Interrogation of inhibitor of nuclear factor κB α/nuclear factor κB (IκBα/NF-κB) negative feedback loop dynamics: From single cells to live animals in vivo

Journal of Biological Chemistry

Volumn 287, Issue 37, 2012, Pages 31359-31370

  Moss, Britney L ^a   Elhammali, Adnan ^a   Fowlkes, Tiffanie ^a   Gross, Shimon ^a   Vinjamoori, Anant ^a,b   Contag, Christopher H ^b   Piwnica Worms, David ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL SIGNIFICANCE; CELL POPULATIONS; DOSE MODULATION; FEEDBACK PROCESS; HEPATOCYTES; IN-VIVO; INNATE IMMUNITY; MODEL SYSTEM; MULTIPLE SCALE; NEGATIVE FEEDBACK LOOP; NUCLEAR FACTORS; PULSE DURATIONS; REPRODUCIBLE BEHAVIOR; SINGLE CELLS; TRANSCRIPTIONAL ACTIVITY;

ANIMALS; BIOLUMINESCENCE; CELL CULTURE; CELL PROLIFERATION; DEGRADATION; DYNAMICS;

CELLS;

I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BIOLUMINESCENCE; CELL HETEROGENEITY; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; LIVER CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE STUDY; REPRODUCIBILITY; TRANSCRIPTION REGULATION;

ANIMALS; GENES, REPORTER; HEP G2 CELLS; HEPATOCYTES; HUMANS; I-KAPPA B PROTEINS; MICE; MODELS, BIOLOGICAL; NF-KAPPA B; TRANSCRIPTION, GENETIC; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA;

EID: 84866085630     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.364018     Document Type: Article

References (44)

1. Cebecauer, M., Spitaler, M., Sergé, A., and Magee, A. I. (2010) Signaling complexes and clusters. Functional advantages and methodological hurdles. J. Cell Sci. 123, 309-320
2. Brandman, O., and Meyer, T. (2008) Feedback loops shape cellular signals in space and time. Science 322, 390-395
3. Alon, U. (2007) Simplicity in biology. Nature 446, 497
4. Lahav, G. (2008) Oscillations by the p53-Mdm2 feedback loop. Adv. Exp. Med. Biol. 641, 28-38
5. Sung, M. H., and McNally, J. G. (2011) Live cell imaging and systems biology. Wiley Interdiscip. Rev. Syst. Biol. Med. 3, 167-182
6. Spiller, D. G., Wood, C. D., Rand, D. A., and White, M. R. (2010) Measurement of single-cell dynamics. Nature 465, 736-745
7. Dothager, R. S., Flentie, K., Moss, B., Pan, M. H., Kesarwala, A., and Piwnica-Worms, D. (2009) Advances in bioluminescence imaging of live animal models. Curr. Opin. Biotechnol. 20, 45-53
8. Prescher, J. A., and Contag, C. H. (2010) Guided by the light. Visualizing biomolecular processes in living animals with bioluminescence. Curr.Opin. Chem. Biol. 14, 80-89
9. Hayden, M. S., West, A. P., and Ghosh, S. (2006) NF-κB and the immune response. Oncogene 25, 6758-6780
10. Pasparakis, M. (2009) Regulation of tissue homeostasis by NF-κB signaling. Implications for inflammatory diseases. Nat. Rev. Immunol. 9, 778-788
11. Perkins, N. D. (2007) Integrating cell-signaling pathways with NF-κB and IKK function. Nat. Rev. Mol. Cell Biol. 8, 49-62
12. Moss, B. L., Gross, S., Gammon, S. T., Vinjamoori, A., and Piwnica-Worms, D. (2008) Identification of a ligand-induced transient refractory period in nuclear factor-κB signaling. J. Biol. Chem. 283, 8687-8698
13. Werner, S. L., Barken, D., and Hoffmann, A. (2005) Stimulus specificity of gene expression programs determined by temporal control of IKK activity. Science 309, 1857-1861
14. Werner, S. L., Kearns, J. D., Zadorozhnaya, V., Lynch, C., O'Dea, E., Boldin, M. P., Ma, A., Baltimore, D., and Hoffmann, A. (2008) Encoding NF-κB temporal control in response to TNF. Distinct roles for the negative regulators IκBα and A20. Genes Dev. 22, 2093-2101
15. Ashall, L., Horton, C. A., Nelson, D. E., Paszek, P., Harper, C. V., Sillitoe, K., Ryan, S., Spiller, D. G., Unitt, J. F., Broomhead, D. S., Kell, D. B., Rand, D. A., Sée, V., and White, M. R. (2009) Pulsatile stimulation determines timing and specificity of NF-κB-dependent transcription. Science 324, 242-246
16. Turner, D. A., Paszek, P., Woodcock, D. J., Nelson, D. E., Horton, C. A., Wang, Y., Spiller, D. G., Rand, D. A., White, M. R., and Harper, C. V. (2010) Physiological levels of TNFα stimulation induce stochastic dynamics of NF-αB responses in single living cells. J. Cell Sci. 123, 2834-2843
17. Tay, S., Hughey, J. J., Lee, T. K., Lipniacki, T., Quake, S. R., and Covert, M. W. (2010) Single-cell NF-κB dynamics reveal digital activation and analogue information processing. Nature 466, 267-271
18. Lee, T. K., Denny, E. M., Sanghvi, J. C., Gaston, J. E., Maynard, N. D., Hughey, J. J., and Covert, M. W. (2009) A noisy paracrine signal determines the cellular NF-κB response to lipopolysaccharide. Sci. Signal. 2, ra65
19. Janes, K. A., Gaudet, S., Albeck, J. G., Nielsen, U. B., Lauffenburger, D. A., and Sorger, P. K. (2006) The response of human epithelial cells to TNF involves an inducible autocrine cascade. Cell 124, 1225-1239
20. David, G. L., Yegnasubramanian, S., Kumar, A., Marchi, V. L., De Marzo, A. M., Lin, X., and Nelson, W. G. (2004) MDR1 promoter hypermethylation in MCF-7 human breast cancer cells. Changes in chromatin structure induced by treatment with 5-aza-cytidine. Cancer Biol. Ther. 3, 540-548
21. Nelson, D. E., Ihekwaba, A. E., Elliott, M., Johnson, J. R., Gibney, C. A., Foreman, B. E., Nelson, G., See, V., Horton, C. A., Spiller, D. G., Edwards, S. W., McDowell, H. P., Unitt, J. F., Sullivan, E., Grimley, R., Benson, N., Broomhead, D., Kell, D. B., and White, M. R. (2004) Oscillations in NF-κB signaling control the dynamics of gene expression. Science 306, 704-708
22. Kearns, J. D., Basak, S., Werner, S. L., Huang, C. S., and Hoffmann, A. (2006) IκBε provides negative feedback to control NF-κB oscillations, signaling dynamics, and inflammatory gene expression. J. Cell Biol. 173, 659-664
23. Sung, M. H., Salvatore, L., De Lorenzi, R., Indrawan, A., Pasparakis, M., Hager, G. L., Bianchi, M. E., and Agresti, A. (2009) Sustained oscillations of NF-κB produce distinct genome scanning and gene expression profiles. PLoS One 4, e7163
24. Tian, B., Nowak, D. E., and Brasier, A. R. (2005) A TNF-induced gene expression program under oscillatory NF-κB control. BMC Genomics 6, 137
25. Friedrichsen, B. N., Neubauer, N., Lee, Y. C., Gram, V. K., Blume, N., Petersen, J. S., Nielsen, J. H., and Møldrup, A. (2006) Stimulation of pancreatic beta-cell replication by incretins involves transcriptional induction of cyclin D1 via multiple signaling pathways. J. Endocrinol. 188, 481-492
26. Gross, S., and Piwnica-Worms, D. (2005) Real time imaging of ligandinduced IKK activation in intact cells and in living mice. Nat. Methods 2, 607-614
27. Hoffmann, A., Levchenko, A., Scott, M. L., and Baltimore, D. (2002) The IκB-NF-κB signaling module. Temporal control and selective gene activation. Science 298, 1241-1245
28. Liu, F., Song, Y., and Liu, D. (1999) Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6, 1258-1266
29. Pichler, A., Zelcer, N., Prior, J. L., Kuil, A. J., and Piwnica-Worms, D. (2005) In vivo RNA interference-mediated ablation of MDR1 P-glycoprotein. Clin. Cancer Res. 11, 4487-4494
30. Paszek, P., Ryan, S., Ashall, L., Sillitoe, K., Harper, C. V., Spiller, D. G., Rand, D. A., and White, M. R. (2010) Population robustness arising from cellular heterogeneity. Proc. Natl. Acad. Sci. U.S.A. 107, 11644-11649
31. Place, R. F., Haspeslagh, D., and Giardina, C. (2003) Induced stabilization of IκBα can facilitate its resynthesis and prevent sequential degradation. J. Cell. Physiol. 195, 470-478
32. Place, R. F., Haspeslagh, D., Hubbard, A. K., and Giardina, C. (2001) Cytokine-induced stabilization of newly synthesized IκBα. Biochem. Biophys. Res. Commun. 283, 813-820
33. Warrington, N. M., Gianino, S. M., Jackson, E., Goldhoff, P., Garbow, J. R., Piwnica-Worms, D., Gutmann, D. H., and Rubin, J. B. (2010) Cyclic AMP suppression is sufficient to induce gliomagenesis in a mouse model of neurofibromatosis-1. Cancer Res. 70, 5717-5727
34. Pichler, A., Prior, J. L., Luker, G. D., and Piwnica-Worms, D. (2008) Generation of a highly inducible Gal43Fluc universal reporter mouse for in vivo bioluminescence imaging. Proc. Natl. Acad. Sci. U.S.A. 105, 15932-15937
35. Villalobos, V., Naik, S., Bruinsma, M., Dothager, R. S., Pan, M. H., Samrakandi, M., Moss, B., Elhammali, A., and Piwnica-Worms, D. (2010) Dualcolor click beetle luciferase heteroprotein fragment complementation assays. Chem. Biol. 17, 1018-1029
36. Harper, C. V., Featherstone, K., Semprini, S., Friedrichsen, S., McNeilly, J., Paszek, P., Spiller, D. G., McNeilly, A. S., Mullins, J. J., Davis, J. R., and White, M. R. (2010) Dynamic organization of prolactin gene expression in living pituitary tissue. J. Cell Sci. 123, 424-430
37. Webb, A. B., Angelo, N., Huettner, J. E., and Herzog, E. D. (2009) Intrinsic, nondeterministic circadian rhythm generation in identified mammalian neurons. Proc. Natl. Acad. Sci. U.S.A. 106, 16493-16498
38. Nelson, G., Paraoan, L., Spiller, D. G., Wilde, G. J., Browne, M. A., Djali, P. K., Unitt, J. F., Sullivan, E., Floettmann, E., and White, M. R. (2002) Multiparameter analysis of the kinetics of NF-κB signaling and transcription in single living cells. J. Cell Sci. 115, 1137-1148
39. Cheong, R., Bergmann, A., Werner, S. L., Regal, J., Hoffmann, A., and Levchenko, A. (2006) Transient IκB kinase activity mediates temporal NF-κB dynamics in response to a wide range of tumor necrosis factor-αdoses. J. Biol. Chem. 281, 2945-2950
40. Kalita, M. K., Sargsyan, K., Tian, B., Paulucci-Holthauzen, A., Najm, H. N., Debusschere, B. J., and Brasier, A. R. (2011) Sources of cell-to-cell variability in canonical nuclear factor-κB (NF-κB) signaling pathway inferred from single cell dynamic images. J. Biol. Chem. 286, 37741-37757
41. Suda, T., and Liu, D. (2007) Hydrodynamic gene delivery. Its principles and applications. Mol. Ther. 15, 2063-2069
42. Shih, V. F., Kearns, J. D., Basak, S., Savinova, O. V., Ghosh, G., and Hoffmann, A. (2009) Kinetic control of negative feedback regulators of NF-κB/RelA determines their pathogen- and cytokine-receptor signaling specificity. Proc. Natl. Acad. Sci. U.S.A. 106, 9619-9624
43. Zandi, E., Chen, Y., and Karin, M. (1998) Direct phosphorylation of IκBby IKKα and IKKβ. Discrimination between free and NF-κB-bound substrate. Science 281, 1360-1363
44. O'Dea, E. L., Barken, D., Peralta, R. Q., Tran, K. T., Werner, S. L., Kearns, J. D., Levchenko, A., and Hoffmann, A. (2007)Ahomeostatic model of IκB metabolism to control constitutive NF-κB activity. Mol. Syst. Biol. 3, 111