DOI: 10.1177/096120339200100308. DNA Binding to Mouse Cells is Mediated by Cell-Surface Molecules: The Role of These DNA-Binding Molecules as Target Antigens in Murine Lupus

DNA Binding to Mouse Cells is Mediated by Cell-Surface Molecules: The Role of These DNA-Binding Molecules as Target Antigens in Murine Lupus

10.1177/096120339200100308

Crossref journal-article

SAGE Publications

Lupus (179)

Abstract

Autoimmunity to a 28-29-kDa cell-surface DNA-binding molecule has previously been described in patients with systemic lupus erythematosus and related autoimmune diseases. This report describes experiments that implicate a similar antigen-antibody system in the evolution of autoimmunity in lupus-prone mice. DNA binding to murine spleen cells was found to be a saturable phenomenon that was inhibited by excess cold DNA and trypsinization. The role of autoimmunity to murine cell-surface DNA-binding molecules in lupus-prone mice (MRL lpr/lpr, MRL + / +, BXSB) was compared to normal mice (BALB/c, C3H.SW) by means of an assay that measured the inhibition of cell-surface DNA binding. Only sera from lupus strains had inhibitory activity and this component was shown to be an IgM autoantibody. Furthermore, we isolated a spontaneously occurring IgM monoclonal antibody from the spleen of an MRL/lpr mouse, which inhibited DNA binding to mouse cells. Time-course studies indicated that young female MRL/lpr mice lacked detectable activity against cell- surface DNA-binding molecules; however, by 8-10 weeks maximal inhibitory activity was observed. This response occurred prior to the development of significant antinuclear antibody activity. With the appearance of overt disease and anti-DNA antibodies, inhibition of DNA- binding activity became undetectable. These findings mirror previous studies on autoimmunity to a cell-surface DNA-binding molecule on human leucocytes, but have the added advantage of permitting the study of the temporal evolution of this inhibitory activity in relation to disease expression.

Bibliography

Hefeneider, S. H., McCoy, S. L., Morton, J. I., Bakke, A. C., Cornell, K. A., Brown, L. E., & Bennett, R. M. (1992). DNA Binding to Mouse Cells is Mediated by Cell-Surface Molecules: The Role of These DNA-Binding Molecules as Target Antigens in Murine Lupus. Lupus, 1(3), 167â173.

Authors 7

Steven H. Hefeneider (first)
Sharon L. McCoy (additional)
Jane I. Morton (additional)
Antony C. Bakke (additional)
Kenneth A. Cornell (additional)
Lisa E. Brown (additional)
Robert M. Bennett (additional)

