Summary:
Histidine-aspartate signaling systems are used by bacteria, archaea and eukarya to integrate stimuli over time and space generating coordinated, fine-tuned cellular responses. A hallmark feature is the high modularity of the signaling protein modules which can form simple ’two-component‘ systems, and also sophisticated ’multi-component’ systems. The deltaproteobacterium Myxococcus xanthus contains a large repertoire of signaling proteins, many of which regulate its complex multicellular developmental program. In this respect, one important systems is the Esp signaling system, consisting of the hybrid histidine protein kinase, EspA, two serine/threonine protein kinases (PktA5 and PktB8), and a putative transport protein (EspB).
In the presented study, I assign an orphan hybrid histidine protein kinase, EspC, to the Esp signaling system which negatively regulates progression through the M. xanthus developmental program. The genetic analysis revealed that EspC is an essential component of this system, because ΔespA, ΔespC, and ΔespAΔespC double mutants shared an identical early developmental phenotype. Surprisingly, disruption of EspC’s auto-phosphorylation in vivo did not produce a mutant developmental phenotype, whereas substitution of its phospho-accepting residue within the receiver domain resulted in the null phenotype. Furthermore, it is shown that although the EspC histidine kinase could efficiently autophosphorylate in vitro, it did not act as a phospho-donor to its own receiver domain. Instead, both, in vitro and in vivo analyses elucidated that the phospho-donor instead is EspA’s histidine kinase. Therefore, EspA and EspC participate in a novel hybrid histidine protein kinase signaling mechanism involving both inter- and intraprotein phosphotransfer. This inter- and intraprotein phosphotransfer results in the combined phosphorylation of EspA’s and EspC’s receiver domains which represents the output of the Esp signaling system. Further genetic analyses suggested that this Esp system is regulated on the level of its phosphatase activity, likely involving the sensing domains of EspC for regulation. Finally, I uncovered that the Esp system stimulates the proteolytic turnover of MrpC, a crucial transcription factor of the developmental program, via as yet unidentified serine protease.
Altogether, these data unravel a novel signaling mechanism of His-Asp signaling systems, and thus expand the knowledge about the complexity and plasticity of these crucial signal transduction systems.
Bibliographie / References
- Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
- Bertani, G. (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62, 293-300
- McEvoy, M.M., et al. (1999) Identification of the binding interfaces on CheY for two of its targets, the phosphatase CheZ and the flagellar switch protein fliM. J Mol Biol 289, 1423-1433
- Harcum, S.W. and Bentley, W.E. (1993) Detection, Quantification, and Characterization of Proteases in Recombinant Escherichia coli. Biotechnology Techniques 7, 441-447
- Rawlings, N.D. (2010) Peptidase inhibitors in the MEROPS database. Biochimie 92, 1463-1483
- Nariya, H. and Inouye, M. (2008) MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132, 55 REFERENCES
- Rolbetzki, A., et al. (2008) Regulated secretion of a protease activates intercellular signaling during fruiting body formation in M. xanthus. Dev Cell 15, 627-634
- Goulian, M. (2010) Two-component signaling circuit structure and properties. Curr Opin Microbiol 13, 184-189
- Yamada, S., et al. (2009) Structure of PAS-linked histidine kinase and the response regulator complex. Structure 17, 1333-1344
- Laub, M.T., et al. (2007) Phosphotransfer profiling: systematic mapping of two- component signal transduction pathways and phosphorelays. Methods Enzymol 423, 531-548
- Lee, B., et al. (2010) Two-component systems and regulation of developmental progression in Myxococcus xanthus. Methods Enzymol 471, 253-278
- Kato, M., et al. (1997) Insights into multistep phosphorelay from the crystal structure of the C-terminal HPt domain of ArcB. Cell 88, 717-723
