{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:52:08Z","timestamp":1790833928792,"version":"4.1.0"},"reference-count":97,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2022,7,5]],"date-time":"2022-07-05T00:00:00Z","timestamp":1656979200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Grant-in Aid for Scientific Research (C) from the Japan Society for the Promotion of Science","award":["19K07054"],"award-info":[{"award-number":["19K07054"]}]},{"name":"Grant-in Aid for Scientific Research (C) from the Japan Society for the Promotion of Science","award":["21K06552"],"award-info":[{"award-number":["21K06552"]}]},{"name":"Research Institute of Meijo University","award":["19K07054"],"award-info":[{"award-number":["19K07054"]}]},{"name":"Research Institute of Meijo University","award":["21K06552"],"award-info":[{"award-number":["21K06552"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The crucial roles of dermatan sulfate (DS) have been demonstrated in tissue development of the cutis, blood vessels, and bone through construction of the extracellular matrix and cell signaling. Although DS classically exerts physiological functions via interaction with collagens, growth factors, and heparin cofactor-II, new functions have been revealed through analyses of human genetic disorders as well as of knockout mice with loss of DS-synthesizing enzymes. Mutations in human genes encoding the epimerase and sulfotransferase responsible for the biosynthesis of DS chains cause connective tissue disorders including spondylodysplastic type Ehlers\u2013Danlos syndrome, characterized by skin hyperextensibility, joint hypermobility, and tissue fragility. DS-deficient mice show perinatal lethality, skin fragility, vascular abnormalities, thoracic kyphosis, myopathy-related phenotypes, acceleration of nerve regeneration, and impairments in self-renewal and proliferation of neural stem cells. These findings suggest that DS is essential for tissue development in addition to the assembly of collagen fibrils in the skin, and that DS-deficient knockout mice can be utilized as models of human genetic disorders that involve impairment of DS biosynthesis. This review highlights a novel role of DS in tissue development studies from the past decade.<\/jats:p>","DOI":"10.3390\/ijms23137485","type":"journal-article","created":{"date-parts":[[2022,7,6]],"date-time":"2022-07-06T05:41:06Z","timestamp":1657086066000},"page":"7485","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":44,"title":["The Specific Role of Dermatan Sulfate as an Instructive Glycosaminoglycan in Tissue Development"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4641-1505","authenticated-orcid":false,"given":"Shuji","family":"Mizumoto","sequence":"first","affiliation":[{"name":"Department of Pathobiochemistry, Faculty of Pharmacy, Meijo University, 150 Yagotoyama, Tempaku-ku, Nagoya 468-8503, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1284-9795","authenticated-orcid":false,"given":"Shuhei","family":"Yamada","sequence":"additional","affiliation":[{"name":"Department of Pathobiochemistry, Faculty of Pharmacy, Meijo University, 150 Yagotoyama, Tempaku-ku, Nagoya 468-8503, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,7,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1016\/S0021-9258(18)51374-0","article-title":"The mucopolysaccharides of skin","volume":"138","author":"Karl","year":"1941","journal-title":"J. Biol. Chem."},{"key":"ref_2","unstructured":"Scott, J.E. (1993). Patterns of epimerization and sulphation in dermatan sulphate chains. Dermatan Sulphate Proteoglycans: Chemistry, Biology, Chemical Pathology, Portland Press."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2431","DOI":"10.1111\/febs.12214","article-title":"Biological functions of iduronic acid in chondroitin\/dermatan sulfate","volume":"280","author":"Thelin","year":"2013","journal-title":"FEBS J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"117R","DOI":"10.1093\/glycob\/cwf066","article-title":"Dermatan sulfate: New functions from an old glycosaminoglycan","volume":"12","author":"Trowbridge","year":"2002","journal-title":"Glycobiology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1016\/j.sbi.2015.06.004","article-title":"Molecular interactions between chondroitin-dermatan sulfate and growth factors\/receptors\/matrix proteins","volume":"34","author":"Mizumoto","year":"2015","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"536","DOI":"10.1016\/j.sbi.2007.08.015","article-title":"Chondroitin\/dermatan sulfate in the central nervous system","volume":"17","author":"Sugahara","year":"2007","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2511","DOI":"10.1042\/BCJ20180283","article-title":"Glycans and glycosaminoglycans in neurobiology: Key regulators of neuronal cell function and fate","volume":"475","author":"Hayes","year":"2018","journal-title":"Biochem. J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1042\/BCJ20170820","article-title":"Biodiversity of CS-proteoglycan sulphation motifs: Chemical messenger recognition modules with roles in information transfer, control of cellular behaviour and tissue morphogenesis","volume":"475","author":"Hayes","year":"2018","journal-title":"Biochem. J."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"696640","DOI":"10.3389\/fcell.2021.696640","article-title":"Neural Tissue Homeostasis and Repair Is Regulated via CS and DS Proteoglycan Motifs","volume":"9","author":"Hayes","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_10","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_11","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1006\/abio.1999.4027","article-title":"Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with a fluorophore 2-aminobenzamide by high-performance liquid chromatography: Application to disaccharide composition analysis and exosequencing of oligosaccharides","volume":"269","author":"Kinoshita","year":"1999","journal-title":"Anal. Biochem."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1002\/ajmg.c.31552","article-title":"The 2017 international classification of the Ehlers-Danlos syndromes","volume":"175","author":"Malfait","year":"2017","journal-title":"Am. J. Med. Genet. C Semin. Med. Genet."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1038\/s41572-020-0194-9","article-title":"The Ehlers-Danlos syndromes","volume":"6","author":"Malfait","year":"2020","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1342","DOI":"10.1073\/pnas.87.4.1342","article-title":"A genetic defect in the biosynthesis of dermatan sulfate proteoglycan: Galactosyltransferase I deficiency in fibroblasts from a patient with a progeroid syndrome","volume":"87","author":"Quentin","year":"1990","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"26165","DOI":"10.1074\/jbc.274.37.26165","article-title":"Cloning and expression of a proteoglycan UDP-galactose:beta-xylose beta1,4-galactosyltransferase I. A seventh member of the human beta4-galactosyltransferase gene family","volume":"274","author":"Almeida","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"28841","DOI":"10.1074\/jbc.274.41.28841","article-title":"Molecular basis for the progeroid variant of Ehlers-Danlos syndrome. Identification and characterization of two mutations in galactosyltransferase I gene","volume":"274","author":"Okajima","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1016\/j.ajhg.2013.04.003","article-title":"Mutations in B3GALT6, which encodes a glycosaminoglycan linker region enzyme, cause a spectrum of skeletal and connective tissue disorders","volume":"92","author":"Nakajima","year":"2013","journal-title":"Am. J. Hum. Genet."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1016\/j.ajhg.2013.04.016","article-title":"Defective initiation of glycosaminoglycan synthesis due to B3GALT6 mutations causes a pleiotropic Ehlers-Danlos-syndrome-like connective tissue disorder","volume":"92","author":"Malfait","year":"2013","journal-title":"Am. J. Hum. Genet."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"22915","DOI":"10.1074\/jbc.274.33.22915","article-title":"Human homolog of Caenorhabditis elegans sqv-3 gene is galactosyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans","volume":"274","author":"Okajima","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"48189","DOI":"10.1074\/jbc.M107339200","article-title":"Biosynthesis of the linkage region of glycosaminoglycans: Cloning and activity of galactosyltransferase II, the sixth member of the \u03b21,3-galactosyltransferase family (beta3GalT6)","volume":"276","author":"Bai","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3761","DOI":"10.1093\/hmg\/ddt227","article-title":"Loss of dermatan sulfate epimerase (DSE) function results in musculocontractural Ehlers-Danlos syndrome","volume":"22","author":"Mizumoto","year":"2013","journal-title":"Hum. Mol. Genet."},{"key":"ref_22","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":"Zhang","year":"2009","journal-title":"Am. J. Hum. Genet."},{"key":"ref_23","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_24","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_25","doi-asserted-by":"crossref","first-page":"11560","DOI":"10.1074\/jbc.M513373200","article-title":"Biosynthesis of dermatan sulfate: Chondroitin-glucuronate C5-epimerase is identical to SART2","volume":"281","author":"Maccarana","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"36344","DOI":"10.1074\/jbc.M105848200","article-title":"Molecular cloning and characterization of a dermatan-specific N-acetylgalactosamine 4-O-sulfotransferase","volume":"276","author":"Evers","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"36115","DOI":"10.1074\/jbc.M306044200","article-title":"Specificities of three distinct human chondroitin\/dermatan N-acetylgalactosamine 4-O-sulfotransferases demonstrated using partially desulfated dermatan sulfate as an acceptor: Implication of differential roles in dermatan sulfate biosynthesis","volume":"278","author":"Mikami","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"5517","DOI":"10.1128\/MCB.00430-09","article-title":"Dermatan sulfate epimerase 1-deficient mice have reduced content and changed distribution of iduronic acids in dermatan sulfate and an altered collagen structure in skin","volume":"29","author":"Maccarana","year":"2009","journal-title":"Mol. Cell. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1016\/j.expneurol.2013.01.025","article-title":"Dermatan 4-O-sulfotransferase1 ablation accelerates peripheral nerve regeneration","volume":"247","author":"Rost","year":"2013","journal-title":"Exp. Neurol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1093\/glycob\/cwaa058","article-title":"Systematic investigation of the skin in Chst14-\/- mice: A model for skin fragility in musculocontractural Ehlers-Danlos syndrome caused by CHST14 variants (mcEDS-CHST14)","volume":"31","author":"Hirose","year":"2021","journal-title":"Glycobiology"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"dmm048963","DOI":"10.1242\/dmm.048963","article-title":"Muscle pathophysiology in mouse models of musculocontractural Ehlers-Danlos syndrome due to CHST14 mutations (mcEDS-CHST14), generated through CRISPR\/Cas9-mediated genomic editing","volume":"14","author":"Mizumoto","year":"2021","journal-title":"Dis. Model. Mech."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"695021","DOI":"10.3389\/fcell.2021.695021","article-title":"Myopathy associated with dermatan sulfate-deficient decorin and myostatin in musculocontractural Ehlers-Danlos syndrome: A mouse model investigation","volume":"9","author":"Mizumoto","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1006\/jmbi.2000.4261","article-title":"Molecular cloning and expression of human UDP-D-Xylose:proteoglycan core protein beta-D-xylosyltransferase and its first isoform XT-II","volume":"304","author":"Kuhn","year":"2000","journal-title":"J. Mol. Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"5201","DOI":"10.1074\/jbc.M611665200","article-title":"Human xylosyltransferase II is involved in the biosynthesis of the uniform tetrasaccharide linkage region in chondroitin sulfate and heparan sulfate proteoglycans","volume":"282","author":"Ambrosius","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"6615","DOI":"10.1074\/jbc.273.12.6615","article-title":"Molecular cloning and expression of glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans","volume":"273","author":"Kitagawa","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_36","unstructured":"Gottschalk, A. (1972). Carbohydrate-protein linkages in proteoglycans of animal, plant and bacterial origin. Glycoproteins: Their Composition, Structure and Function, Elsevier."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1146\/annurev.bi.60.070191.002303","article-title":"Proteoglycans: Structures and interactions","volume":"60","author":"Lindahl","year":"1991","journal-title":"Annu. Rev. Biochem."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"38721","DOI":"10.1074\/jbc.M106871200","article-title":"Molecular cloning and expression of a human chondroitin synthase","volume":"276","author":"Kitagawa","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"23666","DOI":"10.1074\/jbc.M302493200","article-title":"Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization","volume":"278","author":"Kitagawa","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1042\/BJ20061876","article-title":"Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin polymerizing factor","volume":"403","author":"Izumikawa","year":"2007","journal-title":"Biochem. J."