Crystal structure of a TAPBPR–MHC I complex reveals the mechanism of peptide editing in antigen presentation

Jiang, Jiansheng; Natarajan, Kannan; Boyd, Lisa F.; Morozov, Giora I.; Mage, Michael G.; Margulies, David H.

doi:10.1126/science.aao5154

Title: Crystal structure of a TAPBPR–MHC I complex reveals the mechanism of peptide editing in antigen presentation

Journal Article · Thu Oct 12 00:00:00 EDT 2017 · Science

DOI:https://doi.org/10.1126/science.aao5154· OSTI ID:1413322

;

; Mage, Michael G.;

Central to CD8+ T cell–mediated immunity is the recognition of peptide–major histocompatibility complex class I (p–MHC I) proteins displayed by antigen-presenting cells. Chaperone-mediated loading of high-affinity peptides onto MHC I is a key step in the MHC I antigen presentation pathway. However, the structure of MHC I with a chaperone that facilitates peptide loading has not been determined. We report the crystal structure of MHC I in complex with the peptide editor TAPBPR (TAP-binding protein–related), a tapasin homolog. TAPBPR remodels the peptide-binding groove of MHC I, resulting in the release of low-affinity peptide. Changes include groove relaxation, modifications of key binding pockets, and domain adjustments. This structure captures a peptide-receptive state of MHC I and provides insights into the mechanism of peptide editing by TAPBPR and, by analogy, tapasin.

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH)

OSTI ID:: 1413322

Journal Information:: Science, Vol. 358, Issue 6366; ISSN 0036-8075

Publisher:: AAAS

Country of Publication:: United States

Language:: ENGLISH

References (40)

