Diversity and divergence of the glioma-infiltrating T-cell receptor repertoire

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 25, 2016, Pages E3529-E3537

  Sims, Jennifer S ^a   Grinshpun, Boris ^a   Feng, Yaping ^a,b   Ung, Timothy H ^a,c   Neira, Justin A ^a   Samanamud, Jorge L ^a   Canoll, Peter ^a   Shen, Yufeng ^a,d   Sims, Peter A ^a,d   Bruce, Jeffrey N ^a  

^a Department of Medicine   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Glioblastoma; Glioma; Immunooncology; Immunoprofiling; T cell receptor

Indexed keywords

BIOLOGICAL MARKER; T LYMPHOCYTE RECEPTOR; TETANUS TOXOID; TUMOR ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR;

AMINO ACID SEQUENCE; AMPLICON; ANTIGEN BINDING; ARTICLE; CANDIDA ALBICANS; CELL INFILTRATION; CONTROLLED STUDY; ENTROPY; GLIOBLASTOMA; GLIOMA; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN TISSUE; IMMUNOPHENOTYPING; INFORMATION SCIENCE; MULTIPLEX POLYMERASE CHAIN REACTION; MYCOBACTERIUM TUBERCULOSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN MOTIF; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; BRAIN TUMOR; IMMUNOLOGY; PATHOLOGY;

BRAIN NEOPLASMS; GLIOMA; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; RECEPTORS, ANTIGEN, T-CELL;

EID: 84975702030     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1601012113     Document Type: Article

References (62)

