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Immunoproteomics Methods and Techniques

  • Kelly M. Fulton
  • Isabel Baltat
  • Susan M. TwineEmail author
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 2024)

Abstract

The varied landscape of the adaptive immune response is determined by the peptides presented by immune cells, derived from viral or microbial pathogens or cancerous cells. The study of immune biomarkers or antigens is not new, and classical methods such as agglutination, enzyme-linked immunosorbent assay, or Western blotting have been used for many years to study the immune response to vaccination or disease. However, in many of these traditional techniques, protein or peptide identification has often been the bottleneck. Recent progress in genomics and mass spectrometry have led to many of the rapid advances in proteomics approaches. Immunoproteomics describes a rapidly growing collection of approaches that have the common goal of identifying and measuring antigenic peptides or proteins. This includes gel-based, array-based, mass spectrometry-based, DNA-based, or in silico approaches. Immunoproteomics is yielding an understanding of disease and disease progression, vaccine candidates, and biomarkers. This review gives an overview of immunoproteomics and closely related technologies that are used to define the full set of protein antigens targeted by the immune system during disease.

Key words

Immunoproteomics Mass spectrometry Antibody Antigen Cancer Infectious disease SERPA SEREX MHC Epitope 

References

  1. 1.
    Jungblut PR (2001) Proteome analysis of bacterial pathogens. Microbes Infect 3:831–840PubMedCrossRefGoogle Scholar
  2. 2.
    Aebersold R, Mann M (2003) Mass spectrometry-based proteomics. Nature 422:198–207PubMedCrossRefGoogle Scholar
  3. 3.
    Bantscheff M, Lemeer S, Savitski MM, Kuster B (2012) Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal Bioanal Chem 404:939–965PubMedCrossRefGoogle Scholar
  4. 4.
    Tabb DL, Vega-Montoto L, Rudnick PA et al (2009) Repeatability and reproducibility in proteomic identifications by liquid chromatography-tandem mass spectrometry. J Proteome Res 9:761–776CrossRefGoogle Scholar
  5. 5.
    Venable JD, Dong M-Q, Wohlschlegel J et al (2004) Automated approach for quantitative analysis of complex peptide mixtures from tandem mass spectra. Nat Methods 1:39–45PubMedCrossRefGoogle Scholar
  6. 6.
    Gillet LC, Navarro P, Tate S et al (2012) Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis. Mol Cell Proteomics 11:O111.016717PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Lange V, Picotti P, Domon B, Aebersold R (2008) Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 4:222PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Picotti P, Rinner O, Stallmach R et al (2010) High-throughput generation of selected reaction-monitoring assays for proteins and proteomes. Nat Methods 7:43–46PubMedCrossRefGoogle Scholar
  9. 9.
    Westermeier R (2016) Electrophoresis in practice: a guide to methods and applications of DNA and protein separations. Wiley, Hoboken, NJCrossRefGoogle Scholar
  10. 10.
    Pajuaba ACAM, Silva DAO, Almeida KC et al (2012) Immunoproteomics of Brucella abortus reveals differential antibody profiles between S19-vaccinated and naturally infected cattle. Proteomics 12:820–831PubMedCrossRefGoogle Scholar
  11. 11.
    Cha HJ, Yoon HG, Kim YW et al (1998) Molecular and enzymatic characterization of a maltogenic amylase that hydrolyzes and transglycosylates acarbose. Eur J Biochem 253:251–262PubMedCrossRefGoogle Scholar
  12. 12.
    Hamrita B, Chahed K, Kabbage M et al (2008) Identification of tumor antigens that elicit a humoral immune response in breast cancer patients’ sera by serological proteome analysis (SERPA). Clin Chim Acta 393:95–102PubMedCrossRefGoogle Scholar
  13. 13.
    Li L, Chen S-H, Yu C-H et al (2008) Identification of hepatocellular-carcinoma-associated antigens and autoantibodies by serological proteome analysis combined with protein microarray. J Proteome Res 7:611–620PubMedCrossRefGoogle Scholar
  14. 14.
    Forgber M, Gellrich S, Sharav T et al (2009) Proteome-based analysis of serologically defined tumor-associated antigens in cutaneous lymphoma. PLoS One 4:e8376PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Forgber M, Trefzer U, Sterry W, Walden P (2009) Proteome serological determination of tumor-associated antigens in melanoma. PLoS One 4:e5199PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Mou Z, He Y, Wu Y (2009) Immunoproteomics to identify tumor-associated antigens eliciting humoral response. Cancer Lett 278:123–129PubMedCrossRefGoogle Scholar
  17. 17.
    Shukla S, Pranay A, D’Cruz AK et al (2009) Immunoproteomics reveals that cancer of the tongue and the gingivobuccal complex exhibit differential autoantibody response. Cancer Biomark 5:127–135PubMedCrossRefGoogle Scholar
  18. 18.
    Liu R, Wang K, Yuan K et al (2010) Integrative oncoproteomics strategies for anticancer drug discovery. Expert Rev Proteomics 7:411–429PubMedCrossRefGoogle Scholar
  19. 19.
    Suzuki A, Iizuka A, Komiyama M et al (2010) Identification of melanoma antigens using a Serological Proteome Approach (SERPA). Cancer Genomics Proteomics 7:17–23PubMedGoogle Scholar
  20. 20.
    Mojtahedi Z, Safaei A, Yousefi Z, Ghaderi A (2011) Immunoproteomics of HER2-positive and HER2-negative breast cancer patients with positive lymph nodes. OMICS 15:409–418PubMedCrossRefGoogle Scholar
  21. 21.
    O’Meara MM, Disis ML (2011) Therapeutic cancer vaccines and translating vaccinomics science to the global health clinic: emerging applications toward proof of concept. OMICS 15:579–588PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Almeras L, Lefranc D, Drobecq H et al (2004) New antigenic candidates in multiple sclerosis: identification by serological proteome analysis. Proteomics 4:2184–2194PubMedCrossRefGoogle Scholar
  23. 23.
    Gupta S, Manubhai KP, Mukherjee S, Srivastava S (2017) Serum profiling for identification of autoantibody signatures in diseases using protein microarrays. Methods Mol Biol 1619:303–315PubMedCrossRefGoogle Scholar
  24. 24.
    Fang Y, Frutos AG, Lahiri J (2002) Membrane protein microarrays. J Am Chem Soc 124:2394–2395PubMedCrossRefGoogle Scholar
  25. 25.
    Shin I, Cho JW, Boo DW (2004) Carbohydrate arrays for functional studies of carbohydrates. Comb Chem High Throughput Screen 7:565–574PubMedCrossRefGoogle Scholar
  26. 26.
    Davies DH, Liang X, Hernandez JE et al (2005) Profiling the humoral immune response to infection by using proteome microarrays: high-throughput vaccine and diagnostic antigen discovery. Proc Natl Acad Sci U S A 102:547–552PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Eyles JE, Unal B, Hartley MG et al (2007) Immunodominant Francisella tularensis antigens identified using proteome microarray. Proteomics 7:2172–2183PubMedCrossRefGoogle Scholar
  28. 28.
    Sundaresh S, Doolan DL, Hirst S et al (2006) Identification of humoral immune responses in protein microarrays using DNA microarray data analysis techniques. Bioinformatics 22:1760–1766PubMedCrossRefGoogle Scholar
  29. 29.
    Díez P, Dasilva N, González-González M et al (2012) Data analysis strategies for protein microarrays. Microarrays (Basel) 1:64–83CrossRefGoogle Scholar
  30. 30.
    Davies DH, Molina DM, Wrammert J et al (2007) Proteome-wide analysis of the serological response to vaccinia and smallpox. Proteomics 7:1678–1686PubMedCrossRefGoogle Scholar
  31. 31.
    Benhnia MR-E-I, Maybeno M, Blum D et al (2013) Unusual features of vaccinia virus extracellular virion form neutralization resistance revealed in human antibody responses to the smallpox vaccine. J Virol 87:1569–1585PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Pugh C, Keasey S, Korman L, Pittman PR (2014) Human antibody responses to the polyclonal Dryvax vaccine for smallpox prevention can be distinguished from responses to the monoclonal replacement vaccine ACAM2000. Clin Vaccine Immunol 21(6):877–885PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Cruz-Fisher MI, Cheng C, Sun G et al (2011) Identification of immunodominant antigens by probing a whole Chlamydia trachomatis open reading frame proteome microarray using sera from immunized mice. Infect Immun 79:246–257PubMedCrossRefGoogle Scholar
  34. 34.
    Teng A, Cruz-Fisher MI, Cheng C et al (2012) Proteomic identification of immunodominant chlamydial antigens in a mouse model. J Proteome 77:176–186CrossRefGoogle Scholar
  35. 35.
    Kunnath-Velayudhan S, Salamon H, Wang H-Y et al (2010) Dynamic antibody responses to the Mycobacterium tuberculosis proteome. Proc Natl Acad Sci U S A 107:14703–14708PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Kunnath-Velayudhan S, Davidow AL, Wang H-Y et al (2012) Proteome-scale antibody responses and outcome of Mycobacterium tuberculosis infection in nonhuman primates and in tuberculosis patients. J Infect Dis 206:697–705PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Cao SH, Chen YQ, Sun Y et al (2018) Screening of serum biomarkers for distinguishing between latent and active tuberculosis using proteome microarray. Biomed Environ Sci 31:515–526PubMedGoogle Scholar
  38. 38.
