Temporal and evolutionary dynamics of two-component signaling pathways

Current Opinion in Microbiology

Volumn 24, Issue , 2015, Pages 7-14

  Salazar, Michael E ^a   Laub, Michael T ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; TWO COMPONENT SIGNALING PATHWAY; BACTERIUM; ENZYMOLOGY; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

BACTERIAL PROTEIN; PROTEIN HISTIDINE KINASE; PROTEIN KINASE;

BACTERIA; BACTERIAL PROTEINS; BIOLOGICAL EVOLUTION; GENE EXPRESSION REGULATION, BACTERIAL; HISTIDINE KINASE; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 84920736174     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2014.12.003     Document Type: Review

References (51)

1. Stock A.M., Robinson V.L., Goudreau P.N. Two-component signal transduction. Annu Rev Biochem 2000, 69:183-215.
2. Capra E.J., Laub M.T. Evolution of two-component signal transduction systems. Annu Rev Microbiol 2012, 66:325-347.
3. Galperin M.Y. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol 2005, 5:35.
4. Krell T., Lacal J., Busch A., Silva-Jiménez H., Guazzaroni M.-E., Ramos J.L. Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu Rev Microbiol 2010, 64:539-559.
5. Podgornaia A.I., Laub M.T. Determinants of specificity in two-component signal transduction. Curr Opin Microbiol 2013, 16:156-162.
6. Goulian M. Two-component signaling circuit structure and properties. Curr Opin Microbiol 2010, 13:184-189.
7. 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. J Bacteriol 1998, 180:4538-4546.
8. Igo M.M., Ninfa A.J., Stock J.B., Silhavy T.J. Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev 1989, 3:1725-1734.
9. Russo F.D., Silhavy T.J. The essential tension: opposed reactions in bacterial two-component regulatory systems. Trends Microbiol 1993, 1:306-310.
10. Huynh T.N., Noriega C.E., Stewart V. Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX. Proc Natl Acad Sci USA 2010, 107:21140-21145.
11. Gao R., Stock A.M. Probing kinase and phosphatase activities of two-component systems in vivo with concentration-dependent phosphorylation profiling. Proc Natl Acad Sci USA 2013, 110:672-677.
12. Siryaporn A., Goulian M. Cross-talk suppression between the CpxA-CpxR and EnvZ-OmpR two-component systems in E. coli. Mol Microbiol 2008, 70:494-506.
13. Groban E.S., Clarke E.J., Salis H.M., Miller S.M., Voigt C.A. Kinetic buffering of cross talk between bacterial two-component sensors. J Mol Biol 2009, 390:380-393.
14. Boll J.M., Hendrixson D.R. A specificity determinant for phosphorylation in a response regulator prevents in vivo cross-talk and modification by acetyl phosphate. Proc Natl Acad Sci USA 2011, 108:20160-20165.
15. Ram S., Goulian M. The architecture of a prototypical bacterial signaling circuit enables a single point mutation to confer novel network properties. PLoS Genet 2013, 9:e1003706.
16. Shin D., Lee E.-J., Huang H., Groisman E.A. A positive feedback loop promotes transcription surge that jump-starts salmonella virulence circuit. Science 2006, 314:1607-1609.
17. Hutchings M.I., Hong H.-J., Buttner M.J. The vancomycin resistance VanRS two-component signal transduction system of Streptomyces coelicolor. Mol Microbiol 2006, 59:923-935.
18. Yamamoto K., Ishihama A. Transcriptional response of Escherichia coli to external zinc. J Bacteriol 2005, 187:6333-6340.
19. Ray J.C.J., Igoshin O.A. Adaptable functionality of transcriptional feedback in bacterial two-component systems. PLoS Comput Biol 2010, 6:e1000676.
20. Yeo W.-S., Zwir I., Huang H.V., Shin D., Kato A., Groisman E.A. Intrinsic negative feedback governs activation surge in two-component regulatory systems. Mol Cell 2012, 45:409-421.
21. Lippa A.M., Goulian M. Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet 2009, 5:e1000788.
22. Eguchi Y., Ishii E., Yamane M., Utsumi R. The connector SafA interacts with the multi-sensing domain of PhoQ in Escherichia coli. Mol Microbiol 2012, 85:299-313.
23. Miyashiro T., Goulian M. High stimulus unmasks positive feedback in an autoregulated bacterial signaling circuit. Proc Natl Acad Sci USA 2008, 105:17457-17462.
24. Gao R., Stock A.M. Evolutionary tuning of protein expression levels of a positively autoregulated two-component system. PLoS Genet 2013, 9:e1003927.
