Identification of a novel snake peptide toxin displaying high affinity and antagonist behaviour for the α 2-adrenoceptors

British Journal of Pharmacology

Volumn 161, Issue 6, 2010, Pages 1361-1374

  Rouget, Céline ^a   Quinton, Loïc ^b   Maïga, Arhamatoulaye ^a   Gales, Céline ^c   Masuyer, Geoffrey ^d   Malosse, Christian ^e   Chamot Rooke, Julia ^e   Thai, Robert ^a   Mourier, Gilles ^a   De Pauw, Edwin ^b   Gilles, Nicolas ^a   Servent, Denis ^a  

^a SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c INSERM   (France)

^d University of Bath   (United Kingdom)

^e LABORATOIRE HÉTÉROÉLÉMENTS ET COORDINATION   (France)

Author keywords

2 adrenoceptor antagonists; Binding experiments; Mass fragmentation; Snake venoms; Three finger fold toxins; Venom fractionation

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; PEPTIDE RHO DA1B; SNAKE VENOM; UNCLASSIFIED DRUG; YOHIMBINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN SYNAPTOSOME; CHO CELL; DENDROASPIS; DRUG ANTAGONISM; DRUG RECEPTOR BINDING; FEMALE; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SNAKE;

ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; AMINO ACID SEQUENCE; ANIMALS; BINDING, COMPETITIVE; CERCOPITHECUS AETHIOPS; COS CELLS; ELAPID VENOMS; ELAPIDAE; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2;

EID: 78049397452     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2010.00966.x     Document Type: Article

References (58)

