Skip to main content

Advertisement

Log in

Signal transduction and adaptive regulation through bacterial two-component systems: the Escherichia coli AtoSC paradigm

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

Adaptive signal transduction within microbial cells involves a multi-faceted regulated phosphotransfer mechanism that comprises structural rearrangements of sensor histidine kinases upon ligand-binding and phosphorylation-induced conformational changes in response regulators of versatile two-component systems (TCS), arisen early in bacterial evolution. In Escherichia coli, cross-talk between the AtoS histidine kinase and the AtoC response regulator, forming the AtoSC TCS, through His → Asp phosphotransfer, activates AtoC directly to induce atoDAEB operon expression, thus modulating diverse fundamental cellular processes such as short-chain fatty acid catabolism, poly-(R)-3-hydroxybutyrate biosynthesis and chemotaxis. Among the inducers hitherto identified, acetoacetate is the classical activator. The AtoSC TCS functional modulation by polyamines, histamine and Ca2+, as well as the role of AtoC as transcriptional regulator, add new promising perspectives in the physiological significance and potential pharmacological exploitation of this TCS in cell proliferation, bacteria–host interactions, chemotaxis, and adaptation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

Az:

Antizyme

cPHB:

Complexed poly-(R)-3-hydroxybutyrate

HAMP:

Linker domain in HKs, adenyl cyclases, methyl-accepting proteins and phosphatases

HK:

Histidine kinase

IHF:

Integration host factor

LPS:

Lipopolysaccharides

ODC:

Ornithine decarboxylase

RR:

Response regulator

SCFA:

Short-chain fatty acid

TCS:

Two-component system

References

  • Akdis CA, Simons FE (2006) Histamine receptors are hot in immunopharmacology. Eur J Pharmacol 533:69–76

    Article  PubMed  CAS  Google Scholar 

  • Alm E, Huang K, Arkin A (2006) The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLoS Comput Biol 2:e143

    Article  PubMed  CAS  Google Scholar 

  • Anagnostopoulos CG, Kyriakidis DA (1996) Regulation of the Escherichia coli biosynthetic ornithine decarboxylase activity by phosphorylation and nucleotides. Biochim Biophys Acta 1297:228–234

    PubMed  Google Scholar 

  • Barrios H, Valderrama B, Morett E (1999) Compilation and analysis of sigma54-dependent promoter sequences. Nucleic Acids Res 27:4305–4313

    Article  PubMed  CAS  Google Scholar 

  • Berlyn MKB (1998) Linkage map of Escherichia coli K-12, edition 10: the traditional map. Microbiol Mol Biol Rev 62:814–984

    PubMed  CAS  Google Scholar 

  • Blattner FR, Plunkett GIII, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462

    Article  PubMed  CAS  Google Scholar 

  • Bourret RB, Stock AM (2002) Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277:9625–9628

    Article  PubMed  CAS  Google Scholar 

  • Canellakis ES, Viceps-Madore D, Kyriakidis DA, Heller JS (1979) The regulation and function of ornithine decarboxylase and of the polyamines. Curr Top Cell Regul 15:155–202

    PubMed  CAS  Google Scholar 

  • Canellakis ES, Kyriakidis DA, Heller JS, Pawlak JW (1981) The complexity of regulation of ornithine decarboxylase. Med Biol 59:279–285

    PubMed  CAS  Google Scholar 

  • Canellakis ES, Paterakis AA, Huang SC, Panagiotidis CA, Kyriakidis DA (1993) Identification, cloning, and nucleotide sequencing of the ornithine decarboxylase antizyme gene of Escherichia coli. Proc Natl Acad Sci USA 90:7129–7133

    Article  PubMed  CAS  Google Scholar 

  • Chaves P, Correa-Fiz F, Melgarejo E, Urdiales JL, Medina MA, Sánchez-Jiménez F (2007) Development of an expression macroarray for amine metabolism-related genes. Amino Acids 33:315–322

