Streptococcal phosphotransferase system imports unsaturated hyaluronan disaccharide derived from host extracellular matrices

English version

Autoři: Sayoko Oiki ^aff001; Yusuke Nakamichi ^aff001; Yukie Maruyama ^aff002; Bunzo Mikami ^aff003; Kousaku Murata ^aff002; Wataru Hashimoto ^aff001
Působiště autorů: Laboratory of Basic and Applied Molecular Biotechnology, Division of Food Science and Biotechnology, Graduate School of Agriculture, Kyoto University, Uji, Kyoto, Japan ^aff001; Laboratory of Food Microbiology, Department of Life Science, Faculty of Science and Engineering, Setsunan University, Neyagawa, Osaka, Japan ^aff002; Laboratory of Applied Structural Biology, Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Uji, Kyoto, Japan ^aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0224753

Souhrn

Certain bacterial species target the polysaccharide glycosaminoglycans (GAGs) of animal extracellular matrices for colonization and/or infection. GAGs such as hyaluronan and chondroitin sulfate consist of repeating disaccharide units of uronate and amino sugar residues, and are depolymerized to unsaturated disaccharides by bacterial extracellular or cell-surface polysaccharide lyase. The disaccharides are degraded and metabolized by cytoplasmic enzymes such as unsaturated glucuronyl hydrolase, isomerase, and reductase. The genes encoding these enzymes are assembled to form a GAG genetic cluster. Here, we demonstrate the Streptococcus agalactiae phosphotransferase system (PTS) for import of unsaturated hyaluronan disaccharide. S. agalactiae NEM316 was found to depolymerize and assimilate hyaluronan, whereas its mutant with a disruption in the PTS genes included in the GAG cluster was unable to grow on hyaluronan, while retaining the ability to depolymerize hyaluronan. Using toluene-treated wild-type cells, the PTS activity for import of unsaturated hyaluronan disaccharide was significantly higher than that observed in the absence of the substrate. In contrast, the PTS mutant was unable to import unsaturated hyaluronan disaccharide, indicating that the corresponding PTS is the only importer of fragmented hyaluronan, which is suitable for PTS to phosphorylate the substrate at the C-6 position. This is distinct from Streptobacillus moniliformis ATP-binding cassette transporter for import of sulfated and non-sulfated fragmented GAGs without substrate modification. The three-dimensional structure of streptococcal EIIA, one of the PTS components, was found to contain a Rossman-fold motif by X-ray crystallization. Docking of EIIA with another component EIIB by modeling provided structural insights into the phosphate transfer mechanism. This study is the first to identify the substrate (unsaturated hyaluronan disaccharide) recognized and imported by the streptococcal PTS. The PTS and ABC transporter for import of GAGs shed light on bacterial clever colonization/infection system targeting various animal polysaccharides.

Klíčová slova:

Crystal structure – Disaccharides – Lyases – Mannose – Polymerase chain reaction – Streptococcus agalactiae – Sulfates – Chondroitin

Zdroje

1. Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci. 2010; 123: 4195–4200. doi: 10.1242/jcs.023820 21123617

2. Kamhi E, Joo EJ, Dordick JS, Linhardt RJ. Glycosaminoglycans in infectious disease. Biol Rev. 2013; 88: 928–943. doi: 10.1111/brv.12034 23551941

3. Karamanos NK, Piperigkou Z, Theocharis AD, Watanabe H, Franchi M, Baud S, et al. Proteoglycan chemical diversity drives multifunctional cell regulation and therapeutics. Chem Rev. 2018; 118: 9152–9232. doi: 10.1021/acs.chemrev.8b00354 30204432

4. Scott JE. Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB J. 1992; 6: 2639–2645. 1612287

5. Prydz K, Dalen KT. Synthesis and sorting of proteoglycans. J Cell Sci. 2000; 113: 193–205. 10633071

6. Sawitzky D. Protein-glycosaminoglycan interactions: infectiological aspects. Med Microbiol Immun. 1996; 184: 155–161.

7. Ernst S, Langer R, Cooney CL, Sasisekharan R. Enzymatic degradation of glycosaminoglycans. Crit Rev Biochem Mol Biol. 1995; 30: 387–444. doi: 10.3109/10409239509083490 8575190

