HLA-DM acts as a molecular chaperone and rescues empty HLA-DR molecules at lysosomal pH

Immunity

Volumn 6, Issue 3, 1997, Pages 293-302

  Kropshofer, Harald ^a   Arndt, Sven O ^a   Moldenhauer, Gerhard ^a   Hämmerling, Günter J ^a   Vogt, Anne B ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HLA DM ANTIGEN; HLA DR ANTIGEN; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG;

ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; HLA SYSTEM; HUMAN; HUMAN CELL; LYSOSOME; PH; PRIORITY JOURNAL;

EID: 0030978530     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80332-5     Document Type: Article

References (64)

1. Adams, T.E., Bodmer, J.G., and Bodmer, W.F. (1983). Production and characterization of monoclonal antibodies recognizing the α-chain subunits of human la alloantigens. Immunology 50, 613-624.
2. Avva, R., and Cresswell, P. (1994). In vivo and in vitro formation and dissociation of HLA-DR complexes with invariant chain-derived peptides. Immunity 1, 763-774.
3. Bakke, O., and Dobberstein, B. (1990). MHC class II-associated invariant chain contains a sorting signal for endosomal compartments. Cell 63, 707-715.
4. Bijlmakers, M.E., Benaroch, P., and Ploegh, H.L. (1994). Mapping functional regions in the luminal domain of class II-associated invariant chain. J. Exp. Med. 180, 623-629.
5. Bikoff, E.K., Huang, L.-Y., Episkopou, V., Van Meerwijk, J., Germain, R.N., and Robertson, E.J. (1993). Defective major histocompatibility complex class II assembly, transport, peptideacquisition, and CD4+ T cell selection in mice lacking invariant chain expression. J. Exp. Med. 177, 1699-1712.
6. Brooks, A.G., Campbell, P.L., Reynolds, P., Gautam, A.M., and McCluskey, J. (1994). Antigen presentation and assembly by mouse I-Ak class II molecules in human APC containing deleted or mutated HLA-DM genes. J. Immunol. 153, 5382-5392.
7. Busch, R., Cloutier, I., Sékaly, R.-P., and Hämmerling, G.J. (1996). Invariant chain protects class II histocompatibility antigens from binding intact polypeptides in the endoplasmic reticulum. EMBO J. 15, 418-428.
8. Castellino, F., and Germain, R.N. (1995). Extensive trafficking of MHC class II-invariant chain complexes in the endocytic pathway and appearance of peptide-loaded class II in multiple compartments. Immunity 2, 73-88.
9. Chicz, R.M., Urban, R.G., Lane, W.S., Gorga, J.C., Stern, L.J., Vignali, D.A.A., and Strominger, J.L. (1992). Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size. Nature 358, 764-768.
10. Cho, S., Attaya, M., and Monaco, J.J. (1991). New class II-like genes in the murine MHC. Nature 353, 573-576.
11. Denzin, L.K., and Cresswell, P. (1995). HLA-DM induces CLIP dissociation from MHC class II aβ dimers and facilitates peptide loading. Cell 82, 155-165.
12. Denzin, L.K., Hammond, C., and Cresswell, P. (1996). HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J. Exp. Med. 184, 2153-2165.
13. Devaux, B., Wilson, K.J., Aguilar, B., Jorgensen, B., and Rothbard, J.B. (1995). Differential stability of HLA-DR alleles independent of endogenous peptides. J. Immunol. 155, 1921-1928.
14. Ellis, R.J., and van der Vies, S.M. (1991). Molecular chaperones. Annu. Rev. Biochem. 60, 321-347.
15. Fling, S.P., Arp, B., and Pious, D. (1994). The HLA-DMA gene is required for the formation of stable class II/peptide complexes. Nature 368, 554-558.
