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. 1988 Feb;85(4):1209–1212. doi: 10.1073/pnas.85.4.1209

Antigen presentation to HLA class II-restricted measles virus-specific T-cell clones can occur in the absence of the invariant chain.

R P Sekaly 1, S Jacobson 1, J R Richert 1, C Tonnelle 1, H F McFarland 1, E O Long 1
PMCID: PMC279736  PMID: 3257576

Abstract

A human fibroblast line expressing HLA-DR1 antigen on its surface was generated by transfection with DR alpha and DR beta cDNAs. Expression of the invariant chain gene was not detectable in the transfected fibroblasts and was not induced by infection with measles virus. Lysis of measles virus-infected cells occurred with DR1- but not with DR4-restricted measles virus-specific cytotoxic T-lymphocyte (CTL) clones and was inhibited by a monoclonal antibody specific for DR antigen. Therefore, the invariant chain is not required for DR-restricted presentation of measles virus antigens by this fibroblast line. Transfected fibroblasts were lysed as efficiently as an autologous B-cell line even though they expressed much less surface DR antigen. Lysis of both the transfected fibroblasts and the B-cell line was insensitive to treatment with chloroquine. These results demonstrate that expression of a DR alpha beta heterodimer at the surface of this fibroblast line is necessary and sufficient for presentation of measles virus antigens to specific CTL clones.

