DOI: 10.1111/j.1365-2958.1993.tb01254.x. Induction of phagocytic behaviour in human epithelial cells by <i>Escherichia coli</i> cytotoxic necrotizing factor type1

Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type1

10.1111/j.1365-2958.1993.tb01254.x

Crossref journal-article

Wiley

Molecular Microbiology (311)

Abstract

SummaryCytotoxic necrotizing factor type 1 (CNF1) from strains of pathogenic Escherichia coli induces in human epithelial HEp‐2 cells, a profound reorganization of the actin cytoskeleton into prominent stress fibres and membrane ruffles. We report here that this process is associated with induction of phagocytic‐like activity. CNF1‐treated cells acquired the ability to ingest latex beads as well as non‐invasive bacteria such as Listeria innocua, which were taken as a model system. Uptake of bacteria was similar to pathogen‐induced phagocytosis, since L. innocua transformed with DNA coding for the pore‐forming toxin listeriolysln O behaved, with respect to intracellular growth, like the invasive, pathogenic species L. monocytogenes. Our results raise the possibility that, in vivo, pathogenic CNF1 ‐producing E. coli may invade epithelia by this novel induced phagocytic‐like mechanism.

Bibliography

Falzano, L., Fiorentini, C., Donelli, G., Michel, E., Kocks, C., Cossart, P., CabaniÃ©, L., Oswald, E., & Boquet, P. (1993). Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type1. Molecular Microbiology, 9(6), 1247â1254. Portico.

Authors 9

Loredana Falzano (first)
Carla Fiorentini (additional)
Gianfranco Donelli (additional)
Eric Michel (additional)
Christine Kocks (additional)
Pascale Cossart (additional)
Lucien Cabanié (additional)
Eric Oswald (additional)
Patrice Boquet (additional)

References 36 Referenced 156

10.1128/iai.59.6.1997-2005.1991 / Infect Immun / Two novel virulence loci mixiA and mixiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens by Andrews G.P. (1991)
10.1111/j.1574-6968.1987.tb02630.x
10.1017/S002217240006277X
10.1016/0378-1135(88)90095-8
10.1099/00222615-31-3-175
10.1016/0923-2508(92)90074-X
10.1128/IAI.39.3.1300-1306.1983
10.1016/0006-291X(84)91343-3
10.1128/jcm.25.1.146-149.1987
10.1111/j.1574-6968.1990.tb13989.x
10.1083/jcb.105.4.1473
10.1128/IAI.57.11.3629-3636.1989
10.1016/0378-1135(87)90139-8
10.1128/jcm.27.5.983-988.1989 / J Clin Microbiol / Immunochemical identification and biological characterization of cytotoxic necrotizing factor from Escherichia coli by Rycke J. (1989)
10.1128/jcm.28.4.694-699.1990 / J Clin Microbiol / Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates by Rycke J. (1990)
10.1128/IAI.60.6.2182-2187.1992
10.1016/0092-8674(91)90003-H
10.1146/annurev.cb.08.110192.002001
10.1093/clinids/9.Supplement_5.S450
10.1016/0041-0101(88)90203-6
10.1128/IAI.55.11.2822-2829.1987
10.1016/0092-8674(91)90009-N
10.1128/iai.55.7.1641-1646.1987 / Infect Immun / Purification, characterization and toxicity of the sulfhydryl‐activated hemolysin listeriolysin O from Listeria monocytogenes by Geoffroy C. (1987)
10.1016/0092-8674(87)90335-7
10.1093/infdis/155.3.377
10.1111/j.1365-2958.1990.tb00578.x
10.1017/S0022172400060678
10.1111/j.1574-6968.1990.tb13951.x
10.1111/j.1574-6968.1989.tb03025.x
10.1084/jem.167.4.1459
10.1016/0092-8674(92)90163-7
10.1016/0092-8674(92)90164-8
10.1002/bies.950150104
10.1042/bst0200724
{'key': 'e_1_2_1_36_1', 'first-page': '703', 'volume-title': 'Fundamental Immunology', 'author': 'Silverstein S.C.', 'year': '1989'} / Fundamental Immunology by Silverstein S.C. (1989)
10.1016/0378-1119(91)90546-N

Dates

Type	When
Created	18 years, 10 months ago (Oct. 27, 2006, 9:55 p.m.)
Deposited	1 year, 10 months ago (Oct. 25, 2023, 2:51 a.m.)
Indexed	4 months, 3 weeks ago (April 11, 2025, 5:26 a.m.)
Issued	32 years ago (Sept. 1, 1993)
Published	32 years ago (Sept. 1, 1993)
Published Online	18 years, 10 months ago (Oct. 27, 2006)
Published Print	32 years ago (Sept. 1, 1993)

