{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T03:01:33Z","timestamp":1790737293721,"version":"4.1.0"},"reference-count":53,"publisher":"Springer Science and Business Media LLC","issue":"10","license":[{"start":{"date-parts":[[2024,10,1]],"date-time":"2024-10-01T00:00:00Z","timestamp":1727740800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,10,1]],"date-time":"2024-10-01T00:00:00Z","timestamp":1727740800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cell Death Dis"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Alternative splicing (AS) is a crucial mechanism contributing to proteomic diversity, which is highly regulated in tissue- and development-specific patterns. Retinal tissue exhibits one of the highest levels of AS. In particular, photoreceptors have a distinctive AS pattern involving the inclusion of microexons not found in other cell types.\n                    <jats:italic>PROM1<\/jats:italic>\n                    whose encoded protein Prominin-1 is located in photoreceptor outer segments (OSs), undergoes exon 4 inclusion from the 12\n                    <jats:sup>th<\/jats:sup>\n                    post-conception week of human development through adulthood. Exon 4 skipping in\n                    <jats:italic>PROM1<\/jats:italic>\n                    is associated with late-onset mild maculopathy, however its role in photoreceptor maturation and function is unknown. In this study retinal organoids, a valuable model system, were employed in combination with phosphorodiamidate morpholino oligos (PMOs) to assess the role of exon 4 AS in the development of human retina. Retinal organoids were treated with the PMOs for four weeks after which RT-PCR, western blotting and immunofluorescence analysis were performed to assess exon 4 exclusion and its impact on photoreceptors. The transcriptome of treated ROs was studied by bulk RNA-Seq. Our data demonstrate that 55% skipping of\n                    <jats:italic>PROM1<\/jats:italic>\n                    exon 4 resulted in decreased Prominin-1 expression by 40%, abnormal accumulation of cones in the basal side of the retinal organoids as well as detectable cone photoreceptor cilium defects. Transcriptomic and western blot analyses revealed decreased expression of cone, inner segment and connecting cilium basal body markers, increased expression of genes associated with stress response and the ubiquitin-proteasome system, and downregulation of autophagy. Importantly, the use of retinal organoids provides a valuable platform to study AS and unravel disease mechanisms in a more physiologically relevant context, opening avenues for further research and potential therapeutic interventions. Together our data indicate that cones may be more sensitive to\n                    <jats:italic>PROM1<\/jats:italic>\n                    exon 4 skipping and\/or reduced Prominin-1 expression, corroborating the pathogenesis of late-onset mild maculopathy.\n                  <\/jats:p>","DOI":"10.1038\/s41419-024-07105-7","type":"journal-article","created":{"date-parts":[[2024,10,1]],"date-time":"2024-10-01T08:02:28Z","timestamp":1727769748000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Deciphering the impact of PROM1 alternative splicing on human photoreceptor development and maturation"],"prefix":"10.1038","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4787-3015","authenticated-orcid":false,"given":"Marina","family":"Moya-Molina","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4031-4402","authenticated-orcid":false,"given":"Birthe","family":"Dorgau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily","family":"Flood","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stef