DOI: 10.1128/iai.67.2.914-920.1999. Regulation of ExoS Production and Secretion by <i>Pseudomonas aeruginosa</i> in Response to Tissue Culture Conditions

Regulation of ExoS Production and Secretion by Pseudomonas aeruginosa in Response to Tissue Culture Conditions

10.1128/iai.67.2.914-920.1999

Crossref journal-article

American Society for Microbiology

Infection and Immunity (235)

Abstract

ABSTRACT This study was initiated to characterize the regulation and secretion of ExoS by Pseudomonas aeruginosa during contact with eukaryotic cells. The production of ExoS was monitored by a sensitive ADP-ribosyltransferase activity assay, and specific activities were calculated for supernatant and cell-associated fractions. Time course analysis indicated that ExoS was produced after a lag period, suggesting that induction of the regulon is necessary for the expression of detectable amounts of enzyme activity. Under tissue culture growth conditions, ExoS was induced when P. aeruginosa was in contact with Chinese hamster ovary (CHO) cells or after growth in tissue culture medium with serum. The serum induction of ExoS appeared to result in generalized type III secretion, while induction by contact with CHO cells appeared to result in polarized type III secretion. Mutants in the type III secretory system that express a null phenotype for ExoS production in bacteriological medium produced but did not secrete the enzyme when P. aeruginosa was grown under inducing conditions in tissue culture medium. These results suggest that both induction and secretion of ExoS may differ when the bacteria are exposed to different growth environments. The putative type III translocation proteins and secretion apparatus of P. aeruginosa were required for translocation of bacterial factors that mediate changes in CHO cell morphology during infection.

Bibliography

Vallis, A. J., Yahr, T. L., Barbieri, J. T., & Frank, D. W. (1999). Regulation of ExoS Production and Secretion by Pseudomonas aeruginosa in Response to Tissue Culture Conditions. Infection and Immunity, 67(2), 914â920.

Authors 4

Amy J. Vallis (first)
Timothy L. Yahr (additional)
Joseph T. Barbieri (additional)
Dara W. Frank (additional)

References 41 Referenced 119

10.1042/bst0230605
10.1128/iai.24.3.837-842.1979
10.1002/j.1460-2075.1996.tb00904.x
Coburn J. Pseudomonas aeruginosa exoenzyme S.Curr. Top. Microbiol. Immunol.1751992133143 / Curr. Top. Microbiol. Immunol. / Pseudomonas aeruginosa exoenzyme S by Coburn J. (1992)
10.1128/iai.57.3.996-998.1989
10.1128/iai.59.11.4259-4262.1991
10.1016/S0021-9258(18)38137-7
10.1016/S0021-9258(18)81894-4
10.1046/j.1365-2958.1997.2731623.x
10.1046/j.1365-2958.1997.6251991.x
10.1128/iai.62.2.554-563.1994
10.1046/j.1365-2958.1997.5411905.x
10.1046/j.1365-2958.1998.00994.x
10.1073/pnas.90.6.2320
10.1074/jbc.273.13.7332
10.1128/jb.179.5.1646-1654.1997
10.1046/j.1365-2958.1996.5251051.x
10.1073/pnas.75.7.3211
10.1128/iai.65.8.3304-3309.1997
Kudoh I. Wiener-Kronish J. P. Hashimoto S. Pittet J. Frank D. W. Exoproduct secretions of Pseudomonas aeruginosa strains influence severity of alveolar epithelial injury.Am. J. Physiol.2671994L551L556 / Am. J. Physiol. / Exoproduct secretions of Pseudomonas aeruginosa strains influence severity of alveolar epithelial injury by Kudoh I. (1994)
10.1128/iai.63.1.1-8.1995
10.1038/227680a0
10.1016/S0966-842X(97)01029-9
10.1128/IAI.66.6.2607-2613.1998
10.3201/eid0204.960403
10.1002/j.1460-2075.1994.tb06863.x
10.1128/iai.45.2.470-474.1984
10.1128/iai.65.1.248-256.1997
10.1111/j.1365-2958.1995.mmi_18010135.x
10.1126/science.273.5279.1231
Rooney P. J. Frank D. W. Isolation and characterization of insertional mutations affecting exoenzyme S production in Pseudomonas aeruginosa abstr. D-188 Abstracts of the 94th General Meeting of the American Society for Microbiology 1994. 1994 129 American Society for Microbiology Washington D.C
10.1128/iai.59.12.4562-4569.1991
10.1111/j.1365-2958.1992.tb01558.x
10.1111/j.1365-2958.1994.tb02191.x
10.1046/j.1365-2958.1997.6281995.x
Thompson M. R. Bjorn M. J. Sokol P. A. Lile J. D. Iglewski B. H. Exoenzyme S: an ADP-ribosyltransferase produced by Pseudomonas aeruginosa Novel ADP-ribosylations of regulatory enzymes and proteins. Smulson M. Sugimura T. 1980 425 433 Elsevier Amsterdam The Netherlands
10.1016/S0021-9258(18)65874-0
10.1128/jb.178.5.1412-1419.1996
10.1046/j.1365-2958.1996.01554.x
10.1128/jb.179.22.7165-7168.1997
10.1128/iai.63.10.4024-4028.1995

