publication . Article . 2019

Detection of Enriched T Cell Epitope Specificity in Full T Cell Receptor Sequence Repertoires

Gielis, Sofie; Moris, Pieter; Bittremieux, Wout; De Neuter, Nicolas; Ogunjimi, Benson; Laukens, Kris; Meysman, Pieter;
Open Access English
  • Published: 29 Nov 2019 Journal: Frontiers in Immunology, volume 10 (issn: 1664-3224, Copyright policy)
  • Publisher: Frontiers Media SA
  • Country: Belgium
Abstract
Abstract: High-throughput T cell receptor (TCR) sequencing allows the characterization of an individual's TCR repertoire and directly queries their immune state. However, it remains a non-trivial task to couple these sequenced TCRs to their antigenic targets. In this paper, we present a novel strategy to annotate full TCR sequence repertoires with their epitope specificities. The strategy is based on a machine learning algorithm to learn the TCR patterns common to the recognition of a specific epitope. These results are then combined with a statistical analysis to evaluate the occurrence of specific epitope-reactive TCR sequences per epitope in repertoire data. ...
Persistent Identifiers
Subjects
Medical Subject Headings: chemical and pharmacologic phenomenahemic and immune systems
free text keywords: Human medicine, Computer. Automation, Immunology, Original Research, TCR repertoire analysis, epitope specificity, enrichment analysis, immunoinformatics, vaccines, infectious disease, cytomegalovirus (CMV), yellow fever virus (YFV)
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ZENODO
Article . 2019
Provider: ZENODO
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Frontiers
Article . 2019
Provider: Frontiers
35 references, page 1 of 3

1.Dewitt WS Emerson RO Lindau P Vignali M Snyder TM Desmarais C. Dynamics of the cytotoxic T cell response to a model of acute viral infection. J Virol. (2015) 89:4517–26. 10.1128/JVI.03474-14 25653453 [OpenAIRE] [PubMed] [DOI]

2.Pogorelyy MV Minervina AA Touzel MP Sycheva AL Komech EA Koval enko EI. Precise tracking of vaccine-responding T cell clones reveals convergent and personalized response in identical twins. PNAS. (2018) 115:12704–9. 10.1073/pnas.1809642115 30459272 [OpenAIRE] [PubMed] [DOI]

3.Pogorelyy MV Minervina AA Shugay M Chudakov DM Lebedev YB Mora T. Detecting T-cell receptors involved in immune responses from single repertoire snapshots. PLoS Biol. (2019) 17:e3000314. 10.1371/journal.pbio.3000314 31194732 [OpenAIRE] [PubMed] [DOI]

4.Sherwood A Emerson R Scherer D Habermann N Buck K Staffa J. Tumor-infiltrating lymphocytes in colorectal tumors display a diversity of T cell receptor sequences that differ from the T cells in adjacent mucosal tissue. Cancer Immunol Immunother. (2013) 62:1453–61. 10.1007/s00262-013-1446-2 23771160 [OpenAIRE] [PubMed] [DOI]

5.Ahmadzadeh M Pasetto A Jia L Deniger DC StevanovićS Robbins PF. Tumor-infiltrating human CD4 + regulatory T cells display a distinct TCR repertoire and exhibit tumor and neoantigen reactivity. Sci Immunol. (2019) 4:eaao4310. 10.1126/sciimmunol.aao4310 30635355 [OpenAIRE] [PubMed] [DOI]

6.Rius C Attaf M Tungatt K Bianchi V Legut M Bovay A. Peptide–MHC class I tetramers can fail to detec t relevant functional T cell clonotypes and underestimate antigen-reactive T cell populations. J Immunol. (2018) 200:2263–79. 10.4049/jimmunol.1700242 29483360 [OpenAIRE] [PubMed] [DOI]

7.Dolton G Zervoudi E Rius C Wall A Thomas HL Fuller A Optimized peptide – MHC multimer protocols for detection and isolation of autoimmune T-cells. Front Immunol. (2018) 9:1378 10.3389/fimmu.2018.01378 30008714 [OpenAIRE] [PubMed] [DOI]

8.Martin MD Jensen IJ Ishizuka AS Lefebvre M Shan Q Xue H-H. Bystander responses impact accurate detection of murine and human antigen-specific CD8 T cells. J Clin Invest. (2019) 13 0:3894–908. 10.1172/JCI124443 31219804 [OpenAIRE] [PubMed] [DOI]

