MHC class I molecules with superenhanced CD8 binding properties bypass the requirement for cognate TCR recognition and nonspecifically activate CTLs

Journal of Immunology

Volumn 184, Issue 7, 2010, Pages 3357-3366

  Wooldridge, Linda ^a   Clement, Mathew ^a   Lissina, Anna ^a   Edwards, Emily S J ^a   Ladell, Kristin ^a   Ekeruche, Julia ^a   Hewitt, Rachel E ^b   Laugel, Bruno ^a   Gostick, Emma ^a   Cole, David K ^a   Debets, Reno ^c   Berrevoets, Cor ^c   Miles, John J ^a,d   Burrows, Scott R ^d   Price, David A ^a   Sewell, Andrew K ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; CHEMOKINE; CYTOKINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR; HLA ANTIGEN CLASS 1; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE ACTIVATION; ANTIGEN PRESENTATION; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL SEPARATION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM;

ANTIGEN PRESENTATION; ANTIGENS, CD8; CD8-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LYMPHOCYTE ACTIVATION; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES, CYTOTOXIC;

EID: 77951650743     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902398     Document Type: Article

References (50)

1. Davis, M. M., J. J. Boniface, Z. Reich, D. Lyons, J. Hampl, B. Arden, and Y. Chien. 1998. Ligand recognition by alpha beta T cell receptors. Annu. Rev. Immunol. 16: 523-544.
2. Rudolph, M. G., and I. A.Wilson. 2002. The specificity of TCR/pMHC interaction. Curr. Opin. Immunol. 14: 52-65.
3. Zamoyska, R. 1998. CD4 and CD8: modulators of T-cell receptor recognition of antigen and of immune responses? Curr. Opin. Immunol. 10: 82-87.
4. Holler, P. D., and D. M. Kranz. 2003. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18: 255-264.
5. Gakamsky, D. M., I. F. Luescher, A. Pramanik, R. B. Kopito, F. Lemonnier, H. Vogel, R. Rigler, and I. Pecht. 2005. CD8 kinetically promotes ligand binding to the T-cell antigen receptor. Biophys. J. 89: 2121-2133.
6. Laugel, B., H. A. van den Berg, E. Gostick, D. K. Cole, L. Wooldridge, J. Boulter, A. Milicic, D. A. Price, and A. K. Sewell. 2007. Different T cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic T lymphocyte activation and tetramer binding properties. J. Biol. Chem. 282: 23799-23810.
7. van den Berg, H. A., L.Wooldridge, B. Laugel, and A. K. Sewell. 2007. Coreceptor CD8-driven modulation of T cell antigen receptor specificity. J Theor Biol 249: 395-408.
8. Luescher, I. F., E. Vivier, A. Layer, J. Mahiou, F. Godeau, B. Malissen, and P. Romero. 1995. CD8 modulation of T-cell antigen receptor-ligand interactions on living cytotoxic T lymphocytes. Nature 373: 353-356.
9. Wooldridge, L., H. A. van den Berg, M. Glick, E. Gostick, B. Laugel, S. L. Hutchinson, A. Milicic, J. M. Brenchley, D. C. Douek, D. A. Price, and A. K. Sewell. 2005. Interaction between the CD8 coreceptor and major histocompatibility complex class I stabilizes T cell receptor-antigen complexes at the cell surface. J. Biol. Chem. 280: 27491-27501.
10. Veillette, A., M. A. Bookman, E. M. Horak, and J. B. Bolen. 1988. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck. Cell 55: 301-308.
11. Purbhoo, M. A., J. M. Boulter, D. A. Price, A. L. Vuidepot, C. S. Hourigan, P. R. Dunbar, K. Olson, S. J. Dawson, R. E. Phillips, B. K. Jakobsen, et al. 2001. The human CD8 coreceptor effects cytotoxic T cell activation and antigen sensitivity primarily by mediating complete phosphorylation of the T cell receptor zeta chain. J. Biol. Chem. 276: 32786-32792.
