{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,22]],"date-time":"2026-10-22T07:56:16Z","timestamp":1792655776154,"version":"4.5.0"},"reference-count":67,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2016,7,20]],"date-time":"2016-07-20T00:00:00Z","timestamp":1468972800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2016,7,20]],"date-time":"2016-07-20T00:00:00Z","timestamp":1468972800000},"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":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Post-translational modifications are necessary for collagen precursor molecules (procollagens) to acquire final shape and function. However, the mechanism and contribution of collagen modifications that occur outside the endoplasmic reticulum and Golgi are not understood. We discovered that VIPAR, with its partner proteins, regulate sorting of lysyl hydroxylase 3 (LH3, also known as PLOD3) into newly identified post-Golgi collagen IV carriers and that VIPAR-dependent sorting is essential for modification of lysines in multiple collagen types. Identification of structural and functional collagen abnormalities in cells and tissues from patients and murine models of the autosomal recessive multisystem disorder Arthrogryposis, Renal dysfunction and Cholestasis syndrome caused by VIPAR and VPS33B deficiencies confirmed our findings. Thus, regulation of post-Golgi LH3 trafficking is essential for collagen homeostasis and for the development and function of multiple organs and tissues.<\/jats:p>","DOI":"10.1038\/ncomms12111","type":"journal-article","created":{"date-parts":[[2016,7,20]],"date-time":"2016-07-20T09:58:55Z","timestamp":1469008735000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":76,"title":["Regulation of post-Golgi LH3 trafficking is essential for collagen homeostasis"],"prefix":"10.1038","volume":"7","author":[{"given":"Blerida","family":"Banushi","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federico","family":"Forneris","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Straatman-Iwanowska","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Strange","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne-Marie","family":"Lyne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clare","family":"Rogerson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5894-7043","authenticated-orcid":false,"given":"Jemima J.","family":"Burden","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wendy E.","family":"Heywood","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanna","family":"Hanley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivan","family":"Doykov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kornelis R.","family":"Straatman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Holly","family":"Smith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Danai","family":"Bem","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0149-145X","authenticated-orcid":false,"given":"Janos","family":"Kriston-Vizi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gema","family":"Ariceta","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maija","family":"Risteli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunguang","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosalyn E.","family":"Ardill","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marcin","family":"Zaniew","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julita","family":"Latka-Grot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simon N.","family":"Waddington","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"S. J.","family":"Howe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Ferraro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asllan","family":"Gjinovci","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Scott","family":"Lawrence","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Marsh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Girolami","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laurent","family":"Bozec","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin","family":"Mills","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9712-6122","authenticated-orcid":false,"given":"Paul","family":"Gissen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2016,7,20]]},"reference":[{"key":"BFncomms12111_CR1","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1002\/jcp.21036","volume":"212","author":"R Myllyl\u00e4","year":"2007","unstructured":"Myllyl\u00e4, R. et al. Expanding the lysyl hydroxylase toolbox: new insights into the localisation and activities of lysyl hydroxylase 3 (LH3). J. Cell Physiol. 