DOI: 10.1128/jvi.75.21.10446-10454.2001. Role for the Adenovirus IVa2 Protein in Packaging of Viral DNA

Role for the Adenovirus IVa2 Protein in Packaging of Viral DNA

10.1128/jvi.75.21.10446-10454.2001

Crossref journal-article

American Society for Microbiology

Journal of Virology (235)

Abstract

ABSTRACT Although it has been demonstrated that the adenovirus IVa2 protein binds to the packaging domains on the viral chromosome and interacts with the viral L1 52/55-kDa protein, which is required for viral DNA packaging, there has been no direct evidence demonstrating that the IVa2 protein is involved in DNA packaging. To understand in greater detail the DNA packaging mechanisms of adenovirus, we have asked whether DNA packaging is serotype or subgroup specific. We found that Ad7 (subgroup B), Ad12 (subgroup A), and Ad17 (subgroup D) cannot complement the defect of an Ad5 (subgroup C) mutant, pm 8001, which does not package its DNA due to a mutation in the L1 52/55-kDa gene. This indicates that the DNA packaging systems of different serotypes cannot interact productively with Ad5 DNA. Based on this, a chimeric virus containing the Ad7 genome except for the inverted terminal repeats and packaging sequence from Ad5 was constructed. This chimeric virus replicates its DNA and synthesizes Ad7 proteins, but it cannot package its DNA in 293 cells or 293 cells expressing the Ad5 L1 52/55-kDa protein. However, this chimeric virus packages its DNA in 293 cells expressing the Ad5 IVa2 protein. These results indicate that the IVa2 protein plays a role in viral DNA packaging and that its function is serotype specific. Since this chimeric virus cannot package its own DNA, but produces all the components for packaging Ad7 DNA, it may be a more suitable helper virus for the growth of Ad7 gutted vectors for gene transfer.

Bibliography

Zhang, W., Low, J. A., Christensen, J. B., & Imperiale, M. J. (2001). Role for the Adenovirus IVa2 Protein in Packaging of Viral DNA. Journal of Virology, 75(21), 10446â10454.

Authors 4

Wei Zhang (first)
Jonathan A. Low (additional)
Joan B. Christensen (additional)
Michael J. Imperiale (additional)

