Early specification of CD8+T lymphocyte fates during adaptive immunity revealed by single-cell gene-expression analyses

Nature Immunology

Volumn 15, Issue 4, 2014, Pages 365-372

  Arsenio, Janilyn ^a   Kakaradov, Boyko ^b   Metz, Patrick J ^a   Kim, Stephanie H ^a   Yeo, Gene W ^b,c   Chang, John T ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 2 RECEPTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL FATE; CELL HETEROGENEITY; CONTROLLED STUDY; GENE EXPRESSION; IMMUNE RESPONSE; LISTERIA MONOCYTOGENES; LISTERIOSIS; MITOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; PRIORITY JOURNAL;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; COMPUTER SIMULATION; GENE EXPRESSION PROFILING; INFECTION; LISTERIA MONOCYTOGENES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOSIS; OVALBUMIN; RECEPTORS, INTERLEUKIN-2; SINGLE-CELL ANALYSIS; T-LYMPHOCYTE SUBSETS; TRANSCRIPTIONAL ACTIVATION;

EID: 84897059078     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2842     Document Type: Article

References (48)

1. Ahmed, R. & Gray, D. Immunological memory and protective immunity: Understanding their relation. Science 272, 54-60 (1996.
2. Joshi, N.S. et al. Inflammation directs memory precursor and short-lived effector CD8+ T cell fates via the graded expression of T-bet transcription factor. Immunity 27, 281-295 (2007.
3. Masopust, D., Kaech, S.M., Wherry, E.J. & Ahmed, R. The role of programming in memory T-cell development. Curr. Opin. Immunol. 16, 217-225 (2004.
4. Sallusto, F., Lenig, D., Forster, R., Lipp, M. & Lanzavecchia, A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708-712 (1999.
5. Stemberger, C. et al. A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity 27, 985-997 (2007.
6. Gerlach, C. et al. One naive T cell, multiple fates in CD8+ T cell differentiation. J. Exp. Med. 207, 1235-1246 (2010.
7. Buchholz, V.R. et al. Disparate individual fates compose robust CD8+ T cell immunity. Science 340, 630-635 (2013.
8. Gerlach, C. et al. Heterogeneous differentiation patterns of individual CD8+ T cells. Science 340, 635-639 (2013.
9. Chang, J.T. et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315, 1687-1691 (2007.
10. Chang, J.T. et al. Asymmetric proteasome segregation as a mechanism for unequal partitioning of the transcription factor T-bet during T lymphocyte division. Immunity 34, 492-504 (2011.
11. Kaech, S.M., Hemby, S., Kersh, E. & Ahmed, R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111, 837-851 (2002.
12. Best, J.A. et al. Transcriptional insights into the CD8+ T cell response to infection and memory T cell formation. Nat. Immunol. 14, 404-412 (2013.
13. Sarkar, S. et al. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 205, 625-640 (2008.
14. Guo, G. et al. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev. Cell 18, 675-685 (2010.
15. Buganim, Y. et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 150, 1209-1222 (2012.
16. Dalerba, P. et al. Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat. Biotechnol. 29, 1120-1127 (2011.
17. Lu, R., Neff, N.F., Quake, S.R. & Weissman, I.L. Tracking single hematopoietic stem cells in vivo using high-Throughput sequencing in conjunction with viral genetic barcoding. Nat. Biotechnol. 29, 928-933 (2011.
18. Ichii, H. et al. Role for Bcl-6 in the generation and maintenance of memory CD8+ T cells. Nat. Immunol. 3, 558-563 (2002.
19. Kaech, S.M. & Cui, W. Transcriptional control of effector and memory CD8+ T cell differentiation. Nat. Rev. Immunol. 12, 749-761 (2012.
20. Kallies, A., Xin, A., Belz, G.T. & Nutt, S.L. Blimp-1 transcription factor is required for the differentiation of effector CD8+ T cells and memory responses. Immunity 31, 283-295 (2009.
21. Pearce, E.L. et al. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302, 1041-1043 (2003.
