2k0f › Citations

A coupled equilibrium shift mechanism in calmodulin-mediated signal transduction.

Gsponer J, Christodoulou J, Cavalli A, Bui JM, Richter B, Dobson CM, Vendruscolo M
Structure 16 736-46 (2008)
Cited: 77 times
EuropePMC logo PMID: 18462678

Abstract

We used nuclear magnetic resonance data to determine ensembles of conformations representing the structure and dynamics of calmodulin (CaM) in the calcium-bound state (Ca(2+)-CaM) and in the state bound to myosin light chain kinase (CaM-MLCK). These ensembles reveal that the Ca(2+)-CaM state includes a range of structures similar to those present when CaM is bound to MLCK. Detailed analysis of the ensembles demonstrates that correlated motions within the Ca(2+)-CaM state direct the structural fluctuations toward complex-like substates. This phenomenon enables initial ligation of MLCK at the C-terminal domain of CaM and induces a population shift among the substates accessible to the N-terminal domain, thus giving rise to the cooperativity associated with binding. Based on these results and the combination of modern free energy landscape theory with classical allostery models, we suggest that a coupled equilibrium shift mechanism controls the efficient binding of CaM to a wide range of ligands.

Articles - 2k0f mentioned but not cited (9)

  1. A coupled equilibrium shift mechanism in calmodulin-mediated signal transduction. Gsponer J, Christodoulou J, Cavalli A, Bui JM, Richter B, Dobson CM, Vendruscolo M. Structure 16 736-746 (2008)
  2. Assembly of membrane-bound protein complexes: detection and analysis by single molecule diffusion. Ziemba BP, Knight JD, Falke JJ. Biochemistry 51 1638-1647 (2012)
  3. Calmodulin fishing with a structurally disordered bait triggers CyaA catalysis. O'Brien DP, Durand D, Voegele A, Hourdel V, Davi M, Chamot-Rooke J, Vachette P, Brier S, Ladant D, Chenal A. PLoS Biol 15 e2004486 (2017)
  4. Exploring NMR ensembles of calcium binding proteins: perspectives to design inhibitors of protein-protein interactions. Isvoran A, Badel A, Craescu CT, Miron S, Miteva MA. BMC Struct Biol 11 24 (2011)
  5. Structure and mechanism of calmodulin binding to a signaling sphingolipid reveal new aspects of lipid-protein interactions. Kovacs E, Harmat V, Tóth J, Vértessy BG, Módos K, Kardos J, Liliom K. FASEB J 24 3829-3839 (2010)
  6. Secondary structure, a missing component of sequence-based minimotif definitions. Sargeant DP, Gryk MR, Maciejewski MW, Thapar V, Kundeti V, Rajasekaran S, Romero P, Dunker K, Li SC, Kaneko T, Schiller MR. PLoS One 7 e49957 (2012)
  7. PIRT the TRP Channel Regulating Protein Binds Calmodulin and Cholesterol-Like Ligands. Sisco NJ, Luu DD, Kim M, Van Horn WD. Biomolecules 10 E478 (2020)
  8. PYK2 senses calcium through a disordered dimerization and calmodulin-binding element. Momin AA, Mendes T, Barthe P, Faure C, Hong S, Yu P, Kadaré G, Jaremko M, Girault JA, Jaremko Ł, Arold ST. Commun Biol 5 800 (2022)
  9. A Free-Energy Landscape Analysis of Calmodulin Obtained from an NMR Data-Utilized Multi-Scale Divide-and-Conquer Molecular Dynamics Simulation. Shimoyama H, Shigeta Y. Life (Basel) 11 1241 (2021)


Reviews citing this publication (14)

  1. The role of dynamic conformational ensembles in biomolecular recognition. Boehr DD, Nussinov R, Wright PE. Nat Chem Biol 5 789-796 (2009)
  2. Sending signals dynamically. Smock RG, Gierasch LM. Science 324 198-203 (2009)
  3. Insights into Protein-Ligand Interactions: Mechanisms, Models, and Methods. Du X, Li Y, Xia YL, Ai SM, Liang J, Sang P, Ji XL, Liu SQ. Int J Mol Sci 17 (2016)
  4. Structural diversity of calmodulin binding to its target sites. Tidow H, Nissen P. FEBS J 280 5551-5565 (2013)
  5. Protein dynamics and allostery: an NMR view. Tzeng SR, Kalodimos CG. Curr Opin Struct Biol 21 62-67 (2011)
  6. Probing the diverse landscape of protein flexibility and binding. Marsh JA, Teichmann SA, Forman-Kay JD. Curr Opin Struct Biol 22 643-650 (2012)
  7. Protein dynamics and function from solution state NMR spectroscopy. Kovermann M, Rogne P, Wolf-Watz M. Q Rev Biophys 49 e6 (2016)
  8. The ever changing moods of calmodulin: how structural plasticity entails transductional adaptability. Villarroel A, Taglialatela M, Bernardo-Seisdedos G, Alaimo A, Agirre J, Alberdi A, Gomis-Perez C, Soldovieri MV, Ambrosino P, Malo C, Areso P. J Mol Biol 426 2717-2735 (2014)
  9. Pre-existing soft modes of motion uniquely defined by native contact topology facilitate ligand binding to proteins. Meireles L, Gur M, Bakan A, Bahar I. Protein Sci 20 1645-1658 (2011)
  10. Pressure-A Gateway to Fundamental Insights into Protein Solvation, Dynamics, and Function. Luong TQ, Kapoor S, Winter R. Chemphyschem 16 3555-3571 (2015)
  11. How do dynamic cellular signals travel long distances? Nussinov R. Mol Biosyst 8 22-26 (2012)
  12. Enzymatic activity in disordered states of proteins. Vendruscolo M. Curr Opin Chem Biol 14 671-675 (2010)
  13. Native and engineered sensors for Ca2+ and Zn2+: lessons from calmodulin and MTF1. Carpenter MC, Palmer AE. Essays Biochem 61 237-243 (2017)
  14. Regulation of Cardiac Cav1.2 Channels by Calmodulin. Kameyama M, Minobe E, Shao D, Xu J, Gao Q, Hao L. Int J Mol Sci 24 6409 (2023)

Articles citing this publication (54)

