Disruption of Hydrogen Bonds between Major Histocompatibility Complex Class II and the Peptide N-Terminus Is Not Sufficient to Form a Human Leukocyte Antigen-DM Receptive State of Major Histocompatibility Complex Class II

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Schulze, Monika Sarah E D ^a   Anders, Anne Kathrin ^a,b   Sethi, Dhruv K ^a   Call, Melissa J ^c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCYLLYSYLGLUAMINYLASPARAGINYLCYSTEINYLLEUCYLLYSYLLEUCYLALANINETHREONYLLYSINE DINITROPHENOL; HEMAGGLUTININ; HLA DM ANTIGEN; HLA DR1 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; POLYPEPTIDE; PROLYLLYSYLTHREONYLVALYLLYSYLGLUTAMYLASPARAGINYLTHREONYLLEUCYLLYSYLLEUCYLALANYLHREONINE; PROLYLLYSYLTHREONYLVALYLLYSYLGLUTAMYLCYSTEINYLTHREONYLLEUCYLLYSYLLEUCYLALANYLHREONINE; PROLYLLYSYLTYROSYLVALYLLYSYLGLUAMINYLASPARAGINYLCYSTEINYLLEUCYLLYSYLLEUCYLALANINETHREONINE; PROLYLLYSYLTYROSYLVALYLLYSYLGLUAMINYLASPARAGINYLCYSTEINYLLEUCYLLYSYLLEUCYLALANINETHREONYLLYSYL DINITROPHENOL; PROLYLLYSYLVALYLVALYLLYSYLGLUAMINYLASPARAGINYLCYSTEINYLLEUCYLLYSYLLEUCYLALANINETHREONYLLYSINE DINITROPHENOL; TYROSYLVALYLLYSYLASPARAGINYLCYSTEINYLLEUCYLLYSYLALANYLTHREONYLLYSINE DINITROPHENOL; UNCLASSIFIED DRUG; VALYLLYSYLGLUTAMINYLASPARAGINYLCYSTEINYLLEUCYLLYSYLLEUCYLALANYLTHREONYLLYSINE DINITROPHENOL; VALYLVALYLLYSYLGLUAMINYLASPARAGINYLCYSTEINYLLEUCYLLYSYLLEUCYLALANINETHREONYLLYSINE DINITROPHENOL;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN BINDING; ARTICLE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; HYDROGEN BOND; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SPODOPTERA FRUGIPERDA;

AMINO ACID SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; HEMAGGLUTININS; HLA-D ANTIGENS; HLA-DR1 ANTIGEN; HUMANS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; SURFACE PLASMON RESONANCE;

EID: 84880790787     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069228     Document Type: Article

References (46)