16. Geluk, A., van Meijgaarden, K.E., Janson, A.A.M., Drijfhout, J.W., Meloen, R.H., De Vries, R.R.P., and Ottenhoff, T.H.M. (1992). Functional analysis of DR17 (DR3)-restricted mycobacterial T-cell epitopes reveals DR17 binding motif and enables the design of allele-specific competitor peptides. J. Immunol. 149, 2864-2871.
17. Germain, R., and Hendrix, L.R. (1991). MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature 353, 134-139.
18. Germain, R., and Rinker, A.G., Jr. (1993). Peptide binding inhibits protein aggregation of invariant-chain free class II dimers and promotes selective cell surface expression of occupied molecules. Nature 363, 725-728.
19. Green, S.A., Zimmer, K.P., Griffith, G., and Mellman, I. (1987). Kinetics of intracellular transport and sorting of lysosomal membrane and plasma membrane proteins. J. Cell Biol. 105, 1227-1240.
20. Jardetzky, T.S., Gorga, J.C., Busch, R., Rothbard, J., Strominger, J.L., and Wiley, D.C. (1990). Peptide binding to HLA-DR1: apeptide with most residues substituted to alanine retains MHC binding. EMBO J. 9, 1797-1803.
21. Karlsson, L., Peleraux, A., Lindstedt, R., Liljedahl, M., and Peterson, P.A. (1994). Reconstitution of an operational MHC class II compartment in nonantigen-presenting cells. Science 266, 1569-1572.
22. Kelly, A.P., Monaco, J.J., Cho, S., and Trowsdale, J. (1991). A new human HLA class II-related locus. Nature 353, 571-573.
23. Kornfeld, S. (1992). Structure and function of the mannose-6-phosphate/insuline-like growth factor-II receptors. Annu. Rev. Biochem. 61, 307-330.
24. Kropshofer, H., Bohlinger, I., Max, H., and Kalbacher, H. (1991). Self and foreign peptides interact with intact and disassembled MHC class II antigen HLA-DR1 via Trp pockets. Biochemistry 30, 9177-9187.
25. Kropshofer, H., Vogt, A.B., and Hämmerling, G.J. (1995a). Structural features of invariant chain CLIP region controlling rapid release from HLA-DR molecules and inhibition of peptide binding. Proc. Natl. Acad. Sci. USA 92, 8313-8317.
26. Kropshofer, H., Vogt, A.B., Stern, L.J.,and Hämmerling, G.J. (1995b). Self-release of CLIP in peptide loading of HLA-DR molecules. Science 270, 1357-1359.
27. Kropshofer, H., Vogt, A.B., Moldenhauer, G., Hammer, J., Blum, J.S., and Hämmerling, G.J. (1996). Editing of the HLA-DR peptide repertoire by HLA-DM. EMBO J. 15, 6144-6154.
28. Kropshofer, H., Hämmerling, G.J., and Vogt, A.B. (1997). How HLA-DM edits the MHC class II peptide repertoire: survival of the fittest? Immunol. Today 18, 77-82.
29. Lamb, C.A., Yewdell, J.W., Bennink, J.R., and Cresswell, P. (1991). Invariant chain targets HLA clas II molecules to acidic endosomes containing internalized influenza virus. Proc. Natl. Acad. Sci. USA 88, 5998-6002.
30. Lampson, L.A., and Levy, R. (1980). Two populations of la-like molecules on a human B cell line. J. Immunol. 125, 293-299.
31. Lindstedt, R., Liljedahl, M., Péléraux, A., Peterson, P.A., and Karlsson, L. (1995). The MHC class II molecule H2-M is targeted to an endosomal compartment by a tyrosine-based targeting motif. Immunity 3, 561-572.
32. Mane, S.M., Marzella, L., Bainton, D.F., Holt, V.K., Cha, Y., Hildreth, J.E., and August, J.T. (1989). Purification and characterization of human lysosomal glycoproteins. Arch. Biochem. Biophys. 268, 360-378.