25. Hilbert D.W., Piggot P.J. Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol Mol Biol Rev 2004, 68:234-262.
26. Levine J.H., Fontes M.E., Dworkin J., Elowitz M.B. Pulsed feedback defers cellular differentiation. PLoS Biol 2012, 10:e1001252.
27. Veening J.-W., Murray H., Errington J. A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis. Genes Dev 2009, 23:1959-1970.
28. Levine J.H., Elowitz M.B. Polyphasic feedback enables tunable cellular timers. Curr Biol 2014, 24:R994-R995.
29. Fujita M., Losick R. Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev 2005, 19:2236-2244.
30. Fujita M., González-Pastor J.E., Losick R. High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 2005, 187:1357-1368.
31. de Jong I.G., Veening J.-W., Kuipers O.P. Heterochronic phosphorelay gene expression as a source of heterogeneity in Bacillus subtilis spore formation. J Bacteriol 2010, 192:2053-2067.
32. Chastanet A., Vitkup D., Yuan G.-C., Norman T.M., Liu J.S., Losick R.M. Broadly heterogeneous activation of the master regulator for sporulation in Bacillus subtilis. Proc Natl Acad Sci USA 2010, 107:8486-8491.
33. Kinoshita E., Kinoshita-Kikuta E., Koike T. Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat Protoc 2009, 4:1513-1521.
34. Cai S.J., Inouye M. EnvZ-OmpR interaction and osmoregulation in Escherichia coli. J Biol Chem 2002, 277:24155-24161.
35. Li G.-W., Burkhardt D., Gross C., Weissman J.S. Quantifying absolute protein synthesis rates reveals principles underlying allocation of cellular resources. Cell 2014, 157:624-635.
36. Alm E., Huang K., Arkin A. The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLoS Comput Biol 2006, 2:e143.
37. Grimshaw C.E., Huang S., Hanstein C.G., Strauch M.A., Burbulys D., Wang L., Hoch J.A., Whiteley J.M. Synergistic kinetic interactions between components of the phosphorelay controlling sporulation in Bacillus subtilis. Biochemistry (Mosc) 1998, 37:1365-1375.
38. Skerker J.M., Prasol M.S., Perchuk B.S., Biondi E.G., Laub M.T. Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol 2005, 3:e334.
39. Skerker J.M., Perchuk B.S., Siryaporn A., Lubin E.A., Ashenberg O., Goulian M., Laub M.T. Rewiring the specificity of two-component signal transduction systems. Cell 2008, 133:1043-1054.
40. Weigt M., White R.A., Szurmant H., Hoch J.A., Hwa T. Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci USA 2009, 106:67-72.
41. Capra E.J., Perchuk B.S., Lubin E.A., Ashenberg O., Skerker J.M., Laub M.T. Systematic dissection and trajectory-scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways. PLoS Genet 2010, 6:e1001220.
42. Capra E.J., Perchuk B.S., Skerker J.M., Laub M.T. Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families. Cell 2012, 150:222-232.
43. Rowland M.A., Deeds E.J. Crosstalk and the evolution of specificity in two-component signaling. Proc Natl Acad Sci USA 2014, 111:5550-5555.
44. Wuichet K., Zhulin I.B. Origins and diversification of a complex signal transduction system in prokaryotes. Sci Signal 2010, 3:ra50.
45. Capra E.J., Perchuk B.S., Ashenberg O., Seid C.A., Snow H.R., Skerker J.M., Laub M.T. Spatial tethering of kinases to their substrates relaxes evolutionary constraints on specificity. Mol Microbiol 2012, 86:1393-1403.
46. Townsend G.E., Raghavan V., Zwir I., Groisman E.A. Intramolecular arrangement of sensor and regulator overcomes relaxed specificity in hybrid two-component systems. Proc Natl Acad Sci USA 2013, 110:E161-E169.
47. Burbulys D., Trach K.A., Hoch J.A. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 1991, 64:545-552.
48. Galperin M.Y., Mekhedov S.L., Puigbo P., Smirnov S., Wolf Y.I., Rigden D.J. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ Microbiol 2012, 14:2870-2890.
49. Wörner K., Szurmant H., Chiang C., Hoch J.A. Phosphorylation and functional analysis of the sporulation initiation factor Spo0A from Clostridium botulinum. Mol Microbiol 2006, 59:1000-1012.
50. Steiner E., Dago A.E., Young D.I., Heap J.T., Minton N.P., Hoch J.A., Young M. Multiple orphan histidine kinases interact directly with Spo0A to control the initiation of endospore formation in Clostridium acetobutylicum. Mol Microbiol 2011, 80:641-654.
51. Zapf J., Sen U., Madhusudan, Hoch J.A., Varughese K.I. A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 2000, 8:851-862.