    Deng J, Bi L, Zhou L et al (2014) Mycobacterium tuberculosis proteome microarray for global studies of protein function and immunogenicity. Cell Rep 9:2317–2329PubMedCrossRefGoogle Scholar
  39. 39.
    Suwannasaen D, Mahawantung J, Chaowagul W et al (2011) Human immune responses to Burkholderia pseudomallei characterized by protein microarray analysis. J Infect Dis 203:1002–1011PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Barbour AG, Jasinskas A, Kayala MA et al (2008) A genome-wide proteome array reveals a limited set of immunogens in natural infections of humans and white-footed mice with Borrelia burgdorferi. Infect Immun 76:3374–3389PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Sundaresh S, Randall A, Unal B et al (2007) From protein microarrays to diagnostic antigen discovery: a study of the pathogen Francisella tularensis. Bioinformatics 23:i508–i518PubMedCrossRefGoogle Scholar
  42. 42.
    Barry AE, Trieu A, Fowkes FJI et al (2011) The stability and complexity of antibody responses to the major surface antigen of Plasmodium falciparum are associated with age in a malaria endemic area. Mol Cell Proteomics 10:M111.008326PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Nnedu ON, O’Leary MP, Mutua D et al (2011) Humoral immune responses to Plasmodium falciparum among HIV-1-infected Kenyan adults. Proteomics Clin Appl 5:613–623PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Fan Y-T, Wang Y, Ju C et al (2013) Systematic analysis of natural antibody responses to P. falciparum merozoite antigens by protein arrays. J Proteome 78:148–158CrossRefGoogle Scholar
  45. 45.
    Doolan DL, Mu Y, Unal B et al (2008) Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics 8:4680–4694PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Zheng D, Wan J, Cho YG et al (2011) Comparison of humoral immune responses to Epstein-Barr virus and Kaposi’s sarcoma–associated herpesvirus using a viral proteome microarray. J Infect Dis 204:1683–1691PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Liu Z, Coghill AE, Pfeiffer RM et al (2018) Patterns of interindividual variability in the antibody repertoire targeting proteins across the Epstein-Barr virus proteome. J Infect Dis 217:1923–1931PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Dasgupta G, Chentoufi AA, Kalantari M et al (2012) Immunodominant “asymptomatic” herpes simplex virus 1 and 2 protein antigens identified by probing whole-ORFome microarrays with serum antibodies from seropositive asymptomatic versus symptomatic individuals. J Virol 86:4358–4369PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Kalantari-Dehaghi M, Chun S, Chentoufi AA et al (2012) Discovery of potential diagnostic and vaccine antigens in herpes simplex virus 1 and 2 by proteome-wide antibody profiling. J Virol 86:4328–4339PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Pérez-Bercoff L, Valentini D, Gaseitsiwe S et al (2014) Whole CMV proteome pattern recognition analysis after HSCT identifies unique epitope targets associated with the CMV status. PLoS One 9:e89648PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Conejero L, Patel N, de Reynal M et al (2011) Low-dose exposure of C57BL/6 mice to Burkholderia pseudomallei mimics chronic human melioidosis. Am J Pathol 179:270–280PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Cannella AP, Tsolis RM, Liang L et al (2012) Antigen-specific acquired immunity in human brucellosis: implications for diagnosis, prognosis, and vaccine development. Front Cell Infect Microbiol 2:1PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Lee S-J, Liang L, Juarez S et al (2012) Identification of a common immune signature in murine and human systemic Salmonellosis. Proc Natl Acad Sci U S A 109:4998–5003PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Darton TC, Baker S, Randall A et al (2017) Identification of novel serodiagnostic signatures of typhoid fever using a Salmonella proteome array. Front Microbiol 8:1794PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Liang L, Juarez S, Nga TVT et al (2013) Immune profiling with a Salmonella Typhi antigen microarray identifies new diagnostic biomarkers of human typhoid. Sci Rep 3:1043PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Beare PA, Chen C, Bouman T et al (2008) Candidate antigens for Q fever serodiagnosis revealed by immunoscreening of a Coxiella burnetii protein microarray. Clin Vaccine Immunol 15:1771–1779PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Vigil A, Chen C, Jain A et al (2011) Profiling the humoral immune response of acute and chronic Q fever by protein microarray. Mol Cell Proteomics 10:M110.006304PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Xiong X, Wang X, Wen B et al (2012) Potential serodiagnostic markers for Q fever identified in Coxiella burnetii by immunoproteomic and protein microarray approaches. BMC Microbiol 12:35PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Liang L, Döşkaya M, Juarez S et al (2011) Identification of potential serodiagnostic and subunit vaccine antigens by antibody profiling of toxoplasmosis cases in Turkey. Mol Cell Proteomics 10:M110.006916PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Legutki JB, Johnston SA (2013) Immunosignatures can predict vaccine efficacy. Proc Natl Acad Sci U S A 110:18614–18619PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    de Assis RR, Ludolf F, Nakajima R et al (2016) A next-generation proteome array for Schistosoma mansoni. Int J Parasitol 46:411–415PubMedCrossRefGoogle Scholar
  62. 62.
    Zhang A, Xiu B, Zhang H, Li N (2016) Protein microarray-mediated detection of antienterovirus antibodies in serum. J Int Med Res 44:287–296PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Runina AV, Katunin GL, Filippova MA et al (2018) Immunochip for syphilis serodiagnostics with the use of extended array of Treponema pallidum recombinant antigens. Bull Exp Biol Med 165:767–771PubMedCrossRefGoogle Scholar
  64. 64.
    Duarte JG, Blackburn JM (2017) Advances in the development of human protein microarrays. Expert Rev Proteomics 14:627–641PubMedCrossRefGoogle Scholar
  65. 65.
    Schweitzer B, Meng L, Mattoon D, Rai AJ (2010) Immune response biomarker profiling application on ProtoArray® protein microarrays. In: Rai AJ (ed) The urinary proteome: methods and protocols. Humana, Totowa, NJ, pp 243–252CrossRefGoogle Scholar
  66. 66.
    Creaney J, Dick IM, Musk AWB et al (2016) Immune response profiling of malignant pleural mesothelioma for diagnostic and prognostic biomarkers. Biomarkers 21:551–561PubMedCrossRefGoogle Scholar
  67. 67.
    Yang L, Wang J, Li J et al (2016) Identification of serum biomarkers for gastric cancer diagnosis using a human proteome microarray. Mol Cell Proteomics 15:614–623PubMedCrossRefGoogle Scholar
  68. 68.
    Ayoglu B, Schwenk JM, Nilsson P (2016) Antigen arrays for profiling autoantibody repertoires. Bioanalysis 8:1105–1126PubMedCrossRefGoogle Scholar
  69. 69.
    Hakomori S (2002) Glycosylation defining cancer malignancy: new wine in an old bottle. Proc Natl Acad Sci U S A 99:10231–10233PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Coenen D, Verschueren P, Westhovens R, Bossuyt X (2007) Technical and diagnostic performance of 6 assays for the measurement of citrullinated protein/peptide antibodies in the diagnosis of rheumatoid arthritis. Clin Chem 53:498–504PubMedCrossRefGoogle Scholar
  71. 71.
    Hiki Y (2009) O-linked oligosaccharides of the IgA1 hinge region: roles of its aberrant structure in the occurrence and/or progression of IgA nephropathy. Clin Exp Nephrol 13:415–423PubMedCrossRefGoogle Scholar
  72. 72.
    Schietinger A, Philip M, Yoshida BA et al (2006) A mutant chaperone converts a wild-type protein into a tumor-specific antigen. Science 314:304–308CrossRefGoogle Scholar
  73. 73.
    Wandall HH, Blixt O, Tarp MA et al (2010) Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer Res 70:1306–1313PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Rillahan CD, Paulson JC (2011) Glycan microarrays for decoding the glycome. Annu Rev Biochem 80:797–823PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Geissner A, Pereira CL, Leddermann M et al (2016) Deciphering antigenic determinants of Streptococcus pneumoniae serotype 4 capsular polysaccharide using synthetic oligosaccharides. ACS Chem Biol 11:335–344PubMedCrossRefGoogle Scholar
  76. 76.
    Padler-Karavani V (2016) Glycan microarray reveal the sweet side of cancer vaccines. Cell Chem Biol 23:1446–1447PubMedCrossRefGoogle Scholar
  77. 77.
    Smorodin EP, Kurtenkov OA, Shevchuk IN, Tanner RH (2005) The isolation and characterization of human natural alphaGal-specific IgG antibodies applicable to the detection of alphaGal-glycosphingolipids. J Immunoassay Immunochem 26:145–156PubMedCrossRefGoogle Scholar
  78. 78.
    Cheever MA, Allison JP, Ferris AS et al (2009) The prioritization of cancer antigens: a National Cancer Institute pilot project for the acceleration of translational research. Clin Cancer Res 15:5323–5337PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Reis CA, David L, Seixas M et al (1998) Expression of fully and under-glycosylated forms of MUC1 mucin in gastric carcinoma. Int J Cancer 79:402–410PubMedCrossRefGoogle Scholar
  80. 80.
    Brockhausen I (1999) Pathways of O-glycan biosynthesis in cancer cells. Biochim Biophys Acta 1473:67–95PubMedCrossRefGoogle Scholar
  81. 81.
