Förster Resonance Energy Transfer to Study TCR-pMHC Interactions in the Immunological Synapse. 2017

Gerhard J Schütz, and Johannes B Huppa
Institute of Applied Physics, TU Wien, Getreidemarkt 9, 1060, Vienna, Austria. schuetz@iap.tuwien.ac.at.

T-cell antigen recognition is remarkably efficient: when scanning the surface of antigen-presenting cells (APCs), T-cells can detect the presence of just a few single antigenic peptide/MHCs (pMHCs), which are often vastly outnumbered by structurally similar non-stimulatory endogenous pMHCs (Irvine et al., Nature 419(6909):845-849, 2002; Purbhoo et al., Nat Immunol 5(5):524-530, 2004; Huang et al., Immunity 39(5):846-857, 2013). How T-cells achieve this is still enigmatic, in particular in view of the rather moderate affinity that TCRs typically exert for antigenic pMHCs, at least when measured in vitro (Davis et al., Ann Rev Immunol 16:523-544, 1998). To shed light on this in a comprehensive manner, we have developed a microscopy-based assay, which allows us to quantitate TCR-pMHC interactions in situ, i.e., within the special confines of the nascent immunological synapse of a T-cell contacting a planar-supported lipid bilayer functionalized with the costimulatory molecule B7-1, the adhesion molecule ICAM-1, and pMHCs (Huppa et al., Nature 463(7283):963-967, 2010) (Fig. 1). Binding measurements are based on Förster resonance energy transfer (FRET) between site-specifically labeled pMHCs and TCRs, which are decorated with recombinant site-specifically labeled single-chain antibody fragments (scFV) derived from the TCRβ-reactive H57-597 antibody (Huppa et al., Nature 463(7283):963-967, 2010). FRET, a quantum-mechanical phenomenon, involves the non-radiative coupling of dipole moments of two adjacent fluorophores, a donor molecule and an acceptor molecule. FRET efficiency is inversely proportional to the sixth power of the inter-dye distance. Hence, it can be employed as a molecular ruler (Stryer and Haugland, Proc Natl Acad Sci, USA 58(2):719-726, 1967) or, as is the case here, to score for interactions of appropriately labeled molecules. To facilitate both quantitative and single-molecule readout, it is important to conjugate donor and acceptor dyes in a site-specific manner.While SLBs mimic some but certainly not all properties of a plasma membrane of a living cell, their use features a number of operational advantages: SLBs can be prepared in a fluid state, thereby facilitating the spatial rearrangements that accompany the formation of an immunological synapse (Grakoui et al., Science 285(5425):221-227, 1999). The imaging of a three-dimensional binding process is reduced to two dimensions, which saves time and fluorophore-emitted photons and allows for fast measurements. Furthermore, images can be acquired in noise-attenuated total internal reflection (TIR) mode, so far a necessity for single-molecule detection within the immunological synapse. Importantly, the stimulatory potency of pMHCs is very well preserved compared to cell surface-embedded pMHCs. Hence, while in principle artificial, SLBs are still a good approximation of the physiologic scenario a T-cell encounters when approaching an APC. Vice versa, the reconstitutive approach offers unique opportunities to interrogate the influence of accessory molecules on T-cell antigen recognition in a highly quantitative manner.In this chapter we will provide recommendations for the production of proteins used for SLB decoration as well as hands-on protocols for the production of SLBs. We will describe in detail how to perform and analyze FRET-based experiments to determine synaptic binding constants. In the "Notes" section, we will provide some information regarding the microscope setup as well as the mathematical and biophysical foundation underlying data analysis.

UI MeSH Term Description Entries
D010455 Peptides Members of the class of compounds composed of AMINO ACIDS joined together by peptide bonds between adjacent amino acids into linear, branched or cyclical structures. OLIGOPEPTIDES are composed of approximately 2-12 amino acids. Polypeptides are composed of approximately 13 or more amino acids. PROTEINS are considered to be larger versions of peptides that can form into complex structures such as ENZYMES and RECEPTORS. Peptide,Polypeptide,Polypeptides
D011948 Receptors, Antigen, T-Cell Molecules on the surface of T-lymphocytes that recognize and combine with antigens. The receptors are non-covalently associated with a complex of several polypeptides collectively called CD3 antigens (CD3 COMPLEX). Recognition of foreign antigen and the major histocompatibility complex is accomplished by a single heterodimeric antigen-receptor structure, composed of either alpha-beta (RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA) or gamma-delta (RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA) chains. Antigen Receptors, T-Cell,T-Cell Receptors,Receptors, T-Cell Antigen,T-Cell Antigen Receptor,T-Cell Receptor,Antigen Receptor, T-Cell,Antigen Receptors, T Cell,Receptor, T-Cell,Receptor, T-Cell Antigen,Receptors, T Cell Antigen,Receptors, T-Cell,T Cell Antigen Receptor,T Cell Receptor,T Cell Receptors,T-Cell Antigen Receptors
D006649 Histocompatibility Antigens A group of antigens that includes both the major and minor histocompatibility antigens. The former are genetically determined by the major histocompatibility complex. They determine tissue type for transplantation and cause allograft rejections. The latter are systems of allelic alloantigens that can cause weak transplant rejection. Transplantation Antigens,Antigens, Transplantation,Histocompatibility Antigen,LD Antigens,SD Antigens,Antigen, Histocompatibility,Antigens, Histocompatibility,Antigens, LD,Antigens, SD
D006801 Humans Members of the species Homo sapiens. Homo sapiens,Man (Taxonomy),Human,Man, Modern,Modern Man
D000818 Animals Unicellular or multicellular, heterotrophic organisms, that have sensation and the power of voluntary movement. Under the older five kingdom paradigm, Animalia was one of the kingdoms. Under the modern three domain model, Animalia represents one of the many groups in the domain EUKARYOTA. Animal,Metazoa,Animalia
D013601 T-Lymphocytes Lymphocytes responsible for cell-mediated immunity. Two types have been identified - cytotoxic (T-LYMPHOCYTES, CYTOTOXIC) and helper T-lymphocytes (T-LYMPHOCYTES, HELPER-INDUCER). They are formed when lymphocytes circulate through the THYMUS GLAND and differentiate to thymocytes. When exposed to an antigen, they divide rapidly and produce large numbers of new T cells sensitized to that antigen. T Cell,T Lymphocyte,T-Cells,Thymus-Dependent Lymphocytes,Cell, T,Cells, T,Lymphocyte, T,Lymphocyte, Thymus-Dependent,Lymphocytes, T,Lymphocytes, Thymus-Dependent,T Cells,T Lymphocytes,T-Cell,T-Lymphocyte,Thymus Dependent Lymphocytes,Thymus-Dependent Lymphocyte
D054992 Immunological Synapses The interfaces between T-CELLS and ANTIGEN-PRESENTING CELLS. Supramolecular organization of proteins takes place at these synapses involving various types of immune cells. Immunological synapses can have several functions including LYMPHOCYTE ACTIVATION; enhancing, balancing, or terminating signaling; or directing cytokine secretion. Synapses, Immunological,Immunological Synapse,Synapse, Immunological
D031541 Fluorescence Resonance Energy Transfer A type of FLUORESCENCE SPECTROSCOPY using two FLUORESCENT DYES with overlapping emission and absorption spectra, which is used to indicate proximity of labeled molecules. This technique is useful for studying interactions of molecules and PROTEIN FOLDING. Forster Resonance Energy Transfer

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