9.Shugay M Bagaev DV Zvyagin IV Vroomans RM Crawford JC Dolton G. VDJdb: a curated database of T-cell receptor sequences with known antigen specificity. Nucleic Acids Res. (2018) 46:D419–27. 10.1093/nar/gkx760 28977646 [OpenAIRE] [PubMed] [DOI]

10.Tickotsky N Sagiv T Prilusky J Shifrut E Friedman N. McPAS-TCR: a manually curated catalogue of pathology-associated T cell receptor sequences. Bioinformatics. (2017) 33:2924–9. 10.1093/bioinformatics/btx286 28481982 [OpenAIRE] [PubMed] [DOI]

11.Meysman P De Neuter N Gielis S Bui Thi D Ogunjimi B Laukens K. On the viability of unsupervised T-cell receptor sequence clustering for epitope preference. Bioinformatics. (2019) 35:1461–8. 10.1093/bioinformatics/bty821 30247624 [OpenAIRE] [PubMed] [DOI]

12.De Neuter N Bittremieux W Beirnaert C Cuypers B Mrzic A Moris P. On the feasibility of mining CD8+ T cell receptor patterns underlying immunogenic peptide recognition. Immunogenetics. (2018) 70:159–68. 10.1007/s00251-017-1023-5 28779185 [OpenAIRE] [PubMed] [DOI]

13.Dash P Fiore-Gartland AJ Hertz T Wang GC Sharma S Souquette A. Quantifiable predictive features define epitope-specific T cell receptor repertoires. Nature. (2017) 547:89–93. 10.1038/nature22383 28636592 [OpenAIRE] [PubMed] [DOI]

14.Glanville J Huang H Nau A Hatton O Wagar LE Rubelt F. Identifying specificity groups in the T cell receptor repertoire. Nature. (2017) 547:94–8. 10.1038/nature22976 28636589 [OpenAIRE] [PubMed] [DOI]

15.Emerson RO DeWitt WS Vignali M Gravley J Hu JK Osborne EJ. Immunosequencing identifies signatures of cytomegalovirus exposure history and HLA-mediated effects on the T cell repertoire. Nat Genet. (2017) 49:659–65. 10.1038/ng.3822 28369038 [OpenAIRE] [PubMed] [DOI]

35 references, page 1 of 3
Abstract
Abstract: High-throughput T cell receptor (TCR) sequencing allows the characterization of an individual's TCR repertoire and directly queries their immune state. However, it remains a non-trivial task to couple these sequenced TCRs to their antigenic targets. In this paper, we present a novel strategy to annotate full TCR sequence repertoires with their epitope specificities. The strategy is based on a machine learning algorithm to learn the TCR patterns common to the recognition of a specific epitope. These results are then combined with a statistical analysis to evaluate the occurrence of specific epitope-reactive TCR sequences per epitope in repertoire data. ...
Persistent Identifiers
Subjects
Medical Subject Headings: chemical and pharmacologic phenomenahemic and immune systems
free text keywords: Human medicine, Computer. Automation, Immunology, Original Research, TCR repertoire analysis, epitope specificity, enrichment analysis, immunoinformatics, vaccines, infectious disease, cytomegalovirus (CMV), yellow fever virus (YFV)
Download fromView all 4 versions
Open Access
ZENODO
Article . 2019
Provider: ZENODO
Open Access
Frontiers
Article . 2019
Provider: Frontiers
35 references, page 1 of 3

1.Dewitt WS Emerson RO Lindau P Vignali M Snyder TM Desmarais C. Dynamics of the cytotoxic T cell response to a model of acute viral infection. J Virol. (2015) 89:4517–26. 10.1128/JVI.03474-14 25653453 [OpenAIRE] [PubMed] [DOI]

2.Pogorelyy MV Minervina AA Touzel MP Sycheva AL Komech EA Koval enko EI. Precise tracking of vaccine-responding T cell clones reveals convergent and personalized response in identical twins. PNAS. (2018) 115:12704–9. 10.1073/pnas.1809642115 30459272 [OpenAIRE] [PubMed] [DOI]

