{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T04:55:37Z","timestamp":1790398537881,"version":"4.1.0"},"reference-count":101,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2020,4,14]],"date-time":"2020-04-14T00:00:00Z","timestamp":1586822400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100011272","name":"FP7 Health","doi-asserted-by":"publisher","award":["602300"],"award-info":[{"award-number":["602300"]}],"id":[{"id":"10.13039\/100011272","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003407","name":"Ministero dell\u2019Istruzione, dell\u2019Universit\u00e0 e della Ricerca","doi-asserted-by":"publisher","award":["PRIN 2015F3JHMB"],"award-info":[{"award-number":["PRIN 2015F3JHMB"]}],"id":[{"id":"10.13039\/501100003407","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003407","name":"Ministero dell\u2019Istruzione, dell\u2019Universit\u00e0 e della Ricerca","doi-asserted-by":"publisher","award":["Dipartimenti di Eccellenza 2018-2022"],"award-info":[{"award-number":["Dipartimenti di Eccellenza 2018-2022"]}],"id":[{"id":"10.13039\/501100003407","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Proteoglycans (PGs) are macromolecules present on the cell surface and in the extracellular matrix that confer specific mechanical, biochemical, and physical properties to tissues. Sulfate groups present on glycosaminoglycans, linear polysaccharide chains attached to PG core proteins, are fundamental for correct PG functions. Indeed, through the negative charge of sulfate groups, PGs interact with extracellular matrix molecules and bind growth factors regulating tissue structure and cell behavior. The maintenance of correct sulfate metabolism is important in tissue development and function, particularly in cartilage where PGs are fundamental and abundant components of the extracellular matrix. In chondrocytes, the main sulfate source is the extracellular space, then sulfate is taken up and activated in the cytosol to the universal sulfate donor to be used in sulfotransferase reactions. Alteration in each step of sulfate metabolism can affect macromolecular sulfation, leading to the onset of diseases that affect mainly cartilage and bone. This review presents a panoramic view of skeletal dysplasias caused by mutations in genes encoding for transporters or enzymes involved in macromolecular sulfation. Future research in this field will contribute to the understanding of the disease pathogenesis, allowing the development of targeted therapies aimed at alleviating, preventing, or modifying the disease progression.<\/jats:p>","DOI":"10.3390\/ijms21082710","type":"journal-article","created":{"date-parts":[[2020,4,15]],"date-time":"2020-04-15T04:01:46Z","timestamp":1586923306000},"page":"2710","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":41,"title":["Skeletal Dysplasias Caused by Sulfation Defects"],"prefix":"10.3390","volume":"21","author":[{"given":"Chiara","family":"Paganini","sequence":"first","affiliation":[{"name":"Department of Molecular Medicine, Unit of Biochemistry, University of Pavia, 27100 Pavia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chiara","family":"Gramegna Tota","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine, Unit of Biochemistry, University of Pavia, 27100 Pavia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3543-7531","authenticated-orcid":false,"given":"Andrea","family":"Superti-Furga","sequence":"additional","affiliation":[{"name":"Division of Genetic Medicine, Lausanne University Hospital, University of Lausanne, 1011 Lausanne, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2460-8761","authenticated-orcid":false,"given":"Antonio","family":"Rossi","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine, Unit of Biochemistry, University of Pavia, 27100 Pavia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,4,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1146\/annurev.biochem.67.1.609","article-title":"Matrix proteoglycans: From molecular design to cellular function","volume":"67","author":"Iozzo","year":"1998","journal-title":"Annu. Rev. Biochem."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1002\/med.10020","article-title":"Sulfotransferases and sulfated oligosaccharides","volume":"22","author":"Honke","year":"2002","journal-title":"Med. Res. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"R9","DOI":"10.1016\/S1074-5521(99)80014-3","article-title":"Carbohydrate sulfotransferases: Mediators of extracellular communication","volume":"6","author":"Bowman","year":"1999","journal-title":"Chem. Biol."