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van Oijen, A. M.

Publications and source records attributed to van Oijen, A. M..

At least 19 recordsLinked to original sources

Single-molecule visualisation of human Hsp70-driven conformational remodelling during stress

The Hsp70 chaperone system plays a central role in the folding of nascent polypeptides and in preventing protein misfolding and aggregation during cellular stress. However, the precise mechanism by which the human Hsp70, HspA8, remodels the conformations of individual chemically misfolded clients remains unclear. Moreover, it is unknown whether this mechanism differs from that used by Hsp70 to engage clients during heat stress to preserve native function. To address these questions, we report here the use of single-molecule fluorescence resonance energy transfer (smFRET) to temporally interrogate how the human Hsp70 system regulates the conformation of a heat-sensitive client protein, firefly luciferase (Fluc), following chemical denaturation and during heat stress. We find that Hsp70 recognises both chemically denatured and heat-induced misfolded states of Fluc and resolves them by conformational expansion. Release from a Hsp70-bound state, a process driven by the nucleotide exchange factor, Hsp110, guides Fluc toward productive folding trajectories that would otherwise be unlikely to occur spontaneously following collapse from a conformationally unfolded state. Moreover, we demonstrate that both temperature and the conformational state of misfolded Fluc dictate the ability of HspA8 to meaningfully resolve non-native structure within the protein. Collectively, this work provides direct visualisation of the mechanisms by which Hsp70 modulates client conformations under diverse stress conditions to preserve proteome integrity.

biophysics↗

The interplay between supercoiling and DNA modifying enzymes at the single-molecule level

DNA supercoiling refers to the overwinding or underwinding of the double helix, forming plait-like structures called plectonemes. Supercoiling is involved in all biological processes that occur on DNA. Despite this involvement, single-molecule in vitro studies on these processes largely work with relaxed DNA, overlooking the role supercoiling is playing in these processes. We have constructed 18-kb linear DNA substrates that can be tethered to a microscope coverslip at multiple sites, allowing the template to be topologically constrained. We can then use an intercalating dye to induce positive or negative supercoiling, which we can observe at the single-molecule level using TIRF microscopy. We directly visualise plectonemes diffusing along the DNA. However, in the presence of the restriction enzyme EcoRV, plectonemes remain stationary at the EcoRV binding site. We show that EcoRV has an increased cleavage efficiency in the presence of supercoiling, even though its binding efficiency is unaffected. These findings reveal a relationship between DNA topology and the activity of DNA modifying enzymes. We hypothesise that supercoiling makes cleavage more energetically favourable for restriction enzymes that bend DNA. This work reveals the kinetic interplay between supercoiling and enzyme activity, highlighting how DNA itself can modulate the processes that act upon it. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=79 SRC="FIGDIR/small/680164v1_ufig1.gif" ALT="Figure 1"> View larger version (18K): org.highwire.dtl.DTLVardef@1a9890forg.highwire.dtl.DTLVardef@1653ecaorg.highwire.dtl.DTLVardef@1fd7bfcorg.highwire.dtl.DTLVardef@d70357_HPS_FORMAT_FIGEXP M_FIG C_FIG

molecular biology↗

DNA barcoding for parallelised single-molecule characterisation of kinetic phenotypes

Single-molecule techniques provide exceptional resolution of biomolecular dynamics but are limited by low-throughput. We present a barcoding strategy that enables simultaneous kinetic profiling of multiple protein variants at the single-molecule level. Each protein is covalently linked to a unique DNA barcode, decoded via transient hybridisation of fluorescent probes distinguished by colour and binding duration. We applied this method to a library of 16 ClpS variants to systematically explore evolutionary trajectories towards a variant adapted to recognise N-terminal amino acids with binding kinetics optimised for single-molecule peptide sequencing. The approach uncovered [~]5-fold variation in median dissociation rates across variants. Several variants displayed bimodal kinetics, likely reflecting structural subpopulations, and differences in kinetic properties arose primarily from the relative abundance of these phenotypes. This approach offers a general framework for screening and optimising proteins for single-molecule applications, while revealing mechanistic insights that are inaccessible to traditional ensemble methods.

