DOI: 10.1128/iai.67.3.1368-1378.1999. Human Granulocytic Ehrlichiosis Agent and<i>Ehrlichia chaffeensis</i>Reside in Different Cytoplasmic Compartments in HL-60 Cells

Human Granulocytic Ehrlichiosis Agent andEhrlichia chaffeensisReside in Different Cytoplasmic Compartments in HL-60 Cells

10.1128/iai.67.3.1368-1378.1999

Crossref journal-article

American Society for Microbiology

Infection and Immunity (235)

Abstract

ABSTRACTThe human granulocytic ehrlichiosis (HGE) agent resides and multiplies exclusively in cytoplasmic vacuoles of granulocytes. Double immunofluorescence labeling was used to characterize the nature of the HGE agent replicative inclusions and to compare them with inclusions containing the human monocytic ehrlichia,Ehrlichia chaffeensis, in HL-60 cells. Although bothEhrlichiaspp. can coinfect HL-60 cells, they resided in separate inclusions. Inclusions of bothEhrlichiaspp. were not labeled with either anti-lysosome-associated membrane protein 1 or anti-CD63. Accumulation of myeloperoxidase-positive granules were seen around HGE agent inclusions but not aroundE. chaffeensisinclusions. 3-(2,4-Dinitroanilino)-3′-amino-N-methyldipropylamine and acridine orange were not localized to either inclusion type. Vacuolar-type H+-ATPase was not colocalized with HGE agent inclusions but was weakly colocalized withE. chaffeensisinclusions.E. chaffeensisinclusions were labeled with the transferrin receptor, early endosomal antigen 1, and rab5, but HGE agent inclusions were not. Some HGE agent andE. chaffeensisinclusions colocalized with major histocompatibility complex class I and II antigens. These two inclusions were not labeled for annexins I, II, IV, and VI; α-adaptin; clathrin heavy chain; or β-coatomer protein. Vesicle-associated membrane protein 2 colocalized to both inclusions. The cation-independent mannose 6-phosphate receptor was not colocalized with either inclusion type. Endogenously synthesized sphingomyelin, from C6-NBD-ceramide, was not incorporated into either inclusion type. Brefeldin A did not affect the growth of eitherEhrlichiasp. in HL-60 cells. These results suggest that the HGE agent resides in inclusions which are neither early nor late endosomes and does not fuse with lysosomes or Golgi-derived vesicles, whileE. chaffeensisresides in an early endosomal compartment which accumulates the transferrin receptor.

Bibliography

Mott, J., Barnewall, R. E., & Rikihisa, Y. (1999). Human Granulocytic Ehrlichiosis Agent andEhrlichia chaffeensisReside in Different Cytoplasmic Compartments in HL-60 Cells. Infection and Immunity, 67(3), 1368â1378.

Authors 3

Jason Mott (first)
Roy E. Barnewall (additional)
Yasuko Rikihisa (additional)

