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Structural insights into conformational changes of a cyclic nucleotide-binding domain in solution from Mesorhizobium loti K1 channel.

Schünke S, Stoldt M, Lecher J, Kaupp UB, Willbold D
Proc Natl Acad Sci U S A 108 6121-6 (2011)
Cited: 36 times
EuropePMC logo PMID: 21430265

Abstract

Cyclic nucleotide-sensitive ion channels, known as HCN and CNG channels, are activated by binding of ligands to a domain (CNBD) located on the cytoplasmic side of the channel. The underlying mechanisms are not well understood. To elucidate the gating mechanism, structures of both the ligand-free and -bound CNBD are required. Several crystal structures of the CNBD from HCN2 and a bacterial CNG channel (MloK1) have been solved. However, for HCN2, the cAMP-free and -bound state did not reveal substantial structural rearrangements. For MloK1, structural information for the cAMP-free state has only been gained from mutant CNBDs. Moreover, in the crystal, the CNBD molecules form an interface between dimers, proposed to be important for allosteric channel gating. Here, we have determined the solution structure by NMR spectroscopy of the cAMP-free wild-type CNBD of MloK1. A comparison of the solution structure of cAMP-free and -bound states reveals large conformational rearrangement on ligand binding. The two structures provide insights on a unique set of conformational events that accompany gating within the ligand-binding site.

Articles - 2kxl mentioned but not cited (6)

  1. Structural insights into conformational changes of a cyclic nucleotide-binding domain in solution from Mesorhizobium loti K1 channel. Schünke S, Stoldt M, Lecher J, Kaupp UB, Willbold D. Proc. Natl. Acad. Sci. U.S.A. 108 6121-6126 (2011)
  2. Ligand-induced structural changes in the cyclic nucleotide-modulated potassium channel MloK1. Kowal J, Chami M, Baumgartner P, Arheit M, Chiu PL, Rangl M, Scheuring S, Schröder GF, Nimigean CM, Stahlberg H. Nat Commun 5 3106 (2014)
  3. Kinetics of ligand-receptor interaction reveals an induced-fit mode of binding in a cyclic nucleotide-activated protein. Peuker S, Cukkemane A, Held M, Noé F, Kaupp UB, Seifert R. Biophys. J. 104 63-74 (2013)
  4. A cAMP Sensor Based on Ligand-Dependent Protein Stabilization. Sidoli M, Chen LC, Lu AJ, Wandless TJ, Talbot WS. ACS Chem Biol 17 2024-2030 (2022)
  5. Exploring the Alternative Conformation of a Known Protein Structure Based on Contact Map Prediction. Li J, Wang L, Zhu Z, Song C. J Chem Inf Model 64 301-315 (2024)
  6. Structure and electromechanical coupling of a voltage-gated Na+/H+ exchanger. Yeo H, Mehta V, Gulati A, Drew D. Nature 623 193-201 (2023)


Reviews citing this publication (1)

  1. CNG channel structure, function, and gating: a tale of conformational flexibility. Napolitano LMR, Torre V, Marchesi A. Pflugers Arch 473 1423-1435 (2021)

Articles citing this publication (29)

