DOI: 10.1099/mic.0.29088-0. The arginine regulon of Escherichia coli: whole-system transcriptome analysis discovers new genes and provides an integrated view of arginine regulation

The arginine regulon of Escherichia coli: whole-system transcriptome analysis discovers new genes and provides an integrated view of arginine regulation

10.1099/mic.0.29088-0

Crossref journal-article

Microbiology Society

Microbiology (345)

Abstract

Analysis of the response to arginine of theEscherichia coliK-12 transcriptome by microarray hybridization and real-time quantitative PCR provides the first coherent quantitative picture of the ArgR-mediated repression of arginine biosynthesis and uptake genes. Transcriptional repression was shown to be the major control mechanism of the biosynthetic genes, leaving only limited room for additional transcriptional or post-transcriptional regulation. Theartgenes, encoding the specific arginine uptake system, are subject to ArgR-mediated repression, with strong repression ofartJ, encoding the periplasmic binding protein of the system. ThehisJQMPgenes of the histidine transporter (part of the lysine-arginine-ornithine uptake system) were discovered to be a part of the arginine regulon. Analysis of their control region with reporter gene fusions and electrophoretic mobility shift in the presence of pure ArgR repressor showed the involvement in repression of the ArgR protein and an ARG box 120 bp upstream ofhisJ. No repression of the genes of the third uptake system, arginine-ornithine, was observed. Finally, comparison of the time course of arginine repression of gene transcription with the evolution of the specific activities of the cognate enzymes showed that while full genetic repression was achieved 2 min after arginine addition, enzyme concentrations were diluted at the rate of cell division. This emphasizes the importance of feedback inhibition of the first enzymic step in the pathway in controlling the metabolic flow through biosynthesis in the period following the onset of repression.

Bibliography

Caldara, M., Charlier, D., & Cunin, R. (2006). The arginine regulon of Escherichia coli: whole-system transcriptome analysis discovers new genes and provides an integrated view of arginine regulation. Microbiology, 152(11), 3343â3354.

Authors 3

Marina Caldara (first)
Daniel Charlier (additional)
Raymond Cunin (additional)

