Order by chance: origins and benefits of stochasticity in immune cell fate control

Current Opinion in Systems Biology - Tập 18 - Trang 95-103 - 2019
Kathleen Abadie1, Nicholas A. Pease1,2, Matthew J. Wither1, Hao Yuan Kueh1,3
1Department of Bioengineering, University of Washington, United States
2Molecular and Cellular Biology Program, University of Washington, United States
3Institute for Stem Cell and Regenerative Medicine, University of Washington, United States

Tài liệu tham khảo

Gregor, 2007, Stability and nuclear dynamics of the bicoid morphogen gradient, Cell, 130, 141, 10.1016/j.cell.2007.05.026 Gregor, 2005, Diffusion and scaling during early embryonic pattern formation, Proc Natl Acad Sci, 102, 18403, 10.1073/pnas.0509483102 Suda, 1984, Disparate differentiation in mouse hemopoietic colonies derived from paired progenitors, Proc Natl Acad Sci U S A, 81, 2520, 10.1073/pnas.81.8.2520 Weaver, 1998, Heterogeneity in the clonal T cell response: implications for models of T Cell activation and cytokine phenotype development, Immunol Res, 17, 279, 10.1007/BF02786452 Taylor, 2015, Apoptosis and antigen affinity limit effector cell differentiation of a single naive B cell, Science, 347, 784, 10.1126/science.aaa1342 Buchholz, 2013, Disparate individual fates compose robust CD8+ T cell immunity, Science, 340, 630, 10.1126/science.1235454 Hodgkin, 2018, Modifying clonal selection theory with a probabilistic cell, Immunol Rev, 285, 249, 10.1111/imr.12695 Buchholz, 2016, T cell fate at the single-cell level, Annu Rev Immunol, 34, 65, 10.1146/annurev-immunol-032414-112014 Becker, 1963, Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells, Nature, 197, 452, 10.1038/197452a0 Cho, 2017, TCR signal quality modulates fate decisions of single CD4 + T cells in a probabilistic manner, Cell Rep, 20, 806, 10.1016/j.celrep.2017.07.005 Hawkins, 2009, Hodgkin PD: a single-cell pedigree analysis of alternative stochastic lymphocyte fates, Proc Natl Acad Sci, 106, 13457, 10.1073/pnas.0905629106 Gerlach, 2013, Heterogeneous differentiation patterns of individual CD8+ T cells, Science, 340, 635, 10.1126/science.1235487 Duffy, 2012, Hodgkin PD: activation-induced B cell fates are selected by intracellular stochastic competition, Science, 335, 338, 10.1126/science.1213230 Chang, 2007, Asymmetric T lymphocyte division in the initiation of adaptive immune responses, Science, 315, 1687, 10.1126/science.1139393 Verbist, 2016, Metabolic maintenance of cell asymmetry following division in activated T lymphocytes, Nature, 532, 389, 10.1038/nature17442 Hart, 2014, Paradoxical signaling by a secreted molecule leads to homeostasis of cell levels, Cell, 158, 1022, 10.1016/j.cell.2014.07.033 Tkach, 2014, T cells translate individual, quantal activation into collective, analog cytokine responses via time-integrated feedbacks, eLife, 3, 10.7554/eLife.01944 Nish, 2017, Lymphocyte fate and metabolism: a clonal balancing act, Trends Cell Biol, 27, 946, 10.1016/j.tcb.2017.07.005 Kamiński, 2016, Polarization and asymmetry in T cell metabolism, Semin Immunol, 28, 525, 10.1016/j.smim.2016.10.002 Altan-Bonnet, 2019, Cytokine-mediated communication: a quantitative appraisal of immune complexity, Nat Rev Immunol, 19, 205, 10.1038/s41577-019-0131-x Walters, 1995, Enhancers increase the probability but not the level of gene expression, Proc Natl Acad Sci, 92, 7125, 10.1073/pnas.92.15.7125 Hume, 2000, Probability in transcriptional regulation and its implications for leukocyte differentiation and inducible gene expression, Blood, 96, 2323, 10.1182/blood.V96.7.2323 Weintraub, 1988, Formation of stable transcription complexes as assayed by analysis of individual templates, Proc Natl Acad Sci, 85, 5819, 10.1073/pnas.85.16.5819 Raser, 2004, Control of stochasticity in eukaryotic gene expression, Science, 304, 1811, 10.1126/science.1098641 Bintu, 2005, Transcriptional regulation by the numbers: models, Curr Opin Genet Dev, 15, 116, 10.1016/j.gde.2005.02.007 Estrada, 2016, Information integration and energy expenditure in gene regulation, Cell, 166, 234, 10.1016/j.cell.2016.06.012 Liu, 2018, Visualizing transcription factor dynamics in living cells, J Cell Biol, 217, 1181, 10.1083/jcb.201710038 Coulon, 2013, Eukaryotic transcriptional dynamics: from single molecules to cell populations, Nat