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Structures of Streptococcus pneumoniae hyaluronate lyase in complex with chondroitin and chondroitin sulfate disaccharides. Insights into specificity and mechanism of action.

Rigden DJ, Jedrzejas MJ
J Biol Chem 278 50596-606 (2003)
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Cited: 29 times
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Abstract

Streptococcus pneumoniae hyaluronate lyase is a surface enzyme of this Gram-positive bacterium. The enzyme degrades hyaluronan and chondroitin/chondroitin sulfates by cleaving the beta1,4-glycosidic linkage between the glycan units of these polymeric substrates. This degradation helps spreading of this bacterial organism throughout the host tissues and facilitates the disease process caused by pneumococci. The mechanism of this degradative process is based on beta-elimination, is termed proton acceptance and donation, and involves selected residues of a well defined catalytic site of the enzyme. The degradation of hyaluronan alone is thought to proceed through a processive mode of action. The structures of complexes between the enzyme and chondroitin as well as chondroitin sulfate disaccharides allowed for the first detailed insights into these interactions and the mechanism of action on chondroitins. This degradation of chondroitin/chondroitin sulfates is nonprocessive and is selective for the chondroitin sulfates only with certain sulfation patterns. Chondroitin sulfation at the 4-position on the nonreducing site of the linkage to be cleaved or 2-sulfation prevent degradation due to steric clashes with the enzyme. Evolutionary studies suggest that hyaluronate lyases evolved from chondroitin lyases and still retained chondroitin/chondroitin sulfate degradation abilities while being specialized in the degradation of hyaluronan. The more efficient processive degradation mechanism has come to be preferred for the unsulfated substrate hyaluronan.

Articles - 1ojm mentioned but not cited (2)

  1. Crystal structure of exotype alginate lyase Atu3025 from Agrobacterium tumefaciens. Ochiai A, Yamasaki M, Mikami B, Hashimoto W, Murata K. J Biol Chem 285 24519-24528 (2010)
  2. Crystallization and X-ray diffraction analysis of chondroitin lyase from baculovirus: envelope protein ODV-E66. Kawaguchi Y, Sugiura N, Onishi M, Kimata K, Kimura M, Kakuta Y. Acta Crystallogr Sect F Struct Biol Cryst Commun 68 190-192 (2012)


Reviews citing this publication (9)

  1. Hyaluronidases: their genomics, structures, and mechanisms of action. Stern R, Jedrzejas MJ. Chem Rev 106 818-839 (2006)
  2. The many ways to cleave hyaluronan. Stern R, Kogan G, Jedrzejas MJ, Soltés L. Biotechnol Adv 25 537-557 (2007)
  3. Glycosaminoglycans in infectious disease. Kamhi E, Joo EJ, Dordick JS, Linhardt RJ. Biol Rev Camb Philos Soc 88 928-943 (2013)
  4. Structural view of glycosaminoglycan-protein interactions. Imberty A, Lortat-Jacob H, Pérez S. Carbohydr Res 342 430-439 (2007)
  5. Pneumococcal surface proteins: when the whole is greater than the sum of its parts. Pérez-Dorado I, Galan-Bartual S, Hermoso JA. Mol Oral Microbiol 27 221-245 (2012)
  6. CS lyases: structure, activity, and applications in analysis and the treatment of diseases. Linhardt RJ, Avci FY, Toida T, Kim YS, Cygler M. Adv Pharmacol 53 187-215 (2006)
  7. Glycan-metabolizing enzymes in microbe-host interactions: the Streptococcus pneumoniae paradigm. Hobbs JK, Pluvinage B, Boraston AB. FEBS Lett 592 3865-3897 (2018)
  8. Hyaluronic Acid: Known for Almost a Century, but Still in Vogue. Lierova A, Kasparova J, Filipova A, Cizkova J, Pekarova L, Korecka L, Mannova N, Bilkova Z, Sinkorova Z. Pharmaceutics 14 838 (2022)
  9. Advances in understanding the pathogenesis of pneumococcal otitis media. Tonnaer EL, Graamans K, Sanders EA, Curfs JH. Pediatr Infect Dis J 25 546-552 (2006)