References 51 Referenced 65

10.1074/jbc.M103732200 / J Biol Chem / A new yeast metabolon involving at least the two first enzymes of arginine biosynthesis: acetylglutamate synthase activity requires complex formation with acetylglutamate kinase by Abadjieva (2001)
10.1146/annurev.bi.55.070186.002145 / Annu Rev Biochem / Bacterial periplasmic transport systems: structure, mechanism, and evolution by Ames (1986)
{'key': 'R3', 'first-page': '1190', 'article-title': 'Derivations and genotypes of some mutant derivatives of Escherichia coli K-12', 'volume-title': 'Escherichia coli and Salmonella: Cellular and Molecular Biology', 'author': 'Bachmann', 'year': '1987'} / Escherichia coli and Salmonella: Cellular and Molecular Biology / Derivations and genotypes of some mutant derivatives of Escherichia coli K-12 by Bachmann (1987)
10.1111/j.2517-6161.1995.tb02031.x / J R Stat Soc Ser B / Controlling the false discovery rate: a practical and powerful approach to multiple testing by Benjamini (1995)
10.1128/JB.151.1.58-61.1982 / J Bacteriol / Transcription of regions within the divergent argECBH operon of Escherichia coli : evidence for lack of an attenuation mechanism by Beny (1982)
10.1021/bi00123a015 / Biochemistry / Quantifying the allosteric properties of Escherichia coli carbamyl phosphate synthetase: determination of thermodynamic linked-function parameters in an ordered kinetic mechanism by Braxton (1992)
{'key': 'R7', 'first-page': '145', 'article-title': 'Experimental manipulation and mathematical modelling of arginine biosynthesis in Escherichia coli', 'volume-title': 'Abstract in Systems Biology: From Molecules & Modelling to Cells', 'author': 'Caldara', 'year': '2005'} / Abstract in Systems Biology: From Molecules & Modelling to Cells / Experimental manipulation and mathematical modelling of arginine biosynthesis in Escherichia coli by Caldara (2005)
10.1006/jmbi.1999.3308 / J Mol Biol / Repression and activation of arginine transport genes in Escherichia coli K-12 by the ArgP protein by Celis (1999)
10.1128/JB.180.18.4828-4833.1998 / J Bacteriol / Phosphorylation of the periplasmic binding protein in two transport systems for arginine incorporation in Escherichia coli K-12 is unrelated to the function of the transport system by Celis (1998)
10.1128/JB.130.3.1244-1252.1977 / J Bacteriol / Independent regulation of transport and biosynthesis of arginine in Escherichia coli K-12 by Celis (1977a)
10.1128/JB.130.3.1234-1243.1977 / J Bacteriol / Properties of an Escherichia coli K-12 mutant defective in the transport of arginine and ornithine by Celis (1977b)
10.1128/JB.116.2.619-626.1973 / J Bacteriol / Mutant of Escherichia coli K-12 defective in the transport of basic amino acids by Celis (1973)
10.1042/bst0320310 / Biochem Soc Trans / Arginine regulation in Thermotoga neapolitana and Thermotoga maritima by Charlier (2004)
10.1128/ecosalplus.3.6.1.10 / EcoSal(), Section 3.6.1.10 / Biosynthesis of arginine and polyamines by Charlier (2004)
10.1016/0022-2836(92)90953-H / J Mol Biol / Arginine regulon of Escherichia coli K-12. A study of repressor-operator interactions and of in vitro binding affinities versus in vivo repression by Charlier (1992)
10.1093/nar/11.15.5007 / Nucleic Acids Res / Molecular basis for modulated regulation of gene expression in the arginine regulon of Escherichia coli K-12 by Cunin (1983)
10.1128/MMBR.50.3.314-352.1986 / Microbiol Rev / Biosynthesis and metabolism of arginine in bacteria by Cunin (1986)
10.1073/pnas.120163297 / Proc Natl Acad Sci U S A / One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products by Datsenko (2000)
10.1016/j.jmb.2003.12.024 / J Mol Biol / Purine and pyrimidine-specific repression of the Escherichia coli carAB operon are functionally and structurally coupled by Devroede (2004)
10.1093/nar/11.1.141 / Nucleic Acids Res / CAP and RNA polymerase interaction with lac promoter: binding stoichiometry and long range effects by Fried (1983)
10.1146/annurev.ge.13.120179.002141 / Annu Rev Genet / Stringent control in E. coli by Gallant (1979)
10.1186/gb-2004-5-10-r80 / Genome Biol / Bioconductor: open software development for computational biology and bioinformatics by Gentleman (2004)
10.1093/genetics/51.2.167 / Genetics / Topography of cotransducible arginine mutations in Escherichia coli K-12 by Glansdorff (1965)
10.1016/0005-2787(65)90016-X / Biochim Biophys Acta / Coordination of enzyme synthesis in the arginine pathway of Escherichia coli K-12 by Glansdorff (1965)
10.1093/biostatistics/4.2.249 / Biostatistics / Exploration, normalization, and summaries of high density oligonucleotide array probe level data by Irizarry (2003)
10.1128/JB.178.18.5447-5451.1996 / J Bacteriol / Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli : intracellular levels of four species of sigma under various growth conditions by Jishage (1996)
10.1128/JB.132.1.67-72.1977 / J Bacteriol / Regulation of argA operon expression in Escherichia coli K-12: cell-free synthesis of β -galactosidase under argA control by Kelker (1977)