Three-dimensional structure of H-2Dd complexed with an immunodominant peptide from human immunodeficiency virus envelope glycoprotein 120 Li, Hongmin; Natarajan, Kannan; Malchiodi, Emilio L. Journal of Molecular Biology, Vol. 283, Issue 1 https://doi.org/10.1006/jmbi.1998.2091	journal	October 1998
Post-processing intensity measurements at favourable dose values Diederichs, Kay; Junk, Michael Journal of Applied Crystallography, Vol. 42, Issue 1 https://doi.org/10.1107/S0021889808036716	journal	December 2008
H-2Dd exploits a four residue peptide binding motif Corr, M. Journal of Experimental Medicine, Vol. 178, Issue 6 https://doi.org/10.1084/jem.178.6.1877	journal	December 1993
F pocket flexibility influences the tapasin dependence of two differentially disease-associated MHC Class I proteins: Molecular immunology Abualrous, Esam T.; Fritzsche, Susanne; Hein, Zeynep European Journal of Immunology, Vol. 45, Issue 4 https://doi.org/10.1002/eji.201445307	journal	February 2015
Excess β2 microglobulin promoting functional peptide association with purified soluble class I MHC molecules Kozlowski, Steven; Takeshita, Toshiyuki; Boehncke, Wolf-Henning Nature, Vol. 349, Issue 6304 https://doi.org/10.1038/349074a0	journal	January 1991
Differential association of β2-microglobulin mutants with MHC class I heavy chains and structural analysis demonstrate allele-specific interactions Shields, M. Molecular Immunology, Vol. 36, Issue 9 https://doi.org/10.1016/S0161-5890(99)00077-2	journal	June 1999
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
The Binding of TAPBPR and Tapasin to MHC Class I Is Mutually Exclusive Hermann, Clemens; Strittmatter, Lisa M.; Deane, Janet E. The Journal of Immunology, Vol. 191, Issue 11 https://doi.org/10.4049/jimmunol.1300929	journal	October 2013
TAPBPR bridges UDP-glucose:glycoprotein glucosyltransferase 1 onto MHC class I to provide quality control in the antigen presentation pathway Neerincx, Andreas; Hermann, Clemens; Antrobus, Robin eLife, Vol. 6 https://doi.org/10.7554/eLife.23049	journal	April 2017
A Region of Tapasin That Affects L ^d Binding and Assembly Turnquist, Hēth R.; Vargas, Shanna E.; Reber, Adrian J. The Journal of Immunology, Vol. 167, Issue 8 https://doi.org/10.4049/jimmunol.167.8.4443	journal	October 2001
Analysis of interactions in a tapasin/class I complex provides a mechanism for peptide selection Chen, Mingnan; Bouvier, Marlene The EMBO Journal, Vol. 26, Issue 6 https://doi.org/10.1038/sj.emboj.7601624	journal	March 2007
Coupling between side chain interactions and binding pocket flexibility in HLA-B*44:02 molecules investigated by molecular dynamics simulations Ostermeir, Katja; Springer, Sebastian; Zacharias, Martin Molecular Immunology, Vol. 63, Issue 2 https://doi.org/10.1016/j.molimm.2014.07.021	journal	February 2015
Pathways of Antigen Processing Blum, Janice S.; Wearsch, Pamela A.; Cresswell, Peter Annual Review of Immunology, Vol. 31, Issue 1 https://doi.org/10.1146/annurev-immunol-032712-095910	journal	March 2013
A Point Mutation in HLA-A*0201 Results in Failure to Bind the TAP Complex and to Present Virus-Derived Peptides to CTL Peace-Brewer, Amy L.; Tussey, Lynda G.; Matsui, Masanori Immunity, Vol. 4, Issue 5 https://doi.org/10.1016/S1074-7613(00)80416-1	journal	May 1996
Dipeptides promote folding and peptide binding of MHC class I molecules Saini, S. K.; Ostermeir, K.; Ramnarayan, V. R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 38 https://doi.org/10.1073/pnas.1308672110	journal	September 2013
Interaction of TAPBPR, a tapasin homolog, with MHC-I molecules promotes peptide editing Morozov, Giora I.; Zhao, Huaying; Mage, Michael G. Proceedings of the National Academy of Sciences, Vol. 113, Issue 8 https://doi.org/10.1073/pnas.1519894113	journal	February 2016
Differential tapasin dependence of MHC class I molecules correlates with conformational changes upon peptide dissociation: A molecular dynamics simulation study Sieker, Florian; Straatsma, Tjerk P.; Springer, Sebastian Molecular Immunology, Vol. 45, Issue 14 https://doi.org/10.1016/j.molimm.2008.06.009	journal	August 2008
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
TAPBPR alters MHC class I peptide presentation by functioning as a peptide exchange catalyst Hermann, Clemens; van Hateren, Andy; Trautwein, Nico eLife, Vol. 4 https://doi.org/10.7554/eLife.09617	journal	October 2015
Polymorphism at Position 97 in MHC Class I Molecules Affects Peptide Specificity, Cell Surface Stability, and Affinity for β ₂ -Microglobulin Smith, Ruth A.; Myers, Nancy B.; Robinson, Melanie The Journal of Immunology, Vol. 169, Issue 6 https://doi.org/10.4049/jimmunol.169.6.3105	journal	September 2002
Effect of a tapasin mutant on the assembly of the mouse MHC class I molecule H2-K ^d Simone, Laura C.; Wang, Xiaojian; Tuli, Amit Immunology and Cell Biology, Vol. 88, Issue 1 https://doi.org/10.1038/icb.2009.59	journal	August 2009
Proofreading of Peptide—MHC Complexes through Dynamic Multivalent Interactions Thomas, Christoph; Tampé, Robert Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.00065	journal	February 2017
Molecular mechanism of peptide editing in the tapasin–MHC I complex Fisette, Olivier; Wingbermühle, Sebastian; Tampé, Robert Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19085	journal	January 2016
Disulfide by DesignTM: a computational method for the rational design of disulfide bonds in proteins Dombkowski, A. A. Bioinformatics, Vol. 19, Issue 14 https://doi.org/10.1093/bioinformatics/btg231	journal	September 2003
Insights into MHC Class I Peptide Loading from the Structure of the Tapasin-ERp57 Thiol Oxidoreductase Heterodimer Dong, Gang; Wearsch, Pamela A.; Peaper, David R. Immunity, Vol. 30, Issue 1 https://doi.org/10.1016/j.immuni.2008.10.018	journal	January 2009
Comparative molecular dynamics analysis of tapasin-dependent and -independent MHC class I alleles Sieker, F.; Springer, S.; Zacharias, M. Protein Science, Vol. 16, Issue 2 https://doi.org/10.1110/ps.062568407	journal	December 2006
Tapasin-related protein TAPBPR is an additional component of the MHC class I presentation pathway Boyle, Louise H.; Hermann, Clemens; Boname, Jessica M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 9 https://doi.org/10.1073/pnas.1222342110	journal	February 2013
Tapasin dependence of major histocompatibility complex class I molecules correlates with their conformational flexibility Garstka, Malgorzata Anna; Fritzsche, Susanne; Lenart, Izabela The FASEB Journal, Vol. 25, Issue 11 https://doi.org/10.1096/fj.11-190249	journal	November 2011
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Optimization of the MHC Class I Peptide Cargo Is Dependent on Tapasin Williams, Anthony P.; Peh, Chen Au; Purcell, Anthony W. Immunity, Vol. 16, Issue 4 https://doi.org/10.1016/S1074-7613(02)00304-7	journal	April 2002
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
The Interface Between Tapasin and MHC Class I Identification of Amino Acid Residues in Both Proteins That Influence Their Interaction Turnquist, Hēth R.; Vargas, Shanna E.; Schenk, Erin L. Immunologic Research, Vol. 25, Issue 3 https://doi.org/10.1385/IR:25:3:261	journal	January 2002
Peptide ligand structure influences the exchange of 2-microglobulin by cell surface K b Cook, J. R.; Myers, N. B.; Hansen, T. H. Molecular Immunology, Vol. 35, Issue 14-15 https://doi.org/10.1016/S0161-5890(98)00080-7	journal	October 1998
Crystal Structure of the HLA-DM–HLA-DR1 Complex Defines Mechanisms for Rapid Peptide Selection Pos, Wouter; Sethi, Dhruv K.; Call, Melissa J. Cell, Vol. 151, Issue 7 https://doi.org/10.1016/j.cell.2012.11.025	journal	December 2012
HLA-DM captures partially empty HLA-DR molecules for catalyzed removal of peptide Anders, Anne-Kathrin; Call, Melissa J.; Schulze, Monika-Sarah E. D. Nature Immunology, Vol. 12, Issue 1 https://doi.org/10.1038/ni.1967	journal	December 2010
Super-resolution biomolecular crystallography with low-resolution data Schröder, Gunnar F.; Levitt, Michael; Brunger, Axel T. Nature, Vol. 464, Issue 7292 https://doi.org/10.1038/nature08892	journal	April 2010
Present Yourself! By MHC Class I and MHC Class II Molecules Rock, Kenneth L.; Reits, Eric; Neefjes, Jacques Trends in Immunology, Vol. 37, Issue 11 https://doi.org/10.1016/j.it.2016.08.010	journal	November 2016
Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 Å resolution Saper, M. A.; Bjorkman, P. J.; Wiley, D. C. Journal of Molecular Biology, Vol. 219, Issue 2 https://doi.org/10.1016/0022-2836(91)90567-P	journal	May 1991
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007

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