Designing a C84 fullerene as a specific voltage-gated sodium channel blocker

Nanoscale Research Letters

Volumn 8, Issue 1, 2013, Pages

  Hilder, Tamsyn A ^a   Chung, Shin Ho ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Binding; Molecular dynamics; Voltage gated potassium channel Kv1.3

Indexed keywords

AMINO ACIDS; DISEASES; IONS; MAMMALS; MOLECULAR DYNAMICS; SODIUM;

BINDING; BIOLOGICAL APPLICATIONS; BIOLOGICAL ION CHANNELS; FULLERENE DERIVATIVE; MOLECULAR DYNAMICS SIMULATIONS; SODIUM CHANNEL BLOCKERS; STRUCTURAL TEMPLATES; VOLTAGE-GATED POTASSIUM CHANNELS;

FULLERENES;

BACTERIA (MICROORGANISMS); GASTROPODA; HUMAN IMMUNODEFICIENCY VIRUS; MAMMALIA;

EID: 84881237059     PISSN: 19317573     EISSN: 1556276X     Source Type: Journal    
DOI: 10.1186/1556-276X-8-323     Document Type: Review

References (52)

1. Norton RS: μ-Conotoxins as leads in the development of new analgesics. Molecules 2010, 15:2825-2844.
2. Clark RJ, Akcan M, Kaas Q, Daly NL, Craik DJ: Cyclization of conotoxins to improve their biopharmaceutical properties. Toxicon 2012, 59:446-455.
3. Dekan Z, Vetter I, Daly NL, Craik DJ, Lewis RJ, Alewood PF: α-Conotoxin Iml incorporating stable cystathionine bridges maintains full potency and identical threedimensional structure. J. Amer. Chem. Soc 2011, 133:15866-15869.
4. Khoo KK, Wilson MJ, Smith BJ, Zhang MM, Gulyas J, Yoshikami D, Rivier JE, Bulaj G, Norton RS: Lactam-stabilized helical analogues of the analgesic μ-conotoxin KIIIA. J Med Chem 2011, 54:7558-7566.
5. Bakry R, Vallant RM, Najam-ul-Haq M, Rainer M, Szabo Z, Huck CW, Bonn GK: Medicinal applications of fullerenes. Int. J. Nanomed 2007, 2:639-649.
6. Da Ros T: Twenty years of promises: fullerene in medicinal chemistry. In Medicinal Chemistry and Pharmacological Potential of Fullerenes and Carbon Nanotubes. Edited by Cataldo F, Da Ros T. Netherlands: Springer Science; 2008:1-21.
7. Friedman SH, DeCamp DL, Sijbesma RP, Srdanov G, Wudl F, Kenyon GL: Inhibition of the HIV-1 protease by fullerene derivatives: model building studies and experimental verification. J Am Chem Soc 1993, 115:6506-6509.
8. Prinzbach H, Weiler A, Landenberger P, Wahl F, Wörth J, Scott LT, Gelmont M, Olevano D, Issendorff B: Gas-phase production and photoelectron spectroscopy of the smallest fullerene, C20. Nature 2000, 407:60-63.
9. Shinohara H, Sato H, Saito Y, Takayama M, Izuoka A, Sugawara T: Formation and extraction of very large all-carbon fullerenes. J Phys Chem 1991, 95:8449-8451.
10. Park KH, Chhowalla M, Iqbal Z, Sesti F: Single-walled carbon nanotubes are a new class of ion channel blockers. J Biol Chem 2003, 278:50212-50216.
11. Chhowalla M, Unalan HE, Wang Y, Iqbal Z, Park K, Sesti F: Irreversible blocking of ion channels using functionalized single-walled carbon nanotubes. Nanotechnology 2005, 16:2982-2986.
12. Xu H, Bai J, Meng J, Hao W, Xu H, Cao JM: Multi-walled carbon nanotubes suppress potassium channel activities in PC12 cells. Nanotechnology 2009, 20:285102.
13. Kraszewski S, Tarek M, Treptow W, Ramseyer C: Affinity of C60 neat fullerenes with membrane proteins: a computational study on potassium channels. ACS Nano 2010, 4:4158-4164.
