3pgd › Citations

Bidirectional binding of invariant chain peptides to an MHC class II molecule.

Günther S, Schlundt A, Sticht J, Roske Y, Heinemann U, Wiesmüller KH, Jung G, Falk K, Rötzschke O, Freund C
Proc Natl Acad Sci U S A 107 22219-24 (2010)
Related entries: 3pdo, 3pgc

Cited: 50 times
EuropePMC logo PMID: 21115828

Abstract

T-cell recognition of peptides bound to MHC class II (MHCII) molecules is a central event in cell-mediated adaptive immunity. The current paradigm holds that prebound class II-associated invariant chain peptides (CLIP) and all subsequent antigens maintain a canonical orientation in the MHCII binding groove. Here we provide evidence for MHCII-bound CLIP inversion. NMR spectroscopy demonstrates that the interconversion from the canonical to the inverse alignment is a dynamic process, and X-ray crystallography shows that conserved MHC residues form a hydrogen bond network with the peptide backbone in both orientations. The natural catalyst HLA-DM accelerates peptide reorientation and the exchange of either canonically or inversely bound CLIP against antigenic peptide. Thus, noncanonical MHC-CLIP displays the hallmarks of a structurally and functionally intact antigen-presenting complex.

Reviews - 3pgd mentioned but not cited (1)

  1. Conformational variation in structures of classical and non-classical MHCII proteins and functional implications. Painter CA, Stern LJ. Immunol. Rev. 250 144-157 (2012)

Articles - 3pgd mentioned but not cited (8)

  1. Accurate pan-specific prediction of peptide-MHC class II binding affinity with improved binding core identification. Andreatta M, Karosiene E, Rasmussen M, Stryhn A, Buus S, Nielsen M. Immunogenetics 67 641-650 (2015)
  2. Bidirectional binding of invariant chain peptides to an MHC class II molecule. Günther S, Schlundt A, Sticht J, Roske Y, Heinemann U, Wiesmüller KH, Jung G, Falk K, Rötzschke O, Freund C. Proc. Natl. Acad. Sci. U.S.A. 107 22219-22224 (2010)
  3. An effective and effecient peptide binding prediction approach for a broad set of HLA-DR molecules based on ordered weighted averaging of binding pocket profiles. Shen WJ, Zhang S, Wong HS. Proteome Sci 11 S15 (2013)
  4. A Novel Peptide Binding Prediction Approach for HLA-DR Molecule Based on Sequence and Structural Information. Li Z, Zhao Y, Pan G, Tang J, Guo F. Biomed Res Int 2016 3832176 (2016)
  5. Impact of Structural Observables From Simulations to Predict the Effect of Single-Point Mutations in MHC Class II Peptide Binders. Ochoa R, Laskowski RA, Thornton JM, Cossio P. Front Mol Biosci 8 636562 (2021)
  6. Structural Insights Into HLA-DM Mediated MHC II Peptide Exchange. Painter CA, Stern LJ. Curr Top Biochem Res 13 39-55 (2011)
  7. Computational Identification and Characterization of a Promiscuous T-Cell Epitope on the Extracellular Protein 85B of Mycobacterium spp. for Peptide-Based Subunit Vaccine Design. Hossain MS, Azad AK, Chowdhury PA, Wakayama M. Biomed Res Int 2017 4826030 (2017)
  8. Polymorphic Region-Specific Antibody for Evaluation of Affinity-Associated Profile of Chimeric Antigen Receptor. Han C, Choi BK, Kim SH, Sim SJ, Han S, Park B, Tsuchiya Y, Takahashi M, Kim YH, Eom HS, Kitaguchi T, Ueda H, Kwon BS. Mol Ther Oncolytics 17 293-305 (2020)


Reviews citing this publication (7)