References 56 Referenced 100

10.1038/369113a0
10.1073/pnas.81.15.4838
10.1007/BF01701530
10.1001/jama.1994.03520030054028
10.1128/iai.65.4.1497-1504.1997
Barnewall R. E. N. Ohashi and Y. Rikihisa. Ehrlichia chaffeensis and E. sennetsu reside in transferrin endosomes and up-regulate transferrin receptor mRNA by activating IRP1; however the HGE agent does not. Submitted for publication.
10.1128/iai.65.4.1455-1461.1997
10.1083/jcb.99.2.734
10.1016/S0140-6736(95)91544-3
Brummel J. H. Volchuk A. Sengelov H. Borregaard N. Cieutat A.-M. Bainton D. F. Grinstein S. Klip A. Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments.J. Immunol.155199557505759 (10.4049/jimmunol.155.12.5750) / J. Immunol. / Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments by Brummel J. H. (1995)
Chen J. W. Chen G. L. D’Souza M. P. Murphy T. L. August J. T. Lysosomal membrane glycoproteins: properties of LAMP-1 and LAMP-2.Biochem. Soc. Symp.51198697112 / Biochem. Soc. Symp. / Lysosomal membrane glycoproteins: properties of LAMP-1 and LAMP-2 by Chen J. W. (1986)
10.1128/jcm.32.3.589-595.1994
10.1084/jem.175.5.1317
10.1084/jem.181.1.257
10.1182/blood.V70.5.1233.1233
10.1038/283162a0
10.1128/jcm.29.12.2741-2745.1991
10.1016/0962-8924(91)90064-G
10.1016/0046-8177(93)90087-W
10.1093/infdis/175.3.720
10.1093/clinids/17.5.903
10.1093/infdis/173.4.1027
10.1016/S0021-9258(19)81393-5
10.1016/0092-8674(84)90315-5
10.1083/jcb.107.6.2491
10.1128/iai.64.3.796-809.1996
10.1091/mbc.4.12.1251
10.1086/517332
10.1016/0092-8674(91)90534-6
10.1073/pnas.80.9.2608
10.1016/S0021-9258(17)45332-4
10.1128/iai.62.1.126-134.1994
Marquez-Sterling N. I. Herman I. M. Pesacreta T. Arai H. Terres G. Forgac M. Immunolocalization of the vacuolar-type (H+)-ATPase from clathrin-coated vesicles.Eur. J. Cell Biol.5619911933 / Eur. J. Cell Biol. / Immunolocalization of the vacuolar-type (H+)-ATPase from clathrin-coated vesicles by Marquez-Sterling N. I. (1991)
10.1128/iai.61.9.3803-3810.1993
10.1128/iai.62.8.3156-3161.1994
10.1016/S0962-8924(96)10049-0
10.1074/jbc.270.22.13503
10.1152/physrev.1997.77.3.759
10.1016/0092-8674(90)90224-3
10.1128/jcm.35.10.2496-2502.1997
10.1128/jcm.35.6.1556-1559.1997
10.1099/00222615-47-3-235
10.1128/CMR.4.3.286
Rikihisa Y. Ehrlichiae Proceedings of the 5th International Symposium on Rickettsiae and Rickettsial Diseases. 1996 272 286 International Society for Rickettsiae and Rickettsial Diseases Slovak Academy of Sciences Bratislava Slovak Republic
10.1093/infdis/175.1.210
10.1128/iai.62.11.5126-5132.1994
10.1128/iai.63.6.2310-2316.1995
10.1038/372055a0
10.1038/28879
10.1126/science.8303277
10.1016/S0962-8924(96)20042-X
10.1128/iai.65.2.758-766.1997
10.1101/SQB.1995.060.01.024
10.1128/jb.170.11.5012-5017.1988
10.1128/iai.56.12.3209-3215.1988
Wormser G. Mckenna D. Aguero-Rosenfeld M. Human granulocytic ehrlichiosis—New York.Morbid. Mortal. Weekly Rep.441995593595 / Morbid. Mortal. Weekly Rep. / Human granulocytic ehrlichiosis—New York by Wormser G. (1995)

Dates

Type	When
Created	5 years, 7 months ago (Dec. 31, 2019, 10:33 a.m.)
Deposited	1 year, 11 months ago (Sept. 24, 2023, 10:38 a.m.)
Indexed	4 months, 4 weeks ago (March 29, 2025, 1:25 p.m.)
Issued	26 years, 5 months ago (March 1, 1999)
Published	26 years, 5 months ago (March 1, 1999)
Published Print	26 years, 5 months ago (March 1, 1999)

