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. 1993 Oct;67(10):6025–6032. doi: 10.1128/jvi.67.10.6025-6032.1993

Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus.

D Naniche 1, G Varior-Krishnan 1, F Cervoni 1, T F Wild 1, B Rossi 1, C Rabourdin-Combe 1, D Gerlier 1
PMCID: PMC238023  PMID: 8371352

Abstract

A monoclonal antibody (MCI20.6) which inhibited measles virus (MV) binding to host cells was previously used to characterize a 57- to 67-kDa cell surface glycoprotein as a potential MV receptor. In the present work, this glycoprotein (gp57/67) was immunopurified, and N-terminal amino acid sequencing identified it as human membrane cofactor protein (CD46), a member of the regulators of complement activation gene cluster. Transfection of nonpermissive murine cells with a recombinant expression vector containing CD46 cDNA conferred three major properties expected of cells permissive to MV infection. First, expression of CD46 enabled MV to bind to murine cells. Second, the CD46-expressing murine cells were able to undergo cell-cell fusion when both MV hemagglutinin and MV fusion glycoproteins were expressed after infection with a vaccinia virus recombinant encoding both MV glycoproteins. Third, M12.CD46 murine B cells were able to support MV replication, as shown by production of infectious virus and by cell biosynthesis of viral hemagglutinin after metabolic labeling of infected cells with [35S]methionine. These results show that the human CD46 molecule serves as an MV receptor allowing virus-cell binding, fusion, and viral replication and open new perspectives in the study of MV pathogenesis.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beddington R. S., Morgernstern J., Land H., Hogan A. An in situ transgenic enzyme marker for the midgestation mouse embryo and the visualization of inner cell mass clones during early organogenesis. Development. 1989 May;106(1):37–46. doi: 10.1242/dev.106.1.37. [DOI] [PubMed] [Google Scholar]
  2. Bloom B. R. Vaccines for the Third World. Nature. 1989 Nov 9;342(6246):115–120. doi: 10.1038/342115a0. [DOI] [PubMed] [Google Scholar]
  3. Boyer V., Desgranges C., Trabaud M. A., Fischer E., Kazatchkine M. D. Complement mediates human immunodeficiency virus type 1 infection of a human T cell line in a CD4- and antibody-independent fashion. J Exp Med. 1991 May 1;173(5):1151–1158. doi: 10.1084/jem.173.5.1151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Calin-Laurens V., Forquet F., Mottez E., Kanellopoulos J., Godeau F., Kourilsky P., Gerlier D., Rabourdin-Combe C. Cytosolic targeting of hen egg lysozyme gives rise to a short-lived protein presented by class I but not class II major histocompatibility complex molecules. Eur J Immunol. 1991 Mar;21(3):761–769. doi: 10.1002/eji.1830210332. [DOI] [PubMed] [Google Scholar]
  5. Cervoni F., Fenichel P., Akhoundi C., Hsi B. L., Rossi B. Characterization of a cDNA clone coding for human testis membrane cofactor protein (MCP, CD46). Mol Reprod Dev. 1993 Jan;34(1):107–113. doi: 10.1002/mrd.1080340117. [DOI] [PubMed] [Google Scholar]
  6. Dalgleish A. G., Beverley P. C., Clapham P. R., Crawford D. H., Greaves M. F., Weiss R. A. The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature. 1984 Dec 20;312(5996):763–767. doi: 10.1038/312763a0. [DOI] [PubMed] [Google Scholar]
  7. Fingeroth J. D., Weis J. J., Tedder T. F., Strominger J. L., Biro P. A., Fearon D. T. Epstein-Barr virus receptor of human B lymphocytes is the C3d receptor CR2. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4510–4514. doi: 10.1073/pnas.81.14.4510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fénichel P., Dohr G., Grivaux C., Cervoni F., Donzeau M., Hsi B. L. Localization and characterization of the acrosomal antigen recognized by GB24 on human spermatozoa. Mol Reprod Dev. 1990 Oct;27(2):173–178. doi: 10.1002/mrd.1080270214. [DOI] [PubMed] [Google Scholar]
  9. Giraudon P., Wild T. F. Correlation between epitopes on hemagglutinin of measles virus and biological activities: passive protection by monoclonal antibodies is related to their hemagglutination inhibiting activity. Virology. 1985 Jul 15;144(1):46–58. doi: 10.1016/0042-6822(85)90303-4. [DOI] [PubMed] [Google Scholar]
  10. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. The major human rhinovirus receptor is ICAM-1. Cell. 1989 Mar 10;56(5):839–847. doi: 10.1016/0092-8674(89)90688-0. [DOI] [PubMed] [Google Scholar]
