Synthesis, structure, and molecular dynamics of gallium complexes of schizokinen and the amphiphilic siderophore acinetoferrin

Journal of the American Chemical Society

Volumn 126, Issue 38, 2004, Pages 12065-12075

  Fadeev, Evgeny A ^a   Luo, Minkui ^a   Groves, John T ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROPHILICITY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARAMETER ESTIMATION; STRUCTURE (COMPOSITION); SYNTHESIS (CHEMICAL);

ACTIVATION PARAMETERS; GALLIUM COMPLEXES; PHOSPHOLIPID VESICLES; SCHIZOKINEN (SZ);

GALLIUM COMPOUNDS;

ACINETOFERRIN; CITRIC ACID; COORDINATION COMPOUND; DIAMINOPROPANE; GALLIUM; GALLIUM SCHIZOKINEN; HYDROXAMIC ACID; METAL DERIVATIVE; PHOSPHOLIPID; PROPANE; SIDEROPHORE; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ARTICLE; CHELATION; CHEMICAL STRUCTURE; DISSOCIATION CONSTANT; GEOMETRY; HARTREE FOCK CALCULATION; HYDROGEN BOND; HYDROPHILICITY; METAL BINDING; MOLECULAR DYNAMICS; MOLECULAR MODEL; PARTITION COEFFICIENT; PHOSPHOLIPID VESICLE; PROTON NUCLEAR MAGNETIC RESONANCE; RACEMIC MIXTURE; STRUCTURE ANALYSIS; SYNTHESIS;

ACINETOBACTER; CITRATES; GALLIUM; HYDROXAMIC ACIDS; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; ORGANOMETALLIC COMPOUNDS; SIDEROPHORES; STEREOISOMERISM;

EID: 4644329090     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja048145j     Document Type: Article

References (88)

