P-loop flexibility in Na+ channel pores revealed by single- and double- cysteine replacements

Journal of General Physiology

Volumn 110, Issue 1, 1997, Pages 59-72

  Tsushima, Robert G ^a   Li, Ronald A ^a   Backx, Peter H ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

Cd2+ binding; Mutagenesis; Na+ channels; Structure; Xenopus oocytes

Indexed keywords

CADMIUM; CYSTEINE; DITHIOTHREITOL; REDUCING AGENT; SODIUM CHANNEL; SODIUM ION; THIOL DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MUTANT; NONHUMAN; OOCYTE; RAT; SKELETAL MUSCLE; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; CADMIUM; ELECTRIC CONDUCTIVITY; MUSCLE, SKELETAL; MUTATION; OOCYTES; RATS; REPETITIVE SEQUENCES, NUCLEIC ACID; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; XENOPUS;

EID: 0030753096     PISSN: 00221295     EISSN: None     Source Type: Journal    
DOI: 10.1085/jgp.110.1.59     Document Type: Article

References (61)

1. Akabas, M.H., D.A. Stauffer, M. Xu, and A. Karlin. 1992. Acetylcholine receptor channel structure probed in cysteine-substituted mutants. Science (Wash. DC). 258:307-310.
2. Arnold, G.E., J.I. Manchester, B.D. Townsend, and R.L. Ornstein. 1994. Investigation of domain motions in bacteriophage T4 lysozyme. J. Biomol. Struct. Dyn. 12:457-474.
3. Backx, P.H., D.T. Yue, J.H. Lawrence, E. Marban, and G.T. Tomaselli. 1992. Molecular localization of an ion-binding site within the pore of mammalian sodium channels. Science (Wash. DC). 257:248-251.
4. Balaji, V.N., A. Mobasser, and S.N. Rao. 1989. Modification of protein stability by introduction of disulfide bridges and prolines: geometric criteria for mutation sites. Biochem. Biophys. Res. Commun. 160:109-114.
5. Benitah, J.P., G.F. Tomaselli, and E. Marban. 1996. Adjacent pore-lining residues within sodium channels identified by paired cysteine replacements. Proc. Natl. Acad. Sci. USA. 93:7392-7396.
6. Bogartz, R.S. 1994. An Introduction to the Analysis of Variance. Praeger Publishers Inc., Westport, CT. 233-348.
7. Branden, C., and J. Tooze. 1991. Introduction to Protein Structure. Garland Publishing Inc., New York. 11-77.
8. Careaga, C.L., and J.J. Falke. 1992. Structure and dynamics of Eschericlna coli chemosensory receptors. Engineered sulfhydryl studies. Biophys. J. 62:209-216.
9. Catterall, W.A. 1995. Structure and function of voltage-gated ion channels. Annu. Rev. Biochem. 64:493-531.
10. + channel pore revealed cycsteine mutagenesis. Neuron. 16:1037-1047.
11. Colquhoun, D., and F.J. Sigworth. 1983. Fitting and statistical analysis of single-channel records. In Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum Press, New York. 191-263.
12. Cotton, F.A., and G. Wilkinson. 1992. Advanced Inorganic Chemistry: A Comprehensive Text 3rd ed. Interscience Publishers, New York. 503-527.
13. Cottrell, T.J., L.J. Harris, T. Tanaka, and R.Y. Yada. 1995. The sole lysine residue in porcine pepsin works as a key residue for catalysis and conformational flexibility. J. Biol. Chem. 34:19974-19978.
14. Creighton, T.E. 1993. Proteins: Structure and Molecular Properties. W.H. Freeman and Co. New York. 201-269.
15. Eisenherg, R. 1990. Channels as enzymes. J. Membr. Biol. 115:1-12.
16. Eisenman, G. 1984. Ion Transport Through Membranes. B. Pullman and K. Yagi, editors. Academic Press, New York. 101-129.
17. Eisenman, G., and R. Horn. 1983. Ionic selectivity revisited: the role of kinetic and equilibrium processes in ion permeation through channels. J. Membr. Biol. 11:197-225.
18. 2+ interactions. Neuron. 15:1121-1132.
19. Fersht, A. 1985. Enzyme Structure and Mechanism. 2nd ed. W.H. Freeman and Company, New York. 311-344.
20. Gross, A., and R. MacKinnon. 1995. Agitoxin footprinting the Shaker potassium channel pore. Neuron. 16:399-401.
21. + channels. In Ion Channels and Genetic Diseases. D.C. Dawson and R.A. Frizzell, editors. Rockefeller University Press, New York. 1-16.
22. + channels. Science (Wash. DC). 258:1152-1155.
23. Heinemann, S.H., H. Terlau, W. Stühmer, K. Imoto, and S. Numa. 1992. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature (Lond.). 356:441-444.
24. + channel pore through mutant cycles with a peptide inhibitor. Science (Wash. DC). 268:307-310.
25. Hille, B. 1992. Ionic Channels in Excitable Membranes, 2nd ed. Sinauer Associates, Sunderland, MA. 261-389.
26. + channel. Nature (Lond.). 353:86-90.
27. + channel pore. Biophys. J. 72:117-126.
28. Kunkel, T.A. 1985. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci. USA. 82:488-192.
29. + channel probed by sulfhydryl-specific reagents after cysteine-scanning mutagenesis. Biophys. J. 68:900-905.
30. Lan, Y., T. Lu, P.S. Lovett, and D.J. Creighton. 1995. Evidence for a (triosephosphate-like) "catalytic loop" near the active site of glyoxalase I. J. Biol. Chem. 270:12957-12960.
31. Larson, E.M., F.W. Larimer, and F.C. Hartman. 1995. Mechanistic insights provided by deletion of a flexible loop at the active site of ribulose-1,5-biphosphate carboxylase/oxygenase. Biochemistry. 34:4531-4537.
32. Läuger, P. 1987. Dynamics of ion transport systems in membranes. Physiol. Rev. 67:1296-1331.
33. + channel. Biophys. J. 66:1-13.
34. + channel during gating. Neuron. 16: 859-867.
35. + channel comprises part of the pore. Science (Wash. DC). 367:179-182.
36. MacKinnon, R. 1991. Determination of the subunit stoichiometry of a voltage-activated potassium channel. Nature (Lond.). 350:232-235.
37. MacKinnon, R., and C. Miller. 1989. Mutant potassium channels with altered binding of charybdotoxin, a pore-blocking peptide inhibitor. Science (Wash. DC). 245:1382-1385.
38. Miller, C. 1992. Ion channel structure and function. Science (Wash. DC). 258:240-241.
39. + channels. Neuron. 16:123-130.
40. Nicholson, L.K., T. Yamazaki, D.A. Torchia, S. Grzesiek, A. Bax, S.J. Stahl, J.D. Kaufman, P.T. Wingfield, P.Y.S. Lam, P.K. Jadhav, et al. 1995. Flexibility and function in HIV-1 protease. Nature Structural. Biology. 2:274-280.
41. Noda, M., S. Shimizu, T. Tanabe, T. Takai, T. Kayamo, T. Ikeda, H. Takahashi, H. Nakayama, Y. Kanaoka, N. Minamino, et al. 1984. Primary structure of Electrophorus electricus sodium channel from cDNA sequence. Nature (Lond.). 312:121-127.
42. + pore structure revealed by reporter cysteines at inner and outer surfaces. Neuron. 14:1055-1063.
43. Perez-Garcia, M.T., N. Chiamvimonvat, E. Marban, and G.F. Tomaselli. 1995. Structure of the sodium channel pore revealed by serial cysteine mutagenesis. Proc. Natl. Acad. Sci. USA. 93:300-304.
44. Pompliano, D.L., A. Peyman, and J.R. Knowles. 1990. Stabilization of a reaction intermediate as a catalytic device: definition of the functional role of the flexible loop in triosephosphate isomerase. Biochemistry. 29:3186-3194.
45. + channel selectivity filter by mutant cycle-based structure analysis. Neuron. 16:131-139.
46. Satin, J., J.W. Kyle, M. Chen, P. Bell, L.L. Cribbs, H.A. Fozzard, and R.B. Rogart. 1992. A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties. Science (Wash. DC.). 256: 1202-1205.
47. Shaw, C.F., III, M.J. Stillman, and K.T. Suzuki. 1992. Metallothioneins: Synthesis, Structure and Properties of Metallothioneins, Phytochelations and Metal-Thiolate Complexes. VCH Publishers Inc., New York. 1-13.
48. Soman, K.V., J.A. McCammon, and A.M. Brown. 1995. Secondary structure prediction of the H5 pore of potassium channels. Protein Eng. 8:397-401.
49. Stone, M.J., W.J. Fairbrother, A.G. Palmer III, J. Reizer, M.H. Saier, Jr., and P.E. Wright. 1992. Backbone dynamics of the Bacillus substilis glucose permease IIA domain determined from 15N NMR relaxation measurements. Biochemistry. 31:4394-44016.
50. Sun, Z.-P., M.H. Akabas, E.H. Colliding, A. Karlin, and S.A. Siegelbaum. 1996. Exposure of residues in the cyclic nucleotide-gated channel pore: P-region structure and function. Neuron. 16:141-149.
51. Tanaka, T., H. Yamaguchi, H. Kato, T. Nishioka, Y. Katsube, and J. Oda. 1993. Flexibility impaired by mutations revealed the multifunctional roles of the loop in glutathione synthetase. Biochemistry. 32:12398-12404.
52. Terlau, H., S.H. Heinemann, W. Stuhmer, M. Pusch, F. Conti, K. Imoto, and S. Numa. 1991. Mapping the site of block by tetrodotoxin and saxitoxin of sodium channel II. Nature (Lond.). 356: 441-444.
53. Tomaselli, G.F., H.B. Nuss, J.R. Balser, M.T. Perez-Garcia, K. Kluge, D.W. Orias, P.H. Backx, and E. Marban. 1995. A mutation in the pore of the sodium channel alters gating. Biophys. J. 68:1814-1827.
54. Torchinsky, Y.M. 1981. Sulfur in Proteins. Pergamon Press, Oxford. 1-98.
55. Trimmer, J.S., S.S. Cooperman, S.A. Tomiko, J. Zhou, S.M. Crean, M.B. Boyle, R.G. Kallen, Z. Sheng, R.L. Barchi, F.J. Sígworth, R.H. Goodman, W.S. Agnew, and G. Mandel. 1989. Primary structure and functional expression of a mammalian skeletal muscle sodium channel. Neuron. 3:33-49.
56. Tsushima, R.G., R.A. Li, and P.H. Backx. 1997. Altered ionic selectivity of the sodium channel revealed by cysteine mutations within the pore. J. Gen. Physiol. 109:463-467.
57. Vallee, B.L., and K.H. Falchuk. 1993. The biochemical basis of zinc physiology. Physiol. Rev. 73:79-118.
58. Wade, R.C., M.E. Davis, B.A. Luty, J.D. Madura, and J.A. McCammon. 1993. Gating of the active site of triose phosphate isomerase: Brownian dynamics simulations of flexible peptide loops in the enzyme. Biophys. J. 64:9-15.
59. Welch, G.R, B. Somogyi, and S. Damjanovich. 1982. The role of protein fluctuations in enzyme action: a review. Prog. Biophys. Mol. Biol. 39:109-146.
60. + channel. Science (Wash. DC). 251: 939-942.
61. + channel allows inactivation to be modulated by metal binding. Biophys. J. 66: 1068-1075.