{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T06:07:49Z","timestamp":1792130869409,"version":"4.4.0"},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"6938","license":[{"start":{"date-parts":[[2003,5,1]],"date-time":"2003-05-01T00:00:00Z","timestamp":1051747200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nature"],"published-print":{"date-parts":[[2003,5]]},"DOI":"10.1038\/nature01634","type":"journal-article","created":{"date-parts":[[2003,5,21]],"date-time":"2003-05-21T12:52:58Z","timestamp":1053521578000},"page":"439-443","source":"Crossref","is-referenced-by-count":189,"title":["Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis"],"prefix":"10.1038","volume":"423","author":[{"given":"Ho-Yon","family":"Hwang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara K.","family":"Olson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeffrey D.","family":"Esko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"H.","family":"Robert Horvitz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","reference":[{"key":"BFnature01634_CR1","doi-asserted-by":"publisher","first-page":"1342","DOI":"10.1073\/pnas.87.4.1342","volume":"87","author":"E Quentin","year":"1990","unstructured":"Quentin, E., Gladen, A., Roden, L. & Kresse, H. A genetic defect in the biosynthesis of dermatan sulfate proteoglycan: galactosyltransferase I deficiency in fibroblasts from a patient with a progeroid syndrome. Proc. Natl Acad. Sci. USA 87, 1342\u20131346 (1990)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature01634_CR2","doi-asserted-by":"publisher","first-page":"725","DOI":"10.1038\/35008000","volume":"404","author":"N Perrimon","year":"2000","unstructured":"Perrimon, N. & Bernfield, M. Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404, 725\u2013728 (2000)","journal-title":"Nature"},{"key":"BFnature01634_CR3","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1016\/S0304-4165(02)00402-6","volume":"1573","author":"BM Zak","year":"2002","unstructured":"Zak, B. M., Crawford, B. E. & Esko, J. D. Hereditary multiple exostoses and heparan sulfate polymerization. Biochim. Biophys. Acta 1573, 346\u2013355 (2002)","journal-title":"Biochim. Biophys. Acta"},{"key":"BFnature01634_CR4","doi-asserted-by":"publisher","first-page":"57R","DOI":"10.1093\/glycob\/12.4.57R","volume":"12","author":"NB Schwartz","year":"2002","unstructured":"Schwartz, N. B. & Domowicz, M. Chondrodysplasias due to proteoglycan defects. Glycobiology 12, 57R\u201368R (2002)","journal-title":"Glycobiology"},{"key":"BFnature01634_CR5","doi-asserted-by":"publisher","first-page":"968","DOI":"10.1073\/pnas.96.3.968","volume":"96","author":"T Herman","year":"1999","unstructured":"Herman, T., Hartwieg, E. & Horvitz, H. R. sqv mutants of Caenorhabditis elegans are defective in vulval epithelial invagination. Proc. Natl Acad. Sci. USA 96, 968\u2013973 (1999)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature01634_CR6","doi-asserted-by":"publisher","first-page":"14218","DOI":"10.1073\/pnas.172522199","volume":"99","author":"H-Y Hwang","year":"2002","unstructured":"Hwang, H.-Y. & Horvitz, H. R. The SQV-1 UDP-glucuronic acid decarboxylase and the SQV-7 nucleotide-sugar transporter may act in the Golgi apparatus to affect C. elegans vulval morphogenesis and embryonic development. Proc. Natl Acad. Sci. USA 99, 14218\u201314223 (2002)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature01634_CR7","doi-asserted-by":"publisher","first-page":"974","DOI":"10.1073\/pnas.96.3.974","volume":"96","author":"T Herman","year":"1999","unstructured":"Herman, T. & Horvitz, H. R. Three proteins involved in Caenorhabditis elegans vulval invagination are similar to components of a glycosylation pathway. Proc. Natl Acad. Sci. USA 96, 974\u2013979 (1999)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature01634_CR8","doi-asserted-by":"publisher","first-page":"10838","DOI":"10.1073\/pnas.97.20.10838","volume":"97","author":"DA Bulik","year":"2000","unstructured":"Bulik, D. A. et al. sqv-3, -7, and -8, a set of genes affecting morphogenesis in Caenorhabditis elegans, encode enzymes required for glycosaminoglycan biosynthesis. Proc. Natl Acad. Sci. USA 97, 10838\u2013108343 (2000)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature01634_CR9","doi-asserted-by":"publisher","first-page":"3738","DOI":"10.1073\/pnas.061593098","volume":"98","author":"P Berninsone","year":"2001","unstructured":"Berninsone, P., Hwang, H. Y., Zemtseva, I., Horvitz, H. R. & Hirschberg, C. B. SQV-7, a protein involved in Caenorhabditis elegans epithelial invagination and early embryogenesis, transports UDP-glucuronic acid, UDP-N-acetylgalactosamine, and UDP-galactose. Proc. Natl Acad. Sci. USA 98, 3738\u20133743 (2001)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature01634_CR10","doi-asserted-by":"publisher","first-page":"14224","DOI":"10.1073\/pnas.172522499","volume":"99","author":"H-Y Hwang","year":"2002","unstructured":"Hwang, H.