Thermodynamic and kinetic stability of synthetic multifunctional rigid-rod β-barrel pores: Evidence for supramolecular catalysis

Journal of the American Chemical Society

Volumn 126, Issue 32, 2004, Pages 10067-10075

  Litvinchuk, Svetlana ^a   Bollot, Guillaume ^a   Mareda, Jiri ^a   Som, Abhigyan ^a   Ronan, Dawn ^a   Shah, Muhammad Raza ^a,b   Perrottet, Philippe ^a   Sakai, Naomi ^a   Matile, Stefan ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF KARACHI   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; CONCENTRATION (PROCESS); MATHEMATICAL MODELS; MONOMERS; THERMODYNAMIC STABILITY;

ESTEROLYSIS; KINETIC STABILITY; PLANARS BILAYERS;

SUPRAMOLECULAR CHEMISTRY;

1,3,6 PYRENETRISULFONATE; 4 OCTIPHENYL; 8 ACETOXY 1,3,6 PYRENETRISULFONATE; ADENOSINE TRIPHOSPHATE; ION CHANNEL; MONOMER; PHENYL GROUP; POLYGLUTAMIC ACID; PYRANINE; PYRENE DERIVATIVE; TETRAMER; UNCLASSIFIED DRUG;

ADAPTATION; ARTICLE; BETA SHEET; BILAYER MEMBRANE; CATALYSIS; CHEMICAL STRUCTURE; ESTEROLYSIS; HILL REACTION; KINETICS; MOLECULAR MECHANICS; MOLECULAR MODEL; NONLINEAR SYSTEM; PLANAR BILAYER; SATURATION KINETICS; SPHERICAL BILAYER; STRUCTURE ANALYSIS; SUPRAMOLECULAR CHEMISTRY; SYNTHESIS; THERMODYNAMICS;

ARGININE; BACTERIAL TOXINS; HISTIDINE; HYDROPHOBICITY; ION CHANNELS; KINETICS; LEUCINE; LIPID BILAYERS; MODELS, MOLECULAR; OLIGOPEPTIDES; PROTEIN STRUCTURE, SECONDARY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; THERMODYNAMICS;

EID: 4043107662     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja0481878     Document Type: Article

References (143)

