An altered gp100 peptide ligand with decreased binding by TCR and CD8α dissects T cell cytotoxicity from production of cytokines and activation of NFAT

Frontiers in Immunology

Volumn 4, Issue SEP, 2013, Pages

  Schaft, Niels ^a   Coccoris, Miriam ^a   Drexhage, Joost ^a   Knoop, Christiaan ^a   de Vries, I Jolanda M ^b   Adema, Gosse J ^b   Debets, Reno ^a  

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Activation of nuclear factor of activated T cells; Altered peptide ligands; Cytokine production; Cytotoxicity; Human T lymphocytes; T cell receptor

Indexed keywords

CD8ALPHA ANTIGEN; GAMMA INTERFERON; GLYCOPROTEIN GP 100; HLA A2 ANTIGEN; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL ACTIVATION; CELL SELECTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; MOLECULAR CLONING; PROTEIN BINDING; T LYMPHOCYTE ACTIVATION;

EID: 84885969897     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00270     Document Type: Article

References (52)

1. Coccoris M, Straetemans T, Govers C, Lamers C, Sleijfer S, Debets R. T cell receptor (TCR) gene therapy to treat melanoma: lessons from clinical and preclinical studies. Expert Opin Biol Ther (2010) 10:547-62. doi:10.1517/14712591003614756.
2. Rosenberg SA. Raising the bar: the curative potential of human cancer immunotherapy. Sci Transl Med (2012) 4:127s8. doi:10.1126/scitranslmed.3003634.
3. Johnson LA, Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, et al. Gene therapy with human and mouse T cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood (2009) 114:535-46. doi:10.1182/blood-2009-03-211714.
4. Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol (2011) 29:917-24. doi:10.1200/JCO.2010.32.2537.
5. Morgan RA, Dudley ME, Yu YY, Zheng Z, Robbins PF, Theoret MR, et al. High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens. J Immunol (2003) 171:3287-95.
6. Rubinstein MP, Kadima AN, Salem ML, Nguyen CL, Gillanders WE, Nishimura MI, et al. Transfer of TCR genes into mature T cells is accompanied by the maintenance of parental T cell avidity. J Immunol (2003) 170:1209-17.
7. Schaft N, Willemsen RA, de Vries J, Lankiewicz B, Essers BW, Gratama JW, et al. Peptide fine specificity of anti-glycoprotein 100 CTL is preserved following transfer of engineered TCR alpha beta genes into primary human T lymphocytes. J Immunol (2003) 170:2186-94.
8. Kersh GJ, Allen PM. Essential flexibility in the T cell recognition of antigen. Nature (1996) 380:495-8. doi:10.1038/380495a0.
9. Sloan-Lancaster J, Allen PM. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology. Annu Rev Immunol (1996) 14:1-27. doi:10.1146/annurev.immunol.14.1.1.
10. Katsara M, Minigo G, Plebanski M, Apostolopoulos V. The good, the bad and the ugly: how altered peptide ligands modulate immunity. Expert Opin Biol Ther (2008) 8:1873-84. doi:10.1517/14712590802494501.
11. Uhlin M, Masucci M, Levitsky V. Is the activity of partially agonistic MHC:peptide ligands dependent on the quality of immunological help? Scand J Immunol (2006) 64:581-7. doi:10.1111/j.1365-3083.2006.01850.x.
12. Carrabba MG, Castelli C, Maeurer MJ, Squarcina P, Cova A, Pilla L, et al. Suboptimal activation of CD8(+) T cells by melanoma-derived altered peptide ligands: role of Melan-A/MART-1 optimized analogues. Cancer Res (2003) 63:1560-7.
13. Madrenas J, Germain RN. Variant TCR ligands: new insights into the molecular basis of antigen-dependent signal transduction and T cell activation. Semin Immunol (1996) 8:83-101. doi:10.1006/smim.1996.0011.
14. Mitchell MS, Lund TA, Sewell AK, Marincola FM, Paul E, Schroder K, et al. The cytotoxic T cell response to peptide analogs of the HLA-A*0201-restricted MUC1 signal sequence epitope, M1.2. Cancer Immunol Immunother (2007) 56:287-301. doi:10.1007/s00262-006-0191-1.
15. Keogh E, Fikes J, Southwood S, Celis E, Chesnut R, Sette A. Identification of new epitopes from four different tumor-associated antigens: recognition of naturally processed epitopes correlates with HLA-A*0201-binding affinity. J Immunol (2001) 167:787-96.
16. Tanaka Y, Amos KD, Joo HG, Eberlein TJ, Goedegebuure PS. Modification of the HER2/NEU-derived tumor antigen GP2 improves induction of GP2-reactive cytotoxic T lymphocytes. Int J Cancer (2001) 94:540-4. doi:10.1002/ijc.1508.