10.1128/JB.184.11.2940-2950.2002 / J Bacteriol / ArgR-independent induction and ArgR-dependent superinduction of the astCADBE operon in Escherichia coli by Kiupakis (2002)
10.1128/JB.185.10.3139-3146.2003 / J Bacteriol / Transcription regulation coupling of the divergent argG and metY promoters in Escherichia coli K-12 by Krin (2003)
10.1128/JB.116.1.107-113.1973 / J Bacteriol / The HisP protein, a known histidine transport component in Salmonella typhimurium , is also an arginine transport component by Kustu (1973)
10.1128/JB.138.1.218-234.1979 / J Bacteriol / Nitrogen control of Salmonella typhimurium : co-regulation of synthesis of glutamine synthetase and amino acid transport systems by Kustu (1979)
10.1073/pnas.95.7.3495 / Proc Natl Acad Sci U S A / In vitro disassembly and reassembly of an ABC transporter, the histidine permease by Liu (1998)
10.1007/s00253-005-0308-z / Appl Microbiol Biotechnol / Pathways and regulation of bacterial arginine metabolism and perspectives for obtaining arginine overproducing strains by Lu (2006)
10.1016/S0022-2836(64)80200-X / J Mol Biol / Studies on the mechanism of repression or arginine biosynthesis in Escherichia coli . II. Dominance of repressibility in diploids by Maas (1964)
10.1186/gb-2001-2-4-research0013 / Genome Biol / Conservation of the binding site for the arginine repressor in all bacterial lineages by Makarova (2001)
10.1016/S0021-9258(17)40387-5 / J Biol Chem / N-Acetylglutamate synthase of Escherichia coli : purification, characterization, and molecular properties by Marvil (1977)
{'volume-title': 'Experiments in Molecular Genetics', 'year': '1972', 'author': 'Miller', 'key': 'R37'} / Experiments in Molecular Genetics by Miller (1972)
10.1128/JB.186.11.3539-3546.2004 / J Bacteriol / Evidence for an arginine exporter encoded by yggA (argO) that is regulated by the LysR-type transcriptional regulator ArgP in Escherichia coli by Nandineni (2004)
10.1016/S0022-2836(65)80226-1 / J Mol Biol / Control of the biosynthesis of carbamoyl phosphate in Escherichia coli by Piérard (1965)
10.1073/pnas.81.13.4134 / Proc Natl Acad Sci U S A / DNA sequence of the carA gene and the control region of carAB : tandem promoters, respectively controlled by arginine and the pyrimidines, regulate the synthesis of carbamoyl-phosphate synthetase in Escherichia coli K-12 by Piette (1984)
{'key': 'R41', 'first-page': '380', 'article-title': 'Sources of nitrogen and their utilization', 'volume-title': 'Escherichia coli and Salmonella: Cellular and Molecular Biology', 'author': 'Reitzer', 'year': '1996'} / Escherichia coli and Salmonella: Cellular and Molecular Biology / Sources of nitrogen and their utilization by Reitzer (1996)
10.1111/j.1432-1033.1989.tb21080.x / Eur J Biochem / Carbamoyl phosphate biosynthesis and partition in pyrimidine and arginine pathways of Escherichia coli . In situ properties of carbamoyl-phosphate synthase, ornithine transcarbamylase and aspartate transcarbamylase in permeabilized cells by Robin (1989)
10.1016/S0021-9258(18)62178-7 / J Biol Chem / Basic amino acid transport in Escherichia coli by Rosen (1971)
10.1128/JB.116.2.627-635.1973 / J Bacteriol / Basic amino acid transport in Escherichia coli : properties of canavanine-resistant mutants by Rosen (1973)
10.1006/jmbi.1999.2618 / J Mol Biol / A mutation that uncouples allosteric regulation of carbamyl phosphate synthetase in Drosophila by Simmons (1999)
10.1093/nar/26.16.3700 / Nucleic Acids Res / Genetic analysis of prokaryotic and eukaryotic DNA-binding proteins in Escherichia coli by Whipple (1998)
10.1128/JB.175.11.3687-3688.1993 / J Bacteriol / Physical map location of the new artPIQMJ genes of Escherichia coli , encoding a periplasmic arginine transport system by Wissenbach (1993)
10.1111/j.1365-2958.1995.mmi_17040675.x / Mol Microbiol / A third periplasmic transport system for l-arginine in Escherichia coli : molecular characterization of the artPIQMJ genes, arginine binding and transport by Wissenbach (1995)
10.1016/S0022-2836(02)01375-X / J Mol Biol / Regulation of arginine biosynthesis in the psychropiezophilic bacterium Moritella profunda : in vivo repressibility and in vitro repressor-operator contact probing by Xu (2003)
10.1128/JB.159.2.647-651.1984 / J Bacteriol / Positive control of expression of the argECBH gene cluster in vivo by 5′-diphosphate 3′-diphosphate by Zidwick (1984)
10.1073/pnas.97.26.14674 / Proc Natl Acad Sci U S A / Nitrogen regulatory protein C-controlled genes of Escherichia coli : scavenging as a defense against nitrogen limitation by Zimmer (2000)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 30, 2006, 2:52 p.m.)
Deposited	7 months, 3 weeks ago (Jan. 11, 2025, 1:47 p.m.)
Indexed	5 months, 1 week ago (March 19, 2025, 9:40 a.m.)
Issued	18 years, 10 months ago (Nov. 1, 2006)
Published	18 years, 10 months ago (Nov. 1, 2006)
Published Print	18 years, 10 months ago (Nov. 1, 2006)

