Abstract:
In response to light, as part of a two-component system, the Brucella blue light-activated histidine kinase (LOV-HK) increases its autophosphorylation, modulating the virulence of this microorganism. The Brucella histidine kinase (HK) domain belongs to the HWE family, for which there is no structural information. The HWE family is exclusively present in proteobacteria and usually coupled to a wide diversity of light sensor domains. This work reports the crystal structure of the Brucella HK domain, which presents two different dimeric assemblies in the asymmetric unit: one similar to the already described canonical parallel homodimers (C) and the other, an antiparallel non-canonical (NC) dimer, each with distinct relative subdomain orientations and dimerization interfaces. Contrary to these crystallographic structures and unlike other HKs, in solution, the Brucella HK domain is monomeric and still active, showing an astonishing instability of the dimeric interface. Despite this instability, using cross-linking experiments, we show that the C dimer is the functionally relevant species. Mutational analysis demonstrates that the autophosphorylation activity occurs in cis. The different relative subdomain orientations observed for the NC and C states highlight the large conformational flexibility of the HK domain. Through the analysis of these alternative conformations by means of molecular dynamics simulations, we also propose a catalytic mechanism for Brucella LOV-HK. © 2016 Elsevier Ltd. All rights reserved.
Registro:
Documento: |
Artículo
|
Título: | Structural Insights into the HWE Histidine Kinase Family: The Brucella Blue Light-Activated Histidine Kinase Domain |
Autor: | Rinaldi, J.; Arrar, M.; Sycz, G.; Cerutti, M.L.; Berguer, P.M.; Paris, G.; Estrín, D.A.; Martí, M.A.; Klinke, S.; Goldbaum, F.A. |
Filiación: | Fundación Instituto Leloir, IIBBA-CONICET, Avenida Patricias Argentinas 435, Buenos Aires, C1405BWE, Argentina Departamento de Química Inorgánica, Analítica y Química Física e INQUIMAE-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, Buenos Aires, C1428EHA, Argentina Plataforma Argentina de Biología Estructural y Metabolómica PLABEM, Avenida Patricias Argentinas 435, Buenos Aires, C1405BWE, Argentina Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria, Pabellón 2, Buenos Aires, C1428EHA, Argentina Centro de Investigaciones en Bionanociencias, CIBION-CONICET, Godoy Cruz 2390, Buenos Aires, C1425FQD, Argentina
|
Palabras clave: | autophosphorylation mechanism; molecular dynamics simulations; signal transduction; two-component system; X-ray crystallography; dimer; homodimer; protein histidine kinase; protein kinase; protein-histidine kinase; Article; autophosphorylation; blue light; Brucella; conformation; cross linking; crystal structure; crystallography; dimerization; enzyme activity; enzyme structure; molecular dynamics; mutational analysis; nonhuman; priority journal; protein domain; protein family; chemistry; dna mutational analysis; enzymology; genetics; metabolism; phosphorylation; protein conformation; protein multimerization; protein processing; X ray crystallography; Brucella; Crystallography, X-Ray; DNA Mutational Analysis; Molecular Dynamics Simulation; Phosphorylation; Protein Conformation; Protein Kinases; Protein Multimerization; Protein Processing, Post-Translational |
Año: | 2016
|
Volumen: | 428
|
Número: | 6
|
Página de inicio: | 1165
|
Página de fin: | 1179
|
DOI: |
http://dx.doi.org/10.1016/j.jmb.2016.01.026 |
Título revista: | Journal of Molecular Biology
|
Título revista abreviado: | J. Mol. Biol.
