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Structure, substrate recognition and initiation of hyaluronan synthase.

Maloney FP, Kuklewicz J, Corey RA, Bi Y, Ho R, Mateusiak L, Pardon E, Steyaert J, Stansfeld PJ, Zimmer J
Nature 604 195-201 (2022)
Related entries: 7sp6, 7sp8, 7sp9, 7spa

Cited: 33 times
EuropePMC logo PMID: 35355017

Abstract

Hyaluronan is an acidic heteropolysaccharide comprising alternating N-acetylglucosamine and glucuronic acid sugars that is ubiquitously expressed in the vertebrate extracellular matrix1. The high-molecular-mass polymer modulates essential physiological processes in health and disease, including cell differentiation, tissue homeostasis and angiogenesis2. Hyaluronan is synthesized by a membrane-embedded processive glycosyltransferase, hyaluronan synthase (HAS), which catalyses the synthesis and membrane translocation of hyaluronan from uridine diphosphate-activated precursors3,4. Here we describe five cryo-electron microscopy structures of a viral HAS homologue at different states during substrate binding and initiation of polymer synthesis. Combined with biochemical analyses and molecular dynamics simulations, our data reveal how HAS selects its substrates, hydrolyses the first substrate to prime the synthesis reaction, opens a hyaluronan-conducting transmembrane channel, ensures alternating substrate polymerization and coordinates hyaluronan inside its transmembrane pore. Our research suggests a detailed model for the formation of an acidic extracellular heteropolysaccharide and provides insights into the biosynthesis of one of the most abundant and essential glycosaminoglycans in the human body.

Articles - 7sp7 mentioned but not cited (2)

  1. Structure, substrate recognition and initiation of hyaluronan synthase. Maloney FP, Kuklewicz J, Corey RA, Bi Y, Ho R, Mateusiak L, Pardon E, Steyaert J, Stansfeld PJ, Zimmer J. Nature 604 195-201 (2022)
  2. Structural and mechanistic insights into fungal β-1,3-glucan synthase FKS1. Hu X, Yang P, Chai C, Liu J, Sun H, Wu Y, Zhang M, Zhang M, Liu X, Yu H. Nature 616 190-198 (2023)


Reviews citing this publication (10)

  1. The Astounding World of Glycans from Giant Viruses. Speciale I, Notaro A, Abergel C, Lanzetta R, Lowary TL, Molinaro A, Tonetti M, Van Etten JL, De Castro C. Chem Rev 122 15717-15766 (2022)
  2. Effects of Hyaluronan on Breast Cancer Aggressiveness. Parnigoni A, Moretto P, Viola M, Karousou E, Passi A, Vigetti D. Cancers (Basel) 15 3813 (2023)
  3. Role of Hyaluronic Acid in Selected Malignant Neoplasms in Women. Markowska A, Antoszczak M, Markowska J, Huczyński A. Biomedicines 11 304 (2023)
  4. 3D printed scaffolds based on hyaluronic acid bioinks for tissue engineering: a review. Chen H, Xue H, Zeng H, Dai M, Tang C, Liu L. Biomater Res 27 137 (2023)
  5. Genetic Deficiencies of Hyaluronan Degradation. Fink SP, Triggs-Raine B. Cells 13 1203 (2024)
  6. Pseudomonas aeruginosa biofilm exopolysaccharides: assembly, function, and degradation. Gheorghita AA, Wozniak DJ, Parsek MR, Howell PL. FEMS Microbiol Rev 47 fuad060 (2023)
  7. Application of Pro-angiogenic Biomaterials in Myocardial Infarction. Liang T, Liu J, Liu F, Su X, Li X, Zeng J, Chen F, Wen H, Chen Y, Tao J, Lei Q, Li G, Cheng P. ACS Omega 9 37505-37529 (2024)
  8. Atomic-Resolution Experimental Structural Biology and Molecular Dynamics Simulations of Hyaluronan and Its Complexes. Guvench O. Molecules 27 7276 (2022)
  9. Hyaluronan synthases; mechanisms, myths, & mysteries of three types of unique bifunctional glycosyltransferases. DeAngelis PL, Zimmer J. Glycobiology 33 1117-1127 (2023)
  10. Modification and crosslinking strategies for hyaluronic acid-based hydrogel biomaterials. Luo Z, Wang Y, Xu Y, Wang J, Yu Y. Smart Med 2 e20230029 (2023)

Articles citing this publication (21)

