Structure and orientation of a voltage-sensor toxin in lipid membranes

Biophysical Journal

Volumn 99, Issue 2, 2010, Pages 638-646

  Jung, Hyun Ho ^a   Jung, Hoi Jong ^a   Milescu, Mirela ^b   Lee, Chul Won ^c   Lee, Seungkyu ^a   Lee, Ju Yeon ^a   Eu, Young Jae ^a   Kim, Ha Hyung ^d   Swartz, Kenton J ^b   Kim, Jae Il ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d Chung Ang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE LIPID; PHOSPHATIDYLCHOLINE; PROTEIN BINDING; SPIDER VENOM; TRYPTOPHAN;

AMINO ACID SEQUENCE; ANIMAL; CHANNEL GATING; CHEMICAL STRUCTURE; CHEMISTRY; FLUORESCENCE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN SECONDARY STRUCTURE; SPECTROSCOPY;

AMINO ACID SEQUENCE; ANIMALS; DNA MUTATIONAL ANALYSIS; FLUORESCENCE; ION CHANNEL GATING; MEMBRANE LIPIDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLCHOLINES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SPECTRUM ANALYSIS; SPIDER VENOMS; TRYPTOPHAN;

EID: 77955191991     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.04.061     Document Type: Article

References (56)

1. Swartz, K. J. 2008. Sensing voltage across lipid membranes. Nature. 456:891-897.
2. + channel in a lipid membrane-like environment. Nature. 450:376-382.
3. + channel. Science. 309:897-903.
4. + channel and its dependence on the lipid membrane. Proc. Natl. Acad. Sci. USA, 102:15441-15446.
5. + channel, Nature. 423:33-41.
6. + channel. Cell. 123:463-475.
7. + channel. Nature. 423:42-48.
8. + channel in a lipid bilayer. Science. 306:491-495.
9. Chakrapani, S., L. G. Cuello, ..., E. Perozo. 2008. Structural dynamics of an isolated voltage-sensor domain in a lipid bilayer. Structure. 16:398-409.
10. Schmidt, D., Q. X. Jiang, and R. MacKinnon. 2006. Phospholipids and the origin of cationic gating charges in voltage sensors. Nature. 444:775-779.
11. Ramu, Y., Y. Xu, and Z. Lu. 2006. Enzymatic activation of voltagegated potassium channels. Nature. 442:696-699.
12. Alabi, A. A., M. I. Bahamonde, ..., K. J. Swartz. 2007. Portability of paddle motif function and pharmacology in voltage sensors. Nature. 450:370-375.
13. Milescu, M., J. Vobecky, ..., K. J. Swartz. 2007. Tarantula toxins interact with voltage sensors within lipid membranes. J. Gen. Physiol. 130:497-511.
14. + channels. Nature. 451:826-829.
15. Bosmans, F., M. F. Martin-Eauclaire, and K. J. Swartz. 2008. Deconstructing voltage sensor function and pharmacology in sodium channels. Nature. 456:202-208.
16. + channel gating. J. Mol. Biol. 381:569-580.
17. Milescu, M., F. Bosmans, ..., K. J. Swartz. 2009. Interactions between lipids and voltage sensor paddles detected with tarantula toxins. Nat. Struct. Mol. Biol. 16:1080-1085.
18. + channel α subunit. J. Biol. Chem. 271:15950-15962.
19. + channel through multiple binding sites. Neuron. 18:665-673.
20. + channels. Neuron. 18:675-682.
21. Cestèle, S., Y. Qu, ..., W. A. Catterall. 1998. Voltage sensor-trapping: enhanced activation of sodium channels by β-scorpion toxin bound to the S3-S4 loop in domain II. Neuron. 21:919-931.
22. + channel. J. Gen. Physiol. 115:673-684.
23. Cestèle, S., and W. A. Catterall. 2000. Molecular mechanisms of neurotoxin action, on voltage-gated sodium channels. Biochimie. 82:883-892.
24. Li-Smerin, Y., and K. J. Swartz. 2001. Helical structure of the COOH terminus of S3 and its contribution to the gating modifier toxin receptor in voltage-gated ion channels. J. Gen. Physiol, 117:205-218.
25. Lee, H. C., J. M. Wang, and K. J. Swartz. 2003. Interaction between extracellular Hanatoxin and the resting conformation of the voltagesensor paddle in Kv channels. Neuron. 40:527-536.
26. Phillips, L. R., M. Milescu, ..., K. J. Swartz. 2005. Voltage-sensor activation with a tarantula toxin as cargo. Nature. 436:857-860.
27. Lee, S. Y., and R. MacKinnon. 2004. A membrane-access mechanism of ion channel inhibition by voltage sensor toxins from spider venom. Nature. 430:232-235.
28. Suchyna, T. M., S. E. Tape, ..., P. A. Gottlieb. 2004. Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature. 430:235-240.
29. Jung, H. J., J. Y. Lee, ..., J. I. Kim. 2005. Solution structure and lipid membrane partitioning of VSTx1, an inhibitor of the KvAP potassium channel. Biochemistry. 44:6015-6023.
