Vibrio cholerae cytolysin recognizes the heptasaccharide core of complex N-glycans with nanomolar affinity

Journal of Molecular Biology

Volumn 425, Issue 5, 2013, Pages 944-957

  Levan, Sophia ^a   De, Swastik ^a   Olson, Rich ^a  

^a WESLEYAN UNIVERSITY   (United States)

Author keywords

cholera; complex N glycan; hemolysin; lectin; pore forming toxin

Indexed keywords

CARBOHYDRATE; CARBOHYDRATE BINDING PROTEIN; CYTOLYSIN; DISACCHARIDE; GLYCAN; HEPTASACCHARIDE; MANNOSE; MESOGLYCAN; MONOSACCHARIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANISOTROPY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; HEMOLYSIS; HOST RANGE; NONHUMAN; PRIORITY JOURNAL; RABBIT; VIBRIO CHOLERAE;

LOTUS; MAMMALIA; ORYCTOLAGUS CUNICULUS; VIBRIO CHOLERAE;

EID: 84874109172     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.12.016     Document Type: Article

References (67)

1. World Health Organization Weekly Epidemiological Record 2011
2. J. Zhu, M.B. Miller, R.E. Vance, M. Dziejman, B.L. Bassler, and J.J. Mekalanos Quorum-sensing regulators control virulence gene expression in Vibrio cholerae Proc. Natl. Acad. Sci. USA 99 2002 3129 3134 (Pubitemid 34240597)
3. V. Olivier, G.K. Haines 3rd, Y. Tan, and K.J. Satchell Hemolysin and the multifunctional autoprocessing RTX toxin are virulence factors during intestinal infection of mice with Vibrio cholerae El Tor O1 strains Infect. Immun. 75 2007 5035 5042 (Pubitemid 47502177)
4. V. Olivier, J. Queen, and K.J. Satchell Successful small intestine colonization of adult mice by Vibrio cholerae requires ketamine anesthesia and accessory toxins PLoS One 4 2009 e7352
5. A. Zitzer, I. Walev, M. Palmer, and S. Bhakdi Characterization of Vibrio cholerae El Tor cytolysin as an oligomerizing pore-forming toxin Med. Microbiol. Immunol. (Berl) 184 1995 37 44
6. A. Zitzer, T.M. Wassenaar, I. Walev, and S. Bhakdi Potent membrane-permeabilizing and cytocidal action of Vibrio cholerae cytolysin on human intestinal cells Infect. Immun. 65 1997 1293 1298 (Pubitemid 27146615)
7. A. Valeva, I. Walev, S. Weis, F. Boukhallouk, T.M. Wassenaar, and S. Bhakdi Pro-inflammatory feedback activation cycle evoked by attack of Vibrio cholerae cytolysin on human neutrophil granulocytes Med. Microbiol. Immunol. 197 2008 285 293 (Pubitemid 351754684)
8. R.C. Larocque, J.B. Harris, M. Dziejman, X. Li, A.I. Khan, and A.S. Faruque Transcriptional profiling of Vibrio cholerae recovered directly from patient specimens during early and late stages of human infection Infect. Immun. 73 2005 4488 4493 (Pubitemid 41105602)
9. A.M. Tsou, and J. Zhu Quorum sensing negatively regulates hemolysin transcriptionally and posttranslationally in Vibrio cholerae Infect. Immun. 78 2010 461 467
10. J. Queen, and K.J. Satchell Neutrophils are essential for containment of Vibrio cholerae to the intestine during the proinflammatory phase of infection Infect. Immun. 80 2012 2905 2913
11. L. Song, M.R. Hobaugh, C. Shustak, S. Cheley, H. Bayley, and J.E. Gouaux Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore Science 274 1996 1859 1866 (Pubitemid 26424757)
12. K. Yamashita, Y. Kawai, Y. Tanaka, N. Hirano, J. Kaneko, and N. Tomita Crystal structure of the octameric pore of staphylococcal γ-hemolysin reveals the β-barrel pore formation mechanism by two components Proc. Natl. Acad. Sci. USA 108 2011 17314 17319