1. Recent/pertinent reviews/accounts on synthetic ion channels and pores (see also refs 3-6): (a) Koert, U.; Ed. Synthetic Ion Channels. Bioorg. Med. Chem. 2004, 12, 1277-1350.
2. (b) Gokel, G. W.; Schlesinger, P. H.; Djedovi, N. K.; Ferdani, R.; Harder, E. C.; Hu, J.; Leevy, W. M.; Pajewska, J.; Pajewski, R.; Weber, M. E. Bioorg. Med. Chem. 2004, 12, 1291-1304.
3. (c) Biron, E.; Otis, F.; Meillon, J.-C.; Robitaille, M.; Lamothe, J.; Van Hove, P.; Cormier, M.-E.; Voyer, N. Bioorg. Med. Chem. 2004, 12, 1279-1290.
4. (d) Smith, B. D.; Lambert, T. N. Chem. Commun. 2003, 2261-2268.
5. (e) Guo, X.; Szoka, F. C. Acc. Chem. Res. 2003, 36, 335-341.
6. (f) Koert, U.; Reiss, P. J. Supramol. Chem. 2003, 2, 29-37.
7. (g) Boon, J. M.; Smith, B. D. Curr. Opin. Chem. Biol. 2002, 6, 749-756.
8. (h) Savage, P. B.; Li, C.; Taotafa, U.; Ding, B.; Guan, Q. FEBS Microbiol. Lett. 2002, 217, 1-7.
9. (i) Gokel, G. W.; Mukhopadhyay, A. Chem. Soc. Rev. 2001, 30, 274-286.
10. (j) Gokel, G. W. Chem. Eur. J. 2001, 7, 33-39.
11. (k) Matile, S. Chem. Rec. 2001, 1, 162-172.
12. (l) Cheng, R. P.; Gellman, S. H.; DeGrado, W. F. Chem. Rev. 2001, 101, 3219-3232.
13. (m) Shum, P.; Kim, J.-M.; Thompson, D. H. Adv. Drug Delivery Rev. 2001, 53, 273-284.
14. (n) Ranganathan, D. Acc. Chem. Res. 2001, 34, 919-930.
15. (o) Bong, D. T.; Clark, T. D.; Granja, J. R.; Ghadiri, M. R. Angew. Chem., Int. Ed. 2001, 40, 988-1011.
16. (p) Sakai, N.; Matile, S. Chem. Eur. J. 2000, 6, 1731-1737.
17. (q) Kirkovits, G. J.; Hall, C. D. Adv. Supramol. Chem. 2000, 7, 1-47.
18. (r) Scrimin, P.; Tecilla, P. Curr. Opin. Chem. Biol. 1999, 3, 730-735.
19. (s) Fyles, T. M. Curr. Opin. Chem. Biol. 1997, 1, 497-505.
20. (t) Kobuke, Y. Adv. Supramol. Chem. 1997, 4, 163-210.
21. (u) Koert, U. Chem. Unserer Z. 1997, 31, 20-26.
22. (v) Gokel, G. W.; Murillo, O. Acc. Chem. Res. 1996, 29, 425-432.
23. (w) Fyles, T. M.; van Straaten-Nijenhuis, W. F. In Comprehensive Supramolecular Chemistry; Reinhoudt, N. D., Ed.; Elsevier: Oxford, 1996; Vol. 10, pp 53-77.
24. (x) Voyer, N. Top. Curr. Chem. 1996, 184, 1-37.
25. (y) Fuhrhop, J.-H.; Köning, J. Membranes and Molecular Assemblies: The Synkinetic Approach; The Royal Society of Chemistry: Cambridge, UK, 1994.
26. (z) Nolte, R. J. M. Chem. Soc. Rev. 1994, 23, 11-19.
27. Recent publications on synthetic ion channels and pores (see also refs 4-6, 9-12, and 14-26): (a) Pérez-Hernández, N.; Pérez, C.; Rodríguez, M. L.; Foces-Foces, C.; Tolstoy, P. M.; Limbach, H. H.; Morales, E. Q.; Pérez, R.; Martín, J. D. Bioorg. Med. Chem. 2004, 12, 1305-1314.
28. (b) Hall, A. C.; Suarez, C.; Hom-Choudhury, A.; Manu, A. N. A.; Hall, C. D.; Kirkovits, G. J.; Ghiriviga, I. Org. Biomol. Chem. 2003, 1, 2973-2982.
29. (c) Fidzinski, P.; Knoll, A.; Rosenthal, R.; Schrey, A.; Vescovi, A.; Koert, U.; Wiederholt, M.; Strauss, O. Chem. Biol. 2003, 10, 35-43.
30. (d) Vescovi, A.; Knoll, A.; Koert, U. Org. Biomol. Chem. 2003, 1, 2983-2997.
31. (e) Eggers, P. K.; Fyles, T. M.; Mitchell, K. D. D.; Sutherland, T. J. Org. Chem. 2003, 68, 1050-1058.
