High-throughput sequencing of the T-cell receptor repertoire: Pitfalls and opportunities

Briefings in Bioinformatics

Volumn 19, Issue 4, 2018, Pages 554-565

  Heather, James M ^a   Ismail, Mazlina ^b   Oakes, Theres ^b   Chain, Benny ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

generation of diversity; high throughput sequencing; immune repertoire; personalized biomarkers; somatic recombination; T cell receptor

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR;

ALGORITHM; ANTIBODY SPECIFICITY; DNA SEQUENCE; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; IMMUNOGLOBULIN VARIABLE REGION; IMMUNOLOGY; PROCEDURES; SOFTWARE; T LYMPHOCYTE;

ALGORITHMS; ANTIBODY DIVERSITY; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNOGLOBULIN VARIABLE REGION; RECEPTORS, ANTIGEN, T-CELL; SEQUENCE ANALYSIS, DNA; SOFTWARE; T-LYMPHOCYTES;

EID: 85052300336     PISSN: 14675463     EISSN: 14774054     Source Type: Journal    
DOI: 10.1093/bib/bbw138     Document Type: Article

References (106)

1. Alt FW, Oltz EM, Young F, et al. VDJ recombination. Immunol Today 1992; 13:306?14.
2. Krangel MS. Mechanics of T cell receptor gene rearrangement. Curr Opin Immunol 2009; 21:133?9.
3. Bernstein HJ. Recent changes to RasMol, recombining the variants. Trends Biochem Sci 2000; 25:453?5.
4. Vanhanen R, Heikkil?a N, Aggarwal K, et al. T cell receptor diversity in the human thymus. Mol Immunol 2016; 76:116?22.
5. Robins HS, Campregher PV, Srivastava SK, et al. Comprehensive assessment of T-cell receptor beta-chain diversity in alpha beta T cells. Blood 2009; 114:4099?107.
6. Heather JM, Chain B. The sequence of sequencers: the history of sequencing DNA. Genomics 2016;107:1?8.
7. Six A, Mariotti-Ferrandiz ME, Chaara W, et al. The past, present, and future of immune repertoire biology?the rise of next-generation repertoire analysis. Front Immunol 2013; 4:1?16.
8. Attaf M, Huseby E, Sewell AK. ab T cell receptors as predictors of health and disease. Cell Mol Immunol 2015; 12:391?9.
9. Robins H. Immunosequencing: applications of immune repertoire deep sequencing. Curr Opin Immunol 2013; 25:646?52.
10. Calis JJA, Rosenberg BR. Characterizing immune repertoires by high throughput sequencing: strategies and applications. Trends Immunol 2014; 35:581?90.
11. Mori A, Deola S, Xumerle L, et al. Next generation sequencing: new tools in immunology and hematology. Blood Res 2013; 48:242.
12. Woodsworth DJ, Castellarin M, Holt RA. Sequence analysis of T-cell repertoires in health and disease. Genome Med 2013; 5:98.
13. Hou X-L, Wang L, Ding Y-L, et al. Current status and recent advances of next generation sequencing techniques in immunological repertoire. Genes Immun 2016; 17:153?64.
14. Bentley DR, Balasubramanian S, Swerdlow HP, et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 2008; 456:53?9.
15. Heather JM, Best K, Oakes T, et al. Dynamic perturbations of the T-cell receptor repertoire in chronic hiv infection and following antiretroviral therapy. Front Immunol 2016; 6:
16. Mamedov IZ, Britanova OV, Zvyagin IV, et al. Preparing unbiased T-cell receptor and antibody cDNA libraries for the deep next generation sequencing profiling. Front Immunol 2013; 4:1?10.
17. Giudicelli V, Chaume D, Lefranc MP. IMGT/V-QUEST, an integrated software program for immunoglobulin and T cell receptor V-J and V-D-J rearrangement analysis. Nucleic Acids Res 2004; 32:435?40.
18. Alamyar E, Giudicelli V, Li S, et al. IMGT/HIGHV-QUEST: the IMGT web portal for immunoglobulin (Ig) or antibody and T cell receptor (TR) analysis from NGS high throughput and deep sequencing. Immunome Res 2012;8:26.
