An essential serotype recognition pocket on phage P22 tailspike protein forces Salmonella enterica serovar Paratyphi A O-antigen fragments to bind as nonsolution conformers

Glycobiology

Volumn 23, Issue 4, 2013, Pages 486-494

  Andres, Dorothee ^a,e   Gohlke, Ulrich ^b   Broeker, Nina K ^a   Schulze, Stefan ^a   Rabsch, Wolfgang ^c   Heinemann, Udo ^b,d   Barbirz, Stefanie ^a   Seckler, Robert ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c ROBERT KOCH INSTITUTE   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e HARVARD UNIVERSITY   (United States)

Author keywords

bacterial O antigen; carbohydrate interaction; paratose; structural thermodynamics; tailspike protein

Indexed keywords

3,6 DIDEOXYHEXOSE; ABEQUOSE; BACTERIAL PROTEIN; BACTERIOPHAGE P22 TAILSPIKE PROTEIN; CARBOHYDRATE; HEXOSE; HYDROXYL GROUP; LEUCINE; O ANTIGEN; OCTASACCHARIDE; PARATOSE; POLYSACCHARIDE; PROTEIN; TYVELOSE; UNCLASSIFIED DRUG; WATER;

ARTICLE; BACTERIOPHAGE P22; BACTERIUM ISOLATION; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EPIMER; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; SALMONELLA ENTERITIDIS; SALMONELLA PARATYPHI; SALMONELLA TYPHIMURIUM; SEROTYPE;

AMINO ACID SEQUENCE; BACTERIOPHAGE P22; BINDING SITES; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; HEXOSES; MOLECULAR DOCKING SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; O ANTIGENS; PROTEIN BINDING; SALMONELLA PARATYPHI A; VIRAL TAIL PROTEINS;

EID: 84874695816     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cws224     Document Type: Article

References (51)