References 34 Referenced 21

10.1016/S0065-2776(08)60836-6
10.4049/jimmunol.129.2.582 / J Immunol by Okudaira K. (1982)
{'key': 'atypb3', 'first-page': '119', 'volume': '6', 'author': 'Agnello V.', 'year': '1976', 'journal-title': 'Adv Nephrol'} / Adv Nephrol by Agnello V. (1976)
10.1002/art.1780291201
{'key': 'atypb5', 'first-page': '362', 'volume': '16', 'author': 'Lies RB', 'year': '1973', 'journal-title': 'Arthritis Rheum'} / Arthritis Rheum by Lies RB (1973)
10.1172/JCI111261
10.1002/art.1780230301
10.1016/S0074-7696(08)61994-4
10.1016/S0074-7696(08)61258-9
10.1073/pnas.68.6.1212
10.1016/0022-2836(73)90427-0
10.1016/0022-2836(74)90352-0
{'key': 'atypb13', 'first-page': '679', 'volume': '13', 'author': 'Bennett RM', 'year': '1986', 'journal-title': 'J Rheumatol'} / J Rheumatol by Bennett RM (1986)
10.4049/jimmunol.127.1.98 / J Immunol by Pancer LB (1981)
10.1172/JCI109036
10.1172/JCI112226
{'key': 'atypb17', 'first-page': '1034', 'volume': '122', 'author': 'Gabor G.', 'year': '1984', 'journal-title': 'Comm'} / Comm by Gabor G. (1984)
10.4049/jimmunol.140.9.2937 / J Immunol by Bennett RM (1988)
{'key': 'atypb19', 'first-page': '54', 'volume': '133', 'author': 'Emlen W.', 'year': '1988', 'journal-title': 'Am J Pathol'} / Am J Pathol by Emlen W. (1988)
10.1111/j.1751-1097.1990.tb04187.x
10.1073/pnas.86.10.3474
10.1073/pnas.86.17.6454
10.1172/JCI114838
10.1016/S0140-6736(86)90656-2
10.1084/jem.166.4.850
10.1093/ajcp/66.4.743
{'key': 'atypb27', 'first-page': '457', 'volume': '22', 'author': 'Siegle BV', 'year': '1972', 'journal-title': 'Immunol'} / Immunol by Siegle BV (1972)
10.4049/jimmunol.140.7.2431 / J Immunol by Harel-Bellan A. (1988)
10.1111/1523-1747.ep12875170
{'journal-title': 'Clin Exp Immunol', 'author': 'Bennett RM', 'key': 'atypb30'} / Clin Exp Immunol by Bennett RM
{'key': 'atypb31', 'first-page': '87', 'volume': '32', 'author': 'Sudar F.', 'year': '1986', 'journal-title': 'Cell Mol Biol'} / Cell Mol Biol by Sudar F. (1986)
10.1172/JCI114595
10.1172/JCI114716
{'key': 'atypb34', 'first-page': 'R15', 'volume': '34', 'author': 'Hefeneider SH', 'year': '1991', 'journal-title': 'Arthritis Rheum'} / Arthritis Rheum by Hefeneider SH (1991)

Dates

Type	When
Created	17 years, 9 months ago (Nov. 26, 2007, 7:27 p.m.)
Deposited	6 months ago (Feb. 28, 2025, 12:51 p.m.)
Indexed	1 month ago (Aug. 2, 2025, 12:39 a.m.)
Issued	33 years, 4 months ago (May 1, 1992)
Published	33 years, 4 months ago (May 1, 1992)
Published Online	33 years, 4 months ago (May 1, 1992)
Published Print	33 years, 4 months ago (May 1, 1992)