1. Albrecht-Gary, A. M.; Crumbliss, A. L. Met. Ions Biol. Syst. 1998, 35, 239-327.
2. Boukhalfa, H.; Crumbliss, A. L. Biometals 2002, 15, 325-339.
3. Neilands, J. B. J. Biol. Chem. 1995, 270, 26723-26726.
4. Fong, K. P.; Gao, L.; Demuth, D. R. Infect. Immun. 2003, 71, 298-308.
5. Zhu, J.; Dizin, E.; Hu, X.; Wavreille, A.; Park, J.; Pei, D. Biochemistry 2003, 42, 4717-4726.
6. Bollinger, N.; Hasset, D. J.; Iglewski, B. H.; Costerton, J. W.; McDermott, T. R. J. Bacteriol. 2001, 183, 1990-1996.
7. Groves, J. T. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 3569-3574.
8. Lane, S. J.; Marshall, P. S.; Upton, R. J.; Ratledge, C. Biometals 1998, 11, 13-20.
9. Okujo, N.; Sakakibara, Y.; Yoshida, T.; Yamamoto, S. Biometals 1994, 7, 170-176.
10. Snow, G. A. Biochem. J. 1965, 97, 166-175.
11. Snow, G. A. Biochem. J. 1965, 94, 160-165.
12. Persmark, M.; Pittman, P.; Buyer, J. S.; Schwyn, B.; Gill, P. R.; Neilands, J. B. J. Am. Chem. Soc. 1993, 115, 3950-3956.
13. Macrellis, H. M.; Trick, C. G.; Rue, E. L.; Smith, G.; Bruland, K. W. Mar. Chem. 2001, 76, 175-187.
14. Butler, A.; Martinez, J. S.; Barbeau, K. J. Inorg. Biochem. 2001, 86, 30-30.
15. Martinez, J. S.; Zhang, G. P.; Holt, P. D.; Jung, H. T.; Carrano, C. J.; Haygood, M. G.; Butler, A. Science 2000, 287, 1245-1247.
16. Rosenthal, E. A.; Bohlmeyer, T. J.; Monnet, E.; MacPhail, C.; Robertson, A. D.; Horwitz, M. A.; Burchenal, J. E. B.; Horwitz, L. D. Circulation 2001, 104, 2222-2227.
17. Pahl, P. M. B.; Horwitz, M. A.; Horwitz, K. B.; Horwitz, L. D. Breast Cancer Res. Treat. 2001, 69, 69-79.
18. Horwitz, L. D.; Sherman, N. A.; Kong, Y. N.; Pike, A. W.; Gobin, J.; Fennessey, P. V.; Horwitz, M. A. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 5263-5268.
19. Lytton, S. D.; Cabantchik, Z. I.; Libman, J.; Shanzer, A. Mol. Pharmacol. 1991, 40, 584-590.
20. Harpstrite, S. E.; Beatty, A. A.; Collins, S. D.; Oksman, A.; Goldberg, D. E.; Sharma, V. Inorg. Chem. 2003, 42, 2294-2300.
21. Lin, Y. M.; Miller, M. J.; Mollmann, U. Biometals 2001, 14, 153-157.
22. Murray, A. P.; Miller, M. J. J. Org. Chem. 2003, 68, 191-194.
23. Xu, G. F.; Martinez, J. S.; Groves, J. T.; Butler, A. J. Am. Chem. Soc. 2002, 124, 13408-13415.
24. Lahiri, J.; Fate, G. D.; Ungashe, S. B.; Groves, J. T. J. Am. Chem. Soc. 1996, 118, 2347-2358.
25. Groves, J. T.; Fate, G. D.; Lahiri, J. J. Am. Chem. Soc. 1994, 116, 5477-5478.
26. Groves, J. T.; Neumann, R. J. Am. Chem. Soc. 1989, 111, 2900-2909.
27. Groves, J. T.; Neumann, R. J. Am. Chem. Soc. 1987, 709, 5045-5047.
28. Rudant, E.; Courvalin, P.; Lambert, T. Antimicrob. Agents Chemother. 1997, 41, 2646-2651.
29. Yamamoto, S.; Okujo, N.; Sakakibara, Y. Arch. Microbiol. 1994, 162, 249-254.
30. Dorsey, C. W.; Tolmasky, M. E.; Crosa, J. H.; Actis, L. A. Microbiology 2003, 149, 1227-1238.
31. Gibson, F.; Magrath, D. I. Biochim. Biophys. Acta 1969, 792, 175-184.
32. Schafft, M.; Diekmann, H. Arch. Microbiol. 1978, 117, 203-207.
33. Kunze, B.; Trowitzschkienast, W.; Hofle, G.; Reichenbach, H. J. Antibiot. 1992, 45, 147-150.
34. Barbeau, K.; Zhang, G.; Live, D. H.; Butler, A. J. Am. Chem. Soc. 2002, 124, 378-379.
35. Bergeron, R. J.; Huang, G. F.; Smith, R. E.; Bharti, N.; McManis, J. S.; Butler, A. Tetrahedron 2003, 59, 2007-2014.
36. Gardner, R. A.; Kinkade, R.; Wang, C. J.; Phanstiel, O. J. Org. Chem. 2004, 69, 3530-3537.
37. Akers, H. A. Appl. Environ. Microbiol. 1983, 45, 1704-1706.
38. Simpson, F. B.; Neilands, J. B. J. Phycol. 1976, 12, 44-48.
39. Trick, C. G.; Kerry, A. Curr. Microbiol. 1992, 24, 241-245.