1. Adem A, Asblom A, Johansson G, Mbugua PM, Karlsson E (1988). Toxins from the venom of the green mamba Dendroaspis angusticeps that inhibit the binding of quinuclidinyl benzilate to muscarinic acetylcholine receptors. Biochim Biophys Acta 968: 340-345.
2. Agrawal DK, Triggle CR, Daniel EE (1984). Pharmacological characterization of the postsynaptic alpha adrenoceptors in vascular smooth muscle from canine and rat mesenteric vascular beds. J Pharmacol Exp Ther 229: 831-838.
3. Alexander SP, Mathie A, Peters JA (2009). Guide to Receptors and Channels (GRAC). 4th edn. Br J Pharmacol 158 (Suppl. 1): S1-S254.
4. Antosova Z, Mackova M, Kral V, Macek T (2009). Therapeutic application of peptides and proteins: parenteral forever? Trends Biotechnol 27: 628-635.
5. Banerjee Y, Mizuguchi J, Iwanaga S, Kini RM (2005). Hemextin AB complex, a unique anticoagulant protein complex from Hemachatus haemachatus (African Ringhals cobra) venom that inhibits clot initiation and factor VIIa activity. J Biol Chem 280: 42601-42611.
6. Becker S, Terlau H (2008). Toxins from cone snails: properties, applications and biotechnological production. Appl Microbiol Biotechnol 79: 1-9.
7. Bekker A, Sturaitis MK (2005). Dexmedetomidine for neurological surgery. Neurosurgery 57 1-10; discussion 1-10.
8. Blandizzi C (2007). Enteric alpha-2 adrenoceptors: pathophysiological implications in functional and inflammatory bowel disorders. Neurochem Int 51: 282-288.
9. Brotchie JM (2005). Nondopaminergic mechanisms in levodopa-induced dyskinesia. Mov Disord 20: 919-931.
10. Carsi JM, Valentine HH, Potter LT (1999). m2-toxin: a selective ligand for M2 muscarinic receptors. Mol Pharmacol 56: 933-937.
11. Changeux JP, Kasai M, Lee CY (1970). Use of a snake venom toxin to characterize the cholinergic receptor protein. Proc Natl Acad Sci U S A 67: 1241-1247.
12. Chen Z, Rogge G, Hague C, Alewood D, Colless B, Lewis RJ et al. (2004). Subtype-selective noncompetitive or competitive inhibition of human alpha1-adrenergic receptors by rho-TIA. J Biol Chem 279: 35326-35333.
13. Cheng Y, Prusoff WH (1973). Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 22: 3099-3108.
14. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, Kobilka TS et al. (2007). High-resolution crystal structure of an engineered human 2-adrenergic G protein coupled receptor. Science 318: 1258-1265.
15. Craig AG, Norberg T, Griffin D, Hoeger C, Akhtar M, Schmidt K et al. (1999). Contulakin-G, an O-glycosylated invertebrate neurotensin. J Biol Chem 274: 13752-13759.
16. Crassous PA, Denis C, Paris H, Senard JM (2007). Interest of alpha2-adrenergic agonists and antagonists in clinical practice: background, facts and perspectives. Curr Top Med Chem 7: 187-194.
17. Cruz LJ, De Santos V, Zafaralla GC, Ramilo CA, Zeikus R, Gray WR et al. (1987). Invertebrate vasopressin/oxytocin homologs. Characterization of peptides from Conus geographus and Conus straitus venoms. J Biol Chem 262: 15821-15824.
18. Ducancel F (2005). Endothelin-like peptides. Cell Mol Life Sci 62: 2828-2839.
19. Favreau P, Gilles N, Lamthanh H, Bournaud R, Shimahara T, Bouet F et al. (2001). A new omega-conotoxin that targets N-type voltage-sensitive calcium channels with unusual specificity. Biochemistry 40: 14567-14575.
20. Fruchart-Gaillard C, Mourier G, Marquer C, Menez A, Servent D (2006). Identification of various allosteric interaction sites on M1 muscarinic receptor using 125I-Met35-oxidized muscarinic toxin 7. Mol Pharmacol 69: 1641-1651.
21. 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 N-methylscopolamine-occupied states. Mol Pharmacol 74: 1554-1563.
22. Gales C, Van Durm JJ, Schaak S, Pontier S, Percherancier Y, Audet M et al. (2006). Probing the activation-promoted structural rearrangements in preassembled receptor-G protein complexes. Nat Struct Mol Biol 13: 778-786.
23. Halai R, Craik DJ (2009). Conotoxins: natural product drug leads. Nat Prod Rep 26: 526-536.
24. Han TS, Teichert RW, Olivera BM, Bulaj G (2008). Conus venoms - a rich source of peptide-based therapeutics. Curr Pharm Des 14: 2462-2479.
25. Harvey AL, Kornisiuk E, Bradley KN, Cervenansky C, Duran R, Adrover M et al. (2002). Effects of muscarinic toxins MT1 and MT2 from green mamba on different muscarinic cholinoceptors. Neurochem Res 27: 1543-1554.
26. Jaakola VP, Griffith MT, Hanson MA, Cherezov V, Chien EY, Lane JR et al. (2008). The 2.6 angstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 322: 1211-1217.
27. Jolkkonen M, Adem A, Hellman U, Wernstedt C, Karlsson E (1995). A snake toxin against muscarinic acetylcholine receptors: amino acid sequence, subtype specificity and effect on guinea-pig ileum. Toxicon 33: 399-410.
28. Jolkkonen M, Oras A, Toomela T, Karlsson E, Jarv J, Akerman KE (2001). Kinetic evidence for different mechanisms of interaction of black mamba toxins MT alpha and MT beta with muscarinic receptors. Toxicon 39: 377-382.
29. Joubert FJ (1985). The amino acid sequence of protein CM-3 from Dendroaspis polylepis polylepis (black mamba) venom. Int J Biochem 17: 695-699.
30. King GF, Gentz MC, Escoubas P, Nicholson GM (2008). A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon 52: 264-276.
