Pharmacological insights and quirks of bacterial sodium channels

Handbook of Experimental Pharmacology

Volumn 221, Issue , 2014, Pages 251-267

  Corry, Ben ^a   Lee, Sora ^b   Ahern, Christopher A ^b  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Bacteria; Modulation; PH homeostasis; Pharmacology

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL; BACTERIAL PROTEIN; LOCAL ANESTHETIC AGENT; SODIUM; SODIUM CHANNEL; SODIUM CHANNEL BLOCKING AGENT;

ARTICLE; BINDING AFFINITY; CHANNEL GATING; CONFORMATIONAL TRANSITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; MEMBRANE POTENTIAL; METABOLISM; PROTEIN CONFORMATION; REVIEW; STRUCTURE ACTIVITY RELATION;

ANESTHETICS, LOCAL; BACTERIAL PROTEINS; ION CHANNEL GATING; MEMBRANE POTENTIALS; MODELS, MOLECULAR; PROTEIN CONFORMATION; SODIUM; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84903908270     PISSN: 01712004     EISSN: 18650325     Source Type: Book Series    
DOI: 10.1007/978-3-642-41588-3_12     Document Type: Article

References (78)

1. Abu-Qarn M, Eichler J, Sharon N (2008) Not just for Eukarya anymore: protein glycosylation in Bacteria and Archaea. Curr Opin Struct Biol 18:544-550
2. AHERN GP, Hsu SF, Klyachko VA, Jackson MB (2000) Induction of persistent sodium current by exogenous and endogenous nitric oxide. J Biol Chem 275:28810-28815
3. Ahern CA, Zhang JF, Wookalis MJ, Horn R (2005) Modulation of the cardiac sodium channel NaV1.5 by Fyn, a Src family tyrosine kinase. Circ Res 96:991-998
4. Ahern CA, Eastwood AL, Dougherty DA, Horn R (2008) Electrostatic contributions of aromatic residues in the local anesthetic receptor of voltage-gated sodium channels. Circ Res 102:86-94
5. Alberola-Die A, Martinez-Pinna J, Gonzalez-Ros JM, Vorra I, Morales A (2011) Multiple inhibitory actions of lidocaine on Torpedo nicotinic acetylcholine receptors transplanted to Xenopus oocytes. J Neurochem 117:1009-1019
6. Berry A, Janssens D, Humbelin M, Jore JPM, Hoste B, Cleenwerck I, Vancanneyt M, Bretzel W, Mayer AF, Lopez-Ulibarri R et al (2003) Paracoccus zeaxanthinifaciens sp. nov, a zeaxanthinproducing bacterium. Int J Syst Evol Microbiol 53:231-238
7. Blakemore R (1975) Magnetotactic bacteria. Science 190:377-379
8. Blanchet J, Chahine M (2007) Accessibility of four arginine residues on the S4 segment of the Bacillus halodurans sodium channel. J Membr Biol 215:169-180
9. Blanchet J, Pilote S, Chahine M (2007) Acidic residues on the voltage-sensor domain determine the activation of the NaChBac sodium channel. Biophys J 92:3513-3523
10. Booth IR (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49:359-378
11. Brohawn SG, Del Marmol J, Mackinnon R (2012) Crystal structure of the human K2P TRAAK, a lipid-and mechano-sensitive K + ion channel. Science 335:436-441
12. Choi KL, Aldrich RW, Yellen G (1991) Tetraethylammonium blockade distinguishes two inactivation mechanisms in voltage-activated K + channels. Proc Natl Acad Sci U S A 88:5092-5095
13. Costa MR, Catterall WA (1984) Cyclic AMP-dependent phosphorylation of the alpha subunit of the sodium channel in synaptic nerve ending particles. J Biol Chem 259:8210-8218
14. Deutscher J, Saier MH (2005) Ser/Thr/Tyr protein phosphorylation in bacteria-for long time neglected, now well established. J Mol Microbiol Biotechnol 9:125-131
15. Dimroth P, Cook GM (2004) Bacterial Na+-or H+-coupled ATP synthases operating at low electrochemical potential. Adv Microb Physiol 49:175-218
16. Fredrickson JK, Zachara JM, Kennedy DW, Dong H, Onstott TC, Hinman NW, Li S (1998) Biogenic iron mineralization accompanying the dissimilatory reduction of hydrous ferric oxide by a groundwater bacterium. Geochim Cosmochim Acta 62:3239-3257
