Free energy simulations of binding of HsTx1 toxin to Kv1 potassium channels: The basis of Kv1.3/Kv1.1 selectivity

Journal of Physical Chemistry B

Volumn 118, Issue 3, 2014, Pages 707-716

  Rashid, M Harunur ^a   Kuyucak, Serdar ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOIMMUNE DISEASE; BINDING FREE ENERGY; FREE ENERGY SIMULATIONS; MOLECULAR DYNAMICS SIMULATIONS; POTASSIUM CHANNELS; POTENTIAL OF MEAN FORCE; SELECTIVITY FILTER; VOLTAGE-GATED POTASSIUM CHANNELS;

AMINO ACIDS; BINDING ENERGY; MOLECULAR DYNAMICS; POTASSIUM;

TOXIC MATERIALS;

POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.2; POTASSIUM CHANNEL KV1.3; SCORPION VENOM; TX1 TOXIN, HETEROMETRUS SPINNIFER;

ARTICLE; CHEMISTRY; ENZYME SPECIFICITY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; THERMODYNAMICS;

KV1.1 POTASSIUM CHANNEL; KV1.2 POTASSIUM CHANNEL; KV1.3 POTASSIUM CHANNEL; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION; SCORPION VENOMS; SUBSTRATE SPECIFICITY; THERMODYNAMICS;

EID: 84893120991     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp410950h     Document Type: Article

References (60)