1. Andres D, Baxa U, Hanke C, Seckler R, Barbirz S. 2010. Carbohydrate binding of Salmonella phage P22 tailspike protein and its role during host cell infection. Biochem Soc Trans. 38:1386-1389.
2. Andres D, Hanke C, Baxa U, Seul A, Barbirz S, Seckler R. 2010. Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro. J Biol Chem. 285:36768-36775.
3. Andres D, Roske Y, Doering C, Heinemann U, Seckler R, Barbirz S. 2012. Tail morphology controls DNA release in two Salmonella phages with one lipopolysaccharide receptor recognition system. Mol Microbiol. 83: 1244-1253.
4. Bailey S. 1994. The Ccp4 suite - programs for protein crystallography. Acta Crystallogr D. 50:760-763.
5. Baxa U, Cooper A, Weintraub A, Pfeil W, Seckler R. 2001. Enthalpic barriers to the hydrophobic binding of oligosaccharides to phage P22 tailspike protein. Biochemistry. 40:5144-5150. (Pubitemid 32373996)
6. Baxa U, Steinbacher S, Miller S, Weintraub A, Huber R, Seckler R. 1996. Interactions of phage P22 tails with their cellular receptor, Salmonella O-antigen polysaccharide. Biophys J. 71:2040-2048. (Pubitemid 26325982)
7. Berger C, Weber-Bornhauser S, Eggenberger J, Hanes J, Pluckthun A, Bosshard HR. 1999. Antigen recognition by conformational selection. FEBS Lett. 450:149-153. (Pubitemid 29206729)
8. Boehr DD, Nussinov R, Wright PE. 2009. The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol. 5:789-796.
9. Bohne A, Lang E, von der Lieth CW. 1999. SWEET - WWW-based rapid 3D construction of oligo- and polysaccharides. Bioinformatics. 15:767-768. (Pubitemid 29484341)
10. Broeker NK, Gohlke U, Müller JJ, Uetrecht C, Heinemann U, Seckler R, Barbirz S. 2013. Single amino acid exchange in bacteriophage HK620 tailspike protein results in thousand-fold increase of its oligosaccharide affinity. Glycobiology. 23:59-68.
11. Bundle DR, Baumann H, Brisson JR, Gagne SM, Zdanov A, Cygler M. 1994. Solution structure of a trisaccharide-antibody complex: Comparison of NMR measurements with a crystal structure. Biochemistry. 33: 5183-5192. (Pubitemid 24150985)
12. Bundle DR, Eichler E, Gidney MA, Meldal M, Ragauskas A, Sigurskjold BW, Sinnott B, Watson DC, Yaguchi M, Young NM. 1994. Molecular recognition of a Salmonella trisaccharide epitope by monoclonal antibody Se155-4. Biochemistry. 33:5172-5182. (Pubitemid 24150984)
13. Bush CA, Martin-Pastor M, Imberty A. 1999. Structure and conformation of complex carbohydrates of glycoproteins, glycolipids, and bacterial polysaccharides. Annu Rev Biophys Biomol Struct. 28:269-293. (Pubitemid 29319260)
14. Casjens SR. 2008. Diversity among the tailed-bacteriophages that infect the Enterobacteriaceae. Res Microbiol. 159:340-348.
15. Chavelas EA, Garcia-Hernandez E. 2009. Heat capacity changes in carbohydrates and protein-carbohydrate complexes. Biochem J. 420:239-247.
16. Chen VB, Arendall WB, 3rd, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Crystallogr D. 66:12-21.
17. Dam TK, Brewer CF. 2002. Thermodynamic studies of lectin-carbohydrate interactions by isothermal titration calorimetry. Chem Rev. 102:387-429. (Pubitemid 35381635)
18. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA. 97:6640-6645. (Pubitemid 30412767)
19. El-Hawiet A, Kitova EN, Arutyunov D, Simpson DJ, Szymanski CM, Klassen JS. 2012. Quantifying ligand binding to large protein complexes using electrospray ionization mass spectrometry. Anal Chem. 84: 3867-3870.
20. Emsley P, Cowtan K. 2004. Coot: Model-building tools for molecular graphics. Acta Crystallogr D. 60:2126-2132. (Pubitemid 41742764)
21. Eriksson U, Svenson SB, Lonngren J, Lindberg AA. 1979. Salmonella phage glycanases: Substrate specificity of the phage P22 endo-rhamnosidase. J Gen Virol. 43:503-511. (Pubitemid 9206307)
22. Gabius HJ, Siebert HC, Andre S, Jimenez-Barbero J, Rudiger H. 2004. Chemical biology of the sugar code. Chembiochem. 5:740-764. (Pubitemid 39257059)
23. Galan JE, Curtiss R, 3rd. 1991. Distribution of the invA, -B, -C, and -D genes of Salmonella typhimurium among other Salmonella serovars: InvA mutants of Salmonella typhi are deficient for entry into mammalian cells. Infect Immun. 59:2901-2908.
24. Garcia-Hernandez E, Zubillaga RA, Chavelas-Adame EA, Vazquez- Contreras E, Rojo-Dominguez A, Costas M. 2003. Structural energetics of protein-carbohydrate interactions: Insights derived from the study of lysozyme binding to its natural saccharide inhibitors. Protein Sci. 12: 135-142. (Pubitemid 36020142)
25. Gauto DF, Petruk AA, Modenutti CP, Blanco JI, Di Lella S, Martí MA. 2012. Solvent structure improves docking prediction in lectin-carbohydrate complexes. Glycobiology. doi:10.1093/glycob/cws147.