Rev Genet, 14, 572, 10.1038/nrg3484 Bintu, 2016, Dynamics of epigenetic regulation at the single-cell level, Science, 351, 720, 10.1126/science.aab2956 Angel, 2011, A Polycomb-based switch underlying quantitative epigenetic memory, Nature, 476, 105, 10.1038/nature10241 Wu, 2017, Intrinsic transcriptional heterogeneity in B cells controls early class switching to IgE, J Exp Med, 214, 183, 10.1084/jem.20161056 Ng, 2018, A stochastic epigenetic switch controls the dynamics of T-cell lineage commitment, eLife, 7, 10.7554/eLife.37851 Rhoades, 2000, Allele-specific expression patterns of interleukin-2 and Pax-5 revealed by a sensitive single-cell RT-PCR analysis, Curr Biol, 10, 789, 10.1016/S0960-9822(00)00565-0 Guo, 2005, Probabilistic regulation in TH2 cells accounts for monoallelic expression of IL-4 and IL-13, Immunity, 23, 89, 10.1016/j.immuni.2005.05.008 Mariani, 2010, Short-term memory in gene induction reveals the regulatory principle behind stochastic IL-4 expression, Mol Syst Biol, 6, 359, 10.1038/msb.2010.13 Zhao, 2012, Stochastic expression of the interferon-β gene, PLoS Biol, 10, 16, 10.1371/journal.pbio.1001249 Kravitz, 2019, New subtypes of allele-specific epigenetic effects: implications for brain development, function and disease, Curr Opin Neurobiol, 59, 69, 10.1016/j.conb.2019.04.012 Fuxa, 2007, Reporter gene insertions reveal a strictly B lymphoid-specific expression pattern of Pax5 in support of its B cell identity function, J Immunol, 178, 3031, 10.4049/jimmunol.178.5.3031 Ku, 2015, A monoallelic-to-biallelic T-cell transcriptional switch regulates GATA3 abundance, Genes Dev, 29, 1930, 10.1101/gad.265025.115 Regot, 2014, High-sensitivity measurements of multiple kinase activities in live single cells, Cell, 157, 1724, 10.1016/j.cell.2014.04.039 Hughey, 2015, Single-cell variation leads to population invariance in NF-κB signaling dynamics, Mol Biol Cell, 26, 583, 10.1091/mbc.E14-08-1267 Kellogg, 2015, Noise facilitates transcriptional control under dynamic inputs, Cell, 160, 381, 10.1016/j.cell.2015.01.013 Czerkies, 2018, Cell fate in antiviral response arises in the crosstalk of IRF, NF-κB and JAK/STAT pathways, Nat Commun, 9, 493, 10.1038/s41467-017-02640-8 Feinerman, 2008, Variability and robustness in T cell activation from regulated heterogeneity in protein levels, Science, 321, 1081, 10.1126/science.1158013 Lu, 2016, Systematic analysis of cell-to-cell expression variation of T lymphocytes in a human cohort identifies aging and genetic associations, Immunity, 45, 1162, 10.1016/j.immuni.2016.10.025 Marangoni, 2013, The transcription factor NFAT exhibits signal memory during serial T cell interactions with antigen-presenting cells, Immunity, 38, 237, 10.1016/j.immuni.2012.09.012 Rand, 2012, Multi-layered stochasticity and paracrine signal propagation shape the type-I interferon response, Mol Syst Biol, 8, 584, 10.1038/msb.2012.17 Ashouri, 2017, Endogenous Nur77 is a specific indicator of antigen receptor signaling in human T and B cells, J Immunol, 198, 657, 10.4049/jimmunol.1601301 Richard, 2018, T cell cytolytic capacity is independent of initial stimulation strength, Nat Immunol, 19, 849, 10.1038/s41590-018-0160-9 James, 2018, Tuning ITAM multiplicity on T cell receptors can control potency and selectivity to ligand density, Sci Signal, 11, 10.1126/scisignal.aan1088 Lin, 2019, Mapping the stochastic sequence of individual ligand-receptor binding events to cellular activation: T cells act on the rare events, Sci Signal, 12, 10.1126/scisignal.aat8715 Huang, 2013, A single peptide-major histocompatibility complex ligand triggers digital cytokine secretion in CD4+ T cells, Immunity, 39, 846, 10.1016/j.immuni.2013.08.036 Au-Yeung, 2014, A sharp T-cell antigen receptor signaling threshold for T-cell proliferation, Proc Natl Acad Sci U S A, 111, E3679, 10.1073/pnas.1413726111 Das, 2009, Digital signaling and hysteresis characterize ras activation in lymphoid cells, Cell, 136, 337, 10.1016/j.cell.2008.11.051 Altan-Bonnet, 2005, Modeling T cell antigen discrimination based on feedback control of digital ERK responses, PLoS Biol, 3, e356, 10.1371/journal.pbio.0030356 Martins, 2017, Environment tunes propagation of cell-to-cell variation in the human macrophage gene network, Cell Syst, 4, 379, 10.1016/j.cels.2017.03.002 Su, 