- Varughese, K.I., et al. (1998) Formation of a novel four-helix bundle and molecular recognition sites by dimerization of a response regulator phosphotransferase. Mol Cell 2, 485-493
- Jiang, P., et al. (2000) Functional dissection of the dimerization and enzymatic activities of Escherichia coli nitrogen regulator II and their regulation by the PII protein. Biochemistry 39, 13433-13449
- Wanner, B.L. (1996) Signal transduction in the control of phosphate-regulated genes of Escherichia coli. Kidney Int 49, 964-967
- Zusman, D.R., et al. (2007) Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5, 862-872
- Ellehauge, E., et al. (1998) The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in Myxococcus xanthus development. Mol Microbiol 30, 807-817
- Cho, K. and Zusman, D.R. (1999) Sporulation timing in Myxococcus xanthus is controlled by the espAB locus. Mol Microbiol 34, 714-725
- Garza, A.G., et al. (2000) The asgE locus is required for cell-cell signalling during Myxococcus xanthus development. Mol Microbiol 35, 812-824
- Jiang, M., et al. (2000) Multiple histidine kinases regulate entry into stationary phase and sporulation in Bacillus subtilis. Mol Microbiol 38, 535-542
- Kruse, T., et al. (2001) C-signal: a cell surface-associated morphogen that induces and co-ordinates multicellular fruiting body morphogenesis and sporulation in Myxococcus xanthus. Mol Microbiol 40, 156-168
- Klauck, E., et al. (2001) Role of the response regulator RssB in sigma recognition and initiation of sigma proteolysis in Escherichia coli. Mol Microbiol 40, 1381- 1390
- Alves, R. and Savageau, M.A. (2003) Comparative analysis of prototype two- component systems with either bifunctional or monofunctional sensors: differences in molecular structure and physiological function. Molecular Microbiology 48, 25- 51
- Ferrieres, L. and Clarke, D.J. (2003) The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. Mol Microbiol 50, 1665-1682
- Viswanathan, P., et al. (2007) Combinatorial regulation of genes essential for Myxococcus xanthus development involves a response regulator and a LysR-type regulator. Proc Natl Acad Sci U S A 104, 7969-7974
- Strickland, D., et al. (2008) Light-activated DNA binding in a designed allosteric protein. Proc Natl Acad Sci U S A 105, 10709-10714
- Zhu, Y., et al. (2000) Phosphatase activity of histidine kinase EnvZ without kinase catalytic domain. Proc Natl Acad Sci U S A 97, 7808-7813
- Jagadeesan, S., et al. (2009) A Novel "Four-component" Two-component Signal Transduction Mechanism Regulates Developmental Progression in Myxococcus xanthus. Journal of Biological Chemistry 284, 21435-21445
- Fleischer, R., et al. (2007) Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J Biol Chem 282, 8583-8593
- Larkin, M.A., et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948
- Studemann, A., et al. (2003) Sequential recognition of two distinct sites in sigma(S) by the proteolytic targeting factor RssB and ClpX. EMBO J 22, 4111-4120
- Huntley, S., et al. (2011) Comparative genomic analysis of fruiting body formation in Myxococcales. Mol Biol Evol 28, 1083-1097 REFERENCES 111
- Altschul, S.F., et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402
- Zhang, W. and Shi, L. (2005) Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases. Microbiology 151, 2159-2173
- Harris, B.Z., et al. (1998) The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes Dev 12, 1022-1035
- Kearns, D.B. and Losick, R. (2005) Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev 19, 3083-3094
- Lobedanz, S. and Sogaard-Andersen, L. (2003) Identification of the C-signal, a contact-dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes Dev 17, 2151-2161
- Zhou, Y., et al. (2001) The RssB response regulator directly targets sigma(S) for degradation by ClpXP. Genes Dev 15, 627-637
- Singer, M. and Kaiser, D. (1995) Ectopic production of guanosine penta-and tetraphosphate can initiate early developmental gene expression in Myxococcus xanthus. Genes Dev 9, 1633-1644
