Strict major histocompatibility complex molecule class-specific binding by co-receptors enforces MHC-restricted aß TCR recognition during T lineage subset commitment

Frontiers in Immunology

Volumn 4, Issue NOV, 2013, Pages

  Li, Xiao Long ^a,b   Teng, Mai Kun ^a   Reinherz, Ellis L ^c   Wang, Jia Huai ^a,b,c  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b PEKING UNIVERSITY   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Co receptor; Lineage commitment; Structure; TCR; Thymocyte development

Indexed keywords

EID: 84890374271     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00383     Document Type: Article

References (59)

1. Reinherz EL, Schlossman SF. The differentiation and function of human T lymphocytes. Cell (1980) 19:821-7. doi: 10.1016/0092-8674(80)90072-0
2. Meuer SC, Schlossman SF, Reinherz EL. Clonal analysis of human cytotoxic T lymphocytes: T4+ and T8+ effector T cells recognize products of different major histocompatibility complex regions. Proc Natl Acad Sci U S A (1982) 79:4395-9. doi:10.1073/pnas.79.14.4395
3. Meuer SC, Fitzgerald KA, Hussey RE, Hodgdon JC, Schlossman SF, Reinherz EL. Clonotypic structures involved in antigen-specific human T cell function. Relationship to the T3 molecular complex. J Exp Med (1983) 157:705-19. doi:10.1084/jem.157.2.705
4. Reinherz EL, Meuer SC, Schlossman SF. The delineation of antigen receptors on human T lymphocytes. Immunol Today (1983) 4:5-8. doi:10.1016/0167-5699(83)90094-4
5. Gao GF, Tormo J, Gerth UC, Wyer JR, McMichael AJ, Stuart DI, et al. Crystal structure of the complex between human CD8alpha(alpha) and HLA-A2. Nature (1997) 387:630-4. doi:10.1038/42523
6. Kern P, Hussey RE, Spoerl R, Reinherz EL, Chang HC. Expression, purification, and functional analysis of murine ectodomain fragments of CD8alphaalpha and CD8alphabeta dimers. J Biol Chem (1999) 274:27237-43. doi:10.1074/jbc.274.38.27237
7. Wang J-H, Meijers R, Xiong Y, Liu J-H, Sakihama T, Zhang R, et al. Crystal structure of the human CD4 N-terminal two domain fragment complexed to a class II MHC molecule. Proc Natl Acad Sci U S A (2001) 98:10799-804. doi:10.1073/pnas.191124098
8. Chang HC, Tan K, Ouyang J, Parisini E, Liu JH, Le Y, et al. Structural and mutational analyses of a CD8alphabeta heterodimer and comparison with the CD8alphaalpha homodimer. Immunity (2005) 23:661-71. doi:10.1016/j.immuni.2005.11.002
9. Wang R, Natarajan K, Margulies DH. Structural basis of the CD8 alpha beta/MHC class I interaction: focused recognition orients CD8 beta to a T cell proximal position. J Immunol (2009) 183:2554-64. doi:10.4049/jimmunol.0901276
10. Yin Y, Wang XX, Mariuzza RA. Crystal structure of a complete ternary complex of T-cell receptor, peptide-MHC, and CD4. Proc Natl Acad Sci U S A (2012) 109:5405-10. doi:10.1073/pnas.1118801109
11. Wang JH, Reinherz EL. The structural basis of αβ T lineage immune recognition: TCR docking topologies, mechanotransduction and co-receptor function. Immunol Rev (2012) 250:102-19. doi:10.1111/j.1600-065X.2012.01161.x
12. Li Y, Yin Y, Mariuzza RA. Structural and biophysical insights into the role of CD4 and CD8 in T cell activation. Front Immunol (2013) 4:206. doi:10.3389/fimmu.2013.00206