12. Arcaro, A., C. Grégoire, T. R. Bakker, L. Baldi, M. Jordan, L. Goffin, N. Boucheron, F. Wurm, P. A. van der Merwe, B. Malissen, and I. F. Luescher. 2001. CD8beta endows CD8 with efficient coreceptor function by coupling T cell receptor/CD3 to raft-associated CD8/p56(lck) complexes. J. Exp. Med. 194: 1485-1495.
13. Arcaro, A., C. Grégoire, N. Boucheron, S. Stotz, E. Palmer, B. Malissen, and I. F. Luescher. 2000. Essential role of CD8 palmitoylation in CD8 coreceptor function. J. Immunol. 165: 2068-2076. (Pubitemid 30643156)
14. Gao, G. F., J. Tormo, U.C. Gerth, J. R. Wyer, A. J. McMichael, D. I. Stuart, J. I. Bell, E. Y. Jones, and B. K. Jakobsen. 1997. Crystal structure of the complex between human CD8alpha(alpha) and HLA-A2. Nature 387: 630-634. (Pubitemid 27248771)
15. Wyer, J. R., B. E. Willcox, G. F. Gao, U. C. Gerth, S. J. Davis, J. I. Bell, P. A. van der Merwe, and B. K. Jakobsen. 1999. T cell receptor and coreceptor CD8 alphaalpha bind peptide-MHC independently and with distinct kinetics. Immunity 10: 219-225.
16. Gao, G. F., B. E.Willcox, J. R.Wyer, J. M. Boulter, C. A. O'Callaghan, K. Maenaka, D. I. Stuart, E. Y. Jones, P. A. Van Der Merwe, J. I. Bell, and B. K. Jakobsen. 2000. Classical and nonclassical class I major histocompatibility complex molecules exhibit subtle conformational differences that affect binding to CD8alphaalpha. J. Biol. Chem. 275: 15232-15238.
17. Dustin, M. L., D. E. Golan, D. M. Zhu, J. M. Miller, W. Meier, E. A. Davies, and P. A. van der Merwe. 1997. Low affinity interaction of human or rat T cell adhesion molecule CD2 with its ligand aligns adhering membranes to achieve high physiological affinity. J. Biol. Chem. 272: 30889-30898.
18. Cole, D. K., N. J. Pumphrey, J. M. Boulter, M. Sami, J. I. Bell, E. Gostick, D. A. Price, G. F. Gao, A. K. Sewell, and B. K. Jakobsen. 2007. Human TCR-binding affinity is governed by MHC class restriction. J. Immunol. 178: 5727-5734.
19. Varela-Rohena, A., P. E. Molloy, S. M. Dunn, Y. Li, M. M. Suhoski, R. G. Carroll, A. Milicic, T. Mahon, D. H. Sutton, B. Laugel, et al. 2008. Control of HIV-1 immune escape by CD8 T cells expressing enhanced T-cell receptor. Nat. Med. 14: 1390-1395.
20. Stone, J. D., A. S. Chervin, and D. M. Kranz. 2009. T-cell receptor binding affinities and kinetics: impact on T-cell activity and specificity. Immunology 126: 165-176.
21. Hutchinson, S. L., L. Wooldridge, S. Tafuro, B. Laugel, M. Glick, J. M. Boulter, B. K. Jakobsen, D. A. Price, and A. K. Sewell. 2003. The CD8 T cell coreceptor exhibits disproportionate biological activity at extremely low binding affinities. J. Biol. Chem. 278: 24285-24293.
22. Choi, E. M., J. L. Chen, L. Wooldridge, M. Salio, A. Lissina, N. Lissin, I. F.Hermans, J. D. Silk, F. Mirza, M. J. Palmowski, et al. 2003. High avidity antigen-specific CTL identified by CD8-independent tetramer staining. J. Immunol. 171: 5116-5123.
23. Sewell, A. K., G. C. Harcourt, P. J. Goulder, D. A. Price, and R. E. Phillips. 1997. Antagonism of cytotoxic T lymphocyte-mediated lysis by natural HIV-1 altered peptide ligands requires simultaneous presentation of agonist and antagonist peptides. Eur. J. Immunol. 27: 2323-2329.