30. Smith, J. J., S. Alphy, ..., K. M. Blumenthal. 2005. Differential phospholipid binding by site 3 and site 4 toxins. Implications for structural variability between voltage-sensitive sodium channel domains. J. Biol. Chem. 280:11127-11133.
31. + channel gating and voltage sensor toxin sensitivity depend on the mechanical state of the lipid membrane. Proc. Natl. Acad. Sci. USA. 105:19276-19281.
32. + channels: common surface features of gating modifier toxins. J. Mol. Biol. 297:771-780.
33. 2+ channel. J. Mol. Biol. 321:517-526.
34. Lee, C. W., S. Kim, ..., J. I. Kim. 2004. Solution structure and functional characterization of SGTx1, a modifier of Kv2.1 channel gating. Biochemistry. 43:890-897.
35. Marvin, L., E. De, ..., C. Lange. 1999. Isolation, amino acid sequence and functional assays of SGTx 1. The first toxin purified from the venom of the spider Scodra griseipes. Eur. J. Biochem. 265:572-579.
36. Wang, J. M., S. H. Roh, ..., K. J. Swartz. 2004. Molecular surface of tarantula toxins interacting with voltage sensors in K(v) channels. J. Gen. Physiol. 123:455-467.
37. Takahashi, H., T. Nakanishi, ..., I. Shimada. 2000. A novel NMR method for determining the interfaces of large protein-protein complexes. Nat. Struct. Biol. 7:220-223.
38. Nakanishi, T., M. Miyazawa, ..., I. Shimada. 2002. Determination of the interface of a large protein, complex by transferred cross-saturation measurements. J. Mol. Biol. 318:245-249.
39. Takeuchi, K., H. Takahashi, ..., I. Shimada. 2004. Channel-forming membrane permeabilization by an antibacterial protein, sapecin: determination of membrane-buried and oligomerization surfaces by NMR. J. Biol. Chem. 279:4981-4987.
40. Ladokhin, A. S., S. Jayasinghe, and S. H. White. 2000. How to measure and analyze tryptophan fluorescence in membranes properly, and why bother? Anal. Biochem. 285:235-245.
41. Ladokhin, A. S. 1997. Distribution analysis of depth-dependent fluorescence quenching in membranes: a practical guide. Methods Enzymol. 278:462-473.
42. Ladokhin, A. S. 1999. Analysis of protein and peptide penetration into membranes by depth-dependent fluorescence quenching: theoretical considerations. Biophys. J. 76:946-955.
43. Abrams, F. S., and E. London. 1992. Calibration of the parallax fluorescence quenching method for determination of membrane penetration depth: refinement and comparison of quenching by spin-labeled and brominated lipids. Biochemistry. 31:5312-5322.
44. Abrams, F. S., and E. London. 1993. Extension of the parallax analysis of membrane penetration depth to the polar region of model membranes: use of fluorescence quenching by a spin-label attached to the phospholipid polar headgroup. Biochemistry. 32: 10826-10831.
45. Sean Peacock, R., A. M. Weljie, ..., H. J. Vogel. 2005. The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J. Mol. Biol. 345:1185-1197.
46. 2+-regulatory region from soybean calcium-dependent protein kinase-α. J. Biol. Chem. 279:35494-35502.
47. Goddard, T. D., and D. G. Kneller. 2004. SPARKY 3. University of California, San Francisco, San Francisco, CA.
48. Wuttke, D. S., M. P. Foster, ..., P. E. Wright. 1997. Solution structure of the first three zinc fingers of TFITIA bound to the cognate DNA sequence: determinants of affinity and sequence specificity. J. Mol. Biol. 273:183-206.
49. Foster, M. P., D. S. Wuttke, ..., P. E. Wright. 1997. Domain packing and dynamics in the DNA complex of the N-terminal zinc fingers of TFIUA. Nat. Struct. Biol. 4:605-608.
50. Jayalakshmi, V., and N. R. Krishna. 2002. Complete relaxation, and conformational exchange matrix (CORCEMA) analysis of intermolecular saturation transfer effects in reversibly forming ligand-receptor complexes. J. Magn. Reson. 155:106-118.
51. Wee, C. L., D. Bemporad, ..., M. S. Sansom, 2007. SGTx1, a Kv channel gating-modifier toxin, binds to the interfacial region of lipid bilayers. Biophys. J. 92:L07-L09.
52. Nguyen, T. P., and R. Horn. 2002. Movement and crevices around a sodium channel S3 segment. J. Gen. Physiol. 120:419-436.
53. + channel voltage-sensing domain. Neuron. 40:515-525.
54. + channel. J. Gen. Physiol. 128:687-699.
55. Oswald, R. E., T. M. Suchyna, ..., F. Sachs. 2002. Solution structure of peptide toxins that block mechanosensitive ion channels. J. Biol. Chem. 277:34443-34450.
56. Suchyna, T. M., J. H. Johnson, ..., F. Sachs. 2000. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J. Gen. Physiol. 115: 583-598.