HLA-DM: Arbiter conformationis

Immunology

Volumn 138, Issue 2, 2013, Pages 85-92

  Ferrante, Andrea ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

Antigen presentation; Epitopes; HLA DM; Ligand receptor interaction; MHCII

Indexed keywords

EPITOPE; HLA DM ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ADAPTIVE IMMUNITY; ANTIGEN FUNCTION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; CATALYSIS; CD4+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL SELECTION; CELL SURVIVAL; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENDOSOME; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HYDROGEN BOND; NONHUMAN; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW;

ANTIGEN PRESENTATION; BINDING SITES; CD4-POSITIVE T-LYMPHOCYTES; ENDOSOMES; HLA-D ANTIGENS; HUMANS; PEPTIDES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84872554985     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/imm.12030     Document Type: Review

References (69)

1. Benacerraf B. Role of MHC gene products in immune regulation. Science 1981; 212:1229-38.
2. Watts C, Powis S. Pathways of antigen processing and presentation. Rev Immunogenet 1999; 1:60-74.
3. Koch N, Zacharias M, Konig A, Temme S, Neumann J, Springer S. Stoichiometry of HLA class II-invariant chain oligomers. PLoS ONE 2011; 6:e17257.
4. Roche PA, Marks MS, Cresswell P. Formation of a nine-subunit complex by HLA class II glycoproteins and the invariant chain. Nature 1991; 354:392-4.
5. Neefjes J, Jongsma ML, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 2011; 11:823-36.
6. Jardetzky TS, Brown JH, Gorga JC, Stern LJ, Urban RG, Strominger JL, et al. Crystallographic analysis of endogenous peptides associated with HLA-DR1 suggests a common, polyproline II-like conformation for bound peptides. Proc Natl Acad Sci USA 1996; 93:734-8.
7. Nelson CA, Viner NJ, Unanue ER. Appreciating the complexity of MHC class II peptide binding: lysozyme peptide and I-Ak. Immunol Rev 1996; 151:81-105.
8. Sadegh-Nasseri S, Germain RN. A role for peptide in determining MHC class II structure. Nature 1991; 353:167-70.
9. Belmares MP, Busch R, Mellins ED, McConnell HM. Formation of two peptide/MHC II isomers is catalyzed differentially by HLA-DM. Biochemistry 2003; 42:838-47.
10. Kasson PM, Rabinowitz JD, Schmitt L, Davis MM, McConnell HM. Kinetics of peptide binding to the class II MHC protein I-Ek. Biochemistry 2000; 39:1048-58.
11. Lovitch SB, Unanue ER. Conformational isomers of a peptide-class II major histocompatibility complex. Immunol Rev 2005; 207:293-313.
12. Schmitt L, Kratz JR, Davis MM, McConnell HM. Catalysis of peptide dissociation from class II MHC-peptide complexes. Proc Natl Acad Sci USA 1999; 96:6581-6.
13. Kenty G, Martin WD, Van Kaer L, Bikoff EK. MHC class II expression in double mutant mice lacking invariant chain and DM functions. J Immunol. 1998; 160:606-14.
14. Hansen TH, Lybarger L, Yu L, Mitaksov V, Fremont DH. Recognition of open conformers of classical MHC by chaperones and monoclonal antibodies. Immunol Rev 2005; 207:100-11.
15. Zarutskie JA, Sato AK, Rushe MM, Chan IC, Lomakin A, Benedek GB, et al. A conformational change in the human major histocompatibility complex protein HLA-DR1 induced by peptide binding. Biochemistry 1999; 38:5878-87.
16. Rabinowitz JD, Vrljic M, Kasson PM, Liang MN, Busch R, Boniface JJ, et al. Formation of a highly peptide-receptive state of class II MHC. Immunity 1998; 9:699-709.
17. Joshi RV, Zarutskie JA, Stern LJ. A three-step kinetic mechanism for peptide binding to MHC class II proteins. Biochemistry 2000; 39:3751-62.
18. Natarajan SK, Assadi M, Sadegh-Nasseri S. Stable peptide binding to MHC class II molecule is rapid and is determined by a receptive conformation shaped by prior association with low affinity peptides. J Immunol 1999; 162:4030-6.
19. Sato AK, Zarutskie JA, Rushe MM, Lomakin A, Natarajan SK, Sadegh-Nasseri S, et al. Determinants of the peptide-induced conformational change in the human class II major histocompatibility complex protein HLA-DR1. J Biol Chem 2000; 275:2165-73.
20. Carven GJ, Stern LJ. Probing the ligand-induced conformational change in HLA-DR1 by selective chemical modification and mass spectrometric mapping. Biochemistry 2005; 44:13625-37.