40. Plowman, J. E.; Loehr, T. M.; Goldman, S. J.; Sanders-Loehr, J. J. Inorg. Biochem. 1984, 20, 183-197.
41. Harris, W. R.; Carrano, C. J.; Raymond, K. N. J. Am. Chem. Soc. 1979, 101, 2722-2727.
42. Milewska, M. J.; Chimiak, A.; Glowacky, Z. J. Prakt. Chem./Chem.-Ztg. 1987, 329, 447-456.
43. Wang, Q. X.; Phanstiel, O. I. J. Org. Chem. 1998, 63, 1491-1495.
44. Perrin, C. L.; Dwyer, T. J. Chem. Rev. 1989, 90, 935-967.
45. Stott, K.; Keeler, J.; Van, Q. N.; Shaka, A. J. J. Magn. Reson. 1997, 725, 302-324.
46. Becker, E. Hydrogen bonding. In Encyclopedia of Nuclear Magnetic Resonance; John Wiley: New York, 1996; Vol. 4, p 4212.
47. The four-symbol combinations (αααα, αααβ, αγβα, etc.) were used to define the various ring-pucker conformations of GaSz. The label characters reflect orientations of the four groups labeled as i-iv in Figure S25b: left-hand side methylene (i), left-hand side carbonyl (ii), right-hand side carbonyl (iii), and right-hand side methylene (iv) groups, in that order. An additional amide group conformation, "γ", was introduced after we obtained the optimized structures. In that conformation the amide proton was hydrogen-bonded to the uncoordinated citrate central carboxyl oxygen, instead of one of the metal-bound oxygen atoms, as it was in all "αa" and "β" conformations.
48. Keys, A.; Barbarich, T. J.; Bott, S. G.; Barren, A. R. J. Chem. Soc., Dalton Trans. 2000w, 577-588.
49. Beissel, T.; Powers, R. E.; Raymond, K. N. Angew. Chem., Int. Ed. Engl. 1996, 35, 1084-1086.
50. Dietrich, A.; Fidelis, K. A.; Powell, D. R.; Vanderhelm, D.; Engwilmot, D. L. J. Chem. Soc., Dalton Trans. 1991, 231-239.
51. Borgias, B. A.; Barclay, S. J.; Raymond, K. N. J. Coord. Chem. 1986, 15, 109-123.
52. Dhungana, S.; White, P. S.; Crumbliss, A. L. J. Am. Chem. Soc. 2003, 125, 14760-14767.
53. The relative GaSz conformation energies were almost the same when calculated with RHF/6-31G(d)//RHF/6-31G(d), RHF/6-31G(d)//B3LYP/6-31G(d), and B3LYP/6-31G(d)//B3LYP/6-31G(d) method combinations for the geometry optimization and the single point energy calculation
54. Onsager, L. J. Am. Chem. Soc. 1936, 58, 1486-1493.
55. Wong, M. W.; Frisch, M. J.; Wiberg, K. B. J. Am. Chem. Soc. 1991, 113, 4776-4782.
56. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Zakrzewski, V. G.; Montgomery, J. J. A.; Stratmann, R. E.; Burant, J. C.; Dapprich, S.; Millam, J. M.; Daniels, A. D.; Kudin, K. N.; Strain, M. C.; Farkas, O.; Tomasi, J.; Barone, V.; Cossi, M.; Cammi, R.; Mennucci, B.; Pomelli, C.; Adamo, C.; Clifford, S.; Ochterski, J.; Petersson, G. A.; Ayala, P. Y.; Cui, Q.; Morokuma, K.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.; Foresman, J. B.; Cioslowski, J.; Ortiz, J. V.; Baboul, A. G.; Stefanov, B. B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Gomperts, R.; Martin, R. L.; Fox, D. J.; Keith, T.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara, A.; Gonzalez, C.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen, W.; Wong, M. W.; Andres, J. L.; Gonzalez, C.; Head-Gordon, M.; Replogle, E. S.; Pople, J. A. Gaussian 98, version A.7; Gaussian, Inc.: Pittsburgh, PA, 1998.
57. Haasnoot, C. A. G.; Deleeuw, F.; Altona, C. Tetrahedron 1980, 36, 2783-2792.
58. Demarco, A.; Llinas, M.; Wuthrich, K. Biopolymers 1978, 17, 637-650.
59. Gavrilov, Y. D.; Solkan, V. N.; Bystrov, V. F. Bull. Acad. Sci. USSR Div. Chem. Sci. 1975, 24, 2368-2373.
60. Aubry, A.; Giessner, C.; Cung, M. T.; Marraud, M.; Neel, J. Biopolymers 1974, 13, 523-536.
61. Ramachandran, G. N.; Chandrasekaran, R.; Kopple, K. D. Biopolymers 1971, 10, 2113-2131.