Funders 0

None

BibTeX

@article{Caldara_2006, title={The arginine regulon of Escherichia coli: whole-system transcriptome analysis discovers new genes and provides an integrated view of arginine regulation}, volume={152}, ISSN={1465-2080}, url={http://dx.doi.org/10.1099/mic.0.29088-0}, DOI={10.1099/mic.0.29088-0}, number={11}, journal={Microbiology}, publisher={Microbiology Society}, author={Caldara, Marina and Charlier, Daniel and Cunin, Raymond}, year={2006}, month=nov, pages={3343–3354} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        3,
        19
      ]
    ],
    "date-time": "2025-03-19T13:40:17Z",
    "timestamp": 1742391617680,
    "version": "3.32.0"
  },
  "reference-count": 51,
  "publisher": "Microbiology Society",
  "issue": "11",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2006,
        11,
        1
      ]
    ]
  },
  "abstract": "<jats:p>Analysis of the response to arginine of the<jats:italic>Escherichia coli</jats:italic>K-12 transcriptome by microarray hybridization and real-time quantitative PCR provides the first coherent quantitative picture of the ArgR-mediated repression of arginine biosynthesis and uptake genes. Transcriptional repression was shown to be the major control mechanism of the biosynthetic genes, leaving only limited room for additional transcriptional or post-transcriptional regulation. The<jats:italic>art</jats:italic>genes, encoding the specific arginine uptake system, are subject to ArgR-mediated repression, with strong repression of<jats:italic>artJ</jats:italic>, encoding the periplasmic binding protein of the system. The<jats:italic>hisJQMP</jats:italic>genes of the histidine transporter (part of the lysine-arginine-ornithine uptake system) were discovered to be a part of the arginine regulon. Analysis of their control region with reporter gene fusions and electrophoretic mobility shift in the presence of pure ArgR repressor showed the involvement in repression of the ArgR protein and an ARG box 120\u2005bp upstream of<jats:italic>hisJ</jats:italic>. No repression of the genes of the third uptake system, arginine-ornithine, was observed. Finally, comparison of the time course of arginine repression of gene transcription with the evolution of the specific activities of the cognate enzymes showed that while full genetic repression was achieved 2\u2005min after arginine addition, enzyme concentrations were diluted at the rate of cell division. This emphasizes the importance of feedback inhibition of the first enzymic step in the pathway in controlling the metabolic flow through biosynthesis in the period following the onset of repression.</jats:p>",
  "DOI": "10.1099/mic.0.29088-0",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        30
      ]
    ],
    "date-time": "2006-10-30T19:52:12Z",
    "timestamp": 1162237932000
  },
  "page": "3343-3354",
  "source": "Crossref",
  "is-referenced-by-count": 65,
  "title": "The arginine regulon of Escherichia coli: whole-system transcriptome analysis discovers new genes and provides an integrated view of arginine regulation",
  "prefix": "10.1099",
  "volume": "152",
  "author": [
    {
      "given": "Marina",
      "family": "Caldara",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Laboratorium voor Erfelijkheidsleer en Microbiologie, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium"
        }
      ]
    },
    {
      "given": "Daniel",
      "family": "Charlier",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratorium voor Erfelijkheidsleer en Microbiologie, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium"
        }
      ]
    },
    {
      "given": "Raymond",
      "family": "Cunin",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Laboratorium voor Erfelijkheidsleer en Microbiologie, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium"
        }
      ]
    }
  ],
  "member": "345",
  "reference": [
    {
      "key": "R1",
      "doi-asserted-by": "crossref",
      "first-page": "42869",
      "DOI": "10.1074/jbc.M103732200",
      "article-title": "A new yeast metabolon involving at least the two first enzymes of arginine biosynthesis: acetylglutamate synthase activity requires complex formation with acetylglutamate kinase",
      "volume": "276",
      "author": "Abadjieva",
      "year": "2001",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R2",
      "doi-asserted-by": "crossref",
      "first-page": "397",
      "DOI": "10.1146/annurev.bi.55.070186.002145",
      "article-title": "Bacterial periplasmic transport systems: structure, mechanism, and evolution",
      "volume": "55",
      "author": "Ames",
      "year": "1986",
      "journal-title": "Annu Rev Biochem"
    },
    {
      "key": "R3",