13. S. De, and R. Olson Crystal structure of the Vibrio cholerae cytolysin heptamer reveals common features among disparate pore-forming toxins Proc. Natl. Acad. Sci. USA 108 2011 7385 7390
14. L. Abrami, and F.G. van Der Goot Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin J. Cell Biol. 147 1999 175 184 (Pubitemid 30211805)
15. B. Walker, O. Braha, S. Cheley, and H. Bayley An intermediate in the assembly of a pore-forming protein trapped with a genetically-engineered switch Chem. Biol. 2 1995 99 105
16. L. Eidels, R.L. Proia, and D.A. Hart Membrane receptors for bacterial toxins Microbiol. Rev. 47 1983 596 620 (Pubitemid 14210913)
17. I. Iacovache, F.G. van der Goot, and L. Pernot Pore formation: an ancient yet complex form of attack Biochim. Biophys. Acta 1778 2008 1611 1623
18. S. Farrand, E. Hotze, P. Friese, S.K. Hollingshead, D.F. Smith, and R.D. Cummings Characterization of a streptococcal cholesterol-dependent cytolysin with a lewis y and b specific lectin domain Biochemistry 47 2008 7097 7107 (Pubitemid 351958416)
19. R. Olson, and E. Gouaux Crystal structure of the Vibrio cholerae cytolysin (VCC) pro-toxin and its assembly into a heptameric transmembrane pore J. Mol. Biol. 350 2005 997 1016 (Pubitemid 40943458)
20. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
21. J.E. Mills, and P.M. Dean Three-dimensional hydrogen-bond geometry and probability information from a crystal survey J. Comput. Aided Mol. Des. 10 1996 607 622 (Pubitemid 126712453)
22. E. Rutenber, M. Ready, and J.D. Robertus Structure and evolution of ricin B chain Nature 326 1987 624 626 (Pubitemid 17051336)
23. Y. Liu, A.J. Chirino, Z. Misulovin, C. Leteux, T. Feizi, M.C. Nussenzweig, and P.J. Bjorkman Crystal structure of the cysteine-rich domain of mannose receptor complexed with a sulfated carbohydrate ligand J. Exp. Med. 191 2000 1105 1116
24. A.A. Jeyaprakash, A. Srivastav, A. Surolia, and M. Vijayan Structural basis for the carbohydrate specificities of artocarpin: variation in the length of a loop as a strategy for generating ligand specificity J. Mol. Biol. 338 2004 757 770 (Pubitemid 38507420)
25. R. Sankaranarayanan, K. Sekar, R. Banerjee, V. Sharma, A. Surolia, and M. Vijayan A novel mode of carbohydrate recognition in jacalin, a Moraceae plant lectin with a β-prism fold Nat. Struct. Biol. 3 1996 596 603 (Pubitemid 26239207)
26. N.E. Ziolkowska, B.R. O'Keefe, T. Mori, C. Zhu, B. Giomarelli, and F. Vojdani Domain-swapped structure of the potent antiviral protein griffithsin and its mode of carbohydrate binding Structure 14 2006 1127 1135 (Pubitemid 44056021)
27. X. Lee, A. Thompson, Z. Zhang, H. Ton-that, J. Biesterfeldt, and C. Ogata Structure of the complex of Maclura pomifera agglutinin and the T-antigen disaccharide, Galβ1, 3GalNAc J. Biol. Chem. 273 1998 6312 6318 (Pubitemid 28144721)
28. J.D. Li, J. Carroll, and D.J. Ellar Crystal structure of insecticidal Δ-endotoxin from Bacillus thuringiensis at 2.5 Å resolution Nature 353 1991 815 821 (Pubitemid 21912628)
29. N. Saha, and K.K. Banerjee Carbohydrate-mediated regulation of interaction of Vibrio cholerae hemolysin with erythrocyte and phospholipid vesicle J. Biol. Chem. 272 1997 162 167 (Pubitemid 27021139)
30. S. Dutta, B. Mazumdar, K.K. Banerjee, and A.N. Ghosh Three-dimensional structure of different functional forms of the Vibrio cholerae hemolysin oligomer: a cryo-electron microscopic study J. Bacteriol. 192 2010 169 178