1. Hille, B. Ionic Channels of Excitable Membranes, 3 rd ed.; Sinauer Associates: Sunderland, MA, 2001.
2. Ashcroft, F. M. Ion Channels and Disease: Channelopathies; Academic Press: San Diego, CA, 2000.
3. + Channel Modulators for the Treatment of Neurological Disorders and Autoimmune Diseases Chem. Rev. 2008, 108, 1744-1773
4. Wulff, H.; Castle, N. A.; Pardo, L. A. Voltage-Gated Potassium Channels as Therapeutic Targets Nat. Rev. Drug Discovery 2009, 8, 982-1001
5. + Channel in Effector Memory T Cells as New Target for MS J. Clin. Invest. 2003, 111, 1703-1713
6. Beeton, C.; Wulff, H.; Standifer, N. E.; Azam, P.; Mullen, K. M.; Pennington, M. W.; Kolski-Andreaco, A.; Wei, E.; Grino, A.; Counts, D. R. Kv1.3 Channels are a Therapeutic Target for T Cell-Mediated Autoimmune Diseases Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 17414-17419
7. Cahalan, M. D.; Chandy, K. G. The Functional Network of ion Channels in T Lymphocytes Immunol. Rev. 2009, 231, 59-87
8. Schmitz, A.; Sankaranarayanan, A.; Azam, P.; Schmidt-Lassen, K.; Homerick, D.; Hansel, W.; Wulff, H. Design of PAP-1, a Selective Small Molecule Kv1.3 Blocker, for the Suppression of Effector Memory T Cells in Autoimmune Diseases Mol. Pharmacol. 2005, 68, 1254-1270
9. Norton, R. S.; Pennington, M. W.; Wulff, H. Potassium Channel Blockade by the Sea Anemone Toxin ShK for the Treatment of Multiple Sclerosis and Other Autoimmune Diseases Curr. Med. Chem. 2004, 11, 3041-3052
10. Chi, V.; Pennington, M. W.; Norton, R. S.; Tarcha, E. J.; Londono, L. M.; Sims-Fahey, B.; Upadhyay, S. K.; Lakey, J. T.; Iadonato, S.; Wulff, H. Development of a Sea Anemone Toxin as an Immunomodulator for Therapy of Autoimmune Diseases Toxicon 2011, 59, 529-546
11. Castaneda, O.; Sotolongo, V.; Amor, A. M.; Stocklin, R.; Anderson, A. J.; Harvey, A. L.; Engstrom, A.; Wernstedt, C.; Karlsson, E. Characterization of a Potassium Channel Toxin from the Caribbean Sea Anemone Stichodactyla helianthus Toxicon 1995, 33, 603-613
12. Kalman, K.; Pennington, M. W.; Lanigan, M. D.; Nguyen, A.; Rauer, H.; Mahnir, V.; Paschetto, K.; Kem, W. R.; Grissmer, S.; Gutman, G. A. ShK-Dap22, a Potent Kv1.3-Specific Immunosuppressive Polypeptide J. Biol. Chem. 1998, 273, 32697-32707
13. Beeton, C.; Pennington, M. W.; Wulff, H.; Singh, S.; Nugent, D.; Crossley, G.; Khaytin, I.; Calabresi, P. A.; Chen, C. Y.; Gutman, G. A.; Chandy, K. G. Targeting Effector Memory T Cells with a Selective Peptide Inhibitor of Kv1.3 Channels for Therapy of Autoimmune Diseases Mol. Pharmacol. 2005, 67, 1369-1381
14. Pennington, M. W.; Beeton, C.; Galea, C. A.; Smith, B. J.; Chi, V.; Monaghan, K. P.; Garcia, A.; Rangaraju, S.; Giuffrida, A.; Plank, D. Engineering a Stable and Selective Peptide Blocker of the Kv1.3 Channel in T Lymphocytes Mol. Pharmacol. 2009, 75, 762-773
15. + Channels Isolated from Heterometrus Spinnifer (Scorpionidea) Venom Biochem. J. 1997, 328, 321-327
16. Regaya, I.; Beeton, C.; Ferrat, G.; Andreotti, N.; Darbon, H.; De Waard, M.; Sabatier, J. M. Evidence for Domain Specific Recognition of SK and Kv Channels by MTX and HsTx1 Scorpion Toxins J. Biol. Chem. 2004, 279, 55690-55696
17. Gordon, D.; Chen, R.; Chung, S. H. Computational Methods of Studying the Binding of Toxins from Venomous Animals to Biological Ions Channels: Theory and Applications Physiol. Rev. 2013, 93, 767-802
18. Rashid, M. D.; Mahdavi, S.; Kuyucak, S. Computational Studies of Marine Toxins Targeting Ion Channels Mar. Drugs 2013, 11, 848-869
19. Shiau, Y. S.; Lin, T. B.; Liou, H. H.; Huang, P. T.; Lou, K. L.; Shiau, Y. Y. Molecular Simulation Reveals Structural Determinants of the Hanatoxin Binding in Kv2.1 Channels J. Mol. Model. 2002, 8, 253-257
20. Andreotti, N.; di Luccio, E.; Sampieri, F.; De Waard, M.; Sabatier, J. M. Molecular Modeling and Docking Simulations of Scorpion Toxins and Related Analogs on Human SKCa2 and SKCa3 Channels Peptides 2005, 26, 1095-1108
