Remarkably low affinity of CD4/peptide-major histocompatibility complex class II protein interactions

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 20, 2016, Pages 5682-5687

  Jönsson, Peter ^a,b   Southcombe, Jennifer H ^c,d,e   Mafalda Santos, Ana ^c,d   Huo, Jiandong ^c,d   Fernandes, Ricardo A ^c,d   McColl, James ^a   Lever, Melissa ^f   Evans, Edward J ^c,d   Hudson, Alexander ^c,d   Chang, Veronica T ^c,d   Hanke, Tomáš ^c,d   Godkin, Andrew ^g   Dunne, Paul D ^a   Horrocks, Mathew H ^a   Palayret, Matthieu ^a   Screaton, Gavin R ^c   Petersen, Jan ^h   Rossjohn, Jamie ^g,h   Fugger, Lars ^c,d,e   Dushek, Omer ^f   Xu, Xiao Ning ^c   Davis, Simon J ^c,d   Klenerman, David ^a   more..

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f UNIVERSITY OF OXFORD   (United Kingdom)

^g CARDIFF UNIVERSITY   (United Kingdom)

^h MONASH UNIVERSITY   (Australia)

Author keywords

Adhesion; Binding equilibrium and kinetics; Protein interactions; T cell activation; TCR phosphorylation

Indexed keywords

CELL ADHESION MOLECULE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDE MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROTEIN KINASE LCK; SOLUBLE CD4 ANTIGEN; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG; CD4 ANTIGEN; HLA A24 ANTIGEN; HLA DRB1 ANTIGEN; HLA-A*24:02 ANTIGEN; HLA-DRB1*15:01 ANTIGEN; MALTOSE BINDING PROTEIN; PROTEIN BINDING;

ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIPID BILAYER; MAJOR HISTOCOMPATIBILITY COMPLEX; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RECEPTOR AFFINITY; SURFACE PLASMON RESONANCE; T LYMPHOCYTE ACTIVATION; CHEMISTRY; HEK293 CELL LINE; METABOLISM; MOLECULAR MODEL; PHOSPHORYLATION; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN STABILITY;

ANTIGENS, CD4; BINDING SITES; HEK293 CELLS; HLA-A24 ANTIGEN; HLA-DRB1 CHAINS; HUMANS; MALTOSE-BINDING PROTEINS; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STABILITY; SURFACE PLASMON RESONANCE;

EID: 84969786276     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1513918113     Document Type: Article

References (47)