33. Maric, M.A., Taylor, M.D., and Slum, J.S. (1994). Endosomal aspartic proteinases are required for invariant chain processing. Proc. Natl. Acad. Sci. USA 91, 2171-2175.
34. Marks, M.S., Germain, R.N., and Bonifacino, J.S. (1995a). Transient aggregation of major histocompatibility complex class II chains during assembly in normal spleen cells. J. Biol. Chem. 270, 10475-10481.
35. Marks, M.S., Roche, P.A., van Donselaar, E., Woodruff, L., Peters, P.J., and Bonifacino, J.S. (1995b). A lysosomal targeting signal in the cytoplasmic tail of the β chain directs HLA-DM to MHC class II compartments. J. Cell Biol. 131, 351-369.
36. Max, H., Halder, T., Kropshofer, H., Kalbus, M., Müller, C.A., and Kaibacher, H. (1993). Characterization of peptides bound to extracellular and intracellular HLA-DR1 molecules. Hum. Immunol. 38, 193-200.
37. Morris, P., Shaman, J., Attaya, M., Amaya, M., Goodman, S., Bergman, C., Monaco, J.J., and Mellins, E. (1994). An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 368, 551-554.
38. Pierre, P., Denzin, L.K., Hammond, C., Drake, J.R., Amigorena, S., Cresswell, P., and Mellman, I. (1996). HLA-DM is localized to conventional and unconventional MHC class II-containing endocytic compartments. Immunity, 4, 229-239.
39. Ramachandra, L., Kovats, S., Eastman, A., and Rudensky, A.Y. (1996). Variation in HLA-DM expression influences conversion of MHC class II αβclass II-associated invariant chain peptide complexes to mature peptide bound class II αβ dimers in a normal B cell line. J. Immunol. 156, 2196-2204.
40. Riberdy, J.M., Newcomb, J.R., Surman, M.J., Barbosa, J.A., and Cresswell, P. (1992). HLA-DRmolecules from an antigen-processing mutant cell line are associated with invariant chain peptides. Nature 360, 474-477.
41. Riese, R.J., Wolf, P.R., Brömme, D., Natkin, L.R., Villadangos, J.A., Ploegh, H.L., and Chapman, H.A. (1996). Essential role for cathepsin S in MHC class II-associated invariant chain processing and peptide loading. Immunity 4, 357-366.
42. Roche, P.A., and Cresswell, P. (1990). Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 345, 615-618.
43. Roche, P.A., Marks, M.S., and Cresswell, P. (1991). Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature 354, 392-394.
44. Sadegh-Nasseri, S., and Germain, R.N. (1991). A role for peptide in determining MHC class II structure. Nature 353, 167-170.
45. Sadegh-Nasseri, S., Stern, L.J., Wiley, D.C., and Germain, R.N. (1994). MHC class II function preserved by low-affinity peptide interactions preceding stable binding. Nature 370, 647-650.
46. Sanderson, F., Kleijmeer, M., Kelly, A., Verwoerd, D., Tulp, A., Neefjes, J., Geuze, H.J., and Trowsdale, J. (1994). Accumulation of HLA-DM, a regulator of antigen presentation, in MHC class II compartments. Science 266, 1566-1569.
47. Sanderson, F., Thomas, C., Neefjes, J., and Trowsdale, J. (1996). Association between HLA-DM and HLA-DR in vivo. Immunity 4, 87-96.
48. Schafer, P.H., Green, J.M., Malapati, S., Gu, L., and Pierce, S.K. (1996). HLA-DM is present in one-fifth the amount of HLA-DR in the class II peptide loading compartment where it associates with leupeptin-induced peptide (LIP)-HLA-DR complexes. J. Immunol. 157, 5487-5495.
