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Mechanism of hyaluronan degradation by Streptococcus pneumoniae hyaluronate lyase. Structures of complexes with the substrate.

Jedrzejas MJ, Mello LV, de Groot BL, Li S
J Biol Chem 277 28287-97 (2002)
Cited: 69 times
EuropePMC logo PMID: 11991948

Abstract

Hyaluronate lyase enzymes degrade hyaluronan, the main polysaccharide component of the host connective tissues, predominantly into unsaturated disaccharide units, thereby destroying the normal connective tissue structure and exposing the tissue cells to various endo- and exogenous factors, including bacterial toxins. The crystal structures of Streptococcus pneumoniae hyaluronate lyase with tetra- and hexasaccharide hyaluronan substrates bound in the active site were determined at 1.52- and 2.0-A resolution, respectively. Hexasaccharide is the longest substrate segment that binds entirely within the active site of these enzymes. The enzyme residues responsible for substrate binding, positioning, catalysis, and product release were thereby identified and their specific roles characterized. The involvement of three residues in catalysis, Asn(349), His(399), and Tyr(408), is confirmed, and the details of proton acceptance and donation within the catalytic machinery are described. The mechanism of processivity of the enzyme is analyzed. The flexibility (allosteric) behavior of the enzyme may be understood in terms of the results of flexibility analysis of this protein, which identified two modes of motion that are also proposed to be involved in the hyaluronan degradation process. The first motion describes an opening and closing of the catalytic cleft located between the alpha- and beta-domains. The second motion demonstrates the mobility of a binding cleft, which may facilitate the binding of the negatively charged hyaluronan to the enzyme.

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  1. Hyaluronidases: their genomics, structures, and mechanisms of action. Stern R, Jedrzejas MJ. Chem Rev 106 818-839 (2006)
  2. Fatty acid biosynthesis revisited: structure elucidation and metabolic engineering. Beld J, Lee DJ, Burkart MD. Mol Biosyst 11 38-59 (2015)
  3. 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. CHARMM-GUI Drude prepper for molecular dynamics simulation using the classical Drude polarizable force field. Kognole AA, Lee J, Park SJ, Jo S, Chatterjee P, Lemkul JA, Huang J, MacKerell AD, Im W. J Comput Chem 43 359-375 (2022)
  2. The structure of the first representative of Pfam family PF06475 reveals a new fold with possible involvement in glycolipid metabolism. Bakolitsa C, Kumar A, McMullan D, Krishna SS, Miller MD, Carlton D, Najmanovich R, Abdubek P, Astakhova T, Chiu HJ, Clayton T, Deller MC, Duan L, Elias Y, Feuerhelm J, Grant JC, Grzechnik SK, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Marciano D, Morse AT, Nigoghossian E, Okach L, Oommachen S, Paulsen J, Reyes R, Rife CL, Trout CV, van den Bedem H, Weekes D, White A, Xu Q, Hodgson KO, Wooley J, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA. Acta Crystallogr Sect F Struct Biol Cryst Commun 66 1211-1217 (2010)
  3. Modeling Protein-Glycosaminoglycan Complexes: Does the Size Matter? Marcisz M, Zacharias M, Samsonov SA. J Chem Inf Model 61 4475-4485 (2021)
  4. Solution structure of 4'-phosphopantetheine - GmACP3 from Geobacter metallireducens: a specialized acyl carrier protein with atypical structural features and a putative role in lipopolysaccharide biosynthesis. Ramelot TA, Smola MJ, Lee HW, Ciccosanti C, Hamilton K, Acton TB, Xiao R, Everett JK, Prestegard JH, Montelione GT, Kennedy MA. Biochemistry 50 1442-1453 (2011)