},{"key":"ref_4","first-page":"239","article-title":"Heparan sulphates as membrane receptors for the fibroblast growth factors","volume":"32","author":"Gallagher","year":"1994","journal-title":"Eur. J. Clin. Chem. Clin. Biochem."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.earlhumdev.2004.10.021","article-title":"Sulfation of drugs and hormones in mid-gestation human fetus","volume":"81","author":"Pacifici","year":"2005","journal-title":"Early Hum. Dev."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1007\/BF00231827","article-title":"On the role of sulfolipids in mammalian metabolism","volume":"66","author":"Farooqui","year":"1985","journal-title":"Mol. Cell. Biochem."},{"key":"ref_7","first-page":"299","article-title":"Tyrosine sulfation: An increasingly recognised post-translational modification of secreted proteins","volume":"25","author":"Stone","year":"2009","journal-title":"Nat. Biotechnol."},{"key":"ref_8","first-page":"2734","article-title":"Sulfation of thyroid hormone and dopamine during human development: Ontogeny of phenol sulfotransferases and arylsulfatase in liver, lung, and brain","volume":"86","author":"Richard","year":"2001","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_9","first-page":"268","article-title":"Cholesterol sulfation in human liver. Catalysis by dehydroepiandrosterone sulfotransferase","volume":"21","author":"Aksoy","year":"1993","journal-title":"Drug Metab. Dispos."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1093\/toxsci\/kfn268","article-title":"Bile Acid sulfation: A pathway of bile acid elimination and detoxification","volume":"108","author":"Alnouti","year":"2009","journal-title":"Toxicol. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/0960-0760(94)90077-9","article-title":"Steroid sulfation by expressed human cytosolic sulfotransferases","volume":"48","author":"Falany","year":"1994","journal-title":"J. Steroid Biochem. Mol. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3008","DOI":"10.1111\/febs.14984","article-title":"Bone and connective tissue disorders caused by defects in glycosaminoglycan biosynthesis: A panoramic view","volume":"286","author":"Paganini","year":"2019","journal-title":"FEBS J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1097\/GIM.0b013e3181daae9b","article-title":"The skeletal dysplasias","volume":"12","author":"Krakow","year":"2010","journal-title":"Genet. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1146\/annurev-genom-090314-045904","article-title":"Advances in Skeletal Dysplasia Genetics","volume":"16","author":"Geister","year":"2015","journal-title":"Annu. Rev. Genom. Hum. Genet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2393","DOI":"10.1002\/ajmg.a.61366","article-title":"Nosology and classification of genetic skeletal disorders: 2019 revision","volume":"179","author":"Mortier","year":"2019","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1096\/fasebj.11.6.9194521","article-title":"Sulfation and sulfotransferases 5: The importance of 3\u2019- phosphoadenosine 5\u2019-phosphosulfate (PAPS) in the regulation of sulfation","volume":"11","author":"Klaassen","year":"1997","journal-title":"FASEB J."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"515","DOI":"10.3109\/10409239309085137","article-title":"The physical biochemistry and molecular genetics of sulfate activation","volume":"28","author":"Leyh","year":"1993","journal-title":"Crit. Rev. Biochem. Mol. Biol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1126\/science.128.3324.575","article-title":"Biological sulfate activation and transfer","volume":"128","author":"Lipmann","year":"1958","journal-title":"Science"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1016\/0020-711X(80)90003-8","article-title":"3\u2019-phosphoadenosine 5\u2019-phosphosulphate metabolism in mammalian tissues","volume":"12","author":"Farooqui","year":"1980","journal-title":"Int. J. Biochem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/1521654031000072148","article-title":"Human 3\u2019-phosphoadenosine 5\u2019-phosphosulfate (PAPS) synthase: Biochemistry, molecular biology and genetic deficiency","volume":"55","author":"Venkatachalam","year":"2003","journal-title":"Iubmb Life"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/j.jgg.2016.08.001","article-title":"Genetics and pathophysiology of mammalian sulfate biology","volume":"44","author":"Langford","year":"2017","journal-title":"J. Genet. Genom."