663
Views
0
CrossRef citations to date
0
Altmetric
Review

Employing proteomics in the study of antigen presentation: an update

, , , & ORCID Icon
Pages 637-645 | Received 28 Jun 2018, Accepted 03 Aug 2018, Published online: 13 Aug 2018

References

  • Cooper MD, Alder MN. The evolution of adaptive immune systems. Cell. 2006;124(4):815–822.
  • Parham P, Ohta T. Population biology of antigen presentation by MHC class I molecules. Science. 1996;272(5258):67.
  • Robinson J, Halliwell JA, Hayhurst JD, et al. IMGT/HLA database: allele variant databases. Nucleic Acids Res. 2015;43(D1):D423–D431.
  • Prugnolle F, Manica A, Charpentier M, et al. Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol. 2005;15(11):1022–1027.
  • Trowsdale J. The MHC, disease and selection. Immunol Lett. 2011;137(1):1–8.
  • McMurtrey C, Harriff MJ, Swarbrick GM, et al. T cell recognition of mycobacterium tuberculosis peptides presented by HLA-E derived from infected human cells. PLoS One. 2017;12(11).
  • Di Marco M, Schuster H, Backert L, et al. Unveiling the peptide motifs of HLA-C and HLA-G from naturally presented peptides and generation of binding prediction matrices. J Immunol. 2017;199(8):2639–2651.
  • Lalazar G, Preston S, Zigmond E, et al. Glycolipids as immune modulatory tools. Mini-Reviews Med Chem. 2006;6(11):1249–1253.
  • Kjer-Nielsen L, Patel O, Corbett AJ, et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature. 2012;491(7426):717–723.
  • Hassan I, Ahmad F. Structural diversity of class I MHC-like molecules and its implications in binding specificities. Adv Protein Chem Struct Biol. 2011;83:223–270.
  • Birkinshaw RW, Pellicci DG, Cheng TY, et al. αβ T cell antigen receptor recognition of CD1a presenting self lipid ligands. Nat Immunol. 2015;16(3):258–266.
  • Zajonc DM, Flajnik MF. CD1, MR1, NKT, and MAIT: evolution and origins of non-peptidic antigen recognition by T lymphocytes. Immunogenetics. 2016;68(8):489–490.
  • Singhal A, Mori L, De Libero G. T cell recognition of non-peptidic antigens in infectious diseases. Indian J Med Res. 2013;138(NOV):620–631.
  • Hunt DF, Michel H, Dickinson TA, et al. Peptides presented to the immune system by the murine class II major histocompatibility complex molecule I-Ad. Science. 1992;256:1817–1820.
  • Henderson RAM, Michel H, Sakaguchi K, et al. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science. 1992;1264–1266.
  • Hunt DF, Henderson RA, Shabanowitz J, et al. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science. 1992;255:1261–1263.
  • Sette A, Ceman S, Kubo RT, et al. Invariant chain peptides in most HLA-DR molecules of an antigen- processing mutant. Science. 1992;258(5089):1801–1804.
  • Henderson RA, Cox AL, Sakaguchi K, et al. Direct identification of an endogenous peptide recognized by multiple HLA-A2.1-specific cytotoxic T cells. Proc Natl Acad Sci U S A. 1993;90(21):10275–10279.
  • Rotzschke O, Falk K, Deres K, et al. Isolation and analysis of naturally processed viral peptides as recognized by cytotoxic T cells. Nature. 1990;348(6298):252–254.
  • Falk K, Rötzschke O, Deres K, et al. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. J Exp Med. 1991;174:425–434.
  • Falk K, Rötzschke O, Stevanovic S, et al. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature. 1991;351:290–296.
  • Rammensee HG, Falk K, Rotzschke O. Peptides naturally presented by MHC class I molecules. Annu Rev Immunol. 1993;11:213–244.
  • Vita R, Overton JA, Greenbaum JA, et al. The immune epitope database (IEDB) 3.0. Nucleic Acids Res. 2015;43(D1):D405–D412.
  • Wynne JW, Woon AP, Dudek NL, et al. Characterization of the antigen processing machinery and endogenous peptide presentation of a bat MHC class I molecule. J Immunol. 2016;196(11):4468.
  • Cumberbatch JA, Brewer D, Vidavsky I, et al. Chicken major histocompatibility complex class II molecules of the B19 haplotype present self and foreign peptides. Anim Genet. 2006;37(4):393–396.
