DOI: 10.1128/iai.66.5.1878-1884.1998. Role of YopP in Suppression of Tumor Necrosis Factor Alpha Release by Macrophages during<i>Yersinia</i>Infection

Role of YopP in Suppression of Tumor Necrosis Factor Alpha Release by Macrophages duringYersiniaInfection

10.1128/iai.66.5.1878-1884.1998

Crossref journal-article

American Society for Microbiology

Infection and Immunity (235)

Abstract

ABSTRACTTheYersiniaplasmid-encoded Yop virulon enables extracellular adhering bacteria to deliver toxic effector proteins inside their target cells. It includes a type III secretion system (Ysc), at least two translocator proteins (YopB, YopD), and a set of intracellular Yop effectors (YopE, YopH, YopO, YopM, and YopP). Infection of macrophages with a wild-type strain leads to low levels of tumor necrosis factor alpha (TNF-α) release compared to infection with plasmid-cured strains, suggesting that the virulence plasmid encodes a factor impairing the normal TNF-α response of infected macrophages. This effect is correlated with the inhibition of the macrophage mitogen-activated protein kinase (MAPK) activities. To identify the Yop protein responsible for the suppression of TNF-α release, we infected J774A.1 and PU5-1.8 macrophages with a battery of knockoutYersinia enterocoliticamutants and we quantified the TNF-α released. Mutants affected in secretion (yscN), in translocation (yopBandyopD), or in synthesis of all the known Yop effectors (yopH,yopO,yopP,yopE, andyopMpolymutants) were unable to block the TNF-α response of the macrophages. In contrast, singleyopE,yopH,yopO, andyopMmutants behaved like the wild-type strain. AyopPmutant elicited elevated TNF-α release, and complementation of theyopPmutant or theyopeffector polymutant strain withyopPalone led to a drop in TNF-α release. In addition, YopP was also responsible for the inhibition of the extracellular signal-regulated kinase2 (ERK2) and p38 MAPK activities. These results show that YopP is the Yop effector responsible for theYersinia-induced suppression of TNF-α release by infected macrophages.

Bibliography

Boland, A., & Cornelis, G. R. (1998). Role of YopP in Suppression of Tumor Necrosis Factor Alpha Release by Macrophages duringYersiniaInfection. Infection and Immunity, 66(5), 1878â1884.

Authors 2

Anne Boland (first)
Guy R. Cornelis (additional)