  1. Structure of the carboxy-terminal region of a KCNH channel. Brelidze TI, Carlson AE, Sankaran B, Zagotta WN. Nature 481 530-533 (2012)
  2. Double electron-electron resonance reveals cAMP-induced conformational change in HCN channels. Puljung MC, DeBerg HA, Zagotta WN, Stoll S. Proc. Natl. Acad. Sci. U.S.A. 111 9816-9821 (2014)
  3. Structural basis for the mutual antagonism of cAMP and TRIP8b in regulating HCN channel function. Saponaro A, Pauleta SR, Cantini F, Matzapetakis M, Hammann C, Donadoni C, Hu L, Thiel G, Banci L, Santoro B, Moroni A. Proc. Natl. Acad. Sci. U.S.A. 111 14577-14582 (2014)
  4. Regulation of hyperpolarization-activated cyclic nucleotide-gated (HCN) channel activity by cCMP. Zong X, Krause S, Chen CC, Krüger J, Gruner C, Cao-Ehlker X, Fenske S, Wahl-Schott C, Biel M. J. Biol. Chem. 287 26506-26512 (2012)
  5. Gating of the MlotiK1 potassium channel involves large rearrangements of the cyclic nucleotide-binding domains. Mari SA, Pessoa J, Altieri S, Hensen U, Thomas L, Morais-Cabral JH, Müller DJ. Proc. Natl. Acad. Sci. U.S.A. 108 20802-20807 (2011)
  6. A mechanism for the auto-inhibition of hyperpolarization-activated cyclic nucleotide-gated (HCN) channel opening and its relief by cAMP. Akimoto M, Zhang Z, Boulton S, Selvaratnam R, VanSchouwen B, Gloyd M, Accili EA, Lange OF, Melacini G. J. Biol. Chem. 289 22205-22220 (2014)
  7. Cytoplasmic domains and voltage-dependent potassium channel gating. Barros F, Domínguez P, de la Peña P. Front Pharmacol 3 49 (2012)
  8. A secondary structural transition in the C-helix promotes gating of cyclic nucleotide-regulated ion channels. Puljung MC, Zagotta WN. J. Biol. Chem. 288 12944-12956 (2013)
  9. A novel biosensor to study cAMP dynamics in cilia and flagella. Mukherjee S, Jansen V, Jikeli JF, Hamzeh H, Alvarez L, Dombrowski M, Balbach M, Strünker T, Seifert R, Kaupp UB, Wachten D. Elife 5 (2016)
  10. Structure and dynamics underlying elementary ligand binding events in human pacemaking channels. Goldschen-Ohm MP, Klenchin VA, White DS, Cowgill JB, Cui Q, Goldsmith RH, Chanda B. Elife 5 (2016)
  11. Structure of the SthK carboxy-terminal region reveals a gating mechanism for cyclic nucleotide-modulated ion channels. Kesters D, Brams M, Nys M, Wijckmans E, Spurny R, Voets T, Tytgat J, Kusch J, Ulens C. PLoS ONE 10 e0116369 (2015)
  12. A K(+)-selective CNG channel orchestrates Ca(2+) signalling in zebrafish sperm. Fechner S, Alvarez L, Bönigk W, Müller A, Berger TK, Pascal R, Trötschel C, Poetsch A, Stölting G, Siegfried KR, Kremmer E, Seifert R, Kaupp UB. Elife 4 (2015)
  13. Insight into the molecular interaction between the cyclic nucleotide-binding homology domain and the eag domain of the hERG channel. Li Q, Ng HQ, Yoon HS, Kang C. FEBS Lett. 588 2782-2788 (2014)
  14. A KcsA/MloK1 chimeric ion channel has lipid-dependent ligand-binding energetics. McCoy JG, Rusinova R, Kim DM, Kowal J, Banerjee S, Jaramillo Cartagena A, Thompson AN, Kolmakova-Partensky L, Stahlberg H, Andersen OS, Nimigean CM. J. Biol. Chem. 289 9535-9546 (2014)
  15. Conformational rearrangements in the transmembrane domain of CNGA1 channels revealed by single-molecule force spectroscopy. Maity S, Mazzolini M, Arcangeletti M, Valbuena A, Fabris P, Lazzarino M, Torre V. Nat Commun 6 7093 (2015)
  16. Real-time visualization of conformational changes within single MloK1 cyclic nucleotide-modulated channels. Rangl M, Miyagi A, Kowal J, Stahlberg H, Nimigean CM, Scheuring S. Nat Commun 7 12789 (2016)
  17. The gating mechanism in cyclic nucleotide-gated ion channels. Mazzolini M, Arcangeletti M, Marchesi A, Napolitano LMR, Grosa D, Maity S, Anselmi C, Torre V. Sci Rep 8 45 (2018)
  18. Solution structure of the cyclic-nucleotide binding homology domain of a KCNH channel. Li Q, Ng HQ, Yoon HS, Kang C. J. Struct. Biol. 186 68-74 (2014)
  19. Determinants of ligand selectivity in a cyclic nucleotide-regulated potassium channel. Pessoa J, Fonseca F, Furini S, Morais-Cabral JH. J. Gen. Physiol. 144 41-54 (2014)
  20. Structure, dynamics and implied gating mechanism of a human cyclic nucleotide-gated channel. Gofman Y, Schärfe C, Marks DS, Haliloglu T, Ben-Tal N. PLoS Comput. Biol. 10 e1003976 (2014)
  21. Structures of inactive CRP species reveal the atomic details of the allosteric transition that discriminates cyclic nucleotide second messengers. Seok SH, Im H, Won HS, Seo MD, Lee YS, Yoon HJ, Cha MJ, Park JY, Lee BJ. Acta Crystallogr. D Biol. Crystallogr. 70 1726-1742 (2014)
  22. A Quantitative Model for cAMP Binding to the Binding Domain of MloK1. Voß B, Seifert R, Kaupp UB, Grubmüller H. Biophys. J. 111 1668-1678 (2016)
  23. Characterization of a cyclic nucleotide-activated K(+) channel and its lipid environment by using solid-state NMR spectroscopy. Cukkemane A, Baldus M. Chembiochem 14 1789-1798 (2013)
  24. (1)H, (13)C and (15)N chemical shift assignments for the cyclic-nucleotide binding homology domain of a KCNH channel. Li Q, Ng HQ, Kang C. Biomol NMR Assign 9 55-58 (2015)
  25. A novel dimerization interface of cyclic nucleotide binding domain, which is disrupted in presence of cAMP: implications for CNG channels gating. Gushchin IY, Gordeliy VI, Grudinin S. J Mol Model 18 4053-4060 (2012)
  26. Inherited macular degeneration-associated mutations in CNGB3 increase the ligand sensitivity and spontaneous open probability of cone cyclic nucleotide-gated channels. Meighan PC, Peng C, Varnum MD. Front Physiol 6 177 (2015)
  27. Molecular Docking, Molecular Dynamics Simulations, and Free Energy Calculation Insights into the Binding Mechanism between VS-4718 and Focal Adhesion Kinase. Shi M, Chen T, Wei S, Zhao C, Zhang X, Li X, Tang X, Liu Y, Yang Z, Chen L. ACS Omega 7 32442-32456 (2022)
  28. Resonance assignment of the ligand-free cyclic nucleotide-binding domain from the murine ion channel HCN2. Börger C, Schünke S, Lecher J, Stoldt M, Winkhaus F, Kaupp UB, Willbold D. Biomol NMR Assign 9 243-246 (2015)
  29. Structural Heterogeneity of CNGA1 Channels Revealed by Electrophysiology and Single-Molecule Force Spectroscopy. Maity S, Marchesi A, Torre V, Mazzolini M. ACS Omega 1 1205-1219 (2016)


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