49. Schaiff, W.T., Hruska, K.A., Jr., McCourt, D.W., Green, M., and Schwartz, B.D. (1992). HLA-DR associates with specific stress proteins and is retained in the endoplasmic reticulum in invariant chain-negative cells. J. Exp. Med. 176, 657-666.
50. Sette, A., Southwood, S., Miller, J., and Apella, E. (1995). Binding of major histocompatibility complex class II to the invariant chain-derived peptide, CLIP, is regulated by allelic polymorphism in class II. J. Exp. Med. 181, 677-683.
51. Sherman, M.A., Weber, D.A., and Jensen, P. (1995). DM enhances peptide binding to class II MHC by release of invariant chain-derived peptides. Immunity 3, 197-205.
52. Sloan, V.S., Cameron, P., Porter, G., Gammon, M., Amaya, M., Mellins, E., and Zaller, D.M. (1995). Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 375, 802-806.
53. Stam, N.J., Vroom, T.M., Peters, P.J., Pastoors, E.B., and Ploegh, H.L. (1990). HLA-A-and HLA-B-specific monoclonal antibodies reactive with free heavy chains in western blots, in formalin-fixed, paraffin-embedded tissue sections and in cryo-immuno-electron microscopy. Int. Immunol. 2, 113-125.
54. Stebbins, C.S., Peterson, M.E., Suh, W.M., and Sant, A.J. (1996). DM-mediated release of a naturally occurring invariant chain degradation intermediate from MHC class II molecules. J. Immunol. 157, 4892-4898.
55. Stern, L.J., and Wiley, D.C. (1992). The human MHC class II protein HLA-DR1 assembles as empty αβ-heterodimers in the absence of antigenic peptide. Cell 68, 465-477.
56. Tulp, A., Verwoerd, D., Dobberstein, B., Ploegh, H.L., and Pieters, J. (1994). Isolation and characterization of the intracellular MHC class II compartment. Nature 369, 120-126.
57. Urban, R.G., Chicz, R.M., and Strominger, J.L. (1994). Selective release of some invariant chain-derived peptides from HLA-DR1 molecules at endosomal pH. J. Exp. Med. 180, 751-755.
58. van Ham, S.M., Grüneberg, U., Malcharek, G., Bröker, I., Melms, A., and Trowsdale, J. (1996). Human histocompatibility leukocyte antigen (HLA)-DM edits peptides presented by HLA-DR according to their ligand binding motifs. J. Exp. Med. 184, 2019-2024.
59. Verreck, F.A.W., Vermeulen, C., Poel, A.v.d., Jorritsma, P., Amons, R., Coligan, J.E., Drijfthout, J.W., and Koning, F. (1996). The generation of SDS-stable HLA-DR dimers is independent of efficient peptide binding. Int. Immunol. 8, 397-404.
60. Viville, S., Neefjes, J., Lotteau, V., Dierich, A., Lemeur, M., Ploegh, H., Benoist, C., and Mathis, D. (1993). Mice lacking the MHC class II-associated invariant chain. Cell 72, 635-648.
61. Vogt, A.B., Kropshofer, H., Kalbacher, H., Kalbus, M., Rammensee, H.-G., Coligan, J.E., and Martin, R. (1994). Ligand motifs of HLA-DRB5*0101 and DRB1*1501 molecules delineated from self-peptides. J. Immunol. 153, 1665-1673.
62. Vogt, A.B., Stern, L.J., Amshoff, C., Dobberstein, B., Hämmerling, G.J., and Kropshofer, H. (1995). Interference of distinct invariant chain regions with superantigen contact area and antigenic peptide binding groove of HLA-DR. J. Immunol. 155, 4757-4765.
63. Vogt, A.B., Kropshofer, H., Moldenhauer, G., and Hämmerling, G.J. (1996). Kinetic analysis of peptide loading onto HLA-DR molecules mediated by HLA-DM. Proc. Natl. Acad. Sci. USA 93, 9724-9729.
64. Weber, D.A., Evavold, B.D., and Jensen, P.E. (1996). Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 274, 618-620.