The structural biology of molecular recognition by vancomycin

Annual Review of Biophysics and Biomolecular Structure

Volumn 29, Issue , 2000, Pages 265-289

  Loll, Patrick J ^a   Axelsen, Paul H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Allosterism; Cooperativity; Entropy enthalpy compensation; Glycopeptide antibiotics; Molecular dynamics simulation

Indexed keywords

VANCOMYCIN;

ALLOSTERISM; DRUG PROTEIN BINDING; GRAM NEGATIVE BACTERIUM; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANTI-BACTERIAL AGENTS; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DRUG RESISTANCE, MICROBIAL; LIGANDS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; VANCOMYCIN;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; POSIBACTERIA;

EID: 0033880691     PISSN: 10568700     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.biophys.29.1.265     Document Type: Review

References (102)

1. 1. Nagarajan R. 1993. Structure-activity relationships of vancomycin glycopeptide antibiotics. J. Antibiot. 46:1181-95
2. 2. Nagarajan R. 1994. Glycopeptide Antibiotics. New York: Marcel Dekker
3. 3. Tipper DJ, Strominger JL. 1965. Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine. Proc. Natl. Acad. Sci. USA 54:1133-41
4. 4. Popieniek PH, Pratt RF. 1987. A fluorescent ligand for binding studies with glycopeptide antibiotics of the vancomycin class. Anal. Biochem. 165:108-13
5. 5. Shlaes DM, Shlaes JH, Davies J, Williamson R. 1989. Escherichia coli susceptible to glycopeptide antibiotics. Antimicrob. Agents Chemother. 33:192-97
6. 6. Sieradzki K, Roberts RB, Haber SW, Tomasz A. 1999. The development of vancomycin resistance in a patient with methicillin-resistant Staphylococcus aureus infection. N. Engl. J. Med. 340:517-23
7. 7. Smith TL, Pearson ML, Wilcox KR, Cruz C, Lancaster MV, et al. 1999. Emergence of vancomycin resistance in Staphylococcus aureus. N. Engl. J. Med. 340:493-501
8. 8. Novak R, Henriques B, Charpentier E, Normark S, Tuomanen E. 1999. Emergence of vancomycin tolerance in Streptococcus pneumoniae. Nature 399:590-93
9. 9. Reynolds PE. 1998. Control of peptidoglycan synthesis in vancomycin-resistant enterococci: D,D-peptidases and D,D-carboxy-peptidases. Cell. Mol. Life Sci. 54:325-31
10. 10. Billot-Klein D, Gutmann L, Sable S, Guittet E, van Heijenoort J. 1994. Modification of peptidoglycan precursors is a common feature of the low-level vancomycin-resistant vanB-type Enterococcus D366 and of the naturally glycopeptide-resistant species Lactobacillus casei, Pediococcus pentosaceus, Leuconostoc mesenteroides, and Enterococcus gallinarum. J. Bacterial. 176: 2398-405
11. 11. Sheldrick GM, Jones PG, Kennard O, Williams DH, Smith GA. 1978. Structure of vancomycin and its complex with acetyl-D-alanyl-D-alanine. Nature 271:223-25
12. 12. Williamson MP, Williams DH. 1981. Structure revision of the antibiotic vancomycin. The use of nuclear overhauser effect difference spectroscopy. J. Am. Chem. Soc. 103:6580-85
13. 13. Harris CM, Harris TM. 1982. Structure of the glycopeptide antibiotic vancomycin. Evidence for an asparagine residue in the peptide. J. Am. Chem. Soc. 104:4293-95
14. 14. Harris CM, Kopecka H, Harris TM. 1983. Vancomycin: structure and transformation to CDP-1. J. Am. Chem. Soc. 105:6915-22
15. 15. Kalman JR, Williams DH. 1980. An NMR study of the structure of the antibiotic ristocetin A. The negative nuclear overhauser effect in structure elucidation. J. Am. Chem. Soc. 102:897-905
16. 16. Barna JC, Williams DH, Stone DJM, Leung T-WC, Doddrell DM. 1984. Structure elucidation of the teicoplanin antibiotics. J. Am. Chem. Soc. 106:4895-902
17. 17. Schulz GE, Schirmer RH. 1979. Principles of Protein Structure. New York: Springer
