Subtle changes in TCRα CDR1 profoundly increase the sensitivity of CD4 T cells

Molecular Immunology

Volumn 53, Issue 3, 2013, Pages 283-294

  Lynch, Jennifer N ^a   Donermeyer, David L ^a   Weber, K Scott ^a   Kranz, David M ^b   Allen, Paul M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Affinity; Anergy; CD4; CDR1; Selection; T cell

Indexed keywords

INTERLEUKIN 2; MUTANT PROTEIN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR AFFINITY; TRANSGENIC MOUSE;

ANIMALS; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; COMPLEMENTARITY DETERMINING REGIONS; HEMOGLOBINS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HYBRIDOMAS; KINETICS; LIGANDS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA;

MUS MUSCULUS;

EID: 84865957987     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2012.08.020     Document Type: Article

References (71)

1. Adams J.J., Narayanan S., Liu B., Birnbaum M.E., Kruse A.C., Bowerman N.A., Chen W., Levin A.M., Connolly J.M., Zhu C., Kranz D.M., Garcia K.C. T cell receptor signaling is limited by docking geometry to peptide-major histocompatibility complex. Immunity 2011, 35:681-693.
2. Alberola-Ila J., Hogquist K.A., Swan K.A., Bevan M.J., Perlmutter R.M. Positive and negative selection invoke distinct signaling pathways. Journal of Experimental Medicine 1996, 184:9-18.
3. Armstrong K.M., Piepenbrink K.H., Baker B.M. Conformational changes and flexibility in T-cell receptor recognition of peptide-MHC complexes. Biochemical Journal 2008, 415:183-196.
4. Basu D., Horvath S., O'Mara L., Donermeyer D., Allen P.M. Two MHC surface amino acid differences distinguish foreign peptide recognition from autoantigen specificity. Journal of Immunology 2001, 166:4005-4011.
5. Bautista J.L., Lio C.W., Lathrop S.K., Forbush K., Liang Y., Luo J., Rudensky A.Y., Hsieh C.S. Intraclonal competition limits the fate determination of regulatory T cells in the thymus. Nature Immunology 2009, 10:610-617.
6. Beal A.M., Anikeeva N., Varma R., Cameron T.O., Vasiliver-Shamis G., Norris P.J., Dustin M.L., Sykulev Y. Kinetics of early T cell receptor signaling regulate the pathway of lytic granule delivery to the secretory domain. Immunity 2009, 31:632-642.
7. Borg N.A., Ely L.K., Beddoe T., Macdonald W.A., Reid H.H., Clements C.S., Purcell A.W., Kjer-Nielsen L., Miles J.J., Burrows S.R., McCluskey J., Rossjohn J. The CDR3 regions of an immunodominant T cell receptor dictate the 'energetic landscape' of peptide-MHC recognition. Nature Immunology 2005, 6:171-180.
8. Burrows S.R., Chen Z., Archbold J.K., Tynan F.E., Beddoe T., Kjer-Nielsen L., Miles J.J., Khanna R., Moss D.J., Liu Y.C., Gras S., Kostenko L., Brennan R.M., Clements C.S., Brooks A.G., Purcell A.W., McCluskey J., Rossjohn J. Hard wiring of T cell receptor specificity for the major histocompatibility complex is underpinned by TCR adaptability. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:10608-10613.
9. Chlewicki L.K., Holler P.D., Monti B.C., Clutter M.R., Kranz D.M. High-affinity, peptide-specific T cell receptors can be generated by mutations in CDR1, CDR2 or CDR3. Journal of Molecular Biology 2005, 346:223-239.
10. Dai S., Huseby E.S., Rubtsova K., Scott-Browne J., Crawford F., Macdonald W.A., Marrack P., Kappler J.W. Crossreactive T Cells spotlight the germline rules for alphabeta T cell-receptor interactions with MHC molecules. Immunity 2008, 28:324-334.
11. Daniels M.A., Teixeiro E., Gill J., Hausmann B., Roubaty D., Holmberg K., Werlen G., Hollander G.A., Gascoigne N.R., Palmer E. Thymic selection threshold defined by compartmentalization of Ras/MAPK signalling. Nature 2006, 444:724-729.
12. Dao T., Blander J.M., Sant'Angelo D.B. Recognition of a specific self-peptide: self-MHC class II complex is critical for positive selection of thymocytes expressing the D10 TCR. Journal of Immunology 2003, 170:48-54.
