Retinal disease in ciliopathies: Recent advances with a focus on stem cell-based therapies
Open accessAbstract
Ciliopathies display extensive genetic and clinical heterogeneity, varying in severity, age of onset, disease progression and organ systems affected. Retinal involvement, as demonstrated by photoreceptor dysfunction or death, is a highly penetrant phenotype among a vast majority of ciliopathies. Photoreceptor cells possess a specialized and modified sensory cilium with membrane discs where efficient photon capture and ensuing signaling cascade initiate the visual process. Disruptions of cilia biogenesis and protein transport lead to impairment of photoreceptor function and eventually degeneration. Despite advances in elucidation of ciliogenesis and photoreceptor cilia defects, we have limited understanding of pathogenic mechanisms underlying retinal phenotype(s) observed in human ciliopathies. Patient-derived induced pluripotent stem cell (iPSC)-based approaches offer a unique opportunity to complement studies with model organisms and examine cilia disease relevant to humans. Three-dimensional retinal organoids from iPSC lines feature laminated cytoarchitecture, apical-basal polarity and emergence of a ciliary structure, thereby permitting pathogenic modeling of human photoreceptors in vitro. Here, we review the biology of photoreceptor cilia and associated defects and discuss recent progress in evolving treatment modalities, especially using patient-derived iPSCs, for retinal ciliopathies.
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?
A rare form of recessive inherited retinal dystrophy is attributed to variants in CFAP20.
“Here, we attribute a rare form of recessive inherited retinal dystrophy (IRD; a classic non-motile ciliopathy10,65,66) to variants in CFAP20, which encodes a remarkably conserved protein with well-established roles in motile cilia from diverse organisms15–18.”
From The inner junction protein CFAP20 functions in motile and non-motile cilia and is critical for vision (2022) · cites this paper as [65]
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
Takahashi, K., & Yamanaka, S. (2006) · Cell · doi:10.1016/j.cell.2006.07.024 · Cited by 26,673 · see citing works
Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors
Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., & Yamanaka, S. (2007) · Cell · doi:10.1016/j.cell.2007.11.019 · Cited by 20,221 · see citing works
Organoid Models and Applications in Biomedical Research
Xinaris, C., Brizi, V., & Remuzzi, G. (2015) · The Nephron journals/Nephron journals · doi:10.1159/000433566 · Cited by 3,517 · see citing works
Post-transcriptional gene regulation by mRNA modifications
Zhao, B. S., Roundtree, I. A., & He, C. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.132 · Cited by 2,418 · see citing works
Kinesin and Dynein Superfamily Proteins and the Mechanism of Organelle Transport
Hirokawa, N. (1998) · Science · doi:10.1126/science.279.5350.519 · Cited by 1,689 · see citing works
Genes and molecular pathways underpinning ciliopathies
Reiter, J. F., & Leroux, M. R. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2017.60 · Cited by 1,588 · see citing works
Self-formation of optic cups and storable stratified neural retina from human ESCs
Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., Saito, K., Yonemura, S., Eiraku, M., & Sasai, Y. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.05.009 · Cited by 1,447 · see citing works
Rosenbaum, J. L., & Witman, G. B. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm952 · Cited by 1,423 · see citing works
Adeno-Associated Virus (AAV) as a Vector for Gene Therapy
Naso, M. F., Tomkowicz, B., Perry, W. L., & Strohl, W. R. (2017) · BioDrugs · doi:10.1007/s40259-017-0234-5 · Cited by 1,362 · see citing works
Hildebrandt, F., Benzing, T., & Katsanis, N. (2011) · New England Journal of Medicine · doi:10.1056/nejmra1010172 · Cited by 1,331 · see citing works
When cilia go bad: cilia defects and ciliopathies
Fliegauf, M., Benzing, T., & Omran, H. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2278 · Cited by 1,257 · see citing works
The renewal of photoreceptor cell outer segments
Young, R. W. (1967) · The Journal of Cell Biology · doi:10.1083/jcb.33.1.61 · Cited by 1,184 · cited 1× · see citing works
“Another unique feature of this modified cilium is the high rate of OS disc renewal; 8–10% of the membrane discs at the distal end are shed and engulfed by retinal pigment epithelium daily, with new discs formed at the cilia base to compensate for the loss and maintain OS homeostasis [49].”
BackgroundPazour, G. J., Dickert, B. L., Vucica, Y., Seeley, E. S., Rosenbaum, J. L., Witman, G. B., & Cole, D. G. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.3.709 · Cited by 1,147 · see citing works
Retinal repair by transplantation of photoreceptor precursors
MacLaren, R. E., Pearson, R. A., MacNeil, A., Douglas, R. H., Salt, T. E., Akimoto, M., Swaroop, A., Sowden, J. C., & Ali, R. R. (2006) · Nature · doi:10.1038/nature05161 · Cited by 1,099 · see citing works
Self-citationDefective myosin VIIA gene responsible for Usher syndrome type IB
Well, D., Blanchard, S., Kaplan, J., Guilford, P., Gibson, F., Walsh, J., Mburu, P., Varela, A., Levilliers, J., Weston, M. D., et al. (1995) · Nature · doi:10.1038/374060a0 · Cited by 1,068 · see citing works
Proteomic analysis of a eukaryotic cilium
Pazour, G. J., Agrin, N. S., Leszyk, J., & Witman, G. B. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200504008 · Cited by 1,028 · see citing works
Generation of three-dimensional retinal tissue with functional photoreceptors from human iPSCs
Zhong, X., Gutierrez, C., Xue, T., Hampton, C., Vergara, M. N., Cao, L.-H., Peters, A., Park, T. S., Zambidis, E. T., Meyer, J. S., et al. (2014) · Nature Communications · doi:10.1038/ncomms5047 · Cited by 970 · see citing works
Ciliogenesis: building the cell's antenna
Ishikawa, H., & Marshall, W. F. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3085 · Cited by 956 · see citing works
Opportunities and challenges in phenotypic drug discovery: an industry perspective
Moffat, J. G., Vincent, F., Lee, J. A., Eder, J., & Prunotto, M. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.111 · Cited by 939 · see citing works
Mutant sensory cilia in the nematode Caenorhabditis elegans
Perkins, L. A., Hedgecock, E. M., Thomson, J. N., & Culotti, J. G. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90314-3 · Cited by 907 · see citing works
Centrioles, Centrosomes, and Cilia in Health and Disease
Nigg, E. A., & Raff, J. W. (2009) · Cell · doi:10.1016/j.cell.2009.10.036 · Cited by 898 · see citing works
Neural remodeling in retinal degeneration
Marc, R. E., Jones, B. W., Watt, C. B., & Strettoi, E. (2003) · Progress in Retinal and Eye Research · doi:10.1016/s1350-9462(03)00039-9 · Cited by 871 · see citing works
Engineering Stem Cell Organoids
Yin, X., Mead, B. E., Safaee, H., Langer, R., Karp, J. M., & Levy, O. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2015.12.005 · Cited by 866 · see citing works
