Revisiting magnesium chelation by teichoic acid with phosphorus solid-state nmr and theoretical calculations

Journal of Physical Chemistry B

Volumn 113, Issue 7, 2009, Pages 2177-2183

  Wickham, Jason R ^a   Halye, Jeffrey L ^a   Kashtanov, Stepan ^a   Khandogin, Jana ^a   Rice, Charles V ^a  

^a UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDS; ANISOTROPY; BACTERIOLOGY; CELL MEMBRANES; CHELATION; CHEMICAL SHIFT; DENSITY FUNCTIONAL THEORY; HYDRATES; HYDRATION; ISOMERS; MAGNESIUM; MAGNESIUM PRINTING PLATES; MAGNETIC ANISOTROPY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PHOSPHORUS; PROBABILITY DENSITY FUNCTION; SOLID STATE PHYSICS; SULFUR COMPOUNDS; TENSORS;

BACTERIAL CELLS; BACTERIAL GROWTHS; BIDENTATE COORDINATIONS; BINDING MODES; CHEMICAL SHIFT ANISOTROPIES; DENSITY-FUNCTIONAL THEORIES; DFT CALCULATIONS; DIPHOSPHATE; ESSENTIAL COMPONENTS; EXPERIMENTAL DATUM; METAL BINDINGS; METAL CHELATIONS; MODEL COMPOUNDS; MONODENTATE; PHOSPHATE GROUPS; SOLID-STATE NMR; SOLID-STATE NMR SPECTROSCOPIES; TEICHOIC ACIDS; THEORETICAL CALCULATIONS;

BINDING ENERGY;

EID: 65249129189     PISSN: 15206106     EISSN: None     Source Type: Journal    
DOI: 10.1021/jp809313j     Document Type: Article

References (48)