1. Phillips HS, et al. (2006) Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9(3):157-173.
2. Verhaak RG, et al.; Cancer Genome Atlas Research Network (2010) Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17(1):98-110.
3. Ivliev AE, 't Hoen PA, Sergeeva MG (2010) Coexpression network analysis identifies transcriptional modules related to proastrocytic differentiation and sprouty signaling in glioma. Cancer Res 70(24):10060-10070.
4. Doucette T, et al. (2013) Immune heterogeneity of glioblastoma subtypes: Extrapolation from the cancer genome atlas. Cancer Immunol Res 1(2):112-122.
5. Murat A, et al. (2009) Modulation of angiogenic and inflammatory response in glioblastoma by hypoxia. PLoS One 4(6):e5947.
6. Weinstein JA, Jiang N, White RA, 3rd, Fisher DS, Quake SR (2009) High-throughput sequencing of the zebrafish antibody repertoire. Science 324(5928):807-810.
7. 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(4):1518-1523.
8. Boyd SD, et al. (2009) Measurement and clinical monitoring of human lymphocyte clonality by massively parallel VDJ pyrosequencing. Sci Transl Med 1(12):12ra23.
9. 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(10):1817-1824.
10. Woodsworth DJ, Castellarin M, Holt RA (2013) Sequence analysis of T-cell repertoires in health and disease. Genome Med 5(10):98.
11. Han J, et al. (2006) Simultaneous amplification and identification of 25 human papillomavirus types with Templex technology. J Clin Microbiol 44(11):4157-4162.
12. Yang Y, et al. (2015) Distinct mechanisms define murine B cell lineage immunoglobulin heavy chain (IgH) repertoires. eLife 4:e09083.
13. Zvyagin IV, et al. (2014) Distinctive properties of identical twins' TCR repertoires revealed by high-throughput sequencing. Proc Natl Acad Sci USA 111(16):5980-5985.
14. Putintseva EV, et al. (2013) Mother and child T cell receptor repertoires: Deep profiling study. Front Immunol 4:463.
15. Zarnitsyna VI, Evavold BD, Schoettle LN, Blattman JN, Antia R (2013) Estimating the diversity, completeness, and cross-reactivity of the T cell repertoire. Front Immunol 4:485.
16. Merkenschlager J, Kassiotis G (2015) Narrowing the gap: Preserving repertoire diversity despite clonal selection during the CD4 T cell response. Front Immunol 6:413.
17. Murugan A, Mora T, Walczak AM, Callan CG, Jr (2012) Statistical inference of the generation probability of T-cell receptors from sequence repertoires. Proc Natl Acad Sci USA 109(40):16161-16166.
18. Elhanati Y, Murugan A, Callan CG, Jr, Mora T, Walczak AM (2014) Quantifying selection in immune receptor repertoires. Proc Natl Acad Sci USA 111(27):9875-9880.
19. Turner SJ, Doherty PC, McCluskey J, Rossjohn J (2006) Structural determinants of T-cell receptor bias in immunity. Nat Rev Immunol 6(12):883-894.
20. Ndifon W, et al. (2012) Chromatin conformation governs T-cell receptor Jβ gene segment usage. Proc Natl Acad Sci USA 109(39):15865-15870.
21. Britanova OV, et al. (2014) Age-related decrease in TCR repertoire diversity measured with deep and normalized sequence profiling. J Immunol 192(6):2689-2698.
22. Emerson R, et al. (2013) Estimating the ratio of CD4+ to CD8+ T cells using high-throughput sequence data. J Immunol Methods 391(1-2):14-21.
23. Gregersen PK, Hingorani R, Monteiro J (1995) Oligoclonality in the CD8+ T-cell population. Analysis using a multiplex PCR assay for CDR3 length. Ann N Y Acad Sci 756:19-27.
24. Robert L, et al. (2014) CTLA4 blockade broadens the peripheral T-cell receptor repertoire. Clin Cancer Res 20(9):2424-2432.
25. Tumeh PC, et al. (2014) PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515(7528):568-571.
26. Radebe M, et al. (2015) Broad and persistent Gag-specific CD8+ T-cell responses are associated with viral control but rarely drive viral escape during primary HIV-1 infection. AIDS 29(1):23-33.
27. Morris H, et al. (2015) Tracking donor-reactive T cells: Evidence for clonal deletion in tolerant kidney transplant patients. Sci Transl Med 7(272):272ra10.
28. Kmiecik J, et al. (2013) Elevated CD3+ and CD8+ tumor-infiltrating immune cells correlate with prolonged survival in glioblastoma patients despite integrated immunosuppressive mechanisms in the tumor microenvironment and at the systemic level. J Neuroimmunol 264(1-2):71-83.
29. Okada H, Khoury SJ (2012) Type17 T-cells in central nervous system autoimmunity and tumors. J Clin Immunol 32(4):802-808.
30. Waziri A, et al. (2008) Preferential in situ CD4+CD56+ T cell activation and expansion within human glioblastoma. J Immunol 180(11):7673-7680.
31. Fong B, et al. (2012) Monitoring of regulatory T cell frequencies and expression of CTLA-4 on T cells, before and after DC vaccination, can predict survival in GBM patients. PLoS One 7(4):e32614.