17. Gingrich KJ, Beardsley D, Yue DT (1993) Ultra-deep blockade of Na + channels by a quaternary ammonium ion: catalysis by a transition-intermediate state? J Physiol 471:319-341
18. González JM, Covert JS, Whitman WB, Henriksen JR, Mayer F, Scharf B, Schmitt R, Buchan A, Fuhrman JA, Kiene RP et al (2003) Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int J Syst Evol Microbiol 53:1261-1269
19. Hille B (1968) Charges and potentials at the nerve surface. Divalent ions and pH. J Gen Physiol 51:221-236
20. Hille B (1977a) Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 69:497-515
21. Hille B (1977b) The pH-dependent rate of action of local anesthetics on the node of Ranvier. J Gen Physiol 69:475-496
22. Hockerman GH, PETERSON BZ, Johnson BD, Catterall WA (1997) Molecular determinants of drug binding and action on L-type calcium channels. Annu Rev Pharmacol Toxicol 37: 361-396
23. Irie K, Kitagawa K, Nagura H, Imai T, Shimomura T, Fujiyoshi Y (2010) Comparative study of the gating motif and C-type inactivation in prokaryotic voltage-gated sodium channels. J Biol Chem 285:3685-3694
24. Ito M, Xu H, Guffanti AA, Wei Y, Zvi L, Clapham DE, Krulwich TA (2004) The voltage-gated Na+ channel NaVBP has a role in motility, chemotaxis, and pH homeostasis of an alkaliphilic Bacillus. Proc Natl Acad Sci USA 101:10566-10571
25. Isom LL, DE Jongh KS, Patton DE, Reber BF, Offord J, Charbonneau H, Walsh K, Goldin AL, Catterall WA (1992) Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science 256:839-842
26. Josephson IR (1988) Lidocaine blocks Na, Ca and K currents of chick ventricular myocytes. J Mol Cell Cardiol 20:593-604
27. Kassmann M, Hansel A, Leipold E, Birkenbeil J, Lu S, Hoshi T, Heinemann SH (2008) Oxidation of multiple methionine residues impairs rapid sodium channel inactivation. Pflugers Arch 456:1085-1095
28. Kimbrough JT, Gingrich KJ (2000) Quaternary ammonium block of mutant Na + channels lacking inactivation: features of a transition-intermediate mechanism. J Physiol 529(Pt 1):93-106
29. Kindler CH, Paul M, Zou H, Liu C, Winegar BD, Gray AT, Yost CS (2003) Amide local anesthetics potently inhibit the human tandem pore domain background K + channel TASK-2 (KCNK5). J Pharmacol Exp Ther 306:84-92
30. Koishi R, Xu H, Ren D, Navarro B, Spiller BW, Shi Q, Clapham DE (2004) A superfamily of voltage-gated sodium channels in bacteria. J Biol Chem 279:9532-9538
31. Kralj JM, Hochbaum DR, Douglass AD, Cohen AE (2011) Electrical spiking in Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333:345-348
32. Krulwich TA, Guffanti AA (1989) Alkalophilic bacteria. Annu Rev Microbiol 43:435-463
33. Krulwich TA, Ito M, Gilmour R, Guffanti AA (1997) Mechanisms of cytoplasmic pH regulation in alkaliphilic strains of Bacillus. Extremophiles 1:163-169
34. Lee S, Goodchild SJ, Ahern CA (2012a) Local anesthetic inhibition of a bacterial sodium channel. J Gen Physiol 139:507-516
35. Lee S, Goodchild SJ, Ahern CA (2012b) Molecular and functional determinants of local anesthetic inhibition of NaChBac. Channels 6:403-406
36. Lipkind GM, Fozzard HA (2010) Molecular model of anticonvulsant drug binding to the voltagegated sodium channel inner pore. Mol Pharmacol 78:631-638
37. Liu CJ, Dib-Hajj SD, Renganathan M, Cummins TR, Waxman SG (2003) Modulation of the cardiac sodium channel Nav1.5 by fibroblast growth factor homologous factor 1B. J Biol Chem 278:1029-1036
38. Long SB, Tao X, Campbell EB, Mackinnon R (2007) Atomic structure of a voltage-dependent K+ channelinalipidmembrane-likeenvironment.Nature 450:376-382
