DOI: 10.1128/jb.181.5.1623-1629.1999. Roles of <i>Pseudomonas aeruginosa las</i> and <i>rhl</i> Quorum-Sensing Systems in Control of Twitching Motility

Roles of Pseudomonas aeruginosa las and rhl Quorum-Sensing Systems in Control of Twitching Motility

10.1128/jb.181.5.1623-1629.1999

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACT Pseudomonas aeruginosa is a ubiquitous environmental bacterium and an important human pathogen. The production of several virulence factors by P. aeruginosa is controlled through two quorum-sensing systems, las and rhl . We have obtained evidence that both the las and rhl quorum-sensing systems are also required for type 4 pilus-dependent twitching motility and infection by the pilus-specific phage D3112 c ts. Mutants which lack the ability to synthesize PAI-1, PAI-2, or both autoinducers were significantly or greatly impaired in twitching motility and in susceptibility to D3112 c ts. Twitching motility and phage susceptibility in the autoinducer-deficient mutants were partially restored by exposure to exogenous PAI-1 and PAI-2. Both twitching motility and infection by pilus-specific phage are believed to be dependent on the extension and retraction of polar type 4 pili. Western blot analysis of whole-cell lysates and enzyme-linked immunosorbent assays of intact cells were used to measure the amounts of pilin on the cell surfaces of las and rhl mutants relative to that of the wild type. It appears that PAI-2 plays a crucial role in twitching motility and phage infection by affecting the export and assembly of surface type 4 pili. The ability of P. aeruginosa cells to adhere to human bronchial epithelial cells was also found to be dependent on the rhl quorum-sensing system. Microscopic analysis of twitching motility indicated that mutants which were unable to synthesize PAI-1 were defective in the maintenance of cellular monolayers and migrating packs of cells. Thus, PAI-1 appears to have an essential role in maintaining cell-cell spacing and associations required for effective twitching motility.

Bibliography

Glessner, A., Smith, R. S., Iglewski, B. H., & Robinson, J. B. (1999). Roles of Pseudomonas aeruginosa las and rhl Quorum-Sensing Systems in Control of Twitching Motility. Journal of Bacteriology, 181(5), 1623â1629.

Authors 4

Alex Glessner (first)
Roger S. Smith (additional)
Barbara H. Iglewski (additional)
Jayne B. Robinson (additional)