References 61 Referenced 170

10.1128/iai.62.6.2590-2599.1994
10.1007/BF00191545
10.1128/iai.64.4.1357-1368.1996
10.1128/iai.63.4.1270-1277.1995
10.1073/pnas.86.23.9494
10.1093/emboj/16.10.2730
10.1128/iai.63.2.681-685.1995
Bohn E. Autenrieth I. B. IL-12 is essential for resistance against Yersinia enterocolitica by triggering IFN-gamma production in NK cells and CD4+ T cells. J. Immunol. 156 1996 1458 1468 (10.4049/jimmunol.156.4.1458) / J. Immunol. / IL-12 is essential for resistance against Yersinia enterocolitica by triggering IFN-gamma production in NK cells and CD4+ T cells. by Bohn E. (1996)
10.1002/j.1460-2075.1996.tb00904.x
10.1046/j.1365-2958.1998.00691.x
Caron E. Gross A. Liautard J. P. Dornand J. Brucella species release a specific, protease-sensitive, inhibitor of TNF-α expression, active on human macrophage-like cells. J. Immunol. 156 1996 2885 2893 (10.4049/jimmunol.156.8.2885) / J. Immunol. / Brucella species release a specific, protease-sensitive, inhibitor of TNF-α expression, active on human macrophage-like cells. by Caron E. (1996)
10.1128/iai.62.12.5267-5274.1994
Cornelis G. R. Cross-talk between Yersinia and eukaryotic cells Molecular aspects of host-pathogen interactions SGM Symposium 55. McCrae M. A. Saunders J. R. Smyth C. J. Stow N. D. 1996 45 66 Cambridge University Press Cambridge England
10.1046/j.1365-2958.1997.2731623.x
10.1128/iai.64.9.3475-3483.1996
10.1128/mcb.9.11.5223-5227.1989
10.1016/0022-1759(86)90322-4
10.1128/iai.63.8.3117-3124.1995
10.1111/j.1365-2958.1991.tb00773.x
10.1038/361730a0
10.1016/0092-8674(92)90259-F
10.1126/science.2166336
10.1046/j.1365-2958.1996.5251051.x
10.1002/j.1460-2075.1996.tb00968.x
10.1016/0022-1759(89)90397-9
10.1128/iai.62.10.4445-4453.1994
10.1046/j.1365-2958.1997.3211681.x
10.1128/iai.62.10.4432-4439.1994
10.1038/317262a0
10.1016/0378-1119(91)90599-7
10.1038/372739a0
10.1002/jlb.59.2.152
10.1128/iai.58.9.2840-2849.1990
10.1073/pnas.94.23.12638
10.1073/pnas.94.19.10385
10.1128/iai.61.1.23-31.1993
10.1128/iai.63.8.3021-3029.1995
10.1093/emboj/16.9.2307
10.1111/j.1365-2958.1995.mmi_18010135.x
Reimann T. Büscher D. Hipskind R. A. Krautwald S. Lohmann Matthes M. L. Baccarini M. Lipopolysaccharide induces activation of the Raf-1/MAP kinase pathway. A putative role for Raf-1 in the induction of the IL-1β and the TNFα genes. J. Immunol. 153 1994 5740 5749 (10.4049/jimmunol.153.12.5740) / J. Immunol. / Lipopolysaccharide induces activation of the Raf-1/MAP kinase pathway. A putative role for Raf-1 in the induction of the IL-1β and the TNFα genes. by Reimann T. (1994)
Rose D. M. Winston B. W. Chan E. D. Riches D. W. Gerwins P. Johnson G. L. Henson P. M. Fcγ receptor cross-linking activates p42, p38, and JNK/SAPK mitogen-activated protein kinases in murine macrophages: role for p42MAPK in Fcγ receptor-stimulated TNFα synthesis. J. Immunol. 158 1997 3433 3438 (10.4049/jimmunol.158.7.3433) / J. Immunol. / Fcγ receptor cross-linking activates p42, p38, and JNK/SAPK mitogen-activated protein kinases in murine macrophages: role for p42MAPK in Fcγ receptor-stimulated TNFα synthesis. by Rose D. M. (1997)
10.1128/iai.56.8.2139-2143.1988
10.1111/j.1365-2958.1990.tb00635.x
10.1128/iai.59.12.4562-4569.1991
10.1002/j.1460-2075.1994.tb06341.x
10.1074/jbc.272.25.15920
10.1046/j.1365-2958.1997.t01-1-00190.x
10.1128/JB.180.5.1207-1214.1998
Sarker M. R. M.-P. Sory A. Boyd M. Iriarte and G. R. Cornelis. LcrG is required for efficient internalization of Yersinia Yop effector proteins by eukaryotic cells. Infect. Immun. in press.
10.1128/iai.63.10.3759-3764.1995
10.1128/iai.64.6.2106-2113.1996
10.1016/0966-842X(94)90539-8
10.1073/pnas.92.26.11998
10.1111/j.1365-2958.1994.tb02191.x
Sory M.-P. C. Kerbourch and G. R. Cornelis. Unpublished data.
10.1046/j.1365-2958.1997.6281995.x
10.1084/jem.184.3.1027
10.1146/annurev.iy.10.040192.002211
10.1111/j.1365-2958.1993.tb01209.x
10.1128/jb.176.6.1561-1569.1994
10.1046/j.1365-2567.1996.513591.x