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"11396","DOI":"10.1074\/jbc.M707549200","article-title":"Identification of chondroitin sulfate glucuronyltransferase as chondroitin synthase-3 involved in chondroitin polymerization: Chondroitin polymerization is achieved by multiple enzyme complexes consisting of chondroitin synthase family members","volume":"283","author":"Izumikawa","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"8841","DOI":"10.1074\/jbc.M111434200","article-title":"Molecular cloning and expression of human chondroitin N-acetylgalactosaminyltransferase: The key enzyme for chain initiation and elongation of chondroitin\/dermatan sulfate on the protein linkage region tetrasaccharide shared by heparin\/heparan sulfate","volume":"277","author":"Uyama","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"3072","DOI":"10.1074\/jbc.M209446200","article-title":"Molecular cloning and expression of a second chondroitin N-acetylgalactosaminyltransferase involved in the initiation and elongation of chondroitin\/dermatan sulfate","volume":"278","author":"Uyama","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"9788","DOI":"10.1074\/jbc.M809339200","article-title":"Two dermatan sulfate epimerases form iduronic acid domains in dermatan sulfate","volume":"284","author":"Pacheco","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"10474","DOI":"10.1074\/jbc.274.15.10474","article-title":"Molecular cloning and characterization of a human uronyl 2-sulfotransferase that sulfates iduronyl and glucuronyl residues in dermatan\/chondroitin sulfate","volume":"274","author":"Kobayashi","year":"1999","journal-title":"J. Biol. Chem."},{"key":"ref_46","unstructured":"Scott, J.E. (1993). Dermatan Sulphate Proteoglycans: Chemistry, Biology, Chemical Pathology, Portland Press."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1016\/0003-9861(68)90064-7","article-title":"Dermatan sulfate-protein: Isolation from and interaction with collagen","volume":"128","author":"Toole","year":"1968","journal-title":"Arch. Biochem. Biophys."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1042\/bj1970213","article-title":"Dermatan sulphate-rich proteoglycan associates with rat tail-tendon collagen at the d band in the gap region","volume":"197","author":"Scott","year":"1981","journal-title":"Biochem. J."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"23704","DOI":"10.1074\/jbc.M116.733857","article-title":"Ring-Mesh Model of Proteoglycan Glycosaminoglycan Chains in Tendon based on Three-dimensional Reconstruction by Focused Ion Beam Scanning Electron Microscopy","volume":"291","author":"Watanabe","year":"2016","journal-title":"J. Biol. Chem."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1016\/j.bbagen.2018.12.006","article-title":"Structural alteration of glycosaminoglycan side chains and spatial disorganization of collagen networks in the skin of patients with mcEDS-CHST14","volume":"1863","author":"Hirose","year":"2019","journal-title":"Biochim. Biophys. Acta Gen. Subj."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"6713","DOI":"10.1016\/S0021-9258(18)32276-2","article-title":"Activation of heparin cofactor II by dermatan sulfate","volume":"258","author":"Tollefsen","year":"1983","journal-title":"J. Biol. Chem."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"18263","DOI":"10.1016\/S0021-9258(17)44747-8","article-title":"Structure of a dermatan sulfate hexasaccharide that binds to heparin cofactor II with high affinity","volume":"265","author":"Maimone","year":"1990","journal-title":"J. Biol. Chem."