13. Davis M.M., Boniface J.J., Reich Z., Lyons D., Hampl J., Arden B., Chien Y. Ligand recognition by alpha beta T cell receptors. Annual Review of Immunology 1998, 16:523-544.
14. Davis-Harrison R.L., Insaidoo F.K., Baker B.M. T cell receptor binding transition states and recognition of peptide/MHC. Biochemistry 2007, 46:1840-1850.
15. De Boer R.J., Homann D., Perelson A.S. Different dynamics of CD4+ and CD8+ T cell responses during and after acute lymphocytic choriomeningitis virus infection. Journal of Immunology 2003, 171:3928-3935.
16. Delaney J.R., Sykulev Y., Eisen H.N., Tonegawa S. Differences in the level of expression of class I major histocompatibility complex proteins on thymic epithelial and dendritic cells influence the decision of immature thymocytes between positive and negative selection. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:5235-5240.
17. Edwards L.J., Evavold B.D. A unique unresponsive CD4+ T cell phenotype post TCR antagonism. Cellular Immunology 2010, 261:64-68.
18. Evavold B.D., Sloan-Lancaster J., Allen P.M. Tickling the TCR: selective T-cell functions stimulated by altered peptide ligands. Immunology Today 1993, 14:602-609.
19. Evavold B.D., Williams S.G., Hsu B.L., Buus S., Allen P.M. Complete dissection of the Hb(64-76) determinant using T helper 1, T helper 2 clones, and T cell hybridomas. Journal of Immunology 1992, 148:347-353.
20. Felix N.J., Donermeyer D.L., Horvath S., Walters J.J., Gross M.L., Suri A., Allen P.M. Alloreactive T cells respond specifically to multiple distinct peptide-MHC complexes. Nature Immunology 2007, 8:388-397.
21. Gakamsky D.M., Luescher I.F., Pecht I. T cell receptor-ligand interactions: a conformational preequilibrium or an induced fit. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:9063-9066.
22. Garbi N., Hammerling G.J., Probst H.C., van den Broek M. Tonic T cell signalling and T cell tolerance as opposite effects of self-recognition on dendritic cells. Current Opinion in Immunology 2010, 22:601-608.
23. Garcia K.C., Radu C.G., Ho J., Ober R.J., Ward E.S. Kinetics and thermodynamics of T cell receptor-autoantigen interactions in murine experimental autoimmune encephalomyelitis. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:6818-6823.
24. Garcia K.C., Teyton L., Wilson I.A. Structural basis of T cell recognition. Annual Review of Immunology 1999, 17:369-397.
25. Gascoigne N.R., Palmer E. Signaling in thymic selection. Current Opinion in Immunology 2011, 23:207-212.
26. Hogquist K.A., Bevan M.J. The nature of the peptide/MHC ligand involved in positive selection. Seminars in Immunology 1996, 8:63-68.
27. Hogquist K.A., Tomlinson A.J., Kieper W.C., McGargill M.A., Hart M.C., Naylor S., Jameson S.C. Identification of a naturally occurring ligand for thymic positive selection. Immunity 1997, 6:389-399.
28. Holler P.D., Kranz D.M. Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 2003, 18:255-264.
29. Holler P.D., Kranz D.M. T cell receptors: affinities, cross-reactivities, and a conformer model. Molecular Immunology 2004, 40:1027-1031.
30. Holst J., Szymczak-Workman A.L., Vignali K.M., Burton A.R., Workman C.J., Vignali D.A. Generation of T-cell receptor retrogenic mice. Nature Protocols 2006, 1:406-417.
31. Huang J., Zarnitsyna V.I., Liu B., Edwards L.J., Jiang N., Evavold B.D., Zhu C. The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 2010, 464:932-936.
32. Huppa J.B., Axmann M., Mortelmaier M.A., Lillemeier B.F., Newell E.W., Brameshuber M., Klein L.O., Schutz G.J., Davis M.M. TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 2010, 463:963-967.
33. Huseby E.S., Crawford F., White J., Marrack P., Kappler J.W. Interface-disrupting amino acids establish specificity between T cell receptors and complexes of major histocompatibility complex and peptide. Nature Immunology 2006, 7:1191-1199.