    Goldstein DM, Gray NS, Zarrinkar PP (2008) High-throughput kinase profiling as a platform for drug discovery. Nat Rev Drug Discov 7:391–397PubMedCrossRefGoogle Scholar
  82. 82.
    Blixt O, Cló E, Nudelman AS et al (2011) A high-throughput O-glycopeptide discovery platform for seromic profiling. J Proteome Res 10:1436CrossRefGoogle Scholar
  83. 83.
    Kracun SK, Cló E, Clausen H et al (2010) Random glycopeptide bead libraries for seromic biomarker discovery. J Proteome Res 9:6705–6714PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Pedersen JW, Blixt O, Bennett EP et al (2011) Seromic profiling of colorectal cancer patients with novel glycopeptide microarray. Int J Cancer 128:1860–1871PubMedCrossRefGoogle Scholar
  85. 85.
    Burford B, Gentry-Maharaj A, Graham R et al (2013) Autoantibodies to MUC1 glycopeptides cannot be used as a screening assay for early detection of breast, ovarian, lung or pancreatic cancer. Br J Cancer 108:2045–2055PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Pedersen JW, Gentry-Maharaj A, Nøstdal A et al (2014) Cancer-associated autoantibodies to MUC1 and MUC4—a blinded case–control study of colorectal cancer in UK collaborative trial of ovarian cancer screening. Int J Cancer 134:2180–2188CrossRefGoogle Scholar
  87. 87.
    Chow JC, Young DW, Golenbock DT et al (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 274:10689–10692PubMedCrossRefGoogle Scholar
  88. 88.
    Poltorak A, Ricciardi-Castagnoli P, Citterio S, Beutler B (2000) Physical contact between lipopolysaccharide and Toll-like receptor 4 revealed by genetic complementation. Proc Natl Acad Sci U S A 97:2163–2167PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Girardin SE, Boneca IG, Viala J et al (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278:8869–8872PubMedCrossRefGoogle Scholar
  90. 90.
    Girardin SE, Hugot JP, Sansonetti PJ (2003) Lessons from Nod2 studies: towards a link between Crohn’s disease and bacterial sensing. Trends Immunol 24:652–658PubMedCrossRefGoogle Scholar
  91. 91.
    Girardin SE, Travassos LH, Hervé M et al (2003) Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J Biol Chem 278:41702–41708PubMedCrossRefGoogle Scholar
  92. 92.
    Girardin SE, Boneca IG, Carneiro LAM et al (2003) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300:1584–1587PubMedCrossRefGoogle Scholar
  93. 93.
    Verma A, Arora SK, Kuravi SK, Ramphal R (2005) Roles of specific amino acids in the N terminus of Pseudomonas aeruginosa flagellin and of flagellin glycosylation in the innate immune response. Infect Immun 73:8237–8246PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Doig P, Kinsella N, Guerry P, Trust TJ (1996) Characterization of a post-translational modification of Campylobacter flagellin: identification of a sero-specific glycosyl moiety. Mol Microbiol 19:379–387PubMedCrossRefGoogle Scholar
  95. 95.
    Horn C, Namane A, Pescher P et al (1999) Decreased capacity of recombinant 45/47-kDa molecules (Apa) of Mycobacterium tuberculosis to stimulate T lymphocyte responses related to changes in their mannosylation pattern. J Biol Chem 274:32023–32030PubMedCrossRefGoogle Scholar
  96. 96.
    Romain F, Horn C, Pescher P et al (1999) Deglycosylation of the 45/47-kilodalton antigen complex of Mycobacterium tuberculosis decreases its capacity to elicit in vivo or in vitro cellular immune responses. Infect Immun 67:5567–5572PubMedPubMedCentralGoogle Scholar
  97. 97.
    Logan SM, Kelly JF, Thibault P et al (2002) Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins. Mol Microbiol 46:587–597PubMedCrossRefGoogle Scholar
  98. 98.
    Mehta AS, Saile E, Zhong W et al (2006) Synthesis and antigenic analysis of the BclA glycoprotein oligosaccharide from the Bacillus anthracis exosporium. Chemistry 12:9136–9149PubMedCrossRefGoogle Scholar
  99. 99.
    Wang D, Carroll GT, Turro NJ et al (2007) Photogenerated glycan arrays identify immunogenic sugar moieties of Bacillus anthracis exosporium. Proteomics 7:180–184PubMedCrossRefGoogle Scholar
  100. 100.
    Dhénin SGY, Moreau V, Morel N et al (2008) Synthesis of an anthrose derivative and production of polyclonal antibodies for the detection of anthrax spores. Carbohydr Res 343:2101–2110PubMedCrossRefGoogle Scholar
  101. 101.
    Dhénin SGY, Moreau V, Nevers M-C et al (2009) Sensitive and specific enzyme immunoassays for antigenic trisaccharide from Bacillus anthracis spores. Org Biomol Chem 7:5184–5199PubMedCrossRefGoogle Scholar
  102. 102.
    Geissner A, Anish C, Seeberger PH (2014) Glycan arrays as tools for infectious disease research. Curr Opin Chem Biol 18:38–45PubMedCrossRefGoogle Scholar
  103. 103.
    Martin CE, Broecker F, Eller S et al (2013) Glycan arrays containing synthetic Clostridium difficile lipoteichoic acid oligomers as tools toward a carbohydrate vaccine. Chem Commun 49:7159–7161CrossRefGoogle Scholar
  104. 104.
    Shivatare SS, Shivatare VS, Wu C-Y, Wong C-H (2018) Chemo-enzymatic synthesis of N-glycans for array development and HIV antibody profiling. J Vis Exp.  https://doi.org/10.3791/55855
  105. 105.
    Ménová P, Sella M, Sellrie K et al (2018) Identification of the minimal glycotope of Streptococcus pneumoniae 7F capsular polysaccharide using synthetic oligosaccharides. Chemistry 24:4181–4187PubMedCrossRefGoogle Scholar
  106. 106.
    Lee S-Y, Jeoung D (2007) The reverse proteomics for identification of tumor antigens. J Microbiol Biotechnol 17:879–890PubMedGoogle Scholar
  107. 107.
    Sahin U, Türeci O, Pfreundschuh M (1997) Serological identification of human tumor antigens. Curr Opin Immunol 9:709–716PubMedCrossRefGoogle Scholar
  108. 108.
    Scanlan MJ, Gordan JD, Williamson B et al (1999) Antigens recognized by autologous antibody in patients with renal-cell carcinoma. Int J Cancer 83:456–464PubMedCrossRefGoogle Scholar
  109. 109.
    Scanlan MJ, Gout I, Gordon CM et al (2001) Humoral immunity to human breast cancer: antigen definition and quantitative analysis of mRNA expression. Cancer Immun 1:4PubMedGoogle Scholar
  110. 110.
    Vitale M (2013) SEREX: a promising approach for identification of thyroid cancer serological biomarkers. Clin Endocrinol 79:12–13CrossRefGoogle Scholar
  111. 111.
    Koroleva EP, Lagarkova MA, Mesheryakov AA et al (2002) Serological identification of antigens associated with renal cell carcinoma. Russ J Immunol 7:229–238PubMedGoogle Scholar
  112. 112.
    Devitt G, Meyer C, Wiedemann N et al (2006) Serological analysis of human renal cell carcinoma. Int J Cancer 118:2210–2219PubMedCrossRefGoogle Scholar
  113. 113.
    Kobayashi S, Hiwasa T, Arasawa T et al (2018) Identification of specific and common diagnostic antibody markers for gastrointestinal cancers by SEREX screening using testis cDNA phage library. Oncotarget 9:18559–18569PubMedPubMedCentralGoogle Scholar
  114. 114.
    Scanlan MJ, Chen YT, Williamson B et al (1998) Characterization of human colon cancer antigens recognized by autologous antibodies. Int J Cancer 76:652–658PubMedCrossRefGoogle Scholar
  115. 115.
    Line A, Slucka Z, Stengrevics A et al (2002) Characterisation of tumour-associated antigens in colon cancer. Cancer Immunol Immunother 51:574–582PubMedCrossRefGoogle Scholar
  116. 116.
    Ishikawa T, Fujita T, Suzuki Y et al (2003) Tumor-specific immunological recognition of frameshift-mutated peptides in colon cancer with microsatellite instability. Cancer Res 63:5564–5572PubMedGoogle Scholar
  117. 117.
    Garifulin OM, Kykot VO, Gridina NY et al (2015) Application of serex-analysis for identification of human colon cancer antigens. Exp Oncol 37:173–180PubMedCrossRefGoogle Scholar
  118. 118.
    Obata Y, Takahashi T, Tamaki H et al (1999) Identification of cancer antigens in breast cancer by the SEREX expression cloning method. Breast Cancer 6:305–311PubMedCrossRefGoogle Scholar
  119. 119.
    Forti S, Scanlan MJ, Invernizzi A et al (2002) Identification of breast cancer-restricted antigens by antibody screening of SKBR3 cDNA library using a preselected patient’s serum. Breast Cancer Res Treat 73:245–256PubMedCrossRefGoogle Scholar
  120. 120.
    Jäger D, Unkelbach M, Frei C et al (2002) Identification of tumor-restricted antigens NY-BR-1, SCP-1, and a new cancer/testis-like antigen NW-BR-3 by serological screening of a testicular library with breast cancer serum. Cancer Immun 2:5PubMedGoogle Scholar
  121. 121.
