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Structural Determinants in Phycotoxins and Achbp Conferring High Affinity

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Structural Determinants in Phycotoxins and Achbp Conferring High Affinity Structural determinants in phycotoxins and AChBP conferring high affinity binding and nicotinic AChR antagonism Yves Bournea,1, Zoran Radi´cb, Rómulo Aráozc, Todd T. Talleyb, Evelyne Benoitc, Denis Serventd, Palmer Taylorb, Jordi Molgóc, and Pascale Marchote,1 aArchitecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique, Université d’Aix-Marseille, Campus Luminy–Case 932, F-13288 Marseille Cedex 9, France; bDepartment of Pharmacology, Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California at San Diego, La Jolla, CA 92093-0657; cLaboratoire de Neurobiologie Cellulaire et Moléculaire, Centre National de la Recherche Scientifique, Institut de Neurobiologie Alfred Fessard–FRC2118, F-91198 Gif-sur-Yvette Cedex, France; dInstitut de Biologie et Technologies de Saclay, Service d’Ingénierie Moléculaire des Protéines, Laboratoire de Toxinologie Moléculaire, Commissariat à l’Energie Atomique, F-91191 Gif-sur-Yvette, France; and eCentre de Recherche en Neurobiologie-Neurophysiologie de Marseille, Centre National de la Recherche Scientifique, Université d’Aix-Marseille, Institut Fédératif de Recherche Jean Roche, Faculté de Médecine–Secteur Nord, CS80011, F-13344 Marseille Cedex 15, France Edited* by William A. Catterall, University of Washington School of Medicine, Seattle, WA, and approved February 17, 2010 (received for review October 26, 2009) Spirolide and gymnodimine macrocyclic imine phycotoxins belong to an lated from the digestive glands of mussels, scallops, and phytoplankton emerging class of chemical agents associated with marine algal blooms harvested from aquaculture sites (4–6). The dinoflagellate Alexan- and shellfish toxicity. Analysis of 13-desmethyl spirolide C and gymno- drium ostenfeldii has been associated to spirolide production (4, 7–9). dimine A by binding and voltage-clamp recordings on muscle-type Spirolides contain an unusual 5,5,6-bis-spirocetal moiety embedded α12βγδ and neuronal α3β2andα4β2 nicotinic acetylcholine receptors within a 23-membered macrocycle along with a 6,7-spirocyclic imine reveals subnanomolar affinities, potent antagonism, and limited sub- structure that is found in related gymnodimines, pinnatoxins, and type selectivity. Their binding to acetylcholine-binding proteins (AChBP), pteriatoxins (10). They exhibit rapid lethality associated with central as soluble receptor surrogates, exhibits picomolar affinities governed by neurological symptoms when administered i.p. or p.o. to mice (2, 11). diffusion-limited association and slow dissociation, accounting for appa- Gymnodimines (Fig. 1) have been identified from contaminated rent irreversibility. Crystal structures of the phycotoxins bound to Aply- shellfish or from extracts of the dinoflagellate Karenia selliformis (12– sia-AChBP (≈2.4Å) show toxins neatly imbedded within the nest of ar- 15). Similar to spirolides, gymnodimines contain a spirocyclic imine omatic side chains contributed by loops C and F on opposing faces of the but, in contrast to spirolides, they bear a trisubstituted tetrahy- subunit interface, and which in physiological conditions accommodates drofuran embedded within a 16-membered macrocycle. Gymnodi- acetylcholine. The structures also point to three major features: (i)the mines also cause rapid neurotoxic mortality (15, 16). sequence-conserved loop C envelops the bound toxins to maximize sur- Initial research into the mode of action of spirolides A-D had face complementarity; (ii) hydrogen bonding of the protonated imine suggested that they are antagonists of muscarinic acetylcholine nitrogen in the toxins with the carbonyl oxygen of loop C Trp147 tethers (ACh) receptors (11). Later reports revealed that 13-desmethyl spi- the toxin core centered within the pocket; and (iii) the spirolide bis- rolide C caused dose-dependent, widespread mouse brain neuronal spiroacetal or gymnodimine tetrahydrofuran and their common cyclo- damage and up-regulation of muscarinic and nicotinic ACh recep- hexene-butyrolactone further anchor the toxins in apical and mem- tors (nAChR) transcription in rats (2). In contrast to most peptidic brane directions, along the subunit interface. In contrast, the se- toxins, gymnodimines target both muscle and neuronal nAChRs at quence-variable loop F only sparingly contributes contact points to pre- subnanomolar concentrations, explaining their neurotoxicity (15). serve the broad receptor subtype recognition unique to phycotoxins The nAChRs are prototypical cation-selective, ligand-gated ion compared with other nicotinic antagonists. These data offer unique channels (LGIC) that mediate fast neurotransmission in the central means for detecting spiroimine