212, 323\u2013329 (2007).","journal-title":"J. Cell Physiol."},{"key":"BFncomms12111_CR2","doi-asserted-by":"publisher","first-page":"18568","DOI":"10.1074\/jbc.M201389200","volume":"277","author":"C Wang","year":"2002","unstructured":"Wang, C. et al. Identification of amino acids important for the catalytic activity of the collagen glucosyltransferase associated with the multifunctional lysyl hydroxylase 3 (LH3). J. Biol. Chem. 277, 18568\u201318573 (2002).","journal-title":"J. Biol. Chem."},{"key":"BFncomms12111_CR3","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/S8756-3282(97)00279-2","volume":"22","author":"L Knott","year":"1998","unstructured":"Knott, L. & Bailey, A. J. Collagen cross-links in mineralising tissues: a review of their chemistry, function, and clinical relevance. Bone 22, 181\u2013187 (1998).","journal-title":"Bone"},{"key":"BFncomms12111_CR4","doi-asserted-by":"publisher","first-page":"2439","DOI":"10.1096\/fasebj.6.7.1348714","volume":"6","author":"K Reiser","year":"1992","unstructured":"Reiser, K. et al. Enzymatic and nonenzymatic cross-linking of collagen and elastin. FASEB J. 6, 2439\u20132449 (1992).","journal-title":"FASEB J."},{"key":"BFncomms12111_CR5","doi-asserted-by":"publisher","first-page":"33381","DOI":"10.1074\/jbc.M704198200","volume":"282","author":"L Sipila","year":"2007","unstructured":"Sipila, L. et al. Secretion and assembly of type IV and VI collagens depend on glycosylation of hydroxylysines. J. Biol. Chem. 282, 33381\u201333388 (2007).","journal-title":"J. Biol. Chem."},{"key":"BFncomms12111_CR6","doi-asserted-by":"publisher","first-page":"28204","DOI":"10.1074\/jbc.M109.038190","volume":"284","author":"M Risteli","year":"2009","unstructured":"Risteli, M. et al. Reduction of lysyl hydroxylase 3 causes deleterious changes in the deposition and organization of extracellular matrix. J. Biol. Chem. 284, 28204\u201328211 (2009).","journal-title":"J. Biol. Chem."},{"key":"BFncomms12111_CR7","doi-asserted-by":"publisher","first-page":"14120","DOI":"10.1073\/pnas.0404966101","volume":"101","author":"K Rautavuoma","year":"2004","unstructured":"Rautavuoma, K. et al. Premature aggregation of type IV collagen and early lethality in lysyl hydroxylase 3 null mice. Proc. Natl Acad. Sci. USA 101, 14120\u201314125 (2004).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms12111_CR8","doi-asserted-by":"publisher","first-page":"625","DOI":"10.1242\/jcs.02780","volume":"119","author":"H Ruotsalainen","year":"2006","unstructured":"Ruotsalainen, H. et al. Glycosylation catalysed by lysyl hydroxylase 3 is essential for basement membranes. J. Cell Sci. 119, 625\u2013635 (2006).","journal-title":"J. Cell Sci."},{"key":"BFncomms12111_CR9","doi-asserted-by":"publisher","first-page":"508","DOI":"10.1111\/j.1582-4934.2008.00286.x","volume":"13","author":"C Wang","year":"2009","unstructured":"Wang, C. et al. The glycosyltransferase activities of lysyl hydroxylase 3 (LH3) in the extracellular space are important for cell growth and viability. J. Cell Mol. Med. 13, 508\u2013521 (2009).","journal-title":"J. Cell Mol. Med."},{"key":"BFncomms12111_CR10","doi-asserted-by":"publisher","first-page":"668","DOI":"10.1002\/jcp.22774","volume":"227","author":"C Wang","year":"2012","unstructured":"Wang, C., Ristiluoma, M. M., Salo, A. M., Eskelinen, S. & Myllyl\u00e4, R. Lysyl hydroxylase 3 is secreted from cells by two pathways. J. Cell Physiol. 227, 668\u2013675 (2012).","journal-title":"J. Cell Physiol."