Funders 0

None

BibTeX

@article{Hefeneider_1992, title={DNA Binding to Mouse Cells is Mediated by Cell-Surface Molecules: The Role of These DNA-Binding Molecules as Target Antigens in Murine Lupus}, volume={1}, ISSN={1477-0962}, url={http://dx.doi.org/10.1177/096120339200100308}, DOI={10.1177/096120339200100308}, number={3}, journal={Lupus}, publisher={SAGE Publications}, author={Hefeneider, Steven H. and McCoy, Sharon L. and Morton, Jane I. and Bakke, Antony C. and Cornell, Kenneth A. and Brown, Lisa E. and Bennett, Robert M.}, year={1992}, month=may, pages={167–173} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        2
      ]
    ],
    "date-time": "2025-08-02T04:39:53Z",
    "timestamp": 1754109593883,
    "version": "3.38.0"
  },
  "reference-count": 34,
  "publisher": "SAGE Publications",
  "issue": "3",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            1992,
            5,
            1
          ]
        ],
        "date-time": "1992-05-01T00:00:00Z",
        "timestamp": 704678400000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "https://journals.sagepub.com/page/policies/text-and-data-mining-license"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        1992,
        5
      ]
    ]
  },
  "abstract": "<jats:p> Autoimmunity to a 28-29-kDa cell-surface DNA-binding molecule has previously been described in patients with systemic lupus erythematosus and related autoimmune diseases. This report describes experiments that implicate a similar antigen-antibody system in the evolution of autoimmunity in lupus-prone mice. DNA binding to murine spleen cells was found to be a saturable phenomenon that was inhibited by excess cold DNA and trypsinization. The role of autoimmunity to murine cell-surface DNA-binding molecules in lupus-prone mice (MRL lpr/lpr, MRL + / +, BXSB) was compared to normal mice (BALB/c, C3H.SW) by means of an assay that measured the inhibition of cell-surface DNA binding. Only sera from lupus strains had inhibitory activity and this component was shown to be an IgM autoantibody. Furthermore, we isolated a spontaneously occurring IgM monoclonal antibody from the spleen of an MRL/lpr mouse, which inhibited DNA binding to mouse cells. Time-course studies indicated that young female MRL/lpr mice lacked detectable activity against cell- surface DNA-binding molecules; however, by 8-10 weeks maximal inhibitory activity was observed. This response occurred prior to the development of significant antinuclear antibody activity. With the appearance of overt disease and anti-DNA antibodies, inhibition of DNA- binding activity became undetectable. These findings mirror previous studies on autoimmunity to a cell-surface DNA-binding molecule on human leucocytes, but have the added advantage of permitting the study of the temporal evolution of this inhibitory activity in relation to disease expression. </jats:p>",
  "DOI": "10.1177/096120339200100308",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2007,
        11,
        27
      ]
    ],
    "date-time": "2007-11-27T00:27:11Z",
    "timestamp": 1196123231000
  },
  "page": "167-173",
  "source": "Crossref",
  "is-referenced-by-count": 21,
  "title": "DNA Binding to Mouse Cells is Mediated by Cell-Surface Molecules: The Role of These DNA-Binding Molecules as Target Antigens in Murine Lupus",
  "prefix": "10.1177",
  "volume": "1",
  "author": [
    {
      "given": "Steven H.",
      "family": "Hefeneider",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Immunology, Veterans Affairs Medical Center, and Department of Medicine and Clinical Pathology, Oregon Health Sciences University, Portland, Oregon, USA"
        }
      ]
    },
    {
      "given": "Sharon L.",
      "family": "McCoy",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Immunology, Veterans Affairs Medical Center, and Department of Medicine and Clinical Pathology, Oregon Health Sciences University, Portland, Oregon, USA"
        }
      ]
    },
    {
      "given": "Jane I.",
      "family": "Morton",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Immunology, Veterans Affairs Medical Center, and Department of Medicine and Clinical Pathology, Oregon Health Sciences University, Portland, Oregon, USA"
        }
      ]
    },
    {
      "given": "Antony C.",
      "family": "Bakke",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Immunology, Veterans Affairs Medical Center, and Department of Medicine and Clinical Pathology, Oregon Health Sciences University, Portland, Oregon, USA"
        }
      ]
    },
    {
      "given": "Kenneth A.",
      "family": "Cornell",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Immunology, Veterans Affairs Medical Center, and Department of Medicine and Clinical Pathology, Oregon Health Sciences University, Portland, Oregon, USA"
        }
      ]
    },
    {
      "given": "Lisa E.",
      "family": "Brown",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Immunology, Veterans Affairs Medical Center, and Department of Medicine and Clinical Pathology, Oregon Health Sciences University, Portland, Oregon, USA"
        }
      ]
    },
    {
      "given": "Robert M.",
      "family": "Bennett",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Immunology, Veterans Affairs Medical Center, and Department of Medicine and Clinical Pathology, Oregon Health Sciences University, Portland, Oregon, USA"
        }
      ]
    }
  ],
  "member": "179",
  "published-online": {
    "date-parts": [
      [
        1992,
        5,
        1
      ]
    ]
  },
  "reference": [
    {
      "key": "atypb1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0065-2776(08)60836-6"
    },
    {
