Yongmei Xu, Yi-Chi Wang, Eduardo Stancanelli, Haoran Wang, Jianxiang Zhang, Emil Tykesson, Anders Malmström, Jian Liu
Dermatan sulfate epimerase 1 (DS-epi1, DSE) and dermatan sulfate 4-O-sulfotransferase (DS 4-OST, CHST14) are critical enzymes involved in the biosynthesis of dermatan sulfate. In this study, structurally homogeneous chondroitin oligosaccharide substrates were used to investigate the substrate specificity of each individual enzyme, as well as their combined actions. The structures of the enzyme-modified oligosaccharides were confirmed by high-resolution mass spectrometry (MS) and NMR or determined by LC-MS-based sequencing analysis. Our results demonstrate that DS-epi1 catalyzes the reversible conversion between glucuronic acid (GlcA) and iduronic acid (IdoA), with GlcA being the predominant product once the reaction reaches equilibrium. DS 4-OST selectively sulfates the 4-hydroxyl group of N-acetylgalactosamine (GalNAc) residues that are linked to the reducing end of an IdoA unit (-IdoA-GalNAc-). Furthermore, DS-epi1 and DS 4-OST act in a concerted and ordered manner to generate clustered -IdoA-GalNAc4S- domains. During the reaction, the enzyme mixture initiates modifications at the non-reducing end of the saccharide chain and proceeds toward the reducing end consecutively. These findings provide new insights into the regulatory mechanisms governing dermatan sulfate biosynthesis and demonstrate the feasibility of synthesizing structurally defined dermatan sulfate oligosaccharides.