24. Purbhoo, M. A., Y. Li, D. H. Sutton, J. E. Brewer, E. Gostick, G. Bossi, B. Laugel, R. Moysey, E. Baston, N. Liddy, et al. 2007. The HLA A*0201-restricted hTERT(540-548) peptide is not detected on tumor cells by a CTL clone or a high-affinity T-cell receptor. Mol. Cancer Ther. 6: 2081-2091.
25. Gostick, E., D. K. Cole, S. L. Hutchinson, L. Wooldridge, S. Tafuro, B. Laugel, A. Lissina, A. Oxenius, J. M. Boulter, D. A. Price, and A. K. Sewell. 2007. Functional and biophysical characterization of an HLA-A*6801- restricted HIV-specific T cell receptor. Eur. J. Immunol. 37: 479-486.
26. Burrows, S. R., S. L. Silins, D. J. Moss, R. Khanna, I. S. Misko, and V. P. Argaet. 1995. T cell receptor repertoire for a viral epitope in humans is diversified by tolerance to a background major histocompatibility complex antigen. J. Exp. Med. 182: 1703-1715.
27. Kjer-Nielsen, L., C. S. Clements, A. W. Purcell, A. G. Brooks, J. C. Whisstock, S. R. Burrows, J. McCluskey, and J. Rossjohn. 2003. A structural basis for the selection of dominant alphabeta T cell receptors in antiviral immunity. Immunity 18: 53-64. (Pubitemid 36120687)
28. Tynan, F. E., S. R. Burrows, A. M. Buckle, C. S. Clements, N. A. Borg, J. J. Miles, T. Beddoe, J. C. Whisstock, M. C. Wilce, S. L. Silins, et al. 2005. T cell receptor recognition of a 'super-bulged' major histocompatibility complex class I-bound peptide. Nat. Immunol. 6: 1114-1122.
29. Tynan, F. E., N. A. Borg, J. J. Miles, T. Beddoe, D. El-Hassen, S. L. Silins, W. J. van Zuylen, A.W. Purcell, L. Kjer-Nielsen, J. McCluskey, et al. 2005. High resolution structures of highly bulged viral epitopes bound to major histocompatibility complex class I. Implications for T-cell receptor engagement and T-cell immunodominance. J. Biol. Chem. 280: 23900-23909.
30. Willemsen, R., C. Ronteltap, M. Heuveling, R. Debets, and R. Bolhuis. 2005. Redirecting human CD4+ T lymphocytes to the MHC class I-restricted melanoma antigen MAGE-A1 by TCR alphabeta gene transfer requires CD8alpha. Gene Ther. 12: 140-146. (Pubitemid 40185917)
31. Willemsen, R. A., Z. Sebestyén, C. Ronteltap, C. Berrevoets, J. Drexhage, and R. Debets. 2006. CD8 alpha coreceptor to improve TCR gene transfer to treat melanoma: down-regulation of tumor-specific production of IL-4, IL-5, and IL-10. J. Immunol. 177: 991-998.
32. Betts, M. R., J. M. Brenchley, D. A. Price, S. C. De Rosa, D. C. Douek, M. Roederer, and R. A. Koup. 2003. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281: 65-78.
33. Choi, E. M., M. Palmowski, J. Chen, and V. Cerundolo. 2002. The use of chimeric A2K(b) tetramers to monitor HLA A2 immune responses in HLA A2 transgenic mice. J. Immunol. Methods 268: 35-41.
34. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer- Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
35. Wooldridge, L., A. Lissina, D. K. Cole, H. A. van den Berg, D. A. Price, and A. K. Sewell. 2009. Tricks with tetramers: how to get the most from multimeric peptide-MHC. Immunology 126: 147-164.
36. Burrows, S. R., N. Kienzle, A. Winterhalter, M. Bharadwaj, J. D. Altman, and A. Brooks. 2000. Peptide-MHC class I tetrameric complexes display exquisite ligand specificity. J. Immunol. 165: 6229-6234.
37. Schott, E., and H. L. Ploegh. 2002. Mouse MHC class I tetramers that are unable to bind to CD8 reveal the need for CD8 engagement in order to activate naive CD8 T cells. Eur. J. Immunol. 32: 3425-3434.
