Estimating T-cell repertoire diversity: Limitations of classical estimators and a new approach

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 370, Issue 1675, 2015, Pages

  Laydon, Daniel J ^a   Bangham, Charles R M ^a   Asquith, Becca ^a  

^a IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

Author keywords

Diversity; Species richness; T cell receptor repertoire

Indexed keywords

BLOOD; DISEASE CONTROL; IMMUNE SYSTEM; PROTEIN; SPECIES DIVERSITY; SPECIES RICHNESS; VIRAL DISEASE;

LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; GENE REARRANGEMENT; GENETIC VARIATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; LYMPHOCYTE COUNT; NONPARAMETRIC TEST; T LYMPHOCYTE;

ANIMALS; GENE REARRANGEMENT, T-LYMPHOCYTE; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; HUMANS; LYMPHOCYTE COUNT; MODELS, GENETIC; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL; STATISTICS, NONPARAMETRIC; T-LYMPHOCYTES;

EID: 84936980441     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0291     Document Type: Article

References (96)

1. Nikolich-Zugich J, Slifka MK, Messaoudi I. 2004 The many important facets of T-cell repertoire diversity. Nat. Rev. Immunol. 4, 123-132. (doi:10. 1038/ nri1292)
2. Miles JJ, Douek DC, Price DA. 2011 Bias in the [α][β] T-cell repertoire: implications for disease pathogenesis and vaccination. Immunol. Cell Biol. 89, 375-387. (doi:10. 1038/icb. 2010. 139)
3. Bianconi E et al. 2013 An estimation of the number of cells in the human body. Ann. Hum. Biol. 40, 463-471. (doi:10. 3109/03014460. 2013. 807878)
4. Girardi M. 2006 Immunosurveillance and immunoregulation by [γ][δ] T cells. J. Invest. Dermatol. 126, 25-31. (doi:10. 1038/ sj. jid. 5700003)
5. Freeman JD, Warren RL, Webb JR, Nelson BH, Holt RA. 2009 Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res. 19, 1817-1824. (doi:10. 1101/gr. 092924. 109)
6. Wing JB, Sakaguchi S. 2011 TCR diversity and Treg cells, sometimes more is more. Eur. J. Immunol. 41, 3097-3100. (doi:10. 1002/eji. 201142115)
7. Venturi V, Kedzierska K, Price DA, Doherty PC, Douek DC, Turner SJ, Davenport MP. 2006 Sharing of T cell receptors in antigen-specific responses is driven by convergent recombination. Proc. Natl Acad. Sci. USA 103, 18 691-18 696. (doi:10. 1073/ pnas. 0608907103)
8. Venturi V, Price DA, Douek DC, Davenport MP. 2008 The molecular basis for public T-cell responses? Nat. Rev. Immunol. 8, 231-238. (doi:10. 1038/nri2260)
9. Quigley MF, Greenaway HY, Venturi V, Lindsay R, Quinn KM, Seder RA, Douek DC, Davenport MP, Price DA. 2010 Convergent recombination shapes the clonotypic landscape of the naïve T-cell repertoire. Proc. Natl Acad. Sci. USA 107, 19 414-19 419. (doi:10. 1073/pnas. 1010586107)
10. Epstein M, Barenco M, Klein N, Hubank M, Callard RE. 2014 Revealing individual signatures of human T cell CDR3 sequence repertoires with kidera factors. PLoS ONE 9, e86986. (doi:10. 1371/journal. pone. 0086986)
11. Turner SJ, Doherty PC, McCluskey J, Rossjohn J. 2006 Structural determinants of T-cell receptor bias in immunity. Nat. Rev. Immunol. 6, 883-894. (doi:10. 1038/nri1977)
12. Bercovici N, Duffour M-T, Agrawal S, Salcedo M, Abastado J-P. 2000 New methods for assessing T-cell responses. Clin. Diagn. Lab. Immunol. 7, 859-864.
13. Messaoudi I et al. 2002 Direct link between MHC polymorphism, T cell avidity, and diversity in immune defense. Science 298, 1797-1800. (doi:10. 1126/science. 1076064)
14. Davenport MP, Price DA, McMichael AJ. 2007 The T cell repertoire in infection and vaccination: implications for control of persistent viruses. Curr. Opin. Immunol. 19, 294-300. (doi:10. 1016/j. coi. 2007. 04. 001)
15. Chen H et al. 2012 TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat. Immunol. 13, 691-700. (doi:10. 1038/ni. 2342)