Funders 0

None

BibTeX

@article{Mott_1999, title={Human Granulocytic Ehrlichiosis Agent andEhrlichia chaffeensisReside in Different Cytoplasmic Compartments in HL-60 Cells}, volume={67}, ISSN={1098-5522}, url={http://dx.doi.org/10.1128/iai.67.3.1368-1378.1999}, DOI={10.1128/iai.67.3.1368-1378.1999}, number={3}, journal={Infection and Immunity}, publisher={American Society for Microbiology}, author={Mott, Jason and Barnewall, Roy E. and Rikihisa, Yasuko}, editor={Orndorff, P. E.}, year={1999}, month=mar, pages={1368–1378} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        3,
        29
      ]
    ],
    "date-time": "2025-03-29T17:25:03Z",
    "timestamp": 1743269103537
  },
  "reference-count": 56,
  "publisher": "American Society for Microbiology",
  "issue": "3",
  "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><jats:p>The human granulocytic ehrlichiosis (HGE) agent resides and multiplies exclusively in cytoplasmic vacuoles of granulocytes. Double immunofluorescence labeling was used to characterize the nature of the HGE agent replicative inclusions and to compare them with inclusions containing the human monocytic ehrlichia,<jats:italic>Ehrlichia chaffeensis</jats:italic>, in HL-60 cells. Although both<jats:italic>Ehrlichia</jats:italic>spp. can coinfect HL-60 cells, they resided in separate inclusions. Inclusions of both<jats:italic>Ehrlichia</jats:italic>spp. were not labeled with either anti-lysosome-associated membrane protein 1 or anti-CD63. Accumulation of myeloperoxidase-positive granules were seen around HGE agent inclusions but not around<jats:italic>E. chaffeensis</jats:italic>inclusions. 3-(2,4-Dinitroanilino)-3\u2032-amino-<jats:italic>N</jats:italic>-methyldipropylamine and acridine orange were not localized to either inclusion type. Vacuolar-type H<jats:sup>+</jats:sup>-ATPase was not colocalized with HGE agent inclusions but was weakly colocalized with<jats:italic>E. chaffeensis</jats:italic>inclusions.<jats:italic>E. chaffeensis</jats:italic>inclusions were labeled with the transferrin receptor, early endosomal antigen 1, and rab5, but HGE agent inclusions were not. Some HGE agent and<jats:italic>E. chaffeensis</jats:italic>inclusions colocalized with major histocompatibility complex class I and II antigens. These two inclusions were not labeled for annexins I, II, IV, and VI; \u03b1-adaptin; clathrin heavy chain; or \u03b2-coatomer protein. Vesicle-associated membrane protein 2 colocalized to both inclusions. The cation-independent mannose 6-phosphate receptor was not colocalized with either inclusion type. Endogenously synthesized sphingomyelin, from C<jats:sub>6</jats:sub>-NBD-ceramide, was not incorporated into either inclusion type. Brefeldin A did not affect the growth of either<jats:italic>Ehrlichia</jats:italic>sp. in HL-60 cells. These results suggest that the HGE agent resides in inclusions which are neither early nor late endosomes and does not fuse with lysosomes or Golgi-derived vesicles, while<jats:italic>E. chaffeensis</jats:italic>resides in an early endosomal compartment which accumulates the transferrin receptor.</jats:p>",
  "DOI": "10.1128/iai.67.3.1368-1378.1999",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2019,
        12,
        31
      ]
    ],
    "date-time": "2019-12-31T15:33:52Z",
    "timestamp": 1577806432000
  },
  "page": "1368-1378",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 100,
  "title": "Human Granulocytic Ehrlichiosis Agent and<i>Ehrlichia chaffeensis</i>Reside in Different Cytoplasmic Compartments in HL-60 Cells",
  "prefix": "10.1128",
  "volume": "67",
  "author": [
    {
      "given": "Jason",
      "family": "Mott",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio 43210-1092"
        }
      ]
    },
    {
      "given": "Roy E.",
      "family": "Barnewall",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio 43210-1092"
        }
      ]
    },
    {
      "given": "Yasuko",
      "family": "Rikihisa",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Veterinary Biosciences, College of Veterinary Medicine, The Ohio State University, Columbus, Ohio 43210-1092"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/369113a0"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.81.15.4838"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF01701530"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1001/jama.1994.03520030054028"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.4.1497-1504.1997"
    },
    {
      "key": "e_1_3_2_7_2",
      "unstructured": "Barnewall R. E. N. Ohashi and Y. Rikihisa. Ehrlichia chaffeensis and E. sennetsu reside in transferrin endosomes and up-regulate transferrin receptor mRNA by activating IRP1; however the HGE agent does not. Submitted for publication."
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.4.1455-1461.1997"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.99.2.734"
    },
    {
      "key": "e_1_3_2_10_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0140-6736(95)91544-3"
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "crossref",
      "first-page": "5750",
      "DOI": "10.4049/jimmunol.155.12.5750",
      "article-title": "Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments",
      "volume": "155",
      "author": "Brummel J. H.",
      "year": "1995",
      "unstructured": "Brummel J. H. Volchuk A. Sengelov H. Borregaard N. Cieutat A.-M. Bainton D. F. Grinstein S. Klip A. Subcellular distribution of docking/fusion proteins in neutrophils, secretory cells with multiple exocytic compartments.J. Immunol.155199557505759",
      "journal-title": "J. Immunol."
    },
    {
      "key": "e_1_3_2_12_2",
      "first-page": "97",
      "article-title": "Lysosomal membrane glycoproteins: properties of LAMP-1 and LAMP-2",
      "volume": "51",
      "author": "Chen J. W.",
      "year": "1986",