39. Mager T, Rimon A, Padan E, Fendler K (2011) Transport mechanism and pH regulation of the Na+/H+ antiporter NhaA from Escherichia coli. J Biol Chem 286:23570-23581
40. Mandel KG, Guffanti AA, Krulwich TA (1980) Monovalent cation/proton antiporters in membrane vesicles from Bacillus alcalophilus. J Biol Chem 255:7391-7396
41. McCusker EC, Bagnéris C, Naylor CE, Cole AR, D’Avanzo N, Nichols CG, Wallace BA (2012) Structure of a bacterial voltage-gated sodium channel pore reveals mechanisms of opening and closing. Nat Commun 3:1102
42. McLaggan D, Selwyn MJ, Dawson AP (1984) Dependence on Na+ of control of cytoplasmic pH in a facultative alkalophile. FEBS Lett 165:254-258
43. Mcnulty MM, Edgerton GB, Shah RD, Hanck DA, Fozzard HA, Lipkind GM (2007) Charge at the lidocaine binding site residue Phe-1759 affects permeation in human cardiac voltage-gated sodium channels. J Physiol 581:741-755
44. Miller WG, Parker CT, Rubenfield M, Mendz GL, Wosten MMSM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G et al (2007) The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS One 2:e1358
45. Mozhayeva GN, Naumov AP, Nosyreva ED (1984) A study on the potential-dependence of proton block of sodium channels. Biochim Biophys Acta 775:435-440
46. Nardi A, Damann N, Hertrampf T, Kless A (2012) Advances in targeting voltage-gated sodium channels with small molecules. ChemMedChem 7:1712-1740
47. Nielsen P, Fritze D, Priest FG (1995) Phenetic diversity of alkaliphilic Bacillus strains: proposal for nine new species. Microbiology 141:1745-1761
48. Olschewski A, Brau ME, Olschewski H, Hempelmann G, Vogel W (1996) ATP-dependent potassium channel in rat cardiomyocytes is blocked by lidocaine. Possible impact on the antiarrhythmic action of lidocaine. Circulation 93:656-659
49. Paul AA, Witchel HJ, Hancox JC (2002) Inhibition of the current of heterologously expressed HERG potassium channels by flecainide and comparison with quinidine, propafenone and lignocaine. Br J Pharmacol 136:717-729
50. Pavlov E, Bladen C, Winkfein R, Diao C, Dhaliwal P, French RJ (2005) The pore, not cytoplasmic domains, underlies inactivation in a prokaryotic sodium channel. Biophys J 89:232-242
51. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353-358
52. Payandeh J, El-Din TMG, Scheuer T, Zheng N, Catterall WA (2012a) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486:135-U166
53. Payandeh J, Gamal El-Din TM, Scheuer T, Zheng N, Catterall WA (2012b) Crystal structure of a voltagegated sodium channel in two potentially inactivated states. Nature 486:135-139
54. Pless SA, Galpin JD, Frankel A, Ahern CA (2011) Molecular basis for class Ib anti-arrhythmic inhibition of cardiac sodium channels. Nat Commun 2:351
55. Ragsdale DS, Mcphee JC, Scheuer T, Catterall WA (1994a) Molecular determinants of state- dependent block of Na + channels by local anesthetics. Science 265:1724-1728
56. Ragsdale DS, Mcphee JC, Scheuer T, Catterall WA (1994b) Molecular determinants of state- dependent block of Na + channels by local-anesthetics. Science 265:1724-1728
57. Ragsdale DS, Mcphee JC, Scheuer T, Catterall WA (1996) Common molecular determinants of local anesthetic, antiarrhythmic, and anticonvulsant block of voltage-gated Na + channels. Proc Natl Acad Sci U S A 93:9270-9275
58. Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science 294:2372-2375
59. Renganathan M, Cummins TR, Waxman SG (2002) Nitric oxide blocks fast, slow, and persistent Na + channels in C-type DRG neurons by S-nitrosylation. J Neurophysiol 87:761-775
