A multi-scale approach reveals that NF-κB cRel enforces a B-cell decision to divide

Molecular Systems Biology

Volumn 11, Issue 2, 2015, Pages

  Shokhirev, Maxim N ^a,b   Almaden, Jonathan ^a   Davis Turak, Jeremy ^a,b   Birnbaum, Harry A ^a,b,c,d   Russell, Theresa M ^e   Vargas, Jesse A D ^a,b,c,d   Hoffmann, Alexander ^a,b,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California San Diego   (United States)

^c Institute for Quantitative and Computational Biosciences   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e FLUIDIGM CORPORATION   (United States)

Author keywords

apoptosis; B lymphocyte; cell cycle; cell fate decision; NF B cRel

Indexed keywords

CELL CYCLE PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CREL; TRANSCRIPTOME; UNCLASSIFIED DRUG; TRANSCRIPTION FACTOR REL;

ANIMAL CELL; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL CYCLE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL DEATH; CELL DIVISION; CELL FATE; CELL FUNCTION; CELL GROWTH; CELL SURVIVAL; CELL TRACKING; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DECISION MAKING; FLOW CYTOMETRY; GENOTYPE; HUMAN; IMMUNE RESPONSE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOFLUORESCENCE TEST; LYMPHOCYTE SUBPOPULATION; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; POPULATION DYNAMICS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; TIME-LAPSE VIDEO MICROSCOPY; WILD TYPE; ANIMAL; CELL PROLIFERATION; CYTOLOGY; METABOLISM; MOLECULAR MODEL; SEQUENCE ANALYSIS; SPLEEN;

ANIMALS; APOPTOSIS; B-LYMPHOCYTES; CELL DIVISION; CELL PROLIFERATION; MICE; MODELS, MOLECULAR; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-REL; SEQUENCE ANALYSIS, RNA; SIGNAL TRANSDUCTION; SPLEEN;

EID: 84923641128     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20145554     Document Type: Article

References (48)