  1. Major Histocompatibility Complex (MHC) Class I and MHC Class II Proteins: Conformational Plasticity in Antigen Presentation. Wieczorek M, Abualrous ET, Sticht J, Álvaro-Benito M, Stolzenberg S, Noé F, Freund C. Front Immunol 8 292 (2017)
  2. The mechanism of HLA-DM induced peptide exchange in the MHC class II antigen presentation pathway. Schulze MS, Wucherpfennig KW. Curr. Opin. Immunol. 24 105-111 (2012)
  3. Ancient features of the MHC class II presentation pathway, and a model for the possible origin of MHC molecules. Dijkstra JM, Yamaguchi T. Immunogenetics 71 233-249 (2019)
  4. Human leukocyte Antigen-DM polymorphisms in autoimmune diseases. Alvaro-Benito M, Morrison E, Wieczorek M, Sticht J, Freund C. Open Biol 6 (2016)
  5. Analysis of CD74 Occurrence in Oncogenic Fusion Proteins. Vargas J, Pantouris G. Int J Mol Sci 24 15981 (2023)
  6. Stereo electronic principles for selecting fully-protective, chemically-synthesised malaria vaccines. Patarroyo ME, Bermudez A, Alba MP, Patarroyo MA, Suarez C, Aza-Conde J, Moreno-Vranich A, Vanegas M. Front Immunol 13 926680 (2022)
  7. The Role of Molecular Flexibility in Antigen Presentation and T Cell Receptor-Mediated Signaling. Natarajan K, Jiang J, May NA, Mage MG, Boyd LF, McShan AC, Sgourakis NG, Bax A, Margulies DH. Front Immunol 9 1657 (2018)

Articles citing this publication (34)

