From a gene-centric to wholeproteome view of differentiation of T helper cell subsets

Briefings in Functional Genomics

Volumn 12, Issue 6, 2013, Pages 471-482

  Lönnberg, Tapio ^a   Chen, Zhi ^b   Lahesmaa, Riitta ^b  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

Mass spectrometry; Proteomics; Systems biology; T cell activation; T helper cell; Transcriptomics

Indexed keywords

CYCLOPHILIN A; GALECTIN 1; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 6; MESSENGER RNA; PROTEOME; STAT1 PROTEIN; STAT3 PROTEIN; STAT4 PROTEIN; STAT5 PROTEIN; STAT6 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR RUNX1;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION; GENETIC ASSOCIATION; HELPER CELL; HUMAN; INTRACELLULAR SIGNALING; LYMPHOCYTE DIFFERENTIATION; MASS SPECTROMETRY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY;

MASS SPECTROMETRY; PROTEOMICS; SYSTEMS BIOLOGY; T CELL ACTIVATION; T HELPER CELL; TRANSCRIPTOMICS;

ANIMALS; CELL DIFFERENTIATION; HUMANS; MASS SPECTROMETRY; PROTEOME; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84888185946     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/elt033     Document Type: Article

References (93)

1. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations. Annu Rev Immunol 2010;28: 445-89.
2. Kanno Y, Vahedi G, Hirahara K, et al. Transcriptional and epigenetic control of T helper cell specification: molecular mechanisms underlying commitment and plasticity. Annu Rev Immunol 2012;30:707-31.
3. O'Shea JJ, Lahesmaa R, Vahedi G, et al. Genomic views of STAT function in CD4(+) T helper cell differentiation. Nat Rev Immunol 2011;11:239-50.
4. Yamane H, Paul WE. Early signaling events that underlie fate decisions of naive CD4(+) T cells toward distinct T-helper cell subsets. Immunol Rev 2013;252:12-23.
5. Veldhoen M. The role of T helper subsets in autoimmunity and allergy. Curr Opin Immunol 2009;21:606-11.
6. Steen H, Mann M. The ABC's (and XYZ's) of peptide sequencing. Nat RevMol Cell Biol 2004;5:699-711.
7. Cox J, Mann M. Quantitative, high-resolution proteomics for data-driven systems biology. AnnuRev Biochem 2011;80: 273-99.
8. Schulze WX, Usadel B. Quantitation in mass-spectrometry-based proteomics. Annu Rev Plant Biol 2010;61: 491-516.
9. Walther TC, Mann M. Mass spectrometry-based proteomics in cell biology. JCellBiol 2010;190:491-500.
10. Hämäläinen H, Zhou H, Chou W, et al. Distinct gene expression profiles of human type 1 and type 2 T helper cells. Genome Biol 2001;2: RESEARCH0022.
11. Rogge L, Bianchi E, Biffi M, et al. Transcript imaging of the development of human T helper cells using oligonucleotide arrays. Nature Genet 2000;25:96-101.
12. Chen Z, Lund R, Aittokallio T, et al. Identification of novel IL-4/Stat6-regulated genes in T lymphocytes. J Immunol 2003;171:3627-35.
13. Lund RJ, Chen Z, Scheinin J, et al. Early target genes of IL-12 and STAT4 signaling in th cells. J Immunol 2004;172: 6775-82.
14. Lund RJ, Löytömaki M, Naumanen T, et al. Genome-wide identification of novel genes involved in early Th1 and Th2 cell differentiation. J Immunol 2007;178:3648-60.
15. Filén S, Ylikoski E, Tripathi S, et al. Activating transcription factor 3 is a positive regulator of human IFNG gene expression. J Immunol 2010;184:4990-9.
16. Ahlfors H, Limaye A, Elo LL, et al. SATB1 dictates expression of multiple genes including IL-5 involved in human T helper cell differentiation. Blood 2010;116:1443-53.
17. Tahvanainen J, Kallonen T, Lähteenmäki H, et al. PRELI is a mitochondrial regulator of human primary T-helper cell apoptosis, STAT6, and Th2-cell differentiation. Blood 2009; 113:1268-77.
18. Tahvanainen J, Kyläniemi MK, Kanduri K, et al. Proviral integration site for Moloney murine leukemia virus (PIM) kinases promote human T helper 1 cell differentiation. JBiol Chem 2013;288:3048-58.
