Scanning the topography of polyamine blocker binding in an inwardly rectifying potassium channel

Journal of Biological Chemistry

Volumn 288, Issue 9, 2013, Pages 6591-6601

  Kurata, Harley T ^a   Akrouh, Alejandro ^b   Li, Jenny B W ^a   Marton, Laurence J ^c   Nichols, Colin G ^b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING PROPERTIES; EN-ROUTE; HIGH AFFINITY; HIGH-AFFINITY BINDING SITES; POLYAMINES; POSITIVELY CHARGED; POTASSIUM CHANNELS; SPECIFIC LOCATION;

BINDING SITES; ELECTRIC RECTIFIERS;

AMINO ACIDS;

CYSTEINE; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; POLYAMINE DERIVATIVE; SPERMINE;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; BINDING SITE; CYTOPLASM; GENE MUTATION; HYDROGEN BOND; PATCH CLAMP; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE;

ANIMALS; CELL LINE; MICE; POLYAMINES; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN BINDING;

EID: 84874779263     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.383794     Document Type: Article

References (38)

1. Lu, Z. (2004) Mechanism of rectification in inward-rectifier K+ channels. Annu. Rev. Physiol. 66, 103-129
2. Nichols, C. G., and Lopatin, A. N. (1997) Inward rectifier potassium channels. Annu. Rev. Physiol. 59, 171-191
3. Hansen, S. B., Tao, X., and MacKinnon, R. (2011) Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477, 495-498
4. Kuo, A., Gulbis, J. M., Antcliff, J. F., Rahman, T., Lowe, E. D., Zimmer, J., Cuthbertson, J., Ashcroft, F. M., Ezaki, T., and Doyle, D. A. (2003) Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300, 1922-1926
5. Lopatin, A. N., Makhina, E. N., and Nichols, C. G. (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372, 366-369
6. Lopatin, A. N., Makhina, E. N., and Nichols, C. G. (1995) The mechanism of inward rectification of potassium channels: "long-pore plugging" by cytoplasmic polyamines. J. Gen. Physiol. 106, 923-955
7. Ficker, E., Taglialatela, M., Wible, B. A., Henley, C. M., and Brown, A. M. (1994) Spermine and spermidine as gating molecules for inward rectifier K+ channels. Science 266, 1068-1072
8. Fakler, B., Brändle, U., Glowatzki, E., Weidemann, S., Zenner, H. P., and Ruppersberg, J. P. (1995) Strong voltage-dependent inward rectification of inward rectifier K+ channels is caused by intracellular spermine. Cell 80, 149-154
9. Gerner, E. W., and Meyskens, F. L., Jr. (2004) Polyamines and cancer: old molecules, new understanding. Nat. Rev. Cancer 4, 781-792
10. Cerrone, M., Noujaim, S., and Jalife, J. (2006) The short QT syndrome as a paradigm to understand the role of potassium channels in ventricular fibrillation. J. Intern. Med. 259, 24-38
11. Priori, S. G., Pandit, S. V., Rivolta, I., Berenfeld, O., Ronchetti, E., Dhamoon, A., Napolitano, C., Anumonwo, J., di Barletta, M. R., Gudapakkam, S., Bosi, G., Stramba-Badiale, M., and Jalife, J. (2005) A novel form of short QT syndrome (SQT3) is caused by a mutation in the KCNJ2 gene. Circ. Res. 96, 800-807
12. Xu, Y., Shin, H. G., Szép, S., and Lu, Z. (2009) Physical determinants of strong voltage sensitivity of K+ channel block. Nat. Struct. Mol. Biol. 16, 1252-1258
13. Tao, X., Avalos, J. L., Chen, J., and MacKinnon, R. (2009) Crystal structure of the eukaryotic strong inward-rectifier K+ channel Kir2.2 at 3.1 Ä resolution. Science 326, 1668-1674
14. Nishida, M., Cadene, M., Chait, B. T., and MacKinnon, R. (2007) Crystal structure of a Kir3.1-prokaryotic Kir channel chimera. EMBO J. 26, 4005-4015
15. Pegan, S., Arrabit, C., Zhou, W., Kwiatkowski, W., Collins, A., Slesinger, P. A., and Choe, S. (2005) Cytoplasmic domain structures of Kir2.1 and Kir3.1 show sites for modulating gating and rectification. Nat. Neurosci. 8, 279-287
16. Lopatin, A. N., and Nichols, C. G. (1996) [K+] dependence of polyamineinduced rectification in inward rectifier potassium channels (IRK1, Kir2.1). J. Gen. Physiol. 108, 105-113
17. Hagiwara, S., Miyazaki, S., and Rosenthal, N. P. (1976) Potassium current and the effect of cesium on this current during anomalous rectification of the egg cell membrane of a starfish. J. Gen. Physiol. 67, 621-638
