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Sukenik, S.

Publications and source records attributed to Sukenik, S..

At least 19 recordsLinked to original sources

Proteoform plasticity modulates the temperature response in circadian timekeeping

The molecular circadian clock optimally coordinates an organism's physiology with the light/dark cycle. One commonality among circadian molecular clock proteins is that they undergo alternative splicing, yielding multiple proteoforms. The isoform-specific sequences spliced into clock proteins contain intrinsically disordered regions (IDRs), suggesting that these regions might be intricately involved in cellular regulation. However, the functions of these isoform-specific IDRs in the clock remain poorly defined. Here, we use the core clock repressor FREQUENCY (FRQ) from the fungal circadian model system Neurospora crassa to test the hypothesis that alternative splicing of core clock IDRs yields multiple proteoforms that expand the functional regulatory capacity of FRQ. To do so, we biophysically characterized an IDR specific to the long isoform of the core clock repressor FRQ and identified motifs and molecular behaviors that regulate clock robustness in a temperature-dependent manner. We further compared the interactomes of two FRQ isoforms, identifying distinct functions and interacting proteins that could contribute to temperature regulation. Taken together, our data highlight that isoform-specific IDRs in clock-repressor proteins enhance and expand clock function in a context-dependent manner.

biochemistry↗

Infection Tunes the Dynamics of Adenoviral E1A Disordered Regions

Intrinsically Disordered Proteins and protein regions (IDPs) are abundant in many viral proteomes and play diverse roles in the viral infectious cycles. The adenovirus Early Protein 1A (E1A) is one such viral IDP. E1A acts as a molecular hub that regulates viral infection by mediating interactions between viral and multiple host proteins. Like other IDPs, E1A exists in a flexible ensemble of conformations. Despite a demonstrated link between ensemble structure and function in E1A, no real-time measurement of its ensemble has been performed. Here, we use live cell FRET microscopy to measure the local ensemble structure of E1A in human cells, both in healthy cells and in cells infected with adenovirus. We found specific disordered regions undergo significant changes to their ensemble in infected cells. Furthermore, infection also alters the propensity of these regions to partition between the cytoplasm and nucleus, a hallmark of E1A function during infection. Our results showcase that the structural ensembles of viral IDPs are responsive to infection, and suggest that these may play a role in regulating infection progression. SignificanceIntegral to many viral proteomes are intrinsically disordered proteins and protein regions (IDPs), which target and rewire cellular pathways to ensure infection progression. During this process, the physical and chemical composition of the cell changes dramatically: metabolism is rewired, viral proteins are produced en masse, and as a result, the chemical composition of the host proteome is significantly altered. IDPs are known to be structurally sensitive to even mild changes in their environment, and their structural changes can result in a change to function. Here, using live cell FRET microscopy, we show that the structure and spatial localization of an adenovirus IDP, E1A, is altered in cells infected by the virus. Beyond a possible functional role for structural sensitivity in viral IDP function, our findings suggest that host IDPs may also be structurally altered by infection, with downstream functional consequences.

biophysics↗

Intramolecular interactions between folded and disordered regions shape ubiquilin structure and function

Multidomain proteins consist of folded domains connected by intrinsically disordered regions. The flexibility afforded by the disordered regions coupled to the structure and surface chemistry of folded regions allows for unique structural and functional features in these proteins. Yet how intramolecular interactions between disordered regions and folded domains affect multidomain protein structure and function remain poorly understood. Here we use a range of biophysical and computational approaches to measure the intramolecular interactions between the folded domains and disordered regions of ubiquilins (UBQLNs) - essential components of protein quality control that shuttle poly-ubiquitinated client proteins to proteasomal degradation or autophagy. Starting with the yeast UBQLN homolog Dsk2, we find that interactions between two folded domains located at the opposite ends of UBQLN bring about a closed conformation. The prevalence of this closed conformation, however, is modulated by intramolecular interactions involving the disordered regions and folded STI1 domain at the center of the protein. Simulations and analysis of UBQLN homologs across multiple eukaryotic lineages reveals that these disordered:folded domain interactions exist in some UBQLN homologs but are absent in others, indicating possible fundamental differences in function among proteins with the same multidomain architecture.