32. (f) Cameron, L. M.; Fyles, T. M.; Hu, C. J. Org. Chem. 2002, 67, 1548-1553.
33. (g) De Riccardis, F.; Di Philippo, M.; Garrisi, D.; Izzo, I.; Mancin, F.; Pasquato, L.; Scrimin, P.; Tecilla, P. Chem. Commun. 2002, 3066-3067.
34. (h) Avallone, E.; Izzo, I.; Vuolo, G.; Costabile, M.; Garrisi, D.; Pasquato, L.; Scrimin, P.; Tecilla, P.; De Riccardis, F. Tetrahedron Lett. 2003, 44, 6121-6124.
35. (i) Arnt, L.; Tew, G. N. Langmuir 2003, 19, 2404-2408.
36. (j) Zhang, J.; Jing, B.; Regen, S. L. J. Am. Chem. Soc. 2003, 125, 13984-13987.
37. (k) Murthy, N.; Campbell, J.; Fausto, N.; Hoffman, A. S.; Stayton, P. S. Bioconjugate Chem. 2003, 14, 412-419.
38. (l) Murthy, N.; Campbell, J.; Fausto, N.; Hoffman, A. S.; Stayton, P. S. J. Controlled Release 2003, 89, 365-374.
39. (m) Sisson, A. D.; Clare, J. P.; Taylor, L. H.; Charmant, J. P. H.; Davis, A. P. Chem. Commum. 2003, 2246-2247.
40. (n) Epand, R. F.;: Umezawa, N.; Porter, E. A.; Gellman, S. H.; Epand, R. M. Eur. J. Biochem. 2003, 270, 1240-1248.
41. (o) Arvidsson, P. I.; Ryder, N. S.; Weiss, H. M.; Gross, G.; Kretz, O.; Woessner, R.; Seebach, D. ChemBioChem 2003, 4, 1345-1347.
42. (p) Koulov, A. V.; Lambert, T. N.; Shukla, R.; Jain, M.; Boon, J. M.; Smith, B. D.; Li, H.; Sheppard, D. N.; Joos, J.-B.; Clare, J. P.; Davis, A. P. Angew. Chem., Int. Ed. 2003, 42, 4931-4933.
43. (q) Schlesinger, P. H.; Djedovic, N. K.; Ferdani, R.; Pajewska, J.; Pajewski, R.; Gokel, G. W. Chem. Commun. 2003, 308-309.
44. (r) Djedovic, N.; Ferdani, R.; Harder, E.; Pajewska, J.; Pajewski, R.; Schlesinger, P. H.; Gokel, G. W. Chem. Commun. 2003, 2862-2863.
45. (s) Schlesinger, P. H.; Ferdani, R.; Pajewska, J.; Pajewski, R.; Gokel, G. W. New J. Chem. 2003, 26, 60-67.
46. (t) Guo, X.; MacKay, J. A.; Szoka, F. C. Biophys. J. 2003, 84, 1784-1795.
47. (u) Sidorov, V.; Kotch, F. W.; Kuebler, J. L.; Lam, Y.-F.; Davis, J. T. J. Am. Chem. Soc. 2003, 125, 2840-2841.
48. (v) Boon, J. M.; Lambert, T. N.; Sisson, A. L.; Davis, A. P.; Smith, B. D. J. Am. Chem. Soc. 2003, 125, 8195-8201.
49. (w) Sidorov, V.; Kotch, F. W.; Abdrakhmanova, G.; Mizani, R.; Fettinger, J. C.; Davis, J. T. J. Am. Chem. Soc. 2002, 124, 2267-2278.
50. (x) Sanchez-Quesada, J.; Isler, M. P.; Ghadiri, M. R. J. Am. Chem. Soc. 2002, 124, 10004-10005.
51. (y) Schlesinger, P. H.; Ferdani, R.; Liu, J.; Pajewska, J.; Pajewski, R.; Saito, M.; Shabany, H.; Gokel, G. W. J. Am. Chem. Soc. 2002, 124, 1848-1849.
52. (z) Schlesinger, P. H.; Ferdani, R.; Pajewski, R.; Pajewska, J.; Gokel, G. W. Chem. Commun. 2002, 840-841.
53. (aa) Lambert, T. N.; Boon, J. M.; Smith, B. D.; Pérez-Payan, M. N.; Davis, A. P. J. Am. Chem. Soc. 2002, 124, 5276-5277.
54. (bb) Porter, E. A.; Weisblum, B.; Gellman, S. H. J. Am. Chem. Soc. 2002, 124, 7324-7330.
55. (cc) Asokan, A.; Cho, M. J. J. Pharm. Sci. 2002, 91, 903-913.
56. (dd) Tew, G. N.; Liu, D.; Chen, B.; Doerksen, R. J.; Kaplan, J.; Carroll, P. J.; Klein, M. L.; DeGrado, W. F. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 5110-5114.
57. (ee) Arnt, L.; Tew, G. N. J. Am. Chem. Soc. 2002, 124, 7664-7665.
