Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Sep 1;89(17):7915–7918. doi: 10.1073/pnas.89.17.7915

Cationic lipids direct a viral glycoprotein into the class I major histocompatibility complex antigen-presentation pathway.

C Walker 1, M Selby 1, A Erickson 1, D Cataldo 1, J P Valensi 1, G V Van Nest 1
PMCID: PMC49825  PMID: 1518813

Abstract

Recombinant glycoprotein B (gB) of herpes simplex virus (HSV) was processed and presented by class I major histocompatibility complex (MHC) molecules after delivery into cells by using N-[1-(2,3-dioleoyloxy)propyl]-N,N,N-trimethylammonium methyl sulfate (DOTAP), a commercially available cationic lipid used for DNA transfection. Cells treated with DOTAP-associated gB were susceptible to lysis by class I MHC-restricted, HSV-specific cytotoxic T lymphocytes (CTL), and the treated cells restimulated memory gB-specific CTL activity in spleen cells from HSV-infected mice. gB-specific CTL responses were detected in mice immunized with recombinant gB and DOTAP but not in those receiving gB emulsified in complete Freund's adjuvant. Thus, cationic lipids may facilitate induction of CD8+ T-cell responses in vaccinations with recombinant antigens, and they may serve as readily available reagents for dissecting class I MHC immunity to viruses and other intracellular pathogens.

