Expression of chondroitin/dermatan sulfate glycosyltransferases during early zebrafish development

Background: Chondroitin/dermatan sulfate (CS/DS) proteoglycans present in the extracellular matrix have important structural and regulatory functions. Results: Six human genes have previously been shown to catalyze CS/DS polymerization. Here we show that one of these genes, chpf, is represented by two copies in the zebrafish genome, chpfa and chpfb, while the other five human CS/DS glycosyltransferases csgalnact1, csgalnact2, chpf2, chsy1, and chsy3 all have single zebrafish orthologues. The putative zebrafish CS/DS glycosyltransferases are spatially and temporally expressed. Interestingly, overlapping expression of multiple glycosyltransferases coincides with high CS/DS deposition. Finally, whereas the relative levels of the related polysaccharide HS reach steady‐state at around 2 days post fertilization, there is a continued relative increase of the CS amounts per larvae during the first 6 days of development, matching the increased cartilage formation. Conclusions: There are 7 CS/DS glycosyltransferases in zebrafish, which, based on homology, can be divided into the CSGALNACT, CHSY, and CHPF families. The overlap between intense CS/DS production and the expression of multiple CS/DS glycosyltransferases suggests that efficient CS/DS biosynthesis requires a combination of several glycosyltransferases. Developmental Dynamics 242:964–975, 2013. © 2013 Wiley Periodicals, Inc.

[1]  M. Wiweger,et al.  On the Roles and Regulation of Chondroitin Sulfate and Heparan Sulfate in Zebrafish Pharyngeal Cartilage Morphogenesis* , 2012, The Journal of Biological Chemistry.

[2]  J. Silberg,et al.  A transposase strategy for creating libraries of circularly permuted proteins , 2012, Nucleic acids research.

[3]  The UniProt Consortium,et al.  Reorganizing the protein space at the Universal Protein Resource (UniProt) , 2011, Nucleic Acids Res..

[4]  M. Ishii,et al.  Functions of Chondroitin Sulfate and Heparan Sulfate in the Developing Brain , 2011, Neurochemical Research.

[5]  J. Nicolas,et al.  Laminins, via heparan sulfate proteoglycans, participate in zebrafish myotome morphogenesis by modulating the pattern of Bmp responsiveness , 2011, Development.

[6]  R. Hegele,et al.  Temtamy preaxial brachydactyly syndrome is caused by loss-of-function mutations in chondroitin synthase 1, a potential target of BMP signaling. , 2010, American journal of human genetics.

[7]  B. Merriman,et al.  Loss of CHSY1, a secreted FRINGE enzyme, causes syndromic brachydactyly in humans via increased NOTCH signaling. , 2010, American journal of human genetics.

[8]  H. Kitagawa,et al.  Chondroitin sulfate N-acetylgalactosaminyltransferase-1 is required for normal cartilage development , 2010, The Biochemical journal.

[9]  J. Postlethwait,et al.  UDP xylose synthase 1 is required for morphogenesis and histogenesis of the craniofacial skeleton. , 2010, Developmental biology.

[10]  H. Kitagawa,et al.  Impairment of Embryonic Cell Division and Glycosaminoglycan Biosynthesis in Glucuronyltransferase-I-deficient Mice* , 2010, The Journal of Biological Chemistry.

[11]  V. Tran,et al.  Investigating the Elusive Mechanism of Glycosaminoglycan Biosynthesis* , 2009, The Journal of Biological Chemistry.

[12]  Brandi L. Cantarel,et al.  The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics , 2008, Nucleic Acids Res..

[13]  H. Kitagawa,et al.  Identification of Chondroitin Sulfate Glucuronyltransferase as Chondroitin Synthase-3 Involved in Chondroitin Polymerization , 2008, Journal of Biological Chemistry.

[14]  M. Wilén,et al.  Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation , 2008, Proceedings of the National Academy of Sciences.

[15]  H. Kitagawa,et al.  Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor. , 2007, The Biochemical journal.

[16]  Norio Suzuki,et al.  Chondroitin acts in the guidance of gonadal distal tip cells in C. elegans. , 2006, Developmental biology.

[17]  M. Wilén,et al.  Enzymatically Active N-Deacetylase/N-Sulfotransferase-2 Is Present in Liver but Does Not Contribute to Heparan Sulfate N-Sulfation* , 2006, Journal of Biological Chemistry.

[18]  H. Narimatsu Human glycogene cloning: focus on β3-glycosyltransferase and β4-glycosyltransferase families , 2006 .