biophysics↗

Competing chaperone pathways in α-synuclein disaggregation and aggregation dynamics

The aggregation of the protein -synuclein into amyloid fibrils and their subsequent deposition into large proteinaceous inclusions is a pathological hallmark of several neurodegenerative diseases, including Parkinsons disease. Molecular chaperones, including the small heat shock proteins (sHsps) and the Hsp70 chaperone system, are known to interact with -synuclein fibrils, preventing further aggregation and disaggregating fibrillar species respectively. However, it remains unclear if sHsps co-operate with the Hsp70 chaperones to potentially improve the kinetics or effectiveness of Hsp70-mediated disaggregation and how disaggregation kinetics are influenced by aggregation-prone -synuclein monomers. Using thioflavin-T assays, we demonstrate that the sHsps Hsp27 (HSPB1) and B-crystallin (HSPB5) do not synergise with the Hsp70 chaperones during -synuclein seed fibril disaggregation. Moreover, the addition of monomeric -synuclein with fibril seeds results in increased aggregation that overwhelms Hsp70-mediated disaggregation. Upon addition of sHsps to this system, antagonism between the two chaperone classes is observed, likely due to these chaperones competing for productive binding to the ends of -synuclein fibrils. Overall, these results suggest that while Hsp70 and sHsp chaperones are independently capable of binding to and inhibiting fibril elongation, they do not have synergistic effects on disaggregation. Furthermore, Hsp70-mediated disaggregation is ineffectual in the presence of physiological concentrations of -synuclein monomers, conditions that actually lead to further -synuclein aggregation. Overall, these data may offer insight into factors that lead to the failure of the Hsp70 chaperones to clear cells of -synuclein aggregates that leads to neurodegenerative disease.

biochemistry↗

Single-molecule visualization of sequence-specific RNA binding by a designer PPR protein

Pentatricopeptide repeat (PPR) proteins are a large family of modular RNA-binding proteins that recognize specific ssRNA target sequences. There is significant interest in developing designer PPRs for use in diagnostics or as tools to detect and localize target RNA sequences. However, it is unclear how PPRs search for target sequences within complex transcriptomes and current models to predict PPR binding sites struggle to reconcile the effects that RNA mismatches and secondary structure have on PPR binding. To address this, we determined the structure of a designer PPR (dPPR10) bound to its target sequence and used two- and three-colour single-molecule FRET to interrogate the mechanism of ssRNA binding to individual PPR proteins in real time. We demonstrate that longer RNA sequences were significantly slower to bind (or could not bind at all) and that this is, in part, due to their propensity to form stable secondary structures that sequester the target sequence from dPPR10. Importantly, dPPR10 does not associate with non-target flanking sequences, binding specifically to its target sequence within longer ssRNA species. This data provides evidence that PPRs have limited to no capacity to scan RNA transcripts for target sequences and instead rely on diffusion for cognate searching. The kinetic constraints imposed by random three-dimensional diffusion may explain the long-standing conundrum of why PPR proteins are abundant in organelles, but almost unknown outside them (i.e. in the cytosol and nucleus). These findings will inform improved prediction of PPR binding sites for the development of designer PPRs. SummaryPentatricopeptide repeat proteins (PPR) are a large family of modular RNA-binding proteins, whereby each module can be designed to bind to a specific ssRNA nucleobase and thus any RNA sequence of interest. As such, there is substantial interest in developing designer PPRs for a range of biotechnology applications, including diagnostics or in vivo localisation of RNA species; however, the mechanistic details regarding how PPRs search for and bind to target sequences is unclear. As such, we combined structure-based and single- molecule approaches and determined that PPRs bind only to their target sequences (i.e., they do not associate with non-target RNA sequences) and do not scan longer RNA oligonucleotides for the target sequence. Instead, target searching appears kinetically-constrained by random three-dimensional diffusion, providing an explanation as to why PPRs are found almost exclusively in organelle compartments that typically have smaller transcriptomes. Collectively, this work identifies several key considerations for future designer PPR developments.