21. Carven GJ, Chitta S, Hilgert I, Rushe MM, Baggio RF, Palmer M, et al. Monoclonal antibodies specific for the empty conformation of HLA-DR1 reveal aspects of the conformational change associated with peptide binding. J Biol Chem 2004; 279:16561-70.
22. Painter CA, Cruz A, Lopez GE, Stern LJ, Zavala-Ruiz Z. Model for the peptide-free conformation of class II MHC proteins. PLoS ONE 2008; 3:e2403.
23. Yaneva R, Springer S, Zacharias M. Flexibility of the MHC class II peptide binding cleft in the bound, partially filled, and empty states: a molecular dynamics simulation study. Biopolymers 2009; 91:14-27.
24. Denzin LK, Robbins NF, Carboy-Newcomb C, Cresswell P. Assembly and intracellular transport of HLA-DM and correction of the class II antigen-processing defect in T2 cells. Immunity 1994; 1:595-606.
25. Morris P, Shaman J, Attaya M, Amaya M, Goodman S, Bergman C, et al. An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 1994; 368:551-4.
26. Mosyak L, Zaller DM, Wiley DC. The structure of HLA-DM, the peptide exchange catalyst that loads antigen onto class II MHC molecules during antigen presentation. Immunity 1998; 9:377-83.
27. Denzin LK, Cresswell P. HLA-DM induces CLIP dissociation from MHC class II αβ dimers and facilitates peptide loading. Cell 1995; 82:155-65.
28. Sloan VS, Cameron P, Porter G, Gammon M, Amaya M, Mellins E, et al. Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 1995; 375:802-6.
29. Weber DA, Evavold BD, Jensen PE. Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 1996; 274:618-20.
30. Vogt AB, Kropshofer H, Moldenhauer G, Hammerling GJ. Kinetic analysis of peptide loading onto HLA-DR molecules mediated by HLA-DM. Proc Natl Acad Sci USA 1996; 93:9724-9.
31. Denzin LK, Hammond C, Cresswell P. HLA-DM interactions with intermediates in HLA-DR maturation and a role for HLA-DM in stabilizing empty HLA-DR molecules. J Exp Med 1996; 184:2153-65.
32. Kropshofer H, Arndt SO, Moldenhauer G, Hammerling GJ, Vogt AB. HLA-DM acts as a molecular chaperone and rescues empty HLA-DR molecules at lysosomal pH. Immunity 1997; 6:293-302.
33. vogt AB, Moldenhauer G, Hammerling GJ, Kropshofer H. HLA-DM stabilizes empty HLA-DR molecules in a chaperone-like fashion. Immunol Lett 1997; 57:209-11.
34. Schafer PH, Green JM, Malapati S, Gu L, Pierce SK. 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 1996; 157:5487-95.
35. Fremont DH, Crawford F, Marrack P, Hendrickson WA, Kappler J. Crystal structure of mouse H2-M. Immunity 1998; 9:385-93.
36. Sanderson F, Thomas C, Neefjes J, Trowsdale J. Association between HLA-DM and HLA-DR in vivo. Immunity 1996; 4:87-96.
37. Ullrich HJ, Doring K, Gruneberg U, Jahnig F, Trowsdale J, van Ham SM. Interaction between HLA-DM and HLA-DR involves regions that undergo conformational changes at lysosomal pH. Proc Natl Acad Sci USA 1997; 94:13163-8.
38. Doebele RC, Busch R, Scott HM, Pashine A, Mellins ED. Determination of the HLA-DM interaction site on HLA-DR molecules. Immunity 2000; 13:517-27.
39. Stratikos E, Mosyak L, Zaller DM, Wiley DC. Identification of the lateral interaction surfaces of human histocompatibility leukocyte antigen (HLA)-DM with HLA-DR1 by formation of tethered complexes that present enhanced HLA-DM catalysis. J Exp Med 2002; 196:173-83.
40. Davies MN, Lamikanra A, Sansom CE, Flower DR, Moss DS, Travers PJ. Identification of the HLA-DM/HLA-DR interface. Mol Immunol 2008; 45:1063-70.
41. Sant AJ, Beeson C, McFarland B, Cao J, Ceman S, Bryant PW, et al. Individual hydrogen bonds play a critical role in MHC class II: peptide interactions: implications for the dynamic aspects of class II trafficking and DM-mediated peptide exchange. Immunol Rev 1999; 172:239-53.
42. Bandyopadhyay A, Arneson L, Beeson C, Sant AJ. The relative energetic contributions of dominant P1 pocket versus hydrogen bonding interactions to peptide:class II stability: implications for the mechanism of DM function. Mol Immunol 2008; 45:1248-57.
43. Narayan K, Chou CL, Kim A, Hartman IZ, Dalai S, Khoruzhenko S, et al. HLA-DM targets the hydrogen bond between the histidine at position β81 and peptide to dissociate HLA-DR-peptide complexes. Nat Immunol 2007; 8:92-100.
44. Anderson MW, Gorski J. Cooperativity during the formation of peptide/MHC class II complexes. Biochemistry 2005; 44:5617-24.
