{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,4]],"date-time":"2026-05-04T13:11:29Z","timestamp":1777900289834,"version":"3.51.4"},"reference-count":93,"publisher":"The Company of Biologists","license":[{"start":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T00:00:00Z","timestamp":1621296000000},"content-version":"am","delay-in-days":503,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100005440","name":"Center for Scientific Review","doi-asserted-by":"publisher","award":["GM119016"],"award-info":[{"award-number":["GM119016"]}],"id":[{"id":"10.13039\/100005440","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004979","name":"Center for Innovative Technology","doi-asserted-by":"publisher","award":["ER14S-001-LS"],"award-info":[{"award-number":["ER14S-001-LS"]}],"id":[{"id":"10.13039\/100004979","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>A critical barrier in the treatment of endosomal and lysosomal diseases is the lack of understanding of the in vivo functions of the putative causative genes. We addressed this by investigating a key pair of endocytic adaptor proteins, PH domain containing endocytic trafficking adaptor 1 and 2 (PHETA1\/2, also known as FAM109A\/B, Ses1\/2, IPIP27A\/B), which interact with the protein product of OCRL, the causative gene for Lowe syndrome. Here we conducted the first study of PHETA1\/2 in vivo, utilizing the zebrafish system. We found that impairment of both zebrafish orthologs, pheta1 and pheta2, disrupted endocytosis and ciliogenesis in renal tissues. In addition, pheta1\/2 mutant animals exhibited reduced jaw size and delayed chondrocyte differentiation, indicating a role in craniofacial development. Deficiency of pheta1\/2 resulted in dysregulation of cathepsin K, which led to an increased abundance of type II collagen in craniofacial cartilages, a marker of immature cartilage extracellular matrix. Cathepsin K inhibition rescued the craniofacial phenotypes in the pheta1\/2 double mutants. The abnormal renal and craniofacial phenotypes in the pheta1\/2 mutant animals were consistent with the clinical presentations of a patient with a de novo arginine (R) to cysteine (C) variant (R6C) of PHETA1. Expressing the patient-specific variant in zebrafish exacerbated craniofacial deficits, suggesting that the R6C allele acts in a dominant-negative manner. Together, these results provide insights into the in vivo roles of PHETA1\/2 and suggest that the R6C variant is contributory to the pathogenesis of disease in the patient.<\/jats:p>","DOI":"10.1242\/dmm.041913","type":"journal-article","created":{"date-parts":[[2020,3,9]],"date-time":"2020-03-09T19:15:14Z","timestamp":1583781314000},"source":"Crossref","is-referenced-by-count":10,"title":["Deficiency in the endocytic adaptor proteins PHETA1\/2 impair renal and craniofacial development"],"prefix":"10.1242","author":[{"given":"Kristin M.","family":"Ates","sequence":"first","affiliation":[{"name":"Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, Augusta, GA 30912, USA"},{"name":"Center for Neurobiology Research, Fralin Biomedical Research Institute at Virginia Tech Carilion, Virginia Tech, Roanoke, VA 24016, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tong","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, Augusta, GA 30912, USA"},{"name":"JC Self Research Institute, Greenwood Genetic Center, Greenwood, SC 29646, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Trevor","family":"Moreland","sequence":"additional","affiliation":[{"name":"JC Self Research Institute, Greenwood Genetic Center, Greenwood, SC 29646, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rajalakshmi","family":"Veeranan-Karmegam","sequence":"additional","affiliation":[{"name":"Department of Cellular Biology and Anatomy, Medical College of Georgia, Augusta University, Augusta, GA 30912, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1905-3615","authenticated-orcid":false,"given":"Manxiu","family":"Ma","sequence":"additional","affiliation":[{"name":"Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, Augusta, GA 30912, USA"},{"name":"Center for Neurobiology Research, Fralin Biomedical Research Institute at Virginia Tech Carilion, Virginia Tech, Roanoke, VA 24016, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chelsi","family":"Jeter","sequence":"additional","affiliation":[{"name":"JC Self Research Institute, Greenwood Genetic Center, Greenwood, SC 29646, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8248-2514","authenticated-orcid":false,"given":"Priya","family":"Anand","sequence":"additional","affiliation":[{"name":"Institute of Nanotechnology, Karlsruhe