Stoichiometry of HLA class II-invariant chain oligomers

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Koch, Norbert ^a   Zacharias, Martin ^b   König, Angelika ^a   Temme, Sebastian ^a   Neumann, Jürgen ^a   Springer, Sebastian ^c  

^a UNIVERSITY OF BONN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c JACOBS UNIVERSITY BREMEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; HLA ANTIGEN CLASS 2; HLA ANTIGEN CLASS 2 INVARIANT CHAIN; OLIGOMER; UNCLASSIFIED DRUG; B LYMPHOCYTE ANTIGEN; HLA D ANTIGEN; HLA DP ANTIGEN; HLA DQ ANTIGEN; HLA DR ANTIGEN;

ANIMAL CELL; ANTIGEN STRUCTURE; ARTICLE; CHEMICAL BINDING; CHEMICAL COMPOSITION; COMPLEX FORMATION; DENSITY GRADIENT; HUMAN; HUMAN CELL; NONHUMAN; STOICHIOMETRY; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; ANIMAL; ANTIGEN PRESENTING CELL; CELL FRACTIONATION; CELL STRAIN COS1; CERCOPITHECUS; CHEMICAL STRUCTURE; CHEMISTRY; IMMUNOLOGY; INVARIANT CHAIN; METABOLISM; MOLECULAR GENETICS; OSMOLARITY; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; TUMOR CELL LINE; ULTRACENTRIFUGATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; CELL FRACTIONATION; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-D ANTIGENS; HLA-DP ANTIGENS; HLA-DQ ANTIGENS; HLA-DR ANTIGENS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OSMOLAR CONCENTRATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; ULTRACENTRIFUGATION;

EID: 79952052281     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017257     Document Type: Article

References (58)

