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Effect of histamine on the signal transduction of the AtoS–AtoC two component system and involvement in poly-(R)-3-hydroxybutyrate biosynthesis in Escherichia coli

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Summary.

AtoS–AtoC two-component system acts directly on the atoDAEB operon transcription to regulate the biosynthesis of short-chain poly-(R)-3-hydroxybutyrate. This study sought to investigate the effect of histamine and compound 48/80 on the regulation of AtoS–AtoC two-component system in Escherichia coli K-12 MA255 (speC −, speB −) and the isogenic E. coli strains BW25113 (atoSC +) and BW28878 (ΔatoSC) transformed with plasmids carrying related genes. Histamine or compound 48/80 induced or tended to reduce atoC transcription, respectively, while neither compound showed any effect on atoDAEB operon transcription. Moreover, histamine down-regulated poly-(R)-3-hydroxybutyrate biosynthesis, whereas compound 48/80 up-regulated its biosynthesis, maximal induction being obtained in the presence of multiple copies of AtoS–AtoC. Interestingly, co-administration of histamine counteracted this inductive effect of compound 48/80. The reported data provide the first evidence for a differential modulator role of histamine and compound 48/80 on the AtoS–AtoC two-component system signaling in potentially pathogenic bacteria, leading to a new perspective on their symbiotic behavior.

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Abbreviations

atoSC + :

genetic locus encoding the AtoS, AtoC proteins

Az:

antizyme

C48/80:

compound 48/80

cPHB:

complexed poly-(R)-3-hydroxybutyrate

E. coli :

Escherichia coli

GI:

gastrointestinal

HI:

histamine

HK:

histidine kinase

ODC:

ornithine decarboxylase

PHB:

poly-(R)-3-hydroxybutyrate

RR:

response regulator

SCFA:

short-chain fatty acid

TCS:

two-component system

References

  • CA Akdis K Blaser (2003) ArticleTitleHistamine in the immune regulation of allergic inflammation J Allergy Clin Immun 112 15–22 Occurrence Handle12847474 Occurrence Handle10.1067/mai.2003.1585 Occurrence Handle1:CAS:528:DC%2BD3sXlvVGru7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • FR Blattner G Plunkett SuffixIII CA Bloch NT Perna V Burland M Riley J Collado-Vides JD Glasner CK Rode GF Mayhew J Gregor NW Davis HA Kirkpatrick MA Goeden DJ Rose B Mau Y Shao (1997) ArticleTitleThe complete genome sequence of Escherichia coli K-12 Science 277 1453–1474 Occurrence Handle9278503 Occurrence Handle10.1126/science.277.5331.1453 Occurrence Handle1:CAS:528:DyaK2sXlvVGnu78%3D

    Article  PubMed  CAS  Google Scholar 

  • ES Canellakis AA Paterakis SC Huang CA Panagiotidis DA Kyriakidis (1993) ArticleTitleIdentification, cloning, and nucleotide sequencing of the ornithine decarboxylase antizyme gene of Escherichia coli Proc Natl Acad Sci USA 90 7129–7133 Occurrence Handle8346225 Occurrence Handle10.1073/pnas.90.15.7129 Occurrence Handle1:CAS:528:DyaK3sXms1ekt74%3D

    Article  PubMed  CAS  Google Scholar 

  • JH Crosa CT Walsh (2002) ArticleTitleGenetics and assembly line enzymology of siderophore biosynthesis in bacteria Microbiol Mol Biol Rev 66 223–249 Occurrence Handle12040125 Occurrence Handle10.1128/MMBR.66.2.223-249.2002 Occurrence Handle1:CAS:528:DC%2BD38XltFSltr0%3D

    Article  PubMed  CAS  Google Scholar 

  • M Ennis G Atkinson FL Pearce (1980) ArticleTitleInhibition of histamine release induced by compound 48/80 and peptide 401 in the presence and absence of calcium. Implications for the mode of action of anti-allergic compounds Agents Actions 10 222–228 Occurrence Handle6157320 Occurrence Handle10.1007/BF02025939 Occurrence Handle1:CAS:528:DyaL3cXkvVyms70%3D

    Article  PubMed  CAS  Google Scholar 

  • PS Filippou EE Lioliou CA Panagiotidis CM Athanassopoulos T Garnelis D Papaioannou DA Kyriakidis (2007) ArticleTitleEffect of polyamines and synthetic polyamine-analogues on the expression of antizyme (AtoC) and its regulatory genes BMC Biochem 8 1–15 Occurrence Handle17224065 Occurrence Handle10.1186/1471-2091-8-1 Occurrence Handle1:CAS:528:DC%2BD2sXhvFCntL8%3D

    Article  PubMed  CAS  Google Scholar 

  • AI Grigoroudis CA Panagiotidis EE Lioliou M Vlassi DA Kyriakidis (2007) ArticleTitleMutagenesis and 3D-modeling studies of the AtoS–AtoC system: altering the N-terminal AtoC domain mediates differential activities on phosphorylation, ATPase and DNA-binding in Escherichia coli Biochim Biophys Acta 1770 1248–1258 Occurrence Handle17537579 Occurrence Handle1:CAS:528:DC%2BD2sXnsFymsLc%3D