Institute of Technology, Karlsruhe, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wolfgang","family":"Wenzel","sequence":"additional","affiliation":[{"name":"Institute of Nanotechnology, Karlsruhe Institute of Technology, Karlsruhe, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hyung-Goo","family":"Kim","sequence":"additional","affiliation":[{"name":"Neurological Disorder Research Center, Qatar Biomedical Research Institute, Hamad Bin Khalifa University, Doha, Qatar"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7628-5741","authenticated-orcid":false,"given":"Lynne A.","family":"Wolfe","sequence":"additional","affiliation":[{"name":"Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4278-6924","authenticated-orcid":false,"given":"Joshi A.","family":"Stephen","sequence":"additional","affiliation":[{"name":"Advanced Research Computing Unit, Division of Information Technology, Virginia Tech, Blacksburg, VA 24060, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David R.","family":"Adams","sequence":"additional","affiliation":[{"name":"Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2298-9759","authenticated-orcid":false,"given":"Thomas","family":"Markello","sequence":"additional","affiliation":[{"name":"Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3931-1207","authenticated-orcid":false,"given":"Cynthia J.","family":"Tifft","sequence":"additional","affiliation":[{"name":"Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Robert","family":"Settlage","sequence":"additional","affiliation":[{"name":"Advanced Research Computing Unit, Division of Information Technology, Virginia Tech, Blacksburg, VA 24060, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2494-6752","authenticated-orcid":false,"given":"William A.","family":"Gahl","sequence":"additional","affiliation":[{"name":"Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA"},{"name":"National Institutes of Health Undiagnosed Diseases Program, National Institutes of Health, Bethesda, Maryland 20892, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4458-8497","authenticated-orcid":false,"given":"Graydon B.","family":"Gonsalvez","sequence":"additional","affiliation":[{"name":"Department of Cellular Biology and Anatomy, Medical College of Georgia, Augusta University, Augusta, GA 30912, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1697-6959","authenticated-orcid":false,"given":"May Christine","family":"Malicdan","sequence":"additional","affiliation":[{"name":"Medical Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland 20892, USA"},{"name":"National Institutes of Health Undiagnosed Diseases Program, National Institutes of Health, Bethesda, Maryland 20892, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8295-0453","authenticated-orcid":false,"given":"Heather","family":"Flanagan-Steet","sequence":"additional","affiliation":[{"name":"JC Self Research Institute, Greenwood Genetic Center, Greenwood, SC 29646, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6485-5487","authenticated-orcid":false,"given":"Y. Albert","family":"Pan","sequence":"additional","affiliation":[{"name":"Department of Neuroscience and Regenerative Medicine, Medical College of Georgia, Augusta University, Augusta, GA 30912, USA"},{"name":"Center for Neurobiology Research, Fralin Biomedical Research Institute at Virginia Tech Carilion, Virginia Tech, Roanoke, VA 24016, USA"},{"name":"Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, VA 24060, USA"},{"name":"Department of Psychiatry and Behavioral Medicine, Virginia Tech Carilion School of Medicine, Roanoke, VA, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"237","published-online":{"date-parts":[[2020,1,1]]},"reference":[{"key":"2021042700252840500_DMM041913C1","doi-asserted-by":"publisher","first-page":"248","DOI":"10.1038\/nmeth0410-248","article-title":"A method and server for predicting damaging missense mutations","volume":"7","author":"Adzhubei","year":"2010","journal-title":"Nat. Methods"},{"key":"2021042700252840500_DMM041913C2","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1101\/gad.1171104","article-title":"Interactions between Sox9 and beta-catenin control chondrocyte differentiation","volume":"18","author":"Akiyama","year":"2004","journal-title":"Genes Dev."},{"key":"2021042700252840500_DMM041913C3","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1093\/bioinformatics\/btu638","article-title":"HTSeq--a Python framework to work with high-throughput sequencing data","volume":"31","author":"Anders","year":"2015","journal-title":"Bioinformatics"},{"key":"2021042700252840500_DMM041913C4","doi-asserted-by":"publisher","first-page":"2127","DOI":"10.1242\/jcs.02954","article-title":"Elucidation of megalin\/LRP2-dependent endocytic transport processes in the larval zebrafish pronephros","volume":"119","author":"Anzenberger","year":"2006","journal-title":"J. Cell Sci."