22. Rutishauser, R.L. et al. Transcriptional repressor Blimp-1 promotes CD8+ T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 31, 296-308 (2009.
23. Szabo, S.J. et al. Distinct effects of T-bet in TH1 lineage commitment and IFN-γ production in CD4 and CD8 T cells. Science 295, 338-342 (2002.
24. Yang, C.Y. et al. The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8+ T cell subsets. Nat. Immunol. 12, 1221-1229 (2011.
25. Zhou, X. et al. Differentiation and persistence of memory CD8+ T cells depend on T cell factor 1. Immunity 33, 229-240 (2010.
26. Warren, L., Bryder, D., Weissman, I.L. & Quake, S.R. Transcription factor profiling in individual hematopoietic progenitors by digital RT-PCR. Proc. Natl. Acad. Sci. USA 103, 17807-17812 (2006.
27. Masopust, D., Vezys, V., Marzo, A.L. & Lefrancois, L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291, 2413-2417 (2001.
28. Schluns, K.S., Kieper, W.C., Jameson, S.C. & Lefrancois, L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nat. Immunol. 1, 426-432 (2000.
29. Wherry, E.J. et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4, 225-234 (2003.
30. van Der Maaten, L.J.P. & Hinton, G.E. Visualizing high-dimensional data using t-SNE. J. Mach. Learn. Res. 9, 2579-2605 (2008.
31. Freund, Y. & Mason, L. The Alternating Decision Tree Learning Algorithm. In Proceedings of the Sixteenth International Conference on Machine Learning (eds. Bratko, I. & Dzeroski, S.) 124-133 (Morgan Kaufmann Publishers, 1999.
32. Freund, Y. Invited talk: Drifting games, boosting and online learning. In Proceedings of the 26th Annual International Conference on Machine Learning 162, (ACM, 2009.
33. Beerenwinkel, N. & Drton, M. A mutagenetic tree hidden Markov model for longitudinal clonal HIV sequence data. Biostatistics 8, 53-71 (2007.
34. Bulla, J. & Bulla, I. Stylized facts of financial time series and hidden semi-Markov models. Comput. Stat. Data Anal. 51, 2192-2209 (2006.
35. Feau, S., Arens, R., Togher, S. & Schoenberger, S.P. Autocrine IL-2 is required for secondary population expansion of CD8+ memory T cells. Nat. Immunol. 12, 908-913 (2011.
36. Williams, M.A., Tyznik, A.J. & Bevan, M.J. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature 441, 890-893 (2006.
37. Kalia, V. et al. Prolonged interleukin-2Ralpha expression on virus-specific CD8+ T cells favors terminal-effector differentiation in vivo. Immunity 32, 91-103 (2010.
38. Pipkin, M.E. et al. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 32, 79-90 (2010.
39. Obar, J.J. & Lefrancois, L. Early signals during CD8 T cell priming regulate the generation of central memory cells. J. Immunol. 185, 263-272 (2010.
40. Afkarian, M. et al. T-bet is a STAT1-induced regulator of IL-12R expression in naive CD4+ T cells. Nat. Immunol. 3, 549-557 (2002.
41. Lighvani, A.A. et al. T-bet is rapidly induced by interferon-γ in lymphoid and myeloid cells. Proc. Natl. Acad. Sci. USA 98, 15137-15142 (2001.
42. Gebhardt, T. et al. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10, 524-530 (2009.
43. Masopust, D. et al. Dynamic T cell migration program provides resident memory within intestinal epithelium. J. Exp. Med. 207, 553-564 (2010.
44. Olson, J.A., McDonald-Hyman, C., Jameson, S.C. & Hamilton, S.E. Effector-like CD8+ T cells in the memory population mediate potent protective immunity. Immunity 38, 1250-1260 (2013.
45. Tang, F. et al. mRNA-Seq whole-Transcriptome analysis of a single cell. Nat. Methods 6, 377-382 (2009.
46. Shalek, A.K. et al. Single-cell transcriptomics reveals bimodality in expression and splicing in immune cells. Nature 498, 236-240 (2013.
47. Bendall, S.C. et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332, 687-696 (2011.
48. Moon, J.J. et al. Tracking epitope-specific T cells. Nat. Protoc. 4, 565-581 (2009.