    PubMed  CAS  Google Scholar 

  • F Guarner JR Malagelada (2003) ArticleTitleGut flora in health and disease Lancet 361 512–519 Occurrence Handle12583961 Occurrence Handle10.1016/S0140-6736(03)12489-0

    Article  PubMed  Google Scholar 

  • A Haldimann BL Wanner (2001) ArticleTitleConditional-replication, integration, excision and retrieval plasmid-host systems for gene structure-function studies of bacteria J Bacteriol 183 6384–6393 Occurrence Handle11591683 Occurrence Handle10.1128/JB.183.21.6384-6393.2001 Occurrence Handle1:CAS:528:DC%2BD3MXnsl2gsr0%3D

    Article  PubMed  CAS  Google Scholar 

  • JA Hoch TJ Silhavy (Eds) (1995) Two-component signal transduction American Society for Microbiology Washington, DC

    Google Scholar 

  • Y Hori Y Nihei Y Kurokawa A Kuramasu Y Makabe-Kobayashi T Terui H Doi S Satomi E Sakurai A Nagy T Watanabe H Ohtsu (2002) ArticleTitleAccelerated clearance of Escherichia coli in experimental peritonitis of histamine-deficient mice J Immunol 169 1978–1983 Occurrence Handle12165523 Occurrence Handle1:CAS:528:DC%2BD38XmtFejsb8%3D

    PubMed  CAS  Google Scholar 

  • K Igarashi K Kashiwagi (2000) ArticleTitlePolyamines: mysterious modulators of cellular functions Biochem Biophys Res Commun 271 559–564 Occurrence Handle10814501 Occurrence Handle10.1006/bbrc.2000.2601 Occurrence Handle1:CAS:528:DC%2BD3cXjt1SjsrY%3D

    Article  PubMed  CAS  Google Scholar 

  • LS Jenkins WD Nunn (1987) ArticleTitleRegulation of the ato operon by the atoC gene in Escherichia coli J Bacteriol 169 2096–2102 Occurrence Handle2883171 Occurrence Handle1:CAS:528:DyaL2sXksFejurk%3D

    PubMed  CAS  Google Scholar 

  • M Jules C Buchrieser (2007) ArticleTitle Legionella pneumophila adaptation to intracellular life and the host response: clues from genomics and transcriptomics FEMS Lett 581 2829–2838 Occurrence Handle1:CAS:528:DC%2BD2sXmtlWitLs%3D

    CAS  Google Scholar 

  • S Kakavas E Zampeli K Papamichael B Delitheos E Tiligada (2006) ArticleTitleThe mast cell pathway to inflammation and homeostasis: pharmacological insights Anti-Inflamm Anti-Allergy Agents Med Chem 5 323–334 Occurrence Handle1:CAS:528:DC%2BD28XhtFegurrE

    CAS  Google Scholar 

  • T Katsu M Shibata Y Fujita (1985) ArticleTitleDication and trication which can increase the permeability of Escherichia coli outer membrane Biochim Biophys Acta 818 61–66 Occurrence Handle2410026 Occurrence Handle10.1016/0005-2736(85)90138-5 Occurrence Handle1:CAS:528:DyaL2MXltlynsrs%3D

    Article  PubMed  CAS  Google Scholar 

  • DA Kyriakidis JS Heller ES Canellakis (1978) ArticleTitleModulation of ornithine decarboxylase activity in Escherichia coli by positive and negative effectors Proc Natl Acad Sci USA 75 4699–4703 Occurrence Handle368795 Occurrence Handle10.1073/pnas.75.10.4699 Occurrence Handle1:CAS:528:DyaE1MXivFCj

    Article  PubMed  CAS  Google Scholar 

  • EE Lioliou DA Kyriakidis (2004) ArticleTitleThe role of bacterial antizyme: from an inhibitory protein to AtoC transcriptional regulator Microb Cell Fact 3 8–16 Occurrence Handle15200682 Occurrence Handle10.1186/1475-2859-3-8

    Article  PubMed  Google Scholar 

  • EE Lioliou EP Mimitou AI Grigoroudis CH Panagiotidis CA Panagiotidis DA Kyriakidis (2005) ArticleTitlePhosphorylation activity of the response regulator of the two-component signal transduction system AtoS–AtoC/Az in E. coli Biochim Biophys Acta 1725 257–268 Occurrence Handle16153782 Occurrence Handle1:CAS:528:DC%2BD2MXhtVKjsLfI

    PubMed  CAS  Google Scholar 

  • MÁ Medina JL Urdiales C Rodríguez-Caso FJ Ramírez F Sánchez-Jiménez (2003) ArticleTitleBiogenic amines and polyamines: similar biochemistry for different physiological missions and biomedical applications Crit Rev Biochem Mol Biol 38 23–59 Occurrence Handle12641342 Occurrence Handle10.1080/713609209 Occurrence Handle1:CAS:528:DC%2BD3sXisFakt7k%3D

