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J Biol Chem, Vol. 275, Issue 20, 15232-15238, May 19, 2000

Classical and Nonclassical Class I Major Histocompatibility Complex Molecules Exhibit Subtle Conformational Differences That Affect Binding to CD8alpha alpha *

George F. Gaoab, Benjamin E. Willcoxbc, Jessica R. Wyerbc, Jonathan M. Boulterd, Christopher A. O'Callaghance, Katsumi Maenakafg, David I. Stuartdf, E. Yvonne Jonesdfh, P. Anton Van Der Merwei, John I. Bellcd, and Bent K. Jakobsencj

From the a Department of Molecular and Cellular Biology, Howard Hughes Medical Institute, Cambridge, Massachusetts 02138, the c MRC Human Immunology Unit, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford OX3 9DS, United Kingdom, the d Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford OX3 9DS, United Kingdom, the f Division of Structural Biology, Wellcome Trust Centre for Human Genetics, Roosevelt Drive, Oxford OX3 7BN United Kingdom, and the i Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom

The cell surface molecules CD4 and CD8 greatly enhance the sensitivity of T-cell antigen recognition, acting as "co-receptors" by binding to the same major histocompatibility complex (MHC) molecules as the T-cell receptor (TCR). Here we use surface plasmon resonance to study the binding of CD8alpha alpha to class I MHC molecules. CD8alpha alpha bound the classical MHC molecules HLA-A*0201, -A*1101, -B*3501, and -C*0702 with dissociation constants (Kd) of 90-220 µM, a range of affinities distinctly lower than that of TCR/peptide-MHC interaction. We suggest such affinities apply to most CD8alpha alpha /classical class I MHC interactions and may be optimal for T-cell recognition. In contrast, CD8alpha alpha bound both HLA-A*6801 and B*4801 with a significantly lower affinity (>= 1 mM), consistent with the finding that interactions with these alleles are unable to mediate cell-cell adhesion. Interestingly, CD8alpha alpha bound normally to the nonclassical MHC molecule HLA-G (Kd ~150 µM), but only weakly to the natural killer cell receptor ligand HLA-E (Kd >=  1 mM). Site-directed mutagenesis experiments revealed that variation in CD8alpha alpha binding affinity can be explained by amino acid differences within the alpha 3 domain. Taken together with crystallographic studies, these results indicate that subtle conformational changes in the solvent exposed alpha 3 domain loop (residues 223-229) can account for the differential ability of both classical and nonclassical class I MHC molecules to bind CD8.

* This work was supported by the Medical Research Council, United Kingdom and the Nuffield Department of Clinical Medicine, Oxford.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

b These authors contributed equally to this work.

e MRC Clinician Scientist.

g Human Frontiers Science Program Postdoctoral Research Fellow.

h Royal Society University Research Fellow.

j To whom correspondence and reprint requests should be addressed: MRC Human Immunology Unit, Institute of Molecular Medicine, John Radcliffe Hospital, Oxford OX3 9DS, UK. Tel.: 44-1865-222-330; Fax: 44-1865-222-502; E-mail: jakobsen@pinnacle.jr2.ox.ac.uk.

Copyright © 2000 by The American Society for Biochemistry and Molecular Biology, Inc.
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