|
ISSN: | 00222836
|
CODEN: | JMOBA
|
CAS: | protein histidine kinase, 99283-67-7; protein kinase, 9026-43-1; Protein Kinases; protein-histidine kinase
|
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00222836_v428_n6_p1165_Rinaldi |
Referencias:
- Gao, R., Stock, A.M., Biological insights from structures of two-component proteins (2009) Annu. Rev. Microbiol., 63, pp. 133-154
- Igo, M.M., Ninfa, A.J., Stock, J.B., Silhavy, T.J., Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor (1989) Genes Dev., 3, pp. 1725-1734
- Bhate, M.P., Molnar, K.S., Goulian, M., DeGrado, W.F., Signal transduction in histidine kinases: Insights from new structures (2015) Structure, 23, pp. 981-994
- Rivera-Cancel, G., Ko, W.H., Tomchick, D.R., Correa, F., Gardner, K.H., Full-length structure of a monomeric histidine kinase reveals basis for sensory regulation (2014) Proc. Natl. Acad. Sci. U. S. A., 111, pp. 17839-17844
- Casino, P., Rubio, V., Marina, A., Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction (2009) Cell, 139, pp. 325-336
- Marina, A., Waldburger, C.D., Hendrickson, W.A., Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein (2005) EMBO J., 24, pp. 4247-4259
- Ferris, H.U., Coles, M., Lupas, A.N., Hartmann, M.D., Crystallographic snapshot of the Escherichia coli EnvZ histidine kinase in an active conformation (2014) J. Struct. Biol., 186, pp. 376-379
- Tanaka, T., Saha, S.K., Tomomori, C., Ishima, R., Liu, D., Tong, K.I., NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ (1998) Nature, 396, pp. 88-92
- Albanesi, D., Martin, M., Trajtenberg, F., Mansilla, M.C., Haouz, A., Alzari, P.M., Structural plasticity and catalysis regulation of a thermosensor histidine kinase (2009) Proc. Natl. Acad. Sci. U. S. A., 106, pp. 16185-16190
- Trajtenberg, F., Grana, M., Ruetalo, N., Botti, H., Buschiazzo, A., Structural and enzymatic insights into the ATP binding and autophosphorylation mechanism of a sensor histidine kinase (2010) J. Biol. Chem., 285, pp. 24892-24903
- 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
- Kim, D., Forst, S., Genomic analysis of the histidine kinase family in bacteria and archaea (2001) Microbiology, 147, pp. 1197-1212
- Ninfa, E.G., Atkinson, M.R., Kamberov, E.S., Ninfa, A.J., Mechanism of autophosphorylation of Escherichia coli nitrogen regulator II (NRII or NtrB): Trans-Phosphorylation between subunits (1993) J. Bacteriol., 175, pp. 7024-7032
- Yang, Y., Inouye, M., Intermolecular complementation between two defective mutant signal-transducing receptors of Escherichia coli (1991) Proc. Natl. Acad. Sci. U. S. A., 88, pp. 11057-11061
- Cai, S.J., Inouye, M., Spontaneous subunit exchange and biochemical evidence for trans-autophosphorylation in a dimer of Escherichia coli histidine kinase (EnvZ) (2003) J. Mol. Biol., 329, pp. 495-503
- 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
- Casino, P., Miguel-Romero, L., Marina, A., Visualizing autophosphorylation in histidine kinases (2014) Nat. Commun., 5, p. 3258
- Gourley, C.R., Petersen, E., Harms, J., Splitter, G., Decreased in vivo virulence and altered gene expression by a Brucella melitensis light-sensing histidine kinase mutant (2015) Pathog Dis., 73, pp. 1-8
- Swartz, T.E., Tseng, T.S., Frederickson, M.A., Paris, G., Comerci, D.J., Rajashekara, G., Blue-light-activated histidine kinases: Two-component sensors in bacteria (2007) Science, 317, pp. 1090-1093
- Sycz, G., Carrica, M.C., Tseng, T.S., Bogomolni, R.A., Briggs, W.R., Goldbaum, F.A., LOV Histidine kinase modulates the general stress response system and affects the virB operon expression in Brucella abortus (2015) PLoS ONE, 10
- Karniol, B., Vierstra, R.D., The HWE histidine kinases, a new family of bacterial two-component sensor kinases with potentially diverse roles in environmental signaling (2004) J. Bacteriol., 186, pp. 445-453