},{"key":"2021042700252840500_DMM041913C5","doi-asserted-by":"publisher","first-page":"1","DOI":"10.2174\/1875036201307010001","article-title":"Comparison of sequencing utility programs","volume":"7","author":"Aronesty","year":"2013","journal-title":"Open Bioinformatics J."},{"key":"2021042700252840500_DMM041913C6","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1038\/358239a0","article-title":"The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase","volume":"358","author":"Attree","year":"1992","journal-title":"Nature"},{"key":"2021042700252840500_DMM041913C7","doi-asserted-by":"publisher","first-page":"90","DOI":"10.1091\/mbc.E15-06-0329","article-title":"OCRL1 engages with the F-BAR protein pacsin 2 to promote biogenesis of membrane-trafficking intermediates","volume":"27","author":"Billcliff","year":"2016","journal-title":"Mol. Biol. Cell"},{"key":"2021042700252840500_DMM041913C8","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1373\/clinchem.2008.112797","article-title":"The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments","volume":"55","author":"Bustin","year":"2009","journal-title":"Clin. Chem."},{"key":"2021042700252840500_DMM041913C9","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1136\/jmg.2009.067736","article-title":"Phenotype and genotype in mucolipidoses II and III alpha\/beta: a study of 61 probands","volume":"47","author":"Cathey","year":"2010","journal-title":"J. Med. Genet."},{"key":"2021042700252840500_DMM041913C10","doi-asserted-by":"publisher","first-page":"9965","DOI":"10.1074\/jbc.M807442200","article-title":"Differential clathrin binding and subcellular localization of OCRL1 splice isoforms","volume":"284","author":"Choudhury","year":"2009","journal-title":"J. Biol. Chem."},{"key":"2021042700252840500_DMM041913C11","doi-asserted-by":"publisher","first-page":"1835","DOI":"10.1093\/hmg\/ddr615","article-title":"The Lowe syndrome protein OCRL1 is involved in primary cilia assembly","volume":"21","author":"Coon","year":"2012","journal-title":"Hum. Mol. Genet."},{"key":"2021042700252840500_DMM041913C12","doi-asserted-by":"publisher","first-page":"839","DOI":"10.1038\/ncb3386","article-title":"Autophagosome-lysosome fusion triggers a lysosomal response mediated by TLR9 and controlled by OCRL","volume":"18","author":"De Leo","year":"2016","journal-title":"Nat. Cell Biol."},{"key":"2021042700252840500_DMM041913C13","doi-asserted-by":"publisher","first-page":"e2397","DOI":"10.1038\/cddis.2016.299","article-title":"Cnbp ameliorates Treacher Collins Syndrome craniofacial anomalies through a pathway that involves redox-responsive genes","volume":"7","author":"de Peralta","year":"2016","journal-title":"Cell Death Dis"},{"key":"2021042700252840500_DMM041913C14","doi-asserted-by":"publisher","first-page":"e337","DOI":"10.1002\/wdev.337","article-title":"Evolution and development of the fish jaw skeleton","volume":"8","author":"DeLaurier","year":"2019","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"2021042700252840500_DMM041913C15","doi-asserted-by":"publisher","first-page":"857","DOI":"10.1146\/annurev.biochem.78.081307.110540","article-title":"Mechanisms of endocytosis","volume":"78","author":"Doherty","year":"2009","journal-title":"Annu. Rev. Biochem."},{"key":"2021042700252840500_DMM041913C16","doi-asserted-by":"crossref","first-page":"4655","DOI":"10.1242\/dev.125.23.4655","article-title":"Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function","volume":"125","author":"Drummond","year":"1998","journal-title":"Development"},{"key":"2021042700252840500_DMM041913C17","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1002\/(SICI)1098-2302(199712)31:4&lt;267::AID-DEV4&gt;3.0.CO;2-P","article-title":"The development of eye movements in the zebrafish (Danio rerio)","volume":"31","author":"Easter","year":"1997","journal-title":"Dev. Psychobiol."},{"key":"2021042700252840500_DMM041913C18","doi-asserted-by":"publisher","first-page":"207","DOI":"10.1093\/nar\/30.1.207","article-title":"Gene expression omnibus: NCBI gene expression and hybridization array data repository","volume":"30","author":"Edgar","year":"2002","journal-title":"Nucleic Acids Res."},{"key":"2021042700252840500_DMM041913C19","doi-asserted-by":"publisher","DOI":"10.1038\/srep42583","article-title":"Cystinosis (ctns) zebrafish mutant shows pronephric glomerular and tubular dysfunction","volume":"7","author":"Elmonem","year":"2017","journal-title":"Sci. Rep."