  1. Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Csermely P, Palotai R, Nussinov R. Trends Biochem Sci 35 539-546 (2010)
  2. The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding. Bakan A, Bahar I. Proc Natl Acad Sci U S A 106 14349-14354 (2009)
  3. Dynamics connect substrate recognition to catalysis in protein kinase A. Masterson LR, Cheng C, Yu T, Tonelli M, Kornev A, Taylor SS, Veglia G. Nat Chem Biol 6 821-828 (2010)
  4. Dynamically committed, uncommitted, and quenched states encoded in protein kinase A revealed by NMR spectroscopy. Masterson LR, Shi L, Metcalfe E, Gao J, Taylor SS, Veglia G. Proc Natl Acad Sci U S A 108 6969-6974 (2011)
  5. Novel allosteric sites on Ras for lead generation. Grant BJ, Lukman S, Hocker HJ, Sayyah J, Brown JH, McCammon JA, Gorfe AA. PLoS One 6 e25711 (2011)
  6. Relative solvent accessible surface area predicts protein conformational changes upon binding. Marsh JA, Teichmann SA. Structure 19 859-867 (2011)
  7. Thermodynamic basis for the optimization of binding-induced biomolecular switches and structure-switching biosensors. Vallée-Bélisle A, Ricci F, Plaxco KW. Proc Natl Acad Sci U S A 106 13802-13807 (2009)
  8. Transient, sparsely populated compact states of apo and calcium-loaded calmodulin probed by paramagnetic relaxation enhancement: interplay of conformational selection and induced fit. Anthis NJ, Doucleff M, Clore GM. J Am Chem Soc 133 18966-18974 (2011)
  9. Distinct states of methionyl-tRNA synthetase indicate inhibitor binding by conformational selection. Koh CY, Kim JE, Shibata S, Ranade RM, Yu M, Liu J, Gillespie JR, Buckner FS, Verlinde CL, Fan E, Hol WG. Structure 20 1681-1691 (2012)
  10. A docking study using atomistic conformers generated via elastic network model for cyclosporin A/cyclophilin A complex. Akten ED, Cansu S, Doruker P. J Biomol Struct Dyn 27 13-26 (2009)
  11. The N(0)-binding region of the vesicular stomatitis virus phosphoprotein is globally disordered but contains transient α-helices. Leyrat C, Jensen MR, Ribeiro EA, Gérard FC, Ruigrok RW, Blackledge M, Jamin M. Protein Sci 20 542-556 (2011)
  12. Tradeoff between stability and multispecificity in the design of promiscuous proteins. Fromer M, Shifman JM. PLoS Comput Biol 5 e1000627 (2009)
  13. Scale-free flow of life: on the biology, economics, and physics of the cell. Kurakin A. Theor Biol Med Model 6 6 (2009)
  14. Identification of an L-phenylalanine binding site enhancing the cooperative responses of the calcium-sensing receptor to calcium. Zhang C, Huang Y, Jiang Y, Mulpuri N, Wei L, Hamelberg D, Brown EM, Yang JJ. J Biol Chem 289 5296-5309 (2014)
  15. Pivoting between calmodulin lobes triggered by calcium in the Kv7.2/calmodulin complex. Alaimo A, Alberdi A, Gomis-Perez C, Fernández-Orth J, Bernardo-Seisdedos G, Malo C, Millet O, Areso P, Villarroel A. PLoS One 9 e86711 (2014)
  16. Detecting intramolecular dynamics and multiple Förster resonance energy transfer states by fluorescence correlation spectroscopy. Price ES, DeVore MS, Johnson CK. J Phys Chem B 114 5895-5902 (2010)
  17. Conformational equilibrium of N-myristoylated cAMP-dependent protein kinase A by molecular dynamics simulations. Cembran A, Masterson LR, McClendon CL, Taylor SS, Gao J, Veglia G. Biochemistry 51 10186-10196 (2012)
  18. Determination of the individual roles of the linker residues in the interdomain motions of calmodulin using NMR chemical shifts. Kukic P, Camilloni C, Cavalli A, Vendruscolo M. J Mol Biol 426 1826-1838 (2014)
  19. ClustENM: ENM-Based Sampling of Essential Conformational Space at Full Atomic Resolution. Kurkcuoglu Z, Bahar I, Doruker P. J Chem Theory Comput 12 4549-4562 (2016)
