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PMID: 10748235 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Role for cathepsin F in invariant chain processing and major histocompatibility complex class II peptide loading by macrophages.

The Journal of experimental medicine ·Vol. 191 ·No. 7 ·2000-04-03 ·Pages 1177-86

Shi GP, Bryant RA, Riese R, Verhelst S, Driessen C, Li Z, Bromme D, Ploegh HL, Chapman HA

Abstract

The major histocompatibility complex (MHC) class II-associated invariant chain (Ii) regulates intracellular trafficking and peptide loading of MHC class II molecules. Such loading occurs after endosomal degradation of the invariant chain to a approximately 3-kD peptide termed CLIP (class II-associated invariant chain peptide). Cathepsins L and S have both been implicated in degradation of Ii to CLIP in thymus and peripheral lymphoid organs, respectively. However, macrophages from mice deficient in both cathepsins S and L can process Ii and load peptides onto MHC class II dimers normally. Both processes are blocked by a cysteine protease inhibitor, indicating the involvement of an additional Ii-processing enzyme(s). Comparison of cysteine proteases expressed by macrophages with those found in splenocytes and dendritic cells revealed two enzymes expressed exclusively in macrophages, cathepsins Z and F. Recombinant cathepsin Z did not generate CLIP from Ii-MHC class II complexes, whereas cathepsin F was as efficient as cathepsin S in CLIP generation. Inhibition of cathepsin F activity and MHC class II peptide loading by macrophages exhibited similar specificity and activity profiles. These experiments show that cathepsin F, in a subset of antigen presenting cells (APCs), can efficiently degrade Ii. Different APCs can thus use distinct proteases to mediate MHC class II maturation and peptide loading.