References 48 Referenced 165

Alm R. S. Mattick J. S. Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa.Gene19219978998 (10.1016/S0378-1119(96)00805-0) / Gene / Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa by Alm R. S. (1997)
Bradley D. E. A function of Pseudomonas aeruginosa PAO pili: twitching motility.Can. J. Microbiol.261980146154 (10.1139/m80-022) / Can. J. Microbiol. / A function of Pseudomonas aeruginosa PAO pili: twitching motility by Bradley D. E. (1980)
10.1128/jb.177.24.7155-7163.1995
Chapon-Herve V. Akrim M. Latifi A. Williams P. Lazdunski A. Bally M. Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa.Mol. Microbiol.24199711691178 (10.1046/j.1365-2958.1997.4271794.x) / Mol. Microbiol. / Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa by Chapon-Herve V. (1997)
10.1128/jb.175.18.5934-5944.1993
Darzins A. Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus.Mol. Microbiol.111994137153 (10.1111/j.1365-2958.1994.tb00296.x) / Mol. Microbiol. / Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus by Darzins A. (1994)
10.1128/jb.171.7.3909-3916.1989
10.1126/science.280.5361.295
10.1128/iai.56.6.1641-1646.1988
Eberl L. Winson M. K. Sternberg C. Stewart G. S. Christiansen G. Chhabra S. R. Bycroft B. Williams P. Molin S. Givskov M. Involvement of N -acyl-l-homoserine lactone autoinducers in controlling the multicellular behavior of Serratia liquefaciens.Mol. Microbiol.201996127136 (10.1111/j.1365-2958.1996.tb02495.x) / Mol. Microbiol. / Involvement of N -acyl-l-homoserine lactone autoinducers in controlling the multicellular behavior of Serratia liquefaciens by Eberl L. (1996)
10.1128/iai.61.4.1180-1184.1993
10.1016/S0378-1119(97)00116-9
Hazelbauer G. L. Berg H. C. Matsumura P. Bacterial motility and signal transduction.Cell7319931522 (10.1016/0092-8674(93)90156-K) / Cell / Bacterial motility and signal transduction by Hazelbauer G. L. (1993)
Henrichson J. Twitching motility.Annu. Rev. Microbiol.3719838193 (10.1146/annurev.mi.37.100183.000501) / Annu. Rev. Microbiol. / Twitching motility by Henrichson J. (1983)
Hobbs M. Collie E. S. Free P. D. Livingston S. P. Mattick J. S. PilS and PilR, a two component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa.Mol. Microbiol.71993669682 (10.1111/j.1365-2958.1993.tb01158.x) / Mol. Microbiol. / PilS and PilR, a two component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa by Hobbs M. (1993)
Joklik W. K. Willett H. P. Amos D. B. Wilfert C. M. Pseudomonas Zinsser microbiology 20th ed. Joklik W. K. 1992 576 583 Appleton and Lange Norwalk Conn
Koomey M. Prepilin-like molecules in type-4 pilus biogenesis: minor subunits, chaperones or mediators of organelle translocation.Trends Microbiol.31995409411 (10.1016/S0966-842X(00)88989-1) / Trends Microbiol. / Prepilin-like molecules in type-4 pilus biogenesis: minor subunits, chaperones or mediators of organelle translocation by Koomey M. (1995)
10.1128/jb.177.24.7019-7025.1995
Latifi A. Winson M. K. Foglino M. Bycroft B. W. Stewart G. S. A. B. Lazdunski A. Williams P. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1.Mol. Microbiol.171995333343 (10.1111/j.1365-2958.1995.mmi_17020333.x) / Mol. Microbiol. / Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1 by Latifi A. (1995)
Latifi A. Foglino M. Tanaka K. Williams P. Lazdunski A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR to expression of the stationary-phase sigma factor RpoS.Mol. Microbiol.21199611371146 (10.1046/j.1365-2958.1996.00063.x) / Mol. Microbiol. / A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR to expression of the stationary-phase sigma factor RpoS by Latifi A. (1996)
Lory S. Pseudomonas and other nonfermenting bacilli Microbiology. Davis B. D. Dulbecco R. Eisen H. N. Ginsberg H. S. 1990 595 600 Lippincott Philadelphia Pa
Lory S. Lu H.-M. Pepe J. Common steps in extracellular protein secretion and biogenesis of pili in Pseudomonas aeruginosa Molecular biology of Pseudomonas. Nakazawa T. 1996 417 426 American Society for Microbiology Washington D.C
Lu H.-M. Motley S. T. Lory S. Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion.Mol. Microbiol.251997247259 (10.1046/j.1365-2958.1997.4561818.x) / Mol. Microbiol. / Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion by Lu H.-M. (1997)
Masduki A. Nakamura J. Olga T. Umezaki R. Kato J. Ohtake H. Isolation and characterization of chemotaxis mutants and genes of Pseudomonas aeruginosa.J. Bacteriol.1771995333343 (10.1128/jb.177.4.948-952.1995) / J. Bacteriol. / Isolation and characterization of chemotaxis mutants and genes of Pseudomonas aeruginosa by Masduki A. (1995)
Mattick J. S. Whitchurch C. B. Alm R. A. The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa—a review.Gene1791996147155 (10.1016/S0378-1119(96)00441-6) / Gene / The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa—a review by Mattick J. S. (1996)
Mattick J. S. Whitchurch C. B. Martin P. R. Alm R. A. Hobbs M. Regulatory pathways affecting the biogenesis and function of type 4 fimbriae in Pseudomonas aeruginosa abstr. XXI. VI International Congress on Pseudomonas; Molecular Biology and Biotechnology 1997
McBride M. J. Weinberg R. A. Zusman D. R. “Frizzy” aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria.Proc. Natl. Acad. Sci. USA861989424428 (10.1073/pnas.86.2.424) / Proc. Natl. Acad. Sci. USA / “Frizzy” aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria by McBride M. J. (1989)
McLean R. J. C. Whiteley M. Stickler D. J. Fuqua W. C. Evidence of autoinducer activity in naturally occurring biofilms.FEMS Microbiol. Lett.1541997259263 (10.1111/j.1574-6968.1997.tb12653.x) / FEMS Microbiol. Lett. / Evidence of autoinducer activity in naturally occurring biofilms by McLean R. J. C. (1997)
Nasser W. Bouillant M. L. Salmond G. Reverchon S. Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N -acyl-homoserine lactone signal molecules.Mol. Microbiol.29199813911405 (10.1046/j.1365-2958.1998.01022.x) / Mol. Microbiol. / Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N -acyl-homoserine lactone signal molecules by Nasser W. (1998)
Ochsner U. A. Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199564246428 (10.1073/pnas.92.14.6424) / Proc. Natl. Acad. Sci. USA / Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa by Ochsner U. A. (1995)
10.1046/j.1365-2958.1998.01062.x
10.1128/jb.179.18.5756-5767.1997
Pearson J. P. Passador L. Iglewski B. H. Greenberg E. P. A second N -acylhomoserine lactone signal produced by Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199714901494 (10.1073/pnas.92.5.1490) / Proc. Natl. Acad. Sci. USA / A second N -acylhomoserine lactone signal produced by Pseudomonas aeruginosa by Pearson J. P. (1997)
Pemberton J. M. F116: a DNA bacteriophage specific for the pili of Pseudomonas aeruginosa strain PAO.Virology551973558560 (10.1016/0042-6822(73)90203-1) / Virology / F116: a DNA bacteriophage specific for the pili of Pseudomonas aeruginosa strain PAO by Pemberton J. M. (1973)
10.1128/jb.179.10.3127-3132.1997
Pesci E. C. Iglewski B. H. Quorum sensing in Pseudomonas aeruginosa Cell-cell signaling in bacteria. Dunny G. M. Winans S. C. 1999 147 155 ASM Press Washington D.C
Pollack M. Pseudomonas aeruginosa Principles and practices of infectious diseases. Mandell G. L. Douglas R. G. Bennett J. E. 1990 1673 1691 Churchill Livingstone Edinburgh Scotland
10.1126/science.7604262
Rehmat S. Shapiro J. A. Insertion and replication of the Pseudomonas aeruginosa mutator phage D3112.Mol. Gen. Genet.1921983416423 (10.1007/BF00392184) / Mol. Gen. Genet. / Insertion and replication of the Pseudomonas aeruginosa mutator phage D3112 by Rehmat S. (1983)
10.1128/jb.172.4.1899-1904.1990
10.1128/jb.178.4.1134-1140.1996
10.1128/jb.177.3.654-659.1995
Smith J. J. Travis S. Greenberg E. P. Welsh M. J. Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid.Cell851996229236 (10.1016/S0092-8674(00)81099-5) / Cell / Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid by Smith J. J. (1996)
10.1128/jb.173.3.1175-1180.1991
Toder D. S. Gambello M. J. Iglewski B. H. Pseudomonas aeruginosa LasA; a second elastase gene under transcriptional control of lasR.Mol. Microbiol.5199120032010 (10.1111/j.1365-2958.1991.tb00822.x) / Mol. Microbiol. / Pseudomonas aeruginosa LasA; a second elastase gene under transcriptional control of lasR by Toder D. S. (1991)
Tommassen J. Filloux A. Bally M. Murgier M. Lazdunski Andree Protein secretion in Pseudomonas aeruginosa.FEMS Microbiol. Rev.10319927390 (10.1111/j.1574-6968.1992.tb05824.x) / FEMS Microbiol. Rev. / Protein secretion in Pseudomonas aeruginosa by Tommassen J. (1992)
Winson M. K. Camara M. Latifi A. Foglino M. Chhabra S. R. Daykin M. Bally M. Chapon V. Salmond G. P. C. Bycroft B. W. Lazdunski A. Stewart G. S. A. B. Williams P. Multiple N -acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199594279431 (10.1073/pnas.92.20.9427) / Proc. Natl. Acad. Sci. USA / Multiple N -acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa by Winson M. K. (1995)
Wong W. Y. Campbell A. P. McInnes C. Sykes B. D. Paranchych W. Irvin R. T. Hodges R. S. Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa PAK and KB7.Biochemistry3419951296312972 (10.1021/bi00040a006) / Biochemistry / Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa PAK and KB7 by Wong W. Y. (1995)

Dates

Type	When
Created	5 years, 8 months ago (Dec. 31, 2019, 11:46 a.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:51 p.m.)
Indexed	1 week, 6 days ago (Aug. 19, 2025, 6 a.m.)
Issued	26 years, 6 months ago (March 1, 1999)
Published	26 years, 6 months ago (March 1, 1999)
Published Print	26 years, 6 months ago (March 1, 1999)

Funders 0

None

BibTeX

@article{Glessner_1999, title={Roles of Pseudomonas aeruginosa las and rhl Quorum-Sensing Systems in Control of Twitching Motility}, volume={181}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.181.5.1623-1629.1999}, DOI={10.1128/jb.181.5.1623-1629.1999}, number={5}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Glessner, Alex and Smith, Roger S. and Iglewski, Barbara H. and Robinson, Jayne B.}, year={1999}, month=mar, pages={1623–1629} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        19
      ]
    ],
    "date-time": "2025-08-19T10:00:30Z",
    "timestamp": 1755597630544
  },
  "reference-count": 48,
  "publisher": "American Society for Microbiology",
  "issue": "5",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1999,
            3,
            1
          ]
        ],
        "date-time": "1999-03-01T00:00:00Z",
        "timestamp": 920246400000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.asm.org/non-commercial-tdm-license"
    }
  ],
  "content-domain": {
    "domain": [
      "journals.asm.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1999,
        3
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            <jats:italic>Pseudomonas aeruginosa</jats:italic>\n            is a ubiquitous environmental bacterium and an important human pathogen. The production of several virulence factors by\n            <jats:italic>P. aeruginosa</jats:italic>\n            is controlled through two quorum-sensing systems,\n            <jats:italic>las</jats:italic>\n            and\n            <jats:italic>rhl</jats:italic>\n            . We have obtained evidence that both the\n            <jats:italic>las</jats:italic>\n            and\n            <jats:italic>rhl</jats:italic>\n            quorum-sensing systems are also required for type 4 pilus-dependent twitching motility and infection by the pilus-specific phage D3112\n            <jats:italic>c</jats:italic>\n            ts. Mutants which lack the ability to synthesize PAI-1, PAI-2, or both autoinducers were significantly or greatly impaired in twitching motility and in susceptibility to D3112\n            <jats:italic>c</jats:italic>\n            ts. Twitching motility and phage susceptibility in the autoinducer-deficient mutants were partially restored by exposure to exogenous PAI-1 and PAI-2. Both twitching motility and infection by pilus-specific phage are believed to be dependent on the extension and retraction of polar type 4 pili. Western blot analysis of whole-cell lysates and enzyme-linked immunosorbent assays of intact cells were used to measure the amounts of pilin on the cell surfaces of\n            <jats:italic>las</jats:italic>\n            and\n            <jats:italic>rhl</jats:italic>\n            mutants relative to that of the wild type. It appears that PAI-2 plays a crucial role in twitching motility and phage infection by affecting the export and assembly of surface type 4 pili. The ability of\n            <jats:italic>P. aeruginosa</jats:italic>\n            cells to adhere to human bronchial epithelial cells was also found to be dependent on the\n            <jats:italic>rhl</jats:italic>\n            quorum-sensing system. Microscopic analysis of twitching motility indicated that mutants which were unable to synthesize PAI-1 were defective in the maintenance of cellular monolayers and migrating packs of cells. Thus, PAI-1 appears to have an essential role in maintaining cell-cell spacing and associations required for effective twitching motility.\n          </jats:p>",
  "DOI": "10.1128/jb.181.5.1623-1629.1999",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2019,
        12,
        31
      ]
    ],
    "date-time": "2019-12-31T16:46:12Z",
    "timestamp": 1577810772000
  },
  "page": "1623-1629",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 165,
  "title": "Roles of\n            <i>Pseudomonas aeruginosa las</i>\n            and\n            <i>rhl</i>\n            Quorum-Sensing Systems in Control of Twitching Motility",
  "prefix": "10.1128",
  "volume": "181",
  "author": [
    {
      "given": "Alex",
      "family": "Glessner",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Biology, University of Dayton, Dayton, Ohio 45469,1 and"
        }
      ]
    },
    {
      "given": "Roger S.",
      "family": "Smith",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 2-->Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, New York 146422"
        }
      ]
    },
    {
      "given": "Barbara H.",
      "family": "Iglewski",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 2-->Department of Microbiology and Immunology, University of Rochester School of Medicine and Dentistry, Rochester, New York 146422"
        }
      ]
    },
    {
      "given": "Jayne B.",
      "family": "Robinson",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Biology, University of Dayton, Dayton, Ohio 45469,1 and"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "crossref",
      "first-page": "89",
      "DOI": "10.1016/S0378-1119(96)00805-0",
      "article-title": "Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa",
      "volume": "192",
      "author": "Alm R. S.",
      "year": "1997",
      "unstructured": "Alm R. S. Mattick J. S. Genes involved in the biogenesis and function of type-4 fimbriae in Pseudomonas aeruginosa.Gene19219978998",
      "journal-title": "Gene"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "crossref",
      "first-page": "146",
      "DOI": "10.1139/m80-022",
      "article-title": "A function of Pseudomonas aeruginosa PAO pili: twitching motility",
      "volume": "26",
      "author": "Bradley D. E.",
      "year": "1980",
      "unstructured": "Bradley D. E. A function of Pseudomonas aeruginosa PAO pili: twitching motility.Can. J. Microbiol.261980146154",
      "journal-title": "Can. J. Microbiol."
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.177.24.7155-7163.1995"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "crossref",
      "first-page": "1169",
      "DOI": "10.1046/j.1365-2958.1997.4271794.x",
      "article-title": "Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa",
      "volume": "24",
      "author": "Chapon-Herve V.",
      "year": "1997",
      "unstructured": "Chapon-Herve V. Akrim M. Latifi A. Williams P. Lazdunski A. Bally M. Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa.Mol. Microbiol.24199711691178",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.175.18.5934-5944.1993"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "crossref",
      "first-page": "137",
      "DOI": "10.1111/j.1365-2958.1994.tb00296.x",
      "article-title": "Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus",
      "volume": "11",
      "author": "Darzins A.",
      "year": "1994",
      "unstructured": "Darzins A. Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus.Mol. Microbiol.111994137153",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.171.7.3909-3916.1989"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.280.5361.295"
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.56.6.1641-1646.1988"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "crossref",
      "first-page": "127",
      "DOI": "10.1111/j.1365-2958.1996.tb02495.x",
      "article-title": "Involvement of N -acyl-l-homoserine lactone autoinducers in controlling the multicellular behavior of Serratia liquefaciens",
      "volume": "20",
      "author": "Eberl L.",
      "year": "1996",
      "unstructured": "Eberl L. Winson M. K. Sternberg C. Stewart G. S. Christiansen G. Chhabra S. R. Bycroft B. Williams P. Molin S. Givskov M. Involvement of N -acyl-l-homoserine lactone autoinducers in controlling the multicellular behavior of Serratia liquefaciens.Mol. Microbiol.201996127136",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.61.4.1180-1184.1993"
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0378-1119(97)00116-9"
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1016/0092-8674(93)90156-K",
      "article-title": "Bacterial motility and signal transduction",
      "volume": "73",
      "author": "Hazelbauer G. L.",
      "year": "1993",
      "unstructured": "Hazelbauer G. L. Berg H. C. Matsumura P. Bacterial motility and signal transduction.Cell7319931522",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1146/annurev.mi.37.100183.000501",
      "article-title": "Twitching motility",
      "volume": "37",
      "author": "Henrichson J.",
      "year": "1983",
      "unstructured": "Henrichson J. Twitching motility.Annu. Rev. Microbiol.3719838193",
      "journal-title": "Annu. Rev. Microbiol."