    Article  PubMed  CAS  Google Scholar 

  • Chen YT, Chang HY, Lu CL, Peng HL (2004) Evolutionary analysis of the two-component systems in Pseudomonas aeruginosa PAO1. J Mol Evol 59:725–737

    Article  PubMed  CAS  Google Scholar 

  • Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860–867

    Article  PubMed  CAS  Google Scholar 

  • Das S, Reusch RN (1999) Gating kinetics of E. coli poly-3-hydroxybutyrate/polyphosphate channels in planar bilayer membranes. J Membr Biol 170:135–145

    Article  PubMed  CAS  Google Scholar 

  • de Been M, Francke C, Moezelaar R, Abee T, Siezen RJ (2006) Comparative analysis of two-component signal transduction systems of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis. Microbiology 152:3035–3048

    Article  PubMed  CAS  Google Scholar 

  • De Carlo S, Chen B, Hoover TR, Kondrashkina E, Nogales E, Nixon BT (2006) The structural basis for regulated assembly and function of the transcriptional activator NtrC. Genes Dev 20:1485–1495

    Article  PubMed  CAS  Google Scholar 

  • dela Vega AL, Delcour AH (1996) Polyamines decrease Escherichia coli outer membrane permeability. J Bacteriol 178:3715–3721

    PubMed  CAS  Google Scholar 

  • Dortay H, Gruhn N, Pfeifer A, Schwerdtner M, Schmülling T, Heyl A (2008) Toward an interaction map of the two-component signaling pathway of Arabidopsis thaliana. J Proteome Res 7:3649–3660

    Article  PubMed  CAS  Google Scholar 

  • Du L, Jiao F, Chu J, Jin G, Chen M, Wu P (2007) The two-component signal system in rice (Oryza sativa L.): a genome-wide study of cytokinin signal perception and transduction. Genomics 89:697–707

    Article  PubMed  CAS  Google Scholar 

  • Dutta R, Qin L, Inouye M (1999) Histidine kinases: diversity of domain organization. Mol Microbiol 34:633–640

    Article  PubMed  CAS  Google Scholar 

  • Filippou PS, Lioliou EE, Panagiotidis CA, Athanassopoulos CM, Garnelis T, Papaioannou D, Kyriakidis DA (2007) Effect of polyamines and synthetic polyamine-analogues on the expression of antizyme (AtoC) and its regulatory genes. BMC Biochem 8:1

    Article  PubMed  CAS  Google Scholar 

  • Filippou PS, Kasemian LD, Panagiotidis CA, Kyriakidis DA (2008) Functional characterization of the histidine kinase of the E. coli two-component signal transduction system AtoSC. Biochim Biophys Acta 1780:1023–1031

    PubMed  CAS  Google Scholar 

  • Flashner Y, Weiss DS, Keener J, Kustu S (1995) Constitutive forms of the enhancer-binding protein NtrC: evidence that essential oligomerization determinants lie in the central activation domain. J Mol Biol 249:700–713

    Article  PubMed  CAS  Google Scholar 

  • Fong WF, Heller JS, Canellakis ES (1976) The appearance of an ornithine decarboxylase inhibitory protein upon the addition of putrescine to cell cultures. Biochim Biophys Acta 428:456–465

    PubMed  CAS  Google Scholar 

  • Fu W, Yang F, Kang X, Zhang X, Li Y, Xia B, Jin C (2007) First structure of the polymyxin resistance proteins. Biochem Biophys Res Commun 361:1033–1037

    Article  PubMed  CAS  Google Scholar 

  • Galperin MY (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188:4169–4182

    Article  PubMed  CAS  Google Scholar 

  • Gao R, Mack TR, Stock AM (2007) Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem Sci 32:225–234

    Article  PubMed  CAS  Google Scholar 

  • Grebe TW, Stock JB (1999) The histidine protein kinase superfamily. Adv Microb Physiol 41:139–227

    Article  PubMed  CAS  Google Scholar 

  • Grigoroudis AI, Panagiotidis CA, Lioliou EE, Vlassi M, Kyriakidis DA (2007) Molecular modeling and functional analysis of the AtoS-AtoC two-component signal transduction system of Escherichia coli. Biochim Biophys Acta 1770:1248–1258

