Diversity of folds in animal toxins acting on ion channels.

Animal toxins acting on ion channels of excitable cells are principally highly potent short peptides that are present in limited amounts in the venoms of various unrelated species, such as scorpions, snakes, sea anemones, spiders, insects, marine cone snails and worms. These toxins have been used extensively as invaluable biochemical and pharmacological tools to characterize and discriminate between the various ion channel types that differ in ionic selectivity, structure and/or cell function. Alongside the huge molecular and functional diversity of ion channels, a no less impressive structural diversity of animal toxins has been indicated by the discovery of an increasing number of polypeptide folds that are able to target these ion channels. Indeed, it appears that these peptide toxins have evolved over time on the basis of clearly distinct architectural motifs, in order to adapt to different ion channel modulating strategies (pore blockers compared with gating modifiers). Herein, we provide an up-to-date overview of the various types of fold from animal toxins that act on ion channels selective for K+, Na+, Ca2+ or Cl- ions, with special emphasis on disulphide bridge frameworks and structural motifs associated with these peptide folds.

[1]  S. Korn,et al.  Potassium channels , 2005, IEEE Transactions on NanoBioscience.

[2]  S. Grissmer,et al.  Cobatoxin 1 from Centruroides noxius Scorpion venom: Chemical Synthesis, 3-D Structure in Solution, Pharmacology and Docking on K+ channels , 2004 .

[3]  M. Delepierre,et al.  The 'functional' dyad of scorpion toxin Pi1 is not itself a prerequisite for toxin binding to the voltage-gated Kv1.2 potassium channels. , 2004, The Biochemical journal.

[4]  G. Lippens,et al.  Cobatoxin 1 from Centruroides noxius scorpion venom: chemical synthesis, three-dimensional structure in solution, pharmacology and docking on K+ channels. , 2004, The Biochemical journal.

[5]  R. Lewis,et al.  Therapeutic potential of venom peptides , 2003, Nature Reviews Drug Discovery.

[6]  M. Delepierre,et al.  Synthesis and characterization of Pi4, a scorpion toxin from Pandinus imperator that acts on K+ channels. , 2003, European journal of biochemistry.

[7]  S. Grissmer,et al.  A Maurotoxin with Constrained Standard Disulfide Bridging , 2003, Journal of Biological Chemistry.

[8]  Jan Tytgat,et al.  Importance of the conserved aromatic residues in the scorpion alpha-like toxin BmK M1: the hydrophobic surface region revisited. , 2003, The Journal of biological chemistry.

[9]  G. Nicastro,et al.  Solution structure of crotamine, a Na+ channel affecting toxin from Crotalus durissus terrificus venom. , 2003, European journal of biochemistry.

[10]  C. Chi,et al.  Exploration of the functional site of a scorpion alpha-like toxin by site-directed mutagenesis. , 2003, Biochemistry.

[11]  P. Ascenzi,et al.  Contryphan-Vn: a modulator of Ca2+-dependent K+ channels. , 2003, Biochemical and biophysical research communications.

[12]  S. Zinn-Justin,et al.  Motions and structural variability within toxins: Implication for their use as scaffolds for protein engineering , 2003, Protein science : a publication of the Protein Society.

[13]  R. C. Rodríguez de la Vega,et al.  Two novel toxins from the Amazonian scorpion Tityus cambridgei that block Kv1.3 and Shaker B K(+)-channels with distinctly different affinities. , 2002, Biochimica et biophysica acta.

[14]  K. Dyason,et al.  Two new scorpion toxins that target voltage-gated Ca2+ and Na+ channels. , 2002, Biochemical and biophysical research communications.

[15]  S. Liang,et al.  Function and Solution Structure of Huwentoxin-IV, a Potent Neuronal Tetrodotoxin (TTX)-sensitive Sodium Channel Antagonist from Chinese Bird Spider Selenocosmia huwena * , 2002, The Journal of Biological Chemistry.

[16]  R. Kini,et al.  Molecular moulds with multiple missions: Functional sites in three‐finger toxins , 2002, Clinical and experimental pharmacology & physiology.

[17]  Shoba Ranganathan,et al.  kappa-Hefutoxin1, a novel toxin from the scorpion Heterometrus fulvipes with unique structure and function. Importance of the functional diad in potassium channel selectivity. , 2002, The Journal of biological chemistry.

[18]  M. Gage,et al.  The virally encoded fungal toxin KP4 specifically blocks L-type voltage-gated calcium channels. , 2002, Molecular pharmacology.

[19]  D. Craik,et al.  Solution structures of the cis- and trans-Pro30 isomers of a novel 38-residue toxin from the venom of Hadronyche Infensa sp. that contains a cystine-knot motif within its four disulfide bonds. , 2002, Biochemistry.