18. 18. Skelton NJ, Williams DH, Ranee M J, Ruddock JC. 1991. Structure elucidation of a novel antibiotic of the vancomycin group. The influence of ion-dipole interactions on peptide backbone conformation. J. Am. Chem. Soc. 113:3757-65
19. 19. Perkins HR. 1969. Specificity of combination between mucopeptide precursors and vancomycin or ristocetin. Biochem. J. 111:195-205
20. 1H NMR. Acc. Chem. Res. 17:364-69
21. 21. Williams DH, Waltho JP. 1988. Molecular basis of the activity of antibiotics of the vancomycin group. Biochem. Pharmacol. 37:133-41
22. 22. Williams DH. 1996. The glycopeptide story - how to kill the deadly 'superbugs.' Nat. Prod. Rep. 13:469-77
23. 23. Williams DH, Bardsley B. 1999. The vancomycin group of antibiotics and the fight against resistant bacteria. Angew. Chem. Int. Ed. 38:1173-93
24. 24. Kalman JR, Williams DH. 1980. An NMR study of the interaction between the antibiotic ristocetin A and a cell wall peptide analogue. Negative nuclear overhauser effects in the investigation of drug binding sites. J. Am. Chem. Soc. 102:906-12
25. 1H nuclear magnetic resonance study of the interactions of vancomycin with N-Acetyl-D-alanyl-D-alanine andrelatedpeptides. J. Chem. Soc. Perkin Trans. 2, pp. 1262-70
26. 26. Waltho JP, Cavanagh J, Williams DH. 1988. Aspects of molecular recognition: use of a truncated driven pseudo-NOESY experiment to elucidate the environment of intermolecular electrostatic interactions in vancomycin. J. Chem. Soc. Chem. Commun., pp. 707-9
27. 27. Waltho JP, Williams DH. 1989. Aspects of molecular recognition: solvent exclusion and dimerization of the antibiotic ristocetin when bound to a model bacterial cell-wall precursor. J. Am. Chem. Soc. 111:2475-80
28. 28. Waltho JP, Williams DH. 1991. The natural design of vancomycin family antibiotics to bind their target peptides. Ciba Found. Symp. 158:73-91
29. 29. Axelsen PH, Li D. 1998. A rational strategy for enhancing the affinity of vancomycin towards depsipeptide ligands. Bioorg. Med. Chem. 6:877-81
30. 30. Waltho JP, Williams DH, Stone DJM, Skelton NJ. 1988. Intramolecular determinants of conformation and mobility within the antibiotic vancomycin. J. Am. Chem. Soc. 110:5638-43
31. 31. Prowse WG, Kline AD, Skelton MA, Loncharich RJ. 1995. Conformation of A828468B, a glycopeptide antibiotic, complexed with its cell wall fragment: an asymmetric homodimer determined using NMR spectroscopy. Biochemistry 34:9632-44
32. 32. Williams DH, Williamson MP, Butcher DW, Hammond SJ. 1983. Detailed binding sites of the antibiotics vancomycin and ristocetin A: determination of intermolecular distances in antibiotic/substrate complexes by use of the time-dependent NOE. J. Am. Chem. Soc. 105:1332-39
33. 33. Fesik SW, Armitage IM, Ellestad GA, McGahren WJ. 1984. Nuclear magnetic resonance studies on the interaction of avoparcin with model receptors of bacterial cell walls. Mol. Pharmacol. 25:281-86
34. 2-Lys-D-Ala-D-Ala complex using NMR parameters and molecular mode ling. J. Am. Chem. Soc. 108:3165-70
35. 35. Linsdell H, Toiron C, Bruix M, Rivas G, Menendez M. 1996. Dimerization of A82846B, vancomycin and ristocetin: influence on antibiotic complexation with cell wall model peptides. J. Antibiot. 49:181-93
36. 2-Lys-D-Ala-D-Ala. J. Am. Chem. Soc. 118:5874-80
37. 2-L-Lys-D-Ala-D-Ala and Ac-L-Ala-γ-D-Gln-L-Lys(Ac)-D-Ala-D-Ala: an application of nuclear magnetic resonance spectroscopy and distance geometry in modeling of peptides. J. Am. Chem. Soc. 111:496-505
38. 38. Dancer RJ, Try AC, Sharman GJ, Williams DH. 1996. Binding of a vancomycin group antibiotic to a cell wall analogue from vancomycin-resistant bacteria. Chem. Commun., pp. 1445-46
39. 39. van Wageningen AA, Staroske T, Williams DH. 1998. Binding of D-serine-terminating cell-wall analogues to glycopeptide antibiotics. Chem. Commun., pp. 1171-72
