Home LiteratureArticle Details
PMID: 8976171 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules.

The Journal of experimental medicine ·Vol. 184 ·No. 6 ·1996-12-01 ·Pages 2153-65

Denzin LK, Hammond C, Cresswell P

Abstract

Major histocompatibility complex (MHC) class II-positive cell lines which lack HLA-DM expression accumulate class II molecules associated with residual invariant (I) chain fragments (class II-associated invariant chain peptides [CLIP]). In vitro, HLA-DM catalyzes CLIP dissociation from class II-CLIP complexes, promoting binding of antigenic peptides. Here the physical interaction of HLA-DM with HLA-DR molecules was investigated. HLA-DM complexes with class II molecules were detectable transiently in cells, peaking at the time when the class II molecules entered the MHC class II compartment. HLA-DR alpha beta dimers newly released from I chain, and those associated with I chain fragments, were found to associate with HLA-DM in vivo. Mature, peptide-loaded DR molecules also associated at a low level. These same species, but not DR-I chain complexes, were also shown to bind to purified HLA-DM molecules in vitro. HLA-DM interaction was quantitatively superior with DR molecules isolated in association with CLIP. DM-DR complexes generated by incubating HLA-DM with purified DR alpha beta CLIP contained virtually no associated CLIP, suggesting that this superior interaction reflects a prolonged HLA-DM association with empty class II dimers after CLIP dissociation. Incubation of peptide-free alpha beta dimers in the presence of HLA-DM was found to prolong their ability to bind subsequently added antigenic peptides. Stabilization of empty class II molecules may be an important property of HLA-DM in facilitating antigen processing.

