The Effect of Environment on the Recognition and Binding of Vancomycin to Native and Resistant Forms of Lipid II

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2012 Jan 21

PMID 22261057

Citations 13

Authors

Zhiguang Jia

Megan L OMara

Johannes Zuegg

Matthew A Cooper

Alan E Mark

Affiliations

Soon will be listed here.

Abstract

Molecular dynamics simulations and free energy calculations have been used to examine in detail the mechanism by which a receptor molecule (the glycopeptide antibiotic vancomycin) recognizes and binds to a target molecule (lipid II) embedded within a membrane environment. The simulations show that the direct interaction of vancomycin with lipid II, as opposed to initial binding to the membrane, leads most readily to the formation of a stable complex. The recognition of lipid II by vancomycin occurred via the N-terminal amine group of vancomycin and the C-terminal carboxyl group of lipid II. Despite lying at the membrane-water interface, the interaction of vancomycin with lipid II was found to be essentially identical to that of soluble tripeptide analogs of lipid II (Ac-d-Ala-d-Ala; root mean-square deviation 0.11 nm). Free energy calculations also suggest that the relative binding affinity of vancomycin for native, resistant, and synthetic forms of membrane-bound lipid II was unaffected by the membrane environment. The effect of the dimerization of vancomycin on the binding of lipid II, the position of lipid II within a biological membrane, and the effect of the isoamylene tail of lipid II on membrane fluidity have also been examined.

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References

Poger D, Mark A . On the Validation of Molecular Dynamics Simulations of Saturated and cis-Monounsaturated Phosphatidylcholine Lipid Bilayers: A Comparison with Experiment. J Chem Theory Comput. 2015; 6(1):325-36. DOI: 10.1021/ct900487a. View

Loll P, DerHovanessian A, Shapovalov M, Kaplan J, Yang L, Axelsen P . Vancomycin forms ligand-mediated supramolecular complexes. J Mol Biol. 2008; 385(1):200-11. PMC: 2650734. DOI: 10.1016/j.jmb.2008.10.049. View

McComas C, Crowley B, Boger D . Partitioning the loss in vancomycin binding affinity for D-Ala-D-Lac into lost H-bond and repulsive lone pair contributions. J Am Chem Soc. 2003; 125(31):9314-5. DOI: 10.1021/ja035901x. View

Loll P, Kaplan J, Selinsky B, Axelsen P . Vancomycin binding to low-affinity ligands: delineating a minimum set of interactions necessary for high-affinity binding. J Med Chem. 1999; 42(22):4714-9. DOI: 10.1021/jm990361t. View

Rao J, Yan L, Lahiri J, Whitesides G, Weis R, Warren H . Binding of a dimeric derivative of vancomycin to L-Lys-D-Ala-D-lactate in solution and at a surface. Chem Biol. 1999; 6(6):353-9. DOI: 10.1016/S1074-5521(99)80047-7. View

Allen N, LeTourneau D, Hobbs Jr J . Molecular interactions of a semisynthetic glycopeptide antibiotic with D-alanyl-D-alanine and D-alanyl-D-lactate residues. Antimicrob Agents Chemother. 1997; 41(1):66-71. PMC: 163661. DOI: 10.1128/AAC.41.1.66. View

Johnson J, Yalkowsky S . Reformulation of a new vancomycin analog: an example of the importance of buffer species and strength. AAPS PharmSciTech. 2006; 7(1):E5. DOI: 10.1208/pt070105. View

Nieto M, Perkins H . Modifications of the acyl-D-alanyl-D-alanine terminus affecting complex-formation with vancomycin. Biochem J. 1971; 123(5):789-803. PMC: 1177079. DOI: 10.1042/bj1230789. View

Nitanai Y, Kikuchi T, Kakoi K, Hanamaki S, Fujisawa I, Aoki K . Crystal structures of the complexes between vancomycin and cell-wall precursor analogs. J Mol Biol. 2008; 385(5):1422-32. DOI: 10.1016/j.jmb.2008.10.026. View

10.

Poger D, van Gunsteren W, Mark A . A new force field for simulating phosphatidylcholine bilayers. J Comput Chem. 2009; 31(6):1117-25. DOI: 10.1002/jcc.21396. View

11.

van der Spoel D, Lindahl E, Hess B, Groenhof G, Mark A, Berendsen H . GROMACS: fast, flexible, and free. J Comput Chem. 2005; 26(16):1701-18. DOI: 10.1002/jcc.20291. View

12.

Schmid N, Eichenberger A, Choutko A, Riniker S, Winger M, Mark A . Definition and testing of the GROMOS force-field versions 54A7 and 54B7. Eur Biophys J. 2011; 40(7):843-56. DOI: 10.1007/s00249-011-0700-9. View

13.

Hasper H, Kramer N, Smith J, Hillman J, Zachariah C, Kuipers O . An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science. 2006; 313(5793):1636-7. DOI: 10.1126/science.1129818. View

14.

Hess B, Kutzner C, van der Spoel D, Lindahl E . GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation. J Chem Theory Comput. 2015; 4(3):435-47. DOI: 10.1021/ct700301q. View

15.

Cristofaro M, Beauregard D, Yan H, Osborn N, Williams D . Cooperativity between non-polar and ionic forces in the binding of bacterial cell wall analogues by vancomycin in aqueous solution. J Antibiot (Tokyo). 1995; 48(8):805-10. DOI: 10.7164/antibiotics.48.805. View

16.

Kahne D, Leimkuhler C, Lu W, Walsh C . Glycopeptide and lipoglycopeptide antibiotics. Chem Rev. 2005; 105(2):425-48. DOI: 10.1021/cr030103a. View

17.

Malde A, Zuo L, Breeze M, Stroet M, Poger D, Nair P . An Automated Force Field Topology Builder (ATB) and Repository: Version 1.0. J Chem Theory Comput. 2015; 7(12):4026-37. DOI: 10.1021/ct200196m. View

18.

Feenstra K, Hess B, Berendsen H . Improving efficiency of large time-scale molecular dynamics simulations of hydrogen-rich systems. J Comput Chem. 2022; 20(8):786-798. DOI: 10.1002/(SICI)1096-987X(199906)20:8<786::AID-JCC5>3.0.CO;2-B. View

19.

Allen N, LeTourneau D, Hobbs Jr J . The role of hydrophobic side chains as determinants of antibacterial activity of semisynthetic glycopeptide antibiotics. J Antibiot (Tokyo). 1997; 50(8):677-84. DOI: 10.7164/antibiotics.50.677. View

20.

Ganchev D, Hasper H, Breukink E, de Kruijff B . Size and orientation of the lipid II headgroup as revealed by AFM imaging. Biochemistry. 2006; 45(19):6195-202. DOI: 10.1021/bi051913e. View