},{"key":"BFncomms12111_CR11","doi-asserted-by":"publisher","first-page":"644","DOI":"10.1002\/jcp.20596","volume":"207","author":"AM Salo","year":"2006","unstructured":"Salo, A. M. et al. Lysyl hydroxylase 3 (LH3) modifies proteins in the extracellular space, a novel mechanism for matrix remodeling. J. Cell Physiol. 207, 644\u2013653 (2006).","journal-title":"J. Cell Physiol."},{"key":"BFncomms12111_CR12","doi-asserted-by":"publisher","first-page":"1225","DOI":"10.1083\/jcb.200108073","volume":"155","author":"AA Mironov","year":"2001","unstructured":"Mironov, A. A. et al. Small cargo proteins and large aggregates can traverse the Golgi by a common mechanism without leaving the lumen of cisternae. J. Cell Biol. 155, 1225\u20131238 (2001).","journal-title":"J. Cell Biol."},{"key":"BFncomms12111_CR13","doi-asserted-by":"publisher","first-page":"1071","DOI":"10.1038\/ncb1180","volume":"6","author":"A Trucco","year":"2004","unstructured":"Trucco, A. et al. Secretory traffic triggers the formation of tubular continuities across Golgi sub-compartments. Nat. Cell Biol. 6, 1071\u20131081 (2004).","journal-title":"Nat. Cell Biol."},{"key":"BFncomms12111_CR14","doi-asserted-by":"publisher","first-page":"a005215","DOI":"10.1101\/cshperspect.a005215","volume":"3","author":"BS Glick","year":"2011","unstructured":"Glick, B. S. & Luini, A. Models for Golgi traffic: a critical assessment. Cold Spring Harb. Perspect. Biol. 3, a005215\u2013a005215 (2011).","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"BFncomms12111_CR15","doi-asserted-by":"publisher","first-page":"691","DOI":"10.1111\/tra.12060","volume":"14","author":"MB Cutrona","year":"2013","unstructured":"Cutrona, M. B. et al. Silencing of mammalian Sar1 isoforms reveals COPII-independent protein sorting and transport. Traffic 14, 691\u2013708 (2013).","journal-title":"Traffic"},{"key":"BFncomms12111_CR16","doi-asserted-by":"publisher","first-page":"993","DOI":"10.1016\/S0092-8674(00)81723-7","volume":"95","author":"L Bonfanti","year":"1998","unstructured":"Bonfanti, L. et al. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell 95, 993\u20131003 (1998).","journal-title":"Cell"},{"key":"BFncomms12111_CR17","doi-asserted-by":"publisher","first-page":"400","DOI":"10.1038\/ng1325","volume":"36","author":"P Gissen","year":"2004","unstructured":"Gissen, P. et al. Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nat. Genet. 36, 400\u2013404 (2004).","journal-title":"Nat. Genet."},{"key":"BFncomms12111_CR18","doi-asserted-by":"publisher","first-page":"394","DOI":"10.1007\/s00439-006-0232-z","volume":"120","author":"P Gissen","year":"2006","unstructured":"Gissen, P. et al. Clinical and molecular genetic features of ARC syndrome. Hum. Genet. 120, 394\u2013409 (2006).","journal-title":"Hum. Genet."},{"key":"BFncomms12111_CR19","doi-asserted-by":"publisher","first-page":"4159","DOI":"10.1182\/blood-2005-04-1356","volume":"106","author":"B Lo","year":"2005","unstructured":"Lo, B. et al. Requirement of VPS33B, a member of the Sec1\/Munc18 protein family, in megakaryocyte and platelet alpha-granule biogenesis. Blood 106, 4159\u20134166 (2005).","journal-title":"Blood"},{"key":"BFncomms12111_CR20","doi-asserted-by":"publisher","first-page":"303","DOI":"10.1038\/ng.538","volume":"42","author":"A Cullinane","year":"2010","unstructured":"Cullinane, A. et al. Mutations in VIPAR cause an arthrogryposis, renal dysfunction and cholestasis syndrome phenotype with defects in epithelial polarisation. Nat. Genet. 42, 303\u2013312 (2010).","journal-title":"Nat. Genet."},{"key":"BFncomms12111_CR21","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1016\/j.ajhg.2008.09.004","volume":"83","author":"AM Salo","year":"2008","unstructured":"Salo, A. M. et al. A connective tissue disorder caused by mutations of the lysyl hydroxylase 3 gene. Am. J. Hum. Genet. 83, 495\u2013503 (2008).","journal-title":"Am. J. Hum. Genet."},{"key":"BFncomms12111_CR22","doi-asserted-by":"publisher","first-page":"1307","DOI":"10.1242\/jcs.107805","volume":"126","author":"HJ Balderhaar","year":"2013","unstructured":"Balderhaar, H. J. & Ungermann, C. CORVET and HOPS tethering complexes - coordinators of endosome and lysosome fusion. J. Cell Sci. 126, 1307\u20131316 (2013).","journal-title":"J. Cell Sci."