DOI: 10.1128/jvi.72.3.1876-1885.1998. Neutralization Sensitivity of Human Immunodeficiency Virus Type 1 Primary Isolates to Antibodies and CD4-Based Reagents Is Independent of Coreceptor Usage

Neutralization Sensitivity of Human Immunodeficiency Virus Type 1 Primary Isolates to Antibodies and CD4-Based Reagents Is Independent of Coreceptor Usage

10.1128/jvi.72.3.1876-1885.1998

Crossref journal-article

American Society for Microbiology

Journal of Virology (235)

Abstract

ABSTRACT We have investigated whether the identity of the coreceptor (CCR5, CXCR4, or both) used by primary human immunodeficiency virus type 1 (HIV-1) isolates to enter CD4 + cells influences the sensitivity of these isolates to neutralization by monoclonal antibodies and CD4-based agents. Coreceptor usage was not an important determinant of neutralization titer for primary isolates in peripheral blood mononuclear cells. We also studied whether dualtropic primary isolates (able to use both CCR5 and CXCR4) were differentially sensitive to neutralization by the same antibodies when entering U87MG-CD4 cells stably expressing either CCR5 or CXCR4. Again, we found that the coreceptor used by a virus did not greatly affect its neutralization sensitivity. Similar results were obtained for CCR5- or CXCR4-expressing HOS cell lines engineered to express green fluorescent protein as a reporter of HIV-1 entry. Neutralizing antibodies are therefore unlikely to be the major selection pressure which drives the phenotypic evolution (change in coreceptor usage) of HIV-1 that can occur in vivo. In addition, the increase in neutralization sensitivity found when primary isolates adapt to growth in transformed cell lines in vitro has little to do with alterations in coreceptor usage.

Bibliography

Trkola, A., Ketas, T., KewalRamani, V. N., Endorf, F., Binley, J. M., Katinger, H., Robinson, J., Littman, D. R., & Moore, J. P. (1998). Neutralization Sensitivity of Human Immunodeficiency Virus Type 1 Primary Isolates to Antibodies and CD4-Based Reagents Is Independent of Coreceptor Usage. Journal of Virology, 72(3), 1876â1885.

Authors 9

Alexandra Trkola (first)
Tom Ketas (additional)
Vineet N. KewalRamani (additional)
Fred Endorf (additional)
James M. Binley (additional)
Hermann Katinger (additional)
Jim Robinson (additional)
Dan R. Littman (additional)
John P. Moore (additional)