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"28116","DOI":"10.1074\/jbc.273.43.28116","article-title":"Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function","volume":"273","author":"Penc","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"42815","DOI":"10.1074\/jbc.M204959200","article-title":"Dermatan sulfate binds and potentiates activity of keratinocyte growth factor (FGF-7)","volume":"277","author":"Trowbridge","year":"2002","journal-title":"J. Biol. Chem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1074\/jbc.273.1.271","article-title":"Hepatocyte growth factor\/scatter factor binds with high affinity to dermatan sulfate","volume":"273","author":"Lyon","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"5300","DOI":"10.1074\/jbc.M410412200","article-title":"Structural and sequence motifs in dermatan sulfate for promoting fibroblast growth factor-2 (FGF-2) and FGF-7 activity","volume":"280","author":"Taylor","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"43744","DOI":"10.1074\/jbc.M308169200","article-title":"Oversulfated dermatan sulfate exhibits neurite outgrowth-promoting activity toward embryonic mouse hippocampal neurons: Implications of dermatan sulfate in neuritogenesis in the brain","volume":"278","author":"Hikino","year":"2003","journal-title":"J. Biol. Chem."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"50799","DOI":"10.1074\/jbc.M404746200","article-title":"Structural and functional characterization of oversulfated chondroitin sulfate\/dermatan sulfate hybrid chains from the notochord of hagfish. Neuritogenic and binding activities for growth factors and neurotrophic factors","volume":"279","author":"Nandini","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"4058","DOI":"10.1074\/jbc.M412074200","article-title":"Novel 70-kDa chondroitin sulfate\/dermatan sulfate hybrid chains with a unique heterogeneous sulfation pattern from shark skin, which exhibit neuritogenic activity and binding activities for growth factors and neurotrophic factors","volume":"280","author":"Nandini","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"9180","DOI":"10.1074\/jbc.M413423200","article-title":"Heparin-binding growth factor, pleiotrophin, mediates neuritogenic activity of embryonic pig brain-derived chondroitin sulfate\/dermatan sulfate hybrid chains","volume":"280","author":"Bao","year":"2005","journal-title":"J. Biol. Chem."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"27673","DOI":"10.1074\/jbc.M110.118703","article-title":"Structure of pleiotrophin- and hepatocyte growth factor-binding sulfated hexasaccharide determined by biochemical and computational approaches","volume":"285","author":"Li","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1093\/jb\/mvab085","article-title":"Dermatan sulphate is an activating ligand of anaplastic lymphoma kinase","volume":"170","author":"Machino","year":"2021","journal-title":"J. Biochem."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1038\/bjc.1988.12","article-title":"Immunohistochemical localization of chondroitin sulphate and dermatan sulphate proteoglycans in tumour tissues","volume":"57","author":"Fukatsu","year":"1988","journal-title":"Br. J. Cancer"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s00418-009-0592-2","article-title":"Dermatan sulfate domains defined by the novel antibody GD3A12, in normal tissues and ovarian adenocarcinomas","volume":"132","author":"Yamada","year":"2009","journal-title":"Histochem. Cell. Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1943","DOI":"10.1158\/0008-5472.CAN-11-1351","article-title":"Dermatan sulfate is involved in the tumorigenic properties of esophagus squamous cell carcinoma","volume":"72","author":"Thelin","year":"2012","journal-title":"Cancer Res."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1016\/S0008-6215(02)00442-1","article-title":"Purification and characterization of dermatan sulfate from the skin of the eel, Anguilla japonica","volume":"338","author":"Sakai","year":"2003","journal-title":"Carbohydr. Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"31027","DOI":"10.1074\/jbc.270.52.31027","article-title":"A unique dermatan sulfate-like glycosaminoglycan from ascidian. Its structure and the effect of its unusual sulfation pattern on anticoagulant activity","volume":"270","author":"Mulloy","year":"1995","journal-title":"J. Biol. Chem."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"27848","DOI":"10.1074\/jbc.273.43.27848","article-title":"Highly sulfated dermatan sulfates from Ascidians. Structure versus anticoagulant activity of these glycosaminoglycans","volume":"273","author":"Aiello","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1093\/glycob\/11.6.433","article-title":"Embryos of the sea urchin Strongylocentrotus purpuratus synthesize a dermatan sulfate enriched in 4-O- and 6-O-disulfated galactosamine units","volume":"11","author":"Werneck","year":"2001","journal-title":"Glycobiology"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1007\/s10719-008-9124-x","article-title":"Determination of iduronic acid and glucuronic acid in sulfated chondroitin\/dermatan hybrid chains by (1)H-nuclear magnetic resonance spectroscopy","volume":"25","author":"Li","year":"2008","journal-title":"Glycoconj. J."