- Klinke, S., Foos, N., Rinaldi, J.J., Paris, G., Goldbaum, F.A., Legrand, P., S-SAD phasing of monoclinic histidine kinase from Brucella abortus combining data from multiple crystals and orientations: An example of data-collection strategy and a posteriori analysis of different data combinations (2015) Acta Crystallogr. Sect. D: Biol. Crystallogr., 71, pp. 1433-1443
- Bilwes, A.M., Quezada, C.M., Croal, L.R., Crane, B.R., Simon, M.I., Nucleotide binding by the histidine kinase CheA (2001) Nat. Struct. Biol., 8, pp. 353-360
- Hsing, W., Russo, F.D., Bernd, K.K., Silhavy, T.J., Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ (1998) J. Bacteriol., 180, pp. 4538-4546
- Wang, C., Sang, J., Wang, J., Su, M., Downey, J.S., Wu, Q., Mechanistic insights revealed by the crystal structure of a histidine kinase with signal transducer and sensor domains (2013) PLoS Biol., 11
- Diensthuber, R.P., Bommer, M., Gleichmann, T., Moglich, A., Full-length structure of a sensor histidine kinase pinpoints coaxial coiled coils as signal transducers and modulators (2013) Structure, 21, pp. 1127-1136
- 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
- Chen, V.B., Arendall, W.B., 3rd, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., MolProbity: All-atom structure validation for macromolecular crystallography (2010) Acta Crystallogr. Sect. D: Biol. Crystallogr., 66, pp. 12-21
- Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of coot (2010) Acta Crystallogr. Sect. D: Biol. Crystallogr., 66, pp. 486-501
- Humphrey, W., Dalke, A., Schulten, K., VMD: Visual Molecular Dynamics (1996) J. Mol. Graph., 14, pp. 33-38 and 27-28
- Krissinel, E., Henrick, K., Inference of macromolecular assemblies from crystalline state (2007) J. Mol. Biol., 372, pp. 774-797
- Webb, B., Sali, A., Protein structure modeling with MODELLER (2014) Methods Mol. Biol., 1137, pp. 1-15
- Lindorff-Larsen, K., Piana, S., Palmo, K., Maragakis, P., Klepeis, J.L., Dror, R.O., Improved side-chain torsion potentials for the AMBER ff99SB protein force field (2010) Proteins, 78, pp. 1950-1958
- Joung, I.S., Cheatham, T.E., 3rd, Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations (2008) J. Phys. Chem. B, 112, pp. 9020-9041
- 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
- Ryckaert, J.P., Ciccotti, G., Berendsen, H.J.C., Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes (1977) J. Comput. Phys., 23, pp. 327-341
- Case, D.A., Berryman, J.T., Betz, R.M., Cerutti, D.S., Cheatham, T.E., Darden, T.A., (2015) AMBER 2015
- Engh, R.A., Huber, R., Accurate bond and angle parameters for X-ray protein structure refinement (1991) Acta Crystallogr. A, 47, pp. 392-400
Citas:
---------- APA ----------
Rinaldi, J., Arrar, M., Sycz, G., Cerutti, M.L., Berguer, P.M., Paris, G., Estrín, D.A.,..., Goldbaum, F.A.
(2016)
. Structural Insights into the HWE Histidine Kinase Family: The Brucella Blue Light-Activated Histidine Kinase Domain. Journal of Molecular Biology, 428(6), 1165-1179.
http://dx.doi.org/10.1016/j.jmb.2016.01.026---------- CHICAGO ----------
Rinaldi, J., Arrar, M., Sycz, G., Cerutti, M.L., Berguer, P.M., Paris, G., et al.
"Structural Insights into the HWE Histidine Kinase Family: The Brucella Blue Light-Activated Histidine Kinase Domain"
. Journal of Molecular Biology 428, no. 6
(2016) : 1165-1179.
http://dx.doi.org/10.1016/j.jmb.2016.01.026---------- MLA ----------
Rinaldi, J., Arrar, M., Sycz, G., Cerutti, M.L., Berguer, P.M., Paris, G., et al.
"Structural Insights into the HWE Histidine Kinase Family: The Brucella Blue Light-Activated Histidine Kinase Domain"
. Journal of Molecular Biology, vol. 428, no. 6, 2016, pp. 1165-1179.
http://dx.doi.org/10.1016/j.jmb.2016.01.026---------- VANCOUVER ----------
Rinaldi, J., Arrar, M., Sycz, G., Cerutti, M.L., Berguer, P.M., Paris, G., et al. Structural Insights into the HWE Histidine Kinase Family: The Brucella Blue Light-Activated Histidine Kinase Domain. J. Mol. Biol. 2016;428(6):1165-1179.
http://dx.doi.org/10.1016/j.jmb.2016.01.026