60. Rey MW, Ramaiya P, Nelson BA, Brody-Karpin SD, Zaretsky EJ, Tang M, de Leon AL, Xiang H, Gusti V, Clausen IG et al (2004) Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillus species. Genome Biol 5: r77
61. Scheuer T (2011) Regulation of sodium channel activity by phosphorylation. Semin Cell Dev Biol 22:160-165
62. Schmidt JW, Catterall WA (1987) Palmitylation, sulfation, and glycosylation of the alpha subunit of the sodium channel. Role of post-translational modifications in channel assembly. J Biol Chem 262:13713-13723
63. Shiba T (1991) Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a. Syst Appl Microbiol 14:140-145
64. Shin KS, Maertens C, Proenza C, Rothberg BS, Yellen G (2004) Inactivation in HCN channels results from reclosure of the activation gate: desensitization to voltage. Neuron 41:737-744
65. Sugimoto M, Uchida I, Fukami S, Takenoshita M, Mashimo T, Yoshiya I (2000) The alpha and gamma subunit-dependent effects of local anesthetics on recombinant GABA(A) receptors. Eur J Pharmacol 401:329-337
66. Sugiyama S (1995) Na+ driven flagellar motors as a likely Na+ re-entry pathway in alkaliphilic bacteria. Mol Microbiol 15:592
67. Tan HL, Kupershmidt S, Zhang R, Stepanovic S, Roden DM, Wilde AA, Anderson ME, Balser JR (2002) A calcium sensor in the sodium channel modulates cardiac excitability. Nature 415:442-447
68. Takami H, Nogi Y, Horikoshi K (1999) Reidentification of the keratinase-producing facultatively alkaliphilic Bacillus sp. AH-101 as Bacillus halodurans. Extremophiles 3:293-296
69. Trellakis S, Benzenberg D, Urban BW, Friederich P (2006) Differential lidocaine sensitivity of human voltage-gated potassium channels relevant to the auditory system. Otol Neurotol 27:117-123
70. Ulmschneider MB, Bagnéris C, McCusker EC, DeCaen PG, Delling M, Clapham DE, Ulmschneider JP, Wallace BA (2013) Molecular dynamics of ion transport through the open conformation of a bacterial voltage-gated sodium channel. Proc Natl Acad Sci USA 110:6364-6369
71. Van Petegem F, Lobo PA, Ahern CA (2012) Seeing the forest through the trees: towards a unified view on physiological calcium regulation of voltage-gated sodium channels. Biophys J 103:2243-2251
72. Waters MF, Minassian NA, Stevanin G, Figueroa KP, Bannister JP, Nolte D, Mock AF, Evidente VG, Fee DB, Muller U, Durr A, Brice A, Papazian DM, Pulst SM (2006) Mutations in voltage-gated potassium channel KCNC3 cause degenerative and developmental central nervous system phenotypes. Nat Genet 38:447-451
73. West JW, Patton DE, Scheuer T, Wang Y, Goldin AL, Catterall WA (1992) A cluster of hydrophobic amino acid residues required for fast Na(+)-channel inactivation. Proc Natl Acad Sci U S A 89:10910-10914
74. Whorton MR, Mackinnon R (2011) Crystal structure of the mammalian GIRK2 K + channel and gating regulation by G proteins, PIP2, and sodium. Cell 147:199-208
75. Zamponi GW, Doyle DD, French RJ (1993) Fast lidocaine block of cardiac and skeletal muscle sodium channels: one site with two routes of access. Biophys J 65:80-90
76. Zhang X, Ren W, Decaen P, Yan C, Tao X, Tang L, Wang J, Hasegawa K, Kumasaka T, HE J, Clapham DE, Yan N (2012a) Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486:130-134
77. Zhang X, Ren WL, Decaen P, Yan CY, Tao X, Tang L, Wang JJ, Hasegawa K, Kumasaka T, He JH, Wang JW, Clapham DE, Yan N (2012b) Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel. Nature 486:130-U160
78. Zhou Y, Morais-Cabral JH, Kaufman A, Mackinnon R (2001) Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 A resolution. Nature 414:43-48