Leber congenital amaurosis: Genes, proteins and disease mechanisms
den Hollander, A. I., Roepman, R., Koenekoop, R. K., & Cremers, F. P. M. (2008) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2008.05.003 · Cited by 811 · see citing works
Antisense oligonucleotides: the next frontier for treatment of neurological disorders
Rinaldi, C., & Wood, M. J. A. (2018) · Nature Reviews Neurology · doi:10.1038/nrneurol.2017.148 · Cited by 788 · see citing works
Directed differentiation of telencephalic precursors from embryonic stem cells
Watanabe, K., Kamiya, D., Nishiyama, A., Katayama, T., Nozaki, S., Kawasaki, H., Watanabe, Y., Mizuseki, K., & Sasai, Y. (2005) · Nature Neuroscience · doi:10.1038/nn1402 · Cited by 784 · see citing works
Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy
Carter‐Dawson, L. D., & LaVail, M. M. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901880204 · Cited by 695 · see citing works
Efficient generation of retinal progenitor cells from human embryonic stem cells
Lamba, D. A., Karl, M., Ware, C. B., & Reh, T. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601990103 · Cited by 691 · see citing works
A type VII myosin encoded by the mouse deafness gene shaker-1
Gibson, F., Walsh, J. C., Mburu, P., Varela, A., Brown, K. A., Antonio, M., Beisel, K. W., Steel, K. P., & Brown, S. D. M. (1995) · Nature · doi:10.1038/374062a0 · Cited by 682 · see citing works
G Proteins and Phototransduction
Arshavsky, V. Y., Lamb, T. D., & Pugh, E. N. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.082701.102229 · Cited by 650 · see citing works
Primary Cilia and Mammalian Hedgehog Signaling
Bangs, F., & Anderson, K. V. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028175 · Cited by 642 · see citing works
Photoreceptor degeneration: genetic and mechanistic dissection of a complex trait
Wright, A. F., Chakarova, C. F., El-Aziz, M. M. A., & Bhattacharya, S. S. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2717 · Cited by 632 · see citing works
Osakada, F., Ikeda, H. O., Mandai, M., Wataya, T., Watanabe, K., Yoshimura, N., Akaike, A., Sasai, Y., & Takahashi, M. (2008) · Nature Biotechnology · doi:10.1038/nbt1384 · Cited by 629 · see citing works
A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition
García-Gonzalo, F. R., Corbit, K. C., Sirerol-Piquer, M. S., Ramaswami, G., Otto, E. A., Noriega, T. R., Seol, A. D., Robinson, J. F., Bennett, C., Josifova, D. J., et al. (2011) · Nature Genetics · doi:10.1038/ng.891 · Cited by 627 · see citing works
Lamba, D. A., Gust, J., & Reh, T. A. (2009) · Cell stem cell · doi:10.1016/j.stem.2008.10.015 · Cited by 604 · see citing works
Pluripotent stem cells in disease modelling and drug discovery
Avior, Y., Sagi, I., & Benvenisty, N. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2015.27 · Cited by 592 · see citing works
Witman, G. B., Carlson, K., Berliner, J. A., & Rosenbaum, J. L. (1972) · The Journal of Cell Biology · doi:10.1083/jcb.54.3.507 · Cited by 512 · see citing works
Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup
Lamb, T. D., Collin, S. P., & Pugh, E. N. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2283 · Cited by 498 · see citing works
Microglia activation in retinal degeneration
Langmann, T. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.0207114 · Cited by 496 · see citing works
Signaling through the Primary Cilium
Wheway, G., Nazlamova, L., & Hancock, J. T. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00008 · Cited by 483 · see citing works
The Centrosome in Cells and Organisms
Bornens, M. (2012) · Science · doi:10.1126/science.1209037 · Cited by 480 · see citing works
Reiter, J. F., Blacque, O. E., & Leroux, M. R. (2012) · EMBO Reports · doi:10.1038/embor.2012.73 · Cited by 476 · see citing works
Czerniecki, S. M., Cruz, N. M., Harder, J. L., Menon, R., Annis, J., Otto, E. A., Gulieva, R. E., Islas, L. V., Kim, Y. K., Tran, L. M., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.04.022 · Cited by 465 · see citing works
Meyer, J. S., Howden, S. E., Wallace, K. A., Verhoeven, A. D., Wright, L. S., Capowski, E. E., Pinilla, I., Martin, J. M., Tian, S., Stewart, R. M., et al. (2011) · Stem Cells · doi:10.1002/stem.674 · Cited by 464 · see citing works
Williams, C. L., Li, C., Kida, K., Inglis, P. N., Mohan, S., Semenec, L., Bialas, N. J., Stupay, R. M., Chen, N., Blacque, O. E., et al. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201012116 · Cited by 453 · see citing works
Generation of retinal cells from mouse and human induced pluripotent stem cells
Hirami, Y., Osakada, F., Takahashi, K., Okita, K., Yamanaka, S., Ikeda, H. O., Yoshimura, N., & Takahashi, M. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.04.035 · Cited by 422 · see citing works
Centriole distal appendages promote membrane docking, leading to cilia initiationPreprint
Tanos, B. E., Yang, H.-J., Soni, R. K., Wang, W., Macaluso, F., Asara, J. M., & Tsou, M.-F. B. (2013) · Genes & Development · doi:10.1101/gad.207043.112 · Cited by 417 · see citing works
Lamba, D. A., McUsic, A. C., Hirata, R. K., Wang, P.-R., Russell, D., & Reh, T. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008763 · Cited by 395 · see citing works
Evolution of phototransduction, vertebrate photoreceptors and retina
Lamb, T. D. (2013) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.06.001 · Cited by 387 · see citing works
Craige, B., Tsao, C.-C., Diener, D. R., Hou, Y., Lechtreck, K. F., Rosenbaum, J. L., & Witman, G. B. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201006105 · Cited by 385 · see citing works
Chang, B., Khanna, H., Hawes, N. L., Jimeno, D., He, S., Lillo, C., Parapuram, S. K., Cheng, H., Scott, A., Hurd, R. E., et al. (2006) · Human Molecular Genetics · doi:10.1093/hmg/ddl107 · Cited by 379 · see citing works
Self-citationGonzalez-Cordero, A., West, E. L., Pearson, R. A., Durán, Y., Carvalho, L. S., Chu, C. J., Naeem, A., Blackford, S. J. I., Georgiadis, A., Lakowski, J., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2643 · Cited by 373 · see citing works
The proteome of the mouse photoreceptor sensory cilium complex
Liu, Q., Tan, G., Levenkova, N., Li, T., Pugh, E. N., Rux, J. J., Speicher, D. W., & Pierce, E. A. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700054-mcp200 · Cited by 359 · see citing works
Self-citationGeneration of a ciliary margin-like stem cell niche from self-organizing human retinal tissue
Kuwahara, A., Ozone, C., Nakano, T., Saito, K., Eiraku, M., & Sasai, Y. (2015) · Nature Communications · doi:10.1038/ncomms7286 · Cited by 353 · see citing works
Assawachananont, J., Mandai, M., Okamoto, S., Yamada, C., Eiraku, M., Yonemura, S., Sasai, Y., & Takahashi, M. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.03.011 · Cited by 353 · see citing works
Hanein, S., Perrault, I., Gerber, S., Tanguy, G., Barbet, F., Ducroq, D., Calvas, P., Dollfus, H., Hamel, C., Lopponen, T., et al. (2004) · Human Mutation · doi:10.1002/humu.20010 · Cited by 350 · see citing works