biochemistry↗

Development of a generalisable tryptophan-optimised quenchbody biosensor based on a synthetic nanobody library

Quenchbodies, antibodies labelled with fluorophores that increase in intensity upon antigen binding, offer great promise for biosensor development. Nanobody-based quenchbodies are particularly attractive due to their small size, ease of expression, high stability, rapid evolvability, and amenability to protein engineering. However, existing designs for protein detection show limited dynamic range, with fluorescence increases of only 1.1-1.7 fold. Here we identify the tryptophan residues in the nanobody complementarity-determining regions (CDRs) that are critical to quenchbody performance. Using a combination of rational design and molecular dynamics simulations, we developed an optimised nanobody scaffold with tryptophans introduced at key positions. We used this scaffold in an in vitro directed-evolution screen against human inflammatory cytokine interleukin-6 (IL-6). This yielded quenchbodies with 1.5-2.4-fold fluorescence increases, enabling IL-6 detection down to 2 nM. Our scaffold provides a valuable platform for developing biosensors for diverse protein targets, with applications in research, diagnostics, and environmental monitoring.

bioengineering↗

Single-molecule observations of human small heat shock proteins in complex with aggregation-prone client proteins

Small heat shock proteins (sHsps) are molecular chaperones that act to prevent the aberrant aggregation of misfolded proteins. Whilst it is widely suggested that sHsps prevent aggregation by binding to misfolded client proteins, the dynamic and heterogeneous nature of sHsps has hindered attempts to establish the mechanistic details of how sHsp-client protein complexes form. Single-molecule approaches have emerged as a powerful tool to investigate dynamic and heterogeneous interactions such as those that can occur between sHsps and their client proteins. Here, we use total internal reflection fluorescence microscopy to observe and characterise the complexes formed between model aggregation-prone client proteins [firefly luciferase (FLUC), rhodanese, and chloride intracellular channel 1 protein (CLIC)], and the human sHsps B-crystallin (B-c; HSPB1) and Hsp27 (HSPB5). We show that small (monomeric or dimeric) forms of both B-c and Hsp27 bind to misfolded or oligomeric forms of the client proteins at early stages of aggregation, resulting in the formation of soluble sHsp-client complexes. Stoichiometric analysis of these complexes revealed that additional B-c subunits accumulate onto pre-existing sHsp-client complexes to form larger species - this does not occur to the same extent for Hsp27. Instead, Hsp27-client interactions tend to be more transient than those of B-c. Elucidating these mechanisms of sHsp function is crucial to our understanding of how these molecular chaperones act to inhibit protein aggregation and maintain cellular proteostasis.

molecular biology↗

Spatiotemporal dynamics of single-stranded DNA intermediates in Escherichia coli

Single-stranded DNA gaps form within the E. coli chromosome during replication, repair and recombination. However, information about the extent of ssDNA creation in the genome is limited. To complement a recent whole-genome sequencing study revealing ssDNA gap genomic distribution, size, and frequency, we used fluorescence microscopy to monitor the spatiotemporal dynamics of single-stranded DNA within live E. coli cells. The ssDNA was marked by a functional fluorescent protein fusion of the SSB protein that replaces the wild type SSB. During log-phase growth the SSB fusion produces a mixture of punctate foci and diffuse fluorescence spread throughout the cytosol. Many foci are clustered. Fluorescent markers of DNA polymerase III frequently co-localize with SSB foci, often localizing to the outer edge of the large SSB features. Novel SSB-enriched features form and resolve regularly during normal growth. UV irradiation induces a rapid increase in SSB foci intensity and produces large features composed of multiple partially overlapping foci. The results provide a critical baseline for further exploration of ssDNA generation during DNA metabolism. Alterations in the patterns seen in a mutant lacking RecB function tentatively suggest associations of particular SSB features with the repair of double strand breaks and post-replication gaps.

