Retinal regions shape human and murine Müller cell proteome profile and functionality.
EPPK1
Müller cells
glial heterogeneity
macula
retina
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
02 2023
02 2023
Historique:
revised:
29
09
2022
received:
17
07
2022
accepted:
07
10
2022
pubmed:
6
11
2022
medline:
20
12
2022
entrez:
5
11
2022
Statut:
ppublish
Résumé
The human macula is a highly specialized retinal region with pit-like morphology and rich in cones. How Müller cells, the principal glial cell type in the retina, are adapted to this environment is still poorly understood. We compared proteomic data from cone- and rod-rich retinae from human and mice and identified different expression profiles of cone- and rod-associated Müller cells that converged on pathways representing extracellular matrix and cell adhesion. In particular, epiplakin (EPPK1), which is thought to play a role in intermediate filament organization, was highly expressed in macular Müller cells. Furthermore, EPPK1 knockout in a human Müller cell-derived cell line led to a decrease in traction forces as well as to changes in cell size, shape, and filopodia characteristics. We here identified EPPK1 as a central molecular player in the region-specific architecture of the human retina, which likely enables specific functions under the immense mechanical loads in vivo.
Substances chimiques
Proteome
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
391-414Subventions
Organisme : Austrian Science Fund FWF
ID : P 30310
Pays : Austria
Informations de copyright
© 2022 The Authors. GLIA published by Wiley Periodicals LLC.
Références
Adams, M. K., Belyaeva, O. V., Wu, L., & Kedishvili, N. Y. (2014). The retinaldehyde reductase activity of dhrs3 is reciprocally activated by retinol dehydrogenase 10 to control retinoid homeostasis. The Journal of Biological Chemistry, 289, 14868-14880.
Akhmanova, M., Osidak, E., Domogatsky, S., Rodin, S., & Domogatskaya, A. (2015). Physical, spatial, and molecular aspects of extracellular matrix of In vivo niches and artificial scaffolds relevant to stem cells research. Stem Cells International, 2015, 1-35.
Altmann, C., & Schmidt, M. (2018). The role of microglia in diabetic retinopathy: Inflammation, microvasculature defects and neurodegeneration. International Journal of Molecular Sciences, 19, 110.
Bachmann, M., Kukkurainen, S., Hytönen, V. P., & Wehrle-Haller, B. (2019). Cell adhesion by Integrins. Physiological Reviews, 99, 1655-1699.
Balmer, J. E., & Blomhoff, R. (2002). Gene expression regulation by retinoic acid. Journal of Lipid Research, 43, 1773-1808.
Belyaeva, O. V., Adams, M. K., Popov, K. M., & Kedishvili, N. Y. (2019). Generation of retinaldehyde for retinoic acid biosynthesis. Biomolecules, 10, 5.
Benchling. (2021). Cloud-based informatics platform for life sciences R&D | Benchling.
Bhutto, I., & Lutty, G. (2012). Understanding age-related macular degeneration (AMD): Relationships between the photoreceptor/retinal pigment epithelium/Bruch's membrane/choriocapillaris complex. Molecular Aspects of Medicine, 33, 295-317.
Billings, S. E., Pierzchalski, K., Tjaden, N. E. B., Pang, X.-Y., Trainor, P. A., Kane, M. A., & Moise, A. R. (2013). The retinaldehyde reductase DHRS3 is essential for preventing the formation of excess retinoic acid during embryonic development. The FASEB Journal, 27, 4877-4889.
Bollmann, L., Koser, D. E., Shahapure, R., Gautier, H. O. B., Holzapfel, G. A., Scarcelli, G., Gather, M. C., Ulbricht, E., & Franze, K. (2015). Microglia mechanics: Immune activation alters traction forces and durotaxis. Frontiers in Cellular Neuroscience, 9, 363.
Bourgot, I., Primac, I., Louis, T., Noël, A., & Maquoi, E. (2020). Reciprocal interplay between Fibrillar collagens and collagen-binding Integrins: Implications in cancer progression and metastasis. Frontiers in Oncology, 10, 1488.
Bringmann, A., Syrbe, S., Görner, K., Kacza, J., Francke, M., Wiedemann, P., & Reichenbach, A. (2018). The primate fovea: Structure, function and development. Progress in Retinal and Eye Research, 66, 49-84.
