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Mechanism of hyaluronan binding and degradation: structure of Streptococcus pneumoniae hyaluronate lyase in complex with hyaluronic acid disaccharide at 1.7 A resolution.

Ponnuraj K, Jedrzejas MJ
J Mol Biol 299 885-95 (2000)
Cited: 44 times
EuropePMC logo PMID: 10843845

Abstract

Hyaluronic acid (HA) is an important constituent of the extracellular matrix; its bacterial degradation has been postulated to contribute to the spread of certain streptococci through tissue. Pneumococci and other streptococci produce hyaluronate lyase, an enzyme which depolymerizes HA, thus hyaluronate lyase might contribute directly to bacterial invasion. Although two different mechanisms for lyase action have been proposed, there was no crystallographic evidence to support those mechanisms. Here, we report the high-resolution crystal structure of Streptococcus pneumoniae hyaluronate lyase in the presence of HA disaccharide product, which ultimately provides the first crystallographic evidence for the binding of HA to hyaluronate lyase. This structural complex revealed a key interaction between the Streptococcus peneumoniae hyaluronate lyase protein and the product, and supports our previously proposed novel catalytic mechanism for HA degradation based on the native Streptococcus peneumoniae hyaluronate lyase structure. The information provided by this complex structure will likely be useful in the development of antimicrobial pharmaceutical agents.

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  1. Atomic-Resolution Experimental Structural Biology and Molecular Dynamics Simulations of Hyaluronan and Its Complexes. Guvench O. Molecules 27 7276 (2022)

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  1. Enhanced propagation of Granulicatella adiacens from human oral microbiota by hyaluronan. Yabuuchi S, Oiki S, Minami S, Takase R, Watanabe D, Hashimoto W. Sci Rep 12 10948 (2022)


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  7. Crystal structure of unsaturated glucuronyl hydrolase, responsible for the degradation of glycosaminoglycan, from Bacillus sp. GL1 at 1.8 A resolution. Itoh T, Akao S, Hashimoto W, Mikami B, Murata K. J Biol Chem 279 31804-31812 (2004)
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  14. Alternate structural conformations of Streptococcus pneumoniae hyaluronan lyase: insights into enzyme flexibility and underlying molecular mechanism of action. Rigden DJ, Littlejohn JE, Joshi HV, de Groot BL, Jedrzejas MJ. J Mol Biol 358 1165-1178 (2006)
  15. Enzymatic and chemical methods for the generation of pure hyaluronan oligosaccharides with both odd and even numbers of monosaccharide units. Blundell CD, Almond A. Anal Biochem 353 236-247 (2006)
  16. Crystal structures of a family 8 polysaccharide lyase reveal open and highly occluded substrate-binding cleft conformations. Elmabrouk ZH, Vincent F, Zhang M, Smith NL, Turkenburg JP, Charnock SJ, Black GW, Taylor EJ. Proteins 79 965-974 (2011)
  17. Interaction of pneumococcal phase variation, host and pressure/gas composition: virulence expression of NanA, HylA, PspA and CbpA in simulated otitis media. Li-Korotky HS, Lo CY, Banks JM. Microb Pathog 49 204-210 (2010)
  18. An atypical approach identifies TYR234 as the key base catalyst in chondroitin AC lyase. Rye CS, Matte A, Cygler M, Withers SG. Chembiochem 7 631-637 (2006)
  19. Genome-based identification of a carbohydrate binding module in Streptococcus pneumoniae hyaluronate lyase. Rigden DJ, Jedrzejas MJ. Proteins 52 203-211 (2003)
  20. A single nucleotide mutation results in loss of enzymatic activity in the hyaluronate lyase gene of Streptococcus pyogenes. Hynes W, Johnson C, Stokes M. Microb Pathog 47 308-313 (2009)
  21. Domain motions of hyaluronan lyase underlying processive hyaluronan translocation. Joshi HV, Jedrzejas MJ, de Groot BL. Proteins 76 30-46 (2009)
  22. Histochemical and biometric study of the gastrointestinal system of Hyla orientalis (Bedriaga, 1890) (Anura, Hylidae). Akat E, Arıkan H, Göçmen B. Eur J Histochem 58 2452 (2014)
  23. Substrate specificity of Chondroitinase ABC I based on analyses of biochemical reactions and crystal structures in complex with disaccharides. Takashima M, Watanabe I, Miyanaga A, Eguchi T. Glycobiology 31 1571-1581 (2021)
  24. Hyaluronate - parathyroid hormone peptide conjugate for transdermal treatment of osteoporosis. Cho M, Han S, Kim H, Kim KS, Hahn SK. J Biomater Sci Polym Ed 29 793-804 (2018)
  25. Structural insights into the mechanism of pH-selective substrate specificity of the polysaccharide lyase Smlt1473. Pandey S, Mahanta P, Berger BW, Acharya R. J Biol Chem 297 101014 (2021)
  26. The prebiotic and anti-fatigue effects of hyaluronan. Huang G, Su L, Zhang N, Han R, Leong WK, Li X, Ren X, Hsiao WLW. Front Nutr 9 977556 (2022)
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  28. A Safe-by-Design Approach for the Synthesis of a Novel Cross-Linked Hyaluronic Acid with Improved Biological and Physical Properties. Sciabica S, Barbari R, Fontana R, Tafuro G, Semenzato A, Traini D, Silva DM, Reis LGD, Canilli L, Terno M, Marconi P, Baldisserotto A, Vertuani S, Manfredini S. Pharmaceuticals (Basel) 16 431 (2023)
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Related citations provided by authors (1)

  1. Structural Basis of Hyaluronan Degradation by Streptococcus pneumoniae Hyaluronate Lyase. Li S, Kelly SJ, Lamani E, Ferraroni M, Jedrzejas MJ EMBO J. 19 1228-1240 (2000)

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