58. (ff) Bandyopadhyay, P.; Bandyopadhyay, P.; Regen, S. L. J. Am. Chem. Soc. 2002, 124, 11254-11255.
59. (gg) Habaue, S.; Morita, M.; Okamoto, Y. Macromolecules 2002, 35, 2432-2434.
60. (hh) Habaue, S.; Morita, M.; Okamoto, Y. Polymer 2002, 43, 3469-3474.
61. (ii) Leevy, W. M.; Donato, G. M.; Ferdani, R.; Goldman, W. E.; Schlesinger, P. H.; Gokel, G. W. J. Am. Chem. Soc. 2002, 124, 9022-9023.
62. (jj) Vandenburg, Y. R.; Smith, B. D.; Biron, E.; Voyer, N. Chem. Commun. 2002, 1694-1695.
63. (kk) Bandyopadhyay, P.; Bandyopadhyay, P.; Regen, S. L. Bioconjugate Chem. 2002, 13, 1314-1318.
64. (ll) Raguse, T. L.; Porter, E. A.; Weisblum, B.; Gellman, S. H. J. Am. Chem. Soc. 2002, 124, 12774-12785.
65. (mm) Shankaramma, S. C.; Athanassiou, Z.; Zerbe, O.; Moehle, K.; Mouton, C.; Bernardini, F.; Vrijbloed, J. W.; Obrecht, D.; Robinson, J. A. ChemBioChem 2002, 3, 1126-1133.
66. (nn) Ranganathan, D.; Samant, M. P.; Nagaraj, R.; Bikshapathy, E. Tetrahedron Lett. 2002, 43, 5145-5147.
67. (oo) Sanderson, J. M.; Yazdani, S. Chem. Commun. 2002, 1154-1155.
68. Reviews of synthetic multifunctional pores: (a) Sakai, N.; Matile, S. Chem. Commun. 2003, 2514-2523.
69. (b) Matile, S. Chem. Soc. Rev. 2001, 30, 158-167.
70. The term "pore" is used for systems that transport organic molecules, whereas the term "ion channel" used for inorganics (all pores are channels, but not all channels are pores).
71. The term "synthetic ion channels and pores" is used for compounds that have abiotic scaffolds (i.e., scaffolds that are not found in biological ion channels and pores) and act in lipid bilayer membranes. This optional definition does not consider ion channels and pores derived from biological peptide scaffolds [(a) Woolley, G. A.; Loughead, T. Curr. Opin. Chem. Biol. 2003, 7, 710-714.
72. (b) Futaki, S.; Zhang, Y.; Kiwada, T.; Nakase, I.; Yagami, T.; Oiki, S.; Sugiura, Y. Bioorg. Med. Chem. 2004, 12, 1337-1342.
73. (c) Lougheed, T.; Zhang, Z.; Woolley, G. A.; Borisenko, V. Bioorg. Med. Chem. 2004, 12, 1343-1350.
74. (d) Scrimin, P.; Tecilla, P.; Tonellato, U.; Veronese, A.; Crisma, M.; Formaggio, F.; Toniolo, C. Chem. Eur. J. 2002, 8, 2753-2763.
75. (e) Broughman, J. R.; Shank, L. P.; Takeguchi, W.; Schultz, B. D.; Iwamoto, T.; Mitchell, K. E.; Tomich, J. M. Biochemistry 2002, 41, 7350-7358.
76. (f) Futaki, S.; Fukuda, M.; Omote, M.; Yamauchi, K.; Yagami, T.; Niwa, M.; Sugiura, Y. J. Am. Chem. Soc. 2001, 123, 12127-12134.
77. (g) Terrettaz, S.; Ulrich, W.-P.; Guerrini, R.; Verdini, A.; Vogel, H. Angew. Chem., Int. Ed. 2001, 40, 1740-1743.
78. (h) Monoi, H.; Futaki, S.; Kugimiya, S.; Minakata, S.; Yoshihara, K. Biophys. J. 2000, 78, 2892-2899.
79. (i) Lear, J. D.; Schneider, J. P.; Kienker, P. K.; DeGrado, W. F. J. Am. Chem. Soc. 1997, 119, 3212-3217.
80. (j) Oiki, S.; Koeppe II, R. E.; Anderson, O. S. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 2121-2125.
81. (k) Grove, A.; Mutter, M.; Rivier, J. E.; Montal, M. J. Am. Chem. Soc. 1993, 115, 5919-5924.
82. (l) Parente, R. A.; Nir, S.; Szoka, F. C. Biochemistry 1990, 29, 8720-8728.
83. (m) Läuger, P. Angew. Chem., Int. Ed. Engl. 1985, 24, 905-923], polyester scaffolds
84. [(n) Das, S.; Seebach, D.; Reusch, R. N. Biochemistry 2002, 41, 5307-5312],
85. natural products (o) Matsuoka, S.; Matsumori, N.; Murata, M. Org. Biomol. Chem. 2003, 1, 3882-3884.
86. (p) Yamashita, K.; Janout, V.; Bernard, E.; Armstrong, D.; Regen, S. L. J. Am. Chem. Soc. 1995, 117, 6249-6253.
87. (q) Muto, Y.; Matsuoka, T.; Kida, A.; Okano, Y.; Kirino, Y. FEBS Lett. 2001, 508, 423-426.
88. (r) Goudet, C.; Benitah, J.-P.; Milat, M.-L.; Sentenac, H.; Thibaud, J.-B. Biophys. J. 1999, 77, 3052-3059], artificial membranes
89. [(s) Kimizuka, N. Curr. Opin. Chem. Biol. 2003, 7, 702-709],
90. engineered biological pores [(t) Bayley, H.; Martin, C. R. Chem. Rev. 2000, 100, 2575-2594.
91. (u) Luchian, T.; Shin, S.-H.; Bayley, H. Angew. Chem., Int. Ed. 2003, 42, 1926-1929.
92. (v) Luchian, T.; Shin, S.-H.; Bayley, H. Angew. Chem., Int. Ed. 2003, 42, 3766-3771],
93. and porous materials [(w) Li, J.; Stein, D.; McMullan, C.; Branton, D.; Aziz, M. J.; Golovchenko, J. A. Nature 2001, 412, 166-169, and ref 5t].
94. The term "synthetic multifunctional pores" (SMPS) is used for synthetic pores (ref 5) with additional function(s).
95. Hille, B. Ionic Channels of Excitable Membranes, 2nd ed.; Sinauer: Sunderland, MA, 1992.
96. Connors, K. A. Binding Constants; John Wiley & Sons; New York, 1987.
97. Stadler, E.; Dedek, P.; Yamashita, K.; Regen, S. L. J. Am. Chem. Soc. 1994, 116, 6677-6682.
98. Talukdar, P.; Sakai, N.; Sordé, N.; Gerard, D.; Cardona, V. M. F.; Matile, S. Bioorg. Med. Chem. 2004, 12, 1325-1336.
99. Das, G.; Matile, S. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 5183-5188.
100. Das, G.; Ouali, L.; Adrian, M.; Baumeister, B.; Wilkinson, K. J.; Matile, S. Angew. Chem., Int. Ed. 2001, 40, 4657-4661.
101. (a) Menestrina, G.; Dalla Serra, M.; Comai, M.; Coraiola, M.; Viero, G.; Werner, S.; Colin, D. A.; Monteil, H.; Prevost, G. FEBS Lett. 2003, 552, 54-60.
102. (b) Collier, R. J.; Young, J. A. Annu. Rev. Cell Dev. Biol. 2003, 19, 45-70.
103. (c) Heuck, A. P.; Tweten, R. K.; Johnson, A. E. Biochemistry 2001, 40, 9065-9073.
104. (d) Abrami, L.; Fivaz, M.; van der Goot, F. G. Trends Microbiol. 2000, 8, 168-172.
105. (e) Song, L.; Hobaugh, M. R.; Shustak, C.; Cheley, S.; Bayley, H.; Gouaux, J. E. Science 1996, 274, 1859-1866, see also ref 5e.
106. Baumeister, B.; Sakai, N.; Matile, S. Org. Lett. 2001, 3, 4229-4232.
107. Baumeister, B.; Som, A.; Das, G.; Sakai, N.; Vilbois, F.; Gerard, D.; Shahi, S. P.; Matile, S. Helv. Chim. Acta 2002, 85, 2740-2753.
108. Sakai, N.; Sordé, N.; Das, G.; Perrottet, P.; Gerard, D.; Matile, S. Org. Biomol. Chem. 2003, 1, 1226-1231.
109. Sakai, N.; Matile, S. J. Am. Chem. Soc. 2003, 125, 14348-14356.
110. (a) Baumeister, B.; Sakai, N.; Matile, S. Angew. Chem., Int. Ed. 2000, 39, 1955-1958.
111. (b) Sakai, N.; Matile, S. J. Am. Chem. Soc. 2002, 124, 1184-1185.
112. (c) Sakai, N.; Houdebert, D.; Matile, S. Chem. Eur. J. 2003, 9, 223-232.