19. Ye J, Ma N, Madden TL, et al. IgBLAST: an immunoglobulin variable domain sequence analysis tool. Nucleic Acids Res 2013; 41:34?40.
20. Thomas N, Heather J, Ndifon W, et al. Decombinator: a tool for fast, efficient gene assignment in T-cell receptor sequences using a finite state machine. Bioinformatics 2013; 29:542?50.
21. Giraud M, Salson M, Duez M, et al. Fast multiclonal clusterization of V(D)J recombinations from high-throughput sequencing. BMC Genomics 2014; 15:409.
22. Bolotin DA, Poslavsky S, Mitrophanov I, et al. MiXCR: software for comprehensive adaptive immunity profiling. Nat Methods 2015; 12:380?1.
23. Zhang W, Du Y, Su Z, et al. IMonitor: a robust pipeline for TCR and BCR repertoire analysis. Genetics 2015; 201:459?72.
24. Kuchenbecker L, Nienen M, Hecht J, et al. IMSEQ?a fast and error aware approach to immunogenetic sequence analysis. Bioinformatics 2015; 31:btv309?2971.
25. Yu Y, Ceredig R, Seoighe C. LymAnalyzer: a tool for comprehensive analysis of next generation sequencing data of T cell receptors and immunoglobulins. Nucleic Acids Res 2016; 44:e31.
26. Yang X, Liu D, Lv N, et al. TCRklass: a new K-string-based algorithm for human and mouse TCR repertoire characterization. J. Immunol 2015; 194:446?54.
27. Gerritsen B, Pandit A, Andeweg AC, et al. RTCR: a pipeline for complete and accurate recovery of T cell repertoires from high throughput sequencing data. Bioinformatics 2016;32:3098?106.
28. Hung S, Chen Y, Chu C, et al. TRIg: a robust alignment pipeline for non- regular T-cell receptor and immunoglobulin sequences. BMC Bioinformatics 2016;17:433.
29. Lefranc MP, Giudicelli V, Busin C, et al. IMGT, the international ImMunoGeneTics database. Nucleic Acids Res 1998; 26:297?303.
30. Giudicelli V, Chaume D, Lefranc M-P. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res 2005; 33:D256?61.
31. Lefranc M-P, Giudicelli V, Ginestoux C, et al. IMGT, the international ImMunoGeneTics information system. Nucleic Acids Res 2009; 37:D1006?12.
32. Brochet X, Lefranc MP, Giudicelli V. IMGT/V-QUEST: the highly customized and integrated system for IG and TR standardized V-J and V-D-J sequence analysis. Nucleic Acids Res 2008; 36:503?8.
33. Li S, Lefranc M-P, Miles JJ, et al. IMGT/HighV QUEST paradigm for T cell receptor IMGT clonotype diversity and next generation repertoire immunoprofiling. Nat Commun 2013; 4:2333.
34. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012;9:357?9.
35. Tamura K, Hazama S, Yamaguchi R, et al. Characterization of the T cell repertoire by deep T cell receptor sequencing in tissues and blood from patients with advanced colorectal cancer. Oncol Lett 2016; 11:3643?9.
36. Kuchenbecker L, Nienen M, Hecht J, et al. IMSEQ?a fast and error aware approach to immunogenetic sequence analysis. Bioinformatics 2015; 31:2963?71.
37. Aho AV, Corasick MJ. Efficient string matching: an aid to bibliographic search. Commun ACM 1975;18:333?40.
38. Bolotin DA, Shugay M, Mamedov IZ, et al. MiTCR: software for T-cell receptor sequencing data analysis. Nat Methods 2013; 10:813?4.
39. Fisher JPH, Yan M, Heuijerjans J, et al. Neuroblastoma killing properties of Vd2 and Vd2-negative cdT cells following expansion by artificial antigen-presenting cells. Clin Cancer Res 2014; 20:5720?32.
40. Li B, Li T, Pignon J-C, et al. Landscape of tumor-infiltrating T cell repertoire of human cancers. Nat Genet 2016; 48:725?32.
41. Stubbington MJT, Lo?nnberg T, Proserpio V, et al. T cell fate and clonality inference from single-cell transcriptomes. Nat Methods 2016; 13:329?32.