Dates

Type	When
Created	5 years, 8 months ago (Dec. 31, 2019, 10:25 a.m.)
Deposited	1 year, 11 months ago (Sept. 24, 2023, 10:35 a.m.)
Indexed	2 months ago (June 30, 2025, 1:06 a.m.)
Issued	27 years, 4 months ago (May 1, 1998)
Published	27 years, 4 months ago (May 1, 1998)
Published Print	27 years, 4 months ago (May 1, 1998)

Funders 0

None

BibTeX

@article{Boland_1998, title={Role of YopP in Suppression of Tumor Necrosis Factor Alpha Release by Macrophages duringYersiniaInfection}, volume={66}, ISSN={1098-5522}, url={http://dx.doi.org/10.1128/iai.66.5.1878-1884.1998}, DOI={10.1128/iai.66.5.1878-1884.1998}, number={5}, journal={Infection and Immunity}, publisher={American Society for Microbiology}, author={Boland, Anne and Cornelis, Guy R.}, year={1998}, month=may, pages={1878–1884} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        30
      ]
    ],
    "date-time": "2025-06-30T05:06:13Z",
    "timestamp": 1751259973845
  },
  "reference-count": 61,
  "publisher": "American Society for Microbiology",
  "issue": "5",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1998,
            5,
            1
          ]
        ],
        "date-time": "1998-05-01T00:00:00Z",
        "timestamp": 893980800000
      },
      "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": [
      [
        1998,
        5
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title><jats:p>The<jats:italic>Yersinia</jats:italic>plasmid-encoded Yop virulon enables extracellular adhering bacteria to deliver toxic effector proteins inside their target cells. It includes a type III secretion system (Ysc), at least two translocator proteins (YopB, YopD), and a set of intracellular Yop effectors (YopE, YopH, YopO, YopM, and YopP). Infection of macrophages with a wild-type strain leads to low levels of tumor necrosis factor alpha (TNF-\u03b1) release compared to infection with plasmid-cured strains, suggesting that the virulence plasmid encodes a factor impairing the normal TNF-\u03b1 response of infected macrophages. This effect is correlated with the inhibition of the macrophage mitogen-activated protein kinase (MAPK) activities. To identify the Yop protein responsible for the suppression of TNF-\u03b1 release, we infected J774A.1 and PU5-1.8 macrophages with a battery of knockout<jats:italic>Yersinia enterocolitica</jats:italic>mutants and we quantified the TNF-\u03b1 released. Mutants affected in secretion (<jats:italic>yscN</jats:italic>), in translocation (<jats:italic>yopB</jats:italic>and<jats:italic>yopD</jats:italic>), or in synthesis of all the known Yop effectors (<jats:italic>yopH</jats:italic>,<jats:italic>yopO</jats:italic>,<jats:italic>yopP</jats:italic>,<jats:italic>yopE</jats:italic>, and<jats:italic>yopM</jats:italic>polymutants) were unable to block the TNF-\u03b1 response of the macrophages. In contrast, single<jats:italic>yopE</jats:italic>,<jats:italic>yopH</jats:italic>,<jats:italic>yopO</jats:italic>, and<jats:italic>yopM</jats:italic>mutants behaved like the wild-type strain. A<jats:italic>yopP</jats:italic>mutant elicited elevated TNF-\u03b1 release, and complementation of the<jats:italic>yopP</jats:italic>mutant or the<jats:italic>yop</jats:italic>effector polymutant strain with<jats:italic>yopP</jats:italic>alone led to a drop in TNF-\u03b1 release. In addition, YopP was also responsible for the inhibition of the extracellular signal-regulated kinase2 (ERK2) and p38 MAPK activities. These results show that YopP is the Yop effector responsible for the<jats:italic>Yersinia</jats:italic>-induced suppression of TNF-\u03b1 release by infected macrophages.</jats:p>",
  "DOI": "10.1128/iai.66.5.1878-1884.1998",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2019,
        12,
        31
      ]
    ],
    "date-time": "2019-12-31T15:25:02Z",
    "timestamp": 1577805902000
  },
  "page": "1878-1884",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 170,
  "title": "Role of YopP in Suppression of Tumor Necrosis Factor Alpha Release by Macrophages during<i>Yersinia</i>Infection",
  "prefix": "10.1128",
  "volume": "66",
  "author": [
    {
      "given": "Anne",
      "family": "Boland",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Microbial Pathogenesis Unit, Christian de Duve Institute of Cellular Pathology, and Faculte\u0301 de Me\u0301decine, Universite\u0301 Catholique de Louvain, B-1200 Brussels, Belgium"
        }
      ]
    },
    {
      "given": "Guy R.",
