
Advances in retinal pigment epithelial cell transplantation for retinal degenerative diseases
Liu, H., Huang, S. S., Gopal, L., Kai, D., Su, X., & Liu, Z. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-04007-5 · Cited by 38 · see citing works
Soluble EphB4 Inhibition of PDGF-Induced RPE Migration In Vitro
He, S., Kumar, S. R., Zhou, P., Krasnoperov, V. G., Ryan, S. J., Gill, P. S., & Hinton, D. R. (2010) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.09-3475 · Cited by 38 · see citing works
Self-citationUmazume, K., Tsukahara, R., Liu, L., de Castro, J. P. F., McDonald, K., Kaplan, H. J., & Tamiya, S. (2014) · American Journal Of Pathology · doi:10.1016/j.ajpath.2014.01.022 · Cited by 37 · see citing works
Advances in Retinal Tissue Engineering
Trese, M. G. J., Regatieri, C. V., & Young, M. J. (2012) · Materials · doi:10.3390/ma5010108 · Cited by 37 · see citing works
Chambers, C., Soo, G. L., Engel, A. L., Glass, I. A., Frassetto, A., Martini, P. G. V., & Cherry, T. J. (2024) · Translational Vision Science & Technology · doi:10.1167/tvst.13.7.7 · Cited by 36 · see citing works
Human embryonic stem cell applications for retinal degenerations
Reynolds, J. C., & Lamba, D. A. (2013) · Experimental Eye Research · doi:10.1016/j.exer.2013.07.010 · Cited by 36 · see citing works
Recent advances in drug and nutrient transport across the blood-retinal barrier
Kubo, Y., Akanuma, S., & Hosoya, K. (2018) · Expert Opinion on Drug Metabolism & Toxicology · doi:10.1080/17425255.2018.1472764 · Cited by 36 · see citing works
Namba, R., Kaneko, H., Suzumura, A., Shimizu, H., Kataoka, K., Takayama, K., Yamada, K., Funahashi, Y., Ito, S., Nonobe, N., et al. (2019) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.19-26788 · Cited by 36 · see citing works
Ye, K., Takemoto, Y., Ito, A., Onda, M., Morimoto, N., Mandai, M., Takahashi, M., Kato, R., & Osakada, F. (2020) · Scientific Reports · doi:10.1038/s41598-020-70979-y · Cited by 36 · see citing works
Modulation of MCT3 Expression during Wound Healing of the Retinal Pigment Epithelium
Gallagher‐Colombo, S. M., Maminishkis, A., Tate, S., Grunwald, G. B., & Philp, N. J. (2010) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.09-5028 · Cited by 36 · see citing works
- Authors
- Sonoda, S., Spee, C., Barron, E., Ryan, S. J., Kannan, R., & Hinton, D. R.
- Affiliations
- University of Southern California (US)
- Corresponding author
- Hinton, David R
- Venue
- Nature Protocols
- Published
- 2009-04-16
- Volume
- 4
- Issue
- 5
- Pages
- 662-673
- ISSN
- 1750-2799 (ISSN-L)
- 1754-2189
- PMC
- PMC2688697
- OpenAlex
- W2045731328
- Cited by
- 272
- References
- 31
- Citations by year
- 2026: 4 · 2025: 12 · 2024: 15 · 2023: 12 · 2022: 17 · 2021: 19 · 2020: 17 · 2019: 15 · 2018: 20 · 2017: 29 · 2016: 17 · 2015: 24 · 2014: 23 · 2013: 11 · 2012: 12
- FWCI
- 12.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Protocols (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Eye Institute (P30EY003040, #EY03040, R01EY001545, EY01545)
- Topics
- Health Sciences › Medicine › Ophthalmology › Retinal Diseases and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Retinal Imaging and Analysis
- Keywords
- retinal pigment epithelial cells, cell polarization, cell differentiation, transepithelial electrical resistance, retinal disease modeling, in vitro disease model
- MeSH terms
- Cell Differentiation, Cells, Cultured, Culture Media, Dissection, Humans, Tissue Donors, Cell Polarity, Cell Culture Techniques, Retinal Pigment Epithelium
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review