},{"key":"BFncomms12111_CR23","doi-asserted-by":"publisher","first-page":"13345","DOI":"10.1073\/pnas.1307074110","volume":"110","author":"SC Graham","year":"2013","unstructured":"Graham, S. C. et al. Structural basis of Vps33A recruitment to the human HOPS complex by Vps16.. Proc. Natl Acad. Sci. USA 110, 13345\u201313350 (2013).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms12111_CR24","doi-asserted-by":"publisher","first-page":"e67409","DOI":"10.1371\/journal.pone.0067409","volume":"8","author":"RW Baker","year":"2013","unstructured":"Baker, R. W., Jeffrey, P. D. & Hughson, F. M. Crystal structures of the Sec1\/Munc18 (SM) protein Vps33, alone and bound to the homotypic fusion and vacuolar protein sorting (HOPS) subunit Vps16. PLoS ONE 8, e67409 (2013).","journal-title":"PLoS ONE"},{"key":"BFncomms12111_CR25","doi-asserted-by":"publisher","first-page":"1366","DOI":"10.1111\/tra.12232","volume":"15","author":"ED Perini","year":"2014","unstructured":"Perini, E. D., Schaefer, R., St\u00f6ter, M., Kalaidzidis, Y. & Zerial, M. Mammalian CORVET is required for fusion and conversion of distinct early endosome subpopulations. Traffic 15, 1366\u20131389 (2014).","journal-title":"Traffic"},{"key":"BFncomms12111_CR26","doi-asserted-by":"publisher","first-page":"727","DOI":"10.1111\/tra.12283","volume":"16","author":"L Wartosch","year":"2015","unstructured":"Wartosch, L., G\u00fcnesdogan, U., Graham, S. C. & Luzio, J. P. Recruitment of VPS33A to HOPS by VPS16 is required for lysosome fusion with endosomes and autophagosomes. Traffic 16, 727\u2013742 (2015).","journal-title":"Traffic"},{"key":"BFncomms12111_CR27","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1016\/S1534-5807(03)00294-6","volume":"5","author":"AA Mironov","year":"2003","unstructured":"Mironov, A. A. et al. ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains. Dev. Cell 5, 583\u2013594 (2003).","journal-title":"Dev. Cell"},{"key":"BFncomms12111_CR28","doi-asserted-by":"publisher","first-page":"1055","DOI":"10.1016\/j.cell.2008.04.044","volume":"133","author":"GH Patterson","year":"2008","unstructured":"Patterson, G. H. et al. Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133, 1055\u20131067 (2008).","journal-title":"Cell"},{"key":"BFncomms12111_CR29","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1146\/annurev-cellbio-100913-013002","volume":"31","author":"V Malhotra","year":"2015","unstructured":"Malhotra, V. & Erlmann, P. The pathway of collagen secretion. Annu. Rev. Cell Dev. Biol. 31, 109\u2013124 (2015).","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"BFncomms12111_CR30","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1083\/jcb.201306010","volume":"202","author":"FA Barr","year":"2013","unstructured":"Barr, F. A. Review series: Rab GTPases and membrane identity: causal or inconsequential? J. Cell Biol. 202, 191\u2013199 (2013).","journal-title":"J. Cell Biol."},{"key":"BFncomms12111_CR31","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.devcel.2011.11.008","volume":"22","author":"MA Dozynkiewicz","year":"2012","unstructured":"Dozynkiewicz, M. A. et al. Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes\/lysosomes and drive cancer progression. Dev. Cell 22, 131\u2013145 (2012).","journal-title":"Dev. Cell"},{"key":"BFncomms12111_CR32","doi-asserted-by":"publisher","first-page":"2005","DOI":"10.1038\/ncomms3005","volume":"4","author":"Y Liu","year":"2013","unstructured":"Liu, Y. et al. Myosin Vb controls biogenesis of post-Golgi Rab10 carriers during axon development. Nat. Commun. 4, 2005 (2013).","journal-title":"Nat. Commun."},{"key":"BFncomms12111_CR33","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/j.devcel.2012.12.005","volume":"24","author":"DW Lerner","year":"2013","unstructured":"Lerner, D. W. et al. A Rab10-dependent mechanism for polarised basement membrane secretion during organ morphogenesis. Dev. Cell 24, 159\u2013168 (2013).","journal-title":"Dev. Cell"},{"key":"BFncomms12111_CR34","doi-asserted-by":"publisher","first-page":"3","DOI":"10.2202\/1544-6115.1027","volume":"3","author":"GK Smyth","year":"2004","unstructured":"Smyth, G. K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, (1): 3 (2004).","journal-title":"Stat. Appl. Genet. Mol. Biol."