Environmental Laboratory, U.S. Army Engineer Research and Development Center, Vicksburg, MS, United States of America.
PLoS One. 2021 Jan 13;16(1):e0245094. doi: 10.1371/journal.pone.0245094. eCollection 2021.
The transcriptional network determines a cell's internal state by regulating protein expression in response to changes in the local environment. Due to the interconnected nature of this network, information encoded in the abundance of various proteins will often propagate across chains of noisy intermediate signaling events. The data-processing inequality (DPI) leads us to expect that this intracellular game of "telephone" should degrade this type of signal, with longer chains losing successively more information to noise. However, a previous modeling effort predicted that because the steps of these signaling cascades do not truly represent independent stages of data processing, the limits of the DPI could seemingly be surpassed, and the amount of transmitted information could actually increase with chain length. What that work did not examine was whether this regime of growing information transmission was attainable by a signaling system constrained by the mechanistic details of more complex protein-binding kinetics. Here we address this knowledge gap through the lens of information theory by examining a model that explicitly accounts for the binding of each transcription factor to DNA. We analyze this model by comparing stochastic simulations of the fully nonlinear kinetics to simulations constrained by the linear response approximations that displayed a regime of growing information. Our simulations show that even when molecular binding is considered, there remains a regime wherein the transmitted information can grow with cascade length, but ends after a critical number of links determined by the kinetic parameter values. This inflection point marks where correlations decay in response to an oversaturation of binding sites, screening informative transcription factor fluctuations from further propagation down the chain where they eventually become indistinguishable from the surrounding levels of noise.
转录网络通过调节蛋白质表达来响应局部环境的变化,从而决定细胞的内部状态。由于该网络的相互关联性质,各种蛋白质丰度中编码的信息通常会在一连串嘈杂的中间信号事件中传播。数据处理不等式(DPI)使我们预计,这种细胞内的“电话”游戏应该会降低这种类型的信号,较长的链会逐渐失去更多的信息噪声。然而,之前的建模工作预测,由于这些信号级联的步骤并不真正代表数据处理的独立阶段,因此 DPI 的限制似乎可以被超越,并且传递的信息量实际上可以随着链长的增加而增加。该工作没有检查的是,在受更复杂的蛋白质结合动力学的机制细节限制的信号系统中,这种信息传输不断增长的机制是否可行。在这里,我们通过信息理论的视角来解决这一知识空白,通过检查一个明确考虑每个转录因子与 DNA 结合的模型。我们通过将完全非线性动力学的随机模拟与显示信息不断增长的线性响应近似的模拟进行比较来分析这个模型。我们的模拟表明,即使考虑分子结合,仍然存在一个传递信息可以随级联长度增长的区域,但在由动力学参数值决定的临界链接数之后结束。这个拐点标志着在结合位点过饱和的情况下相关性的衰减,从而筛选出有意义的转录因子波动,阻止它们进一步向下游传播,最终与周围的噪声水平难以区分。