Dates

Type	When
Created	5 years, 7 months ago (Dec. 31, 2019, 10:33 a.m.)
Deposited	3 years, 5 months ago (March 4, 2022, 7:50 p.m.)
Indexed	4 weeks, 1 day ago (July 27, 2025, 3:17 a.m.)
Issued	26 years, 6 months ago (Feb. 1, 1999)
Published	26 years, 6 months ago (Feb. 1, 1999)
Published Print	26 years, 6 months ago (Feb. 1, 1999)

Funders 0

None

BibTeX

@article{Vallis_1999, title={Regulation of ExoS Production and Secretion by Pseudomonas aeruginosa in Response to Tissue Culture Conditions}, volume={67}, ISSN={1098-5522}, url={http://dx.doi.org/10.1128/iai.67.2.914-920.1999}, DOI={10.1128/iai.67.2.914-920.1999}, number={2}, journal={Infection and Immunity}, publisher={American Society for Microbiology}, author={Vallis, Amy J. and Yahr, Timothy L. and Barbieri, Joseph T. and Frank, Dara W.}, editor={Orndorff, P. E.}, year={1999}, month=feb, pages={914–920} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        7,
        27
      ]
    ],
    "date-time": "2025-07-27T07:17:42Z",
    "timestamp": 1753600662062
  },
  "reference-count": 41,
  "publisher": "American Society for Microbiology",
  "issue": "2",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1999,
            2,
            1
          ]
        ],
        "date-time": "1999-02-01T00:00:00Z",
        "timestamp": 917827200000
      },
      "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,
        2
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            This study was initiated to characterize the regulation and secretion of ExoS by\n            <jats:italic>Pseudomonas aeruginosa</jats:italic>\n            during contact with eukaryotic cells. The production of ExoS was monitored by a sensitive ADP-ribosyltransferase activity assay, and specific activities were calculated for supernatant and cell-associated fractions. Time course analysis indicated that ExoS was produced after a lag period, suggesting that induction of the regulon is necessary for the expression of detectable amounts of enzyme activity. Under tissue culture growth conditions, ExoS was induced when\n            <jats:italic>P. aeruginosa</jats:italic>\n            was in contact with Chinese hamster ovary (CHO) cells or after growth in tissue culture medium with serum. The serum induction of ExoS appeared to result in generalized type III secretion, while induction by contact with CHO cells appeared to result in polarized type III secretion. Mutants in the type III secretory system that express a null phenotype for ExoS production in bacteriological medium produced but did not secrete the enzyme when\n            <jats:italic>P. aeruginosa</jats:italic>\n            was grown under inducing conditions in tissue culture medium. These results suggest that both induction and secretion of ExoS may differ when the bacteria are exposed to different growth environments. The putative type III translocation proteins and secretion apparatus of\n            <jats:italic>P. aeruginosa</jats:italic>\n            were required for translocation of bacterial factors that mediate changes in CHO cell morphology during infection.\n          </jats:p>",
  "DOI": "10.1128/iai.67.2.914-920.1999",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2019,
        12,
        31
      ]
    ],
    "date-time": "2019-12-31T15:33:05Z",
    "timestamp": 1577806385000
  },
  "page": "914-920",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 119,
  "title": "Regulation of ExoS Production and Secretion by\n            <i>Pseudomonas aeruginosa</i>\n            in Response to Tissue Culture Conditions",
  "prefix": "10.1128",
  "volume": "67",
  "author": [
    {
      "given": "Amy J.",
      "family": "Vallis",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology, Medical College of Wisconsin, Milwaukee, Wisconsin 53226"
        }
      ]
    },
    {
      "given": "Timothy L.",
      "family": "Yahr",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology, Medical College of Wisconsin, Milwaukee, Wisconsin 53226"
        }
      ]
    },
    {
      "given": "Joseph T.",
      "family": "Barbieri",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology, Medical College of Wisconsin, Milwaukee, Wisconsin 53226"
        }
      ]
    },
    {
      "given": "Dara W.",
      "family": "Frank",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology, Medical College of Wisconsin, Milwaukee, Wisconsin 53226"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bst0230605"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.24.3.837-842.1979"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1996.tb00904.x"
    },
    {
      "key": "e_1_3_2_5_2",
      "first-page": "133",
      "article-title": "Pseudomonas aeruginosa exoenzyme S",
      "volume": "175",
      "author": "Coburn J.",
      "year": "1992",
      "unstructured": "Coburn J. Pseudomonas aeruginosa exoenzyme S.Curr. Top. Microbiol. Immunol.1751992133143",
