Systems biology of cancer: entropy, disorder, and selection-driven evolution to independence, invasion and “swarm intelligence”

Tarabichi, Maxime; Antoniou, Aline; Saiselet, Manuel; Pita, Jaime Miguel Gomes; Andry, Guy; Dumont, Jacques Emile; Detours, Vincent; Maenhaut, Carine

doi:10.1007/s10555-013-9431-y

Cited by 46 publications

(47 citation statements)

References 248 publications

(292 reference statements)

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“…The cancer problem has been considered from many different modeling perspectives ranging from the standard mechanistic models [21][22][23][24][25], to applications of population dynamics [26][27][28][29], evolutionary game theory [30][31][32], and models of swarm dynamics [33,34]. However, these methods generally only consider one or two levels of organization in describing the dynamics of the systems they consider, and almost exclusively view the lowest level as giving rise to the higher levels.…”

Section: Information In Biological Systemsmentioning

confidence: 99%

Cancer as a disorder of patterning information: computational and biophysical perspectives on the cancer problem

Moore

Walker

Levin

2017

Converg. Sci. Phys. Oncol.

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TOPICAL REVIEWCancer as a disorder of patterning information: computational and biophysical perspectives on the cancer problem IntroductionCancer is well-recognized not only as an extremely pernicious medical problem, but also as a group of phenomena deeply connected to the fundamental questions of evolution, multicellularity, pattern (disregulation, and the interplay between the genome and the environment [1,2]. Two fundamental paradigms currently divide the field. One is that cancer results from disorders of genetics: cancer cells are fundamentally broken due to genomic mutation or instability, and their clonal progeny form tumors and metastases. This view is sometimes called the SMT, somatic mutation theory [3][4][5]. A competing perspective is that of cancer as a circuit disease-a disorder of the complex biophysical, transcriptional, and epigenetic dynamics that regulate cellular state and the ability of cells to cooperate in vivo [6][7][8]. Under this view (sometimes called the tissue organization field theory or TOFT, [9,10]), cancer is akin to a traffic jam [11]-the problem is not a permanent discrete alteration within a founder cell and all of its clonal descendants, but an undesirable stable attractor in the complex network of controls that normally guides anatomical homeostasis [12].The relative merits of the two models have been discussed extensively [10,[13][14][15][16][17] AbstractThe current paradigm views cancer as arising clonally from a degradation of genetic information in single cells. A complementary perspective, originating at the dawn of modern developmental biology, is that cancer is the result of a system disorder of algorithms that normally orchestrate individual cell activities toward specific anatomical structures and away from tumorigenesis. A view of cancer as a disease of geometry focuses on the pathways that allow cells to cooperate to build and maintain large-scale anatomical patterning. Cancer may result when cells stop maintaining higher-order structures and reduce the boundary of their computational selves to a single-cell level, reverting to a unicellular lifestyle in which the rest of the organism is merely part of the environment at the expense of which all living things survive. While this view has been widely discussed, little progress has been made in providing a quantitative, mechanistic framework within which this perspective's specific and unique implications for treatment strategies can be tested and biomedically exploited. Here, we highlight two recent areas of progress which may facilitate much-needed progress on the cancer problem. First, we review the roles that endogenous bioelectrical networks, operating across many tissues in vivo, play as a medium of information processing in tumor suppression, progression, and reprogramming. Second, we provide a primer to the development of computational theory and tools for quantifying the information and causal control structures in cancer and other complex biological systems. Rigorous mathematical formalisms now exist to...

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Section: Information In Biological Systemsmentioning

confidence: 99%

Cancer as a disorder of patterning information: computational and biophysical perspectives on the cancer problem

Moore

Walker

Levin

2017

Converg. Sci. Phys. Oncol.