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.semcdb.2011.03.004","article-title":"Sulfate in fetal development","volume":"22","author":"Dawson","year":"2011","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.placenta.2017.01.001","article-title":"Review: Nutrient sulfate supply from mother to fetus: Placental adaptive responses during human and animal gestation","volume":"54","author":"Dawson","year":"2017","journal-title":"Placenta"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"135","DOI":"10.1016\/0009-8981(80)90423-4","article-title":"Age-dependent serum sulfate levels in children and adolescents","volume":"107","author":"Cole","year":"1980","journal-title":"Clin. Chim. Acta"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1093\/clinchem\/31.6.866","article-title":"Increased serum sulfate in pregnancy: Relationship to gestational age","volume":"31","author":"Cole","year":"1985","journal-title":"Clin. Chem."},{"key":"ref_26","first-page":"1192","article-title":"Sulfate metabolism is abnormal in patients with rheumatoid arthritis. Confirmation by in vivo biochemical findings","volume":"21","author":"Bradley","year":"1994","journal-title":"J. Rheumatol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1007\/BF01869697","article-title":"Proton fluxes associated with erythrocyte membrane anion exchange","volume":"28","author":"Jennings","year":"1976","journal-title":"J. Membr. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1007\/s004240050147","article-title":"Immunolocalization of Na\/SO4-cotransport (NaSi-1) in rat kidney","volume":"432","author":"Custer","year":"1996","journal-title":"Pflug. Arch."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1016\/j.placenta.2013.01.017","article-title":"Human placental sulfate transporter mRNA profiling from term pregnancies identifies abundant SLC13A4 in syncytiotrophoblasts and SLC26A2 in cytotrophoblasts","volume":"34","author":"Simmons","year":"2013","journal-title":"Placenta"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"385","DOI":"10.2174\/0929867053363144","article-title":"Pathogenetics of the human SLC26 transporters","volume":"12","author":"Dawson","year":"2005","journal-title":"Curr. Med. Chem."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"494","DOI":"10.1016\/j.mam.2012.07.009","article-title":"The SLC26 gene family of anion transporters and channels","volume":"34","author":"Alper","year":"2013","journal-title":"Mol. Asp. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1007\/s00424-013-1388-8","article-title":"Na+-sulfate cotransporter SLC13A1","volume":"466","author":"Markovich","year":"2014","journal-title":"Pflug. Arch."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.ymgme.2017.03.010","article-title":"Molecular analysis of sequence and splice variants of the human SLC13A4 sulfate transporter","volume":"121","author":"Zhang","year":"2017","journal-title":"Mol. Genet. Metab."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1016\/0092-8674(94)90281-X","article-title":"The diastrophic dysplasia gene encodes a novel sulfate transporter: Positional cloning by fine-structure linkage disequilibrium mapping","volume":"78","author":"Mahtani","year":"1994","journal-title":"Cell"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1016\/0006-2952(83)90126-0","article-title":"The effectiveness of different sulfate precursors in supporting extrahepatic sulfate conjugation","volume":"32","author":"Dawson","year":"1983","journal-title":"Biochem. Pharm."},{"key":"ref_36","first-page":"L450","article-title":"Sulfation by human lung fibroblasts: SO4(2-) and sulfur- containing amino acids as sources for macromolecular sulfation","volume":"260","author":"Elgavish","year":"1991","journal-title":"Am. J. Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1042\/bj2350707","article-title":"Lysosomal degradation of glycoproteins and glycosaminoglycans. Efflux and recycling of sulphate and N-acetylhexosamines","volume":"235","author":"Rome","year":"1986","journal-title":"Biochem. J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"5920","DOI":"10.1021\/bi00185a032","article-title":"Rat chondrosarcoma ATP sulfurylase and adenosine 5\u2019-phosphosulfate kinase reside on a single bifunctional protein","volume":"33","author":"Lyle","year":"1994","journal-title":"Biochemistry"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1006\/bbrc.2000.2123","article-title":"Human 3\u2019-phosphoadenosine 5\u2019-phosphosulfate synthetase 1 (PAPSS1) and PAPSS2: Gene cloning, characterization and chromosomal localization","volume":"268","author":"Xu","year":"2000","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1038\/2458","article-title":"Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse","volume":"20","author":"King","year":"1998","journal-title":"Nat. Genet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"8681","DOI":"10.1073\/pnas.95.15.8681","article-title":"A member of a family of sulfate-activating enzymes causes murine brachymorphism","volume":"95","author":"Kurima","year":"1998","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2310","DOI":"10.1056\/NEJMoa0810489","article-title":"Inactivating PAPSS2 mutations in a patient with premature pubarche","volume":"360","author":"Noordam","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1210\/er.2001-0040","article-title":"Sulfonation and molecular action","volume":"23","author":"Strott","year":"2002","journal-title":"Endocr. Rev."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1042\/bj20020044","article-title":"Characterization and expression of human bifunctional 3\u2019-phosphoadenosine 5\u2019-phosphosulphate synthase isoforms","volume":"365","author":"Fuda","year":"2002","journal-title":"Biochem. J."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Schroder, E., Gebel, L., Eremeev, A.A., Morgner, J., Grum, D., Knauer, S.K., Bayer, P., and Mueller, J.W. (2012). Human PAPS Synthase Isoforms Are Dynamically Regulated Enzymes with Access to Nucleus and Cytoplasm. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0029559"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"10945","DOI":"10.1074\/jbc.M508991200","article-title":"Molecular cloning and characterization of a novel 3\u2019-phosphoadenosine 5\u2019-phosphosulfate transporter, PAPST2","volume":"281","author":"Kamiyama","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"25958","DOI":"10.1074\/jbc.M302439200","article-title":"Molecular cloning and identification of 3\u2019-phosphoadenosine 5\u2019-phosphosulfate transporter","volume":"278","author":"Kamiyama","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"12293","DOI":"10.1074\/jbc.REV119.007422","article-title":"Sulfation pathways from red to green","volume":"294","author":"Hardman","year":"2019","journal-title":"J. Biol. Chem."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.sbi.2019.03.019","article-title":"Gateway to the Golgi: Molecular mechanisms of nucleotide sugar transporters","volume":"57","author":"Parker","year":"2019","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1002\/path.2824","article-title":"Cartilage ultrastructure in proteoglycan-deficient zebrafish mutants brings to light new candidate genes for human skeletal disorders","volume":"223","author":"Wiweger","year":"2011","journal-title":"J. Pathol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1016\/j.cbpa.2008.06.018","article-title":"Sulfotransferases, sulfatases and formylglycine-generating enzymes: A sulfation fascination","volume":"12","author":"Bojarova","year":"2008","journal-title":"Curr. Opin. Chem. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.cbi.2016.05.005","article-title":"Function and organization of the human cytosolic sulfotransferase (SULT) family","volume":"259","author":"Coughtrie","year":"2016","journal-title":"Chem. Biol. Interact."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/S0014-5793(01)02129-9","article-title":"The dimerization motif of cytosolic sulfotransferases","volume":"490","author":"Petrotchenko","year":"2001","journal-title":"FEBS Lett."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1404","DOI":"10.1016\/j.jmb.2015.01.021","article-title":"Heterodimers of tyrosylprotein sulfotransferases suggest existence of a higher organization level of transferases in the membrane of the trans-Golgi apparatus","volume":"427","author":"Trusch","year":"2015","journal-title":"J. Mol. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"55811","DOI":"10.18632\/oncotarget.10046","article-title":"Sulfonation, an underexploited area: From skeletal development to infectious diseases and cancer","volume":"7","author":"Leung","year":"2016","journal-title":"Oncotarget"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1016\/j.ajhg.2011.04.002","article-title":"Chondrodysplasia and abnormal joint development associated with mutations in IMPAD1, encoding the Golgi-resident nucleotide phosphatase, gPAPP","volume":"88","author":"Vissers","year":"2011","journal-title":"Am. J. Hum. Genet."