21. Fu, W.; Cui, M.; Briggs, J. M.; Huang, X.; Xiong, B.; Zhang, Y.; Luo, X.; Shen, J.; Ji, R.; Jiang, H.; Chen, K. Brownian Dynamics Simulations of the Recognition of the Scorpion Toxin Maurotoxin with the Voltage-Gated Potassium Ion Channels Biophys. J. 2002, 83, 2370-2385
22. Yu, K.; Fu, W.; Liu, H.; Luo, X.; Chen, K. X.; Ding, J. P.; Shen, J.; Jiang, H. Computational Simulations of Interactions of Scorpion Toxins with the Voltage-Gated Potassium Ion Channel Biophys. J. 2004, 86, 3542-3555
23. + Channel: A Computational Approach Based on Experimental Distance Restraints Extracted from Thermodynamic Mutant Cycles Biophys. J. 2002, 83, 2595-2609
24. Huang, X.; Dong, F.; Zhou, H. X. Electrostatic Recognition and Induced Fit in the κ-PVIIA Toxin Binding to Shaker Potassium Channel J. Am. Chem. Soc. 2005, 127, 6836-6849
25. Alonso, H.; Bliznyuk, A. A.; Gready, J. E. Combining Docking and Molecular Dynamic Simulations in Drug Design Med. Res. Rev. 2006, 26, 531-568
26. Zarrabi, M.; Naderi-Manesh, H. The investigation of Interactions of κ-Hefutoxin1 with the Voltage-Gated Potassium Channels: A Computational Simulation Proteins 2007, 71, 1441-1449
27. Yi, H.; Qiu, S.; Cao, Z.; Wu, Y.; Li, W. Molecular Basis of Inhibitory Peptide Maurotoxin Recognizing Kv1.2 Channel Explored by ZDOCK and Molecular Dynamic Simulations Proteins 2008, 70, 844-854
28. Yi, M. G.; Tjong, H. T.; Zhou, H. X. Spontaneous Conformational Change and Toxin Binding in α7 Acetylcholine Receptor: Insight into Channel Activation and Inhibition Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 8280-8285
29. Pietra, F. Docking and MD Simulations of the Interaction of the Tarantula Peptide Psalmotoxin-1 with ASIC1a Channels Using a Homology Model J. Chem. Inf. Model. 2009, 49, 972-977
30. Ander, M.; Luzhkov, V. B; Aqvist, J. Ligand Binding to the Voltage-Gated Kv1.5 Potassium Channel in the Open State-Docking and Computer Simulations of a Homology Model Biophys. J. 2008, 94, 820-831
31. Chen, P. C.; Kuyucak, S. Mechanism and Energetics of Charybdotoxin Unbinding from a Potassium Channel from Molecular Dynamics Simulations Biophys. J. 2009, 96, 2577-2588
32. Chen, P. C.; Kuyucak, S. Accurate Determination of the Binding Free Energy for KcsA-Charybdotoxin Complex from the Potential of Mean Force Calculations with Restraints Biophys. J. 2011, 100, 2466-2474
33. Khabiri, M.; Nikouee, A.; Cwiklik, L.; Grissmer, S.; Ettrich, R.; Charybdotoxin, R. Unbinding from the mKv1.3 Potassium Channel: A Combined Computational and Experimental Study J. Phys. Chem. B 2011, 115, 11490-11500
34. Chen, R.; Robinson, A.; Gordon, D.; Chung, S. H. Modeling the Binding of three Toxins to the Voltage-Gated Potassium Channel (Kv1.3) Biophys. J. 2011, 101, 2652-2660
35. Chen, R.; Chung, S. H. Engineering a Potent and Specific Blocker of Voltage-Gated Potassium Channel Kv1.3, a Target for Autoimmune Diseases Biochemistry 2012, 51, 7775-7782
36. Chen, R.; Chung, S. H. Structural Basis of the Selective Block of Kv1.2 by Maurotoxin from Computer Simulations PLoS One 2012, 7, e47253
37. Chen, R.; Chung, S. H. Binding Modes of μ-Conotoxin to the Bacterial Sodium Channel (NaVAb) Biophys. J. 2012, 102, 483-488
38. Chen, R.; Chung, S. H. Conserved Functional Surface of Antimammalian Scorpion β-Toxins J. Phys. Chem. B 2012, 116, 4796-4800
39. Chen, P. C.; Kuyucak, S. Developing a Comparative Docking Protocol for the Prediction of Peptide Selectivity Profiles: Investigation of Potassium Channel Toxins Toxins 2012, 4, 110-138
40. Rashid, M. H.; Kuyucak, S. Affinity and Selectivity of ShK Toxin for the Kv1 Potassium Channels from Free Energy Simulations J. Phys. Chem. B 2012, 116, 4812-4822
