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Covino, R.

Publications and source records attributed to Covino, R..

14 recordsLinked to original sources

Quantifying RNA Folding Equilibria from Unclassified Cryo-EM Particle Images

Functional RNA structures are typically far more dynamic than most proteins solved by cryo-electron microscopy (cryo-EM). Flexible junctions and weak tertiary contacts produce broad conformational ensembles, and cryo-EM particle classification analyses discard unaligned particles, which inherently contain the information needed to quantify such broad ensembles. Here, we infer compositional and conformational distributions from unclassified particle images by Bayesian ensemble reweighting. We tested our approach on the P4-P6 domain of the Tetrahymena thermophila group I intron, a classic model system of Mg2+-dependent RNA folding. While stable monomeric and dimeric states yielded high-resolution reconstructions, analyses of abundant, flexible conformations required Bayesian ensemble inference. Our approach quantitatively captured the Mg2+-dependent folding transition, indicating that cryo-EM can report the abundance of coexisting RNA states in agreement with bulk solution measurements. These results showcase how quantitative studies of RNA folding can be achieved by combining cryo-EM measurements with statistical ensemble-inference tools.

biochemistry↗

Counting particles could give wrong probabilities in Cryo-Electron Microscopy

Cryo-electron microscopy (cryo-EM) experiments take 2D snapshots of individual proteins. In principle, these snapshots contain not only the main biomolecular conformations but also scarcely populated states and rare transitions between intermediates. This makes cryo-EM a powerful tool, not only for investigating the structure of biomolecules at high resolution but also for inferring the entire conformational ensemble distribution. Some recent works have reported conformational state populations by counting particle-images from cryo-EM. We wish to caution the community that these measurements are highly susceptible to noise and should not be relied upon as a precise estimate of the thermodynamic landscape of a biomolecule for understanding its biological function. Here, we demonstrate that the extremely noisy nature of cryo-EM images and uncertainty in the viewing orientations of biomolecules lead to ambiguities when assigning images to structures. If ignored, this ambiguity can introduce inherent bias when determining the populations of conformational states through individual particle assignment. We further show that modeling the conformational probability distribution using the entire image dataset mitigates these biases.

biophysics↗

The Structural Dynamics of IRE1 and its Interaction with Unfolded Peptides

The unfolded protein response (UPR) is a crucial signaling network that preserves endoplasmic reticulum (ER) homeostasis, impacting both health and disease. When ER stress occurs, often due to an accumulation of unfolded proteins in the ER lumen, the UPR initiates a broad cellular program to counteract cytotoxic effects. Inositol-requiring enzyme 1 (IRE1), a conserved ER-bound protein, is a key sensor of ER stress and activator of the UPR. While biochemical studies confirm IRE1s role in recognizing unfolded polypeptides, high-resolution structures showing direct interactions remain elusive. Consequently, the precise structural mechanism by which IRE1 senses unfolded proteins is debated. In this study, we employed advanced molecular modeling and 136,7 s of atomistic molecular dynamics simulations to clarify how IRE1 detects unfolded proteins. Our results demonstrate that IRE1s luminal domain directly interacts with unfolded peptides and reveal how these interactions can stabilize higher-order oligomers. We provide a detailed molecular characterization of unfolded peptide binding, identifying two distinct binding pockets at the dimers center, separate from its central groove. Furthermore, we present high-resolution structures illustrating how BiP associates with IRE1s oligomerization interface, thus preventing the formation of larger complexes. Our structural model reconciles seemingly contradictory experimental findings, offering a unified perspective on the diverse sensing models proposed. We elucidate the structural dynamics of unfolded protein sensing by IRE1, providing key insights into the initial activation of the UPR.

biochemistry↗

Amortized template-matching of molecular conformations from cryo-electron microscopy images using simulation-based inference