  • Nielsen M, Connelley T, Ternette N. Improved Prediction of Bovine Leucocyte Antigens (BoLA) presented ligands by use of mass-spectrometry-determined ligand and in vitro binding data. J Proteome Res. 2018;17(1):559–567.
  • Purcell AW, Croft NP, Tscharke DC. Immunology by numbers: quantitation of antigen presentation completes the quantitative milieu of systems immunology! Curr Opin Immunol. 2016;40:88–95.
  • Rock KL, Reits E, Neefjes J. Present yourself! by MHC class I and MHC class II molecules. Trends Immunol. 2016;37(11):724–737.
  • Mishto M, Liepe J. Post-translational peptide splicing and T cell responses. Trends Immunol. 2017;38(12):904–915.
  • Engelhard VH, Brickner AG, Zarling AL. Insights into antigen processing gained by direct analysis of the naturally processed class I MHC associated peptide repertoire. Mol Immunol. 2002;39(3–4):127–137.
  • Duffy EB, Drake JR, Harton JA. Evolving Insights for MHC class II antigen processing and presentation in health and disease. Curr Pharmacol Rep. 2017;3(5):213–220.
  • Stern LJ, Santambrogio L. The melting pot of the MHC II peptidome. Curr Opin Immunol. 2016;40:70–77.
  • Sadegh-Nasseri S. A step-by-step overview of the dynamic process of epitope selection by major histocompatibility complex class II for presentation to helper T cells [version 1; referees: 4 approved]. F1000 Res. 2016;5:1305.
  • Vaughan K, Xu X, Caron E, et al. Deciphering the MHC-associated peptidome: a review of naturally processed ligand data. Expert Rev Proteomics. 2017;14(9):729–736.
  • Uy R, Wold F. Posttranslational covalent modification of proteins. Science. 1977;198(4320):890.
  • Engelhard VH, Altrich-Vanlith M, Ostankovitch M, et al. Post-translational modifications of naturally processed MHC-binding epitopes. Curr Opin Immunol. 2006;18(1):92–97.
  • Gerstner C, Dubnovitsky A, Sandin C, et al. Functional and structural characterization of a novel HLA-DRB1*04: 01-restricted α-enolase T cell epitope in rheumatoid arthritis. Front Immunol. 2016;7(NOV).
  • Mazzeo MF, De Giulio B, Senger S, et al. Identification of transglutaminase-mediated deamidation sites in a recombinant α-gliadin by advanced mass-spectrometric methodologies. Protein Sci. 2003;12(11):2434–2442.
  • Cobbold M, De La Peña H, Norris A, et al. MHC class I–associated Phosphopeptides are the targets of memory-like immunity in Leukemia. Sci Transl Med. 2013;5(203):203ra125.
  • Meyer VS, Drews O, Günder M, et al. Identification of natural MHC class II presented phosphopeptides and tumor-derived MHC class I Phospholigands. J Proteome Res. 2009;8(7):3666–3674.
  • Zarling AL, Ficarro SB, White FM, et al. Phosphorylated peptides are naturally processed and presented by major histocompatibility complex class I molecules in vivo. J Exp Med. 2000;192(12):1755–1762.
  • Yagüe J, Vázquez J, López De Castro JA. A post-translational modification of nuclear proteins, NG,NG-dimethyl-Arg, found in a natural HLA class I peptide ligand. Protein Sci. 2000;9(11):2210–2217.
  • Sidney J, Becart S, Zhou M, et al. Citrullination only infrequently impacts peptide binding to HLA class II MHC. PLoS One. 2017;12(5):e0177140.
  • Petersen J, Purcell AW, Rossjohn J. Post-translationally modified T cell epitopes: immune recognition and immunotherapy. J Mol Med (Berl). 2009;87(11):1045–1051.
  • Mohammed F, Cobbold M, Zarling AL, et al. Phosphorylation-dependent interaction between antigenic peptides and MHC class I: a molecular basis for the presentation of transformed self. Nat Immunol. 2008;9(11):1236–1243.
  • Petersen J, Wurzbacher SJ, Williamson NA, et al. Phosphorylated self-peptides alter human leukocyte antigen class I-restricted antigen presentation and generate tumor-specific epitopes. Proc Natl Acad Sci U S A. 2009;106(8):2776–2781.
  • Zarling AL, Polefrone JM, Evans AM, et al. Identification of class I MHC-associated phosphopeptides as targets for cancer immunotherapy. Proc Natl Acad Sci. 2006;103(40):14889.