References 60 Referenced 66

10.1128/JVI.72.2.926-933.1998
10.1128/jvi.71.3.2408-2416.1997
10.1128/mcb.6.6.2115-2124.1986
10.1128/jvi.71.12.9206-9213.1997
10.1128/jvi.70.9.6497-6501.1996
10.1128/jvi.70.7.4805-4810.1996
10.1073/pnas.94.5.1645
10.1128/JVI.72.7.6138-6145.1998
Clemens P. R. Kochanek S. Sunada Y. Chan S. Chen H. H. Campbell K. P. Caskey C. T. In vivo muscle gene transfer of full-length dystrophin with an adenoviral vector that lacks all viral genes.Gene Ther. 3 1996 965 972 / Gene Ther. / In vivo muscle gene transfer of full-length dystrophin with an adenoviral vector that lacks all viral genes by Clemens P. R. (1996)
10.1073/pnas.92.5.1401
10.1128/jvi.71.6.4626-4637.1997
D'Halluin J. C. Virus assembly.Curr. Top. Microbiol. Immunol. 199 Pt. 1 1995 47 66 / Curr. Top. Microbiol. Immunol. / Virus assembly by D'Halluin J. C. (1995)
10.1016/0042-6822(73)90404-2
10.1006/viro.1996.0088
10.1128/jvi.70.12.8934-8943.1996
10.1016/0092-8674(83)90011-9
10.1128/jvi.70.6.4173-4178.1996
10.1128/JVI.73.7.6048-6055.1999
10.1128/jvi.64.5.2047-2056.1990
10.1128/jvi.66.2.723-731.1992
Graham F. L. Prevec L. Manipulation of adenovirus vectors.Methods Mol. Biol. 7 1991 109 128 / Methods Mol. Biol. / Manipulation of adenovirus vectors by Graham F. L. (1991)
10.1099/0022-1317-36-1-59
10.1128/JVI.72.10.7860-7870.1998
10.1128/jvi.70.9.6463-6467.1996
10.1016/0092-8674(80)90325-6
10.1128/jvi.71.3.1842-1849.1997
10.1128/jvi.70.4.2378-2386.1996
10.1016/0022-2836(88)90438-X
10.1128/jvi.66.10.6133-6142.1992
10.1128/jvi.63.9.3612-3621.1989
10.1099/0022-1317-67-2-321
10.1016/0092-8674(83)90012-0
10.1128/mcb.4.5.867-874.1984
Jones N. Transcriptional modulation by the adenovirus E1A gene.Curr. Top. Microbiol. Immunol. 199 1995 59 80 / Curr. Top. Microbiol. Immunol. / Transcriptional modulation by the adenovirus E1A gene by Jones N. (1995)
10.1073/pnas.93.12.5731
10.1093/hmg/5.7.913
10.1016/0042-6822(75)90175-0
10.1128/JVI.72.3.2022-2032.1998
10.1128/jvi.70.3.1396-1405.1996
10.1016/0042-6822(68)90122-0
10.1093/nar/20.15.3881
10.1007/BF03402113
10.1128/JVI.75.1.45-51.2001
10.1073/pnas.93.24.13565
10.1128/jvi.71.5.3375-3384.1997
10.1128/JVI.72.8.6339-6347.1998
10.1128/jvi.44.2.530-537.1982
10.1128/jvi.37.1.139-147.1981
10.1073/pnas.80.21.6446
Thomas C. E. Schiedner G. Kochanek S. Castro M. G. Löwenstein P. R. Peripheral infection with adenovirus causes unexpected long-term brain inflammation in animals injected intracranially with first-generation, but not with high-capacity, adenovirus vectors: toward realistic long-term neurological gene therapy for chronic diseases.Proc. Natl. Acad. Sci. USA 97 2000 7482 7487 (10.1073/pnas.120474397) / Proc. Natl. Acad. Sci. USA / Peripheral infection with adenovirus causes unexpected long-term brain inflammation in animals injected intracranially with first-generation, but not with high-capacity, adenovirus vectors: toward realistic long-term neurological gene therapy for chronic diseases by Thomas C. E. (2000)
10.1089/104303401750148829
10.1016/0092-8674(77)90202-1
10.1128/jvi.68.7.4450-4457.1994
10.1038/sj.gt.3300404
10.1016/1074-7613(94)90074-4
10.1128/jvi.69.4.2004-2015.1995
10.1128/JVI.74.6.2687-2693.2000
10.1128/jvi.70.10.7030-7038.1996
10.1089/104303401750061249
10.1006/mthe.2000.0104

Dates

Type	When
Created	23 years, 1 month ago (July 27, 2002, 6:06 a.m.)
Deposited	3 years, 6 months ago (March 5, 2022, 1:27 a.m.)
Indexed	1 year, 2 months ago (June 6, 2024, 1:56 p.m.)
Issued	23 years, 10 months ago (Nov. 1, 2001)
Published	23 years, 10 months ago (Nov. 1, 2001)
Published Print	23 years, 10 months ago (Nov. 1, 2001)