31. Y. He, and R. Olson Three-dimensional structure of the detergent-solubilized Vibrio cholerae cytolysin (VCC) heptamer by electron cryomicroscopy J. Struct. Biol. 169 2010 6 13
32. K. Drickamer, and M.E. Taylor Glycan arrays for functional glycomics Genome Biol. 3 2002 REVIEWS1034
33. A. Varki, R.D. Cummings, J.D. Esko, H.H. Freeze, P. Stanley, and C.R. Bertozzi Essentials of Glycobiology 2nd ed. 2009 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
34. H. Ikigai, A. Akatsuka, H. Tsujiyama, T. Nakae, and T. Shimamura Mechanism of membrane damage by El Tor hemolysin of Vibrio cholerae O1 Infect. Immun. 64 1996 2968 2973 (Pubitemid 26256134)
35. S.T. Miyata, M. Kitaoka, L. Wieteska, C. Frech, N. Chen, and S. Pukatzki The Vibrio cholerae type VI secretion system: evaluating its role in the human disease cholera Front. Microbiol. 1 2010 117
36. S. Pukatzki, A.T. Ma, D. Sturtevant, B. Krastins, D. Sarracino, and W.C. Nelson Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system Proc. Natl. Acad. Sci. USA 103 2006 1528 1533 (Pubitemid 43191199)
37. J. Beneteau, D. Renard, L. Marche, E. Douville, L. Lavenant, and Y. Rahbe Binding properties of the N-acetylglucosamine and high-mannose N-glycan PP2-A1 phloem lectin in Arabidopsis Plant Physiol. 153 2010 1345 1361
38. L.D. Hung, Y. Sato, and K. Hori High-mannose N-glycan-specific lectin from the red alga Kappaphycus striatum (Carrageenophyte) Phytochemistry 72 2011 855 861
39. B. Al Atalah, E. Fouquaert, D. Vanderschaeghe, P. Proost, J. Balzarini, and D.F. Smith Expression analysis of the nucleocytoplasmic lectin 'Orysata' from rice in Pichia pastoris FEBS J. 278 2011 2064 2079
40. N.N. Nagre, V.B. Chachai, P.M. Sundaram, R.S. Naik, R. Pujari, and P. Shastry A potent mitogenic lectin from the mycelia of a phytopathogenic fungus, Rhizoctonia bataticola, with complex sugar specificity and cytotoxic effect on human ovarian cancer cells Glycoconj. J. 27 2010 375 386
41. E. Fouquaert, D.F. Smith, W.J. Peumans, P. Proost, J. Balzarini, S.N. Savvides, and E.J. Damme Related lectins from snowdrop and maize differ in their carbohydrate-binding specificity Biochem. Biophys. Res. Commun. 380 2009 260 265
42. J.P. Gourdine, G. Cioci, L. Miguet, C. Unverzagt, D.V. Silva, and A. Varrot High affinity interaction between a bivalve C-type lectin and a biantennary complex-type N-glycan revealed by crystallography and microcalorimetry J. Biol. Chem. 283 2008 30112 30120
43. M.A. Kerr, and S.C. Stocks The role of CD15-(Le(X))-related carbohydrates in neutrophil adhesion Histochem. J. 24 1992 811 826
44. A. Torii, A. Nakayama, A. Harada, A. Nakao, T. Nonami, and J. Sakamoto Expression of the CD15 antigen in hepatocellular carcinoma Cancer 71 1993 3864 3867 (Pubitemid 23172962)
45. N. Malagolini, D. Santini, M. Chiricolo, and F. Dall'Olio Biosynthesis and expression of the Sda and sialyl Lewis x antigens in normal and cancer colon Glycobiology 17 2007 688 697 (Pubitemid 47050658)
46. J. Mahdavi, B. Sonden, M. Hurtig, F.O. Olfat, L. Forsberg, and N. Roche Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation Science 297 2002 573 578 (Pubitemid 34815336)
47. K.D. Tucker, and T.D. Wilkins Toxin A of Clostridium difficile binds to the human carbohydrate antigens I, X, and Y Infect. Immun. 59 1991 73 78
48. M.C. Chung, B.D. Wines, H. Baker, R.J. Langley, E.N. Baker, and J.D. Fraser The crystal structure of staphylococcal superantigen-like protein 11 in complex with sialyl Lewis X reveals the mechanism for cell binding and immune inhibition Mol. Microbiol. 66 2007 1342 1355 (Pubitemid 350179672)
