TCR repertoire analysis by next generation sequencing allows complex differential diagnosis of T cell-related pathology

American Journal of Transplantation

Volumn 13, Issue 11, 2013, Pages 2842-2854

  Dziubianau, M ^a   Hecht, J ^a,b   Kuchenbecker, L ^a,c,d   Sattler, A ^a   Stervbo, U ^a   Rodelsperger C ^a   Nickel, P ^a   Neumann, A U ^a,d   Robinson, P N ^a   Mundlos, S ^a,b   Volk, H D ^a   Thiel, A ^a   Reinke, P ^a   Babel, N ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c INTERNATIONAL MAX PLANCK RESEARCH SCHOOL FOR COMPUTATIONAL BIOLOGY AND SCIENTIFIC COMPUTING   (Germany)

^d BAR ILAN UNIVERSITY   (Israel)

Author keywords

Acute cellular rejection; BKV; differential diagnosis; kidney transplantation; next generation sequencing; polyoma

Indexed keywords

ALLOANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; DNA; RNA; T LYMPHOCYTE RECEPTOR;

ACUTE GRAFT REJECTION; ANALYTIC METHOD; ANTIGEN SPECIFICITY; ARTICLE; BK VIRUS; CLONE; CONTROLLED STUDY; CYTOMEGALOVIRUS; DIFFERENTIAL DIAGNOSIS; EX VIVO STUDY; GENE SEQUENCE; GRAFT DYSFUNCTION; HUMAN; HUMAN CELL; KIDNEY ALLOGRAFT; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; T LYMPHOCYTE; TUMOR IMMUNITY; VIRUS REACTIVATION;

ACUTE CELLULAR REJECTION; BKV; DIFFERENTIAL DIAGNOSIS; KIDNEY TRANSPLANTATION; NEXT GENERATION SEQUENCING; POLYOMA;

BK VIRUS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DIAGNOSIS, DIFFERENTIAL; GRAFT REJECTION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; KIDNEY TRANSPLANTATION; POLYOMAVIRUS INFECTIONS; RECEPTORS, ANTIGEN, T-CELL; RETROSPECTIVE STUDIES; T-LYMPHOCYTES; TUMOR VIRUS INFECTIONS; VIRUS ACTIVATION;

EID: 84886772223     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.12431     Document Type: Article

References (58)