},{"key":"2021042700252840500_DMM041913C20","doi-asserted-by":"publisher","first-page":"2063","DOI":"10.2353\/ajpath.2009.090210","article-title":"Altered chondrocyte differentiation and extracellular matrix homeostasis in a zebrafish model for mucolipidosis II","volume":"175","author":"Flanagan-Steet","year":"2009","journal-title":"Am. J. Pathol."},{"key":"2021042700252840500_DMM041913C21","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1002\/jbmr.2722","article-title":"Cathepsin-mediated alterations in TGFss-related signaling underlie disrupted cartilage and bone maturation associated with impaired lysosomal targeting","volume":"31","author":"Flanagan-Steet","year":"2016","journal-title":"J. Bone Miner. Res."},{"key":"2021042700252840500_DMM041913C22","doi-asserted-by":"publisher","first-page":"2964","DOI":"10.1016\/j.celrep.2018.02.066","article-title":"TGF-ss regulates cathepsin activation during normal and pathogenic development","volume":"22","author":"Flanagan-Steet","year":"2018","journal-title":"Cell Rep"},{"key":"2021042700252840500_DMM041913C23","doi-asserted-by":"publisher","first-page":"8343","DOI":"10.1074\/jbc.M413913200","article-title":"Smad3 induces chondrogenesis through the activation of SOX9 via CREB-binding protein\/p300 recruitment","volume":"280","author":"Furumatsu","year":"2005","journal-title":"J. Biol. Chem."},{"key":"2021042700252840500_DMM041913C24","doi-asserted-by":"publisher","first-page":"e98186","DOI":"10.1371\/journal.pone.0098186","article-title":"Efficient mutagenesis by Cas9 protein-mediated oligonucleotide insertion and large-scale assessment of single-guide RNAs","volume":"9","author":"Gagnon","year":"2014","journal-title":"PLoS ONE"},{"key":"2021042700252840500_DMM041913C25","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1038\/gim.0b013e318232a005","article-title":"The national institutes of health undiagnosed diseases program: insights into rare diseases","volume":"14","author":"Gahl","year":"2012","journal-title":"Genet. Med."},{"key":"2021042700252840500_DMM041913C26","doi-asserted-by":"publisher","first-page":"1797","DOI":"10.1001\/jama.2015.12249","article-title":"The undiagnosed diseases network of the national institutes of health: a national extension","volume":"314","author":"Gahl","year":"2015","journal-title":"JAMA"},{"key":"2021042700252840500_DMM041913C27","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1016\/j.ymgme.2016.01.007","article-title":"The NIH undiagnosed diseases program and network: applications to modern medicine","volume":"117","author":"Gahl","year":"2016","journal-title":"Mol. Genet. Metab."},{"key":"2021042700252840500_DMM041913C28","doi-asserted-by":"publisher","first-page":"40996","DOI":"10.1074\/jbc.M509394200","article-title":"The modular adaptor protein autosomal recessive hypercholesterolemia (ARH) promotes low density lipoprotein receptor clustering into clathrin-coated pits","volume":"280","author":"Garuti","year":"2005","journal-title":"J. Biol. Chem."},{"key":"2021042700252840500_DMM041913C29","doi-asserted-by":"publisher","first-page":"923","DOI":"10.1016\/j.bmcl.2007.12.047","article-title":"The discovery of odanacatib (MK-0822), a selective inhibitor of cathepsin K","volume":"18","author":"Gauthier","year":"2008","journal-title":"Bioorg. Med. Chem. Lett."},{"key":"2021042700252840500_DMM041913C30","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1002\/jcb.20652","article-title":"The control of chondrogenesis","volume":"97","author":"Goldring","year":"2006","journal-title":"J. Cell. Biochem."},{"key":"2021042700252840500_DMM041913C31","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1111\/gbb.12220","article-title":"Differences in inhibitory avoidance, cortisol and brain gene expression in TL and AB zebrafish","volume":"14","author":"Gorissen","year":"2015","journal-title":"Genes Brain Behav."},{"key":"2021042700252840500_DMM041913C32","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1002\/bdrc.20064","article-title":"Aspects of extracellular matrix remodeling in development and disease","volume":"78","author":"Holmbeck","year":"2006","journal-title":"Birth Defects Res. C Embryo Today"},{"key":"2021042700252840500_DMM041913C33","doi-asserted-by":"publisher","first-page":"1899","DOI":"10.2741\/2810","article-title":"The optokinetic response in zebrafish and its applications","volume":"13","author":"Huang","year":"2008","journal-title":"Front. Biosci."