40. 40. Molinari H, Pastore A, Lian L, Hawkes GE, Sales K. 1990. Structure of vancomycin and a vancomycin/D-Ala-D-Ala complex in solution. Biochemistry 29:2271-77
41. 41. Li DH, Sreenivasan U, Juranic N, Macura S, Puga FJI, et al. 1997. Simulated dipeptide recognition by vancomycin. J. Mol. Recogn. 10:73-87
42. 42. Sheldrick GM, Paulus E, Vertesy L, Hahn F. 1995. Structure of ureido-balhiniycin. Acta Crystallogr. B51:89-98
43. 43. Sheldrick GM, Dauter Z, Wilson KS, Hope H, Sieker LC. 1993. The application of direct methods and Patterson interpretation to high-resolution native protein data. Acta Crystallogr. D 49:18-23
44. 44. Schafer M, Pohl E, Schmidt Base K, Sheldrick GM, Hermann R, et al. 1996. The molecular and crystal structure of the glycopeptide A-40926 aglycone. Helv. Chim. Acta 19:1916-24
45. 45. Sheldrick GM, Gould RO. 1995. Structure solution by interactive peaklist optimization and tangent expansion in space group P1. Acta Crystallogr. B 51:423-31
46. 46. Schafer M, Schneider TR, Sheldrick GM. 1996. Crystal structure of vancomycin. Structure 4:1509-15
47. 47. Loll PJ, Bevivino AE, Korty BD, Axelsen PH. 1997. Simultaneous recognition of a carboxylate-containing ligand and an intramolecular surrogate ligand in the crystal structure of an asymmetric vancomycin dimer. J. Am. Chem. Soc. 119:1516-22
48. 48. Loll PJ, Miller R, Weeks CM, Axelsen PH. 1998. A ligand-mediated dimerization mode for vancomycin. Chem. Biol. 5:293-98
49. 49. Schafer M, Sheldrick GM, Schneider TR, Vertesy L. 1998. Structure of balhimycin and its complex with solvent molecules. Acta Crystallogr. D 54:175-83
50. 50. Eberstadt M, Cuba W, Kessler H, Kogler H, Mierke DF. 1995. Conformation and dynamics of dimeric ureido-balhimycin. Biopolymers 36:429-37
51. 51. Williams DH, Searle MS, Mackay JP, Gerhard U, Maplestone RA. 1993. Toward an estimation of binding constants in aqueous solution: studies of associations of vancomycin group antibiotics. Proc. Natl. Acad. Sci. USA 90:1172-78
52. 13C NMR spectroscopy. J. Chem. Soc. Perkin Trans. 2, pp. 2:159-63
53. 53. Stack DR, Letourneau DL, Mullen DL, Butler TF, Allen NE, et al. 1998. Covalent glycopeptide dimers: synthesis, physical characterization, and antibacterial activity. 37th Intersci. Conf. Antimicrob. Agents Chemother. 37:146
54. 54. Williams DH. 1991. The molecular basis of biological order. Aldrichim. Acta 24:71-80
55. 55. Williams DH, Cox JPL, Doig AJ, Gardner M, Gerhard U, et al. 1991. Toward the semiquantitative estimation of binding constants. Guides for peptide-peptide binding in aqueous solution. J. Am. Chem. Soc. 113:7020-30
56. 56. Searle MS, Williams DH, Gerhard U. 1992. Partitioning of free energy contributions in the estimation of binding constants: residual motions and consequences for amideamide hydrogen bond strengths. J. Am. Chem. Soc. 114:10697-704
57. 57. Gerhard U, Searle MS, Williams DH. 1993. The free energy change of restricting a bond rotation in the binding of peptide analogues to vancomycin group antibiotics. Bioorg. Med. Chem. Lett. 3:803-8
58. 58. Searle MS, Williams DH. 1992. The cost of conformational order: entropy changes in molecular associations. J. Am. Chem. Soc. 114:10690-97
59. 59. Williams DH, Westwell MS. 1996. Weak interactions and lessons from crystallization. Chem. Biol. 3:695-701
60. 60. Breslow R. 1979. Biomimetic chemistry in oriented systems. Isr. J. Chem. 18:187-91
61. 61. Popieniek PH, Pratt RE 1991. Kinetics and mechanism of binding of specific peptides to vancomycin and other glycopeptide antibiotics. J. Am. Chem. Soc. 113:2264-70
62. 62. Williamson MP, Williams DH. 1984. Hydrophobic interactions affect hydrogen bond strengths in complexes between peptides and vancomycin or ristocetin. Eur. J. Biochem. 138:345-48
63. 63. Groves P, Searle MS, Westwell MS, Williams DH. 1994. Expression of electrostatic binding cooperativity in the recognition of cell-wall peptide analogues by vancomycin group antibiotics. J. Chem. Soc. Chem. Commun., pp. 1519-20