Funders 0

None

BibTeX

@article{Falzano_1993, title={Induction of phagocytic behaviour in human epithelial cells by Escherichia coli cytotoxic necrotizing factor type1}, volume={9}, ISSN={1365-2958}, url={http://dx.doi.org/10.1111/j.1365-2958.1993.tb01254.x}, DOI={10.1111/j.1365-2958.1993.tb01254.x}, number={6}, journal={Molecular Microbiology}, publisher={Wiley}, author={Falzano, Loredana and Fiorentini, Carla and Donelli, Gianfranco and Michel, Eric and Kocks, Christine and Cossart, Pascale and Cabanié, Lucien and Oswald, Eric and Boquet, Patrice}, year={1993}, month=sep, pages={1247–1254} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        4,
        11
      ]
    ],
    "date-time": "2025-04-11T09:26:41Z",
    "timestamp": 1744363601200
  },
  "reference-count": 36,
  "publisher": "Wiley",
  "issue": "6",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2006,
            10,
            27
          ]
        ],
        "date-time": "2006-10-27T00:00:00Z",
        "timestamp": 1161907200000
      },
      "content-version": "vor",
      "delay-in-days": 4804,
      "URL": "http://onlinelibrary.wiley.com/termsAndConditions#vor"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1993,
        9
      ]
    ]
  },
  "abstract": "<jats:title>Summary</jats:title><jats:p>Cytotoxic necrotizing factor type 1 (CNF1) from strains of pathogenic <jats:italic>Escherichia coli</jats:italic> induces in human epithelial HEp\u20102 cells, a profound reorganization of the actin cytoskeleton into prominent stress fibres and membrane ruffles. We report here that this process is associated with induction of phagocytic\u2010like activity. CNF1\u2010treated cells acquired the ability to ingest latex beads as well as non\u2010invasive bacteria such as <jats:italic>Listeria innocua</jats:italic>, which were taken as a model system. Uptake of bacteria was similar to pathogen\u2010induced phagocytosis, since <jats:italic>L. innocua</jats:italic> transformed with DNA coding for the pore\u2010forming toxin listeriolysln O behaved, with respect to intracellular growth, like the invasive, pathogenic species <jats:italic>L. monocytogenes.</jats:italic> Our results raise the possibility that, <jats:italic>in vivo</jats:italic>, pathogenic CNF1 \u2010producing <jats:italic>E. coli</jats:italic> may invade epithelia by this novel induced phagocytic\u2010like mechanism.</jats:p>",
  "DOI": "10.1111/j.1365-2958.1993.tb01254.x",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        28
      ]
    ],
    "date-time": "2006-10-28T01:55:04Z",
    "timestamp": 1162000504000
  },
  "page": "1247-1254",
  "source": "Crossref",
  "is-referenced-by-count": 156,
  "title": "Induction of phagocytic behaviour in human epithelial cells by <i>Escherichia coli</i> cytotoxic necrotizing factor type1",
  "prefix": "10.1111",
  "volume": "9",
  "author": [
    {
      "given": "Loredana",
      "family": "Falzano",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Carla",
      "family": "Fiorentini",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Gianfranco",
      "family": "Donelli",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Eric",
      "family": "Michel",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Christine",
      "family": "Kocks",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Pascale",
      "family": "Cossart",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Lucien",
      "family": "Cabani\u00e9",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Eric",
      "family": "Oswald",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Patrice",
      "family": "Boquet",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "311",
  "published-online": {
    "date-parts": [
      [
        2006,
        10,
        27
      ]
    ]
  },
  "reference": [
    {
      "key": "e_1_2_1_2_1",
      "doi-asserted-by": "crossref",
      "first-page": "1997",
      "DOI": "10.1128/iai.59.6.1997-2005.1991",
      "article-title": "Two novel virulence loci mixiA and mixiB, in Shigella flexneri 2a facilitate excretion of invasion plasmid antigens",
      "volume": "59",
      "author": "Andrews G.P.",
      "year": "1991",
      "journal-title": "Infect Immun"
    },
    {
      "key": "e_1_2_1_3_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1574-6968.1987.tb02630.x"
    },
    {
      "key": "e_1_2_1_4_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1017/S002217240006277X"
    },
    {
      "key": "e_1_2_1_5_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1135(88)90095-8"
    },
    {
      "key": "e_1_2_1_6_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00222615-31-3-175"
    },
    {
      "key": "e_1_2_1_7_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0923-2508(92)90074-X"
    },
    {
      "key": "e_1_2_1_8_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.39.3.1300-1306.1983"
    },
    {
      "key": "e_1_2_1_9_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0006-291X(84)91343-3"
    },
    {