},{"key":"2021042700252840500_DMM041913C34","doi-asserted-by":"publisher","first-page":"13904","DOI":"10.1073\/pnas.1308335110","article-title":"Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system","volume":"110","author":"Jao","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042700252840500_DMM041913C35","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1016\/S0091-679X(04)76018-5","article-title":"Development of cartilage and bone","volume":"76","author":"Javidan","year":"2004","journal-title":"Methods Cell Biol."},{"issue":"Suppl. 1","key":"2021042700252840500_DMM041913C36","doi-asserted-by":"publisher","first-page":"S7","DOI":"10.1186\/gb-2007-8-s1-s7","article-title":"Tol2: a versatile gene transfer vector in vertebrates","volume":"8","author":"Kawakami","year":"2007","journal-title":"Genome Biol."},{"key":"2021042700252840500_DMM041913C37","doi-asserted-by":"publisher","first-page":"845","DOI":"10.1038\/nprot.2015.053","article-title":"The Phyre2 web portal for protein modeling, prediction and analysis","volume":"10","author":"Kelley","year":"2015","journal-title":"Nat. Protoc."},{"key":"2021042700252840500_DMM041913C38","doi-asserted-by":"publisher","first-page":"656","DOI":"10.1101\/gr.229202","article-title":"BLAT--the BLAST-like alignment tool","volume":"12","author":"Kent","year":"2002","journal-title":"Genome Res."},{"key":"2021042700252840500_DMM041913C39","doi-asserted-by":"publisher","first-page":"996","DOI":"10.1101\/gr.229102","article-title":"The human genome browser at UCSC","volume":"12","author":"Kent","year":"2002","journal-title":"Genome Res."},{"key":"2021042700252840500_DMM041913C40","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"HISAT: a fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat. Methods"},{"key":"2021042700252840500_DMM041913C41","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1006\/dbio.1998.9016","article-title":"The shaping of pharyngeal cartilages during early development of the zebrafish","volume":"203","author":"Kimmel","year":"1998","journal-title":"Dev. Biol."},{"key":"2021042700252840500_DMM041913C42","doi-asserted-by":"publisher","first-page":"1570","DOI":"10.1016\/j.bbadis.2016.05.018","article-title":"Mannose 6-phosphate-dependent targeting of lysosomal enzymes is required for normal craniofacial and dental development","volume":"1862","author":"Koehne","year":"2016","journal-title":"Biochim. Biophys. Acta"},{"key":"2021042700252840500_DMM041913C43","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.ejcb.2009.10.008","article-title":"Mannose phosphorylation in health and disease","volume":"89","author":"Kollmann","year":"2010","journal-title":"Eur. J. Cell Biol."},{"key":"2021042700252840500_DMM041913C44","doi-asserted-by":"publisher","first-page":"152","DOI":"10.1016\/j.ygeno.2011.05.009","article-title":"Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies","volume":"98","author":"Kong","year":"2011","journal-title":"Genomics"},{"key":"2021042700252840500_DMM041913C45","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1172\/JCI112262","article-title":"Trafficking of lysosomal enzymes in normal and disease states","volume":"77","author":"Kornfeld","year":"1986","journal-title":"J. Clin. Invest."},{"key":"2021042700252840500_DMM041913C46","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1086\/500849","article-title":"Mucolipidosis II (I-cell disease) and mucolipidosis IIIA (classical pseudo-hurler polydystrophy) are caused by mutations in the GlcNAc-phosphotransferase \u03b1\/\u03b2-subunits precursor gene","volume":"78","author":"Kudo","year":"2006","journal-title":"Am. J. Hum. Genet."},{"key":"2021042700252840500_DMM041913C47","doi-asserted-by":"publisher","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: molecular evolutionary genetics analysis across computing platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"2021042700252840500_DMM041913C48","doi-asserted-by":"publisher","first-page":"13982","DOI":"10.1523\/JNEUROSCI.4226-07.2007","article-title":"The G59S mutation in p150glued causes dysfunction of dynactin in mice","volume":"27","author":"Lai","year":"2007","journal-title":"J. Neurosci."},{"key":"2021042700252840500_DMM041913C49","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0070172","article-title":"Inter-individual and inter-strain variations in zebrafish locomotor ontogeny","volume":"8","author":"Lange","year":"2013","journal-title":"PLoS ONE"},{"key":"2021042700252840500_DMM041913C50","doi-asserted-by":"publisher","first-page":"e1004726","DOI":"10.1371\/journal.pgen.1004726","article-title":"Fat-dachsous signaling coordinates cartilage differentiation and polarity during craniofacial development","volume":"10","author":"Le Pabic","year":"2014","journal-title":"PLoS Genet."