    PubMed  CAS  Google Scholar 

  • Guarner F, Malagelada JR (2003) Gut flora in health and disease. Lancet 361:512–519

    Article  PubMed  Google Scholar 

  • Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, Choi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T (2006) Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2: 2006.0007

  • Heller JS, Fong WF, Canellakis ES (1976) Induction of a protein inhibitor of ornithine decarboxylase by the end products of its reaction. Proc Natl Acad Sci USA 73:1858–1862

    Article  PubMed  CAS  Google Scholar 

  • Heller JS, Kyriakidis DA, Canellakis ES (1983) Purification and properties of the antizymes of Escherichia coli to ornithine decarboxylase. Biochim Biophys Acta 760:154–162

    PubMed  CAS  Google Scholar 

  • Hirakawa H, Nishino K, Hirata T, Yamaguchi A (2003) Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Bacteriol 185:1851–1856

    Article  PubMed  CAS  Google Scholar 

  • Hoang HH, Gurich N, González JE (2008) Regulation of motility by the ExpR/Sin quorum-sensing system in Sinorhizobium meliloti. J Bacteriol 190:861–871

    Article  PubMed  CAS  Google Scholar 

  • Hoch JA (2000) Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3:165–170

    Article  PubMed  CAS  Google Scholar 

  • Hong HJ, Hutchings MI, Hill LM, Buttner MJ (2005) The role of the novel Fem protein VanK in vancomycin resistance in Streptomyces coelicolor. J Biol Chem 280:13055–13061

    Article  PubMed  CAS  Google Scholar 

  • Hori Y, Nihei Y, Kurokawa Y, Kuramasu A, Makabe-Kobayashi Y, Terui T, Doi H, Satomi S, Sakurai E, Nagy A, Watanabe T, Ohtsu H (2002) Accelerated clearance of Escherichia coli in experimental peritonitis of histamine-deficient mice. J Immunol 169:1978–1983

    PubMed  CAS  Google Scholar 

  • Huang R, Reusch RN (1996) Poly(3-hydroxybutyrate) is associated with specific proteins in the cytoplasm and membranes of Escherichia coli. J Biol Chem 271:22196–22202

    Article  PubMed  CAS  Google Scholar 

  • Igarashi K, Kashiwagi K (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271:559–564

    Article  PubMed  CAS  Google Scholar 

  • Itoh T, Aiba H, Baba T, Hayashi K, Inada T, Isono K, Kasai H, Kimura S, Kitakawa M, Kitagawa M, Makino K, Miki T, Mizobuchi K, Mori H, Mori T, Motomura K, Nakade S, Nakamura Y, Nashimoto H, Nishio Y, Oshima T, Saito N, Sampei G, Seki Y, Horiuchi T (1996) A 460-kb DNA sequence of the Escherichia coli K-12 genome corresponding to the 40.1–50.0 min region on the linkage map. DNA Res 3:379–392

    Article  PubMed  CAS  Google Scholar 

  • Ivanov IP, Atkins JF (2007) Ribosomal frameshifting in decoding antizyme mRNAs from yeast and protists to humans: close to 300 cases reveal remarkable diversity despite underlying conservation. Nucleic Acids Res 35:1842–1858

    Article  PubMed  CAS  Google Scholar 

  • Ivanov IP, Gesteland RF, Atkins JF (1998) Does antizyme exist in Escherichia coli? Mol Microbiol 29:1521–1522

    Article  PubMed  CAS  Google Scholar 

  • Jenkins LS, Nunn WD (1987a) Genetic and molecular characterization of the genes involved in short-chain fatty acid degradation in Escherichia coli: the ato system. J Bacteriol 169:42–52

    PubMed  CAS  Google Scholar 

  • Jenkins LS, Nunn WD (1987b) Regulation of the ato operon by the atoC gene in Escherichia coli. J Bacteriol 169:2096–2102

