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Unconventional Peptide Presentation by Major Histocompatibility Complex (MHC) Class I Allele HLA-A*02:01: BREAKING CONFINEMENT.

Remesh SG, Andreatta M, Ying G, Kaever T, Nielsen M, McMurtrey C, Hildebrand W, Peters B, Zajonc DM
J Biol Chem 292 5262-5270 (2017)
Related entries: 5enw, 5eot, 5f7d, 5f9j, 5fa4, 5fdw

Cited: 35 times
EuropePMC logo PMID: 28179428

Abstract

Peptide antigen presentation by major histocompatibility complex (MHC) class I proteins initiates CD8+ T cell-mediated immunity against pathogens and cancers. MHC I molecules typically bind peptides with 9 amino acids in length with both ends tucked inside the major A and F binding pockets. It has been known for a while that longer peptides can also bind by either bulging out of the groove in the middle of the peptide or by binding in a zigzag fashion inside the groove. In a recent study, we identified an alternative binding conformation of naturally occurring peptides from Toxoplasma gondii bound by HLA-A*02:01. These peptides were extended at the C terminus (PΩ) and contained charged amino acids not more than 3 residues after the anchor amino acid at PΩ, which enabled them to open the F pocket and expose their C-terminal extension into the solvent. Here, we show that the mechanism of F pocket opening is dictated by the charge of the first charged amino acid found within the extension. Although positively charged amino acids result in the Tyr-84 swing, amino acids that are negatively charged induce a not previously described Lys-146 lift. Furthermore, we demonstrate that the peptides with alternative binding modes have properties that fit very poorly to the conventional MHC class I pathway and suggest they are presented via alternative means, potentially including cross-presentation via the MHC class II pathway.

Articles - 5fa3 mentioned but not cited (3)

  1. Structure Based Prediction of Neoantigen Immunogenicity. Riley TP, Keller GLJ, Smith AR, Davancaze LM, Arbuiso AG, Devlin JR, Baker BM. Front Immunol 10 2047 (2019)
  2. Unconventional Peptide Presentation by Major Histocompatibility Complex (MHC) Class I Allele HLA-A*02:01: BREAKING CONFINEMENT. Remesh SG, Andreatta M, Ying G, Kaever T, Nielsen M, McMurtrey C, Hildebrand W, Peters B, Zajonc DM. J Biol Chem 292 5262-5270 (2017)
  3. The Use of Molecular Dynamics Simulation Method to Quantitatively Evaluate the Affinity between HBV Antigen T Cell Epitope Peptides and HLA-A Molecules. Mei X, Li X, Zhao C, Liu A, Ding Y, Shen C, Li J. Int J Mol Sci 23 4629 (2022)


Reviews citing this publication (10)

  1. Predicting Antigen Presentation-What Could We Learn From a Million Peptides? Gfeller D, Bassani-Sternberg M. Front Immunol 9 1716 (2018)
  2. Unfinished Business: Evolution of the MHC and the Adaptive Immune System of Jawed Vertebrates. Kaufman J. Annu Rev Immunol 36 383-409 (2018)
  3. The Immune Epitope Database and Analysis Resource Program 2003-2018: reflections and outlook. Martini S, Nielsen M, Peters B, Sette A. Immunogenetics 72 57-76 (2020)
  4. The pockets guide to HLA class I molecules. Nguyen AT, Szeto C, Gras S. Biochem Soc Trans 49 2319-2331 (2021)
  5. Employing proteomics in the study of antigen presentation: an update. Ramarathinam SH, Croft NP, Illing PT, Faridi P, Purcell AW. Expert Rev Proteomics 15 637-645 (2018)
  6. From Chickens to Humans: The Importance of Peptide Repertoires for MHC Class I Alleles. Kaufman J. Front Immunol 11 601089 (2020)
  7. Antigen processing and presentation in HIV infection. Boucau J, Le Gall S. Mol Immunol 113 67-74 (2019)
  8. Mechanistic diversity in MHC class I antigen recognition. Barbosa CRR, Barton J, Shepherd AJ, Mishto M. Biochem J 478 4187-4202 (2021)
  9. Unconventional Peptide Presentation by Classical MHC Class I and Implications for T and NK Cell Activation. Zajonc DM. Int J Mol Sci 21 E7561 (2020)
  10. New vistas unfold: Chicken MHC molecules reveal unexpected ways to present peptides to the immune system. Halabi S, Kaufman J. Front Immunol 13 886672 (2022)

Articles citing this publication (22)