      "key": "atypb2",
      "doi-asserted-by": "crossref",
      "first-page": "582",
      "DOI": "10.4049/jimmunol.129.2.582",
      "volume": "129",
      "author": "Okudaira K.",
      "year": "1982",
      "journal-title": "J Immunol"
    },
    {
      "key": "atypb3",
      "first-page": "119",
      "volume": "6",
      "author": "Agnello V.",
      "year": "1976",
      "journal-title": "Adv Nephrol"
    },
    {
      "key": "atypb4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/art.1780291201"
    },
    {
      "key": "atypb5",
      "first-page": "362",
      "volume": "16",
      "author": "Lies RB",
      "year": "1973",
      "journal-title": "Arthritis Rheum"
    },
    {
      "key": "atypb6",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI111261"
    },
    {
      "key": "atypb7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1002/art.1780230301"
    },
    {
      "key": "atypb8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0074-7696(08)61994-4"
    },
    {
      "key": "atypb9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0074-7696(08)61258-9"
    },
    {
      "key": "atypb10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.68.6.1212"
    },
    {
      "key": "atypb11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(73)90427-0"
    },
    {
      "key": "atypb12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/0022-2836(74)90352-0"
    },
    {
      "key": "atypb13",
      "first-page": "679",
      "volume": "13",
      "author": "Bennett RM",
      "year": "1986",
      "journal-title": "J Rheumatol"
    },
    {
      "key": "atypb14",
      "doi-asserted-by": "crossref",
      "first-page": "98",
      "DOI": "10.4049/jimmunol.127.1.98",
      "volume": "127",
      "author": "Pancer LB",
      "year": "1981",
      "journal-title": "J Immunol"
    },
    {
      "key": "atypb15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI109036"
    },
    {
      "key": "atypb16",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI112226"
    },
    {
      "key": "atypb17",
      "first-page": "1034",
      "volume": "122",
      "author": "Gabor G.",
      "year": "1984",
      "journal-title": "Comm"
    },
    {
      "key": "atypb18",
      "doi-asserted-by": "crossref",
      "first-page": "2937",
      "DOI": "10.4049/jimmunol.140.9.2937",
      "volume": "140",
      "author": "Bennett RM",
      "year": "1988",
      "journal-title": "J Immunol"
    },
    {
      "key": "atypb19",
      "first-page": "54",
      "volume": "133",
      "author": "Emlen W.",
      "year": "1988",
      "journal-title": "Am J Pathol"
    },
    {
      "key": "atypb20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/j.1751-1097.1990.tb04187.x"
    },
    {
      "key": "atypb21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.10.3474"
    },
    {
      "key": "atypb22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.86.17.6454"
    },
    {
      "key": "atypb23",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI114838"
    },
    {
      "key": "atypb24",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0140-6736(86)90656-2"
    },
    {
      "key": "atypb25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1084/jem.166.4.850"
    },
    {
      "key": "atypb26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/ajcp/66.4.743"
    },
    {
      "key": "atypb27",
      "first-page": "457",
      "volume": "22",
      "author": "Siegle BV",
      "year": "1972",
      "journal-title": "Immunol"
    },
    {
      "key": "atypb28",
      "doi-asserted-by": "crossref",
      "first-page": "2431",
      "DOI": "10.4049/jimmunol.140.7.2431",
      "volume": "140",
      "author": "Harel-Bellan A.",
      "year": "1988",
      "journal-title": "J Immunol"
    },
    {
      "key": "atypb29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1111/1523-1747.ep12875170"
    },
    {
      "journal-title": "Clin Exp Immunol",
      "author": "Bennett RM",
      "key": "atypb30"
    },
    {
      "key": "atypb31",
      "first-page": "87",
      "volume": "32",
      "author": "Sudar F.",
      "year": "1986",
      "journal-title": "Cell Mol Biol"
    },
    {
      "key": "atypb32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI114595"
    },
    {
      "key": "atypb33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1172/JCI114716"
    },
    {
      "key": "atypb34",
      "first-page": "R15",
      "volume": "34",
      "author": "Hefeneider SH",
      "year": "1991",
      "journal-title": "Arthritis Rheum"
    }
  ],
  "container-title": "Lupus",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://journals.sagepub.com/doi/pdf/10.1177/096120339200100308",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "https://journals.sagepub.com/doi/pdf/10.1177/096120339200100308",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2025,
        2,
        28
      ]
    ],
    "date-time": "2025-02-28T17:51:41Z",
    "timestamp": 1740765101000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://journals.sagepub.com/doi/10.1177/096120339200100308"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1992,
        5
      ]
    ]
  },
  "references-count": 34,
  "journal-issue": {
    "issue": "3",
    "published-print": {
      "date-parts": [
        [
          1992,
          5
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1177/096120339200100308"
  ],
  "URL": "http://dx.doi.org/10.1177/096120339200100308",
  "relation": {},
  "ISSN": [
    "0961-2033",
    "1477-0962"
  ],
  "subject": [],
  "container-title-short": "Lupus",
  "published": {
    "date-parts": [
      [
        1992,
        5
      ]
    ]
  }
}