Structural Basis of the Selective Block of Kv1.2 by Maurotoxin from Computer Simulations

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Chen, Rong ^a   Chung, Shin Ho ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MAUROTOXIN; POLYPEPTIDE; POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.2; POTASSIUM CHANNEL KV1.3; TOXIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPUTER SIMULATION; CONCENTRATION RESPONSE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DRUG SELECTIVITY; IC 50; INHIBITION KINETICS; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PHARMACOLOGICAL BLOCKING; PROTEIN BINDING; STRUCTURE ACTIVITY RELATION; VESTIBULE;

AMINO ACID SEQUENCE; BINDING SITES; KV1.2 POTASSIUM CHANNEL; KV1.3 POTASSIUM CHANNEL; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; SCORPION VENOMS;

EID: 84867391072     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047253     Document Type: Article

References (50)

1. Pallaghy PK, Nielsen KJ, Craik DJ, Norton RS, (1994) A common structural motif incorporating a cystine knot and a triple-stranded β-sheet in toxic and inhibitory polypeptides. Protein Sci 3: 1833-1839.
2. Chi V, Pennington MW, Norton RS, Tarcha EJ, Londono LM, et al. (2012) Development of a sea anemone toxin as an immunomodulator for therapy of autoimmune diseases. Toxicon 59: 529-546.
3. Staats PS, Yearwood T, Charapata SG, Presley RW, Wallace MS, et al. (2004) Intrathecal ziconotide in the treatment of refractory pain in patients with cancer or AIDS: a randomized controlled trial. JAMA 291: 63-70.
4. Kharrat R, Mabrouk K, Crest M, Darbon H, Oughideni R, et al. (1996) Chemical synthesis and characterization of maurotoxin, a short scorpion toxin with four disulfide bridges that acts on K+ channels. Eur J Biochem 242: 491-498.
5. Visan V, Fajloun Z, Sabatier JM, Grissmer S, (2004) Mapping of maurotoxin binding sites on hKv1.2, hKv1.3, and hIKCa1 channels. Mol Pharmacol 66: 1103-1112.
6. Visan V, Sabatier JM, Grissmer S, (2004) Block of maurotoxin and charybdotoxin on human intermediate-conductance calcium-activated potassium channels (hIKCa1). Toxicon 43: 973-980.
7. Castle NA, London DO, Creech C, Fajloun Z, Stocker JW, et al. (2003) Maurotoxin: a potent inhibitor of intermediate conductance Ca2+-activated potassium channels. Mol Pharmacol 63: 409-418.
8. Grissmer S, Nguyen AN, Aiyar J, Hanson DC, Mather RJ, et al. (1994) Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol Pharmacol 45: 1227-1234.
9. Kalman K, Pennington MW, Lanigan MD, Nguyen A, Rauer H, et al. (1998) ShK-Dap22, a potent Kv1.3-specific immunosuppressive polypeptide. J Biol Chem 273: 32697-32707.
10. Mouhat S, Visan V, Ananthakrishnan S, Wulff H, Andreotti N, et al. (2005) K+ channel types targeted by synthetic OSK1, a toxin from Orthochirus scrobiculosus scorpion venom. Biochem J 385: 95-104.
11. Avdonin V, Nolan B, Sabatier JM, De Waard M, Hoshi T, (2000) Mechanisms of maurotoxin action on Shaker potassium channels. Biophys J 79: 776-787.
12. Carlier E, Avdonin V, Geib S, Fajloun Z, Kharrat R, et al. (2000) Effect of maurotoxin, a four disulfide-bridged toxin from the chactoid scorpion Scorpio maurus, on Shaker K+ channels. J Pept Res 55: 419-427.
13. Fajloun Z, Mosbah A, Carlier E, Mansuelle P, Sandoz G, et al. (2000) Maurotoxin versus Pi1/HsTx1 scorpion toxins. Toward new insights in the understanding of their distinct disulfide bridge patterns. J Biol Chem 275: 39394-39402.
14. Lecomte C, Ben Khalifa R, Kharrat R, El Ayeb M, Darbon H, et al. (2000) Maurotoxin and the Kv1.1 channel: voltage-dependent binding upon enantiomerization of the scorpion toxin disulfide bridge Cys31-Cys34. J Peptide Res 55: 246-254.
15. Fajloun Z, Andreotti N, Fathallah M, Sabatier JM, De Waard M, (2011) Analysis of the interacting surface of maurotoxin with the voltage-gated Shaker B K+ channel. J Pept Sci 17: 200-210.
16. Fu W, Cui M, Briggs JM, Huang X, Xiong B, et al. (2002) Brownian dynamics simulations of the recognition of the scorpion toxin maurotoxin with the voltage-gated potassium ion channels. Biophys J 83: 2370-2385.
17. Yi H, Qiu S, Cao Z, Wu Y, Li W, (2008) Molecular basis of inhibitory peptide maurotoxin recognizing Kv1.2 channel explored by ZDOCK and molecular dynamic simulations. Proteins 70: 844-854.
18. Yi H, Qiu S, Wu Y, Li WX, Wang B, (2011) Differential molecular information of maurotoxin peptide recognizing IKCa and Kv1.2 channels explored by computational simulation. BMC Struct Biol 11: 3.
19. Jin L, Wu Y, (2011) Molecular mechanism of δ-dendrotoxin-potassium channel recognition explored by docking and molecular dynamic simulations. J Mol Recognit 24: 101-107.