  1. High-throughput and Sensitive Immunopeptidomics Platform Reveals Profound Interferonγ-Mediated Remodeling of the Human Leukocyte Antigen (HLA) Ligandome. Chong C, Marino F, Pak H, Racle J, Daniel RT, Müller M, Gfeller D, Coukos G, Bassani-Sternberg M. Mol Cell Proteomics 17 533-548 (2018)
  2. The Length Distribution and Multiple Specificity of Naturally Presented HLA-I Ligands. Gfeller D, Guillaume P, Michaux J, Pak HS, Daniel RT, Racle J, Coukos G, Bassani-Sternberg M. J Immunol 201 3705-3716 (2018)
  3. Quantification of epitope abundance reveals the effect of direct and cross-presentation on influenza CTL responses. Wu T, Guan J, Handel A, Tscharke DC, Sidney J, Sette A, Wakim LM, Sng XYX, Thomas PG, Croft NP, Purcell AW, La Gruta NL. Nat Commun 10 2846 (2019)
  4. An in silico-in vitro Pipeline Identifying an HLA-A*02:01+ KRAS G12V+ Spliced Epitope Candidate for a Broad Tumor-Immune Response in Cancer Patients. Mishto M, Mansurkhodzhaev A, Ying G, Bitra A, Cordfunke RA, Henze S, Paul D, Sidney J, Urlaub H, Neefjes J, Sette A, Zajonc DM, Liepe J. Front Immunol 10 2572 (2019)
  5. Discrimination Between Human Leukocyte Antigen Class I-Bound and Co-Purified HIV-Derived Peptides in Immunopeptidomics Workflows. Partridge T, Nicastri A, Kliszczak AE, Yindom LM, Kessler BM, Ternette N, Borrow P. Front Immunol 9 912 (2018)
  6. The C-terminal extension landscape of naturally presented HLA-I ligands. Guillaume P, Picaud S, Baumgaertner P, Montandon N, Schmidt J, Speiser DE, Coukos G, Bassani-Sternberg M, Filippakopoulos P, Gfeller D. Proc Natl Acad Sci U S A 115 5083-5088 (2018)
  7. A Recurrent Mutation in Anaplastic Lymphoma Kinase with Distinct Neoepitope Conformations. Toor JS, Rao AA, McShan AC, Yarmarkovich M, Nerli S, Yamaguchi K, Madejska AA, Nguyen S, Tripathi S, Maris JM, Salama SR, Haussler D, Sgourakis NG. Front Immunol 9 99 (2018)
  8. ERAP1 enzyme-mediated trimming and structural analyses of MHC I-bound precursor peptides yield novel insights into antigen processing and presentation. Li L, Batliwala M, Bouvier M. J Biol Chem 294 18534-18544 (2019)
  9. A systematic re-examination of processing of MHCI-bound antigenic peptide precursors by endoplasmic reticulum aminopeptidase 1. Mavridis G, Arya R, Domnick A, Zoidakis J, Makridakis M, Vlahou A, Mpakali A, Lelis A, Georgiadis D, Tampé R, Papakyriakou A, Stern LJ, Stratikos E. J Biol Chem 295 7193-7210 (2020)
  10. 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)
  11. Machine learning reveals a non-canonical mode of peptide binding to MHC class II molecules. Andreatta M, Jurtz VI, Kaever T, Sette A, Peters B, Nielsen M. Immunology 152 255-264 (2017)
  12. Antibody-mediated delivery of a viral MHC-I epitope into the cytosol of target tumor cells repurposes virus-specific CD8+ T cells for cancer immunotherapy. Jung K, Son MJ, Lee SY, Kim JA, Ko DH, Yoo S, Kim CH, Kim YS. Mol Cancer 21 102 (2022)
  13. Overlapping Peptides Elicit Distinct CD8+ T Cell Responses following Influenza A Virus Infection. Assmus LM, Guan J, Wu T, Farenc C, Sng XYX, Zareie P, Nguyen A, Nguyen AT, Tscharke DC, Thomas PG, Rossjohn J, Gras S, Croft NP, Purcell AW, La Gruta NL. J Immunol 205 1731-1742 (2020)
  14. Introductory Journal Article Immunopeptidomics Special Issue. Ternette N, Purcell AW. Proteomics 18 e1800145 (2018)
  15. Immunoproteomic analysis of a Chikungunya poxvirus-based vaccine reveals high HLA class II immunoprevalence. Lorente E, Barriga A, Barnea E, Palomo C, García-Arriaza J, Mir C, Esteban M, Admon A, López D. PLoS Negl Trop Dis 13 e0007547 (2019)
  16. Releasing the concept of HLA-allele specific peptide anchors in viral infections: A non-canonical naturally presented human cytomegalovirus-derived HLA-A*24:02 restricted peptide drives exquisite immunogenicity. Pump WC, Schulz R, Huyton T, Kunze-Schumacher H, Martens J, Hò GT, Blasczyk R, Bade-Doeding C. HLA 94 25-38 (2019)
  17. Flipping out the peptide. Gras S. Nat Chem Biol 14 905-906 (2018)
  18. The polymorphism at residue 156 determines the HLA-B*35 restricted peptide repertoire during HCMV infection. Abels WC, Manandhar T, Kunze-Schumacher H, Blasczyk R, Bade-Döding C. Immunogenetics 70 639-646 (2018)
  19. Charge-based interactions through peptide position 4 drive diversity of antigen presentation by human leukocyte antigen class I molecules. Jackson KR, Antunes DA, Talukder AH, Maleki AR, Amagai K, Salmon A, Katailiha AS, Chiu Y, Fasoulis R, Rigo MM, Abella JR, Melendez BD, Li F, Sun Y, Sonnemann HM, Belousov V, Frenkel F, Justesen S, Makaju A, Liu Y, Horn D, Lopez-Ferrer D, Huhmer AF, Hwu P, Roszik J, Hawke D, Kavraki LE, Lizée G. PNAS Nexus 1 pgac124 (2022)
  20. High-throughput, targeted MHC class I immunopeptidomics using a functional genetics screening platform. Bruno PM, Timms RT, Abdelfattah NS, Leng Y, Lelis FJN, Wesemann DR, Yu XG, Elledge SJ. Nat Biotechnol 41 980-992 (2023)
  21. Identification of neoepitope reactive T-cell receptors guided by HLA-A*03:01 and HLA-A*11:01 immunopeptidomics. Ade CM, Sporn MJ, Das S, Yu Z, Hanada KI, Qi YA, Maity T, Zhang X, Guha U, Andresson T, Yang JC. J Immunother Cancer 11 e007097 (2023)
  22. The use of tyrosinases in a chemoenzymatic cascade as a peptide ligation strategy. Ni Y, Wang Y, Tabor AB, Ward JM, Hailes HC. RSC Chem Biol 4 132-137 (2023)


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