Direct observation of a transient ternary complex during IκBα-mediated dissociation of NF-κB from DNA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 1, 2014, Pages 225-230

  Alverdi, Vera ^a   Hetrick, Byron ^b   Joseph, Simpson ^a   Komives, Elizabeth A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF OREGON   (United States)

Author keywords

DNA binding; NF B post induction repression; NF B transcription; Stopped flow fluorescence kinetics; Transcription activation

Indexed keywords

DNA; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PYRENE; TRYPTOPHAN;

ARTICLE; CONTROLLED STUDY; DNA BINDING; DNA PROTEIN COMPLEX; DNA TRANSCRIPTION; FLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS;

DNA BINDING; NF-ΚB POST-INDUCTION REPRESSION; NF-ΚB TRANSCRIPTION; STOPPED-FLOW FLUORESCENCE KINETICS; TRANSCRIPTION ACTIVATION;

CELL NUCLEUS; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUORESCENT DYES; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B PROTEINS; KINETICS; MICROSCOPY, FLUORESCENCE; MUTATION; NF-KAPPA B P50 SUBUNIT; PROTEIN BINDING; PROTEIN CONFORMATION; PYRENES; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRYPTOPHAN;

EID: 84891955366     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1318115111     Document Type: Article

References (40)

1. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132(3): 344-362.
2. Ghosh S, May MJ, Kopp EB (1998) NF-kappa B and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu Rev Immunol 16: 225-260.
3. Martone R, et al. (2003) Distribution of NF-kappaB-binding sites across human chromosome 22. Proc Natl Acad Sci USA 100(21): 12247-12252.
4. Hoffmann A, Natoli G, Ghosh G (2006) Transcriptional regulation via the NF-kappaB signaling module. Oncogene 25(51): 6706-6716.
5. Schreiber J, et al. (2006) Coordinated binding of NF-kappaB family members in the response of human cells to lipopolysaccharide. Proc Natl Acad Sci USA 103(15): 5899-5904.
6. Baldwin AS, Jr. (2001) Series introduction: The transcription factor NF-kappaB and human disease. J Clin Invest 107(1): 3-6.
7. Kumar A, Takada Y, Boriek AM, Aggarwal BB (2004) Nuclear factor-kappaB: Its role in health and disease. J Mol Med (Berl) 82(7): 434-448.
8. Lee CH, Jeon YT, Kim SH, Song YS (2007) NF-kappaB as a potential molecular target for cancer therapy. Biofactors 29(1): 19-35.
9. Sen R, Baltimore D (1986) Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell 47(6): 921-928.
10. Chen FE, Huang DB, Chen YQ, Ghosh G (1998) Crystal structure of p50/p65 heterodimer of transcription factor NF-kappaB bound to DNA. Nature 391(6665): 410-413.
11. Huxford T, Huang DB, Malek S, Ghosh G (1998) The crystal structure of the Ikappa- Balpha/NF-kappaB complex reveals mechanisms of NF-kappaB inactivation. Cell 95(6): 759-770.
12. Jacobs MD, Harrison SC (1998) Structure of an IkappaBalpha/NF-kappaB complex. Cell 95(6): 749-758.
13. Baeuerle PA, Baltimore D (1996) NF-kappa B: Ten years after. Cell 87(1): 13-20.
14. Hoffmann A, Levchenko A, Scott ML, Baltimore D (2002) The IkappaB-NF-kappaB signaling module: Temporal control and selective gene activation. Science 298(5596): 1241-1245.
15. O'Dea EL, et al. (2007) A homeostatic model of IkappaB metabolism to control constitutive NF-kappaB activity. Mol Syst Biol 3:111.
16. Bergqvist S, et al. (2006) Thermodynamics reveal that helix four in the NLS of NFkappaB p65 anchors IkappaBalpha, forming a very stable complex. J Mol Biol 360(2): 421-434.
17. Traenckner EB, et al. (1995) Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J 14(12): 2876-2883.