20. Chen R, Robinson A, Gordon D, Chung SH, (2011) Modeling the binding of three toxins to the voltage-gated potassium channel (Kv1.3). Biophys J 101: 2652-2660.
21. Chen PC, Kuyucak S, (2012) Developing a comparative docking protocol for the prediction of peptide selectivity profiles: investigation of potassium channel toxins. Toxins 4: 110-138.
22. Khabiri M, Nikouee A, Cwiklik L, Grissmer S, Ettrich R, (2011) Charybdotoxin unbinding from the mKv1.3 potassium channel: A combined computational and experimental study. J Phys Chem B 115: 11490-11500.
23. Cui M, Shen JH, Briggs JM, Luo XM, Tan XJ, et al. (2001) Brownian dynamics simulations of interaction between scorpion toxin Lq2 and potassium ion channel. Biophys J 80: 1659-1669.
24. Yu K, Fu W, Liu H, Luo X, Chen KX, et al. (2004) Computational simulations of interactions of scorpion toxins with the voltage-gated potassium ion channel. Biophys J 86: 3542-3555.
25. Gordon D, Chen R, Ho J, Coote ML, Chung SH, (2012) Rigid body Brownian dynamics as a tool for studying ion channel blockers. J Phys Chem B 116: 1933-1941.
26. Eriksson MA, Roux B, (2002) Modeling the structure of agitoxin in complex with the Shaker K+ channel: a computational approach based on experimental distance restraints extracted from thermodynamic mutant cycles. Biophys J 83: 2595-2609.
27. Yu L, Sun C, Song D, Shen J, Xu N, et al. (2005) Nuclear magnetic resonance structural studies of a potassium channel-charybdotoxin complex. Biochemistry 44: 15834-15841.
28. Lange A, Giller K, Hornig S, Martin-Eauclaire MF, Pongs O, et al. (2006) Toxin-induced conformational changes in a potassium channel revealed by solid-state NMR. Nature 440: 959-962.
29. Long SB, Campbell EB, Mackinnon R, (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309: 897-903.
30. Chen X, Wang Q, Ni F, Ma J, (2010) Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement. Proc Natl Acad Sci U S A 107: 11352-11357.
31. Chen R, Chung SH, (2012) Engineering a potent and specific blocker of voltage-gated potassium channel Kv1.3, a target for autoimmune diseases. Biochemistry 51: 1976-1982.
32. Blanc E, Sabatier JM, Kharrat R, Meunier S, el Ayeb M, et al. (1997) Solution structure of maurotoxin, a scorpion toxin from Scorpio maurus, with high affinity for voltage-gated potassium channels. Proteins 29: 321-333.
33. Caves LS, Evanseck JD, Karplus M, (1998) Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin. Protein Sci 7: 649-666.
34. Leontiadou H, Mark AE, Marrink SJ, (2006) Antimicrobial peptides in action. J Am Chem Soc 128: 12156-12161.
35. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
36. Klauda JB, Venable RM, Freites JA, O'Connor JW, Tobias DJ, et al. (2010) Update of the CHARMM all-atom additive force field for lipids: validation on six lipid types. J Phys Chem B 114: 7830-7843.
37. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
38. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML, (1982) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
39. Ryckaert JP, Ciccotti G, Berendsen HJC, (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23: 327-341.
40. Miyamoto S, Kollman PA, (1992) SETTLE: An analytical version of the SHAKE and RATTLE algorithm for rigid water models. J Comput Chem 13: 952-962.
41. Martyna GJ, Tobias DJ, Klein ML, (1994) Constant pressure molecular dynamics algorithms. J Chem Phys 101: 4177-4189.
42. Allen TW, Andersen OS, Roux B, (2004) Energetics of ion conduction through the gramicidin channel. Proc Natl Acad Sci U S A 101: 117-122.
43. Kumar S, Bouzida D, Swendsen RH, Kollman PA, Rosenberg JM, (1992) The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J Comput Chem 13: 1011-1021.
44. Mills JE, Dean PM, (1996) Three-dimensional hydrogen-bond geometry and probability information from a crystal survey. J Comput Aided Mol Des 10: 607-622.
45. Kumar S, Nussinov R, (2002) Close-range electrostatic interactions in proteins. ChemBioChem 3: 604-617.
46. Mintseris J, Pierce B, Wiehe K, Anderson R, Chen R, et al. (2007) Integrating statistical pair potentials into protein complex prediction. Proteins 69: 511-520.
47. Chen R, Li L, Weng Z, (2003) ZDOCK: an initial-stage protein-docking algorithm. Proteins 52: 80-87.
48. Jin L, Wu Y, (2007) Molecular mechanism of the sea anemone toxin ShK recognizing the Kv1.3 channel explored by docking and molecular dynamic simulations. J Chem Inf Model 47: 1967-1972.
49. Hansson T, Marelius J, Åqvist J, (1998) Ligand binding affinity prediction by linear interaction energy methods. J Comput Aided Mol Des 12: 27-35.
50. Moon CP, Fleming KG, (2011) Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers. Proc Natl Acad Sci U S A 108: 10174-10177.