Bringmann, A., Unterlauft, J. D., Wiedemann, R., Barth, T., Rehak, M., & Wiedemann, P. (2020). Two different populations of Müller cells stabilize the structure of the fovea: An optical coherence tomography study. International Ophthalmology, 40, 2931-2948.
Bringmann, A., Unterlauft, J. D., Wiedemann, R., Barth, T., Rehak, M., & Wiedemann, P. (2021). Degenerative lamellar macular holes: Tractional development and morphological alterations. International Ophthalmology, 41, 1203-1221.
Brunner, A.-D., Thielert, M., Vasilopoulou, C., Ammar, C., Coscia, F., Mund, A., Hoerning, O. B., Bache, N., Apalategui, A., Lubeck, M., Richter, S., Fischer, D. S., Raether, O., Park, M. A., Meier, F., Theis, F. J., & Mann, M. (2022). Ultra-high sensitivity mass spectrometry quantifies single-cell proteome changes upon perturbation. Molecular Systems Biology, 18, e10798.
Chambers, D. C., Carew, A. M., Lukowski, S. W., & Powell, J. E. (2019). Transcriptomics and single-cell RNA-sequencing. Respirology, 24, 29-36.
Cowan, C. S., Renner, M., De Gennaro, M., Gross-Scherf, B., Goldblum, D., Hou, Y., Munz, M., Rodrigues, T. M., Krol, J., Szikra, T., Papasaikas, P., Cuttat, R., Waldt, A., Diggelmann, R., Patino-Alvarez, C. P., Gerber-Hollbach, N., Schuierer, S., Hou, Y., Srdanovic, A., … Roska, B. (2020). Cell types of the human retina and its organoids at single-cell resolution. Cell, 182, 1623-1640.e34.
da Silva, S., & Cepko, C. L. (2017). Fgf8 expression and degradation of retinoic acid are required for patterning a high-acuity area in the retina. Developmental Cell, 42, 68-81.e6.
Domdei, N., Reiniger, J. L., Holz, F. G., & Harmening, W. M. (2021). The relationship between visual sensitivity and eccentricity, cone density and outer segment length in the human Foveola. Investigative Ophthalmology & Visual Science, 62, 31.
Doncheva, N. T., Morris, J. H., Gorodkin, J., & Jensen, L. J. (2019). Cytoscape StringApp: Network analysis and visualization of proteomics data. Journal of Proteome Research, 18, 623-632.
Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M., Yoshie, O., & Geuze, H. J. (1998). Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. The Journal of Biological Chemistry, 273, 20121-20127.
Ferrara, M., Lugano, G., Sandinha, M. T., Kearns, V. R., Geraghty, B., & Steel, D. H. W. (2021). Biomechanical properties of retina and choroid: A comprehensive review of techniques and translational relevance. Eye, 35, 1818-1832.
Franz, J., Brinkmann, B. F., König, M., Hüve, J., Stock, C., Ebnet, K., & Riethmüller, C. (2016). Nanoscale imaging reveals a Tetraspanin-CD9 coordinated elevation of endothelial ICAM-1 clusters. PLoS One, 11, e0146598.
Franze, K., Grosche, J., Skatchkov, S. N., Schinkinger, S., Foja, C., Schild, D., Uckermann, O., Travis, K., Reichenbach, A., & Guck, J. (2007). Müller cells are living optical fibers in the vertebrate retina. Proceedings of the National Academy of Sciences, 104, 8287-8292.
Gantner, M. L., Eade, K., Wallace, M., Handzlik, M. K., Fallon, R., Trombley, J., Bonelli, R., Giles, S., Harkins-Perry, S., Heeren, T. F. C., Sauer, L., Ideguchi, Y., Baldini, M., Scheppke, L., Dorrell, M. I., Kitano, M., Hart, B. J., Cai, C., Nagasaki, T., … Friedlander, M. (2019). Serine and lipid metabolism in macular disease and peripheral neuropathy. The New England Journal of Medicine, 381, 1422-1433.
Ghaseminejad, F., Kaplan, L., Pfaller, A. M., Hauck, S. M., & Grosche, A. (2020). The role of Müller cell glucocorticoid signaling in diabetic retinopathy. Graefe's Archive for Clinical and Experimental Ophthalmology, 258, 221-230.
Goldman, D. (2014). Müller glial cell reprogramming and retina regeneration. Nature Reviews. Neuroscience, 15, 431-442.
