Design principles for robust oscillatory behavior

Castillo-Hair, Sebastian M.; Villota, Elizabeth R.; Coronado, Alberto M.

doi:10.1007/s11693-015-9178-6

Cited by 16 publications

(14 citation statements)

References 43 publications

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“…In agreement with previous work (Castillo-Hair et al, 2015; Goldbeter, 2002; Novak and Tyson, 2008), we found that certain core network topologies are essential for robust oscillations. However, we also found that local modifications on a node of the network have a significant impact on the global network robustness.…”

Section: Introductionsupporting

confidence: 93%

“…Despite the complexity and diversity of these oscillators, their central network architectures are highly conserved (Bell-Pedersen et al, 2005; Cross et al, 2011), suggesting that network topology is a key factor in determining the properties of biological oscillations. Studies have focused on the core topologies of oscillators, to understand the systems-level characteristics such as periodicity and robustness (Castillo-Hair et al, 2015; Lomnitz and Savageau, 2014; Nguyen, 2012; Novak and Tyson, 2008; Woods et al, 2016). …”

Section: Introductionmentioning

confidence: 99%

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Incoherent Inputs Enhance the Robustness of Biological Oscillators

Liu

Yang

2017

Cell Systems

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SUMMARY Robust biological oscillators retain the critical ability to function in the presence of environmental perturbations. Although central architectures that support robust oscillations have been extensively studied, networks containing the same core vary drastically in their potential to oscillate, and it remains elusive what peripheral modifications to the core contribute to this functional variation. Here, we have generated a complete atlas of two- and three-node oscillators computationally, then systematically analyzed the association between network structure and robustness. We found that, while certain core topologies are essential for producing a robust oscillator, local structures can substantially modulate the robustness of oscillations. Notably, local nodes receiving incoherent or coherent inputs respectively promote or attenuate the overall network robustness in an additive manner. We validated these relationships in larger-scale networks reflective of real biological oscillators. Our findings provide an explanation for why auxiliary structures not required for oscillation are evolutionarily conserved and suggest simple ways to evolve or design robust oscillators.

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Section: Introductionsupporting

confidence: 93%

Section: Introductionmentioning

confidence: 99%

Incoherent Inputs Enhance the Robustness of Biological Oscillators

Liu

Yang

2017

Cell Systems

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“…Philosophically, structure determines function, and the topology of networks is key to understanding their central properties [ 28 – 31 ]. The core topologies capturing the backbone of practically complex networks have been investigated for simple functions such as oscillations [ 32 ], adaptation [ 33 ] switch-like responses [ 34 ], dose-response alignment [ 35 ] and patterning in response to morphogen gradients [ 36 ].…”

Section: Introductionmentioning

confidence: 99%

Robust network topologies for generating oscillations with temperature-independent periods

Ouyang

Wang

2017

PLoS ONE

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Nearly all living systems feature a temperature-independent oscillation period in circadian clocks. This ubiquitous property occurs at the system level and is rooted in the network architecture of the clock machinery. To investigate the mechanism of this prominent property of the circadian clock and provide general guidance for generating robust genetic oscillators with temperature-compensated oscillations, we theoretically explored the design principle and core network topologies preferred by oscillations with a temperature-independent period. By enumerating all topologies of genetic regulatory circuits with three genes, we obtained four network motifs, namely, a delayed negative feedback oscillator, repressilator, activator-inhibitor oscillator and substrate-depletion oscillator; hybrids of these motifs constitute the vast majority of target network topologies. These motifs are biased in their capacities for achieving oscillations and the temperature sensitivity of the period. The delayed negative feedback oscillator and repressilator are more robust for oscillations, whereas the activator-inhibitor and substrate-depletion oscillators are superior for maintaining a temperature-independent oscillation period. These results suggest that thermally robust oscillation can be more plausibly achieved by hybridizing these two categories of network motifs. Antagonistic balance and temperature insulation mechanisms for achieving temperature compensation are typically found in these topologies with temperature robustness. In the temperature insulation approach, the oscillation period relies on very few parameters, and these parameters are influenced only slightly by temperature. This approach prevents the temperature from affecting the oscillation period and generates circadian rhythms that are robust against environmental perturbations.

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“…The complexity of natural oscillatory systems makes it difficult to analyze their behaviors quantitatively. Uncovering functional properties of simple biological oscillators then becomes important for the understanding of various intracellular processes and the characterization of complex biological oscillators, and it is also helpful for the elucidation of design principles of biological oscillators [36,16,7]. In the spirit of synthetic biology, biological oscillators can be classified according to their topology [28,18,23,19], e.g., the oscillators of negative feedback loops, and those of interlocked positive feedback loop (PFL) and negative feedback loop (NFL), which are denoted by iPNFL for brevity.…”

mentioning

confidence: 99%

Interlocked multi-node positive and negative feedback loops facilitate oscillations

Li¹

2019

Discrete &Amp; Continuous Dynamical Systems - B

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Positive and negative feedback loops in biological regulatory networks appear often in a multi-node manner since regulatory processes are in general multi-step. Although it is well known that interlocked positive and negative feedback loops (iPNFLs) can generate sustained oscillations, how the number of nodes in each loop affects the oscillations remains elusive. By analyzing a model of iPNFLs with multiple nodes, we find that the node number of the negative loop mainly plays a role of amplifying oscillation amplitudes whereas that of the positive loop mainly plays a role of reducing oscillatory regions, both depending on the (competitive or noncompetitive) way of interaction between the two loops. We also find that given an iPNFL network of the same structure, the noncompetitive model is more likely to produce large-amplitude oscillations than the competitive model. These results not only indicate that multi-node iPNFLs are an effective mechanism of promoting oscillations but also are helpful for the design of synthetic oscillators.

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Design principles for robust oscillatory behavior

Cited by 16 publications

References 43 publications

Incoherent Inputs Enhance the Robustness of Biological Oscillators

Incoherent Inputs Enhance the Robustness of Biological Oscillators

Robust network topologies for generating oscillations with temperature-independent periods

Interlocked multi-node positive and negative feedback loops facilitate oscillations

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