References 107 Referenced 135

10.1128/jvi.59.2.284-291.1986
10.1128/jvi.69.2.1001-1012.1995
10.1097/00002030-199507000-00029
10.1126/science.272.5270.1955
10.1089/aid.1995.11.533
10.1089/aid.1996.12.1247
10.1128/jvi.68.7.4572-4579.1994
10.1038/382829a0
Burton D. R. and D. Montefiori. 1997. The antibody response in HIV-1 infection. AIDS 11 (Suppl. A) : 587–598.
10.1089/aid.1996.12.173
10.1128/jvi.66.11.6547-6554.1992
10.1016/S0092-8674(00)81313-6
10.1126/science.270.5243.1811
10.1038/nm1196-1244
10.1126/science.7824947
10.1128/jvi.66.12.7517-7521.1992
10.1128/jvi.68.7.4400-4408.1994
10.1084/jem.185.4.621
10.1128/jvi.69.3.1493-1499.1995
10.1128/jvi.69.3.1810-1818.1995
10.1073/pnas.87.17.6574
10.1128/jvi.66.11.6777-6780.1992
10.1038/381661a0
10.1038/40894
10.1038/385495a0
10.1016/S0092-8674(00)81314-8
10.1097/00042560-199612010-00002
10.1038/381667a0
10.1086/516443
10.1084/jem.186.3.405
10.1038/384529a0
10.1126/science.272.5263.872
10.1006/viro.1994.1534
10.1089/aid.1996.12.1585
10.1128/jvi.66.5.3183-3187.1992
10.1006/viro.1996.0225
10.1073/pnas.94.9.4653
10.1128/jvi.69.8.4628-4632.1995
10.1128/jvi.66.12.7538-7542.1992
10.1128/jvi.69.1.523-527.1995
10.1016/S0021-9258(17)46662-2
10.1128/jvi.71.9.6296-6304.1997
10.1128/jvi.65.1.489-493.1991
10.1128/jvi.69.10.6342-6351.1995
10.1128/jvi.70.6.3589-3598.1996
10.1093/infdis/170.6.1367
10.1128/jvi.70.9.6136-6142.1996
KewalRamani V. N. and D. R. Littman. Unpublished data.
10.1128/jvi.66.4.2232-2239.1992
10.1128/jvi.70.6.3668-3677.1996
10.7326/0003-4819-118-9-199305010-00004
10.1093/infdis/173.2.349
10.1128/jvi.71.2.873-882.1997
10.1128/JVI.72.3.2491-2495.1998
10.1084/jem.185.11.2015
10.1128/jvi.69.5.3167-3170.1995
10.1128/jvi.67.9.5623-5634.1993
10.1074/jbc.271.32.19084
Montefiori D. C. Personal communication.
10.1128/JVI.72.3.1886-1893.1998
10.1089/aid.1993.9.529
10.1128/jvi.69.1.101-109.1995
Moore J. P. and D. D. Ho. 1995. HIV-1 neutralization: the consequences of viral adaptation to growth on transformed T cells. AIDS 9 (Suppl. A) : S117–S136.
10.1128/jvi.68.12.8350-8364.1994
10.1128/jvi.66.1.235-243.1992
Moore J. P. and P. L. Nara. 1991. The role of the V3 domain of gp120 in HIV infection. AIDS 5 (Suppl. 2) : S21–S33. (10.1097/00002030-199101001-00004)
10.1128/jvi.69.1.122-130.1995
10.1089/aid.1993.9.1185
10.1016/S0021-9258(18)53154-9
10.1128/jvi.68.6.4031-4034.1994
10.1038/382833a0
10.1038/348069a0
10.1097/00002030-199509050-00003
10.1089/aid.1995.11.335
10.1016/0042-6822(91)90537-L
10.1128/jvi.71.2.883-890.1997
10.1093/infdis/169.5.968
10.1128/jvi.71.6.4847-4851.1997
Saag M. S. S. M. Hammer and J. M. A. Lange. 1994. Pathogenicity and diversity of HIV and implications for clinical management: a review. J. Acquired Immune Defic. Syndr. 7 (Suppl. 2) : S2–S11.
10.1084/jem.182.1.185
10.1128/jvi.68.3.1342-1349.1994
10.1006/viro.1993.1637
10.1128/jvi.66.3.1354-1360.1992
10.1099/0022-1317-76-7-1665
10.1093/infdis/173.6.1485
10.1128/jvi.69.7.4453-4462.1995
10.1038/349167a0
10.1089/aid.1994.10.1679
10.1073/pnas.91.4.1214
10.1128/jvi.70.12.8355-8360.1996
10.1093/infdis/169.3.491
10.1128/jvi.69.10.6191-6198.1995
10.1128/jvi.62.6.2026-2032.1988
10.1089/aid.1996.12.191
10.1038/384184a0
10.1128/jvi.70.2.1100-1108.1996
10.1128/jvi.69.11.6609-6617.1995
10.1073/pnas.89.4.1335
10.1006/viro.1997.8606
10.1002/jlb.59.1.53
10.1128/jvi.68.2.1029-1039.1994
10.1093/infdis/173.4.877
10.1128/jvi.69.1.39-48.1995
10.1038/384179a0
10.1084/jem.185.9.1681
10.1128/jvi.70.6.3724-3733.1996
10.1126/science.8356453

Dates

Type	When
Created	5 years, 8 months ago (Dec. 31, 2019, 1:08 p.m.)
Deposited	3 years, 6 months ago (March 4, 2022, 9:47 p.m.)
Indexed	4 months, 4 weeks ago (April 8, 2025, 5:42 p.m.)
Issued	27 years, 6 months ago (March 1, 1998)
Published	27 years, 6 months ago (March 1, 1998)
Published Print	27 years, 6 months ago (March 1, 1998)