34. Jones L.L., Colf L.A., Bankovich A.J., Stone J.D., Gao Y.G., Chan C.M., Huang R.H., Garcia K.C., Kranz D.M. Different thermodynamic binding mechanisms and peptide fine specificities associated with a panel of structurally similar high-affinity T cell receptors. Biochemistry 2008, 47:12398-12408.
35. Kersh G.J., Allen P.M. Essential flexibility in the T-cell recognition of antigen. Nature 1996, 380:495-498.
36. Kersh G.J., Donermeyer D.L., Frederick K.E., White J.M., Hsu B.L., Allen P.M. TCR transgenic mice in which usage of transgenic alpha- and beta-chains is highly dependent on the level of selecting ligand. Journal of Immunology 1998, 161:585-593.
37. Kirberg J., Swat W., Rocha B., Kisielow P., von Boehmer H. Induction of tolerance in immature and mature T cells. Transplantation Proceedings 1993, 25:279-280.
38. Klein L., Hinterberger M., Wirnsberger G., Kyewski B. Antigen presentation in the thymus for positive selection and central tolerance induction. Nature Reviews. Immunology 2009, 9:833-844.
39. Kosmrlj A., Jha A.K., Huseby E.S., Kardar M., Chakraborty A.K. How the thymus designs antigen-specific and self-tolerant T cell receptor sequences. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:16671-16676.
40. Krogsgaard M., Prado N., Adams E.J., He X.L., Chow D.C., Wilson D.B., Garcia K.C., Davis M.M. Evidence that structural rearrangements and/or flexibility during TCR binding can contribute to T cell activation. Molecular Cell 2003, 12:1367-1378.
41. Lathrop S.K., Santacruz N.A., Pham D., Luo J., Hsieh C.S. Antigen-specific peripheral shaping of the natural regulatory T cell population. Journal of Experimental Medicine 2008, 205:3105-3117.
42. Lo W.L., Felix N.J., Walters J.J., Rohrs H., Gross M.L., Allen P.M. An endogenous peptide positively selects and augments the activation and survival of peripheral CD4+ T cells. Nature Immunology 2009, 10:1155-1161.
43. Lyons D.S., Lieberman S.A., Hampl J., Boniface J.J., Chien Y., Berg L.J., Davis M.M. A TCR binds to antagonist ligands with lower affinities and faster dissociation rates than to agonists. Immunity 1996, 5:53-61.
44. Macian F., Im S.H., Garcia-Cozar F.J., Rao A. T-cell anergy. Current Opinion in Immunology 2004, 16:209-216.
45. Manning T.C., Parke E.A., Teyton L., Kranz D.M. Effects of complementarity determining region mutations on the affinity of an alpha/beta T cell receptor: measuring the energy associated with CD4/CD8 repertoire skewing. Journal of Experimental Medicine 1999, 189:461-470.
46. Marrack P., Rubtsova K., Scott-Browne J., Kappler J.W. T cell receptor specificity for major histocompatibility complex proteins. Current Opinion in Immunology 2008, 20:203-207.
47. Masteller E.L., Warner M.R., Ferlin W., Judkowski V., Wilson D., Glaichenhaus N., Bluestone J.A. Peptide-MHC class II dimers as therapeutics to modulate antigen-specific T cell responses in autoimmune diabetes. Journal of Immunology 2003, 171:5587-5595.
48. Mirshahidi S., Ferris L.C., Sadegh-Nasseri S. The magnitude of TCR engagement is a critical predictor of T cell anergy or activation. Journal of Immunology 2004, 172:5346-5355.
49. Naeher D., Daniels M.A., Hausmann B., Guillaume P., Luescher I., Palmer E. A constant affinity threshold for T cell tolerance. Journal of Experimental Medicine 2007, 204:2553-2559.
50. Nalefski E.A., Wong J.G., Rao A. Amino acid substitutions in the first complementarity-determining region of a murine T-cell receptor alpha chain affect antigen-major histocompatibility complex recognition. Journal of Biological Chemistry 1990, 265:8842-8846.
51. Persaud S.P., Donermeyer D.L., Weber K.S., Kranz D.M., Allen P.M. High-affinity T cell receptor differentiates cognate peptide-MHC and altered peptide ligands with distinct kinetics and thermodynamics. Molecular Immunology 2010, 47:1793-1801.
52. Pierce B.G., Haidar J.N., Yu Y., Weng Z. Combinations of affinity-enhancing mutations in a T cell receptor reveal highly nonadditive effects within and between complementarity determining regions and chains. Biochemistry 2010, 49:7050-7059.