1. Grim SA, Clark NM., Management of infectious complications in solid-organ transplant recipients. Clin Pharmacol Ther 2011; 90: 333-342.
2. Baum PD, McCune JM., Direct measurement of T-cell receptor repertoire diversity with AmpliCot. Nat Methods 2006; 3: 895-901.
3. Langerak AW, van Den Beemd R, Wolvers-Tettero IL, et al. Molecular and flow cytometric analysis of the Vbeta repertoire for clonality assessment in mature TCRalphabeta T-cell proliferations. Blood 2001; 98: 165-173.
4. Tembhare P, Yuan CM, Morris JC, Janik JE, Filie AC, Stetler-Stevenson M., Flow cytometric immunophenotypic assessment of T-cell clonality by vbeta repertoire analysis in fine-needle aspirates and cerebrospinal fluid. Am J Clin Pathol 2012; 137: 220-226.
5. Salameire D, Le Bris Y, Fabre B, et al. Efficient characterization of the TCR repertoire in lymph nodes by flow cytometry. Cytometry A 2009; 75: 743-751.
6. van den Beemd R, Boor PP, van Lochem EG, et al. Flow cytometric analysis of the Vbeta repertoire in healthy controls. Cytometry 2000; 40: 336-345.
7. Schatz DG, Ji Y., Recombination centres and the orchestration of V(D)J recombination. Nat Rev Immunol 2011; 11: 251-263.
8. Arstila TP, Casrouge A, Baron V, Even J, Kanellopoulos J, Kourilsky P., A direct estimate of the human alphabeta T cell receptor diversity. Science 1999; 286: 958-961.
9. 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: 4285-4294.
10. Messaoudi I, Guevara Patino JA, Dyall R, LeMaoult J, Nikolich-Zugich J., Direct link between mhc polymorphism, T cell avidity, and diversity in immune defense. Science 2002; 298: 1797-1800.
11. Turner SJ, LaGruta NL, Kedzierska K, Thomas PG, Doherty PC., Functional implications of T cell receptor diversity. Curr Opin Immunol 2009; 21: 286-290.
12. Wang GC, Dash P, McCullers JA, Doherty PC, Thomas PG., T cell receptor alphabeta diversity inversely correlates with pathogen-specific antibody levels in human cytomegalovirus infection. Sci Transl Med 2012; 4: 128ra42.
13. Valkenburg SA, Day EB, Swan NG, et al. Fixing an irrelevant TCR alpha chain reveals the importance of TCR beta diversity for optimal TCR alpha beta pairing and function of virus-specific CD8+ T cells. Eur J Immunol 2010; 40: 2470-2481.
14. Giest S, McWhinnie A, Lefranc MP, et al. Cytomegalovirus-specific CD8+ T cells targeting different peptide/HLA combinations demonstrate varying T-cell receptor diversity. Immunology 2012; 135: 27-39.
15. Mardis ER., Next-generation DNA sequencing methods. Annu Rev Genomics Hum Genet 2008; 9: 387-402.
16. Freeman JD, Warren RL, Webb JR, Nelson BH, Holt RA., Profiling the T-cell receptor beta-chain repertoire by massively parallel sequencing. Genome Res 2009; 19: 1817-1824.
17. Robins HS, Campregher PV, Srivastava SK, et al. Comprehensive assessment of T-cell receptor beta-chain diversity in alphabeta T cells. Blood 2009; 114: 4099-4107.
18. Boyd SD, Marshall EL, Merker JD, et al. Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci Transl Med 2009; 1: 12ra23.
19. Trydzenskaya H, Sattler A, Muller K, et al. Novel approach for improved assessment of phenotypic and functional characteristics of BKV-specific T-cell immunity. Transplantation 2011; 92: 1269-1277.
20. Bestard O, Nickel P, Cruzado JM, et al. Circulating alloreactive T cells correlate with graft function in longstanding renal transplant recipients. J Am Soc Nephrol 2008; 19: 1419-1429.
21. Frentsch M, Arbach O, Kirchhoff D, et al. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression. Nat Med 2005; 11: 1118-1124.
22. Wolfl M, Kuball J, Ho WY, et al. Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities. Blood 2007; 110: 201-210.
23. Hammer MH, Brestrich G, Andree H, et al. HLA type-independent method to monitor polyoma BK virus-specific CD4 and CD8 T-cell immunity. Am J Transplant 2006; 6: 625-631.
24. Kalendar R, Lee D, Schulman AH., Java web tools for PCR, in silico PCR, and oligonucleotide assembly and analysis. Genomics 2011; 98: 137-144.
25. Kalendar R, Lee D, Schulman AH., FastPCR software for PCR primer and probe design and repeat search. Genes Genomes Genomics 2009; 3: 1-14.
26. Yousfi Monod M, Giudicelli V, Chaume D, Lefranc MP., IMGT/ JunctionAnalysis: The first tool for the analysis of the immunoglobulin and T cell receptor complex V-J and V-D-J JUNCTIONs. Bioinformatics 2004; 20 (Suppl 1): i379-i385.
27. Rempala GA, Seweryn M, Ignatowicz L., Model for comparative analysis of antigen receptor repertoires. J Theor Biol 2011; 269: 1-15.
28. Venturi V, Kedzierska K, Tanaka MM, Turner SJ, Doherty PC, Davenport MP., Method for assessing the similarity between subsets of the T cell receptor repertoire. J Immunol Methods 2008; 329: 67-80.
29. Babel N, Brestrich G, Gondek LP, et al. Clonotype analysis of cytomegalovirus-specific cytotoxic T lymphocytes. J Am Soc Nephrol 2009; 20: 344-352.