Goto, M., Sumiyoshi, H., Sakai, T., Fassler, R., Ohashi, S., Adachi, E., Yoshioka, H., & Fujiwara, S. (2006). Elimination of Epiplakin by gene targeting results in acceleration of keratinocyte migration in mice. Molecular and Cellular Biology, 26, 548-558.
Grosche, A., Hauser, A., Lepper, M. F., Mayo, R., von Toerne, C., Merl-Pham, J., & Hauck, S. M. (2016). The proteome of native adult Müller glial cells from murine retina. Molecular & Cellular Proteomics, 15, 462-480.
Handa, J. T. (2012). How does the macula protect itself from oxidative stress? Molecular Aspects of Medicine, 33, 418-435.
Hao, Y., Hao, S., Andersen-Nissen, E., Mauck, W. M., Zheng, S., Butler, A., Lee, M. J., Wilk, A. J., Darby, C., Zager, M., Hoffman, P., Stoeckius, M., Papalexi, E., Mimitou, E. P., Jain, J., Srivastava, A., Stuart, T., Fleming, L. M., Yeung, B., … Satija, R. (2021). Integrated analysis of multimodal single-cell data. Cell, 184, 3573-3587.e29.
Heeren, T. F. C., Chew, E. Y., Clemons, T., Fruttiger, M., Balaskas, K., Schwartz, R., Egan, C. A., & Charbel Issa, P. (2020). Macular telangiectasia type 2: Visual acuity, disease end stage, and the MacTel area. Ophthalmology, 127, 1539-1548.
Hoon, M., Okawa, H., Della Santina, L., & Wong, R. O. L. (2014). Functional architecture of the retina: Development and disease. Progress in Retinal and Eye Research, 42, 44-84.
Hu, L., Huang, Z., Wu, Z., Ali, A., & Qian, A. (2018). Mammalian plakins, giant cytolinkers: Versatile biological functions and roles in cancer. International Journal of Molecular Sciences, 19, 974.
Hurley, J. B., Lindsay, K. J., & Du, J. (2015). Glucose, lactate, and shuttling of metabolites in vertebrate retinas. Journal of Neuroscience Research, 93, 1079-1092.
Hutmacher, F. (2019). Why is there so much more research on vision than on any other sensory modality? Frontiers in Psychology, 10, 2246.
Inaba, Y., Chauhan, V., van Loon, A. P., Choudhury, L. S., & Sagasti, A. (2020). Keratins and the plakin family cytolinker proteins control the length of epithelial microridge protrusions. eLife, 9, 1-27.
Ishikawa, K., Furuhashi, M., Sasaki, T., Kudoh, J., Tsuchisaka, A., Hashimoto, T., Sasaki, T., Yoshioka, H., Eshima, N., Matsuda-Hirose, H., Sakai, T., Hatano, Y., & Fujiwara, S. (2018). Intragenic copy number variation within human epiplakin 1 (EPPK1) generates variation of molecular size of epiplakin. Journal of Dermatological Science, 91, 228-231.
Jang, S.-I., Kalinin, A., Takahashi, K., Marekov, L. N., & Steinert, P. M. (2005). Characterization of human epiplakin: RNAi-mediated epiplakin depletion leads to the disruption of keratin and vimentin IF networks. Journal of Cell Science, 118, 781-793.
Janssen, A. F. J., Breusegem, S. Y., & Larrieu, D. (2022). Current methods and pipelines for image-based quantitation of nuclear shape and nuclear envelope abnormalities. Cell, 11, 347.
Jones, T. R., Kang, I. H., Wheeler, D. B., Lindquist, R. A., Papallo, A., Sabatini, D. M., Golland, P., & Carpenter, A. E. (2008). CellProfiler analyst: Data exploration and analysis software for complex image-based screens. BMC Bioinformatics, 9, 482.
Käll, L., Canterbury, J. D., Weston, J., Noble, W. S., & MacCoss, M. J. (2007). Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nature Methods, 4, 923-925.
Kam, R. K. T., Deng, Y., Chen, Y., & Zhao, H. (2012). Retinoic acid synthesis and functions in early embryonic development. Cell & Bioscience, 2, 11.
Kassambara A. & Mundt F. (2020). Extract and visualize the results of multivariate data analyses [R package factoextra version 1.0.7].
