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PMID: 16013435 Published · ppublish English Journal Article

The immune function of MHC class II molecules mutated in the putative superdimer interface.

Molecular and cellular biochemistry ·Vol. 273 ·No. 1-2 ·2005-05-00 ·Pages 1-9

Hayball JD, Lake RA

Abstract

Analysis of the crystal structure of human class II (HLA-DR1) molecules suggests that the alphabeta heterodimer may be further ordered as a dimer of heterodimers (superdimer), leading to the hypothesis that T cell receptor dimerisation is a mechanism for initiating signaling events preceding T cell activation. The interface between pairs of molecules is stabilised by both salt bridges, polar and hydrophobic interactions. The residues that form the superdimer interface occur in three areas distinct from the antigen-binding groove. They can be defined as follows: region 1, beta-beta contacts in the helix of the beta1 domain; region 2, alpha-alpha contacts near the alpha 1/alpha2 domain junction and region 3; alpha-beta contacts in the alpha2/beta2 domains adjacent to the plasma membrane. To determine whether salt bridges and polar interactions formed within these regions are involved in the immune function of the murine MHC class II molecule, I-A(b), appropriate residues in both the alpha and beta chain were identified and mutated to uncharged alanine. Cell lines transfected with different combinations of mutated alpha and beta chains were generated and tested for MHC class II expression, peptide binding capabilities, and ability to present antigenic peptide to an OVA-specific T cell hybridoma. With the exception of two residues in region 2, the substitutions tested did not modulate MHC class II expression, or peptide binding function. When tested for ability to present peptide to an antigen-specific T cell hybridoma, with the exception of mutations in region 2, the substitutions did not appear to abrogate the ability of I-A(b) to stimulate the T cells. These results suggest that mutation of residues in region 2 of the putative superdimer interface have a gross effect on the ability of I-A(b) to be expressed on the cell surface. However, abrogation of salt bridges in region 1 and 3 do not influence I-A(b) cell surface expression, peptide binding or ability to stimulate antigen-specific T cells.