AO_SCPLOWBSTRACTC_SCPLOWBiomolecules undergo conformational changes to perform their function. Cryo-electron microscopy (cryo-EM) can capture snapshots of biomolecules in various conformations. However, these images are noisy and display the molecule in unknown orientations, making it difficult to separate conformational differences from differences due to noise or projection directions. Here, we introduce cryo-EM simulation-based inference (cryoSBI) to infer the conformations of biomolecules and the uncertainties associated with the inference from individual cryo-EM images. CryoSBI builds on simulation-based inference, a combination of physics-based simulations and probabilistic deep learning, allowing us to use Bayesian inference even when likelihoods are too expensive to calculate. We begin with an ensemble of conformations, which can be templates from molecular simulations or modelling, and use them as structural hypotheses. We train a neural network approximating the Bayesian posterior using simulated images from these templates, and then use it to accurately infer the conformations of biomolecules from experimental images. Training is only done once, and after that, it takes just a few milliseconds to make inference on an image, making cryoSBI suitable for arbitrarily large datasets. CryoSBI eliminates the need to estimate particle pose and imaging parameters, significantly enhancing the computational speed in comparison to explicit likelihood methods. We illustrate and benchmark cryoSBI on synthetic data and showcase its promise on experimental single-particle cryo-EM data.

biophysics↗

Single-molecule FRET and molecular dynamics simulations reveal early activation steps of MET receptor by Listeria monocytogenes

The assembly of membrane receptors into signaling complexes is at the origin of key cellular events. Yet, we often lack detailed structural mechanistic understanding. Receptors are embedded into a complex cellular membrane, which defines their dynamics but also complicates their experimental characterizations significantly. Here, we showcase an integrative structural biology approach to investigate the activation mechanism of the human growth factor receptor MET. MET is a receptor tyrosine kinase involved in cell proliferation, migration, and survival. MET is also hijacked by the intracellular pathogen Listeria monocytogenes. Its invasion protein, internalin B (InlB), binds to MET and promotes the formation of a signaling dimer that triggers the internalization of the pathogen. Crystallography had suggested two different 2:2 MET:InlB complexes. Here, we use a combination of structural biology, modeling, molecular dynamics simulations, and in situ single-molecule Forster resonance energy transfer (smFRET) to elucidate the early events in MET activation. Simulations show that InlB binding stabilizes MET in a conformation that promotes dimer formation. smFRET identifies the organization of the in situ signaling dimer, which resembles one of the two crystal structures yet shows differences. Further MD simulations resulted in a refinement of the dimer model, which is in quantitative agreement with smFRET results. We accurately describe the structural dynamics underpinning an important cellular event and introduce a powerful methodological pipeline applicable to studying the activation of other plasma membrane receptors in situ.

biophysics↗

IGF2BP1 phosphorylation regulates ribonucleoprotein condensate formation by impairing low-affinity protein and RNA interactions

The insulin-like growth factor 2 mRNA binding protein (IGF2BP1) is a conserved RNA-binding protein that regulates RNA stability, localization, and translation. IGF2BP1 is part of various ribonucleoprotein (RNP) condensates regulating RNA outputs. However, the mechanism that regulates its assembly into condensates remains unknown. Here we found, using proteomics, that IGF2BP1 phosphorylation at S181 in a disordered linker is regulated in a stress-dependent manner. Phosphomimetic mutations in two disordered linkers, S181E and Y396E, modulated RNP condensate formation by IGF2BP1 without impacting its binding affinity for RNA. Intriguingly, the S181E mutant, which lies in linker 1, impaired IGF2BP1 condensate formation in vitro and in cells, whereas a Y396E mutant in the second linker increased condensate size and dynamics. Structural approaches showed that the first linker binds RNAs nonspecifically through its RGG/RG motif, an interaction weakened in the S181E mutant. Notably, linker 2 interacts with IGF2BP1s folded domains and these interactions were partially impaired in the Y396E mutant. Our data reveal how phosphorylation modulates low affinity interaction networks in disordered linkers to regulate RNP condensate formation.

biochemistry↗

P116 from Mycoplasma is a self-sufficient lipid uptake and delivery machinery

Lipid acquisition and transport are fundamental processes in all organisms. Here, we investigate the lipid uptake and delivery mechanism of the minimal model organism Mycoplasma pneumoniae. We show that the essential protein P116 can transport lipids between liposomes independently and without ATP consumption. Our structural data and molecular dynamics simulations reveal the mechanism by which the N-terminal region of P116 perturbs the membrane, the lipid transfer route, and the regulation of membrane binding by the cargo mass within P116s large hydrophobic cavity. When adequately filled with cargo, P116 undergoes a rapid conformational change that modulates membrane binding. Taken together, our results show that Mycoplasma developed one integrated lipid uptake and delivery machinery that simplifies the complex multi-protein pathways used by higher developed organisms.