19. Tuomela S, Salo V, Tripathi SK, et al. Identification of early gene expression changes during human Th17 cell differentiation. Blood 2012;119:e151-60.
20. Yosef N, Shalek AK, Gaublomme JT, et al. Dynamic regulatory network controlling TH17 cell differentiation. Nature 2014;496:461-8.
21. Wei G, Wei L, Zhu J, et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009;30:155-67.
22. Wei L, Vahedi G, Sun H-W, et al. Discrete roles of STAT4 and STAT6 transcription factors in tuning epigenetic modifications and transcription during T helper cell differentiation. Immunity 2010;32:840-51.
23. Aijö T, Edelman SM, Lönnberg T, et al. An integrative computational systems biology approach identifies differentially regulated dynamic transcriptome signatures which drive the initiation of human T helper cell differentiation. BMCGenomics 2012;13:572.
24. Durant L, Watford WT, Ramos HL, et al. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 2010;32:605-15.
25. Liao W, Schones DE, Oh J, et al. Priming for T helper type 2 differentiation by interleukin 2-mediated induction of interleukin 4 receptor _-chain expression. Nat Immunol 2008;9:1288-96.
26. Kwon H, Thierry-Mieg D, Thierry-Mieg J, et al. Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors. Immunity 2009;31:941-52.
27. Yang X-P, Ghoreschi K, Steward-Tharp SM, et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat Immunol 2011;12:247-54.
28. Elo LL, Järvenpää H, Tuomela S, et al. Genome-wide profiling of interleukin-4 and STAT6 transcription factor regulation of human Th2 cell programming. Immunity 2010;32: 852-62.
29. Jenner RG, Townsend MJ, Jackson I, et al. The transcription factors T-bet and GATA-3 control alternative pathways of T-cell differentiation through a shared set of target genes. ProcNatl Acad SciUSA 2009;106:17876-81.
30. Wei G, Abraham BJ, Yagi R, et al. Genome-wide analyses of transcription factor GATA3-mediated gene regulation in distinct T cell types. Immunity 2011;35:299-311.
31. Vahedi G, Takahashi H, Nakayamada S, et al. STATs shape the active enhancer landscape of T cell populations. Cell 2012;151:981-93.
32. Hawkins RD, Larjo A, Tripathi SK, et al. Global chromatin state analysis reveals lineage-specific enhancers during the initiation of human T helper 1 and T helper 2 cell polarization. Immunity 2013;38:1271-84.
33. Vogel C, Marcotte EM. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet 2012;13:227-32.
34. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000;18:217-42.
35. Rosengren AT, Nyman TA, Lahesmaa R. Proteome profiling of interleukin-12 treated human T helper cells. Proteomics 2005;5:3137-41.
36. Rautajoki K, Nyman TA, Lahesmaa R. Proteome characterization of human T helper 1 and 2 cells. Proteomics 2004; 4:84-92.
37. Nyman TA, Matikainen S, Sareneva T, et al. Proteome analysis reveals ubiquitin-conjugating enzymes to be a new family of interferon-alpha-regulated genes. Eur J Biochem 2000;267:4011-9.
38. Rautajoki KJ, Marttila EM, Nyman TA, et al. Interleukin-4 inhibits caspase-3 by regulating several proteins in the Fas pathway during initial stages of human T helper 2 cell differentiation. Mol Cell Proteomics 2007;6:238-51.
39. Tuomela S, Rautajoki KJ, Moulder R, et al. Identification of novel Stat6 regulated proteins in IL-4-treated mouse lymphocytes. Proteomics 2009;9:1087-98.
40. Komine O, Hayashi K, Natsume W, et al. The Runx1 transcription factor inhibits the differentiation of naive CD4+ T cells into the Th2 lineage by repressing GATA3 expression. J ExpMed 2003;198:51-61.
41. Kitoh A, Ono M, Naoe Y, et al. Indispensable role of the Runx1-Cbfbeta transcription complex for in vivo-suppressive function of FoxP3+ regulatory T cells. Immunity 2009; 31:609-20.
