Artículo

El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Sensor histidine kinases (SHKs) are an integral component of the molecular machinery that permits bacteria to adapt to widely changing environmental conditions. CpxA, an extensively studied SHK, is a multidomain homodimeric protein with each subunit consisting of a periplasmic sensor domain, a transmembrane domain, a signal-transducing HAMP domain, a dimerization and histidine phospho-acceptor sub-domain (DHp) and a catalytic and ATP-binding subdomain (CA). The key activation event involves the rearrangement of the HAMP-DHp helical core and translation of the CA towards the acceptor histidine, which presumably results in an autokinase-competent complex. In the present work we integrate coarse-grained, all-atom, and hybrid QM-MM computer simulations to probe the large-scale conformational reorganization that takes place from the inactive to the autokinase-competent state (conformational step), and evaluate its relation to the autokinase reaction itself (chemical step). Our results highlight a tight coupling between conformational and chemical steps, underscoring the advantage of CA walking along the DHp core, to favor a reactive tautomeric state of the phospho-acceptor histidine. The results not only represent an example of multiscale modelling, but also show how protein dynamics can promote catalysis. © 2017 Elsevier Inc.

Registro:

Documento: Artículo
Título:Multiscale approach to the activation and phosphotransfer mechanism of CpxA histidine kinase reveals a tight coupling between conformational and chemical steps
Autor:Marsico, F.; Burastero, O.; Defelipe, L.A.; Lopez, E.D.; Arrar, M.; Turjanski, A.G.; Marti, M.A.
Filiación:Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2620, Ciudad Autónoma de Buenos Aires, Argentina
IQUIBICEN-UBA/CONICET, Intendente Güiraldes 2620, Ciudad Autónoma de Buenos Aires, Argentina
Instituto de Química-Física de los Materiales, Medio Ambiente y Energía, CONICET-Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Coarse grain; CpxA; Histidine kinase; QM/MM; Two component system; histidine; protein CpxA; protein histidine kinase; unclassified drug; adenosine triphosphate; CpxA protein, E coli; Escherichia coli protein; histidine; protein kinase; Article; autophosphorylation; catalysis; computer simulation; enzyme activation; enzyme conformation; enzyme mechanism; enzyme phosphorylation; molecular dynamics; priority journal; chemistry; metabolism; molecular dynamics; pH; phosphorylation; protein conformation; protein domain; Adenosine Triphosphate; Escherichia coli Proteins; Histidine; Hydrogen-Ion Concentration; Molecular Dynamics Simulation; Phosphorylation; Protein Conformation; Protein Domains; Protein Kinases
Año:2018
Volumen:498
Número:2
Página de inicio:305
Página de fin:312
DOI: http://dx.doi.org/10.1016/j.bbrc.2017.09.039
Título revista:Biochemical and Biophysical Research Communications
Título revista abreviado:Biochem. Biophys. Res. Commun.
ISSN:0006291X
CODEN:BBRCA
CAS:histidine, 645-35-2, 7006-35-1, 71-00-1; protein histidine kinase, 99283-67-7; adenosine triphosphate, 15237-44-2, 56-65-5, 987-65-5; protein kinase, 9026-43-1; Adenosine Triphosphate; CpxA protein, E coli; Escherichia coli Proteins; Histidine; Protein Kinases
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0006291X_v498_n2_p305_Marsico

Referencias:

  • Albanesi, D., Mansilla, M.C., De Mendoza, D., The membrane fluidity sensor DesK of Bacillus subtilis controls the signal decay of its cognate response regulator (2004) J. Bacteriol., 186, pp. 2655-2663. , 186
  • D. y, Silhavy, T.J., Danese, P.N., Snyder, W.B., The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP (1995) Genes Dev., 15, pp. 387-398. , 9
  • Rinaldi, J., Arrar, M., Sycz, G., Structural insights into the HWE histidine kinase family: the Brucella blue light-activated histidine kinase domain (2016) J. Biol. Mol., 24, pp. 4247-4259
  • Dutta, R., Qin, L., Inouye, M., Microreview histidine kinases: diversity of domain organization (1999), 34, pp. 633-640; Ferris, H.U., Dunin-Horkawicz, S., Hornig, N., Hulko, M., Martin, J., Schultz, J.E., Zeth, K., Coles, M., Mechanism of regulation of receptor histidine kinases (2012) Structure, 20, pp. 56-66
  • C.M., L.A.N., Ferris, H.U., Hartmann, M.D., Crystallographic snapshot of the Escherichia coli EnvZ histidine kinase in an active conformation (2014) J. Struct. Biol., 186, pp. 1-4
  • Diensthuber, R.P., Bommer, M., Gleichmann, T., Möglich, A., Full- length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators (2013) Structure, 106, pp. 1127-1136
  • Albanesi, D., Marti, M., Trajtenberg, F., Structural plasticity and catalysis regulation of a thermosensor histidine kinase (2014) PNAS, 106, pp. 6185-16190
  • Wolanin, P.M., Thomason, P.A., Stock, J.B., (2002), pp. 1-8. , Protein family review Histidine protein kinases: key signal transducers outside the animal kingdom; Mechaly, A.E., Soto Diaz, S., Sassoon, N., Structural coupling between autokinase and phosphotransferase reactions in a bacterial histidine kinase (2017) Structure, 24, pp. 4247-4259
  • Trajtenberg, F., Imelio, J.A., Machado, M.R., Larrieux, N., Marti, M.A., Obal, G., Mechaly, A.E., Buschiazzo, A., Regulation of signaling directionality revealed by 3D snapshots of a kinase: regulator complex in action (2016) Elife, 5, p. e21422
  • Nakayama, S., Watanabe, H., Involvement of cpxA, a sensor of a two-component regulatory system, in the pH-dependent regulation of expression of Shigella sonnei virF gene (1995) J. Bacteriol., 177, pp. 5062-5069. , 177
  • C.J. y Hendrickson, W.A., Cheung, J., Hendrickson, W.A., Sensor domains of two-component regulatory systems (2010) Curr. Opin. Microbiol., 13.2, pp. 116-123. , 13
  • Mechaly, A.E., Sassoon, N., Betton, J.M., Alzari, P.M., Segmental helical motions and dynamical asymmetry modulate histidine kinase autophosphorylation (2014) PLoS Biol., 12
  • M.-R.L.M.A. y Casino, P., Casino, P., Miguel-Romero, L., Marina, A., Casino, P., Miguel-Romero, L., Visualizing autophosphorylation in histidine kinases (2014) Nat. Commun., 5, p. 3258
  • Šali, A., Blundell, T.L., Comparative protein modelling by satisfaction of spatial restraints (1993) J. Mol. Biol., 234, pp. 779-815
  • HU1, F., Dunin-Horkawicz, S., Hornig, N., Mechanism of regulation of receptor histidine kinases (2012) Structure, 20, pp. 56-66
  • Salomon-Ferrer, R., Götz, A.W., Poole, D., Le Grand, S., Walker, R.C., Routine microsecond molecular dynamics simulations with AMBER on GPUs. 2. Explicit solvent particle mesh Ewald (2013) J. Chem. Theory Comput., 9, pp. 3878-3888
  • Case, D.A., Betz, R.M., Botello-Smith, W., AMBER 2016 (2016), Univ. California San Fr; Maier, J.A., Martinez, C., Kasavajhala, K., Wickstrom, L., Hauser, K.E., Simmerling, C., ff14SB: improving the accuracy of protein side chain and backbone parameters from ff99SB (2015) J. Chem. Theory Comput., 11, pp. 3696-3713
  • Jorgensen, W.L., Chandrasekhar, J., Madura, J.D., Impey, R.W., Klein, M.L., Comparison of simple potential functions for simulating liquid water (1983) J. Chem. Phys., 79, pp. 926-935
  • Meagher, K.L., Redman, L.T., Carlson, H.A., Development of polyphosphate parameters for use with the AMBER force field (2003) J. Comput. Chem., 24, pp. 1016-1025
  • Hills, R.D., Jr., Lu, L., Voth, G., Multiscale coarse-graining of the protein energy landscape (2010) PLoS Comput. Biol., pp. 1-12
  • y Luciana Capece, L.E.L.M.A.M., Lombardi, L.E., Mart’∖i, M.A., Capece, L., CG2AA: backmapping protein coarse-grained structures (2015) Bioinforma, 32, pp. 1235-1237. , 32
  • Amadei, A., Linssen, A., Berendsen, H.J.C., Essential dynamics of proteins (1993) Proteins Struct. Funct. Bioinforma., 17, pp. 412-425
  • Miyazawa, S., Jernigan, R.L., Self-consistent estimation of inter-residue protein contact energies based on an equilibrium mixture approximation of residues (1999) Proteins Struct. Funct. Bioinforma., 34, pp. 49-68
  • Ramírez, C.L., Petruk, A., Bringas, M., Estrin, D.A., Roitberg, A.E., Marti, M.A., Capece, L., Coarse-grained simulations of heme proteins: validation and study of large conformational transitions (2016) J. Chem. Theory Comput., 12, pp. 3390-3397
  • Mongan, J., Case, D.A., McCAMMON, J.A., Constant pH molecular dynamics in generalized born implicit solvent (2004) J. Comput. Chem., 25, pp. 2038-2048
  • Defelipe, L.A., Lanzarotti, E., Gauto, D., Marti, M.A., Turjanski, A.G., Protein topology determines cysteine oxidation fate: the case of sulfenyl amide formation among protein families (2015) PLoS Comput. Biol., 11, p. e1004051
  • Nitsche, M.A., Ferreria, M., Mocskos, E.E., Gonzalez Lebrero, M.C., GPU accelerated implementation of density functional theory for hybrid QM/MM simulations (2014) J. Chem. Theory Comput., 10, pp. 959-967
  • Project, L.I.O., https://github.com/MALBECC/lio, (n.d.); Perdew, J.P., Burke, K., Ernzerhof, M., Generalized gradient approximation made simple (1996) Phys. Rev. Lett., 77, p. 3865
  • Ram’∖irez, C.L., Mart’∖i, M.A., Roitberg, A.E., Chapter six-steered molecular dynamics methods applied to enzyme mechanism and energetics (2016) Methods Enzymol., 578, pp. 123-143
  • Martí, M.A., Estrin, D.A., Roitberg, A.E., Molecular basis for the pH dependent structural transition of Nitrophorin 4 (2009) J. Phys. Chem. B, 113, pp. 2135-2142
  • Atkinson, M.R., Ninfa, A.J., Mutational analysis of the bacterial signal-transducing protein kinase/phosphatase nitrogen regulator II (NRII or NtrB) (1993) J. Bacteriol., 175, pp. 7016-7023
  • Willett, J.W., Kirby, J.R., Genetic and biochemical dissection of a HisKA domain identifies residues required exclusively for kinase and phosphatase activities (2012) PLoS Genet., 8, p. e1003084
  • Marina, A., Mott, C., Auyzenberg, A., Hendrickson, W.A., Waldburger, C.D., Structural and mutational analysis of the PhoQ histidine kinase catalytic domain insight into the reaction mechanism (2001) J. Biol. Chem., 276, pp. 41182-41190
  • Möglich, A., Ayers, R.A., Moffat, K., Design and signaling mechanism of light-regulated histidine kinases (2009) J. Mol. Biol., 385, pp. 1433-1444
  • Ferris, H.U., Dunin-Horkawicz, S., Mondéjar, L.G., The mechanisms of HAMP-mediated signaling in transmembrane receptors. (2011) Structure, 19, pp. 378-385
  • C.L.-L., Appleman, J.A., Stewart, V., Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases (2003) J. Bacteriol., 185, pp. 4872-4882
  • Parkinson, J.S., Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases (2010) Annu. Rev. Microbiol., 64, pp. 101-122
  • Hulko, M., Berndt, F., Gruber, M., The HAMP domain structure implies helix rotation in transmembrane signaling (2006) Cell, 126, pp. 929-940
  • Gutu, A.D., Wayne, K.J., Sham, L.T., Winkler, M.E., Kinetic characterization of the WalRKSpn (VicRK) two-component system of Streptococcus pneumoniae: dependence of WalKSpn (VicK) phosphatase activity on its PAS domain (2010) J. Bacteriol., 192, pp. 2346-2358
  • Warshel, A., Bora, R.P., Perspective: defining and quantifying the role of dynamics in enzyme catalysis (2016) J. Chem. Phys., 144, p. 180901
  • Klinman, J.P., Kohen, A., Hydrogen tunneling links protein dynamics to enzyme catalysis (2013) Annu. Rev. Biochem., 82, pp. 471-496
  • Henzler-Wildman, K.A., Lei, M., Thai, V., Kerns, S.J., Karplus, M., Kern, D., A hierarchy of timescales in protein dynamics is linked to enzyme catalysis (2007) Nature, 450, pp. 913-916
  • Capra, E.J., Laub, M.T., Evolution of two-component signal transduction systems (2012) Annu. Rev. Microbiol., 66, pp. 325-347
  • Ashenberg, O., Keating, A.E., Laub, M.T., Helix bundle loops determine whether histidine kinases autophosphorylate in cis or in trans (2013) J. Mol. Biol., 425, pp. 1198-1209