      "journal-title": "Curr. Top. Microbiol. Immunol."
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.57.3.996-998.1989"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.59.11.4259-4262.1991"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)38137-7"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)81894-4"
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.2731623.x"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.6251991.x"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.2.554-563.1994"
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.5411905.x"
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1998.00994.x"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.90.6.2320"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.273.13.7332"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.5.1646-1654.1997"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1996.5251051.x"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.75.7.3211"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.8.3304-3309.1997"
    },
    {
      "key": "e_1_3_2_21_2",
      "first-page": "L551",
      "article-title": "Exoproduct secretions of Pseudomonas aeruginosa strains influence severity of alveolar epithelial injury",
      "volume": "267",
      "author": "Kudoh I.",
      "year": "1994",
      "unstructured": "Kudoh I. Wiener-Kronish J. P. Hashimoto S. Pittet J. Frank D. W. Exoproduct secretions of Pseudomonas aeruginosa strains influence severity of alveolar epithelial injury.Am. J. Physiol.2671994L551L556",
      "journal-title": "Am. J. Physiol."
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.1.1-8.1995"
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/227680a0"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0966-842X(97)01029-9"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.66.6.2607-2613.1998"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.3201/eid0204.960403"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1994.tb06863.x"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.45.2.470-474.1984"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.1.248-256.1997"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1995.mmi_18010135.x"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.273.5279.1231"
    },
    {
      "key": "e_1_3_2_32_2",
      "unstructured": "Rooney\nP. J.\nFrank\nD. W.\nIsolation and characterization of insertional mutations affecting exoenzyme S production in Pseudomonas aeruginosa abstr. D-188\nAbstracts of the 94th General Meeting of the American Society for Microbiology 1994.\n1994\n129\nAmerican Society for Microbiology\nWashington D.C"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.59.12.4562-4569.1991"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1992.tb01558.x"
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1994.tb02191.x"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.6281995.x"
    },
    {
      "key": "e_1_3_2_37_2",
      "unstructured": "Thompson\nM. R.\nBjorn\nM. J.\nSokol\nP. A.\nLile\nJ. D.\nIglewski\nB. H.\nExoenzyme S: an ADP-ribosyltransferase produced by Pseudomonas aeruginosa Novel ADP-ribosylations of regulatory enzymes and proteins.\nSmulson\nM.\nSugimura\nT.\n1980\n425\n433\nElsevier\nAmsterdam The Netherlands"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)65874-0"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.178.5.1412-1419.1996"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1996.01554.x"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.179.22.7165-7168.1997"
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.10.4024-4028.1995"
    }
  ],
  "container-title": "Infection and Immunity",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.67.2.914-920.1999",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.67.2.914-920.1999",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        3,
        5
      ]
    ],
    "date-time": "2022-03-05T00:50:15Z",
    "timestamp": 1646441415000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/IAI.67.2.914-920.1999"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "P. E.",
      "family": "Orndorff",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        2
      ]
    ]
  },
  "references-count": 41,
  "journal-issue": {
    "issue": "2",
    "published-print": {
      "date-parts": [
        [
          1999,
          2
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/IAI.67.2.914-920.1999"
  ],
  "URL": "http://dx.doi.org/10.1128/IAI.67.2.914-920.1999",
  "relation": {},
  "ISSN": [
    "0019-9567",
    "1098-5522"
  ],
  "subject": [],
  "container-title-short": "Infect Immun",
  "published": {
    "date-parts": [
      [
        1999,
        2
      ]
    ]
  },
  "assertion": [
    {
      "value": "1998-08-28",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1998-11-05",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1999-02-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}