3.Pogorelyy MV Minervina AA Shugay M Chudakov DM Lebedev YB Mora T. Detecting T-cell receptors involved in immune responses from single repertoire snapshots. PLoS Biol. (2019) 17:e3000314. 10.1371/journal.pbio.3000314 31194732 [OpenAIRE] [PubMed] [DOI]

4.Sherwood A Emerson R Scherer D Habermann N Buck K Staffa J. Tumor-infiltrating lymphocytes in colorectal tumors display a diversity of T cell receptor sequences that differ from the T cells in adjacent mucosal tissue. Cancer Immunol Immunother. (2013) 62:1453–61. 10.1007/s00262-013-1446-2 23771160 [OpenAIRE] [PubMed] [DOI]

5.Ahmadzadeh M Pasetto A Jia L Deniger DC StevanovićS Robbins PF. Tumor-infiltrating human CD4 + regulatory T cells display a distinct TCR repertoire and exhibit tumor and neoantigen reactivity. Sci Immunol. (2019) 4:eaao4310. 10.1126/sciimmunol.aao4310 30635355 [OpenAIRE] [PubMed] [DOI]

6.Rius C Attaf M Tungatt K Bianchi V Legut M Bovay A. Peptide–MHC class I tetramers can fail to detec t relevant functional T cell clonotypes and underestimate antigen-reactive T cell populations. J Immunol. (2018) 200:2263–79. 10.4049/jimmunol.1700242 29483360 [OpenAIRE] [PubMed] [DOI]

7.Dolton G Zervoudi E Rius C Wall A Thomas HL Fuller A Optimized peptide – MHC multimer protocols for detection and isolation of autoimmune T-cells. Front Immunol. (2018) 9:1378 10.3389/fimmu.2018.01378 30008714 [OpenAIRE] [PubMed] [DOI]

8.Martin MD Jensen IJ Ishizuka AS Lefebvre M Shan Q Xue H-H. Bystander responses impact accurate detection of murine and human antigen-specific CD8 T cells. J Clin Invest. (2019) 13 0:3894–908. 10.1172/JCI124443 31219804 [OpenAIRE] [PubMed] [DOI]

9.Shugay M Bagaev DV Zvyagin IV Vroomans RM Crawford JC Dolton G. VDJdb: a curated database of T-cell receptor sequences with known antigen specificity. Nucleic Acids Res. (2018) 46:D419–27. 10.1093/nar/gkx760 28977646 [OpenAIRE] [PubMed] [DOI]

10.Tickotsky N Sagiv T Prilusky J Shifrut E Friedman N. McPAS-TCR: a manually curated catalogue of pathology-associated T cell receptor sequences. Bioinformatics. (2017) 33:2924–9. 10.1093/bioinformatics/btx286 28481982 [OpenAIRE] [PubMed] [DOI]

11.Meysman P De Neuter N Gielis S Bui Thi D Ogunjimi B Laukens K. On the viability of unsupervised T-cell receptor sequence clustering for epitope preference. Bioinformatics. (2019) 35:1461–8. 10.1093/bioinformatics/bty821 30247624 [OpenAIRE] [PubMed] [DOI]

12.De Neuter N Bittremieux W Beirnaert C Cuypers B Mrzic A Moris P. On the feasibility of mining CD8+ T cell receptor patterns underlying immunogenic peptide recognition. Immunogenetics. (2018) 70:159–68. 10.1007/s00251-017-1023-5 28779185 [OpenAIRE] [PubMed] [DOI]

13.Dash P Fiore-Gartland AJ Hertz T Wang GC Sharma S Souquette A. Quantifiable predictive features define epitope-specific T cell receptor repertoires. Nature. (2017) 547:89–93. 10.1038/nature22383 28636592 [OpenAIRE] [PubMed] [DOI]

14.Glanville J Huang H Nau A Hatton O Wagar LE Rubelt F. Identifying specificity groups in the T cell receptor repertoire. Nature. (2017) 547:94–8. 10.1038/nature22976 28636589 [OpenAIRE] [PubMed] [DOI]

15.Emerson RO DeWitt WS Vignali M Gravley J Hu JK Osborne EJ. Immunosequencing identifies signatures of cytomegalovirus exposure history and HLA-mediated effects on the T cell repertoire. Nat Genet. (2017) 49:659–65. 10.1038/ng.3822 28369038 [OpenAIRE] [PubMed] [DOI]

35 references, page 1 of 3
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