Funders 0

None

BibTeX

@article{Zhang_2001, title={Role for the Adenovirus IVa2 Protein in Packaging of Viral DNA}, volume={75}, ISSN={1098-5514}, url={http://dx.doi.org/10.1128/jvi.75.21.10446-10454.2001}, DOI={10.1128/jvi.75.21.10446-10454.2001}, number={21}, journal={Journal of Virology}, publisher={American Society for Microbiology}, author={Zhang, Wei and Low, Jonathan A. and Christensen, Joan B. and Imperiale, Michael J.}, year={2001}, month=nov, pages={10446–10454} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        6,
        6
      ]
    ],
    "date-time": "2024-06-06T17:56:13Z",
    "timestamp": 1717696573578
  },
  "reference-count": 60,
  "publisher": "American Society for Microbiology",
  "issue": "21",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2001,
            11,
            1
          ]
        ],
        "date-time": "2001-11-01T00:00:00Z",
        "timestamp": 1004572800000
      },
      "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,
        11
      ]
    ]
  },
  "abstract": "<jats:title>ABSTRACT</jats:title>\n          <jats:p>\n            Although it has been demonstrated that the adenovirus IVa2 protein binds to the packaging domains on the viral chromosome and interacts with the viral L1 52/55-kDa protein, which is required for viral DNA packaging, there has been no direct evidence demonstrating that the IVa2 protein is involved in DNA packaging. To understand in greater detail the DNA packaging mechanisms of adenovirus, we have asked whether DNA packaging is serotype or subgroup specific. We found that Ad7 (subgroup B), Ad12 (subgroup A), and Ad17 (subgroup D) cannot complement the defect of an Ad5 (subgroup C) mutant,\n            <jats:italic>pm</jats:italic>\n            8001, which does not package its DNA due to a mutation in the L1 52/55-kDa gene. This indicates that the DNA packaging systems of different serotypes cannot interact productively with Ad5 DNA. Based on this, a chimeric virus containing the Ad7 genome except for the inverted terminal repeats and packaging sequence from Ad5 was constructed. This chimeric virus replicates its DNA and synthesizes Ad7 proteins, but it cannot package its DNA in 293 cells or 293 cells expressing the Ad5 L1 52/55-kDa protein. However, this chimeric virus packages its DNA in 293 cells expressing the Ad5 IVa2 protein. These results indicate that the IVa2 protein plays a role in viral DNA packaging and that its function is serotype specific. Since this chimeric virus cannot package its own DNA, but produces all the components for packaging Ad7 DNA, it may be a more suitable helper virus for the growth of Ad7 gutted vectors for gene transfer.\n          </jats:p>",
  "DOI": "10.1128/jvi.75.21.10446-10454.2001",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        27
      ]
    ],
    "date-time": "2002-07-27T10:06:37Z",
    "timestamp": 1027764397000
  },
  "page": "10446-10454",
  "update-policy": "http://dx.doi.org/10.1128/asmj-crossmark-policy-page",
  "source": "Crossref",
  "is-referenced-by-count": 66,
  "title": "Role for the Adenovirus IVa2 Protein in Packaging of Viral DNA",
  "prefix": "10.1128",
  "volume": "75",
  "author": [
    {
      "given": "Wei",
      "family": "Zhang",
      "sequence": "first",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology and Immunology, Center for Gene Therapy and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, Michigan 48109-0942"
        }
      ]
    },
    {
      "given": "Jonathan A.",
      "family": "Low",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology and Immunology, Center for Gene Therapy and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, Michigan 48109-0942"
        }
      ]
    },
    {
      "given": "Joan B.",
      "family": "Christensen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology and Immunology, Center for Gene Therapy and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, Michigan 48109-0942"
        }
      ]
    },
    {
      "given": "Michael J.",
      "family": "Imperiale",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "<!--label omitted: 1-->Department of Microbiology and Immunology, Center for Gene Therapy and Comprehensive Cancer Center, University of Michigan Medical School, Ann Arbor, Michigan 48109-0942"
        }
      ]
    }
  ],
  "member": "235",
  "reference": [
    {
      "key": "e_1_3_2_2_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.72.2.926-933.1998"
    },
    {
      "key": "e_1_3_2_3_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.3.2408-2416.1997"
    },
    {
      "key": "e_1_3_2_4_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/mcb.6.6.2115-2124.1986"
    },
    {
      "key": "e_1_3_2_5_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.12.9206-9213.1997"