      "first-page": "1190",
      "article-title": "Derivations and genotypes of some mutant derivatives of Escherichia coli K-12",
      "volume-title": "Escherichia coli and Salmonella: Cellular and Molecular Biology",
      "author": "Bachmann",
      "year": "1987"
    },
    {
      "key": "R4",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1111/j.2517-6161.1995.tb02031.x",
      "article-title": "Controlling the false discovery rate: a practical and powerful approach to multiple testing",
      "volume": "57",
      "author": "Benjamini",
      "year": "1995",
      "journal-title": "J R Stat Soc Ser B"
    },
    {
      "key": "R5",
      "doi-asserted-by": "crossref",
      "first-page": "58",
      "DOI": "10.1128/JB.151.1.58-61.1982",
      "article-title": "Transcription of regions within the divergent argECBH operon of Escherichia coli : evidence for lack of an attenuation mechanism",
      "volume": "151",
      "author": "Beny",
      "year": "1982",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R6",
      "doi-asserted-by": "crossref",
      "first-page": "2309",
      "DOI": "10.1021/bi00123a015",
      "article-title": "Quantifying the allosteric properties of Escherichia coli carbamyl phosphate synthetase: determination of thermodynamic linked-function parameters in an ordered kinetic mechanism",
      "volume": "31",
      "author": "Braxton",
      "year": "1992",
      "journal-title": "Biochemistry"
    },
    {
      "key": "R7",
      "first-page": "145",
      "article-title": "Experimental manipulation and mathematical modelling of arginine biosynthesis in Escherichia coli",
      "volume-title": "Abstract in Systems Biology: From Molecules & Modelling to Cells",
      "author": "Caldara",
      "year": "2005"
    },
    {
      "key": "R10",
      "doi-asserted-by": "crossref",
      "first-page": "1087",
      "DOI": "10.1006/jmbi.1999.3308",
      "article-title": "Repression and activation of arginine transport genes in Escherichia coli K-12 by the ArgP protein",
      "volume": "294",
      "author": "Celis",
      "year": "1999",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R12",
      "doi-asserted-by": "crossref",
      "first-page": "4828",
      "DOI": "10.1128/JB.180.18.4828-4833.1998",
      "article-title": "Phosphorylation of the periplasmic binding protein in two transport systems for arginine incorporation in Escherichia coli K-12 is unrelated to the function of the transport system",
      "volume": "180",
      "author": "Celis",
      "year": "1998",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R8",
      "doi-asserted-by": "crossref",
      "first-page": "1244",
      "DOI": "10.1128/JB.130.3.1244-1252.1977",
      "article-title": "Independent regulation of transport and biosynthesis of arginine in Escherichia coli K-12",
      "volume": "130",
      "author": "Celis",
      "year": "1977a",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R9",
      "doi-asserted-by": "crossref",
      "first-page": "1234",
      "DOI": "10.1128/JB.130.3.1234-1243.1977",
      "article-title": "Properties of an Escherichia coli K-12 mutant defective in the transport of arginine and ornithine",
      "volume": "130",
      "author": "Celis",
      "year": "1977b",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R11",
      "doi-asserted-by": "crossref",
      "first-page": "619",
      "DOI": "10.1128/JB.116.2.619-626.1973",
      "article-title": "Mutant of Escherichia coli K-12 defective in the transport of basic amino acids",
      "volume": "116",
      "author": "Celis",
      "year": "1973",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R13",
      "doi-asserted-by": "crossref",
      "first-page": "310",
      "DOI": "10.1042/bst0320310",
      "article-title": "Arginine regulation in Thermotoga neapolitana and Thermotoga maritima",
      "volume": "32",
      "author": "Charlier",
      "year": "2004",
      "journal-title": "Biochem Soc Trans"
    },
    {
      "key": "R14",
      "doi-asserted-by": "crossref",
      "DOI": "10.1128/ecosalplus.3.6.1.10",
      "article-title": "Biosynthesis of arginine and polyamines",
      "volume-title": "EcoSal(), Section 3.6.1.10",
      "author": "Charlier",
      "year": "2004"
    },
    {
      "key": "R15",
      "doi-asserted-by": "crossref",
      "first-page": "367",
      "DOI": "10.1016/0022-2836(92)90953-H",
      "article-title": "Arginine regulon of Escherichia coli K-12. A study of repressor-operator interactions and of in vitro binding affinities versus in vivo repression",
      "volume": "226",
      "author": "Charlier",
      "year": "1992",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R16",
      "doi-asserted-by": "crossref",