The Intraflagellar Transport Machinery
Taschner, M., & Lorentzen, E. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028092 · Cited by 349 · see citing works
To beat or not to beat: roles of cilia in development and disease
Ibáñez-Tallon, I. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg061 · Cited by 349 · see citing works
Proteomic Analysis of Isolated Chlamydomonas Centrioles Reveals Orthologs of Ciliary-Disease Genes
Keller, L. C., Romijn, E. P., Zamora, I., Yates, J. R., & Marshall, W. F. (2005) · Current Biology · doi:10.1016/j.cub.2005.05.024 · Cited by 338 · see citing works
Generation of Rx + /Pax6 + neural retinal precursors from embryonic stem cells
Ikeda, H. O., Osakada, F., Watanabe, K., Mizuseki, K., Haraguchi, T., Miyoshi, H., Kamiya, D., Honda, Y., Sasai, N., Yoshimura, N., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500010102 · Cited by 335 · see citing works
Shirai, H., Mandai, M., Matsushita, K., Kuwahara, A., Yonemura, S., Nakano, T., Assawachananont, J., Kimura, T., Saito, K., Terasaki, H., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1512590113 · Cited by 323 · see citing works
Akimoto, M., Cheng, H., Zhu, D., Brzezinski, J. A., Khanna, R., Filippova, E. V., Oh, E. C. T., Jing, Y., Linares, J., Brooks, M., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0508214103 · Cited by 314 · see citing works
Self-citationTucker, B. A., Park, I., Qi, S. D., Klassen, H. J., Jiang, C., Yao, J., Redenti, S., Daley, G. Q., & Young, M. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018992 · Cited by 311 · see citing works
Pearson, R. A., Gonzalez-Cordero, A., West, E. L., Ribeiro, J., Aghaizu, N. D., Goh, D., Sampson, R. D., Georgiadis, A., Waldron, P. V., Durán, Y., et al. (2016) · Nature Communications · doi:10.1038/ncomms13029 · Cited by 311 · see citing works
Parfitt, D. A., Lane, A., Ramsden, C. M., Carr, A. F., Munro, P., Jovanovic, K., Schwarz, N., Kanuga, N., Muthiah, M. N., Hull, S., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.03.021 · Cited by 302 · see citing works
CEP290, a gene with many faces: mutation overview and presentation of CEP290base
Coppieters, F., Lefever, S., Leroy, B. P., & Baere, E. B. W. D. (2010) · Human Mutation · doi:10.1002/humu.21337 · Cited by 301 · see citing works
Repair of the degenerate retina by photoreceptor transplantation
Barber, A. C., Hippert, C., Durán, Y., West, E. L., Bainbridge, J. W., Warre-Cornish, K. M., Luhmann, U. F. O., Lakowski, J., Sowden, J. C., Ali, R. R., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1212677110 · Cited by 280 · see citing works
Cilium assembly and disassembly
Sánchez, I., & Dynlacht, B. D. (2016) · Nature Cell Biology · doi:10.1038/ncb3370 · Cited by 279 · see citing works
Retinal transplantation of photoreceptors results in donor–host cytoplasmic exchange
Santos‐Ferreira, T., Llonch, S., Borsch, O., Postel, K., Haas, J., & Ader, M. (2016) · Nature Communications · doi:10.1038/ncomms13028 · Cited by 277 · see citing works
Retinal organoids from pluripotent stem cells efficiently recapitulate retinogenesis
Völkner, M., Zschätzsch, M., Rostovskaya, M., Overall, R. W., Busskamp, V., Anastassiadis, K., & Karl, M. O. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.03.001 · Cited by 273 · see citing works
Hong, D.-H., Pawlyk, B. S., Shang, J., Sandberg, M. A., Berson, E. L., & Li, T. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.7.3649 · Cited by 257 · see citing works
Self-citationDeng, W.-L., Gao, M., Lei, X., Lv, J., Zhao, H., He, K.-W., Xia, X.-X., Li, L., Chen, Y., Li, Y.-P., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.02.003 · Cited by 257 · see citing works
Wahlin, K. J., Maruotti, J., Sripathi, S. R., Ball, J. M., Angueyra, J. M., Kim, C., Grebe, R. R., Li, W., Jones, B. W., & Zack, D. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-00774-9 · Cited by 247 · see citing works
Molecular Anatomy of the Developing Human Retina
Hoshino, A., Ratnapriya, R., Brooks, M. J., Chaitankar, V., Wilken, M. S., Zhang, C., Starostik, M. R., Gieser, L. M., Torre, A. L., Nishio, M., et al. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.10.029 · Cited by 247 · see citing works
Self-citationMazzoni, F., Novelli, E., & Strettoi, E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4968-08.2008 · Cited by 245 · see citing works
Breuer, D. K., Yashar, B. M., Filippova, E. V., Hiriyanna, S., Lyons, R. H., Mears, A. J., Asaye, B., Acar, C., Vervoort, R., Wright, A. F., et al. (2002) · The American Journal of Human Genetics · doi:10.1086/340848 · Cited by 245 · see citing works
Self-citationGonzalez-Cordero, A., Kruczek, K., Naeem, A., Fernando, M., Kloc, M., Ribeiro, J., Goh, D., Durán, Y., Blackford, S. J. I., Abelleira, L. E., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.07.022 · Cited by 245 · see citing works
Singh, M. S., Balmer, J., Barnard, A. R., Aslam, S. A., Moralli, D., Green, C., Barnea-Cramer, A. O., Duncan, I. L., & MacLaren, R. E. (2016) · Nature Communications · doi:10.1038/ncomms13537 · Cited by 234 · see citing works
Biology and therapy of inherited retinal degenerative disease: insights from mouse models
Veleri, S., Lazar, C. H., Chang, B., Sieving, P. A., Banin, E., & Swaroop, A. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.017913 · Cited by 232 · see citing works
Self-citationPerrault, I., Delphin, N., Hanein, S., Gerber, S., Dufier, J., Roche, O., Defoort‐Dhellemmes, S., Dollfus, H., Fazzi, E., Münnich, A., et al. (2007) · Human Mutation · doi:10.1002/humu.9485 · Cited by 231 · see citing works
Modeling Retinal Degeneration Using Patient-Specific Induced Pluripotent Stem Cells
Jin, Z.-B., Okamoto, S., Osakada, F., Homma, K., Assawachananont, J., Hirami, Y., Iwata, T., & Takahashi, M. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017084 · Cited by 231 · see citing works
Different RPGR exon ORF15 mutations in Canids provide insights into photoreceptor cell degeneration
Zhang, Q. (2002) · Human Molecular Genetics · doi:10.1093/hmg/11.9.993 · Cited by 229 · see citing works
Gorden, N. T., Arts, H. H., Parisi, M. A., Coene, K. L. M., Letteboer, S. J. F., van Beersum, S. E. C., Mans, D. A., Hikida, A., Eckert, M. L., Knutzen, D. M., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.10.002 · Cited by 229 · see citing works
Buskin, A., Zhu, L., Chichagova, V., Basu, B., Mozaffari‐Jovin, S., Dolan, D., Droop, A., Collin, J., Bronstein, R., Mehrotra, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06448-y · Cited by 228 · see citing works
RP2 and RPGR Mutations and Clinical Correlations in Patients with X-Linked Retinitis Pigmentosa
Sharon, D., Sandberg, M. A., Rabe, V. W., Stillberger, M. A., Dryja, T. P., & Berson, E. L. (2003) · The American Journal of Human Genetics · doi:10.1086/379379 · Cited by 227 · see citing works
RPGR Isoforms in Photoreceptor Connecting Cilia and the Transitional Zone of Motile Cilia