8. Jedrzejas MJ. Pneumococcal virulence factors: structure and function. Microbiol Mol Biol Rev. 2001; 65: 187–207. doi: 10.1128/MMBR.65.2.187-207.2001 11381099

9. Stern R, Jedrzejas MJ. Hyaluronidases: their genomics, structures, and mechanisms of action. Chem. Rev. 2006; 106: 818–839. doi: 10.1021/cr050247k 16522010

10. Jedrzejas M. Unveiling molecular mechanisms of bacterial surface proteins: Streptococcus pneumoniae as a model organism for structural studies. Cell Mol Life Sci. 2007; 64: 2799–2822. doi: 10.1007/s00018-007-7125-8 17687514

11. Li S, Jedrzejas MJ. Hyaluronan binding and degradation by Streptococcus agalactiae hyaluronate lyase. J Biol Chem. 2001; 276: 41407–41416. doi: 10.1074/jbc.M106634200 11527972

12. Ibberson CB, Jones CL, Singh S, Wise MC, Hart ME, Zurawski DV, et al. Staphylococcus aureus hyaluronidase is a CodY-regulated virulence factor. Infect Immun. 2014; 82: 1710–1714. doi: 10.1128/IAI.00073-14

13. Hashimoto W, Kobayashi E, Nankai H, Sato N, Miya T, Kawai S, et al. Unsaturated glucuronyl hydrolase of Bacillus sp. GL1: novel enzyme prerequisite for metabolism of unsaturated oligosaccharides produced by polysaccharide lyases. Arch Biochem Biophys. 1999; 368: 367–374. doi: 10.1006/abbi.1999.1305

14. Itoh T, Hashimoto W, Mikami B, Murata K. Crystal structure of unsaturated glucuronyl hydrolase complexed with substrate molecular insights into its catalytic reaction mechanism. J Biol Chem. 2006; 281: 29807–29816. doi: 10.1074/jbc.M604975200 16893885

15. Nakamichi Y, Maruyama Y, Mikami B, Hashimoto W, Murata K. Structural determinants in streptococcal unsaturated glucuronyl hydrolase for recognition of glycosaminoglycan sulfate groups. J Biol Chem. 2011; 286: 6262–6271. doi: 10.1074/jbc.M110.182618 21147778

16. Maruyama Y, Oiki S, Takase R, Mikami B, Murata K, Hashimoto W. Metabolic fate of unsaturated glucuronic/iduronic acids from glycosaminoglycans: molecular identification and structure determination of streptococcal isomerase and dehydrogenase. J Biol Chem. 2015; 290: 6281–6292. doi: 10.1074/jbc.M114.604546 25605731

17. Kuivanen J, Sugai-Guerios MH, Arvas M, Richard P. A novel pathway for fungal D-glucuronate catabolism contains an L-idonate forming 2-keto-L-gulonate reductase. Sci Rep. 2016; 6: 26329 doi: 10.1038/srep26329 27189775

18. Oiki S, Mikami B, Maruyama Y, Murata K, Hashimoto W. A bacterial ABC transporter enables import of mammalian host glycosaminoglycans. Sci Rep. 2017; 7: 1069. doi: 10.1038/s41598-017-00917-y 28432302

19. Patterson MJ. Streptococcus. Chapter 13 In: Baron S., editor. Medical Microbiology. 4 th edition. Galveston (TX): University of Texas Medical Branch at Galveston. 1996.

20. Deutscher J, Ake FMD, Derkaoui M, Zebre AC, Cao TN, Bouraoui H, et al. The bacterial phosphoenolpyruvate:carbohydrate phosphotransferase system: regulation by protein phosphorylation and phosphorylation-dependent protein-protein interactions. Microbiol Mol Biol Rev. 2014; 78: 231–256. doi: 10.1128/MMBR.00001-14 24847021

21. Postma P, Lengeler J. Phosphoenolpyruvate:carbohydrate phosphotransferase system of bacteria. Microbiol Rev. 1985; 49: 232–269. 3900671

22. Habuchi O. Diversity and functions of glycosaminoglycan sulfotransferases. Biochim Biophys Acta Gen Subj. 2000; 1474: 115–127.

