• Please log in or register to access this feature.

Regular Article

You have full text access to this OnlineOpen article

Inefficient exogenous loading of a tapasin-dependent peptide onto HLA-B*44:02 can be improved by acid treatment or fixation of target cells

  1. Vincent Stroobant1,2,†,
  2. Nathalie Demotte1,2,†,
  3. Rosalie M. Luiten3,
  4. Ralf M. Leonhardt4,
  5. Peter Cresswell4,5,
  6. Aude Bonehill6,
  7. Alexandre Michaux1,2,
  8. Wenbin Ma1,2,
  9. Arend Mulder7,
  10. Benoît J. Van den Eynde1,2,
  11. Pierre van der Bruggen1,2,
  12. Nathalie Vigneron1,2,*

Article first published online: 8 JUN 2012

DOI: 10.1002/eji.201141954

Issue

European Journal of Immunology

European Journal of Immunology

Volume 42, Issue 6, pages 1417–1428, June 2012

Additional Information

How to Cite

Stroobant, V., Demotte, N., Luiten, R. M., Leonhardt, R. M., Cresswell, P., Bonehill, A., Michaux, A., Ma, W., Mulder, A., Van den Eynde, B. J., van der Bruggen, P. and Vigneron, N. (2012), Inefficient exogenous loading of a tapasin-dependent peptide onto HLA-B*44:02 can be improved by acid treatment or fixation of target cells. Eur. J. Immunol., 42: 1417–1428. doi: 10.1002/eji.201141954

Author Information

  1. 1

    Ludwig Institute for Cancer Research, Brussels, Belgium

  2. 2

    WELBIO and de Duve Institute, Université catholique de Louvain, Brussels, Belgium

  3. 3

    Department of Dermatology, Academic Medical Center, University of Amsterdam, The Netherlands

  4. 4

    Department of Immunobiology, Yale University School of Medicine, New Haven, CT, USA

  5. 5

    Howard Hughes Medical Institute, Chevy Chase, MD, USA

  6. 6

    Laboratory of Molecular and Cellular Therapy, Department of Physiology and Immunology, Medical School of Vrije Universiteit Brussel (VUB), Brussels, Belgium

  7. 7

    Department of Immunohematology, Leiden University Medical Center, Leiden, The Netherlands

  1. †

    These authors contributed equally to the work.

*Correspondence: Dr. Nathalie Vigneron, Ludwig Institute for Cancer Research, de Duve Institute, Avenue Hippocrate 74, UCL 7459; B-1200 Brussels, Belgium
Fax: +32-27647590
e-mail: nathalie.vigneron@bru.licr.org

  1. †

    These authors contributed equally to the work.

Publication History

  1. Issue published online: 8 JUN 2012
  2. Article first published online: 8 JUN 2012
  3. Manuscript Accepted: 22 FEB 2012
  4. Manuscript Revised: 5 FEB 2012
  5. Manuscript Received: 15 JUL 2011

Funded by

  • European Union. Grant Number: LSHC-CT-2006-518234
  • Belgian State (Prime Minister's Office, Science Policy Programming)
  • Fonds National de la Recherche Scientifique (FNRS, Belgium)
  • Fondation contre le Cancer (nonprofit organization, Belgium)
  • Fonds J. Maisin (Belgium)
  • Fondation Salus Sanguinis (Belgium)
  • Howard Hughes Medical Institute. Grant Number: 5P50 CA121974
  • NIH/National Institute of General Medical Sciences

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (907K)

