Solution and Crystal Structures of a Sugar Binding Site Mutant of Cyanovirin-N: No Evidence of Domain Swapping

Structure

Volumn 16, Issue 8, 2008, Pages 1183-1194

  Matei, Elena ^a   Furey, William ^a,b   Gronenborn, Angela M ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

PROTEIN

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; CYANOVIRIN N; MANNOSE; MUTANT PROTEIN;

ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; CYANOBACTERIUM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN DOMAIN; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; CARBOHYDRATES; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

CYANOBACTERIA;

EID: 48149091784     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2008.05.011     Document Type: Article

References (58)

1. Adler P., Wood S.J., Lee Y.C., Lee R.T., Petri Jr. W.A., and Schnaar R.L. High affinity binding of the Entamoeba histolytica lectin to polyvalent N-acetylgalactosaminides. J. Biol. Chem. 270 (1995) 5164-5171
2. Barrientos L.G., and Gronenborn A.M. The domain-swapped dimer of cyanovirin-N contains two sets of oligosaccharide binding sites in solution. Biochem. Biophys. Res. Commun. 298 (2002) 598-602
3. Barrientos L.G., and Gronenborn A.M. The highly specific carbohydrate-binding protein cyanovirin-N: structure, anti-HIV/Ebola activity and possibilities for therapy. Mini Rev. Med. Chem. 5 (2005) 21-31
4. Barrientos L.G., Louis J.M., Botos I., Mori T., Han Z., O'Keefe B.R., Boyd M.R., Wlodawer A., and Gronenborn A.M. The domain-swapped dimer of cyanovirin-N is in a metastable folded state: reconciliation of X-ray and NMR structures. Structure 10 (2002) 673-686
5. Barrientos L.G., Matei E., Lasala F., Delgado R., and Gronenborn A.M. Dissecting carbohydrate-Cyanovirin-N binding by structure-guided mutagenesis: functional implications for viral entry inhibition. Protein Eng. Des. Sel. 19 (2006) 525-535
6. Bax A., and Grzesiek S. Methodological advances in protein NMR. Acc. Chem. Res. 26 (1993) 131-138
7. Bewley C.A., and Otero-Quintero S. The potent anti-HIV protein cyanovirin-N contains two novel carbohydrate binding sites that selectively bind to Man(8) D1D3 and Man(9) with nanomolar affinity: implications for binding to the HIV envelope protein gp120. J. Am. Chem. Soc. 123 (2001) 3892-3902
8. Bewley C.A., Gustafson K.R., Boyd M.R., Covell D.G., Bax A., Clore G.M., and Gronenborn A.M. Solution structure of cyanovirin-N, a potent HIV-inactivating protein. Nat. Struct. Biol. 5 (1998) 571-578
9. Bewley C.A., Kiyonaka S., and Hamachi I. Site-specific discrimination by cyanovirin-N for α-linked trisaccharides comprising the three arms of Man(8) and Man(9). J. Mol. Biol. 322 (2002) 881-889
10. Bolmstedt A.J., O'Keefe B.R., Shenoy S.R., McMahon J.B., and Boyd M.R. Cyanovirin-N defines a new class of antiviral agent targeting N-linked, high-mannose glycans in an oligosaccharide-specific manner. Mol. Pharmacol. 59 (2001) 949-954
11. Botos I., O'Keefe B.R., Shenoy S.R., Cartner L.K., Ratner D.M., Seeberger P.H., Boyd M.R., and Wlodawer A. Structures of the complexes of a potent anti-HIV protein cyanovirin-N and high mannose oligosaccharides. J. Biol. Chem. 277 (2002) 34336-34342
12. Botos I., Mori T., Cartner L.K., Boyd M.R., and Wlodawer A. Domain-swapped structure of a mutant of cyanovirin-N. Biochem. Biophys. Res. Commun. 294 (2002) 184-190
13. Boyd M.R., Gustafson K.R., McMahon J.B., Shoemaker R.H., O'Keefe B.R., Mori T., Gulakowski R.J., Wu L., Rivera M.I., Laurencot C.M., et al. Discovery of cyanovirin-N, a novel human immunodeficiency virus-inactivating protein that binds viral surface envelope glycoprotein gp120: potential applications to microbicide development. Antimicrob. Agents Chemother. 41 (1997) 1521-1530
14. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
15. Bundle D.R., and Young N.M. Carbohydrate-protein interactions in antibodies and lectins. Curr. Opin. Struct. Biol. 2 (1992) 666-673
16. Carson M. Ribbons 2.0. J. Appl. Cryst. 24 (1991) 958-961
17. Chang L.C., and Bewley C.A. Potent inhibition of HIV-1 fusion by cyanovirin-N requires only a single high affinity carbohydrate binding site: characterization of low affinity carbohydrate binding site knockout mutants. J. Mol. Biol. 318 (2002) 1-8
18. Cornilescu G., Marquardt J.L., Ottiger M., and Bax A. Validation of protein structure from anisotropic carbonyl chemical shifts in a dilute liquid crystalline phase. J. Am. Chem. Soc. 120 (1998) 6836-6837
19. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
20. DeFrees S., Phillips L., Guo L., and Zalipsky S. Sialyl Lewis x liposomes as a multivalent ligand and inhibitor of E-Selectin mediated cellular adhesion. J. Am. Chem. Soc. 118 (1996) 6101-6104
21. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
22. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
23. Fesik S.W., and Zuiderweg E.R. Heteronuclear three-dimensional NMR spectroscopy of isotopically labelled biological macromolecules. Q. Rev. Biophys. 23 (1990) 97-131
24. Fromme R., Katiliene Z., Giomarelli B., Bogani F., Mc Mahon J., Mori T., Fromme P., and Ghirlanda G. A monovalent mutant of cyanovirin-N provides insight into the role of multiple interactions with gp120 for antiviral activity. Biochemistry 46 (2007) 9199-9207
25. Grzesiek S., Vuister G.W., and Bax A. A simple and sensitive experiment for measurement of JCC couplings between backbone carbonyl and methyl carbons in isotopically enriched proteins. J. Biomol. NMR 3 (1993) 487-493
26. Güntert P., Mumenthaler C., and Wüthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273 (1997) 283-298
27. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
28. Herrmann T., Güntert P., and Wüthrich K. Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol. 319 (2002) 209-227
29. Hooft R.W., Vriend G., Sander C., and Abola E.E. Errors in protein structures. Nature 381 (1996) 272
30. Johnson B.A. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278 (2004) 313-352
31. Kiessling L.L., and Pohl N.L. Strength in numbers: non-natural polyvalent carbohydrate derivatives. Chem. Biol. 3 (1996) 71-77
32. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK - a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26 (1993) 283-291
33. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8 (1996) 477-486
34. Lee Y.C. Biochemistry of carbohydrate-protein interaction. FASEB J. 6 (1992) 3193-3200
35. Lees W.J., Spaltenstein A., Kingery-Wood J.E., and Whitesides G.M. Polyacrylamides bearing pendant alpha-sialoside groups strongly inhibit agglutination of erythrocytes by influenza A virus: multivalency and steric stabilization of particulate biological systems. J. Med. Chem. 37 (1994) 3419-3433
36. Lis H., and Sharon N. Lectins: carbohydrate-specific proteins that mediate cellular recognition. Chem. Rev. 98 (1998) 637-674
37. Liu Y., and Eisenberg D. 3D domain swapping: as domains continue to swap. Protein Sci. 11 (2002) 1285-1299
38. Logan T.M., Olejniczak E.T., Xu R.X., and Fesik S.W. A general method for assigning NMR spectra of denatured proteins using 3D HC(CO)NH-TOCSY triple resonance experiments. J. Biomol. NMR 3 (1993) 225-231
