Physics of Biological Oscillators: New Insights into Non-Equilibrium and Non-Autonomous Systems

435 Pages·2021·16.843 MB·English

by  Aneta Stefanovska, Peter V. E. McClintock

Understanding Complex Systems
Aneta Stefanovska
Peter V. E. McClintock   Editors
Physics
of Biological
Oscillators
New Insights into Non-Equilibrium and
Non-Autonomous Systems
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Understanding Complex Systems
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Aneta Stefanovska Peter V. E. McClintock
(cid:129)
Editors
Physics of Biological
Oscillators
New Insights into Non-Equilibrium
and Non-Autonomous Systems
123
Editors
Aneta Stefanovska PeterV.E. McClintock
Department ofPhysics Department ofPhysics
Lancaster University Lancaster University
Lancaster,UK Lancaster,UK
ISSN 1860-0832 ISSN 1860-0840 (electronic)
Understanding ComplexSystems
ISBN978-3-030-59804-4 ISBN978-3-030-59805-1 (eBook)
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Foreword by Alex A. R. Webb
An oscillation is the repetitive variation in time of some measure, or between two
ormoredifferentstates.Oscillationsoccurnotonlyinmechanicalsystems,butalso
inotherkindsofdynamicalsystem.Tothenon-specialistitmightbeasurprisethat
biologicalsystemscanarrangeintonetworksthatformrobustoscillatingdynamical
systems, but this is a frequent property of biological networks. By biological
oscillators we mean any system with repeated cycles of activity or abundance of a
biological component (e.g., metabolite or protein). Biological oscillators include
communitybehaviors, suchasseeninecologicalstudies;howeverinthisbookthe
focus is on oscillations in cellular or physiological activities within a single
organism.
Broadly, biological oscillators can be divided into three categories. First, there
are those that oscillate for a short period before damping and arise from a pertur-
bation to the system, such as metabolic and homeostatic control mechanisms,
includingtheoscillatorydynamicsinglycolysis.Thesecondcategoryofbiological
oscillators involves stimulus-induced oscillatory behaviors including oscillatory
dynamics of signal relays within and between cells, oscillations of blood flow and
oscillations in firing of neurons in the brain. Lastly there are the self-sustaining
endogenous rhythms including the heart pacemaker, breathing and blood flow in
mammals, circadian oscillations, cell division cycles and developmental clocks.
Thesedistinctionsbetweenthedifferenttypesofbiologicaloscillationsarearbitrary
andtheboundariesareblurredbecauseallhavesomeself-sustainingproperties,and
all can have nonautonomous properties affected by other signals. These are some
of the complex issues discussed in the pages of this book.
Another level of complexity is introduced by the hierarchy of interactions
between oscillators. In both single- and multi-cellular organisms, oscillators often
can occur within a single cell, however, interactions between cells can reinforce,
amplify and make the oscillations more robust, such as found in the oscillations
between the neurons of the suprachiasmatic nucleus of the circadian pacemaker of
mammalian brains. In the mammalian circadian pacemaker, the oscillatory
dynamics are generated by transcriptional feedback loops of gene expression,
v
vi ForewordbyAlexA.R.Webb
proteinsynthesisandproteindegradationintheindividualcells,andarereinforced
by electrical coupling between the cells, resulting in a very robust multicellular
circadian oscillator.
Physics has developed powerful conceptual and mathematical tools to under-
stand the behavior of physical oscillators, such as pendula. Remarkably, the
analogiesfromthephysicalworldhaveproventobeusefulindescribing,modeling
and understanding the behaviors and dynamics of biological oscillators. Physics
offers much to the biologist, providing formal descriptions of systems that are too
complex to be understood intuitively, and predictive power, which is required to
turn discovery into application. Whilst useful, there are challenges in applying
concepts from the physical world to biological oscillators. Physical descriptions of
oscillatorsareoftenappliedtodesignedmechanicalorelectronicsystemsinwhich
thecomponentsandconnectionsareknownandwellunderstood.Often,instudying
biologicaloscillators,thenumberofcomponents,thenatureofthecomponents,the
network of interactions between the components and the mechanisms by which
these interactions occur are either assumed, or known for only a few of the com-
ponents that make up the oscillator.
Biological oscillators can be formed by very simple systems comprising only
twocomponents,butareoftenformedofverycomplexnetworksthatcanbenearly
fully connected and therefore have a high degree of feedback. For example, the
mutualgeneregulatorynetworksthatarepartofthe24-hourcircadianoscillatorof
