Role of the S4-S5 linker in CNG channel activation

Biophysical Journal

Volumn 99, Issue 8, 2010, Pages 2488-2496

  Kusch, Jana ^a   Zimmer, Thomas ^a   Holschuh, Jascha ^a   Biskup, Christoph ^a   Schulz, Eckhard ^b   Nache, Vasilica ^a   Benndorf, Klaus ^a  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b University of Applied Sciences Schmalkalden   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 78049270899     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.07.041     Document Type: Article

References (51)

1. Kaupp, U. B. 1991. The cyclic nucleotide-gated channels of vertebrate photoreceptors and olfactory epithelium. Trends Neurosci. 14:150-157.
2. Distler, M., M. Biel,., F. Hofmann. 1994. Expression of cyclic nucleotide- gated cation channels in non-sensory tissues and cells. Neuropharmacology. 33:1275-1282.
3. Kaupp, U. B., and R. Seifert. 2002. Cyclic nucleotide-gated ion channels. Physiol. Rev. 82:769-824.
4. Zagotta, W. N., and S. A. Siegelbaum. 1996. Structure and function of cyclic nucleotide-gated channels. Annu. Rev. Neurosci. 19:235-263.
5. Chen, T. Y., Y. W. Peng, ⋯, K. W. Yau. 1993. A new subunit of the cyclic nucleotide-gated cation channel in retinal rods. Nature. 362:764-767.
6. Körschen, H. G., M. Illing,., R. S. Molday. 1995. A 240 kDa protein represents the complete b subunit of the cyclic nucleotide-gated channel from rod photoreceptor. Neuron. 15:627-636.
7. Bönigk, W., J. Bradley, ⋯, S. Frings. 1999. The native rat olfactory cyclic nucleotide-gated channel is composed of three distinct subunits. J. Neurosci. 19:5332-5347.
8. Zheng, J., W. N. Zagotta, and W. N. Zagotta. 2000. Gating rearrangements in cyclic nucleotide-gated channels revealed by patch-clamp fluorometry. Neuron. 28:369-374.
9. Weitz, D., N. Ficek, ⋯, U. B. Kaupp. 2002. Subunit stoichiometry of the CNG channel of rod photoreceptors. Neuron. 36:881-889.
10. Zhong, H., L. L. Molday, ⋯, K. W. Yau. 2002. The heteromeric cyclic nucleotide-gated channel adopts a 3A:1B stoichiometry. Nature. 420:193-198.
11. Kaupp, U. B., T. Niidome, ⋯, S. Numa. 1989. Primary structure and functional expression from complementary DNA of the rod photoreceptor cyclic GMP-gated channel. Nature. 342:762-766.
12. Gordon, S. E., and W. N. Zagotta. 1995. Localization of regions affecting an allosteric transition in cyclic nucleotide-activated channels. Neuron. 14:857-864.
13. Gordon, S. E., and W. N. Zagotta. 1995. A histidine residue associated with the gate of the cyclic nucleotide-activated channels in rod photoreceptors. Neuron. 14:177-183.
14. Zong, X., H. Zucker, ⋯, M. Biel. 1998. Three amino acids in the C-linker are major determinants of gating in cyclic nucleotide-gated channels. EMBO J. 17:353-362.
15. Paoletti, P., E. C. Young, and S. A. Siegelbaum. 1999. C-Linker of cyclic nucleotide-gated channels controls coupling of ligand binding to channel gating. J. Gen. Physiol. 113:17-34.
16. Johnson, Jr., J. P., and W. N. Zagotta. 2001. Rotational movement during cyclic nucleotide-gated channel opening. Nature. 412:917-921.
17. Broillet, M. C., and S. Firestein. 1996. Direct activation of the olfactory cyclic nucleotide-gated channel through modification of sulfhydryl groups by NO compounds. Neuron. 16:377-385.
18. Gordon, S. E., M. D. Varnum, and W. N. Zagotta. 1997. Direct interaction between amino- and carboxyl-terminal domains of cyclic nucleotide- gated channels. Neuron. 19:431-441.
19. Goulding, E. H., G. R. Tibbs, and S. A. Siegelbaum. 1994. Molecular mechanism of cyclic-nucleotide-gated channel activation. Nature. 372:369-374.
20. Möttig, H., J. Kusch, ⋯, K. Benndorf. 2001. Molecular regions controlling the activity of CNG channels. J. Gen. Physiol. 118: 183-192.
21. Varnum, M. D., and W. N. Zagotta. 1997. Interdomain interactions underlying activation of cyclic nucleotide-gated channels. Science. 278:110-113.
22. Rosenbaum, T., and S. E. Gordon. 2002. Dissecting intersubunit contacts in cyclic nucleotide-gated ion channels. Neuron. 33:703-713.
23. Zagotta,W. N., N. B. Olivier,., E. Gouaux. 2003. Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature. 425:200-205.
24. Craven, K. B., and W. N. Zagotta. 2004. Salt bridges and gating in the COOH-terminal region of HCN2 and CNGA1 channels. J. Gen. Physiol. 124:663-677.
25. Hua, L., and S. E. Gordon. 2005. Functional interactions between A0 helices in the C-linker of open CNG channels. J. Gen. Physiol. 125:335-344.
26. Ludwig, J., T. Margalit, ⋯, U. B. Kaupp. 1990. Primary structure of cAMP-gated channel from bovine olfactory epithelium. FEBS Lett. 270:24-29.
27. + channel. Nature. 353:86-90.
28. + channel. J. Gen. Physiol. 108:195-206.
29. Ohlenschläger, O., H. Hojo, ⋯, P. I. Haris. 2002. Three-dimensional structure of the S4-S5 segment of the Shaker potassium channel. Biophys. J. 82:2995-3002.
30. Anselmi, C., P. Carloni, and V. Torre. 2007. Origin of functional diversity among tetrameric voltage-gated channels. Proteins. 66:136-146.
31. Rosenbaum, T., A. Gordon-Shaag, ⋯, S. E. Gordon. 2004. Statedependent block of CNG channels by dequalinium. J. Gen. Physiol. 123:295-304.
32. Nache, V., E. Schulz, ⋯, K. Benndorf. 2005. Activation of olfactorytype cyclic nucleotide-gated channels is highly cooperative. J. Physiol. 569:91-102.
33. Biskup, C., J. Kusch,., K. Benndorf. 2007. Relating ligand binding to activation gating in CNGA2 channels. Nature. 446:440-443.
34. Colquhoun, D. 1998. Binding, gating, affinity and efficacy: The interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br. J. Pharmacol. 125:924-947.
35. Li, J., W. N. Zagotta, and H. A. Lester. 1997. Cyclic nucleotide-gated channels: Structural basis of ligand efficacy and allosteric modulation. Q. Rev. Biophys. 30:177-193.
36. Weiss, J. N. 1997. The Hill equation revisited: Uses and misuses. FASEB J. 11:835-841.
37. Hamill, O. P., A. Marty, ⋯, F. J. Sigworth. 1981. Improved patchclamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391:85-100.
38. Wells, J. A. 1990. Additivity of mutational effects in proteins. Biochemistry. 29:8509-8517.
39. Mildvan, A. S., D. J. Weber, and A. Kuliopulos. 1992. Quantitative interpretations of double mutations of enzymes. Arch. Biochem. Biophys. 294:327-340.
40. Horovitz, A. 1996. Double-mutant cycles: A powerful tool for analyzing protein structure and function. Fold. Des. 1:R121-R126.
41. Scholle, A., T. Zimmer, ⋯, K. Benndorf. 2004. Effects of Kv1.2 intracellular regions on activation of Kv2.1 channels. Biophys. J. 87: 873-882.
42. Sanguinetti, M. C., and Q. P. Xu. 1999. Mutations of the S4-S5 linker alter activation properties of HERG potassium channels expressed in Xenopus oocytes. J. Physiol. 514:667-675.
43. Sunderman, E. R., andW. N. Zagotta. 1999. Sequence of events underlying the allosteric transition of rod cyclic nucleotide-gated channels. J. Gen. Physiol. 113:621-640.
44. + channel. Nature. 423:33-41.
45. Chen, J., J. S. Mitcheson,., M. C. Sanguinetti. 2001. The S4-S5 linker couples voltage sensing and activation of pacemaker channels. Proc. Natl. Acad. Sci. USA. 98:11277-11282.
46. Decher, N., J. Chen, and M. C. Sanguinetti. 2004. Voltage-dependent gating of hyperpolarization-activated, cyclic nucleotide-gated pacemaker channels: Molecular coupling between the S4-S5 and C-linkers. J. Biol. Chem. 279:13859-13865.
47. Prole, D. L., and G. Yellen. 2006. Reversal of HCN channel voltage dependence via bridging of the S4-S5 linker and Post-S6. J. Gen. Physiol. 128:273-282.
48. Terlau, H., S. H. Heinemann, ⋯, J. Ludwig. 1997. Amino terminaldependent gating of the potassium channel rat EAG is compensated by a mutation in the S4 segment. J. Physiol. 502:537-543.
49. Wang, J., M. C. Trudeau, ⋯, G. A. Robertson. 1998. Regulation of deactivation by an amino terminal domain in human Ether-á- Go-Go-related gene potassium channels. J. Gen. Physiol. 112: 637-647.
50. Chen, J., A. Zou, ⋯, M. C. Sanguinetti. 1999. Long QT syndromeassociated mutations in the Per-Arnt-Sim (PAS) domain of HERG potassium channels accelerate channel deactivation. J. Biol. Chem. 274:10113-10118.
51. Nishizawa, M., and K. Nishizawa. 2009. Coupling of S4 helix translocation and S6 gating analyzed by molecular-dynamics simulations of mutated Kv channels. Biophys. J. 97:90-100.