Hierarchical cooperativity mediated by chromatin remodeling; the model of the MMTV transcription regulation. (English) Zbl 1397.92214
Summary: Chromatin remodeling machineries are abundant and diverse in eukaryotic cells but their importance in gene expression remains unclear. Although the influence of nucleosome position on the regulation of gene expression is generally envisioned under the equilibrium perspective, it is proposed that given the ATP-dependence of chromatin remodeling enzymes, certain mechanisms necessitate non-equilibrium treatments. In particular, examination of the celebrated chromatin remodeling system of the mouse mammary tumor virus, in which the binding of transcription factors opens the way to other ones, reveals that breaking equilibrium offers a subtle mode of transcription factor cooperativity, avoids molecular trapping phenomena and allows to reconcile previously conflicting experimental data. The mechanism proposed here provides a control lever of promoter sensitivity and responsiveness, increasing the discernment of gene expression.
MSC:
| 92C40 | Biochemistry, molecular biology |
| 92C45 | Kinetics in biochemical problems (pharmacokinetics, enzyme kinetics, etc.) |
References:
| [1] | Archer, T.K.; Lefebvre, P.; Wolford, R.G.; Hager, G.L., Transcription factor loading on the MMTV promoter: a bimodal mechanism for promoter activation, Science, 255, 1573-1576, (1992) |
| [2] | Belikov, S.; Gelius, B.; Wrange, O., Hormone-induced nucleosome positioning in the MMTV promoter is reversible, Embo j., 20, 2802-2811, (2001) |
| [3] | Belikov, S.; Holmqvist, P.H.; Astrand, C.; Wrange, O., Nuclear factor 1 and octamer transcription factor 1 binding preset the chromatin structure of the mouse mammary tumor virus promoter for hormone induction, J. biol. chem, 279, 49857-49867, (2004) |
| [4] | Bendall, H.H.; Schrerer, D.C.; Edson, C.R.; Ballard, D.W.; Oltz, E.M., Transcription factor NF-kb regulates inducible oct-2 gene expression in precursor B lymphocytes, J. biol. chem., 272, 28826-28828, (1997) |
| [5] | Bintu, L.; Buchler, N.E.; Garcia, H.G.; Gerland, U.; Hwa, T.; Kondev, J.; Phillips, R., Transcriptional regulation by the numbers: models, Curr. opin. genet. dev., 15, 116-124, (2005) |
| [6] | Bolouri, H.; Davidson, E.H., Modeling DNA sequence-based cis-regulatory gene networks, Dev. biol., 246, 2-13, (2002) |
| [7] | Cha, S., A simple method for derivation of rate equations for enzyme-catalyzed reactions under the rapid equilibrium assumption or combined assumptions of equilibrium and steady state, J. biol. chem., 243, 820-825, (1968) |
| [8] | Chávez, S.; Beato, M., Nucleosome-mediated synergism between transcription factors on the mouse mammary tumor virus promoter, Proc. natl. acad. sci. USA, 94, 2885-2890, (1997) |
| [9] | Cherry, J.L.; Adler, F.R., How to make a biological switch, J. theor. biol., 203, 117-133, (2000) |
| [10] | Chu, D.; Zabet, N.R.; Mitavskiy, B., Models of transcription factor binding: sensitivity of activation functions to model assumptions, J. theor. biol., 257, 419-429, (2009) · Zbl 1400.92182 |
| [11] | Cornish-Bowden, A.; Koshland, D.E.J., Diagnostic uses of the Hill (logit and Nernst) plots, J. mol. biol., 25, 201-212, (1975) |
| [12] | Dahlquist, F.W., The meaning of scatchard and Hill plots, Methods enzymol., 48, 270-299, (1978) |
| [13] | Dodd, I.B.; Micheelsen, M.A.; Sneppen, K.; Thon, G., Theoretical analysis of epigenetic cell memory by nucleosome modification, Cell, 129, 813-822, (2007) |
