α-conotoxin PeIA[S9H,V10A,E14N] potently and selectively blocks α6β2β3 versus α6β4 nicotinic acetylcholine receptors

Molecular Pharmacology

Volumn 82, Issue 5, 2012, Pages 972-982

  Hone, Arik J ^a   Scadden, Mick'l ^a   Gajewiak, Joanna ^a   Christensen, Sean ^a   Lindstrom, Jon ^c   McIntosh, J Michael ^a,b  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6BETA2BETA3 NICOTINIC ACETYLCHOLINE RECEPTOR; ALPHA6BETA4 NICOTINIC ACETYLCHOLINE RECEPTOR; CHOLINERGIC RECEPTOR BLOCKING AGENT; NICOTINIC RECEPTOR; PEIA [E14N]; PEIA [S9H]; PEIA [V10A]; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CHIMERA; CONTROLLED STUDY; DRUG POTENCY; DRUG SCREENING; DRUG SELECTIVITY; DRUG SYNTHESIS; IC 50; LIGAND BINDING; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; XENOPUS;

AMINO ACID SUBSTITUTION; ANIMALS; CONOTOXINS; FEMALE; HUMANS; MICE; MUTATION; NICOTINIC ANTAGONISTS; OOCYTES; PATCH-CLAMP TECHNIQUES; PROTEIN SUBUNITS; RATS; RECEPTORS, NICOTINIC; XENOPUS LAEVIS;

EID: 84867810291     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.080853     Document Type: Article

References (47)