1. Heptinstall, S.; Archibald, A. R.; Baddiley, J. Teichoic acids and membrane function in bacteria. Nature (London) 1970, 225, 519-21.
2. Ellwood, D. C. Wall content and composition of Bacillus subtilis varniger grown in a chemostat. Biochem. J. 1970, 118, 367-73.
3. Ellwood, D. C.; Tempest, D. W. Effects of environment on bacterial wall content and composition. Adv. Microb. Physiol. 1972, 7, 83-117.
4. Beveridge, T. J.; Murray, R. G. E. Sites of metal deposition in the cell wall of Bacillus subtilis. J. Bacteriol. 1980, 141, 876-87.
5. Lambert, P. A.; Hancock, I. C.; Baddiley, J. Influence of alanyl ester residues on the binding of magnesium ions to teichoic acids. Biochem. J. 1975, 151, 671-6.
6. Ginsburg, I. Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2002, 2, 171-9.
7. Graham, L. L.; Beveridge, T. J. Structural differentiation of the Bacillus-subtilis-168 cell-wall. J. Bacteriol. 1994, 176, 1413-21.
8. Neuhaus, F. C.; Baddiley, J. A continuum of anionic charge: structures and functions of D-alanyl-teichoic acid in Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 2003, 67, 686-723.
9. Baddiley, J.; Hancock, I. C.; Sherwood, P. M. A. X-Ray photoelectron studies of magnesium ions bound to the cell walls of Gram-positive bacteria. Nature (London) 1973, 243, 43-5.
10. Peschel, A. How do bacteria resist human antimicrobial peptides. Trends Microbiol. 2002, 10, 179-86.
11. Roethlisberger, P.; Iida-Tanaka, N.; Hollemeyer, K.; Heinzle, E.; Ishizuka, I.; Fischer, W. Unique poly(glycerophosphate) lipoteichoic acid and the glycolipids of a Streptococcus sp. closely related to Streptococcus pneumoniae. Eur. J. Biochem. 2000, 267, 5520-30.
12. Stadelmaier, A.; Morath, S.; Hartung, T.; Schmidt, R. R. Synthesis of the first fully active lipoteichoic acid. Angew. Chem., Int. Ed. 2003, 42, 916-20.
13. Potekhina, N. V.; Shashkov, A. S.; Evtushenko, L. I.; Senchenkova, S. y. N.; Naumova, I. B. A mannitol teichoic acid containing rhamnose and pyruvic acid acetal from the cell wall of Brevibacterium permense VKM Ac-2280. Carbohyd. Res. 2003, 338, 2745-9.
14. Morath, S.; Geyer, A.; Spreitzer, I.; Hermann, C.; Hartung, T. Structural decomposition and heterogeneity of commercial lipoteichoic acid preparations. Infect. Immun. 2002, 70, 938-44.
15. Morath, S.; Stadelmaier, A.; Geyer, A.; Schmidt, R. R.; Hartung, T. Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J. Exp. Med. 2002, 195, 1635-40.
16. Volkman, B. F.; Zhang, Q.; Debabov, D. V.; Rivera, E.; Kresheck, G. C.; Neuhaus, F. C. Biosynthesis of D-alanyl-lipoteichoic acid: the tertiary structure of apo-D-alanyl carrier protein. Biochem. J. 2001, 40, 7964-72.
17. Fischer, W.; Behr, T.; Hartmann, R.; Peter-Katalinic, J.; Egge, H. Teichoic acid and lipoteichoic acid of Streptococcus pneumoniae possess identical chain structures. A reinvestigation of teichoid acid (C polysaccharide). Eur. J. Biochem. 1993, 215, 851-7.
18. Heaton, M. P.; Neuhaus, F. C. Role of the D-alanyl carrier protein in the biosynthesis of D-alanyl-lipoteichoic acid. J. Bacteriol. 1994, 176, 681-90.
19. Behr, T.; Fischer, W.; Peterakatalinic, J.; Egge, H. The structure of Pneumococcal lipoteichoic acid - improved preparation, chemical and mass-spectrometric studies. Eur. J. Biochem. 1992, 207, 1063-75.
20. Iwasaki, H.; Shimada, A.; Yokoyama, K.; Ito, E. Structure and glycosylation of lipoteichoic acids in Bacillus strains. J. Bacteriol. 1989, 171, 424-9.
21. Gross, M.; Cramton, S. E.; Gotz, F.; Peschel, A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun. 2001, 69, 3423-6.
22. Amako, K.; Umeda, A.; Murata, K. Arrangement of peptidoglycan in the cell-wall of Staphylococcus spp. J. Bacteriol. 1982, 150, 844-50.
23. Umeda, A.; Ueki, Y.; Amako, K. Structure of the Staphylococcusaureus cell-wall determined by freeze-substitution method. J. Bacteriol. 1987, 169, 2482-7.
24. Umeda, A.; Yokoyama, S.; Arizono, T.; Amako, K. Location of peptidoglycan and teichoic-acid on the cell-wall surface of Staphylococcusaureus as determined by immunoelectron microscopy. J. Electron Microsc. 1992, 41, 46-52.
25. Eichele, K.; Wasylishen, R. E. Herzfeld-Berger Analysis, 1.5.8; Dalhousie University and Universität Tübingen, 2006.
26. Dennington, R., II.; Keith, T.; Millam, J.; Eppinnett, K.; Hovell, W. L.; Gilliland, R. GaussView, 3.09, Semichem, Inc., 2003.
27. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Montgomery, J., J. A.; Vreven, T.; Kudin, K. N.; Burant, J. C.; Millam, J. M.; Iyengar, S. S.; Tomasi, J.; Barone, V.; Mennucci, B.; Cossi, M.; Scalmani, G.; Rega, N.; Petersson, G. A.; Nakatsuji, H.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Klene, M.; Li, X.; Knox, J. E.; Hratchian, H. P.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Ayala, P. Y.; Morokuma, K.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Zakrzewski, V. G.; Dapprich, S.; Daniels, A. D.; Strain, M. C.; Farkas, O.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Ortiz, J. V.; Cui, Q.; Baboul, A. G.; Clifford, S.; Cioslowski, J.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Gonzalez, C.; Pople, J. A. Gaussian 03, Revision C.02; Gaussian, Inc., 2004.