    Minenkova O, Pucci A, Pavoni E et al (2003) Identification of tumor-associated antigens by screening phage-displayed human cDNA libraries with sera from tumor patients. Int J Cancer 106:534–544PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Jäger D, Taverna C, Zippelius A, Knuth A (2004) Identification of tumor antigens as potential target antigens for immunotherapy by serological expression cloning. Cancer Immunol Immunother 53:144–147PubMedCrossRefGoogle Scholar
  123. 123.
    Qian F, Odunsi K, Blatt LM et al (2005) Tumor associated antigen recognition by autologous serum in patients with breast cancer. Int J Mol Med 15:137–144PubMedGoogle Scholar
  124. 124.
    Shimada H, Nakashima K, Ochiai T et al (2005) Serological identification of tumor antigens of esophageal squamous cell carcinoma. Int J Oncol 26:77–86PubMedGoogle Scholar
  125. 125.
    Jäger D (2007) Potential target antigens for immunotherapy identified by serological expression cloning (SEREX). In: Sioud M (ed) Target discovery and validation reviews and protocols. Springer, New York, pp 319–326Google Scholar
  126. 126.
    Kiyamova R, Kostianets O, Malyuchik S et al (2010) Identification of tumor-associated antigens from medullary breast carcinoma by a modified SEREX approach. Mol Biotechnol 46:105–112PubMedCrossRefGoogle Scholar
  127. 127.
    Song M-H, Ha J-C, Lee S-M et al (2011) Identification of BCP-20 (FBXO39) as a cancer/testis antigen from colon cancer patients by SEREX. Biochem Biophys Res Commun 408:195–201PubMedCrossRefGoogle Scholar
  128. 128.
    Kostianets O, Shyian M, Sergiy D et al (2012) Serological analysis of SEREX-defined medullary breast carcinoma-associated antigens. Cancer Investig 30:519–527CrossRefGoogle Scholar
  129. 129.
    Song M-H, Choi K-U, Shin D-H et al (2012) Identification of the cancer/testis antigens AKAP3 and CTp11 by SEREX in hepatocellular carcinoma. Oncol Rep 28:1792–1798PubMedCrossRefGoogle Scholar
  130. 130.
    Kostianets O, Shyyan M, Antoniuk SV et al (2017) Panel of SEREX-defined antigens for breast cancer autoantibodies profile detection. Biomarkers 22:149–156PubMedCrossRefGoogle Scholar
  131. 131.
    Chen Y-T, Scanlan MJ et al (1997) A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc Natl Acad Sci U S A 94:1914–1918PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Jäger E, Jäger D, Knuth A (1999) CTL-defined cancer vaccines: perspectives for active immunotherapeutic interventions in minimal residual disease. Cancer Metastasis Rev 18:143–150PubMedCrossRefGoogle Scholar
  133. 133.
    Heubeck B, Wendler O, Bumm K et al (2013) Tumor-associated antigenic pattern in squamous cell carcinomas of the head and neck—analysed by SEREX. Eur J Cancer 49:e1–e7PubMedCrossRefGoogle Scholar
  134. 134.
    Dyachenko L, Havrysh K, Lytovchenko A et al (2016) Autoantibody response to ZRF1 and KRR1 SEREX antigens in patients with breast tumors of different histological types and grades. Dis Markers 2016:5128720PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Hou Q, Chen K, Shan Z (2015) The construction of cDNA library and the screening of related antigen of ascitic tumor cells of ovarian cancer. Eur J Gynaecol Oncol 36:590–594PubMedGoogle Scholar
  136. 136.
    Izawa S, Okamura T, Matsuzawa K et al (2013) Autoantibody against WD repeat domain 1 is a novel serological biomarker for screening of thyroid neoplasia. Clin Endocrinol 79:35–42CrossRefGoogle Scholar
  137. 137.
    Jongeneel V (2001) Towards a cancer immunome database. Cancer Immun 1:3PubMedPubMedCentralGoogle Scholar
  138. 138.
    Muto M, Mori M, Hiwasa T et al (2015) Novel serum autoantibodies against talin1 in multiple sclerosis: possible pathogenetic roles of the antibodies. J Neuroimmunol 284:30–36PubMedCrossRefGoogle Scholar
  139. 139.
    Hao S, Fu R, Wang H, Shao Z (2017) Screening novel autoantigens targeted by serum IgG autoantibodies in immunorelated pancytopenia by SEREX. Int J Hematol 106:622–630PubMedCrossRefGoogle Scholar
  140. 140.
    Boder ET, Dane Wittrup K (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat Biotechnol 15:553–557PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    Mischo A, Wadle A, Wätzig K et al (2003) Recombinant antigen expression on yeast surface (RAYS) for the detection of serological immune responses in cancer patients. Cancer Immun 3:5PubMedPubMedCentralGoogle Scholar
  142. 142.
    Wadle A, Mischo A, Imig J et al (2005) Serological identification of breast cancer-related antigens from a Saccharomyces cerevisiae surface display library. Int J Cancer 117:104–113PubMedCrossRefGoogle Scholar
  143. 143.
    Kim M-S, Choi HY, Choi YS et al (2007) Optimized serological isolation of lung-cancer-associated antigens from a yeast surface-expressed cDNA library. J Microbiol Biotechnol 17:993–1001PubMedGoogle Scholar
  144. 144.
    Caron M, Choquet-Kastylevsky G, Joubert-Caron R (2007) Cancer immunomics using autoantibody signatures for biomarker discovery. Mol Cell Proteomics 6:1115–1122PubMedCrossRefGoogle Scholar
  145. 145.
    Hardouin J, Lasserre J-P, Canelle L et al (2007) Usefulness of autoantigens depletion to detect autoantibody signatures by multiple affinity protein profiling. J Sep Sci 30:352–358PubMedCrossRefGoogle Scholar
  146. 146.
    Hardouin J-P, Lasserre J, Sylvius L et al (2007) Cancer immunomics: from serological proteome analysis to multiple affinity protein profiling. Ann N Y Acad Sci 1107:223–230PubMedCrossRefGoogle Scholar
  147. 147.
    Roozendaal R, Carroll MC (2007) Complement receptors CD21 and CD35 in humoral immunity. Immunol Rev 219:157–166PubMedCrossRefGoogle Scholar
  148. 148.
    Solomon S, Kassahn D, Illges H (2005) The role of the complement and the Fc gamma R system in the pathogenesis of arthritis. Arthritis Res Ther 7:129–135PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Aibara N, Ichinose K, Baba M et al (2018) Proteomic approach to profiling immune complex antigens in cerebrospinal fluid samples from patients with central nervous system autoimmune diseases. Clin Chim Acta 484:26–31PubMedCrossRefGoogle Scholar
  150. 150.
    Croce MV, Fejes M, Riera N et al (1985) Clinical importance of circulating immune complexes in human acute lymphoblastic leukemia. Cancer Immunol Immunother 20:91–95PubMedCrossRefGoogle Scholar
  151. 151.
    Liu P, Overman RG, Yates NL et al (2011) Dynamic antibody specificities and virion concentrations in circulating immune complexes in acute to chronic HIV-1 infection. J Virol 85:11196–11207PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Hadi SA, Waters WR, Palmer M et al (2018) Development of a multidimensional proteomic approach to detect circulating immune complexes in cattle experimentally infected with Mycobacterium bovis. Front Vet Sci 5:141PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Ohyama K, Kuroda N (2012) Proteomic approaches to profiling the humoral immune response and identifying disease-associated antigens. Biol Pharm Bull 35:1409–1412PubMedCrossRefGoogle Scholar
  154. 154.
    Coppo R, Bosticardo GM, Basolo B et al (1982) Clinical significance of the detection of circulating immune complexes in lupus nephritis. Nephron 32:320–328PubMedCrossRefGoogle Scholar
  155. 155.
    Soltis RD, Hasz DE (1983) The effect of serum immunoglobulin concentration on immune complex detection by polyethylene glycol. J Immunol Methods 57:275–282PubMedCrossRefGoogle Scholar
  156. 156.
    Valentijn RM, van Overhagen H, Hazevoet HM et al (1985) The value of complement and immune complex determinations in monitoring disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 28:904–913PubMedCrossRefGoogle Scholar
  157. 157.
    Lock RJ, Unsworth DJ (2000) Measurement of immune complexes is not useful in routine clinical practice. Ann Clin Biochem 37:253–261PubMedCrossRefGoogle Scholar
  158. 158.
    Ohyama K, Ueki Y, Kawakami A et al (2011) Immune complexome analysis of serum and its application in screening for immune complex antigens in rheumatoid arthritis. Clin Chem 57:905–909CrossRefGoogle Scholar
  159. 159.
    Ohyama K, Kawakami A, Tamai M et al (2012) Serum immune complex containing thrombospondin-1: a novel biomarker for early rheumatoid arthritis. Ann Rheum Dis 71:1916–1917CrossRefGoogle Scholar
  160. 160.
    Ohyama K, Kuroda N (2013) Immune complexome analysis. Adv Clin Chem 60:129–141PubMedCrossRefGoogle Scholar
  161. 161.
    Aibara N, Kamohara C, Chauhan AK et al (2018) Selective, sensitive and comprehensive detection of immune complex antigens by immune complexome analysis with papain-digestion and elution. J Immunol Methods 461:85–90PubMedCrossRefGoogle Scholar
  162. 162.
