"The King is dead": Checkmating ion channels with tethered toxins

Toxicon

Volumn 56, Issue 8, 2010, Pages 1293-1298

  Auer, Sebastian ^a   Ibañez Tallon, Inés ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Antagonist; Ion channel; Neuron; Peptide toxin; Receptor; Tethered toxin

Indexed keywords

BUNGAROTOXIN; GLYCOSYLPHOSPHATIDYLINOSITOL; ION CHANNEL; MEMBRANE PROTEIN; NEUROTRANSMITTER; NICOTINIC RECEPTOR; PROTEIN LYNX1; SNAKE VENOM; TETHERED TOXIN; TOXIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

AMINO ACID SEQUENCE; HUMAN; MEMBRANE BINDING; NEUROMUSCULAR SYNAPSE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; REVIEW; TOXIN STRUCTURE;

ANIMALS; CELL MEMBRANE; HUMANS; ION CHANNEL GATING; ION CHANNELS; ION TRANSPORT; MEMBRANE TRANSPORT MODULATORS; MICE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; NEUROTRANSMITTER AGENTS; ORGANISMS, GENETICALLY MODIFIED; RATS; SUBSTRATE SPECIFICITY; TOXINS, BIOLOGICAL; VENOMS; ZEBRAFISH;

EID: 77958508093     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2010.09.016     Document Type: Review

References (44)