64. 64. Sharman GJ, Searle MS, Benhamu B, Groves P, Williams DH. 1995. Burial of hydrocarbon causes cooperative enhancement of electrostatic binding. Angew. Chem. Int. Ed. 34:1483-85
65. 65. Cristofaro MF, Beauregard DA, Yan HS, Osborn NJ, Williams DH. 1995. Cooperativity between nonpolar and ionic forces in the binding of bacterial-cell wall analogs by vancomycin in aqueous solution. J. Antibiot. 48:805-10
66. 66. Searle MS, Sharman GJ, Groves P, Benhamu B, Beauregard DA, et al. 1996. Enthalpic (electrostatic) contribution to the chelate effect: a correlation between ligand binding constant and a specific hydrogen bond strength in complexes of glycopeptide antibiotics with cell wall analogues. J. Chem. Soc. Perkin Trans. 1, pp. 2781-86
67. 67. Williams DH, Searle MS, Westwell MS, Mackay JP, Groves P, Beauregard DA. 1994. The role of weak interactions, dimerization, and cooperativity in antibiotic action and biological signaling. Chemtracsts Org. Chem. 7:133-55
68. 68. Searle MS, Westwell MS, Williams DH. 1995. Application of a generalized enthalpy-entropy relationship to binding cooperativity and weak associations in solution. J. Chem. Soc. Perkin Trans. 2, pp. 141-51
69. 69. Westwell MS, Searle MS, Klein J, Williams DH. 1996. Successful predictions of the residual motion of weakly associated species as a function of the bonding between them. J. Phys. Chem. 100:16000-1
70. 70. Smith PE, van Gunsteren WF. 1994. When are free-energy components meaningful? J. Phys. Chem. 98:13735-40
71. 71. Boresch S, Archontis G, Karplus M. 1994. Free energy simulations: the meaning of the individual contributions from a component analysis. Proteins: Struct. Funct. Genet. 20:25-33
72. 72. Groves P, Searle MS, Mackay JP, Williams DH. 1994. The structure of an asymmetric dinier relevant to the mode of action of the glycopeptide antibiotics. Structure 2:747-53
73. 73. Mackay JP, Gerhard U, Beauregard DA, Westwell MS, Searle MS, Williams DH. 1994. Glycopeptide antibiotic-activity and the possible role of dimerization-a model for biological signaling. J. Am. Chem. Soc. 116:4581-90
74. 74. Mackay JP, Gerhard U, Beauregard DA, Maplestone RA, Williams DH. 1994. Dissection of the contributions toward dimerization of glycopeptide antibiotics. J. Am. Chem. Soc. 116:4573-80
75. 75. Groves P, Searle MS, Waltho JP, Williams DH. 1995. Asymmetry in the structure of glycopeptide antibiotic dimers: NMR studies of the ristocetin a complex with a bacterial cell wall analog. J. Am. Chem. Soc. 117:7958-64
76. 76. Gerhard U, Mackay JP, Maplestone RA, Williams DH. 1993. The role of the sugar and chlorine substituents in the dimerization of vancomycin antibiotics. J. Am. Chem. Soc. 115:232-37
77. 77. Batta G, Cristofaro MF, Sharman GJ, Williams DH. 1996. Demonstration of the difference in binding affinity between the two binding sites of the ristocetin A asymmetric dinier. Chem. Commun., pp. 101-3
78. 78. Cho YR, Maguire AJ, Try AC, Westwell MS, Groves P, Williams DH. 1996. Cooperativity and anti-cooperativity between ligand binding and the dimerization of ristocetin A: asymmetry of a homodimer complex and implications for signal transduction. Chem. Biol. 3:207-15
79. 79. Bardsley B, Williams DH. 1998. Cooperativity between ligand binding and dimerisation in a derivative of ristocetin A. J. Chem. Soc. Perkin Trans. 2, pp. 1925-29
80. 80. Bardsley B, Williams DH. 1997. Measurement of the different affinities of the two halves of glycopeptide dimers for acetate. Chem. Commun., pp. 1049-50
81. 81. Westwell MS, Bardsley B, Dancer RJ, Try AC, Williams DH. 1996. Cooperativity in ligand binding expressed at a model cell membrane by the vancomycin group antibiotics. Chem. Commun., pp. 589-90