Funders 0

None

BibTeX

@article{Trkola_1998, title={Neutralization Sensitivity of Human Immunodeficiency Virus Type 1 Primary Isolates to Antibodies and CD4-Based Reagents Is Independent of Coreceptor Usage}, volume={72}, ISSN={1098-5514}, url={http://dx.doi.org/10.1128/jvi.72.3.1876-1885.1998}, DOI={10.1128/jvi.72.3.1876-1885.1998}, number={3}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={Trkola, Alexandra and Ketas, Tom and KewalRamani, Vineet N. and Endorf, Fred and Binley, James M. and Katinger, Hermann and Robinson, Jim and Littman, Dan R. and Moore, John P.}, year={1998}, month=mar, pages={1876–1885} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        4,
        8
      ]
    ],
    "date-time": "2025-04-08T21:42:54Z",
    "timestamp": 1744148574435
  },
  "reference-count": 107,
  "publisher": "American Society for Microbiology",
  "issue": "3",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1998,
            3,
            1
          ]
        ],
        "date-time": "1998-03-01T00:00:00Z",
        "timestamp": 888710400000
      },
      "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,
        3
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            We have investigated whether the identity of the coreceptor (CCR5, CXCR4, or both) used by primary human immunodeficiency virus type 1 (HIV-1) isolates to enter CD4\n            <jats:sup>+</jats:sup>\n            cells influences the sensitivity of these isolates to neutralization by monoclonal antibodies and CD4-based agents. Coreceptor usage was not an important determinant of neutralization titer for primary isolates in peripheral blood mononuclear cells. We also studied whether dualtropic primary isolates (able to use both CCR5 and CXCR4) were differentially sensitive to neutralization by the same antibodies when entering U87MG-CD4 cells stably expressing either CCR5 or CXCR4. Again, we found that the coreceptor used by a virus did not greatly affect its neutralization sensitivity. Similar results were obtained for CCR5- or CXCR4-expressing HOS cell lines engineered to express green fluorescent protein as a reporter of HIV-1 entry. Neutralizing antibodies are therefore unlikely to be the major selection pressure which drives the phenotypic evolution (change in coreceptor usage) of HIV-1 that can occur in vivo. In addition, the increase in neutralization sensitivity found when primary isolates adapt to growth in transformed cell lines in vitro has little to do with alterations in coreceptor usage.\n          </jats:p>",
  "DOI": "10.1128/jvi.72.3.1876-1885.1998",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2019,
        12,
        31
      ]
    ],
    "date-time": "2019-12-31T18:08:34Z",
    "timestamp": 1577815714000
  },
  "page": "1876-1885",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 135,
  "title": "Neutralization Sensitivity of Human Immunodeficiency Virus Type 1 Primary Isolates to Antibodies and CD4-Based Reagents Is Independent of Coreceptor Usage",
  "prefix": "10.1128",
  "volume": "72",
  "author": [
    {
      "given": "Alexandra",
      "family": "Trkola",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Aaron Diamond AIDS Research Center, The Rockefeller University,1 and"
        }
      ]
    },
    {
      "given": "Tom",
      "family": "Ketas",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Aaron Diamond AIDS Research Center, The Rockefeller University,1 and"
        }
      ]
    },
    {
      "given": "Vineet N.",
      "family": "KewalRamani",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 2-->The Skirball Institute of BioMolecular Medicine, New York University School of Medicine,2"
        }
      ]
    },
    {
      "given": "Fred",
      "family": "Endorf",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Aaron Diamond AIDS Research Center, The Rockefeller University,1 and"
        }
      ]
    },
    {
      "given": "James M.",
      "family": "Binley",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Aaron Diamond AIDS Research Center, The Rockefeller University,1 and"
        }
      ]
    },
    {
      "given": "Hermann",
      "family": "Katinger",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 3-->Institute of Applied Microbiology, University of Agriculture, Vienna, Austria3; and"
        }
      ]
    },
    {
      "given": "Jim",
      "family": "Robinson",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 4-->Department of Pediatrics, Tulane University Medical Center, New Orleans, Louisiana 701124"
        }
      ]
    },
    {
      "given": "Dan R.",
      "family": "Littman",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 2-->The Skirball Institute of BioMolecular Medicine, New York University School of Medicine,2"
        },
        {
          "name": "<!--label omitted: 5-->Howard Hughes Medical Institute,5 New York, New York 10016;"
        }
      ]
    },
    {
      "given": "John P.",
      "family": "Moore",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Aaron Diamond AIDS Research Center, The Rockefeller University,1 and"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.59.2.284-291.1986"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.2.1001-1012.1995"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00002030-199507000-00029"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.272.5270.1955"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1995.11.533"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1996.12.1247"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.68.7.4572-4579.1994"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/382829a0"
