Weak toxin WTX from Naja kaouthia cobra venom interacts with both nicotinic and muscarinic acetylcholine receptors

FEBS Journal

Volumn 276, Issue 18, 2009, Pages 5065-5075

  Mordvintsev, Dmitry Yu ^a   Polyak, Yakov L ^a,d   Rodionov, Dmitry I ^a,e   Jakubik, Jan ^b   Dolezal, Vladimir ^b   Karlsson, Evert ^c   Tsetlin, Victor I ^a   Utkin, Yuri N ^a  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b Institute of Physiology   (Czech Republic)

^c Institute of Biochemistry and Organic Chemistry   (Sweden)

^d MAX PLANCK INSTITUT FÜR KOHLENFORSCHUNG   (Germany)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

Muscarinic acetylcholine receptor; Nicotinic acetylcholine receptor; Snake venom; Weak neurotoxin

Indexed keywords

ACETYLCHOLINE; ATROPINE; BUNGAROTOXIN RECEPTOR; COBROTOXIN; G PROTEIN COUPLED RECEPTOR; IODINE 125; METHYLSCOPOLAMINE; MUSCARINIC M1 RECEPTOR; MUSCARINIC M4 RECEPTOR; MUSCARINIC M5 RECEPTOR; MUSCARINIC RECEPTOR; OXOTREMORINE; RECEPTOR SUBTYPE; SNAKE VENOM; TRITIUM;

ADRENAL GLAND; ALLOSTERISM; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; CHO CELL; CONTROLLED STUDY; FEMALE; ISOTOPE LABELING; MALE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR AFFINITY; RECEPTOR BINDING;

ACETYLCHOLINE; ADRENAL GLANDS; ANIMALS; CHO CELLS; COBRA VENOMS; CRICETINAE; CRICETULUS; FEMALE; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); MALE; MICE; N-METHYLSCOPOLAMINE; RATS; RATS, WISTAR; RECEPTORS, MUSCARINIC; RECEPTORS, NICOTINIC;

CRICETULUS GRISEUS; DENDROASPIS ANGUSTICEPS; MUS; NAJA KAOUTHIA; RATTUS;

EID: 69449092043     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07203.x     Document Type: Article

References (46)