42. Brown SD, Raeburn LA, Holt RA, et al. Profiling tissueresident T cell repertoires by RNA sequencing. Genome Med 2015; 7:125.
43. Redmond D, Poran A, Elemento O, et al. Single-cell TCRseq: paired recovery of entire T-cell alpha and beta chain transcripts in T-cell receptors from single-cell RNAseq. Genome Med 2016; 8:80.
44. Eltahla AA, Rizzetto S, Pirozyan MR, et al. Linking the T cell receptor to the single cell transcriptome in antigen-specific human T cells. Immunol Cell Biol 2016; 94:604?11.
45. Bjorkman PJ. MHC restriction in three dimensions: a view of T cell receptor/ligand interactions. Cell 1997; 89:167?70.
46. Cock PJA, Antao T, Chang JT, et al. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 2009; 25:1422?3.
47. Page`s H, Aboyoun P, Gentleman R, et al. Biostrings: String Objects Representing Biological Sequences, and Matching Algorithms. R package version 2. 42. 1, 2016.
48. Lefranc M-P. Immunoglobulin and T Cell Receptor Genes: IMGT(VR ) and the Birth and Rise of Immunoinformatics. Front Immunol 2014; 5:22.
49. Lefranc M-P, Pommie? C, Ruiz M, et al. IMGT unique numbering for immunoglobulin and T cell receptor variable domains and Ig superfamily V-like domains. Dev Comp Immunol 2003; 27:55?77.
50. Kinde I, Wu J, Papadopoulos N, et al. Detection and quantification of rare mutations with massively parallel sequencing. Proc Natl Acad Sci USA 2011;108:9530?5.
51. McInerney P, Adams P, Hadi MZ. Error rate comparison during polymerase chain reaction by DNA polymerase. Mol Biol Int 2014; 2014:287430.
52. Demotz S, Lanzavecchia A, Eisel U, et al. Delineation of several DR-restricted tetanus toxin T cell epitopes. J Immunol 1989; 142:394?402.
53. Warren RL, Freeman JD, Zeng T, et al. Exhaustive T-cell repertoire sequencing of human peripheral blood samples reveals signatures of antigen selection and a directly measured repertoire size of at least 1 million clonotypes. Genome Res 2011; 21:790?7.
54. Nguyen P, Ma J, Pei D, et al. Identification of errors introduced during high throughput sequencing of the T cell receptor repertoire. BMC Genomics 2011; 12:106.
55. Ewing B, Green P. Base-calling of automated sequencer traces using Phred. II. error probabilities. Genome Res 1998;8:186?94.
56. DePristo MA, Banks E, Poplin R, et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011; 43:491?8.
57. Schirmer M, Ijaz UZ, D?Amore R, et al. Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform. Nucleic Acids Res 2015; 43:1?16.
58. Robins H, Desmarais C, Matthis J, et al. Ultra-sensitive detection of rare T cell clones. J Immunol Methods 2011; 375:14?9.
59. Bolotin DA, Mamedov IZ, Britanova OV, et al. Next generation sequencing for TCR repertoire profiling: platformspecific features and correction algorithms. Eur J Immunol 2012; 42:3073?83.
60. Weinstein JA, Jiang N, White RA, et al. High-throughput sequencing of the zebrafish antibody repertoire. Science 2009; 324:807?10.
61. Kivioja T, V?ah?arautio A, Karlsson K, et al. Counting absolute numbers of molecules using unique molecular identifiers. Nat Methods 2012; 9:72?4.
62. Casbon JA, Osborne RJ, Brenner S, et al. A method for counting PCR template molecules with application to nextgeneration sequencing. Nucleic Acids Res 2011; 39:e81.
63. Fu GK, Hu J, Wang P-H, et al. Counting individual DNA molecules by the stochastic attachment of diverse labels. Proc Natl Acad Sci USA 2011; 108:9026?31.
64. Shugay M, Britanova OV, Merzlyak EM, et al. Towards errorfree profiling of immune repertoires. Nat Methods 2014; 11:653?5.