},{"key":"2021042700252840500_DMM041913C51","doi-asserted-by":"publisher","first-page":"2550","DOI":"10.1002\/dvdy.22086","article-title":"Craniofacial skeletal defects of adult zebrafish Glypican 4 (knypek) mutants","volume":"238","author":"LeClair","year":"2009","journal-title":"Dev. Dyn."},{"key":"2021042700252840500_DMM041913C52","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1002\/cbin.10424","article-title":"The effect of the size of fluorescent dextran on its endocytic pathway","volume":"39","author":"Li","year":"2015","journal-title":"Cell Biol. Int."},{"key":"2021042700252840500_DMM041913C53","doi-asserted-by":"publisher","first-page":"1111","DOI":"10.1242\/dev.02806","article-title":"Notch signaling controls the differentiation of transporting epithelia and multiciliated cells in the zebrafish pronephros","volume":"134","author":"Liu","year":"2007","journal-title":"Development"},{"key":"2021042700252840500_DMM041913C54","doi-asserted-by":"publisher","first-page":"711","DOI":"10.1111\/j.1600-0854.2005.00311.x","article-title":"Structure and function of the Lowe syndrome protein OCRL1","volume":"6","author":"Lowe","year":"2005","journal-title":"Traffic"},{"key":"2021042700252840500_DMM041913C55","doi-asserted-by":"publisher","first-page":"3333","DOI":"10.1093\/hmg\/dds163","article-title":"OCRL localizes to the primary cilium: a new role for cilia in Lowe syndrome","volume":"21","author":"Luo","year":"2012","journal-title":"Hum. Mol. Genet."},{"key":"2021042700252840500_DMM041913C56","doi-asserted-by":"publisher","first-page":"895","DOI":"10.1046\/j.1095-8649.2003.00074.x","article-title":"Morphological development of the gonads in zebrafish","volume":"62","author":"Maack","year":"2003","journal-title":"J. Fish Biol."},{"key":"2021042700252840500_DMM041913C57","doi-asserted-by":"publisher","first-page":"1831","DOI":"10.1038\/emboj.2009.155","article-title":"A PH domain within OCRL bridges clathrin-mediated membrane trafficking to phosphoinositide metabolism","volume":"28","author":"Mao","year":"2009","journal-title":"EMBO J."},{"key":"2021042700252840500_DMM041913C58","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1111\/tra.12160","article-title":"The cellular and physiological functions of the Lowe syndrome protein OCRL1","volume":"15","author":"Mehta","year":"2014","journal-title":"Traffic"},{"key":"2021042700252840500_DMM041913C59","doi-asserted-by":"publisher","first-page":"W401","DOI":"10.1093\/nar\/gku410","article-title":"CHOPCHOP: a CRISPR\/Cas9 and TALEN web tool for genome editing","volume":"42","author":"Montague","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"2021042700252840500_DMM041913C60","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/bs.ctdb.2015.07.001","article-title":"Zebrafish craniofacial development: a window into early patterning","volume":"115","author":"Mork","year":"2015","journal-title":"Curr. Top. Dev. Biol."},{"key":"2021042700252840500_DMM041913C61","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1242\/dev.059345","article-title":"Ubiquitous transgene expression and Cre-based recombination driven by the ubiquitin promoter in zebrafish","volume":"138","author":"Mosimann","year":"2011","journal-title":"Development"},{"key":"2021042700252840500_DMM041913C62","doi-asserted-by":"publisher","first-page":"606","DOI":"10.1091\/mbc.e10-08-0730","article-title":"The PH domain proteins IPIP27A and B link OCRL1 to receptor recycling in the endocytic pathway","volume":"22","author":"Noakes","year":"2011","journal-title":"Mol. Biol. Cell"},{"key":"2021042700252840500_DMM041913C63","doi-asserted-by":"publisher","first-page":"F244","DOI":"10.1152\/ajprenal.2001.280.2.F244","article-title":"An endocytosis defect as a possible cause of proteinuria in polycystic kidney disease","volume":"280","author":"Obermuller","year":"2001","journal-title":"Am. J. Physiol. Renal. Physiol."},{"key":"2021042700252840500_DMM041913C64","doi-asserted-by":"publisher","first-page":"e1005058","DOI":"10.1371\/journal.pgen.1005058","article-title":"The Lowe syndrome protein OCRL1 is required for endocytosis in the zebrafish pronephric tubule","volume":"11","author":"Oltrabella","year":"2015","journal-title":"PLoS Genet."