1. Tsetlin VI (1999) Snake venom alpha-neurotoxins and other 'three-finger' proteins. Eur J Biochem 264, 281 286.
2. Karlsson E, Jolkkonen M, Mulugeta E, Onali P Adem A (2000) Snake toxins with high selectivity for subtypes of muscarinic acetylcholine receptors. Biochimie 82, 793 806.
3. Nirthanan S Gwee MC (2004) Three-finger alpha-neurotoxins and the nicotinic acetylcholine receptor, forty years on. J Pharmacol Sci 94, 1 17.
4. Tsetlin VI Hucho F (2004) Snake and snail toxins acting on nicotinic acetylcholine receptors: fundamental aspects and medical applications. FEBS Lett 557, 9 13.
5. Nirthanan S, Gopalokrishnakope P, Gwee MCE, Khoo HE Kini RM (2003) Non-conventional toxins from Elapidae venoms. Toxicon 41, 397 407.
6. Utkin YN, Kukhtina VV, Kryukova EV, Chiodini F, Bertrand D, Methfessel C Tsetlin VI (2001) Weak toxin from Naja kaouthia is a nontoxic antagonist of α 7 and muscle-type nicotinic acetylcholine receptors. J Biol Chem 276, 15810 15815.
7. Chang LS, Lin SR, Wang JJ, Hu WP, Wu BN Huang HB (2000) Structure-function studies on Taiwan cobra long neurotoxin homologue. Biochim Biophys Acta 1480, 293 301.
8. Chang LS, Chung C, Wu B Yang C (2002) Characterization and gene organization of Taiwan banded krait (Bungarus multicinctus) γ- bungarotoxin. J Protein Chem 21, 223 229. (Pubitemid 34839919)
9. Poh SL, Mourier G, Thai R, Armugam A, Molgo J, Servent D, Jeyaseelan K Menez A (2002) A synthetic weak neurotoxin binds with low affinity to Torpedo and chicken α7 nicotinic acetylcholine receptor. Eur J Biochem 269, 4247 4256.
10. Nirthanan S, Charpantier E, Gopalakrishnakone P, Gwee MCE, Khoo HE, Ceah LS, Kini RM Bertrand D (2003) Neuromuscular effects of candoxin, a novel toxin from the venom of the Malayan krait (Bungarus candidus). Br J Pharmacol 139, 832 844. (Pubitemid 36819611)
11. Adermann K, Wattler F, Wattler S, Heine G, Meyer M, Forssmann WG Nehls M (1999) Structural and phylogenetic characterization of human SLURP-1, the first secreted mammalian member of the Ly-6/uPAR protein superfamily. Protein Sci 8, 810 819.
12. Miwa JM, Ibañez-Tallon I, Grabtree GW, Sanchez R, Sali A, Role LW Heintz N (1999) Lynx 1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 23, 105 114.
13. Mordvintsev DY, Rodionov DI, Makarova MV, Kamensky AA, Levitskaya NG, Ogay AY, Rzhevsky DI, Murashev AN, Tsetlin VI Utkin YN (2007) Behavioural effects in mice and intoxication symptomatology of weak neurotoxin from cobra Naja kaouthia. Basic Clin Pharmacol Toxicol 100, 273 278.
14. Ogay AY, Rzhevsky DI, Murashev AN, Tsetlin VI Utkin YN (2005) Weak neurotoxin from Naja kaouthia cobra venom affects haemodynamic regulation by acting on acetylcholine receptors. Toxicon 45, 93 99.
15. Criado M, Domínguez del Toro E, Carrasco-Serrano C, Smillie FI, Juíz JM, Viniegra S Ballesta JJ (1997) Differential expression of alpha-bungarotoxin-sensitive neuronal nicotinic receptors in adrenergic chromaffin cells: a role for transcription factor Egr-1. J Neurosci 17, 6554 6564.
16. Di Angelantonio S, Matteoni C, Fabbretti E Nistri A (2003) Molecular biology and electrophysiology of neuronal nicotinic receptors of rat chromaffin cells. Eur J Neurosci 17, 2313 2322.
17. Campos-Caro A, Smillie FI, DomInguez del Toro E, Rovira JC, Vicente-Agulló F, Chapuli J, Julz M, Sala S, Sala F, Ballesta JJ et al. (1997) Neuronal nicotinic acetylcholine receptors on bovine chromaffin cells: cloning, expression, and genomic organization of receptor subunits. J Neurochem 68, 488 497.
18. Garcia-Guzman M, Sala F, Sala S, Campos-Caro A, Stuhmer W, Gutierrez LM Criado M (1995) alpha-Bungarotoxin-sensitive nicotinic receptors on bovine chromaffin cells: molecular cloning, functional expression and alternative splicing of the alpha 7 subunit. Eur J Neurosci 7, 647 655.
19. Maneu V, Roje J, Mulet J, Valor ML, Sala F, Criada M, Garcia AG Candia L (2002) A single neuronal acetylcholine receptor α3α7α4* is present in bovine chromaffin cells. Ann NY Acad Sci 971, 165 167.
20. Mordvintsev DY, Polyak YL, Kuzmin DA, Levtsova OV, Tourleigh YV, Utkin YN, Shaitan KV Tsetlin VI (2007) Computer modeling of binding of diverse weak toxins to nicotinic acetylcholine receptors. Comput Biol Chem 31, 72 81.
21. Kornisiuk E, Jerusalinsky D, Cervenansky C Harvey AL (1995) Binding of muscarinic toxins MTx1 and MTx2 from the venom of the green mamba Dendroaspis angusticeps to cloned human muscarinic cholinoceptors. Toxicon 33, 11 18.
22. Harvey AL, Kornisiuk E, Bradley KN, Cerveñansky C, Durán R, Adrover M, Sanchez G Jerusalinsky D (2002) Effects of muscarinic toxins MT1 and MT2 from green mamba on different muscarinic cholinoceptors. Neurochem Res 27, 1543 1554.
23. Olianas MC, Ingianni A, Maullu C, Adem A, Karlsson E Onali P (1999) Selectivity profile of muscarinic toxin 3 in functional assays of cloned and native receptors. J Pharmacol Exp Ther 288, 164 170.
24. Tobin JR, Breslow MJ Traystman RJ (1992) Muscarinic cholinergic receptors in canine adrenal gland. Am J Physiol 263, H1208 H1212.
25. Ballesta JJ, Borges R, García AG Hidalgo MJ (1989) Secretory and radioligand binding studies on muscarinic receptors in bovine and feline chromaffin cells. J Physiol 418, 411 426.
26. Barbara JG, Lemos VS Takeda K (1998) Pre- and post-synaptic muscarinic receptors in thin slices of rat adrenal gland. Eur J Neurosci 10, 3535 3545.
27. Janossy A, Orso E, Szalay KS, Juranyi Z, Beck M, Vizi ES Vinson GP (1998) Cholinergic regulation of the rat adrenal zona glomerulosa. J Endocrinol 157, 305 315.
28. Tucek S Proska J (1995) Allosteric modulation of muscarinic acetylcholine receptors. Trends Pharmacol Sci 16, 205 212.
29. Birdsall NJ Lazareno S (2005) Allosterism at muscarinic receptors: ligands and mechanisms. Mini Rev Med Chem 5, 523 543.
30. Jakubik J, Krejci A Dolezal V (2005) Asparagine, valine, and threonine in the third extracellular loop of muscarinic receptor have essential roles in the positive cooperativity of strychnine-like allosteric modulators. J Pharmacol Exp Ther 313, 688 696.
31. Gregory KJ, Sexton PM Christopoulos A (2007) Allosteric modulation of muscarinic acetylcholine receptors. Curr Neuropharmacol 5, 157 167. (Pubitemid 351863857)
32. Fruchart-Gaillard C, Mourier G, Marquer C, Stura E, Birdsall NJ Servent D (2008) Different interactions between MT7 toxin and the human muscarinic M1 receptor in its free and NMS-occupied states. Mol Pharmacol 74, 1554 1563.
33. Jakubik J, Bacakova L, Lisa V, el-Fakahany EE Tucek S (1996) Activation of muscarinic acetylcholine receptors via their allosteric binding sites. Proc Natl Acad Sci USA 93, 8705 8709.
34. Kenakin T (2007) Allosteric agonist modulators. J Recept Signal Transduct Res 27, 247 259.
35. Lazareno S, Dolezal V, Popham A Birdsall NJ (2004) Thiochrome enhances acetylcholine affinity at muscarinic M4 receptors: receptor subtype selectivity via cooperativity rather than affinity. Mol Pharmacol 65, 257 266.
36. Thomas RL, Mistry R, Langmead CJ, Wood MD Challiss RA (2008) G protein coupling and signaling pathway activation by m1 muscarinic acetylcholine receptor orthosteric and allosteric agonists. J Pharmacol Exp Ther 327, 365 374.
37. Machova E, Jakubik J, El-Fakahany EE Dolezal V (2007) Wash-resistantly bound xanomeline inhibits acetylcholine release by persistent activation of presynaptic M(2) and M(4) muscarinic receptors in rat brain. J Pharmacol Exp Ther 322, 316 323.
38. Fry BG (2005) From genome to 'venome': molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res 15, 403 420.
39. Kryukova EV, Mordvintsev DY, Daya S, Utkin YN Tsetlin VI (2005) Polyclonal antibodies against native weak toxin Naja kaouthia discriminate native weak toxins and some other three-fingered toxins against their denaturated forms. Toxicon 46, 24 30.
40. Evenas J, Malmendal A Forsen S (1998) Calcium. Curr Opin Chem Biol 2, 293 302.
41. Brini M Carafoli E (2000) Calcium signaling: a historical account, recent developments and future perspectives. Cell Mol Life Sci 57, 354 370.
42. Carafoli E (2002) Calcium signaling: a tale for all seasons. Proc Natl Acad Sci USA 99, 1115 1122.
43. Wang GK Schmidt J (1980) Primary structure and binding properties of iodinated derivatives of alpha-bungarotoxin. J Biol Chem 255, 11156 11162.
44. Maeda T, Balakrishnan K Mehdi SQ (1983) A simple and rapid method for the preparation of plasma membranes. Biochim Biophys Acta 731, 115 120.
45. Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83, 346 356.
46. Jakubik J, El-Fakahany EE Dolezal V (2006) Differences in kinetics of xanomeline binding and selectivity of activation of G proteins at M(1) and M(2) muscarinic acetylcholine receptors. Mol Pharmacol 70, 656 666.