-Y. & Horvitz, H. R. The C. elegans vulval morphogenesis gene sqv-4 encodes a UDP-glucose dehydrogenase that is temporally and spatially regulated. Proc. Natl Acad. Sci. USA 99, 14224\u201314229 (2002)","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnature01634_CR11","doi-asserted-by":"publisher","first-page":"11735","DOI":"10.1074\/jbc.C200518200","volume":"278","author":"H-Y Hwang","year":"2003","unstructured":"Hwang, H.-Y., Olson, S. K., Brown, J. R., Esko, J. D. & Horvitz, H. R. The C. elegans genes sqv-2 and sqv-6, which are involved in vulval morphogenesis, encode glycosaminoglycan galactosyltransferase II and xylosyltransferase. J. Biol. Chem. 278, 11735\u201311738 (2003)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR12","doi-asserted-by":"publisher","first-page":"255","DOI":"10.1152\/physrev.1978.58.1.255","volume":"58","author":"WD Comper","year":"1978","unstructured":"Comper, W. D. & Laurent, T. C. Physiological function of connective tissue polysaccharides. Physiol. Rev. 58, 255\u2013315 (1978)","journal-title":"Physiol. Rev."},{"key":"BFnature01634_CR13","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1146\/annurev.cb.04.110188.001305","volume":"4","author":"E Ruoslahti","year":"1988","unstructured":"Ruoslahti, E. Structure and biology of proteoglycans. Annu. Rev. Cell Biol. 4, 229\u2013255 (1988)","journal-title":"Annu. Rev. Cell Biol."},{"key":"BFnature01634_CR14","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1146\/annurev.biochem.71.110601.135458","volume":"71","author":"JD Esko","year":"2002","unstructured":"Esko, J. D. & Selleck, S. B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435\u2013471 (2002)","journal-title":"Annu. Rev. Biochem."},{"key":"BFnature01634_CR15","doi-asserted-by":"publisher","first-page":"177","DOI":"10.1080\/15216540214923","volume":"54","author":"JE Silbert","year":"2002","unstructured":"Silbert, J. E. & Sugumaran, G. Biosynthesis of chondroitin\/dermatan sulfate. Intl Union Biochem. Mol. Biol. Life 54, 177\u2013186 (2002)","journal-title":"Intl Union Biochem. Mol. Biol. Life"},{"key":"BFnature01634_CR16","volume-title":"Fertilization","author":"CR Austin","year":"1965","unstructured":"Austin, C. R. Fertilization (New Jersey, Prentice Hall, Englewood Cliffs, 1965)"},{"key":"BFnature01634_CR17","doi-asserted-by":"publisher","first-page":"26165","DOI":"10.1074\/jbc.274.37.26165","volume":"274","author":"R Almeida","year":"1999","unstructured":"Almeida, R. et al. Cloning and expression of a proteoglycan UDP-galactose: \u03b2-xylose \u03b21,4-galactosyltransferase I. J. Biol. Chem. 274, 26165\u201326171 (1999)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR18","doi-asserted-by":"publisher","first-page":"28841","DOI":"10.1074\/jbc.274.41.28841","volume":"274","author":"T Okajima","year":"1999","unstructured":"Okajima, T., Fukumoto, S., Furukawa, K. & Urano, T. Molecular basis for the progeroid variant of Ehlers\u2013Danlos syndrome. J. Biol. Chem. 274, 28841\u201328844 (1999)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR19","doi-asserted-by":"publisher","first-page":"38721","DOI":"10.1074\/jbc.M106871200","volume":"276","author":"H Kitagawa","year":"2001","unstructured":"Kitagawa, H., Uyama, T. & Sugahara, K. Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276, 38721\u201338726 (2001)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR20","doi-asserted-by":"publisher","first-page":"8841","DOI":"10.1074\/jbc.M111434200","volume":"277","author":"T Uyama","year":"2002","unstructured":"Uyama, T., Kitagawa, H., Tamura Ji, J. & Sugahara, K. Molecular cloning and expression of human chondroitin N-acetylgalactosaminyltransferase. J. Biol. Chem. 277, 8841\u20138846 (2002)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR21","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1016\/S0014-5793(99)01286-7","volume":"459","author":"S Yamada","year":"1999","unstructured":"Yamada, S. et al. Demonstration of glycosaminoglycans in Caenorhabditis elegans. FEBS Lett. 459, 327\u2013331 (1999)","journal-title":"FEBS Lett."