},{"key":"2021042700252840500_DMM041913C65","doi-asserted-by":"publisher","first-page":"591","DOI":"10.1242\/dev.076588","article-title":"Robo2 determines subtype-specific axonal projections of trigeminal sensory neurons","volume":"139","author":"Pan","year":"2012","journal-title":"Development"},{"key":"2021042700252840500_DMM041913C66","doi-asserted-by":"publisher","first-page":"1073","DOI":"10.1093\/bioinformatics\/btm076","article-title":"COBALT: constraint-based alignment tool for multiple protein sequences","volume":"23","author":"Papadopoulos","year":"2007","journal-title":"Bioinformatics"},{"key":"2021042700252840500_DMM041913C67","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1242\/dmm.008219","article-title":"Excessive activity of cathepsin K is associated with cartilage defects in a zebrafish model of mucolipidosis II","volume":"5","author":"Petrey","year":"2012","journal-title":"Dis. Model. Mech."},{"key":"2021042700252840500_DMM041913C68","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1242\/dmm.015545","article-title":"Zebrafish models in translational research: tipping the scales toward advancements in human health","volume":"7","author":"Phillips","year":"2014","journal-title":"Dis. Model. Mech."},{"key":"2021042700252840500_DMM041913C69","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1038\/nsmb.2071","article-title":"Recognition of the F&H motif by the Lowe syndrome protein OCRL","volume":"18","author":"Pirruccello","year":"2011","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2021042700252840500_DMM041913C70","doi-asserted-by":"publisher","first-page":"10102","DOI":"10.1523\/JNEUROSCI.2740-08.2008","article-title":"Zebrafish TRPA1 channels are required for chemosensation but not for thermosensation or mechanosensory hair cell function","volume":"28","author":"Prober","year":"2008","journal-title":"J. Neurosci."},{"key":"2021042700252840500_DMM041913C71","doi-asserted-by":"publisher","first-page":"1744","DOI":"10.1093\/hmg\/ddr608","article-title":"Impaired neural development in a zebrafish model for Lowe syndrome","volume":"21","author":"Ramirez","year":"2012","journal-title":"Hum. Mol. Genet."},{"key":"2021042700252840500_DMM041913C72","doi-asserted-by":"publisher","first-page":"1039","DOI":"10.1038\/nmeth.3581","article-title":"Whole-brain activity mapping onto a zebrafish brain atlas","volume":"12","author":"Randlett","year":"2015","journal-title":"Nat. Methods"},{"key":"2021042700252840500_DMM041913C73","doi-asserted-by":"publisher","first-page":"1295","DOI":"10.1111\/j.1600-0854.2012.01387.x","article-title":"OCRL1 modulates cilia length in renal epithelial cells","volume":"13","author":"Rbaibi","year":"2012","journal-title":"Traffic"},{"key":"2021042700252840500_DMM041913C74","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1038\/nprot.2010.5","article-title":"I-TASSER: a unified platform for automated protein structure and function prediction","volume":"5","author":"Roy","year":"2010","journal-title":"Nat. Protoc."},{"key":"2021042700252840500_DMM041913C75","doi-asserted-by":"publisher","first-page":"294","DOI":"10.3389\/fnmol.2018.00294","article-title":"Zebrafish models of neurodevelopmental disorders: past, present, and future","volume":"11","author":"Sakai","year":"2018","journal-title":"Front. Mol. Neurosci."},{"key":"2021042700252840500_DMM041913C76","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1016\/j.plipres.2009.06.001","article-title":"Mammalian phosphoinositide kinases and phosphatases","volume":"48","author":"Sasaki","year":"2009","journal-title":"Prog. Lipid Res."},{"key":"2021042700252840500_DMM041913C77","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nat. Methods"},{"key":"2021042700252840500_DMM041913C78","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1038\/nmeth.2890","article-title":"MutationTaster2: mutation prediction for the deep-sequencing age","volume":"11","author":"Schwarz","year":"2014","journal-title":"Nat. Methods"},{"key":"2021042700252840500_DMM041913C79","doi-asserted-by":"publisher","first-page":"W452","DOI":"10.1093\/nar\/gks539","article-title":"SIFT web server: predicting effects of amino acid substitutions on proteins","volume":"40","author":"Sim","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"2021042700252840500_DMM041913C80","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.jgg.2016.02.001","article-title":"Zebrafish as a model for human ciliopathies","volume":"43","author":"Song","year":"2016","journal-title":"J. Genet. Genomics"},{"key":"2021042700252840500_DMM041913C81","doi-asserted-by":"publisher","first-page":"3511","DOI":"10.1073\/pnas.0914658107","article-title":"Two closely related endocytic proteins that share a common OCRL-binding motif with APPL1","volume":"107","author":"Swan","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2021042700252840500_DMM041913C82","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1111\/j.0009-9163.2004.00215.x","article-title":"The clinical picture of the B\u00f6rjeson-Forssman-Lehmann syndrome in males and heterozygous females with PHF6 mutations","volume":"65","author":"Turner","year":"2004","journal-title":"Clin. Genet."