Transcript-indexed ATAC-seq for precision immune profiling

Nature Medicine

Volumn 24, Issue 5, 2018, Pages 580-590

  Satpathy, Ansuman T ^a   Saligrama, Naresha ^a   Buenrostro, Jason D ^b,c   Wei, Yuning ^a   Wu, Beijing ^a   Rubin, Adam J ^a   Granja, Jeffrey M ^a   Lareau, Caleb A ^b   Li, Rui ^a   Qi, Yanyan ^a   Parker, Kevin R ^a   Mumbach, Maxwell R ^a   Serratelli, William S ^a   Gennert, David G ^a   Schep, Alicia N ^a   Corces, M Ryan ^a   Khodadoust, Michael S ^a   Kim, Youn H ^a   Khavari, Paul A ^a   Greenleaf, William J ^a,d,e   Davis, Mark M ^a   Chang, Howard Y ^a   more..

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c HARVARD UNIVERSITY   (United States)

^d STANFORD UNIVERSITY   (United States)

^e CHAN ZUCKERBERG BIOHUB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CCAAT ENHANCER BINDING PROTEIN; CELL SURFACE MARKER; CHEMOKINE RECEPTOR CCR7; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INHIBITOR OF DIFFERENTIATION 2; INTERFERON REGULATORY FACTOR 4; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 22; INTERLEUKIN 26; LAT PROTEIN; LYMPHOID ENHANCER FACTOR 1; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; STAT PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR MAF; TRANSCRIPTION FACTOR RUNX; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR RUNX3; TRANSCRIPTION FACTOR T BET; ZINC FINGER E BOX BINDING HOMEOBOX 2; LYMPHOCYTE ANTIGEN RECEPTOR; MESSENGER RNA; TRANSPOSASE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANTIGEN SPECIFICITY; ARTICLE; CANCER PATIENT; CD4+ T LYMPHOCYTE; CELL IMMORTALIZATION; COMPARATIVE STUDY; CONTROLLED STUDY; CUTANEOUS T CELL LYMPHOMA; EPIGENETICS; GENE SEQUENCE; GENETIC TRANSCRIPTION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIMARY CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T CELL LEUKEMIA; T LYMPHOCYTE RECEPTOR GENE; T LYMPHOCYTE SUBPOPULATION; TRANSPOSASE ACCESSIBLE CHROMATIN WITH SEQUENCING; TUMOR IMMUNITY; CELL CLONE; CHROMATIN; GENETICS; IMMUNITY; IMMUNOLOGY; JURKAT CELL LINE; LEUKEMIA; METABOLISM; PATHOLOGY; PROCEDURES; SINGLE CELL ANALYSIS; TRANSFORMED CELL LINE; CANCER IMMUNOTHERAPY; EMBRYONIC STEM CELL; GENE IDENTIFICATION; GENETIC CODE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; K-562 CELL LINE; LETTER; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR CLONING; PROMOTER REGION; TRANSCRIPT INDEXED ASSAY FOR TRANSPOSASE ACCESSIBLE CHROMATIN WITH SEQUENCING;

CD4-POSITIVE T-LYMPHOCYTES; CELL LINE, TRANSFORMED; CHROMATIN; CLONE CELLS; EPIGENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IMMUNITY; JURKAT CELLS; LEUKEMIA; RECEPTORS, ANTIGEN, T-CELL; RNA, MESSENGER; SINGLE-CELL ANALYSIS; TRANSPOSASES;

EID: 85045857015     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/s41591-018-0008-8     Document Type: Article

References (61)