[19]  Jeffrey D. Esko,et al.  Identification of novel chondroitin proteoglycans in Caenorhabditis elegans: embryonic cell division depends on CPG-1 and CPG-2 , 2006, The Journal of cell biology.

[20]  H. Kitagawa,et al.  Nematode Chondroitin Polymerizing Factor Showing Cell-/Organ-specific Expression Is Indispensable for Chondroitin Synthesis and Embryonic Cell Division* , 2004, Journal of Biological Chemistry.

[21]  M. P. Cummings PHYLIP (Phylogeny Inference Package) , 2004 .

[22]  Johan Ledin,et al.  Heparan Sulfate Structure in Mice with Genetically Modified Heparan Sulfate Production* , 2004, Journal of Biological Chemistry.

[23]  L. Kjellén,et al.  Sulfotransferases in glycosaminoglycan biosynthesis. , 2003, Current Opinion in Structural Biology.

[24]  M. Shionyu,et al.  Chondroitin Sulfate Synthase-2 , 2003, Journal of Biological Chemistry.

[25]  H. Kitagawa,et al.  Molecular Cloning of a Chondroitin Polymerizing Factor That Cooperates with Chondroitin Synthase for Chondroitin Polymerization* , 2003, Journal of Biological Chemistry.

[26]  Martin Vingron,et al.  New evidence for genome-wide duplications at the origin of vertebrates using an amphioxus gene set and completed animal genomes. , 2003, Genome research.

[27]  H. Horvitz,et al.  Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis , 2003, Nature.

[28]  H. Kitagawa,et al.  Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans , 2003, Nature.

[29]  T. Vogt,et al.  Molecular genetic analysis of the glycosyltransferase Fringe in Drosophila , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  H. Kitagawa,et al.  Molecular Cloning and Expression of a Second Chondroitin N-Acetylgalactosaminyltransferase Involved in the Initiation and Elongation of Chondroitin/Dermatan Sulfate* , 2003, The Journal of Biological Chemistry.

[31]  T. Imamura,et al.  Differential roles of two N-acetylgalactosaminyltransferases, CSGalNAcT-1, and a novel enzyme, CSGalNAcT-2. Initiation and elongation in synthesis of chondroitin sulfate. , 2003, The Journal of biological chemistry.

[32]  H. Narimatsu,et al.  Molecular Cloning and Characterization of a Novel Chondroitin Sulfate Glucuronyltransferase That Transfers Glucuronic Acid toN-Acetylgalactosamine* , 2002, The Journal of Biological Chemistry.

[33]  H. Kitagawa,et al.  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. , 2002, The Journal of biological chemistry.

[34]  H. Kitagawa,et al.  Molecular Cloning and Expression of a Human Chondroitin Synthase* , 2001, The Journal of Biological Chemistry.

[35]  H. Kitagawa,et al.  The EXT1/EXT2 tumor suppressors: catalytic activities and role in heparan sulfate biosynthesis , 2000, EMBO reports.

[36]  C. McCormick,et al.  The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  P. Holland,et al.  Gene duplication: past, present and future. , 1999, Seminars in cell & developmental biology.

[38]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[39]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[40]  Stephen W. Wilson,et al.  Regulatory gene expression boundaries demarcate sites of neuronal differentiation in the embryonic zebrafish forebrain , 1994, Neuron.

[41]  J. Esko,et al.  Proteoglycans and Sulfated Glycosaminoglycans , 2009 .

[42]  R. Sasisekharan,et al.  The biosynthesis and catabolism of galactosaminoglycans. , 2006, Advances in pharmacology.

[43]  H. Narimatsu Human glycogene cloning: focus on beta 3-glycosyltransferase and beta 4-glycosyltransferase families. , 2006, Current opinion in structural biology.

[44]  M. Shionyu,et al.  Chondroitin Sulfate Synthase-2 MOLECULAR CLONING AND CHARACTERIZATION OF A NOVEL HUMAN GLYCOSYLTRANSFERASE HOMOLOGOUS TO CHONDROITIN SULFATE GLUCURONYLTRANSFERASE, WHICH HAS DUAL ENZYMATIC ACTIVITIES* , 2003 .

[45]  Ralf Dahm,et al.  Zebrafish: A Practical Approach. Edited by C. NÜSSLEIN-VOLHARD and R. DAHM. Oxford University Press. 2002. 322 pages. ISBN 0 19 963808 X. Price £40.00 (paperback). ISBN 0 19 963809 8. Price £80.00 (hardback). , 2003 .

[46]  S. Selleck,et al.  Order out of chaos: assembly of ligand binding sites in heparan sulfate. , 2002, Annual review of biochemistry.

[47]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.