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"11605","DOI":"10.1073\/pnas.0801182105","article-title":"A role for a lithium-inhibited Golgi nucleotidase in skeletal development and sulfation","volume":"105","author":"Frederick","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2215","DOI":"10.1242\/dev.019950","article-title":"JAWS coordinates chondrogenesis and synovial joint positioning","volume":"135","author":"Sohaskey","year":"2008","journal-title":"Development"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1146\/annurev.genom.6.080604.162334","article-title":"Sulfatases and human disease","volume":"6","author":"Ballabio","year":"2005","journal-title":"Annu. Rev. Genom. Hum. Genet."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1002\/humu.1","article-title":"Mutations in the diastrophic dysplasia sulfate transporter (DTDST) gene (SLC26A2): 22 Novel mutations, mutation review, associated skeletal phenotypes, and diagnostic relevance","volume":"17","author":"Rossi","year":"2001","journal-title":"Hum. Mutat."},{"key":"ref_61","first-page":"759","article-title":"A rare lethal bone dysplasia with recessive autosomic transmission","volume":"29","author":"Maroteaux","year":"1972","journal-title":"Arch. Fr. Pediatr."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1007\/BF00355348","article-title":"A new neonatal short limbed dwarfism","volume":"13","author":"McAlister","year":"1985","journal-title":"Skelet. Radiol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1136\/jmg.2007.057158","article-title":"A novel mutation in the sulfate transporter gene SLC26A2 (DTDST) specific to the Finnish population causes de la Chapelle dysplasia","volume":"45","author":"Bonafe","year":"2008","journal-title":"J. Med. Genet."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1111\/j.1432-1033.1997.t01-1-00741.x","article-title":"Undersulfation of cartilage proteoglycans ex vivo and increased contribution of amino acid sulfur to sulfation in vitro in McAlister dysplasia atelosteogenesis type 2","volume":"248","author":"Rossi","year":"1997","journal-title":"Eur. J. Biochem."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1485","DOI":"10.1093\/hmg\/10.14.1485","article-title":"Mutations in the diastrophic dysplasia sulfate transporter (DTDST) gene: Correlation between sulfate transport activity and chondrodysplasia phenotype","volume":"10","author":"Karniski","year":"2001","journal-title":"Hum. Mol. Genet."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/S0945-053X(98)90088-9","article-title":"Proteoglycan sulfation in cartilage and cell cultures from patients with sulfate transporter chondrodysplasias: Relationship to clinical severity and indications on the role of intracellular sulfate production","volume":"17","author":"Rossi","year":"1998","journal-title":"Matrix Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"859","DOI":"10.1093\/hmg\/ddi079","article-title":"A diastrophic dysplasia sulfate transporter (SLC26A2) mutant mouse: Morphological and biochemical characterization of the resulting chondrodysplasia phenotype","volume":"14","author":"Forlino","year":"2005","journal-title":"Hum. Mol. Genet."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/j.matbio.2010.05.001","article-title":"Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signalling","volume":"29","author":"Gualeni","year":"2010","journal-title":"Matrix Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1779","DOI":"10.1002\/jcb.24844","article-title":"Altered signaling in the G1 phase deregulates chondrocyte growth in a mouse model with proteoglycan undersulfation","volume":"115","author":"Monti","year":"2014","journal-title":"J. Cell. Biochem."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"5570","DOI":"10.1093\/hmg\/ddv289","article-title":"N-acetylcysteine treatment ameliorates the skeletal phenotype of a mouse model of diastrophic dysplasia","volume":"24","author":"Monti","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1016\/j.ebiom.2019.01.010","article-title":"Suppressing UPR-dependent overactivation of FGFR3 signaling ameliorates SLC26A2-deficient chondrodysplasias","volume":"40","author":"Zheng","year":"2019","journal-title":"EBioMedicine"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"468","DOI":"10.1002\/(SICI)1096-8628(19980806)78:5<468::AID-AJMG13>3.0.CO;2-D","article-title":"Distinct, autosomal recessive form of spondyloepimetaphyseal dysplasia segregating in an inbred Pakistani kindred","volume":"78","author":"Ahmad","year":"1998","journal-title":"Am. J. Med. Genet."