1. Davis, M. M. & Bjorkman, P. J. T cell antigen receptor genes and T cell recognition. Nature 334, 395-402 (1988).
2. Shalek, A. K. et al. Single-cell RNA-seq reveals dynamic paracrine control of cellular variation. Nature 510, 363-369 (2014).
3. H17 cell pathogenicity. Cell 163, 1400-1412 (2015).
4. Paul, F. et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163, 1663-1677 (2015).
5. Tirosh, I. et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189-196 (2016).
6. Han, A., Glanville, J., Hansmann, L. & Davis, M. M. Linking T cell receptor sequence to functional phenotype at the single-cell level. Nat. Biotechnol. 32, 684-692 (2014).
7. Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213-1218 (2013).
8. Buenrostro, J. D. et al. Single-cell chromatin accessibility reveals principles of regulatory variation. Nature 523, 486-490 (2015).
9. Corces, M. R. et al. Lineage-specific and single-cell chromatin accessibility charts human hematopoiesis and leukemia evolution. Nat. Genet. 48, 1193-1203 (2016).
10. Buenrostro, J. D. et al. Single-cell epigenomics maps the continuous regulatory landscape of human hematopoietic differentiation. bioRxiv http://dx.doi.org/10.1101/109843 (2017).
11. Schep, A. N., Wu, B., Buenrostro, J. D. & Greenleaf, W. J. chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data. Nat. Methods 14, 975-978 (2017).
12. Stubbington, M. J. T. et al. T cell fate and clonality inference from single-cell transcriptomes. Nat. Methods 13, 329-332 (2016).
13. Afik, S. et al. Targeted reconstruction of T cell receptor sequence from single-cell RNA-seq links CDR3 length to T cell differentiation state. Nucleic Acids Res. 45, e148 (2017).
14. Cusanovich, D. A. et al. Multiplex single-cell profiling of chromatin accessibility by combinatorial cellular indexing. Science 348, 910-914 (2015).
15. Weber, B. N. et al. A critical role for TCF-1 in T lineage specification and differentiation. Nature 476, 63-68 (2011).
16. Collins, A., Littman, D. R. & Taniuchi, I. RUNX proteins in transcription factor networks that regulate T cell lineage choice. Nat. Rev. Immunol. 9, 106-115 (2009).
17. + T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 34, 108-121 (2011).
18. Fontenot, J. D., Rasmussen, J. P., Gavin, M. A. & Rudensky, A. Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6, 1142-1151 (2005).
19. Ouyang, W., Kolls, J. K. & Zheng, Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28, 454-467 (2008).
20. H17 cells promote microbial killing and innate immune sensing of DNA via interleukin 26. Nat. Immunol. 16, 970-979 (2015).
21. van der Maaten, L. & Hinton, G. Visualizing data using t-SNE. J. Mach. Learn. Res. 9, 2579-2605 (2008).
22. Kimmig, S. et al. Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood. J. Exp. Med. 195, 789-794 (2002).
23. Boursalian, T. E., Golob, J., Soper, D. M., Cooper, C. J. & Fink, P. J. Continued maturation of thymic emigrants in the periphery. Nat. Immunol. 5, 418-425 (2004).
24. Harari, A., Vallelian, F. & Pantaleo, G. Phenotypic heterogeneity of antigen-specific CD4 T cells under different conditions of antigen persistence and antigen load. Eur. J. Immunol. 34, 3525-3533 (2004).
25. + T cell precursor for naive, memory and regulatory T cells. J. Exp. Med. 207, 2883-2894 (2010).
26. + memory T cells reveals early branched pathways of T cell differentiation in humans. Proc. Natl Acad. Sci. USA 102, 7916-7921 (2005).
27. Gattinoni, L. et al. A human memory T cell subset with stem-cell-like properties. Nat. Med. 17, 1290-1297 (2011).
28. + T cells associated with protective immunity. Proc. Natl Acad. Sci. USA 112, E4256-E4263 (2015).
29. Yui, M. A. & Rothenberg, E. V. Developmental gene networks: A triathlon on the course to T cell identity. Nat. Rev. Immunol. 14, 529-545 (2014).
30. H2 cytokine gene expression in CD4 T cells. Cell 89, 587-596 (1997).
31. Lohoff, M. & Mak, T. W. Roles of interferon-regulatory factors in T helper cell differentiation. Nat. Rev. Immunol. 5, 125-135 (2005).