      "unstructured": "Chen J. W. Chen G. L. D\u2019Souza M. P. Murphy T. L. August J. T. Lysosomal membrane glycoproteins: properties of LAMP-1 and LAMP-2.Biochem. Soc. Symp.51198697112",
      "journal-title": "Biochem. Soc. Symp."
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jcm.32.3.589-595.1994"
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.175.5.1317"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.181.1.257"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1182/blood.V70.5.1233.1233"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/283162a0"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jcm.29.12.2741-2745.1991"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0962-8924(91)90064-G"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0046-8177(93)90087-W"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/175.3.720"
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/clinids/17.5.903"
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/173.4.1027"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(19)81393-5"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(84)90315-5"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1083/jcb.107.6.2491"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.64.3.796-809.1996"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.4.12.1251"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1086/517332"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(91)90534-6"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.80.9.2608"
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(17)45332-4"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.1.126-134.1994"
    },
    {
      "key": "e_1_3_2_34_2",
      "first-page": "19",
      "article-title": "Immunolocalization of the vacuolar-type (H+)-ATPase from clathrin-coated vesicles",
      "volume": "56",
      "author": "Marquez-Sterling N. I.",
      "year": "1991",
      "unstructured": "Marquez-Sterling N. I. Herman I. M. Pesacreta T. Arai H. Terres G. Forgac M. Immunolocalization of the vacuolar-type (H+)-ATPase from clathrin-coated vesicles.Eur. J. Cell Biol.5619911933",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.61.9.3803-3810.1993"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.8.3156-3161.1994"
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0962-8924(96)10049-0"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.270.22.13503"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/physrev.1997.77.3.759"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(90)90224-3"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jcm.35.10.2496-2502.1997"
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jcm.35.6.1556-1559.1997"
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/00222615-47-3-235"
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/CMR.4.3.286"
    },
    {
      "key": "e_1_3_2_45_2",
      "unstructured": "Rikihisa Y. Ehrlichiae Proceedings of the 5th International Symposium on Rickettsiae and Rickettsial Diseases. 1996 272 286 International Society for Rickettsiae and Rickettsial Diseases Slovak Academy of Sciences Bratislava Slovak Republic"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/175.1.210"
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.62.11.5126-5132.1994"
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.63.6.2310-2316.1995"
    },
    {
      "key": "e_1_3_2_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/372055a0"
    },
    {
      "key": "e_1_3_2_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/28879"
    },
    {
      "key": "e_1_3_2_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8303277"
    },
    {
      "key": "e_1_3_2_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0962-8924(96)20042-X"
    },
    {
      "key": "e_1_3_2_53_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.65.2.758-766.1997"
    },
    {
      "key": "e_1_3_2_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1101/SQB.1995.060.01.024"
    },
    {
      "key": "e_1_3_2_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.170.11.5012-5017.1988"
    },
    {
      "key": "e_1_3_2_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/iai.56.12.3209-3215.1988"
    },
    {
      "key": "e_1_3_2_57_2",
      "first-page": "593",
      "article-title": "Human granulocytic ehrlichiosis\u2014New York",
      "volume": "44",
      "author": "Wormser G.",
      "year": "1995",
      "unstructured": "Wormser G. Mckenna D. Aguero-Rosenfeld M. Human granulocytic ehrlichiosis\u2014New York.Morbid. Mortal. Weekly Rep.441995593595",
      "journal-title": "Morbid. Mortal. Weekly Rep."
    }
  ],
  "container-title": "Infection and Immunity",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.67.3.1368-1378.1999",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/IAI.67.3.1368-1378.1999",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        9,
        24
      ]
    ],
    "date-time": "2023-09-24T14:38:22Z",
    "timestamp": 1695566302000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/IAI.67.3.1368-1378.1999"
    }
  },
  "subtitle": [],
  "editor": [
    {
      "given": "P. E.",
      "family": "Orndorff",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        3
      ]
    ]
  },
  "references-count": 56,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1999,
          3
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/IAI.67.3.1368-1378.1999"
  ],
  "URL": "http://dx.doi.org/10.1128/IAI.67.3.1368-1378.1999",
  "relation": {},
  "ISSN": [
    "0019-9567",
    "1098-5522"
  ],
  "subject": [],
  "container-title-short": "Infect Immun",
  "published": {
    "date-parts": [
      [
        1999,
        3
      ]
    ]
  },
  "assertion": [
    {
      "value": "1998-08-19",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1998-11-18",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1999-03-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}