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Macklin, P.

Publications and source records attributed to Macklin, P..

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PhysiCelldFBA: Linking single-cell genome-scale metabolism to spatially explicit multicellular dynamics

Genome-scale metabolic models can predict how individual cells allocate resources and respond to their environment, yet few frameworks link single-cell metabolism to the spatial organisation of multicellular systems. Here we introduce PhysiCelldFBA, an extension of the PhysiCell agent-based framework that couples genome-scale dynamic flux balance analysis to off-lattice multicellular simulations. Each simulated cell carries its own metabolic model, allowing local environmental conditions to shape metabolism while metabolic activity feeds back on the surrounding environment, cellular behaviour, and spatial organisation. We first validate this coupling by showing that glucose consumption, CO2 production, and biomass accumulation remain mass-balanced in a closed E. coli system, with simulated biomass agreeing with analytical predictions to within 1%. We then demonstrate how metabolic phenotypes emerge from this coupling across microbial and mammalian systems. Spatial nutrient gradients generate metabolic stratification and acetate cross-feeding in growing E. coli colonies; diffusion-limited metabolism produces proliferative, hypoxic, and necrotic zones across a broad panel of metabolites in a tumour-like tissue; distinct, organism-specific metabolic networks give rise to syntrophic cross-feeding and spatial niche formation in a two-species consortium; and metabolic state couples energy availability to transitions between cellular motility and growth. Across these examples, metabolic stratification, cross-feeding, and phenotypic adaptation emerge from local metabolic optimisation and environmental feedback rather than being explicitly prescribed. PhysiCelldFBA therefore provides a general framework for simulating genome-scale metabolism at single-cell resolution and linking intracellular metabolic state to cellular behaviour and emergent organisation across scales.

systems biology

PhysiBoSS: a multi-scale agent based modelling framework integrating physical dimension and cell signalling

Due to the complexity of biological systems, their heterogeneity, and the internal regulation of each cell and its surrounding, mathematical models that take into account cell signalling, cell population behaviour and the extracellular environment are particularly helpful to understand such complex systems. However, very few of these tools, freely available and computationally efficient, are currently available. To fill this gap, we present here our open-source software, PhysiBoSS, which is built on two available software packages that focus on different scales: intracellular signalling using continuous-time markovian Boolean modelling (MaBoSS) and multicellular behaviour using agent-based modelling (PhysiCell).\n\nThe multi-scale feature of PhysiBoSS - its agent-based structure and the possibility to integrate any Boolean network to it - provide a flexible and computationally efficient framework to study heterogeneous cell population growth in diverse experimental set-ups. This tool allows one to explore the effect of environmental and genetic alterations of individual cells at the population level, bridging the critical gap from genotype to phenotype. PhysiBoSS thus becomes very useful when studying population response to treatment, mutations effects, cell modes of invasion or isomorphic morphogenesis events.\n\nTo illustrate potential use of PhysiBoSS, we studied heterogeneous cell fate decisions in response to TNF treatment in a 2-D cell population and in a tumour cell 3-D spheroid. We explored the effect of different treatment regimes and the behaviour and selection of several resistant mutants. We highlighted the importance of spatial information on the population dynamics by considering the effect of competition for resources like oxygen. PhysiBoSS is freely available on GitHub (https://github.com/gletort/PhysiBoSS), and is distributed open source under the BSD 3-clause license. It is compatible with most Unix systems, and a Docker package (https://hub.docker.com/r/gletort/physiboss/) is provided to ease its deployment in other systems.

systems biology

Open source tools and standardized data in cancer systems biology

To reach the full potential of multicellular systems biology, mathematical and computational modelers must pool their efforts to share and curate biophysical measurements, create and combine mathematical models, analyze and visualize model predictions, and validate and refine against shared data. An ecosystem of open source software that reads standardized data is essential. We review the state-of-the-art in open source software and data standards in multicellular systems biology, and point out areas of needed growth to move beyond isolated models to community-driven frameworks that shed light on complex problems in multicellular systems biology.

systems biology

High-throughput cancer hypothesis testing with an integrated PhysiCell-EMEWS workflow