J. F.","family":"Letteboer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Esben","family":"Lorentzen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan","family":"Coxhead","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Graham","family":"Smith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5178-8163","authenticated-orcid":false,"given":"Ronald","family":"Roepman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sushma","family":"Nagaraja Grellscheid","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lyle","family":"Armstrong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1327-8573","authenticated-orcid":false,"given":"Majlinda","family":"Lako","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,10,1]]},"reference":[{"key":"7105_CR1","doi-asserted-by":"crossref","unstructured":"Weisschuh N, Buena-Atienza E, Wissinger B. Splicing mutations in inherited retinal diseases. Progr Retinal Eye Res. 2021;80:100874.","DOI":"10.1016\/j.preteyeres.2020.100874"},{"key":"7105_CR2","doi-asserted-by":"publisher","unstructured":"Ciampi L, Mantica F, L\u00f3pez-Blanch L, Permanyer J, Rodriguez-Mar\u00edn C, Zang J, et al. Specialization of the photoreceptor transcriptome by Srrm3-dependent microexons is required for outer segment maintenance and vision. PNAS. 2022;119. Available from: https:\/\/doi.org\/10.1073\/pnas.2117090119.","DOI":"10.1073\/pnas.2117090119"},{"key":"7105_CR3","doi-asserted-by":"crossref","unstructured":"Corbeil D. Prominin-1 (CD133): New Insights on Stem & Cancer Stem Cell Biology. Advances in Experimental Medicine and Biology. New York: Springer Science+Business Media; 2013. 1\u2013255 p. Available from: http:\/\/www.springer.com\/series\/5584.","DOI":"10.1007\/978-1-4614-5894-4"},{"key":"7105_CR4","doi-asserted-by":"publisher","first-page":"715","DOI":"10.1016\/j.biocel.2004.08.010","volume":"37","author":"SV Shmelkov","year":"2005","unstructured":"Shmelkov SV, St.Clair R, Lyden D, Rafii S. AC133\/CD133\/Prominin-1. Int J Biochem Cell Biol. 2005;37:715\u20139.","journal-title":"Int J Biochem Cell Biol"},{"key":"7105_CR5","doi-asserted-by":"publisher","first-page":"12425","DOI":"10.1073\/pnas.94.23.12425","volume":"94","author":"A Weigmann","year":"1997","unstructured":"Weigmann A, Corbeil D, Hellwig A, Huttner WB. Prominin, a novel microvilli-specific polytopic membrane protein of the apical surface of epithelial cells, is targeted to plasmalemmal protrusions of non-epithelial cells. Proc Natl Acad Sci USA. 1997;94:12425\u201330.","journal-title":"Proc Natl Acad Sci USA"},{"key":"7105_CR6","doi-asserted-by":"publisher","first-page":"5013","DOI":"10.1182\/blood.V90.12.5013","volume":"90","author":"S Miraglia","year":"1997","unstructured":"Miraglia S, Godfrey W, Yin AH, Atkins K, Warnke R, Holden JT, et al. A Novel Five-Transmembrane Hematopoietic Stem Cell Antigen: Isolation, Characterization, and Molecular Cloning. Blood. 1997;90:5013\u201321.","journal-title":"Blood"},{"key":"7105_CR7","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1034\/j.1600-0854.2001.020202.x","volume":"2","author":"D Corbeil","year":"2001","unstructured":"Corbeil D, Roandper K, Fargeas CA, Joester A, Huttner WB. Prominin: A story of cholesterol, plasma membrane protrusions and human pathology. Traffic. 2001;2:82\u201391.","journal-title":"Traffic"},{"key":"7105_CR8","doi-asserted-by":"publisher","first-page":"399","DOI":"10.1007\/978-90-481-8622-8_14","volume":"51","author":"D Corbeil","year":"2010","unstructured":"Corbeil D, Marzesco AM, Fargeas CA, Huttner WB. Prominin-1: A distinct cholesterol-binding membrane protein and the organisation of the apical plasma membrane of epithelial cells. Subcell Biochem. 