17. Mimura K, Kono K, Southwood S, Fikes J, Takahashi A, Miyagawa N, et al. Substitution analog peptide derived from HER-2 can efficiently induce HER-2-specific, HLA-A24 restricted CTLs. Cancer Immunol Immunother (2006) 55:1358-66. doi:10.1007/s00262-006-0123-0.
18. Valmori D, Fonteneau JF, Lizana CM, Gervois N, Lienard D, Rimoldi D, et al. Enhanced generation of specific tumor-reactive CTL in vitro by selected Melan-A/MART-1 immunodominant peptide analogues. J Immunol (1998) 160:1750-8.
19. Parkhurst MR, Salgaller ML, Southwood S, Robbins PF, Sette A, Rosenberg SA, et al. Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A*0201-binding residues. J Immunol (1996) 157:2539-48.
20. Tang Y, Lin Z, Ni B, Wei J, Han J, Wang H, et al. An altered peptide ligand for naive cytotoxic T lymphocyte epitope of TRP-2(180-188) enhanced immunogenicity. Cancer Immunol Immunother (2007) 56:319-29. doi:10.1007/s00262-006-0195-x.
21. Terasawa H, Tsang KY, Gulley J, Arlen P, Schlom J. Identification and characterization of a human agonist cytotoxic T-lymphocyte epitope of human prostate-specific antigen. Clin Cancer Res (2002) 8:41-53.
22. Chen JL, Dunbar PR, Gileadi U, Jager E, Gnjatic S, Nagata Y, et al. Identification of NY-ESO-1 peptide analogues capable of improved stimulation of tumor-reactive CTL. J Immunol (2000) 165:948-55.
23. Parker KC, Bednarek MA, Hull LK, Utz U, Cunningham B, Zweerink HJ, et al. Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2. J Immunol (1992) 149:3580-7.
24. Cole DK, Edwards ES, Wynn KK, Clement M, Miles JJ, Ladell K, et al. Modification of MHC anchor residues generates heteroclitic peptides that alter TCR binding and T cell recognition. J Immunol (2010) 185:2600-10. doi:10.4049/jimmunol.1000629.
25. Speiser DE, Baumgaertner P, Voelter V, Devevre E, Barbey C, Rufer N, et al. Unmodified self antigen triggers human CD8 T cells with stronger tumor reactivity than altered antigen. Proc Natl Acad Sci U S A (2008) 105:3849-54. doi:10.1073/pnas.0800080105.
26. Lesterhuis WJ, Schreibelt G, Scharenborg NM, Brouwer HM, Gerritsen MJ, Croockewit S, et al. Wild-type and modified gp100 peptide-pulsed dendritic cell vaccination of advanced melanoma patients can lead to long-term clinical responses independent of the peptide used. Cancer Immunol Immunother (2011) 60:249-60. doi:10.1007/s00262-010-0942-x.
27. Bakker AB, Schreurs MW, de Boer AJ, Kawakami Y, Rosenberg SA, Adema GJ, et al. Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J Exp Med (1994) 179:1005-9. doi:10.1084/jem.179.3.1005.
28. Kawakami Y, Eliyahu S, Delgado CH, Robbins PF, Sakaguchi K, Appella E, et al. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc Natl Acad Sci U S A (1994) 91:6458-62. doi:10.1073/pnas.91.14.6458.
29. Nijman HW, Houbiers JG, van der Burg SH, Vierboom MP, Kenemans P, Kast WM, et al. Characterization of cytotoxic T lymphocyte epitopes of a self-protein, p53, and a non-self-protein, influenza matrix: relationship between major histocompatibility complex peptide binding affinity and immune responsiveness to peptides. J Immunother Emphasis Tumor Immunol (1993) 14:121-6. doi:10.1097/00002371-199308000-00007.
30. van der Burg SH, Ras E, Drijfhout JW, Benckhuijsen WE, Bremers AJ, Melief CJ, et al. An HLA class I peptide-binding assay based on competition for binding to class I molecules on intact human B cells. Identification of conserved HIV-1 polymerase peptides binding to HLA-A*0301. Hum Immunol (1995) 44:189-98. doi:10.1016/0198-8859(95)00105-0.
31. Govers C, Berrevoets C, Treffers-Westerlaken E, Broertjes M, Debets R. Magnetic-activated cell sorting of TCR-engineered T cells using tCD34 as a gene marker, but not pMHC multimers, results in significant numbers of functional CD4 and CD8 T cells. Hum Gene Ther Methods (2012): doi:10.1089/hgtb.2012.074. [Epub ahead of print].
32. Lamers CH, Willemsen RA, van Elzakker P, van Krimpen BA, Gratama JW, Debets R. Phoenix-ampho outperforms PG13 as retroviral packaging cells to transduce human T cells with tumor-specific receptors: implications for clinical immunogene therapy of cancer. Cancer Gene Ther (2006) 13:503-9. doi:10.1038/sj.cgt.7700916.
33. Schaft N, Lankiewicz B, Drexhage J, Berrevoets C, Moss DJ, Levitsky V, et al. T cell re-targeting to EBV antigens following TCR gene transfer: CD28-containing receptors mediate enhanced antigen-specific IFNgamma production. Int Immunol (2006) 18:591-601. doi:10.1093/intimm/dxh401.