BackgroundCancer is a complex, multiscale dynamical system, with interactions between tumor cells and non-cancerous host systems. Therapies act on this combined cancer-host system, sometimes with unexpected results. Systematic investigation of mechanistic computational models can augment traditional laboratory and clinical studies, helping identify the factors driving a treatments success or failure. However, given the uncertainties regarding the underlying biology, these multiscale computational models can take many potential forms, in addition to encompassing high-dimensional parameter spaces. Therefore, the exploration of these models is computationally challenging. We propose that integrating two existing technologies--one to aid the construction of multiscale agent-based models, the other developed to enhance model exploration and optimization--can provide a computational means for high-throughput hypothesis testing, and eventually, optimization.\n\nResultsIn this paper, we introduce a high throughput computing (HTC) framework that integrates a mechanistic 3-D multicellular simulator (PhysiCell) with an extreme-scale model exploration platform (EMEWS) to investigate high-dimensional parameter spaces. We show early results in applying PhysiCell-EMEWS to 3-D cancer immunotherapy and show insights on therapeutic failure. We describe a generalized PhysiCell-EMEWS workflow for high-throughput cancer hypothesis testing, where hundreds or thousands of mechanistic simulations are compared against data-driven error metrics to perform hypothesis optimization.\n\nConclusionsWhile key notational and computational challenges remain, mechanistic agent-based models and high-throughput model exploration environments can be combined to systematically and rapidly explore key problems in cancer. These high-throughput computational experiments can improve our understanding of the underlying biology, drive future experiments, and ultimately inform clinical practice.

systems biology

Computational investigation of biological and technical variability in high throughput phenotyping and cell line identification

High-throughput cell profiling experiments are characterizing cell phenotype under a broad variety of microenvironmental and therapeutic conditions. However, biological and technical variability are contributing to wide ranges of reported parameter values, even for standard cell lines grown in identical conditions. In this paper, we develop a mathematical model of cell proliferation assays that account for biological and technical variability and limitations of the experimental platforms, including (1) cell confluency effects, (2) biological variability and technical errors in pipetting, (3) biological variability in proliferation characteristics, (4) technical variability and uncertainty in measurement timing, (5) cell counting errors, and (6) the impact of limited temporal sampling. We use this model to create synthetic datasets with growth rates and measurement times typical of cancer cell cultures, and investigate the impact of the initial cell seeding density and the common practice of fitting exponential growth curves to three cell count measurements. We find that the combined sources of variability mask the sub-exponential growth characteristics of the synthetic datasets, and that researchers profiling the same cell lines under different seeding characteristics can find significant (p < 0.05) differences in the measured growth rates. Even seeding the cells at 1% of the confluent limit can cause significant (p < 0.05) differences in the measured growth rate from the ground truth. We explored the effect of reducing errors in each part of the virtual experimental system, and found the best improvements from reducing timing errors, reducing cell counting errors, or reducing the interval between measurements (to reduce the inaccuracy of the exponential growth assumption when fitting curves). Reducing biological variability and pipetting errors had the least impact, because any improvements are still masked by cell counting errors. We close with a discussion of recommended practices for high-throughput cell phenotyping and cell line identification systems.

cell biology

Quantification of Cancer Cell Migration with an Integrated Experimental-Computational Pipeline

We describe an integrated experimental-computational pipeline for quantifying cell migration in vitro. This pipeline is robust to image noise, open source, and user friendly. The experimental component uses the Oris cell migration assay (Platypus Technologies) to create migration regions. The computational component of the pipeline creates masks in Matlab (MathWorks) to cell-covered regions, uses a genetic algorithm to automatically select the migration region, and outputs a metric to quantify the migration of cells. In this work we demonstrate the utility of our pipeline by quantifying the effects of a drug (Taxol) and of the secreted Anterior Gradient 2 (sAGR2) protein in the migration of MDA-MB-231 cells (a breast cancer cell line). In particular, we show that blocking sAGR2 reduces migration of MDA-MB-231 cells.

bioinformatics

MultiCellDS: a standard and a community for sharing multicellular data

Cell biology is increasingly focused on cellular heterogeneity and multicellular systems. To make the fullest use of experimental, clinical, and computational efforts, we need standardized data formats, community-curated \"public data libraries\", and tools to combine and analyze shared data. To address these needs, our multidisciplinary community created MultiCellDS (MultiCellular Data Standard): an extensible standard, a library of digital cell lines and tissue snapshots, and support software. With the help of experimentalists, clinicians, modelers, and data and library scientists, we can grow this seed into a community-owned ecosystem of shared data and tools, to the benefit of basic science, engineering, and human health.

systems biology

MultiCellDS: a community-developed standard for curating microenvironment-dependent multicellular data