  20. Designing molecular dynamics simulations to shift populations of the conformational states of calmodulin. Aykut AO, Atilgan AR, Atilgan C. PLoS Comput Biol 9 e1003366 (2013)
  21. DNA energy landscapes via calorimetric detection of microstate ensembles of metastable macrostates and triplet repeat diseases. Völker J, Klump HH, Breslauer KJ. Proc Natl Acad Sci U S A 105 18326-18330 (2008)
  22. Ligand depletion in vivo modulates the dynamic range and cooperativity of signal transduction. Edelstein SJ, Stefan MI, Le Novère N. PLoS One 5 e8449 (2010)
  23. Effect of Ca2+ on the promiscuous target-protein binding of calmodulin. Westerlund AM, Delemotte L. PLoS Comput Biol 14 e1006072 (2018)
  24. MOAG-4 promotes the aggregation of α-synuclein by competing with self-protective electrostatic interactions. Yoshimura Y, Holmberg MA, Kukic P, Andersen CB, Mata-Cabana A, Falsone SF, Vendruscolo M, Nollen EAA, Mulder FAA. J Biol Chem 292 8269-8278 (2017)
  25. Molecular dynamics simulations indicate an induced-fit mechanism for LSD1/CoREST-H3-histone molecular recognition. Vellore NA, Baron R. BMC Biophys 6 15 (2013)
  26. Probing conformational and functional substates of calmodulin by high pressure FTIR spectroscopy: influence of Ca2+ binding and the hypervariable region of K-Ras4B. Erwin N, Patra S, Winter R. Phys Chem Chem Phys 18 30020-30028 (2016)
  27. Toward High-Throughput Predictive Modeling of Protein Binding/Unbinding Kinetics. Chiu SH, Xie L. J Chem Inf Model 56 1164-1174 (2016)
  28. Calmodulin-Calcineurin Interaction beyond the Calmodulin-Binding Region Contributes to Calcineurin Activation. Sun B, Vaughan D, Tikunova S, Creamer TP, Davis JP, Kekenes-Huskey PM. Biochemistry 58 4070-4085 (2019)
  29. FRET-FCS detection of intralobe dynamics in calmodulin. Price ES, Aleksiejew M, Johnson CK. J Phys Chem B 115 9320-9326 (2011)
  30. Identification of potential small molecule binding pockets on Rho family GTPases. Ortiz-Sanchez JM, Nichols SE, Sayyah J, Brown JH, McCammon JA, Grant BJ. PLoS One 7 e40809 (2012)
  31. A general framework to characterize inhibitors of calmodulin: use of calmodulin inhibitors to study the interaction between calmodulin and its calmodulin binding domains. Audran E, Dagher R, Gioria S, Tsvetkov PO, Kulikova AA, Didier B, Villa P, Makarov AA, Kilhoffer MC, Haiech J. Biochim Biophys Acta 1833 1720-1731 (2013)
  32. Fluorescence, circular dichroism, NMR, and docking studies of the interaction of the alkaloid malbrancheamide with calmodulin. Figueroa M, González-Andrade M, Sosa-Peinado A, Madariaga-Mazón A, Del Río-Portilla F, González Mdel C, Mata R. J Enzyme Inhib Med Chem 26 378-385 (2011)
  33. Biosynthesis of a Novel Glutamate Racemase Containing a Site-Specific 7-Hydroxycoumarin Amino Acid: Enzyme-Ligand Promiscuity Revealed at the Atomistic Level. Dean SF, Whalen KL, Spies MA. ACS Cent Sci 1 364-373 (2015)
  34. Crystallographic snapshots of initial steps in the collapse of the calmodulin central helix. Kursula P. Acta Crystallogr D Biol Crystallogr 70 24-30 (2014)
  35. Conformational Ensembles of Calmodulin Revealed by Nonperturbing Site-Specific Vibrational Probe Groups. Kelly KL, Dalton SR, Wai RB, Ramchandani K, Xu RJ, Linse S, Londergan CH. J Phys Chem A 122 2947-2955 (2018)
  36. Energetics and structural characterization of the "DFG-flip" conformational transition of B-RAF kinase: a SITS molecular dynamics study. Shao Q, Xu Z, Wang J, Shi J, Zhu W. Phys Chem Chem Phys 19 1257-1267 (2017)