Full text

PDF
7916

Selected References

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

  1. Aichele P., Hengartner H., Zinkernagel R. M., Schulz M. Antiviral cytotoxic T cell response induced by in vivo priming with a free synthetic peptide. J Exp Med. 1990 May 1;171(5):1815–1820. doi: 10.1084/jem.171.5.1815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carbone F. R., Moore M. W., Sheil J. M., Bevan M. J. Induction of cytotoxic T lymphocytes by primary in vitro stimulation with peptides. J Exp Med. 1988 Jun 1;167(6):1767–1779. doi: 10.1084/jem.167.6.1767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Debs R. J., Freedman L. P., Edmunds S., Gaensler K. L., Düzgünes N., Yamamoto K. R. Regulation of gene expression in vivo by liposome-mediated delivery of a purified transcription factor. J Biol Chem. 1990 Jun 25;265(18):10189–10192. [PubMed] [Google Scholar]
  4. Deres K., Schild H., Wiesmüller K. H., Jung G., Rammensee H. G. In vivo priming of virus-specific cytotoxic T lymphocytes with synthetic lipopeptide vaccine. Nature. 1989 Nov 30;342(6249):561–564. doi: 10.1038/342561a0. [DOI] [PubMed] [Google Scholar]
  5. Fayolle C., Deriaud E., Leclerc C. In vivo induction of cytotoxic T cell response by a free synthetic peptide requires CD4+ T cell help. J Immunol. 1991 Dec 15;147(12):4069–4073. [PubMed] [Google Scholar]
  6. Felgner P. L., Gadek T. R., Holm M., Roman R., Chan H. W., Wenz M., Northrop J. P., Ringold G. M., Danielsen M. Lipofection: a highly efficient, lipid-mediated DNA-transfection procedure. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7413–7417. doi: 10.1073/pnas.84.21.7413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Hanke T., Graham F. L., Rosenthal K. L., Johnson D. C. Identification of an immunodominant cytotoxic T-lymphocyte recognition site in glycoprotein B of herpes simplex virus by using recombinant adenovirus vectors and synthetic peptides. J Virol. 1991 Mar;65(3):1177–1186. doi: 10.1128/jvi.65.3.1177-1186.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Harding C. V., Collins D. S., Kanagawa O., Unanue E. R. Liposome-encapsulated antigens engender lysosomal processing for class II MHC presentation and cytosolic processing for class I presentation. J Immunol. 1991 Nov 1;147(9):2860–2863. [PubMed] [Google Scholar]
  10. Hart M. K., Weinhold K. J., Scearce R. M., Washburn E. M., Clark C. A., Palker T. J., Haynes B. F. Priming of anti-human immunodeficiency virus (HIV) CD8+ cytotoxic T cells in vivo by carrier-free HIV synthetic peptides. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9448–9452. doi: 10.1073/pnas.88.21.9448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ishioka G. Y., Colon S., Miles C., Grey H. M., Chesnut R. W. Induction of class I MHC-restricted, peptide-specific cytolytic T lymphocytes by peptide priming in vivo. J Immunol. 1989 Aug 15;143(4):1094–1100. [PubMed] [Google Scholar]
  12. Kast W. M., Roux L., Curren J., Blom H. J., Voordouw A. C., Meloen R. H., Kolakofsky D., Melief C. J. Protection against lethal Sendai virus infection by in vivo priming of virus-specific cytotoxic T lymphocytes with a free synthetic peptide. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2283–2287. doi: 10.1073/pnas.88.6.2283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lawman M. J., Rouse B. T., Courtney R. J., Walker R. D. Cell-mediated immunity against herpes simplex induction of cytotoxic T lymphocytes. Infect Immun. 1980 Jan;27(1):133–139. doi: 10.1128/iai.27.1.133-139.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ljunggren H. G., Stam N. J., Ohlén C., Neefjes J. J., Höglund P., Heemels M. T., Bastin J., Schumacher T. N., Townsend A., Kärre K. Empty MHC class I molecules come out in the cold. Nature. 1990 Aug 2;346(6283):476–480. doi: 10.1038/346476a0. [DOI] [PubMed] [Google Scholar]
  15. Lopes L. M., Chain B. M. Liposome-mediated delivery stimulates a class I-restricted cytotoxic T cell response to soluble antigen. Eur J Immunol. 1992 Jan;22(1):287–290. doi: 10.1002/eji.1830220143. [DOI] [PubMed] [Google Scholar]
  16. Moore M. W., Carbone F. R., Bevan M. J. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell. 1988 Sep 9;54(6):777–785. doi: 10.1016/s0092-8674(88)91043-4. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Nair S., Zhou F., Reddy R., Huang L., Rouse B. T. Soluble proteins delivered to dendritic cells via pH-sensitive liposomes induce primary cytotoxic T lymphocyte responses in vitro. J Exp Med. 1992 Feb 1;175(2):609–612. doi: 10.1084/jem.175.2.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Noguchi Y., Noguchi T., Sato T., Yokoo Y., Itoh S., Yoshida M., Yoshiki T., Akiyoshi K., Sunamoto J., Nakayama E. Priming for in vitro and in vivo anti-human T lymphotropic virus type 1 cellular immunity by virus-related protein reconstituted into liposome. J Immunol. 1991 May 15;146(10):3599–3603. [PubMed] [Google Scholar]
  20. Nuchtern J. G., Bonifacino J. S., Biddison W. E., Klausner R. D. Brefeldin A implicates egress from endoplasmic reticulum in class I restricted antigen presentation. Nature. 1989 May 18;339(6221):223–226. doi: 10.1038/339223a0. [DOI] [PubMed] [Google Scholar]
  21. Pachl C., Burke R. L., Stuve L. L., Sanchez-Pescador L., Van Nest G., Masiarz F., Dina D. Expression of cell-associated and secreted forms of herpes simplex virus type 1 glycoprotein gB in mammalian cells. J Virol. 1987 Feb;61(2):315–325. doi: 10.1128/jvi.61.2.315-325.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pfizenmaier K., Jung H., Starzinski-Powitz A., Röllinghoff M., Wagner H. The role of T cells in anti-herpes simplex virus immunity. I. Induction of antigen-specific cytotoxic T lymphocytes. J Immunol. 1977 Sep;119(3):939–944. [PubMed] [Google Scholar]
  23. Reddy R., Zhou F., Huang L., Carbone F., Bevan M., Rouse B. T. pH sensitive liposomes provide an efficient means of sensitizing target cells to class I restricted CTL recognition of a soluble protein. J Immunol Methods. 1991 Aug 9;141(2):157–163. doi: 10.1016/0022-1759(91)90142-3. [DOI] [PubMed] [Google Scholar]
  24. Rötzschke O., Falk K., Deres K., Schild H., Norda M., Metzger J., Jung G., Rammensee H. G. Isolation and analysis of naturally processed viral peptides as recognized by cytotoxic T cells. Nature. 1990 Nov 15;348(6298):252–254. doi: 10.1038/348252a0. [DOI] [PubMed] [Google Scholar]
  25. Schumacher T. N., Heemels M. T., Neefjes J. J., Kast W. M., Melief C. J., Ploegh H. L. Direct binding of peptide to empty MHC class I molecules on intact cells and in vitro. Cell. 1990 Aug 10;62(3):563–567. doi: 10.1016/0092-8674(90)90020-f. [DOI] [PubMed] [Google Scholar]
  26. Stuve L. L., Brown-Shimer S., Pachl C., Najarian R., Dina D., Burke R. L. Structure and expression of the herpes simplex virus type 2 glycoprotein gB gene. J Virol. 1987 Feb;61(2):326–335. doi: 10.1128/jvi.61.2.326-335.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Takahashi H., Takeshita T., Morein B., Putney S., Germain R. N., Berzofsky J. A. Induction of CD8+ cytotoxic T cells by immunization with purified HIV-1 envelope protein in ISCOMs. Nature. 1990 Apr 26;344(6269):873–875. doi: 10.1038/344873a0. [DOI] [PubMed] [Google Scholar]
  28. Townsend A. R., Gotch F. M., Davey J. Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell. 1985 Sep;42(2):457–467. doi: 10.1016/0092-8674(85)90103-5. [DOI] [PubMed] [Google Scholar]
  29. Townsend A., Bodmer H. Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol. 1989;7:601–624. doi: 10.1146/annurev.iy.07.040189.003125. [DOI] [PubMed] [Google Scholar]
  30. Van Bleek G. M., Nathenson S. G. Isolation of an endogenously processed immunodominant viral peptide from the class I H-2Kb molecule. Nature. 1990 Nov 15;348(6298):213–216. doi: 10.1038/348213a0. [DOI] [PubMed] [Google Scholar]
  31. Walker C. M., Paetkau V., Rawls W. E., Rosenthal K. L. Abrogation of anti-Pichinde virus cytotoxic T cell memory by cyclophosphamide and restoration by coinfection or interleukin 2. J Immunol. 1985 Aug;135(2):1401–1407. [PubMed] [Google Scholar]
  32. Witmer L. A., Rosenthal K. L., Graham F. L., Friedman H. M., Yee A., Johnson D. C. Cytotoxic T lymphocytes specific for herpes simplex virus (HSV) studied using adenovirus vectors expressing HSV glycoproteins. J Gen Virol. 1990 Feb;71(Pt 2):387–396. doi: 10.1099/0022-1317-71-2-387. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES