2019, Número 1
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TIP Rev Esp Cienc Quim Biol 2019; 22 (1)
Mecanismos de autofosforilación y transfosforilación en sistemas de dos componentes bacterianos
Terán-Melo JL, Rodríguez-Rangel C, Georgellis D, Álvarez AF
Idioma: Español
Referencias bibliográficas: 57
Paginas: 1-11
Archivo PDF: 843.34 Kb.
RESUMEN
Los Sistemas de señalización de Dos Componentes (SDCs) permiten a las bacterias detectar estímulos ambientales y
responder a estos de manera adaptativa. Estos sistemas de transducción de señales se basan en la autofosforilación y
transferencia de grupos fosforilo entre residuos de histidina y aspartato de una proteína cinasa sensora y un regulador
de respuesta. Cuando la cinasa sensora percibe un estímulo específico se autofosforila, en una reacción que puede ser
inter o intramolecular, y transfosforila a su regulador de respuesta cognado, que actúa generalmente como regulador
transcripcional para ejercer una respuesta fisiológica. Con frecuencia, en ausencia de estímulo, la misma cinasa
sensora se encarga de desfosforilar a su regulador de respuesta cognado. Además, algunas cinasas sensoras tienen
módulos adicionales que participan en un fosforelevo que termina en la fosforilación del regulador de respuesta, y en
un fosforelevo reverso que permite su desfosforilación. Al igual que en la autofosforilación, las trasferencias de grupos
fosforilo implicadas en el fosforelevo y el fosforelevo reverso pueden ser inter o intramoleculares. En esta revisión
exponemos algunas de las más importantes características de los SDCs bacterianos, poniendo especial énfasis en los
procesos de autofosforilación y fosfotransferencia.
REFERENCIAS (EN ESTE ARTÍCULO)
Aguilar, P.S., Hernández-Arriaga, A. M., Cybulski, L. E., Erazo, A. C., & de Mendoza, D. (2001). Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. The EMBO Journal, 20(7), 1681–1691. https://doi.org/10.1093/ emboj/20.7.1681
Álvarez, A. F., Barba-Ostria, C., Silva-Jiménez, H., & Georgellis, D. (2016). Organization and mode of action of two component system signaling circuits from the various kingdoms of life. Environmental Microbiology, 18(10), 3210–3226. https://doi.org/10.1111/1462-2920.13397
Álvarez, A. F., & Georgellis, D. (2010). In vitro and in vivo analysis of the ArcB/A redox signaling pathway. Methods in Enzymology, 471(10), 205–228. https://doi. org/10.1016/S0076-6879(10)71012-0
Ashby, M. K. (2006). Distribution, structure and diversity of “bacterial” genes encoding two-component proteins in the Euryarchaeota. Archaea (Vancouver, B.C.), 2(1), 11–30. https://doi.org/10.1155/2006/562404
Ashenberg, O., Keating, A. E., & Laub, M. T. (2013). Helix bundle loops determine whether histidine kinases autophosphorylate in cis or in trans. Journal of Molecular Biology, 425(7), 1198–1209. https://doi.org/10.1016/j. jmb.2013.01.011
Bourret, R. B., Hess, J. F., Borkovich, K. A., Pakula, A. A., & Simon, M. I. (1989). Protein phosphorylation in chemotaxis and two-component regulatory systems of bacteria. The Journal of Biological Chemistry, 264(13), 7085–7088. Retrieved from http://www.ncbi.nlm.nih. gov/pubmed/2540171
Brencic, A., Xia, Q., & Winans, S. C. (2004). VirA of Agrobacterium tumefaciens is an intradimer transphosphorylase and can actively block vir gene expression in the absence of phenolic signals. Molecular Microbiology, 52(5), 1349–1362. https://doi.org/10.1111/ j.1365-2958.2004.04057.x
Burbulys, D., Trach, K. A., & Hoch, J. A. (1991). Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell, 64(3), 545–552. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1846779
Casino, P., Rubio, V., & Marina, A. (2009). Structural insight into partner specificity and phosphoryl transfer in twocomponent signal transduction. Cell, 139(2), 325–336. https://doi.org/10.1016/j.cell.2009.08.032