62. 1H NMR resonances were the only signals not reliably assigned to a particular conformation, but it is likely that the ab-quartet centered at δ 2.45 belongs to the conformationally restrained chain I, and the singlet at d 2.55 to the more flexible and equilibrating chain II.
63. Brumaghim, J. L.; Raymond, K. N. J. Am. Chem. Soc. 2003, 125, 12066-12067.
64. Karpishin, T. B.; Stack, T. D. P.; Raymond, K. N. J. Am. Chem. Soc. 1993, 115, 6115-6125.
65. Kersting, B.; Telford, J. R.; Meyer, M.; Raymond, K. N. J. Am. Chem. Soc. 1996, 118, 5712-5721.
66. Kersting, B.; Meyer, M.; Powers, R. E.; Raymond, K. N. J. Am. Chem. Soc. 1996, 118, 7221-7222.
67. Matsumoto, K.; Ozawa, T.; Jitsukawa, K.; Einaga, H.; Masuda, H. Inorg. Chem. 2001, 40, 190-191.
68. Tor, Y.; Libman, J.; Shanzer, A.; Felder, C. E.; Lifson, S. J. Am. Chem. Soc. 1992, 114, 6661-6671.
69. Casanova, D.; Cirera, J.; Llunell, M.; Alemany, P.; Avnir, D.; Alvarez, S. J. Am. Chem. Soc. 2004, 126, 1755-1763.
70. Montgomery, C. D.; Shorrock, C. J. Inorg. Chim. Acta 2002, 328, 259-262.
71. It is clear that the analogue of the Bailar twist mechanism (Figure S27 a and b), if it is not preceded by dissociation of at least one chelating group, cannot be operative in the GaSz epimerization. Such a process requires rotation of all the chelating groups in the same direction, thus minimizing the unfavorable nonbonding interactions in the transition state. Such a process, if applied to the GaSz, would lead to an unstable trans-trans isomer (Figure S27 b). Thus, a nondissociative epimerization of GaSz would require a more complex and energetically prohibitive pathway.
72. Raymond, K. N.; Dertz, E. A.; Kim, S. S. Proc. Natl. Acad. Sci. U.S.A. 2003, 700, 3584-3588.
73. Gromova, M.; Jarjayes, O.; Hamman, S.; Nardin, R.; Beguin, C.; Willem, R. Eur. J. Inorg. Chem. 2000, 545-550.
74. Hutchison, J. R.; Gordon, J. G.; Holm, R. H. Inorg. Chem. 1971, 10, 1004-1017.
75. 2O, to the distal part of the molecule further stabilizing the transition state compared to the nondissociative mechanism.
76. Hawkes, G. E.; O'Brien, P.; Salacinski, H.; Motevalli, M.; Abrahams, I. Eur. J. Inorg. Chem. 2001, 1005-1011.
77. Matzapetakis, M.; Raptopoulou, C. P.; Tsohos, A.; Papaefthymiou, V.; Moon, N.; Salifoglou, A. J. Am. Chem. Soc. 1998, 120, 13266-13267.
78. Cohen, S. M.; Petoud, S.; Raymond, K. N. Inorg. Chem. 1999, 38, 4522-4529.
79. Wasielewski, E.; Atkinson, R. A.; Abdallah, M. A.; Kieffer, B. Biochemistry 2002, 41, 12488-12497.
80. Atkinson, A. R.; Din, A. L. M. S.; Keiffer, B.; Lefevre, J.-F.; Abdallah, M. A. Biochemistry 1998, 37, 15965-15973.
81. Stephan, H.; Freund, S.; Meyer, J. M.; Winkelmann, G.; Jung, G. Liebigs Ann. Chem. 1995, 43-48.
82. Our preliminary results show rapid paramagnetic NMR line broadening of DMPC choline methyl groups on the interior surface of the DMPC small unilamellar vesicles upon mixing with FeAf solution. This indicates that FeAf is capable of rapidly diffusing across the lipid layers. A further account of these phenomena will be reported elsewhere.
83. Smallcombe, S. H.; Patt, S. L.; Keifer, P. A. J. Magn. Reson., Ser. A 1995, 117, 295-303.
84. Glasoe, P. K.; Long, F. A. J. Phys. Chem. 1960, 64, 188-190.
85. Becke, A. D. Phys. Rev. A 1988, 38, 3098-3100.
86. Lee, C. T.; Yang, W. T.; Parr, R. G. Phys. Rev. B 1988, 37, 785-789.
87. Vosko, S. H.; Wilk, L.; Nusair, M. Can. J. Phys. 1980, 58, 1200-1211.
88. Koradi, R.; Billeter, M.; Wuthrich, K. J. Mol. Graphics 1996, 14, 51-55.