  1. Risk for ACPA-positive rheumatoid arthritis is driven by shared HLA amino acid polymorphisms in Asian and European populations. Okada Y, Kim K, Han B, Pillai NE, Ong RT, Saw WY, Luo M, Jiang L, Yin J, Bang SY, Lee HS, Brown MA, Bae SC, Xu H, Teo YY, de Bakker PI, Raychaudhuri S. Hum. Mol. Genet. 23 6916-6926 (2014)
  2. Structural basis for RNA recognition in roquin-mediated post-transcriptional gene regulation. Schlundt A, Heinz GA, Janowski R, Geerlof A, Stehle R, Heissmeyer V, Niessing D, Sattler M. Nat. Struct. Mol. Biol. 21 671-678 (2014)
  3. HLA-DRB1*07:01 is associated with a higher risk of asparaginase allergies. Fernandez CA, Smith C, Yang W, Daté M, Bashford D, Larsen E, Bowman WP, Liu C, Ramsey LB, Chang T, Turner V, Loh ML, Raetz EA, Winick NJ, Hunger SP, Carroll WL, Onengut-Gumuscu S, Chen WM, Concannon P, Rich SS, Scheet P, Jeha S, Pui CH, Evans WE, Devidas M, Relling MV. Blood 124 1266-1276 (2014)
  4. Anti-LGI1 encephalitis is associated with unique HLA subtypes. Kim TJ, Lee ST, Moon J, Sunwoo JS, Byun JI, Lim JA, Shin YW, Jun JS, Lee HS, Lee WJ, Yang AR, Choi Y, Park KI, Jung KH, Jung KY, Kim M, Lee SK, Chu K. Ann. Neurol. 81 183-192 (2017)
  5. Novel in silico tools for designing peptide-based subunit vaccines and immunotherapeutics. Dhanda SK, Usmani SS, Agrawal P, Nagpal G, Gautam A, Raghava GPS. Brief. Bioinformatics 18 467-478 (2017)
  6. Characterization of structural features controlling the receptiveness of empty class II MHC molecules. Rupp B, Günther S, Makhmoor T, Schlundt A, Dickhaut K, Gupta S, Choudhary I, Wiesmüller KH, Jung G, Freund C, Falk K, Rötzschke O, Kühne R. PLoS ONE 6 e18662 (2011)
  7. HLA-DRα1 constructs block CD74 expression and MIF effects in experimental autoimmune encephalomyelitis. Meza-Romero R, Benedek G, Yu X, Mooney JL, Dahan R, Duvshani N, Bucala R, Offner H, Reiter Y, Burrows GG, Vandenbark AA. J. Immunol. 192 4164-4173 (2014)
  8. Re-Directing CD4(+) T Cell Responses with the Flanking Residues of MHC Class II-Bound Peptides: The Core is Not Enough. Holland CJ, Cole DK, Godkin A. Front Immunol 4 172 (2013)
  9. Structural and dynamical insights on HLA-DR2 complexes that confer susceptibility to multiple sclerosis in Sardinia: a molecular dynamics simulation study. Kumar A, Cocco E, Atzori L, Marrosu MG, Pieroni E. PLoS ONE 8 e59711 (2013)
  10. Susceptibility to HLA-DM protein is determined by a dynamic conformation of major histocompatibility complex class II molecule bound with peptide. Yin L, Trenh P, Guce A, Wieczorek M, Lange S, Sticht J, Jiang W, Bylsma M, Mellins ED, Freund C, Stern LJ. J. Biol. Chem. 289 23449-23464 (2014)
  11. NMR spectroscopy reveals unexpected structural variation at the protein-protein interface in MHC class I molecules. Beerbaum M, Ballaschk M, Erdmann N, Schnick C, Diehl A, Uchanska-Ziegler B, Ziegler A, Schmieder P. J. Biomol. NMR 57 167-178 (2013)
  12. Gauche(+) side-chain orientation as a key factor in the search for an immunogenic peptide mixture leading to a complete fully protective vaccine. Bermúdez A, Calderon D, Moreno-Vranich A, Almonacid H, Patarroyo MA, Poloche A, Patarroyo ME. Vaccine 32 2117-2126 (2014)
  13. The nonconventional MHC class II molecule DM governs diabetes susceptibility in NOD mice. Morgan MA, Muller PS, Mould A, Newland SA, Nichols J, Robertson EJ, Cooke A, Bikoff EK. PLoS ONE 8 e56738 (2013)
  14. HLA-DMA polymorphisms differentially affect MHC class II peptide loading. Álvaro-Benito M, Wieczorek M, Sticht J, Kipar C, Freund C. J Immunol 194 803-816 (2015)
  15. MHC class II complexes sample intermediate states along the peptide exchange pathway. Wieczorek M, Sticht J, Stolzenberg S, Günther S, Wehmeyer C, El Habre Z, Álvaro-Benito M, Noé F, Freund C. Nat Commun 7 13224 (2016)
  16. Antigenic peptide molecular recognition by the DRB1-DQB1 haplotype modulates multiple sclerosis susceptibility. Kumar A, Melis P, Genna V, Cocco E, Marrosu MG, Pieroni E. Mol Biosyst 10 2043-2054 (2014)