42. Loyet KM, Ouyang W, Eaton DL, et al. Proteomic profiling of surface proteins on Th1 and Th2 cells. J ProteomeRes 2005;4:400-9.
43. Billcliff PG, Rollason R, Prior I, et al. CD317/tetherin is an organiser of membrane microdomains. J Cell Sci 2013;126: 1553-64.
44. Swamy M, Siegers GM, Fiala GJ, et al. Stoichiometry and intracellular fate of TRIM-containing TCR complexes. Cell Commun Signal 2010;8:5.
45. Koelsch U, Schraven B, Simeoni L. SIT and TRIM determine T cell fate in the thymus. JImmunol 2008;181:5930-9.
46. Filén J-J, Nyman TA, Korhonen J, et al. Characterization of microsomal fraction proteome in human lymphoblasts reveals the down-regulation of galectin-1 by interleukin-Proteomics 2005;5:4719-32.
47. Motran CC, Molinder KM, Liu SD, et al. Galectin-1 functions as a Th2 cytokine that selectively induces Th1 apoptosis and promotes Th2 function. Eur J Immunol 2008;38: 3015-27.
48. Filén J-J, Filén S, Moulder R, et al. Quantitative proteomics reveals GIMAP family proteins 1 and 4 to be differentially regulated during human T helper cell differentiation. Mol Cell Proteomics 2009;8:32-44.
49. Hu Q, Noll RJ, Li H, et al. The Orbitrap: a new mass spectrometer. JMass Spectrom 2005;40:430-43.
50. Filén S, Lahesmaa R. GIMAP Proteins in T-Lymphocytes. J SignalTransduct 2010;2010:1-10.
51. Moulder R, Lönnberg T, Elo LL, et al. Quantitative proteomics analysis of the nuclear fraction of human CD4+ cells in the early phases of IL-4-induced Th2 differentiation. Mol Cell Proteomics 2010;9:1937-53.
52. Thomas RM, Chen C, Chunder N, et al. Ikaros silences Tbet expression and interferon-gamma production during T helper 2 differentiation. J BiolChem 2010;285:2545-53.
53. Quirion MR, Gregory GD, Umetsu SE, et al. Cutting edge: Ikaros is a regulator of Th2 cell differentiation. J Immunol 2009;182:741-5.
54. Schwanhäusser B, Busse D, Li N, et al. Global quantification of mammalian gene expression control. Nature 2011;473: 337-42.
55. Bjur E, Larsson O, Yurchenko E, et al. Distinct translational control in CD4(+) T cell subsets. PLoS Genet 2013;9: e1003494.
56. Braber den I, Mugwagwa T, Vrisekoop N, et al. Maintenance of peripheral naive T cells is sustained by thymus outputin mice but not humans. Immunity 2012;36: 288-97.
57. Orr SJ, Boutz DR, Wang R, et al. Proteomic and protein interaction network analysis of human T lymphocytes during cell-cycle entry. Mol Syst Biol 2012;8:573.
58. de Wet B, Zech T, Salek M, et al. Proteomic characterization of plasma membrane-proximal T cell activation responses. J BiolChem 2011;286:4072-80.
59. Paterson AM, Vanguri VK, Sharpe AH. SnapShot: B7/ CD28 costimulation. Cell 2009;137:974-4.
60. Kronfeld K, Hochleitner E, Mendler S, et al. B7/CD28 costimulation of T cells induces a distinct proteome pattern. Mol. Cell Proteomics 2005;4:1876-87.
61. Lichtenfels R, Rappl G, Hombach AA, et al. A proteomic view at T cell costimulation. PLoS One 2012;7:e32994.
62. Papin JA, Hunter T, Palsson BO, et al. Reconstruction of cellular signalling networks and analysis of their properties. Nature reviews. Mol Cell Biol 2005;6:99-111.
63. Thingholm TE, Jensen ON, Larsen MR. Analytical strategies for phosphoproteomics. Proteomics 2009;9:1451-68.
64. Abraham RT, Weiss A. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat Rev Immunol 2004;4:301-8.
65. Mayya V, Lundgren DH, Hwang S-I, et al. Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci Signal 2009;2:ra46.
66. Ruperez P, Gago-Martinez A, Burlingame AL, et al. Quantitative phosphoproteomic analysis reveals a role for serine and threonine kinases in the cytoskeletal reorganization in early T-cell receptor (TCR) activation in human primary T-cells. Mol Cell Proteomics 2012;11:171-86.
67. Carrascal M, Ovelleiro D, Casas V, et al. Phosphorylation analysis of primary human T lymphocytes using sequential IMAC and titanium oxide enrichment. J ProteomeRes 2008; 7:5167-76.