- Tsuzuki, M., et al. (1995) Phosphotransfer circuitry of the putative multi-signal transducer, ArcB, of Escherichia coli: in vitro studies with mutants. Mol Microbiol 18, 953-962
- Rasmussen, A.A., et al. (2006) Four signalling domains in the hybrid histidine protein kinase RodK of Myxococcus xanthus are required for activity. Mol Microbiol 60, 525-534
- Stein, E.A., et al. (2006) Two Ser/Thr protein kinases essential for efficient aggregation and spore morphogenesis in Myxococcus xanthus. Mol Microbiol 60, 1414-1431
- Inclan, Y.F., et al. (2008) The receiver domain of FrzE, a CheA-CheY fusion protein, regulates the CheA histidine kinase activity and downstream signalling to the A-and S-motility systems of Myxococcus xanthus. Mol Microbiol 68, 1328- 1339
- Siryaporn, A. and Goulian, M. (2008) Cross-talk suppression between the CpxA- CpxR and EnvZ-OmpR two-component systems in E. coli. Mol Microbiol 70, 494- 506
- Petters, T., et al. (2012) The orphan histidine protein kinase SgmT is a c-di-GMP receptor and regulates composition of the extracellular matrix together with the orphan DNA binding response regulator DigR in Myxococcus xanthus. Mol Microbiol 84, 147-165
- Konovalova, A., et al. (2012) Two intercellular signals required for fruiting body formation in Myxococcus xanthus act sequentially but non-hierarchically. Mol Microbiol 86, 65-81
- Sudha, V.T., et al. (2008) Identification of a serine protease as a major allergen (Per a 10) of Periplaneta americana. Allergy 63, 768-776
- Catlett, N.L., et al. (2003) Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot Cell 2, 1151-1161
- Huntley, S., et al. (2012) Complete genome sequence of the fruiting myxobacterium Corallococcus coralloides DSM 2259. J Bacteriol 194, 3012-3013
- Chen, Y.E., et al. (2009) Dynamics of Two Phosphorelays Controlling Cell Cycle Progression in Caulobacter crescentus. Journal of Bacteriology 191, 7417-7429
- Romagnoli, S. and Tabita, F.R. (2007) Phosphotransfer reactions of the CbbRRS three-protein two-component system from Rhodopseudomonas palustris CGA010 appear to be controlled by an internal molecular switch on the sensor kinase. J Bacteriol 189, 325-335
- Wegener-Feldbrugge, S. and Sogaard-Andersen, L. (2009) The atypical hybrid histidine protein kinase RodK in Myxococcus xanthus: spatial proximity supersedes kinetic preference in phosphotransfer reactions. J Bacteriol 191, 1765-1776
- Gutu, A.D., et al. (2010) Kinetic characterization of the WalRKSpn (VicRK) two- component system of Streptococcus pneumoniae: dependence of WalKSpn (VicK) phosphatase activity on its PAS domain. J Bacteriol 192, 2346-2358
- Galperin, M.Y. (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188, 4169-4182
- Li, Z.F., et al. (2011) Genome sequence of the halotolerant marine bacterium Myxococcus fulvus HW-1. J Bacteriol 193, 5015-5016
- Cho, K., et al. (2000) Developmental aggregation of Myxococcus xanthus requires frgA, an frz-related gene. J Bacteriol 182, 6614-6621
- Garza, A.G., et al. (2000) Control of asgE expression during growth and development of Myxococcus xanthus. J Bacteriol 182, 6622-6629
- Teplitski, M., et al. (2003) Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J Bacteriol 185, 7257-7265
- Carmany, D.O., et al. (2003) Genetic and biochemical studies of phosphatase activity of PhoR. J Bacteriol 185, 1112-1115
- Baruah, A., et al. (2004) Mutational analysis of the signal-sensing domain of ResE histidine kinase from Bacillus subtilis. J Bacteriol 186, 1694-1704
- Willett, J.W. and Kirby, J.R. (2011) CrdS and CrdA comprise a two-component system that is cooperatively regulated by the Che3 chemosensory system in Myxococcus xanthus. MBio 2
- Kroos, L. (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet 41, 13-39
- Bueno, R., et al. (1985) Role of Glnb and Glnd Gene-Products in Regulation of the Glnalg Operon of Escherichia-Coli. Journal of Bacteriology 164, 816-822
- Tojo, N., et al. (1993) Cloning and nucleotide sequence of the Myxococcus xanthus lon gene: indispensability of lon for vegetative growth. J Bacteriol 175, 2271-2277
- Hagiwara, D., et al. (2003) Genome-wide analyses revealing a signaling network of the RcsC-YojN-RcsB phosphorelay system in Escherichia coli. J Bacteriol 185, 5735-5746
