Water-templated transmembrane nanopores from shape-persistent oligocholate macrocycles

Journal of the American Chemical Society

Volumn 133, Issue 1, 2011, Pages 141-147

  Cho, Hongkwan ^a   Widanapathirana, Lakmini ^a   Zhao, Yan ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AQUEOUS PHASE; DRIVING FORCES; HYDROPHILIC MOLECULES; HYDROPHOBIC EFFECT; HYDROPHOBIC ENVIRONMENT; HYDROPHOBIC INTERACTIONS; INTERNAL CAVITIES; LIPID MEMBRANES; MACROCYCLES; MACROCYCLICS; MALTOTRIOSE; SELF-ASSEMBLE; SELF-ASSEMBLING; TEMPLATED; TETRAMERS; TRANSMEMBRANES; TRANSPORT BEHAVIOR; WATER MOLECULE;

CHOLESTEROL; GLUCOSE; HYDROPHILICITY; LIPIDS; MOLECULES; NANOPORES; OLIGOMERS;

HYDROPHOBICITY;

CHOLIC ACID DERIVATIVE; GLUCOSE; MACROCYCLIC COMPOUND; MALTOTRIOSE; WATER;

AQUEOUS SOLUTION; ARTICLE; HYDROPHILICITY; HYDROPHOBICITY; LIPID MEMBRANE; MEMBRANE PERMEABILITY; MEMBRANE TRANSPORT; MOLECULAR INTERACTION; NANOPORE;

CELL MEMBRANE; CHOLATES; CHOLESTEROL; GLUCOSE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MACROCYCLIC COMPOUNDS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; NANOPORES; PERMEABILITY; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLGLYCEROLS; UNILAMELLAR LIPOSOMES; WATER;

EID: 78650969248     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja109036z     Document Type: Article

References (91)

1. Kasianowicz, J. J., Robertson, J. W. F., Chan, E. R., Reiner, J. E., and Stanford, V. M. Annu. Rev. Anal. Chem. 2008, 1, 737-766
2. Kasianowicz, J. J., Brandin, E., Branton, D., and Deamer, D. W. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 13770-13773
3. Akeson, M., Branton, D., Kasianowicz, J. J., Brandin, E., and Deamer, D. W. Biophys. J. 1999, 77, 3227-3233
4. Meller, A., Nivon, L., Brandin, E., Golovchenko, J., and Branton, D. Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 1079-1084
5. Vercoutere, W., Winters-Hilt, S., Olsen, H., Deamer, D., Haussler, D., and Akeson, M. Nat. Biotechnol. 2001, 19, 248-252
6. Howorka, S., Cheley, S., and Bayley, H. Nat. Biotechnol. 2001, 19, 636-639
7. Clarke, J., Wu, H. C., Jayasinghe, L., Patel, A., Reid, S., and Bayley, H. Nat. Biotechnol. 2009, 4, 265-270
8. Matile, S., Som, A., and Sordé, N. Tetrahedron 2004, 60, 6405-6435
9. Sisson, A. L., Shah, M. R., Bhosale, S., and Matile, S. Chem. Soc. Rev. 2006, 35, 1269-1286
10. Granja, J. R. and Ghadiri, M. R. J. Am. Chem. Soc. 1994, 116, 10785-10786
11. Sánchez-Quesada, J., Kim, H. S., and Ghadiri, M. R. Angew. Chem., Int. Ed. 2001, 40, 2503-2506
12. Sakai, N., Mareda, J., and Matile, S. Acc. Chem. Res. 2005, 38, 79-87
13. Das, G., Talukdar, P., and Matile, S. Science 2002, 298, 1600-1602
14. Sakai, N., Sordé, N., and Matile, S. J. Am. Chem. Soc. 2003, 125, 7776-7777
15. Satake, A., Yamamura, M., Oda, M., and Kobuke, Y. J. Am. Chem. Soc. 2008, 130, 6314-6315
16. Helsel, A. J., Brown, A. L., Yamato, K., Feng, W., Yuan, L. H., Clements, A. J., Harding, S. V., Szabo, G., Shao, Z. F., and Gong, B. J. Am. Chem. Soc. 2008, 130, 15784-15785
17. Fyles, T. M. and Tong, C. C. New J. Chem. 2007, 31, 655-661
18. Ma, L., Melegari, M., Colombini, M., and Davis, J. T. J. Am. Chem. Soc. 2008, 130, 2938-2939
19. Gokel, G. W. and Mukhopadhyay, A. Chem. Soc. Rev. 2001, 30, 274-286
20. Fyles, T. M. Chem. Soc. Rev. 2007, 36, 335-347
21. Koert, U., Al-Momani, L., and Pfeifer, J. R. Synthesis-Stuttgart 2004, 1129-1146
22. Gokel, G. W. and Murillo, O. Acc. Chem. Res. 1996, 29, 425-432
23. Jung, M., Kim, H., Baek, K., and Kim, K. Angew. Chem., Int. Ed. 2008, 47, 5755-5757
24. Li, X., Shen, B., Yao, X. Q., and Yang, D. J. Am. Chem. Soc. 2009, 131, 13676-13680
25. Nezil, F. A. and Bloom, M. Biophys. J. 1992, 61, 1176-1183
26. Holthuis, J. C. M., van Meer, G., and Huitema, K. Mol. Membr. Biol. 2003, 20, 231-241
27. Bandyopadhyay, P., Janout, V., Zhang, L. H., Sawko, J. A., and Regen, S. L. J. Am. Chem. Soc. 2000, 122, 12888-12889
28. Goto, C., Yamamura, M., Satake, A., and Kobuke, Y. J. Am. Chem. Soc. 2001, 123, 12152-12159
29. Maulucci, N., De Riccardis, F., Botta, C. B., Casapullo, A., Cressina, E., Fregonese, M., Tecilla, P., and Izzo, I. Chem. Commun. 2005, 1354-1356
30. Wilson, C. P. and Webb, S. J. Chem. Commun. 2008, 4007-4009
31. Janout, V., Di Giorgio, C., and Regen, S. L. J. Am. Chem. Soc. 2000, 122, 2671-2672
32. Janout, V., Staina, I. V., Bandyopadhyay, P., and Regen, S. L. J. Am. Chem. Soc. 2001, 123, 9926-9927
33. Janout, V., Jing, B. W., Staina, I. V., and Regen, S. L. J. Am. Chem. Soc. 2003, 125, 4436-4437
34. Janout, V. and Regen, S. L. J. Am. Chem. Soc. 2005, 127, 22-23
35. Koulov, A. V., Lambert, T. N., Shukla, R., Jain, M., Boon, J. M., Smith, B. D., Li, H. Y., Sheppard, D. N., Joos, J. B., Clare, J. P., and Davis, A. P. Angew. Chem., Int. Ed. 2003, 42, 4931-4933
36. Whitmarsh, S. D., Redmond, A. P., Sgarlata, V., and Davis, A. P. Chem. Commun. 2008, 3669-3671
37. For several representative reviews, see: Gellman, S. H. Acc. Chem. Res. 1998, 31, 173-180
38. Hill, D. J., Mio, M. J., Prince, R. B., Hughes, T. S., and Moore, J. S. Chem. Rev. 2001, 101, 3893-4012
39. Hecht, S. and Huc, I. Foldamers: structure, properties, and applications; Wiley-VCH: Weinheim, 2007.
40. Cubberley, M. S. and Iverson, B. L. Curr. Opin. Chem. Biol. 2001, 5, 650-653
41. Kirshenbaum, K., Zuckermann, R. N., and Dill, K. A. Curr. Opin. Struct. Biol. 1999, 9, 530-535
42. Goodman, C. M., Choi, S., Shandler, S., and DeGrado, W. F. Nat. Chem. Biol. 2007, 3, 252-262
43. Bautista, A. D., Craig, C. J., Harker, E. A., and Schepartz, A. Curr. Opin. Chem. Biol. 2007, 11, 685-692
44. Zhao, Y. and Zhong, Z. J. Am. Chem. Soc. 2005, 127, 17894-17901
45. Zhao, Y., Zhong, Z., and Ryu, E. H. J. Am. Chem. Soc. 2007, 129, 218-225
46. Cho, H. and Zhao, Y. J. Am. Chem. Soc. 2010, 132, 9890-9899
47. Zhao, Y. J. Org. Chem. 2009, 74, 834-843
48. Pan, X. and Zhao, Y. Org. Lett. 2009, 11, 69-72
49. Som, A. and Matile, S. Chem. Biodiv. 2005, 2, 717-729
50. Rostovtsev, V. V., Green, L. G., Fokin, V. V., and Sharpless, K. B. Angew. Chem., Int. Ed. 2002, 41, 2596-2599
51. Kolb, H. C., Finn, M. G., and Sharpless, K. B. Angew. Chem., Int. Ed. 2001, 40, 2004-2021
52. Dunitz, J. D. Science 1994, 264, 670
53. Bonar Law, R. P., Davis, A. P., and Murray, B. A. Angew. Chem., Int. Ed. Engl. 1990, 29, 1407-1408
54. Davis, A. P. and Walsh, J. J. Chem. Commun. 1996, 449-451
55. Brotherhood, P. R. and Davis, A. P. Chem. Soc. Rev. 2010, 39, 3633-3647
56. Brady, P. A., Bonar Law, R. P., Rowan, S. J., Suckling, C. J., and Sanders, J. K. M. Chem. Commun. 1996, 319-320
57. Ghosh, S., Choudhury, A. R., Row, T. N. G., and Maitra, U. Org. Lett. 2005, 7, 1441-1444
58. In our leakage assay, we added 1 to the liposomal solution as a solution of DMSO (10-20 μL). The amount of DMSO was tested and found to have negligible effects on the LUVs.
59. Kinsky, S. C., Haxby, J. A., Zopf, D. A., Alving, C. R., and Kinsky, C. B. Biochemistry 1969, 8, 4149-4158
60. Struck, D. K., Hoekstra, D., and Pagano, R. E. Biochemistry 1981, 20, 4093-4099
61. The 100% end point in a fusion assay can be measured either after a surfactant such as Triton X-100 is added to destroy the liposomes or through a "mock" fusion product (i.e., liposomes whose probe density corresponds to that of completely fused liposomes). Although the Triton method gave similar results, we mainly used the second approach for our fusion experiments because Triton X-100 impacts the quantum yield of NBD. For a discussion on different lipid-mixing fusion assays, see: Hoesktra, D. and Düzgüneš, N. Methods Enzymol. 1993, 220, 15-32
62. Smith, B. D. and Lambert, T. N. Chem. Commun. 2003, 2261-2268
63. Deng, G., Merritt, M., Yamashita, K., Janout, V., Sadownik, A., and Regen, S. L. J. Am. Chem. Soc. 1996, 118, 3307-3308
64. Merritt, M., Lanier, M., Deng, G., and Regen, S. L. J. Am. Chem. Soc. 1998, 120, 8494-8501
65. Hille, B. Ionic channels of excitable membranes; 2nd ed.; Sinauer Associates: Sunderland, MA, 1992.
66. Litvinchuk, S., Bollot, G., Mareda, J., Som, A., Ronan, D., Shah, M. R., Perrottet, P., Sakai, N., and Matile, S. J. Am. Chem. Soc. 2004, 126, 10067-10075
67. Leakage at 60 min gave similar results, but the curve fitting to the Hill equation was less certain because the data points clustered at either very high (Y > 90%) or very low (Y < 30%) leakage.
68. Lewis, B. A. and Engelman, D. M. J. Mol. Biol. 1983, 166, 203-210
69. Hydrogen bonds among the amides along the pore axis are unlikely to contribute significantly because the amides are exposed to water molecules inside the pore. Also, the steroid backbone is large on the amino end and small near the carboxy tail. The geometry of the macrocycle thus prohibits close contact of the amide bonds in the z -direction.
70. Demel, R. A., Bruckdorfer, K. R., and Van Deenen, L. L. Biochim. Biophys. Acta 1972, 255, 321-330
71. Papahadjopoulos, D., Nir, S., and Ohki, S. Biochim. Biophys. Acta 1972, 266, 561-583
72. London, E. Curr. Opin. Struct. Biol. 2002, 12, 480-486
73. Edidin, M. Annu. Rev. Biophys. Biomol. Struct. 2003, 32, 257-283
74. Silvius, J. R. Biochim. Biophys. Acta 2003, 1610, 174-183
75. Zhao, J., Wu, J., Heberle, F. A., Mills, T. T., Klawitter, P., Huang, G., Costanza, G., and Feigenson, G. W. Biochim. Biophys. Acta 2007, 1768, 2764-2776
76. Lambert, J. B. and Mark, H. W. J. Am. Chem. Soc. 1978, 100, 2501-2505
77. Lambert, J. B. and Larson, E. G. J. Am. Chem. Soc. 1985, 107, 7546-7550
78. Talukdar, P., Sakai, N., Sordé, N., Gerard, D., Cardona, V. M. F., and Matile, S. Bioorg. Med. Chem. 2004, 12, 1325-1336
79. Bhosale, S. and Matile, S. Chirality 2006, 18, 849-856
80. Shank, L. P., Broughman, J. R., Takeguchi, W., Cook, G., Robbins, A. S., Hahn, L., Radke, G., Iwamoto, T., Schultz, B. D., and Tomich, J. M. Biophys. J. 2006, 90, 2138-2150
81. Ferdani, R., Pajewski, R., Djedovič, N., Pajewska, J., Schlesinger, P. H., and Gokel, G. W. New J. Chem. 2005, 29, 673-680
82. Chen, W. H., Shao, X. B., and Regen, S. L. J. Am. Chem. Soc. 2005, 127, 12727-12735
83. Weiss, J. N. FASEB J. 1997, 11, 835-841
84. Birks, J. B., Munro, I. H., and Dyson, D. J. Proc. R. Soc. London Ser. A 1963, 275, 575-588
85. Olson, F., Hunt, C. A., Szoka, F. C., Vail, W. J., and Papahadjopoulos, D. Biochim. Biophys. Acta 1979, 557, 9-23
86. Smith, S. A. and Morrissey, J. H. J. Thromb. Haemost. 2004, 2, 1155-1162
87. Chan, H. S., Bromberg, S., and Dill, K. A. Philos. Trans. R. Soc. London B 1995, 348, 61-70
88. For an example of water-promoted assembly in the solid state, see: Carrasco, H., Foces-Foces, C., Pérez, C., Rodríguez, M. L., and Martín, J. D. J. Am. Chem. Soc. 2001, 123, 11970-11981
89. Saier, M. H., Jr. In The Structure of biological membranes; Yeagle, P., Ed; CRC Press: Boca Raton, 1992; Chapter 18.
90. For boronic acid-based sugar transporters, see: Westmark, P. R. and Smith, B. D. J. Am. Chem. Soc. 1994, 116, 9343-9344
91. Westmark, P. R., Gardiner, S. J., and Smith, B. D. J. Am. Chem. Soc. 1996, 118, 11093-11100