26. Gupta D, Cho M, Cummings RD, Brewer CF. 1996. Thermodynamics of carbohydrate binding to galectin-1 from Chinese hamster ovary cells and two mutants. A comparison with four galactose-specific plant lectins. Biochemistry. 35:15236-15243. (Pubitemid 26408856)
27. Heinemann U, Bussow K, Mueller U, Umbach P. 2003. Facilities and methods for the high-throughput crystal structural analysis of human proteins. Acc Chem Res. 36:157-163.
28. Israel V. 1976. Role of the bacteriophage P22 tail in the early stages of infection. J Virol. 18:361-364.
29. Iwashita S, Kanegasaki S. 1973. Smooth specific phage adsorption: Endorhamnosidase activity of tail parts of P22. Biochem Biophys Res Commun. 55:403-409.
30. Kabsch W. 2010. XDS. Acta Crystallogr D Biol Crystallogr. 66:125-132.
31. Kadirvelraj R, Foley BL, Dyekjaer JD, Woods RJ. 2008. Involvement of water in carbohydrate-protein binding: Concanavalin A revisited. J Am Chem Soc. 130:16933-16942.
32. Keegan RM, Winn MD. 2007. Automated search-model discovery and preparation for structure solution by molecular replacement. Acta Crystallogr D. 63:447-457. (Pubitemid 46465938)
33. Klein E, Ferrand Y, Barwell NP, Davis AP. 2008. Solvent effects in carbohydrate binding by synthetic receptors: Implications for the role of water in natural carbohydrate recognition. Angew Chem Int Ed Engl. 47:2693-2696.
34. Landstrom J, Nordmark EL, Eklund R, Weintraub A, Seckler R, Widmalm G. 2008. Interaction of a Salmonella enteritidis O-antigen octasaccharide with the phage P22 tailspike protein by NMR spectroscopy and docking studies. Glycoconj J. 25:137-143. (Pubitemid 351238190)
35. Langer G, Cohen S, Lamzin V, Perrakis A. 2008. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protocols. 3:1171-1179.
36. Leder L, Berger C, Bornhauser S, Wendt H, Ackermann F, Jelesarov I, Bosshard HR. 1995. Spectroscopic, calorimetric, and kinetic demonstration of conformational adaptation in peptide-antibody recognition. Biochemistry. 34:16509-16518. (Pubitemid 26006498)
37. Lerouge I, Vanderleyden J. 2002. O-antigen structural variation: Mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev. 26:17-47. (Pubitemid 34454774)
38. Lüderitz O, Staub AM, Westphal O. 1966. Immunochemistry of O and R antigens of Salmonella and related Enterobacteriaceae. Bacteriol Rev. 30:192-255.
39. Lutteke T, Frank M, von der Lieth CW. 2005. Carbohydrate structure suite (CSS): Analysis of carbohydrate 3D structures derived from the PDB. Nucleic Acids Res. 33:D242-246. (Pubitemid 40207870)
40. Lutteke T, von der Lieth CW. 2004. pdb-care (PDB carbohydrate residue check): A program to support annotation of complex carbohydrate structures in PDB files. BMC Bioinformatics. 5:69.
41. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. 2007. Phaser crystallographic software. J Appl Crystallogr. 40: 658-674. (Pubitemid 47080256)
42. Meltzer E, Schwartz E. 2010. Enteric fever: A travel medicine oriented view. Curr Opin Infect Dis. 23:432-437.
43. Muller JJ, Barbirz S, Heinle K, Freiberg A, Seckler R, Heinemann U. 2008. An intersubunit active site between supercoiled parallel beta helices in the trimeric tailspike endorhamnosidase of Shigella flexneri phage Sf6. Structure. 16:766-775. (Pubitemid 351615015)
44. Murshudov GN, Vagin AA, Dodson EJ. 1997. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D. 53:240-255. (Pubitemid 27235885)
45. Schuttelkopf AW, van Aalten DM. 2004. PRODRG: A tool for highthroughput crystallography of protein-ligand complexes. Acta Crystallogr D. 60:1355-1363. (Pubitemid 41079731)
46. Steinbacher S, Baxa U, Miller S, Weintraub A, Seckler R, Huber R. 1996. Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. O-antigen receptors. Proc Natl Acad Sci USA. 93: 10584-10588. (Pubitemid 26333030)
47. Steinbacher S, Seckler R, Miller S, Steipe B, Huber R, Reinemer P. 1994. Crystal structure of P22 tailspike protein: Interdigitated subunits in a thermostable trimer. Science. 265:383-386. (Pubitemid 24259969)
48. Tindall BJ, Grimont PA, Garrity GM, Euzéby JP. 2005. Nomenclature and taxonomy of the genus Salmonella. Int J Syst Evol Microbiol. 55:521-524. (Pubitemid 40192484)
49. Turnbull WB, Daranas AH. 2003. On the value of c: Can low affinity systems be studied by isothermal titration calorimetry? J AmChem Soc. 125:14859-14866. (Pubitemid 37475576)
50. Worrall LJ, Lameignere E, Strynadka NCJ. 2011. Structural overview of the bacterial injectisome. Curr Opin Microbiol. 14:3-8.
51. Zaccheus MV, Broeker NK, Lundborg M, Uetrecht C, Barbirz S, Widmalm G. 2012. Structural studies of the O-antigen polysaccharide from Escherichia coli TD2158 having O18 serogroup specificity and aspects of its interaction with the tailspike endoglycosidase of the infecting bacteriophage HK620. Carbohydr Res. 357:118-125.