41. Pennington, M. W.; Rashid, M. H.; Tajhya, R. B.; Beeton, C.; Kuyucak, S.; Norton, R. S. A C-Terminally Amidated Analogue of ShK is a Potent and Selective Blocker of the Voltage-Gated Potassium Channel Kv1.3 FEBS Lett. 2012, 586, 3996-4001
42. Rashid, M. H.; Heinzelmann, G.; Huq, R.; Tajhya, R. B.; Chang, S. C.; Chhabra, S.; Pennington, M. W.; Beeton, C.; Norton, R. S.; Kuyucak, S. A Potent and Selective Peptide Blocker of the Kv1.3 Channel: Prediction from Free-Energy Simulations and Experimental Confirmation PLoS One 2013, 8, e78712
43. + Channel is not a Good Model for Ligand Binding to Voltage-Gated Kv1 Channels Biochemistry 2013, 52, 1631-1640
44. Gilson, M. K.; Zhou, H. X. Calculation of Protein-Ligand Binding Energies Annu. Rev. Biophys. Biomol. Struct. 2007, 36, 21-42
45. Deng, Y.; Roux, B. Computations of Standard Binding Free Energies with Molecular Dynamics Simulations J. Phys. Chem. B 2009, 113, 2234-2246
46. Steinbrecher, T.; Labahn, A. Towards Accurate Free Energy Calculations in Ligand-Protein Binding Studies Curr. Med. Chem. 2010, 17, 767-785
47. Yu, L. P.; Sun, C. H.; Song, D. Y.; Shen, J. W.; Xu, N.; Gunasekera, A.; Hajduk, P. J.; Olejniczak, E. T. Nuclear Magnetic Resonance Structural Studies of a Potassium Channel-Charybdotoxin Complex Biochemistry 2005, 44, 15834-15841
48. + Channel in a Lipid Membrane-Like Environment Nature 2007, 450, 376-382
49. Rauer, H.; Pennington, M.; Cahalan, M.; Chandy, K. G. Structural Conservation of the Pores of Calcium-Activated and Voltage-Gated Potassium Channels Determined by a Sea Anemone Toxin J. Biol. Chem. 1999, 274, 21885-21892
50. Humphrey, W.; Dalke, A.; Schulten, K. VMD-Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38
51. Bastug, T.; Kuyucak, S. Importance of the Peptide Backbone Description in Modeling the Selectivity Filter in Potassium Channels Biophys. J. 2009, 96, 4006-4012
52. Savarin, P.; Romi-Lebrun, R.; Zinn-Justin, S.; Lebrun, B.; Nakajima, T.; Gilquin, B.; Menez, A. Structural and Functional Consequences of the Presence of a Fourth Disulfide Bridge in the Scorpion Short Toxins: Solution Structure ot the Potassium Channel Inhibitor HsTx1 Protein Sci. 1999, 8, 2672-2685
53. Mouhat, S.; Jouirou, B.; Mosbah, A.; De Waard, M.; Sabatier, J. M. Animal Toxins Acting on Voltage-Gated Potassium Channels Biochem. J. 2004, 378, 717-726
54. Carrega, L.; Mosbah, A.; Ferrat, G.; Beeton, C.; Andreotti, N.; Mansuelle, P.; Darbon, H.; De Waard, M.; Sabatier, J. M. The Impact of the Fourth Disulfide Bridge in Scorpion Toxins of the α-KTx6 Subfamily Proteins 2005, 61, 1010-1023
55. Dominguez, C.; Boelens, R.; Bonvin, A. M. J. J. HADDOCK: A Protein-Protein Docking Approach Based on Biochemical or Biophysical Information J. Am. Chem. Soc. 2003, 125, 1731-1737
56. de Vries, S.; J.; van Dijk, A. D. J.; Krzeminski, M.; van Dijk, M.; Thureau, A.; Hsu, V.; Wassenaar, T.; Bonvin, A. M. J. J. HADDOCK versus HADDOCK: New Features and Performance of HADDOCK 2.0 on the CAPRI Targets Proteins 2007, 69, 726-733
57. Phillips, J. C.; Braun, R.; Wang, W.; Gumbart, J.; Tajkhorshid, E.; Villa, E.; Chipot, C.; Skeel, R. D.; Kale, L.; Schulten, K. NAMD2: Greater Scalability for Parallel Molecular Dynamics J. Comput. Chem. 2005, 26, 1781-1802
58. Klauda, J. B.; Venable, R. M; Freites, J. A.; O'Connor, J. W.; Tobias, D. J.; Mondragon-Ramirez, C.; Vorobyov, I.; MacKerell, A. D.; Pastor, R. W. Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types J. Phys. Chem. B 2012, 114, 7830-7843
59. Kumar, S.; Bouzida, D.; Swensen, R. H.; Kollman, P. A.; Rosenberg, J. M. The Weighted Histogram Analysis Method for Free-Energy Calculations on Biomolecules J. Comput. Chem. 1992, 13, 1011-1021
60. Roux, B.; Allen, T.; Berneche, S.; Im, W. Theoretical and Computational Models of Biological Ion Channels Q. Rev. Biophys. 2004, 37, 15-103