    Baba M, Ohyama K, Kishikawa N, Kuroda N (2013) Optimization of separation and digestion conditions in immune complexome analysis. Anal Biochem 443:181–186CrossRefGoogle Scholar
  163. 163.
    Bhat S, Jagadeeshaprasad MG, Patil YR et al (2016) Proteomic insight reveals elevated levels of albumin in circulating immune complexes in diabetic plasma. Mol Cell Proteomics 15:2011–2020PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Ohyama K, Baba M, Tamai M et al (2015) Proteomic profiling of antigens in circulating immune complexes associated with each of seven autoimmune diseases. Clin Biochem 48:181–185CrossRefGoogle Scholar
  165. 165.
    Ohyama K, Yoshimi H, Aibara N et al (2017) Immune complexome analysis reveals the specific and frequent presence of immune complex antigens in lung cancer patients: a pilot study. Int J Cancer 140:370–380CrossRefGoogle Scholar
  166. 166.
    Ohyama K, Huy NT, Yoshimi H et al (2016) Proteomic profile of circulating immune complexes in chronic Chagas disease. Parasite Immunol 38:609–617CrossRefGoogle Scholar
  167. 167.
    Jamal F, Shivam P, Kumari S et al (2017) Identification of Leishmania donovani antigen in circulating immune complexes of visceral leishmaniasis subjects for diagnosis. PLoS One 12:e0182474PubMedPubMedCentralCrossRefGoogle Scholar
  168. 168.
    Aibara N, Ohyama K, Hidaka M et al (2018) Immune complexome analysis of antigens in circulating immune complexes from patients with acute cellular rejection after living donor liver transplantation. Transpl Immunol 48:60–64PubMedCrossRefGoogle Scholar
  169. 169.
    Beyer NH, Schou C, Houen G, Heegaard NHH (2008) Extraction and identification of electroimmunoprecipitated proteins from agarose gels. J Immunol Methods 330:24–33CrossRefGoogle Scholar
  170. 170.
    Grubb AO (1974) Crossed immunoelectrophoresis and electroimmunoassay of IgM. J Immunol 112:1420–1425PubMedGoogle Scholar
  171. 171.
    Grubb AO (1974) Crossed immunoelectrophoresis and electroimmunoassay of IgG. J Immunol 113:343–347PubMedGoogle Scholar
  172. 172.
    Laurell CB (1966) Quantitative estimation of proteins by electrophoresis in agarose gel containing antibodies. Anal Biochem 15:45–52CrossRefGoogle Scholar
  173. 173.
    Gershoni JM, Roitburd-Berman A, Siman-Tov DD et al (2007) Epitope mapping. BioDrugs 21:145–156PubMedCrossRefGoogle Scholar
  174. 174.
    Malito E, Carfi A, Bottomley MJ (2015) Protein crystallography in vaccine research and development. Int J Mol Sci 16:13106–13140PubMedPubMedCentralCrossRefGoogle Scholar
  175. 175.
    Becker W, Bhattiprolu KC, Gubensäk N, Zangger K (2018) Investigating protein-ligand interactions by solution nuclear magnetic resonance spectroscopy. ChemPhysChem 19:895–906PubMedPubMedCentralCrossRefGoogle Scholar
  176. 176.
    Opuni KFM, Al-Majdoub M, Yefremova Y et al (2018) Mass spectrometric epitope mapping. Mass Spectrom Rev 37:229–241PubMedCrossRefGoogle Scholar
  177. 177.
    Oganesyan I, Lento C, Wilson DJ (2018) Contemporary hydrogen deuterium exchange mass spectrometry. Methods 144:27–42PubMedCrossRefGoogle Scholar
  178. 178.
    Forsström B, Axnäs BB, Stengele K-P et al (2014) Proteome-wide epitope mapping of antibodies using ultra-dense peptide arrays. Mol Cell Proteomics 13:1585–1597PubMedPubMedCentralCrossRefGoogle Scholar
  179. 179.
    Pimenova T, Nazabal A, Roschitzki B et al (2008) Epitope mapping on bovine prion protein using chemical cross-linking and mass spectrometry. J Mass Spectrom 43:185–195PubMedCrossRefGoogle Scholar
  180. 180.
    Potocnakova L, Bhide M, Pulzova LB (2016) An introduction to B-cell epitope mapping and in silico epitope prediction. J Immunol Res 2016:6760830PubMedPubMedCentralCrossRefGoogle Scholar
  181. 181.
    Caron E, Kowalewski DJ, Chiek Koh C et al (2015) Analysis of major histocompatibility complex (MHC) immunopeptidomes using mass spectrometry. Mol Cell Proteomics 14:3105–3117PubMedPubMedCentralCrossRefGoogle Scholar
  182. 182.
    Adler M (2005) Immuno-PCR as a clinical laboratory tool. Adv Clin Chem 39:239–292PubMedCrossRefGoogle Scholar
  183. 183.
    Adler M, Wacker R, Niemeyer CM (2003) A real-time immuno-PCR assay for routine ultrasensitive quantification of proteins. Biochem Biophys Res Commun 308:240–250PubMedCrossRefGoogle Scholar
  184. 184.
    Dinarello CA (2007) Historical insights into cytokines. Eur J Immunol 37:S34–S45PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    Dinarello CA (2010) Anti-inflammatory agents: present and future. Cell 140:935–950PubMedPubMedCentralCrossRefGoogle Scholar
  186. 186.
    Stenken JA, Poschenrieder AJ (2015) Bioanalytical chemistry of cytokines—a review. Anal Chim Acta 853:95–115PubMedCrossRefGoogle Scholar
  187. 187.
    Bruserud O (2010) The chemokine system in experimental and clinical hematology. Springer Science & Business Media, BerlinCrossRefGoogle Scholar
  188. 188.
    Thorpe R, Wadhwa M, Bird CR, Mire-Sluis AR (1992) Detection and measurement of cytokines. Blood Rev 6:133–148PubMedCrossRefGoogle Scholar
  189. 189.
    Whiteside TL (2003) Chapter 61 - Assays for cytokines. In: Thomson AW, Lotze MT (eds) The cytokine handbook, 4th edn. Academic, London, pp 1375–1396CrossRefGoogle Scholar
  190. 190.
    Mire-Sluis AR, Page L, Thorpe R (1995) Quantitative cell line based bioassays for human cytokines. J Immunol Methods 187:191–199PubMedCrossRefGoogle Scholar
  191. 191.
    House RV (1999) Cytokine bioassays: an overview. Dev Biol Stand 97:13–19PubMedGoogle Scholar
  192. 192.
    Favre N, Bordmann G, Rudin W (1997) Comparison of cytokine measurements using ELISA, ELISPOT and semi-quantitative RT-PCR. J Immunol Methods 204:57–66PubMedCrossRefGoogle Scholar
  193. 193.
    Leng SX, McElhaney JE, Walston JD et al (2008) ELISA and multiplex technologies for cytokine measurement in inflammation and aging research. J Gerontol A Biol Sci Med Sci 63:879–884PubMedPubMedCentralCrossRefGoogle Scholar
  194. 194.
    Yu X, Schneiderhan-Marra N, Hsu H-Y et al (2009) Protein microarrays: effective tools for the study of inflammatory diseases. Methods Mol Biol 577:199–214PubMedCrossRefGoogle Scholar
  195. 195.
    Han K-C, Ahn D-R, Yang EG (2010) An approach to multiplexing an immunosorbent assay with antibody-oligonucleotide conjugates. Bioconjug Chem 21:2190–2196PubMedCrossRefGoogle Scholar
  196. 196.
    Szarka A, Rigó J Jr, Lázár L et al (2010) Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol 11:59PubMedPubMedCentralCrossRefGoogle Scholar
  197. 197.
    Yu X, Hartmann M, Wang Q et al (2010) μFBI: a microfluidic bead-based immunoassay for multiplexed detection of proteins from a μL sample volume. PLoS One 5.  https://doi.org/10.1371/journal.pone.0013125PubMedPubMedCentralCrossRefGoogle Scholar
  198. 198.
    Han K-C, Yang EG, Ahn D-R (2012) A highly sensitive, multiplex immunoassay using gold nanoparticle-enhanced signal amplification. Chem Commun 48:5895–5897CrossRefGoogle Scholar
  199. 199.
    Niemeyer CM, Adler M, Wacker R (2007) Detecting antigens by quantitative immuno-PCR. Nat Protoc 2:1918–1930PubMedCrossRefGoogle Scholar
  200. 200.
    Adler M, Wacker R, Niemeyer CM (2008) Sensitivity by combination: immuno-PCR and related technologies. Analyst 133:702–718PubMedCrossRefGoogle Scholar
  201. 201.
    Sano T, Smith CL, Cantor CR (1992) Immuno-PCR: very sensitive antigen detection by means of specific antibody-DNA conjugates. Science 258:120–122PubMedCrossRefGoogle Scholar
  202. 202.
    Kasai N, Kobayashi K, Shioya S et al (2012) Soluble heparin-binding EGF-like growth factor (HB-EGF) detected by newly developed immuno-PCR method is a clear-cut serological biomarker for ovarian cancer. Am J Transl Res 4:415–421PubMedPubMedCentralGoogle Scholar
  203. 203.