2010;51:399\u2013433.","journal-title":"Subcell Biochem"},{"key":"7105_CR9","doi-asserted-by":"crossref","unstructured":"Gisina A, Kim Y, Yarygin K, Lupatov A. Can CD133 Be Regarded as a Prognostic Biomarker in Oncology: Pros and Cons. Int J Mol Sci. 2023;24:17398.","DOI":"10.3390\/ijms242417398"},{"key":"7105_CR10","doi-asserted-by":"publisher","first-page":"2849","DOI":"10.1242\/jcs.02439","volume":"118","author":"AM Marzesco","year":"2005","unstructured":"Marzesco AM, Janich P, Wilsch-Br\u00e4uninger M, Dubreuil V, Langenfeld K, Corbeil D, et al. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci. 2005;118:2849\u201358.","journal-title":"J Cell Sci"},{"key":"7105_CR11","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1083\/jcb.200608137","volume":"176","author":"V Dubreuil","year":"2007","unstructured":"Dubreuil V, Marzesco AM, Corbeil D, Huttner WB, Wilsch-Br\u00e4uninger M. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J Cell Biol. 2007;176:483\u201395.","journal-title":"J Cell Biol"},{"key":"7105_CR12","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1093\/hmg\/9.1.27","volume":"9","author":"MA Maw","year":"2000","unstructured":"Maw MA, Corbeil D, Koch J, Hellwig A, Wilson-Wheeler JC, Bridges RJ, et al. A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet. 2000;9:27\u201334.","journal-title":"Hum Mol Genet"},{"key":"7105_CR13","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1007\/s00439-007-0395-2","volume":"122","author":"Q Zhang","year":"2007","unstructured":"Zhang Q, Zulfiqar F, Xiao X, Riazuddin SA, Ahmad Z, Caruso R, et al. Severe retinitis pigmentosa mapped to 4p15 and associated with a novel mutation in the PROM1 gene. Hum Genet. 2007;122:293\u20139.","journal-title":"Hum Genet"},{"key":"7105_CR14","doi-asserted-by":"publisher","first-page":"2656","DOI":"10.1167\/iovs.09-4857","volume":"51","author":"J Permanyer","year":"2010","unstructured":"Permanyer J, Navarro R, Friedman J, Pomares E, Navarro JC, Marfany G, et al. Autosomal recessive retinitis pigmentosa with early macular affectation caused by premature truncation in PROM1. Invest Ophthalmol Vis Sci. 2010;51:2656\u201363.","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"7105_CR15","first-page":"1295","volume":"21","author":"O Eidinger","year":"2015","unstructured":"Eidinger O, Leibu R, Newman H, Rizel L, Perlman I, Ben-Yosef T. An intronic deletion in the PROM1 gene leads to autosomal recessive cone-rod dystrophy. Mol Vis. 2015;21:1295\u2013306.","journal-title":"Mol Vis"},{"key":"7105_CR16","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1038\/ejhg.2015.144","volume":"24","author":"AK Mayer","year":"2016","unstructured":"Mayer AK, Rohrschneider K, Strom TM, Gl\u00f6ckle N, Kohl S, Wissinger B, et al. Homozygosity mapping and whole-genome sequencing reveals a deep intronic PROM1 mutation causing cone-rod dystrophy by pseudoexon activation. Eur J Hum Genet. 2016;24:459\u201362.","journal-title":"Eur J Hum Genet"},{"key":"7105_CR17","doi-asserted-by":"publisher","first-page":"619","DOI":"10.1007\/s00417-018-04206-w","volume":"257","author":"J Liang","year":"2019","unstructured":"Liang J, She X, Chen J, Zhai Y, Liu Y, Zheng K, et al. Identification of novel PROM1 mutations responsible for autosomal recessive maculopathy with rod-cone dystrophy. Graefe\u2019s Arch Clin Exp Ophthalmol. 2019;257:619\u201328.","journal-title":"Graefe\u2019s Arch Clin Exp Ophthalmol"},{"key":"7105_CR18","doi-asserted-by":"crossref","first-page":"2908","DOI":"10.1172\/JCI35876","volume":"118","author":"Z Yang","year":"2008","unstructured":"Yang Z, Chen Y, Lillo C, Chien J, Yu Z, Michaelides M, et al. Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice. J Clin Investig. 