MeSH Terms
Amino Acid Sequence Cell Line, Transformed Dimerization HLA-D Antigens/biosynthesis,immunology HLA-DR Antigens/immunology HLA-DR3 Antigen/biosynthesis,chemistry,immunology Histocompatibility Antigens Class II Humans Kinetics Molecular Sequence Data Peptide Fragments/chemical synthesis,immunology Protein Binding Time Factors Transfection Tumor Cells, Cultured
Chemicals
H2-M antigens HLA-D Antigens HLA-DM antigens HLA-DR Antigens HLA-DR3 Antigen Histocompatibility Antigens Class II Peptide Fragments
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Denzin L K
Howard Hughes Medical Institute, Yale University School of Medicine, Section of Immunobiology, New Haven, Connecticut 06510, USA.
Hammond C
Cresswell P
References (57)
57 references, click to expand
  1. 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
  2. Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells.
    Immunity. 1994 Oct;1(7):595-606 PMID: 7600288
  3. Peptide binding inhibits protein aggregation of invariant-chain free class II dimers and promotes surface expression of occupied molecules.
    Nature. 1993 Jun 24;363(6431):725-8 PMID: 8515815
  4. 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
  5. A role for calnexin (IP90) in the assembly of class II MHC molecules.
    EMBO J. 1994 Feb 1;13(3):675-82 PMID: 8313912
  6. Endosomal aspartic proteinases are required for invariant-chain processing.
    Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2171-5 PMID: 8134367
  7. Separation of subcellular compartments containing distinct functional forms of MHC class II.
    J Cell Biol. 1994 May;125(3):595-605 PMID: 7909813
  8. 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
  9. Isolation and characterization of the intracellular MHC class II compartment.
    Nature. 1994 May 12;369(6476):120-6 PMID: 8177317
  10. Antigen processing and class II MHC peptide-loading compartments in human B-lymphoblastoid cells.
    Nature. 1994 May 12;369(6476):147-51 PMID: 8177319
  11. 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
  12. Assembly, transport, and function of MHC class II molecules.
    Annu Rev Immunol. 1994;12:259-93 PMID: 8011283
  13. 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
  14. MHC class II function preserved by low-affinity peptide interactions preceding stable binding.
    Nature. 1994 Aug 25;370(6491):647-50 PMID: 8065450
  15. A segment of the MHC class II beta chain plays a critical role in targeting class II molecules to the endocytic pathway.
    Int Immunol. 1994 Jul;6(7):973-82 PMID: 7947465
  16. Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments.
    Science. 1994 Dec 2;266(5190):1566-9 PMID: 7985027
  17. 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
  18. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide.
    Immunity. 1995 Aug;3(2):197-205 PMID: 7648393
  19. A lysosomal targeting signal in the cytoplasmic tail of the beta chain directs HLA-DM to MHC class II compartments.
    J Cell Biol. 1995 Oct;131(2):351-69 PMID: 7593164
  20. The MHC class II molecule H2-M is targeted to an endosomal compartment by a tyrosine-based targeting motif.
    Immunity. 1995 Nov;3(5):561-72 PMID: 7584146
  21. Invariant chain made in Escherichia coli has an exposed N-terminal segment that blocks antigen binding to HLA-DR1 and a trimeric C-terminal segment that binds empty HLA-DR1.
    Proc Natl Acad Sci U S A. 1995 Nov 21;92(24):11289-93 PMID: 7479981
  22. The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3.
    Nature. 1995 Nov 30;378(6556):457-62 PMID: 7477400
  23. Association between HLA-DM and HLA-DR in vivo.
    Immunity. 1996 Jan;4(1):87-96 PMID: 8574855
  24. Mice lacking H2-M complexes, enigmatic elements of the MHC class II peptide-loading pathway.
    Cell. 1996 Feb 23;84(4):531-41 PMID: 8598040
  25. H2-M mutant mice are defective in the peptide loading of class II molecules, antigen presentation, and T cell repertoire selection.
    Cell. 1996 Feb 23;84(4):543-50 PMID: 8598041
  26. Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading.
    Immunity. 1996 Apr;4(4):357-66 PMID: 8612130
  27. Trafficking of major histocompatibility complex class II molecules through intracellular compartments containing HLA-DM.
    Hum Immunol. 1996 Jan;45(1):13-23 PMID: 8655355
  28. Detection of a common polypeptide chain in I--A and I--E sub-region immunoprecipitates.
    Mol Immunol. 1979 Jan;16(1):51-60 PMID: 376435
  29. Use of a monoclonal antibody (W6/32) in structural studies of HLA-A,B,C, antigens.
    J Immunol. 1979 Jul;123(1):342-9 PMID: 87477
  30. Two populations of Ia-like molecules on a human B cell line.
    J Immunol. 1980 Jul;125(1):293-9 PMID: 6966655
  31. Biosynthesis and glycosylation of the invariant chain associated with HLA-DR antigens.
    J Immunol. 1982 Dec;129(6):2564-9 PMID: 6982931
  32. Analysis of the oligosaccharides on the HLA-DR and DC1 B cell antigens.
    J Immunol. 1983 Jan;130(1):274-82 PMID: 6600184
  33. Differential expression and serologically distinct subpopulations of human Ia antigens detected with monoclonal antibodies to Ia alpha and beta chains.
    Eur J Immunol. 1982 Nov;12(11):942-8 PMID: 6185348
  34. Monensin prevents terminal glycosylation of the N- and O-linked oligosaccharides of the HLA-DR-associated invariant chain and inhibits its dissociation from the alpha-beta chain complex.
    Proc Natl Acad Sci U S A. 1984 Mar;81(5):1287-91 PMID: 6608726
  35. Monoclonal antibody to HLA-A3.
    Hybridoma. 1982;1(2):87-90 PMID: 6208124
  36. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids.
    Immunogenetics. 1985;21(3):235-46 PMID: 3872841
  37. Antigen-presenting function of the macrophage.
    Annu Rev Immunol. 1984;2:395-428 PMID: 6242349
  38. Role for intracellular proteases in the processing and transport of class II HLA antigens.
    Proc Natl Acad Sci U S A. 1988 Jun;85(11):3975-9 PMID: 3287381
  39. MHC class II-associated invariant chain contains a sorting signal for endosomal compartments.
    Cell. 1990 Nov 16;63(4):707-16 PMID: 2121367
  40. Segregation of MHC class II molecules from MHC class I molecules in the Golgi complex for transport to lysosomal compartments.
    Nature. 1991 Feb 21;349(6311):669-76 PMID: 1847504
  41. 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
  42. A new human HLA class II-related locus, DM.
    Nature. 1991 Oct 10;353(6344):571-3 PMID: 1922365
  43. New class II-like genes in the murine MHC.
    Nature. 1991 Oct 10;353(6344):573-6 PMID: 1922366
  44. 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
  45. A gene required for class II-restricted antigen presentation maps to the major histocompatibility complex.
    J Exp Med. 1991 Dec 1;174(6):1607-15 PMID: 1744588
  46. The human class II MHC protein HLA-DR1 assembles as empty alpha beta heterodimers in the absence of antigenic peptide.
    Cell. 1992 Feb 7;68(3):465-77 PMID: 1371238
  47. Inhibition of endosomal proteolytic activity by leupeptin blocks surface expression of MHC class II molecules and their conversion to SDS resistance alpha beta heterodimers in endosomes.
    EMBO J. 1992 Feb;11(2):411-6 PMID: 1311249
  48. The antigen-processing mutant T2 suggests a role for MHC-linked genes in class II antigen presentation.
    J Immunol. 1992 Apr 15;148(8):2586-90 PMID: 1373173
  49. Assembly and transport properties of invariant chain trimers and HLA-DR-invariant chain complexes.
    J Immunol. 1992 Jun 1;148(11):3478-82 PMID: 1588042
  50. Antigen presentation and T cell development in H2-M-deficient mice.
    Science. 1996 Mar 1;271(5253):1278-81 PMID: 8638109
  51. 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
  52. Developing and shedding inhibitions: how MHC class II molecules reach maturity.
    Curr Opin Immunol. 1996 Feb;8(1):51-8 PMID: 8729446
  53. Reconstitution of an operational MHC class II compartment in nonantigen-presenting cells.
    Science. 1994 Dec 2;266(5190):1569-73 PMID: 7985028
  54. In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides.
    Immunity. 1994 Dec;1(9):763-74 PMID: 7895165
  55. Antigen capture and major histocompatibility class II compartments of freshly isolated and cultured human blood dendritic cells.
    J Exp Med. 1995 Jul 1;182(1):163-74 PMID: 7790816
  56. Mediation by HLA-DM of dissociation of peptides from HLA-DR.
    Nature. 1995 Jun 29;375(6534):802-6 PMID: 7596415
  57. Invariant chain peptides in most HLA-DR molecules of an antigen-processing mutant.
    Science. 1992 Dec 11;258(5089):1801-4 PMID: 1465617
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1996-12-01
Pages
2153-65
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2196380
Subset
IM
Grants
NIAID NIH HHS · AI23081 · 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: product@genelibs.com