Co-potentiation of antigen recognition: A mechanism to boost weak T cell responses and provide immunotherapy in vivo

Science Advances

Volumn 1, Issue 9, 2015, Pages

  Hoffmann, Michele M ^a,c   Molina Mendiola, Carlos ^a,b,d,e   Nelson, Alfreda D ^a,c   Parks, Christopher A ^a,d   Reyes, Edwin E ^a,c   Hansen, Michael J ^a   Rajagopalan, Govindarajan ^a   Pease, Larry R ^a   Schrum, Adam G ^a   Gil, Diana ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITAT POLITÈCNICA DE CATALUNYA   (Spain)

^c Initiative to Maximize Student Diversity   (United States)

^d Undergraduate Research Employment Program   (United States)

^e Indra Business Consulting   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; ANTIGENS; CELL MEMBRANES; CELLS; CYTOLOGY; DERMATOLOGY; ONCOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTIVE IMMUNITY; ANTIGEN RECEPTORS; ANTIGEN RECOGNITION; IMMUNE RESPONSE; IMMUNOTHERAPEUTIC; MULTI-PROTEIN COMPLEX; SIGNAL INTENSITIES; T-CELL RECEPTORS;

T-CELLS;

EID: 85042065811     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1500415     Document Type: Article

References (44)