    PubMed  CAS  Google Scholar 

  • Jones HE, Holland IB, Jacq A, Wall T, Campbell AK (2003) Escherichia coli lacking the AcrAB multidrug efflux pump also lacks nonproteinaceous, PHB-polyphosphate Ca2+ channels in the membrane. Biochim Biophys Acta 1612:90–97

    Article  PubMed  CAS  Google Scholar 

  • Katsu T, Yoshimura S, Fujita Y (1984) Increases in permeability of Escherichia coli outer membrane induced by polycations. FEBS Lett 166:175–178

    Article  PubMed  CAS  Google Scholar 

  • Kim D, Forst S (2001) Genomic analysis of the histidine kinase family in bacteria and archaea. Microbiology 147:1197–1212

    PubMed  CAS  Google Scholar 

  • Kofoid EC, Parkinson JS (1988) Transmitter and receiver modules in bacterial signaling proteins. Proc Natl Acad Sci USA 85:4981–4985

    Article  PubMed  CAS  Google Scholar 

  • Koretke KK, Lupas AN, Warren PV, Rosenberg M, Brown JR (2000) Evolution of two-component signal transduction. Mol Biol Evol 17:1956–1970

    PubMed  CAS  Google Scholar 

  • Krämer S, Sellge G, Lorentz A, Krueger D, Schemann M, Feilhauer K, Gunzer F, Bischoff SC (2008) Selective activation of human intestinal mast cells by Escherichia colihemolysin. J Immunol 181:1438–1445

    PubMed  Google Scholar 

  • Kwon DH, Lu CD (2006) Polyamines induce resistance to cationic peptide, aminoglycoside, and quinolone antibiotics in Pseudomonas aeruginosa PAO1. Antimicrob Agents Chemother 50:1615–1622

    Article  PubMed  CAS  Google Scholar 

  • Kwon DH, Lu CD (2007) Polyamine effects on antibiotic susceptibility in bacteria. Antimicrob Agents Chemother 51:2070–2077

    Article  PubMed  CAS  Google Scholar 

  • Kyriakidis DA, Heller JS, Canellakis ES (1978) Modulation of ornithine decarboxylase activity in Escherichia coli by positive and negative effectors. Proc Natl Acad Sci USA 75:4699–4703

    Article  PubMed  CAS  Google Scholar 

  • Kyriakidis DA, Theodorou MC, Filippou PS, Kyriakidis KD, Tiligada E (2008) Effect of histamine on the signal transduction of the AtoSC two component system and involvement in poly-(R)-3-hydroxybutyrate biosynthesis in Escherichia coli. Amino Acids 35:45–52

    Article  PubMed  CAS  Google Scholar 

  • Kyriakidis K, Zampeli E, Tiligada E (2009) Histamine levels in whole peripheral blood from women with ductal breast cancer: a pilot study. Inflamm Res (in press)

  • Laub MT, Biondi EG, Skerker JM (2007) Phosphotransfer profiling: systematic mapping of two-component signal transduction pathways and phosphorelays. Methods Enzymol 423:531–548

    Article  PubMed  CAS  Google Scholar 

  • Lee SY, DeLaTorre A, Yan D, Kustu S, Nixon BT, Wemmer DE (2003) Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ ATPase domains. Genes Dev 17:2552–2563

    Article  PubMed  CAS  Google Scholar 

  • Lioliou EE, Kyriakidis DA (2004) The role of bacterial antizyme: From an inhibitory protein to AtoC transcriptional regulator. Microb Cell Fact 3:8

    Article  PubMed  Google Scholar 

  • Lioliou EE, Mimitou EP, Grigoroudis AI, Panagiotidis CH, Panagiotidis CA, Kyriakidis DA (2005) Phosphorylation activity of the response regulator of the two-component signal transduction system AtoSC in E. coli. Biochim Biophys Acta 1725:257–268

    PubMed  CAS  Google Scholar 

  • Lolkema JS (2006) Domain structure and pore loops in the 2-hydroxycarboxylate transporter family. J Mol Microbiol Biotechnol 11:318–325