Kaylor, J. J., Yuan, Q., Cook, J., Sarfare, S., Makshanoff, J., Miu, A., Kim, A., Kim, P., Habib, S., Roybal, C. N., Xu, T., Nusinowitz, S., & Travis, G. H. (2013). Identification of DES1 as a vitamin a isomerase in Müller glial cells of the retina. Nature Chemical Biology, 9, 30-36.
Kelly, R. T. (2020). Single-cell proteomics: Progress and prospects. Molecular & Cellular Proteomics, 19, 1739-1748.
Kolb H. (1995). Photoreceptors University of Utah Health Sciences Center.
Kolde R. (2019). CRAN - Package pheatmap.
Lenis, T. L., Hu, J., Ng, S. Y., Jiang, Z., Sarfare, S., Lloyd, M. B., Esposito, N. J., Samuel, W., Jaworski, C., Bok, D., Finnemann, S. C., Radeke, M. J., Redmond, T. M., Travis, G. H., & Radu, R. A. (2018). Expression of ABCA4 in the retinal pigment epithelium and its implications for stargardt macular degeneration. Proceedings of the National Academy of Sciences of the United States of America, 115, E11120-E11127.
Limb, G. A., Salt, T. E., Munro, P. M. G., Moss, S. E., & Khaw, P. T. (2002). In vitro characterization of a spontaneously immortalized human Müller cell line (MIO-M1). Investigative Ophthalmology & Visual Science, 43, 864-869.
Liu, L., MacKenzie, K. R., Putluri, N., Maletić-Savatić, M., & Bellen, H. J. (2017). The glia-neuron lactate shuttle and elevated ROS promote lipid synthesis in neurons and lipid droplet accumulation in glia via APOE/D. Cell Metabolism, 26, 719-737.e6.
Liu, Y., Beyer, A., & Aebersold, R. (2016). On the dependency of cellular protein levels on mRNA abundance. Cell, 165, 535-550.
Lobo, J., See, E. Y.-S., Biggs, M., & Pandit, A. (2016). An insight into morphometric descriptors of cell shape that pertain to regenerative medicine. Journal of Tissue Engineering and Regenerative Medicine, 10, 539-553.
Lowe, D. G. (2004). Distinctive image features from scale-invariant Keypoints. International Journal of Computer Vision, 60, 91-110.
Lu, Y.-B., Franze, K., Seifert, G., Steinhäuser, C., Kirchhoff, F., Wolburg, H., Guck, J., Janmey, P., Wei, E.-Q., Käs, J., & Reichenbach, A. (2006). Viscoelastic properties of individual glial cells and neurons in the CNS. Proceedings of the National Academy of Sciences of the United States of America, 103, 17759-17764.
MacDonald, R. B., Randlett, O., Oswald, J., Yoshimatsu, T., Franze, K., & Harris, W. A. (2015). Müller glia provide essential tensile strength to the developing retina. The Journal of Cell Biology, 210, 1075-1083.
Mages, K., Grassmann, F., Jägle, H., Rupprecht, R., Weber, B. H. F., Hauck, S. M., & Grosche, A. (2019). The agonistic TSPO ligand XBD173 attenuates the glial response thereby protecting inner retinal neurons in a murine model of retinal ischemia. Journal of Neuroinflammation, 16, 43.
Margiotta, A., & Bucci, C. (2016). Role of intermediate filaments in vesicular traffic. Cell, 5, 20.
McQuin, C., Goodman, A., Chernyshev, V., Kamentsky, L., Cimini, B. A., Karhohs, K. W., Doan, M., Ding, L., Rafelski, S. M., Thirstrup, D., Wiegraebe, W., Singh, S., Becker, T., Caicedo, J. C., & Carpenter, A. E. (2018). CellProfiler 3.0: Next-generation image processing for biology. PLoS Biology, 16, e2005970.
Naito, Y., Hino, K., Bono, H., & Ui-Tei, K. (2015). CRISPRdirect: Software for designing CRISPR/Cas guide RNA with reduced off-target sites. Bioinformatics, 31, 1120-1123.
Napoli, J. L. (2012). Physiological insights into all-trans-retinoic acid biosynthesis. Biochimica et Biophysica Acta, Molecular and Cell Biology of Lipids, 1821, 152-167.
Navarro, P., Trevisan-Herraz, M., Bonzon-Kulichenko, E., Núñez, E., Martínez-Acedo, P., Pérez-Hernández, D., Jorge, I., Mesa, R., Calvo, E., Carrascal, M., Hernáez, M. L., García, F., Bárcena, J. A., Ashman, K., Abian, J., Gil, C., Redondo, J. M., & Vázquez, J. (2014). General statistical framework for quantitative proteomics by stable isotope labeling. Journal of Proteome Research, 13, 1234-1247.