31. Kostenis E (2001). Is Galpha16 the optimal tool for fishing ligands of orphan G-protein-coupled receptors? Trends Pharmacol Sci 22: 560-564.
32. Kukkonen A, Perakyla M, Akerman KE, Nasman J (2004). Muscarinic toxin 7 selectivity is dictated by extracellular receptor loops. J Biol Chem 279: 50923-50929.
33. Kumar TK, Jayaraman G, Lee CS, Arunkumar AI, Sivaraman T, Samuel D et al. (1997). Snake venom cardiotoxins-structure, dynamics, function and folding. J Biomol Struct Dyn 15: 431-463.
34. Leppik RA, Mynett A, Lazareno S, Birdsall NJ (2000). Allosteric interactions between the antagonist prazosin and amiloride analogs at the human alpha(1A)-adrenergic receptor. Mol Pharmacol 57: 436-445.
35. McIntosh JM, Olivera BM, Cruz LJ (1999). Conus peptides as probes for ion channels. Methods Enzymol 294: 605-624.
36. Mourier G, Dutertre S, Fruchart-Gaillard C, Menez A, Servent D (2003). Chemical synthesis of MT1 and MT7 muscarinic toxins: critical role of Arg-34 in their interaction with M1 muscarinic receptor. Mol Pharmacol 63: 26-35.
37. Olianas MC, Maullu C, Adem A, Mulugeta E, Karlsson E, Onali P (2000). Inhibition of acetylcholine muscarinic M(1) receptor function by the M(1)-selective ligand muscarinic toxin 7 (MT-7). Br J Pharmacol 131: 447-452.
38. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, Fox BA et al. (2000). Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289: 739-745.
39. Pang CC (2001). Autonomic control of the venous system in health and disease: effects of drugs. Pharmacol Ther 90: 179-230.
40. Pratt BL, Takahashi JS (1987). Alpha-2 adrenergic regulation of melatonin release in chick pineal cell cultures. J Neurosci 7: 3665-3674.
41. Putnam NH, Srivastava M, Hellsten U, Dirks B, Chapman J, Salamov A et al. (2007). Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317: 86-94.
42. Quinton L, Demeure K, Dobson R, Gilles N, Gabelica V, De Pauw E (2007). New method for characterizing highly disulfide-bridged peptides in complex mixtures: application to toxin identification from crude venoms. J Proteome Res 6: 3216-3223.
43. Quinton L, Girard E, Maiga A, Rekik M, Lluel P, Masuyer G et al. (2010). Isolation and pharmacological characterization of AdTx1, a natural peptide displaying specific insurmountable antagonism of the alpha(1A)-adrenoceptor. Br J Pharmacol 159: 316-325.
44. Rajagopalan N, Pung YF, Zhu YZ, Wong PT, Kumar PP, Kini RM (2007). Beta-cardiotoxin: a new three-finger toxin from Ophiophagus hannah (king cobra) venom with beta-blocker activity. FASEB J 21: 3685-3695.
45. Rasmussen SG, Choi HJ, Rosenbaum DM, Kobilka TS, Thian FS, Edwards PC et al. (2007). Crystal structure of the human beta2 adrenergic G-protein-coupled receptor. Nature 450: 383-387.
46. Ribeiro CA, Macedo TA (1986). Pharmacological characterization of the postsynaptic alpha-adrenoceptors in human uterine artery. J Pharm Pharmacol 38: 600-605.
47. Rosengren AH, Jokubka R, Tojjar D, Granhall C, Hansson O, Li DQ et al. (2009). Overexpression of alpha2A-adrenergic receptors contributes to type 2 diabetes. Science 327: 217-220.
48. Selvam C, Oueslati N, Lemasson IA, Brabet I, Rigault D, Courtiol T et al. (2010). A virtual screening hit reveals new possibilities for developing group III metabotropic glutamate receptor agonists. J Med Chem 53: 2797-2813.
49. Servent D, Fruchart-Gaillard C (2009). Muscarinic toxins: tools for the study of the pharmacological and functional properties of muscarinic receptors. J Neurochem 109: 1193-1202.
50. Servent D, Menez A (2001). Snake neurotoxins that interact with nicotinic acetylcholine receptors. In: Massaro EJ (ed.). Handbook of Neurotoxicology. Humana Press: Totowa, NJ, pp. 385-425.
51. Servent D, Winckler-Dietrich V, Hu HY, Kessler P, Drevet P, Bertrand D et al. (1997). Only snake curaremimetic toxins with a fifth disulfide bond have high affinity for the neuronal alpha7 nicotinic receptor. J Biol Chem 272: 24279-24286.
52. Sharpe IA, Gehrmann J, Loughnan ML, Thomas L, Adams DA, Atkins A et al. (2001). Two new classes of conopeptides inhibit the alpha1-adrenoceptor and noradrenaline transporter. Nat Neurosci 4: 902-907.
53. Suckau D, Resemann A, Schuerenberg M, Hufnagel P, Franzen J, Holle A (2003). A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal Bioanal Chem 376: 952-965.
54. Terlau H, Olivera BM (2004). Conus venoms: a rich source of novel ion channel-targeted peptides. Physiol Rev 84: 41-68.
55. Tytgat J, Chandy KG, Garcia ML, Gutman GA, Martin-Eauclaire MF, Van Der Walt JJ et al. (1999). A unified nomenclature for short-chain peptides isolated from scorpion venoms: alpha-KTx molecular subfamilies. Trends Pharmacol Sci 20: 444-447.
56. De Weille JR, Schweitz H, Maes P, Tartar A, Lazdunski M (1991). Calciseptine, a peptide isolated from black mamba venom, is a specific blocker of the L-type calcium channel. Proc Natl Acad Sci U S A 88: 2437-2440.
57. Williams JA, Day M, Heavner JE (2008). Ziconotide: an update and review. Expert Opin Pharmacother 9: 1575-1583.
58. Wu PL, Lee SC, Chuang CC, Mori S, Akakura N, Wu WG et al. (2006). Non-cytotoxic cobra cardiotoxin A5 binds to alpha(v)beta3 integrin and inhibits bone resorption. Identification of cardiotoxins as non-RGD integrin-binding proteins of the Ly-6 family. J Biol Chem 281: 7937-7945.