68. Pawson T, Scott JD. Protein phosphorylation in signaling- 50 years and counting. Trends Biochem Sci 2005;30:286-90.
69. Kim J-E, White FM. Quantitative analysis of phosphotyrosine signaling networks triggered by CD3 and CD28 costimulation in Jurkat cells. J Immunol 2006;176:2833-43.
70. Osinalde N, Moss H, Arrizabalaga O, et al. Interleukin-2 signaling pathway analysis by quantitative phosphoproteomics. J Proteomics 2011;75:177-91.
71. Wieczorek M, Ginter T, Brand P, et al. Acetylation modulates the STAT signaling code. Cytokine Growth Factor Rev 2012;23:293-305.
72. Fathman JW, Gurish MF, Hemmers S, et al. NIP45 controls the magnitude of the type 2 T helper cell response. ProcNatl Acad SciUSA 2010;107:3663-8.
73. Choudhary C, Mann M. Decoding signalling networks by mass spectrometry-based proteomics. Nature reviews. Molecular Cell Biol 2010;11:427-39.
74. Zhao Y, Jensen ON. Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques. Proteomics 2009;9:4632-41.
75. Köcher T, Superti-Furga G. Mass spectrometry-based functional proteomics: from molecular machines to protein networks. NatMethods 2007;4:807-15.
76. Hosokawa H, Tanaka T, Suzuki Y, et al. Functionally distinct Gata3/Chd4 complexes coordinately establish T helper 2 (Th2) cell identity. Proc Natl Acad Sci USA 2013; 110:4691-6.
77. Rudra D, Deroos P, Choudhry A, et al. Transcription factor Foxp3 and its protein partners form a complex regulatory network. Nat Immunol 2012;13:1010-9.
78. Hwang E-S, Szabo SJ, Schwartzberg PL, et al. T helper cell fate specified by kinase-mediated interaction of T-bet with GATA-3. Science 2005;307:430-3.
79. Oestreich KJ, Huang AC, Weinmann AS. The lineagedefining factors T-bet and Bcl-6 collaborate to regulate Th1 gene expression patterns. JExpMed 2011;208:1001-13.
80. Oestreich KJ, Weinmann AS. Master regulators or lineagespecifying? Changing views on CD4+ T cell transcription factors. Nat Rev Immunol 2012;12:799-804.
81. Beck M, Schmidt A, Malmstroem J, et al. The quantitative proteome of a human cell line. Mol Syst Biol 2011;7:549.
82. Rubakhin SS, Romanova EV, Nemes P, et al. Profiling metabolites and peptides in single cells. Nat Methods 2011; 8:S20-9.
83. Bendall SC, Nolan GP, Roederer M, et al. A deep profiler's guide to cytometry. Trends Immunol 2012;33:323-32.
84. Geiger T, Wehner A, Schaab C, et al. Comparative proteomic analysis of eleven common cell lines reveals ubiquitous but varying expression of most proteins. Mol Cell Proteomics 2012;11: M111.014050.
85. Altelaar AFM, Heck AJR. Trends in ultrasensitive proteomics. Curr Opin Chem Biol 2012;16:206-13.
86. Gallien S, Duriez E, Domon B. Selected reaction monitoring applied to proteomics. JMassSpectrom 2011;46:298-312.
87. Picotti P, Bodenmiller B, Mueller LN, et al. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009;138:795-806.
88. Gillet LC, Navarro P, Tate S, et al. Targeted data extraction of the MS/MS spectra generated by data-independent acquisition: a new concept for consistent and accurate proteome analysis. Mol Cell Proteomics 2012;11: O111.016717.
89. ÖGarra A, Gabryšovà L, Spits H. Quantitative events determine the differentiation and function of helper T cells. Nat Immunol 2011;12:288-94.
90. O'Shea JJ, Paul WE. Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 2010;327:1098-102.
91. Gerber SA, Rush J, Stemman O, et al. Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc Natl Acad Sci USA 2003;100: 6940-5.
92. Lu P, Vogel C, Wang R, et al. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol 2007;25: 117-24.
93. Simicevic J, Schmid AW, Gilardoni PA, et al. Absolute quantification of transcription factors during cellular differentiation using multiplexed targeted proteomics. Nat Methods 2013;10:570-6.