Single-cell variation leads to population invariance in NF-κB signaling dynamics

Molecular Biology of the Cell

Volumn 26, Issue 3, 2015, Pages 583-590

  Hughey, Jacob J ^a   Gutschow, Miriam V ^a   Bajar, Bryce T ^a   Covert, Markus W ^a  

^a Stanford University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ARTICLE; CELL DIVISION; CELL NUCLEUS MEMBRANE; DAUGHTER CELL; GENE EXPRESSION; MOLECULAR DYNAMICS; OSCILLATION; OUTER MEMBRANE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; ACTIVE TRANSPORT; ANIMAL; CELL NUCLEUS; CHEMISTRY; KINETICS; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; KINETICS; MICE; NF-KAPPA B; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SINGLE-CELL ANALYSIS;

EID: 84921842476     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E14-08-1267     Document Type: Article

References (34)

1. Alves BN, Tsui R, Almaden J, Shokhirev MN, Davis-Turak J, Fujimoto J, Hoffmann A (2014). IκBε 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. Ashall L, Horton CA, Nelson DE, Paszek P, Harper CV, Sillitoe K, Ryan S, Spiller DG, Unitt JF, Broomhead DS, et al. (2009). Pulsatile stimulation determines timing and specificity of NF-κB-dependent transcription. Science 324, 242-246.
3. Barken D, Wang CJ, Kearns J, Cheong R, Hoffmann A, Levchenko A (2005). Comment on "Oscillations in NF-kappaB signaling control the dynamics of gene expression." Science 308, 52.
4. Cheng CS, Feldman KE, Lee J, Verma S, Huang DB, Huynh K, Chang M, Ponomarenko JV, Sun SC, Benedict CA, et al. (2011). The specificity of innate immune responses is enforced by repression of interferon response elements by NF-κB p50. Sci Signal 4, ra11.
5. Cheong R, Rhee A, Wang CJ, Nemenman I, Levchenko A (2011). Information transduction capacity of noisy biochemical signaling networks. Science 334, 354-358.
6. Covert MW, Leung TH, Gaston JE, Baltimore D (2005). Achieving stability of lipopolysaccharide-induced NF-kappaB activation. Science 309, 1854-1857.
7. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N (2010). Computer control of microscopes using μManager. Curr Protoc Mol Biol Chapter 14, Unit 14.20.
8. Elowitz MB, Levine AJ, Siggia ED, Swain PS (2002). Stochastic gene expression in a single cell. Science 297, 1183-1186.
9. 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.
10. Geva-Zatorsky N, Rosenfeld N, Itzkovitz S, Milo R, Sigal A, Dekel E, Yarnitzky T, Liron Y, Polak P, Lahav G, Alon U (2006). Oscillations and variability in the p53 system. Mol Syst Biol 2, 2006.0033.
11. Gitlin L, Benoit L, Song C, Cella M, Gilfillan S, Holtzman MJ, Colonna M (2010). Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog 6, e1000734.
12. Gutschow MV, Hughey JJ, Ruggero NA, Bajar BT, Valle SD, Covert MW (2013). Single-cell and population NF-κB dynamic responses depend on lipopolysaccharide preparation. PLoS One 8, e53222.
13. Hayden MS, West AP, Ghosh S (2006). NF-κB and the immune response. Oncogene 25, 6758-6780.
14. Hirschfeld M, Kirschning CJ, Schwandner R, Wesche H, Weis JH, Wooten RM, Weis JJ (1999). Inflammatory signaling by Borrelia burgdorferi lipoproteins is mediated by toll-like receptor 2. J Immunol 163, 2382-2386.
15. Hoffmann A, Levchenko A, Scott ML, Baltimore D (2002). The IκB-NF-κB signaling module: temporal control and selective gene activation. Science 298, 1241-1245.