2016, Phase separation of signaling molecules promotes T cell receptor signal transduction, Science, 352, 595, 10.1126/science.aad9964 Balagopalan, 2015, The linker for activation of T cells (LAT) signaling hub: from signaling complexes to microclusters, J Biol Chem, 290, 26422, 10.1074/jbc.R115.665869 Kagan, 2014, SMOCs: supramolecular organizing centres that control innate immunity, Nat Rev Immunol, 14, 821, 10.1038/nri3757 Larson, 2017, Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin, Nature, 547, 236, 10.1038/nature22822 Plys, 2019, Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2, Genes Dev, 33, 799, 10.1101/gad.326488.119 Dine, 2018, Protein phase separation provides long-term memory of transient spatial stimuli, Cell Syst, 6, 655, 10.1016/j.cels.2018.05.002 Bracha, 2018, Mapping local and global liquid phase behavior in living cells using photo-oligomerizable seeds, Cell, 175, 1467, 10.1016/j.cell.2018.10.048 Hnisz, 2017, A phase separation model for transcriptional control, Cell, 169, 13, 10.1016/j.cell.2017.02.007 Howard, 2001 Banani, 2017, Biomolecular condensates: organizers of cellular biochemistry, Nat Rev Mol Cell Biol, 18, 285, 10.1038/nrm.2017.7 Zikherman, 2015, The role of T cell receptor signaling thresholds in guiding T cell fate decisions, Curr Opin Immunol, 33, 43, 10.1016/j.coi.2015.01.012 Lo, 2019, Slow phosphorylation of a tyrosine residue in LAT optimizes T cell ligand discrimination, Nat Immunol, 20, 1481, 10.1038/s41590-019-0502-2 Cheng, 2017, Themis2 lowers the threshold for B cell activation during positive selection, Nat Immunol, 18, 205, 10.1038/ni.3642 Symmons, 2016, What's luck got to do with it: single cells, multiple fates, and biological nondeterminism, Mol Cell, 62, 788, 10.1016/j.molcel.2016.05.023 Monahan, 2015, Monoallelic expression of olfactory receptors, Annu Rev Cell Dev Biol, 31, 721, 10.1146/annurev-cellbio-100814-125308 Germain, 2001, The art of the probable: system control in the adaptive immune system, Science, 293, 240, 10.1126/science.1062946 Fatehi, 2018, Stochastic effects in autoimmune dynamics, Front Physiol, 9, 45, 10.3389/fphys.2018.00045 Held, 1998, An allele-specific, stochastic gene expression process controls the expression of multiple Ly49 family genes and generates a diverse, MHC-specific NK cell receptor repertoire, Eur J Immunol, 28, 2407, 10.1002/(SICI)1521-4141(199808)28:08<2407::AID-IMMU2407>3.0.CO;2-D Freund, 2016, Activating receptor signals drive receptor diversity in developing natural killer cells, PLoS Biol, 14 Antebi, 2013, Mapping differentiation under mixed culture conditions reveals a tunable continuum of T cell fates, PLoS Biol, 11, 10.1371/journal.pbio.1001616 Fang, 2017, Dynamic balance between master transcription factors determines the fates and functions of CD4 T cell and innate lymphoid cell subsets, J Exp Med, 214, 1861, 10.1084/jem.20170494 Yang, 2016, Foxp3+ T cells expressing RORγt represent a stable regulatory T-cell effector lineage with enhanced suppressive capacity during intestinal inflammation, Mucosal Immunol, 9, 444, 10.1038/mi.2015.74 Kim, 2017, Generation of RORγt + antigen-specific T regulatory 17 cells from Foxp3 + precursors in autoimmunity, Cell Rep, 21, 195, 10.1016/j.celrep.2017.09.021 Levine, 2017, Stability and function of regulatory T cells expressing the transcription factor T-bet, Nature, 546, 421, 10.1038/nature22360 Eizenberg-Magar, 2017, Diverse continuum of CD4 + T-cell states is determined by hierarchical additive integration of cytokine signals, Proc Natl Acad Sci, 114, E6447, 10.1073/pnas.1615590114 Sugimoto, 2006, Differential cell division history between neutrophils and macrophages in their development from granulocyte–macrophage progenitors, Br J Haematol, 135, 725, 10.1111/j.1365-2141.2006.06367.x Heinzel, 2017, A Myc-dependent division timer complements a cell-death timer to regulate T cell and B cell responses, Nat Immunol, 18, 96, 10.1038/ni.3598 Elowitz, 2002, Stochastic gene expression in a single cell, Science, 297, 1183, 10.1126/science.1070919 Lo, 2018, Lck promotes Zap70-dependent LAT phosphorylation by bridging Zap70 to LAT, Nat Immunol, 19, 733, 10.1038/s41590-018-0131-1 Simeonov, 2017, Discovery of stimulation-responsive immune enhancers with CRISPR activation, Nature, 549, 111, 10.1038/nature23875