},{"key":"BFncomms12111_CR35","doi-asserted-by":"publisher","first-page":"R183","DOI":"10.1186\/gb-2007-8-9-r183","volume":"8","author":"DW Huang","year":"2007","unstructured":"Huang, D. W. et al. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyse large gene lists. Genome Biol. 8, R183 (2007).","journal-title":"Genome Biol."},{"key":"BFncomms12111_CR36","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1186\/1471-2105-10-47","volume":"10","author":"M Ackermann","year":"2009","unstructured":"Ackermann, M. & Strimmer, K. A general modular framework for gene set enrichment analysis. BMC Bioinformatics 10, 47 (2009).","journal-title":"BMC Bioinformatics"},{"key":"BFncomms12111_CR37","doi-asserted-by":"publisher","first-page":"15545","DOI":"10.1073\/pnas.0506580102","volume":"102","author":"A Subramanian","year":"2005","unstructured":"Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545\u201315550 (2005).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms12111_CR38","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1182\/blood-2014-12-614677","volume":"126","author":"D Bem","year":"2015","unstructured":"Bem, D. et al. VPS33B regulates protein sorting into and maturation of \u03b1-granule progenitor organelles in mouse megakaryocytes. Blood 126, 133\u2013143 (2015).","journal-title":"Blood"},{"key":"BFncomms12111_CR39","doi-asserted-by":"publisher","first-page":"22998","DOI":"10.1074\/jbc.M112.343954","volume":"287","author":"M Sricholpech","year":"2012","unstructured":"Sricholpech, M. et al. Lysyl hydroxylase 3-mediated glucosylation in type I collagen. J. Biol. Chem. 287, 22998\u201323009 (2012).","journal-title":"J. Biol. Chem."},{"key":"BFncomms12111_CR40","doi-asserted-by":"publisher","first-page":"1223","DOI":"10.1091\/mbc.e08-07-0728","volume":"20","author":"GD Zhu","year":"2009","unstructured":"Zhu, G. D. et al. SPE-39 family proteins interact with the HOPS complex and function in lysosomal delivery. Mol. Biol. Cell 20, 1223\u20131240 (2009).","journal-title":"Mol. Biol. Cell"},{"key":"BFncomms12111_CR41","doi-asserted-by":"publisher","first-page":"5215","DOI":"10.1093\/hmg\/ddt378","volume":"22","author":"K Tornieri","year":"2013","unstructured":"Tornieri, K. et al. Vps33b pathogenic mutations preferentially affect VIPAS39\/SPE-39-positive endosomes. Hum. Mol. Genet. 22, 5215\u20135228 (2013).","journal-title":"Hum. Mol. Genet."},{"key":"BFncomms12111_CR42","doi-asserted-by":"publisher","first-page":"2743","DOI":"10.1111\/febs.12151","volume":"280","author":"JA Solinger","year":"2013","unstructured":"Solinger, J. A. & Spang, A. Tethering complexes in the endocytic pathway: CORVET and HOPS. FEBS J. 280, 2743\u20132757 (2013).","journal-title":"FEBS J."},{"key":"BFncomms12111_CR43","doi-asserted-by":"publisher","first-page":"735","DOI":"10.1016\/j.cell.2005.06.043","volume":"122","author":"J Rink","year":"2005","unstructured":"Rink, J., Ghigo, E., Kalaidzidis, Y. & Zerial, M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735\u2013749 (2005).","journal-title":"Cell"},{"key":"BFncomms12111_CR44","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1016\/j.cell.2010.03.011","volume":"141","author":"D Poteryaev","year":"2010","unstructured":"Poteryaev, D., Datta, S., Ackema, K., Zerial, M. & Spang, A. Identification of the switch in early-to-late endosome transition. Cell 141, 497\u2013508 (2010).","journal-title":"Cell"},{"key":"BFncomms12111_CR45","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1186\/gb-2006-7-3-211","volume":"7","author":"U Yazdani","year":"2006","unstructured":"Yazdani, U. & Terman, J. R. The semaphorins. Genome Biol. 7, 211 (2006).","journal-title":"Genome Biol."},{"key":"BFncomms12111_CR46","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1038\/nrc2404","volume":"8","author":"G Neufeld","year":"2008","unstructured":"Neufeld, G. & Kessler, O. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat. Rev. Cancer 8, 632\u2013645 (2008).","journal-title":"Nat. Rev. Cancer"},{"key":"BFncomms12111_CR47","doi-asserted-by":"publisher","first-page":"13763","DOI":"10.1074\/jbc.M114.622274","volume":"290","author":"C Dayer","year":"2015","unstructured":"Dayer, C. & Stamenkovic, I. Recruitment of matrix metalloproteinase-9 (MMP-9) to the fibroblast cell surface by lysyl hydroxylase 3 (LH3) triggers transforming growth factor-\u00df (TGF- \u00df) activation and fibroblast differentiation. J. Biol. Chem. 290, 13763\u201313778 (2015).","journal-title":"J. Biol. Chem."},{"key":"BFncomms12111_CR48","doi-asserted-by":"publisher","first-page":"671","DOI":"10.1038\/nmeth.2089","volume":"9","author":"CA Schneider","year":"2012","unstructured":"Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671\u2013675 (2012).","journal-title":"Nat. Methods"},{"key":"BFncomms12111_CR49","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1038\/nm1366","volume":"12","author":"PB Mills","year":"2006","unstructured":"Mills, P. B. et al. Mutations in antiquitin in individuals with pyridoxine-dependent seizures. Nat. Med. 12, 307\u2013309 (2006).","journal-title":"Nat. Med."},{"key":"BFncomms12111_CR50","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","volume":"9","author":"J Schindelin","year":"2012","unstructured":"Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676\u2013682 (2012).","journal-title":"Nat. Methods"},{"key":"BFncomms12111_CR51","doi-asserted-by":"publisher","first-page":"3993","DOI":"10.1529\/biophysj.103.038422","volume":"86","author":"SV Costes","year":"2004","unstructured":"Costes, S. V. et al. Automatic and quantitative measurement of protein-protein colocalisation in live cells. Biophys. J. 86, 3993\u20134003 (2004).","journal-title":"Biophys. J."},{"key":"BFncomms12111_CR52","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1083\/jcb.148.1.45","volume":"148","author":"RS Polishchuk","year":"2000","unstructured":"Polishchuk, R. S. et al. Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J. Cell Biol. 148, 45\u201358 (2000).","journal-title":"J. Cell Biol."},{"key":"BFncomms12111_CR53","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1016\/S0091-679X(08)61626-X","volume":"31","author":"WJ Brown","year":"1989","unstructured":"Brown, W. J. & Farquhar, M. G. Immunoperoxidase methods for the localization of antigens in cultured cells and tissue sections by electron microscopy. Methods Cell Biol. 31, 553\u2013569 (1989).","journal-title":"Methods Cell Biol."},{"key":"BFncomms12111_CR54","doi-asserted-by":"publisher","first-page":"2363","DOI":"10.1093\/bioinformatics\/btq431","volume":"26","author":"BS Carvalho","year":"2010","unstructured":"Carvalho, B. S. & Irizarry, R. A. A framework for oligonucleotide microarray preprocessing. Bioinformatics 26, 2363\u20132367 (2010).","journal-title":"Bioinformatics"},{"key":"BFncomms12111_CR55","doi-asserted-by":"publisher","first-page":"W244","DOI":"10.1093\/nar\/gki408","volume":"33","author":"J Soding","year":"2005","unstructured":"Soding, J., Biegert, A. & Lupas, A. N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244\u2013W248 (2005).","journal-title":"Nucleic Acids Res."},{"key":"BFncomms12111_CR56","doi-asserted-by":"publisher","first-page":"W337","DOI":"10.1093\/nar\/gku366","volume":"42","author":"G Yachdav","year":"2014","unstructured":"Yachdav, G. et al. PredictProtein-an open resource for online prediction of protein structural and functional features. Nucleic Acids Res. 42, W337\u2013W343 (2014).","journal-title":"Nucleic Acids Res."},{"key":"BFncomms12111_CR57","doi-asserted-by":"publisher","first-page":"19040","DOI":"10.3390\/ijms160819040","volume":"16","author":"JD Atkins","year":"2015","unstructured":"Atkins, J. D., Boateng, S. Y., Sorensen, T. & McGuffin, L. J. Disorder prediction methods, their applicability to different protein targets and their usefulness for guiding experimental studies. Int. J. Mol. Sci. 16, 19040\u201319054 (2015).","journal-title":"Int. J. Mol. Sci."