18. Traenckner EB, Baeuerle PA (1995) Appearance of apparently ubiquitin-conjugated I kappa B-alpha during its phosphorylation-induced degradation in intact cells. J Cell Sci Suppl 19: 79-84.
19. Pahl HL (1999) Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18(49): 6853-6866.
20. Chen ZJ, Parent L, Maniatis T (1996) Site-specific phosphorylation of IkappaBalpha by a novel ubiquitination-dependent protein kinase activity. Cell 84(6): 853-862.
21. ScottML, Fujita T, Liou HC, Nolan GP, Baltimore D (1993) The p65 subunit of NF-kappa B regulates I kappa B by two distinct mechanisms. Genes Dev 7(7A): 1266-1276.
22. Sun SC, Ganchi PA, Ballard DW, Greene WC (1993) NF-kappa B controls expression of inhibitor I kappa B alpha: Evidence for an inducible autoregulatory pathway. Science 259(5103): 1912-1915.
23. de Martin R, et al. (1993) Cytokine-inducible expression in endothelial cells of an I kappa B alpha-like gene is regulated by NF kappa B. EMBO J 12(7): 2773-2779.
24. Bergqvist S, et al. (2009) Kinetic enhancement of NF-kappaB-DNA dissociation by IkappaBalpha. Proc Natl Acad Sci USA 106(46): 19328-19333.
25. Sue SC, Alverdi V, Komives EA, Dyson HJ (2011) Detection of a ternary complex of NFkappaB and IkappaBalpha with DNA provides insights into how IkappaBalpha removes NF-kappaB from transcription sites. Proc Natl Acad Sci USA 108(4): 1367-1372.
26. Ferreiro DU, et al. (2007) Stabilizing IkappaBalpha by "consensus" design. J Mol Biol 365(4): 1201-1216.
27. Hoffmann A, Leung TH, Baltimore D (2003) Genetic analysis of NF-kappaB/Rel transcription factors defines functional specificities. EMBO J 22(20): 5530-5539.
28. Ferreiro DU, de Prat-Gay G (2003) A protein-DNA binding mechanism proceeds through multi-state or two-state parallel pathways. J Mol Biol 331(1): 89-99.
29. Ferreiro DU, Sánchez IE, de Prat Gay G (2008) Transition state for protein-DNA recognition. Proc Natl Acad Sci USA 105(31): 10797-10802.
30. Truhlar SME, Torpey JW, Komives EA (2006) Regions of IkappaBalpha that are critical for its inhibition of NF-kappaB.DNA interaction fold upon binding to NF-kappaB.. Proc Natl Acad Sci USA 103: 18951-18956.
31. Bosisio D, et al. (2006) A hyper-dynamic equilibrium between promoter-bound and nucleoplasmic dimers controls NF-kappaB-dependent gene activity. EMBO J 25(4): 798-810.
32. Turner DA, et al. (2010) Physiological levels of TNFalpha stimulation induce stochastic dynamics of NF-kappaB responses in single living cells. J Cell Sci 123(Pt 16): 2834-2843.
33. Riggs AD, Newby RF, Bourgeois S (1970) lac repressor-operator interaction. II. Effect of galactosides and other ligands. J Mol Biol 51(2): 303-314.
34. Liou HC, Baltimore D (1993) Regulation of the NF-kappa B/rel transcription factor and I kappa B inhibitor system. Curr Opin Cell Biol 5(3): 477-487.
35. Lewis M (2005) The lac repressor. C R Biol 328(6): 521-548.
36. Huang TT, Kudo N, Yoshida M, Miyamoto S (2000) A nuclear export signal in the Nterminal regulatory domain of IkappaBalpha controls cytoplasmic localization of inactive NF-kappaB/IkappaBalpha complexes. Proc Natl Acad Sci USA 97(3): 1014-1019.
37. Kalita MK, et al. (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(43): 37741-37757.
38. Croy CH, Bergqvist S, Huxford T, Ghosh G, Komives EA (2004) Biophysical characterization of the free IkappaBalpha ankyrin repeat domain in solution. Protein Sci 13(7): 1767-1777.
39. Sue SC, Cervantes C, Komives EA, Dyson HJ (2008) Transfer of flexibility between ankyrin repeats in IkappaB* upon formation of the NF-kappaB complex. J Mol Biol 380(5): 917-931.
40. Studer SM, Joseph S (2007) Binding of mRNA to the bacterial translation initiation complex. Methods Enzymol 430: 31-44.