1. Alves BN, Tsui R, Almaden J, Shokhirev MN, Davis-Turak J, Fujimoto J, Birnbaum H, Ponomarenko J, Hoffmann A, (2014) IkappaB} is a key regulator of B cell expansion by providing negative feedback on cRel and RelA in a stimulus-specific manner. J Immunol 192: 3121-3132
2. An G, (2008) Introduction of an agent-based multi-scale modular architecture for dynamic knowledge representation of acute inflammation. Theor Biol Med Model 5: 11
3. An G, Mi Q, Dutta-Moscato J, Vodovotz Y, (2009) Agent-based models in translational systems biology. Wiley Interdiscip Rev Syst Biol Med 1: 159-171
4. Basak S, Behar M, Hoffmann A, (2012) Lessons from mathematically modeling the NF-kappaB pathway. Immunol Rev 246: 221-238
5. Browne EP, (2012) Regulation of B-cell responses by Toll-like receptors. Immunology 136: 370-379
6. Chakravorty R, Rawlinson D, Zhang A, Markham J, Dowling MR, Wellard C, Zhou JH, Hodgkin PD, (2014) Labour-efficient in vitro lymphocyte population tracking and fate prediction using automation and manual review. PLoS ONE 9: e83251
7. Chattopadhyay PK, Gierahn TM, Roederer M, Love JC, (2014) Single-cell technologies for monitoring immune systems. Nat Immunol 15: 128-135
8. Chen F, Demers LM, Vallyathan V, Lu Y, Castranova V, Shi X, (1999) Involvement of 5-flanking kappaB-like sites within bcl-x gene in silica-induced Bcl-x expression. J Biol Chem 274: 35591-35595
9. Church DM, Goodstadt L, Hillier LW, Zody MC, Goldstein S, She X, Bult CJ, Agarwala R, Cherry JL, DiCuccio M, Hlavina W, Kapustin Y, Meric P, Maglott D, Birtle Z, Marques AC, Graves T, Zhou S, Teague B, Potamousis K, et al, (2009) Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 7: e1000112
10. Conradie R, Bruggeman FJ, Ciliberto A, Csikasz-Nagy A, Novak B, Westerhoff HV, Snoep JL, (2010) Restriction point control of the mammalian cell cycle via the cyclin E/Cdk2:p27 complex. FEBS J 277: 357-367
11. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR, (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21
12. Duffy KR, Wellard CJ, Markham JF, Zhou JH, Holmberg R, Hawkins ED, Hasbold J, Dowling MR, Hodgkin PD, (2012) Activation-induced B cell fates are selected by intracellular stochastic competition. Science 335: 338-341
13. Duyao MP, Buckler AJ, Sonenshein GE, (1990) Interaction of an NF-kappa B-like factor with a site upstream of the c-myc promoter. Proc Natl Acad Sci USA 87: 4727-4731
14. Flusberg DA, Roux J, Spencer SL, Sorger PK, (2013) Cells surviving fractional killing by TRAIL exhibit transient but sustainable resistance and inflammatory phenotypes. Mol Biol Cell 24: 2186-2200
15. Gaudet S, Spencer SL, Chen WW, Sorger PK, (2012) Exploring the contextual sensitivity of factors that determine cell-to-cell variability in receptor-mediated apoptosis. PLoS Comput Biol 8: e1002482
16. Gerondakis S, Grumont R, Rourke I, Grossmann M, (1998) The regulation and roles of Rel/NF-kappa B transcription factors during lymphocyte activation. Curr Opin Immunol 10: 353-359
17. Gerondakis S, Siebenlist U, (2010) Roles of the NF-kappaB pathway in lymphocyte development and function. Cold Spring Harb Perspect Biol 2: a000182
18. Grumont RJ, Rourke IJ, O'Reilly LA, Strasser A, Miyake K, Sha W, Gerondakis S, (1998) B lymphocytes differentially use the Rel and nuclear factor kappaB1 (NF-kappaB1) transcription factors to regulate cell cycle progression and apoptosis in quiescent and mitogen-activated cells. J Exp Med 187: 663-674
19. Grumont RJ, Strasser A, Gerondakis S, (2002) B cell growth is controlled by phosphatidylinosotol 3-kinase-dependent induction of Rel/NF-kappaB regulated c-myc transcription. Mol Cell 10: 1283-1294
20. Guttridge DC, Albanese C, Reuther JY, Pestell RG, Baldwin AS Jr, (1999) NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1. Mol Cell Biol 19: 5785-5799
21. Hawkins ED, Hommel M, Turner ML, Battye FL, Markham JF, Hodgkin PD, (2007a) Measuring lymphocyte proliferation, survival and differentiation using CFSE time-series data. Nat Protoc 2: 2057-2067
22. Hawkins ED, Turner ML, Dowling MR, van Gend C, Hodgkin PD, (2007b) A model of immune regulation as a consequence of randomized lymphocyte division and death times. Proc Natl Acad Sci USA 104: 5032-5037