    Chia-Ching L, Subramaniam S, Sivasubramanian S, Feng-Huei L (2016) MWCNT-Fe3O4-based immuno-PCR for the early screening of nasopharyngeal carcinoma. Mater Sci Eng C Mater Biol Appl 61:422–428PubMedCrossRefGoogle Scholar
  204. 204.
    Kuczius T, Becker K, Fischer A, Zhang W (2012) Simultaneous detection of three CNS indicator proteins in complex suspensions using a single immuno-PCR protocol. Anal Biochem 431:4–10PubMedCrossRefGoogle Scholar
  205. 205.
    Malou N, Renvoise A, Nappez C, Raoult D (2012) Immuno-PCR for the early serological diagnosis of acute infectious diseases: the Q fever paradigm. Eur J Clin Microbiol Infect Dis 31:1951–1960PubMedCrossRefGoogle Scholar
  206. 206.
    Mehta PK, Dahiya B, Sharma S et al (2017) Immuno-PCR, a new technique for the serodiagnosis of tuberculosis. J Microbiol Methods 139:218–229PubMedCrossRefGoogle Scholar
  207. 207.
    Xie Q, Zhang J, Shao H et al (2016) Development of a novel immuno-PCR for detection of avian leukosis virus. J Virol Methods 236:25–28PubMedCrossRefGoogle Scholar
  208. 208.
    Mehta PK, Singh N, Dharra R et al (2016) Diagnosis of tuberculosis based on the detection of a cocktail of mycobacterial antigen 85B, ESAT-6 and cord factor by immuno-PCR. J Microbiol Methods 127:24–27PubMedCrossRefGoogle Scholar
  209. 209.
    Halpern MD, Molins CR, Schriefer M, Jewett MW (2014) Simple objective detection of human lyme disease infection using immuno-PCR and a single recombinant hybrid antigen. Clin Vaccine Immunol 21:1094–1105PubMedPubMedCentralCrossRefGoogle Scholar
  210. 210.
    Mehta PK, Raj A, Singh NP, Khuller GK (2014) Detection of potential microbial antigens by immuno-PCR (PCR-amplified immunoassay). J Med Microbiol 63:627–641PubMedCrossRefGoogle Scholar
  211. 211.
    Potůčková L, Franko F, Bambousková M, Dráber P (2011) Rapid and sensitive detection of cytokines using functionalized gold nanoparticle-based immuno-PCR, comparison with immuno-PCR and ELISA. J Immunol Methods 371:38–47PubMedCrossRefGoogle Scholar
  212. 212.
    Assumpção ALFV, da Silva RC (2016) Immuno-PCR in cancer and non-cancer related diseases: a review. Vet Q 36:63–70PubMedCrossRefGoogle Scholar
  213. 213.
    Chao H-Y, Wang Y-C, Tang S-S, Liu H-W (2004) A highly sensitive immuno-polymerase chain reaction assay for Clostridium botulinum neurotoxin type A. Toxicon 43:27–34PubMedCrossRefGoogle Scholar
  214. 214.
    Allen RC, Rogelj S, Cordova SE, Kieft TL (2006) An immuno-PCR method for detecting Bacillus thuringiensis Cry1Ac toxin. J Immunol Methods 308:109–115PubMedCrossRefGoogle Scholar
  215. 215.
    Fischer A, von Eiff C, Kuczius T et al (2007) A quantitative real-time immuno-PCR approach for detection of staphylococcal enterotoxins. J Mol Med 85:461–469PubMedCrossRefGoogle Scholar
  216. 216.
    Zhang W, Bielaszewska M, Pulz M et al (2008) New immuno-PCR assay for detection of low concentrations of shiga toxin 2 and its variants. J Clin Microbiol 46:1292–1297PubMedPubMedCentralCrossRefGoogle Scholar
  217. 217.
    He X, Qi W, Quiñones B et al (2011) Sensitive detection of Shiga toxin 2 and some of its variants in environmental samples by a novel immuno-PCR assay. Appl Environ Microbiol 77:3558–3564PubMedPubMedCentralCrossRefGoogle Scholar
  218. 218.
    Simonova MA, Pivovarov VD, Ryazantsev DY et al (2018) Comparative diagnostics of allergy using quantitative immuno-PCR and ELISA. Bioanalysis 10:757–767PubMedCrossRefGoogle Scholar
  219. 219.
    Rahmatpour S, Khan AH, Nasiri Kalmarzi R et al (2017) Application of immuno-PCR assay for the detection of serum IgE specific to Bermuda allergen. Mol Cell Probes 32:1–4PubMedCrossRefGoogle Scholar
  220. 220.
    Kolesnikov AV, Kozyr AV, Ryabko AK, Shemyakin IG (2016) Ultrasensitive detection of protease activity of anthrax and botulinum toxins by a new PCR-based assay. Pathog Dis 74:ftv112PubMedCrossRefGoogle Scholar
  221. 221.
    Lind K, Kubista M (2005) Development and evaluation of three real-time immuno-PCR assemblages for quantification of PSA. J Immunol Methods 304:107–116PubMedCrossRefGoogle Scholar
  222. 222.
    Niemeyer CM, Adler M, Wacker R (2005) Immuno-PCR: high sensitivity detection of proteins by nucleic acid amplification. Trends Biotechnol 23:208–216PubMedCrossRefGoogle Scholar
  223. 223.
    Malou N, Raoult D (2011) Immuno-PCR: a promising ultrasensitive diagnostic method to detect antigens and antibodies. Trends Microbiol 19:295–302PubMedCrossRefGoogle Scholar
  224. 224.
    Ryazantsev DY, Voronina DV, Zavriev SK (2016) Immuno-PCR: achievements and perspectives. Biochemistry 81:1754–1770PubMedGoogle Scholar
  225. 225.
    Chang L, Li J, Wang L (2016) Immuno-PCR: an ultrasensitive immunoassay for biomolecular detection. Anal Chim Acta 910:12–24PubMedCrossRefGoogle Scholar
  226. 226.
    Fuson KL, Zheng M, Craxton M et al (2009) Structural mapping of post-translational modifications in human interleukin-24: role of N-linked glycosylation and disulfide bonds in secretion and activity. J Biol Chem 284:30526–30533PubMedPubMedCentralCrossRefGoogle Scholar
  227. 227.
    Guzman NA, Phillips TM (2005) Immunoaffinity CE for proteomics studies. Anal Chem 77:60A–67ACrossRefGoogle Scholar
  228. 228.
    Guzman NA, Blanc T, Phillips TM (2008) Immunoaffinity capillary electrophoresis as a powerful strategy for the quantification of low-abundance biomarkers, drugs, and metabolites in biological matrices. Electrophoresis 29:3259–3278PubMedPubMedCentralCrossRefGoogle Scholar
  229. 229.
    Guzman NA, Phillips TM (2011) Immunoaffinity capillary electrophoresis: a new versatile tool for determining protein biomarkers in inflammatory processes. Electrophoresis 32:1565–1578PubMedGoogle Scholar
  230. 230.
    Boyle M, Hess J, Nuara A, Buller R (2006) Application of immunoproteomics to rapid cytokine detection. Methods 38:342–350PubMedCrossRefGoogle Scholar
  231. 231.
    Hortin GL, Sviridov D, Anderson NL (2008) High-abundance polypeptides of the human plasma proteome comprising the top 4 logs of polypeptide abundance. Clin Chem 54:1608–1616PubMedCrossRefGoogle Scholar
  232. 232.
    Björhall K, Miliotis T, Davidsson P (2005) Comparison of different depletion strategies for improved resolution in proteomic analysis of human serum samples. Proteomics 5:307–317PubMedCrossRefGoogle Scholar
  233. 233.
    Tirumalai RS, Chan KC, Prieto DA et al (2003) Characterization of the low molecular weight human serum proteome. Mol Cell Proteomics 2:1096–1103PubMedPubMedCentralCrossRefGoogle Scholar
  234. 234.
    Harper RG, Workman SR, Schuetzner S et al (2004) Low-molecular-weight human serum proteome using ultrafiltration, isoelectric focusing, and mass spectrometry. Electrophoresis 25:1299–1306PubMedCrossRefGoogle Scholar
  235. 235.
    Groessl M, Luksch H, Rösen-Wolff A et al (2012) Profiling of the human monocytic cell secretome by quantitative label-free mass spectrometry identifies stimulus-specific cytokines and proinflammatory proteins. Proteomics 12:2833–2842PubMedCrossRefGoogle Scholar
  236. 236.
    de Jesus JR, da Silva Fernandes R, de Souza Pessôa G et al (2017) Depleting high-abundant and enriching low-abundant proteins in human serum: an evaluation of sample preparation methods using magnetic nanoparticle, chemical depletion and immunoaffinity techniques. Talanta 170:199–209PubMedCrossRefGoogle Scholar
  237. 237.
    Wiederin J, Ciborowski P (2016) 6 - Immunoaffinity depletion of highly abundant proteins for proteomic sample preparation. In: Ciborowski P, Silberring J (eds) Proteomic profiling and analytical chemistry, 2nd edn. Elsevier, Boston, pp 101–114CrossRefGoogle Scholar
  238. 238.
    Alečković M, Wei Y, LeRoy G et al (2017) Identification of Nidogen 1 as a lung metastasis protein through secretome analysis. Genes Dev 31:1439–1455PubMedPubMedCentralCrossRefGoogle Scholar
  239. 239.