13. Moody AM, Chui D, Reche PA, Priatel JJ, Marth JD, Reinherz EL. Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell (2001) 107:501-12. doi:10.1016/S0092-8674(01)00577-3
14. Moebius U, Kober G, Griscelli AL, Hercend T, Meuer SC. Expression of different CD8 isoforms on distinct human lymphocyte subpopulations. Eur J Immunol (1991) 21:1793-800. doi:10.1002/eji.1830210803
15. Poussier P, Julius M. Thymus independent T cell development and selection in the intestinal epithelium. Annu Rev Immunol (1994) 12:521-53. doi:10.1146/annurev.iy.12.040194.002513
16. Kim PW, Sun ZY, Blacklow SC, Wagner G, Eck MJ. A zinc clasp structure tethers Lck to T cell coreceptors CD4 and CD8. Science (2003) 301:1725-8. doi:10.1126/science.1085643
17. Weiss A. T cell antigen receptor signal transduction: a tale of tails and cytoplasmic protein-tyrosine kinases. Cell (1993) 73:209-12. doi:10.1016/0092-8674(93)90221-B
18. Xiong Y, Kern P, Chang H, Reinherz E. T cell receptor binding to a pMHCII ligand Is kinetically distinct from and Independent of CD4. J Biol Chem (2001) 276:5659-67. doi:10.1074/jbc.M009580200
19. Gao GF, Rao Z, Bell JI. Molecular coordination of alphabeta T-cell receptors and coreceptors CD8 and CD4 in their recognition of peptide-MHC ligands. Trends Immunol (2002) 23:408-13. doi:10.1016/S1471-4906(02)02282-2
20. Stone JD, Chervin AS, Kranz DM. T-cell receptor binding affinities and kinetics: impact on T-cell activity and specificity. Immunology (2009) 126:165-76. doi:10.1111/j.1365-2567.2008.03015.x
21. Jiang N, Huang J, Edwards LJ, Liu B, Zhang Y, Beal CD, et al. Two-stage cooperative T cell receptor-peptide major histocompatibility complex-CD8 trimolecular interactions amplify antigen discrimination. Immunity (2011) 34:13-23. doi:10.1016/j.immuni.2010.12.017
22. Kappler JW, Roehm N, Marrack P. T cell tolerance by clonal elimination in the thymus. Cell (1987) 49:273-80. doi:10.1016/0092-8674(87)90568-X
23. Kisielow P, Blüthmann H, Staerz UD, Steinmetz M, von Boehmer H. Tolerance in T-cell-receptor transgenic mice involves deletion of nonmature CD4+8+ thymocytes. Nature (1988) 333:742-6. doi:10.1038/333742a0
24. Ghendler Y, Teng M-K, Liu JH, Witte T, Liu J, Kim KS, et al. Differential thymic selection outcomes stimulated by focal structural alteration in peptide/major histocompatibility complex ligands. Proc Natl Acad Sci U S A (1998) 95:10061-6. doi:10.1073/pnas.95.17.10061
25. Mariathasan S, Jones RG, Ohashi PS. Signals involved in thymocyte positive and negative selection. Semin Immunol (1999) 11:263-72. doi:10.1006/smim.1999.0182
26. Love PE, Lee J, Shores EW. Critical relationship between TCR signaling potential and TCR affinity during thymocyte selection. J Immunol (2000) 165:3080-7.
27. Haks MC, Pepin E, van den Brakel JHN, Smeele SAA, Belkowski SM, Kessels HW, et al. Contribution of the T cell receptor-associated CD3γ-ITAM to thymocyte selection. J Exp Med (2002) 196:1-13. doi:10.1084/jem.20020268
28. von Boehmer H, Aifantis I, Gounari F, Azogui O, Haughn L, Apostolou I, et al. Thymic selection revisited: how essential is it? Immunol Rev (2003) 191:62-78. doi:10.1034/j.1600-065X.2003.00010.x
29. Starr TK, Jameson SC, Hogquist KA. Positive and negative selection of T cells. Annu Rev Immunol (2003) 21:139-76. doi:10.1146/annurev.immunol.21.120601.141107