23. Simoni RD, Levinthal M, Kundig FD, Kundig W, Anderson B, Hartman PE, et al. Genetic evidence for the role of a bacterial phosphotransferase system in sugar transport. Proc Natl Acad Sci USA. 1967; 58: 1963–1970. doi: 10.1073/pnas.58.5.1963 4866983

24. Barabote RD, Saier MH. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev. 2005; 69: 608–634. doi: 10.1128/MMBR.69.4.608-634.2005 16339738

25. Maruyama Y, Nakamichi Y, Itoh T, Mikami B, Hashimoto W, Murata K. Substrate specificity of streptococcal unsaturated glucuronyl hydrolases for sulfated glycosaminoglycan. J Biol Chem. 2009; 284: 18059–18069. doi: 10.1074/jbc.M109.005660 19416976

26. Marion C, Stewart JM, Tazi MF, Burnaugh AM, Linke CM, Woodiga SA, et al. Streptococcus pneumoniae can utilize multiple sources of hyaluronic acid for growth. Infect Immun. 2012; 80: 1390–1398. doi: 10.1128/IAI.05756-11 22311922

27. Terleckyj B, Willett N, Shockman G. Growth of several cariogenic strains of oral streptococci in a chemically defined medium. Infect Immun. 1975; 11: 649–655. 1091546

28. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA. 1977; 74: 5463–5467. doi: 10.1073/pnas.74.12.5463 271968

29. Ricci ML, Manganelli R, Berneri C, Orefici G, Pozzi G. Electrotransformation of Streptococcus agalactiae with plasmid DNA. FEMS Microbiol Lett. 1994; 119: 47–52. doi: 10.1111/j.1574-6968.1994.tb06865.x 8039669

30. Kornberg HL, Reeves RE. Inducible phosphoenolpyruvate-dependent hexose phosphotransferase activities in Escherichia coli. Biochem J. 1972; 128: 1339–1344. doi: 10.1042/bj1281339 4345358

31. Moye ZD, Burne RA, Zeng L. Uptake and metabolism of N-acetylglucosamine and glucosamine by Streptococcus mutans. Appl Environ Microbiol. 2014; 80: 5053–5067. doi: 10.1128/AEM.00820-14 24928869

32. Smith PK, Krohn RI, Hermanson G, Mallia A, Gartner F, Provenzano M, et al. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985; 150: 76–85. doi: 10.1016/0003-2697(85)90442-7 3843705

33. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Meth Enzymol. 1997; 276: 307–326.

34. Vagin A, Teplyakov A. MOLREP: an automated program for molecular replacement. J App Crystallog. 1997; 30: 1022–1025.

35. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D Cryst Struct Commun. 2010; 66: 213–221.

36. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr Sect D Cryst Struct Commun. 2010; 66: 486–501.

37. DeLano WL. The PyMOL molecular graphics system. 2002.

38. Baker JR, Hao Y, Morrison K, Averett WF, Pritchard DG. Specificity of the hyaluronate lyase of group-B streptococcus toward unsulphated regions of chondroitin sulphate. Biochem J. 1997; 327: 65–71. doi: 10.1042/bj3270065 9355736

39. Foot M, Mulholland M. Classification of chondroitin sulfate A, chondroitin sulfate C, glucosamine hydrochloride and glucosamine 6 sulfate using chemometric techniques. J Pharm Biomed Anal. 2005; 38: 397–407. doi: 10.1016/j.jpba.2005.01.026 15925239

40. Mathews MB, Inouye M. The determination of chondroitin sulfate C-type polysaccharides in mixture with other acid mucopolysaccharides. Biochim Biophys Acta. 1961; 53: 509–513. doi: 10.1016/0006-3002(61)90209-8 14471105