49. F. Nakayama, S. Nishihara, H. Iwasaki, T. Kudo, R. Okubo, and M. Kaneko CD15 expression in mature granulocytes is determined by α1, 3-fucosyltransferase IX, but in promyelocytes and monocytes by α1,3-fucosyltransferase IV J. Biol. Chem. 276 2001 16100 16106
50. M.V. Croce, M. Isla-Larrain, M.E. Rabassa, S. Demichelis, A.G. Colussi, and M. Crespo Lewis x is highly expressed in normal tissues: a comparative immunohistochemical study and literature revision Pathol. Oncol. Res. 13 2007 130 138 (Pubitemid 47204735)
51. V. Olivier, N.H. Salzman, and K.J. Satchell Prolonged colonization of mice by Vibrio cholerae El Tor O1 depends on accessory toxins Infect. Immun. 75 2007 5043 5051 (Pubitemid 47502178)
52. L.G. Yu The oncofetal Thomsen-Friedenreich carbohydrate antigen in cancer progression Glycoconj. J. 24 2007 411 420
53. F. van den Akker, E. Steensma, and W.G. Hol Tumor marker disaccharide d-Gal-β1,3-GalNAc complexed to heat-labile enterotoxin from Escherichia coli Protein Sci. 5 1996 1184 1188 (Pubitemid 26172907)
54. J.U. Baenziger, and D. Fiete Structure of the complex oligosaccharides of fetuin J. Biol. Chem. 254 1979 789 795 (Pubitemid 9145936)
55. E.D. Green, G. Adelt, J.U. Baenziger, S. Wilson, and H. Van Halbeek The asparagine-linked oligosaccharides on bovine fetuin. Structural analysis of N-glycanase-released oligosaccharides by 500-megahertz 1H NMR spectroscopy J. Biol. Chem. 263 1988 18253 18268 (Pubitemid 19005103)
56. M.G. Yet, C.C. Chin, and F. Wold The covalent structure of individual N-linked glycopeptides from ovomucoid and asialofetuin J. Biol. Chem. 263 1988 111 117
57. H. Connaris, P.R. Crocker, and G.L. Taylor Enhancing the receptor affinity of the sialic acid-binding domain of Vibrio cholerae sialidase through multivalency J. Biol. Chem. 284 2009 7339 7351
58. K. Nagamune, K. Yamamoto, and T. Honda Cloning and sequencing of a novel hemolysis gene of Vibrio cholerae FEMS Microbiol. Lett. 128 1995 265 269
59. G.F. Clark, S. Oehninger, and M. Seppala Role for glycoconjugates in cellular communication in the human reproductive system Mol. Hum. Reprod. 2 1996 513 517 (Pubitemid 126717490)
60. M. Sutton-Smith, N.K. Wong, K.H. Khoo, S.W. Wu, S.Y. Yu, and M.S. Patankar Analysis of protein-linked glycosylation in a sperm-somatic cell adhesion system Glycobiology 17 2007 553 567 (Pubitemid 47064313)
61. G.A. Wilke, and J. Bubeck Wardenburg Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus α-hemolysin-mediated cellular injury Proc. Natl. Acad. Sci. USA 107 2010 13473 13478
62. C.L. Fisher, and G.K. Pei Modification of a PCR-based site-directed mutagenesis method Biotechniques 23 1997 574
63. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
64. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
65. P.V. Afonine, R.W. Grosse-Kunstleve, N. Echols, J.J. Headd, N.W. Moriarty, and M. Mustyakimov Towards automated crystallographic structure refinement with phenix.refine Acta Crystallogr., Sect. D: Biol. Crystallogr. 68 2012 352 367
66. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
67. O. Blixt, S. Head, T. Mondala, C. Scanlan, M.E. Huflejt, and R. Alvarez Printed covalent glycan array for ligand profiling of diverse glycan binding proteins Proc. Natl. Acad. Sci. USA 101 2004 17033 17038 (Pubitemid 39627769)