      "family": "Cornelis",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Microbial Pathogenesis Unit, Christian de Duve Institute of Cellular Pathology, and Faculte\u0301 de Me\u0301decine, Universite\u0301 Catholique de Louvain, B-1200 Brussels, Belgium"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.6.2590-2599.1994"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF00191545"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.4.1357-1368.1996"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.4.1270-1277.1995"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.23.9494"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/16.10.2730"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.2.681-685.1995"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "crossref",
      "first-page": "1458",
      "DOI": "10.4049/jimmunol.156.4.1458",
      "article-title": "IL-12 is essential for resistance against Yersinia enterocolitica by triggering IFN-gamma production in NK cells and CD4+ T cells.",
      "volume": "156",
      "author": "Bohn E.",
      "year": "1996",
      "unstructured": "Bohn E. Autenrieth I. B. IL-12 is essential for resistance against Yersinia enterocolitica by triggering IFN-gamma production in NK cells and CD4+ T cells. J. Immunol. 156 1996 1458 1468",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1996.tb00904.x"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1998.00691.x"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "crossref",
      "first-page": "2885",
      "DOI": "10.4049/jimmunol.156.8.2885",
      "article-title": "Brucella species release a specific, protease-sensitive, inhibitor of TNF-\u03b1 expression, active on human macrophage-like cells.",
      "volume": "156",
      "author": "Caron E.",
      "year": "1996",
      "unstructured": "Caron E. Gross A. Liautard J. P. Dornand J. Brucella species release a specific, protease-sensitive, inhibitor of TNF-\u03b1 expression, active on human macrophage-like cells. J. Immunol. 156 1996 2885 2893",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.12.5267-5274.1994"
    },
    {
      "key": "e_1_3_2_14_2",
      "unstructured": "Cornelis G. R. Cross-talk between Yersinia and eukaryotic cells Molecular aspects of host-pathogen interactions SGM Symposium 55. McCrae M. A. Saunders J. R. Smyth C. J. Stow N. D. 1996 45 66 Cambridge University Press Cambridge England"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.2731623.x"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.9.3475-3483.1996"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/mcb.9.11.5223-5227.1989"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-1759(86)90322-4"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.8.3117-3124.1995"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1991.tb00773.x"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/361730a0"
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(92)90259-F"
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2166336"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1996.5251051.x"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1996.tb00968.x"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-1759(89)90397-9"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.10.4445-4453.1994"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.3211681.x"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.10.4432-4439.1994"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/317262a0"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1119(91)90599-7"
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/372739a0"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jlb.59.2.152"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.58.9.2840-2849.1990"
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.94.23.12638"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.94.19.10385"
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.61.1.23-31.1993"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.8.3021-3029.1995"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/emboj/16.9.2307"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1995.mmi_18010135.x"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "crossref",
      "first-page": "5740",
      "DOI": "10.4049/jimmunol.153.12.5740",
      "article-title": "Lipopolysaccharide induces activation of the Raf-1/MAP kinase pathway. A putative role for Raf-1 in the induction of the IL-1\u03b2 and the TNF\u03b1 genes.",
      "volume": "153",