16. Naylor K et al. 2005 The influence of age on T cell generation and TCR diversity. J. Immunol. 174, 7446-7452. (doi:10. 4049/jimmunol. 174. 11. 7446)
17. Yager EJ, Ahmed M, Lanzer K, Randall TD, Woodland DL, Blackman MA. 2008 Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med. 205, 711-723. (doi:10. 1084/ jem. 20071140)
18. Boyd SD, Liu Y, Wang C, Martin V, Dunn-Walters DK. 2013 Human lymphocyte repertoires in ageing. Curr. Opin. Immunol. 25, 511-515. (doi:10. 1016/j. coi. 2013. 07. 007)
19. Qi Q et al. 2014 Diversity and clonal selection in the human T-cell repertoire. Proc. Natl Acad. Sci. USA 111, 13 139-13 144. (doi:10. 1073/pnas. 1409155111)
20. Meyer-Olson D et al. 2004 Limited T cell receptor diversity of HCV-specific T cell responses is associated with CTL escape. J. Exp. Med. 200, 307-319. (doi:10. 1084/jem. 20040638)
21. Long SA, Khalili J, Ashe J, Berenson R, Ferrand C, Bonyhadi M. 2006 Standardized analysis for the quantification of Vβ CDR3 T-cell receptor diversity. J. Immunol. Methods 317, 100-113. (doi:10. 1016/j. jim. 2006. 09. 015)
22. Höhn H, Neukirch C, Freitag K, Necker A, Hitzler W, Seliger B, Maeurer MJ. 2002 Longitudinal analysis of the T-cell receptor (TCR)-VA and-VB repertoire in CD8+ T cells from individuals immunized with recombinant hepatitis B surface antigen. Clin. Exp. Immunol. 129, 309-317. (doi:10. 1046/j. 1365-2249. 2002. 01841. x)
23. Muraro PA et al. 2014 T cell repertoire following autologous stem cell transplantation for multiple sclerosis. J. Clin. Invest. 124, 1168-1172. (doi:10. 1172/JCI71691)
24. Madi A, Shifrut E, Reich-Zeliger S, Gal H, Best K, Ndifon W, Chain B, Cohen IR, Friedman N. 2014 T-cell receptor repertoires share a restricted set of public and abundant CDR3 sequences that are associated with self-related immunity. Genome Res. 24, 1603-1612. (doi:10. 1101/gr. 170753. 113)
25. Ferreira C et al. 2009 Non-obese diabetic mice select a low-diversity repertoire of natural regulatory T cells. Proc. Natl Acad. Sci. USA 106, 8320-8325. (doi:10. 1073/pnas. 0808493106)
26. Matsumoto Y, Matsuo H, Sakuma H, Park I-K, Tsukada Y, Kohyama K, Kondo T, Kotorii S, Shibuya N. 2006 CDR3 spectratyping analysis of the TCR repertoire in Myasthenia gravis. J. Immunol. 176, 5100-5107. (doi:10. 4049/jimmunol. 176. 8. 5100)
27. Robins HS, Srivastava SK, Campregher PV, Turtle CJ, Andriesen J, Riddell SR, Carlson CS, Warren EH. 2010 Overlap and effective size of the human CD8+ T cell receptor repertoire. Sci. Translational Med. 2, 47ra64. (doi:10. 1126/scitranslmed. 3001442)
28. Venturi V et al. 2011 A mechanism for TCR sharing between T cell subsets and individuals revealed by pyrosequencing. J. Immunol. 186, 4285-4294. (doi:10. 4049/jimmunol. 1003898)
29. Mamedov IZ et al. 2011 Quantitative tracking of T cell clones after haematopoietic stem cell transplantation. EMBO Mol. Med. 3, 201-207. (doi:10. 1002/emmm. 201100129)
30. Weinstein JA, Jiang N, White RA, Fisher DS, Quake SR. 2009 High-throughput sequencing of the zebrafish antibody repertoire. Science 324, 807-810. (doi:10. 1126/science. 1170020)
31. Glanville J et al. 2009 Precise determination of the diversity of a combinatorial antibody library gives insight into the human immunoglobulin repertoire. Proc. Natl Acad. Sci. USA 106, 20 216-20 221. (doi:10. 1073/pnas. 0909775106)
32. Temperton B, Giovannoni SJ. 2012 Metagenomics: microbial diversity through a scratched lens. Curr. Opin. Microbiol. 15, 605-612. (doi:10. 1016/j. mib. 2012. 07. 001)
33. Shakya M, Quince C, Campbell JH, Yang ZK, Schadt CW, Podar M. 2013 Comparative metagenomic and rRNA microbial diversity characterization using archaeal and bacterial synthetic communities. Environ. Microbiol. 15, 1882-1899. (doi:10. 1111/ 1462-2920. 12086)
34. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R. 2006 Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439, 344-348. (doi:10. 1038/nature04388)
35. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. 2002 Lymphocytes and the cellular basis of adaptive immunity. In Molecular biology of the cell (eds B Alberts et al.), 4th edn. New York, NY: Garland Science. Available at http://www. ncbi. nlm. nih. gov/books/NBK26921/.
36. Arstila TP et al. 1999 A direct estimate of the human αβ T cell receptor diversity. Science 286, 958-961. (doi:10. 1126/science. 286. 5441. 958)
37. Klarenbeek PL et al. 2010 Human T-cell memory consists mainly of unexpanded clones. Immunol. Lett. 133, 42-48. (doi:10. 1016/j. imlet. 2010. 06. 011)
38. Casrouge A, Beaudoing E, Dalle S, Pannetier C, Kanellopoulos J, Kourilsky P. 2000 Size estimate of the αβ TCR repertoire of naive mouse splenocytes. J. Immunol. 164, 5782-5787. (doi:10. 4049/ jimmunol. 164. 11. 5782)
39. Wang C et al. 2010 High throughput sequencing reveals a complex pattern of dynamic interrelationships among human T cell subsets. Proc. Natl Acad. Sci. USA 107, 1518-1523. (doi:10. 1073/pnas. 0913939107)
40. Thomas N et al. 2014 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 30, 3181-3188. (doi:10. 1093/bioinformatics/btu523)
41. Rempala GA, Seweryn M, Ignatowicz L. 2011 Model for comparative analysis of antigen receptor repertoires. J. Theor. Biol. 269, 1-15. (doi:10. 1016/ j. jtbi. 2010. 10. 001)
42. Breit T, Wolvers-Tettero I, Beishuizen A, Verhoeven M, van Wering E, van Dongen JJ. 1993 Southern blot patterns, frequencies, and junctional diversity of T-cell receptor-delta gene rearrangements in acute lymphoblastic leukemia. Blood 82, 3063-3074.
43. Mizoguchi A, Mizoguchi E, Saubermann LJ, Higaki K, Blumberg RS, Bhan AK. 2000 Limited CD4 T-cell diversity associated with colitis in T-cell receptor α mutant mice requires a T helper 2 environment. Gastroenterology 119, 983-995. (doi:10. 1053/gast. 2000. 18153)
44. Swanson SJ, Rosenzweig A, Seidman JG, Libby P. 1994 Diversity of T-cell antigen receptor V beta gene utilization in advanced human atheroma. Arterioscler. Thromb. Vasc. Biol. 14, 1210-1214. (doi:10. 1161/01. ATV. 14. 7. 1210)
45. Wagner UG, Koetz K, Weyand CM, Goronzy JJ. 1998 Perturbation of the T cell repertoire in rheumatoid arthritis. Proc. Natl Acad. Sci. USA 95, 14 447-14 452. (doi:10. 1073/pnas. 95. 24. 14447)
46. Koga M, Yuki N, Tsukada Y, Hirata K, Matsumoto Y. 2003 CDR3 spectratyping analysis of the T cell receptor repertoire in Guillain-Barré and Fisher syndromes. J. Neuroimmunol. 141, 112-117. (doi:10. 1016/S0165-5728(03)00212-1)
47. Robins HS et al. 2009 Comprehensive assessment of T-cell receptor β-chain diversity in αβ T cells. Blood 114, 4099-4107. (doi:10. 1182/blood-2009-04-217604)
48. Gil A, Yassai MB, Naumov YN, Selin LK. 2015 Narrowing of human influenza A virus specific T cell receptor α and β repertoire with increasing age. J. Virol. 89, 4102-4116. (doi:10. 1128/JVI. 03020-14)
49. Bousso P et al. 2000 Diversity, functionality, and stability of the T cell repertoire derived in vivo from a single human T cell precursor. Proc. Natl Acad. Sci. USA 97, 274-278. (doi:10. 1073/pnas. 97. 1. 274)
50. Bolotin DA et al. 2012 Next generation sequencing for TCR repertoire profiling: platform-specific features and correction algorithms. Eur. J. Immunol. 42, 3073-3083. (doi:10. 1002/eji. 201242517)
51. He L et al. 2014 Toward a more accurate view of human B-cell repertoire by next-generation sequencing, unbiased repertoire capture and singlemolecule barcoding. Sci. Rep. 4, 6778. (doi:10. 1038/ srep06778)
52. Warren RL, Freeman JD, Zeng T, Choe G, Munro S, Moore R, Webb JR, Holt RA. 2011 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. 21, 790-797. (doi:10. 1101/gr. 115428. 110)