30. Nixon DF, Douek D, Kuebler PJ, et al. Molecular tracking of an Human Immunodeficiency Virus nef specific cytotoxic T-cell clone shows persistence of clone-specific T-cell receptor DNA but not mRNA following early combination antiretroviral therapy. Immunol Lett 1999; 66: 219-228.
31. Kieper WC, Burghardt JT, Surh CD., A role for TCR affinity in regulating naïve T cell homeostasis. J Immunol 2004; 172: 40-44.
32. Babel N, Volk HD, Reinke P., BK polyomavirus infection and nephropathy: The virus-immune system interplay. Nat Rev Nephrol 2011; 7: 399-406.
33. Ito Y, Nishi S, Imai N, et al. The case of BK virus infection in which it was difficult to differentiate from acute rejection. Clin Transplant 2011; 25 (Suppl 23): 44-48.
34. Drachenberg CB, Papadimitriou JC, Hirsch HH, et al. Histological patterns of polyomavirus nephropathy: Correlation with graft outcome and viral load. Am J Transplant 2004; 4: 2082-2092.
35. Bohl DL, Brennan DC., BK virus nephropathy and kidney transplantation. Clin J Am Soc Nephrol 2007; 2 (Suppl 1): S36-S46.
36. Crough T, Khanna R., Immunobiology of human cytomegalovirus: From bench to bedside. Clin Microbiol Rev 2009; 22: 76-98, Table of Contents.
37. Bitmansour AD, Waldrop SL, Pitcher CJ, et al. Clonotypic structure of the human CD4+ memory T cell response to cytomegalovirus. J Immunol 2001; 167: 1151-1163.
38. Bonarius HP, Baas F, Remmerswaal EB, et al. Monitoring the T-cell receptor repertoire at single-clone resolution. PLoS ONE 2006; 1: e55.
39. 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: 790-797.
40. Klarenbeek PL, Tak PP, van Schaik BD, et al. Human T-cell memory consists mainly of unexpanded clones. Immunol Lett 2010; 133: 42-48.
41. Robins H, Desmarais C, Matthis J, et al. Ultra-sensitive detection of rare T cell clones. J Immunol Methods 2012; 375: 14-19.
42. Logan AC, Gao H, Wang C, et al. High-throughput VDJ sequencing for quantification of minimal residual disease in chronic lymphocytic leukemia, immune reconstitution assessment. Proc Natl Acad Sci USA 2011; 108: 21194-21199.
43. Miconnet I, Marrau A, Farina A, et al. Large TCR diversity of virus-specific CD8 T cells provides the mechanistic basis for massive TCR renewal after antigen exposure. J Immunol 2011; 186: 7039-7049.
44. Robins HS, Srivastava SK, Campregher PV, et al. Overlap and effective size of the human CD8+ T cell receptor repertoire. Sci Transl Med 2010; 2: 47ra64.
45. Holtappels R, Simon CO, Munks MW, et al. Subdominant CD8 T-cell epitopes account for protection against cytomegalovirus independent of immunodomination. J Virol 2008; 82: 5781-5796.
46. Speiser DE, Wieckowski S, Gupta B, et al. Single cell analysis reveals similar functional competence of dominant, nondominant CD8 T-cell clonotypes. Proc Natl Acad Sci USA 2011; 108: 15318-15323.
47. Yewdell JW, Bennink JR., Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 1999; 17: 51-88.
48. van der Most RG, Sette A, Oseroff C, et al. Analysis of cytotoxic T cell responses to dominant and subdominant epitopes during acute and chronic lymphocytic choriomeningitis virus infection. J Immunol 1996; 157: 5543-5554.
49. Maekawa Y, Yasutomo K., Antigen-driven T-cell repertoire selection. Crit Rev Immunol 2005; 25: 59-74.
50. Zhou H, Deem MW., Sculpting the immunological response to dengue fever by polytopic vaccination. Vaccine 2006; 24: 2451-2459.
51. Rodriguez F, Slifka MK, Harkins S, Whitton JL., Two overlapping subdominant epitopes identified by DNA immunization induce protective CD8(+) T-cell populations with differing cytolytic activities. J Virol 2001; 75: 7399-7409.
52. Olsen AW, Hansen PR, Holm A, Andersen P., Efficient protection against Mycobacterium tuberculosis by vaccination with a single subdominant epitope from the ESAT-6 antigen. Eur J Immunol 2000; 30: 1724-1732.
53. Chen Y, Webster RG, Woodland DL., Induction of CD8+ T cell responses to dominant and subdominant epitopes and protective immunity to Sendai virus infection by DNA vaccination. J Immunol 1998; 160: 2425-2432.
54. Chen W, McCluskey J., Immunodominance and immunodomination: Critical factors in developing effective CD8+ T-cell-based cancer vaccines. Adv Cancer Res 2006; 95: 203-247.
55. Kern F, Faulhaber N, Frommel C, et al. Analysis of CD8 T cell reactivity to cytomegalovirus using protein-spanning pools of overlapping pentadecapeptides. Eur J Immunol 2000; 30: 1676-1682.
56. Sylwester AW, Mitchell BL, Edgar JB, et al. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 2005; 202: 673-685.
57. Price DA, Bitmansour AD, Edgar JB, et al. Induction and evolution of cytomegalovirus-specific CD4+ T cell clonotypes in rhesus macaques. J Immunol 2008; 180: 269-280.
58. Hirsch HH, Drachenberg CB, Steiger J, Ramos E., Polyomavirus-associated nephropathy in renal transplantation: Critical issues of screening and management. Adv Exp Med Biol 2006; 577: 160-173.