},{"key":"BFncomms12111_CR58","first-page":"175","volume":"6","author":"EL Sonnhammer","year":"1998","unstructured":"Sonnhammer, E. L., von Heijne, G. & Krogh, A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6, 175\u2013182 (1998).","journal-title":"Proc. Int. Conf. Intell. Syst. Mol. Biol."},{"key":"BFncomms12111_CR59","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1006\/jmbi.1998.2107","volume":"283","author":"GE Tusnady","year":"1998","unstructured":"Tusnady, G. E. & Simon, I. Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J. Mol. Biol. 283, 489\u2013506 (1998).","journal-title":"J. Mol. Biol."},{"key":"BFncomms12111_CR60","first-page":"Unit 5","volume":"Chapter 5","author":"N Eswar","year":"2006","unstructured":"Eswar, N. et al. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chapter 5, Unit 5\u2013Unit 6 (2006).","journal-title":"Curr. Protoc. Bioinformatics"},{"key":"BFncomms12111_CR61","doi-asserted-by":"publisher","first-page":"486","DOI":"10.1107\/S0907444910007493","volume":"66","author":"P Emsley","year":"2010","unstructured":"Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486\u2013501 (2010).","journal-title":"Acta Crystallogr. D"},{"key":"BFncomms12111_CR62","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1107\/S0907444909052925","volume":"66","author":"PD Adams","year":"2010","unstructured":"Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213\u2013221 (2010).","journal-title":"Acta Crystallogr. D Biol. Crystallogr."},{"key":"BFncomms12111_CR63","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1093\/nar\/29.1.221","volume":"29","author":"RA Laskowski","year":"2001","unstructured":"Laskowski, R. A. PDBsum: summaries and analyses of PDB structures. Nucleic Acids Res. 29, 221\u2013222 (2001).","journal-title":"Nucleic Acids Res."},{"key":"BFncomms12111_CR64","doi-asserted-by":"publisher","first-page":"W510","DOI":"10.1093\/nar\/gkp322","volume":"37","author":"P Benkert","year":"2009","unstructured":"Benkert, P., Kunzli, M. & Schwede, T. QMEAN server for protein model quality estimation. Nucleic Acids Res. 37, W510\u2013W514 (2009).","journal-title":"Nucleic Acids Res."},{"key":"BFncomms12111_CR65","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1006\/abio.2000.4698","volume":"284","author":"Y Durocher","year":"2000","unstructured":"Durocher, Y. et al. A reporter gene assay for high-throughput screening of G-protein-coupled receptors stably or transiently expressed in HEK293 EBNA cells grown in suspension culture. Anal. Biochem. 284, 316\u2013326 (2000).","journal-title":"Anal. Biochem."},{"key":"BFncomms12111_CR66","doi-asserted-by":"publisher","first-page":"3471","DOI":"10.1021\/pr400328g","volume":"12","author":"WE Heywood","year":"2013","unstructured":"Heywood, W. E. et al. A new method for the rapid diagnosis of protein N-linked congenital disorders of glycosylation. J. Proteome Res. 12, 3471\u20133479 (2013).","journal-title":"J. Proteome Res."},{"key":"BFncomms12111_CR67","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1007\/978-1-61779-415-5_2","volume":"816","author":"AD Bakker","year":"2012","unstructured":"Bakker, A. D. & Klein-Nulend, J. Osteoblast isolation from murine calvaria and long bones. Methods Mol. Biol. 816, 19\u201329 (2012).","journal-title":"Methods Mol. Biol."}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/ncomms12111.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms12111","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms12111.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,4]],"date-time":"2023-01-04T11:11:12Z","timestamp":1672830672000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/ncomms12111"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2016,7,20]]},"references-count":67,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2016,11,25]]}},"alternative-id":["BFncomms12111"],"URL":"https:\/\/doi.org\/10.1038\/ncomms12111","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2016,7,20]]},"assertion":[{"value":"9 September 2015","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 June 2016","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 July 2016","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"12111"}}