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  1. A Novel Polyester Hydrolase From the Marine Bacterium Pseudomonas aestusnigri - Structural and Functional Insights. Bollinger A, Thies S, Knieps-Grünhagen E, Gertzen C, Kobus S, Höppner A, Ferrer M, Gohlke H, Smits SHJ, Jaeger KE. Front Microbiol 11 114 (2020)
  2. Docking server for the identification of heparin binding sites on proteins. Mottarella SE, Beglov D, Beglova N, Nugent MA, Kozakov D, Vajda S. J Chem Inf Model 54 2068-2078 (2014)
  3. Structures of vertebrate hyaluronidases and their unique enzymatic mechanism of hydrolysis. Jedrzejas MJ, Stern R. Proteins 61 227-238 (2005)
  4. The K5 lyase KflA combines a viral tail spike structure with a bacterial polysaccharide lyase mechanism. Thompson JE, Pourhossein M, Waterhouse A, Hudson T, Goldrick M, Derrick JP, Roberts IS. J Biol Chem 285 23963-23969 (2010)
  5. A 3D-structural model of unsulfated chondroitin from high-field NMR: 4-sulfation has little effect on backbone conformation. Sattelle BM, Shakeri J, Roberts IS, Almond A. Carbohydr Res 345 291-302 (2010)
  6. Exploiting enzyme specificities in digestions of chondroitin sulfates A and C: production of well-defined hexasaccharides. Pomin VH, Park Y, Huang R, Heiss C, Sharp JS, Azadi P, Prestegard JH. Glycobiology 22 826-838 (2012)
  7. Computational analysis of interactions in structurally available protein-glycosaminoglycan complexes. Samsonov SA, Pisabarro MT. Glycobiology 26 850-861 (2016)
  8. A novel hyaluronidase produced by Bacillus sp. A50. Guo X, Shi Y, Sheng J, Wang F. PLoS One 9 e94156 (2014)
  9. Sulfation and cation effects on the conformational properties of the glycan backbone of chondroitin sulfate disaccharides. Faller CE, Guvench O. J Phys Chem B 119 6063-6073 (2015)
  10. Induced-fit motion of a lid loop involved in catalysis in alginate lyase A1-III. Mikami B, Ban M, Suzuki S, Yoon HJ, Miyake O, Yamasaki M, Ogura K, Maruyama Y, Hashimoto W, Murata K. Acta Crystallogr D Biol Crystallogr 68 1207-1216 (2012)
  11. 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)
  12. The crystal structure of novel chondroitin lyase ODV-E66, a baculovirus envelope protein. Kawaguchi Y, Sugiura N, Kimata K, Kimura M, Kakuta Y. FEBS Lett 587 3943-3948 (2013)
  13. Insight into the role of substrate-binding residues in conferring substrate specificity for the multifunctional polysaccharide lyase Smlt1473. MacDonald LC, Berger BW. J Biol Chem 289 18022-18032 (2014)
  14. Domain motions of hyaluronan lyase underlying processive hyaluronan translocation. Joshi HV, Jedrzejas MJ, de Groot BL. Proteins 76 30-46 (2009)
  15. The Influences of Sulphation, Salt Type, and Salt Concentration on the Structural Heterogeneity of Glycosaminoglycans. Samantray S, Olubiyi OO, Strodel B. Int J Mol Sci 22 11529 (2021)
  16. Active Expression of Human Hyaluronidase PH20 and Characterization of Its Hydrolysis Pattern. Pang B, He J, Zhang W, Huang H, Wang Y, Wang M, Du G, Kang Z. Front Bioeng Biotechnol 10 885888 (2022)
  17. Conformational Change in the Active Site of Streptococcal Unsaturated Glucuronyl Hydrolase Through Site-Directed Mutagenesis at Asp-115. Nakamichi Y, Oiki S, Mikami B, Murata K, Hashimoto W. Protein J 35 300-309 (2016)
  18. Streptococcal hyaluronate lyase reveals the presence of a structurally significant C-H⋅⋅⋅O hydrogen bond. Moore KB, Migues AN, Schaefer HF, Vergenz RA. Chemistry 20 990-998 (2014)


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 1228-40 (2000)

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