Home LiteratureArticle Details
PMID: 7836921 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Binding of major histocompatibility complex class II to the invariant chain-derived peptide, CLIP, is regulated by allelic polymorphism in class II.

The Journal of experimental medicine ·Vol. 181 ·No. 2 ·1995-02-01 ·Pages 677-83

Sette A, Southwood S, Miller J, Appella E

Abstract

Major histocompatibility complex class II-associated invariant chain (Ii) provides several important functions that regulate class II expression and function. One of these is the ability to inhibit class II peptide loading early in biosynthesis. This allows for efficient class II folding and egress from the endoplasmic reticulum, and protects the class II peptide binding site from loading with peptides before entry into endosomal compartments. The ability of Ii to interact with class II and interfere with peptide loading has been mapped to Ii exon 3, which encodes amino acids 82-107. This same region of Ii has been described as a nested set of class II-associated Ii peptides (CLIPs) that are transiently associated with class II in normal cells and accumulate in human histocompatibility leukocyte antigen-DM-negative cell lines. Currently it is not clear how CLIP and the CLIP region of Ii blocks peptide binding. CLIP may bind directly to the class II peptide binding site, or may bind elsewhere on class II and modulate class II peptide binding allosterically. In this report, we show that CLIP can interact with many different murine and human class II molecules, but that the affinity of this interaction is controlled by polymorphic residues in the class II chains. Likewise, structural changes in CLIP also modulate class II binding in an allele-dependent manner. Finally, the specificity and kinetics of CLIP binding to class II molecule is similar to antigenic peptide binding to class II. These data indicate that CLIP binds to class II in an analogous fashion as conventional antigenic peptides, suggesting that the CLIP segment of Ii may actually occupy the class II peptide binding site.