45. McFarland BJ, Beeson C, Sant AJ. Cutting edge: a single, essential hydrogen bond controls the stability of peptide-MHC class II complexes. J Immunol 1999; 163:3567-71.
46. Stratikos E, Wiley DC, Stern LJ. Enhanced catalytic action of HLA-DM on the exchange of peptides lacking backbone hydrogen bonds between their N-terminal region and the MHC class II α-chain. J Immunol 2004; 172:1109-17.
47. Ferrante A, Gorski J. Cutting edge: HLA-DM-mediated peptide exchange functions normally on MHC class II-peptide complexes that have been weakened by elimination of a conserved hydrogen bond. J Immunol 2010; 184:1153-8.
48. Zhou Z, Callaway KA, Weber DA, Jensen PE. Cutting edge: HLA-DM functions through a mechanism that does not require specific conserved hydrogen bonds in class II MHC-peptide complexes. J Immunol 2009; 183:4187-91.
49. Chou CL, Sadegh-Nasseri S. HLA-DM recognizes the flexible conformation of major histocompatibility complex class II. J Exp Med 2000; 192:1697-706.
50. Painter CA, Negroni MP, Kellersberger KA, Zavala-Ruiz Z, Evans JE, Stern LJ. Conformational lability in the class II MHC 310 helix and adjacent extended strand dictate HLA-DM susceptibility and peptide exchange. Proc Natl Acad Sci USA 2011; 108:19329-34.
51. Anders AK, Call MJ, Schulze MS, Fowler KD, Schubert DA, Seth NP, et al. HLA-DM captures partially empty HLA-DR molecules for catalyzed removal of peptide. Nat Immunol 2011; 12:54-61.
52. Ferrante A, Anderson MW, Klug CS, Gorski J. HLA-DM mediates epitope selection by a "compare-exchange" mechanism when a potential peptide pool is available. PLoS ONE 2008; 3:e3722.
53. Horovitz A, Fersht AR. Strategy for analysing the co-operativity of intramolecular interactions in peptides and proteins. J Mol Biol 1990; 214:613-17.
54. Horovitz A, Fersht AR. Co-operative interactions during protein folding. J Mol Biol 1992; 224:733-40.
55. Ferrante A, Gorski J. Cooperativity of hydrophobic anchor interactions: evidence for epitope selection by MHC class II as a folding process. J Immunol 2007; 178:7181-9.
56. McFarland BJ, Katz JF, Sant AJ, Beeson C. Energetics and cooperativity of the hydrogen bonding and anchor interactions that bind peptides to MHC class II protein. J Mol Biol 2005; 350:170-83.
57. Ferrante A, Gorski J. A Peptide/MHCII conformer generated in the presence of exchange peptide is substrate for HLA-DM editing. Sci Rep 2012; 2:386.
58. de Kroon AI, McConnell HM. Enhancement of peptide antigen presentation by a second peptide. Proc Natl Acad Sci USA 1993; 90:8797-801.
59. de Kroon AI, McConnell HM. Kinetics and specificity of peptide-MHC class II complex displacement reactions. J Immunol 1994; 152:609-19.
60. Pedrazzini T, Sette A, Albertson M, Grey HM. Free ligand-induced DISSOCIATION of MHC-antigen complexes. J Immunol 1991; 146:3496-501.
61. Brooks AG, Campbell PL, Reynolds P, Gautam AM, McCluskey J. Antigen presentation and assembly by mouse I-Ak class II molecules in human APC containing deleted or mutated HLA DM genes. J Immunol 1994; 153:5382-92.
62. Stebbins CC, Loss GE, Elias CG, Chervonsky A, Sant AJ. The requirement for DM in class II-restricted antigen presentation and SDS-stable dimer formation is allele-dependent and species-dependent. J Exp Med 1995; 181:223-34.
63. Stebbins CC, Peterson ME, Suh WM, Sant AJ. DM-mediated release of a naturally occurring invariant chain degradation intermediate from MHC class II molecules. J Immunol 1996; 157:4892-8.
64. Weenink S, Averdunk H, Boston T, Boswarva V, Guery JC, Adorini L, et al. Impaired antigen presentation by murine I-Ad class II MHC molecules expressed in normal and HLA-DM-defective human B cell lines. Int Immunol 1997; 9:889-96.
65. + T cell maturation in BALB/c mice. J Immunol 2001; 166:5087-98.
66. Koonce CH, Wutz G, Robertson EJ, Vogt AB, Kropshofer H, Bikoff EK. DM loss in k haplotype mice reveals isotype-specific chaperone requirements. J Immunol 2003; 170:3751-61.
67. van Lith M, McEwen-Smith RM, Benham AM. HLA-DP, HLA-DQ, and HLA-DR have different requirements for invariant chain and HLA-DM. J Biol Chem 2010; 285:40800-8.
68. Busch R, Reich Z, Zaller DM, Sloan V, Mellins ED. Secondary structure composition and pH-dependent conformational changes of soluble recombinant HLA-DM. J Biol Chem 1998; 273:27557-64.
69. DeLano W. The PyMOL Molecular Graphics System. San Carlos, CA, USA 2002.