30. Juang J, Ebert PJ, Feng D, Garcia KC, Krogsgaard M, Davis MM. Peptide-MHC heterodimers show that thymic positive selection requires a more restricted set of self-peptides than negative selection. J Exp Med (2010) 207(6):1223-34. doi:10.1084/jem.20092170
31. Gallegos AM, Bevan MJ. Central tolerance: good but imperfect. Immunol Rev (2006) 209:290-6. doi:10.1111/j.0105-2896.2006.00348.x
32. Ashton-Rickardt PG. Studying T-cell repertoire selection using fetal thymus organ culture. Methods Mol Biol (2007) 380:171-84. doi:10.1007/978-1-59745-395-0_10
33. Griesemer AD, Sorenson EC, Hardy MA. The role of the thymus in tolerance. Transplantation (2010) 90:465-74. doi:10.1097/TP.0b013e3181e7e54f
34. Kelly K, Pilarski L, Shortman K, Scollay R. CD4+CD8+ cells are rare among in vitro activated mouse or human T lymphocytes. Cell Immunol (1988) 117:414-24. doi:10.1016/0008-8749(88)90130-X
35. Tikhonova AN, Van Laethem F, Hanada K, Lu J, Pobezinsky LA, Hong C, et al. αβ T cell receptors that do not undergo major histocompatibility complex-specific thymic selection possess antibody-like recognition specificities. Immunity (2012) 36:79-91. doi:10.1016/j.immuni.2011.11.013
36. Van Laethem F, Tikhonova AN, Pobezinsky LA, Tai X, Kimura MY, Le Saout C, et al. Lck availability during thymic selection determines the recognition specificity of the T cell repertoire. Cell (2013) 154:1326-41. doi:10.1016/j.cell.2013.08.009
37. Classon BJ, Brown MH, Garnett D, Somoza C, Barclay AN, Willis AC, et al. The hinge region of the CD8 alpha chain: structure, antigenicity, and utility in expression of immunoglobulin superfamily domains. Int Immunol (1992) 4:215-25. doi:10.1093/intimm/4.2.215
38. Rudd PM, Wormald MR, Stanfield RL, Huang M, Mattsson N, Speir JA, et al. Roles for glycosylation of cell surface receptors involved in cellular immune recognition. J Mol Biol (1999) 293:351-66. doi:10.1006/jmbi.1999.3104
39. Moody AM, North SJ, Reinhold B, Van Dyken SJ, Rogers ME, Panico M, et al. Sialic acid capping of CD8beta core 1-O-glycans controls thymocyte-major histocompatibility complex class I interaction. J Biol Chem (2003) 278:7240-6. doi:10.1074/jbc.M210468200
40. Singer A, Adoro S, Park JH. Lineage fate and intense debate: myths, models and mechanisms of CD4-versus CD8-lineage choice. Nat Rev Immunol (2008) 8:788-801. doi:10.1038/nri2416
41. Itano A, Robey E. Highly efficient selection of CD4 and CD8 lineage thymocytes supports an instructive model of lineage commitment. Immunity (2000) 12:383-9. doi:10.1016/S1074-7613(00)80190-9
42. Wiest DL, Yuan L, Jefferson J, Benveniste P, Tsokos M, Klausner RD, et al. Regulation of T cell receptor expression in immature CD4+CD8+ thymocytes by p56lck tyrosine kinase: basis for differential signaling by CD4 and CD8 in immature thymocytes expressing both coreceptor molecules. J Exp Med (1993) 178:1701-12. doi:10.1084/jem.178.5.1701
43. Itano A, Salmon P, Kioussis D, Tolaini M, Corbella P, Robey E. The cytoplasmic domain of CD4 promotes the development of CD4 lineage T cells. J Exp Med (1996) 83:731-41. doi:10.1084/jem.183.3.731
44. Holst J, Wang H, Eder KD, Workman CJ, Boyd KL, Baquet Z, et al. Scalable signaling mediated by T cell antigen receptor-CD3 ITAMs ensures effective negative selection and prevents autoimmunity. Nat Immunol (2008) 9:658-66. doi:10.1038/ni.1611