1. Akopian A.N., Souslova V., England S., Okuse K., Ogata N., Ure J., Smith A., Kerr B.J., McMahon S.B., Boyce S., Hill R., Stanfa L.C., Dickenson A.H., Wood J.N. The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat. Neurosci. 1999, 2:541-548.
2. Auer S., Sturzebecher A.S., Juttner R., Santos-Torres J., Hanack C., Frahm S., Liehl B., Ibanez-Tallon I. Silencing neurotransmission with membrane-tethered toxins. Nat. Methods 2010, 7:229-236.
3. Baker M.D., Wen H. Tethered-toxin debut gets cold reception. J. Physiol. 2010, 588:1663.
4. Carr R.W., Pianova S., Brock J.A. The effects of polarizing current on nerve terminal impulses recorded from polymodal and cold receptors in the guinea-pig cornea. J. Gen. Physiol. 2002, 120:395-405.
5. Catterall W.A., Cestele S., Yarov-Yarovoy V., Yu F.H., Konoki K., Scheuer T. Voltage-gated ion channels and gating modifier toxins. Toxicon 2007, 49:124-141.
6. Catterall W.A., Few A.P. Calcium channel regulation and presynaptic plasticity. Neuron 2008, 59:882-901.
7. Changeux J.P., Kasai M., Lee C.Y. Use of a snake venom toxin to characterize the cholinergic receptor protein. Proc. Natl. Acad. Sci. U S A 1970, 67:1241-1247.
8. Drago J., McColl C.D., Horne M.K., Finkelstein D.I., Ross S.A. Neuronal nicotinic receptors: insights gained from gene knockout and knockin mutant mice. Cell. Mol. Life Sci. 2003, 60:1267-1280.
9. Dutertre S., Lewis R.J. Use of venom peptides to probe ion channel structure and function. J. Biol. Chem. 2010, 285:13315-13320.
10. George A.L. Inherited disorders of voltage-gated sodium channels. J. Clin. Invest. 2005, 115:1990-1999.
11. Gong S., Yang X.W., Li C., Heintz N. Highly efficient modification of bacterial artificial chromosomes (BACs) using novel shuttle vectors containing the R6Kgamma origin of replication. Genome Res. 2002, 12:1992-1998.
12. Hatten M.E., Heintz N. Large-scale genomic approaches to brain development and circuitry. Annu. Rev. Neurosci. 2005, 28:89-108.
13. Holford M., Auer S., Laqua M., Ibañez-Tallon I. Manipulating neuronal circuits with endogenous and recombinant cell-surface tethered modulators. Front. Mol. Neurosci. 2009, 2:21.
14. Hruska M., Ibañez-Tallon I., Nishi R. Cell-autonomous inhibition of alpha 7-containing nicotinic acetylcholine receptors prevents death of parasympathetic neurons during development. J. Neurosci. 2007, 27:11501-11509.
15. Hruska M., Keefe J., Wert D., Tekinay A.B., Hulce J., Ibanez-Tallon I., Nishi R. Prostate stem cell antigen is an endogenous lynx1-like prototoxin that antagonizes alpha7 containing nicotinic receptors and prevents programmed cell death of parasympathetic neurons. J. Neurosci. 2009.
16. Ibañez-Tallon I., Miwa J.M., Wang H.L., Adams N.C., Crabtree G.W., Sine S.M., Heintz N. Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron 2002, 33:893-903.
17. Ibañez-Tallon I., Wen H., Miwa J.M., Xing J., Tekinay A.B., Ono F., Brehm P., Heintz N. Tethering naturally occurring peptide toxins for cell-autonomous modulation of ion channels and receptors in vivo. Neuron 2004, 43:305-311.
18. Inchauspe C.G., Martini F.J., Forsythe I.D., Uchitel O.D. Functional Compensation of P/Q by N-type channels blocks short-term plasticity at the calyx of held presynaptic terminal. J. Neurosci. 2004, 24:10379-10383.
19. Klaassen A., Glykys J., Maguire J., Labarca C., Mody I., Boulter J. Seizures and enhanced cortical GABAergic inhibition in two mouse models of human autosomal dominant nocturnal frontal lobe epilepsy. Proc. Natl. Acad. Sci. U S A 2006, 103:19152-19157.
20. Le Novere N., Changeux J.P. Molecular evolution of the nicotinic acetylcholine receptor: an example of multigene family in excitable cells. J. Mol. Evol. 1995, 40:155-172.
21. Leipold E., DeBie H., Zorn S., Borges A., Olivera B.M., Terlau H., Heinemann S.H. muO conotoxins inhibit NaV channels by interfering with their voltage sensors in domain-2. Channels (Austin) 2007, 1:253-262.
22. Leonard S., Bertrand D. Neuronal nicotinic receptors: from structure to function. Nicotine Tob. Res. 2001, 3:203-223.
23. Lewis R.J. Conotoxins: molecular and therapeutic targets. Prog. Mol. Subcell. Biol. 2009, 46:45-65.
24. Luo L., Callaway E.M., Svoboda K. Genetic dissection of neural circuits. Neuron 2008, 57:634-660.
25. Miljanich G.P. Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr. Med. Chem. 2004, 11:3029-3040.
