Jagiella Nick, Müller Benedikt, Müller Margareta, Vignon-Clementel Irene E, Drasdo Dirk
Institute for Computational Biology, Helmholtz Zentrum München, Neuherberg, Germany.
INRIA Paris, Centre de recherche Inria de Paris, Paris, France.
PLoS Comput Biol. 2016 Feb 11;12(2):e1004412. doi: 10.1371/journal.pcbi.1004412. eCollection 2016 Feb.
We develop a quantitative single cell-based mathematical model for multi-cellular tumor spheroids (MCTS) of SK-MES-1 cells, a non-small cell lung cancer (NSCLC) cell line, growing under various nutrient conditions: we confront the simulations performed with this model with data on the growth kinetics and spatial labeling patterns for cell proliferation, extracellular matrix (ECM), cell distribution and cell death. We start with a simple model capturing part of the experimental observations. We then show, by performing a sensitivity analysis at each development stage of the model that its complexity needs to be stepwise increased to account for further experimental growth conditions. We thus ultimately arrive at a model that mimics the MCTS growth under multiple conditions to a great extent. Interestingly, the final model, is a minimal model capable of explaining all data simultaneously in the sense, that the number of mechanisms it contains is sufficient to explain the data and missing out any of its mechanisms did not permit fit between all data and the model within physiological parameter ranges. Nevertheless, compared to earlier models it is quite complex i.e., it includes a wide range of mechanisms discussed in biological literature. In this model, the cells lacking oxygen switch from aerobe to anaerobe glycolysis and produce lactate. Too high concentrations of lactate or too low concentrations of ATP promote cell death. Only if the extracellular matrix density overcomes a certain threshold, cells are able to enter the cell cycle. Dying cells produce a diffusive growth inhibitor. Missing out the spatial information would not permit to infer the mechanisms at work. Our findings suggest that this iterative data integration together with intermediate model sensitivity analysis at each model development stage, provide a promising strategy to infer predictive yet minimal (in the above sense) quantitative models of tumor growth, as prospectively of other tissue organization processes. Importantly, calibrating the model with two nutriment-rich growth conditions, the outcome for two nutriment-poor growth conditions could be predicted. As the final model is however quite complex, incorporating many mechanisms, space, time, and stochastic processes, parameter identification is a challenge. This calls for more efficient strategies of imaging and image analysis, as well as of parameter identification in stochastic agent-based simulations.
我们针对非小细胞肺癌(NSCLC)细胞系SK-MES-1细胞在多种营养条件下生长形成的多细胞肿瘤球体(MCTS),开发了一种基于单细胞的定量数学模型:我们将该模型的模拟结果与细胞增殖、细胞外基质(ECM)、细胞分布和细胞死亡的生长动力学及空间标记模式数据进行对比。我们从一个能捕捉部分实验观察结果的简单模型开始。然后,通过在模型的每个开发阶段进行敏感性分析,我们表明需要逐步增加模型的复杂性,以考虑更多的实验生长条件。最终,我们得到了一个在很大程度上模拟多种条件下MCTS生长的模型。有趣的是,最终模型是一个最小模型,能够在某种意义上同时解释所有数据,即它所包含的机制数量足以解释数据,并且在生理参数范围内遗漏任何一个机制都无法使所有数据与模型拟合。然而,与早期模型相比,它相当复杂,即它包含了生物学文献中讨论的广泛机制。在这个模型中,缺氧的细胞从有氧糖酵解转变为无氧糖酵解并产生乳酸。过高的乳酸浓度或过低的ATP浓度会促进细胞死亡。只有当细胞外基质密度超过一定阈值时,细胞才能进入细胞周期。死亡细胞会产生一种扩散性生长抑制剂。遗漏空间信息将无法推断起作用的机制。我们的研究结果表明,这种迭代数据整合以及在每个模型开发阶段进行中间模型敏感性分析,为推断肿瘤生长的预测性且最小(上述意义上)定量模型提供了一种有前景的策略,对于其他组织构建过程也是如此。重要的是,用两种营养丰富的生长条件校准模型后,可以预测两种营养匮乏生长条件下的结果。然而,由于最终模型相当复杂,包含许多机制、空间、时间和随机过程,参数识别是一个挑战。这就需要更有效的成像和图像分析策略,以及基于随机代理模拟的参数识别策略。