53. Laydon DJ et al. 2014 Quantification of HTLV-1 clonality and TCR diversity. PLoS Comput. Biol. 10, e1003646. (doi:10. 1371/journal. pcbi. 1003646)
54. Zarnitsyna V, Evavold B, Schoettle L, Blattman J, Antia R. 2013 Estimating the diversity, completeness, and cross-reactivity of the T cell repertoire. Front. Immunol. 4. (doi:10. 3389/fimmu. 2013. 00485)
55. Kivioja T, Vaharautio A, Karlsson K, Bonke M, Enge M, Linnarsson S, Taipale J. 2012 Counting absolute numbers of molecules using unique molecular identifiers. Nat. Methods 9, 72-74. (doi:10. 1038/ nmeth. 1778)
56. Gillet NA et al. 2011 The host genomic environment of the provirus determines the abundance of HTLV-1-infected T-cell clones. Blood 117, 3113-3122. (doi:10. 1182/blood-2010-10-312926)
57. Berry CC, Gillet NA, Melamed A, Gormley N, Bangham CRM, Bushman FD. 2012 Estimating abundances of retroviral insertion sites from DNA fragment length data. Bioinformatics 28, 755-762. (doi:10. 1093/bioinformatics/bts004)
58. Bunge J, Fitzpatrick M. 1993 Estimating the number of species: a review. J. Am. Stat. Assoc. 88, 364-373.
59. Sepúlveda N, Paulino CD, Carneiro J. 2010 Estimation of T-cell repertoire diversity and clonal size distribution by Poisson abundance models. J. Immunol. Methods 353, 124-137. (doi:10. 1016/j. jim. 2009. 11. 009)
60. Gotelli NJ, Colwell RK. 2001 Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379-391. (doi:10. 1046/j. 1461-0248. 2001. 00230. x)
61. May RM. 1988 How many species are there on earth? Science 241, 1441-1449. (doi:10. 1126/ science. 241. 4872. 1441)
62. Iknayan KJ, Tingley MW, Furnas BJ, Beissinger SR. 2014 Detecting diversity: emerging methods to estimate species diversity. Trends Ecol. Evol. 29, 97-106. (doi:10. 1016/j. tree. 2013. 10. 012)
63. Hsieh C-S, Zheng Y, Liang Y, Fontenot JD, Rudensky AY. 2006 An intersection between the self-reactive regulatory and nonregulatory T cell receptor repertoires. Nat. Immunol. 7, 401-410. (doi:10. 1038/ni1318)
64. + T cells. Immunity 25, 249-259. (doi:10. 1016/j. immuni. 2006. 05. 016)
65. Venturi V, Kedzierska K, Turner SJ, Doherty PC, Davenport MP. 2007 Methods for comparing the diversity of samples of the T cell receptor repertoire. J. Immunol. Methods 321, 182-195. (doi:10. 1016/j. jim. 2007. 01. 019)
66. Cebula A et al. 2013 Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota. Nature 497, 258-262. (doi:10. 1038/ nature12079)
67. Venturi V, Kedzierska K, Tanaka MM, Turner SJ, Doherty PC, Davenport MP. 2008 Method for assessing the similarity between subsets of the T cell receptor repertoire. J. Immunol. Methods 329, 67-80. (doi:10. 1016/j. jim. 2007. 09. 016)
68. Chao A. 1984 Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11, 265-270.
69. Chao A. 2005 Species estimation and applications. In Encyclopedia of statistical sciences (eds N Balakrishman, CB Read, B Vidakovic), 2nd edn, pp. 7907-7916. New York, NY: Wiley Press.
70. La Gruta NL, Rothwell WT, Cukalac T, Swan NG, Valkenburg SA, Kedzierska K, Thomas PG, Doherty PC, Turner SJ. 2010 Primary CTL response magnitude in mice is determined by the extent of naive T cell recruitment and subsequent clonal expansion. J. Clin. Invest. 120, 1885-1894. (doi:10. 1172/JCI41538)
71. Shugay M, Bolotin DA, Putintseva EV, Pogorelyy MV, Mamedov IZ, Chudakov DM. 2013 Huge overlap of individual TCR beta repertoires. Front. Immunol. 4. (doi:10. 3389/fimmu. 2013. 00466)
72. Eren MI, Chao A, Hwang W-H, Colwell RK. 2012 Estimating the richness of a population when the maximum number of classes is fixed: a nonparametric solution to an archaeological problem. PLoS ONE 7, e34179. (doi:10. 1371/journal. pone. 0034179)