34. Willemsen RA, Sebestyen Z, Ronteltap C, Berrevoets C, Drexhage J, Debets R. 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 (2006) 177:991-8.
35. Schaft N, Lankiewicz B, Gratama JW, Bolhuis RL, Debets R. Flexible and sensitive method to functionally validate tumor-specific receptors via activation of NFAT. J Immunol Methods (2003) 280:13-24. doi:10.1016/S0022-1759(03)00067-X.
36. Weijtens M, Willemsen R, Hart E, Bolhuis R. A retroviral vector system 'STITCH' in combination with an optimized single chain antibody chimeric receptor gene structure allows efficient gene transduction and expression in human T lymphocytes. Gene Ther (1998) 5:1195-203. doi:10.1038/sj.gt.3300696.
37. Bakker AB, Marland G, de Boer AJ, Huijbens RJ, Danen EH, Adema GJ, et al. Generation of antimelanoma cytotoxic T lymphocytes from healthy donors after presentation of melanoma-associated antigen-derived epitopes by dendritic cells in vitro. Cancer Res (1995) 55:5330-4.
38. Micheletti F, Canella A, Vertuani S, Marastoni M, Tosi L, Volinia S, et al. Supra-agonist peptides enhance the reactivation of memory CTL responses. J Immunol (2000) 165:4264-71.
39. Bachmann MF, Oxenius A, Speiser DE, Mariathasan S, Hengartner H, Zinkernagel RM, et al. Peptide-induced T cell receptor down-regulation on naive T cells predicts agonist/partial agonist properties and strictly correlates with T cell activation. Eur J Immunol (1997) 27:2195-203. doi:10.1002/eji.1830270912.
40. Griffiths GM, Mueller C. Expression of perforin and granzymes in vivo: potential diagnostic markers for activated cytotoxic cells. Immunol Today (1991) 12:415-9. doi:10.1016/0167-5699(91)90145-J.
41. Hollsberg P, Weber WE, Dangond F, Batra V, Sette A, Hafler DA. Differential activation of proliferation and cytotoxicity in human T cell lymphotropic virus type I Tax-specific CD8 T cells by an altered peptide ligand. Proc Natl Acad Sci U S A (1995) 92:4036-40. doi:10.1073/pnas.92.9.4036.
42. Itoh Y, Hemmer B, Martin R, Germain RN. Serial TCR engagement and down-modulation by peptide:MHC molecule ligands: relationship to the quality of individual TCR signaling events. J Immunol (1999) 162:2073-80.
43. Valitutti S, Muller S, Dessing M, Lanzavecchia A. Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J Exp Med (1996) 183:1917-21. doi:10.1084/jem.183.4.1917.
44. Chau LA, Bluestone JA, Madrenas J. Dissociation of intracellular signaling pathways in response to partial agonist ligands of the T cell receptor. J Exp Med (1998) 187:1699-709. doi:10.1084/jem.187.10.1699.
45. Hemmer B, Stefanova I, Vergelli M, Germain RN, Martin R. Relationships among TCR ligand potency, thresholds for effector function elicitation, and the quality of early signaling events in human T cells. J Immunol (1998) 160:5807-14.
46. Wei CH, Beeson C, Masucci MG, Levitsky V. A partially agonistic peptide acts as a selective inducer of apoptosis in CD8+ CTLs. J Immunol (1999) 163:2601-9.
47. Kim JR, Irie A, Tsukamoto H, Nishimura Y. A role of kinase inactive ZAP-70 in altered peptide ligand stimulated T cell activation. Biochem Biophys Res Commun (2006) 341:19-27. doi:10.1016/j.bbrc.2005.12.143.
48. Madrenas J. Differential signalling by variant ligands of the T cell receptor and the kinetic model of T cell activation. Life Sci (1999) 64:717-31. doi:10.1016/S0024-3205(98)00381-6.
49. Krummel MF, Davis MM. Dynamics of the immunological synapse: finding, establishing and solidifying a connection. Curr Opin Immunol (2002) 14:66-74. doi:10.1016/S0952-7915(01)00299-0.
50. Abe BT, Macian F. Uncovering the mechanisms that regulate tumor-induced T cell anergy. Oncoimmunology (2013) 2:e22679. doi:10.4161/onci.22679.
51. Cole DK, Laugel B, Clement M, Price DA, Wooldridge L, Sewell AK. The molecular determinants of CD8 co-receptor function. Immunology (2012) 137:139-48. doi:10.1111/j.1365-2567.2012.03625.x.
52. Laugel B, van den Berg HA, Gostick E, Cole DK, Wooldridge L, Boulter J, et al. Different T cell receptor affinity thresholds and CD8 coreceptor dependence govern cytotoxic T lymphocyte activation and tetramer binding properties. J Biol Chem (2007) 282:23799-810. doi:10.1074/jbc. M700976200.