  37. Quantitative approaches to defining normal and aberrant protein homeostasis. Vendruscolo M, Dobson CM. Faraday Discuss 143 277-91; discussion 359-72 (2009)
  38. Cyanylated Cysteine Reports Site-Specific Changes at Protein-Protein-Binding Interfaces Without Perturbation. Dalton SR, Vienneau AR, Burstein SR, Xu RJ, Linse S, Londergan CH. Biochemistry 57 3702-3712 (2018)
  39. Photounbinding of calmodulin from a family of CaM binding peptides. Neumüller KG, Elsayad K, Reisecker JM, Waxham MN, Heinze KG. PLoS One 5 e14050 (2010)
  40. Size-dependent impact of CNTs on dynamic properties of calmodulin. Gao J, Wang L, Kang SG, Zhao L, Ji M, Chen C, Zhao Y, Zhou R, Li J. Nanoscale 6 12828-12837 (2014)
  41. Structural dynamics of calmodulin-ryanodine receptor interactions: electron paramagnetic resonance using stereospecific spin labels. Her C, Thompson AR, Karim CB, Thomas DD. Sci Rep 8 10681 (2018)
  42. Letter Competitive inhibition of TRPV1-calmodulin interaction by vanilloids. Hetényi A, Németh L, Wéber E, Szakonyi G, Winter Z, Jósvay K, Bartus É, Oláh Z, Martinek TA. FEBS Lett 590 2768-2775 (2016)
  43. Computing energy landscape maps and structural excursions of proteins. Sapin E, Carr DB, De Jong KA, Shehu A. BMC Genomics 17 Suppl 4 546 (2016)
  44. Distinguishing unfolding and functional conformational transitions of calmodulin using ultraviolet resonance Raman spectroscopy. Jones EM, Balakrishnan G, Squier TC, Spiro TG. Protein Sci 23 1094-1101 (2014)
  45. Ensemblator v3: Robust atom-level comparative analyses and classification of protein structure ensembles. Brereton AE, Karplus PA. Protein Sci 27 41-50 (2018)
  46. Assessing the Role of Calmodulin's Linker Flexibility in Target Binding. Sun B, Kekenes-Huskey PM. Int J Mol Sci 22 (2021)
  47. From Optimization to Mapping: An Evolutionary Algorithm for Protein Energy Landscapes. Sapin E, De Jong KA, Shehu A. IEEE/ACM Trans Comput Biol Bioinform 15 719-731 (2018)
  48. Increasing the sampling efficiency of protein conformational transition using velocity-scaling optimized hybrid explicit/implicit solvent REMD simulation. Yu Y, Wang J, Shao Q, Shi J, Zhu W. J Chem Phys 142 125105 (2015)
  49. Binding and backbone dynamics of protein under topological constraint: calmodulin as a model system. Katyal P, Yang Y, Fu YJ, Iandosca J, Vinogradova O, Lin Y. Chem Commun (Camb) 54 8917-8920 (2018)
  50. NaV1.2 EFL domain allosterically enhances Ca2+ binding to sites I and II of WT and pathogenic calmodulin mutants bound to the channel CTD. Mahling R, Hovey L, Isbell HM, Marx DC, Miller MS, Kilpatrick AM, Weaver LD, Yoder JB, Kim EH, Andresen CNJ, Li S, Shea MA. Structure 29 1339-1356.e7 (2021)
  51. A structural comparison of 'real' and 'model' calmodulin clarified allosteric interactions regulating domain motion. Shimoyama H. J Biomol Struct Dyn 37 1567-1581 (2019)
  52. Dynamics and structural changes of calmodulin upon interaction with the antagonist calmidazolium. Léger C, Pitard I, Sadi M, Carvalho N, Brier S, Mechaly A, Raoux-Barbot D, Davi M, Hoos S, Weber P, Vachette P, Durand D, Haouz A, Guijarro JI, Ladant D, Chenal A. BMC Biol 20 176 (2022)
  53. Non-Canonical Interaction between Calmodulin and Calcineurin Contributes to the Differential Regulation of Plant-Derived Calmodulins on Calcineurin. Sun B, Fang X, Johnson CN, Hauck G, Kou Y, Davis JP, Kekenes-Huskey PM. J Chem Inf Model 61 5223-5233 (2021)
  54. Visualizing Heterogeneous Protein Conformations with Multi-Tilt Nanoparticle-Aided Cryo-Electron Microscopy Sampling. Kim C, Kim Y, Lee SJ, Yun SR, Choi J, Kim SO, Yang Y, Ihee H. Nano Lett 23 3334-3343 (2023)


Quick links