- Sambrook, J., et al. (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y
- Iuchi, S., et al. (1989) A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli. J Bacteriol 171, 868-873
- Kuspa, A., et al. (1992) A-signalling and the cell density requirement for Myxococcus xanthus development. J Bacteriol 174, 7360-7369
- Ng, W.L. and Bassler, B.L. (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43, 197-222
- Menon, A.S. and Goldberg, A.L. (1987) Binding of nucleotides to the ATP- dependent protease La from Escherichia coli. J Biol Chem 262, 14921-14928
- Shi, X., et al. (2008) Bioinformatics and experimental analysis of proteins of two- component systems in Myxococcus xanthus. J Bacteriol 190, 613-624
- Schneiker, S., et al. (2007) Complete genome sequence of the myxobacterium Sorangium cellulosum. Nat Biotechnol 25, 1281-1289
- Varughese, K.I. (2005) Conformational changes of Spo0F along the phosphotransfer pathway. J Bacteriol 187, 8221-8227
- Huynh, T.N., et al. (2010) Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX. Proc Natl Acad Sci U S A 107, 21140-21145
- Ninfa, A.J., et al. (1988) Crosstalk between bacterial chemotaxis signal transduction proteins and regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. Proc Natl Acad Sci U S A 85, 5492-5496
- Fisher, S.L., et al. (1995) Cross-talk between the histidine protein kinase VanS and the response regulator PhoB. Characterization and identification of a VanS domain that inhibits activation of PhoB. J Biol Chem 270, 23143-23149
- O'Connor, K.A. and Zusman, D.R. (1991) Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J Bacteriol 173, 3318-3333
- Thony-Meyer, L. and Kaiser, D. (1993) devRS, an autoregulated and essential genetic locus for fruiting body development in Myxococcus xanthus. J Bacteriol 175, 7450-7462
- Swamy, K.H. and Goldberg, A.L. (1981) E. coli contains eight soluble proteolytic activities, one being ATP dependent. Nature 292, 652-654
- Plamann, L., et al. (1994) Evidence that asgB encodes a DNA-binding protein essential for growth and development of Myxococcus xanthus. J Bacteriol 176, 2013-2020
- Capra, E.J. and Laub, M.T. (2012) Evolution of Two-Component Signal Transduction Systems. Annu Rev Microbiol 180 Groban, E.S., et al. (2009) Kinetic buffering of cross talk between bacterial two- component sensors. J Mol Biol 390, 380-393
- Lopez, D. and Kolter, R. (2010) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS Microbiol Rev 34, 134-149
- Ogawa, M., et al. (1996) FruA, a putative transcription factor essential for the development of Myxococcus xanthus. Mol Microbiol 22, 757-767
- Hsing, W. and Silhavy, T.J. (1997) Function of conserved histidine-243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli. J Bacteriol 179, 3729-3735 REFERENCES 103
- Kuspa, A. and Kaiser, D. (1989) Genes required for developmental signalling in Myxococcus xanthus: three asg loci. J Bacteriol 171, 2762-2772
- Salmon, K.A., et al. (2005) Global gene expression profiling in Escherichia coli K12: effects of oxygen availability and ArcA. J Biol Chem 280, 15084-15096
- Gao, Z., et al. (2008) Heteromeric interactions among ethylene receptors mediate signaling in Arabidopsis. J Biol Chem 283, 23801-23810 REFERENCES 101
- Inoue, H., et al. (1990) High efficiency transformation of Escherichia coli with plasmids. Gene 96, 23-28
- Yadav, S.C., et al. (2011) Identification and characterization of cysteine proteinases of Trypanosoma evansi. Parasitol Res 109, 559-565
- Abramoff, M.D., Magalhaes, P.J., Ram, S.J. (2004) Image Processing with ImageJ. Biophotonics International 11, 7
- Burbulys, D., et al. (1991) Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell 64, 545-552
- Schramm, A., et al. (2012) Intra-and Interprotein Phosphorylation between Two- hybrid Histidine Kinases Controls Myxococcus xanthus Developmental Progression. J Biol Chem 287, 25060-25072
- Georgellis, D., et al. (1997) In vitro phosphorylation study of the arc two- component signal transduction system of Escherichia coli. J Bacteriol 179, 5429- 5435