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1136\/jmedgenet-2012-101039","article-title":"PAPSS2 mutations cause autosomal recessive brachyolmia","volume":"49","author":"Miyake","year":"2012","journal-title":"J. Med. Genet."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1002\/ajmg.1320020408","article-title":"Recessively inherited, late onset spondylar dysplasia and peripheral corneal opacity with anomalies in urinary mucopolysaccharides: A possible error of chondroitin-6-sulfate synthesis","volume":"2","author":"Toledo","year":"1978","journal-title":"Am. J. Med. Genet."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1016\/0006-291X(81)90852-4","article-title":"Spondyloepiphyseal dysplasia, chondroitin sulfate type: A possible defect of PAPS--chondroitin sulfate sulfotransferase in humans","volume":"98","author":"Mourao","year":"1981","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1381","DOI":"10.1002\/humu.22377","article-title":"Clinical and radiographic features of the autosomal recessive form of brachyolmia caused by PAPSS2 mutations","volume":"34","author":"Iida","year":"2013","journal-title":"Hum. Mutat."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"2183","DOI":"10.1002\/ajmg.a.35504","article-title":"IMPAD1 mutations in two Catel-Manzke like patients","volume":"158A","author":"Nizon","year":"2012","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"2543","DOI":"10.1002\/ajmg.a.33641","article-title":"Phenotypic features of carbohydrate sulfotransferase 3 (CHST3) deficiency in 24 patients: Congenital dislocations and vertebral changes as principal diagnostic features","volume":"152A","author":"Unger","year":"2010","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"10155","DOI":"10.1073\/pnas.0400334101","article-title":"Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement","volume":"101","author":"Thiele","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"1368","DOI":"10.1016\/j.ajhg.2008.05.006","article-title":"Congenital joint dislocations caused by carbohydrate sulfotransferase 3 deficiency in recessive Larsen syndrome and humero-spinal dysostosis","volume":"82","author":"Hermanns","year":"2008","journal-title":"Am. J. Hum. Genet."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"2376","DOI":"10.1002\/ajmg.a.32482","article-title":"Spondyloepiphyseal dysplasia, Omani type: Further definition of the phenotype","volume":"146A","author":"Mizumoto","year":"2008","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1111\/j.1399-0004.2009.01167.x","article-title":"Omani-type spondyloepiphyseal dysplasia with cardiac involvement caused by a missense mutation in CHST3","volume":"75","author":"Tuysuz","year":"2009","journal-title":"Clin. Genet."},{"key":"ref_83","first-page":"407","article-title":"Humero-spinal dysostosis with congenital heart disease","volume":"127","author":"Kozlowski","year":"1974","journal-title":"Am. J. Dis. Child."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1097\/01202412-199701000-00003","article-title":"Humero-spinal dysostosis: Report of the fourth case with emphasis on generalized skeletal involvement, abnormal craniofacial features, and mitral valve thickening","volume":"6","author":"Hall","year":"1997","journal-title":"J. Pediatr. Orthop. B"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1002\/humu.21355","article-title":"Musculocontractural Ehlers-Danlos Syndrome (former EDS type VIB) and adducted thumb clubfoot syndrome (ATCS) represent a single clinical entity caused by mutations in the dermatan-4-sulfotransferase 1 encoding CHST14 gene","volume":"31","author":"Malfait","year":"2010","journal-title":"Hum. Mutat."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1002\/ajmg.a.37383","article-title":"The phenotype of the musculocontractural type of Ehlers-Danlos syndrome due to CHST14 mutations","volume":"170","author":"Janecke","year":"2016","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1016\/j.ajhg.2009.11.010","article-title":"Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome","volume":"85","author":"Dundar","year":"2009","journal-title":"Am. J. Hum. Genet."