32. + T cell clones primed by pathogens or vaccines. Science 347(6220):400-406.
33. Venturi V, et al. (2008) TCR beta-chain sharing in human CD8+ T cell responses to cytomegalovirus and EBV. J Immunol 181(11):7853-7862.
34. Lim A, et al. (2000) Frequent contribution of T cell clonotypes with public TCR features to the chronic response against a dominant EBV-derived epitope: Application to direct detection of their molecular imprint on the human peripheral T cell repertoire. J Immunol 165(4):2001-2011.
35. McCluskey J, Kanaan C, Diviney M (2003) Nomenclature and serology of HLA class I and class II alleles. Curr Protoc Immunol 52(1S):A.1S.1-A.1S.8.
36. Wucherpfennig KW, Strominger JL (1995) Molecular mimicry in T cell-mediated autoimmunity: Viral peptides activate human T cell clones specific for myelin basic protein. Cell 80(5):695-705.
37. Tosato G, Cohen JI (2007) Generation of Epstein-Barr virus (EBV)-immortalized B cell lines. Curr Protoc Immunol Chap 7:Unit 7.22.
38. Bhaduri-McIntosh S, Rotenberg MJ, Gardner B, Robert M, Miller G (2008) Repertoire and frequency of immune cells reactive to Epstein-Barr virus-derived autologous lymphoblastoid cell lines. Blood 111(3):1334-1343.
39. Lossius A, et al. (2014) High-throughput sequencing of TCR repertoires in multiple sclerosis reveals intrathecal enrichment of EBV-reactive CD8+ T cells. Eur J Immunol 44(11):3439-3452.
40. Suessmuth Y, et al. (2015) CMV reactivation drives posttransplant T-cell reconstitution and results in defects in the underlying TCRβ repertoire. Blood 125(25):3835-3850.
41. Angelova M, et al. (2015) Characterization of the immunophenotypes and antigenomes of colorectal cancers reveals distinct tumor escape mechanisms and novel targets for immunotherapy. Genome Biol 16:64.
42. Drake CG, Lipson EJ, Brahmer JR (2014) Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer. Nat Rev Clin Oncol 11(1):24-37.
43. Sims JS, Ung TH, Neira JA, Canoll P, Bruce JN (2015) Biomarkers for glioma immunotherapy: The next generation. J Neurooncol 123(3):359-372.
44. Carson MJ, Doose JM, Melchior B, Schmid CD, Ploix CC (2006) CNS immune privilege: Hiding in plain sight. Immunol Rev 213:48-65.
45. Guan X, et al. (2014) Molecular subtypes of glioblastoma are relevant to lower grade glioma. PLoS One 9(3):e91216.
46. Sensi M, Parmiani G (1995) Analysis of TCR usage in human tumors: A new tool for assessing tumor-specific immune responses. Immunol Today 16(12):588-595.
47. + tumor-reactive repertoire infiltrating human tumors. J Clin Invest 124(5):2246-2259.
48. Linnemann C, et al. (2013) High-throughput identification of antigen-specific TCRs by TCR gene capture. Nat Med 19(11):1534-1541.
49. Hitchcock ER, Morris CS (1988) Mononuclear cell infiltration in central portions of human astrocytomas. J Neurosurg 68(3):432-437.
50. Magoč T, Salzberg SL (2011) FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957-2963.
51. Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26(5):589-595.
52. Shannon CE (1948) A mathematical theory of communication. At&T Tech J 27(3):379-423.
53. Warren RL, et al. (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(5):790-797.
54. Lefranc MP, et al. (2015) IMGT®, the international ImMunoGeneTics information system® 25 years on. Nucleic Acids Res 43(Database issue):D413-D422.
55. Krzywinski M, et al. (2009) Circos: An information aesthetic for comparative genomics. Genome Res 19(9):1639-1645.
56. Endres DM, Schindelin JE (2003) A new metric for probability distributions. Ieee T Inform Theory 49(7):1858-1860.
57. Klarenbeek PL, et al. (2012) Deep sequencing of antiviral T-cell responses to HCMV and EBV in humans reveals a stable repertoire that is maintained for many years. PLoS Pathog 8(9):e1002889.
58. Emerson R, et al. (September 10, 2015) Immunosequencing reveals diagnostic signatures of chronic viral infection in T cell memory. BioRxiv, 10.1101/026567.
59. Dziubianau M, et al. (2013) TCR repertoire analysis by next generation sequencing allows complex differential diagnosis of T cell-related pathology. Am J Transplant 13(11):2842-2854.
60. Hong J, et al. (1999) A common TCR V-D-J sequence in V beta 13.1 T cells recognizing an immunodominant peptide of myelin basic protein in multiple sclerosis. J Immunol 163(6):3530-3538.
61. Junker A, et al. (2007) Multiple sclerosis: T-cell receptor expression in distinct brain regions. Brain 130(Pt 11):2789-2799.
62. Bolotin DA, et al. (2012) Next generation sequencing for TCR repertoire profiling: Platform-specific features and correction algorithms. Eur J Immunol 42(11):3073-3083.