Noya, S. B., Colameo, D., Brüning, F., Spinnler, A., Mircsof, D., Opitz, L., Mann, M., Tyagarajan, S. K., Robles, M. S., & Brown, S. A. (2019). The forebrain synaptic transcriptome is organized by clocks but its proteome is driven by sleep. Science (80-), 366, eaav2642.
Pannicke, T., Wagner, L., Reichenbach, A., & Grosche, A. (2018). Electrophysiological characterization of Müller cells from the ischemic retina of mice deficient in the leukemia inhibitory factor. Neuroscience Letters, 670, 69-74.
Pauly, D., Agarwal, D., Dana, N., Schäfer, N., Biber, J., Wunderlich, K. A., Jabri, Y., Straub, T., Zhang, N. R., Gautam, A. K., Weber, B. H. F., Hauck, S. M., Kim, M., Curcio, C. A., Stambolian, D., Li, M., & Grosche, A. (2019). Cell-type-specific complement expression in the healthy and diseased retina. Cell Reports, 29, 2835-2848.e4.
Potokar, M., Kreft, M., Li, L., Daniel Andersson, J., Pangršič, T., Chowdhury, H. H., Pekny, M., & Zorec, R. (2007). Cytoskeleton and vesicle mobility in astrocytes. Traffic, 8, 12-20.
Potokar, M., Morita, M., Wiche, G., & Jorgačevski, J. (2020). The diversity of intermediate filaments in astrocytes. Cell, 9, 1604.
Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., & Zhang, F. (2013). Genome engineering using the CRISPR-Cas9 system. Nature Protocols, 8, 2281-2308.
Reichenbach, A., & Bringmann, A. (2020). Glia of the human retina. Glia, 68, 768-796.
Reyes, R., Cardeñes, B., Machado-Pineda, Y., & Cabañas, C. (2018). Tetraspanin CD9: A key regulator of cell adhesion in the immune system. Frontiers in Immunology, 9, 863.
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015). Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Research, 43, e47.
Samardzija, M., Caprara, C., Heynen, S. R., DeParis, S. W., Meneau, I., Traber, G., Agca, C., von Lintig, J., & Grimm, C. (2014). A mouse model for studying cone photoreceptor pathologies. Investigative Ophthalmology and Visual Science, 55, 5304-5313.
Samardzija, M., Von lintig, J., Tanimoto, N., Oberhauser, V., Thiersch, M., Seeliger, M., Remé, C. E., Grimm, C., & Wenzel, A. (2008). R91W mutation in Rpe65 leads to milder early-onset retinal dystrophy due to the generation of low levels of 11-cis-retinal. Human Molecular Genetics, 17, 281-292.
Scerri, T. S., Quaglieri, A., Cai, C., Zernant, J., Matsunami, N., Baird, L., Scheppke, L., Bonelli, R., Yannuzzi, L. A., Friedlander, M., MacTel Project Consortium, Egan, C. A., Fruttiger, M., Leppert, M., Allikmets, R., & Bahlo, M. (2017). Genome-wide analyses identify common variants associated with macular telangiectasia type 2. Nature Genetics, 49, 559-567.
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J. Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9, 676-682.
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003). Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Research, 13, 2498-2504.
Sharma, K., Schmitt, S., Bergner, C. G., Tyanova, S., Kannaiyan, N., Manrique-Hoyos, N., Kongi, K., Cantuti, L., Hanisch, U.-K., Philips, M.-A., Rossner, M. J., Mann, M., & Simons, M. (2015). Cell type- and brain region-resolved mouse brain proteome. Nature Neuroscience, 18, 1819-1831.
Slezak, M., Grosche, A., Niemiec, A., Tanimoto, N., Pannicke, T., Münch, T. A., Crocker, B., Isope, P., Härtig, W., Beck, S. C., Huber, G., Ferracci, G., Perraut, M., Reber, M., Miehe, M., Demais, V., Lévêque, C., Metzger, D., Szklarczyk, K., … Pfrieger, F. W. (2012). Relevance of Exocytotic glutamate release from retinal glia. Neuron, 74, 504-516.
Sonnenberg, A., & Liem, R. K. H. (2007). Plakins in development and disease. Experimental Cell Research, 313, 2189-2203.