1. B. Alarcón, D. Gil, P. Delgado, W. W. Schamel, Initiation of TCR signaling: Regulation within CD3 dimers. Immunol. Rev. 191, 38–46 (2003).
2. P. A. van der Merwe, O. Dushek, Mechanisms for T cell receptor triggering. Nat. Rev. Immunol. 11, 47–55 (2011).
3. T. Beddoe, Z. Chen, C. S. Clements, L. K. Ely, S. R. Bushell, J. P. Vivian, L. Kjer-Nielsen, S. S. Pang, M. A. Dunstone, Y. C. Liu, W. A. Macdonald, M. A. Perugini, M. C. J. Wilce, S. R. Burrows, A. W. Purcell, T. Tiganis, S. P. Bottomley, J. McCluskey, J. Rossjohn, Antigen ligation triggers a conformational change within the constant domain of the ab T cell receptor. Immunity 30, 777–788 (2009).
4. C. A. Janeway Jr., Ligands for the T-cell receptor: Hard times for avidity models. Immunol. Today 16, 223–225 (1995).
5. C. A. Janeway Jr., U. Dianzani, P. Portoles, S. Rath, E.-P. Reich, J. Rojo, J. Yagi, D. B. Murphy, Cross-linking and conformational change in T-cell receptors: Role in activation and in repertoire selection. Cold Spring Harb. Symp. Quant. Biol. 54, 657–666 (1989).
6. L. Kjer-Nielsen, C. S. Clements, A. G. Brooks, A. W. Purcell, J. McCluskey, J. Rossjohn, The 1.5 Å crystal structure of a highly selected antiviral T cell receptor provides evidence for a structural basis of immunodominance. Structure 10, 1521–1532 (2002).
7. J. M. Rojo, C. A. Janeway Jr., The biologic activity of anti–T cell receptor V region monoclonal antibodies is determined by the epitope recognized. J. Immunol. 140, 1081–1088 (1988).
8. J. M. Rojo, K. Saizawa, C. A. Janeway Jr., Physical association of CD4 and the T-cell receptor can be induced by anti–T-cell receptor antibodies. Proc. Natl. Acad. Sci. U.S.A. 86, 3311–3315 (1989).
9. D. Gil, W. W. A. Schamel, M. Montoya, F. Sánchez-Madrid, B. Alarcón, Recruitment of Nck by CD3e reveals a ligand-induced conformational change essential for T cell receptor signaling and synapse formation. Cell 109, 901–912 (2002).
10. S. Minguet, M. Swamy, B. Alarcón, I. F. Luescher, W. W. A. Schamel, Full activation of the T cell receptor requires both clustering and conformational changes at CD3. Immunity 26, 43–54 (2007).
11. R. M. Risueno, W. W. Schamel, B. Alarcon, T cell receptor engagement triggers its CD3e and CD3z subunits to adopt a compact, locked conformation. PLOS One 3, e1747 (2008).
12. C. Xu, E. Gagnon, M. E. Call, J. R. Schnell, C. D. Schwieters, C. V. Carman, J. J. Chou, K. W. Wucherpfennig, Regulation of T cell receptor activation by dynamic membrane binding of the CD3e cytoplasmic tyrosine-based motif. Cell 135, 702–713 (2008).
13. Z.-Y. J. Sun, K. S. Kim, G. Wagner, E. L. Reinherz, Mechanisms contributing to T cell receptor signaling and assembly revealed by the solution structure of an ectodomain fragment of the CD3eg heterodimer. Cell 105, 913–923 (2001).
14. M. S. Kuhns, M. M. Davis, K. C. Garcia, Deconstructing the form and function of the TCR/ CD3 complex. Immunity 24, 133–139 (2006).
15. S. T. Kim, K. Takeuchi, Z.-Y. J. Sun, M. Touma, C. E. Castro, A. Fahmy, M. J. Lang, G. Wagner, E. L. Reinherz, The ab T cell receptor is an anisotropic mechanosensor. J. Biol. Chem. 284, 31028–31037 (2009).
16. S. T. Kim, M. Touma, K. Takeuchi, Z.-Y. J. Sun, V. P. Dave, D. J. Kappes, G. Wagner, E. L. Reinherz, Distinctive CD3 heterodimeric ectodomain topologies maximize antigen-triggered activation of ab T cell receptors. J. Immunol. 185, 2951–2959 (2010).
17. D. K. Das, Y. Feng, R. J. Mallis, X. Li, D. B. Keskin, R. E. Hussey, S. K. Brady, J.-H. Wang, G. Wagner, E. L. Reinherz, M. J. Lang, Force-dependent transition in the T-cell receptor b-subunit allosterically regulates peptide discrimination and pMHC bond lifetime. Proc. Natl. Acad. Sci. U.S.A. 112, 1517–1522 (2015).
18. M. Krogsgaard, N. Prado, E. J. Adams, X.-L. He, D.-C. Chow, D. B. Wilson, K. C. Garcia, M. M. Davis, Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Mol. Cell 12, 1367–1378 (2003).
19. Y. Wang, D. Becker, T. Vass, J. White, P. Marrack, J. W. Kappler, A conserved CXXC motif in CD3e is critical for T cell development and TCR signaling. PLOS Biol. 7, e1000253 (2009).
20. W. F. Hawse, M. M. Champion, M. V. Joyce, L. M. Hellman, M. Hossain, V. Ryan, B. G. Pierce, Z. Weng, B. M. Baker, Cutting edge: Evidence for a dynamically driven T cell signaling mechanism. J. Immunol. 188, 5819–5823 (2012).
21. A. D. Nelson, M. M. Hoffmann, C. A. Parks, S. Dasari, A. G. Schrum, D. Gil, IgG Fab fragments forming bivalent complexes by a conformational mechanism that is reversible by osmo-lytes. J. Biol. Chem. 287, 42936–42950 (2012).
22. J. de la Cruz, T. Kruger, C. A. Parks, R. L. Silge, N. S. C. van Oers, I. F. Luescher, A. G. Schrum, D. Gil, Basal and antigen-induced exposure of the proline-rich sequence in CD3e. J. Immunol. 186, 2282–2290 (2011).