      "first-page": "5007",
      "DOI": "10.1093/nar/11.15.5007",
      "article-title": "Molecular basis for modulated regulation of gene expression in the arginine regulon of Escherichia coli K-12",
      "volume": "11",
      "author": "Cunin",
      "year": "1983",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "R17",
      "doi-asserted-by": "crossref",
      "first-page": "314",
      "DOI": "10.1128/MMBR.50.3.314-352.1986",
      "article-title": "Biosynthesis and metabolism of arginine in bacteria",
      "volume": "50",
      "author": "Cunin",
      "year": "1986",
      "journal-title": "Microbiol Rev"
    },
    {
      "key": "R18",
      "doi-asserted-by": "crossref",
      "first-page": "6640",
      "DOI": "10.1073/pnas.120163297",
      "article-title": "One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products",
      "volume": "97",
      "author": "Datsenko",
      "year": "2000",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R19",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1016/j.jmb.2003.12.024",
      "article-title": "Purine and pyrimidine-specific repression of the Escherichia coli carAB operon are functionally and structurally coupled",
      "volume": "336",
      "author": "Devroede",
      "year": "2004",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R20",
      "doi-asserted-by": "crossref",
      "first-page": "141",
      "DOI": "10.1093/nar/11.1.141",
      "article-title": "CAP and RNA polymerase interaction with lac promoter: binding stoichiometry and long range effects",
      "volume": "11",
      "author": "Fried",
      "year": "1983",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "R21",
      "doi-asserted-by": "crossref",
      "first-page": "393",
      "DOI": "10.1146/annurev.ge.13.120179.002141",
      "article-title": "Stringent control in E. coli",
      "volume": "13",
      "author": "Gallant",
      "year": "1979",
      "journal-title": "Annu Rev Genet"
    },
    {
      "key": "R22",
      "doi-asserted-by": "crossref",
      "first-page": "R80",
      "DOI": "10.1186/gb-2004-5-10-r80",
      "article-title": "Bioconductor: open software development for computational biology and bioinformatics",
      "volume": "5",
      "author": "Gentleman",
      "year": "2004",
      "journal-title": "Genome Biol"
    },
    {
      "key": "R23",
      "doi-asserted-by": "crossref",
      "first-page": "167",
      "DOI": "10.1093/genetics/51.2.167",
      "article-title": "Topography of cotransducible arginine mutations in Escherichia coli K-12",
      "volume": "51",
      "author": "Glansdorff",
      "year": "1965",
      "journal-title": "Genetics"
    },
    {
      "key": "R24",
      "doi-asserted-by": "crossref",
      "first-page": "308",
      "DOI": "10.1016/0005-2787(65)90016-X",
      "article-title": "Coordination of enzyme synthesis in the arginine pathway of Escherichia coli K-12",
      "volume": "108",
      "author": "Glansdorff",
      "year": "1965",
      "journal-title": "Biochim Biophys Acta"
    },
    {
      "key": "R25",
      "doi-asserted-by": "crossref",
      "first-page": "249",
      "DOI": "10.1093/biostatistics/4.2.249",
      "article-title": "Exploration, normalization, and summaries of high density oligonucleotide array probe level data",
      "volume": "4",
      "author": "Irizarry",
      "year": "2003",
      "journal-title": "Biostatistics"
    },
    {
      "key": "R26",
      "doi-asserted-by": "crossref",
      "first-page": "5447",
      "DOI": "10.1128/JB.178.18.5447-5451.1996",
      "article-title": "Regulation of RNA polymerase sigma subunit synthesis in Escherichia coli : intracellular levels of four species of sigma under various growth conditions",
      "volume": "178",
      "author": "Jishage",
      "year": "1996",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R27",
      "doi-asserted-by": "crossref",
      "first-page": "67",
      "DOI": "10.1128/JB.132.1.67-72.1977",
      "article-title": "Regulation of argA operon expression in Escherichia coli K-12: cell-free synthesis of \u03b2 -galactosidase under argA control",
      "volume": "132",
      "author": "Kelker",
      "year": "1977",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R28",
      "doi-asserted-by": "crossref",
      "first-page": "2940",
      "DOI": "10.1128/JB.184.11.2940-2950.2002",
      "article-title": "ArgR-independent induction and ArgR-dependent superinduction of the astCADBE operon in Escherichia coli",
      "volume": "184",
      "author": "Kiupakis",
      "year": "2002",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R29",
      "doi-asserted-by": "crossref",
      "first-page": "3139",