  5. Functional divergence of a bacterial enzyme promotes healthy or acneic skin. Hajam IA, Katiki M, McNally R, Lázaro-Díez M, Kolar S, Chatterjee A, Gonzalez C, Paulchakrabarti M, Choudhury B, Caldera JR, Desmond T, Tsai CM, Du X, Li H, Murali R, Liu GY. Nat Commun 14 8061 (2023)


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  1. The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Kadioglu A, Weiser JN, Paton JC, Andrew PW. Nat Rev Microbiol 6 288-301 (2008)
  2. The magic glue hyaluronan and its eraser hyaluronidase: a biological overview. Girish KS, Kemparaju K. Life Sci 80 1921-1943 (2007)
  3. Structural view of glycosaminoglycan-protein interactions. Imberty A, Lortat-Jacob H, Pérez S. Carbohydr Res 342 430-439 (2007)
  4. Bacteriophage polysaccharide depolymerases and biomedical applications. Yan J, Mao J, Xie J. BioDrugs 28 265-274 (2014)
  5. Breakdown of oligosaccharides by the process of elimination. Yip VL, Withers SG. Curr Opin Chem Biol 10 147-155 (2006)
  6. Diversity of Three-Dimensional Structures and Catalytic Mechanisms of Alginate Lyases. Xu F, Wang P, Zhang YZ, Chen XL. Appl Environ Microbiol 84 e02040-17 (2018)
  7. Glycan-metabolizing enzymes in microbe-host interactions: the Streptococcus pneumoniae paradigm. Hobbs JK, Pluvinage B, Boraston AB. FEBS Lett 592 3865-3897 (2018)
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  1. L-Ascorbic acid 6-hexadecanoate, a potent hyaluronidase inhibitor. X-ray structure and molecular modeling of enzyme-inhibitor complexes. Botzki A, Rigden DJ, Braun S, Nukui M, Salmen S, Hoechstetter J, Bernhardt G, Dove S, Jedrzejas MJ, Buschauer A. J Biol Chem 279 45990-45997 (2004)
  2. High-resolution crystal structure of Arthrobacter aurescens chondroitin AC lyase: an enzyme-substrate complex defines the catalytic mechanism. Lunin VV, Li Y, Linhardt RJ, Miyazono H, Kyogashima M, Kaneko T, Bell AW, Cygler M. J Mol Biol 337 367-386 (2004)
  3. A structural basis for depolymerization of alginate by polysaccharide lyase family-7. Yamasaki M, Ogura K, Hashimoto W, Mikami B, Murata K. J Mol Biol 352 11-21 (2005)
  4. The link module from ovulation- and inflammation-associated protein TSG-6 changes conformation on hyaluronan binding. Blundell CD, Mahoney DJ, Almond A, DeAngelis PL, Kahmann JD, Teriete P, Pickford AR, Campbell ID, Day AJ. J Biol Chem 278 49261-49270 (2003)
  5. Four Arabidopsis berberine bridge enzyme-like proteins are specific oxidases that inactivate the elicitor-active oligogalacturonides. Benedetti M, Verrascina I, Pontiggia D, Locci F, Mattei B, De Lorenzo G, Cervone F. Plant J 94 260-273 (2018)
  6. 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)
  7. Techniques, tools and best practices for ligand electron-density analysis and results from their application to deposited crystal structures. Pozharski E, Weichenberger CX, Rupp B. Acta Crystallogr D Biol Crystallogr 69 150-167 (2013)
  8. Structure of a PL17 family alginate lyase demonstrates functional similarities among exotype depolymerases. Park D, Jagtap S, Nair SK. J Biol Chem 289 8645-8655 (2014)
  9. Reductive evolution in Streptococcus agalactiae and the emergence of a host adapted lineage. Rosinski-Chupin I, Sauvage E, Mairey B, Mangenot S, Ma L, Da Cunha V, Rusniok C, Bouchier C, Barbe V, Glaser P. BMC Genomics 14 252 (2013)
  10. Substrate recognition by family 7 alginate lyase from Sphingomonas sp. A1. Ogura K, Yamasaki M, Mikami B, Hashimoto W, Murata K. J Mol Biol 380 373-385 (2008)
  11. Biochemical characterization of the chondroitinase ABC I active site. Prabhakar V, Raman R, Capila I, Bosques CJ, Pojasek K, Sasisekharan R. Biochem J 390 395-405 (2005)