biophysics↗

A geothermal amoeba sets a new upper temperature limit for eukaryotes

The study of temperature limits has transformed our knowledge of the boundaries of life but has been largely focused on bacteria and archaea. We isolated a novel geothermal amoeba, Incendiamoeba cascadensis, that divides at 63{degrees}C (145.4{degrees}F), establishing a new record for the upper temperature limit across all eukaryotes. We demonstrated cellular proliferation with growth experiments and visualized mitosis via expansion microscopy. Using high-temperature live-cell imaging, we quantified movement up to 64{degrees}C. We assembled the genome of I. cascadensis and using comparative genomics found an enrichment of genes related to proteostasis, genome stability, and sensing the external environment. Taken together, our findings challenge the current paradigm of temperature constraints on eukaryotic cells and reshape our understanding of where and how eukaryotic life can persist.

microbiology↗

Functional diversity of Arabidopsis late embryogenesis abundant proteins in response to changes in the physicochemical environment

Some desiccation-tolerant organisms accumulate intrinsically disordered proteins (IDPs), such as Late Embryogenesis Abundant (LEA) proteins, which help protect other proteins from inactivation and/or aggregation during desiccation. Like other IDPs, LEA proteins adopt ensembles of extended conformations that shift in response to environmental changes. Desiccation causes dramatic changes in the cellular environment, but it is unclear how the structural malleability of LEAs is related to their protective function. In this work, we measured the in vitro protective function and structural sensitivity to changes in the environment of four Arabidopsis thaliana LEA proteins from different families. We found that all LEAs showed different protection efficiencies of the labile enzyme lactate dehydrogenase under desiccation in vitro. In line with this, we identified distinct ensemble structural changes when these LEA proteins were exposed to different physicochemical environments. Specifically, AtEM1, AtLEA7, and AtLEA4-5 showed compaction when the solution was crowded with polymers, whereas AtLEA6-2.2 showed larger structural changes when salt concentrations were increased. Furthermore, the ensembles of AtEM1, AtLEA7, and AtLEA4-5 gained helicity under desiccated conditions, while that of AtLEA6-2.2 remained largely disordered. Our results highlight how ensemble properties of LEA proteins contribute to their distinct functional activities in vitro. This work advances our understanding of the molecular features that contribute to functional diversity in desiccation-related IDPs.

biophysics↗

Correlating Disordered Activation Domain Ensembles with Gene Expression Levels

Transcription factor proteins bind to specific DNA promoter sequences and initiate gene transcription. In eukaryotes, most transcription factors contain intrinsically disordered activation domains (ADs) that regulate their transcriptional activity. Like other disordered protein regions, ADs do not have a fixed three-dimensional structure and instead exist in an ensemble of conformations. Disordered ensembles contain sequence-encoded structural preferences which are often linked to their function. We hypothesize this link exists between the structural preferences of disordered AD ensembles and their ability to induce gene expression. To test this, we used FRET microscopy to measure the ensemble dimensions of two activation domains, HIF-1 and CITED2, in live cells, and correlate this structural information with transcriptional activity. We find that point mutations that expanded the HIF-1 ensemble increased transcriptional activity, while those that compacted it reduced activity. Conversely, CITED2 showed no correlation between ensemble dimensions and activity. Our results reveal a sequence-dependent relationship between AD ensemble dimensions and their transcriptional activity. WHY IT MATTERSTranscription factors have activation domains (ADs) that bind to coactivator complexes to initiate gene transcription. Despite their key role, a comprehensive understanding of what drives their transcriptional activity has remained elusive. Efforts to understand AD activity have largely focused on their amino acid composition. In recent years, it is increasingly realized that the structural ensembles of disordered proteins contain biases that dictate their structural properties. For ADs, ensemble structures remain poorly explored, especially in relation to their activity. Here we report a mutational study of two ADs, HIF-1 and CITED2, that examines how ensemble dimensions correlate with activity. Our findings suggest that ensemble dimensions may drive activity in some ADs, and that AD ensemble dimensions can be modulated not only through mutations, but also through changes in the cellular environment.

biophysics↗

LEA_4 motifs function alone and in conjunction with synergistic cosolutes to protect a labile enzyme during desiccation