    },
    {
      "key": "e_1_3_2_10_2",
      "unstructured": "Burton D. R. and D. Montefiori. 1997. The antibody response in HIV-1 infection. AIDS 11 (Suppl. A) : 587\u2013598."
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1996.12.173"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.11.6547-6554.1992"
    },
    {
      "key": "e_1_3_2_13_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81313-6"
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.270.5243.1811"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nm1196-1244"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.7824947"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.12.7517-7521.1992"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.68.7.4400-4408.1994"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.185.4.621"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.3.1493-1499.1995"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.3.1810-1818.1995"
    },
    {
      "key": "e_1_3_2_22_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.87.17.6574"
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.11.6777-6780.1992"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/381661a0"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/40894"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/385495a0"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0092-8674(00)81314-8"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00042560-199612010-00002"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/381667a0"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1086/516443"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.186.3.405"
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/384529a0"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.272.5263.872"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/viro.1994.1534"
    },
    {
      "key": "e_1_3_2_35_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1996.12.1585"
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.5.3183-3187.1992"
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/viro.1996.0225"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.94.9.4653"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.8.4628-4632.1995"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.12.7538-7542.1992"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.1.523-527.1995"
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(17)46662-2"
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.9.6296-6304.1997"
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.65.1.489-493.1991"
    },
    {
      "key": "e_1_3_2_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.10.6342-6351.1995"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.6.3589-3598.1996"
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/170.6.1367"
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.9.6136-6142.1996"
    },
    {
      "key": "e_1_3_2_49_2",
      "unstructured": "KewalRamani V. N. and D. R. Littman. Unpublished data."
    },
    {
      "key": "e_1_3_2_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.4.2232-2239.1992"
    },
    {
      "key": "e_1_3_2_51_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.6.3668-3677.1996"
    },
    {
      "key": "e_1_3_2_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.7326/0003-4819-118-9-199305010-00004"
    },
    {
      "key": "e_1_3_2_53_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/173.2.349"
    },
    {
      "key": "e_1_3_2_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.2.873-882.1997"
    },
    {
      "key": "e_1_3_2_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.72.3.2491-2495.1998"
    },
    {
      "key": "e_1_3_2_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.185.11.2015"
    },
    {
      "key": "e_1_3_2_57_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.5.3167-3170.1995"
    },
    {
      "key": "e_1_3_2_58_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.67.9.5623-5634.1993"
    },
    {
      "key": "e_1_3_2_59_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1074/jbc.271.32.19084"
    },
    {
      "key": "e_1_3_2_60_2",
      "unstructured": "Montefiori D. C. Personal communication."
    },
    {
      "key": "e_1_3_2_61_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.72.3.1886-1893.1998"
    },
    {
      "key": "e_1_3_2_62_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1993.9.529"
    },
    {
      "key": "e_1_3_2_63_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.1.101-109.1995"
    },
    {
      "key": "e_1_3_2_64_2",
      "unstructured": "Moore J. P. and D. D. Ho. 1995. HIV-1 neutralization: the consequences of viral adaptation to growth on transformed T cells. AIDS 9 (Suppl. A) : S117\u2013S136."
    },
    {
      "key": "e_1_3_2_65_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.68.12.8350-8364.1994"
    },
    {
      "key": "e_1_3_2_66_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.1.235-243.1992"
    },
    {
      "key": "e_1_3_2_67_2",
      "doi-asserted-by": "crossref",
      "unstructured": "Moore J. P. and P. L. Nara. 1991. The role of the V3 domain of gp120 in HIV infection. AIDS 5 (Suppl. 2) : S21\u2013S33.",
      "DOI": "10.1097/00002030-199101001-00004"
    },
    {
      "key": "e_1_3_2_68_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.1.122-130.1995"
    },
    {
      "key": "e_1_3_2_69_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1993.9.1185"