32. + T helper cells. Cell 126, 1121-1133 (2006).
33. Yang, X. O. et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR-α and ROR-γ. Immunity 28, 29-39 (2008).
34. H17 cells. Nat. Immunol. 10, 167-175 (2009).
35. H17 differentiation. Nature 460, 405-409 (2009).
36. + T helper cell differentiation. Nat. Rev. Immunol. 11, 239-250 (2011).
37. H17 cells. Nat. Immunol. 12, 1238-1245 (2011).
38. H17 cell specification. Cell 151, 289-303 (2012).
39. Bigler, R. D., Boselli, C. M., Foley, B. & Vonderheid, E. C. Failure of anti-T cell receptor Vβ antibodies to consistently identify a malignant T cell clone in Sézary syndrome. Am. J. Pathol. 149, 1477-1483 (1996).
40. Kelemen, K., Guitart, J., Kuzel, T. M., Goolsby, C. L. & Peterson, L. C. The usefulness of CD26 in flow cytometric analysis of peripheral blood in Sézary syndrome. Am. J. Clin. Pathol. 129, 146-156 (2008).
41. Weng, W. K. et al. Minimal residual disease monitoring with high-throughput sequencing of T cell receptors in cutaneous T cell lymphoma. Sci. Transl. Med. 5, 214ra171 (2013).
42. Sufficool, K. E. et al. T cell clonality assessment by next-generation sequencing improves detection sensitivity in mycosis fungoides. J. Am. Acad. Dermatol. 73, 228-236 (2015).
43. Rook, A. H., Vowels, B. R., Jaworsky, C., Singh, A. & Lessin, S. R. The immunopathogenesis of cutaneous T cell lymphoma. Abnormal cytokine production by Sézary T cells. Arch. Dermatol. 129, 486-489 (1993).
44. H2 cytokine mRNA expression in skin in cutaneous T cell lymphoma. J. Invest. Dermatol. 103, 669-673 (1994).
45. Krejsgaard, T., Odum, N., Geisler, C., Wasik, M. A. & Woetmann, A. Regulatory T cells and immunodeficiency in mycosis fungoides and Sézary syndrome. Leukemia 26, 424-432 (2012).
46. Ungewickell, A. et al. Genomic analysis of mycosis fungoides and Sézary syndrome identifies recurrent alterations in TNFR2. Nat. Genet. 47, 1056-1060 (2015).
47. Choi, J. et al. Genomic landscape of cutaneous T cell lymphoma. Nat. Genet. 47, 1011-1019 (2015).
48. Bernengo, M. G. et al. Prognostic factors in Sézary syndrome: A multivariate analysis of clinical, hematological and immunological features. Ann. Oncol. 9, 857-863 (1998).
49. Kirsch, I. R. et al. TCR sequencing facilitates diagnosis and identifies mature T cells as the cell of origin in CTCL. Sci. Transl. Med. 7, 308ra158 (2015).
50. Bolden, J. E., Peart, M. J. & Johnstone, R. W. Anticancer activities of histone deacetylase inhibitors. Nat. Rev. Drug Discov. 5, 769-784 (2006).
51. Qu, K. et al. Chromatin accessibility landscape of cutaneous T cell lymphoma and dynamic response to HDAC inhibitors. Cancer Cell 32, 27-41.e4 (2017).
52. Regev, A. et al. The Human Cell Atlas. Elife 6, e27041 (2017).
53. Birnbaum, M. E. et al. Deconstructing the peptide-MHC specificity of T cell recognition. Cell 157, 1073-1087 (2014).
54. Newell, E. W. & Davis, M. M. Beyond model antigens: high-dimensional methods for the analysis of antigen-specific T cells. Nat. Biotechnol. 32, 149-157 (2014).
55. Letourneur, F. & Malissen, B. Derivation of a T cell hybridoma variant deprived of functional T cell receptor α- and β-chain transcripts reveals a nonfunctional α-mRNA of BW5147 origin. Eur. J. Immunol. 19, 2269-2274 (1989).
56. Huse, M. et al. Spatial and temporal dynamics of T cell receptor signaling with a photoactivatable agonist. Immunity 27, 76-88 (2007).
57. Glanville, J. et al. Identifying specificity groups in the T cell receptor repertoire. Nature 547, 94-98 (2017).
58. Mathelier, A. et al. JASPAR 2016: A major expansion and update of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 44.D1, D110-D115 (2016).
59. Jolma, A. et al. DNA-binding specificities of human transcription factors. Cell 152, 327-339 (2013).
60. Weirauch, M. T. et al. Determination and inference of eukaryotic transcription factor sequence specificity. Cell 158, 1431-1443 (2014).
61. Mumbach, M. R. et al. Enhancer connectome in primary human cells identifies target genes of disease-associated DNA elements. Nat. Genet. 49, 1602-1612 (2017).