390
Interactions of TCRs with MHC-peptide complexes: a
quantitative basis for mechanistic models
David H Margulies
The activation of T lymphocytes is initiated by the binding
of MHC-peptide complexes on antigen-presenting cells to
MHC-restricted, peptide specific TCRs. Significant progress
has recently been made in understanding the structure of the
TCR and in the direct quantitative examination of the primary
binding interactions between MHC-peptide complexes and
the TCR. Attempts to develop quantitative models for the
differential activation of T cells by MHC-peptide ligands
that differ subtly in their structure have largely been based
on either the affinity of the MHC-peptide complexe s for
the TCR in question or on the dissociation kinetics of the
MHC-peptide complex from the T cell.
Addresses
Molecular Biology Section, Laboratoryof Immunology, National
Institutes of Allergy and Infectious Diseases, National Institutes of
Health, Bethesda, MD 90892-1892, USA; e-mail: dhm@helix.nih.gov
Current Opinion in Immunology 1997, 9:390-395
http:llbiomednet.com/elecref10952791500900390
© Current Biology Ltd ISSN 0952-7915
Abbreviations
APC
C
CDR
ITAM
MHC
MHC-I
MHC-II
sc
SPR
TCR
V
antigen-presenting cell
constant domain
complementarity determining region
immunoreceptor tyrosine based activation motif
major histocompatibilitycomplex
MHC-encoded class I protein
MHC-encoded class II protein
single chain
surface plasmon resonance
T cell receptor
variable domain
Introduction
T lymphocytes exert managerial control over the immune
response. Like good administrators, they recognize the
need for action, recruit aid from others, and perform some
of the work themselves. They must sense when to begin
their efforts, when to freeze production, and when to
divert activity from one line to another. To initiate the
immune response, ~13 receptors on the surface of the T cell
must bind molecular complexes containing MHC-encoded
class I (MHC-I) or class II (MHC-II) glycoproteins.
These MHC molecules are tightly complexed with
antigenic or self peptide fragments derived from the
degradation of proteins either synthesized in the same
cell (for MHC-I) or ingested through the endocytic path-
way (for MHC-II). The TCR-MHC-peptide recognition
event forms the basis of the phenomenon known as
antigen-specific MHC-restricted T cell recognition. This
process controls the rejection of genetically disparate graft
tissues (histoincompatibility), the identification of tissues
infected by viruses or intracellular parasitic organisms
(infected-self recognition), the immune responses to
tumors produced in the host animal (tumor rejection), and
it falls under the general heading of self versus nonself
discrimination, a function for which the entire immune
system clearly evolved. Another result of the engagement
of MHC-peptide complexes by the TCR is that which
occurs in the thymus where the developmental fate of
new clones bearing TCRs is determined as a result of
both positive and negative selective events (for reviews
see [1,2]).
In the past few years, our understanding of the molecular
events involved in initiating the immune response has
benefited from the determination, at high resolution,
of the structures of MHC molecules complexed with
peptides [3], TCR fragments [4,5°°,6°], and most re-
cently of TCR-MHC-peptide complexes [7°',8"°,9]. In
addition, studies of the binding of the TCR to purified
MHC-peptide complexes have provided indications of
some of the parameters that govern the initial binding
events [10-13,14°,15°,16°°]. An added complexity in the
nature of the TCR signals delivered by MHC-peptide
complexes arises from the identification of variant peptides
that signal differently as compared with antigenic peptides
[17-19]. The antigenic peptide is commonly referred
to as an 'agonisr peptide in that it contributes to a
stimulatory form of the MHC-peptide complex. Using
terminology borrowed from pharmacologists, peptides that
exert negative signals capable of countering the agonist
are known as 'antagonists'. Similarly, those peptides that
contribute to an intermediate signal are 'weak agonists'.
These must be distinguished from 'partial agonists' that
elicit some, but not all, downstream signals or functions
[20]. Binding measurements have been undertaken to
understand the behavior of the antagonist peptide-MHC
complexes and their effects on mature peripheral T cells
[21°°], and to understand other variant MHC-peptide
complexes that have differential effects on positive and
negative selection in the thymic development of T cells
[22"]. Interactions of MHC-peptide complexes with the
TCR in the presence of co-receptors have also been
evaluated [23°,24°°].
In parallel with the efforts to develop model systems for
measuring the initial TCR binding events, several groups
have examined the immunological and biochemical conse-
quences of signaling T cells via different MHC-peptide
stimuli [17-19]. The intriguing phenomenon by which
MHC-peptide complexes containing synthetic variant
peptides can cause functional antagonism, partial agonism,