Cross-presentation

The term cross-presentation denotes the ability of certain antigen-presenting cells to take up, process and present extracellular antigens with MHC class I molecules to CD8 T cells (cytotoxic T cells). Cross-priming describes the stimulation of naive cytotoxic CD8+ T cells by this process[1]. This process is necessary for immunity against most tumors and against viruses that do not infect antigen-presenting cells.[2][3]

It is also required for induction of cytotoxic immunity by vaccination with protein antigens, for example in tumor vaccination.[4]

Contents

History

The first evidence of cross-presentation was reported 1976 by Michael J. Bevan after injection of cells carrying alloantigens into experimental animals. This resulted in CD8 T cell responses that were induced by antigen-presenting cells of the recipient, implying that these must have taken up and processed the injected cells. This observation was termed “cross-priming”.[5]

Later, there had been much controversy about cross-presentation, which now is believed to have been due to particularities and limitations of some experimental systems used.[6]

Relevance for immunity

Cross-presentation has been shown to play a role in the immune defense against many viruses (herpesvirus, influenzavirus, CMV, EBV, SIV, papillomavirus, and others), bacteria (listeria, salmonella, E. coli, M. tuberculosis, and others) and tumors (brain, pancreas, melanoma, leukemia, and others).[7][8]

Cross-priming avoids viral immune evasion strategies, such as suppression of antigen-processing. Consequently, immune responses against viruses that are able to do so, such as herpes viruses, are largely dependent on cross-presentation.

Relevance for immune tolerance

Some self-antigens (autoantigens) are cross-presented, resulting in the elimination of autoreactive CD8 T cells. This mechanism to maintain self tolerance has been termed cross-tolerance.[9].

Cell biology

Antigen-presenting cells capable of cross-presentation are primarily dendritic cells,[10][11] but macrophages, B lymphocytes and liver sinusoidal endothelial cells have also been shown to be able to do so. The intracellular mechanisms of cross-presentation are still unclear, but seem to involve specialized subcellular compartments bearing characteristics of both the endoplasmic reticulum and the endosome.[12][13]

Endocytosed proteins are transported out of this compartment into the cytoplasm by unknown mechanisms. There they are processed by the proteasome into peptides, which are transported by the TAP transporter into the endoplasmic reticulum [14][12], or back into the same endosomes [15], where they associate with MHC class I molecules.

Finally, MHC class I - peptide complexes are transported to the cell surface, where they can be detected by specific CD8 T cells.

References

  1. ^ Bevan, Michael J. (2006). "Cross-priming". Nature Immunology (Nature Publishing Group) 7 (4): 363–5. doi:10.1038/ni0406-363. PMID 16550200. http://www.nature.com/ni/journal/v7/n4/full/ni0406-363.html. 
  2. ^ Heath WR, Carbone FR. 2001. Cross-presentation in viral immunity and self-tolerance. Nat Rev Immunol 1: 126-34
  3. ^ Rock KL. 1996. A new foreign policy: MHC class I molecules monitor the outside world. Immunol. Today 17: 131-7
  4. ^ Melief CJ. 2003. Mini-review: Regulation of cytotoxic T lymphocyte responses by dendritic cells: peaceful coexistence of cross-priming and direct priming? Eur J Immunol 33: 2645-54
  5. ^ Bevan MJ. 1976. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143: 1283-8
  6. ^ Wolkers MC, Brouwenstijn N, Bakker AH, Toebes M, Schumacher TN. 2004. Antigen bias in T cell cross-priming. Science 304: 1314-7
  7. ^ Huang AY, Golumbek P, Ahmadzadeh M, Jaffee E, Pardoll D, Levitsky H. 1994. Role of bone marrow-derived cells in presenting MHC class I-restricted tumor antigens. Science 264: 961-5
  8. ^ Sigal LJ, Crotty S, Andino R, Rock KL. 1999. Cytotoxic T-cell immunity to virus-infected non-haematopoietic cells requires presentation of exogenous antigen. Nature 398: 77-80
  9. ^ Kurts C, H Kosaka, FR Carbone, JFAP Miller und WR Heath. 1997. Exogenous class I-restricted cross-presentation of self antigens can lead to deletion of autoreactive CD8+ T cells. J Exp Med 186: 239-245
  10. ^ den Haan JM, Lehar SM, Bevan MJ. 2000. CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 192: 1685-96.
  11. ^ Kurts C, Cannarile M, Klebba I, Brocker T. 2001. Dendritic cells are sufficient to cross-present self-antigens to CD8 T cells in vivo. J Immunol 166: 1439-42.
  12. ^ a b Guermonprez P, Saveanu L, Kleijmeer M, Davoust J, Van Endert P, Amigorena S. 2003. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425: 397-402
  13. ^ Burgdorf S, Kautz A, Böhnert V, Knolle PA, Kurts C. 2007. Distinct antigen uptake and intracellular routing mechanisms in CD4 and CD8 T cell activation. Science, 316: 612-6
  14. ^ Cresswell P, Bangia N, Dick T, Diedrich G. 1999. The nature of the MHC class I peptide loading complex. Immunol Rev 172: 21-8
  15. ^ Burgdorf S, Schölz C, Kautz A, Tampé R, Kurts C. 2008. Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nature Immunol, 9: 558-566.

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