14. Monticelli L, Barnoud J, Orlowski A, Vattulainen I: Interaction of C70 with the Kv1.2 potassium channel. Phys Chem Chem Phys 2012, 14:12526-12533.
15. Wong-Ekkabut J, Baoukina S, Triampo W, Tang IM, Tieleman DP, Monticelli L: Computer simulation study of fullerene translocation through lipid membranes. Nature Nanotech. 2008, 3:363-368.
16. Chen R, Chung SH: Binding modes of μ-conotoxin to the bacterial sodium channel (NavAb). Biophys J 2012, 102:483-488.
17. Finol-Urdaneta RK, Glavica R, McArthur JR, French RJ: Polymodal, high affinity actions of μ-conotoxins on a bacterial voltage-gated sodium channel [abstract]. Biophys J 2013, 104:136a-137a.
18. Stevens M, Peigneur S, Tytgat J: Neurotoxins and their binding areas on voltage-gated sodium channels. Front Pharmacol 2011, 2:1-13.
19. Eijkelkamp N, Linley JE, Baker MD, Minett MS, Cregg R, Werdehausen R, Rugiero F, Wood JN: Neurological perspectives on voltage-gated sodium channels. Brain 2012, 135:2585-2612.
20. Ekberg J, Jayamanne A, Vaughan CW, Aslan S, Thomas L, Mould J, Drinkwater R, Baker MD, Abrahamsen B, Wood JN, Adams DJ, Christie MJ, Lewis RJ: μO-Conotoxin MrVIB selectively blocks Nav1.8 sensory neuron specific sodium channels and chronic pain behavior without motor deficits. Proc Natl Acad Sci USA 2006, 103:17030-17035.
21. Koishi R, Xu H, Ren D, Navarro B, Spiller BW, Shi Q, Clapham DE: A superfamily of voltage-gated sodium channels in bacteria. J Biol Chem 2004, 279:9532-9538.
22. Macnab RM: The bacterial flagellum: reversible rotary propeller and type III export apparatus. J Bacteriol 1999, 181:7149-7153.
23. Wadhams GH, Armitage JP: Making sense of it all: bacterial chemotaxis. Nature Rev. Mol. Cell Biol 2004, 5:1024-1037.
24. Diederich F, Ettl R, Rubin Y, Whetten RL, Beck R, Alvarez M, Anz S, Sensharma D, Wudl F, Khemani KC, Koch A: The higher fullerenes: isolation and characterization of C76, C84, C90, C94, and C70O, an oxide of D5h-C70. Science 1991, 252:548-551.
25. Liu X, Schmalz TG, Klein DJ: Favorable structures for higher fullerenes. Chem Phys Lett 1992, 188:550-554.
26. Diederich F, Whetten RL: Beyond C60: the higher fullerenes. Acc Chem Res 1992, 25:119-126.
27. JCrystalSoft: Nanotube modeler. Version 1.7.3. Copyright JCrystalSoft, 2005-2012. [http://www.jcrystal.com].
28. Balch AL, Ginwalla AS, Lee JW, Noll BC, Olmstead MM: Partial separation and structural characterization of C84 isomers by crystallization of (η 2-C84)Ir(CO)Cl(P(C6H5)3)2. J Am Chem Soc 1994, 116:2227-2228.
29. Bakowies D, Kolb M, Thiel W, Richard S, Ahlrichs R, Kappes MM: Quantumchemistry study of C84 fullerene isomers. Chem Phys Lett 1992, 200:411-417.
30. Strom TA, Barron AR: A simple quick route to fullerene amino acid derivatives. Chem Commun 2010, 46:4764-4766.
31. Yang J, Alemany LB, Driver J, Hartgerink JD, Barron AR: Fullerene-derivatized amino acids: synthesis, characterization, antioxidant properties, and solid-phase peptide synthesis. Chem. Eur. J 2007, 13:2530-2545.
32. Taylor R: Lecture Notes on Fullerene Chemistry. London: Imperial College Press; 1999.
33. ArgusLab: Mark Thompson and Planaria Software LLC. Version 4.0.1. Copyright 1997-2004. [http://www.arguslab.com].
34. Hu Z, Guan W, Wang W, Huang L, Xing H, Zhu Z: Protective effect of a novel cystine C60 derivative on hydrogen peroxide-induced apoptosis in rat pheochromocytoma PC12 cells. Chem Biol Interact 2007, 167:135-144.