    },
    {
      "key": "e_1_3_2_70_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0021-9258(18)53154-9"
    },
    {
      "key": "e_1_3_2_71_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.68.6.4031-4034.1994"
    },
    {
      "key": "e_1_3_2_72_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/382833a0"
    },
    {
      "key": "e_1_3_2_73_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/348069a0"
    },
    {
      "key": "e_1_3_2_74_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1097/00002030-199509050-00003"
    },
    {
      "key": "e_1_3_2_75_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1995.11.335"
    },
    {
      "key": "e_1_3_2_76_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0042-6822(91)90537-L"
    },
    {
      "key": "e_1_3_2_77_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.2.883-890.1997"
    },
    {
      "key": "e_1_3_2_78_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/169.5.968"
    },
    {
      "key": "e_1_3_2_79_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.6.4847-4851.1997"
    },
    {
      "key": "e_1_3_2_80_2",
      "unstructured": "Saag M. S. S. M. Hammer and J. M. A. Lange. 1994. Pathogenicity and diversity of HIV and implications for clinical management: a review. J. Acquired Immune Defic. Syndr. 7 (Suppl. 2) : S2\u2013S11."
    },
    {
      "key": "e_1_3_2_81_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.182.1.185"
    },
    {
      "key": "e_1_3_2_82_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.68.3.1342-1349.1994"
    },
    {
      "key": "e_1_3_2_83_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/viro.1993.1637"
    },
    {
      "key": "e_1_3_2_84_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.3.1354-1360.1992"
    },
    {
      "key": "e_1_3_2_85_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/0022-1317-76-7-1665"
    },
    {
      "key": "e_1_3_2_86_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/173.6.1485"
    },
    {
      "key": "e_1_3_2_87_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.7.4453-4462.1995"
    },
    {
      "key": "e_1_3_2_88_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/349167a0"
    },
    {
      "key": "e_1_3_2_89_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1994.10.1679"
    },
    {
      "key": "e_1_3_2_90_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.91.4.1214"
    },
    {
      "key": "e_1_3_2_91_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.12.8355-8360.1996"
    },
    {
      "key": "e_1_3_2_92_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/169.3.491"
    },
    {
      "key": "e_1_3_2_93_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.10.6191-6198.1995"
    },
    {
      "key": "e_1_3_2_94_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.62.6.2026-2032.1988"
    },
    {
      "key": "e_1_3_2_95_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/aid.1996.12.191"
    },
    {
      "key": "e_1_3_2_96_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/384184a0"
    },
    {
      "key": "e_1_3_2_97_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.2.1100-1108.1996"
    },
    {
      "key": "e_1_3_2_98_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.11.6609-6617.1995"
    },
    {
      "key": "e_1_3_2_99_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.89.4.1335"
    },
    {
      "key": "e_1_3_2_100_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/viro.1997.8606"
    },
    {
      "key": "e_1_3_2_101_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/jlb.59.1.53"
    },
    {
      "key": "e_1_3_2_102_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.68.2.1029-1039.1994"
    },
    {
      "key": "e_1_3_2_103_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/infdis/173.4.877"
    },
    {
      "key": "e_1_3_2_104_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.1.39-48.1995"
    },
    {
      "key": "e_1_3_2_105_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/384179a0"
    },
    {
      "key": "e_1_3_2_106_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.185.9.1681"
    },
    {
      "key": "e_1_3_2_107_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.6.3724-3733.1996"
    },
    {
      "key": "e_1_3_2_108_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.8356453"
    }
  ],
  "container-title": "Journal of Virology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JVI.72.3.1876-1885.1998",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JVI.72.3.1876-1885.1998",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        3,
        5
      ]
    ],
    "date-time": "2022-03-05T02:47:45Z",
    "timestamp": 1646448465000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/JVI.72.3.1876-1885.1998"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1998,
        3
      ]
    ]
  },
  "references-count": 107,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1998,
          3
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/JVI.72.3.1876-1885.1998"
  ],
  "URL": "http://dx.doi.org/10.1128/JVI.72.3.1876-1885.1998",
  "relation": {},
  "ISSN": [
    "0022-538X",
    "1098-5514"
  ],
  "subject": [],
  "container-title-short": "J Virol",
  "published": {
    "date-parts": [
      [
        1998,
        3
      ]
    ]
  },
  "assertion": [
    {
      "value": "1997-09-15",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1997-12-04",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "1998-03-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}