2008;118:2908\u201316.","journal-title":"J Clin Investig"},{"key":"7105_CR19","doi-asserted-by":"publisher","first-page":"122","DOI":"10.18632\/oncotarget.22343","volume":"9","author":"S Imani","year":"2018","unstructured":"Imani S, Cheng J, Dehghan Shasaltaneh M, Wei C, Yang L, Fu S, et al. Genetic identification and molecular modeling characterization reveal a novel PROM1 mutation in Stargardt4-like macular dystrophy. Oncotarget. 2018;9:122\u201341.","journal-title":"Oncotarget"},{"key":"7105_CR20","doi-asserted-by":"publisher","first-page":"4771","DOI":"10.1167\/iovs.09-4561","volume":"51","author":"M Michaelides","year":"2010","unstructured":"Michaelides M, Gaillard MC, Escher P, Tiab L, Bedell M, Borruat FX, et al. The PROM1 mutation p.R373C causes an autosomal dominant bull\u2019s eye maculopathy associated with rod, rod-cone, and macular dystrophy. Invest Ophthalmol Vis Sci. 2010;51:4771\u201380.","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"7105_CR21","doi-asserted-by":"crossref","unstructured":"Goldberg AFX, Moritz OL, Williams DS. Molecular basis for photoreceptor outer segment architecture. Progr Retinal Eye Res. 2016;55:52\u201381.","DOI":"10.1016\/j.preteyeres.2016.05.003"},{"key":"7105_CR22","doi-asserted-by":"publisher","first-page":"2366","DOI":"10.1167\/iovs.16-21162","volume":"58","author":"S Bhattacharya","year":"2017","unstructured":"Bhattacharya S, Yin J, Winborn CS, Zhang Q, Yue J, Chaum E. Prominin-1 is a novel regulator of autophagy in the human retinal pigment epithelium. Invest Ophthalmol Vis Sci. 2017;58:2366\u201387.","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"7105_CR23","doi-asserted-by":"publisher","first-page":"2373","DOI":"10.1002\/jcp.31094","volume":"238","author":"S Bhattacharya","year":"2023","unstructured":"Bhattacharya S, Yin J, Huo W, Chaum E. Loss of Prom1 impairs autophagy and promotes epithelial-mesenchymal transition in mouse retinal pigment epithelial cells. J Cell Physiol. 2023;238:2373\u201389.","journal-title":"J Cell Physiol"},{"key":"7105_CR24","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1111\/j.1399-0039.2007.00825.x","volume":"69","author":"CA Fargeas","year":"2007","unstructured":"Fargeas CA, Huttner WB, Corbeil D. Nomenclature of prominin-1 (CD133) splice variants - An update. Tissue Antigens. 2007;69:602\u20136.","journal-title":"Tissue Antigens"},{"key":"7105_CR25","doi-asserted-by":"publisher","first-page":"dev169474","DOI":"10.1242\/dev.169474","volume":"146","author":"CB Mellough","year":"2019","unstructured":"Mellough CB, Bauer R, Collin J, Dorgau B, Zerti D, Dolan DWP, et al. An integrated transcriptional analysis of the developing human retina. Development. 2019;146:dev169474.","journal-title":"Development"},{"key":"7105_CR26","doi-asserted-by":"publisher","first-page":"204","DOI":"10.1016\/j.ajo.2019.05.014","volume":"207","author":"M Del Pozo-Valero","year":"2019","unstructured":"Del Pozo-Valero M, Martin-Merida I, Jimenez-Rolando B, Arteche A, Avila-Fernandez A, Blanco-Kelly F, et al. Expanded Phenotypic Spectrum of Retinopathies Associated with Autosomal Recessive and Dominant Mutations in PROM1. Am J Ophthalmol. 2019;207:204\u201314.","journal-title":"Am J Ophthalmol"},{"key":"7105_CR27","doi-asserted-by":"publisher","DOI":"10.1038\/s41419-017-0141-1","volume":"9","author":"D Melguizo-Sanchis","year":"2018","unstructured":"Melguizo-Sanchis D, Xu Y, Taheem D, Yu M, Tilgner K, Barta T, et al. iPSC modeling of severe aplastic anemia reveals impaired differentiation and telomere shortening in blood progenitors. Cell Death Dis. 2018;9:128.","journal-title":"Cell Death Dis"},{"key":"7105_CR28","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1002\/stem.2240","volume":"34","author":"J Collin","year":"2016","unstructured":"Collin J, Mellough CB, Dorgau B, Przyborski S, Moreno-Gimeno I, Lako M. Using Zinc Finger Nuclease Technology to Generate CRX-Reporter Human Embryonic Stem Cells as a Tool to Identify and Study the Emergence of Photoreceptors Precursors during Pluripotent Stem Cell Differentiation. Stem Cells. 