      "key": "e_1_2_1_10_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jcm.25.1.146-149.1987"
    },
    {
      "key": "e_1_2_1_11_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1574-6968.1990.tb13989.x"
    },
    {
      "key": "e_1_2_1_12_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.105.4.1473"
    },
    {
      "key": "e_1_2_1_13_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.57.11.3629-3636.1989"
    },
    {
      "key": "e_1_2_1_14_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1135(87)90139-8"
    },
    {
      "key": "e_1_2_1_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "983",
      "DOI": "10.1128/jcm.27.5.983-988.1989",
      "article-title": "Immunochemical identification and biological characterization of cytotoxic necrotizing factor from Escherichia coli",
      "volume": "27",
      "author": "Rycke J.",
      "year": "1989",
      "journal-title": "J Clin Microbiol"
    },
    {
      "key": "e_1_2_1_16_1",
      "doi-asserted-by": "crossref",
      "first-page": "694",
      "DOI": "10.1128/jcm.28.4.694-699.1990",
      "article-title": "Evidence for two types of cytotoxic necrotizing factor in human and animal clinical isolates",
      "volume": "28",
      "author": "Rycke J.",
      "year": "1990",
      "journal-title": "J Clin Microbiol"
    },
    {
      "key": "e_1_2_1_17_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.60.6.2182-2187.1992"
    },
    {
      "key": "e_1_2_1_18_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90003-H"
    },
    {
      "key": "e_1_2_1_19_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.cb.08.110192.002001"
    },
    {
      "key": "e_1_2_1_20_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/clinids/9.Supplement_5.S450"
    },
    {
      "key": "e_1_2_1_21_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0041-0101(88)90203-6"
    },
    {
      "key": "e_1_2_1_22_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.55.11.2822-2829.1987"
    },
    {
      "key": "e_1_2_1_23_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90009-N"
    },
    {
      "key": "e_1_2_1_24_1",
      "doi-asserted-by": "crossref",
      "first-page": "1641",
      "DOI": "10.1128/iai.55.7.1641-1646.1987",
      "article-title": "Purification, characterization and toxicity of the sulfhydryl\u2010activated hemolysin listeriolysin O from Listeria monocytogenes",
      "volume": "55",
      "author": "Geoffroy C.",
      "year": "1987",
      "journal-title": "Infect Immun"
    },
    {
      "key": "e_1_2_1_25_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(87)90335-7"
    },
    {
      "key": "e_1_2_1_26_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/155.3.377"
    },
    {
      "key": "e_1_2_1_27_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1990.tb00578.x"
    },
    {
      "key": "e_1_2_1_28_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1017/S0022172400060678"
    },
    {
      "key": "e_1_2_1_29_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1574-6968.1990.tb13951.x"
    },
    {
      "key": "e_1_2_1_30_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1574-6968.1989.tb03025.x"
    },
    {
      "key": "e_1_2_1_31_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.167.4.1459"
    },
    {
      "key": "e_1_2_1_32_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90163-7"
    },
    {
      "key": "e_1_2_1_33_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90164-8"
    },
    {
      "key": "e_1_2_1_34_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/bies.950150104"
    },
    {
      "key": "e_1_2_1_35_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1042/bst0200724"
    },
    {
      "key": "e_1_2_1_36_1",
      "first-page": "703",
      "volume-title": "Fundamental Immunology",
      "author": "Silverstein S.C.",
      "year": "1989"
    },
    {
      "key": "e_1_2_1_37_1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1119(91)90546-N"
    }
  ],
  "container-title": "Molecular Microbiology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fj.1365-2958.1993.tb01254.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-2958.1993.tb01254.x",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        10,
        25
      ]
    ],
    "date-time": "2023-10-25T06:51:06Z",
    "timestamp": 1698216666000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://onlinelibrary.wiley.com/doi/10.1111/j.1365-2958.1993.tb01254.x"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1993,
        9
      ]
    ]
  },
  "references-count": 36,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          1993,
          9
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1111/j.1365-2958.1993.tb01254.x"
  ],
  "URL": "http://dx.doi.org/10.1111/j.1365-2958.1993.tb01254.x",
  "relation": {},
  "ISSN": [
    "0950-382X",
    "1365-2958"
  ],
  "subject": [],
  "container-title-short": "Molecular Microbiology",
  "published": {
    "date-parts": [
      [
        1993,
        9
      ]
    ]
  }
}