23. Hawkins ED, Markham JF, McGuinness LP, Hodgkin PD, (2009) A single-cell pedigree analysis of alternative stochastic lymphocyte fates. Proc Natl Acad Sci USA 106: 13457-13462
24. Huang Y, Ohtani K, Iwanaga R, Matsumura Y, Nakamura M, (2001) Direct trans-activation of the human cyclin D2 gene by the oncogene product Tax of human T-cell leukemia virus type I. Oncogene 20: 1094-1102
25. Hyrien O, Chen R, Zand MS, (2010) An age-dependent branching process model for the analysis of CFSE-labeling experiments. Biol Direct 5: 41
26. Jiao B, Ma H, Shokhirev MN, Drung A, Yang Q, Shin J, Lu S, Byron M, Kalantry S, Mercurio AM, Lawrence JB, Hoffmann A, Bach I, (2012) Paternal RLIM/Rnf12 is a survival factor for milk-producing alveolar cells. Cell 149: 630-641
27. Lee TJ, Yao G, Bennett DC, Nevins JR, You L, (2010) Stochastic E2F activation and reconciliation of phenomenological cell-cycle models. PLoS Biol 8: e1000488
28. Link JM, Hurlin PJ, (2014) The activities of MYC, MNT and the Max-Interactome in lymphocyte proliferation and oncogenesis. Biochim Biophys Acta, doi: 10.1016/j.bbagrm.2014.04.004
29. Loriaux PM, Hoffmann A, (2012) A framework for modeling the relationship between cellular steady-state and stimulus-responsiveness. Methods Cell Biol 110: 81-109
30. Loriaux PM, Tesler G, Hoffmann A, (2013) Characterizing the relationship between steady state and response using analytical expressions for the steady states of mass action models. PLoS Comput Biol 9: e1002901
31. Macaulay IC, Voet T, (2014) Single cell genomics: advances and future perspectives. PLoS Genet 10: e1004126
32. Murphy K, Travers P, Walport M, (2007) Janeway's Immunobiology. New York, NY: Garland Science
33. Narang V, Decraene J, Wong SY, Aiswarya BS, Wasem AR, Leong SR, Gouaillard A, (2012) Systems immunology: a survey of modeling formalisms, applications and simulation tools. Immunol Res 53: 251-265
34. Pogson M, Smallwood R, Qwarnstrom E, Holcombe M, (2006) Formal agent-based modelling of intracellular chemical interactions. Biosystems 85: 37-45
35. Pohl T, Gugasyan R, Grumont RJ, Strasser A, Metcalf D, Tarlinton D, Sha W, Baltimore D, Gerondakis S, (2002) The combined absence of NF-kB1 and c-Rel reveals that overlapping roles of these transcription factors in the B cell lineage are restricted to the activation and function of mature cells. PNAS 99: 4514-4519
36. Rawlings DJ, Schwartz MA, Jackson SW, Meyer-Bahlburg A, (2012) Integration of B cell responses through Toll-like receptors and antigen receptors. Nat Rev Immunol 12: 282-294
37. Renault TT, Chipuk JE, (2013) Getting away with murder: how does the BCL-2 family of proteins kill with immunity? Ann N Y Acad Sci 1285: 59-79
38. Shokhirev MN, Hoffmann A, (2013) FlowMax: a computational tool for maximum likelihood deconvolution of CFSE time courses. PLoS ONE 8: e67620
39. Shokhirev MN, Johnson AA, (2014) Effects of extrinsic mortality on the evolution of aging: a stochastic modeling approach. PLoS ONE 9: e86602
40. Spencer SL, Gaudet S, Albeck JG, Burke JM, Sorger PK, (2009) Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 459: 428-432
41. Spencer SL, Sorger PK, (2011) Measuring and modeling apoptosis in single cells. Cell 144: 926-939
42. Spencer SL, Cappell SD, Tsai FC, Overton KW, Wang CL, Meyer T, (2013) The proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit. Cell 155: 369-383
43. Staudt LM, (2010) Oncogenic activation of NF-kappaB. Cold Spring Harb Perspect Biol 2: a000109
44. Walker DC, Hill G, Wood SM, Smallwood RH, Southgate J, (2004) Agent-based computational modeling of wounded epithelial cell monolayers. IEEE Trans Nanobiosci 3: 153-163
45. Wang Z, Sicinski P, Weinberg RA, Zhang Y, Ravid K, (1996) Characterization of the mouse cyclin D3 gene: exon/intron organization and promoter activity. Genomics 35: 156-163
46. Wang R, Dillon CP, Shi LZ, Milasta S, Carter R, Finkelstein D, McCormick LL, Fitzgerald P, Chi H, Munger J, Green DR, (2011) The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity 35: 871-882
47. Wang J, Duncan D, Shi Z, Zhang B, (2013) WEB-based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Res 41: W77-W83
48. Yusuf I, Fruman DA, (2003) Regulation of quiescence in lymphocytes. Trends Immunol 24: 380-386