biophysics↗

Single-molecule visualization of stalled replication-fork rescue by the Escherichia coli Rep helicase

Genome duplication occurs while the template DNA is bound by numerous DNA-binding proteins. Each of these proteins act as potential roadblocks to the replication fork and can have deleterious effects on cells. In Escherichia coli, these roadblocks are displaced by the accessory helicase Rep, a DNA translocase and helicase that interacts with the replisome. The mechanistic details underlying the coordination with replication and roadblock removal by Rep remain poorly understood. Through real-time fluorescence imaging of the DNA produced by individual E. coli replisomes and the simultaneous visualization of fluorescently-labeled Rep, we show that Rep continually surveils elongating replisomes. We found that this association of Rep with the replisome is stochastic and occurs independently of whether the fork is stalled or not. Further, we visualize the efficient rescue of stalled replication forks by directly imaging individual Rep molecules as they remove a model protein roadblock, dCas9, from the template DNA. Using roadblocks of varying DNA-binding stabilities, we conclude that replication restart is the rate-limiting step of stalled replication rescue.

biochemistry↗

Superfast Evolution of Multi-drug Antibiotic Resistance

The killing mechanism of many antibiotics involves the induction of DNA damage, either directly or indirectly, which activates the SOS response. RecA, the master regulator of the SOS response, has shown to play a central role in the evolution of resistance to fluoroquinolones, even after short-term exposure. While this paradigm is well established for DNA-damaging antibiotics, it remains unclear whether {beta}-lactams elicit similar resistance dynamics or depend on RecA and SOS-mediated mechanisms. In this study, we observed a rapid and stable evolution of {beta}-lactam resistance (20-fold MIC increase within 8 hours) in Escherichia coli lacking RecA after a single exposure to ampicillin. Contrary to expectation, this resistance emerged through an SOS-independent mechanism involving two distinct evolutionary forces: increased mutational supply and antibiotic-driven selection. Specifically, we found that RecA deletion impaired DNA repair and downregulated base excision repair pathways, while concurrently repressing the transcription of antioxidative defence genes. This dual impairment led to excessive accumulation of reactive oxygen species (ROS), which in turn promoted the emergence of resistance-conferring mutations. While ampicillin treatment did not alter survival, it selectively enriched for rare mutants arising in the RecA-deficient and ROS-elevated background. Collectively, our findings demonstrate that this oxidative environment, together with compromised DNA repair capacity, increases genetic instability and creates a selective landscape favouring the expansion of resistant clones. These results highlight the repair-redox axis as a key determinant of bacterial evolvability under antimicrobial stress.

microbiology↗

Rapid single-molecule characterisation of nucleic-acid enzymes

The activity of enzymes is traditionally characterised through bulk-phase biochemical methods that only report on population averages. Single-molecule methods are advantageous in elucidating kinetic and population heterogeneity but are often complicated, time consuming, and lacking statistical power. We present a highly generalisable and high-throughput single-molecule assay to rapidly characterise proteins involved in DNA metabolism. The assay exclusively relies on changes in total fluorescence intensity of surface-immobilised DNA templates as a result of DNA synthesis, unwinding or digestion. Combined with an automated data-analysis pipeline, our method provides enzymatic activity data of thousands of molecules in less than an hour. We demonstrate our method by characterising three fundamentally different nucleic-acid enzyme activities: digestion by the phage{lambda} exonuclease, synthesis by the phage Phi29 polymerase, and unwinding by the E. coli UvrD helicase. We observe a previously unknown activity of the UvrD helicase to remove proteins tightly bound to the ends of DNA.

biophysics↗

Defects in DNA double-strand break repair re-sensitise antibiotic-resistant Escherichia coli tomultiple bactericidal antibiotics