- Silva, J.C., et al. (1998) In vivo characterization of the type A and B vancomycin- resistant enterococci (VRE) VanRS two-component systems in Escherichia coli: a nonpathogenic model for studying the VRE signal transduction pathways. Proc Natl Acad Sci U S A 95, 11951-11956
- Nakano, M.M. and Zhu, Y. (2001) Involvement of ResE phosphatase activity in down-regulation of ResD-controlled genes in Bacillus subtilis during aerobic growth. J Bacteriol 183, 1938-1944
- Hoch, J.A. and Varughese, K.I. (2001) Keeping signals straight in phosphorelay signal transduction. J Bacteriol 183, 4941-4949
- Iuchi, S. and Lin, E.C. (1992) Mutational analysis of signal transduction by ArcB, a membrane sensor protein responsible for anaerobic repression of operons involved in the central aerobic pathways in Escherichia coli. J Bacteriol 174, 3972-3980
- Zhou, H., et al. (1995) NMR studies of the phosphotransfer domain of the histidine kinase CheA from Escherichia coli: assignments, secondary structure, general fold, and backbone dynamics. Biochemistry 34, 13858-13870
- Igo, M.M., et al. (1989) Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. Genes Dev 3, 1725-1734
- Ueki, T., et al. (1996) Positive-negative KG cassettes for construction of multi-gene deletions using a single drug marker. Gene 183, 153-157
- Yu, C.S., et al. (2004) Predicting subcellular localization of proteins for Gram- negative bacteria by support vector machines based on n-peptide compositions. Protein Sci 13, 1402-1406
- Yu, C.S., et al. (2006) Prediction of protein subcellular localization. Proteins 64, 643-651
- Mastro, R. and Hall, M. (1999) Protein delipidation and precipitation by tri-n- butylphosphate, acetone, and methanol treatment for isoelectric focusing and two- dimensional gel electrophoresis. Anal Biochem 273, 313-315
- Belle, A., et al. (2006) Quantification of protein half-lives in the budding yeast proteome. Proc Natl Acad Sci U S A 103, 13004-13009
- Schweder, T., et al. (1996) Regulation of Escherichia coli starvation sigma factor (sigma s) by ClpXP protease. J Bacteriol 178, 470-476
- Suzuki, K., et al. (2002) Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 184, 5130-5140
- Batchelor, E. and Goulian, M. (2003) Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. Proc Natl Acad Sci U S A 100, 691-696
- Kinoshita, E., et al. (2009) Separation and detection of large phosphoproteins using Phos-tag SDS-PAGE. Nat Protoc 4, 1513-1521 REFERENCES 107
- Francez-Charlot, A., et al. (2009) Sigma factor mimicry involved in regulation of general stress response. Proc Natl Acad Sci U S A 106, 3467-3472
- Kaiser, D. (2004) Signaling in myxobacteria. Annu Rev Microbiol 58, 75-98
- Amerik, A., et al. (1991) Site-directed mutagenesis of La protease. A catalytically active serine residue. FEBS Lett 287, 211-214
- Mullis, K., et al. (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harb Symp Quant Biol 51 Pt 1, 263-273
- Albanesi, D., et al. (2009) Structural plasticity and catalysis regulation of a thermosensor histidine kinase. Proc Natl Acad Sci U S A 106, 16185-16190
- Arias, I.M., et al. (1969) Studies on the synthesis and degradation of proteins of the endoplasmic reticulum of rat liver. J Biol Chem 244, 3303-3315
- Capra, E.J., et al. (2010) Systematic dissection and trajectory-scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways. PLoS Genet 6, e1001220
- Tojo, N., et al. (1993) The lonD gene is homologous to the lon gene encoding an ATP-dependent protease and is essential for the development of Myxococcus xanthus. J Bacteriol 175, 4545-4549
- Thomas, S.H., et al. (2008) The mosaic genome of Anaeromyxobacter dehalogenans strain 2CP-C suggests an aerobic common ancestor to the delta- proteobacteria. PLoS One 3, e2103 252 Ivanova, N., et al. (2010) Complete genome sequence of Haliangium ochraceum type strain (SMP-2). Stand Genomic Sci 2, 96-106
- Plamann, L., et al. (1995) The Myxococcus xanthus asgA gene encodes a novel signal transduction protein required for multicellular development. J Bacteriol 177, 2014-2020