Catlett, N. L., Yoder, O. C., & Turgeon, B. G. (2003). Wholegenome analysis of two-component signal transduction genes in fungal pathogens. Eukaryotic Cell, 2(6), 1151– 1161. https://doi.org/10.1128/EC.2.6.1151-1161.2003
Cotter, P. A., & Jones, A. M. (2003). Phosphorelay control of virulence gene expression in Bordetella. Trends in Microbiology, 11(8), 367–373. https://doi.org/10.1016/ S0966-842X(03)00156-2
Devi, S. N., Kiehler, B., Haggett, L., & Fujita, M. (2015). Evidence that autophosphorylation of the major sporulation kinase in Bacillus subtilis is able to occur in trans. Journal of Bacteriology, 197(16), 2675–2684. https://doi.org/10.1128/JB.00257-15
Dutta, R., Qin, L., & Inouye, M. (1999). Histidine kinases: diversity of domain organization. Molecular Microbiology, 34(4), 633–640. https://doi.org/10.1046/ j.1365-2958.1999.01646.x
Eguchi, Y., & Utsumi, R. (2014). Alkali metals in addition to acidic pH activate the EvgS histidine kinase sensor in Escherichia coli. Journal of Bacteriology, 196(17), 3140–3149. https://doi.org/10.1128/JB.01742-14
Filippou, P. S., Kasemian, L. D., Panagiotidis, C. A., & Kyriakidis, D. A. (2008). Functional characterization of the histidine kinase of the E. coli two-component signal transduction system AtoS-AtoC. Biochimica et Biophysica Acta, 1780(9), 1023–1031. https://doi. org/10.1016/j.bbagen.2008.05.002
Forst, S. A., & Roberts, D. L. (1994). Signal transduction by the EnvZ-OmpR phosphotransfer system in bacteria. Research in Microbiology, 145(5–6), 363–373. https:// doi.org/10.1016/0923-2508(94)90083-3
Galperin, M. Y. (2005). A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiology, 5, 35. https://doi.org/10.1186/1471-2180-5-35
Gao, R., & Stock, A. M. (2009). Biological insights from structures of two-component proteins. Annual Review of Microbiology, 63, 133–154. https://doi.org/10.1146/ annurev.micro.091208.073214
George Cisar, E. A., Geisinger, E., Muir, T. W., & Novick, R. P. (2009). Symmetric signalling within asymmetric dimers of the Staphylococcus aureus receptor histidine kinase AgrC. Molecular Microbiology, 74(1), 44–57. https://doi.org/10.1111/j.1365-2958.2009.06849.x
Georgellis, D., Kwon, O., De Wulf, P., & Lin, E. C. (1998). Signal decay through a reverse phosphorelay in the Arc two-component signal transduction system. J. Biol. Chem., 273(49), 32864–32869. https://doi.org/10.1074/ jbc.273.49.32864
Georgellis, D., Kwon, O., & Lin, E. C. (2001). Quinones as the redox signal for the Arc two-component system of bacteria. Science (New York, N.Y.), 292(5525), 2314– 2316. https://doi.org/10.1126/science.1059361
Georgellis, D., Lynch, A. S., & Lin, E. C. (1997). In vitro phosphorylation study of the Arc two-component signal transduction system of Escherichia coli. J. Bacteriol., 179(17), 5429–5435. https://doi.org/10.1128/ jb.179.17.5429-5435.1997
Hutchings, M. I., Hong, H.-J., & Buttner, M. J. (2006). The vancomycin resistance VanRS two-component signal transduction system of Streptomyces coelicolor. Molecular Microbiology, 59(3), 923–935. https://doi. org/10.1111/j.1365-2958.2005.04953.x
Huynh, T. N., Noriega, C. E., & Stewart, V. (2010). Conserved mechanism for sensor phosphatase control of twocomponent signaling revealed in the nitrate sensor NarX. Proc. Natl. Acad. Sci. U S A, 107(49), 21140–21145. https://doi.org/10.1073/pnas.1013081107
Huynh, T. N., & Stewart, V. (2011). Negative control in twocomponent signal transduction by transmitter phosphatase activity. Molecular Microbiology, 82(2), 275–286. https:// doi.org/10.1111/j.1365-2958.2011.07829.x
Iuchi, S., & Lin, E. C. C. (1993). Adaptation of Escherichia coli to redox environments by gene expression. Molecular Microbiology, 9(1), 9–15. https://doi. org/10.1111/j.1365-2958.1993.tb01664.x