1. Marks MS, Blum JS, Cresswell P, (1990) Invariant Chain Trimers Are Sequestered in the Rough Endoplasmic Reticulum in the Absence of Association with HLA Class II Antigens. J Cell Biol 111: 839-855.
2. Park S-J, Sadegh-Nasser S, Wiley DC, (1995) 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 USA 92: 11289-11293.
3. Jasanoff A, Wagner G, Wiley DC, (1998) Structure of a trimeric domain of the MHC class II-associated chaperonin and targeting protein Ii. EMBO J 17: 6812-6818.
4. Romagnoli P, Germain RN, (1994) 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 180: 1107-1113.
5. Avva RR, Cresswell P, (1994) In Vivo and In Vitro Formation and Dissociation of HLA-DR Complexes with Invariant Chain-Derived Peptides. Immunity 1: 763-774.
6. Ghosh P, Amaya M, Mellins E, Wiley D C, (1995) The structure of an intermediate in class II MHC maturation: CLIP bound to HLA-DR3. Nature 378: 457-462.
7. Siebenkotten IM, Carstens C, Koch N, (1998) Identification of a sequence that mediates promiscuous binding of invariant chain to major histocompatibility complex class II allotypes. J Immunol 160: 3355-3362.
8. Ashman JB, Miller J, (1999) A role for the transmembrane domain in the trimerization of the MHC Class II-associates invariant chain. J Immunol 163: 2704-2712.
9. Castellino F, Han R, Germain RN, (2001) The transmembrane segment of invariant chain mediates binding to MHC class II molecules in a CLIP-independent manner. Eur J Immunol 31: 841-850.
10. Neumann J, Koch N, (2006) A novel domain on HLA-DRβ chain regulates the chaperone role of invariant chain. J Cell Sci 119: 4207-4212.
11. King G, Dixon AM, (2010) Evidence for role of transmembrane helix-helix interactions in the assembly of the class II major histocompatibility complex. Mol Biosystems 6: 1650-1661.
12. Roche PA, Marks MS, Cresswell P, (1991) Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature 354: 392-394.
13. Lamb CA, Cresswell P, (1992) Assembly and transport properties of invariant chain trimers and HLA-DR invariant chain complexes. J Immunol 148: 3478-3482.
14. Cresswell P, (1994) Assembly, Transport, and Function of MHC Class II Molecules. Ann Rev Immunol 12: 259-293.
15. Jones PP, Murphy DB, McDevitt HO, (1978) Two-gene control of the expression of a murine Ia antigen. J Exp Med 148: 925-939.
16. Arunachalam B, Lamb CA, Cresswell P, (1994) Transport properties of free and MHC class II-associates oligomers containing different isoforms of human invariant chain. Int Immunol 6: 439-451.
17. Neumann J, Schach N, Koch N, (2001) Glycosylation Signals that Separate the Trimerization from the MHC Class II-binding Domain Control Intracellular Degradation of Invariant Chain. J Biol Chem 276: 13469-13475.
18. Machamer CE, Cresswell P, (1982) Biosynthesis and glycosylation of the invariant chain associates with HLA-DR antigens. J Immunol 129: 2564-2569.
19. Jasanoff A, Song S, Dinner AR, Wagner G, Wiley DC, (1999) One of Two Unstructured Domains of Ii Becomes Ordered in Complexes with MHC Class II Molecules. Immunity 10: 761-768.
20. Hayes SM, Love PE, (2006) Stoichiometry of the murine γδ T cell receptor. J Exp Med 203: 47-52.
21. Schamel WWA, Reth M, (2000) Monomeric and Oligomeric Complexes of the B Cell Antigen Receptor. Immunity 13: 5-14.
22. Germain RN, Rinker AG Jr, (1993) Peptide binding inhibits protein aggregation of invariant-chain free class II dimers and promotes surface expression of occupied molecules. Nature 363: 725-728.
23. Verreck FA, Fargeas CA, Hämmerling GJ, (2001) Conformational alterations during biosynthesis of HLA-DR3 molecules controlled by invariant chain and HLA-DM. Eur J Immunol 31: 1029-1036.
24. Koch N, Hämmerling GJ, (1986) The HLA-D-associated invariant chain binds palmitic acid at the cysteine adjacent to the membrane segment. J Biol Chem 261: 3434-3440.
25. Lennon-Dumenil AM, Roberts RA, Valentijn K, Driessen C, Overkleeft HS, et al. (2001) The p41 isoform of invariant chain is chaperoned for cathepsin L. EMBO J 20: 4055-4064.
26. Rodionov DG, Höning S, Silye A, Kongsvik TL, von Figura K, et al. (2002) Structural requirements for interactions between leucine-sorting signals and clathrin-associated adaptor protein complex AP3. J Biol Chem 277: 47436-47443.
27. Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, et al. (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nature Med 13: 587-596.
28. Faure-Andre G, Vargas P, Yuseff MI, Heuze M, Diaz J, et al. (2008) Regulation of dendritic cell migration by CD74, the MHC class II-associated invariant chain. Science 322: 1705-1710.
29. Ye L, Lui X, Rout SN, Li Z, Yan Y, et al. (2008) The MHC class II-associated invariant chain interacts with the neonatal Fc gamma receptor and modulates its trafficking to endosomal/lysosomal compartments. J Immunol 181: 2572-2585.
