DOI: 10.1128/iai.69.10.6276-6283.2001. Motility and Chemotaxis in Tissue Penetration of Oral Epithelial Cell Layers by<i>Treponema denticola</i>

Motility and Chemotaxis in Tissue Penetration of Oral Epithelial Cell Layers byTreponema denticola

10.1128/iai.69.10.6276-6283.2001

Crossref journal-article

American Society for Microbiology

Infection and Immunity (235)

Abstract

ABSTRACTThe ability to penetrate tissue is an important virulence factor for pathogenic spirochetes. Previous studies have recognized the role of motility in allowing pathogenic spirochetes to invade tissues and migrate to sites favorable for bacterial proliferation. However, the nature of the movements, whether they are random or controlled by chemotaxis systems, has yet to be established. In this study, we addressed the role of motility and chemotaxis in tissue penetration by the periodontal disease-associated oral spirocheteTreponema denticolausing an oral epithelial cell line-based experimental approach. Wild-typeT. denticolaATCC 35405 was found to penetrate the tissue layers effectively, whereas a nonmotile mutant was unable to overcome the tissue barrier. Interestingly, the chemotaxis mutants also showed impaired tissue penetration. AcheAmutant that is motile but lacks the central kinase of the chemotaxis pathway showed only about 2 to 3% of the wild-type penetration rate. The two known chemoreceptors ofT. denticola, DmcA and DmcB, also appear to be involved in the invasion process. Thedmcmutants were actively motile but exhibited reduced tissue penetration of about 30 and 10% of the wild-type behavior, respectively. These data suggest that not only motility but also chemotaxis is involved in the tissue penetration byT. denticola.

Bibliography

Lux, R., Miller, J. N., Park, N.-H., & Shi, W. (2001). Motility and Chemotaxis in Tissue Penetration of Oral Epithelial Cell Layers byTreponema denticola. Infection and Immunity, 69(10), 6276â6283.

Authors 4

Renate Lux (first)
James N. Miller (additional)
No-Hee Park (additional)
Wenyuan Shi (additional)