MeSH Terms
Animals Antigen Presentation/immunology Antigen-Presenting Cells/immunology,metabolism Cells, Cultured Histocompatibility Antigens Class II/genetics,immunology Humans Hybridomas Jurkat Cells Lymphocyte Activation Mice Mice, Inbred C57BL Mutagenesis, Site-Directed Peptide Fragments/genetics,immunology Protein Binding T-Lymphocytes/immunology,metabolism
Chemicals
Histocompatibility Antigens Class II Peptide Fragments
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Hayball John D
School of Pharmacy and Medical Sciences, University of South Australia, North Tce, Adelaide, South Australia, Australia. [email protected]
Lake Richard A
References (48)
48 references, click to expand
  1. Effect of natural polymorphism at residue 86 of the HLA-DR beta chain on peptide binding.
    J Immunol. 1991 Aug 15;147(4):1292-8 PMID: 1869824
  2. Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain.
    Nature. 1991 Dec 5;354(6352):392-4 PMID: 1956401
  3. A study of complexes of class II invariant chain peptide: major histocompatibility complex class II molecules using a new complex-specific monoclonal antibody.
    Eur J Immunol. 1996 Feb;26(2):385-93 PMID: 8617308
  4. Identification of a CD4 binding site on the beta 2 domain of HLA-DR molecules.
    Nature. 1992 Apr 30;356(6372):799-801 PMID: 1574119
  5. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1.
    Nature. 1993 Jul 1;364(6432):33-9 PMID: 8316295
  6. 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. 1995 Sep 1;182(3):779-87 PMID: 7650484
  7. Sodium dodecyl sulfate-resistant HLA-DR "superdimer" bands are in some cases class II heterodimers bound to antibody.
    J Immunol. 1999 Apr 15;162(8):4671-6 PMID: 10202007
  8. Diversity in MHC class II antigen presentation.
    Immunology. 2002 Mar;105(3):252-62 PMID: 11918686
  9. Mutational analysis of two DR alpha residues involved in dimers of HLA-DR molecules.
    J Immunol. 1995 Aug 1;155(3):1210-7 PMID: 7636189
  10. Major histocompatibility complex independent clonal T cell anergy by direct interaction of Staphylococcus aureus enterotoxin B with the T cell antigen receptor.
    J Exp Med. 1992 Jun 1;175(6):1493-9 PMID: 1588277
  11. Transient accumulation of new class II MHC molecules in a novel endocytic compartment in B lymphocytes.
    Nature. 1994 May 12;369(6476):113-20 PMID: 8177316
  12. The CD4 and CD8 T cell surface antigens are associated with the internal membrane tyrosine-protein kinase p56lck.
    Cell. 1988 Oct 21;55(2):301-8 PMID: 3262426
  13. Evidence for dimers of MHC class II molecules in B lymphocytes and their role in low affinity T cell responses.
    Immunity. 1994 Nov;1(8):699-707 PMID: 7600295
  14. Signal transduction by receptors with tyrosine kinase activity.
    Cell. 1990 Apr 20;61(2):203-12 PMID: 2158859
  15. Three-dimensional structure of a human class II histocompatibility molecule complexed with superantigen.
    Nature. 1994 Apr 21;368(6473):711-8 PMID: 8152483
  16. CD4 augments the response of a T cell to agonist but not to antagonist ligands.
    Immunity. 1997 Sep;7(3):379-85 PMID: 9324358
  17. Capture and processing of exogenous antigens for presentation on MHC molecules.
    Annu Rev Immunol. 1997;15:821-50 PMID: 9143708
  18. MHC class II interaction with CD4 mediated by a region analogous to the MHC class I binding site for CD8.
    Nature. 1992 Apr 30;356(6372):796-8 PMID: 1574118
  19. Conformation of human leukocyte antigen class II molecules. Evidence for superdimers and empty molecules on human antigen presenting cells.
    J Biol Chem. 1996 Jun 14;271(24):13993-4000 PMID: 8662817
  20. Detection of dimers of dimers of human leukocyte antigen (HLA)-DR on the surface of living cells by single-particle fluorescence imaging.
    J Cell Biol. 1998 Jan 12;140(1):71-9 PMID: 9425155
  21. MHC class II function preserved by low-affinity peptide interactions preceding stable binding.
    Nature. 1994 Aug 25;370(6491):647-50 PMID: 8065450
  22. Structure of the human class I histocompatibility antigen, HLA-A2.
    Nature. 1987 Oct 8-14;329(6139):506-12 PMID: 3309677
  23. MHC multimerization, antigen expression and the induction of APC amnesia in the developing immune response.
    Immunol Cell Biol. 1999 Feb;77(1):99-104 PMID: 10101691
  24. Ligand-specific oligomerization of T-cell receptor molecules.
    Nature. 1997 Jun 5;387(6633):617-20 PMID: 9177351
  25. Structures of an MHC class II molecule with covalently bound single peptides.
    Science. 1996 May 17;272(5264):1001-4 PMID: 8638119
  26. Human class II MHC molecule HLA-DR1: X-ray structure determined from three crystal forms.
    Acta Crystallogr D Biol Crystallogr. 1995 Nov 1;51(Pt 6):946-61 PMID: 15299764
  27. Dimerization of cell surface receptors in signal transduction.
    Cell. 1995 Jan 27;80(2):213-23 PMID: 7834741
  28. pEF-BOS, a powerful mammalian expression vector.
    Nucleic Acids Res. 1990 Sep 11;18(17):5322 PMID: 1698283
  29. Monoclonal antibodies specific for Ia glycoproteins raised by immunization with activated T cells: possible role of T cellbound Ia antigens as targets of immunoregulatory T cells.
    J Immunol. 1984 Feb;132(2):662-7 PMID: 6228596
  30. Induction of T cell responses to the invariant chain derived peptide CLIP in mice immunized with the group 1 allergen of house dust mite.
    Int Immunol. 1996 Jul;8(7):1091-8 PMID: 8757954
  31. Coclustering of CD4 (L3T4) molecule with the T-cell receptor is induced by specific direct interaction of helper T cells and antigen-presenting cells.
    Proc Natl Acad Sci U S A. 1987 Aug;84(16):5888-92 PMID: 2956608
  32. Structure of the complex between human T-cell receptor, viral peptide and HLA-A2.
    Nature. 1996 Nov 14;384(6605):134-41 PMID: 8906788
  33. Crystal structure of the V alpha domain of a T cell antigen receptor.
    Science. 1995 Dec 15;270(5243):1821-4 PMID: 8525376
  34. A T cell clone with three potential TCR alpha chain rearrangements expresses only one receptor combination at the cell surface.
    Mol Immunol. 1996 Oct;33(15):1177-81 PMID: 9070666
  35. Invariant chain cleavage and peptide loading in major histocompatibility complex class II vesicles.
    J Exp Med. 1995 May 1;181(5):1729-41 PMID: 7722451
  36. HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading.
    Cell. 1995 Jul 14;82(1):155-65 PMID: 7606781
  37. Signal transduction by lymphocyte antigen receptors.
    Cell. 1994 Jan 28;76(2):263-74 PMID: 8293463
  38. A series of mammalian expression vectors and characterisation of their expression of a reporter gene in stably and transiently transfected cells.
    Nucleic Acids Res. 1990 Feb 25;18(4):1068 PMID: 2156225
  39. Toxic shock syndrome toxin-1 complexed with a class II major histocompatibility molecule HLA-DR1.
    Science. 1994 Dec 16;266(5192):1870-4 PMID: 7997880
  40. A shared alloantigenic determinant on Ia antigens encoded by the I-A and I-E subregions: evidence for I region gene duplication.
    J Immunol. 1981 Dec;127(6):2488-95 PMID: 6170707
  41. Variation in HLA-DM expression influences conversion of MHC class II alpha beta:class II-associated invariant chain peptide complexes to mature peptide-bound class II alpha beta dimers in a normal B cell line.
    J Immunol. 1996 Mar 15;156(6):2196 - 2204 PMID: 8690909
  42. Physical association of CD4 with the T cell receptor.
    J Immunol. 1992 Feb 1;148(3):678-88 PMID: 1370513
  43. Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide.
    Nature. 1994 Mar 17;368(6468):215-21 PMID: 8145819
  44. The MHC class II-associated invariant chain contains two endosomal targeting signals within its cytoplasmic tail.
    J Cell Sci. 1993 Nov;106 ( Pt 3):831-46 PMID: 8308066
  45. MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding.
    Nature. 1991 Sep 12;353(6340):134-9 PMID: 1891045
  46. An alphabeta T cell receptor structure at 2.5 A and its orientation in the TCR-MHC complex.
    Science. 1996 Oct 11;274(5285):209-19 PMID: 8824178
  47. Sorting signals in the MHC class II invariant chain cytoplasmic tail and transmembrane region determine trafficking to an endocytic processing compartment.
    J Cell Biol. 1994 Jul;126(2):317-30 PMID: 8034737
  48. The crystal structure of a T cell receptor in complex with peptide and MHC class II.
    Science. 1999 Dec 3;286(5446):1913-21 PMID: 10583947
Article Info
Journal
Molecular and cellular biochemistry
Abbr.
Mol Cell Biochem
ISSN
0300-8177
Published
2005-05-00
Pages
1-9
Language
English
Region
Netherlands
NLM ID
0364456
Subset
IM
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