1. Kaiko GE, Horvat JC, Beagley KW, Hansbro PM, (2008) Immunological decision-making: how does the immune system decide to mount a helper T-cell response? Immunology 123: 326-338. doi:10.1111/j.1365-2567.2007.02719.x. PubMed: 17983439.
2. Mempel TR, Henrickson SE, Von Andrian UH, (2004) T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427: 154-159. doi:10.1038/nature02238. PubMed: 14712275.
3. Lanzavecchia A, Reid PA, Watts C, (1992) Irreversible association of peptides with class II MHC molecules in living cells. Nature 357: 249-252. doi:10.1038/357249a0. PubMed: 1375347.
4. Roche PA, Cresswell P, (1990) High-affinity binding of an influenza hemagglutinin-derived peptide to purified HLA-DR. J Immunol 144: 1849-1856. PubMed: 2307844.
5. Rabinowitz JD, Vrljic M, Kasson PM, Liang MN, Busch R, et al. (1998) Formation of a highly peptide-receptive state of class II MHC. Immunity 9: 699-709. doi:10.1016/S1074-7613(00)80667-6. PubMed: 9846491.
6. 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. doi:10.1038/363725a0. PubMed: 8515815.
7. 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. doi:10.1038/368551a0. PubMed: 8139689.
8. Roche PA, Cresswell P, (1990) Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 345: 615-618. doi:10.1038/345615a0. PubMed: 2190094.
9. 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. doi:10.1016/S1074-7613(94)80018-9. PubMed: 7895165.
10. Denzin LK, Cresswell P, (1995) HLA-DM induces CLIP dissociation from MHC class II alpha beta dimers and facilitates peptide loading. Cell 82: 155-165. doi:10.1016/0092-8674(95)90061-6. PubMed: 7606781.
11. Sloan VS, Cameron P, Porter G, Gammon M, Amaya M, et al. (1995) Mediation by HLA-DM of dissociation of peptides from HLA-DR. Nature 375: 802-806. doi:10.1038/375802a0. PubMed: 7596415.
12. Sherman MA, Weber DA, Jensen PE, (1995) DM enhances peptide binding to class II MHC by release of invariant chain-derived peptide. Immunity 3: 197-205. doi:10.1016/1074-7613(95)90089-6. PubMed: 7648393.
13. Belmares MP, Busch R, Wucherpfennig KW, McConnell HM, Mellins ED, (2002) Structural factors contributing to DM susceptibility of MHC class II/peptide complexes. J Immunol 169: 5109-5117. PubMed: 12391227.
14. Weber DA, Evavold BD, Jensen PE, (1996) Enhanced dissociation of HLA-DR-bound peptides in the presence of HLA-DM. Science 274: 618-620. doi:10.1126/science.274.5287.618. PubMed: 8849454.
15. Vogt AB, Kropshofer H, Moldenhauer G, Hämmerling GJ, (1996) Kinetic analysis of peptide loading onto HLA-DR molecules mediated by HLA-DM. Proc Natl Acad Sci U S A 93: 9724-9729. doi:10.1073/pnas.93.18.9724. PubMed: 8790398.
16. Zarutskie JA, Busch R, Zavala-Ruiz Z, Rushe M, Mellins ED, et al. (2001) The kinetic basis of peptide exchange catalysis by HLA-DM. Proc Natl Acad Sci U S A 98: 12450-12455. doi:10.1073/pnas.211439398. PubMed: 11606721.
17. Pos W, Sethi DK, Call MJ, Schulze MS, Anders AK, et al. (2012) Crystal Structure of the HLA-DM-HLA-DR1 Complex Defines Mechanisms for Rapid Peptide Selection. Cell 151: 1557-1568. doi:10.1016/j.cell.2012.11.025. PubMed: 23260142.
18. Chou CL, Sadegh-Nasseri S, (2000) HLA-DM recognizes the flexible conformation of major histocompatibility complex class II. J Exp Med 192: 1697-1706. doi:10.1084/jem.192.12.1697. PubMed: 11120767.
19. Anders AK, Call MJ, Schulze MS, Fowler KD, Schubert DA, et al. (2011) HLA-DM captures partially empty HLA-DR molecules for catalyzed removal of peptide. Nat Immunol 12: 54-61. doi:10.1038/ni.1967. PubMed: 21131964.
20. Sadegh-Nasseri S, Germain RN, (1991) A role for peptide in determining MHC class II structure. Nature 353: 167-170. doi:10.1038/353167a0. PubMed: 1653903.
21. Natarajan SK, Stern LJ, Sadegh-Nasseri S, (1999) Sodium dodecyl sulfate stability of HLA-DR1 complexes correlates with burial of hydrophobic residues in pocket 1. J Immunol 162: 3463-3470. PubMed: 10092802.
22. Sato AK, Zarutskie JA, Rushe MM, Lomakin A, Natarajan SK, et al. (2000) Determinants of the peptide-induced conformational change in the human class II major histocompatibility complex protein HLA-DR1. J Biol Chem 275: 2165-2173. doi:10.1074/jbc.275.3.2165. PubMed: 10636922.
23. Jardetzky TS, Brown JH, Gorga JC, Stern LJ, Urban RG, et al. (1996) Crystallographic analysis of endogenous peptides associated with HLA-DR1 suggests a common, polyproline II-like conformation for bound peptides. Proc Natl Acad Sci U S A 93: 734-738. doi:10.1073/pnas.93.2.734. PubMed: 8570625.