References

  • 1
    Vigneron, N. and Van den Eynde, B. J., Insights into the processing of MHC class I ligands gained from the study of human tumor epitopes. Cell. Mol. Life Sci. 2011. 68: 1503–1520.
  • 2
    Kawakami, Y., Eliyahu, S., Jennings, C., Sakaguchi, K., Kang, X., Southwood, S., Robbins, P. F. et al., Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J. Immunol. 1995. 154: 3961–3968.
  • 3
    Zarour, H., De Smet, C., Lehmann, F., Marchand, M., Lethé, B., Romero, P., Boon, T. et al., The majority of autologous cytolytic T-lymphocyte clones derived from peripheral blood lymphocytes of a melanoma patient recognize an antigenic peptide derived from gene Pmel17/gp100. J. Invest. Dermatol. 1996. 107: 63–67.
  • 4
    Germeau, C., Ma, W., Schiavetti, F., Lurquin, C., Henry, E., Vigneron, N., Brasseur, F. et al., High frequency of anti-tumor T cells in the blood of melanoma patients before and after vaccination with tumor antigens. J. Exp. Med. 2005. 201: 241–248.
  • 5
    Rock, K. L., Gramm, C., Rothstein, L., Clark, K., Stein, R., Dick, L., Hwang, D. et al., Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 1994. 78: 761–771.
  • 6
    Peaper, D. R. and Cresswell, P., Regulation of MHC class I assembly and peptide binding. Annu. Rev. Cell Dev. Biol. 2008. 24: 343–368.
  • 7
    DiBrino, M., Parker, K. C., Margulies, D. H., Shiloach, J., Turner, R. V., Biddison, W. E. and Coligan, J. E., Identification of the peptide binding motif for HLA-B44, one of the most common HLA-B alleles in the Caucasian population. Biochemistry 1995. 34: 10130–10138.
  • 8
    Hérin, M., Lemoine, C., Weynants, P., Vessière, F., Van Pel, A., Knuth, A., Devos, R. et al., Production of stable cytolytic T-cell clones directed against autologous human melanoma. Int. J. Cancer 1987. 39: 390–396.
    Direct Link:
  • 9
    Rock, K. L. and Goldberg, A. L., Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 1999. 17: 739–779.
  • 10
    Zernich, D., Purcell, A. W., Macdonald, W. A., Kjer-Nielsen, L., Ely, L. K., Laham, N., Crockford, T. et al., Natural HLA class I polymorphism controls the pathway of antigen presentation and susceptibility to viral evasion. J. Exp. Med. 2004. 200: 13–24.
  • 11
    Praveen, P. V., Yaneva, R., Kalbacher, H. and Springer, S., Tapasin edits peptides on MHC class I molecules by accelerating peptide exchange. Eur. J. Immunol. 2010. 40: 214–224.
    Direct Link:
  • 12
    Williams, A. P., Peh, C. A., Purcell, A. W., McCluskey, J. and Elliott, T., Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 2002. 16: 509–520.
  • 13
    Dick, T. P., Bangia, N., Peaper, D. R. and Cresswell, P., Disulfide bond isomerization and the assembly of MHC class I-peptide complexes. Immunity 2002. 16: 87–98.
  • 14
    Chiari, R., Foury, F., De Plaen, E., Baurain, J.-F., Thonnard, J. and Coulie, P. G., Two antigens recognized by autologous CTL on a melanoma result from a single point mutation in an essential housekeeping gene. Cancer Res. 1999. 59: 5785–5792.
  • 15
    Tussey, L. G. and Frelinger, J. A., Detergent enhances binding of a secreted HLA-A2 molecule to solid phase peptides. Hum. Immunol. 1991. 32: 183–193.
  • 16
    Stryhn, A., Pedersen, L. O., Romme, T., Olsen, A. C., Nissen, M. H., Thorpe, C. J. and Buus, S., pH dependence of MHC class I-restricted peptide presentation. J. Immunol. 1996. 156: 4191–4197.
  • 17
    Leonhardt, R. M., Keusekotten, K., Bekpen, C. and Knittler, M. R., Critical role for the tapasin-docking site of TAP2 in the functional integrity of the MHC class I-peptide-loading complex. J. Immunol. 2005. 175: 5104–5114.
  • 18
    Ojcius, D. M., Gapin, L. and Kourilsky, P., Dissociation of the peptide/MHC class I complex: pH dependence and effect of endogenous peptides on the activation energy. Biochem. Biophys. Res. Commun. 1993. 197: 1216–1222.
  • 19
    Gromme, M., Uytdehaag, F. G., Janssen, H., Calafat, J., van Binnendijk, R. S., Kenter, M. J., Tulp, A. et al., Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. USA 1999. 96: 10326–10331.
  • 20
    Mantegazza, A. R., Savina, A., Vermeulen, M., Perez, L., Geffner, J., Hermine, O., Rosenzweig, S. D. et al., NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells. Blood 2008. 112: 4712–4722.
  • 21
    Ojcius, D. M., Abastado, J. P., Casrouge, A., Mottez, E., Cabanie, L. and Kourilsky, P., Dissociation of the peptide-MHC class I complex limits the binding rate of exogenous peptide. J. Immunol. 1993. 151: 6020–6026.
  • 22