References 64 Referenced 110

Carranza F. A. J. Newman M. G. Clinical periodontology 8th ed. 1996 W. B. Saunders Company Philadelphia Pa
10.1128/iai.58.9.3158-3161.1990
10.1099/00207713-43-2-196
10.1128/iai.57.5.1626-1628.1989
10.1128/IAI.68.4.2016-2023.2000
10.1038/37551
10.1126/science.281.5375.375
10.1128/iai.34.1.241-249.1981
10.1128/iai.34.1.222-233.1981
10.1128/iai.34.1.234-240.1981
10.1016/S0378-1119(99)00115-8
Haake D. A. Lovett M. A. Interjunctional invasion of endothelial cell monolayers Bacterial pathogenesis. Clark V. L. Bavoil P. M. 1997 711 727 Academic Press San Diego Calif
10.1128/jb.171.10.5668-5671.1989
10.1128/iai.65.6.2041-2051.1997
Hiramune T. Shiraiwa C. Kikuchi N. Yanagawa R. A basic study of chemotaxis of leptospiras.Zentbl. Vetmed.371990749752 / Zentbl. Vetmed. / A basic study of chemotaxis of leptospiras by Hiramune T. (1990)
10.1128/iai.60.6.2475-2480.1992
10.1128/iai.65.10.4011-4016.1997
10.1016/S0378-1097(97)00244-9
10.1016/0378-1135(95)00174-3
10.1016/S0006-3495(93)81317-1
10.1126/science.2814477
10.1073/pnas.89.5.1847
Li C. Motaleb A. Sal M. Goldstein S. T. Charon N. W. Spirochete periplasmic flagella and motility.J. Mol. Microbiol. Biotechnol.22000345354 / J. Mol. Microbiol. Biotechnol. / Spirochete periplasmic flagella and motility by Li C. (2000)
Li C. Y. Tsai J. P. Han Y. W. Yang Z. Wolinsky L. E. Kuramitsu H. Shi W. Chemotaxis and the cheA mutant of Treponema denticola.J. Dent. Res.771998228 / J. Dent. Res. / Chemotaxis and the cheA mutant of Treponema denticola by Li C. Y. (1998)
10.1128/IAI.67.2.694-699.1999
10.1128/jb.178.12.3664-3667.1996
10.1128/JB.181.12.3743-3750.1999
10.1093/clinids/16.Supplement_4.S203
Lux R. Moter A. Shi W. Chemotaxis in pathogenic spirochetes: directed movement toward targeting tissues? J. Mol. Microbiol. Biotechnol. 2 2000 355 364 / J. Mol. Microbiol. Biotechnol. / Chemotaxis in pathogenic spirochetes: directed movement toward targeting tissues? by Lux R. (2000)
10.1128/JB.180.5.1009-1022.1998
Mayo J. A. Blake A. Donze D. Chemotaxis by Treponema denticola.J. Dent. Res.691990382 / J. Dent. Res. / Chemotaxis by Treponema denticola by Mayo J. A. (1990)
10.1128/iai.55.3.621-625.1987
Miller J. N. Immunity in experimental syphilis. VI. Successful vaccination of rabbits with Treponema pallidum, Nichols strain, attenuated by gamma-irradiation.J. Immunol.110197312061215 / J. Immunol. / Immunity in experimental syphilis. VI. Successful vaccination of rabbits with Treponema pallidum, Nichols strain, attenuated by gamma-irradiation by Miller J. N. (1973)
10.1128/iai.62.9.4095-4099.1994
10.1099/00221287-144-9-2459
10.1128/iai.53.1.213-220.1986
10.1128/JB.182.8.2326-2328.2000
10.1128/JB.181.14.4308-4317.1999
10.1046/j.1365-2958.1996.412927.x
10.1046/j.1365-2958.1997.4281787.x
10.1093/carcin/12.9.1627
10.1128/jb.151.1.106-113.1982
10.1034/j.1399-302X.1999.140609.x
10.1902/jop.1992.63.2.131
10.1128/iai.57.8.2267-2271.1989
10.1128/iai.59.10.3377-3380.1991
10.1128/iai.62.5.1749-1754.1994
10.1128/iai.63.10.3973-3979.1995
10.1172/JCI115308
10.1111/j.1600-051X.1998.tb02388.x
10.1111/j.1600-0765.1997.tb00558.x
Shenker B. J. Listgarten M. A. Taichman N. S. Suppression of human lymphocyte responses by oral spirochetes: a monocyte-dependent phenomenon.J. Immunol.132198420392045 (10.4049/jimmunol.132.4.2039) / J. Immunol. / Suppression of human lymphocyte responses by oral spirochetes: a monocyte-dependent phenomenon by Shenker B. J. (1984)
10.1128/JB.180.2.231-235.1998
10.1111/j.1600-051X.1998.tb02419.x
10.1111/j.1574-6968.1999.tb08703.x
10.1146/annurev.bb.20.060191.000545
Stock J. B. Surette M. G. Chemotaxis Escherichia coli and Salmonella: cellular and molecular biology. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Reznikoff W. S. Riley M. Schaechter M. Umbarger H. E. 1996 1103 1129 ASM Press Washington D.C.
10.1128/iai.60.9.3596-3600.1992
10.1128/iai.58.3.581-585.1990
10.1073/pnas.85.10.3608
10.1128/iai.56.10.2717-2722.1988
10.1034/j.1600-051x.2000.027009648.x
10.1046/j.1365-2958.1997.2861650.x
10.1128/iai.61.5.2270-2272.1993

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 6:01 a.m.)
Deposited	2 years, 4 months ago (April 23, 2023, 11:26 a.m.)
Indexed	4 weeks ago (Aug. 6, 2025, 9:23 a.m.)
Issued	23 years, 11 months ago (Oct. 1, 2001)
Published	23 years, 11 months ago (Oct. 1, 2001)
Published Print	23 years, 11 months ago (Oct. 1, 2001)

Funders 0

None

BibTeX

@article{Lux_2001, title={Motility and Chemotaxis in Tissue Penetration of Oral Epithelial Cell Layers byTreponema denticola}, volume={69}, ISSN={1098-5522}, url={http://dx.doi.org/10.1128/iai.69.10.6276-6283.2001}, DOI={10.1128/iai.69.10.6276-6283.2001}, number={10}, journal={Infection and Immunity}, publisher={American Society for Microbiology}, author={Lux, Renate and Miller, James N. and Park, No-Hee and Shi, Wenyuan}, editor={Barbieri, J. T.}, year={2001}, month=oct, pages={6276–6283} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        6
      ]
    ],
    "date-time": "2025-08-06T13:23:15Z",
    "timestamp": 1754486595354
  },
  "reference-count": 64,
  "publisher": "American Society for Microbiology",
  "issue": "10",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2001,
            10,
            1
          ]
        ],
        "date-time": "2001-10-01T00:00:00Z",
        "timestamp": 1001894400000
      },
      "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": [
      [
        2001,
        10
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title><jats:p>The ability to penetrate tissue is an important virulence factor for pathogenic spirochetes. Previous studies have recognized the role of motility in allowing pathogenic spirochetes to invade tissues and migrate to sites favorable for bacterial proliferation. However, the nature of the movements, whether they are random or controlled by chemotaxis systems, has yet to be established. In this study, we addressed the role of motility and chemotaxis in tissue penetration by the periodontal disease-associated oral spirochete<jats:italic>Treponema denticola</jats:italic>using an oral epithelial cell line-based experimental approach. Wild-type<jats:italic>T. denticola</jats:italic>ATCC 35405 was found to penetrate the tissue layers effectively, whereas a nonmotile mutant was unable to overcome the tissue barrier. Interestingly, the chemotaxis mutants also showed impaired tissue penetration. A<jats:italic>cheA</jats:italic>mutant that is motile but lacks the central kinase of the chemotaxis pathway showed only about 2 to 3% of the wild-type penetration rate. The two known chemoreceptors of<jats:italic>T. denticola</jats:italic>, DmcA and DmcB, also appear to be involved in the invasion process. The<jats:italic>dmc</jats:italic>mutants were actively motile but exhibited reduced tissue penetration of about 30 and 10% of the wild-type behavior, respectively. These data suggest that not only motility but also chemotaxis is involved in the tissue penetration by<jats:italic>T. denticola</jats:italic>.</jats:p>",
  "DOI": "10.1128/iai.69.10.6276-6283.2001",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        27
      ]
    ],
    "date-time": "2002-07-27T10:01:19Z",
    "timestamp": 1027764079000
  },
  "page": "6276-6283",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 110,
  "title": "Motility and Chemotaxis in Tissue Penetration of Oral Epithelial Cell Layers by<i>Treponema denticola</i>",
  "prefix": "10.1128",
  "volume": "69",
  "author": [
    {
      "given": "Renate",
      "family": "Lux",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->School of Dentistry and Molecular Biology Institute1 and"
        }
      ]
    },
    {
      "given": "James N.",
      "family": "Miller",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 2-->Department of Microbiology, Immunology, and Molecular Genetics,2 University of California, Los Angeles, California 90095-1668"
        }
      ]
    },
    {
      "given": "No-Hee",
      "family": "Park",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->School of Dentistry and Molecular Biology Institute1 and"
        }
      ]
    },
    {
      "given": "Wenyuan",
      "family": "Shi",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->School of Dentistry and Molecular Biology Institute1 and"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "unstructured": "Carranza F. A. J. Newman M. G. Clinical periodontology 8th ed. 1996 W. B. Saunders Company Philadelphia Pa"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.58.9.3158-3161.1990"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00207713-43-2-196"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.57.5.1626-1628.1989"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.68.4.2016-2023.2000"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/37551"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.281.5375.375"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.34.1.241-249.1981"
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.34.1.222-233.1981"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.34.1.234-240.1981"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0378-1119(99)00115-8"
    },
    {
      "key": "e_1_3_2_13_2",
      "unstructured": "Haake D. A. Lovett M. A. Interjunctional invasion of endothelial cell monolayers Bacterial pathogenesis. Clark V. L. Bavoil P. M. 1997 711 727 Academic Press San Diego Calif"
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.171.10.5668-5671.1989"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.6.2041-2051.1997"
    },
    {
      "key": "e_1_3_2_16_2",
      "first-page": "749",
      "article-title": "A basic study of chemotaxis of leptospiras",
      "volume": "37",
      "author": "Hiramune T.",
      "year": "1990",
      "unstructured": "Hiramune T. Shiraiwa C. Kikuchi N. Yanagawa R. A basic study of chemotaxis of leptospiras.Zentbl. Vetmed.371990749752",
      "journal-title": "Zentbl. Vetmed."
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.60.6.2475-2480.1992"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.10.4011-4016.1997"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0378-1097(97)00244-9"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0378-1135(95)00174-3"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0006-3495(93)81317-1"
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.2814477"
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.5.1847"
    },
    {
      "key": "e_1_3_2_24_2",
      "first-page": "345",
      "article-title": "Spirochete periplasmic flagella and motility",
      "volume": "2",
      "author": "Li C.",
      "year": "2000",
      "unstructured": "Li C. Motaleb A. Sal M. Goldstein S. T. Charon N. W. Spirochete periplasmic flagella and motility.J. Mol. Microbiol. Biotechnol.22000345354",
      "journal-title": "J. Mol. Microbiol. Biotechnol."
    },
    {
      "key": "e_1_3_2_25_2",
      "first-page": "228",
      "article-title": "Chemotaxis and the cheA mutant of Treponema denticola",
      "volume": "77",
      "author": "Li C. Y.",
      "year": "1998",
      "unstructured": "Li C. Y. Tsai J. P. Han Y. W. Yang Z. Wolinsky L. E. Kuramitsu H. Shi W. Chemotaxis and the cheA mutant of Treponema denticola.J. Dent. Res.771998228",
      "journal-title": "J. Dent. Res."
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/IAI.67.2.694-699.1999"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.178.12.3664-3667.1996"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.181.12.3743-3750.1999"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/clinids/16.Supplement_4.S203"
    },
    {
      "key": "e_1_3_2_30_2",
      "first-page": "355",
      "article-title": "Chemotaxis in pathogenic spirochetes: directed movement toward targeting tissues?",
      "volume": "2",
      "author": "Lux R.",
      "year": "2000",
      "unstructured": "Lux R. Moter A. Shi W. Chemotaxis in pathogenic spirochetes: directed movement toward targeting tissues? J. Mol. Microbiol. Biotechnol. 2 2000 355 364",
      "journal-title": "J. Mol. Microbiol. Biotechnol."
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.5.1009-1022.1998"
    },
    {
      "key": "e_1_3_2_32_2",
      "first-page": "382",
      "article-title": "Chemotaxis by Treponema denticola",
      "volume": "69",
      "author": "Mayo J. A.",
      "year": "1990",
      "unstructured": "Mayo J. A. Blake A. Donze D. Chemotaxis by Treponema denticola.J. Dent. Res.691990382",
      "journal-title": "J. Dent. Res."
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.55.3.621-625.1987"
    },
    {
      "key": "e_1_3_2_34_2",
      "first-page": "1206",
      "article-title": "Immunity in experimental syphilis. VI. Successful vaccination of rabbits with Treponema pallidum, Nichols strain, attenuated by gamma-irradiation",
      "volume": "110",
      "author": "Miller J. N.",
      "year": "1973",
      "unstructured": "Miller J. N. Immunity in experimental syphilis. VI. Successful vaccination of rabbits with Treponema pallidum, Nichols strain, attenuated by gamma-irradiation.J. Immunol.110197312061215",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.9.4095-4099.1994"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00221287-144-9-2459"
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.53.1.213-220.1986"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.182.8.2326-2328.2000"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.181.14.4308-4317.1999"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1996.412927.x"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.4281787.x"