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "crossref",
      "first-page": "669",
      "DOI": "10.1111/j.1365-2958.1993.tb01158.x",
      "article-title": "PilS and PilR, a two component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa",
      "volume": "7",
      "author": "Hobbs M.",
      "year": "1993",
      "unstructured": "Hobbs M. Collie E. S. Free P. D. Livingston S. P. Mattick J. S. PilS and PilR, a two component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa.Mol. Microbiol.71993669682",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_17_2",
      "unstructured": "Joklik\nW. K.\nWillett\nH. P.\nAmos\nD. B.\nWilfert\nC. M. Pseudomonas Zinsser microbiology\n20th ed.\nJoklik\nW. K.\n1992\n576\n583\nAppleton and Lange\nNorwalk Conn"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "crossref",
      "first-page": "409",
      "DOI": "10.1016/S0966-842X(00)88989-1",
      "article-title": "Prepilin-like molecules in type-4 pilus biogenesis: minor subunits, chaperones or mediators of organelle translocation",
      "volume": "3",
      "author": "Koomey M.",
      "year": "1995",
      "unstructured": "Koomey M. Prepilin-like molecules in type-4 pilus biogenesis: minor subunits, chaperones or mediators of organelle translocation.Trends Microbiol.31995409411",
      "journal-title": "Trends Microbiol."
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.177.24.7019-7025.1995"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "crossref",
      "first-page": "333",
      "DOI": "10.1111/j.1365-2958.1995.mmi_17020333.x",
      "article-title": "Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1",
      "volume": "17",
      "author": "Latifi A.",
      "year": "1995",
      "unstructured": "Latifi A. Winson M. K. Foglino M. Bycroft B. W. Stewart G. S. A. B. Lazdunski A. Williams P. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1.Mol. Microbiol.171995333343",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "crossref",
      "first-page": "1137",
      "DOI": "10.1046/j.1365-2958.1996.00063.x",
      "article-title": "A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR to expression of the stationary-phase sigma factor RpoS",
      "volume": "21",
      "author": "Latifi A.",
      "year": "1996",
      "unstructured": "Latifi A. Foglino M. Tanaka K. Williams P. Lazdunski A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR to expression of the stationary-phase sigma factor RpoS.Mol. Microbiol.21199611371146",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_22_2",
      "unstructured": "Lory\nS. Pseudomonas and other nonfermenting bacilli\nMicrobiology.\nDavis\nB. D.\nDulbecco\nR.\nEisen\nH. N.\nGinsberg\nH. S.\n1990\n595\n600\nLippincott\nPhiladelphia Pa"
    },
    {
      "key": "e_1_3_2_23_2",
      "unstructured": "Lory\nS.\nLu\nH.-M.\nPepe\nJ.\nCommon steps in extracellular protein secretion and biogenesis of pili in Pseudomonas aeruginosa Molecular biology of Pseudomonas.\nNakazawa\nT.\n1996\n417\n426\nAmerican Society for Microbiology\nWashington D.C"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "crossref",
      "first-page": "247",
      "DOI": "10.1046/j.1365-2958.1997.4561818.x",
      "article-title": "Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion",
      "volume": "25",
      "author": "Lu H.-M.",
      "year": "1997",
      "unstructured": "Lu H.-M. Motley S. T. Lory S. Interactions of the components of the general secretion pathway: role of Pseudomonas aeruginosa type IV pilin subunits in complex formation and extracellular protein secretion.Mol. Microbiol.251997247259",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "crossref",
      "first-page": "333",
      "DOI": "10.1128/jb.177.4.948-952.1995",
      "article-title": "Isolation and characterization of chemotaxis mutants and genes of Pseudomonas aeruginosa",
      "volume": "177",
      "author": "Masduki A.",
      "year": "1995",
      "unstructured": "Masduki A. Nakamura J. Olga T. Umezaki R. Kato J. Ohtake H. Isolation and characterization of chemotaxis mutants and genes of Pseudomonas aeruginosa.J. Bacteriol.1771995333343",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "crossref",
      "first-page": "147",
      "DOI": "10.1016/S0378-1119(96)00441-6",
      "article-title": "The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa\u2014a review",
      "volume": "179",
      "author": "Mattick J. S.",
      "year": "1996",
      "unstructured": "Mattick J. S. Whitchurch C. B. Alm R. A. The molecular genetics of type-4 fimbriae in Pseudomonas aeruginosa\u2014a review.Gene1791996147155",