molecular biology↗

Stress-induced clustering of the UPR sensor IRE1 is driven by disordered regions within its ER lumenal domain

Upon accumulation of unfolded proteins at the endoplasmic reticulum (ER), IRE1 activates the unfolded protein response (UPR) to restore protein-folding homeostasis. During ER stress, IRE1s ER lumenal domain (LD) drives its clustering on the ER membrane to initiate signaling. How IRE1s LD assembles into high-order oligomers remains largely unknown. By in vitro reconstitution experiments we show that human IRE1 LD forms dynamic biomolecular condensates. IRE1 LD condensates were stabilized when IRE1 LD was tethered to model membranes and upon binding of unfolded polypeptide ligands. Molecular dynamics simulations suggested that weak multivalent interactions are involved in IRE1 LD assemblies. Mutagenesis showed that disordered regions in IRE1 LD control its clustering in vitro and in cells. Importantly, dysregulated clustering led to defects in IRE1 signaling. Our results reveal that membranes and unfolded polypeptides act as scaffolds to assemble dynamic IRE1 condensates into stable, signaling competent clusters.

cell biology↗

Unique Amphipathic α-helix Drives Membrane Insertion and Enzymatic Activity of ATG3

AbstractAutophagosome biogenesis requires a localized perturbation of lipid membrane dynamics and a unique protein-lipid conjugate. Autophagy-related (ATG) proteins catalyze this biogenesis on cellular membranes, but the underlying molecular mechanism remains unclear. Focusing on the final step of the protein-lipid conjugation reaction, ATG8/LC3 lipidation, we show how membrane association of the conjugation machinery is organized and fine-tuned at the atomistic level. Amphipathic -helices in ATG3 proteins (AHATG3) are found to have low hydrophobicity and to be less bulky. Molecular dynamics simulations reveal that AHATG3 regulates the dynamics and accessibility of the thioester bond of the ATG3[~]LC3 conjugate to lipids, allowing covalent lipidation of LC3. Live cell imaging shows that the transient membrane association of ATG3 with autophagic membranes is governed by the less bulky- hydrophobic feature of AHATG3. Collectively, the unique properties of AHATG3 facilitate protein- lipid bilayer association leading to the remodeling of the lipid bilayer required for the formation of autophagosomes. TeaserWe uncover the unique biophysical property of amphipathic -helix essential for autophagy

cell biology↗

The evolutionary making of SARS-CoV-2

A mechanistic understanding of how SARS-CoV-2 (sarbecovirus, betacoronavirus) infects human cells is emerging, but the evolutionary trajectory that gave rise to this pathogen is poorly understood. Here we scan SARS-CoV-2 protein sequences in-silico for innovations along the evolutionary lineage starting with the last common ancestor of coronaviruses. SARS-CoV-2 substantially differs from viruses outside sarbecovirus both in its set of encoded proteins and in their domain architectures, indicating divergent functional demands. Within sarbecoviruses, sub-domain level profiling using predicted linear epitopes reveals how the primary interface between host cell and virus, the spike, was gradually reshaped. The only epitope that is private to SARS-CoV-2 overlaps with the furin cleavage site, a "switch" that modulates spikes conformational landscape in response to host-cell interaction. This cleavage site has fundamental relevance for both immune evasion and cell infection, and the apparently ongoing evolutionary fine-tuning of its use by SARS-CoV-2 should be monitored.

evolutionary biology↗

Map of SARS-CoV-2 spike epitopes not shielded by glycans.