      "DOI": "10.1128/JB.185.10.3139-3146.2003",
      "article-title": "Transcription regulation coupling of the divergent argG and metY promoters in Escherichia coli K-12",
      "volume": "185",
      "author": "Krin",
      "year": "2003",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R30",
      "doi-asserted-by": "crossref",
      "first-page": "107",
      "DOI": "10.1128/JB.116.1.107-113.1973",
      "article-title": "The HisP protein, a known histidine transport component in Salmonella typhimurium , is also an arginine transport component",
      "volume": "116",
      "author": "Kustu",
      "year": "1973",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R31",
      "doi-asserted-by": "crossref",
      "first-page": "218",
      "DOI": "10.1128/JB.138.1.218-234.1979",
      "article-title": "Nitrogen control of Salmonella typhimurium : co-regulation of synthesis of glutamine synthetase and amino acid transport systems",
      "volume": "138",
      "author": "Kustu",
      "year": "1979",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R32",
      "doi-asserted-by": "crossref",
      "first-page": "3495",
      "DOI": "10.1073/pnas.95.7.3495",
      "article-title": "In vitro disassembly and reassembly of an ABC transporter, the histidine permease",
      "volume": "95",
      "author": "Liu",
      "year": "1998",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R33",
      "doi-asserted-by": "crossref",
      "first-page": "261",
      "DOI": "10.1007/s00253-005-0308-z",
      "article-title": "Pathways and regulation of bacterial arginine metabolism and perspectives for obtaining arginine overproducing strains",
      "volume": "70",
      "author": "Lu",
      "year": "2006",
      "journal-title": "Appl Microbiol Biotechnol"
    },
    {
      "key": "R34",
      "doi-asserted-by": "crossref",
      "first-page": "365",
      "DOI": "10.1016/S0022-2836(64)80200-X",
      "article-title": "Studies on the mechanism of repression or arginine biosynthesis in Escherichia coli . II. Dominance of repressibility in diploids",
      "volume": "8",
      "author": "Maas",
      "year": "1964",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R35",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1186/gb-2001-2-4-research0013",
      "article-title": "Conservation of the binding site for the arginine repressor in all bacterial lineages",
      "volume": "2",
      "author": "Makarova",
      "year": "2001",
      "journal-title": "Genome Biol"
    },
    {
      "key": "R36",
      "doi-asserted-by": "crossref",
      "first-page": "3295",
      "DOI": "10.1016/S0021-9258(17)40387-5",
      "article-title": "N-Acetylglutamate synthase of Escherichia coli : purification, characterization, and molecular properties",
      "volume": "252",
      "author": "Marvil",
      "year": "1977",
      "journal-title": "J Biol Chem"
    },
    {
      "volume-title": "Experiments in Molecular Genetics",
      "year": "1972",
      "author": "Miller",
      "key": "R37"
    },
    {
      "key": "R38",
      "doi-asserted-by": "crossref",
      "first-page": "3539",
      "DOI": "10.1128/JB.186.11.3539-3546.2004",
      "article-title": "Evidence for an arginine exporter encoded by yggA (argO) that is regulated by the LysR-type transcriptional regulator ArgP in Escherichia coli",
      "volume": "186",
      "author": "Nandineni",
      "year": "2004",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R39",
      "doi-asserted-by": "crossref",
      "first-page": "23",
      "DOI": "10.1016/S0022-2836(65)80226-1",
      "article-title": "Control of the biosynthesis of carbamoyl phosphate in Escherichia coli",
      "volume": "14",
      "author": "Pie\u0301rard",
      "year": "1965",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R40",
      "doi-asserted-by": "crossref",
      "first-page": "4134",
      "DOI": "10.1073/pnas.81.13.4134",
      "article-title": "DNA sequence of the carA gene and the control region of carAB : tandem promoters, respectively controlled by arginine and the pyrimidines, regulate the synthesis of carbamoyl-phosphate synthetase in Escherichia coli K-12",
      "volume": "81",
      "author": "Piette",
      "year": "1984",
      "journal-title": "Proc Natl Acad Sci U S A"
    },
    {
      "key": "R41",
      "first-page": "380",
      "article-title": "Sources of nitrogen and their utilization",
      "volume-title": "Escherichia coli and Salmonella: Cellular and Molecular Biology",
      "author": "Reitzer",
      "year": "1996"
    },
    {
      "key": "R42",
      "doi-asserted-by": "crossref",
      "first-page": "519",
      "DOI": "10.1111/j.1432-1033.1989.tb21080.x",