Spazierer, D., Fuchs, P., Pröll, V., Janda, L., Oehler, S., Fischer, I., Hauptmann, R., & Wiche, G. (2003). Epiplakin gene analysis in mouse reveals a single exon encoding a 725-kDa protein with expression restricted to epithelial tissues. The Journal of Biological Chemistry, 278, 31657-31666.
Spazierer, D., Fuchs, P., Reipert, S., Fischer, I., Schmuth, M., Lassmann, H., & Wiche, G. (2006). Epiplakin is dispensable for skin barrier function and for integrity of keratin network cytoarchitecture in simple and stratified epithelia. Molecular and Cellular Biology, 26, 559-568.
Spazierer, D., Raberger, J., Groß, K., Fuchs, P., & Wiche, G. (2008). Stress-induced recruitment of epiplakin to keratin networks increases their resistance to hyperphosphorylation-induced disruption. Journal of Cell Science, 121, 825-833.
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019). Comprehensive integration of single-cell data. Cell, 177, 1888-1902.e21.
Syrbe, S., Kuhrt, H., Gärtner, U., Habermann, G., Wiedemann, P., Bringmann, A., & Reichenbach, A. (2018). Müller glial cells of the primate foveola: An electron microscopical study. Experimental Eye Research, 167, 110-117.
Szabo, S., Wögenstein, K. L., Österreicher, C. H., Guldiken, N., Chen, Y., Doler, C., Wiche, G., Boor, P., Haybaeck, J., Strnad, P., & Fuchs, P. (2015). Epiplakin attenuates experimental mouse liver injury by chaperoning keratin reorganization. Journal of Hepatology, 62, 1357-1366.
Théry, C., Regnault, A., Garin, J., Wolfers, J., Zitvogel, L., Ricciardi-Castagnoli, P., Raposo, G., & Amigorena, S. (1999). Molecular characterization of dendritic cell-derived exosomes: Selective accumulation of the heat shock protein hsc73. The Journal of Cell Biology, 147, 599-610.
Théry, C., Witwer, K. W., Aikawa, E., Alcaraz, M. J., Anderson, J. D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin-Smith, G. K., Ayre, D. C., Bach, J. M., Bachurski, D., Baharvand, H., Balaj, L., Baldacchino, S., Bauer, N. N., Baxter, A. A., Bebawy, M., … Zuba-Surma, E. K. (2018). Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. Journal of Extracellular Vesicles, 7, 1535750.
Thompson, B., Katsanis, N., Apostolopoulos, N., Thompson, D. C., Nebert, D. W., & Vasiliou, V. (2019). Genetics and functions of the retinoic acid pathway, with special emphasis on the eye. Human Genomics, 13, 61.
Toft-Kehler, A. K., Skytt, D. M., & Kolko, M. (2018). A perspective on the Müller cell-neuron metabolic partnership in the inner retina. Molecular Neurobiology, 55, 5353-5361.
Tonoike, Y., Matsushita, K., Tomonaga, T., Katada, K., Tanaka, N., Shimada, H., Nakatani, Y., Okamoto, Y., & Nomura, F. (2011). Adhesion molecule periplakin is involved in cellular movement and attachment in pharyngeal squamous cancer cells. BMC Cell Biology, 12, 41.
Tschulakow, A. V., Oltrup, T., Bende, T., Schmelzle, S., & Schraermeyer, U. (2018). The anatomy of the foveola reinvestigated. PeerJ, 6, e4482.
Tseng Q. (2011). Etude d'architecture multicellulaire avec le microenvironnement contrôlé.
Tseng, Q., Duchemin-Pelletier, E., Deshiere, A., Balland, M., Guilloud, H., Filhol, O., & Theŕy, M. (2012). Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proceedings of the National Academy of Sciences of the United States of America, 109, 1506-1511.
Ueo, D., Furuhashi, M., Sasaki, T., Kudoh, J., Parry, D. A. D., Winter, D. J., Sasaki, T., Hashimoto, T., Tsuruta, D., & Fujiwara, S. (2021). Intragenic copy number variation in mouse epiplakin 1 (Eppk1) and the conservation of the repeat structures in the lower vertebrates. Journal of Dermatological Science, 103, 186-189.