45. Singer A. New perspectives on a developmental dilemma: the kinetic signaling model and the importance of signal duration for the CD4/CD8 lineage decision. Curr Opin Immunol (2002) 14:207-15. doi:10.1016/S0952-7915(02)00323-0
46. McCaughtry TM, Etzensperger R, Alag A, Tai X, Kurtulus S, Park JH, et al. Conditional deletion of cytokine receptor chains reveals that IL-7 and IL-15 specify CD8 cytotoxic lineage fate in the thymus. J Exp Med (2012) 209:2263-76. doi:10.1084/jem.20121505
47. Adoro S, Park JH, Singer A. Coreceptor gene "imprinting:" a genetic solution to a developmental dilemma in T cells. Cell Cycle (2012) 11:833-4. doi:10.4161/cc.11.5.19596
48. Wang XX, Li Y, Yin Y, Mo M, Wang Q, Gao W, et al. Affinity maturation of human CD4 by yeast surface display and crystal structure of a CD4-HLA-DR1 complex. Proc Natl Acad Sci U S A (2011) 108:15960-5. doi:10.1073/pnas.1109438108
49. Mosyak L, Zaller DM, Wiley DC. The structure of HLA-DM, the peptide exchange catalyst that loads antigen onto class II MHC molecules during antigen presentation. Immunity (1998) 9:377-83. doi:10.1016/S1074-7613(00)80620-2
50. Kern PS, Teng M-K, Smolyar A, Liu J-H, Liu J, Hussey RE, et al. Structural basis of CD8 co-receptor function revealed by crystallographic analysis of a murine CD8αα ectodomain fragment in complex with H-2Kb. Immunity (1998) 9:519-30. doi:10.1016/S1074-7613(00)80635-4
51. Liu Y, Xiong Y, Naidenko OV, Liu JH, Zhang R, Joachimiak A, et al. The crystal structure of a TL/CD8alphaalpha complex at 2.1 A resolution: implications for modulation of T cell activation and memory. Immunity (2003) 18:205-15. doi:10.1016/S1074-7613(03)00027-X
52. Salter RD, Benjamin RJ, Wesley PK, Buxton SE, Garrett TP, Clayberger C, et al. A binding site for the T-cell co-receptor CD8 on the alpha 3 domain of HLA-A2. Nature (1990) 45:41-6. doi:10.1038/345041a0
53. Durairaj M, Sharma R, Varghese JC, Kane KP. Requirement for Q226, but not multiple charged residues, in the class I MHC CD loop/D strand for TCR-activated CD8 accessory function. Eur J Immunol (2003) 33:676-84. doi:10.1002/eji.200323499
54. Cole DK, Pumphrey NJ, Boulter JM, Sami M, Bell JI, Gostick E, et al. Human TCR-binding affinity is governed by MHC class restriction. J Immunol (2007) 178:5727-34.
55. van der Merwe PA, Davis SJ. Molecular interactions mediating T cell antigen recognition. Annu Rev Immunol (2003) 21:659-84. doi:10.1146/annurev.immunol.21.120601.141036
56. Kim ST, Takeuchi K, Sun Z-YJ, Touma M, Castro CE, Fahmy A, et al. The αβ T cell receptor is an anisotropic mechanosensor. J Biol Chem (2009) 284:31028-37. doi:10.1074/jbc.M109.052712
57. Zhu C, Jiang N, Huang J, Zarnitsyna VI, Evavold BD. Insights from in situ analysis of TCR-pMHC recognition: response of an interaction network. Immunol Rev (2013) 251:49-64. doi:10.1111/imr.12016
58. Sinclair C, Bains I, Yates AJ, Seddon B. Asymmetric thymocyte death underlies the CD4:CD8 T-cell ratio in the adaptive immune system. Proc Natl Acad Sci U S A (2013) 110:E2905-14. doi:10.1073/pnas.1304859110
59. Teh HS, Kisielow P, Scott B, Kishi H, Uematsu Y, Blüthmann H, et al. Thymic major histocompatibility complex antigens and the alpha beta T-cell receptor determine the CD4/CD8 phenotype of T cells. Nature (1988) 335:229-33. doi:10.1038/335229a0