},{"key":"BFnature01634_CR22","doi-asserted-by":"publisher","first-page":"2269","DOI":"10.1074\/jbc.275.4.2269","volume":"275","author":"H Toyoda","year":"2000","unstructured":"Toyoda, H., Kinoshita-Toyoda, A. & Selleck, S. B. Structural analysis of glycosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumour suppressors, affects heparan sulfate in vivo. J. Biol. Chem. 275, 2269\u20132275 (2000)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR23","doi-asserted-by":"publisher","first-page":"854","DOI":"10.1038\/27579","volume":"395","author":"L Timmons","year":"1998","unstructured":"Timmons, L. & Fire, A. Specific interference by ingested dsRNA. Nature 395, 854 (1998)","journal-title":"Nature"},{"key":"BFnature01634_CR24","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1242\/dev.117.3.1049","volume":"117","author":"MC Lane","year":"1993","unstructured":"Lane, M. C., Koehl, M. A., Wilt, F. & Keller, R. A role for regulated secretion of apical extracellular matrix during epithelial invagination in the sea urchin. Development 117, 1049\u20131060 (1993)","journal-title":"Development"},{"key":"BFnature01634_CR25","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1093\/genetics\/139.2.561","volume":"139","author":"RE Ellis","year":"1995","unstructured":"Ellis, R. E. & Kimble, J. The fog-3 gene and regulation of cell fate in the germ line of Caenorhabditis elegans. Genetics 139, 561\u2013577 (1995)","journal-title":"Genetics"},{"key":"BFnature01634_CR26","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1038\/ng0997-119","volume":"17","author":"G Jansen","year":"1997","unstructured":"Jansen, G., Hazendonk, E., Thijssen, K. L. & Plasterk, R. H. Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nature Genet. 17, 119\u2013121 (1997)","journal-title":"Nature Genet."},{"key":"BFnature01634_CR27","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/S0008-6215(00)83402-3","volume":"58","author":"K Nagasawa","year":"1977","unstructured":"Nagasawa, K., Inoue, Y. & Kamata, T. Solvolytic desulfation of glycosaminoglycuronan sulfates with dimethyl sulfoxide containing water or methanol. Carbohydr. Res. 58, 47\u201355 (1977)","journal-title":"Carbohydr. Res."},{"key":"BFnature01634_CR28","doi-asserted-by":"crossref","first-page":"28809","DOI":"10.1016\/S0021-9258(19)61978-2","volume":"269","author":"TA Fritz","year":"1994","unstructured":"Fritz, T. A., Gabb, M. M., Wei, G. & Esko, J. D. Two N-acetylglucosaminyltransferases catalyze the biosynthesis of heparan sulfate. J. Biol. Chem. 269, 28809\u201328814 (1994)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR29","doi-asserted-by":"crossref","first-page":"27733","DOI":"10.1074\/jbc.M002990200","volume":"275","author":"G Wei","year":"2000","unstructured":"Wei, G. et al. Location of the glucuronosyltransferase domain in the heparan sulfate copolymerase EXT1 by analysis of Chinese hamster ovary cell mutants. J. Biol. Chem. 275, 27733\u201327740 (2000)","journal-title":"J. Biol. Chem."},{"key":"BFnature01634_CR30","first-page":"17.2.1","volume-title":"Current Protocols in Molecular Biology","author":"JD Esko","year":"1993","unstructured":"Esko, J. D. in Current Protocols in Molecular Biology (ed. Ausubel, F.) 17.2.1\u201317.2.9 (John Wiley and Sons, New York, 1993)"}],"container-title":["Nature"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/nature01634.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nature01634","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nature01634.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,18]],"date-time":"2023-05-18T14:15:00Z","timestamp":1684419300000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/nature01634"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,5]]},"references-count":30,"journal-issue":{"issue":"6938","published-print":{"date-parts":[[2003,5]]}},"alternative-id":["BFnature01634"],"URL":"https:\/\/doi.org\/10.1038\/nature01634","relation":{"has-review":[{"id-type":"doi","id":"10.3410\/f.1014046.192614","asserted-by":"object"}]},"ISSN":["0028-0836","1476-4687"],"issn-type":[{"value":"0028-0836","type":"print"},{"value":"1476-4687","type":"electronic"}],"subject":[],"published":{"date-parts":[[2003,5]]}}}