  • Depontieu FR, Qian J, Zarling AL, et al. Identification of tumor-associated, MHC class II-restricted phosphopeptides as targets for immunotherapy. Proc Natl Acad Sci U S A. 2009;106(29):12073–12078.
  • Neugebauer KM, Merrill JT, Wener MH, et al. SR proteins are autoantigens in patients with systemic lupus erythematosus. Importance of phosphoepitopes. Arthritis Rheum. 2000;43(8):1768–1778.
  • Doyle HA, Mamula MJ. Autoantigenesis: the evolution of protein modifications in autoimmune disease. Curr Opin Immunol. 2012;24(1):112–118.
  • Hindupur SK, Colombi M, Fuhs SR, et al. The protein histidine phosphatase LHPP is a tumour suppressor. Nature. 2018;555:678.
  • Kee J-M, Muir TW. Chasing phosphohistidine, an elusive sibling in the phosphoamino acid family. ACS Chem Biol. 2012;7(1):44–51.
  • Marcilla M, Alpizar A, Lombardia M, et al. Increased diversity of the hla-b40 ligandome by the presentation of peptides phosphorylated at their main anchor residue. Mol Cell Proteomics. 2014;13(2):462–474.
  • Alpízar A, Marino F, Ramos-Fernández A, et al. A molecular basis for the presentation of phosphorylated peptides by HLA-B antigens. Mol Cell Proteomics. 2017;16(2):181–193.
  • Frese CK, Altelaar AFM, van den Toorn H, et al. Toward full peptide sequence coverage by dual fragmentation combining electron-transfer and higher-energy collision dissociation tandem mass spectrometry. Anal Chem. 2012;84(22):9668–9673.
  • Mommen GPM, Frese CK, Meiring HD, et al. Expanding the detectable HLA peptide repertoire using electron-transfer/higher-energy collision dissociation (EThcD). Proc Natl Acad Sci U S A. 2014;111(12):4507–4512.
  • Suzuki A, Yamada R, Chang X, et al. Functional haplotypes of PADI4, encoding citrullinating enzyme peptidylarginine deiminase 4, are associated with rheumatoid arthritis. Nat Genet. 2003;34(4):395–402.
  • van Venrooij WJ, van Beers JJ, Pruijn GJ. Anti-CCP antibodies: the past, the present and the future. Nat Rev Rheumatol. 2011;7(7):391–398.
  • Scally SW, Petersen J, Law SC, et al. A molecular basis for the association of the HLA-DRB1 locus, citrullination, and rheumatoid arthritis. J Exp Med. 2013;210(12):2569–2582.
  • Nguyen H, James EA. Immune recognition of citrullinated epitopes. Immunology. 2016;149(2):131–138.
  • Clancy KW, Weerapana E, Thompson PR. Detection and identification of protein citrullination in complex biological systems. Curr Opin Chem Biol. 2016;30:1–6.
  • Tutturen AEV, Holm A, Jørgensen M, et al. A technique for the specific enrichment of citrulline-containing peptides. Anal Biochem. 2010;403(1):43–51.
  • Moremen KW, Tiemeyer M, Nairn AV. Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Biol. 2012;13:448.
  • Lu H, Zhang Y, Yang P. Advancements in mass spectrometry-based glycoproteomics and glycomics. Natl Sci Rev. 2016;3(3):345–364.
  • Yang Y, Franc V, Heck AJR. Glycoproteomics: a balance between high-throughput and in-depth analysis. Trends Biotechnol. 2017;35(7):598–609.
  • Engelhard VH. A tyrosinase epitope is processed after translation into the endoplasmic reticulum. FASEB J. 1996;10:6.
  • Malaker SA, Ferracane MJ, Depontieu FR, et al. Identification and characterization of complex glycosylated peptides presented by the MHC class II processing pathway in melanoma. J Proteome Res. 2017;16(1):228–237.
  • Dengjel J, Rammensee HG, Stevanovic S. Glycan side chains on naturally presented MHC class II ligands. J Spectrom. 2005;40(1):100–104.
  • Chicz RM, Urban RG, Gorga JC, et al. Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J Exp Med. 1993;178(1):27.
  • Marino F, Bern M, Mommen GPM, et al. Extended O-GlcNAc on HLA class-I-bound peptides. J Am Chem Soc. 2015;137(34):10922–10925.
  • Murn J, Shi Y. The winding path of protein methylation research: milestones and new frontiers. Nat Rev Mol Biol. 2017;18:517.