  12. Structures of vertebrate hyaluronidases and their unique enzymatic mechanism of hydrolysis. Jedrzejas MJ, Stern R. Proteins 61 227-238 (2005)
  13. Origin and diversity of alginate lyases of families PL-5 and -7 in Sphingomonas sp. strain A1. Miyake O, Ochiai A, Hashimoto W, Murata K. J Bacteriol 186 2891-2896 (2004)
  14. 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 50596-50606 (2003)
  15. Crystal structure of Bacillus sp. GL1 xanthan lyase, which acts on the side chains of xanthan. Hashimoto W, Nankai H, Mikami B, Murata K. J Biol Chem 278 7663-7673 (2003)
  16. The function of hydrophobic residues in the catalytic cleft of Streptococcus pneumoniae hyaluronate lyase. Kinetic characterization of mutant enzyme forms. Nukui M, Taylor KB, McPherson DT, Shigenaga MK, Jedrzejas MJ. J Biol Chem 278 3079-3088 (2003)
  17. A novel hyaluronidase produced by Bacillus sp. A50. Guo X, Shi Y, Sheng J, Wang F. PLoS One 9 e94156 (2014)
  18. Crystal structure of unsaturated glucuronyl hydrolase complexed with substrate: molecular insights into its catalytic reaction mechanism. Itoh T, Hashimoto W, Mikami B, Murata K. J Biol Chem 281 29807-29816 (2006)
  19. Pneumococcal protein PavA is important for nasopharyngeal carriage and development of sepsis. Kadioglu A, Brewin H, Härtel T, Brittan JL, Klein M, Hammerschmidt S, Jenkinson HF. Mol Oral Microbiol 25 50-60 (2010)
  20. Pneumococcal surface protein A contributes to secondary Streptococcus pneumoniae infection after influenza virus infection. King QO, Lei B, Harmsen AG. J Infect Dis 200 537-545 (2009)
  21. Structural analysis of Escherichia coli OpgG, a protein required for the biosynthesis of osmoregulated periplasmic glucans. Hanoulle X, Rollet E, Clantin B, Landrieu I, Odberg-Ferragut C, Lippens G, Bohin JP, Villeret V. J Mol Biol 342 195-205 (2004)
  22. 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)
  23. Novel 6-O-acylated vitamin C derivatives as hyaluronidase inhibitors with selectivity for bacterial lyases. Spickenreither M, Braun S, Bernhardt G, Dove S, Buschauer A. Bioorg Med Chem Lett 16 5313-5316 (2006)
  24. Polysaccharide binding sites in hyaluronate lyase--crystal structures of native phage-encoded hyaluronate lyase and its complexes with ascorbic acid and lactose. Mishra P, Prem Kumar R, Ethayathulla AS, Singh N, Sharma S, Perbandt M, Betzel C, Kaur P, Srinivasan A, Bhakuni V, Singh TP. FEBS J 276 3392-3402 (2009)
  25. Crystal structure of Bacillus sp. GL1 xanthan lyase complexed with a substrate: insights into the enzyme reaction mechanism. Maruyama Y, Hashimoto W, Mikami B, Murata K. J Mol Biol 350 974-986 (2005)
  26. Cloning of the Trichoderma reesei cDNA encoding a glucuronan lyase belonging to a novel polysaccharide lyase family. Konno N, Igarashi K, Habu N, Samejima M, Isogai A. Appl Environ Microbiol 75 101-107 (2009)
  27. Insights into molecular plasticity of choline binding proteins (pneumococcal surface proteins) by SAXS. Buey RM, Monterroso B, Menéndez M, Diakun G, Chacón P, Hermoso JA, Díaz JF. J Mol Biol 365 411-424 (2007)
  28. 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)
  29. Serotype Distribution, Antimicrobial Susceptibility, Multilocus Sequencing Type and Virulence of Invasive Streptococcus pneumoniae in China: A Six-Year Multicenter Study. Zhou M, Wang Z, Zhang L, Kudinha T, An H, Qian C, Jiang B, Wang Y, Xu Y, Liu Z, Zhang H, Zhang J. Front Microbiol 12 798750 (2021)
  30. 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)
  31. A polysaccharide lyase from Stenotrophomonas maltophilia with a unique, pH-regulated substrate specificity. MacDonald LC, Berger BW. J Biol Chem 289 312-325 (2014)