113. Sakai, N.; Baumeister, B.; Matile, S. ChemBioChem 2000, 1, 123-125.
114. Internal charge repulsion (ICR): number of charged groups at the inner surface of a pore, increases with pH for acidic residues (e.g., aspartate), decreases with pH for basic residues (e.g., lysine, histidine, and arginine). ICR model: pore activity is maximal at intermediate ICR. See ref 15.
115. Som, A.; Sakai, N.; Matile, S. Bioorg. Med. Chem. 2003, 11, 1363-1369.
116. (a) Das, G.; Onouchi, H.; Yashima, E.; Sakai, N.; Matile, S. ChemBioChem 2002, 3, 1089-1096.
117. (b) Sordé, N.; Matile, S. J. Supramol. Chem. 2002, 2, 191-199.
118. (a) Das, G.; Talukdar, P.; Matile, S. Science 2002, 298, 1600-1602.
119. (b) Sordé, N.; Das, G.; Matile, S. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 11964-11969.
120. (c) Sordé, N.; Matile, S. Peptide Sci. 2004, 76, 55-65.
121. Sakai, N.; Sordé, N.; Matile, S. J. Am. Chem. Soc. 2003, 125, 7776-7777.
122. Som, A.; Matile, S. Eur. J. Org. Chem. 2002, 3874-3883.
123. Baumeister, B.; Matile, S. Macromolecules 2002, 35, 1549-1555.
124. Bainbridge, G.; Gokce, I.; Lakey, J. H. FEBS Lett. 1998, 431, 305-308.
125. (a) Smart, O. S.; Breed, J.; Smith, G. R.; Sansom, M. S. P. Biophys. J. 1997, 72, 1109-1126.
126. (b) Cruickshank, C. C.; Minchin, R. F.; Le Dain, A. C.; Martinac, B. Biophys. J. 1997, 73, 1925-1931.
127. Applied to host-guest chemistry, the meaning of the Hill coefficient n (or sometimes h) can be more complex as well and include cooperativity beyond the number n of guests bound per host. Compare, e.g.: Connors, K. A. Binding Constants; John Wiley & Sons: New York, 1987; pp 59-101.
128. Maestro 4.1; Schrödinger Inc.: Portland OR, 2001.
129. (a) Halgren, T. A. J. Comput. Chem. 1996, 17, 490-641.
130. (b) Halgren, T. A. J. Comput. Chem. 1999, 20, 720-748.
131. (a) MacroModel 7.0; Schrödinger, Inc.: Portland OR, 1999.
132. (b) Mohamadi, F.; Richards, N. G. J.; Guida, W. C.; Liskamp, R.; Lipton, M.; Caufield, C.; Chang, G.; Hendrickson, T.; Still, W. C. J. Comput. Chem. 1990, 11, 440-467.
133. (a) Richardson, J. S. Nature 1977, 268, 495-500.
134. (b) Flower, D. R. FEBS Lett. 1994, 344, 247-250.
135. (c) Nagano, N.; Hutchinson, E. G.; Thornton, J. M. Protein Sci. 1999, 8, 2072-2084 (see also ref 13).
136. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Montgomery, J. A., Jr.; 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.; 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 A.1; Gaussian, Inc.: Pittsburgh, PA, 2003.
137. (a) Becke, A. D. Phys. Rev. A 1988, 38, 3098-3100.
138. (b) Lee, C.; Yang, W.; Parr, R. G. Phys. Rev. B 1988, 37, 785-789.
139. (c) Miehlich, B.; Savin, A.; Stoll, H.; Preuss, H. Chem. Phys. Lett. 1989, 157, 200-206.
140. (a) Doyle, D. A.; Cabral, J. M.; Pfuetzner, R. A.; Kuo, A.; Gulbis, J. M.; Cohen, S. L.; Chait, B. T.; MacKinnon, R. Science 1998, 280, 69-77.
141. (b) MacKinnon R.; Cohen, S. L.; Kuo, A.; Lee, A.; Chait, B. T. Science 1998, 280, 106-109.
142. (c) Roux, B.; MacKinnon, R. Science 1999, 285, 100-102.
143. Ronan, D.; Sordé, N.; Matile, S. J. Phys. Org. Chem., in press.