Jiang, M., Shao, W., Perego, M., & Hoch, J. A. (2000). Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Molecular Microbiology, 38(3), 535–542. https://doi.org/10.1046/ j.1365-2958.2000.02148.x
Jourlin, C., Ansaldi, M., & Mejean, V. (1997). Transphosphorylation of the TorR response regulator requires the three phosphorylation sites of the TorS unorthodox sensor in Escherichia coli. Journal of Molecular Biology, 267(4), 770–777. https://doi. org/10.1006/jmbi.1997.0919
Jovanovic, G., Sheng, X., Ale, A., Feliu, E., Harrington, H. A., Kirk, P., Wiuf, C., Buck, M., & Stumpf, M. P. H. (2015). Phosphorelay of non-orthodox two component systems functions through a bi-molecular mechanism in vivo: the case of ArcB. Mol. BioSyst. Mol. BioSyst, 11(11), 1348– 1359. https://doi.org/10.1039/c4mb00720d
Kenney, L. J. (2010). How important is the phosphatase activity of sensor kinases? Current Opinion in Microbiology, 13(2), 168–176. https://doi.org/10.1016/j. mib.2010.01.013
Kinoshita-Kikuta, E., Kinoshita, E., Eguchi, Y., & Koike, T. (2016). Validation of cis and trans modes in multistep phosphotransfer signaling of bacterial tripartite sensor kinases by using Phos-Tag SDS-PAGE. PLOS ONE, 11(2), e0148294. https://doi.org/10.1371/journal.pone.0148294
Koretke, K. K., Lupas, A. N., Warren, P. V, Rosenberg, M., & Brown, J. R. (2000). Evolution of two-component signal transduction. Molecular Biology and Evolution, 17(12), 1956–1970. https://doi.org/doi.org/10.1093/ oxfordjournals.molbev.a026297
Kwon, O., Georgellis, D., & Lin, E. C. (2000). Phosphorelay as the sole physiological route of signal transmission by the Arc two-component system of Escherichia coli. J. Bacteriol., 182(13), 3858–3862. https://doi.org/10.1128/ JB.182.13.3858-3862.2000
Levit, M., Liu, Y., Surette, M., & Stock, J. (1996). Active Site Interference and Asymmetric Activation in the Chemotaxis Protein Histidine Kinase CheA. Journal of Biological Chemistry, 271(50), 32057–32063. https://doi. org/10.1074/jbc.271.50.32057
Lynch, A. S., & Lin, E. C. (1996). Regulation of gene expression in Escherichia coli. In F. C. Neidhardt, R. Curtis, A. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, & H. E. Umbarger (Eds.), Escherichia coli and Salmonella: Cellular and Molecular Biology (pp. 1526–1538). Washington, DC: Am. Soc. Microbiol.
Malpica, R., Sandoval, G. R., Rodriguez, C., Franco, B., & Georgellis, D. (2006). Signaling by the Arc twocomponent system provides a link between the redox state of the quinone pool and gene expression. Antioxid. Redox Signal, 8(5–6), 781–795. https://doi.org/10.1089/ ars.2006.8.781
Ninfa, E. G., Atkinson, M. R., Kamberov, E. S., & Ninfa, A. J. (1993). Mechanism of autophosphorylation of Escherichia coli nitrogen regulator II (NRII or NtrB): trans-phosphorylation between subunits. Journal of Bacteriology, 175(21), 7024–7032. https://doi. org/10.1128/jb.175.21.7024-7032.1993
Nohno, T., Noji, S., Taniguchi, S., & Saito, T. (1989). The narX and narL genes encoding the nitrate-sensing regulators of Escherichia coli are homologous to a family of prokaryotic two-component regulatory genes. Nucleic Acids Research, 17(8), 2947–2957. Retrieved from http:// www.ncbi.nlm.nih.gov/pubmed/2657652
Peña-Sandoval, G. R., & Georgellis, D. (2010). The ArcB sensor kinase of Escherichia coli autophosphorylates by an intramolecular reaction. Journal of Bacteriology, 192(6), 1735–1739. https://doi.org/10.1128/JB.01401- 09
Peña-Sandoval, G. R., Kwon, O., & Georgellis, D. (2005). Requirement of the receiver and phosphotransfer domains of ArcB for efficient dephosphorylation of phosphorylated ArcA in vivo. Journal of Bacteriology, 187(9), 3267– 3272. https://doi.org/10.1128/JB.187.9.3267-3272.2005