[20]  K. Chandy,et al.  Selective blockade of T lymphocyte K+ channels ameliorates experimental autoimmune encephalomyelitis, a model for multiple sclerosis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[21]  K. Chandy,et al.  Design and Characterization of a Highly Selective Peptide Inhibitor of the Small Conductance Calcium-activated K+Channel, SkCa2* , 2001, The Journal of Biological Chemistry.

[22]  T. Nakajima,et al.  Solution structure of Ptu1, a toxin from the assassin bug Peirates turpis that blocks the voltage-sensitive calcium channel N-type. , 2001, Biochemistry.

[23]  J. Sabatier Chemical Synthesis and Characterization of Small Proteins: Example of Scorpion Toxins , 2001 .

[24]  K. Chandy,et al.  Design and Characterization of a Highly Selective Peptide Inhibitor of the Small Conductance Calcium-activated K Channel , SkCa 2 * , 2001 .

[25]  E. Carlier,et al.  Maurotoxin Versus Pi1/HsTx1 Scorpion Toxins , 2000, The Journal of Biological Chemistry.

[26]  P. Escoubas,et al.  Structure and pharmacology of spider venom neurotoxins. , 2000, Biochimie.

[27]  D. Craik,et al.  Conotoxin TVIIA, a novel peptide from the venom of Conus tulipa 1. Isolation, characterization and chemical synthesis. , 2000, European journal of biochemistry.

[28]  T. Yamazaki,et al.  Structural basis for the biological activity of dendrotoxin-I, a potent potassium channel blocker. , 2000, Biopolymers.

[29]  J. J. Wu,et al.  The gene cloning and sequencing of Bm-12, a chlorotoxin-like peptide from the scorpion Buthus martensi Karsch. , 2000, Toxicon : official journal of the International Society on Toxinology.

[30]  I. Shimada,et al.  Solution structure of hanatoxin1, a gating modifier of voltage-dependent K(+) channels: common surface features of gating modifier toxins. , 2000, Journal of molecular biology.

[31]  P. Allen,et al.  Chemical synthesis and characterization of maurocalcine, a scorpion toxin that activates Ca2+ release channel/ryanodine receptors , 2000, FEBS letters.

[32]  K. Nielsen,et al.  Structure–activity relationships of ω‐conotoxins at N‐type voltage‐sensitive calcium channels , 2000, Journal of molecular recognition : JMR.

[33]  D. Craik,et al.  Conotoxin TVIIA, a novel peptide from the venom of Conus tulipa 2. Three-dimensional solution structure. , 2000, European journal of biochemistry.

[34]  Pi7, an orphan peptide from the scorpion Pandinus imperator: a 1H-NMR analysis using a nano-NMR Probe. , 1999, Biochemistry.

[35]  A. Ménez,et al.  Mapping the Functional Anatomy of BgK on Kv1.1, Kv1.2, and Kv1.3 , 1999, The Journal of Biological Chemistry.

[36]  M. Delepierre,et al.  Scorpion toxins specific for Na+-channels. , 1999, European journal of biochemistry.

[37]  R. Norton,et al.  Erratum: Roles of key functional groups in ω-conotoxin GVIA. Synthesis, structure and functional assay of selected peptide analogues (European Journal of Biochemistry (1999) 262 (447-455)) , 1999 .

[38]  J. Fletcher,et al.  Spider toxins : A new group of potassium channel modulators , 1999 .

[39]  L. Possani,et al.  Structure and function of scorpion toxins affecting K+-channels , 1999 .

[40]  R. Norton,et al.  Sea anemone toxins as templates for the design of immunosuppressant drugs , 1999 .

[41]  K. Swartz,et al.  Inhibition of T-type voltage-gated calcium channels by a new scorpion toxin , 1998, Nature Neuroscience.

[42]  A. Ménez,et al.  Functional architectures of animal toxins: a clue to drug design? , 1998, Toxicon : official journal of the International Society on Toxinology.

[43]  D. Gordon,et al.  δ-Atracotoxins from Australian Funnel-web Spiders Compete with Scorpion α-Toxin Binding but Differentially Modulate Alkaloid Toxin Activation of Voltage-gated Sodium Channels* , 1998, The Journal of Biological Chemistry.

[44]  S. Zinn-Justin,et al.  Delineation of the functional site of alpha-dendrotoxin. The functional topographies of dendrotoxins are different but share a conserved core with those of other Kv1 potassium channel-blocking toxins. , 1998, The Journal of biological chemistry.

[45]  O. Froy,et al.  An excitatory scorpion toxin with a distinctive feature: an additional alpha helix at the C terminus and its implications for interaction with insect sodium channels. , 1998, Structure.