      "journal-title": "Gene"
    },
    {
      "key": "e_1_3_2_27_2",
      "unstructured": "Mattick\nJ. S.\nWhitchurch\nC. B.\nMartin\nP. R.\nAlm\nR. A.\nHobbs\nM.\nRegulatory pathways affecting the biogenesis and function of type 4 fimbriae in Pseudomonas aeruginosa abstr. XXI. VI International Congress on Pseudomonas; Molecular Biology and Biotechnology\n1997"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "crossref",
      "first-page": "424",
      "DOI": "10.1073/pnas.86.2.424",
      "article-title": "\u201cFrizzy\u201d aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria",
      "volume": "86",
      "author": "McBride M. J.",
      "year": "1989",
      "unstructured": "McBride M. J. Weinberg R. A. Zusman D. R. \u201cFrizzy\u201d aggregation genes of the gliding bacterium Myxococcus xanthus show sequence similarities to the chemotaxis genes of enteric bacteria.Proc. Natl. Acad. Sci. USA861989424428",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "crossref",
      "first-page": "259",
      "DOI": "10.1111/j.1574-6968.1997.tb12653.x",
      "article-title": "Evidence of autoinducer activity in naturally occurring biofilms",
      "volume": "154",
      "author": "McLean R. J. C.",
      "year": "1997",
      "unstructured": "McLean R. J. C. Whiteley M. Stickler D. J. Fuqua W. C. Evidence of autoinducer activity in naturally occurring biofilms.FEMS Microbiol. Lett.1541997259263",
      "journal-title": "FEMS Microbiol. Lett."
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "crossref",
      "first-page": "1391",
      "DOI": "10.1046/j.1365-2958.1998.01022.x",
      "article-title": "Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N -acyl-homoserine lactone signal molecules",
      "volume": "29",
      "author": "Nasser W.",
      "year": "1998",
      "unstructured": "Nasser W. Bouillant M. L. Salmond G. Reverchon S. Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N -acyl-homoserine lactone signal molecules.Mol. Microbiol.29199813911405",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "crossref",
      "first-page": "6424",
      "DOI": "10.1073/pnas.92.14.6424",
      "article-title": "Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa",
      "volume": "92",
      "author": "Ochsner U. A.",
      "year": "1995",
      "unstructured": "Ochsner U. A. Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199564246428",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1998.01062.x"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.18.5756-5767.1997"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "crossref",
      "first-page": "1490",
      "DOI": "10.1073/pnas.92.5.1490",
      "article-title": "A second N -acylhomoserine lactone signal produced by Pseudomonas aeruginosa",
      "volume": "92",
      "author": "Pearson J. P.",
      "year": "1997",
      "unstructured": "Pearson J. P. Passador L. Iglewski B. H. Greenberg E. P. A second N -acylhomoserine lactone signal produced by Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199714901494",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "crossref",
      "first-page": "558",
      "DOI": "10.1016/0042-6822(73)90203-1",
      "article-title": "F116: a DNA bacteriophage specific for the pili of Pseudomonas aeruginosa strain PAO",
      "volume": "55",
      "author": "Pemberton J. M.",
      "year": "1973",
      "unstructured": "Pemberton J. M. F116: a DNA bacteriophage specific for the pili of Pseudomonas aeruginosa strain PAO.Virology551973558560",
      "journal-title": "Virology"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.10.3127-3132.1997"
    },
    {
      "key": "e_1_3_2_37_2",
      "unstructured": "Pesci\nE. C.\nIglewski\nB. H.\nQuorum sensing in Pseudomonas aeruginosa Cell-cell signaling in bacteria.\nDunny\nG. M.\nWinans\nS. C.\n1999\n147\n155\nASM Press\nWashington D.C"
    },
    {
      "key": "e_1_3_2_38_2",
      "unstructured": "Pollack\nM. Pseudomonas aeruginosa Principles and practices of infectious diseases.\nMandell\nG. L.\nDouglas\nR. G.\nBennett\nJ. E.\n1990\n1673\n1691\nChurchill Livingstone\nEdinburgh Scotland"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7604262"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "crossref",
      "first-page": "416",
      "DOI": "10.1007/BF00392184",
      "article-title": "Insertion and replication of the Pseudomonas aeruginosa mutator phage D3112",
      "volume": "192",