35. Payandeh J, Scheuer T, Zheng N, Catterall WA: The crystal structure of a voltagegated sodium channel. Nature 2011, 475:353-359.
36. Chen X, Wang Q, Ni F, Ma J: Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement. Proc. Natl. Acad. Sci. USA 2010, 107:11352-11357.
37. Chen R, Robinson A, Gordon D, Chung SH: Modeling the binding of three toxins to the voltage-gated potassium channel (Kv1.3). Biophys J 2011, 101:2652-2660.
38. Chen R, Chung SH: Engineering a potent and specific blocker of voltage-gated potassium channel Kv1.3, a target for autoimmune diseases. Biochem 2012, 51:1976-1982.
39. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K: Scalable molecular dynamics with NAMD. J Comput Chem 2005, 26:1781-1802.
40. Humphrey W, Dalke A, Schulten K: VMD: visual molecular dynamics. J. Mol. Graphics 1996, 14:33-38.
41. MacKerell AD Jr, Feig M, Brooks CL III: Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 2004, 25:1400-1415.
42. MacKerell AD Jr, Bashford D, Bellott M, Dunbrack RL Jr, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE III, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiórkiewicz-Kuczera J, Yin D, Karplus M: All-atom empirical potential for molecular modeling and dynamic studies of proteins. J Phys Chem B 1998, 102:3586-3616.
43. Hilder TA, Chung SH: Conduction and block of inward rectifier K+ channels: predicted structure of a potent blocker of Kir2.1. Biochem 2013, 52:967-974.
44. Kumar S, Rosenberg JM, Bouzida D, Swendsen RH, Kollman PA: Multidimensional free-energy calculations using the weighted histogram analysis method. J Comput Chem 1995, 16:1339-1350.
45. Allen TW, Andersen OS, Roux B: Energetics of ion conduction through the gramicidin channel. Proc. Natl. Acad. Sci. USA 2004, 101:117-122.
46. Gordon D, Chen R, Chung SH: Computational methods of studying the binding of toxins from venomous animals to biological ion channels: theory and application. Physiol Rev 2013, 93:767-802.
47. De Leon A, Jalbout AF, Basiuk VA: Fullerene-amino acid interactions. A theoretical study. Chem Phys Lett 2008, 452:306-314.
48. EMBL-EBI: MUSCLE-multiple sequence comparison by log-expectation. Copyright © EMBL-EBI 2013. [http://www.ebi.ac.uk/Tools/msa/muscle/].
49. Zhang MM, Wilson MJ, Gajewiak J, Rivier JE, Bulaj G, Olivera BM, Yoshikami D: Pharmacological fractionation of tetrodotoxin-sensitive sodium currents in rat dorsal root ganglion neurons by μ-conotoxins. British J. Pharmacology 2013, 169:102-114.
50. Faber CG, Lauria G, Merkies ISJ, Cheng X, Han C, Ahn HS, Persson AK, Hoeijmakers JGJ, Gerrits MM, Pierro T, Lombardi R, Kapetis D, Dib-Hajj SD Waxman SG: Gain-offunction Nav1.8 mutations in painful neuropathy. Proc. Natl. Acad. Sci. USA 2012, 109:19444-19449.
51. Heister E, Brunner EW, Dieckmann GR, Jurewicz I, Dalton AB: Are carbon nanotubes a natural solution? Applications in biology and medicine. ACS Appl Mater Interfaces 2013, 5:1870-1891.
52. Safo P, Rosenbaum T, Shcherbatko A, Choi DY, Han E, Toledo-Aral JJ, Olivera BM, Brehm P, Mendel G: Distinction among neuronal subtypes of voltage-activated sodium channels by μ-conotoxin PIIIA. J Neurosci 2000, 20:76-80.