  32. Hyaluronate lyase of a deep-sea Bacillus niacini. Kurata A, Matsumoto M, Kobayashi T, Deguchi S, Kishimoto N. Mar Biotechnol (NY) 17 277-284 (2015)
  33. 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)
  34. Constructing 3-Dimensional Atomic-Resolution Models of Nonsulfated Glycosaminoglycans with Arbitrary Lengths Using Conformations from Molecular Dynamics. Whitmore EK, Martin D, Guvench O. Int J Mol Sci 21 E7699 (2020)
  35. Domain motions of hyaluronan lyase underlying processive hyaluronan translocation. Joshi HV, Jedrzejas MJ, de Groot BL. Proteins 76 30-46 (2009)
  36. Evidence for inhibitory interaction of hyaluronan-binding protein 1 (HABP1/p32/gC1qR) with Streptococcus pneumoniae hyaluronidase. Yadav G, Prasad RL, Jha BK, Rai V, Bhakuni V, Datta K. J Biol Chem 284 3897-3905 (2009)
  37. Genome-based identification of a carbohydrate binding module in Streptococcus pneumoniae hyaluronate lyase. Rigden DJ, Jedrzejas MJ. Proteins 52 203-211 (2003)
  38. 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)
  39. Preparation of the methyl ester of hyaluronan and its enzymatic degradation. Hirano K, Sakai S, Ishikawa T, Avci FY, Linhardt RJ, Toida T. Carbohydr Res 340 2297-2304 (2005)
  40. 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)
  41. Conformational analysis of the Streptococcus pneumoniae hyaluronate lyase and characterization of its hyaluronan-specific carbohydrate-binding module. Suits MDL, Pluvinage B, Law A, Liu Y, Palma AS, Chai W, Feizi T, Boraston AB. J Biol Chem 289 27264-27277 (2014)
  42. Engineering broad-spectrum digestion of polyuronides from an exolytic polysaccharide lyase. MacDonald LC, Weiler EB, Berger BW. Biotechnol Biofuels 9 43 (2016)
  43. Processive cleavage of substrate at individual proteolytic active sites of the Lon protease complex. Li S, Hsieh KY, Kuo CI, Su SC, Huang KF, Zhang K, Chang CI. Sci Adv 7 eabj9537 (2021)
  44. Histone Tail Sequences Balance Their Role in Genetic Regulation and the Need To Protect DNA against Destruction in Nucleosome Core Particles Containing Abasic Sites. Yang K, Greenberg MM. Chembiochem 20 78-82 (2019)
  45. Substrate recognition by unsaturated glucuronyl hydrolase from Bacillus sp. GL1. Itoh T, Hashimoto W, Mikami B, Murata K. Biochem Biophys Res Commun 344 253-262 (2006)
  46. Super-channel in bacteria: structural and functional aspects of a novel biosystem for the import and depolymerization of macromolecules. Hashimoto W, Yamasaki M, Itoh T, Momma K, Mikami B, Murata K. J Biosci Bioeng 98 399-413 (2004)
  47. Letter Crystal structure of exo-rhamnogalacturonan lyase from Penicillium chrysogenum as a member of polysaccharide lyase family 26. Kunishige Y, Iwai M, Nakazawa M, Ueda M, Tada T, Nishimura S, Sakamoto T. FEBS Lett 592 1378-1388 (2018)
  48. Sequence diversity and ligand-induced structural rearrangements of viper hyaluronidase. Bharathi AC, Yadav PK, Syed Ibrahim B. Mol Biosyst 12 1128-1138 (2016)
  49. Cloning, Expression, and Characterization of a New Glycosaminoglycan Lyase from Microbacterium sp. H14. Sun J, Han X, Song G, Gong Q, Yu W. Mar Drugs 17 E681 (2019)
  50. 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)
  51. Reactivity of the Major Product of C5'-Oxidative DNA Damage in Nucleosome Core Particles. Rana A, Yang K, Greenberg MM. Chembiochem 20 672-676 (2019)
  52. Functional role of R462 in the degradation of hyaluronan catalyzed by hyaluronate lyase from Streptococcus pneumoniae. Li F, Xu D. J Mol Model 21 196 (2015)
  53. 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)


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