65. Best K, Oakes T, Heather JM, et al. Computational analysis of stochastic heterogeneity in PCR amplification efficiency revealed by single molecule barcoding. Sci Rep 2015; 5:14629.
66. Hall B, Micheletti JM, Satya P, et al. Design, synthesis, and amplification of DNA pools for in vitro selection. Curr Protoc Mol Biol 2009;Chapter 24:Unit 24. 2
67. Egorov ES, Merzlyak EM, Shelenkov AA, et al. Quantitative profiling of immune repertoires for minor lymphocyte counts using unique molecular identifiers. J Immunol 2015; 194:6155?63.
68. Freeman JD, Warren RL, Webb JR, et al. Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res 2009; 19:1817?24.
69. Nakamura K, Oshima T, Morimoto T, et al. Sequence-specific error profile of Illumina sequencers. Nucleic Acids Res 2011;39:e90.
70. Allhoff M, Scho?nhuth A, Martin M, et al. Discovering motifs that induce sequencing errors. BMC Bioinformatics 2013;14(Suppl 5):S1.
71. Schirmer M, D?Amore R, Ijaz UZ, et al. Illumina error profiles: resolving fine-scale variation in metagenomic sequencing data. BMC Bioinformatics 2016;17:125.
72. Murugan A, Mora T, Walczak AM, et al. Statistical inference of the generation probability of T-cell receptors from sequence repertoires. Proc Natl Acad Sci USA 2012;109:16161?6.
73. Gerlinger M, Quezada SA, Peggs KS, et al. Ultra-deep T-cell receptor sequencing reveals the complexity and intratumour heterogeneity of T-cell clones in renal cell carcinomas. J Pathol 2013;231:424?32.
74. Ciupe SM, Devlin BH, Markert ML, et al. Quantification of total T-cell receptor diversity by flowcytometry and spectratyping. BMC Immunol 2013; 14:35.
75. Gea-Banacloche JC, Martino L, Mican JM, et al. Longitudinal changes in CD4? T cell antigen receptor diversity and naive/ memory cell phenotype during 9 to 26 months of antiretroviral therapy of HIV-infected patients. AIDS Res Hum Retroviruses 2000; 16:1877?86.
76. Wu J, Liu D, Tu W, et al. T-cell receptor diversity is selectively skewed in T-cell populations of patients with Wiskott- Aldrich syndrome. J Allergy Clin Immunol 2015; 135:209?16.
77. Kou ZC, Puhr JS, Rojas M, et al. T-Cell receptor Vbeta repertoire CDR3 length diversity differs within CD45RA and CD45RO Tcell subsets in healthy and human immunodeficiency virusinfected children. Clin Diagn Lab Immunol 2000; 7:953?9.
78. Tembhare P, Yuan CM, Xi L, et al. Flow cytometric immunophenotypic assessment of T-cell clonality by Vbeta repertoire analysis: detection of T-cell clonality at diagnosis and monitoring of minimal residual disease following therapy. Am J Clin Pathol 2011; 135:890?900.
79. Ndifon W, Gal H, Shifrut E, et al. Chromatin conformation governs T-cell receptor Jb gene segment usage. Proc Natl Acad Sci USA 2012; 109:15865?70.
80. Gopalakrishnan S, Majumder K, Predeus A, et al. Unifying model for molecular determinants of the preselection Vb repertoire. Proc Natl Acad Sci USA 2013; 110:E3206?15.
81. Shugay M, Bagaev DV, Turchaninova MA, et al. VDJtools: unifying post-analysis of T cell receptor repertoires. PLoS Comput Biol 2015; 11:e1004503.
82. Nazarov VI, Pogorelyy MV, Komech EA, et al. tcR: an R package for T cell receptor repertoire advanced data analysis. BMC Bioinformatics 2015; 16:175.
83. Bystry V, Reigl T, Krejci A, et al. ARResT/Interrogate: an interactive immunoprofiler for IG/TR NGS data. Bioinformatics 2016; btw634.
84. Aouinti S, Giudicelli V, Duroux P, et al. IMGT/StatClonotype for pairwise evaluation and visualization of NGS IG and TR IMGT clonotype (AA) diversity or expression from IMGT/ HighV-QUEST. Front Immunol 2016; 7:339.