  11. Hubbard A. L., Cohn Z. A. The enzymatic iodination of the red cell membrane. J Cell Biol. 1972 Nov;55(2):390–405. doi: 10.1083/jcb.55.2.390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Joling P., Bakker L. J., Van Strijp J. A., Meerloo T., de Graaf L., Dekker M. E., Goudsmit J., Verhoef J., Schuurman H. J. Binding of human immunodeficiency virus type-1 to follicular dendritic cells in vitro is complement dependent. J Immunol. 1993 Feb 1;150(3):1065–1073. [PubMed] [Google Scholar]
  13. Klatzmann D., Champagne E., Chamaret S., Gruest J., Guetard D., Hercend T., Gluckman J. C., Montagnier L. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature. 1984 Dec 20;312(5996):767–768. doi: 10.1038/312767a0. [DOI] [PubMed] [Google Scholar]
  14. Liszewski M. K., Post T. W., Atkinson J. P. Membrane cofactor protein (MCP or CD46): newest member of the regulators of complement activation gene cluster. Annu Rev Immunol. 1991;9:431–455. doi: 10.1146/annurev.iy.09.040191.002243. [DOI] [PubMed] [Google Scholar]
  15. Lublin D. M., Coyne K. E. Phospholipid-anchored and transmembrane versions of either decay-accelerating factor or membrane cofactor protein show equal efficiency in protection from complement-mediated cell damage. J Exp Med. 1991 Jul 1;174(1):35–44. doi: 10.1084/jem.174.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lublin D. M., Liszewski M. K., Post T. W., Arce M. A., Le Beau M. M., Rebentisch M. B., Lemons L. S., Seya T., Atkinson J. P. Molecular cloning and chromosomal localization of human membrane cofactor protein (MCP). Evidence for inclusion in the multigene family of complement-regulatory proteins. J Exp Med. 1988 Jul 1;168(1):181–194. doi: 10.1084/jem.168.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Maddon P. J., Dalgleish A. G., McDougal J. S., Clapham P. R., Weiss R. A., Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 1986 Nov 7;47(3):333–348. doi: 10.1016/0092-8674(86)90590-8. [DOI] [PubMed] [Google Scholar]
  18. Mendelsohn C. L., Wimmer E., Racaniello V. R. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell. 1989 Mar 10;56(5):855–865. doi: 10.1016/0092-8674(89)90690-9. [DOI] [PubMed] [Google Scholar]
  19. Naniche D., Wild T. F., Rabourdin-Combe C., Gerlier D. A monoclonal antibody recognizes a human cell surface glycoprotein involved in measles virus binding. J Gen Virol. 1992 Oct;73(Pt 10):2617–2624. doi: 10.1099/0022-1317-73-10-2617. [DOI] [PubMed] [Google Scholar]
  20. Naniche D., Wild T. F., Rabourdin-Combe C., Gerlier D. Measles virus haemagglutinin induces down-regulation of gp57/67, a molecule involved in virus binding. J Gen Virol. 1993 Jun;74(Pt 6):1073–1079. doi: 10.1099/0022-1317-74-6-1073. [DOI] [PubMed] [Google Scholar]
  21. Nemerow G. R., Wolfert R., McNaughton M. E., Cooper N. R. Identification and characterization of the Epstein-Barr virus receptor on human B lymphocytes and its relationship to the C3d complement receptor (CR2). J Virol. 1985 Aug;55(2):347–351. doi: 10.1128/jvi.55.2.347-351.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Purcell D. F., McKenzie I. F., Lublin D. M., Johnson P. M., Atkinson J. P., Oglesby T. J., Deacon N. J. The human cell-surface glycoproteins HuLy-m5, membrane co-factor protein (MCP) of the complement system, and trophoblast leucocyte-common (TLX) antigen, are CD46. Immunology. 1990 Jun;70(2):155–161. [PMC free article] [PubMed] [Google Scholar]
  23. Russell S. M., Sparrow R. L., McKenzie I. F., Purcell D. F. Tissue-specific and allelic expression of the complement regulator CD46 is controlled by alternative splicing. Eur J Immunol. 1992 Jun;22(6):1513–1518. doi: 10.1002/eji.1830220625. [DOI] [PubMed] [Google Scholar]
  24. Tomassini J. E., Graham D., DeWitt C. M., Lineberger D. W., Rodkey J. A., Colonno R. J. cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4907–4911. doi: 10.1073/pnas.86.13.4907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Wild T. F., Bernard A., Spehner D., Drillien R. Construction of vaccinia virus recombinants expressing several measles virus proteins and analysis of their efficacy in vaccination of mice. J Gen Virol. 1992 Feb;73(Pt 2):359–367. doi: 10.1099/0022-1317-73-2-359. [DOI] [PubMed] [Google Scholar]
  26. Wild T. F., Malvoisin E., Buckland R. Measles virus: both the haemagglutinin and fusion glycoproteins are required for fusion. J Gen Virol. 1991 Feb;72(Pt 2):439–442. doi: 10.1099/0022-1317-72-2-439. [DOI] [PubMed] [Google Scholar]

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