Hong, D.-H., Pawlyk, B. S., Sokolov, M., Strissel, K. J., Yang, J., TULLOCH, B. R., Wright, A. F., Arshavsky, V. Y., & Li, T. (2003) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.02-1206 · Cited by 222 · see citing works
Self-citationiPSC-Derived Retina Transplants Improve Vision in rd1 End-Stage Retinal-Degeneration Mice
Mandai, M., Fujii, M., Hashiguchi, T., Sunagawa, G. A., Shinichiro, I. T. O., Sun, J., Kaneko, J., Sho, J., Yamada, C., & Takahashi, M. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.12.008 · Cited by 219 · see citing works
Emerging therapies for inherited retinal degeneration
Scholl, H. P. N., Strauss, R. W., Singh, M. S., Dalkara, D., Roska, B., Picaud, S., & Sahel, J.-A. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aaf2838 · Cited by 219 · see citing works
Singh, R., Shen, W., Kuai, D., Martin, J. M., Guo, X., Smith, M. A., Perez, E. T., Phillips, M. J., Simonett, J. M., Wallace, K. A., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds469 · Cited by 213 · see citing works
(1978) · PubMed · Cited by 208 · see citing works
Recombinant Adeno-Associated Viral Integration and Genotoxicity: Insights from Animal Models
Chandler, R. J., Sands, M. S., & Venditti, C. P. (2017) · Human Gene Therapy · doi:10.1089/hum.2017.009 · Cited by 203 · see citing works
Phillips, M. J., Wallace, K. A., Dickerson, S., Miller, M. J., Verhoeven, A. D., Martin, J. M., Wright, L. S., Shen, W., Capowski, E. E., Perçin, E. F., et al. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.11-9313 · Cited by 201 · see citing works
Brown, J., & Witman, G. B. (2014) · BioScience · doi:10.1093/biosci/biu174 · Cited by 197 · see citing works
DiStefano, T. J., Chen, H. Y., Panebianco, C. J., Kaya, K. D., Brooks, M. J., Gieser, L. M., Morgan, N. Y., Pohida, T., & Swaroop, A. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.11.001 · Cited by 195 · see citing works
Self-citationPhotoreceptor Cilia and Retinal Ciliopathies
Bujakowska, K. M., Liu, Q., & Pierce, E. A. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028274 · Cited by 194 · see citing works
The regulation of cilium assembly and disassembly in development and disease
Wang, L., & Dynlacht, B. D. (2018) · Development · doi:10.1242/dev.151407 · Cited by 194 · see citing works
The Ciliary Transition Zone: Finding the Pieces and Assembling the Gate
Gonçalves, J., & Pelletier, L. (2017) · Molecules and Cells · doi:10.14348/molcells.2017.0054 · Cited by 191 · see citing works
Hallam, D., Hilgen, G., Dorgau, B., Zhu, L., Yu, M., Bojić, S., Hewitt, P. G., Schmitt, M. W., Uteng, M., Kustermann, S., et al. (2018) · Stem Cells · doi:10.1002/stem.2883 · Cited by 187 · see citing works
CRISPR-SKIP: programmable gene splicing with single base editors
Gapinske, M., Luu, A., Winter, J., Woods, W. S., Kostan, K. A., Shiva, N., Song, J. S., & Pérez‐Piñera, P. (2018) · Genome biology · doi:10.1186/s13059-018-1482-5 · Cited by 183 · see citing works
Tubby family proteins are adapters for ciliary trafficking of integral membrane proteins
Badgandi, H. B., Hwang, S.-H., Shimada, I. S., Loriot, E., & Mukhopadhyay, S. (2017) · Journal of Cell Biology · doi:10.1083/jcb.201607095 · Cited by 182 · see citing works
Gagliardi, G., M’Barek, K. B., Chaffiol, A., Slembrouck-Brec, A., Conart, J., Nanteau, C., Rabesandratana, O., Sahel, J., Duebel, J., Orieux, G., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.07.005 · Cited by 176 · see citing works
McEwen, D. P., Koenekoop, R. K., Khanna, H., Jenkins, P. M., López, I., Swaroop, A., & Martens, J. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704140104 · Cited by 169 · see citing works
Self-citationCurrent topics of functional links between primary cilia and cell cycle
Izawa, I., Goto, H., Kasahara, K., & Inagaki, M. (2015) · Cilia · doi:10.1186/s13630-015-0021-1 · Cited by 168 · see citing works
Khanna, H., Hurd, T. W., Lillo, C., Shu, X., Parapuram, S. K., He, S., Akimoto, M., Wright, A. F., Margolis, B. L., Williams, D. S., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m505827200 · Cited by 166 · see citing works
Self-citationCharacterizing the morbid genome of ciliopathies
WorkingGroup, C., Shaheen, R., Szymańska, K., Basu, B., Patel, N., Ewida, N., Faqeih, E., Alhashem, A. M., Derar, N., Alsharif, H., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1099-5 · Cited by 164 · see citing works
West, E. L., Pearson, R. A., Tschernutter, M., Sowden, J. C., MacLaren, R. E., & Ali, R. R. (2008) · Experimental Eye Research · doi:10.1016/j.exer.2008.01.004 · Cited by 163 · see citing works
Mellough, C. B., Sernagor, E., Moreno-Gimeno, I., Steel, D. H. W., & Lako, M. (2012) · Stem Cells · doi:10.1002/stem.1037 · Cited by 162 · see citing works
Retinal dystrophy in Bardet–Biedl syndrome and related syndromic ciliopathies
Mockel, A., Perdomo-Trujillo, Y., Stutzmann, F., Letsch, J., Marion, V., & Dollfus, H. (2011) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2011.03.001 · Cited by 162 · see citing works
Chapter 5 Modeling Ciliopathies
Quinlan, R., Tobin, J. L., & Beales, P. L. (2008) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)00605-4 · Cited by 160 · see citing works
Gilliam, J. C., Chang, J. T., Sandoval, I. M., Zhang, Y., Li, T., Pittler, S. J., Chiu, W., & Wensel, T. G. (2012) · Cell · doi:10.1016/j.cell.2012.10.038 · Cited by 160 · see citing works
Self-citationCilia - The sensory antennae in the eye
May‐Simera, H., Nagel‐Wolfrum, K., & Wolfrum, U. (2017) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2017.05.001 · Cited by 159 · see citing works
Cilia in vertebrate development and disease
Oh, E. C. T., & Katsanis, N. (2012) · Development · doi:10.1242/dev.050054 · Cited by 158 · see citing works
Cideciyan, A. V., Alemán, T. S., Jacobson, S. G., Khanna, H., Sumaroka, A., Aguirre, G. K., Schwartz, S., Windsor, E. A. M., He, S., Chang, B., et al. (2007) · Human Mutation · doi:10.1002/humu.20565 · Cited by 157 · see citing works
Self-citation1001 model organisms to study cilia and flagella
Vincensini, L., Blisnick, T., & Bastin, P. (2011) · Biology of the Cell · doi:10.1042/bc20100104 · Cited by 153 · see citing works
TULP1 mutation in two extended Dominican kindreds with autosomal recessive Retinitis pigmentosa
Banerjee, P., Kleyn, P. W., Knowles, J. A., Lewis, C. A., Ross, B. M., Parano, E., Kovats, S. G., Lee, J. J., Penchaszadeh, G. K., Ott, J., et al. (1998) · Nature Genetics · doi:10.1038/ng0298-177 · Cited by 153 · see citing works
Cell replacement and visual restoration by retinal sheet transplants
Seiler, M. J., & Aramant, R. B. (2012) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2012.06.003 · Cited by 152 · see citing works
Function of human pluripotent stem cell-derived photoreceptor progenitors in blind mice
Barnea-Cramer, A. O., Wang, W., Lu, S., Singh, M. S., Luo, C., Huo, H., McClements, M. E., Barnard, A. R., MacLaren, R. E., & Lanza, R. (2016) · Scientific Reports · doi:10.1038/srep29784 · Cited by 151 · see citing works
Organoid technology for retinal repair