      "article-title": "Carbamoyl phosphate biosynthesis and partition in pyrimidine and arginine pathways of Escherichia coli . In situ properties of carbamoyl-phosphate synthase, ornithine transcarbamylase and aspartate transcarbamylase in permeabilized cells",
      "volume": "183",
      "author": "Robin",
      "year": "1989",
      "journal-title": "Eur J Biochem"
    },
    {
      "key": "R43",
      "doi-asserted-by": "crossref",
      "first-page": "3653",
      "DOI": "10.1016/S0021-9258(18)62178-7",
      "article-title": "Basic amino acid transport in Escherichia coli",
      "volume": "246",
      "author": "Rosen",
      "year": "1971",
      "journal-title": "J Biol Chem"
    },
    {
      "key": "R44",
      "doi-asserted-by": "crossref",
      "first-page": "627",
      "DOI": "10.1128/JB.116.2.627-635.1973",
      "article-title": "Basic amino acid transport in Escherichia coli : properties of canavanine-resistant mutants",
      "volume": "116",
      "author": "Rosen",
      "year": "1973",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R45",
      "doi-asserted-by": "crossref",
      "first-page": "277",
      "DOI": "10.1006/jmbi.1999.2618",
      "article-title": "A mutation that uncouples allosteric regulation of carbamyl phosphate synthetase in Drosophila",
      "volume": "287",
      "author": "Simmons",
      "year": "1999",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R46",
      "doi-asserted-by": "crossref",
      "first-page": "3700",
      "DOI": "10.1093/nar/26.16.3700",
      "article-title": "Genetic analysis of prokaryotic and eukaryotic DNA-binding proteins in Escherichia coli",
      "volume": "26",
      "author": "Whipple",
      "year": "1998",
      "journal-title": "Nucleic Acids Res"
    },
    {
      "key": "R47",
      "doi-asserted-by": "crossref",
      "first-page": "3687",
      "DOI": "10.1128/JB.175.11.3687-3688.1993",
      "article-title": "Physical map location of the new artPIQMJ genes of Escherichia coli , encoding a periplasmic arginine transport system",
      "volume": "175",
      "author": "Wissenbach",
      "year": "1993",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R48",
      "doi-asserted-by": "crossref",
      "first-page": "675",
      "DOI": "10.1111/j.1365-2958.1995.mmi_17040675.x",
      "article-title": "A third periplasmic transport system for l-arginine in Escherichia coli : molecular characterization of the artPIQMJ genes, arginine binding and transport",
      "volume": "17",
      "author": "Wissenbach",
      "year": "1995",
      "journal-title": "Mol Microbiol"
    },
    {
      "key": "R49",
      "doi-asserted-by": "crossref",
      "first-page": "353",
      "DOI": "10.1016/S0022-2836(02)01375-X",
      "article-title": "Regulation of arginine biosynthesis in the psychropiezophilic bacterium Moritella profunda : in vivo repressibility and in vitro repressor-operator contact probing",
      "volume": "326",
      "author": "Xu",
      "year": "2003",
      "journal-title": "J Mol Biol"
    },
    {
      "key": "R50",
      "doi-asserted-by": "crossref",
      "first-page": "647",
      "DOI": "10.1128/JB.159.2.647-651.1984",
      "article-title": "Positive control of expression of the argECBH gene cluster in vivo by 5\u2032-diphosphate 3\u2032-diphosphate",
      "volume": "159",
      "author": "Zidwick",
      "year": "1984",
      "journal-title": "J Bacteriol"
    },
    {
      "key": "R51",
      "doi-asserted-by": "crossref",
      "first-page": "14674",
      "DOI": "10.1073/pnas.97.26.14674",
      "article-title": "Nitrogen regulatory protein C-controlled genes of Escherichia coli : scavenging as a defense against nitrogen limitation",
      "volume": "97",
      "author": "Zimmer",
      "year": "2000",
      "journal-title": "Proc Natl Acad Sci U S A"
    }
  ],
  "container-title": "Microbiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://www.microbiologyresearch.org/content/journal/micro/10.1099/mic.0.29088-0?crawler=true",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        1,
        11
      ]
    ],
    "date-time": "2025-01-11T18:47:58Z",
    "timestamp": 1736621278000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.microbiologyresearch.org/content/journal/micro/10.1099/mic.0.29088-0"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2006,
        11,
        1
      ]
    ]
  },
  "references-count": 51,
  "journal-issue": {
    "issue": "11",
    "published-print": {
      "date-parts": [
        [
          2006,
          11,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1099/mic.0.29088-0",
  "relation": {},
  "ISSN": [
    "1350-0872",
    "1465-2080"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2006,
        11,
        1
      ]
    ]
  }
}