- Lee, B., et al. (2011) The Myxococcus xanthus spore cuticula protein C is a fragment of FibA, an extracellular metalloprotease produced exclusively in aggregated cells. PLoS One 6, e28968 174 Avery, L. and Wasserman, S. (1992) Ordering gene function: the interpretation of epistasis in regulatory hierarchies. Trends Genet 8, 312-316
- Bren, A. and Eisenbach, M. (1998) The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY. J Mol Biol 278, 507-514 REFERENCES 109
- Dahl, M.K., et al. (1992) The phosphorylation state of the DegU response regulator acts as a molecular switch allowing either degradative enzyme synthesis or expression of genetic competence in Bacillus subtilis. J Biol Chem 267, 14509- 14514
- Muffler, A., et al. (1996) The response regulator RssB controls stability of the sigma(S) subunit of RNA polymerase in Escherichia coli. EMBO J 15, 1333-1339
- Simon, G., et al. (1994) The torR gene of Escherichia coli encodes a response regulator protein involved in the expression of the trimethylamine N-oxide reductase genes. J Bacteriol 176, 5601-5606
- Eguchi, Y., et al. (2003) Transcriptional regulation of drug efflux genes by EvgAS, a two-component system in Escherichia coli. Microbiology 149, 2819-2828
- Haldimann, A., et al. (1997) Transcriptional regulation of the Enterococcus faecium BM4147 vancomycin resistance gene cluster by the VanS-VanR two-component regulatory system in Escherichia coli K-12. J Bacteriol 179, 5903-5913
- Raivio, T.L. and Silhavy, T.J. (1997) Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J Bacteriol 179, 7724-7733
- Qian, W., et al. (2008) Two-component signal transduction systems of Xanthomonas spp.: a lesson from genomics. Mol Plant Microbe Interact 21, 151 REFERENCES
- Rodrigue, A., et al. (2000) Two-component systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8, 498-504
- Garcia Vescovi, E., et al. (2010) Two component systems in the spatial program of bacteria. Curr Opin Microbiol 13, 210-218
- Birnboim, H.C. and Doly, J. (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7, 1513-1523
- Cho, K. and Zusman, D.R. (1999) AsgD, a new two-component regulator required for A-signalling and nutrient sensing during early development of Myxococcus xanthus. Mol Microbiol 34, 268-281
- Inclan, Y.F., et al. (2007) FrzZ, a dual CheY-like response regulator, functions as an output for the Frz chemosensory pathway of Myxococcus xanthus. Mol Microbiol 65, 90-102
- Thomas, S.A., et al. (2008) Two variable active site residues modulate response regulator phosphoryl group stability. Mol Microbiol 69, 453-465
- Gonnet, G.H., et al. (1992) Exhaustive matching of the entire protein sequence database. Science 256, 1443-1445
- Shapiro, J.A. (1998) Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol 52, 81-104
- Moreno, M., et al. (2000) Regulation of sigma S degradation in Salmonella enterica var typhimurium: in vivo interactions between sigma S, the response regulator MviA(RssB) and ClpX. J Mol Microbiol Biotechnol 2, 245-254
- 244 Nath, K. and Koch, A.L. (1971) Protein degradation in Escherichia coli. II. Strain differences in the degradation of protein and nucleic acid resulting from starvation. J Biol Chem 246, 6956-6967
- Biondi, E.G., et al. (2006) Regulation of the bacterial cell cycle by an integrated genetic circuit. Nature 444, 899-904
- Higgs, P.I., et al. (2005) Four unusual two-component signal transduction homologs, RedC to RedF, are necessary for timely development in Myxococcus xanthus. J Bacteriol 187, 8191-8195
- Boysen, A., et al. (2002) The DevT protein stimulates synthesis of FruA, a signal transduction protein required for fruiting body morphogenesis in Myxococcus xanthus. J Bacteriol 184, 1540-1546
- Kearns, D.B., et al. (2002) An extracellular matrix-associated zinc metalloprotease is required for dilauroyl phosphatidylethanolamine chemotactic excitation in Myxococcus xanthus. J Bacteriol 184, 1678-1684
- Iniesta, A.A., et al. (2006) A phospho-signaling pathway controls the localization and activity of a protease complex critical for bacterial cell cycle progression. Proc Natl Acad Sci U S A 103, 10935-10940