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1002\/humu.21300","article-title":"Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome","volume":"31","author":"Miyake","year":"2010","journal-title":"Hum. Mutat."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Hirose, T., Takahashi, N., Tangkawattana, P., Minaguchi, J., Mizumoto, S., Yamada, S., Miyake, N., Hayashi, S., Hatamochi, A., and Nakayama, J. (2018). Structural alteration of glycosaminoglycan side chains and spatial disorganization of collagen networks in the skin of patients with mcEDS-CHST14. Biochim. Biophys. Acta Gen. Subj.","DOI":"10.1016\/j.bbagen.2018.12.006"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1136\/jmedgenet-2017-105003","article-title":"Homozygous CHST11 mutation in chondrodysplasia, brachydactyly, overriding digits, clino-symphalangism and synpolydactyly","volume":"55","author":"Shabbir","year":"2018","journal-title":"J. Med. Genet."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1002\/mgg3.152","article-title":"Inherited CHST11\/MIR3922 deletion is associated with a novel recessive syndrome presenting with skeletal malformation and malignant lymphoproliferative disease","volume":"3","author":"Chopra","year":"2015","journal-title":"Mol. Genet. Genom. Med."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"3989","DOI":"10.1242\/dev.01948","article-title":"Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis","volume":"132","author":"Kluppel","year":"2005","journal-title":"Development"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1038\/ng0196-100","article-title":"Achondrogenesis type IB is caused by mutations in the diastrophic dysplasia sulphate transporter gene","volume":"12","author":"SupertiFurga","year":"1996","journal-title":"Nat. Genet."},{"key":"ref_94","first-page":"255","article-title":"Atelosteogenesis type II is caused by mutations in the diastrophic dysplasia sulfate-transporter gene (DTDST): Evidence for a phenotypic series involving three chondrodysplasias","volume":"58","author":"Wilcox","year":"1996","journal-title":"Am. J. Hum. Genet."},{"key":"ref_95","first-page":"621","article-title":"Recessively inherited multiple epiphyseal dysplasia with normal stature, club foot, and double layered patella caused by a DTDST mutation","volume":"36","author":"Neumann","year":"1999","journal-title":"J. Med. Genet."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.bone.2013.01.036","article-title":"Alteration of proteoglycan sulfation affects bone growth and remodeling","volume":"54","author":"Gualeni","year":"2013","journal-title":"Bone"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"1697","DOI":"10.1242\/dev.030742","article-title":"Sulfation of chondroitin sulfate proteoglycans is necessary for proper Indian hedgehog signaling in the developing growth plate","volume":"136","author":"Cortes","year":"2009","journal-title":"Development"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1517\/21678707.2015.1006197","article-title":"Treatment options for osteogenesis imperfecta","volume":"3","author":"Besio","year":"2015","journal-title":"Expert Opin. Orphan Drugs"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"1137","DOI":"10.1517\/21678707.2015.1083853","article-title":"New therapeutic targets in rare genetic skeletal diseases","volume":"3","author":"Briggs","year":"2015","journal-title":"Expert Opin. Orphan Drugs"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1002\/dvdy.24479","article-title":"Achondroplasia: Development, pathogenesis, and therapy","volume":"246","author":"Ornitz","year":"2017","journal-title":"Dev. Dyn."},{"key":"ref_101","doi-asserted-by":"crossref","unstructured":"Marzin, P., and Cormier-Daire, V. (2020). New perspectives on the treatment of skeletal dysplasia. Adv. Endocrinol. Metab., 11.","DOI":"10.1177\/2042018820904016"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/8\/2710\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:30:46Z","timestamp":1760362246000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/8\/2710"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,14]]},"references-count":101,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2020,4]]}},"alternative-id":["ijms21082710"],"URL":"https:\/\/doi.org\/10.3390\/ijms21082710","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,4,14]]}}}