From physical to biological individuation

Miquel, Paul-Antoine; Hwang, Su-Young

doi:10.1016/j.pbiomolbio.2016.07.002

Cited by 23 publications

(17 citation statements)

References 17 publications

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“…Another notion that becomes fundamental through this principle of variation is that of contextuality. Indeed, understanding biological organization requires taking into account its interaction with the surrounding environment, both at a given time-point and through the successive environments that biological objects traverse (Soto and Sonnenschein, 2005) (see Miquel and Hwang, 2016; Montévil et al, 2016; Sonnenschein and Soto, 2016). In addition to the role that constraints play in canalizing processes, they make possible the appearance of new constraints and thus changes of organization.…”

Section: Theoretical Principlesmentioning

confidence: 99%

Modeling mammary organogenesis from biological first principles: Cells and their physical constraints

Montévil

Speroni

Sonnenschein

et al. 2016

Progress in Biophysics and Molecular Biology

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In multicellular organisms, relations among parts and between parts and the whole are contextual and interdependent. These organisms and their cells are ontogenetically linked: an organism starts as a cell that divides producing non-identical cells, which organize in tri-dimensional patterns. These association patterns and cells types change as tissues and organs are formed. This contextuality and circularity makes it difficult to establish detailed cause and effect relationships. Here we propose an approach to overcome these intrinsic difficulties by combining the use of two models; 1) an experimental one that employs 3D culture technology to obtain the structures of the mammary gland, namely, ducts and acini, and 2) a mathematical model based on biological principles. The typical approach for mathematical modeling in biology is to apply mathematical tools and concepts developed originally in physics or computer sciences. Instead, we propose to construct a mathematical model based on proper biological principles. Specifically, we use principles identified as fundamental for the elaboration of a theory of organisms, namely i) the default state of cell proliferation with variation and motility and ii) the principle of organization by closure of constraints. This model has a biological component, the cells, and a physical component, a matrix which contains collagen fibers. Cells display agency and move and proliferate unless constrained; they exert mechanical forces that i) act on collagen fibers and ii) on other cells. As fibers organize, they constrain the cells on their ability to move and to proliferate. The model exhibits a circularity that can be interpreted in terms of closure of constraints. Implementing the mathematical model shows that constraints to the default state are sufficient to explain ductal and acinar formation, and points to a target of future research, namely, to inhibitors of cell proliferation and motility generated by the epithelial cells. The success of this model suggests a step-wise approach whereby additional constraints imposed by the tissue and the organism could be examined in silico and rigorously tested by in vitro and in vivo experiments, in accordance with the organicist perspective we embrace.

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Section: Theoretical Principlesmentioning

confidence: 99%

Modeling mammary organogenesis from biological first principles: Cells and their physical constraints

Montévil

Speroni

Sonnenschein

et al. 2016

Progress in Biophysics and Molecular Biology

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“…This means that a zygote is both a cell and an organism, and with each cell division by the zygote and its progeny, these two levels of individuation become more obvious. In other words, following Gilbert Simon-don, individuation in multicellular organisms becomes a process rather than a thing [7]. All along, the cell theory plays a unifying role between evolutionary and organismal biology because it provides a link between the uni- or the multi-cellular individual and its progeny in which the cell itself is a vehicle of inheritance.…”

Section: Part I From the Inert To The Alivementioning

confidence: 99%

An Integrative Approach Toward Biology, Organisms, and Cancer

Sonnenschein

Soto

2017

Methods in Molecular Biology

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Over the last two decades, we have challenged the hegemony of the somatic mutation theory of carcino-genesis (SMT) based on the lack of theoretical coherence of the premises adopted by its followers. We offered instead a theoretical alternative, the tissue organization field theory (TOFT), that is based on the premises that cancer is a tissue-based disease and that proliferation and motility is the default state of all cells. We went on to use a theory-neutral experimental protocol that simultaneously tested the TOFT and the SMT. The results of this test favored adopting the TOFT and rejecting the SMT. Recently, an analysis of the differences between the Physics of the inanimate and that of the living matter has led us to propose principles for the construction of a much needed theory of organisms. The three biological principles are(a) a default state, (b) a principle of variation, and (c) one of organization. The TOFT, defined as “development gone awry,” fits well within the principles that we propose for a theory of organisms. This radical conceptual change opened up the possibility of anchoring mathematical modeling on genuine biological principles. By identifying constraints to the default state, multilevel biomechanical explanations become as legitimate as the molecular ones on which other modelers that adopt the SMT rely. Expanding research based on the premises of our theory of organisms will enrich a comprehensive understanding of normal development and of the one that goes awry.

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“…Philosophers, particularly those from the “Continental” tradition have long observed the differences between these two disciplines, and the radical difference between alive and inert (Kant, 2000; Canguilhem, 2008; Bergson, 2007). That is, the agency and normativity of the living and the process of individuation (Miquel and Hwang, 2016). We biologists need to address the relentless change of the living objects and their individuality, their incessant change of symmetries, and their creativity.…”

Section: From “Physics” To “Nature” and Toward An Autonomous Biologymentioning

confidence: 99%

Why do we need theories?

Longo

Soto

2016

Progress in Biophysics and Molecular Biology

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Theories organize knowledge and construct objectivity by framing observations and experiments. The elaboration of theoretical principles is examined in the light of the rich interactions between physics and mathematics. These two disciplines share common principles of construction of concepts and of the proper objects of inquiry. Theory construction in physics relies on mathematical symmetries that preserve the key invariants observed and proposed by such theory; these invariants buttress the idea that the objects of physics are generic and thus interchangeable and they move along specific trajectories which are uniquely determined, in classical and relativistic physics. In contrast to physics, biology is a historical science that centers on the changes that organisms experience while undergoing ontogenesis and phylogenesis. Biological objects, namely organisms, are not generic but specific; they are individuals. The incessant changes they undergo represent the breaking of symmetries, and thus the opposite of symmetry conservation, a central component of physical theories. This instability corresponds to the changes of the environment and the phenotypes. Inspired by Galileo’s principle of inertia, the “default state” of inert matter, we propose a “default state” for biological dynamics following Darwin’s first principle, “descent with modification” that we transform into “proliferation with variation and motility” as a property that spans life, including cells in an organism. These dissimilarities between theories of the inert and of biology also apply to causality: biological causality is to be understood in relation to the distinctive role that constraints assume in this discipline. Consequently, the notion of cause will be reframed in a context where constraints to activity are seen as the core component of biological analyses. Finally, we assert that the radical materiality of life rules out distinctions such as “software vs. hardware.”

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From physical to biological individuation

Cited by 23 publications

References 17 publications

Modeling mammary organogenesis from biological first principles: Cells and their physical constraints

Modeling mammary organogenesis from biological first principles: Cells and their physical constraints

An Integrative Approach Toward Biology, Organisms, and Cancer

Why do we need theories?

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