16. Kamentsky L, Jones TR, Fraser A, Bray MA, Logan DJ, Madden KL, Carpenter AE (2011). Improved structure, function and compatibility for CellProfiler: modular high-throughput image analysis software. Bioinformatics 27, 1179-1180.
17. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, et al. (2006). Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105.
18. Kawai T, Akira S (2006). TLR signaling. Cell Death Differ 13, 816-825.
19. Lee TK, Denny EM, Sanghvi JC, Gaston JE, Maynard ND, Hughey JJ, Covert MW (2009). A noisy paracrine signal determines the cellular NF-kappaB response to lipopolysaccharide. Sci Signal 2, ra65.
20. Leise TL, Wang CW, Gitis PJ, Welsh DK (2012). Persistent cell-autonomous circadian oscillations in fibroblasts revealed by six-week single-cell imaging of PER2::LUC bioluminescence. PLoS One 7, e33334.
21. Lipniacki T, Paszek P, Brasier AR, Luxon B, Kimmel M (2004). Mathematical model of NF-κB regulatory module. J Theor Biol 228, 195-215.
22. Longo DM, Selimkhanov J, Kearns JD, Hasty J, Hoffmann A, Tsimring LS (2013). Dual delayed feedback provides sensitivity and robustness to the NF- κB signaling module. PLoS Comput Biol 9, e1003112.
23. Nelson DE, Ihekwaba AE, Elliott M, Johnson JR, Gibney CA, Foreman BE, Nelson G, See V, Horton CA, Spiller DG, et al. (2004). Oscillations in NF-kappaB signaling control the dynamics of gene expression. Science 306, 704-708.
24. Ozinsky A, Underhill DM, Fontenot JD, Hajjar AM, Smith KD, Wilson CB, Schroeder L, Aderem A (2000). The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc Natl Acad Sci USA 97, 13766-13771.
25. Pahl HL (1999). Activators and target genes of Rel/NF-kB transcription factors. Oncogene 18, 6853-6866.
26. Paszek P, Ryan S, Ashall L, Sillitoe K, Harper CV, Spiller DG, Rand DA, White MRH (2010). Population robustness arising from cellular heterogeneity. Proc Natl Acad Sci USA 107, 11644-9.
27. Pekalski J, Zuk PJ, Kochanczyk M, Junkin M, Kellogg R, Tay S, Lipniacki T (2013). Spontaneous NF-κB activation by autocrine TNFα signaling: a computational analysis. PLoS One 8, e78887.
28. Purvis JE, Karhohs KW, Mock C, Batchelor E, Loewer A, Lahav G (2012). P53 dynamics control cell fate. Science 336, 1440-1444.
29. Shinohara H, Behar M, Inoue K, Hiroshima M, Yasuda T, Nagashima T, Kimura S, Sanjo H, Maeda S, Yumoto N, et al. (2014). Positive feedback within a kinase signaling complex functions as a switch mechanism for NF-κB activation. Science 344, 760-764.
30. 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.
31. Sung MH, Li N, Lao Q, Gottschalk RA, Hager GL, Fraser ID (2014). Switching of relative dominance between feedback mechanisms in lipopolysaccharide-induced NF-κB signaling. Sci Signal 7, ra6.
32. Sung MH, Salvatore L, De Lorenzi R, Indrawan A, Pasparakis M, Hager GL, Bianchi ME, Agresti A (2009). Sustained oscillations of NF-κB produce distinct genome scanning and gene expression profiles. PLoS One 4, e7163.
33. Tay S, Hughey JJ, Lee TK, Lipniacki T, Quake SR, Covert MW (2010). Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 466, 267-271.
34. Turner DA, Paszek P, Woodcock DJ, Nelson DE, Horton CA, Wang Y, Spiller DG, Rand DA, White MRH, Harper CV (2010). Physiological levels of TNFalpha stimulation induce stochastic dynamics of NF-kappaB responses in single living cells. J Cell Sci 123, 2834-2843.