    },
    {
      "key": "e_1_3_2_6_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.9.6497-6501.1996"
    },
    {
      "key": "e_1_3_2_7_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.7.4805-4810.1996"
    },
    {
      "key": "e_1_3_2_8_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.94.5.1645"
    },
    {
      "key": "e_1_3_2_9_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.72.7.6138-6145.1998"
    },
    {
      "key": "e_1_3_2_10_2",
      "first-page": "965",
      "article-title": "In vivo muscle gene transfer of full-length dystrophin with an adenoviral vector that lacks all viral genes",
      "volume": "3",
      "author": "Clemens P. R.",
      "year": "1996",
      "unstructured": "Clemens P. R. Kochanek S. Sunada Y. Chan S. Chen H. H. Campbell K. P. Caskey C. T. In vivo muscle gene transfer of full-length dystrophin with an adenoviral vector that lacks all viral genes.Gene Ther. 3 1996 965 972",
      "journal-title": "Gene Ther."
    },
    {
      "key": "e_1_3_2_11_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.92.5.1401"
    },
    {
      "key": "e_1_3_2_12_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.6.4626-4637.1997"
    },
    {
      "issue": "1",
      "key": "e_1_3_2_13_2",
      "first-page": "47",
      "article-title": "Virus assembly",
      "volume": "199",
      "author": "D'Halluin J. C.",
      "year": "1995",
      "unstructured": "D'Halluin J. C. Virus assembly.Curr. Top. Microbiol. Immunol. 199 Pt. 1 1995 47 66",
      "journal-title": "Curr. Top. Microbiol. Immunol."
    },
    {
      "key": "e_1_3_2_14_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0042-6822(73)90404-2"
    },
    {
      "key": "e_1_3_2_15_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/viro.1996.0088"
    },
    {
      "key": "e_1_3_2_16_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.12.8934-8943.1996"
    },
    {
      "key": "e_1_3_2_17_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(83)90011-9"
    },
    {
      "key": "e_1_3_2_18_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.6.4173-4178.1996"
    },
    {
      "key": "e_1_3_2_19_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.73.7.6048-6055.1999"
    },
    {
      "key": "e_1_3_2_20_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.64.5.2047-2056.1990"
    },
    {
      "key": "e_1_3_2_21_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.2.723-731.1992"
    },
    {
      "key": "e_1_3_2_22_2",
      "first-page": "109",
      "article-title": "Manipulation of adenovirus vectors",
      "volume": "7",
      "author": "Graham F. L.",
      "year": "1991",
      "unstructured": "Graham F. L. Prevec L. Manipulation of adenovirus vectors.Methods Mol. Biol. 7 1991 109 128",
      "journal-title": "Methods Mol. Biol."
    },
    {
      "key": "e_1_3_2_23_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/0022-1317-36-1-59"
    },
    {
      "key": "e_1_3_2_24_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.72.10.7860-7870.1998"
    },
    {
      "key": "e_1_3_2_25_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.9.6463-6467.1996"
    },
    {
      "key": "e_1_3_2_26_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(80)90325-6"
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.3.1842-1849.1997"
    },
    {
      "key": "e_1_3_2_28_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.4.2378-2386.1996"
    },
    {
      "key": "e_1_3_2_29_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(88)90438-X"
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.66.10.6133-6142.1992"
    },
    {
      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.63.9.3612-3621.1989"
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1099/0022-1317-67-2-321"
    },
    {
      "key": "e_1_3_2_33_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(83)90012-0"
    },
    {
      "key": "e_1_3_2_34_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/mcb.4.5.867-874.1984"
    },
    {
      "key": "e_1_3_2_35_2",
      "first-page": "59",
      "article-title": "Transcriptional modulation by the adenovirus E1A gene",
      "volume": "199",
      "author": "Jones N.",
      "year": "1995",
      "unstructured": "Jones N. Transcriptional modulation by the adenovirus E1A gene.Curr. Top. Microbiol. Immunol. 199 1995 59 80",
      "journal-title": "Curr. Top. Microbiol. Immunol."
    },
    {
      "key": "e_1_3_2_36_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.93.12.5731"
    },
    {
      "key": "e_1_3_2_37_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/hmg/5.7.913"
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0042-6822(75)90175-0"
    },
    {
      "key": "e_1_3_2_39_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.72.3.2022-2032.1998"