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Selected References

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

  1. Barbosa J. A., Mentzer S. J., Minowada G., Strominger J. L., Burakoff S. J., Biro P. A. Recognition of HLA-A2 and -B7 antigens by cloned cytotoxic T lymphocytes after gene transfer into human and monkey, but not mouse, cells. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7549–7553. doi: 10.1073/pnas.81.23.7549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bernabeu C., Maziarz R., Spits H., de Vries J., Burakoff S. J., Terhorst C. Coexpression of the human HLA-A2 or HLA-B7 heavy chain gene and human beta 2-microglobulin gene in L cells. J Immunol. 1984 Dec;133(6):3188–3194. [PubMed] [Google Scholar]
  3. Church W. R., Walker L. E., Houghten R. A., Reisfeld R. A. Anti-HLA antibodies of predetermined specificity: a chemically synthesized peptide induces antibodies specific for HLA-A,B heavy chain. Proc Natl Acad Sci U S A. 1983 Jan;80(1):255–258. doi: 10.1073/pnas.80.1.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Collins T., Krensky A. M., Clayberger C., Fiers W., Gimbrone M. A., Jr, Burakoff S. J., Pober J. S. Human cytolytic T lymphocyte interactions with vascular endothelium and fibroblasts: role of effector and target cell molecules. J Immunol. 1984 Oct;133(4):1878–1884. [PubMed] [Google Scholar]
  5. Cowan E. P., Coligan J. E., Biddison W. E. Human cytotoxic T-lymphocyte recognition of an HLA-A3 gene product expressed on murine L cells: the only human gene product required on the target cells for lysis is the class I heavy chain. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4490–4494. doi: 10.1073/pnas.82.13.4490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cresswell P. Intracellular class II HLA antigens are accessible to transferrin-neuraminidase conjugates internalized by receptor-mediated endocytosis. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8188–8192. doi: 10.1073/pnas.82.23.8188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dustin M. L., Sanders M. E., Shaw S., Springer T. A. Purified lymphocyte function-associated antigen 3 binds to CD2 and mediates T lymphocyte adhesion. J Exp Med. 1987 Mar 1;165(3):677–692. doi: 10.1084/jem.165.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Germain R. N. Immunology. The ins and outs of antigen processing and presentation. Nature. 1986 Aug 21;322(6081):687–689. doi: 10.1038/322687a0. [DOI] [PubMed] [Google Scholar]
  9. Jacobson S., Flerlage M. L., McFarland H. F. Impaired measles virus-specific cytotoxic T cell responses in multiple sclerosis. J Exp Med. 1985 Sep 1;162(3):839–850. doi: 10.1084/jem.162.3.839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jacobson S., Richert J. R., Biddison W. E., Satinsky A., Hartzman R. J., McFarland H. F. Measles virus-specific T4+ human cytotoxic T cell clones are restricted by class II HLA antigens. J Immunol. 1984 Aug;133(2):754–757. [PubMed] [Google Scholar]
  11. Kaufman J. F., Auffray C., Korman A. J., Shackelford D. A., Strominger J. The class II molecules of the human and murine major histocompatibility complex. Cell. 1984 Jan;36(1):1–13. doi: 10.1016/0092-8674(84)90068-0. [DOI] [PubMed] [Google Scholar]
  12. Koch N., Harris A. W. Differential expression of the invariant chain in mouse tumor cells: relationship to B lymphoid development. J Immunol. 1984 Jan;132(1):12–15. [PubMed] [Google Scholar]
  13. Malissen B., Price M. P., Goverman J. M., McMillan M., White J., Kappler J., Marrack P., Pierres A., Pierres M., Hood L. Gene transfer of H-2 class II genes: antigen presentation by mouse fibroblast and hamster B-cell lines. Cell. 1984 Feb;36(2):319–327. doi: 10.1016/0092-8674(84)90225-3. [DOI] [PubMed] [Google Scholar]
  14. Massa P. T., Dörries R., ter Meulen V. Viral particles induce Ia antigen expression on astrocytes. Nature. 1986 Apr 10;320(6062):543–546. doi: 10.1038/320543a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Miller J., Germain R. N. Efficient cell surface expression of class II MHC molecules in the absence of associated invariant chain. J Exp Med. 1986 Nov 1;164(5):1478–1489. doi: 10.1084/jem.164.5.1478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Morrison L. A., Lukacher A. E., Braciale V. L., Fan D. P., Braciale T. J. Differences in antigen presentation to MHC class I-and class II-restricted influenza virus-specific cytolytic T lymphocyte clones. J Exp Med. 1986 Apr 1;163(4):903–921. doi: 10.1084/jem.163.4.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nagai Y., Hamaguchi M., Toyoda T., Yoshida T. The uncoating of paramyxoviruses may not require a low pH mediated step. Virology. 1983 Oct 15;130(1):263–268. doi: 10.1016/0042-6822(83)90138-1. [DOI] [PubMed] [Google Scholar]
  18. Norcross M. A., Bentley D. M., Margulies D. H., Germain R. N. Membrane Ia expression and antigen-presenting accessory cell function of L cells transfected with class II major histocompatibility complex genes. J Exp Med. 1984 Nov 1;160(5):1316–1337. doi: 10.1084/jem.160.5.1316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Nowell J., Quaranta V. Chloroquine affects biosynthesis of Ia molecules by inhibiting dissociation of invariant (gamma) chains from alpha-beta dimers in B cells. J Exp Med. 1985 Oct 1;162(4):1371–1376. doi: 10.1084/jem.162.4.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rabourdin-Combe C., Mach B. Expression of HLA-DR antigens at the surface of mouse L cells co-transfected with cloned human genes. Nature. 1983 Jun 23;303(5919):670–674. doi: 10.1038/303670a0. [DOI] [PubMed] [Google Scholar]
  21. Schwartz R. H. T-lymphocyte recognition of antigen in association with gene products of the major histocompatibility complex. Annu Rev Immunol. 1985;3:237–261. doi: 10.1146/annurev.iy.03.040185.001321. [DOI] [PubMed] [Google Scholar]
  22. Sekaly R. P., Tonnelle C., Strubin M., Mach B., Long E. O. Cell surface expression of class II histocompatibility antigens occurs in the absence of the invariant chain. J Exp Med. 1986 Nov 1;164(5):1490–1504. doi: 10.1084/jem.164.5.1490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shaw S., Luce G. E., Quinones R., Gress R. E., Springer T. A., Sanders M. E. Two antigen-independent adhesion pathways used by human cytotoxic T-cell clones. Nature. 1986 Sep 18;323(6085):262–264. doi: 10.1038/323262a0. [DOI] [PubMed] [Google Scholar]
  24. Tonnelle C., DeMars R., Long E. O. DO beta: a new beta chain gene in HLA-D with a distinct regulation of expression. EMBO J. 1985 Nov;4(11):2839–2847. doi: 10.1002/j.1460-2075.1985.tb04012.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Townsend A. R. Recognition of influenza virus proteins by cytotoxic T lymphocytes. Immunol Res. 1987;6(1-2):80–100. doi: 10.1007/BF02918106. [DOI] [PubMed] [Google Scholar]
  26. Unanue E. R. Antigen-presenting function of the macrophage. Annu Rev Immunol. 1984;2:395–428. doi: 10.1146/annurev.iy.02.040184.002143. [DOI] [PubMed] [Google Scholar]

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