Organisms from all kingdoms of life depend on Late Embryogenesis Abundant (LEA) proteins to survive desiccation. LEA proteins are divided into broad families distinguished by the presence of family-specific motif sequences. The LEA_4 family, characterized by eleven-residue motifs, plays a crucial role in the desiccation tolerance of numerous species. However, the role of these motifs in the function of LEA_4 proteins is unclear, with some studies finding that they recapitulate the function of full-length LEA_4 proteins in vivo, and other studies finding the opposite result. In this study, we characterize the ability of LEA_4 motifs to protect a desiccation-sensitive enzyme, citrate synthase, from loss of function during desiccation. We show here that LEA_4 motifs not only prevent the loss of function of citrate synthase during desiccation, but also that they can do so more robustly via synergistically interactions with cosolutes. Our analysis further suggests that cosolutes induce synergy with LEA_4 motifs in a manner that correlates with transfer free energy (TFE). This research advances our understanding of LEA_4 proteins by demonstrating that during desiccation their motifs can protect specific clients to varying degrees and that their protective capacity is modulated by their chemical environment. Our findings extend beyond the realm of desiccation tolerance, offering insights into the interplay between IDPs and cosolutes. By investigating the function of LEA_4 motifs, we highlight broader strategies for understanding protein stability and function.

biochemistry↗

Protein surface chemistry encodes an adaptive resistance to desiccation

Cellular desiccation - the loss of nearly all water from the cell - is a recurring stress in an increasing number of ecosystems that can drive protein unfolding and aggregation. For cells to survive, at least some of the proteome must resume function upon rehydration. Which proteins tolerate desiccation, and the molecular determinants that underlie this tolerance, are largely unknown. Here, we apply quantitative and structural proteomic mass spectrometry to show that certain proteins possess an innate capacity to tolerate rehydration following extreme water loss. Structural analysis points to protein surface chemistry as a key determinant for desiccation tolerance, which we test by showing that rational surface mutants can convert a desiccation sensitive protein into a tolerant one. Desiccation tolerance also has strong overlap with cellular function, with highly tolerant proteins responsible for production of small molecule building blocks, and intolerant proteins involved in energy-consuming processes such as ribosome biogenesis. As a result, the rehydrated proteome is preferentially enriched with metabolite and small molecule producers and depleted of some of the cells heaviest consumers. We propose this functional bias enables cells to kickstart their metabolism and promote cell survival following desiccation and rehydration. TeaserProteins can resist extreme dryness by tuning the amino acids on their surfaces.

biophysics↗

Disordered proteins interact with the chemical environment to tune their protective function during drying

The conformational ensemble and function of intrinsically disordered proteins (IDPs) are sensitive to their solution environment. The inherent malleability of disordered proteins combined with the exposure of their residues accounts for this sensitivity. One context in which IDPs play important roles that is concomitant with massive changes to the intracellular environment is during desiccation (extreme drying). The ability of organisms to survive desiccation has long been linked to the accumulation of high levels of cosolutes such as trehalose or sucrose as well as the enrichment of IDPs, such as late embryogenesis abundant (LEA) proteins or cytoplasmic abundant heat soluble (CAHS) proteins. Despite knowing that IDPs play important roles and are co-enriched alongside endogenous, species-specific cosolutes during desiccation, little is known mechanistically about how IDP-cosolute interactions influence desiccation tolerance. Here, we test the notion that the protective function of desiccation-related IDPs is enhanced through conformational changes induced by endogenous cosolutes. We find that desiccation-related IDPs derived from four different organisms spanning two LEA protein families and the CAHS protein family, synergize best with endogenous cosolutes during drying to promote desiccation protection. Yet the structural parameters of protective IDPs do not correlate with synergy for either CAHS or LEA proteins. We further demonstrate that for CAHS, but not LEA proteins, synergy is related to self-assembly and the formation of a gel. Our results suggest that functional synergy between IDPs and endogenous cosolutes is a convergent desiccation protection strategy seen among different IDP families and organisms, yet, the mechanisms underlying this synergy differ between IDP families.

biochemistry↗

Sequence-ensemble-function relationships for disordered proteins in live cells

Despite lacking a stable three-dimensional structure, intrinsically disordered protein regions (IDRs) are ubiquitous across all kingdoms of life and play essential cellular roles. While rational design of folded proteins has seen substantial recent progress, our ability to design IDRs remains limited. Here, we present GOOSE, a comprehensive computational framework for the rational design of IDRs. GOOSEs versatility and throughput enable us to test thousands of IDR sequences, revealing distinct sequence-ensemble-function relationships. By using GOOSE to rapidly explore these relationships, we design IDRs that can alter their ensembles in response to cell volume changes, create scaffolds for the self-assembly of specific clients, and protect cells from desiccation. Taken together, this work highlights how sequence-function relationships are encoded in IDRs and provides a powerful tool for further exploration.