24. Brown JH, Jardetzky TS, Gorga JC, Stern LJ, Urban RG, et al. (1993) Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364: 33-39. doi:10.1038/364033a0. PubMed: 8316295.
25. Stratikos E, Wiley DC, Stern LJ, (2004) 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 alpha-chain. J Immunol 172: 1109-1117. PubMed: 14707085.
26. Narayan K, Chou CL, Kim A, Hartman IZ, Dalai S, et al. (2007) HLA-DM targets the hydrogen bond between the histidine at position beta81 and peptide to dissociate HLA-DR-peptide complexes. Nat Immunol 8: 92-100. doi:10.1038/nrg2061. PubMed: 17143275.
27. Zhou Z, Callaway KA, Weber DA, Jensen PE, (2009) Cutting edge: HLA-DM functions through a mechanism that does not require specific conserved hydrogen bonds in class II MHC-peptide complexes. J Immunol 183: 4187-4191. doi:10.4049/jimmunol.0901663. PubMed: 19767569.
28. Ferrante A, Gorski,. (2010) 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 184: 1153-1158. doi:10.4049/jimmunol.0902878. PubMed: 20038641.
29. Stern LJ, Brown JH, Jardetzky TS, Gorga JC, Urban RG, et al. (1994) Crystal structure of the human class II MHC protein HLA-DR1 complexed with an influenza virus peptide. Nature 368: 215-221. doi:10.1038/368215a0. PubMed: 8145819.
30. Ullrich HJ, Döring K, Grüneberg U, Jähnig F, Trowsdale J, et al. (1997) Interaction between HLA-DM and HLA-DR involves regions that undergo conformational changes at lysosomal pH. Proc Natl Acad Sci U S A 94: 13163-13168. doi:10.1073/pnas.94.24.13163. PubMed: 9371817.
31. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221. doi:10.1107/S0907444909052925. PubMed: 20124702.
32. Nicholson MJ, Moradi B, Seth NP, Xing X, Cuny GD, et al. (2006) Small molecules that enhance the catalytic efficiency of HLA-DM. J Immunol 176: 4208-4220. PubMed: 16547258.
33. McFarland BJ, Katz JF, Beeson C, Sant AJ, (2001) Energetic asymmetry among hydrogen bonds in MHC class II*peptide complexes. Proc Natl Acad Sci U S A 98: 9231-9236. doi:10.1073/pnas.151131498. PubMed: 11470892.
34. Painter CA, Negroni MP, Kellersberger KA, Zavala-Ruiz Z, Evans JE, et al. (2011) Conformational lability in the class II MHC 310 helix and adjacent extended strand dictate HLA-DM susceptibility and peptide exchange. Proc Natl Acad Sci U S A 108: 19329-19334. doi:10.1073/pnas.1108074108. PubMed: 22084083.
35. Hammer J, Belunis C, Bolin D, Papadopoulos J, Walsky R, et al. (1994) High-affinity binding of short peptides to major histocompatibility complex class II molecules by anchor combinations. Proc Natl Acad Sci U S A 91: 4456-4460. doi:10.1073/pnas.91.10.4456. PubMed: 8183931.
36. Doebele RC, Busch R, Scott HM, Pashine A, Mellins ED, (2000) Determination of the HLA-DM interaction site on HLA-DR molecules. Immunity 13: 517-527. doi:10.1016/S1074-7613(00)00051-0. PubMed: 11070170.
37. Pashine A, Busch R, Belmares MP, Munning JN, Doebele RC, et al. (2003) Interaction of HLA-DR with an acidic face of HLA-DM disrupts sequence-dependent interactions with peptides. Immunity 19: 183-192. doi:10.1016/S1074-7613(03)00200-0. PubMed: 12932352.
38. Stratikos E, Mosyak L, Zaller DM, Wiley DC, (2002) 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 196: 173-183. doi:10.1084/jem.20020117. PubMed: 12119342.
39. Denzin LK, Hammond C, 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. doi:10.1084/jem.184.6.2153. PubMed: 8976171.
40. Kropshofer H, Vogt AB, Moldenhauer G, Hammer J, Blum JS, et al. (1996) Editing of the HLA-DR-peptide repertoire by HLA-DM. EMBO J 15: 6144-6154. PubMed: 8947036.
41. van Ham SM, Grüneberg U, Malcherek G, Bröker I, Melms A, et al. (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. doi:10.1084/jem.184.5.2019. PubMed: 8920889.
42. Otwinowski Z, Minor W, (1997) Processing of X-ray diffraction data collected in oscillation mode. Macromol Crystallogr Pt A 276: 307-326. doi:10.1016/S0076-6879(97)76066-X.
43. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674. doi:10.1107/S0021889807021206. PubMed: 19461840.
44. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21. doi:10.1107/S1744309109042018. PubMed: 20057044.
45. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132. doi:10.1107/S0907444904019158. PubMed: 15572765.
46. Brünger AT, (1992) Free R-Value- a Novel Statistical Quantity for Assessing the Accuracy of Crystal-Structures. Nature 355: 472-475. doi:10.1038/355472a0. PubMed: 18481394.