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.3.1396-1405.1996"
    },
    {
      "key": "e_1_3_2_41_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0042-6822(68)90122-0"
    },
    {
      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/nar/20.15.3881"
    },
    {
      "key": "e_1_3_2_43_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1007/BF03402113"
    },
    {
      "key": "e_1_3_2_44_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.75.1.45-51.2001"
    },
    {
      "key": "e_1_3_2_45_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.93.24.13565"
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.71.5.3375-3384.1997"
    },
    {
      "key": "e_1_3_2_47_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.72.8.6339-6347.1998"
    },
    {
      "key": "e_1_3_2_48_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.44.2.530-537.1982"
    },
    {
      "key": "e_1_3_2_49_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.37.1.139-147.1981"
    },
    {
      "key": "e_1_3_2_50_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.80.21.6446"
    },
    {
      "key": "e_1_3_2_51_2",
      "doi-asserted-by": "crossref",
      "first-page": "7482",
      "DOI": "10.1073/pnas.120474397",
      "article-title": "Peripheral infection with adenovirus causes unexpected long-term brain inflammation in animals injected intracranially with first-generation, but not with high-capacity, adenovirus vectors: toward realistic long-term neurological gene therapy for chronic diseases",
      "volume": "97",
      "author": "Thomas C. E.",
      "year": "2000",
      "unstructured": "Thomas C. E. Schiedner G. Kochanek S. Castro M. G. L\u00f6wenstein P. R. Peripheral infection with adenovirus causes unexpected long-term brain inflammation in animals injected intracranially with first-generation, but not with high-capacity, adenovirus vectors: toward realistic long-term neurological gene therapy for chronic diseases.Proc. Natl. Acad. Sci. USA 97 2000 7482 7487",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_52_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/104303401750148829"
    },
    {
      "key": "e_1_3_2_53_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0092-8674(77)90202-1"
    },
    {
      "key": "e_1_3_2_54_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.68.7.4450-4457.1994"
    },
    {
      "key": "e_1_3_2_55_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/sj.gt.3300404"
    },
    {
      "key": "e_1_3_2_56_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/1074-7613(94)90074-4"
    },
    {
      "key": "e_1_3_2_57_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.69.4.2004-2015.1995"
    },
    {
      "key": "e_1_3_2_58_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JVI.74.6.2687-2693.2000"
    },
    {
      "key": "e_1_3_2_59_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jvi.70.10.7030-7038.1996"
    },
    {
      "key": "e_1_3_2_60_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1089/104303401750061249"
    },
    {
      "key": "e_1_3_2_61_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1006/mthe.2000.0104"
    }
  ],
  "container-title": "Journal of Virology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JVI.75.21.10446-10454.2001",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.asm.org/doi/pdf/10.1128/JVI.75.21.10446-10454.2001",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2022,
        3,
        5
      ]
    ],
    "date-time": "2022-03-05T06:27:07Z",
    "timestamp": 1646461627000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.asm.org/doi/10.1128/JVI.75.21.10446-10454.2001"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        11
      ]
    ]
  },
  "references-count": 60,
  "journal-issue": {
    "issue": "21",
    "published-print": {
      "date-parts": [
        [
          2001,
          11
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1128/JVI.75.21.10446-10454.2001"
  ],
  "URL": "http://dx.doi.org/10.1128/JVI.75.21.10446-10454.2001",
  "relation": {},
  "ISSN": [
    "0022-538X",
    "1098-5514"
  ],
  "subject": [],
  "container-title-short": "J Virol",
  "published": {
    "date-parts": [
      [
        2001,
        11
      ]
    ]
  },
  "assertion": [
    {
      "value": "2001-06-21",
      "order": 0,
      "name": "received",
      "label": "Received",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2001-08-06",
      "order": 1,
      "name": "accepted",
      "label": "Accepted",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    },
    {
      "value": "2001-11-01",
      "order": 2,
      "name": "published",
      "label": "Published",
      "group": {
        "name": "publication_history",
        "label": "Publication History"
      }
    }
  ]
}