30. Schwartz V, Lue H, Kraemer S, Korbiel J, Krohn R, et al. (2009) A functional heteromeric MIF receptor formed by CD74 and CXCR4. FEBS Lett 583: 2749-2757.
31. Grüneberg U, Rich T, Roucard C, van Ham M, Charron D, et al. (1997) Two widely used anti-DR monoclonal antibodies bind to an intracellular C-terminal epitope. Hum Immunol 53: 34-38.
32. Dixon AM, Stanley BJ, Matthews EE, Dawson JP, Engelman DM, (2006) Invariant chain transmembrane domain trimerization: a step in MHC class II assembly. Biochemistry 45: 5228-5234.
33. Marks MS, Germain RN, Bonifacino JS, (1995) Transient Aggregation of Major Histocompatibility Complex Class II Chains during Assembly in Normal Spleen Cells. J Biol Chem 18: 10475-10481.
34. Bonnerot C, Marks MS, Robertson EJ, Bikoff EK, Germain RN, et al. (1994) Association with BiP and aggregation of class II MHC molecules synthesized in the absence of invariant chain. EMBO J 13: 934-944.
35. Cresswell P, (1996) Invariant Chain Structure and MHC Class II Function. Cell 84: 505-507.
36. Sung E, Jones PP, (1981) The invariant chain of murine Ia antigens: Its glycosylation, abundance and subcellular localisation. Molecular Immunology 18: 899-913.
37. Graf L, Koch N, Schirrmacher V, (1985) Expression of Ia Antigens in a Murine T-Lymphoma Variant. Mol Immunol 22: 1371-1377.
38. Pollet RJ, Haase BA, Standaert ML, (1981) Characterization of Detergent-solubilized Membrane Proteins. J Biol Chem 256: 12118-12126.
39. Jasanoff A, Park S-J, Wiley DC, (1995) Direct observation of disordered regions in the major histocompatility complex class II-associated invariant chain. Proc Natl Acad Sci USA 92: 9900-9904.
40. Mitra AK, Celia H, Ren G, Luz JG, Wilson IA, et al. (2004) Supine orientation of a murine MHC class I molecule on the membrane bilayer. Current Biol 14: 718-724.
41. Hofmann MW, Honing S, Rodionov D, Dobberstein B, von Figura K, et al. (1999) The leucine-based sorting motif in the cytoplasmic domain of the invariant chain are recognized by the clathrin adaptors AP1 and AP2 and their medium chains. J Biol Chem 274: 36153-36158.
42. Arneson LS, Miller J, (1995) Efficient Endosomal Localization of Major Histocompatibility Complex Class II-Invariant Chain Complexes Requires Multimerization of the Invariant Chain Targeting Sequence. J Cell Biol 129: 1217-1228.
43. Nordeng TW, Gregers TF, Kongsvik TL, Meresse S, Gorvel JP, et al. (2002) The cytoplasmic tail of invariant chain regulates endosome fusion and morphology. Mol Biol Cell 13: 1846-1856.
44. Springer S, Spang A, Schekman R, (1999) A primer on vesicle budding. Cell 97: 145-148.
45. Lee MCS, Miller EA, (2007) Molecular mechanism of COPII vesicle formation. Semin Cell Dev Biol 18: 424-434.
46. Leng L, Bucalla R, (2006) Insight into the biology of macrophage migration inhibitory factor (MIF) revealed by the cloning of its cell surface receptor. Cell Research 16: 162-168.
47. Zhong G, Castellino F, Romagnoli P, Germain RN, (1996) Evidence that binding site occupancy is necessary and sufficient for effective major histocompatibility complex (MHC) class II transport through the secretory pathway redefines the primary function of class II-associates invariant chain peptides (CLIP). J Exp Med 184: 2061-2066.
48. Koch N, McLellan AD, Neumann J, (2007) A revised model for invariant chain-mediated assembly of major histocompatibility complex class II assembly and isotype pairing. TiBS 32: 532-537.
49. Anderson KS, Cresswell P, (1994) A role for calnexin (IP90) in the assembly of class II MHC molecules. EMBO J 13: 675-682.
50. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: An environment for comparative protein modelling. Electrophoresis 18: 2714-2723.
51. Case DA, Cheatham TE, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
52. Neumann J, (2005) Novel antibody tags from the rat lysosomal protein RT1.DM for immunodetection of recombinant proteins. J Immunol Meth 301: 66-76.
53. Adams TE, Bodmer JG, Bodmer WF, (1983) Production and characterization of monoclonal antibodies recognizing the a-chain subunits of human Ia alloantigens. Immunol 50: 613-624.
54. Pesando JM, Graf L, (1986) Differential expression of HLA-DR,-DQ, and-DP antigens on malignant B cells. J Immunol 136: 4311-4318.
55. Watanabe M, Suzuki T, Taniguchi M, Shinohara N, (1983) Monoclonal anti-Ia murine alloantibodies crossreactive with the Ia-homologous of other mammalian species including humans. Transplantation 36: 712-718.
56. Morris P, Shaman J, Attaya M, Amaya M, Goodman S, et al. (1994) An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 368: 551-554.
57. Koch S, Schultz A, Koch N, (1987) The production of recombinant HLA-DR beta and invariant chain polypeptides by cDNA expression in E. coli. J Immunol Meth 103: 211-220.
58. Wraight CJ, van Endert P, Möller P, Lipp J, Ling NR, et al. (1990) Human major histocompatibility complex class II invariant chain is expressed on the cell surface. J Biol Chem 265: 5787-5792.