  1. Structural basis for directional chitin biosynthesis. Chen W, Cao P, Liu Y, Yu A, Wang D, Chen L, Sundarraj R, Yuchi Z, Gong Y, Merzendorfer H, Yang Q. Nature 610 402-408 (2022)
  2. Structure of a fungal 1,3-β-glucan synthase. Zhao CR, You ZL, Chen DD, Hang J, Wang ZB, Ji M, Wang LX, Zhao P, Qiao J, Yun CH, Bai L. Sci Adv 9 eadh7820 (2023)
  3. Structural basis for heparan sulfate co-polymerase action by the EXT1-2 complex. Li H, Chapla D, Amos RA, Ramiah A, Moremen KW, Li H. Nat Chem Biol 19 565-574 (2023)
  4. Insights into substrate coordination and glycosyl transfer of poplar cellulose synthase-8. Verma P, Kwansa AL, Ho R, Yingling YG, Zimmer J. Structure 31 1166-1173.e6 (2023)
  5. A multi-enzyme machine polymerizes the Haemophilus influenzae type b capsule. Cifuente JO, Schulze J, Bethe A, Di Domenico V, Litschko C, Budde I, Eidenberger L, Thiesler H, Ramón Roth I, Berger M, Claus H, D'Angelo C, Marina A, Gerardy-Schahn R, Schubert M, Guerin ME, Fiebig T. Nat Chem Biol 19 865-877 (2023)
  6. Mechanism of mixed-linkage glucan biosynthesis by barley cellulose synthase-like CslF6 (1,3;1,4)-β-glucan synthase. Purushotham P, Ho R, Yu L, Fincher GB, Bulone V, Zimmer J. Sci Adv 8 eadd1596 (2022)
  7. Structure, catalysis, chitin transport, and selective inhibition of chitin synthase. Chen DD, Wang ZB, Wang LX, Zhao P, Yun CH, Bai L. Nat Commun 14 4776 (2023)
  8. Imaging of Escherichia coli K5 and glycosaminoglycan precursors via targeted metabolic labeling of capsular polysaccharides in bacteria. Wang YJ, Li L, Yu J, Hu HY, Liu ZX, Jiang WJ, Xu W, Guo XP, Wang FS, Sheng JZ. Sci Adv 9 eade4770 (2023)
  9. Letter Structures and mechanism of chitin synthase and its inhibition by antifungal drug Nikkomycin Z. Wu Y, Zhang M, Yang Y, Ding X, Yang P, Huang K, Hu X, Zhang M, Liu X, Yu H. Cell Discov 8 129 (2022)
  10. Structure-function analysis of the cyclic β-1,2-glucan synthase from Agrobacterium tumefaciens. Sedzicki J, Ni D, Lehmann F, Stahlberg H, Dehio C. Nat Commun 15 1844 (2024)
  11. Tetrahedral framework nucleic acids/hyaluronic acid-methacrylic anhydride hybrid hydrogel with antimicrobial and anti-inflammatory properties for infected wound healing. Qi C, Sun Q, Xiao D, Zhang M, Gao S, Guo B, Lin Y. Int J Oral Sci 16 30 (2024)
  12. Age related changes in hyaluronan expression leads to Meibomian gland dysfunction. Verma S, Moreno IY, Sun M, Gesteira TF, Coulson-Thomas VJ. Matrix Biol 124 23-38 (2023)
  13. Enzymes in 3D: Synthesis, remodelling, and hydrolysis of cell wall (1,3;1,4)-β-glucans. Hrmova M, Zimmer J, Bulone V, Fincher GB. Plant Physiol 194 33-50 (2023)
  14. Identification of a Small Molecule Inhibitor of Hyaluronan Synthesis, DDIT, Targeting Breast Cancer Cells. Karalis T, Shiau AK, Gahman TC, Skandalis SS, Heldin CH, Heldin P. Cancers (Basel) 14 5800 (2022)
  15. Targeted Analysis of the Size Distribution of Heavy Chain-Modified Hyaluronan with Solid-State Nanopores. Erxleben DA, Dodd RJ, Day AJ, Green DE, DeAngelis PL, Poddar S, Enghild JJ, Huebner JL, Kraus VB, Watkins AR, Reesink HL, Rahbar E, Hall AR. Anal Chem 96 1606-1613 (2024)
  16. Comment Earliest known surgery was of a child in Borneo 31,000 years ago. Roberts CA. Nature 609 472-473 (2022)
  17. Molecular insights into capsular polysaccharide secretion. Kuklewicz J, Zimmer J. Nature 628 901-909 (2024)
  18. Historical Article Prehistoric child's amputation is oldest surgery of its kind. Prillaman M. Nature 609 453-454 (2022)
  19. Strongly ROS-Correlated, Time-Dependent, and Selective Antiproliferative Effects of Synthesized Nano Vesicles on BRAF Mutant Melanoma Cells and Their Hyaluronic Acid-Based Hydrogel Formulation. Alfei S, Zuccari G, Athanassopoulos CM, Domenicotti C, Marengo B. Int J Mol Sci 25 10071 (2024)
  20. Structural insights into translocation and tailored synthesis of hyaluronan. Górniak I, Stephens Z, Erramilli SK, Gawda T, Kossiakoff AA, Zimmer J. Nat Struct Mol Biol (2024)
  21. Targeting hyaluronan metabolism-related molecules associated with resistant tumor-initiating cells potentiates chemotherapy efficacy in lung cancer. Díaz MA, Fusco M, Benítez CA, Gayet F, García L, Victoria L, Jaramillo S, Bayo J, Zubieta MR, Rizzo MM, Piccioni F, Malvicini M. Sci Rep 14 16803 (2024)


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