    Article  PubMed  CAS  Google Scholar 

  • JH Miller (1992) A short course in bacterial genetics SeriesTitleCold Spring Harbor Laboratory Cold Spring Harbor New York

    Google Scholar 

  • I Novak A Falus (1997) ArticleTitleMolecular biology and role of histamine in physiological and pathological reactions: a review Acta Biol Hung 48 385–394 Occurrence Handle9847451 Occurrence Handle1:CAS:528:DyaK1MXjvFKru7k%3D

    PubMed  CAS  Google Scholar 

  • CA Panagiotidis S-C Huang ES Canellakis (1994) ArticleTitlePost-translational and transcriptional regulation of polyamine biosynthesis in Escherichia coli Int J Biochem 26 991–1001 Occurrence Handle8088419 Occurrence Handle10.1016/0020-711X(94)90070-1 Occurrence Handle1:CAS:528:DyaK2cXlsFejtr0%3D

    Article  PubMed  CAS  Google Scholar 

  • RN Reush R Huang LL Bramble (1995) ArticleTitlePoly-3-hydroxybutyrate/polyphosphate complexes form voltage-activated Ca2+ channels in the plasma membranes of Escherichia coli Biophys J 69 754–766 Occurrence Handle10.1016/S0006-3495(95)79958-1

    Article  Google Scholar 

  • S Tagushi A Maehara K Takase M Nakahara H Nakamura Y Doi (2001) ArticleTitleAnalysis of mutational effects of a polyhydroxybutyrate (PHB) polymerase on bacterial PHB accumulation using an in vivo assay system FEMS Microbiol Lett 198 65–71 Occurrence Handle10.1111/j.1574-6968.2001.tb10620.x

    Article  Google Scholar 

  • MC Theodorou CA Panagiotidis CH Panagiotidis AA Pantazaki DA Kyriakidis (2006) ArticleTitleInvolvement of the AtoS–AtoC signal transduction system in poly-(R)-3-hydroxybutyrate biosynthesis in Escherichia coli Biochim Biophys Acta 1760 896–906 Occurrence Handle16564134 Occurrence Handle1:CAS:528:DC%2BD28XltlKiu7w%3D

    PubMed  CAS  Google Scholar 

  • MC Theodorou EC Theodorou CA Panagiotidis DA Kyriakidis (2007) ArticleTitleSpermidine triggering effect to the signal transduction through the AtoS–AtoC/Az two component system in Escherichia coli Biochim Biophys Acta 1770 1104–1114 Occurrence Handle17475408 Occurrence Handle1:CAS:528:DC%2BD2sXnsFyms70%3D

    PubMed  CAS  Google Scholar 

  • E Tiligada V Miligkos A Delitheos (2002) ArticleTitleCross-talk between cellular stress, cell cycle and anticancer agents: mechanistic aspects Curr Med Chem – Anti-Cancer Agents 2 553–566 Occurrence Handle10.2174/1568011023353976 Occurrence Handle1:CAS:528:DC%2BD38Xksl2ju7g%3D

    Article  CAS  Google Scholar 

  • L Zhou X-H Lei BR Bochner BL Wanner (2003) ArticleTitlePhenotype microarray analysis of Escherichia coli K-12 mutants with deletions of all two-component systems J Bacteriol 185 4956–4972 Occurrence Handle12897016 Occurrence Handle10.1128/JB.185.16.4956-4972.2003 Occurrence Handle1:CAS:528:DC%2BD3sXmt1GjtrY%3D

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Biochemistry, Department of Chemistry, Aristotle University of Thessaloniki, Thessaloniki, Greece

    D. A. Kyriakidis, M. C. Theodorou & P. S. Filippou

  2. National Hellenic Research Foundation, Athens, Greece

    D. A. Kyriakidis

  3. Department of Pharmacology, Medical School, University of Athens, Athens, Greece

    K. D. Kyriakidis & E. Tiligada

Authors
  1. D. A. Kyriakidis
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  2. M. C. Theodorou
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  3. P. S. Filippou
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  4. K. D. Kyriakidis
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  5. E. Tiligada
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Authors’ address: Ekaterini Tiligada, PhD (Wales), Assistant Professor of Pharmacology, Department of Pharmacology, Medical School, University of Athens, M. Asias 75, GR-115 27 Athens, Greece

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Kyriakidis, D., Theodorou, M., Filippou, P. et al. Effect of histamine on the signal transduction of the AtoS–AtoC two component system and involvement in poly-(R)-3-hydroxybutyrate biosynthesis in Escherichia coli . Amino Acids 35, 45–52 (2008). https://doi.org/10.1007/s00726-007-0635-8

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  • DOI: https://doi.org/10.1007/s00726-007-0635-8

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