82. 82. Entress RM, Dancer RJ, O'Brien DP, Try AC, Cooper MA, Williams DH. 1998. 19F NMR in the measurement of binding affinities of chloroeremomycin to model bacterial cell-wall surfaces that mimic VanA and VanB resistance. Chem. Biol. 5:329-37
83. 83. O'Brien DP, Entress RH, Cooper MA, O'Brien SW, Hopkinson A, Williams DH. 1999. High affinity surface binding of a strongly dimerizing vancomycin-group antibiotic to a model of resistant bacteria. J. Am. Chem. Soc. 121:5259-65
84. 84. Beauregard DA, Williams DH, Gwynn MN, Knowles DJC. 1995. Dimerization and membrane anchors in extracelluar targetting of vancomycin group antibiotics. Antimicrob. Agents. Chemother. 39:781-85
85. 85. Beauregard DA, Maguire AJ, Williams DH, Reynolds PE. 1997. Semiquantitation of cooperativity in binding of vancomycin group antibiotics to vancomycin susceptible and resistant organisms. Antimicrob. Agents Chemother. 41:2418-23
86. 86. Cooper MA, Williams DH, Cho YR. 1997. Surface plasmon resonance analysis of glycopeptide antibiotic activity at a model membrane surface. Chem. Commun., pp. 1625-26
87. 87. Sharman GJ, Try AC, Dancer RJ, Cho YR, Staroske T, et al. 1997. The roles of dimerization and membrane anchoring in activity of glycopeptide antibiotics against vancomycin-resistant bacteria. J. Am. Chem. Soc. 119:12041-47
88. 88. Ge M, Chen Z, Onishi HR, Kohler J, Silver LL, et al. 1999. Vancomycin derivatives that inhibit peptidoglycan biosynthesis without binding D-Ala-D-Ala. Science 284:507-11
89. 89. Nesloney CL, Kelly JW 1996. Progress towards understanding beta-sheet structure. Bioorg. Med. Chem. 4:739-66
90. 90. Williams DH, Maguire AJ, Tsuzuki W, Westwell MS. 1998. An analysis of the origins of a cooperative binding energy of dimerization. Science 280:711-14
91. 91. Williams DH, Searle MS, Westwell MS, Gerhard U, Holroyd SE. 1993. Towards a semi-quantitative description of a biomolecular association involving weak interactions in aqueous solution. Philos. Trans. R. Soc. London Ser. A. 345:11-21
92. 92. Cooper A, Dryden DTF. 1984. Allostery without conformational change: a plausible model. Eur. Biophys. J. 11:103-9
93. 93. Axelsen PH, Loll PJ. 1998. Allosteric regulation of ligand recognition in the vancomycin dimier. Biophys. J. 74:A281
94. 1H-NMR Studies of the effects of ligand binding on antibiotic dimerization. J. Chem. Soc. Perkin Trans.1, pp. 6:659-65
95. 95. Malabarba A, Nicas TI, Thompson RC. 1997. Structural modifications of glycopeptide antibiotics. Med. Res. Rev. 17:69-137
96. 96. Cooper RD, Snyder NJ, Zweifel MJ, Staszak MA, Wilkie SC, et al. 1996. Reductive alkylation of glycopeptide antibiotics: synthesis and antibacterial activity. J. Antibiot. 49:575-81
97. 97. Sundram UN, Griffin JH. 1996. Novel vancomycin dimers with activity against vancomycin-resistant enterococci. J. Am. Chem. Soc. 118:13107-8
98. 98. Rao JH, Colton IJ, Whitesides GM. 1997. Using capillary electrophoresis to study the electrostatic interactions involved in the association of D-Ala-D-Ala with vancomycin. J. Am. Chem. Soc. 119:9336-40
99. 99. Rao JH, Whitesides GM. 1997. Tight binding of a dimeric derivative of vancomycin with dimeric L-Lys-D-Ala-D-Ala. J. Am. Chem. Soc. 119:10286-90
100. 100. Rao JH, Yan L, Xu B, Whitesides GM. 1999. Using surface plasmon resonance to study the binding of vancomycin and its dimer to self-assembled monolayers presenting D-Ala-D-Ala. J. Am. Chem. Soc. 121:2629-30
101. 101. Rao JH, Lahiri J, Isaacs L, Weis RM, Whitesides GM. 1998. A trivalent system from vancomycin.D-ala-D-Ala with higher affinity than avidin-biotin. Science 280:708-11
102. 102. Loll PJ, Kaplan J, Selinsky BS, Axelsen PH. 1999. Vancomycin Binding to Low Affinity Ligands: Delineating a Minimum Set of Interactions Necessary for High Affinity Binding. J. Med. Chem. 42:4714-4719