    Article  PubMed  CAS  Google Scholar 

  • Lopatin AN, Makhina EN, Nichols CG (1994) Potassium channel block by cytoplasmic polyamines as the mechanism of intrinsic rectification. Nature 372:366–369

    Article  PubMed  CAS  Google Scholar 

  • Madison LL, Huisman GW (1999) Metabolic engineering of poly(3-hydroxyalkanoates): From DNA to Plastic. Microbiol Mol Biol Rev 63:21–53

    PubMed  CAS  Google Scholar 

  • Marceau M, Sebbane F, Ewann F, Collyn F, Lindner B, Campos MA, Bengoechea JA, Simonet M (2004) The pmrF polymyxin-resistance operon of Yersinia pseudotuberculosis is upregulated by the PhoP-PhoQ two-component system but not by PmrA-PmrB, and is not required for virulence. Microbiology 150:3947–3957

    Article  PubMed  CAS  Google Scholar 

  • Maris AE, Kaczor-Grzeskowiak M, Ma Z, Kopka ML, Gunsalus RP, Dickerson RE (2005) Primary and secondary modes of DNA recognition by the NarL two-component response regulator. Biochemistry 44:14538–14552

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Hackert E, Stock AM (1997) Structural relationships in the OmpR family of winged-helix transcription factors. J Mol Biol 269:301–312

    Article  PubMed  Google Scholar 

  • Matta MK, Lioliou EE, Panagiotidis CH, Kyriakidis DA, Panagiotidis CA (2007) Interactions of the antizyme/AtoC with regulatory elements of the Escherichia coli atoDAEB operon. J Bacteriol 189:6324–6332

    Article  PubMed  CAS  Google Scholar 

  • Medina MÁ, Urdiales JL, Rodríguez-Caso C, Ramírez FJ, Sánchez-Jiménez F (2003) Biogenic amines and polyamines: similar biochemistry for different physiological missions and biomedical applications. Crit Rev Biochem Mol Biol 38:23–59

    Article  PubMed  CAS  Google Scholar 

  • Merighi M, Majerczak DR, Stover EH, Coplin DL (2003) The HrpX/HrpY two-component system activates hrpS expression, the first step in the regulatory cascade controlling the Hrp regulon in Pantoea stewartii subsp. stewartii. Mol Plant Microbe Interact 16:238–248

    Article  PubMed  CAS  Google Scholar 

  • Mizuno T (1997) Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res 4:161–168

    Article  PubMed  CAS  Google Scholar 

  • Möker N, Brocker M, Schaffer S, Krämer R, Morbach S, Bott M (2004) Deletion of the genes encoding the MtrA-MtrB two-component system of Corynebacterium glutamicum has a strong influence on cell morphology, antibiotics susceptibility and expression of genes involved in osmoprotection. Mol Microbiol 54:420–438

    Article  PubMed  CAS  Google Scholar 

  • Morris DR, Boeker EA (1983) Biosynthetic and biodegradative ornithine and arginine decarboxylases from Escherichia coli. Methods Enzymol 94:125–134

    Article  PubMed  CAS  Google Scholar 

  • Nikaido H (1996) Multidrug efflux pumps of gram-negative bacteria. J Bacteriol 178:5853–5859

    PubMed  CAS  Google Scholar 

  • Ninfa AJ, Ninfa EG, Lupas AN, Stock A, Magasanik B, Stock J (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 USA 85:5492–5496

    Article  PubMed  CAS  Google Scholar 

  • Ogra PL, Welliver RC Sr (2008) Effects of early environment on mucosal immunologic homeostasis, subsequent immune responses and disease outcome. Nestle Nutr Workshop Ser Pediatr Program 61:145–181

    Article  PubMed  Google Scholar 

  • Oshima T, Aiba H, Masuda Y, Kanaya S, Sugiura M, Wanner BL, Mori H, Mizuno T (2002) Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 46:281–291