Santos, J. L., & Shiozaki, K. (2001). Fungal histidine kinases. Science’s STKE, 2001(98), re1. https://doi.org/10.1126/ stke.2001.98.re1
Schaller, G. E., Shiu, S.-H., & Armitage, J. P. (2011). Twocomponent systems and their co-option for eukaryotic signal transduction. Current Biology : CB, 21(9), R320- 330. https://doi.org/10.1016/j.cub.2011.02.045
Stock, A. M., Robinson, V. L., & Goudreau, P. N. (2000). Two-component signal transduction. Annual Review of Biochemistry, 69, 183–215. https://doi.org/10.1146/ annurev.biochem.69.1.183
Swanson, R. V, Bourret, R. B., & Simon, M. I. (1993). Intermolecular complementation of the kinase activity of CheA. Molecular Microbiology, 8(3), 435–441. https:// doi.org/10.1111/j.1365-2958.1993.tb01588.x
Takeda, S., Fujisawa, Y., Matsubara, M., Aiba, H., & Mizuno, T. (2001). A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC --> YojN --> RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Molecular Microbiology, 40(2), 440–450. https://doi.org/10.1046/ j.1365-2958.2001.02393.x
Tanaka, T., Saha, S. K., Tomomori, C., Ishima, R., Liu, D., Tong, K. I., Park, H., Dutta, R., Qing, L., Swindells, M. B., Yamazaki, T., Ono, A. M., Kainosho, M., Inouye, M., & Ikura, M. (1998). NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ. Nature, 396(6706), 88–92. https://doi.org/10.1038/23968
Terán-Melo, J. L., Peña-Sandoval, G. R., Silva-Jiménez, H., Rodríguez, C., Álvarez, A. F., & Georgellis, D. (2018). Routes of phosphoryl group transfer during signal transmission and signal decay in the dimeric sensor histidine kinase ArcB. The Journal of Biological Chemistry, 293(34), 13214–13223. https://doi. org/10.1074/jbc.RA118.003910
Thomason, P., & Kay, R. (2000). Eukaryotic signal transduction via histidine-aspartate phosphorelay. Journal of Cell Science, 113, 3141–3150.
Trajtenberg, F., Graña, M., Ruétalo, N., Botti, H., & Buschiazzo, A. (2010). Structural and enzymatic insights into the ATP binding and autophosphorylation mechanism of a sensor histidine kinase. The Journal of Biological Chemistry, 285(32), 24892–24903. https://doi. org/10.1074/jbc.M110.147843
Uhl, M. A., & Miller, J. F. (1996a). Central role of the BvgS receiver as a phosphorylated intermediate in a complex two-component phosphorelay. The Journal of Biological Chemistry, 271(52), 33176–33180. https://doi. org/10.1074/jbc.271.52.33176
Uhl, M. A., & Miller, J. F. (1996b). Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. The EMBO Journal, 15(5), 1028–1036. https://doi.org/10.1002/j.1460-2075.1996. tb00440.x
Ulrich, L. E., & Zhulin, I. B. (2010). The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Research, 38(Database issue), D401-407. https://doi.org/10.1093/nar/gkp940
West, A. H., & Stock, A. M. (2001). Histidine kinases and response regulator proteins in two-component signaling systems. Trends in Biochemical Sciences, 26(6), 369– 376. https://doi.org/10.1016/S0968-0004(01)01852-7
Williams, R. H. N., & Whitworth, D. E. (2010). The genetic organisation of prokaryotic two-component system signalling pathways. BMC Genomics, 11, 720. https://doi. org/10.1186/1471-2164-11-720
Wolanin, P. M., Thomason, P. A., & Stock, J. B. (2002). Histidine protein kinases: key signal transducers outside the animal kingdom. Genome Biology, 3(10), 1–8. https:// doi.org/10.1186/gb-2002-3-10-reviews3013
Wuichet, K., Cantwell, B. J., & Zhulin, I. B. (2010). Evolution and phyletic distribution of two-component signal transduction systems. Current Opinion in Microbiology, 13(2), 219–225. https://doi.org/10.1016/j. mib.2009.12.011
Yang, Y., & Inouye, M. (1991). Intermolecular complementation between two defective mutant signaltransducing receptors of Escherichia coli. Proc. Natl. Acad. Sci. U S A, 88(24), 11057–11061. https://doi. org/10.1073/pnas.88.24.11057