toxins in shellfish and identify distinctive and peripheral nervous systems (17, 18). They belong to the Cys-loop ligands, functional determinants and binding regions for the design of superfamily of LGICs and are formed by distinct combinations of five new drugs able to target several receptor subtypes with high affinity. subunits that confer selectivity in pharmacological properties and cellular location (19). acetylcholine binding protein | marine phycotoxins | nicotinic acetylcholine The soluble ACh-binding proteins (AChBP) from mollusks receptor | pharmacological and structural analyses | seafood poisoning form homopentameric assemblies of subunits homologous to the N-terminal, extracellular ligand-binding domain (LBD) of the nAChR arine algal toxins and the associated phytoplankton species are (20–22) (Fig. S1). In addition to the overall structural features of the Mresponsible for >60,000 toxicity incidents worldwide per year subunits, the aromatic side chains that form the ligand binding pocket with a mortality rate of 1.5%. The major source of these bioactive at the subunit interfaces are well conserved in the nAChR family, with toxins is unicellular algae that proliferate to form dense cell concen- greater variability for residues at the complementary or (-) face than trations or “blooms.”When deposited throughout the marine environs by emptying of ship ballasts, harmful algal blooms are associated with the demise of wildlife, including birds and marine mammals. The Author contributions: Y.B., P.T., J.M., and P.M. designed research; Y.B., Z.R., R.A., T.T.T., toxins also move up the food chain through shellfish, a rich worldwide E.B., D.S., J.M., and P.M. performed research; Y.B., Z.R., D.S., P.T., J.M., and P.M. analyzed data; and Y.B., D.S., P.T., J.M., and P.M. wrote the paper. food resource: Shellfish contaminated by toxins serve to concentrate fl and direct them to animals and humans (1). Given their capacity to The authors declare no con ict of interest. cross the blood–brain barrier (2), their lipophilic properties and their *This Direct Submission article had a prearranged editor. modest volatility, when concentrated they represent an environmental Data deposition: The atomic coordinates and structure factors of the SPX and GYM com- fi plexes with Aplysia californica AChBP have been deposited in the Protein Data Bank, and human health risk and a threat to the shery industry. However, www.pdb.org (PDB codes 2WZY and 2X00, respectively). the complexity of their chemical synthesis (3) has hampered studies on 1To whom correspondence may be addressed. E-mail: [email protected] or their mechanism(s) of action. [email protected]. Spirolides (Fig. 1) are a family of unique macrocyclic imine phy- This article contains supporting information online at www.pnas.org/cgi/content/full/ cotoxins detected in North American and European coasts, first iso- 0912372107/DCSupplemental. 6076–6081 | PNAS | March 30, 2010 | vol. 107 | no. 13 www.pnas.org/cgi/doi/10.1073/pnas.0912372107 Downloaded by guest on September 25, 2021 tions in the central and peripheral nervous systems, may have vari- able stoichiometries involving at least two ligand binding sites at the α-β subunit interfaces. Typically, agonist binding to the two sites in the closed state induces a sequence of conformational transitions leading to channel opening followed by nAChR desensitization. Competitive antagonist binding to a single site is sufficient to block channel function. When the two sites have different affinities, competitive antagonism of function correlates with occupation of the higher affinity site (26). Characteristics of SPX and GYM Binding to nAChRs. Binding of the phycotoxins SPX and GYM to the muscle-type α12βγδ and neuronal α3β2andα4β2nAChRsexpressedinmammaliancellswasrecorded by competition against labeled peptidic antagonist, α-bungarotoxin, and alkaloid agonist, epibatidine. Subnanomolar dissociation Fig. 1. Chemical structures of the spirolides (Left) and gymnodimines (Right). constants were obtained (Table 1). In fact, the α3β2 subtype dis- The seven- and six-membered cyclic imines common to the phycotoxins are plays one order of magnitude higher affinity for SPX compared highlighted with a gray background, and the chemical groups specifictoeach are boxed. Locations of group substitutions that differ among the various spi- with GYM, whereas the other two nAChR subtypes do not dis- criminate significantly between the two toxins. This feature sug- rolides and gymnodimines are indicated. SPX (13-desmethyl spirolide C): R1 = CH3,R2 =H,R3 =CH3. GYM (gymnodimine A): R1 =CH3. Substitutionsfound inSPX gests common toxin interactions among these subtypes. and GYM congeners are described in the SI Appendix. Functional analysis of SPX and GYM used voltage-clamp record- ings on Xenopus oocytes either transplanted
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