Verbakel, S. K., van Huet, R. A. C., Boon, C. J. F., den Hollander, A. I., Collin, R. W. J., Klaver, C. C. W., Hoyng, C. B., Roepman, R., & Klevering, B. J. (2018). Non-syndromic retinitis pigmentosa. Progress in Retinal and Eye Research, 66, 157-186.
Vogel, C., & Marcotte, E. M. (2012). Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews. Genetics, 13, 227-232.
Voigt, A. P., Mullin, N. K., Stone, E. M., Tucker, B. A., Scheetz, T. E., & Mullins, R. F. (2021). Single-cell RNA sequencing in vision research: Insights into human retinal health and disease. Progress in Retinal and Eye Research, 83, 100934.
Voigt, A. P., Whitmore, S. S., Flamme-Wiese, M. J., Riker, M. J., Wiley, L. A., Tucker, B. A., Stone, E. M., Mullins, R. F., & Scheetz, T. E. (2019). Molecular characterization of foveal versus peripheral human retina by single-cell RNA sequencing. Experimental Eye Research, 184, 234-242.
Wan, J., & Goldman, D. (2016). Retina regeneration in zebrafish. Current Opinion in Genetics & Development, 40, 41-47.
Wang, J. S., & Kefalov, V. J. (2009). An alternative pathway mediates the mouse and human cone visual cycle. Current Biology, 19, 1665-1669.
Wang, J.-S., & Kefalov, V. J. (2011). The cone-specific visual cycle. Progress in Retinal and Eye Research, 30, 115-128.
Wang, W., Sumiyoshi, H., Yoshioka, H., & Fujiwara, S. (2006). Interactions between epiplakin and intermediate filaments. The Journal of Dermatology, 33, 518-527.
Wässle, H., Haverkamp, S., & Grünert, U. (2002). The cone pedicle a complex synapse in the retina. The Keio Journal of Medicine, 51, 19-20.
Whitmore, S. S., Wagner, A. H., DeLuca, A. P., Drack, A. V., Stone, E. M., Tucker, B. A., Zeng, S., Braun, T. A., Mullins, R. F., & Scheetz, T. E. (2014). Transcriptomic analysis across nasal, temporal, and macular regions of human neural retina and RPE/choroid by RNA-Seq. Experimental Eye Research, 129, 93-106.
Wiśniewski, J. R., Zougman, A., Nagaraj, N., & Mann, M. (2009). Universal sample preparation method for proteome analysis. Nature Methods, 65(6), 359-362.
Wögenstein, K. L., Szabo, S., Lunova, M., Wiche, G., Haybaeck, J., Strnad, P., Boor, P., Wagner, M., & Fuchs, P. (2014). Epiplakin deficiency aggravates murine caerulein-induced acute pancreatitis and favors the formation of acinar keratin granules. PLoS One, 9, e108323.
Wunderlich, K. A., Tanimoto, N., Grosche, A., Zrenner, E., Pekny, M., Reichenbach, A., Seeliger, M. W., Pannicke, T., & Perez, M.-T. (2015). Retinal functional alterations in mice lacking intermediate filament proteins glial fibrillary acidic protein and vimentin. The FASEB Journal, 29, 4815-4828.
Xue, Y., Sato, S., Razafsky, D., Sahu, B., Shen, S. Q., Potter, C., Sandell, L. L., Corbo, J. C., Palczewski, K., Maeda, A., Hodzic, D., & Kefalov, V. J. (2017). The role of retinol dehydrogenase 10 in the cone visual cycle. Scientific Reports, 7, 2390.
Xue, Y., Shen, S. Q., Jui, J., Rupp, A. C., Byrne, L. C., Hattar, S., Flannery, J. G., Corbo, J. C., & Kefalov, V. J. (2015). CRALBP supports the mammalian retinal visual cycle and cone vision. The Journal of Clinical Investigation, 125, 727-738.
Yeo, N. J. Y., Chan, E. J. J., & Cheung, C. (2019). Choroidal neovascularization: Mechanisms of endothelial dysfunction. Frontiers in Pharmacology, 10, 1363.
Yuodelis, C., & Hendrickson, A. (1986). A qualitative and quantitative analysis of the human fovea during development. Vision Research, 26, 847-855.
Zhang, T., Zhu, L., Madigan, M. C., Liu, W., Shen, W., Cherepanoff, S., Zhou, F., Zeng, S., Du, J., & Gillies, M. C. (2019). Human macular Müller cells rely more on serine biosynthesis to combat oxidative stress than those from the periphery. eLife, 8, 1-19.