    Collins BC, Hunter CL, Liu Y et al (2017) Multi-laboratory assessment of reproducibility, qualitative and quantitative performance of SWATH-mass spectrometry. Nat Commun 8:291PubMedPubMedCentralCrossRefGoogle Scholar
  240. 240.
    Luo Y, Mok TS, Lin X et al (2017) SWATH-based proteomics identified carbonic anhydrase 2 as a potential diagnosis biomarker for nasopharyngeal carcinoma. Sci Rep 7:41191PubMedPubMedCentralCrossRefGoogle Scholar
  241. 241.
    Lin Q, Lim HSR, Lin HL et al (2015) Analysis of colorectal cancer glyco-secretome identifies laminin β-1 (LAMB1) as a potential serological biomarker for colorectal cancer. Proteomics 15:3905–3920PubMedCrossRefGoogle Scholar
  242. 242.
    Percy AJ, Chambers AG, Yang J et al (2014) Advances in multiplexed MRM-based protein biomarker quantitation toward clinical utility. Biochim Biophys Acta 1844:917–926PubMedCrossRefGoogle Scholar
  243. 243.
    Hugues S, Malherbe L, Filippi C, Glaichenhaus N (2002) Generation and use of alternative multimers of peptide/MHC complexes. J Immunol Methods 268:83–92PubMedCrossRefGoogle Scholar
  244. 244.
    Watts C, Moss CX, Mazzeo D et al (2003) Creation versus destruction of T cell epitopes in the class II MHC pathway. Ann N Y Acad Sci 987:9–14PubMedCrossRefGoogle Scholar
  245. 245.
    Saunders PM, van Endert P (2011) Running the gauntlet: from peptide generation to antigen presentation by MHC class I. Tissue Antigens 78:161–170PubMedCrossRefGoogle Scholar
  246. 246.
    Rudensky AY, Preston-Hurlburt P, Hong SC et al (1991) Sequence analysis of peptides bound to MHC class II molecules. Nature 353:622–627PubMedCrossRefGoogle Scholar
  247. 247.
    Rudensky AY, Preston-Hurlburt P, al-Ramadi BK et al (1992) Truncation variants of peptides isolated from MHC class II molecules suggest sequence motifs. Nature 359:429–431PubMedCrossRefGoogle Scholar
  248. 248.
    Engelhard VH (1994) Structure of peptides associated with MHC class I molecules. Curr Opin Immunol 6:13–23PubMedCrossRefGoogle Scholar
  249. 249.
    Engelhard VH (1994) Structure of peptides associated with class I and class II MHC molecules. Annu Rev Immunol 12:181–207PubMedCrossRefGoogle Scholar
  250. 250.
    Alfonso C, Karlsson L (2000) Nonclassical MHC class II molecules. Annu Rev Immunol 18:113–142PubMedCrossRefGoogle Scholar
  251. 251.
    Santambrogio L, Strominger JL (2006) The ins and outs of MHC class II proteins in dendritic cells. Immunity 25:857–859PubMedCrossRefGoogle Scholar
  252. 252.
    Cole DK (2015) The ultimate mix and match: making sense of HLA alleles and peptide repertoires. Immunol Cell Biol 93:515–516PubMedCrossRefGoogle Scholar
  253. 253.
    Storkus WJ, Zeh HJ III, Salter RD, Lotze MT (1993) Identification of T-cell epitopes: rapid isolation of class I-presented peptides from viable cells by mild acid elution. J Immunother Emphasis Tumor Immunol 14:94–103PubMedCrossRefGoogle Scholar
  254. 254.
    Rotzschke O, Falk K, Wallny HJ, Faath S (1990) Characterization of naturally occurring minor histocompatibility peptides including H-4 and HY. Science 249(4966):283–287PubMedCrossRefGoogle Scholar
  255. 255.
    Rötzschke O, Falk K, Deres K et al (1990) Isolation and analysis of naturally processed viral peptides as recognized by cytotoxic T cells. Nature 348:252–254PubMedCrossRefGoogle Scholar
  256. 256.
    Falk K, Rötzschke O, Rammensee HG (1990) Cellular peptide composition governed by major histocompatibility complex class I molecules. Nature 348:248–251PubMedCrossRefGoogle Scholar
  257. 257.
    Van Bleek GM, Nathenson SG (1990) Isolation of an endogenously processed immunodominant viral peptide from the class I H–2Kb molecule. Nature 348:213–216PubMedCrossRefGoogle Scholar
  258. 258.
    Duyar H, Dengjel J, de Graaf KL et al (2005) Peptide motif for the rat MHC class II molecule RT1.Da: similarities to the multiple sclerosis-associated HLA-DRB1∗1501 molecule. Immunogenetics 57:69–76PubMedCrossRefGoogle Scholar
  259. 259.
    Fissolo N, Haag S, de Graaf KL et al (2009) Naturally presented peptides on major histocompatibility complex I and II molecules eluted from central nervous system of multiple sclerosis patients. Mol Cell Proteomics 8:2090–2101PubMedPubMedCentralCrossRefGoogle Scholar
  260. 260.
    Wahlström J, Dengjel J, Persson B et al (2007) Identification of HLA-DR–bound peptides presented by human bronchoalveolar lavage cells in sarcoidosis. J Clin Invest 117:3576–3582PubMedPubMedCentralCrossRefGoogle Scholar
  261. 261.
    Demine R, Sherev T, Walden P (2003) Biochemical determination of natural tumor-associated T-cell epitopes. Mol Biotechnol 25:71–78PubMedCrossRefPubMedCentralGoogle Scholar
  262. 262.
    Verma B, Hawkins OE, Neethling FA et al (2010) Direct discovery and validation of a peptide/MHC epitope expressed in primary human breast cancer cells using a TCRm monoclonal antibody with profound antitumor properties. Cancer Immunol Immunother 59:563–573PubMedCrossRefPubMedCentralGoogle Scholar
  263. 263.
    McMurtrey CP, Lelic A, Piazza P et al (2008) Epitope discovery in West Nile virus infection: identification and immune recognition of viral epitopes. Proc Natl Acad Sci U S A 105:2981–2986PubMedPubMedCentralCrossRefGoogle Scholar
  264. 264.
    Hunt DF, Michel H, Dickinson TA et al (1992) Peptides presented to the immune system by the murine class II major histocompatibility complex molecule I-Ad. Science 256:1817–1820PubMedCrossRefGoogle Scholar
  265. 265.
    Lemmel C, Weik S, Eberle U et al (2004) Differential quantitative analysis of MHC ligands by mass spectrometry using stable isotope labeling. Nat Biotechnol 22:450–454PubMedCrossRefGoogle Scholar
  266. 266.
    Lanoix J, Durette C, Courcelles M et al (2018) Comparison of the MHC I immunopeptidome repertoire of B-cell lymphoblasts using two isolation methods. Proteomics 18:e1700251PubMedCrossRefGoogle Scholar
  267. 267.
    Jappe EC, Kringelum J, Trolle T, Nielsen M (2018) Predicted MHC peptide binding promiscuity explains MHC class I “hotspots” of antigen presentation defined by mass spectrometry eluted ligand data. Immunology 154:407–417PubMedPubMedCentralCrossRefGoogle Scholar
  268. 268.
    Rozanov DV, Rozanov ND, Chiotti KE et al (2018) MHC class I loaded ligands from breast cancer cell lines: a potential HLA-I-typed antigen collection. J Proteome 176:13–23CrossRefGoogle Scholar
  269. 269.
    Murphy JP, Konda P, Kowalewski DJ et al (2017) MHC-I ligand discovery using targeted database searches of mass spectrometry data: implications for T-cell immunotherapies. J Proteome Res 16:1806–1816CrossRefGoogle Scholar
  270. 270.
    Escobar H, Reyes-Vargas E, Jensen PE et al (2011) Utility of characteristic QTOF MS/MS fragmentation for MHC class I peptides. J Proteome Res 10:2494–2507PubMedCrossRefGoogle Scholar
  271. 271.
    Mommen GPM, Marino F, Meiring HD et al (2016) Sampling from the proteome to the HLA-DR ligandome proceeds via high specificity. Mol Cell Proteomics 15(4):1412–1423PubMedPubMedCentralCrossRefGoogle Scholar
  272. 272.
    Henderson RA, Cox AL, Sakaguchi K et al (1993) Direct identification of an endogenous peptide recognized by multiple HLA-A2.1-specific cytotoxic T cells. Proc Natl Acad Sci U S A 90:10275–10279PubMedPubMedCentralCrossRefGoogle Scholar
  273. 273.
    Cox AL, Skipper J, Chen Y et al (1994) Identification of a peptide recognized by five melanoma-specific human cytotoxic T cell lines. Science 264:716–719PubMedCrossRefGoogle Scholar
  274. 274.
    den Haan JM, Sherman NE, Blokland E et al (1995) Identification of a graft versus host disease-associated human minor histocompatibility antigen. Science 268:1476–1480CrossRefGoogle Scholar
  275. 275.
    Carralot J-P, Lemmel C, Stevanovic S, Pascolo S (2008) Mass spectrometric identification of an HLA-A∗0201 epitope from Plasmodium falciparum MSP-1. Int Immunol 20:1451–1456PubMedCrossRefGoogle Scholar
  276. 276.