Antibiotic resistance is becoming increasingly prevalent amongst bacterial pathogens and there is an urgent need to develop new types of antibiotics with novel modes of action. One promising strategy is to develop resistance-breaker compounds, which inhibit resistance mechanisms and thus re-sensitise bacteria to existing antibiotics. In the current study, we identify bacterial DNA double-strand break repair as a promising target for the development of resistance-breaking co-therapies. We examined genetic variants of Escherichia coli that combined antibiotic-resistance determinants with DNA repair defects. We observed that defects in the double-strand break repair pathway led to significant re-sensitisation towards five bactericidal antibiotics representing different functional classes. Effects ranged from partial to full re-sensitisation. For ciprofloxacin and nitrofurantoin, sensitisation manifested as a reduction in the minimum inhibitory concentration. For kanamycin and trimethoprim, sensitivity manifested through increased rates of killing at high antibiotic concentrations. For ampicillin, repair defects dramatically reduced antibiotic tolerance. Ciprofloxacin, nitrofurantoin, and trimethoprim induce the pro-mutagenic SOS response. Disruption of double-strand break repair strongly dampened the induction of SOS by these antibiotics. Our findings suggest that if break-repair inhibitors can be developed they could re-sensitise antibiotic-resistant bacteria to multiple classes of existing antibiotics and may supress the development of de novo antibiotic-resistance mutations.

microbiology↗

Rapid exchange of stably bound protein and DNA cargo on a DNA origami receptor

Biomolecular complexes can form stable assemblies yet can also rapidly exchange their subunits to adapt to environmental changes. Simultaneously allowing for both stability and rapid exchange expands the functional capacity of biomolecular machines and enables continuous function while navigating a complex molecular world. Inspired by biology, we design and synthesize a DNA origami receptor that exploits multi-valent interactions to form stable complexes that are simultaneously capable of rapid subunit exchange. The system utilizes a mechanism first outlined in the context of the DNA replisome, known as multi-site competitive exchange, and achieves a large separation of time scales between spontaneous subunit dissociation, which requires days, and rapid subunit exchange, which occurs in minutes. In addition, we use the DNA origami receptor to demonstrate stable interactions with rapid exchange of both DNA and protein subunits, thus highlighting the applicability of our approach to arbitrary molecular cargo; an important distinction with canonical toehold exchange between single-stranded DNA. We expect this study to be the first of many that use DNA origami structures to exploit multi-valent interactions for the design and synthesis of a wide range of possible kinetic behaviors.

synthetic biology↗

The E. coli helicase does not use ATP during replication.

The replisome is responsible for replication of DNA in all domains of life, with several of its individual enzyme components relying on hydrolysis of nucleoside triphosphates to provide energy for replisome function. Half a century of biochemical studies have demonstrated a dependence on ATP as an energy source for helicases to unwind duplex DNA during replication. Through single-molecule visualization of DNA replication by the Escherichia coli replisome, we demonstrate that the DnaB helicase does not rely on hydrolysis of ATP (or any ribo-NTPs) in the context of the elongating replisome. We establish that nucleotide incorporation by the leading-strand polymerase is the main motor driving the replication process. One Sentence SummaryPolymerases provide the energy for helicase-mediated DNA unwinding during E. coli DNA replication.

biochemistry↗

Mechanism of transcription modulation by the transcription-repair coupling factor

Elongation by RNA polymerase is dynamically modulated by accessory factors. The transcription-repair coupling factor (TRCF) recognizes distressed RNAPs and either rescues transcription or initiates transcription termination. Precisely how TRCFs choose to execute either outcome remains unclear. With Escherichia coli as a model, we used single-molecule assays to study dynamic modulation of elongation by Mfd, the bacterial TRCF. We found that nucleotide-bound Mfd converts the elongation complex (EC) into a catalytically poised state, presenting the EC with an opportunity to restart transcription. After long-lived residence in this catalytically poised state, ATP hydrolysis by Mfd remodels the EC through an irreversible process leading to loss of the RNA transcript. Further, biophysical studies revealed that the motor domain of Mfd binds and partially melts DNA containing a template strand overhang. The results explain pathway choice determining the fate of the EC and provide a molecular mechanism for transcription modulation by TRCF.