Llonch, S., Carido, M., & Ader, M. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.09.028 · Cited by 151 · see citing works
Shimada, H., Lü, Q., Insinna-Kettenhofen, C., Nagashima, K., English, M. A., Semler, E. M., Mahgerefteh, J., Cideciyan, A. V., Li, T., Brooks, B. P., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.06.045 · Cited by 148 · see citing works
Self-citationPhotoreceptor sensory cilia and ciliopathies: focus on CEP290, RPGR and their interacting proteins
Rachel, R. A., Li, T., & Swaroop, A. (2012) · Cilia · doi:10.1186/2046-2530-1-22 · Cited by 147 · see citing works
Self-citationMukhopadhyay, S., & Jackson, P. K. (2011) · Genome biology · doi:10.1186/gb-2011-12-6-225 · Cited by 146 · see citing works
Identification of CC2D2A as a Meckel Syndrome Gene Adds an Important Piece to the Ciliopathy Puzzle
Tallila, J., Jakkula, E., Peltonen, L., Salonen, R., & Kestilä, M. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.05.004 · Cited by 145 · see citing works
RPGR: Its role in photoreceptor physiology, human disease, and future therapies
Megaw, R. D., Soares, D. C., & Wright, A. F. (2015) · Experimental Eye Research · doi:10.1016/j.exer.2015.06.007 · Cited by 141 · see citing works
Stem Cells, Genome Editing, and the Path to Translational Medicine
Soldner, F., & Jaenisch, R. (2018) · Cell · doi:10.1016/j.cell.2018.09.010 · Cited by 139 · see citing works
Collin, R. W. J., den Hollander, A. I., van der Velde-Visser, S. D., Bennicelli, J. L., Bennett, J., & Cremers, F. P. M. (2012) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2012.3 · Cited by 137 · see citing works
A Reinterpretation of Cell Transplantation: GFP Transfer From Donor to Host Photoreceptors
Ortín-Martínez, A., Tsai, E. L. S., Nickerson, P. E. B., Bergeret, M., Lu, Y., Smiley, S., Comanita, L., & Wallace, V. A. (2016) · Stem Cells · doi:10.1002/stem.2552 · Cited by 136 · see citing works
RPGRmutation analysis and disease: an update
Shu, X., Black, G. C. M., Rice, J. M., Hart‐Holden, N., Jones, A., O’Grady, A., Ramsden, S., & Wright, A. F. (2006) · Human Mutation · doi:10.1002/humu.20461 · Cited by 133 · see citing works
Mutations in RPGR and RP2 Account for 15% of Males with Simplex Retinal Degenerative Disease
Branham, K. E. H., Othman, M., Brumm, M. V., Karoukis, A. J., Atmaca-Sönmez, P., Yashar, B. M., Schwartz, S., Stover, N. B., Trzupek, K. M., Wheaton, D. K., et al. (2012) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-11025 · Cited by 131 · see citing works
Self-citationCEP290 gene transfer rescues Leber congenital amaurosis cellular phenotype
Burnight, E. R., Wiley, L. A., Drack, A. V., Braun, T. A., Anfinson, K. R., Kaalberg, E. E., Halder, J. A., Affatigato, L. M., Mullins, R. F., Stone, E. M., et al. (2014) · Gene Therapy · doi:10.1038/gt.2014.39 · Cited by 128 · see citing works
Expanding the genetic architecture and phenotypic spectrum in the skeletal ciliopathies
Zhang, W., Taylor, S. P., Ennis, H. A., Forlenza, K. N., Durán, I., Li, B., Sanchez, J. A. O., Nevarez, L., Nickerson, D. A., Bamshad, M. J., et al. (2017) · Human Mutation · doi:10.1002/humu.23362 · Cited by 128 · see citing works
BBS mutations modify phenotypic expression of CEP290-related ciliopathies
Zhang, Y., Seo, S., Bhattarai, S., Bugge, K., Searby, C. C., Zhang, Q., Drack, A. V., Stone, E. M., & Sheffield, V. C. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt394 · Cited by 127 · see citing works
Rachel, R. A., Yamamoto, E. A., Dewanjee, M. K., May‐Simera, H., Sergeev, Y. V., Hackett, A. N., Pohida, K., Munasinghe, J., Gotoh, N., Wickstead, B., et al. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv123 · Cited by 126 · see citing works
Self-citationNon-syndromic retinal ciliopathies: translating gene discovery into therapy
Estrada‐Cuzcano, A., Roepman, R., Cremers, F. P. M., den Hollander, A. I., & Mans, D. A. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds298 · Cited by 126 · see citing works
Estrada‐Cuzcano, A., Koenekoop, R. K., Sénéćhal, A., Baere, E. B. W. D., de Ravel, T. J. L., Banfi, S., Kohl, S., Ayuso, C., Sharon, D., Hoyng, C. B., et al. (2012) · Archives of Ophthalmology · doi:10.1001/archophthalmol.2012.2434 · Cited by 125 · see citing works
Beltran, W. A., Hammond, P., Acland, G. M., & Aguirre, G. K. (2006) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.05-0845 · Cited by 124 · see citing works
Brown, J., Marsala, C., Kosoy, R., & Gaertig, J. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.10.3081 · Cited by 124 · see citing works
Waldron, P. V., Marco, F. D., Kruczek, K., Ribeiro, J., Graca, A. B., Hippert, C., Aghaizu, N. D., Kalargyrou, A. A., Barber, A. C., Grimaldi, G., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.12.008 · Cited by 124 · see citing works
Use of bioreactors for culturing human retinal organoids improves photoreceptor yields
Ovando-Roche, P., West, E. L., Branch, M. J., Sampson, R. D., Fernando, M., Munro, P., Georgiadis, A., Rizzi, M., Kloc, M., Naeem, A., et al. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0907-0 · Cited by 123 · see citing works
Cideciyan, A. V., Rachel, R. A., Alemán, T. S., Świder, M., Schwartz, S., Sumaroka, A., Román, A. J., Stone, E. M., Jacobson, S. G., & Swaroop, A. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr022 · Cited by 117 · see citing works
Self-citationIannaccone, A., Breuer, D. K., Wang, X. F., Kuo, S. F., Normando, E. M., Filippova, E., Baldi, A., Hiriyanna, S., MacDonald, C. B., Baldi, F., et al. (2003) · Journal of Medical Genetics · doi:10.1136/jmg.40.11.e118 · Cited by 114 · see citing works
Self-citationDifferentiation of embryonic stem cells into retinal neurons
Zhao, X., Liu, J., & Ahmad, I. (2002) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02126-5 · Cited by 112 · see citing works
A role for the Tubby-like protein 1 in rhodopsin transport.
Hagstrom, S. A., Adamian, M., Scimeca, M. S., Pawlyk, B. S., Yue, G., & Li, T. (2001) · PubMed · Cited by 106 · see citing works
Self-citationGérard, X., Perrault, I., Hanein, S., Silva, E. D., Bigot, K., Defoort‐Dhellemmes, S., Rio, M., Münnich, A., Scherman, D., Kaplan, J., et al. (2012) · Molecular Therapy — Nucleic Acids · doi:10.1038/mtna.2012.21 · Cited by 106 · see citing works
Homma, K., Okamoto, S., Mandai, M., Gotoh, N., Rajasimha, H. K., Chang, Y.-S., Chen, S., Li, W., Cogliati, T., Swaroop, A., et al. (2013) · Stem Cells · doi:10.1002/stem.1372 · Cited by 99 · see citing works
Self-citationNoor, A., Windpassinger, C., Patel, M., Stachowiak, B., Mikhailov, A., Azam, M., Irfan, M., Siddiqui, Z. K., Naeem, F., Paterson, A. D., et al. (2008) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2008.01.021 · Cited by 99 · see citing works
Welby, E., Lakowski, J., Foggia, V. D., Budinger, D., Gonzalez-Cordero, A., Lun, A. T. L., Epstein, M., Patel, A., Cuevas, E., Kruczek, K., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.10.018 · Cited by 98 · see citing works
Self-citationAdeno-associated Virus (AAV) Dual Vector Strategies for Gene Therapy Encoding Large Transgenes.