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/carcin/12.9.1627"
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.151.1.106-113.1982"
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1034/j.1399-302X.1999.140609.x"
    },
    {
      "key": "e_1_3_2_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1902/jop.1992.63.2.131"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.57.8.2267-2271.1989"
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.59.10.3377-3380.1991"
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.5.1749-1754.1994"
    },
    {
      "key": "e_1_3_2_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.10.3973-3979.1995"
    },
    {
      "key": "e_1_3_2_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI115308"
    },
    {
      "key": "e_1_3_2_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1600-051X.1998.tb02388.x"
    },
    {
      "key": "e_1_3_2_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1600-0765.1997.tb00558.x"
    },
    {
      "key": "e_1_3_2_53_2",
      "doi-asserted-by": "crossref",
      "first-page": "2039",
      "DOI": "10.4049/jimmunol.132.4.2039",
      "article-title": "Suppression of human lymphocyte responses by oral spirochetes: a monocyte-dependent phenomenon",
      "volume": "132",
      "author": "Shenker B. J.",
      "year": "1984",
      "unstructured": "Shenker B. J. Listgarten M. A. Taichman N. S. Suppression of human lymphocyte responses by oral spirochetes: a monocyte-dependent phenomenon.J. Immunol.132198420392045",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.180.2.231-235.1998"
    },
    {
      "key": "e_1_3_2_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1600-051X.1998.tb02419.x"
    },
    {
      "key": "e_1_3_2_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1574-6968.1999.tb08703.x"
    },
    {
      "key": "e_1_3_2_57_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.bb.20.060191.000545"
    },
    {
      "key": "e_1_3_2_58_2",
      "unstructured": "Stock J. B. Surette M. G. Chemotaxis Escherichia coli and Salmonella: cellular and molecular biology. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Reznikoff W. S. Riley M. Schaechter M. Umbarger H. E. 1996 1103 1129 ASM Press Washington D.C."
    },
    {
      "key": "e_1_3_2_59_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.60.9.3596-3600.1992"
    },
    {
      "key": "e_1_3_2_60_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.58.3.581-585.1990"
    },
    {
      "key": "e_1_3_2_61_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.85.10.3608"
    },
    {
      "key": "e_1_3_2_62_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.56.10.2717-2722.1988"
    },
    {
      "key": "e_1_3_2_63_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1034/j.1600-051x.2000.027009648.x"
    },
    {
      "key": "e_1_3_2_64_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1365-2958.1997.2861650.x"
    },
    {
      "key": "e_1_3_2_65_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.61.5.2270-2272.1993"
    }
  ],
  "container-title": "Infection and Immunity",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.69.10.6276-6283.2001",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.69.10.6276-6283.2001",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        4,
        23
      ]
    ],
    "date-time": "2023-04-23T15:26:01Z",
    "timestamp": 1682263561000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/IAI.69.10.6276-6283.2001"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "J. T.",
      "family": "Barbieri",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        10
      ]
    ]
  },
  "references-count": 64,
  "journal-issue": {
    "issue": "10",
    "published-print": {
      "date-parts": [
        [
          2001,
          10
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/IAI.69.10.6276-6283.2001"
  ],
  "URL": "http://dx.doi.org/10.1128/IAI.69.10.6276-6283.2001",
  "relation": {},
  "ISSN": [
    "0019-9567",
    "1098-5522"
  ],
  "subject": [],
  "container-title-short": "Infect Immun",
  "published": {
    "date-parts": [
      [
        2001,
        10
      ]
    ]
  },
  "assertion": [
    {
      "value": "2001-05-29",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2001-07-22",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2001-10-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}