- Goldman, B.S., et al. (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci U S A 103, 15200-15205
- Ueki, T. and Inouye, S. (2003) Identification of an activator protein required for the induction of fruA, a gene essential for fruiting body development in Myxococcus xanthus. Proc Natl Acad Sci U S A 100, 8782-8787
- Rasmussen, A.A. and Sogaard-Andersen, L. (2003) TodK, a putative histidine protein kinase, regulates timing of fruiting body morphogenesis in Myxococcus xanthus. J Bacteriol 185, 5452-5464
- Kuspa, A., et al. (1992) Identification of heat-stable A-factor from Myxococcus xanthus. J Bacteriol 174, 3319-3326
- 'Connor, K.A. and Zusman, D.R. (1991) Analysis of Myxococcus xanthus cell types by two-dimensional polyacrylamide gel electrophoresis. J Bacteriol 173, 3334-3341
- Connor, K.A. and Zusman, D.R. (1991) Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus. J Bacteriol 173, 3342-3355
- Wireman, J.W. and Dworkin, M. (1977) Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J Bacteriol 129, 798-802
- Mittal, S. and Kroos, L. (2009) A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression. Proc Natl Acad Sci U S A 106, 1965-1970
- Mittal, S. and Kroos, L. (2009) Combinatorial regulation by a novel arrangement of FruA and MrpC2 transcription factors during Myxococcus xanthus development. J Bacteriol 191, 2753-2763
- Jenal, U. and Galperin, M.Y. (2009) Single domain response regulators: molecular switches with emerging roles in cell organization and dynamics. Curr Opin Microbiol 12, 152-160
- Bulyha, I., et al. (2009) Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol 74, 691-706
- Paul, R., et al. (2008) Allosteric regulation of histidine kinases by their cognate response regulator determines cell fate. Cell 133, 452-461
- Chung, C.T., et al. (1989) One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A 86, 2172-2175
- Sarkar, M.K., et al. (2010) Chemotaxis signaling protein CheY binds to the rotor protein FliN to control the direction of flagellar rotation in Escherichia coli. Proc Natl Acad Sci U S A 107, 9370-9375
- Lee, B., et al. (2012) Myxococcus xanthus developmental cell fate production: heterogeneous accumulation of developmental regulatory proteins and reexamination of the role of MazF in developmental lysis. J Bacteriol 194, 3058- 3068
- Shi, W., et al. (1996) Cell density regulates cellular reversal frequency in Myxococcus xanthus. Proc Natl Acad Sci U S A 93, 4142-4146
- Sogaard-Andersen, L. and Kaiser, D. (1996) C factor, a cell-surface-associated intercellular signaling protein, stimulates the cytoplasmic Frz signal transduction system in Myxococcus xanthus. Proc Natl Acad Sci U S A 93, 2675-2679
- Sun, H. and Shi, W. (2001) Analyses of mrp genes during Myxococcus xanthus development. J Bacteriol 183, 6733-6739
- Sun, H. and Shi, W. (2001) Genetic studies of mrp, a locus essential for cellular aggregation and sporulation of Myxococcus xanthus. J Bacteriol 183, 4786-4795 REFERENCES 105
- Segal, H.L. and Kim, Y.S. (1963) Glucocorticoid Stimulation of the Biosynthesis of Glutamic-Alanine Transaminase. Proc Natl Acad Sci U S A 50, 912-918
- Campos, J.M. and Zusman, D.R. (1975) Regulation of development in Myxococcus xanthus: effect of 3':5'-cyclic AMP, ADP, and nutrition. Proc Natl Acad Sci U S A 72, 518-522
- Iuchi, S. and Lin, E.C. (1988) arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc Natl Acad Sci U S A 85, 1888-1892
- Domian, I.J., et al. (1997) Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90, 415-424
- Skerker, J.M., et al. (2008) Rewiring the specificity of two-component signal transduction systems. Cell 133, 1043-1054
- Peterson, R., et al. (2009) Fungal proteins with mannanase activity identified directly from a Congo Red stained zymogram by mass spectrometry. J Microbiol Methods 79, 374-377
- 112 Silversmith, R.E. (2010) Auxiliary phosphatases in two-component signal transduction. Current Opinion in Microbiology 13, 177-183
- Pazy, Y., et al. (2010) Identical phosphatase mechanisms achieved through distinct modes of binding phosphoprotein substrate. Proc Natl Acad Sci U S A 107, 1924- 1929