biophysics↗

Highly-parallel, microfluidics-based force spectroscopy on single motor proteins

Cytoskeletal motors transform chemical energy into mechanical work to drive essential cellular functions. Optical trapping experiments have provided crucial insights into the operation of these molecular machines under load. However, the throughput of such force spectroscopy experiments is typically limited to one measurement at a time. Here, we introduce a highly-parallel, microfluidics-based method that allows for rapid collection of force-dependent motility parameters of cytoskeletal motors with two orders of magnitude improvement in throughput compared to currently available methods. We apply tunable hydrodynamic forces to stepping kinesin-1 motors via DNA-tethered beads and utilize a large field of view to simultaneously track the velocities, run lengths and interaction times of hundreds of individual kinesin-1 molecules under varying resisting and assisting loads. Importantly, the 16-m long DNA tethers between the motors and the beads significantly reduces the vertical component of the applied force pulling the motors away from the microtubule. Our approach is readily applicable to other molecular systems and constitutes a new methodology for parallelized single-molecule force studies on cytoskeletal motors.

biophysics↗

An α-cyanostilbene derivative for the enhanced detection and imaging of amyloid fibril aggregates

The aggregation of proteins into amyloid fibrils has been implicated in the pathogenesis of a variety of neurodegenerative diseases, including Alzheimer’s and Parkinson’s disease. Benzothiazole dyes such as Thioflavin T (ThT) are well characterised and widely used fluorescent probes for monitoring amyloid fibril formation. However, existing dyes lack sensitivity and specificity to oligomeric intermediates formed during fibril formation. In this work we describe the use of an α-cyanostilbene derivative with aggregation-induced emission properties (called ASCP) as a fluorescent probe for the detection of amyloid fibrils. Similar to ThT, ASCP is fluorogenic in the presence of amyloid fibrils and upon binding and excitation at 460 nm produces a red-shifted emission with a large Stokes shift of 145 nm. ASCP has a higher binding affinity to fibrillar α-synuclein than ThT and likely shares the same binding sites to amyloid fibrils. Importantly, ASCP was found to also be fluorogenic in the presence of amorphous aggregates and can detect oligomeric species formed early during aggregation. Moreover, ASCP can be used to visualise fibrils via Total Internal Reflection Fluorescence (TIRF) microscopy and, due to its large Stokes shift, simultaneously monitor the fluorescence emission of other labelled proteins following excitation with the same laser used to excite ASCP. Consequently, ASCP possesses enhanced and unique spectral characteristics compared to ThT that make it a promising alternative for the in vitro study of amyloid fibrils and the mechanisms by which they form.Competing Interest StatementThe authors have declared no competing interest.View Full Text

biochemistry↗

Cooperative Chikungunya virus membrane fusion and its sub-stoichiometric inhibition by CHK-152 antibody

Chikungunya virus (CHIKV) presents a major burden on healthcare systems worldwide, but specific treatment remains unavailable. Attachment and fusion of CHIKV to the host cell membrane is mediated by the E1/E2 protein spikes. We used an in vitro single-particle fusion assay to study the effect of the potent, neutralizing antibody CHK-152 on CHIKV binding and fusion. We find that CHK-152 shields the virions, inhibiting interaction with the target membrane and inhibiting fusion. Analysis of the ratio of bound antibodies to epitopes implied that CHIKV fusion is a highly cooperative process. Further, dissociation of the antibody at lower pH results in a finely balanced kinetic competition between inhibition and fusion, suggesting a window of opportunity for the spike proteins to act and mediate fusion even in the presence of antibody.

microbiology↗