85. Wu D, Sherwood A, Fromm JR, et al. High-throughput sequencing detects minimal residual disease in acute T lymphoblastic leukemia. Sci Transl. Med 2012; 4:134ra63.
86. Wu D, Emerson RO, Sherwood A, et al. Detection of minimal residual disease in B lymphoblastic leukemia by highthroughput sequencing of IGH. Clin Cancer Res 2014; 20:4540?8.
87. Ferret Y, Caillault A, Sebda S, et al. Multi-loci diagnosis of acute lymphoblastic leukaemia with high-throughput sequencing and bioinformatics analysis. Br J Haematol 2016; 173:413?20.
88. Elhanati Y, Murugan A, Callan CG, et al. Quantifying selection in immune receptor repertoires. Proc Natl Acad Sci USA 2014; 111:9875?80.
89. Elhanati Y, Marcou Q, Mora T, et al. repgenHMM: a dynamic programming tool to infer the rules of immune receptor generation fromsequence data. Bioinformatics 2016; 32:1943?51.
90. Mora T, Walczak AM. Quantifying lymphocyte receptor diversity. bioRxiv 2016.
91. Laydon DJ, Bangham CRM, Asquith B. Estimating T-cell repertoire diversity: limitations of classical estimators and a new approach. Philos Trans R Soc Lond B Biol Sci 2015; 370.
92. Jost L. Entropy and diversity. Oikos 2006; 113:363?75.
93. Yu X, Almeida JR, Darko S, et al. Human syndromes of immunodeficiency and dysregulation are characterized by distinct defects in T-cell receptor repertoire development. J Allergy Clin Immunol 2014; 133:1109?15. e14.
94. Greiff V, Bhat P, Cook SC, et al. A bioinformatic framework for immune repertoire diversity profiling enables detection of immunological status. Genome Med 2015; 7:49.
95. Venturi V, Quigley MF, Greenaway HY, et al. A mechanism for TCR sharing between T cell subsets and individuals revealed by pyrosequencing. J Immunol 2011; 186:4285?94.
96. Iglesias MC, Almeida JR, Fastenackels S, et al. Escape from highly effective public CD8? T-cell clonotypes by HIV. Blood 2011; 118:2138?49.
97. Covacu R, Philip H, Jaronen M, et al. System-wide analysis of the T cell response. Cell Rep 2016; 14:2733?44.
98. Madi A, Shifrut E, Reich-Zeliger S, et al. T-cell receptor repertoires share a restricted set of public and abundant CDR3 sequences that are associated with self-related immunity. Genome Res 2014; 24:1603?12.
99. Miles JJ, Bulek AM, Cole DK, et al. Genetic and structural basis for selection of a ubiquitous T cell receptor deployed in Epstein-Barr virus infection. PLoS Pathog 2010; 6:e1001198.
100. Benati D, Galperin M, Lambotte O, et al. Public T cell receptors confer high-avidity CD4 responses to HIV controllers. J Clin Invest 2016; 126:2093?108.
101. Van Den Berg HA, Molina-Par_?s C, Sewell AK. Specific T-cell activation in an unspecific T-cell repertoire. Sci Prog 2011; 94:245?64.
102. Wooldridge L, Ekeruche-Makinde J, van den Berg HA, et al. A single autoimmune T cell receptor recognizes more than a million different peptides. J Biol Chem 2011; 287:1168?77.
103. Birnbaum ME, Mendoza JL, Sethi DK, et al. Deconstructing the peptide-MHC specificity of T cell recognition. Cell 2014; 157:1073?87.
104. Kosmrlj A, Jha AK, Huseby ES, et al. How the thymus designs antigen-specific and self-tolerant T cell receptor sequences. Proc Natl Acad Sci USA 2008; 105:16671?6.
105. Thomas N, Best K, Cinelli M, et al. Tracking global changes induced in the CD4 T-cell receptor repertoire by immunization with a complex antigen using short stretches of CDR3 protein sequence. Bioinformatics 2014; 30:1?8.
106. Kedzierska K, Turner SJ, Doherty PC. Conserved T cell receptor usage in primary and recall responses to an immunodominant influenza virus nucleoprotein epitope. Proc Natl Acad Sci USA 2004; 101:4942?7.