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“…The models also predict an asymmetric migration of cells by the budding and the splitting-off of small populations of cells from the primary tumor. The migration of small groups of cells from the primary tumor is termed collective invasion, and has been observed both in vivo and in vitro (12)(13)(14)(15)(16)(17)(18).…”

Section: Introductionmentioning

confidence: 99%

A paper-based invasion assay: Assessing chemotaxis of cancer cells in gradients of oxygen

et al. 2015

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This work describes a 3D, paper-based assay that can isolate subpopulations of cells based on their invasiveness (i.e., distance migrated in a hydrogel) in a gradient of concentration of oxygen (O 2 ). Layers of paper impregnated with a cell-compatible hydrogel are stacked and placed in a plastic holder to form the invasion assay. Stacking the layers of paper assembles them into 3D tissue-like constructs of defined thickness and composition. The plastic holder ensures the layers of paper are in conformal contact; this geometry allows the cells to migrate between adjacent layers through the embedded hydrogel. In most assays, the stack comprises a single layer of paper containing mammalian cells suspended in a hydrogel, sandwiched between multiple layers of paper containing only hydrogel (into which the cells migrate). Cells in the stack consume and produce small molecules; these molecules diffuse throughout the stack to generate gradients both in the stack, and between the stack and the bulk culture medium. Placing the cell-containing layer in different positions of the stack, or modifying the permeability of the holder to oxygen or proteins, alters the profile of the gradients within the stack. Physically separating the layers after culture isolates subpopulations of cells that migrated different distances, and enables their subsequent analysis or culture. Using this system, three independent cell lines derived from A549 cancer cells are shown to produce distinguishable migration behavior in a gradient of oxygen. This result is the first experimental demonstration that oxygen acts as a chemoattractant for cancer cells. Page 3 of 35 Significance StatementThe invasion of cancerous cells from a tumor into surrounding tissues is one contribution to metastasis-a major contributor to death for patients with cancer. There is a strong link between the directed invasion of cancer cells and the gradients of molecules formed in the microenvironment of the tumor. Using a paper-based invasion assay, this work demonstrates that oxygen-a nutrient known to induce significant behavioral changes to cells within a tumor in a concentration-dependent manner-can also act as a chemoattractant, resulting in the migration of cancer cells towards higher concentrations of oxygen. This finding, and the invasion assay described, could lead to a better understanding of oxygen-based chemotaxis in cancer, and ultimately new strategies for managing metastasis.

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“…For instance, apoptotic and other recently dead cells have low entropy and GLIE fluctuations [18,20,27], while malignant cells have high entropy and GLIE fluctuation in comparison to matched normal healthy cells [2,29,30].…”

Section: The Immediate Applicative Aspect Of Glie Fluctuation-based Mmentioning

confidence: 99%

Fluctuation of Information Entropy Measures in Cell Image

Wohl

Zurgil

Hakuk

et al. 2017

Entropy

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A simple, label-free cytometry technique is introduced. It is based on the analysis of the fluctuation of image Gray Level Information Entropy (GLIE) which is shown to reflect intracellular biophysical properties like generalized entropy. In this study, the analytical relations between cellular thermodynamic generalized entropy and diffusivity and GLIE fluctuation measures are explored for the first time. The standard deviation (SD) of GLIE is shown by experiments, simulation and theoretical analysis to be indifferent to microscope system "noise". Then, the ability of GLIE fluctuation measures to reflect basic cellular entropy conditions of early death and malignancy is demonstrated in a cell model of human, healthy-donor lymphocytes, malignant Jurkat cells, as well as dead lymphocytes and Jurkat cells. Utilization of GLIE-based fluctuation measures seems to have the advantage of displaying biophysical characterization of the tested cells, like diffusivity and entropy, in a novel, unique, simple and illustrative way.

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Systems biology of cancer: entropy, disorder, and selection-driven evolution to independence, invasion and “swarm intelligence”

Cited by 46 publications

References 248 publications

Cancer as a disorder of patterning information: computational and biophysical perspectives on the cancer problem

Cancer as a disorder of patterning information: computational and biophysical perspectives on the cancer problem

A paper-based invasion assay: Assessing chemotaxis of cancer cells in gradients of oxygen

Fluctuation of Information Entropy Measures in Cell Image

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