  • Biggar KK, Li SSC. Non-histone protein methylation as a regulator of cellular signalling and function. Nat Rev Mol Biol. 2014;16:5.
  • Jarmalavicius S, Trefzer U, Walden P. Differential arginine methylation of the G-protein pathway suppressor GPS-2 recognized by tumor-specific T cells in melanoma. FASEB J. 2010;24(3):937–946.
  • Marino F, Mommen GPM, Jeko A, et al. Arginine (Di)methylated human leukocyte antigen class i peptides are favorably presented by HLA-B∗07. J Proteome Res. 2017;16(1):34–44.
  • Ramarathinam SH, Gras S, Alcantara S, et al. Identification of Native and Posttranslationally Modified HLA-B*57:01-Restricted HIV Envelope Derived Epitopes Using Immunoproteomics. Proteomics. 2018;18(12):e1700253.
  • Qi Q, Hua S, Clish CB, et al. Plasma Tryptophan-Kynurenine Metabolites Are Altered in Human Immunodeficiency Virus Infection and Associated With Progression of Carotid Artery Atherosclerosis. Clin Infect Dis. 2018;67(2):235–242.
  • Hascitha J, Priya R, Jayavelu S, et al. Analysis of Kynurenine/Tryptophan ratio and expression of IDO1 and 2 mRNA in tumour tissue of cervical cancer patients. Clin Biochem. 2016;49(12):919–924.
  • Routy JP, Mehraj V, Vyboh K, et al. Clinical relevance of kynurenine pathway in HIV/AIDS: an immune checkpoint at the crossroads of metabolism and inflammation. AIDS Rev. 2015;17(2):96–106.
  • Bilir C, Sarisozen C. Indoleamine 2,3-dioxygenase (IDO): only an enzyme or a checkpoint controller? J Oncological Sci. 2017;3(2):52–56.
  • Takikawa O. Biochemical and medical aspects of the indoleamine 2,3-dioxygenase-initiated l-tryptophan metabolism. Biochem Biophys Res Commun. 2005;338(1):12–19.
  • Yague J, Alvarez I, Rognan D, et al. An N-acetylated natural ligand of human histocompatibility leukocyte antigen (HLA)-B39: classical major histocompatibility complex class I proteins bind peptides with a blocked NH2 terminus in vivo. J Exp Med. 2000;191(12):2083–2092.
  • Seward RJ, Drouin EE, Steere AC, et al. Peptides presented by HLA-DR molecules in synovia of patients with rheumatoid arthritis or antibiotic-refractory lyme arthritis. Mol Cell Proteomics. 2011;10:3.
  • Trujillo JA, Croft NP, Dudek NL, et al. The cellular redox environment alters antigen presentation. J Biol Chem. 2014;289(40):27979–27991.
  • Matsumura M, Fremont DH, Peterson PA, et al. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science. 1992;257(5072):927.
  • Collins EJ, Garboczi DN, Wiley DC. Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature. 1994;371(6498):626–629.
  • Tenzer S, Wee E, Burgevin A, et al. Antigen processing influences HIV-specific cytotoxic T lymphocyte immunodominance. Nat Immunol. 2009;10(6):636–646.
  • Stryhn A, Pedersen LØ, HolmA, et al. Longer peptide can be accommodated in the MHC class I binding site by a protrusion mechanism. Eur J Immunol. 2000;30(11):3089–3099.
  • McMurtrey C, Trolle T, Sansom T, et al. Toxoplasma gondii peptide ligands open the gate of the HLA class I binding groove. Elife. 2016;5:e12556.
  • Remesh SG, Andreatta M, Ying G, et al. Unconventional peptide presentation by Major Histocompatibility Complex (MHC) class I allele HLA-A*02:01: BREAKING CONFINEMENT. J Biol Chem. 2017;292(13):5262–5270.
  • Pymm P, Illing PT, Ramarathinam SH, et al. MHC-I peptides get out of the groove and enable a novel mechanism of HIV-1 escape. Nat Struct Mol Biol. 2017;24(4):387–394.
  • Li X, Lamothe PA, Walker BD, et al. Crystal structure of HLA-B*5801 with a TW10 HIV Gag epitope reveals a novel mode of peptide presentation. Cell Mol Immunol. 2017;14(7):631–634.
  • Guillaume P, Picaud S, Baumgaertner P, et al. The C-terminal extension landscape of naturally presented HLA-I ligands. Proc Natl Acad Sci. 2018.