    Hawkins OE, Vangundy RS, Eckerd AM et al (2008) Identification of breast cancer peptide epitopes presented by HLA-A∗0201. J Proteome Res 7:1445–1457PubMedCrossRefGoogle Scholar
  277. 277.
    Weinzierl AO, Maurer D, Altenberend F et al (2008) A cryptic vascular endothelial growth factor T-cell epitope: identification and characterization by mass spectrometry and T-cell assays. Cancer Res 68:2447–2454PubMedCrossRefGoogle Scholar
  278. 278.
    Seward RJ, Drouin EE, Steere AC, Costello CE (2010) Peptides presented by HLA-DR molecules in synovia of patients with rheumatoid arthritis or antibiotic-refractory Lyme arthritis. Mol Cell Proteomics 10:M110.002477PubMedPubMedCentralCrossRefGoogle Scholar
  279. 279.
    Sahin U, Derhovanessian E, Miller M et al (2017) Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer. Nature 547:222–226PubMedCrossRefGoogle Scholar
  280. 280.
    Yadav M, Jhunjhunwala S, Phung QT et al (2014) Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature 515:572–576PubMedCrossRefGoogle Scholar
  281. 281.
    Gygi SP, Rist B, Griffin TJ et al (2002) Proteome analysis of low-abundance proteins using multidimensional chromatography and isotope-coded affinity tags. J Proteome Res 1:47–54PubMedCrossRefGoogle Scholar
  282. 282.
    Ross PL, Huang YN, Marchese JN et al (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3:1154–1169PubMedCrossRefGoogle Scholar
  283. 283.
    Cagney G, Emili A (2002) De novo peptide sequencing and quantitative profiling of complex protein mixtures using mass-coded abundance tagging. Nat Biotechnol 20:163–170PubMedCrossRefGoogle Scholar
  284. 284.
    Bozzacco L, Yu H, Zebroski HA et al (2011) Mass spectrometry analysis and quantitation of peptides presented on the MHC II molecules of mouse spleen dendritic cells. J Proteome Res 10:5016–5030PubMedPubMedCentralCrossRefGoogle Scholar
  285. 285.
    Hogan KT, Sutton JN, Chu KU et al (2005) Use of selected reaction monitoring mass spectrometry for the detection of specific MHC class I peptide antigens on A3 supertype family members. Cancer Immunol Immunother 54:359–371PubMedCrossRefPubMedCentralGoogle Scholar
  286. 286.
    Ishioka GY, Lamont AG, Thomson D et al (1992) MHC interaction and T cell recognition of carbohydrates and glycopeptides. J Immunol 148:2446–2451PubMedPubMedCentralGoogle Scholar
  287. 287.
    Carbone FR, Gleeson PA (1997) Carbohydrates and antigen recognition by T cells. Glycobiology 7:725–730PubMedCrossRefPubMedCentralGoogle Scholar
  288. 288.
    Kastrup IB, Andersen MH, Elliott T, Haurum JS (2001) MHC-restricted T cell responses against posttranslationally modified peptide antigens. Adv Immunol 78:267–289PubMedCrossRefPubMedCentralGoogle Scholar
  289. 289.
    Kastrup IB, Stevanovic S, Arsequell G et al (2000) Lectin purified human class I MHC-derived peptides: evidence for presentation of glycopeptides in vivo. Tissue Antigens 56:129–135PubMedCrossRefGoogle Scholar
  290. 290.
    Haurum JS, Arsequell G, Lellouch AC et al (1994) Recognition of carbohydrate by major histocompatibility complex class I-restricted, glycopeptide-specific cytotoxic T lymphocytes. J Exp Med 180:739–744PubMedCrossRefGoogle Scholar
  291. 291.
    Haurum JS, Tan L, Arsequell G et al (1995) Peptide anchor residue glycosylation: effect on class I major histocompatibility complex binding and cytotoxic T lymphocyte recognition. Eur J Immunol 25:3270–3276PubMedCrossRefGoogle Scholar
  292. 292.
    Haurum JS, Høier IB, Arsequell G et al (1999) Presentation of cytosolic glycosylated peptides by human class I major histocompatibility complex molecules in vivo. J Exp Med 190:145–150PubMedPubMedCentralCrossRefGoogle Scholar
  293. 293.
    Glithero A, Tormo J, Haurum JS et al (1999) Crystal structures of two H-2Db/glycopeptide complexes suggest a molecular basis for CTL cross-reactivity. Immunity 10:63–74PubMedCrossRefGoogle Scholar
  294. 294.
    Zhang H, Li X-J, Martin DB, Aebersold R (2003) Identification and quantification of N-linked glycoproteins using hydrazide chemistry, stable isotope labeling and mass spectrometry. Nat Biotechnol 21:660–666PubMedCrossRefGoogle Scholar
  295. 295.
    Malaker SA, Ferracane MJ, Depontieu FR et al (2017) Identification and characterization of complex glycosylated peptides presented by the MHC class II processing pathway in melanoma. J Proteome Res 16:228–237PubMedCrossRefGoogle Scholar
  296. 296.
    Morita D, Sugita M (2016) Lipopeptides: a novel antigen repertoire presented by major histocompatibility complex class I molecules. Immunology 149:139–145PubMedPubMedCentralCrossRefGoogle Scholar
  297. 297.
    Andersen MH, Bonfill JE, Neisig A et al (1999) Phosphorylated peptides can be transported by TAP molecules, presented by class I MHC molecules, and recognized by phosphopeptide-specific CTL. J Immunol 163:3812–3818PubMedGoogle Scholar
  298. 298.
    Meyer VS, Drews O, Günder M et al (2009) Identification of natural MHC class II presented phosphopeptides and tumor-derived MHC class I phospholigands. J Proteome Res 8:3666–3674PubMedCrossRefGoogle Scholar
  299. 299.
    Zarling AL, Ficarro SB, White FM et al (2000) Phosphorylated peptides are naturally processed and presented by major histocompatibility complex class I molecules in vivo. J Exp Med 192:1755–1762PubMedPubMedCentralCrossRefGoogle Scholar
  300. 300.
    Mohammed F, Stones DH, Zarling AL et al (2017) The antigenic identity of human class I MHC phosphopeptides is critically dependent upon phosphorylation status. Oncotarget 8:54160–54172PubMedPubMedCentralGoogle Scholar
  301. 301.
    Zarling AL, Polefrone JM, Evans AM et al (2006) Identification of class I MHC-associated phosphopeptides as targets for cancer immunotherapy. Proc Natl Acad Sci U S A 103:14889–14894PubMedPubMedCentralCrossRefGoogle Scholar
  302. 302.
    Depontieu FR, Qian J, Zarling AL et al (2009) Identification of tumor-associated, MHC class II-restricted phosphopeptides as targets for immunotherapy. Proc Natl Acad Sci U S A 106:12073–12078PubMedPubMedCentralCrossRefGoogle Scholar
  303. 303.
    Li Y, Depontieu FR, Sidney J et al (2010) Structural basis for the presentation of tumor-associated MHC class II-restricted phosphopeptides to CD4+ T cells. J Mol Biol 399:596–603PubMedPubMedCentralCrossRefGoogle Scholar
  304. 304.
    Ferreira L, Sánchez-Juanes F, Munoz-Bellido JL, González-Buitrago JM (2011) Rapid method for direct identification of bacteria in urine and blood culture samples by matrix-assisted laser desorption ionization time-of-flight mass spectrometry: intact cell vs. extraction method. Clin Microbiol Infect 17:1007–1012PubMedCrossRefGoogle Scholar
  305. 305.
    Welker M (2011) Proteomics for routine identification of microorganisms. Proteomics 11:3143–3153PubMedCrossRefGoogle Scholar
  306. 306.
    Welker M, Moore ERB (2011) Applications of whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry in systematic microbiology. Syst Appl Microbiol 34:2–11PubMedCrossRefGoogle Scholar
  307. 307.
    Sogawa K, Watanabe M, Sato K et al (2012) Rapid identification of microorganisms by mass spectrometry: improved performance by incorporation of in-house spectral data into a commercial database. Anal Bioanal Chem 403:1811–1822PubMedCrossRefGoogle Scholar
  308. 308.
    El-Bouri K, Johnston S, Rees E et al (2012) Comparison of bacterial identification by MALDI-TOF mass spectrometry and conventional diagnostic microbiology methods: agreement, speed and cost implications. Br J Biomed Sci 69:47–55PubMedCrossRefGoogle Scholar
  309. 309.
    Ouedraogo R, Flaudrops C, Ben Amara A et al (2010) Global analysis of circulating immune cells by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. PLoS One 5:e13691PubMedPubMedCentralCrossRefGoogle Scholar
  310. 310.
    Ouedraogo R, Daumas A, Ghigo E et al (2012) Whole-cell MALDI-TOF MS: a new tool to assess the multifaceted activation of macrophages. J Proteome 75:5523–5532CrossRefGoogle Scholar
  311. 311.
    Portevin D, Pflüger V, Otieno P et al (2015) Quantitative whole-cell MALDI-TOF MS fingerprints distinguishes human monocyte sub-populations activated by distinct microbial ligands. BMC Biotechnol 15:24PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Kelly M. Fulton
    • 1
  • Isabel Baltat
    • 1
  • Susan M. Twine
    • 1
    Email author
  1. 1.Human Health Therapeutics Research CentreNational Research Council of CanadaOttawaCanada

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