plant cells involve mutual regulation between at least 30 genes in a nearly fully
connected network. This means it is often difficult to obtain a model of the inter-
actions in the network in which one can have full confidence. The nature of the
oscillatory dynamics in biological systems can be complex, involving many
changes in state, abundance and location of thecomponents. In the plant circadian
oscillator as an example, feedback between components can occur through
protein-DNA interactions regulating the expression of component parts, phospho-
rylation to affect protein activity, ubiquitination to affect protein stability and
translocation between the cytoplasm and nucleus to regulate accessibility of tran-
scriptional regulators to DNA.
Oneofthemostchallengingfeaturesofbiologicaloscillators,comparedtothose
designedbyhumans,isthatatdifferenttimesintheoscillatorycycle,thenetworkof
regulatory connections in the oscillator can change. For example, in the circadian
oscillatorsthat drive 24 hourrhythms in plants and humans,the proteins that form
the regulatory network vary greatly in their abundance over the cycle because of
oscillations in protein translation and breakdown, which are the basis of the
oscillatorydynamics.Thus,theoreticalandmathematicaldescriptionsofbiological
oscillatorsmustdescribenotonlythedynamicsandpropertiesoftheoscillator,but
also how those change through the oscillatory cycle. This is a particular challenge
when considering non-autonomous oscillators that respond to external inputs,
which probably represents most biological oscillators, because regulation by an
external signal can be affected by the state and availability of a component in the
oscillator,meaningthatregulatoryinputsaresubjectthemselvestofeedbackcontrol
from the oscillator.
ForewordbyAlexA.R.Webb vii
Itisthesesimilaritiesanddifferencesbetweenphysicalandbiologicaloscillators
which resulted in the Physics of Biological Oscillators (POBO) conference at
Chicheley Hall, UK in 2018, a meeting held in celebration of the 60th birthday of
AnetaStefanovskawhohascontributedsomuchtothedevelopmentofthesubject.
This book captures the discussions and presentations during three wonderful days
of exciting science, in which experts in different disciplines grappled with the
immenseintellectualchallengesoffindingthebestwaystodescribe,analyze,model
and understand the properties, functions, behaviors and uses of biological oscilla-
tors.Thechapterssummarizingthepresentationsbyresearchersacrossthedifferent
disciplines give an insight into the different biological systems being investigated
andthevarietyofPhysicsapproachesbeingused.Itwasexhilaratingtospendthree
days in the company of researchers from different disciplines trying to bridge the
gaps between the experts in different fields to understand these fundamental bio-
logical behaviors. This seems an even more amazing experience looking back
through the lens of the COVID-19 pandemic which hit during the final stages of
production of this book. I hope you enjoy the invigorating intellectual stimulation
contained within these chapters as much as I have.
August 2020 Alex A. R. Webb
Department of Plant Sciences
University of Cambridge
Cambridge, UK
Preface
This book derives mainly from a Research Workshop Physics of Biological
Oscillators: New Insights into Non-Equilibrium and Non-Autonomous Systems1
held in Chicheley Hall (27–30 November 2018): see photograph. It was a highly
interdisciplinary event that brought together some of the best international experts
workingonthevexedproblemofhowbesttotreatthenon-autonomousoscillatory
systems that crop up so often in biology. They included life scientists who inves-
tigate and measure the oscillations and the physicists, chemists, mathematicians,
informationtheorists,andengineersseekingtounderstandtheirfundamentalnature
and origins and to devise useful applications of this knowledge. Thus, although
their work lies in seemingly very different scientific areas—ranging from mathe-
matics to the experimental recording and analysis of real data—they were all
addressing in one way or another the problem of time-variability in oscillatory
systems. They gave presentations about how to measure, analyze, model, and
understand such data as well as considering applications to medicine, both actual
andpotential.Nearlyalloftheexperts,assembledfrom19countries,kindlyagreed
to write up their presentations for publication thereby providing the basis for the
book.
Lancaster, UK Aneta Stefanovska
Peter V. E. McClintock
1www.physicsoflife.org.uk/physics-of-biological-oscillators.html.
ix
x Preface
Participants in the POBO Research Workshop Physics of Biological Oscillators:
NewInsightsintoNon-EquilibriumandNon-AutonomousSystems,outsidethefront
door of Chicheley Hall, Buckinghamshire, UK, where the event took place.
Photograph by M. G. Rosenblum (University of Potsdam)