23. D. Gil, A. G. Schrum, B. Alarcón, E. Palmer, T cell receptor engagement by peptide–MHC ligands induces a conformational change in the CD3 complex of thymocytes. J. Exp. Med. 201, 517–522 (2005).
24. R. M. Risueño, D. Gil, E. Fernández, F. Sánchez-Madrid, B. Alarcón, Ligand-induced conformational change in the T-cell receptor associated with productive immune synapses. Blood 106, 601–608 (2005).
25. P. Tailor, S. Tsai, A. Shameli, P. Serra, J. Wang, S. Robbins, M. Nagata, A. L. Szymczak-Workman, D. A. A. Vignali, P. Santamaria, The proline-rich sequence of CD3e as an amplifier of low-avidity TCR signaling. J. Immunol. 181, 243–255 (2008).
26. D. Gil, A. G. Schrum, M. A. Daniels, E. Palmer, A role for CD8 in the developmental tuning of antigen recognition and CD3 conformational change. J. Immunol. 180, 3900–3909 (2008).
27. F. S. Hodi, S. J. O’Day, D. F. McDermott, R. W. Weber, J. A. Sosman, J. B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J. C. Hassel, W. Akerley, A. J. M. van den Eertwegh, J. Lutzky, P. Lorigan, J. M. Vaubel, G. P. Linette, D. Hogg, C. H. Ottensmeier, C. Lebbé, C. Peschel, I. Quirt, J. I. Clark, J. D. Wolchok, J. S. Weber, J. Tian, M. J. Yellin, G. M. Nichol, A. Hoos, W. J. Urba, Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363, 711–723 (2010).
28. P. G. Coulie, C. Uyttenhove, P. Wauters, N. Manolios, R. D. Klausner, L. E. Samelson, J. Van Snick, Identification of a murine monoclonal antibody specific for an allotypic determinant on mouse CD3. Eur. J. Immunol. 21, 1703–1709 (1991).
29. R. J. Salmond, R. J. Brownlie, V. L. Morrison, R. Zamoyska, The tyrosine phosphatase PTPN22 discriminates weak self peptides from strong agonist TCR signals. Nat. Immunol. 15, 875–883 (2014).
30. M. Alegre, P. Vandenabeele, V. Flamand, M. Moser, O. Leo, D. Abramowicz, J. Urbain, W. Fiers, M. Goldman, Hypothermia and hypoglycemia induced by anti-CD3 monoclonal antibody in mice: Role of tumor necrosis factor. Eur. J. Immunol. 20, 707–710 (1990).
31. V. R. Chowdhary, A. Y. Tilahun, C. R. Clark, J. P. Grande, G. Rajagopalan, Chronic exposure to staphylococcal superantigen elicits a systemic inflammatory disease mimicking lupus. J. Immunol. 189, 2054–2062 (2012).
32. I. J. Fidler, D. M. Gersten, M. B. Budmen, Characterization in vivo and in vitro of tumor cells selected for resistance to syngeneic lymphocyte-mediated cytotoxicity. Cancer Res. 36, 3160–3165 (1976).
33. + T cells are differentiated effector cells expressing high levels of CD11a and PD-1 but are unable to control tumor growth. Oncoimmunology 2, e23972 (2013).
34. N. Wang, B. Wang, M. Salio, D. Allen, J. She, C. Terhorst, Expression of a CD3 epsilon trans-gene in CD3 epsilon(null) mice does not restore CD3 gamma and delta expression but efficiently rescues T cell development from a subpopulation of prothymocytes. Int. Immunol. 10, 1777–1788 (1998).
35. A. Ferrer, A. G. Schrum, D. Gil, A PCR-based method to genotype mice knocked out for all four CD3 subunits, the standard recipient strain for retrogenic TCR/CD3 bone marrow reconstitution technology. Biores. Open Access 2, 222–226 (2013).
36. + T cells. J. Exp. Med. 198, 569–580 (2003).
37. W. W. Overwijk, A. Tsung, K. R. Irvine, M. R. Parkhurst, T. J. Goletz, K. Tsung, M. W. Carroll, C. Liu, B. Moss, S. A. Rosenberg, N. P. Restifo, gp100/pmel 17 is a murine tumor rejection antigen: Induction of “self”-reactive, tumoricidal T cells using high-affinity, altered peptide ligand. J. Exp. Med. 188, 277–286 (1998).
38. W. W. Overwijk, N. P. Restifo, B16 as a mouse model for human melanoma. Curr. Protoc. Immunol. Chapter 20, Unit 20 1 (2001).
39. R. Das, R. Verma, M. Sznol, C. S. Boddupalli, S. N. Gettinger, H. Kluger, M. Callahan, J. D. Wolchok, R. Halaban, M. V. Dhodapkar, K. M. Dhodapkar, Combination therapy with anti–CTLA-4 and anti–PD-1 leads to distinct immunologic changes in vivo. J. Immunol. 194, 950–959 (2015).
40. S. Yao, Y. Zhu, L. Chen, Advances in targeting cell surface signalling molecules for immune modulation. Nat. Rev. Drug Discov. 12, 130–146 (2013).
41. J. J. Boniface, J. D. Rabinowitz, C. Wülfing, J. Hampl, Z. Reich, J. D. Altman, R. M. Kantor, C. Beeson, H. M. McConnell, M. M. Davis, Initiation of signal transduction through the T cell receptor requires the multivalent engagement of peptide/MHC ligands. Immunity 9, 459–466 (1998).
42. J. D. Stone, L. J. Stern, CD8 T cells, like CD4 T cells, are triggered by multivalent engagement of TCRs by MHC-peptide ligands but not by monovalent engagement. J. Immunol. 176, 1498–1505 (2006).
43. + T cells. Cancer Res. 71, 5455–5466 (2011).
44. 130 in the absence of endogenous CD4 help, tumor necrosis factor alpha, gamma interferon, perforin, or costimulation through CD28. J. Virol. 73, 3702–3708 (1999).