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1093\/jb\/mvaa087","article-title":"Dermatan sulphate promotes neuronal differentiation in mouse and human stem cells","volume":"169","author":"Ogura","year":"2021","journal-title":"J. Biochem."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"733964","DOI":"10.3389\/fcell.2021.733964","article-title":"Dermatan-4-O-Sulfotransferase-1 Contributes to the Undifferentiated State of Mouse Embryonic Stem Cells","volume":"9","author":"Ogura","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"2252","DOI":"10.1096\/fj.201800852RR","article-title":"Knockdown of chondroitin-4-sulfotransferase-1, but not of dermatan-4-sulfotransferase-1, accelerates regeneration of zebrafish after spinal cord injury","volume":"33","author":"Sahu","year":"2019","journal-title":"FASEB J."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1083\/jcb.136.3.729","article-title":"Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility","volume":"136","author":"Danielson","year":"1997","journal-title":"J. Cell Biol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1038\/sj.mp.4001190","article-title":"A novel CpG-associated brain-expressed candidate gene for chromosome 18q-linked bipolar disorder","volume":"8","author":"Goossens","year":"2003","journal-title":"Mol. Psychiatry"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2565","DOI":"10.4049\/jimmunol.164.5.2565","article-title":"Identification of a gene coding for a new squamous cell carcinoma antigen recognized by the CTL","volume":"164","author":"Nakao","year":"2000","journal-title":"J. Immunol."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Stachtea, X.N., Tykesson, E., van Kuppevelt, T.H., Feinstein, R., Malmstr\u00f6m, A., Reijmers, R.M., and Maccarana, M. (2015). Dermatan sulfate-free mice display embryological defects and are neonatal lethal despite normal lymphoid and non-lymphoid organogenesis. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0140279"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1093\/glycob\/cws065","article-title":"Mouse development is not obviously affected by the absence of dermatan sulfate epimerase 2 in spite of a modified brain dermatan sulfate composition","volume":"22","author":"Bartolini","year":"2021","journal-title":"Glycobiology"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"4051","DOI":"10.1242\/jcs.088120","article-title":"Dermatan sulfotransferase Chst14\/D4st1, but not chondroitin sulfotransferase Chst11\/C4st1, regulates proliferation and neurogenesis of neural progenitor cells","volume":"124","author":"Bian","year":"2011","journal-title":"J. Cell Sci."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1093\/glycob\/cwx099","article-title":"Vascular abnormalities in the placenta of Chst14-\/- fetuses: Implications in the pathophysiology of perinatal lethality of the murine model and vascular lesions in human CHST14\/D4ST1 deficiency","volume":"28","author":"Yoshizawa","year":"2018","journal-title":"Glycobiology"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1002\/humu.22774","article-title":"Genetic heterogeneity and clinical variability in musculocontractural Ehlers-Danlos syndrome caused by impaired dermatan sulfate biosynthesis","volume":"36","author":"Syx","year":"2015","journal-title":"Hum. Mutat."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"103798","DOI":"10.1016\/j.ejmg.2019.103798","article-title":"DSE associated musculocontractural EDS, a milder phenotype or phenotypic variability","volume":"63","author":"Schirwani","year":"2020","journal-title":"Eur. J. Med. Genet."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"e1197","DOI":"10.1002\/mgg3.1197","article-title":"Delineation of musculocontractural Ehlers-Danlos syndrome caused by dermatan sulfate epimerase deficiency","volume":"8","author":"Lautrup","year":"2020","journal-title":"Mol. Genet. Genom. Med."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1111\/cga.12436","article-title":"A novel variant in the DSE gene leads to Ehlers-Danlos musculocontractural type 2 in a Pakistani family","volume":"61","author":"Ullah","year":"2021","journal-title":"Congenit. Anom."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1038\/mp.2009.124","article-title":"Genome-wide association study of recurrent early-onset major depressive disorder","volume":"16","author":"Shi","year":"2011","journal-title":"Mol. Psychiatry"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1002\/ajmg.a.33341","article-title":"A maternally inherited chromosome 18q22.1 deletion in a male with late-presenting diaphragmatic hernia and microphthalmia-evaluation of DSEL as a candidate gene for the diaphragmatic defect","volume":"152A","author":"Zayed","year":"2010","journal-title":"Am. J. Med. Genet."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1002\/ajmg.a.33498","article-title":"A new Ehlers-Danlos syndrome with craniofacial characteristics, multiple congenital contractures, progressive joint and skin laxity, and multisystem fragility-related manifestations","volume":"152A","author":"Kosho","year":"2010","journal-title":"Am. J. Med. Genet."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1002\/ajmg.a.35232","article-title":"Myopathy in a 20-year-old female patient with D4ST-1 deficient Ehlers-Danlos syndrome due to a homozygous CHST14 mutation","volume":"158A","author":"Voermans","year":"2012","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"2935","DOI":"10.1002\/ajmg.a.35613","article-title":"Re-assigned diagnosis of D4ST1-deficient Ehlers-Danlos syndrome (adducted thumb-clubfoot syndrome) after initial diagnosis of Marden-Walker syndrome","volume":"158A","author":"Winters","year":"2012","journal-title":"Am. J. Med. Genet. A."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1949","DOI":"10.1002\/ajmg.a.34115","article-title":"Delineation of dermatan 4-O-sulfotransferase 1 deficient Ehlers-Danlos syndrome: Observation of two additional patients and comprehensive review of 20 reported patients","volume":"155A","author":"Shimizu","year":"2011","journal-title":"Am. J. Med. Genet. A."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1002\/ajmg.a.35339","article-title":"Extracellular matrix and platelet function in patients with musculocontractural Ehlers-Danlos syndrome caused by mutations in the CHST14 gene","volume":"158A","author":"Chitayat","year":"2012","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_92","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":"170A","author":"Janecke","year":"2016","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1007\/s00439-016-1660-z","article-title":"Expanding the clinical and genetic heterogeneity of hereditary disorders of connective tissue","volume":"135","author":"Alazami","year":"2016","journal-title":"Hum. Genet."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"bcr2018226165","DOI":"10.1136\/bcr-2018-226165","article-title":"Novel mutation in the CHST14 gene causing musculocontractural type of Ehlers-Danlos syndrome","volume":"2018","author":"Sandal","year":"2018","journal-title":"BMJ Case Rep."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"2331","DOI":"10.1002\/ajmg.a.40507","article-title":"Spinal manifestations in 12 patients with musculocontractural Ehlers-Danlos syndrome caused by CHST14\/D4ST1 deficiency (mcEDS-CHST14)","volume":"176","author":"Uehara","year":"2018","journal-title":"Am. J. Med. Genet. A"},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Minatogawa, M., Unzaki, A., Morisaki, H., Syx, D., Sonoda, T., Janecke, A.R., Slavotinek, A., Voermans, N.C., Lacassie, Y., and Mendoza-Londono, R. Clinical and molecular features of 66 patients with musculocontractural Ehlers-Danlos syndrome caused by pathogenic variants in CHST14 (mcEDS-CHST14). J. Med. Genet., 2021. in press.","DOI":"10.1136\/jmedgenet-2020-107623"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1093\/glycob\/cwq208","article-title":"Dermatan sulfate epimerase 2 is the predominant isozyme in the formation of the chondroitin sulfate\/dermatan sulfate hybrid structure in postnatal developing mouse brain","volume":"21","author":"Akatsu","year":"2011","journal-title":"Glycobiology"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/13\/7485\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:43:12Z","timestamp":1760139792000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/13\/7485"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,5]]},"references-count":97,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2022,7]]}},"alternative-id":["ijms23137485"],"URL":"https:\/\/doi.org\/10.3390\/ijms23137485","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,5]]}}}