Switching of the relative dominance between feedback mechanisms in lipopolysaccharide-induced NF-κB signaling

Science Signaling

Volumn 7, Issue 308, 2014, Pages

  Sung, Myong Hee ^a   Li, Ning ^b   Lao, Qizong ^a   Gottschalk, Rachel A ^b   Hager, Gordon L ^a   Fraser, Iain D C ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IKAROS TRANSCRIPTION FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; FEEDBACK SYSTEM; GENE EXPRESSION; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LYMPHOID CELL; MACROPHAGE; MATHEMATICAL MODEL; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

FEEDBACK; LIPOPOLYSACCHARIDES; NF-KAPPA B; SIGNAL TRANSDUCTION;

EID: 84892634483     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004764     Document Type: Article

References (37)

1. A. Banerjee, S. Gerondakis, Coordinating TLR-activated signaling pathways in cells of the immune system. Immunol. Cell Biol. 85, 420-424 (2007).
2. R. Medzhitov, Recognition of microorganisms and activation of the immune response. Nature 449, 819-826 (2007).
3. T. P. Monie, C. E. Bryant, N. J. Gay, Activating immunity: Lessons from the TLRs and NLRs. Trends Biochem. Sci. 34, 553-561 (2009).
4. S. T. Smale, Selective transcription in response to an inflammatory stimulus. Cell 140, 833-844 (2010).
5. E. O'Dea, A. Hoffmann, The regulatory logic of the NF-κB signaling system. Cold Spring Harb. Perspect. Biol. 2, a000216 (2010).
6. D. E. Nelson, A. E. Ihekwaba, M. Elliott, J. R. Johnson, C. A. Gibney, B. E. Foreman, G. Nelson, V. See, C. A. Horton, D. G. Spiller, S. W. Edwards, H. P. McDowell, J. F. Unitt, E. Sullivan, R. Grimley, N. Benson, D. Broomhead, D. B. Kell, M. R. White, Oscillations in NF-κB signaling control the dynamics of gene expression. Science 306, 704-708 (2004).
7. M. H. Sung, L. Salvatore, R. De Lorenzi, A. Indrawan, M. Pasparakis, G. L. Hager, M. E. Bianchi, A. Agresti, Sustained oscillations of NF-κB produce distinct genome scanning and gene expression profiles. PLOS One 4, e7163 (2009).
8. J. D. Kearns, S. Basak, S. L. Werner, C. S. Huang, A. Hoffmann, IκBε provides negative feedback to control NF-κB oscillations, signaling dynamics, and inflammatory gene expression. J. Cell Biol. 173, 659-664 (2006).
9. P. Paszek, S. Ryan, L. Ashall, K. Sillitoe, C. V. Harper,D. G. Spiller, D. A. Rand, M. R.White, Population robustness arising from cellular heterogeneity. Proc. Natl. Acad. Sci. U.S.A. 107, 11644-11649 (2010).
10. S. L. Werner, J. D. Kearns, V. Zadorozhnaya, C. Lynch, E. O'Dea, M. P. Boldin, A. Ma, D. Baltimore, A. Hoffmann, Encoding NF-κB temporal control in response to TNF: Distinct roles for the negative regulators IκBα and A20. Genes Dev. 22, 2093-2101 (2008).
11. L. Ashall, C. A. Horton, D. E. Nelson, P. Paszek, C. V. Harper, K. Sillitoe, S. Ryan, D. G. Spiller, J. F. Unitt, D. S. Broomhead, D. B. Kell, D. A. Rand, V. Sée, M. R. White, Pulsatile stimulation determines timing and specificity of NF-κB-dependent transcription. Science 324, 242-246 (2009).
12. S. Bartfeld, S. Hess, B. Bauer, N. Machuy, L. A. Ogilvie, J. Schuchhardt, T. F. Meyer, High-throughput and single-cell imaging of NF-κB oscillations using monoclonal cell lines. BMC Cell Biol. 11, 21 (2010).
13. T. K. Lee, E. M. Denny, J. C. Sanghvi, J. E. Gaston, N. D. Maynard, J. J. Hughey, M. W. Covert, A noisy paracrine signal determines the cellular NF-κB response to lipopolysaccharide. Sci. Signal. 2, ra65 (2009).
14. S. Tay, J. J. Hughey, T. K. Lee, T. Lipniacki, S. R. Quake, M. W. Covert, Single-cell NF-κB dynamics reveal digital activation and analogue information processing. Nature 466, 267-271 (2010).
15. U. Rand, M. Rinas, J. Schwerk, G. Nöhren, M. Linnes, A. Kröger, M. Flossdorf, K. Kály-Kullai, H. Hauser, T. Höfer, M. Köster, Multi-layered stochasticity and paracrine signal propagation shape the type-I interferon response. Mol. Syst. Biol. 8, 584 (2012).
16. E. M. Ozbudak, M. Thattai, I. Kurtser, A. D. Grossman, A. van Oudenaarden, Regulation of noise in the expression of a single gene. Nat. Genet. 31, 69-73 (2002).
17. J. M. Raser, E. K. O'Shea, Noise in gene expression: Origins, consequences, and control. Science 309, 2010-2013 (2005).
18. V. Litvak, S. A. Ramsey, A. G. Rust, D. E. Zak, K. A. Kennedy, A. E. Lampano, M. Nykter, I. Shmulevich, A. Aderem, Function of C/EBPδ in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat. Immunol. 10, 437-443 (2009).
19. P. Rao, M. S. Hayden, M. Long, M. L. Scott, A. P. West, D. Zhang, A. Oeckinghaus, C. Lynch, A. Hoffmann, D. Baltimore, S. Ghosh, IκBβ acts to inhibit and activate gene expression during the inflammatory response. Nature 466, 1115-1119 (2010).
20. G. D. Barish, R. T. Yu, M. Karunasiri, C. B. Ocampo, J. Dixon, C. Benner, A. L. Dent, R. K. Tangirala, R. M. Evans, Bcl-6 and NF-κB cistromes mediate opposing regulation of the innate immune response. Genes Dev. 24, 2760-2765 (2010).
21. S. Doyle, S. Vaidya, R. O' Connell, H. Dadgostar, P. Dempsey, T. Wu, G. Rao, R. Sun, M. Haberland, R. Modlin, G. Cheng, IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity 17, 251-263 (2002).
22. M. Gilchrist, V. Thorsson, B. Li, A. G. Rust, M. Korb, J. C. Roach, K. Kennedy, T. Hai, H. Bolouri, A. Aderem, Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441, 173-178 (2006).
23. M. Garber, N. Yosef, A. Goren, R. Raychowdhury, A. Thielke, M. Guttman, J. Robinson, B. Minie, N. Chevrier, Z. Itzhaki, R. Blecher-Gonen, C. Bornstein, D. Amann-Zalcenstein, A. Weiner, D. Friedrich, J. Meldrim, O. Ram, C. Cheng, A. Gnirke, S. Fisher, N. Friedman, B.Wong, B. E. Bernstein, C. Nusbaum, N. Hacohen, A. Regev, I. Amit, A high-throughput chromatin immunoprecipitation approach reveals principles of dynamic gene regulation in mammals. Mol. Cell 47, 810-822 (2012).
24. E. A. Wall, J. R. Zavzavadjian, M. S. Chang, B. Randhawa, X. Zhu, R. C. Hsueh, J. Liu, A. Driver, X. R. Bao, P. C. Sternweis, M. I. Simon, I. D. Fraser, Suppression of LPS-induced TNF-α production in macrophages by cAMP is mediated by PKA-AKAP95-p105. Sci. Signal. 2, ra28 (2009).
25. L. Escoubet-Lozach, C. Benner, M. U. Kaikkonen, J. Lozach, S. Heinz, N. J. Spann, A. Crotti, J. Stender, S. Ghisletti, D. Reichart, C. S. Cheng, R. Luna, C. Ludka, R. Sasik, I. Garcia-Bassets, A. Hoffmann, S. Subramaniam, G. Hardiman, M. G. Rosenfeld, C. K. Glass, Mechanisms establishing TLR4-responsive activation states of inflammatory response genes. PLOS Genet. 7, e1002401 (2011).
26. J. H. Wang, A. Nichogiannopoulou, L. Wu, L. Sun, A. H. Sharpe, M. Bigby, K. Georgopoulos, Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 5, 537-549 (1996).
27. A. Hoffmann, A. Levchenko, M. L. Scott, D. Baltimore, The IκB-NF-κB signaling module: Temporal control and selective gene activation. Science 298, 1241-1245 (2002).
28. D. A. Turner, P. Paszek, D. J. Woodcock, D. E. Nelson, C. A. Horton, Y.Wang, D. G. Spiller, D. A. Rand, M. R. White, C. V. Harper, Physiological levels of TNFα stimulation induce stochastic dynamics of NF-κB responses in single living cells. J. Cell Sci. 123, 2834-2843 (2010).
29. L. M. Coussens, Z. Werb, Inflammation and cancer. Nature 420, 860-867 (2002).
30. T. Yoshida, S. Y. Ng, K. Georgopoulos, Awakening lineage potential by Ikaros-mediated transcriptional priming. Curr. Opin. Immunol. 22, 154-160 (2010).
31. R. Cheong, A. Rhee, C. J. Wang, I. Nemenman, A. Levchenko, Information transduction capacity of noisy biochemical signaling networks. Science 334, 354-358 (2011).
32. M. V. Gutschow, J. J. Hughey, N. A. Ruggero, B. T. Bajar, S. D. Valle, M. W. Covert, Singlecell and population NF-κB dynamic responses depend on lipopolysaccharide preparation. PLOS One 8, e53222 (2013).
33. I. Fraser,W. Liu, R. Rebres, T. Roach, J. Zavzavadjian, L. Santat, J. Liu, E.Wall, M. Mumby, The use of RNA interference to analyze protein phosphatase function in mammalian cells. Methods Mol. Biol. 365, 261-286 (2007).
34. X. Li, X. Zhao, Y. Fang, X. Jiang, T. Duong, C. Fan, C. C. Huang, S. R. Kain, Generation of destabilized green fluorescent protein as a transcription reporter. J. Biol. Chem. 273, 34970-34975 (1998).
35. M. W. Covert, T. H. Leung, J. E. Gaston, D. Baltimore, Achieving stability of lipopolysaccharide-induced NF-κB activation. Science 309, 1854-1857 (2005).
36. J. C. Kagan, T. Su, T. Horng, A. Chow, S. Akira, R. Medzhitov, TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-β. Nat. Immunol. 9, 361-368 (2008).
37. I. Zanoni, R. Ostuni, L. R. Marek, S. Barresi, R. Barbalat, G.M. Barton, F. Granucci, J. C. Kagan, CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147, 868-880 (2011).