26. Miwa J., Stevens T., King S., Caldarone B., Ibaneztallon I., Xiao C., Fitzsimonds R., Pavlides C., Lester H., Picciotto M. The prototoxin lynx1 acts on nicotinic acetylcholine receptors to balance neuronal activity and survival in vivo. Neuron 2006, 51:587-600.
27. Miwa J.M., Ibanez-Tallon I., Crabtree G.W., Sánchez R., Sali A., Role L.W., Heintz N. lynx1, an endogenous toxin-like modulator of nicotinic acetylcholine receptors in the mammalian CNS. Neuron 1999, 23:105-114.
28. Ophoff R.A., Terwindt G.M., Vergouwe M.N., van Eijk R., Oefner P.J., Hoffman S.M., Lamerdin J.E., Mohrenweiser H.W., Bulman D.E., Ferrari M., Haan J., Lindhout D., van Ommen G.J., Hofker M.H., Ferrari M.D., Frants R.R. Familial hemiplegic migraine and episodic ataxia type-2 are caused by mutations in the Ca2+ channel gene CACNL1A4. Cellule 1996, 87:543-552.
29. Phui Yee J.S., Nanling G., Afifiyan F., Donghui M., Siew Lay P., Armugam A., Jeyaseelan K. Snake postsynaptic neurotoxins: gene structure, phylogeny and applications in research and therapy. Biochimie 2004, 86:137-149.
30. Quiram P.A., McIntosh J.M., Sine S.M. Pairwise interactions between neuronal alpha(7) acetylcholine receptors and alpha-conotoxin PnIB. J. Biol. Chem. 2000, 275:4889-4896.
31. Salminen O., Whiteaker P., Grady S.R., Collins A.C., McIntosh J.M., Marks M.J. The subunit composition and pharmacology of alpha-Conotoxin MII-binding nicotinic acetylcholine receptors studied by a novel membrane-binding assay. Neuropharmacology 2005, 48:696-705.
32. Staats P.S., Yearwood T., Charapata S.G., Presley R.W., Wallace M.S., Byas-Smith M., Fisher R., Bryce D.A., Mangieri E.A., Luther R.R., Mayo M., McGuire D., Ellis D. Intrathecal ziconotide in the treatment of refractory pain in patients with cancer or AIDS: a randomized controlled trial. J. Am. Med. Assoc. 2004, 291:63-70.
33. Steinlein O.K., Mulley J.C., Propping P., Wallace R.H., Phillips H.A., Sutherland G.R., Scheffer I.E., Berkovic S.F. A missense mutation in the neuronal nicotinic acetylcholine receptor alpha 4 subunit is associated with autosomal dominant nocturnal frontal lobe epilepsy. Nat. Genet. 1995, 11:201-203.
34. Stürzebecher A.S., Hu J., Smith E.S., Frahm S., Santos-Torres J., Kampfrath B., Auer S., Lewin G.R., Ibanez-Tallon I. An in vivo tethered toxin approach for the cell-autonomous inactivation of voltage-gated sodium channel currents in nociceptors. J. Physiol. 2010, 588:1695-1707.
35. Tekinay A.B., Nong Y., Miwa J.M., Lieberam I., Ibanez-Tallon I., Greengard P., Heintz N. A role for LYNX2 in anxiety-related behavior. Proc. Natl. Acad. Sci. 2009, 106:4477-4482.
36. Terlau H., Olivera B.M. Conus Venoms: a rich source of novel ion channel-targeted peptides. Physiol. Rev. 2004, 84:41-68.
37. Tolu S., Avale M.E., Nakatani H., Pons S., Parnaudeau S., Tronche F., Vogt A., Monyer H., Vogel R., de Chaumont F., Olivo-Marin J.C., Changeux J.P., Maskos U. A versatile system for the neuronal subtype specific expression of lentiviral vectors. FASEB J. 2010, 24:723-730.
38. Tottene A., Conti R., Fabbro A., Vecchia D., Shapovalova M., Santello M., van den Maagdenberg A.M.J.M., Ferrari M.D., Pietrobon D. Enhanced excitatory transmission at cortical synapses as the basis for facilitated spreading depression in Ca(v)2.1 knockin migraine mice. Neuron 2009, 61:762-773.
39. Tsetlin V.I., Hucho F. Snake and snail toxins acting on nicotinic acetylcholine receptors: fundamental aspects and medical applications. FEBS. Lett. 2004, 557:9-13.
40. Twede V.D., Miljanich G., Olivera B.M., Bulaj G. Neuroprotective and cardioprotective conopeptides: an emerging class of drug leads. Curr. Opin. Drug Discov. Devel. 2009, 12:231-239.
41. Wu Y., Cao G., Pavlicek B., Luo X., Nitabach M.N. Phase coupling of a circadian neuropeptide with rest/activity rhythms detected using a membrane-tethered spider toxin. PLoS Biol. 2008, 6:e273.
42. Zamponi G.W., Lewis R.J., Todorovic S.M., Arneric S.P., Snutch T.P. Role of voltage-gated calcium channels in ascending pain pathways. Brain Res. Rev. 2009, 60:84-89.
43. Zimmermann K., Leffler A., Babes A., Cendan C.M., Carr R.W., Kobayashi J., Nau C., Wood J.N., Reeh P.W. Sensory neuron sodium channel Nav1.8 is essential for pain at low temperatures. Nature 2007, 447:855-858.
44. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 2002, 64:355-405.