biophysics↗

Helicity of a tardigrade disordered protein promotes desiccation tolerance

In order to survive extreme drying (anhydrobiosis), many organisms, spanning every kingdom of life, accumulate intrinsically disordered proteins (IDPs). For decades, the ability of anhydrobiosis-related IDPs to form transient amphipathic helices has been suggested to be important for promoting desiccation tolerance. However, evidence empirically supporting the necessity and/or sufficiency of helicity in mediating anhydrobiosis is lacking. Here we demonstrate that the linker region of CAHS D, a desiccation-related IDP from tardigrades that contains significant helical structure, is the protective portion of this protein. Perturbing the sequence composition and grammar of the linker region of CAHS D, through the insertion of helix-breaking prolines, modulating the identity of charged residues, sequence scrambling, or replacement of hydrophobic amino acids with serine or glycine residues results in variants with different degrees of helical structure. Importantly, the resulting helicity of these variants generated through similar helix breaking modalities correlates strongly with their ability to promote desiccation tolerance, providing direct evidence that helical structure is necessary for robust protection conferred by this desiccation-related IDP. However, correlation of protective capacity and helical content in variants generated through different helix perturbing modalities do not show as strong a trend, suggesting that while helicity is important it is not the only property that makes a protein protective during desiccation. These results provide direct evidence for the decades old theory that helicity of desiccation-related IDPs is linked to their anhydrobiotic capacity.

biochemistry↗

Labile assembly of a tardigrade protein induces biostasis

Tardigrades are microscopic animals that survive desiccation by inducing biostasis. To survive drying tardigrades rely on intrinsically disordered CAHS proteins that form gels. However, the sequence features and mechanisms underlying gel formation and the necessity of gelation for protection have not been demonstrated. Here we report a mechanism of gelation for CAHS D similar to that of intermediate filaments. We show that gelation restricts molecular motion, immobilizing and protecting labile material from the harmful effects of drying. In vivo, we observe that CAHS D forms fiber-like condensates during osmotic stress. Condensation of CAHS D improves survival of osmotically shocked cells through at least two mechanisms: reduction of cell volume change and reduction of metabolic activity. Importantly, condensation of CAHS D is reversible and metabolic rates return to control levels after CAHS condensates are resolved. This work provides insights into how tardigrades induce biostasis through the self-assembly of CAHS gels.

physiology↗

Structural preferences shape the entropic force of disordered protein ensembles

Intrinsically disordered protein regions (IDRs) make up over 30% of the human proteome and instead of a native, well-folded structure exist in a dynamic conformational ensemble. Tethering IDRs to a surface (for example, the surface of a well-folded region of the same protein) can reduce the number of accessible conformations in IDR ensembles. This reduces the ensembles conformational entropy, generating an effective entropic force that pulls away from the point of tethering. Recent experimental work has shown that this entropic force causes measurable, physiologically relevant changes to protein function, but how the magnitude of this force depends on the IDR sequence remains unexplored. Here we use all-atom simulations to analyze how structural preferences encoded in dozens of IDR ensembles contribute to the entropic force they exert upon tethering. We show that sequence-encoded structural preferences play an important role in determining the magnitude of this force and that compact, spherical ensembles generate an entropic force that can be several times higher than more extended ensembles. We further show that changes in the surrounding solutions chemistry can modulate IDR entropic force strength. We propose that the entropic force is a sequence-dependent, environmentally tunable property of terminal IDR sequences.

biophysics↗

YAP condensates are highly organized hubs for YAP/TEAD transcription

YAP/TEAD signaling is essential for organismal development, cell proliferation, and cancer progression. As a transcriptional coactivator, how YAP activates its downstream target genes is incompletely understood. YAP forms biomolecular condensates in response to hyperosmotic stress, concentrating transcription-related factors to activate downstream target genes. However, whether YAP forms condensates under other signals, how YAP condensates organize and function, and how YAP condensates activate transcription in general are unknown. Here, we report that endogenous YAP forms sub-micron scale condensates in response to Hippo pathway regulation and actin cytoskeletal tension. The transcription factor TEAD1 actively stabilizes YAP condensates, which also recruit BRD4, a coactivator that is enriched at active enhancers. Using single molecule tracking, we found that YAP condensates slowed YAP diffusion within condensate boundaries, a possible mechanism for promoting YAP target search. These results reveal that YAP condensate formation is a highly regulated process that is critical for YAP/TEAD target gene expression.