      "author": "Rehmat S.",
      "year": "1983",
      "unstructured": "Rehmat S. Shapiro J. A. Insertion and replication of the Pseudomonas aeruginosa mutator phage D3112.Mol. Gen. Genet.1921983416423",
      "journal-title": "Mol. Gen. Genet."
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.172.4.1899-1904.1990"
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.178.4.1134-1140.1996"
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.177.3.654-659.1995"
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "crossref",
      "first-page": "229",
      "DOI": "10.1016/S0092-8674(00)81099-5",
      "article-title": "Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid",
      "volume": "85",
      "author": "Smith J. J.",
      "year": "1996",
      "unstructured": "Smith J. J. Travis S. Greenberg E. P. Welsh M. J. Cystic fibrosis airway epithelia fail to kill bacteria because of abnormal airway surface fluid.Cell851996229236",
      "journal-title": "Cell"
    },
    {
      "key": "e_1_3_2_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.173.3.1175-1180.1991"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "crossref",
      "first-page": "2003",
      "DOI": "10.1111/j.1365-2958.1991.tb00822.x",
      "article-title": "Pseudomonas aeruginosa LasA; a second elastase gene under transcriptional control of lasR",
      "volume": "5",
      "author": "Toder D. S.",
      "year": "1991",
      "unstructured": "Toder D. S. Gambello M. J. Iglewski B. H. Pseudomonas aeruginosa LasA; a second elastase gene under transcriptional control of lasR.Mol. Microbiol.5199120032010",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1111/j.1574-6968.1992.tb05824.x",
      "article-title": "Protein secretion in Pseudomonas aeruginosa",
      "volume": "103",
      "author": "Tommassen J.",
      "year": "1992",
      "unstructured": "Tommassen J. Filloux A. Bally M. Murgier M. Lazdunski Andree Protein secretion in Pseudomonas aeruginosa.FEMS Microbiol. Rev.10319927390",
      "journal-title": "FEMS Microbiol. Rev."
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "crossref",
      "first-page": "9427",
      "DOI": "10.1073/pnas.92.20.9427",
      "article-title": "Multiple N -acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa",
      "volume": "92",
      "author": "Winson M. K.",
      "year": "1995",
      "unstructured": "Winson M. K. Camara M. Latifi A. Foglino M. Chhabra S. R. Daykin M. Bally M. Chapon V. Salmond G. P. C. Bycroft B. W. Lazdunski A. Stewart G. S. A. B. Williams P. Multiple N -acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa.Proc. Natl. Acad. Sci. USA92199594279431",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_49_2",
      "doi-asserted-by": "crossref",
      "first-page": "12963",
      "DOI": "10.1021/bi00040a006",
      "article-title": "Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa PAK and KB7",
      "volume": "34",
      "author": "Wong W. Y.",
      "year": "1995",
      "unstructured": "Wong W. Y. Campbell A. P. McInnes C. Sykes B. D. Paranchych W. Irvin R. T. Hodges R. S. Structure-function analysis of the adherence-binding domain on the pilin of Pseudomonas aeruginosa PAK and KB7.Biochemistry3419951296312972",
      "journal-title": "Biochemistry"
    }
  ],
  "container-title": "Journal of Bacteriology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JB.181.5.1623-1629.1999",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JB.181.5.1623-1629.1999",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2021,
        7,
        29
      ]
    ],
    "date-time": "2021-07-29T17:51:25Z",
    "timestamp": 1627581085000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/JB.181.5.1623-1629.1999"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        3
      ]
    ]
  },
  "references-count": 48,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          1999,
          3
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/JB.181.5.1623-1629.1999"
  ],
  "URL": "http://dx.doi.org/10.1128/JB.181.5.1623-1629.1999",
  "relation": {},
  "ISSN": [
    "0021-9193",
    "1098-5530"
  ],
  "subject": [],
  "container-title-short": "J Bacteriol",
  "published": {
    "date-parts": [
      [
        1999,
        3
      ]
    ]
  },
  "assertion": [
    {
      "value": "1998-08-27",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1998-12-17",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2020-12-20",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}