  • Hanada K, Yewdell JW, Yang JC. Immune recognition of a human renal cancer antigen through post-translational protein splicing. Nature. 2004;427(6971):252–256.
  • Vigneron N, Stroobant V, Chapiro J, et al. An antigenic peptide produced by peptide splicing in the proteasome. Science. 2004;304(5670):587–590.
  • Warren EH, Vigneron NJ, Gavin MA, et al. An antigen produced by splicing of noncontiguous peptides in the reverse order. Science. 2006;313(5792):1444–1447.
  • Vigneron N, Ferrari V, Stroobant V, et al. Peptide splicing by the proteasome. J Biol Chem. 2017;292(51):21170–21179.
  • Berkers CR, de Jong A, Ovaa H, et al. Transpeptidation and reverse proteolysis and their consequences for immunity. Int J Biochem Cell Biol. 2009;41(1):66–71.
  • Liepe J, Marino F, Sidney J, et al. A large fraction of HLA class I ligands are proteasome-generated spliced peptides. Science. 2016;354(6310):354–358.
  • Platteel AC, Mishto M, Textoris-Taube K, et al. CD8(+) T cells of Listeria monocytogenes-infected mice recognize both linear and spliced proteasome products. Eur J Immunol. 2016;46(5):1109–1118.
  • Platteel ACM, Liepe J, Textoris-Taube K, et al. multi-level strategy for identifying proteasome-catalyzed spliced epitopes targeted by CD8+ T cells during bacterial infection. Cell Rep. 2017;20(5):1242–1253.
  • Delong T, Wiles TA, Baker RL, et al. Pathogenic CD4 T cells in type 1 diabetes recognize epitopes formed by peptide fusion. Science. 2016;351(6274):711.
  • Faridi P, Purcell AW, Croft NP. In Immunopeptidomics We Need a Sniper Instead of a Shotgun. Proteomics. 2018;18(12):e1700464.
  • Liepe J, Mishto M, Textoris-Taube K, et al. The 20S proteasome splicing activity discovered by SpliceMet. PLoS Comput Biol. 2010;6(6):e1000830.
  • Mishto M, Goede A, Taube KT, et al. Driving forces of proteasome-catalyzed peptide splicing in yeast and humans. Molecular & Cellular Proteomics: MCP. 2012;11(10):1008–1023.
  • Michaux A, Larrieu P, Stroobant V, et al. A spliced antigenic peptide comprising a single spliced amino acid is produced in the proteasome by reverse splicing of a longer peptide fragment followed by trimming. J Immunol. 2014;192(4):1962–1971.
  • Ebstein F, Textoris-Taube K, Keller C, et al. Proteasomes generate spliced epitopes by two different mechanisms and as efficiently as non-spliced epitopes. Sci Rep. 2016;6:24032.
  • Berkers CR, de Jong A, Schuurman KG, et al. Definition of proteasomal peptide splicing rules for high-efficiency spliced peptide presentation by MHC class I molecules. Journal of Immunology (Baltimore, Md.: 1950). 2015;195(9):4085–4095.
  • Lill JR, van Veelen PA, Tenzer S, et al. Minimal Information About an Immuno-Peptidomics Experiment (MIAIPE). Proteomics. 2018;18(12):e1800110.
  • Zolg DP, Wilhelm M, Schmidt T, et al. ProteomeTools: systematic characterization of 21 post-translational protein modifications by LC-MS/MS using synthetic peptides. Mol Cell Proteomics. 2018.
  • Shao W, Pedrioli PGA, Wolski W, et al. The SysteMHC Atlas project. Nucleic Acids Res. 2018;46(D1):D1237–D1247.
  • Ritz D, Kinzi J, Neri D, et al. Data-independent acquisition of HLA class I peptidomes on the Q exactive mass spectrometer platform. Proteomics. 2017;17:19.
  • Ritz D, Sani E, Debiec H, et al. Membranal and blood-soluble HLA class II peptidome analyses using data-dependent and independent acquisition. Proteomics. 2018;18(12):e1700246.
  • Schittenhelm RB, Sivaneswaran S, Lim Kam Sian TC, et al. Human Leukocyte Antigen (HLA) B27 allotype-specific binding and candidate arthritogenic peptides revealed through heuristic clustering of Data-independent Acquisition Mass Spectrometry (DIA-MS) Data. Molecular & Cellular Proteomics: MCP. 2016;15(6):1867–1876.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.