MeSH Terms
Alleles Amino Acid Sequence Animals Antigens, Differentiation, B-Lymphocyte Cell Line, Transformed Histocompatibility Antigens Class II/genetics,metabolism Humans Kinetics Mice Molecular Sequence Data Peptides/metabolism Polymorphism, Genetic Protein Binding
Chemicals
Antigens, Differentiation, B-Lymphocyte Histocompatibility Antigens Class II Peptides invariant chain
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sette A
Department of Immunology, Cytel, San Diego, CA 92121.
Southwood S
Miller J
Appella E
References (46)
46 references, click to expand
  1. HLA-DMA and -DMB genes are both required for MHC class II/peptide complex formation in antigen-presenting cells.
    Nature. 1994 Apr 7;368(6471):554-8 PMID: 8139690
  2. An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules.
    Nature. 1994 Apr 7;368(6471):551-4 PMID: 8139689
  3. MHC class II antigen processing: biology of invariant chain.
    Curr Opin Immunol. 1994 Feb;6(1):57-63 PMID: 8172680
  4. Transport and intracellular distribution of MHC class II molecules and associated invariant chain in normal and antigen-processing mutant cell lines.
    J Cell Biol. 1994 Jun;125(6):1225-37 PMID: 8207055
  5. Assembly of HLA DR1 molecules translated in vitro: binding of peptide in the endoplasmic reticulum precludes association with invariant chain.
    EMBO J. 1994 Jun 1;13(11):2699-707 PMID: 8013468
  6. 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
  7. Invariant chain prevents the HLA-DR-restricted presentation of a cytosolic peptide.
    J Immunol. 1994 Aug 15;153(4):1487-94 PMID: 8046228
  8. Mapping functional regions in the lumenal domain of the class II-associated invariant chain.
    J Exp Med. 1994 Aug 1;180(2):623-9 PMID: 7519244
  9. Selective release of some invariant chain-derived peptides from HLA-DR1 molecules at endosomal pH.
    J Exp Med. 1994 Aug 1;180(2):751-5 PMID: 8046351
  10. The CLIP region of invariant chain plays a critical role in regulating major histocompatibility complex class II folding, transport, and peptide occupancy.
    J Exp Med. 1994 Sep 1;180(3):1107-13 PMID: 8064228
  11. THE PREPARATION OF I-131-LABELLED HUMAN GROWTH HORMONE OF HIGH SPECIFIC RADIOACTIVITY.
    Biochem J. 1963 Oct;89:114-23 PMID: 14097352
  12. Purification and characterization of class II histocompatibility antigens from a homozygous human B cell line.
    J Biol Chem. 1987 Nov 25;262(33):16087-94 PMID: 2824477
  13. Structural analysis of peptides capable of binding to more than one Ia antigen.
    J Immunol. 1989 Jan 1;142(1):35-40 PMID: 2535860
  14. Defective processing and presentation of exogenous antigens in mutants with normal HLA class II genes.
    Nature. 1990 Jan 4;343(6253):71-4 PMID: 1967485
  15. Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding.
    Nature. 1990 Jun 14;345(6276):615-8 PMID: 2190094
  16. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments.
    Cell. 1990 Nov 16;63(4):707-16 PMID: 2121367
  17. Invariant chain distinguishes between the exogenous and endogenous antigen presentation pathways.
    Nature. 1990 Nov 1;348(6296):39-44 PMID: 2234057
  18. Intracellular transport of class II MHC molecules directed by invariant chain.
    Nature. 1990 Dec 13;348(6302):600-5 PMID: 2250716
  19. Invariant chain promotes egress of poorly expressed, haplotype-mismatched class II major histocompatibility complex A alpha A beta dimers from the endoplasmic reticulum/cis-Golgi compartment.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2346-50 PMID: 1900941
  20. Invariant chain influences post-translational processing of HLA-DR molecules.
    J Immunol. 1991 Jul 15;147(2):603-8 PMID: 2071896
  21. Sequence analysis of peptides bound to MHC class II molecules.
    Nature. 1991 Oct 17;353(6345):622-7 PMID: 1656276
  22. Effect of pH on MHC class II-peptide interactions.
    J Immunol. 1992 Feb 1;148(3):844-51 PMID: 1730877
  23. Invariant chain can function as a chaperone protein for class II major histocompatibility complex molecules.
    Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2282-6 PMID: 1549594
  24. Antigen presentation enhanced by the alternatively spliced invariant chain gene product p41.
    Nature. 1992 Jun 18;357(6379):596-8 PMID: 1608470
  25. Peptides presented to the immune system by the murine class II major histocompatibility complex molecule I-Ad.
    Science. 1992 Jun 26;256(5065):1817-20 PMID: 1319610
  26. Stable surface expression of invariant chain prevents peptide presentation by HLA-DR.
    EMBO J. 1992 Aug;11(8):2841-7 PMID: 1639058
  27. High affinity for class II molecules as a necessary but not sufficient characteristic of encephalitogenic determinants.
    Int Immunol. 1992 Jul;4(7):773-7 PMID: 1379827
  28. Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size.
    Nature. 1992 Aug 27;358(6389):764-8 PMID: 1380674
  29. HLA-DR molecules from an antigen-processing mutant cell line are associated with invariant chain peptides.
    Nature. 1992 Dec 3;360(6403):474-7 PMID: 1448172
  30. Invariant chain peptides in most HLA-DR molecules of an antigen-processing mutant.
    Science. 1992 Dec 11;258(5089):1801-4 PMID: 1465617
  31. Binding of myelin basic protein peptides to human histocompatibility leukocyte antigen class II molecules and their recognition by T cells from multiple sclerosis patients.
    J Clin Invest. 1993 Feb;91(2):616-28 PMID: 7679413
  32. Mice lacking the MHC class II-associated invariant chain.
    Cell. 1993 Feb 26;72(4):635-48 PMID: 7679955
  33. Putting together an MHC class I molecule.
    Curr Opin Immunol. 1993 Feb;5(1):21-6 PMID: 8095788
  34. Defective major histocompatibility complex class II assembly, transport, peptide acquisition, and CD4+ T cell selection in mice lacking invariant chain expression.
    J Exp Med. 1993 Jun 1;177(6):1699-712 PMID: 8098731
  35. Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles.
    J Exp Med. 1993 Jul 1;178(1):27-47 PMID: 8315383
  36. The chondroitin sulfate form of invariant chain can enhance stimulation of T cell responses through interaction with CD44.
    Cell. 1993 Jul 30;74(2):257-68 PMID: 8343954
  37. Prominent role of secondary anchor residues in peptide binding to HLA-A2.1 molecules.
    Cell. 1993 Sep 10;74(5):929-37 PMID: 8104103
  38. The segment of invariant chain that is critical for association with major histocompatibility complex class II molecules contains the sequence of a peptide eluted from class II polypeptides.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9703-6 PMID: 8415765
  39. Enhanced antigen presentation in the absence of the invariant chain endosomal localization signal.
    J Exp Med. 1993 Dec 1;178(6):1959-69 PMID: 7902408
  40. Comparison of peptides bound to spleen and thymus class II.
    J Exp Med. 1993 Dec 1;178(6):2173-83 PMID: 8245790
  41. A mutant human histocompatibility leukocyte antigen DR molecule associated with invariant chain peptides.
    J Exp Med. 1994 Feb 1;179(2):541-9 PMID: 8294865
  42. The invariant chain is required for intracellular transport and function of major histocompatibility complex class II molecules.
    J Exp Med. 1994 Feb 1;179(2):681-94 PMID: 8294875
  43. 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
  44. Association with BiP and aggregation of class II MHC molecules synthesized in the absence of invariant chain.
    EMBO J. 1994 Feb 15;13(4):934-44 PMID: 8112308
  45. Diversity of endogenous epitopes bound to MHC class II molecules limited by invariant chain.
    Science. 1994 Mar 4;263(5151):1284-6 PMID: 7510069
  46. A disease-related epitope of Torpedo acetylcholine receptor. Residues involved in I-Ab binding, self-nonself discrimination, and TCR antagonism.
    J Immunol. 1994 May 1;152(9):4526-36 PMID: 8157967
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1995-02-01
Pages
677-83
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2191868
Subset
IM
Grants
NIAID NIH HHS · AI-18634 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]