53. Qi S., Krogsgaard M., Davis M.M., Chakraborty A.K. Molecular flexibility can influence the stimulatory ability of receptor-ligand interactions at cell-cell junctions. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:4416-4421.
54. Rabinowitz J.D., Beeson C., Wulfing C., Tate K., Allen P.M., Davis M.M., McConnell H.M. Altered T cell receptor ligands trigger a subset of early T cell signals. Immunity 1996, 5:125-135.
55. Reiser J.B., Darnault C., Gregoire C., Mosser T., Mazza G., Kearney A., van der Merwe P.A., Fontecilla-Camps J.C., Housset D., Malissen B. CDR3 loop flexibility contributes to the degeneracy of TCR recognition. Nature Immunology 2003, 4:241-247.
56. Schwartz R.H. Models of T cell anergy: is there a common molecular mechanism?. Journal of Experimental Medicine 1996, 184:1-8.
57. Shusta E.V., Kieke M.C., Parke E., Kranz D.M., Wittrup K.D. Yeast polypeptide fusion surface display levels predict thermal stability and soluble secretion efficiency. Journal of Molecular Biology 1999, 292:949-956.
58. Sim B.C., Zerva L., Greene M.I., Gascoigne N.R. Control of MHC restriction by TCR Valpha CDR1 and CDR2. Science 1996, 273:963-966.
59. Sloan-Lancaster J., Evavold B.D., Allen P.M. Induction of T-cell anergy by altered T-cell-receptor ligand on live antigen-presenting cells. Nature 1993, 363:156-159.
60. Sykulev Y., Brunmark A., Jackson M., Cohen R.J., Peterson P.A., Eisen H.N. Kinetics and affinity of reactions between an antigen-specific T cell receptor and peptide-MHC complexes. Immunity 1994, 1:15-22.
61. Udaka K., Tsomides T.J., Eisen H.N. A naturally occurring peptide recognized by alloreactive CD8+ cytotoxic T lymphocytes in association with a class I MHC protein. Cell 1992, 69:989-998.
62. Varani L., Bankovich A.J., Liu C.W., Colf L.A., Jones L.L., Kranz D.M., Puglisi J.D., Garcia K.C. Solution mapping of T cell receptor docking footprints on peptide-MHC. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:13080-13085.
63. Weber K.S., Donermeyer D.L., Allen P.M., Kranz D.M. Class II-restricted T cell receptor engineered in vitro for higher affinity retains peptide specificity and function. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:19033-19038.
64. Willcox B.E., Gao G.F., Wyer J.R., Ladbury J.E., Bell J.I., Jakobsen B.K., van der Merwe P.A. TCR binding to peptide-MHC stabilizes a flexible recognition interface. Immunity 1999, 10:357-365.
65. Williams C.B., Engle D.L., Kersh G.J., Michael White J., Allen P.M. A kinetic threshold between negative and positive selection based on the longevity of the T cell receptor-ligand complex. Journal of Experimental Medicine 1999, 189:1531-1544.
66. Xing Y., Hogquist K.A. T-cell tolerance: central and peripheral. Cold Spring Harbor Perspectives in Biology 2012, 1:4.
67. Yin Y., Li Y., Kerzic M.C., Martin R., Mariuzza R.A. Structure of a TCR with high affinity for self-antigen reveals basis for escape from negative selection. EMBO Journal 2011, 30:1137-1148.
68. Yu P., Haymaker C.L., Divekar R.D., Ellis J.S., Hardaway J., Jain R., Tartar D.M., Hoeman C.M., Cascio J.A., Ostermeier A., Zaghouani H. Fetal exposure to high-avidity TCR ligand enhances expansion of peripheral T regulatory cells. Journal of Immunology 2008, 181:73-80.
69. Zehn D., Bevan M.J. T cells with low avidity for a tissue-restricted antigen routinely evade central and peripheral tolerance and cause autoimmunity. Immunity 2006, 25:261-270.
70. Zehn D., Lee S.Y., Bevan M.J. Complete but curtailed T-cell response to very low-affinity antigen. Nature 2009, 458:211-214.
71. Zhao Y., Bennett A.D., Zheng Z., Wang Q.J., Robbins P.F., Yu L.Y., Li Y., Molloy P.E., Dunn S.M., Jakobsen B.K., Rosenberg S.A., Morgan R.A. High-affinity TCRs generated by phage display provide CD4+ T cells with the ability to recognize and kill tumor cell lines. Journal of Immunology 2007, 179:5845-5854.