[46]  S. Zinn-Justin,et al.  Three-dimensional structure of kappa-conotoxin PVIIA, a novel potassium channel-blocking toxin from cone snails. , 1998, Biochemistry.

[47]  J. Dodge,et al.  Structure/activity relationships , 1998 .

[48]  David J. Craik,et al.  Solution structure and proposed binding mechanism of a novel potassium channel toxin κ-conotoxin PVIIA , 1997 .

[49]  J. Mackay,et al.  The structure of versutoxin (delta-atracotoxin-Hv1) provides insights into the binding of site 3 neurotoxins to the voltage-gated sodium channel. , 1997, Structure.

[50]  E. Blanc,et al.  Solution structure of maurotoxin, a scorpion toxin from Scorpio maurus, with high affinity for voltage‐gated potassium channels , 1997, Proteins.

[51]  R. Norton,et al.  Structure of neurotoxin B-IV from the marine worm Cerebratulus lacteus: a helical hairpin cross-linked by disulphide bonding. , 1997, Journal of molecular biology.

[52]  C. Roumestand,et al.  On the Convergent Evolution of Animal Toxins , 1997, The Journal of Biological Chemistry.

[53]  C. Legros,et al.  [Scorpion toxins]. , 1997, Comptes rendus des seances de la Societe de biologie et de ses filiales.

[54]  H. Rochat,et al.  Chemical synthesis and characterization of maurotoxin, a short scorpion toxin with four disulfide bridges that acts on K+ channels. , 1996, European journal of biochemistry.

[55]  W. Catterall,et al.  Molecular Determinants of High Affinity Binding of α-Scorpion Toxin and Sea Anemone Toxin in the S3-S4 Extracellular Loop in Domain IV of the Na+ Channel α Subunit* , 1996, The Journal of Biological Chemistry.

[56]  L. Possani,et al.  A novel structural class of K+-channel blocking toxin from the scorpion Pandinus imperator. , 1996, The Biochemical journal.

[57]  R. Norton,et al.  Solution structure of ShK toxin, a novel potassium channel inhibitor from a sea anemone , 1996, Nature Structural Biology.

[58]  A. Khimani,et al.  Structure and function of a virally encoded fungal toxin from Ustilago maydis: a fungal and mammalian Ca2+ channel inhibitor. , 1995, Structure.

[59]  M. Blackledge,et al.  NMR and restrained molecular dynamics study of the three-dimensional solution structure of toxin FS2, a specific blocker of the L-type calcium channel, isolated from black mamba venom. , 1995, Biochemistry.

[60]  S. Wodak,et al.  NMR sequential assignments and solution structure of chlorotoxin, a small scorpion toxin that blocks chloride channels. , 1995, Biochemistry.

[61]  V. Basus,et al.  Solution structure of omega-conotoxin MVIIA using 2D NMR spectroscopy. , 1995, FEBS letters.

[62]  D. Craik,et al.  A common structural motif incorporating a cystine knot and a triple‐stranded β‐sheet in toxic and inhibitory polypeptides , 1994, Protein science : a publication of the Protein Society.

[63]  D. Marion,et al.  Proteinase inhibitor homologues as potassium channel blockers , 1994, Nature Structural Biology.

[64]  J. Fontecilla-Camps,et al.  Crystal structure of toxin II from the scorpion Androctonus australis Hector refined at 1.3 A resolution. , 1994, Journal of molecular biology.

[65]  J Ramachandran,et al.  Solution structure of omega-conotoxin GVIA using 2-D NMR spectroscopy and relaxation matrix analysis. , 1993, Biochemistry.

[66]  H. Rochat,et al.  P05, a new leiurotoxin I-like scorpion toxin: synthesis and structure-activity relationships of the alpha-amidated analog, a ligand of Ca(2+)-activated K+ channels with increased affinity. , 1993, Biochemistry.

[67]  C. Roumestand,et al.  Analysis of side-chain organization on a refined model of charybdotoxin: structural and functional implications. , 1992, Biochemistry.

[68]  C. Roumestand,et al.  Refined structure of charybdotoxin: common motifs in scorpion toxins and insect defensins. , 1991, Science.

[69]  R. Norton,et al.  Structure and structure-function relationships of sea anemone proteins that interact with the sodium channel. , 1991, Toxicon : official journal of the International Society on Toxinology.

[70]  M. Billeter,et al.  Three‐dimensional structure of the neurotoxin ATX Ia from Anemonia sulcata in aqueous solution determined by nuclear magnetic resonance spectroscopy , 1989, Proteins.

[71]  W. A. Sexton,et al.  STRUCTURE—ACTIVITY RELATIONSHIPS , 1958, The Journal of pharmacy and pharmacology.