},{"key":"2021042700252840500_DMM041913C83","doi-asserted-by":"publisher","first-page":"14726","DOI":"10.1021\/ja4056068","article-title":"Improved quenched fluorescent probe for imaging of cysteine cathepsin activity","volume":"135","author":"Verdoes","year":"2013","journal-title":"J. Am. Chem. Soc."},{"key":"2021042700252840500_DMM041913C84","doi-asserted-by":"publisher","first-page":"722","DOI":"10.1086\/367847","article-title":"Mutations in the small GTP-ase late endosomal protein RAB7 cause Charcot-Marie-Tooth type 2B neuropathy","volume":"72","author":"Verhoeven","year":"2003","journal-title":"Am. J. Hum. Genet."},{"key":"2021042700252840500_DMM041913C85","doi-asserted-by":"publisher","first-page":"4970","DOI":"10.1038\/emboj.2011.354","article-title":"OCRL controls trafficking through early endosomes via PtdIns4,5P2-dependent regulation of endosomal actin","volume":"30","author":"Vicinanza","year":"2011","journal-title":"EMBO J."},{"key":"2021042700252840500_DMM041913C86","doi-asserted-by":"publisher","first-page":"264","DOI":"10.3390\/cells8030264","article-title":"Cysteine cathepsins and their extracellular roles: shaping the microenvironment","volume":"8","author":"Vidak","year":"2019","journal-title":"Cells"},{"key":"2021042700252840500_DMM041913C87","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1080\/10520290701333558","article-title":"A two-color acid-free cartilage and bone stain for zebrafish larvae","volume":"82","author":"Walker","year":"2007","journal-title":"Biotech. Histochem."},{"key":"2021042700252840500_DMM041913C88","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.1534\/genetics.114.169284","article-title":"Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains","volume":"198","author":"Wilson","year":"2014","journal-title":"Genetics"},{"key":"2021042700252840500_DMM041913C89","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1002\/prot.21945","article-title":"MUSTER: improving protein sequence profile-profile alignments by using multiple sources of structure information","volume":"72","author":"Wu","year":"2008","journal-title":"Proteins"},{"key":"2021042700252840500_DMM041913C90","doi-asserted-by":"crossref","first-page":"5065","DOI":"10.1242\/dev.129.21.5065","article-title":"A zebrafish sox9 gene required for cartilage morphogenesis","volume":"129","author":"Yan","year":"2002","journal-title":"Development"},{"key":"2021042700252840500_DMM041913C91","doi-asserted-by":"publisher","first-page":"973","DOI":"10.1016\/j.addr.2004.12.013","article-title":"The role of cathepsins in osteoporosis and arthritis: rationale for the design of new therapeutics","volume":"57","author":"Yasuda","year":"2005","journal-title":"Adv. Drug Deliv. Rev."},{"key":"2021042700252840500_DMM041913C92","doi-asserted-by":"publisher","first-page":"D754","DOI":"10.1093\/nar\/gkx1098","article-title":"Ensembl 2018","volume":"46","author":"Zerbino","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"2021042700252840500_DMM041913C93","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1038\/ng1514","article-title":"Mutations in the pleckstrin homology domain of dynamin 2 cause dominant intermediate Charcot-Marie-Tooth disease","volume":"37","author":"Z\u00fcchner","year":"2005","journal-title":"Nat. Genet."}],"container-title":["Disease Models &amp; Mechanisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1242\/dmm.041913","content-type":"unspecified","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dmm\/article-pdf\/doi\/10.1242\/dmm.041913\/1973479\/dmm041913.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dmm\/article-pdf\/doi\/10.1242\/dmm.041913\/2065787\/dmm_041913v1.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/journals.biologists.com\/dmm\/article-pdf\/doi\/10.1242\/dmm.041913\/2065787\/dmm_041913v1.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,18]],"date-time":"2021-05-18T18:44:24Z","timestamp":1621363464000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.biologists.com\/dmm\/article\/doi\/10.1242\/dmm.041913\/267164\/Deficiency-in-the-endocytic-adaptor-proteins"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,1]]},"references-count":93,"URL":"https:\/\/doi.org\/10.1242\/dmm.041913","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/727578","asserted-by":"object"}]},"ISSN":["1754-8411","1754-8403"],"issn-type":[{"value":"1754-8411","type":"electronic"},{"value":"1754-8403","type":"print"}],"subject":[],"published":{"date-parts":[[2020,1,1]]},"article-number":"dmm.041913"}}