  17. HLA-B*40:02 and DRB1*04:03 are risk factors for oxcarbazepine-induced maculopapular eruption. Moon J, Kim TJ, Lim JA, Sunwoo JS, Byun JI, Lee ST, Jung KH, Park KI, Jung KY, Jeon D, Yu KS, Jang IJ, Chu K, Lee SK. Epilepsia 57 1879-1886 (2016)
  18. Peptide linkage to the α-subunit of MHCII creates a stably inverted antigen presentation complex. Schlundt A, Günther S, Sticht J, Wieczorek M, Roske Y, Heinemann U, Freund C. J. Mol. Biol. 423 294-302 (2012)
  19. Differential scanning fluorimetry based assessments of the thermal and kinetic stability of peptide-MHC complexes. Hellman LM, Yin L, Wang Y, Blevins SJ, Riley TP, Belden OS, Spear TT, Nishimura MI, Stern LJ, Baker BM. J. Immunol. Methods 432 95-101 (2016)
  20. Structure of an α-Helical Peptide and Lipopeptide Bound to the Nonclassical Major Histocompatibility Complex (MHC) Class I Molecule CD1d. Girardi E, Wang J, Zajonc DM. J. Biol. Chem. 291 10677-10683 (2016)
  21. Structural Comparison Between MHC Classes I and II; in Evolution, a Class-II-Like Molecule Probably Came First. Wu Y, Zhang N, Hashimoto K, Xia C, Dijkstra JM. Front Immunol 12 621153 (2021)
  22. HLA-DP2 binding prediction by molecular dynamics simulations. Doytchinova I, Petkov P, Dimitrov I, Atanasova M, Flower DR. Protein Sci. 20 1918-1928 (2011)
  23. HLA-DR7 and HLA-DQ2: Transgenic mouse strains tested as a model system for ximelagatran hepatotoxicity. Lundgren H, Martinsson K, Cederbrant K, Jirholt J, Mucs D, Madeyski-Bengtson K, Havarinasab S, Hultman P. PLoS ONE 12 e0184744 (2017)
  24. Unraveling the structural basis for the unusually rich association of human leukocyte antigen DQ2.5 with class-II-associated invariant chain peptides. Nguyen TB, Jayaraman P, Bergseng E, Madhusudhan MS, Kim CY, Sollid LM. J. Biol. Chem. 292 9218-9228 (2017)
  25. Flanking residues are central to DO11.10 T cell hybridoma stimulation by ovalbumin 323-339. Roy BM, Zhukov DV, Maynard JA. PLoS ONE 7 e47585 (2012)
  26. HLA Class II Presentation Is Specifically Altered at Elevated Temperatures in the B-Lymphoblastic Cell Line JY. Demmers LC, Wu W, Heck AJR. Mol Cell Proteomics 20 100089 (2021)
  27. HLA Risk Alleles in Aromatic Antiepileptic Drug-Induced Maculopapular Exanthema. Shi YW, Wang J, Min FL, Bian WJ, Mao BJ, Mao Y, Qin B, Li BM, Ou YM, Hou YQ, Zou X, Guan BZ, He N, Chen YJ, Li XL, Wang J, Deng WY, Liu HK, Shen NX, Liu XR, Yi YH, Zhou LM, Zhou D, Kwan P, Liao WP. Front Pharmacol 12 671572 (2021)
  28. Impact of HLA-DR Antigen Binding Cleft Rigidity on T Cell Recognition. Szeto C, Bloom JI, Sloane H, Lobos CA, Fodor J, Jayasinghe D, Chatzileontiadou DSM, Grant EJ, Buckle AM, Gras S. Int J Mol Sci 21 E7081 (2020)
  29. A Missing Switch in Peptide Exchange for MHC Class II Molecules. Freund C, Höfer T. Front Immunol 10 2513 (2019)
  30. A novel RNA pol II CTD interaction site on the mRNA capping enzyme is essential for its allosteric activation. Bage MG, Almohammed R, Cowling VH, Pisliakov AV. Nucleic Acids Res 49 3109-3126 (2021)
  31. Combinatorial recognition of clustered RNA elements by the multidomain RNA-binding protein IMP3. Schneider T, Hung LH, Aziz M, Wilmen A, Thaum S, Wagner J, Janowski R, Müller S, Schreiner S, Friedhoff P, Hüttelmaier S, Niessing D, Sattler M, Schlundt A, Bindereif A. Nat Commun 10 2266 (2019)
  32. Human T cells recognize HLA-DP-bound peptides in two orientations. Klobuch S, Lim JJ, van Balen P, Kester MGD, de Klerk W, de Ru AH, Pothast CR, Jedema I, Drijfhout JW, Rossjohn J, Reid HH, van Veelen PA, Falkenburg JHF, Heemskerk MHM. Proc Natl Acad Sci U S A 119 e2214331119 (2022)
  33. MHC-II dynamics are maintained in HLA-DR allotypes to ensure catalyzed peptide exchange. Abualrous ET, Stolzenberg S, Sticht J, Wieczorek M, Roske Y, Günther M, Dähn S, Boesen BB, Calvo MM, Biese C, Kuppler F, Medina-García Á, Álvaro-Benito M, Höfer T, Noé F, Freund C. Nat Chem Biol (2023)
  34. The complex pattern of genetic associations of leprosy with HLA class I and class II alleles can be reduced to four amino acid positions. Dallmann-Sauer M, Fava VM, Gzara C, Orlova M, Van Thuc N, Thai VH, Alcaïs A, Abel L, Cobat A, Schurr E. PLoS Pathog 16 e1008818 (2020)


Quick links