Exchanging and understanding scientific data and their context represents a significant barrier to advancing research, especially with respect to information siloing. Maintaining information provenance and providing data curation and quality control help overcome common concerns and barriers to the effective sharing of scientific data. To address these problems in and the unique challenges of multicellular systems, we assembled a panel composed of investigators from several disciplines to create the MultiCellular Data Standard (MultiCellDS) with a use-case driven development process. The standard includes (1) digital cell lines, which are analogous to traditional biological cell lines, to record metadata, cellular microenvironment, and cellular phenotype variables of a biological cell line, (2) digital snapshots to consistently record simulation, experimental, and clinical data for multicellular systems, and (3) collections that can logically group digital cell lines and snapshots. We have created a MultiCellular DataBase (MultiCellDB) to store digital snapshots and the 200+ digital cell lines we have generated. MultiCellDS, by having a fixed standard, enables discoverability, extensibility, maintainability, searchability, and sustainability of data, creating biological applicability and clinical utility that permits us to identify upcoming challenges to uplift biology and strategies and therapies for improving human health.

systems biology

PhysiCell: an Open Source Physics-Based Cell Simulator for 3-D Multicellular Systems

Many multicellular systems problems can only be understood by studying how cells move, grow, divide, interact, and die. Tissue-scale dynamics emerge from systems of many interacting cells as they respond to and influence their microenvironment. The ideal \"virtual laboratory\" for such multicellular systems simulates both the biochemical microenvironment (the \"stage\") and many mechanically and biochemically interacting cells (the \"players\" upon the stage).\n\nPhysiCell--physics-based multicellular simulator--is an open source agent-based simulator that provides both the stage and the players for studying many interacting cells in dynamic tissue microenvironments. It builds upon a multi-substrate biotransport solver to link cell phenotype to multiple diffusing substrates and signaling factors. It includes biologically-driven sub-models for cell cycling, apoptosis, necrosis, solid and fluid volume changes, mechanics, and motility \"out of the box.\" The C++ code has minimal dependencies, making it simple to maintain and deploy across platforms. PhysiCell has been parallelized with OpenMP, and its performance scales linearly with the number of cells. Simulations up to 105-106 cells are feasible on quad-core desktop workstations; larger simulations are attainable on single HPC compute nodes.\n\nWe demonstrate PhysiCell by simulating the impact of necrotic core biomechanics, 3-D geometry, and stochasticity on the dynamics of hanging drop tumor spheroids and ductal carcinoma in situ (DCIS) of the breast. We demonstrate stochastic motility, chemical and contact-based interaction of multiple cell types, and the extensibility of PhysiCell with examples in synthetic multicellular systems (a \"cellular cargo delivery\" system, with application to anti-cancer treatments), cancer heterogeneity, and cancer immunology. PhysiCell is a powerful multicellular systems simulator that will be continually improved with new capabilities and performance improvements. It also represents a significant independent code base for replicating results from other simulation platforms. The PhysiCell source code, examples, documentation, and support are available under the BSD license at http://PhysiCell.MathCancer.org and http://PhysiCell.sf.net.\n\nAuthor SummaryThis paper introduces PhysiCell: an open source, agent-based modeling framework for 3-D multicellular simulations. It includes a standard library of sub-models for cell fluid and solid volume changes, cycle progression, apoptosis, necrosis, mechanics, and motility. PhysiCell is directly coupled to a biotransport solver to simulate many diffusing substrates and cell-secreted signals. Each cell can dynamically update its phenotype based on its microenvironmental conditions. Users can customize or replace the included sub-models.\n\nPhysiCell runs on a variety of platforms (Linux, OSX, and Windows) with few software dependencies. Its computational cost scales linearly in the number of cells. It is feasible to simulate 500,000 cells on quad-core desktop workstations, and millions of cells on single HPC compute nodes. We demonstrate PhysiCell by simulating the impact of necrotic core biomechanics, 3-D geometry, and stochasticity on hanging drop tumor spheroids (HDS) and ductal carcinoma in situ (DCIS) of the breast. We demonstrate contact- and chemokine-based interactions among multiple cell types with examples in synthetic multicellular bioengineering, cancer heterogeneity, and cancer immunology.\n\nWe developed PhysiCell to help the scientific community tackle multicellular systems biology problems involving many interacting cells in multi-substrate microenvironments. PhysiCell is also an independent, cross-platform codebase for replicating results from other simulators.

systems biology