cell biology↗

Hidden structure in disordered proteins is adaptive to intracellular changes

Intrinsically disordered proteins and protein regions (IDPs) are essential to cellular function in all proteomes. Unlike folded proteins, IDPs exist in an ensemble of rapidly interchanging conformations. IDP sequences encode interactions that create structural biases within the ensemble. Such structural biases determine the three-dimensional shape of IDP ensembles and can affect their activity. However, the plasticity and sensitivity of IDP ensembles means structural biases, often measured in vitro, may differ in the dynamic and heterogeneous intracellular environment. Here we reveal that structural biases found in vitro in well-studied IDPs persist inside human-derived cells. We further show that a subset of IDPs are able to sense changes in cellular physical-chemical composition and modulate their ensemble in response. We propose that IDP ensembles can evolve to sense and respond to intracellular physicochemical changes, or to resist them. This property can be leveraged for biological function, be the underlying cause of IDP-driven pathology, or be leveraged for the design of disorder-based biosensors and actuators.

biophysics↗

Molecular Swiss Army Knives: Tardigrade CAHS Proteins Mediate Desiccation Tolerance Through Multiple Mechanisms

Tardigrades, also known as water bears, make up a phylum of small but extremely hardy animals, renowned for their ability to survive extreme stresses, including desiccation. How tardigrades survive desiccation is one of the enduring mysteries of animal physiology. Here we show that CAHS D, an intrinsically disordered protein belonging to a unique family of proteins possessed only by tardigrades, undergoes a liquid-to-gel phase transition in a concentration dependent manner. Unlike other gelling proteins, such as gelatin, our data support a mechanism in which gel formation of CAHS D is driven by intermolecular {beta}-{beta} interactions. We find that gel formation corresponds with strong coordination of water and slowing of water diffusion. The degree of water coordination correlates with the ability of CAHS D to protect lactate dehydrogenase from unfolding when dried. This implies that the mechanism for unfolding protection can be attributed to a combination of hydration and slowed molecular motion. Conversely, rapid diffusion leading to efficient molecular shielding appears to be the predominant mechanism preventing protein aggregation. Our study demonstrates that distinct mechanisms are required for holistic protection during desiccation, and that protectants, such as CAHS D, can act as molecular Swiss Army Knives capable of providing protection through several different mechanisms simultaneously.

biophysics↗

Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells

Cell homeostasis is perturbed when dramatic shifts in the external environment cause the physical-chemical properties inside the cell to change. Methods that dynamically monitor these intracellular effects are currently lacking. Here, we leveraged the environmental sensitivity and structural plasticity of intrinsically disordered regions (IDRs) to develop a FRET biosensor capable of monitoring rapid intracellular changes caused by osmotic stress. The biosensor, named SED1, utilizes the Arabidopsis intrinsically disordered AtLEA4-5 protein expressed in plants under water deficit. Computational modeling and in vitro studies reveal that SED1 is highly sensitive to macromolecular crowding. SED1 exhibits large and near-linear osmolarity-dependent changes in FRET inside living bacteria, yeast, plant, and human cells, demonstrating the broad utility of this tool for studying water-associated stress. This study demonstrates the remarkable ability of IDRs to sense the cellular environment across the tree of life and provides a blueprint for their use in environmentally-responsive molecular tools.

cell biology↗

Modeling the Opening SARS-CoV-2 Spike: an Investigation of its Dynamic Electro-Geometric Properties

The recent COVID-19 pandemic has brought about a surge of crowd-sourced initiatives aimed at simulating the proteins of the SARS-CoV-2 virus. A bottleneck currently exists in translating these simulations into tangible predictions that can be leveraged for pharmacological studies. Here we report on extensive electrostatic calculations done on an exascale simulation of the opening of the SARS-CoV-2 spike protein, performed by the Folding@home initiative. We compute the electric potential as the solution of the non-linear Poisson-Boltzmann equation using a parallel sharp numerical solver. The inherent multiple length scales present in the geometry and solution are reproduced using highly adaptive Octree grids. We analyze our results focusing on the electro-geometric properties of the receptor-binding domain and its vicinity. This work paves the way for a new class of hybrid computational and data-enabled approaches, where molecular dynamics simulations are combined with continuum modeling to produce high-fidelity computational measurements serving as a basis for protein bio-mechanism investigations.

biophysics↗