18. Shin, H. G., and Lu, Z. (2005) Mechanism of the voltage sensitivity of IRK1 inward-rectifier K+ channel block by the polyamine spermine. J. Gen. Physiol. 125, 413-426
19. Kurata, H. T., Marton, L. J., and Nichols, C. G. (2006) The polyamine binding site in inward rectifier K+ channels. J. Gen. Physiol. 127, 467-480
20. Kurata, H. T., Cheng, W. W., Arrabit, C., Slesinger, P. A., and Nichols, C. G. (2007) The role of the cytoplasmic pore in inward rectification of Kir2.1 channels. J. Gen. Physiol. 130, 145-155
21. Guo, D., Ramu, Y., Klem, A. M., and Lu, Z. (2003) Mechanism of rectification in inward-rectifier K+ channels. J. Gen. Physiol. 121, 261-275
22. Kurata, H. T., Phillips, L. R., Rose, T., Loussouarn, G., Herlitze, S., Fritzenschaft, H., Enkvetchakul, D., Nichols, C. G., and Baukrowitz, T. (2004) Molecular basis of inward rectification: polyamine interaction sites located by combined channel and ligand mutagenesis. J. Gen. Physiol. 124, 541-554
23. Shyng, S., Ferrigni, T., and Nichols, C. G. (1997) Control of rectification and gating of cloned KATP channels by the Kir6.2 subunit. J. Gen. Physiol. 110, 141-153
24. Wible, B. A., Taglialatela, M., Ficker, E., and Brown, A. M. (1994) Gating of inwardly rectifying K+ channels localized to a single negatively charged residue. Nature 371, 246-249
25. Yang, J., Jan, Y. N., and Jan, L. Y. (1995) Control of rectification and permeation by residues in two distinct domains in an inward rectifier K+ channel. Neuron 14, 1047-1054
26. Kubo, Y., and Murata, Y. (2001) Control of rectification and permeation by two distinct sites after the second transmembrane region in Kir2.1 K+ channel. J. Physiol. 531, 645-660
27. Fujiwara, Y., and Kubo, Y. (2006) Functional roles of charged amino acid residues on the wall of the cytoplasmic pore of Kir2.1. J. Gen. Physiol. 127, 401-419
28. Robertson, J. L., Palmer, L. G., and Roux, B. (2008) Long-pore electrostatics in inward-rectifier potassium channels. J. Gen. Physiol. 132, 613-632
29. Loussouarn, G., Marton, L. J., and Nichols, C. G. (2005) Molecular basis of inward rectification: structural features of the blocker defined by extended polyamine analogs. Mol. Pharmacol. 68, 298-304
30. Mitchell, J. L., Leyser, A., Holtorff, M. S., Bates, J. S., Frydman, B., Valasinas, A. L., Reddy, V. K., and Marton, L. J. (2002) Antizyme induction by polyamine analogues as a factor of cell growth inhibition. Biochem. J. 366, 663-671
31. Valasinas, A., Sarkar, A., Reddy, V. K., Marton, L. J., Basu, H. S., and Frydman, B. (2001) Conformationally restricted analogues of 1N, 14Nbisethylhomospermine (BE-4-4-4): synthesis and growth inhibitory effects on human prostate cancer cells. J. Med. Chem. 44, 390-403
32. Kurata, H. T., Zhu, E. A., and Nichols, C. G. (2010) Locale and chemistry of spermine binding in the archetypal inward rectifier Kir2.1. J. Gen. Physiol. 135, 495-508
33. Kurata, H. T., Diraviyam, K., Marton, L. J., and Nichols, C. G. (2008) Blocker protection by short spermine analogs: refined mapping of the spermine binding site in a Kir channel. Biophysical Journal 95, 3827-3839
34. Chang, H. K., Yeh, S. H., and Shieh, R. C. (2003) The effects of spermine on the accessibility of residues in the M2 segment of Kir2.1 channels expressed in Xenopus oocytes. J. Physiol. 553, 101-112
35. Loussouarn, G., Phillips, L. R., Masia, R., Rose, T., and Nichols, C. G. (2001) Flexibility of the Kir6.2 inward rectifier K+ channel pore. Proc. Natl. Acad. Sci. U.S.A. 98, 4227-4232
36. Lu, T., Nguyen, B., Zhang, X., and Yang, J. (1999) Architecture of a K+ channel inner pore revealed by stoichiometric covalent modification. Neuron 22, 571-580
37. Bushman, J. D., Gay, J. W., Tewson, P., Stanley, C. A., and Shyng, S. L. (2010) Characterization and functional restoration of a potassium channel Kir6.2 pore mutation identified in congenital hyperinsulinism. J. Biol. Chem. 285, 6012-6023
38. Mavri, J., and Vogel, H. J. (1994) Ion pair formation involving methylated lysine side chains: a theoretical study. Proteins 18, 381-389