28. Baerends, E. J.; Autschbach, J.; Bérces, A.; Bickelhaupt, F. M.; Bo, C.; Boerrigter, P. M.; Cavallo, L.; Chong, D. P.; Deng, L.; Dickson, R. M.; Ellis, D. E.; Faassen, M. v.; Fan, L.; Fischer, T. H.; Guerra, C. F.; Gisbergen, S. J. A. v.; Götz, A. W.; Groeneveld, J. A.; Gritsenko, O. V.; Grüning, M.; Harris, F. E.; Hoek, P. v. d.; Jacob, C. R.; Jacobsen, H.; Jensen, L.; Kessel, G. v.; Kootstra, F.; Krykunov, M. V.; Lenthe, E. v.; McCormack, D. A.; Michalak, A.; Neugebauer, J.; Nicu, V. P.; Osinga, V. P.; Patchkovskii, S.; Philipsen, P. H. T.; Post, D.; Pye, C. C.; Ravenek, W.; Rodriguez, J. I.; Ros, P.; Schipper, P. R. T.; Schreckenbach, G.; Snijders, J. G.; Solà, M.; Swart, M.; Swerhone, D.; Velde, G. t.; Vernooijs, P.; Versluis, L.; Visscher, L.; Visser, O.; Wang, F.; Wesolowski, T. A.; Wezenbeek, E. M. v.; Wiesenekker, G.; Wolff, S. K.; Woo, T. K.; Yakovlev, A. L.; Ziegler, T. Amsterdam Density Functional, 2008.01; SCM, Theoretical Chemistry, Vrije Universiteit, 2008.
29. te Velde, G.; Bickelhaupt, F. M.; van Gisbergen, S. J. A.; Fonseca Guerra, C.; Baerends, E. J.; Snijders, J. G.; Ziegler, T. Chemistry with ADF. J. Comput. Chem. 2001, 22, 931-67.
30. Fry, R. A.; Kwon, K. D.; Komarneni, S.; Kubicki, J. D.; Mueller, K. T. Solid-state NMR and computational chemistry study of mononucleotides adsorbed to alumina. Langmuir 2006, 22, 9281-6.
31. Lee, C.; Yang, W.; Parr, R. G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys. Rev. B 1988, 37, 785-9.
32. Dudev, T.; Cowan, J. A.; Lim, C. Competitive binding in magnesium coordination chemistry: Water versus ligands of biological interest. J. Am. Chem. Soc. 1999, 121, 7665-73.
33. Dudev, T.; Lim, C. Metal selectivity in metalloproteins: Zn2+ vs Mg2+. J. Phys. Chem. B 2001, 105, 4446-52.
34. Haeberlen, U. Advances in Magnetic Resonance; Academic Press: New York, 1976.
35. Mehring, M. Principles of High Resolution NMR in Solids, 2nd ed.; Springer Verlag: Berlin, 1983.
36. Spevacek, J.; Brus, J. Solid-state NMR study of intercalate complexes of poly(ethylene oxide) and small molecules. Macromol. Symp. 2003, 203, 111-21.
37. Spevacek, J.; Dybal, J. Polymer electrolyte poly(ethylene oxide)/ LiCF3SO3 studied by solid-state 13C NMR spectroscopy and ab initio calculations. Macromol. Rapid Commun. 1999, 20, 435-9.
38. Alam, T. M. Ab initio calculations of 31P NMR chemical shielding anisotropy tensors in phosphates: variations due to ring formation. Int. J. Mol. Sci. 2002, 3, 888-906.
39. Alam, T. M. Ab Initio Calculations of 31P NMR Chemical Shielding Anisotropy Tensors in Phospates: The Effect of Geometry on Shielding. In Modeling NMR Chemical Shifts; Facelli, J. C., Dios, A. C. d., Eds.; American Chemical Society: Washington, DC, 1999; pp 320-34.
40. Yoshikawa, K.; Shinohara, Y.; Terada, H.; Kato, S. Why is magnesium necessary for specific cleavage of the terminal phosphoryl group of ATP. Biophys. Chem. 1987, 27, 251-4.
41. Liebmann, P.; Loew, G.; McLean, A. D.; Pack, G. R. Ab initio SCF studies of interactions of lithium(+), sodium(+), beryllium(2+), and magnesium(2+) ions with dihydrogen phosphate(-) ion: model for cation binding to nucleic acids. J. Am. Chem. Soc. 1982, 104, 691-7.
42. Marynick, D. S.; Schaefer, H. F., III. Theoretical studies of metalphosphate interactions. Interaction of lithium(1+), sodium(1+), potassium( 1+), beryllium(2+), magnesium(2+), and calcium(2+) with dihydrogen phosphate (H2PO4-) and dimethyl phosphate ((CH3O)2PO2-). Implications for nucleic acid solvation. Proc. Natl. Acad. Sci. U.S.A. 1975, 72, 3794-8.
43. Petrov, A. S.; Funseth-Smotzer, J.; Pack, G. R. Computational study of dimethyl phosphate anion and its complexes with water, magnesium, and calcium. Int. J. Quantum Chem. 2005, 102, 645-55.
44. Schneider, B.; Kabelae, M.; Hobza, P. Geometry of the phosphate group and its interactions with metal cations in crystals and ab initio calculations. J. Am. Chem. Soc. 1996, 118, 12207-17.
45. Herzfeld, J.; Berger, A. E. Sideband intensities in NMR spectra of samples spinning at the magic angle. J. Chem. Phys. 1980, 73, 6021-30.
46. Hodgkinson, P.; Elmsley, L. The reliability of the determination of tensor parameters by solid-state nuclear magnetic resonance. J. Chem. Phys. 1997, 107, 4808-16.
47. Heckels, J. E.; Lambert, P. A.; Baddiley, J. Binding of magnesium ions to cell walls of Bacillus subtilis W23 containing teichoic acid or teichuronic acid. Biochem. J. 1977, 162, 359-65.
48. Doyle, R. J.; Matthews, T. H.; Streips, U. N. J. Chemical basis for selectivity of metal ions by the Bacillus subtilis cell wall. J. Bacteriol. 1980, 143, 471-80.