    Article  PubMed  CAS  Google Scholar 

  • Palotai R, Szalay MS, Csermely P (2008) Chaperones as integrators of cellular networks: changes of cellular integrity in stress and diseases. IUBMB Life 60:10–18

    Article  PubMed  CAS  Google Scholar 

  • Parkinson JS, Kofoid EC (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26:71–112

    Article  PubMed  CAS  Google Scholar 

  • Pauli G, Overath P (1972) ato Operon: a highly inducible system for acetoacetate and butyrate degradation in Escherichia coli. Eur J Biochem 29:553–562

    Article  PubMed  CAS  Google Scholar 

  • Pavlov E, Grimbly C, Diao CT, French RJ (2005) A high-conductance mode of a poly-3-hydroxybutyrate/calcium/polyphosphate channel isolated from competent Escherichia coli cells. FEBS Lett 579:5187–5192

    Article  PubMed  CAS  Google Scholar 

  • Pelton JG, Kustu S, Wemmer DE (1999) Solution structure of the DNA-binding domain of NtrC with three alanine substitutions. J Mol Biol 292:1095–1110

    Article  PubMed  CAS  Google Scholar 

  • Perron K, Caille O, Rossier C, Van Delden C, Dumas JL, Köhler T (2004) CzcR-CzcS, a two-component system involved in heavy metal and carbapenem resistance in Pseudomonas aeruginosa. J Biol Chem 279:8761–8768

    Article  PubMed  CAS  Google Scholar 

  • Pilalis E, Grigoroudis A, Chatziioannou A, Panagiotidis AC, Kolisis F, Kyriakidis DA (2008) E. coli genome-wide promoter analysis in search for potential AtoC target elements. FEBS J 275(Suppl 1):286

    Google Scholar 

  • Rabin RS, Stewart V (1993) Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J Bacteriol 175:3259–3268

    PubMed  CAS  Google Scholar 

  • Reading NC, Torres AG, Kendall MM, Hughes DT, Yamamoto K, Sperandio V (2007) A novel two-component signaling system that activates transcription of an enterohemorrhagic Escherichia coli effector involved in remodeling of host actin. J Bacteriol 189:2468–2476

    Article  PubMed  CAS  Google Scholar 

  • Reed JL, Vo TD, Schilling CH, Palsson BO (2003) An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol 4:R54

    Article  PubMed  Google Scholar 

  • Reitzer L, Schneider BL (2001) Metabolic context and possible physiological themes of σ54-dependent genes in Escherichia coli. Microbiol Mol Biol Rev 65:422–444

    Article  PubMed  CAS  Google Scholar 

  • Reusch RN, Huang R, Bramble LL (1995) Poly-3-hydroxybutyrate/polyphosphate complexes form voltage-activated Ca2+ channels in the plasma membranes of Escherichia coli. Biophys J 69:754–766

    Article  PubMed  CAS  Google Scholar 

  • Rhie HG, Dennis D (1995) Role of fadR and atoC(Con) mutations in poly(3-hydroxybutyrate-co-3-hydroxyvalerate) synthesis in recombinant pha + Escherichia coli. Appl Environ Microbiol 61:2487–2492

    PubMed  CAS  Google Scholar 

  • Rogers PD, Liu TT, Barker KS, Hilliard GM, English BK, Thornton J, Swiatlo E, McDaniel LS (2007) Gene expression profiling of the response of Streptococcus pneumoniae to penicillin. J Antimicrob Chemother 59:616–626

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Chica AJ, Soriano A, Tuñón I, Sánchez-Jiménez F, Silla E, Ramírez FJ (2006) FT-Raman and QM/MM study of the interaction between histamine and DNA. Chem Phys 324:579–590

    Article  CAS  Google Scholar 

  • Santos JL, Shiozaki K (2001) Fungal histidine kinases. Sci STKE 98:RE1

    Google Scholar 

  • Stock AM, Wylie DC, Mottonen JM, Lupas AN, Ninfa EG, Ninfa AJ, Schutt CE, Stock JB (1988) Phosphoproteins involved in bacterial signal transduction. Cold Spring Harb Symp Quant Biol 53:49–57