MeSH Terms
Animals Antigen Presentation/immunology Antigens, Differentiation, B-Lymphocyte/immunology Cathepsin F Cathepsin L Cathepsins/antagonists & inhibitors,genetics,immunology Cricetinae Cysteine Endopeptidases Cysteine Proteinase Inhibitors/pharmacology Dipeptides/pharmacology Endopeptidases Gene Expression Histocompatibility Antigens Class II/immunology Humans Immunoglobulin E/immunology Leucine/analogs & derivatives,pharmacology Macrophages, Alveolar/immunology Mice Mice, Inbred C57BL Mice, Knockout Peptides/immunology Sulfones/pharmacology
Chemicals
Antigens, Differentiation, B-Lymphocyte Cysteine Proteinase Inhibitors Dipeptides Histocompatibility Antigens Class II JPM 565 Peptides Sulfones invariant chain morpholin- urea-phenylalanyl-homophenylalanyl-vinylsulfone-phenyl Immunoglobulin E Cathepsins Endopeptidases Cysteine Endopeptidases CTSL protein, human Cathepsin L Ctsl protein, mouse cathepsin S CTSF protein, human Cathepsin F Ctsf protein, mouse Leucine
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Shi G P
Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Harvard Medical School, Boston, Massachusetts 02115, USA.
Bryant R A
Riese R
Verhelst S
Driessen C
Li Z
Bromme D
Ploegh H L
Chapman H A
References (42)
42 references, click to expand
  1. Cathepsin S controls the trafficking and maturation of MHC class II molecules in dendritic cells.
    J Cell Biol. 1999 Nov 15;147(4):775-90 PMID: 10562280
  2. Molecular cloning of human cathepsin O, a novel endoproteinase and homologue of rabbit OC2.
    FEBS Lett. 1995 Jan 3;357(2):129-34 PMID: 7805878
  3. Influence of acute exposure to cigarette smoke on the alveolar macrophage system.
    J Lab Clin Med. 1977 Jun;89(6):1215-24 PMID: 864302
  4. The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies.
    J Exp Med. 1990 May 1;171(5):1753-71 PMID: 2185332
  5. Mediation by HLA-DM of dissociation of peptides from HLA-DR.
    Nature. 1995 Jun 29;375(6534):802-6 PMID: 7596415
  6. DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide.
    Immunity. 1995 Aug;3(2):197-205 PMID: 7648393
  7. Vinyl sulfones as mechanism-based cysteine protease inhibitors.
    J Med Chem. 1995 Aug 18;38(17):3193-6 PMID: 7650671
  8. 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
  9. 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
  10. 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
  11. Antigen presentation and T cell development in H2-M-deficient mice.
    Science. 1996 Mar 1;271(5253):1278-81 PMID: 8638109
  12. How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway.
    Annu Rev Cell Dev Biol. 1995;11:267-306 PMID: 8689559
  13. High level expression and crystallization of recombinant human cathepsin S.
    Protein Sci. 1996 Apr;5(4):789-91 PMID: 8845771
  14. Mechanistic studies on the inactivation of papain by epoxysuccinyl inhibitors.
    J Med Chem. 1996 Aug 16;39(17):3357-66 PMID: 8765519
  15. Human cathepsin W, a putative cysteine protease predominantly expressed in CD8+ T-lymphocytes.
    FEBS Lett. 1997 Apr 1;405(3):253-9 PMID: 9108299
  16. Capture and processing of exogenous antigens for presentation on MHC molecules.
    Annu Rev Immunol. 1997;15:821-50 PMID: 9143708
  17. Degradation of mouse invariant chain: roles of cathepsins S and D and the influence of major histocompatibility complex polymorphism.
    J Exp Med. 1997 Aug 18;186(4):549-60 PMID: 9254653
  18. The role of macrophages in the induction and regulation of immunity elicited by exogenous antigens.
    Eur J Immunol. 1998 Feb;28(2):479-87 PMID: 9521056
  19. In vivo effects of T helper cell type 2 cytokines on macrophage antigen-presenting cell induction of T helper subsets.
    J Immunol. 1997 Dec 15;159(12):5834-40 PMID: 9550379
  20. Cathepsin L: critical role in Ii degradation and CD4 T cell selection in the thymus.
    Science. 1998 Apr 17;280(5362):450-3 PMID: 9545226
  21. Cathepsin S activity regulates antigen presentation and immunity.
    J Clin Invest. 1998 Jun 1;101(11):2351-63 PMID: 9616206
  22. Cathepsin Z, a novel human cysteine proteinase with a short propeptide domain and a unique chromosomal location.
    J Biol Chem. 1998 Jul 3;273(27):16816-23 PMID: 9642240
  23. Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells.
    Cell. 1998 Jun 26;93(7):1135-45 PMID: 9657147
  24. Cysteine protease inhibitors cure an experimental Trypanosoma cruzi infection.
    J Exp Med. 1998 Aug 17;188(4):725-34 PMID: 9705954
  25. Switch of CD4+ T cell differentiation from Th2 to Th1 by treatment with cathepsin B inhibitor in experimental leishmaniasis.
    J Immunol. 1998 Sep 1;161(5):2120-7 PMID: 9725203
  26. Human cathepsin X: a novel cysteine protease of the papain family with a very short proregion and unique insertions.
    FEBS Lett. 1998 Aug 28;434(1-2):135-9 PMID: 9738465
  27. Antigen detection in vivo after immunization with different presentation forms of rabies virus antigen, II. Cellular, but not humoral, systemic immune responses against rabies virus immune-stimulating complexes are macrophage dependent.
    Immunology. 1998 Aug;94(4):455-60 PMID: 9767431
  28. Human cathepsin F. Molecular cloning, functional expression, tissue localization, and enzymatic characterization.
    J Biol Chem. 1998 Nov 27;273(48):32000-8 PMID: 9822672
  29. Distinct dendritic cell subsets differentially regulate the class of immune response in vivo.
    Proc Natl Acad Sci U S A. 1999 Feb 2;96(3):1036-41 PMID: 9927689
  30. Cathepsin S required for normal MHC class II peptide loading and germinal center development.
    Immunity. 1999 Feb;10(2):197-206 PMID: 10072072
  31. Impaired invariant chain degradation and antigen presentation and diminished collagen-induced arthritis in cathepsin S null mice.
    Immunity. 1999 Feb;10(2):207-17 PMID: 10072073
  32. Full-length cDNA of human cathepsin F predicts the presence of a cystatin domain at the N-terminus of the cysteine protease zymogen.
    Biochem Biophys Res Commun. 1999 Apr 13;257(2):313-8 PMID: 10198209
  33. The occluding loop in cathepsin B defines the pH dependence of inhibition by its propeptide.
    Biochemistry. 1999 Apr 20;38(16):5017-23 PMID: 10213604
  34. Molecular cloning and structural and functional characterization of human cathepsin F, a new cysteine proteinase of the papain family with a long propeptide domain.
    J Biol Chem. 1999 May 14;274(20):13800-9 PMID: 10318784
  35. Cysteine protease inhibitors as chemotherapy for parasitic infections.
    Bioorg Med Chem. 1999 Apr;7(4):639-44 PMID: 10353643
  36. Increased expression of the CD80 accessory molecule by alveolar macrophages in asthmatic subjects and its functional involvement in allergen presentation to autologous TH2 lymphocytes.
    J Allergy Clin Immunol. 1999 Jun;103(6):1136-42 PMID: 10359896
  37. Human cathepsin X: A cysteine protease with unique carboxypeptidase activity.
    Biochemistry. 1999 Sep 28;38(39):12648-54 PMID: 10504234
  38. Molecular cloning and expression of human alveolar macrophage cathepsin S, an elastinolytic cysteine protease.
    J Biol Chem. 1992 Apr 15;267(11):7258-62 PMID: 1373132
  39. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation.
    Cell. 1994 Jan 28;76(2):287-99 PMID: 8293464
  40. Human cathepsin S: chromosomal localization, gene structure, and tissue distribution.
    J Biol Chem. 1994 Apr 15;269(15):11530-6 PMID: 8157683
  41. Assembly, transport, and function of MHC class II molecules.
    Annu Rev Immunol. 1994;12:259-93 PMID: 8011283
  42. Exercise suppresses macrophage antigen presentation.
    J Appl Physiol (1985). 1999 Dec;87(6):2253-8 PMID: 10601175
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
2000-04-03
Pages
1177-86
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2193169
Subset
IM
Grants
NHLBI NIH HHS · HL48716 · United States
NHLBI NIH HHS · HL60942 · United States
NIAID NIH HHS · K08AI01555 · United States
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