The severity of the COVID-19 pandemic, caused by the SARS-CoV-2 coronavirus, calls for the urgent development of a vaccine. The primary immunological target is the SARS-CoV-2 spike (S) protein. S is exposed on the viral surface to mediate viral entry into the host cell. To identify possible antibody binding sites not shielded by glycans, we performed multi-microsecond molecular dynamics simulations of a 4.1 million atom system containing a patch of viral membrane with four full-length, fully glycosylated and palmitoylated S proteins. By mapping steric accessibility, structural rigidity, sequence conservation and generic antibody binding signatures, we recover known epitopes on S and reveal promising epitope candidates for vaccine development. We find that the extensive and inherently flexible glycan coat shields a surface area larger than expected from static structures, highlighting the importance of structural dynamics in epitope mapping.Competing Interest StatementThe authors have declared no competing interest.View Full Text

biophysics↗

In situ structural analysis of SARS-CoV-2 spike reveals flexibility mediated by three hinges

The spike (S) protein of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is required for cell entry and is the major focus for vaccine development. We combine cryo electron tomography, subtomogram averaging and molecular dynamics simulations to structurally analyze S in situ. Compared to recombinant S, the viral S is more heavily glycosylated and occurs predominantly in a closed pre-fusion conformation. We show that the stalk domain of S contains three hinges that give the globular domain unexpected orientational freedom. We propose that the hinges allow S to scan the host cell surface, shielded from antibodies by an extensive glycan coat. The structure of native S contributes to our understanding of SARS-CoV-2 infection and the development of safe vaccines. The large scale tomography data set of SARS-CoV-2 used for this study is therefore sufficient to resolve structural features to below 5 [A]ngstrom, and is publicly available at EMPIAR-10453.

molecular biology↗

Systematic cysteine-crosslinking in native membranes establishes the transmembrane architecture in Ire1 clusters

The endoplasmic reticulum (ER) is a key organelle of membrane biogenesis and crucial for the folding of both membrane and secretory proteins. Sensors of the unfolded protein response (UPR) monitor the unfolded protein load in the ER and convey effector functions for maintaining ER homeostasis. Aberrant compositions of the ER membrane, referred to as lipid bilayer stress, are equally potent activators of the UPR. How the distinct signals from lipid bilayer stress and unfolded proteins are processed by the conserved UPR transducer Ire1 remains unknown. Here, we have generated a functional, cysteine-less variant of Ire1 and performed systematic cysteine crosslinking experiments in native membranes to establish its transmembrane architecture in signaling-active clusters. We show that the transmembrane helices of two neighboring Ire1 molecules adopt an X-shaped configuration independent of the primary cause for ER stress. This suggests that different forms of stress converge in a common, signaling-active transmembrane architecture of Ire1. SummaryThe endoplasmic reticulum (ER) is a hotspot of lipid biosynthesis and crucial for the folding of membrane and secretory proteins. The unfolded protein response (UPR) controls the size and folding capacity of the ER. The conserved UPR transducer Ire1 senses both unfolded proteins and aberrant lipid compositions to mount adaptive responses. Using a biochemical assay to study Ire1 in signaling-active clusters, Vath et al. provide evidence that the neighboring transmembrane helices of clustered Ire1 form an X irrespectively of the primary cause of ER stress. Hence, different forms of ER stress converge in a common, signaling-active transmembrane architecture of Ire1.

biochemistry↗

The molecular recognition of phosphatidic acid by an amphipathic helix in Opi1

A key event in cellular physiology is the decision between membrane biogenesis and fat storage. Phosphatidic acid (PA) is an important lipid intermediate and signaling lipid at the branch point of these pathways and constantly monitored by the transcriptional repressor Opi1 to orchestrate lipid metabolism. Here, we report on the mechanism of membrane recognition by Opi1 and identify an amphipathic helix (AH) for the selective binding to membranes containing PA over phosphatidylserine (PS). The insertion of the AH into the hydrophobic core of the membrane renders Opi1 sensitive to the lipid acyl chain composition as an important factor contributing to the regulation of membrane biogenesis. Based on these findings, we rationally designed the membrane binding properties of Opi1 to control its responsiveness in the physiological context. Using extensive molecular dynamics (MD) simulations, we identified two PA-selective three-finger grips that tightly bind the phosphate headgroup, while interacting less intimately and more transiently with PS. This work establishes lipid headgroup selectivity as a new feature in the family of AH-containing membrane property sensors.

biochemistry↗