CRISPR-induced null alleles show that <i>Frost</i> protects <i>Drosophila melanogaster</i> reproduction after cold exposure

Newman, C. E.; Toxopeus, Jantina; Udaka, Hiroko; Ahn, Soohyun; Martynowicz, David M.; Graether, Steffen P.; Sinclair, Brent J.; Percival‐Smith, Anthony

doi:10.1242/jeb.160176

Cited by 13 publications

(12 citation statements)

References 60 publications

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“…Frost-an intrinsically disordered, cold-response protein in Drosophila-is a protein rich in Pro, Glu, Ser, and Thr. It was found to have a protective effect worse than negative control proteins such as lysozyme despite Frost's large R h (79). If the cryoprotective effect was solely driven by a molecular shield effect originating from hard, steric interactions, one would expect that the larger dehydrins and PEG molecules would always be more efficient than the smaller ones.…”

Section: Discussionmentioning

confidence: 99%

Effect of an Intrinsically Disordered Plant Stress Protein on the Properties of Water

Ferreira¹,

Walczyk-Mooradally

Zaslavsky³

et al. 2018

Biophysical Journal

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Dehydrins are plant proteins that are able to protect plants from various forms of dehydrative stress such as drought, cold, and high salinity. Dehydrins can prevent enzymes from losing activity after freeze/thaw treatments. Previous studies had suggested that the dehydrins function by a molecular shield effect, essentially preventing a denatured enzyme from aggregating with another enzyme. Therefore, the larger the dehydrin, the larger the shield and theoretically the more effective the protection. Although this relationship holds for smaller dehydrins, it fails to explain why larger dehydrins are less efficient than would be predicted from their size. Using solvatochromic dyes to probe the solvent features of water, we first confirm that the dehydrins do not bind the dyes, which would interfere with interpretation of the data. We then show that the dehydrins have an effect on three solvent properties of water (dipolarity/polarizability, hydrogen-bond donor acidity and hydrogen-bond acceptor basicity), which can contribute to the protective mechanism of these proteins. Interpretation of these data suggests that although polyethylene glycol and dehydrins have similar protective effects, dehydrins may more efficiently modify the hydrogen-bonding ability of bulk water to prevent enzyme denaturation. This possibly explains why dehydrins recover slightly more enzyme activity than polyethylene glycol.

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Section: Discussionmentioning

confidence: 99%

Effect of an Intrinsically Disordered Plant Stress Protein on the Properties of Water

Ferreira¹,

Walczyk-Mooradally

Zaslavsky³

et al. 2018

Biophysical Journal

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“…Thus, Hero proteins play essential roles in human cell proliferation and Drosophila early development. We note that Frost in Drosophila, which is highly up-regulated after cold shock [33] and required for maintaining female fertility following cold exposure [34], is extremely disordered and charged, and presumably represents another example of Hero proteins with physiological functions in flies.…”

Section: Hero Proteins Are Essential Both In Cells and In Vivomentioning

confidence: 93%

A widespread family of heat-resistant obscure (Hero) proteins protect against protein instability and aggregation

et al. 2020

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Proteins are typically denatured and aggregated by heating at near-boiling temperature. Exceptions to this principle include highly disordered and heat-resistant proteins found in extremophiles, which help these organisms tolerate extreme conditions such as drying, freezing, and high salinity. In contrast, the functions of heat-soluble proteins in non-extremophilic organisms including humans remain largely unexplored. Here, we report that heatresistant obscure (Hero) proteins, which remain soluble after boiling at 95˚C, are widespread in Drosophila and humans. Hero proteins are hydrophilic and highly charged, and function to stabilize various "client" proteins, protecting them from denaturation even under stress conditions such as heat shock, desiccation, and exposure to organic solvents. Hero proteins can also block several different types of pathological protein aggregations in cells and in Drosophila strains that model neurodegenerative diseases. Moreover, Hero proteins can extend life span of Drosophila. Our study reveals that organisms naturally use Hero proteins as molecular shields to stabilize protein functions, highlighting their biotechnological and therapeutic potential.

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“…Proline (Rudolph & Crowe, ) and arginine (Arakawa & Tsumoto, ; Das et al, ) may reduce protein aggregation by forming chains/clusters to physically buffer proteins from each other (Koštál et al, ). We speculate that freeze‐tolerant insects may also accumulate intrinsically disordered proteins (Table ), which prevent protein aggregation under cold and dehydrating conditions (Toxopeus et al, ; Newman et al, ). Several freeze‐tolerant insects accumulate HSPs (Rinehart et al, ; Zhang et al, ; Lu et al, ).…”

Section: Mechanisms Conferring Freeze Tolerancementioning

confidence: 99%

Mechanisms underlying insect freeze tolerance

2018

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Freeze tolerance - the ability to survive internal ice formation - has evolved repeatedly in insects, facilitating survival in environments with low temperatures and/or high risk of freezing. Surviving internal ice formation poses several challenges because freezing can cause cellular dehydration and mechanical damage, and restricts the opportunity to metabolise and respond to environmental challenges. While freeze-tolerant insects accumulate many potentially protective molecules, there is no apparent 'magic bullet' - a molecule or class of molecules that appears to be necessary or sufficient to support this cold-tolerance strategy. In addition, the mechanisms underlying freeze tolerance have been minimally explored. Herein, we frame freeze tolerance as the ability to survive a process: freeze-tolerant insects must withstand the challenges associated with cooling (low temperatures), freezing (internal ice formation), and thawing. To do so, we hypothesise that freeze-tolerant insects control the quality and quantity of ice, prevent or repair damage to cells and macromolecules, manage biochemical processes while frozen/thawing, and restore physiological processes post-thaw. Many of the molecules that can facilitate freeze tolerance are also accumulated by other cold- and desiccation-tolerant insects. We suggest that, when freezing offered a physiological advantage, freeze tolerance evolved in insects that were already adapted to low temperatures or desiccation, or in insects that could withstand small amounts of internal ice formation. Although freeze tolerance is a complex cold-tolerance strategy that has evolved multiple times, we suggest that a process-focused approach (in combination with appropriate techniques and model organisms) will facilitate hypothesis-driven research to understand better how insects survive internal ice formation.

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CRISPR-induced null alleles show that Frost protects Drosophila melanogaster reproduction after cold exposure

Cited by 13 publications

References 60 publications

Effect of an Intrinsically Disordered Plant Stress Protein on the Properties of Water

Effect of an Intrinsically Disordered Plant Stress Protein on the Properties of Water

A widespread family of heat-resistant obscure (Hero) proteins protect against protein instability and aggregation

Mechanisms underlying insect freeze tolerance

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