McClements, M. E., & MacLaren, R. E. (2017) · PubMed Central · Cited by 95 · see citing works
Lakowski, J., Welby, E., Budinger, D., Marco, F. D., Foggia, V. D., Bainbridge, J. W., Wallace, K., Gamm, D. M., Ali, R. R., & Sowden, J. C. (2018) · Stem Cells · doi:10.1002/stem.2775 · Cited by 91 · 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
Self-citationXenopus: An Undervalued Model Organism to Study and Model Human Genetic Disease
Blum, M., & Ott, T. (2018) · Cells Tissues Organs · doi:10.1159/000490898 · Cited by 88 · see citing works
The intraflagellar transport machinery in ciliary signaling
Mourão, A., Christensen, S. T., & Lorentzen, E. (2016) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2016.06.009 · Cited by 83 · see citing works
Hynes, A. M., Giles, R. H., Srivastava, S., Eley, L., Whitehead, J. L., Danilenko, M., Raman, S. R., Slaats, G. G. G., Colville, J. G., Ajzenberg, H., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1322373111 · Cited by 83 · see citing works
Basal exon skipping and genetic pleiotropy: A predictive model of disease pathogenesis
Drivas, T. G., Wojno, A. P., Tucker, B. A., Stone, E. M., & Bennett, J. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.aaa5370 · Cited by 82 · see citing works
Strategies for retinal repair: cell replacement and regeneration
Lamba, D. A., Karl, M., & Reh, T. A. (2009) · Progress in brain research · doi:10.1016/s0079-6123(09)17502-7 · Cited by 81 · see citing works
Bachmann‐Gagescu, R., Dona, M., Hetterschijt, L., Tonnaer, E. L. G. M., Peters, T. A., de Vrieze, E., Mans, D. A., van Beersum, S. E. C., Phelps, I. G., Arts, H. H., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005575 · Cited by 81 · see citing works
Disruption of CEP290 microtubule/membrane-binding domains causes retinal degeneration
Drivas, T. G., Holzbaur, E. L. F., & Bennett, J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci69448 · Cited by 81 · see citing works
Suzuki, T., Akimoto, M., Imai, H., Ueda, Y., Mandai, M., Yoshimura, N., Swaroop, A., & Takahashi, M. (2007) · Cell Transplantation · doi:10.3727/000000007783464966 · Cited by 81 · see citing works
Self-citationCentrosomal protein CP110 controls maturation of mother centriole during cilia biogenesis
Yadav, S. P., Sharma, N. K., Liu, C., Dong, L., Li, T., & Swaroop, A. (2016) · Development · doi:10.1242/dev.130120 · Cited by 80 · see citing works
Self-citationChen, H. Y., Kaya, K. D., Dong, L., & Swaroop, A. (2016) · Europe PMC (PubMed Central) · Cited by 80 · see citing works
Self-citationRachel, R. A., May‐Simera, H., Veleri, S., Gotoh, N., Choi, B. Y., Murga‐Zamalloa, C., McIntyre, J. C., Marek, J., López, I., Hackett, A. N., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60981 · Cited by 80 · see citing works
Self-citationCP110 and its network of partners coordinately regulate cilia assembly
Tsang, W. Y., & Dynlacht, B. D. (2013) · Cilia · doi:10.1186/2046-2530-2-9 · Cited by 79 · see citing works
Thompson, D. A., Khan, N. W., Othman, M., Chang, B., Jia, L., Grahek, G., Wu, Z., Hiriyanna, S., Nellissery, J. K., Li, T., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035865 · Cited by 77 · see citing works
Self-citationVeleri, S., Manjunath, S. H., Fariss, R. N., May‐Simera, H., Brooks, M., Foskett, T. A., Gao, C., Longo, T. A., Liu, P., Nagashima, K., et al. (2014) · Nature Communications · doi:10.1038/ncomms5207 · Cited by 76 · see citing works
Self-citationMouse Models for Studies of Retinal Degeneration and Diseases
Chang, B. (2012) · Methods in molecular biology · doi:10.1007/978-1-62703-080-9_2 · Cited by 73 · see citing works
Advances in AAV Vector Development for Gene Therapy in the Retina
Day, T. P., Byrne, L. C., Schaffer, D. V., & Flannery, J. G. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3209-8_86 · Cited by 71 · see citing works
Unexpected CEP290 mRNA Splicing in a Humanized Knock-In Mouse Model for Leber Congenital Amaurosis
Garanto, A., van Beersum, S. E. C., Peters, T. A., Roepman, R., Cremers, F. P. M., & Collin, R. W. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079369 · Cited by 62 · see citing works
Abnormal respiratory cilia in non-syndromic Leber congenital amaurosis with CEP290 mutations
Papon, J., Perrault, I., Coste, A., Louis, B., Gérard, X., Hanein, S., Fares‐Taie, L., Gerber, S., Defoort‐Dhellemmes, S., Vojtek, A.-M., et al. (2010) · Journal of Medical Genetics · doi:10.1136/jmg.2010.077883 · Cited by 55 · see citing works
iPSC-Derived Retina Transplants Improve Vision in rd1 End-Stage Retinal-Degeneration Mice
Mandai, M., Fujii, M., Hashiguchi, T., Sunagawa, G. A., Shinichiro, I. T. O., Sun, J., Kaneko, J., Sho, J., Yamada, C., & Takahashi, M. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.03.024 · Cited by 51 · see citing works
Photoreceptor Intersegmental Transport and Retinal Degeneration
Besharse, J. C., Baker, S. A., Luby‐Phelps, K., & Pazour, G. J. (2003) · Advances in experimental medicine and biology · doi:10.1007/978-1-4615-0067-4_20 · Cited by 49 · see citing works
Schueler, M., Halbritter, J., Phelps, I. G., Braun, D. A., Otto, E. A., Porath, J. D., Gee, H. Y., Shendure, J., O’Roak, B. J., Lawson, J. A., et al. (2015) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2015-103304 · Cited by 48 · see citing works
Sorusch, N., Wunderlich, K. A., Bauß, K., Nagel‐Wolfrum, K., & Uwe Wolfrum, B. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3209-8_67 · Cited by 48 · see citing works
Drivas, T. G., & Bennett, J. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-3209-8_66 · Cited by 42 · see citing works
Mookherjee, S., Chen, H. Y., Isgrig, K., Yu, W., Hiriyanna, S., Levron, R., Li, T., Colosi, P., Chien, W., Swaroop, A., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.043 · Cited by 41 · see citing works
Self-citationPhelan, M. A., Lelkes, P. I., & Swaroop, A. (2018) · Stem Cell Investigation · doi:10.21037/sci.2018.09.06 · Cited by 39 · see citing works
Self-citationKaewkhaw, R., Swaroop, M., Homma, K., Nakamura, J., Brooks, M., Kaya, K. D., Chaitankar, V., Michael, S., Tawa, G. J., Zou, J., et al. (2016) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.15-17639 · Cited by 38 · see citing works
Self-citationChen, Y., Palczewska, G., Masuho, I., Gao, S., Jin, H., Dong, Z., Gieser, L. M., Brooks, M. J., Kiser, P. D., Kern, T. S., et al. (2016) · Science Signaling · doi:10.1126/scisignal.aag0245 · Cited by 36 · see citing works
Self-citationOlfactory Loss and Dysfunction in Ciliopathies: Molecular Mechanisms and Potential Therapies
Uytingco, C. R., Green, W. W., & Martens, J. R. (2019) · Current Medicinal Chemistry · doi:10.2174/0929867325666180105102447 · Cited by 30 · see citing works