Citas:

---------- APA ----------
Marsico, F., Burastero, O., Defelipe, L.A., Lopez, E.D., Arrar, M., Turjanski, A.G. & Marti, M.A. (2018) . Multiscale approach to the activation and phosphotransfer mechanism of CpxA histidine kinase reveals a tight coupling between conformational and chemical steps. Biochemical and Biophysical Research Communications, 498(2), 305-312.
http://dx.doi.org/10.1016/j.bbrc.2017.09.039
---------- CHICAGO ----------
Marsico, F., Burastero, O., Defelipe, L.A., Lopez, E.D., Arrar, M., Turjanski, A.G., et al. "Multiscale approach to the activation and phosphotransfer mechanism of CpxA histidine kinase reveals a tight coupling between conformational and chemical steps" . Biochemical and Biophysical Research Communications 498, no. 2 (2018) : 305-312.
http://dx.doi.org/10.1016/j.bbrc.2017.09.039
---------- MLA ----------
Marsico, F., Burastero, O., Defelipe, L.A., Lopez, E.D., Arrar, M., Turjanski, A.G., et al. "Multiscale approach to the activation and phosphotransfer mechanism of CpxA histidine kinase reveals a tight coupling between conformational and chemical steps" . Biochemical and Biophysical Research Communications, vol. 498, no. 2, 2018, pp. 305-312.
http://dx.doi.org/10.1016/j.bbrc.2017.09.039
---------- VANCOUVER ----------
Marsico, F., Burastero, O., Defelipe, L.A., Lopez, E.D., Arrar, M., Turjanski, A.G., et al. Multiscale approach to the activation and phosphotransfer mechanism of CpxA histidine kinase reveals a tight coupling between conformational and chemical steps. Biochem. Biophys. Res. Commun. 2018;498(2):305-312.
http://dx.doi.org/10.1016/j.bbrc.2017.09.039