      "author": "Reimann T.",
      "year": "1994",
      "unstructured": "Reimann T. B\u00fcscher D. Hipskind R. A. Krautwald S. Lohmann Matthes M. L. Baccarini M. Lipopolysaccharide induces activation of the Raf-1/MAP kinase pathway. A putative role for Raf-1 in the induction of the IL-1\u03b2 and the TNF\u03b1 genes. J. Immunol. 153 1994 5740 5749",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "crossref",
      "first-page": "3433",
      "DOI": "10.4049/jimmunol.158.7.3433",
      "article-title": "Fc\u03b3 receptor cross-linking activates p42, p38, and JNK/SAPK mitogen-activated protein kinases in murine macrophages: role for p42MAPK in Fc\u03b3 receptor-stimulated TNF\u03b1 synthesis.",
      "volume": "158",
      "author": "Rose D. M.",
      "year": "1997",
      "unstructured": "Rose D. M. Winston B. W. Chan E. D. Riches D. W. Gerwins P. Johnson G. L. Henson P. M. Fc\u03b3 receptor cross-linking activates p42, p38, and JNK/SAPK mitogen-activated protein kinases in murine macrophages: role for p42MAPK in Fc\u03b3 receptor-stimulated TNF\u03b1 synthesis. J. Immunol. 158 1997 3433 3438",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.56.8.2139-2143.1988"
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1990.tb00635.x"
    },
    {
      "key": "e_1_3_2_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.59.12.4562-4569.1991"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/j.1460-2075.1994.tb06341.x"
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.272.25.15920"
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.t01-1-00190.x"
    },
    {
      "key": "e_1_3_2_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.5.1207-1214.1998"
    },
    {
      "key": "e_1_3_2_50_2",
      "unstructured": "Sarker M. R. M.-P. Sory A. Boyd M. Iriarte and G. R. Cornelis. LcrG is required for efficient internalization of Yersinia Yop effector proteins by eukaryotic cells. Infect. Immun. in press."
    },
    {
      "key": "e_1_3_2_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.10.3759-3764.1995"
    },
    {
      "key": "e_1_3_2_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.6.2106-2113.1996"
    },
    {
      "key": "e_1_3_2_53_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0966-842X(94)90539-8"
    },
    {
      "key": "e_1_3_2_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.92.26.11998"
    },
    {
      "key": "e_1_3_2_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1994.tb02191.x"
    },
    {
      "key": "e_1_3_2_56_2",
      "unstructured": "Sory M.-P. C. Kerbourch and G. R. Cornelis. Unpublished data."
    },
    {
      "key": "e_1_3_2_57_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.6281995.x"
    },
    {
      "key": "e_1_3_2_58_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.184.3.1027"
    },
    {
      "key": "e_1_3_2_59_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.iy.10.040192.002211"
    },
    {
      "key": "e_1_3_2_60_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1365-2958.1993.tb01209.x"
    },
    {
      "key": "e_1_3_2_61_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.176.6.1561-1569.1994"
    },
    {
      "key": "e_1_3_2_62_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2567.1996.513591.x"
    }
  ],
  "container-title": "Infection and Immunity",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.66.5.1878-1884.1998",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.66.5.1878-1884.1998",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        9,
        24
      ]
    ],
    "date-time": "2023-09-24T14:35:00Z",
    "timestamp": 1695566100000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/IAI.66.5.1878-1884.1998"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1998,
        5
      ]
    ]
  },
  "references-count": 61,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          1998,
          5
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/IAI.66.5.1878-1884.1998"
  ],
  "URL": "http://dx.doi.org/10.1128/IAI.66.5.1878-1884.1998",
  "relation": {},
  "ISSN": [
    "0019-9567",
    "1098-5522"
  ],
  "subject": [],
  "container-title-short": "Infect Immun",
  "published": {
    "date-parts": [
      [
        1998,
        5
      ]
    ]
  },
  "assertion": [
    {
      "value": "1997-11-06",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1998-02-12",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1998-05-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}