39. McCoy A.J., Grosse-Kunstleve R.W., Storoni L.C., and Read R.J. Likelihood-enhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61 (2005) 458-464
40. Meunier S.J., and Roy R. Polysialosides scaffolded on p-Tert-butylcalix[4]arene. Tetrahedron Lett. 37 (1996) 5469-5472
41. Mortell K., Weatherman R., and Kiessling L. Recognition specificity of neoglycopolymers prepared by ring-opening metathesis polymerization. J. Am. Chem. Soc. 118 (1996) 2297-2298
42. Mori S., Abeygunawardana C., Johnson M.O., and van Zijl P.C. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new fast HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson. B. 108 (1995) 94-98
43. 2O. J. Magn. Reson. B. 102 (1993) 317-321
44. Nagi A.D., and Regan L. An inverse correlation between loop length and stability in a four-helix-bundle protein. Fold. Des. 2 (1997) 67-75
45. Newcomer M.E. Protein folding and three-dimensional domain swapping: a strained relationship?. Curr. Opin. Struct. Biol. 12 (2002) 48-53
46. O'Keefe B.R., Shenoy S.R., Xie D., Zhang W., Muschik J.M., Currens M.J., Chaiken I., and Boyd M.R. Analysis of the interaction between the HIV-inactivating protein cyanovirin-N and soluble forms of the envelope glycoproteins gp120 and gp41. Mol. Pharmacol. 58 (2000) 982-992
47. Ottiger M., Delaglio F., and Bax A. Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra. J. Magn. Reson. 131 (1998) 373-378
48. Patterson G.M.L., Baker K.K., Baldwin C.L., Bolis C.M., Caplan F.R., Larsen L.K., Levine I.A., Moore R.E., Nelson C.S., Tschappat K.D., et al. Antiviral activity of cultured blue-green algae (Cyanophyta). J. Phycol. 29 (1993) 125-130
49. Pflugrath J.W. The finer things in X-ray diffraction data collection. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 1718-1725
50. Ramachandran G.N., and Sasisekharan V. RPMS: Ramachandran plot for multiple structures. Adv. Protein Chem. 23 (1968) 283-438
51. Sabesan S., Bock K., and Paulson J.C. Conformational analysis of sialyloligosaccharides. Carbohydr. Res. 218 (1991) 27-54
52. Sandström C., Berteau O., Gemma E., Oscarson S., Kenne L., and Gronenborn A.M. Atomic mapping of the interactions between the antiviral agent cyanovirin-N and oligomannosides by saturation-transfer difference NMR. Biochemistry 43 (2004) 13926-13931
53. Shenoy S.R., O'Keefe B.R., Bolmstedt A.J., Cartner L.K., and Boyd M.R. Selective interactions of the human immunodeficiency virus-inactivating protein cyanovirin-N with high-mannose oligosaccharides on gp120 and other glycoproteins. J. Pharmacol. Exp. Ther. 297 (2001) 704-710
54. Shenoy S.R., Barrientos L.G., Ratner D.M., O'Keefe B.R., Seeberger P.H., Gronenborn A.M., and Boyd M.R. Multisite and multivalent binding between cyanovirin-N and branched oligomannosides: calorimetric and NMR characterization. Chem. Biol. 9 (2002) 1109-1118
55. Sigal G.B., Mammen M., Dahmann G., and Whitesides G.M. Polyacrylamides bearing pendant α-Sialoside groups strongly inhibit agglutination of erythrocytes by influenza virus: the strong inhibition reflects enhanced binding through cooperative polyvalent interactions. J. Am. Chem. Soc. 118 (1996) 3789-3800
56. Spengard U., Schudok M., Schmidt W., Wolfgang S., Kretzschmar G., and Kunz H. Multiple sialyl Lewis(x) N-glycopeptides: effective ligands for E-selectin. Angew. Chem. Int. Ed. Engl. 35 (1996) 321-324
57. Talluri S., and Wagner G. An optimized 3D NOESY-HSQC. J. Magn. Reson. B. 112 (1996) 200-205
58. Yang F., Bewley C.A., Louis J.M., Gustafson K.R., Boyd M.R., Gronenborn A.M., Clore G.M., and Wlodawer A. Crystal structure of cyanovirin-N, a potent HIV-inactivating protein, shows unexpected domain swapping. J. Mol. Biol. 288 (1999) 403-412