2016;34:311\u201321.","journal-title":"Stem Cells"},{"key":"7105_CR29","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1016\/j.biomaterials.2019.01.028","volume":"199","author":"B Dorgau","year":"2019","unstructured":"Dorgau B, Felemban M, Hilgen G, Kiening M, Zerti D, Hunt NC, et al. Decellularised extracellular matrix-derived peptides from neural retina and retinal pigment epithelium enhance the expression of synaptic markers and light responsiveness of human pluripotent stem cell derived retinal organoids. Biomaterials. 2019;199:63\u201375.","journal-title":"Biomaterials"},{"key":"7105_CR30","doi-asserted-by":"publisher","first-page":"1575","DOI":"10.3390\/cells12121575","volume":"12","author":"JC Corral-Serrano","year":"2023","unstructured":"Corral-Serrano JC, Sladen PE, Ottaviani D, Rezek OF, Athanasiou D, Jovanovic K, et al. Eupatilin Improves Cilia Defects in Human CEP290 Ciliopathy Models. Cells. 2023;12:1575.","journal-title":"Cells"},{"key":"7105_CR31","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","volume":"596","author":"J Jumper","year":"2021","unstructured":"Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583\u20139.","journal-title":"Nature"},{"key":"7105_CR32","doi-asserted-by":"publisher","unstructured":"Evans R, O\u2019neill M, Pritzel A, Antropova N, Senior A, Green T, et al. Protein complex prediction with AlphaFold-Multimer. bioRxiv. 2022; Available from: https:\/\/doi.org\/10.1101\/2021.10.04.463034.","DOI":"10.1101\/2021.10.04.463034"},{"key":"7105_CR33","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1038\/nmeth.4197","volume":"14","author":"R Patro","year":"2017","unstructured":"Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 2017;14:417\u20139.","journal-title":"Nat Methods"},{"key":"7105_CR34","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-014-0550-8","volume":"15","author":"MI Love","year":"2014","unstructured":"Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.","journal-title":"Genome Biol"},{"key":"7105_CR35","doi-asserted-by":"crossref","unstructured":"Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019:1;10.","DOI":"10.1038\/s41467-019-09234-6"},{"key":"7105_CR36","doi-asserted-by":"crossref","unstructured":"Letteboer SJ, Roepman R. Versatile Screening for Binary Protein\u2013Protein Interactions by Yeast Two-Hybrid Mating. In: Thompson JD, editor. Functional Proteomics: Methods and Protocols. Totowa NJ: Humana Press; 2008. p. 145\u201359. (Methods in Molecular Biology; vol. 484). Available from: http:\/\/link.springer.com\/10.1007\/978-1-59745-398-1.","DOI":"10.1007\/978-1-59745-398-1_10"},{"key":"7105_CR37","doi-asserted-by":"publisher","first-page":"e1006256","DOI":"10.1371\/journal.pgen.1006256","volume":"12","author":"D Murphy","year":"2016","unstructured":"Murphy D, Cieply B, Carstens R, Ramamurthy V, Stoilov P. The Musashi 1 Controls the Splicing of Photoreceptor-Specific Exons in the Vertebrate Retina. PLoS Genet. 2016;12:e1006256.","journal-title":"PLoS Genet"},{"key":"7105_CR38","doi-asserted-by":"crossref","unstructured":"Dorgau B, Collin J, Rozanska A, Boczonadi V, Moya-Molina M, Unsworth A, et al. Deciphering the spatiotemporal transcriptional and chromatin accessibility of human retinal organoid development at the single-cell level. iScience. 2024;27. Available from: https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2589004224006187.","DOI":"10.1016\/j.isci.2024.109397"},{"key":"7105_CR39","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1002\/ajmg.c.31826","volume":"184","author":"K Fujinami","year":"2020","unstructured":"Fujinami K, Oishi A, Yang L, Arno G, Pontikos N, Yoshitake K, et al. Clinical and genetic characteristics of 10 Japanese patients with PROM1-associated retinal disorder: A report of the phenotype spectrum and a literature review in the Japanese population. Am J Med Genet C Semin Med Genet. 