Centrosomal protein CP110 controls maturation of the mother centriole during cilia biogenesis
Yadav, S. P., Sharma, N. K., Liu, C., Dong, L., Li, T., & Swaroop, A. (2016) · Journal of Cell Science · doi:10.1242/jcs.191601 · Cited by 30 · see citing works
Self-citationLeber congenital amaurosis, from darkness to light: An ode to Irene Maumenee
Coussa, R. G., López, I., & Koenekoop, R. K. (2017) · Ophthalmic Genetics · doi:10.1080/13816810.2016.1275021 · Cited by 29 · see citing works
Wang, W., Zhou, L., Lee, S. J., Liu, Y., de Castro, J. P. F., Emery, D., Vukmanic, E. V., Kaplan, H. J., & Dean, D. C. (2013) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.13-12600 · Cited by 28 · see citing works
Directed Differentiation of Human Induced Pluripotent Stem Cells: A Retina Perspective
Gamm, D. M., & Meyer, J. S. (2010) · Regenerative Medicine · doi:10.2217/rme.10.28 · Cited by 24 · see citing works
Benmerah, A., Durand, B., Giles, R. H., Harris, T., Kohl, L., Laclef, C., Meilhac, S. M., Mitchison, H. M., Pedersen, L. B., Roepman, R., et al. (2015) · Cilia · doi:10.1186/s13630-015-0014-0 · Cited by 10 · see citing works
Retina ciliopathies: From genes to mechanisms and treatment
Khanna, H., & Baehr, W. (2012) · Vision Research · doi:10.1016/j.visres.2012.11.007 · Cited by 10 · see citing works
Thompson, J. A., Roach, J. N. D., McLaren, T. L., & Lamey, T. M. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-75402-4_32 · Cited by 9 · see citing works
Using zebrafish to study the function of nephronophthisis and related ciliopathy genes
Molinari, E., Ramsbottom, S. A., Sammut, V., Hughes, F. E. P., & Sayer, J. A. (2018) · F1000Research · doi:10.12688/f1000research.15511.1 · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [9]Quinlan R.J., Tobin J.L. and Beales P.L., Modeling ciliopathies: Primary cilia in development and disease, Curr Topics Dev Biol 84 (2008), 249– 310. 19186246
- [100]Pazour G.J., et al., Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella, J Cell Biol 151(3) (2000), 709– 718. 11062270 PMC2185580
Cited by
Sorted by citations
Pluripotent stem cell-derived retinal organoids for disease modeling and development of therapies
Kruczek, K., & Swaroop, A. (2020) · Stem Cells · doi:10.1002/stem.3239 · Cited by 148 · see citing works
Self-citationExpanding the genetic architecture and phenotypic spectrum in the skeletal ciliopathies
Zhang, W., Taylor, S. P., Ennis, H. A., Forlenza, K. N., Durán, I., Li, B., Sanchez, J. A. O., Nevarez, L., Nickerson, D. A., Bamshad, M. J., et al. (2017) · Human Mutation · doi:10.1002/humu.23362 · Cited by 128 · see citing works
Waldron, P. V., Marco, F. D., Kruczek, K., Ribeiro, J., Graca, A. B., Hippert, C., Aghaizu, N. D., Kalargyrou, A. A., Barber, A. C., Grimaldi, G., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.12.008 · Cited by 124 · see citing works
Retinitis Pigmentosa: Current Clinical Management and Emerging Therapies
Nguyen, X., Moekotte, L., Plomp, A. S., Bergen, A. A. B., van Genderen, M. M., & Boon, C. J. F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24087481 · Cited by 135 · see citing works
Primary cilia biogenesis and associated retinal ciliopathies
Chen, H. Y., Kelley, R. A., Li, T., & Swaroop, A. (2020) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2020.07.013 · Cited by 106 · see citing works
Self-citationThe Use of Stem Cell-Derived Organoids in Disease Modeling: An Update
Azar, J. H., Bahmad, H. F., Daher, D., Moubarak, M. M., Hadadeh, O., Monzer, A., Bitar, S. A., Jamal, M., Al‐Sayegh, M., & Abou-Kheir, W. G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147667 · Cited by 101 · see citing works
Kozycki, C. T., Kodati, S., Huryn, L. A., Wang, H., Warner, B. M., Jani, P. H., Hammoud, D. A., Abu-Asab, M. S., Jittayasothorn, Y., Mattapallil, M. J., et al. (2022) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2022-222629 · Cited by 73 · see citing works
Singh, R. K., & Nasonkin, I. O. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00179 · Cited by 66 · see citing works
Human Organoids for the Study of Retinal Development and Disease
Bell, C. M., Zack, D. J., & Berlinicke, C. A. (2020) · Annual Review of Vision Science · doi:10.1146/annurev-vision-121219-081855 · Cited by 63 · see citing works
Murro, V., Banfi, S., Testa, F., Iarossi, G., Falsini, B., Sodi, A., Signorini, S. G., Iolascon, A., Russo, R., Mucciolo, D. P., et al. (2023) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-023-02798-z · Cited by 47 · see citing works
Chrystal, P. W., Lambacher, N. J., Doucette, L. P., Bellingham, J., Schiff, E. R., Noel, N. C. L., Li, C., Tsiropoulou, S., Casey, G. A., Zhai, Y., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33820-w · Cited by 31 · see citing works
Kruczek, K., Qu, Z., Welby, E., Shimada, H., Hiriyanna, S., English, M. A., Zein, W. M., Brooks, B. P., & Swaroop, A. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.08.006 · Cited by 30 · see citing works
Self-citationJoubert syndrome: Molecular basis and treatment
Spahıu, L., Behluli, E., Grajçevci-Uka, V., Liehr, T., & Temaj, G. (2024) · PubMed Central · doi:10.34763/jmotherandchild.20222601.d-22-00034 · Cited by 28 · see citing works
The Rise of Retinal Organoids for Vision Research
Sharma, K., Krohne, T. U., & Busskamp, V. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228484 · Cited by 26 · see citing works
On the Wrong Track: Alterations of Ciliary Transport in Inherited Retinal Dystrophies
Sánchez-Bellver, L., Toulis, V., & Marfany, G. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.623734 · Cited by 25 · see citing works
Human asthenozoospermia: Update on genetic causes, patient management, and clinical strategies
Cavarocchi, E., Drouault, M., Ribeiro, J. C., Simon, V., Whitfield, M., & Touré, A. (2025) · Andrology · doi:10.1111/andr.13828 · Cited by 26 · see citing works
Liu, X., Pacwa, A., Bresciani, G., Swierczynska, M., Dorecka, M., & Smędowski, A. (2024) · Molecular Medicine · doi:10.1186/s10020-024-00875-y · Cited by 22 · see citing works
Accogli, A., Shakya, S., Yang, T., Insinna, C., Kim, S. Y., Bell, D. R., Butov, K. R., Severino, M., Niceta, M., Scala, M., et al. (2024) · Nature Communications · doi:10.1038/s41467-023-44611-2 · Cited by 19 · see citing works
2-IPMA Ameliorates PM2.5-Induced Inflammation by Promoting Primary Ciliogenesis in RPE Cells
Choi, J. Y., Bae, J.-E., Kim, J. B., Jo, D. S., Park, N. Y., Kim, Y. H., Lee, H. J., Kim, S. H., Ys, K., Jeon, H. B., et al. (2021) · Molecules · doi:10.3390/molecules26175409 · Cited by 17 · see citing works