    PubMed  CAS  Google Scholar 

  • Stock AM, Mottonen JM, Stock JB, Schutt CE (1989) Three-dimensional structure of CheY, the response regulator of bacterial chemotaxis. Nature 337:745–749

    Article  PubMed  CAS  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two component signal transduction. Ann Rev Biochem 69:183–215

    Article  PubMed  CAS  Google Scholar 

  • Theodorou MC, Panagiotidis CA, Panagiotidis CH, Pantazaki AA, Kyriakidis DA (2006) Involvement of the AtoSC signal transduction system in poly-(R)-3-hydroxybutyrate biosynthesis in Escherichia coli. Biochim Biophys Acta 1760:896–906

    PubMed  CAS  Google Scholar 

  • Theodorou MC, Theodorou EC, Panagiotidis CA, Kyriakidis DA (2007) Spermidine triggering effect to the signal transduction through the AtoSC/Az two-component system in Escherichia coli. Biochim Biophys Acta 1770:1104–1114

    PubMed  CAS  Google Scholar 

  • Theodorou MC, Tiligada E, Kyriakidis DA (2008a) The involvement of AtoSC two-component system in E. coli chemotaxis FEBS J 275(Suppl 1):290

    Google Scholar 

  • Theodorou MC, Tiligada E, Kyriakidis DA (2008b) Extracellular Ca2+ transients affect poly-(R)-3-hydroxybutyrate regulation by the AtoSC system in E. coli, Biochem J Submitted

    Google Scholar 

  • Ulrich LE, Zhulin IB (2007) MiST: a microbial signal transduction database. Nucleic Acids Res 35:D386–D390

    Article  PubMed  CAS  Google Scholar 

  • Volkman BF, Lipson D, Wemmer DE, Kern D (2001) Two-state allosteric behavior in a single-domain signaling protein. Science 291:2429–2433

    Article  PubMed  CAS  Google Scholar 

  • West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26:369–376

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson MG, Millar JBA (2000) Control of the eukaryotic cell cycle by MAP kinase signaling pathways. FASEB J 14:2147–2157

    Article  PubMed  CAS  Google Scholar 

  • Wright JS, Olekhnovich IN, Touchie G, Kadner RJ (2000) The histidine kinase domain of UhpB inhibits UhpA action at the Escherichia coli uhpT promoter. J Bacteriol 182:6279–6286

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto K, Hirao K, Oshima T, Aiba H, Utsumi R, Ishihama A (2005) Functional characterization in vitro of all two-component signal transduction systems from Escherichia coli. J Biol Chem 280:1448–1456

    Article  PubMed  CAS  Google Scholar 

  • Zampeli E, Pitychoutis P, Papadopoulou-Daifoti Z, Tiligada E (2009) Systemic challenge with lipopolysaccharide increases histamine levels in the conjunctiva and cartilage, but not hypothalamus of Sprague-Dawley rats. Inflamm Res (in press)

  • Zhou L, Lei XH, Bochner BR, Wanner BL (2003) Phenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems. J Bacteriol 185:4956–4972

    Article  PubMed  CAS  Google Scholar 

  • Zimmer DP, Soupene E, Lee HL, Wendisch VF, Khodursky AB, Peter BJ, Bender RA, Kustu S (2000) Nitrogen regulatory protein C-controlled genes of Escherichia coli: scavenging as a defense against nitrogen limitation. Proc Natl Acad Sci USA 97:14674–14679

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the Ph.D. students and Post-Doc fellows in our laboratories, who have contributed to the cited research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dimitrios A. Kyriakidis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kyriakidis, D.A., Tiligada, E. Signal transduction and adaptive regulation through bacterial two-component systems: the Escherichia coli AtoSC paradigm. Amino Acids 37, 443–458 (2009). https://doi.org/10.1007/s00726-009-0241-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-009-0241-z

Keywords

Navigation