    Vigneron, N., Peaper, D. R., Leonhardt, R. M. and Cresswell, P., Functional significance of tapasin membrane association and disulfide linkage to ERp57 in MHC class I presentation. Eur. J. Immunol. 2009. 39: 2371–2376.
    Direct Link:
  • 23
    Luiten, R. M., Demotte, N., Tine, J. and van der Bruggen, P., A MAGE-A1 peptide presented to cytolytic T lymphocytes by both HLA-B35 and HLA-A1 molecules. Tissue Antigens 2000. 56: 77–81.
    Direct Link:
  • 24
    Williams, A. P., Bevan, S., Bunce, M., Houlston, R., Welsh, K. I. and Elliott, T., Identification of novel tapasin polymorphisms and linkage disequilibrium to MHC class I alleles. Immunogenetics 2000. 52: 9–11.
  • 25
    Pu, Z., Carrero, J. A. and Unanue, E. R., Distinct recognition by two subsets of T cells of an MHC class II-peptide complex. Proc. Natl. Acad. Sci. USA 2002. 99: 8844–8849.
  • 26
    Akatsuka, Y., Nishida, T., Kondo, E., Miyazaki, M., Taji, H., Iida, H., Tsujimura, K. et al., Identification of a polymorphic gene, BCL2A1, encoding two novel hematopoietic lineage-specific minor histocompatibility antigens. J. Exp. Med. 2003. 197: 1489–1500.
  • 27
    van der Bruggen, P., Stroobant, V., Vigneron, N. and Van den Eynde, B., Peptide database of T-cell defined tumor antigens 2011. http://www.cancerimmunity.org/peptidedatabase/Tcellepitopes.htm
  • 28
    Sieker, F., Straatsma, T. P., Springer, S. and Zacharias, M., Differential tapasin dependence of MHC class I molecules correlates with conformational changes upon peptide dissociation: a molecular dynamics simulation study. Mol. Immunol. 2008. 45: 3714–3722.
  • 29
    Leonhardt, R. M., Fiegl, D., Rufer, E., Karger, A., Bettin, B. and Knittler, M. R., Post-endoplasmic reticulum rescue of unstable MHC class I requires proprotein convertase PC7. J. Immunol. 2010. 184: 2985–2998.
  • 30
    Lee, T. D., Distributions of HLA antigens. In Lee, J. (Ed.) The HLA System. A New Approach. Springer Verlag, New York, 1990, pp 141–178.
  • 31
    Hsu, D. H., Paz, P., Villaflor, G., Rivas, A., Mehta-Damani, A., Angevin, E., Zitvogel, L. et al., Exosomes as a tumor vaccine: enhancing potency through direct loading of antigenic peptides. J. Immunother. 2003. 26: 440–450.
  • 32
    Greenwood, R., Shimizu, Y., Sekhon, G. S. and DeMars, R., Novel allele-specific, post-translational reduction in HLA class I surface expression in a mutant human B-cell line. J. Immunol. 1994. 153: 5525–5536.
  • 33
    Peh, C. A., Burrows, S. R., Barnden, M., Khanna, R., Cresswell, P., Moss, D. J. and McCluskey, J., HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity 1998. 8: 531–542.
  • 34
    Mavilio, F., Ferrari, G., Rossini, S., Nobili, N., Bonini, C., Casorati, G., Traversari, C. et al., Peripheral blood lymphocytes as target cells of retroviral vector-mediated gene transfer. Blood 1994. 83: 1988–1997.
  • 35
    Chaux, P., Luiten, R., Demotte, N., Vantomme, V., Stroobant, V., Traversari, C., Russo, V. et al., Identification of five MAGE-A1 epitopes recognized by cytolytic T lymphocytes obtained by in vitro stimulation with dendritic cells transduced with MAGE-A1. J. Immunol. 1999. 163: 2928–2936.
  • 36
    Murata, M., Warren, E. H. and Riddell, S. R., A human minor histocompatibility antigen resulting from differential expression due to a gene deletion. J. Exp. Med. 2003. 197: 1279–1289.
  • 37
    Gaugler, B., Van den Eynde, B., van der Bruggen, P., Romero, P., Gaforio, J. J., De Plaen, E., Lethé, B. et al., Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes. J. Exp. Med. 1994. 179: 921–930.
  • 38
    Seed, B. and Aruffo, A., Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc. Natl. Acad. Sci. USA 1987. 84: 3365–3369.
  • 39
    Traversari, C., van der Bruggen, P., Van den Eynde, B., Hainaut, P., Lemoine, C., Ohta, N., Old, L. et al., Transfection and expression of a gene coding for a human melanoma antigen recognized by autologous cytolytic T lymphocytes. Immunogenetics 1992. 35: 145–152.
  • 40
    Mulder, A., Kardol, M. J., Arn, J. S., Eijsink, C., Franke, M. E., Schreuder, G. M., Haasnoot, G. W. et al., Human monoclonal HLA antibodies reveal interspecies crossreactive swine MHC class I epitopes relevant for xenotransplantation. Mol. Immunol. 2010. 47: 809–815.
  • 41
    Vigneron, N., Stroobant, V., Chapiro, J., Ooms, A., Degiovanni, G., Morel, S., van der Bruggen, P. et al., An antigenic peptide produced by peptide splicing in the proteasome. Science 2004. 304: 587–590.
View Full Article with Supporting Information (HTML) Get PDF (907K)