| [14] | Eisfeld, K.; Candau, R.; Truss, M.; Beato, M., Binding of NF1 to the MMTV promoter in nucleosomes: influence of rotational phasing, translational positioning and histone H1, Nucl. acids res., 25, 3733-3742, (1997) |
| [15] | Fletcher, T.M.; Ryu, B.W.; Baumann, C.T.; Warren, B.S.; Fragoso, G.; John, S.; Hager, G.L., Structure and dynamic properties of a glucocorticoid receptor-induced chromatin transition, Mol. cell. biol., 20, 6466-6475, (2000) |
| [16] | Fryer, C.J.; Archer, T.K., Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex, Nature, 393, 88-91, (1998) |
| [17] | Hager, G.L.; Fletcher, T.M.; Xiao, N.; Baumann, C.T.; Muller, W.G.; McNally, J.G., Dynamics of gene targeting and chromatin remodelling by nuclear receptors, Biochem. soc. trans., 28, 405-410, (2000) |
| [18] | Hebbar, P.B.; Archer, T.K., Nuclear factor 1 is required for both hormone-dependent chromatin remodeling and transcriptional activation of the mouse mammary tumor virus promoter, Mol. cell. biol., 23, 887-898, (2003) |
| [19] | Hebbar, P.B.; Archer, T.K., Chromatin-dependent cooperativity between site-specific transcription factors in vivo, J. biol. chem., 282, 8284-8291, (2007) |
| [20] | Johnson, T.A.; Elbi, C.; Parekh, B.S.; Hager, G.L.; John, S., Chromatin remodeling complexes interact dynamically with a glucocorticoid receptor-regulated promoter, Mol. biol. cell, 19, 3308-3322, (2008) |
| [21] | Lacal, J.; Guazzaroni, M.E.; Busch, A.; Krell, T.; Ramos, J.L., Hierarchical binding of the todt response regulator to its multiple recognition sites at the tod pathway operon promoter, J. mol. biol., 376, 325-337, (2008) |
| [22] | Mackay, J.P.; Sunde, M.; Lowry, J.A.; Crossley, M.; Matthews, J.M., Protein interactions: is seeing believing?, Trends biochem. sci, 32, 530-531, (2007) |
| [23] | Michel, D., How transcription factors can adjust the gene expression floodgates, Prog. biophys. mol. biol., 32, 16-37, (2010) |
| [24] | Mirny, L.A., Nucleosome-mediated cooperativity between transcription factors, Proc. natl. acad. sci. USA, 107, 22534-22539, (2010) |
| [25] | Pina, B.; Barettino, D.; Truss, M.; Beato, M., Structural features of a regulatory nucleosome, J. mol. biol., 216, 975-990, (1990) |
| [26] | Rhee, J.M.; Trieu, M.; Turner, E.E., Optimal oct-2 affinity for an extended DNA site and the effect of GST fusion on site preference, Arch. biochem. biophys., 385, 397-405, (2001) |
| [27] | Richard-Foy, H.; Hager, G.L., Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter, Embo j., 6, 2321-2328, (1987) |
| [28] | Rippe, K.; Schrader, A.; Riede, P.; Strohner, R.; Lehmann, E.; Längst, G., DNA sequence- and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes, Proc. natl. acad. sci. USA, 104, 15635-15640, (2007) |
| [29] | Segal, E.; Widom, J., From. DNA sequence to transcriptional behaviour: a quantitative approach, Nat. rev. genet., 10, 443-456, (2009) |
| [30] | Smith, C.L.; Htun, H.; Wolford, R.G.; Hager, G.L., Differential activity of progesterone and glucocorticoid receptors on mouse mammary tumor virus templates differing in chromatin structure, J. biol. chem., 272, 14227-14235, (1997) |
| [31] | Sprague, B.L.; Pego, R.L.; Stavreva, D.A.; McNally, J.G., Analysis of binding reactions by fluorescence recovery after photobleaching, Biophys. J., 86, 3473-3495, (2004) |
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.