Primary Cilia in Amacrine Cells in Retinal Development
Ning, K., Sendayen, B. E., Kowal, T. J., Wang, B., Jones, B. W., Hu, Y., & Sun, Y. (2021) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.62.9.15 · Cited by 16 · see citing works
Sánchez-Bellver, L., Férriz-Gordillo, A., Carrillo-Pz, M., Rabanal, L., García-Gonzalo, F. R., & Marfany, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012527 · Cited by 13 · see citing works
Andreazzoli, M., Barravecchia, I., Cesari, C. D., Angeloni, D., & Demontis, G. C. (2021) · Cells · doi:10.3390/cells10092489 · Cited by 13 · see citing works
Retinal Degeneration Animal Models in Bardet–Biedl Syndrome and Related CiliopathiesPreprint
Delvallée, C., & Dollfus, H. (2023) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a041303 · Cited by 14 · see citing works
Characterization of Primary Cilia Formation in Human ESC-Derived Retinal Organoids
Ning, K., Luo, Z., Kowal, T. J., Tran, M., Majumder, R., Jarin, T. M., Wu, A. Y., Goldberg, J. L., & Sun, Y. (2023) · Stem Cells International · doi:10.1155/2023/6494486 · Cited by 10 · see citing works
Wong, N., Yip, S. P., & Huang, C.-L. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241713652 · Cited by 8 · see citing works
Case Report: ROSAH syndrome presents diagnostic and therapeutic challenges
Shunyakova, J., Reynolds, M. A., Taylor, A., Sieck, E. G., Walsh, J. T., & Hassman, L. M. (2025) · Frontiers in Ophthalmology · doi:10.3389/fopht.2025.1535805 · Cited by 6 · see citing works
Chiu, N., Lee, W., Liu, P., Levi, S. R., Wang, H.-H., Chen, N., Kang, E. Y., Seo, G. H., Lee, H., Liu, L., et al. (2021) · Ophthalmic Genetics · doi:10.1080/13816810.2021.2010773 · Cited by 6 · see citing works
Gene and epigenetic editing in the treatment of primary ciliopathies
Molinari, E., & Sayer, J. A. (2021) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2021.01.027 · Cited by 6 · see citing works
Using zebrafish to study the function of nephronophthisis and related ciliopathy genes
Molinari, E., Ramsbottom, S. A., Sammut, V., Hughes, F. E. P., & Sayer, J. A. (2018) · F1000Research · doi:10.12688/f1000research.15511.1 · Cited by 6 · see citing works
Molins, B., Mesquida, M., & Adán, A. (2022) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2022.101097 · Cited by 5 · see citing works
RetractedAdvances in Ubiquitination and Proteostasis in Retinal Degeneration
Wei, J., Chen, X., Xiong, Y., & Gao, Y. (2024) · Frontiers in Bioscience-Landmark · doi:10.31083/j.fbl2907260 · Cited by 4 · see citing works
Ren, Z.-L., 电子科技大学医学院四川省人民医院临床医学检验中心, 四. 成., Zhang, H., Li, L., Yang, Z., Jiang, L., 电子科技大学医学院四川省人民医院人类疾病基因研究四川省重点实验室, 四. 成., & 中国医学科学院防盲研究单元(2019RU026), 四. 成. (2022) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2021.387 · Cited by 4 · see citing works
Kruczek, K., & Swaroop, A. (2023) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2023.09.003 · Cited by 4 · see citing works
Self-citationGenetic and Clinical Analyses of the KIZ-c.226C>T Variant Resulting in a Dual Mutational Mechanism
Sundaresan, Y., Rivera, A., Obolensky, A., Gopalakrishnan, P., Hadad, H. O., Shemesh, A., Khateb, S., Ross, M., Ofri, R., Durst, S., et al. (2024) · Genes · doi:10.3390/genes15060804 · Cited by 3 · see citing works
Silfhout, A. T. V., Jazet, I. M., Yzer, S., Pas, J. A. A. H., Demirdas, S., van Rossum, E. F. C., Thiadens, A. A. H. J., van Beek, R., Haer‐Wigman, L., Barge‐Schaapveld, D. Q. C. M., et al. (2025) · Genetics in Medicine · doi:10.1016/j.gim.2025.101513 · Cited by 2 · see citing works
Exon Skipping Therapy Restores Ciliary Function in USH2A -Related Retinal Degeneration
Li, W., Li, Y., Zhou, Y., Liu, Y., Liu, H., Wei, X., Sun, Z., Han, X., Zou, X., Li, H., et al. (2025) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.66.12.46 · Cited by 2 · see citing works
Barbelanne, M., Lu, Y., Kumar, K., Zhang, X., Li, C., Park, K., Warner, A., Xu, X. Z. S., Shaham, S., & Leroux, M. R. (2024) · Scientific Reports · doi:10.1038/s41598-024-79057-z · Cited by 1 · see citing works
Eiumtrakul, W., Tim‐Aroon, T., Wuthisiri, W., Sujirakul, T., Chansakul, T., Khongkraparn, A., Noojarern, S., Wattanasirichaigoon, D., & Wongkittichote, P. (2025) · Journal of Human Genetics · doi:10.1038/s10038-025-01371-9 · Cited by 1 · see citing works
Antonelou, M., Hameed, Z., Abdall-Razak, A., Egan, C. A., & Böckenhauer, D. (2022) · Springer eBooks · doi:10.1007/978-3-030-76419-7_42
Refractive errors in patients with Bardet Biedl syndrome
Saricay, L. Y., Baldwin, G. E., Moulton, E. A., Gonzalez, J. E., Rajabi, F., Hunter, D. G., & Fulton, A. B. (2024) · Ophthalmic Genetics · doi:10.1080/13816810.2024.2357296
Whiting, K., Aslanyan, M. G., van Summeren, L., Beyer, T., Dahlke, K., Theil, T., Boldt, K., & Roepman, R. (2026) · Journal of Cell Science · doi:10.1242/jcs.264431
Investigating motile ciliopathies in a pediatric case of an abnormal optic nerve head
Amuzie, C., Lin, B. R., Hucko, L., Shah, S. M., Negron, C. I., McKeown, C. A., & Berrocal, A. M. (2025) · Ophthalmic Genetics · doi:10.1080/13816810.2025.2555469
Liu, X., Pacwa, A., Bresciani, G., Świerczyńska, M., Dorecka, M., & Smedowski, A. (2024) · Figshare · doi:10.6084/m9.figshare.26754157
Le cil primaire : une nouvelle cible pour la remyélinisation ?
Delfino, G. (2020) · theses.fr (ABES) · doi:10.70675/a62c179az64bfz4247zb041zc7cfc961677c
Unusual presentation of cone dysfunction consequent upon a homozygous FAM161A variant
Alhamad, J., Magharbil, E., Nowilaty, S. R., & Ba‐Abbad, R. (2026) · Ophthalmic Genetics · doi:10.1080/13816810.2026.2653146
- Authors
- Chen, H. Y., Welby, E., Li, T., & Swaroop, A.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Swaroop, Anand
- Venue
- Translational Science of Rare Diseases
- Publisher
- SAGE Publications
- Published
- 2019-07-04
- Volume
- 4
- Issue
- 1-2
- Pages
- 97-115
- ISSN
- 2214-6490 (ISSN-L)
- 2214-6512
- PMC
- PMC6839492
- OpenAlex
- W2953550035
- Cited by
- 44
- References
- 185
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 7 · 2023: 6 · 2022: 7 · 2021: 7 · 2020: 6 · 2018: 2 · 2017: 1
- FWCI
- 1.65
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Translational Science of Rare Diseases (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- National Eye Institute (EY000450, EY000474)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinal Development and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
- Keywords
- ciliopathies, retinal disease, photoreceptor cilia, photoreceptor degeneration, ciliogenesis, induced pluripotent stem cells, retinal organoids, stem cell therapy, ciliary defects, pathophysiological mechanisms
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