73. Chao A, Lee S-M. 1992 Estimating the number of classes via sample coverage. J. Am. Stat. Assoc. 87, 210-217. (doi:10. 1080/01621459. 1992. 10475194)
74. + T cell receptors. Immunity 21, 267-277. (doi:10. 1016/j. immuni. 2004. 07. 009)
75. Colwell RK, Coddington JA. 1994 Estimating terrestrial biodiversity through extrapolation. Phil. Trans. R. Soc. Lond. B 345, 101-118. (doi:10. 1098/ rstb. 1994. 0091)
76. Smith EP, Belle GV. 1984 Nonparametric estimation of species richness. Biometrics 40, 119-129. (doi:10. 2307/2530750)
77. Good IJ. 1953 The population frequencies of species and the estimation of population parameters. Biometrika 40, 237-264. (doi:10. 1093/biomet/40. 3-4. 237)
78. Lee S-M, Chao A. 1994 Estimating population size via sample coverage for closed capture-recapture models. Biometrics 50, 88-97. (doi:10. 2307/ 2533199)
79. Chao A. 1987 Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43, 783-791. (doi:10. 2307/2531532)
80. Efron B, Thisted R. 1976 Estimating the number of unseen species: how many words did Shakespeare know? Biometrika 63, 435-447. (doi:10. 1093/ biomet/63. 3. 435)
81. Ionita-Laza I, Lange C, Laird MN. 2009 Estimating the number of unseen variants in the human genome. Proc. Natl Acad. Sci. USA 106, 5008-5013. (doi:10. 1073/pnas. 0807815106)
82. Greene J, Birtwistle MR, Ignatowicz L, Rempala GA. 2013 Bayesian multivariate Poisson abundance models for T-cell receptor data. J. Theor. Biol. 326, 1-10. (doi:10. 1016/j. jtbi. 2013. 02. 009)
83. Wang J-PZ, Lindsay BG, Cui L, Wall PK, Marion J, Zhang J, dePamphilis CW. 2005 Gene capture prediction and overlap estimation in EST sequencing from one or multiple libraries. BMC Bioinform. 6, 300. (doi:10. 1186/1471-2105-6-300)
84. + memory T cell repertoire could optimize potential for immune responses. J. Immunol. 170, 3994-4001. (doi:10. 4049/jimmunol. 170. 8. 3994)
85. Meier J et al. 2013 Fractal organization of the human T cell repertoire in health and after stem cell transplantation. Biol. Blood Marrow Transplant. 19, 366-377. (doi:10. 1016/j. bbmt. 2012. 12. 004)
86. Hong S-H, Bunge J, Jeon S-O, Epstein SS. 2006 Predicting microbial species richness. Proc. Natl Acad. Sci. USA 103, 117-122. (doi:10. 1073/pnas. 0507245102)
87. Zuendorf A, Bunge J, Behnke A, Barger KJA, Stoeck T. 2006 Diversity estimates of microeukaryotes below the chemocline of the anoxic Mariager Fjord, Denmark. FEMS Microbiol. Ecol. 58, 476-491. (doi:10. 1111/j. 1574-6941. 2006. 00171. x)
88. Flather C. 1996 Fitting species-accumulation functions and assessing regional land use impacts on avian diversity. J. Biogeogr. 23, 155-168. (doi:10. 1046/j. 1365-2699. 1996. 00980. x)
89. Scheiner SM. 2003 Six types of species-area curves. Glob. Ecol. Biogeogr. 12, 441-447. (doi:10. 1046/j. 1466-822X. 2003. 00061. x)
90. R Developer Core Team. 2012 R: a language and environment for statistical computing. 2. 14. 2 ed. Vienna, Austria: R Foundation for Statistical Computing.
91. Laydon DJ, Sim A, Bangham CRM, Asquith B. 2014 DivE: diversity estimator. R package version 1. 0. Available at http://CRAN. R-project. org/ package=DivE.
92. Tipper JC. 1979 Rarefaction and rarefiction-the use and abuse of a method in paleoecology. Paleobiology 5, 423-434.
93. Fager EW. 1972 Diversity: a sampling study. Am. Nat. 106, 293-310. (doi:10. 1086/282772)
94. Colwell RK, Mao CX, Chang J. 2004 Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85, 2717-2727. (doi:10. 1890/03-0557)
95. Xuan Mao C, Colwell RK, Chang J. 2005 Estimating the species accumulation curve using mixtures. Biometrics 61, 433-441. (doi:10. 1111/j. 1541-0420. 2005. 00316. x)
96. Colwell RK, Chao A, Gotelli NJ, Lin S-Y, Mao CX, Chazdon RL, Longino JT. 2012 Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J. Plant Ecol. 5, 3-21. (doi:10. 1093/jpe/rtr044)