1. Singer A, Adoro S, Park J-H (2008) Lineage fate and intense debate: Myths, models and mechanisms of CD4- versus CD8-lineage choice. Nat Rev Immunol 8(10):788-801.
2. Norment AM, Salter RD, Parham P, Engelhard VH, Littman DR (1988) Cell-cell adhesion mediated by CD8 and MHC class I molecules. Nature 336(6194):79-81.
3. Doyle C, Strominger JL (1987) Interaction between CD4 and class II MHC molecules mediates cell adhesion. Nature 330(6145):256-259.
4. Clayton LK, Sieh M, Pious DA, Reinherz EL (1989) Identification of human CD4 residues affecting class II MHC versus HIV-1 gp120 binding. Nature 339(6225):548-551.
5. Wang XX, et al. (2011) Affinity maturation of human CD4 by yeast surface display and crystal structure of a CD4-HLA-DR1 complex. Proc Natl Acad Sci USA 108(38):15960-15965.
6. Wang JH, et al. (2001) Crystal structure of the human CD4 N-terminal two-domain fragment complexed to a class II MHC molecule. Proc Natl Acad Sci USA 98(19):10799-10804.
7. Irvine DJ, Purbhoo MA, Krogsgaard M, Davis MM (2002) Direct observation of ligand recognition by T cells. Nature 419(6909):845-849.
8. Artyomov MN, Lis M, Devadas S, Davis MM, Chakraborty AK (2010) CD4 and CD8 binding to MHC molecules primarily acts to enhance Lck delivery. Proc Natl Acad Sci USA 107(39):16916-16921.
9. Stepanek O, et al. (2014) Coreceptor scanning by the T cell receptor provides a mechanism for T cell tolerance. Cell 159(2):333-345.
10. van der Merwe PA, Davis SJ (2003) Molecular interactions mediating T cell antigen recognition. Annu Rev Immunol 21:659-684.
11. Davis SJ, et al. (2003) The nature of molecular recognition by T cells. Nat Immunol 4(3):217-224.
12. Huang J, et al. (2010) The kinetics of two-dimensional TCR and pMHC interactions determine T-cell responsiveness. Nature 464(7290):932-936.
13. Huppa JB, et al. (2010) TCR-peptide-MHC interactions in situ show accelerated kinetics and increased affinity. Nature 463(7283):963-967.
14. Wu Y, Vendome J, Shapiro L, Ben-Shaul A, Honig B (2011) Transforming binding affinities from three dimensions to two with application to cadherin clustering. Nature 475(7357):510-513.
15. Dustin ML, et al. (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(49):30889-30898.
16. Zhu D-M, Dustin ML, Cairo CW, Golan DE (2007) Analysis of two-dimensional dissociation constant of laterally mobile cell adhesion molecules. Biophys J 92(3):1022-1034.
17. Dustin ML (2009) Supported bilayers at the vanguard of immune cell activation studies. J Struct Biol 168(1):152-160.
18. Davis SJ, et al. (1992) Antibody and HIV-1 gp120 recognition of CD4 undermines the concept of mimicry between antibodies and receptors. Nature 358(6381):76-79.
19. Yin Y, Wang XX, Mariuzza RA (2012) Crystal structure of a complete ternary complex of T-cell receptor, peptide-MHC, and CD4. Proc Natl Acad Sci USA 109(14):5405-5410.
20. König R, Huang LY, Germain RN (1992) MHC class II interaction with CD4 mediated by a region analogous to the MHC class I binding site for CD8. Nature 356(6372):796-798.
21. König R, Shen X, Germain RN (1995) Involvement of both major histocompatibility complex class II alpha and beta chains in CD4 function indicates a role for ordered oligomerization in T cell activation. J Exp Med 182(3):779-787.
22. James JR, Vale RD (2012) Biophysical mechanism of T-cell receptor triggering in a reconstituted system. Nature 487(7405):64-69.
23. Evans EJ, et al. (2006) Crystal structure and binding properties of the CD2 and CD244 (2B4)-binding protein, CD48. J Biol Chem 281(39):29309-29320.
24. Grakoui A, et al. (1999) The immunological synapse: A molecular machine controlling T cell activation. Science 285(5425):221-227.
25. Rossjohn J, et al. (2015) T cell antigen receptor recognition of antigen-presenting molecules. Annu Rev Immunol 33(1):169-200.
26. Dushek O, van der Merwe PA (2014) An induced rebinding model of antigen discrimination. Trends Immunol 35(4):153-158.
27. Xu H, Littman DR (1993) A kinase-independent function of Lck in potentiating antigen-specific T cell activation. Cell 74(4):633-643.
28. Hui E, Vale RD (2014) In vitro membrane reconstitution of the T-cell receptor proximal signaling network. Nat Struct Mol Biol 21(2):133-142.
29. Tolentino TP, et al. (2008) Measuring diffusion and binding kinetics by contact area FRAP. Biophys J 95(2):920-930.
30. Hong J, et al. (2015) Force-regulated in situ TCR-peptide-bound MHC class II kinetics determine functions of CD4+ T cells. J Immunol 195(8):3557-3564.
31. Li Q-J, et al. (2004) CD4 enhances T cell sensitivity to antigen by coordinating Lck accumulation at the immunological synapse. Nat Immunol 5(8):791-799.
32. Vidal K, Daniel C, Hill M, Littman DR, Allen PM (1999) Differential requirements for CD4 in TCR-ligand interactions. J Immunol 163(9):4811-4818.
33. Huse M, et al. (2007) Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist. Immunity 27(1):76-88.
34. Hu J, Lipowsky R, Weikl TR (2013) Binding constants of membrane-anchored receptors and ligands depend strongly on the nanoscale roughness of membranes. Proc Natl Acad Sci USA 110(38):15283-15288.
35. Harkiolaki M, et al. (2009) T cell-mediated autoimmune disease due to low-affinity crossreactivity to common microbial peptides. Immunity 30(3):348-357.
36. Scally SW, et al. (2013) A molecular basis for the association of the HLA-DRB1 locus, citrullination, and rheumatoid arthritis. J Exp Med 210(12):2569-2582.
37. Dushek O, et al. (2008) Effects of intracellular calcium and actin cytoskeleton on TCR mobility measured by fluorescence recovery. PLoS One 3(12):e3913.
38. Wu J, et al. (2008) A coupled diffusion-kinetics model for analysis of contact-area FRAP experiment. Biophys J 95(2):910-919.
39. Sprague BL, Pego RL, Stavreva DA, McNally JG (2004) Analysis of binding reactions by fluorescence recovery after photobleaching. Biophys J 86(6):3473-3495.
40. Altan-Bonnet G, Germain RN (2005) Modeling T cell antigen discrimination based on feedback control of digital ERK responses. PLoS Biol 3(11):e356.
41. Kumar GS (2014) Orban's Oral Histology & Embryology (Elsevier Health Sciences, New Delhi), 13th Ed.
42. Maroun CR, Julius M (1994) Distinct roles for CD4 and CD8 as co-receptors in T cell receptor signalling. Eur J Immunol 24(4):959-966.
43. Nika K, et al. (2010) Constitutively active Lck kinase in T cells drives antigen receptor signal transduction. Immunity 32(6):766-777.
44. Ballek O, Valečka J, Manning J, Filipp D (2015) The pool of preactivated Lck in the initiation of T-cell signaling: A critical re-evaluation of the Lck standby model. Immunol Cell Biol 93(4):384-395.
45. Davis SJ, et al. (1990) High level expression in Chinese hamster ovary cells of soluble forms of CD4 T lymphocyte glycoprotein including glycosylation variants. J Biol Chem 265(18):10410-10418.
46. Horrocks MH, et al. (2013) Single-molecule measurements of transient biomolecular complexes through microfluidic dilution. Anal Chem 85(14):6855-6859.
47. Johansson B, Höök F, Klenerman D, Jönsson P (2014) Label-free measurements of the diffusivity of molecules in lipid membranes. Chemphyschem 15(3):486-491.