1. Armishaw CJ (2010) Synthetic α-conotoxin mutants as probes for studying nicotinic acetylcholine receptors and in the development of novel drug leads. Toxins (Basel) 2:1471-1499.
2. Azam L, Maskos U, Changeux JP, Dowell CD, Christensen S, De Biasi M, and McIntosh JM (2010) α-Conotoxin BuIA[T5A;P6O]: a novel ligand that discriminates between α6β4 and α6α2 nicotinic acetylcholine receptors and blocks nicotine-stimulated norepinephrine release. FASEB J 24:5113-5123.
3. 3H]norepinephrine release from mouse hippocampal synaptosomes. Mol Pharmacol 70:967-976.
4. Azam L and McIntosh JM (2009) α-Conotoxins as pharmacological probes of nicotinic acetylcholine receptors. Acta Pharmacol Sin 30:771-783.
5. Azam L, Yoshikami D, and McIntosh JM (2008) Amino acid residues that confer high selectivity of the α6 nicotinic acetylcholine receptor subunit to α-conotoxin MII[S4A,E11A,L15A]. J Biol Chem 283:11625-11632.
6. Bibevski S, Zhou Y, McIntosh JM, Zigmond RE, and Dunlap ME(2000) Functional nicotinic acetylcholine receptors that mediate ganglionic transmission in cardiac parasympathetic neurons. J Neurosci 20:5076-5082. (Pubitemid 30421711)
7. Bordia T, Grady SR, McIntosh JM, and Quik M (2007) Nigrostriatal damage preferentially decreases a subpopulation of α6β2*nAChRs in mouse, monkey, and Parkinson's disease striatum. Mol Pharmacol 72:52-61. (Pubitemid 46998524)
8. Brunzell DH, Boschen KE, Hendrick ES, Beardsley PM, and McIntosh JM (2010) α-Conotoxin MII-sensitive nicotinic acetylcholine receptors in the nucleus accumbens shell regulate progressive ratio responding maintained by nicotine. Neuropsychopharmacology 35:665-673.
9. Capelli AM, Castelletti L, Chen YH, Van der Keyl H, Pucci L, Oliosi B, Salvagno C, Bertani B, Gotti C, Powell A, et al. (2011) Stable expression and functional characterization of a human nicotinic acetylcholine receptor with α6β2 properties: discovery of selective antagonists. Br J Pharmacol 163:313-329.
10. Cartier GE, Yoshikami D, Gray WR, Luo S, Olivera BM, and McIntosh JM (1996) A new α-conotoxin which targets α3β2 nicotinic acetylcholine receptors. J Biol Chem 271:7522-7528. (Pubitemid 26107027)
11. B receptor-coupled N-type calcium channels. J Biol Chem 286:10233-10237.
12. Dash B, Bhakta M, Chang Y, and Lukas RJ (2011) Identification of N-terminal extracellular domain determinants in nicotinic acetylcholine receptor (nAChR) α6 subunits that influence effects of wild-type or mutant α3 subunits on function of α6β2*- or α6β 4*-nAChR. J Biol Chem 286:37976-37989.
13. David R, Ciuraszkiewicz A, Simeone X, Orr-Urtreger A, Papke RL, McIntosh JM, Huck S, and Scholze P (2010) Biochemical and functional properties of distinct nicotinic acetylcholine receptors in the superior cervical ganglion of mice with targeted deletions of nAChR subunit genes. Eur J Neurosci 31:978-993.
14. Dowell C, Olivera BM, Garrett JE, Staheli ST, Watkins M, Kuryatov A, Yoshikami D, Lindstrom JM, and McIntosh JM (2003) α-Conotoxin PIA is selective for α6 subunit-containing nicotinic acetylcholine receptors. J Neurosci 23:8445-8452. (Pubitemid 37158743)
15. Exley R, Maubourguet N, David V, Eddine R, Evrard A, Pons S, Marti F, Threlfell S, Cazala P, McIntosh JM, et al. (2011) Distinct contributions of nicotinic acetylcholine receptor subunit α4 and subunit α6 to the reinforcing effects of nicotine. Proc Natl Acad Sci USA 108:7577-7582.
16. Gotti C, Guiducci S, Tedesco V, Corbioli S, Zanetti L, Moretti M, Zanardi A, Rimondini R, Mugnaini M, Clementi F, et al. (2010) Nicotinic acetylcholine receptors in the mesolimbic pathway: primary role of ventral tegmental area α6β2*receptors in mediating systemic nicotine effects on dopamine release, locomotion, and reinforcement. J Neurosci 30:5311-5325.
17. Grady SR, Salminen O, Laverty DC, Whiteaker P, McIntosh JM, Collins AC, and Marks MJ (2007) The subtypes of nicotinic acetylcholine receptors on dopaminergic terminals of mouse striatum. Biochem Pharmacol 74:1235-1246. (Pubitemid 47417935)
18. Hill JM, Oomen CJ, Miranda LP, Bingham JP, Alewood PF, and Craik DJ (1998) Three-dimensional solution structure of α-conotoxin MII by NMR spectroscopy: effects of solution environment on helicity. Biochemistry 37:15621-15630. (Pubitemid 28524732)
19. Hogg RC, Miranda LP, Craik DJ, Lewis RJ, Alewood PF, and Adams DJ (1999) Single amino acid substitutions in α-conotoxin PnIA shift selectivity for subtypes of the mammalian neuronal nicotinic acetylcholine receptor. J Biol Chem 274:36559-36564.
20. Hone AJ, Meyer EL, McIntyre M, and McIntosh JM (2012) Nicotinic acetylcholine receptors in dorsal root ganglion neurons include the α6β4*subtype. FASEB J 26:917-926.
21. Hone AJ, Whiteaker P, Christensen S, Xiao Y, Meyer EL, and McIntosh JM (2009) A novel fluorescent α-conotoxin for the study of α7 nicotinic acetylcholine receptors. J Neurochem 111:80-89.
22. Hu SH, Gehrmann J, Guddat LW, Alewood PF, Craik DJ, and Martin JL (1996) The 1.1 A crystal structure of the neuronal acetylcholine receptor antagonist, α-conotoxin PnIA from Conus pennaceus. Structure 4:417-423. (Pubitemid 126657536)
23. Jackson KJ, McIntosh JM, Brunzell DH, Sanjakdar SS, and Damaj MI (2009) The role of α6-containing nicotinic acetylcholine receptors in nicotine reward and withdrawal. J Pharmacol Exp Ther 331:547-554.
