Phenotypic suppression caused by resonance with light-dark cycles indicates the presence of a 24-hours oscillator in yeast and suggests a new role of intrinsically disordered protein regions as internal mediators

Camponeschi, Ilaria; Damasco, Achille; Uversky, Vladimir N.; Giuliani, Alessandro; Bianchi, Michele M.

doi:10.1080/07391102.2020.1749133

Cited by 7 publications

(6 citation statements)

References 70 publications

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“…Resonance phenomena are present at every level of biological organization ( Lerner et al, 2018 ; van der Groen et al, 2018 ) and are at the basis of the new (and very promising) research avenue of “allosteric drugs” that are able to “generalize” an incoming pharmacological stimulus thanks to resonance phenomena similar to what happens in musical instruments ( Zhang et al, 2018 ; Ni et al, 2019 ). In a recent work, we found that an ensemble of interacting proteins made of many IDP/IDPR elements was able to greatly enhance the global phenotypic plasticity of yeast cells ( Camponeschi et al, 2021 ). This is an example of a microscopic level stimulus made evident at the macroscopic phenotypic scale thanks to resonance phenomena with external oscillatory stimuli.…”

Section: Discussionmentioning

confidence: 99%

Networks of Networks: An Essay on Multi-Level Biological Organization

Uversky

Giuliani

2021

Front. Genet.

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The multi-level organization of nature is self-evident: proteins do interact among them to give rise to an organized metabolism, while in the same time each protein (a single node of such interaction network) is itself a network of interacting amino-acid residues allowing coordinated motion of the macromolecule and systemic effect as allosteric behavior. Similar pictures can be drawn for structure and function of cells, organs, tissues, and ecological systems. The majority of biologists are used to think that causally relevant events originate from the lower level (the molecular one) in the form of perturbations, that “climb up” the hierarchy reaching the ultimate layer of macroscopic behavior (e.g., causing a specific disease). Such causative model, stemming from the usual genotype-phenotype distinction, is not the only one. As a matter of fact, one can observe top-down, bottom-up, as well as middle-out perturbation/control trajectories. The recent complex network studies allow to go further the pure qualitative observation of the existence of both non-linear and non-bottom-up processes and to uncover the deep nature of multi-level organization. Here, taking as paradigm protein structural and interaction networks, we review some of the most relevant results dealing with between networks communication shedding light on the basic principles of complex system control and dynamics and offering a more realistic frame of causation in biology.

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Section: Discussionmentioning

confidence: 99%

Networks of Networks: An Essay on Multi-Level Biological Organization

Uversky

Giuliani

2021

Front. Genet.

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“…Moreover, polyploidy permits DNA replication but stops cell division and induces suppression of the bivalent genes regulating circadian rhythms, which entrain many cellular processes, including cell cycles [121]. The cell-autonomous circadian timers established already in cyanobacteria are composed of a transcription-translation-based auto-regulatory feedback loops [122]. Apparently, this detrainment is an important factor causing along with epigenetic bibivalency a metastable dynamic state, which can also favour a reshape and glide from the multi-cellular to unicellular gene expression network.…”

Section: Discussionmentioning

confidence: 99%

Phylostratic Shift of Whole-Genome Duplications in Normal Mammalian Tissues towards Unicellularity Is Driven by Developmental Bivalent Genes and Reveals a Link to Cancer

Anatskaya

Vinogradov

Vainshelbaum

et al. 2020

IJMS

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Tumours were recently revealed to undergo a phylostratic and phenotypic shift to unicellularity. As well, aggressive tumours are characterized by an increased proportion of polyploid cells. In order to investigate a possible shared causation of these two features, we performed a comparative phylostratigraphic analysis of ploidy-related genes, obtained from transcriptomic data for polyploid and diploid human and mouse tissues using pairwise cross-species transcriptome comparison and principal component analysis. Our results indicate that polyploidy shifts the evolutionary age balance of the expressed genes from the late metazoan phylostrata towards the upregulation of unicellular and early metazoan phylostrata. The up-regulation of unicellular metabolic and drug-resistance pathways and the downregulation of pathways related to circadian clock were identified. This evolutionary shift was associated with the enrichment of ploidy with bivalent genes (p < 10−16). The protein interactome of activated bivalent genes revealed the increase of the connectivity of unicellulars and (early) multicellulars, while circadian regulators were depressed. The mutual polyploidy-c-MYC-bivalent genes-associated protein network was organized by gene-hubs engaged in both embryonic development and metastatic cancer including driver (proto)-oncogenes of viral origin. Our data suggest that, in cancer, the atavistic shift goes hand-in-hand with polyploidy and is driven by epigenetic mechanisms impinging on development-related bivalent genes.

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“…It has been shown that light induces oxidative stress in S. cerevisiae (Bodvard et al, 2017) and a similar activity could be envisaged also in K. lactis with the involvement of KlMga2, because of the effect of light on the detoxifying enzymes catalase and SOD. The deletion of KlMGA2 gene has pleiotropic effects, suggesting that KlMga2, possibly because of its biochemical characteristics (Camponeschi et al, 2020), participates in various pathways: uncovering the detail of these pathways requires further investigation.…”

Section: Discussionmentioning

confidence: 99%

“…To our knowledge, studies on response to light have never been reported in K. lactis except the resonance response to light-dark 12 + 12 hour cycles generating an increase of phenotypic suppression in KlMGA2 deletion mutant (Camponeschi et al, 2020). Interestingly, the desaturase gene FAD2 is a light-dependent gene in plants (Kargiotidou et al, 2008;Dar et al, 2017) and its transcription is increased also at low temperatures (Byfield and Upchurch, 2007).…”

Section: Introductionmentioning

confidence: 94%

Light-Stress Response Mediated by the Transcription Factor KlMga2 in the Yeast Kluyveromyces lactis

et al. 2021

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In unicellular organisms like yeasts, which do not have specialized tissues for protection against environmental challenges, the presence of cellular mechanisms to respond and adapt to stress conditions is fundamental. In this work, we aimed to investigate the response to environmental light in Kluyveromyces lactis. Yeast lacks specialized light-sensing proteins; however, Saccharomyces cerevisiae has been reported to respond to light by increasing hydrogen peroxide level and triggering nuclear translocation of Msn2. This is a stress-sensitive transcription factor also present in K. lactis. To investigate light response in this yeast, we analyzed the different phenotypes generated by the deletion of the hypoxia responsive and lipid biosynthesis transcription factor KlMga2. Alterations in growth rate, mitochondrial functioning, ROS metabolism, and fatty acid biosynthesis provide evidence that light was a source of stress in K. lactis and that KlMga2 had a role in the light-stress response. The involvement of KlMsn2 and KlCrz1 in light stress was also explored, but the latter showed no function in this response.

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Phenotypic suppression caused by resonance with light-dark cycles indicates the presence of a 24-hours oscillator in yeast and suggests a new role of intrinsically disordered protein regions as internal mediators

Cited by 7 publications

References 70 publications

Networks of Networks: An Essay on Multi-Level Biological Organization

Networks of Networks: An Essay on Multi-Level Biological Organization

Phylostratic Shift of Whole-Genome Duplications in Normal Mammalian Tissues towards Unicellularity Is Driven by Developmental Bivalent Genes and Reveals a Link to Cancer

Light-Stress Response Mediated by the Transcription Factor KlMga2 in the Yeast Kluyveromyces lactis

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