Browning Alexander P, Crossley Rebecca M, Villa Chiara, Maini Philip K, Jenner Adrianne L, Cassidy Tyler, Hamis Sara
School of Mathematics and Statistics, University of Melbourne, Melbourne, Victoria, Australia.
Mathematical Institute, University of Oxford, Oxford, United Kingdom.
PLoS Comput Biol. 2025 Jun 24;21(6):e1013202. doi: 10.1371/journal.pcbi.1013202. eCollection 2025 Jun.
Phenotypic plasticity contributes significantly to treatment failure in many cancers. Despite the increased prevalence of experimental studies that interrogate this phenomenon, there remains a lack of applicable quantitative tools to characterise data, and importantly to distinguish between resistance as a discrete phenotype and a continuous distribution of phenotypes. To address this, we develop a stochastic individual-based model of plastic phenotype adaptation through a continuously-structured phenotype space in low-cell-count proliferation assays. That our model corresponds probabilistically to common partial differential equation models of resistance allows us to formulate a likelihood that captures the intrinsic noise ubiquitous to such experiments. We apply our framework to assess the identifiability of key model parameters in several population-level data collection regimes; in particular, parameters relating to the adaptation velocity and cell-to-cell heterogeneity. Significantly, we find that cell-to-cell heterogeneity is practically non-identifiable from both cell count and proliferation marker data, implying that population-level behaviours may be well characterised by homogeneous ordinary differential equation models. Additionally, we demonstrate that population-level data are insufficient to distinguish resistance as a discrete phenotype from a continuous distribution of phenotypes. Our results inform the design of both future experiments and future quantitative analyses that probe phenotypic plasticity in cancer.
表型可塑性在许多癌症的治疗失败中起着重要作用。尽管探究这一现象的实验研究越来越普遍,但仍然缺乏适用的定量工具来表征数据,更重要的是,无法区分作为离散表型的耐药性和连续的表型分布。为了解决这个问题,我们在低细胞计数增殖试验中,通过连续结构的表型空间,开发了一个基于个体的可塑性表型适应随机模型。我们的模型在概率上与常见的耐药性偏微分方程模型相对应,这使我们能够构建一个似然函数,以捕捉此类实验中普遍存在的内在噪声。我们应用我们的框架来评估在几种群体水平数据收集方式下关键模型参数的可识别性;特别是与适应速度和细胞间异质性相关的参数。值得注意的是,我们发现从细胞计数和增殖标记数据中实际上无法识别细胞间异质性,这意味着群体水平的行为可能可以用齐次常微分方程模型很好地描述。此外,我们证明群体水平的数据不足以区分作为离散表型的耐药性和连续的表型分布。我们的结果为未来探究癌症表型可塑性的实验设计和定量分析提供了参考。