24. Jones IW and Wonnacott S (2004) Precise localization of α7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J Neurosci 24:11244-11252. (Pubitemid 39658259)
25. Kuryatov A and Lindstrom J (2011) Expression of functional human α6β2β3*acetylcholine receptors in Xenopus laevis oocytes achieved through subunit chimeras and concatamers. Mol Pharmacol 79:126-140.
26. Kuryatov A, Olale F, Cooper J, Choi C, and Lindstrom J (2000) Human α6 AChR subtypes: subunit composition, assembly, and pharmacological responses. Neuropharmacology 39:2570-2590.
27. Léna C, de Kerchove D'Exaerde A, Cordero-Erausquin M, Le Novère N, del Mar Arroyo-Jimenez M, and Changeux JP (1999) Diversity and distribution of nicotinic acetylcholine receptors in the locus ceruleus neurons. Proc Natl Acad Sci USA 96:12126-12131. (Pubitemid 29502869)
28. Letchworth SR and Whiteaker P (2011) Progress and challenges in the study of α6-containing nicotinic acetylcholine receptors. Biochem Pharmacol 82:862-872.
29. Liu L, Zhao-Shea R, McIntosh JM, Gardner PD, and Tapper AR (2012) Nicotine persistently activates ventral tegmental area dopaminergic neurons via nicotinic acetylcholine receptors containing α4 and α6 subunits. Mol Pharmacol 81:541-548.
30. Luo S, Nguyen TA, Cartier GE, Olivera BM, Yoshikami D, and McIntosh JM (1999) Single-residue alteration in α-conotoxin PnIA switches its nAChR subtype selectivity. Biochemistry 38:14542-14548.
31. Mao D, Yasuda RP, Fan H, Wolfe BB, and Kellar KJ (2006) Heterogeneity of nicotinic cholinergic receptors in rat superior cervical and nodose ganglia. Mol Pharmacol 70:1693-1699.
32. Marritt AM, Cox BC, Yasuda RP, McIntosh JM, Xiao Y, Wolfe BB, and Kellar KJ (2005) Nicotinic cholinergic receptors in the rat retina: simple and mixed heteromeric subtypes. Mol Pharmacol 68:1656-1668. (Pubitemid 41654349)
33. McIntosh JM, Azam L, Staheli S, Dowell C, Lindstrom JM, Kuryatov A, Garrett JE, Marks MJ, and Whiteaker P (2004) Analogs of α-conotoxin MII are selective for α6-containing nicotinic acetylcholine receptors. Mol Pharmacol 65:944-952. (Pubitemid 38420500)
34. McIntosh JM, Plazas PV, Watkins M, Gomez-Casati ME, Olivera BM, and Elgoyhen AB (2005) A novel α-conotoxin, PeIA, cloned from Conus pergrandis, discriminates between rat α9α10 and α7 nicotinic cholinergic receptors. J Biol Chem 280:30107-30112. (Pubitemid 41216187)
35. Moretti M, Vailati S, Zoli M, Lippi G, Riganti L, Longhi R, Viegi A, Clementi F, and Gotti C (2004) Nicotinic acetylcholine receptor subtypes expression during rat retina development and their regulation by visual experience. Mol Pharmacol 66:85-96. (Pubitemid 38822090)
36. Papke RL, Buhr JD, Francis MM, Choi KI, Thinschmidt JS, and Horenstein NA (2005) The effects of subunit composition on the inhibition of nicotinic receptors by the amphipathic blocker 2,2,6,6-tetramethylpiperidin-4-yl heptanoate. Mol Pharmacol 67:1977-1990. (Pubitemid 41007779)
37. Perez XA, Bordia T, McIntosh JM, Grady SR, and Quik M (2008) Long-term nicotine treatment differentially regulates striatal α6α4β 2*and α6(nonα4)β2*nAChR expression and function. Mol Pharmacol 74:844-853.
38. Pérez-Alvarez A, Hernández-Vivanco A, McIntosh JM, and Albillos A (2012) Native α6β4*nicotinic receptors control exocytosis in human chromaffin cells of the adrenal gland. FASEB J 26:346-354.
39. 3H]dopamine release. Eur J Pharmacol 658:132-139.
40. Pons S, Fattore L, Cossu G, Tolu S, Porcu E, McIntosh JM, Changeux JP, Maskos U, and Fratta W (2008) Crucial role of α4 and α6 nicotinic acetylcholine receptor subunits from ventral tegmental area in systemic nicotine self-administration. J Neurosci 28:12318-12327.
41. Pucci L, Grazioso G, Dallanoce C, Rizzi L, De Micheli C, Clementi F, Bertrand S, Bertrand D, Longhi R, De Amici M, et al.(2011) Engineering of α-conotoxin MII-derived peptides with increased selectivity for native α6β2*nicotinic acetylcholine receptors. FASEB J 25:3775-3789.
42. Quik M, Polonskaya Y, Gillespie A, Jakowec M, Lloyd GK, and Langston JW (2000) Localization of nicotinic receptor subunit mRNAs in monkey brain by in situ hybridization. J Comp Neurol 425:58-69.
43. Rogers JP, Luginbühl P, Shen GS, McCabe RT, Stevens RC, and Wemmer DE (1999) NMR solution structure of α-conotoxin ImI and comparison to other conotoxins specific for neuronal nicotinic acetylcholine receptors. Biochemistry 38:3874-3882.
44. Vincler MA and Eisenach JC (2003) Immunocytochemical localization of the α3, α4, α5, α7, β2, β3 and β4 nicotinic acetylcholine receptor subunits in the locus coeruleus of the rat. Brain Res 974:25-36. (Pubitemid 36549217)
45. Wooltorton JR, Pidoplichko VI, Broide RS, and Dani JA (2003) Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci 23:3176-3185.
46. Wu J, George AA, Schroeder KM, Xu L, Marxer-Miller S, Lucero L, and Lukas RJ (2004) Electrophysiological, pharmacological, and molecular evidence for α7-nicotinic acetylcholine receptors in rat midbrain dopamine neurons. J Pharmacol Exp Ther 311:80-91. (Pubitemid 39287786)
47. Yang K, Hu J, Lucero L, Liu Q, Zheng C, Zhen X, Jin G, Lukas RJ, and Wu J (2009) Distinctive nicotinic acetylcholine receptor functional phenotypes of rat ventral tegmental area dopaminergic neurons. J Physiol 587:345-361.