41. Wang Z, Guo C, Xu Y, Liu G, Lu C, Liu Y. Two novel functions of hyaluronidase from Streptococcus agalactiae are enhanced intracellular survival and inhibition of proinflammatory cytokine expression. Infect Immun. 2014; 82: 2615–2625. doi: 10.1128/IAI.00022-14 24711564

42. Shafeeq S, Kloosterman TG, Kuipers OP. CelR-mediated activation of the cellobiose-utilization gene cluster in Streptococcus pneumoniae. Microbiology. 2011; 157: 2854–2861. doi: 10.1099/mic.0.051359-0 21778207

43. Krissinel E, Henrick K. Protein interfaces, surfaces and assemblies service PISA at European Bioinformatics Institute. J Mol Biol. 2007; 372: 774–797. doi: 10.1016/j.jmb.2007.05.022 17681537

44. Williams DC, Cai M, Suh J, Peterkofsky A, Clore GM. Solution NMR structure of the 48-kDa IIAMannose-HPr complex of the Escherichia coli mannose phosphotransferase system. J Biol Chem. 2005; 280: 20775–20784. doi: 10.1074/jbc.M501986200 15788390

45. Hu J, Hu K, Williams DC, Komlosh ME, Cai M, Clore GM. Solution NMR structures of productive and non-productive complexes between the A and B domains of the cytoplasmic subunit of the mannose transporter of the Escherichia coli phosphotransferase system. J Biol Chem. 2008; 283: 11024–11037. doi: 10.1074/jbc.M800312200 18270202

46. Nunn RS. et al. Structure of the IIA domain of the mannose transporter from Escherichia coli at 1.7 Å resolution. J Mol Biol. 1996; 259: 502–511. doi: 10.1006/jmbi.1996.0335 8676384

47. Saier MH Jr. Bacterial phosphoenolpyruvate:sugar phosphotransferase systems: structural, functional, and evolutionary interrelationships. Bacteriol Rev. 1977; 41: 856–871. 339892

48. Saier M, Hvorup R, Barabote R. Evolution of the bacterial phosphotransferase system: from carriers and enzymes to group translocators. Biochem Soc Trans. 2005; 33: 220–224. doi: 10.1042/BST0330220 15667312

49. Holm L, Rosenstrom P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 2010; 38: W545–W549. doi: 10.1093/nar/gkq366 20457744

50. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018; 46: W296–W303. doi: 10.1093/nar/gky427 29788355

51. Oiki S, Kamochi R, Mikami B, Murata K, Hashimoto W. Alternative substrate-bound conformation of bacterial solute-binding protein involved in the import of mammalian host glycosaminoglycans. Sci Rep. 2017; 7: 17005. doi: 10.1038/s41598-017-16801-8 29208901

52. Davidson AL, Chen J. ATP-binding cassette transporters in bacteria. Annu Rev Biochem. 2004; 73: 241–268. doi: 10.1146/annurev.biochem.73.011303.073626 15189142

53. Edelstam G, Lundkvist OE, Wells AF, Laurent TC. Localization of hyaluronan in regions of the human female reproductive tract. J Histochem Cytochem. 1991; 39: 1131–1135. doi: 10.1177/39.8.1856461 1856461

54. Lev-Sagie A, Nyirjesy P, Tarangelo N, Bongiovanni AM, Bayer C, Linhares IM, et al. Hyaluronan in vaginal secretions: association with recurrent vulvovaginal candidiasis. Am J Obstet Gynecol. 2009; 201: 206. e201–205.

55. Franz CM, Huch M, Abriouel H, Holzapfel W, Galvez A. Enterococci as probiotics and their implidations in food safety. Int J Food Microbiol. 2011; 151: 125–140. doi: 10.1016/j.ijfoodmicro.2011.08.014 21962867

56. Kawai K, Kamochi R, Oiki S, Murata K, Hashimoto W. Probiotics in human gut microbiota can degrade host glycosaminoglycans. Sci Rep. 2018; 8: 10674. doi: 10.1038/s41598-018-28886-w 30006634

Streptococcal phosphotransferase system imports unsaturated hyaluronan disaccharide derived from host extracellular matrices

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií