Double electron - Electron resonance reveals cAMP-induced conformational change in HCN channels

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 27, 2014, Pages 9816-9821

  Puljung, Michael C ^a   DeBerg, Hannah A ^a   Zagotta, William N ^a   Stoll, Stefan ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Allosteric regulation; Hyperpolarization activated ion channels

Indexed keywords

CYCLIC AMP; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL;

ALLOSTERISM; ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DOUBLE ELECTRON ELECTRON RESONANCE SPECTROSCOPY; ELECTRON SPIN RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPECTROSCOPY; SPIN LABELING;

ALLOSTERIC REGULATION; HYPERPOLARIZATION-ACTIVATED ION CHANNELS;

ANIMALS; CYCLIC AMP; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; MICE; MODELS, MOLECULAR; POTASSIUM CHANNELS; PROTEIN CONFORMATION; SPECTRUM ANALYSIS; SPIN LABELS;

EID: 84903957215     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1405371111     Document Type: Article

References (46)

1. Hille B (2001) Ion Channels of Excitable Membranes (Sinauer, Sunderland, MA), 3rd Ed.
2. Robinson RB, Siegelbaum SA (2003) Hyperpolarization-activated cation currents: From molecules to physiological function. Annu Rev Physiol 65:453-480. (Pubitemid 38249163)
3. DiFrancesco D (1986) Characterization of single pacemaker channels in cardiac sinoatrial node cells. Nature 324(6096):470-473.
4. DiFrancesco D (1993) Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol 55:455-472.
5. DiFrancesco D, Tortora P (1991) Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351(6322):145-147. (Pubitemid 21896552)
6. Magee JC (1999) Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2(9):848.
7. Pape HC, McCormick DA (1989) Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature 340(6236):715-718.
8. Williams SR, Stuart GJ (2000) Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol 83(5):3177-3182. (Pubitemid 30321508)
9. Craven KB, Olivier NB, Zagotta WN (2008) C-terminal movement during gating in cyclic nucleotide-modulated channels. J Biol Chem 283(21):14728-14738.
10. Flynn GE, Black KD, Islas LD, Sankaran B, Zagotta WN (2007) Structure and re-arrangements in the carboxy-terminal region of SpIH channels. Structure 15(6):671-682. (Pubitemid 46874078)
11. Lolicato M, et al. (2011) Tetramerization dynamics of C-terminal domain underlies isoform-specific cAMP gating in hyperpolarization-activated cyclic nucleotide-gated channels. J Biol Chem 286(52):44811-44820.
12. Taraska JW, Puljung MC, Olivier NB, Flynn GE, Zagotta WN (2009) Mapping the structure and conformational movements of proteins with transition metal ion FRET. Nat Methods 6(7):532-537.
13. Xu X, Vysotskaya ZV, Liu Q, Zhou L (2010) Structural basis for the cAMP-dependent gating in the human HCN4 channel. J Biol Chem 285(47):37082-37091.
14. Zagotta WN, et al. (2003) Structural basis for modulation and agonist specificity of HCN pacemaker channels. Nature 425(6954):200-205. (Pubitemid 37150901)
15. Clayton GM, Silverman WR, Heginbotham L, Morais-Cabral JH (2004) Structural basis of ligand activation in a cyclic nucleotide regulated potassium channel. Cell 119(5):615-627. (Pubitemid 39535750)
16. Kim C, Xuong NH, Taylor SS (2005) Crystal structure of a complex between the catalytic and regulatory (RIalpha) subunits of PKA. Science 307(5710):690-696. (Pubitemid 40194632)
17. Kim JJ, et al. (2011) Co-crystal structures of PKG Iβ (92-227) with cGMP and cAMP reveal the molecular details of cyclic-nucleotide binding. PLoS ONE 6(4):e18413.
18. Rehmann H, et al. (2003) Structure and regulation of the cAMP-binding domains of Epac2. Nat Struct Biol 10(1):26-32. (Pubitemid 36034173)
19. Weber IT, Gilliland GL, Harman JG, Peterkofsky A (1987) Crystal structure of a cyclic AMP-independent mutant of catabolite gene activator protein. J Biol Chem 262(12):5630-5636.
20. Brelidze TI, Carlson AE, Sankaran B, Zagotta WN (2012) Structure of the carboxyterminal region of a KCNH channel. Nature 481(7382):530-533.
21. Brelidze TI, Gianulis EC, DiMaio F, Trudeau MC, Zagotta WN (2013) Structure of the C-terminal region of an ERG channel and functional implications. Proc Natl Acad Sci USA 110(28):11648-11653.
22. Craven KB, Zagotta WN (2004) Salt bridges and gating in the COOH-terminal region of HCN2 and CNGA1 channels. J Gen Physiol 124(6):663-677. (Pubitemid 39628134)
23. Paoletti P, Young EC, Siegelbaum SA (1999) C-Linker of cyclic nucleotide-gated channels controls coupling of ligand binding to channel gating. J Gen Physiol 113(1):17-34.
24. Matulef K, Flynn GE, Zagotta WN (1999) Molecular rearrangements in the ligand-binding domain of cyclic nucleotide-gated channels. Neuron 24(2):443-452. (Pubitemid 29508417)
25. Matulef K, Zagotta WN (2002) Multimerization of the ligand binding domains of cyclic nucleotide-gated channels. Neuron 36(1):93-103.
26. Puljung MC, Zagotta WN (2013) A secondary structural transition in the C-helix promotes gating of cyclic nucleotide-regulated ion channels. J Biol Chem 288(18):12944-12956.
27. Tibbs GR, Liu DT, Leypold BG, Siegelbaum SA (1998) A state-independent interaction between ligand and a conserved arginine residue in cyclic nucleotide-gated channels reveals a functional polarity of the cyclic nucleotide binding site. J Biol Chem 273(8):4497-4505. (Pubitemid 28103190)
28. Varnum MD, Black KD, Zagotta WN (1995) Molecular mechanism for ligand discrimination of cyclic nucleotide-gated channels. Neuron 15(3):619-625.
29. Zhou L, Siegelbaum SA (2007) Gating of HCN channels by cyclic nucleotides: Residue contacts that underlie ligand binding, selectivity, and efficacy. Structure 15(6):655-670. (Pubitemid 46874082)
30. Pannier M, Veit S, Godt A, Jeschke G, Spiess HW (2000) Dead-time free measurement of dipole-dipole interactions between electron spins. J Magn Reson 142(2):331-340.
31. Milov AD, Ponomarev AB, Tsvetkov YD (1984) Electron electron double-resonance in electron-spin echo-model biradical systems and the sensitized photolysis of dDecalin. Chem Phys Lett 110(1):67-72.
32. Martin RE, et al. (1998) Determination of end-to-end distances in a series of TEMPO diradicals of up to 2.8 nm length with a new four-pulse double electron electron resonance experiment. Angew Chem Int Ed Engl 37(20):2834-2837. (Pubitemid 29008565)
33. Jeschke G (2012) Characterization of protein conformational changes with sparse spin-label distance constraints. J Chem Theory Comput 8(10):3854-3863.
34. Chow SS, Van Petegem F, Accili EA (2012) Energetics of cyclic AMP binding to HCN channel C terminus reveal negative cooperativity. J Biol Chem 287(1):600-606.
35. Milov AD, Naumov BD, Tsvetkov YD (2004) The effect of microwave pulse duration on the distance distribution function between spin labels obtained by PELDOR data analysis. Appl Magn Reson 26(4):587- 599.
36. Zhou L, Siegelbaum SA (2008) Pathway and endpoint free energy calculations for cyclic nucleotide binding to HCN channels. Biophys J 94(12):L90-L92.
37. Craven KB, Zagotta WN (2006) CNG and HCN channels: Two peas, one pod. Annu Rev Physiol 68:375-401.
38. Taraska JW, Puljung MC, Zagotta WN (2009) Short-distance probes for protein backbone structure based on energy transfer between bimane and transition metal ions. Proc Natl Acad Sci USA 106(38):16227- 16232.
39. Schünke S, Stoldt M, Lecher J, Kaupp UB, Willbold D (2011) Structural insights into conformational changes of a cyclic nucleotide-binding domain in solution from Mesorhizobium loti K1 channel. Proc Natl Acad Sci USA 108(15):6121-6126.
40. Schünke S, Stoldt M, Novak K, Kaupp UB, Willbold D (2009) Solution structure of the Mesorhizobium loti K1 channel cyclic nucleotide-binding domain in complex with cAMP. EMBO Rep 10(7):729-735.
41. Popovych N, Tzeng SR, Tonelli M, Ebright RH, Kalodimos CG (2009) Structural basis for cAMP-mediated allosteric control of the catabolite activator protein. Proc Natl Acad Sci USA 106(17):6927-6932.
42. Altieri SL, et al. (2008) Structural and energetic analysis of activation by a cyclic nucleotide binding domain. J Mol Biol 381(3):655-669.
43. Jeschke G, et al. (2006) DeerAnalysis2006-A comprehensive software package for analyzing pulsed ELDOR data. Appl Magn Reson 30(3-4):473-498.
44. Stoll S, Schweiger A (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J Magn Reson 178(1):42-55. (Pubitemid 41774010)
45. Polyhach Y, Bordignon E, Jeschke G (2011) Rotamer libraries of spin labelled cysteines for protein studies. Phys Chem Chem Phys 13(6):2356-2366.
46. Zheng W, Brooks BR (2006) Modeling protein conformational changes by iterative fitting of distance constraints using reoriented normal modes. Biophys J 90(12):4327-4336. (Pubitemid 43830881)