38. Valitutti, S., S. Müller, M. Cella, E. Padovan, and A. Lanzavecchia. 1995. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature 375: 148-151.
39. Zippelius, A., M. J. Pittet, P. Batard, N. Rufer, M. de Smedt, P. Guillaume, K. Ellefsen, D. Valmori, D. Liénard, J. Plum, et al. 2002. Thymic selection generates a large T cell pool recognizing a self-peptide in humans. J. Exp. Med. 195: 485-494.
40. Salio, M., M. J. Palmowski, A. Atzberger, I. F. Hermans, and V. Cerundolo. 2004. CpG-matured murine plasmacytoid dendritic cells are capable of in vivo priming of functional CD8 T cell responses to endogenous but not exogenous antigens. J. Exp. Med. 199: 567-579.
41. Yachi, P. P., J. Ampudia, N. R. Gascoigne, and T. Zal. 2005. Nonstimulatory peptides contribute to antigen-induced CD8-T cell receptor interaction at the immunological synapse. Nat. Immunol. 6: 785-792.
42. Anikeeva, N., T. Lebedeva, A. R. Clapp, E. R. Goldman, M. L. Dustin, H. Mattoussi, and Y. Sykulev. 2006. Quantum dot/peptide-MHC biosensors reveal strong CD8- dependent cooperation between self and viral antigens that augment the T cell response. Proc. Natl. Acad. Sci. USA 103: 16846-16851.
43. Kern, P. S., M. K. Teng, A. Smolyar, J. H. Liu, J. Liu, R. E. Hussey, R. Spoerl, H. C. Chang, E. L. Reinherz, and J. H. Wang. 1998. Structural basis of CD8 coreceptor function revealed by crystallographic analysis of a murine CD8alphaalpha ectodomain fragment in complex with H-2Kb. Immunity 9: 519-530.
44. Leishman, A. J., O. V. Naidenko, A. Attinger, F. Koning, C. J. Lena, Y. Xiong, H. C. Chang, E. Reinherz, M. Kronenberg, and H. Cheroutre. 2001. T cell responses modulated through interaction between CD8alphaalpha and the nonclassical MHC class I molecule, TL. Science 294: 1936-1939.
45. Tsujimura, K., Y. Obata, E. Kondo, K. Nishida, Y. Matsudaira, Y. Akatsuka, K. Kuzushima, and T. Takahashi. 2003. Thymus leukemia antigen (TL)-specific cytotoxic T lymphocytes recognize the alpha1/alpha2 domain of TL free from antigenic peptides. Int. Immunol. 15: 1319-1326.
46. Cole, D. K., and G. F. Gao. 2004. CD8: adhesion molecule, co-receptor and immunomodulator. Cell. Mol. Immunol. 1: 81-88.
47. Wooldridge, L., A. Lissina, J. Vernazza, E. Gostick, B. Laugel, S. L. Hutchinson, F. Mirza, P. R. Dunbar, J. M. Boulter, M. Glick, et al. 2007. Enhanced immunogenicity of CTL antigens through mutation of the CD8 binding MHC class I invariant region. Eur. J. Immunol. 37: 1323-1333.
48. Grebe, K. M., R. L. Clarke, and T. A. Potter. 2004. Ligation of CD8 leads to apoptosis of thymocytes that have not undergone positive selection. Proc. Natl. Acad. Sci. USA 101: 10410-10415.
49. Clarke, R. L., S. Thiemann, Y. Refaeli, G. Werlen, and T. A. Potter. 2009. A new function for LAT and CD8 during CD8-mediated apoptosis that is independent of TCR signal transduction. Eur. J. Immunol. 39: 1619-1631.
50. Wooldridge, L., S. L. Hutchinson, E. M. Choi, A. Lissina, E. Jones, F. Mirza, P. R. Dunbar, D. A. Price, V. Cerundolo, and A. K. Sewell. 2003. Anti-CD8 antibodies can inhibit or enhance peptide-MHC class I (pMHCI) multimer binding: this is paralleled by their effects on CTL activation and occurs in the absence of an interaction between pMHCI and CD8 on the cell surface. J. Immunol. 171: 6650-6660. (Pubitemid 37532097)