2020;184:656\u201374.","journal-title":"Am J Med Genet C Semin Med Genet"},{"key":"7105_CR40","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1111\/tra.12618","volume":"20","author":"K Thamm","year":"2019","unstructured":"Thamm K, \u0160imait\u0117 D, Karbanov\u00e1 J, Berm\u00fadez V, Reichert D, Morgenstern A, et al. Prominin-1 (CD133) modulates the architecture and dynamics of microvilli. Traffic. 2019;20:39\u201360.","journal-title":"Traffic"},{"key":"7105_CR41","doi-asserted-by":"publisher","first-page":"e195752","DOI":"10.1001\/jamanetworkopen.2019.5752","volume":"2","author":"J Cehajic-Kapetanovic","year":"2019","unstructured":"Cehajic-Kapetanovic J, Birtel J, McClements ME, Shanks ME, Clouston P, Downes SM, et al. Clinical and Molecular Characterization of PROM1-Related Retinal Degeneration. JAMA Netw Open. 2019;2:e195752.","journal-title":"JAMA Netw Open"},{"key":"7105_CR42","doi-asserted-by":"publisher","first-page":"2297","DOI":"10.1523\/JNEUROSCI.2034-08.2009","volume":"29","author":"S Zacchigna","year":"2009","unstructured":"Zacchigna S, Oh H, Wilsch-Br\u00e4uninger M, Missol-Kolka E, J\u00e1szai J, Jansen S, et al. Loss of the cholesterol-binding protein Prominin-1\/CD133 causes disk dysmorphogenesis and photoreceptor degeneration. J Neurosci. 2009;29:2297\u2013308.","journal-title":"J Neurosci"},{"key":"7105_CR43","doi-asserted-by":"publisher","first-page":"164","DOI":"10.1167\/iovs.14-15479","volume":"56","author":"M Dellett","year":"2015","unstructured":"Dellett M, Sasai N, Nishide K, Becker S, Papadaki V, Astrid Limb G, et al. Genetic background and light-dependent progression of photoreceptor cell degeneration in Prominin-1 knockout mice. Invest Ophthalmol Vis Sci. 2015;56:164\u201376.","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"7105_CR44","first-page":"1709","volume":"15","author":"E Pras","year":"2009","unstructured":"Pras E, Abu A, Rotenstreich Y, Avni I, Reish O, Morad Y, et al. Cone-rod dystrophy and a frameshift mutation in the PROM1 gene. Mol Vis. 2009;15:1709\u201316.","journal-title":"Mol Vis"},{"key":"7105_CR45","doi-asserted-by":"publisher","first-page":"349","DOI":"10.3109\/13816810.2014.886266","volume":"36","author":"AO Khan","year":"2015","unstructured":"Khan AO, Bolz HJ. Pediatric Cone-Rod Dystrophy with High Myopia and Nystagmus Suggests Recessive PROM1 Mutations. Ophthalmic Genet. 2015;36:349\u201352.","journal-title":"Ophthalmic Genet"},{"key":"7105_CR46","doi-asserted-by":"publisher","first-page":"13953","DOI":"10.1074\/jbc.RA119.008618","volume":"294","author":"Z Lu","year":"2019","unstructured":"Lu Z, Hu X, Reilly J, Jia D, Liu F, Yu S, et al. Deletion of the transmembrane protein Prom1b in zebrafish disrupts outer-segment morphogenesis and causes photoreceptor degeneration. J Biol Chem. 2019;294:13953\u201363.","journal-title":"J Biol Chem"},{"key":"7105_CR47","first-page":"jcs253906","volume":"134","author":"BJ Carr","year":"2021","unstructured":"Carr BJ, Stanar P, Moritz OL. Distinct roles for prominin-1 and photoreceptor cadherin in outer segment disc morphogenesis in CRISPR-altered X. laevis. J Cell Sci. 2021;134:jcs253906.","journal-title":"J Cell Sci"},{"key":"7105_CR48","doi-asserted-by":"crossref","unstructured":"Barrio R, Sutherland JD, Rodriguez MS. Proteostasis and Disease From Basic Mechanisms to Clinics. Switzerland: Springer Nature; 2020. Vol. 1233. Available from: http:\/\/www.springer.com\/series\/5584.","DOI":"10.1007\/978-3-030-38266-7"},{"key":"7105_CR49","volume-title":"Proteostasis and Disease From Basic Mechanisms to Clinics","author":"V Toulis","year":"2020","unstructured":"Toulis V, Marfany G. By the Tips of Your Cilia: Ciliogenesis in the Retina and the Ubiquitin-Proteasome System. Proteostasis and Disease From Basic Mechanisms to Clinics. Springer Nature Switzerland; 2020. p. 303\u201310. http:\/\/www.springer.com\/series\/5584."},{"key":"7105_CR50","doi-asserted-by":"publisher","first-page":"6007","DOI":"10.1074\/jbc.RA119.011253","volume":"295","author":"J J\u00e1szai","year":"2020","unstructured":"J\u00e1szai J, Thamm K, Karbanov\u00e1 J, Janich P, Fargeas CA, Huttner WB, et al. Prominins control ciliary length throughout the animal kingdom: New lessons from human prominin-1 and zebrafish prominin-3. J Biol Chem. 2020;295:6007\u201322.","journal-title":"J Biol Chem"},{"key":"7105_CR51","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-15303-y","volume":"11","author":"HF Renard","year":"2020","unstructured":"Renard HF, Tyckaert F, Lo Giudice C, Hirsch T, Valades-Cruz CA, Lemaigre C, et al. Endophilin-A3 and Galectin-8 control the clathrin-independent endocytosis of CD166. Nat Commun. 2020;11:1457.","journal-title":"Nat Commun"},{"key":"7105_CR52","doi-asserted-by":"publisher","first-page":"190","DOI":"10.1111\/tra.12883","volume":"24","author":"C Lemaigre","year":"2023","unstructured":"Lemaigre C, Ceuppens A, Valades-Cruz CA, Ledoux B, Vanbeneden B, Hassan M, et al. N-BAR and F-BAR proteins\u2014endophilin-A3 and PSTPIP1\u2014control clathrin-independent endocytosis of L1CAM. Traffic. 2023;24:190\u2013212.","journal-title":"Traffic"},{"key":"7105_CR53","doi-asserted-by":"publisher","first-page":"161","DOI":"10.15403\/jgld.2014.1121.232.cm1","volume":"23","author":"C M\u01cergaritescu","year":"2014","unstructured":"M\u01cergaritescu C, Pirici D, Cherciu I, B\u01cerb\u01celan A, C\u00e2rt\u00e2n\u01ce T, S\u01ceftoiu A. CD133\/CD166\/Ki-67 Triple immunofluorescence assessment for putative cancer stem cells in colon carcinoma. J Gastrointestin Liver Dis. 2014;23:161\u201370.","journal-title":"J Gastrointestin Liver Dis"}],"container-title":["Cell Death &amp; Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07105-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07105-7","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07105-7.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,1]],"date-time":"2024-10-01T09:02:54Z","timestamp":1727773374000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41419-024-07105-7"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,1]]},"references-count":53,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2024,10]]}},"alternative-id":["7105"],"URL":"https:\/\/doi.org\/10.1038\/s41419-024-07105-7","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-4348361\/v1","asserted-by":"object"}]},"ISSN":["2041-4889"],"issn-type":[{"value":"2041-4889","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,1]]},"assertion":[{"value":"30 April 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"15 September 2024","order":2,"name":"revised","label":"Revised","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 September 2024","order":3,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 October 2024","order":4,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Human embryonic and foetal ocular material was provided with appropriate maternal written consent and approval from the Newcastle and North Tyneside NHS Health Authority Joint Ethics Committee (REC number: 08\/H0906\/21\u2009+\u20095). Adult human retinal samples were collected with proper consent and approval from NRES Committee Northeast - Newcastle & North Tyneside 1 (REC number: 18\/YH\/04\/20).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}}],"article-number":"721"}}