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Kamerlin, S. C. L.

Publications and source records attributed to Kamerlin, S. C. L..

14 recordsLinked to original sources

Nucleotide-binding motifs nucleated folding of the first enzymes

The earliest stages of protein evolution remain a mystery: the nature of the first protein forms, their roles in emergent biological systems, and the forces that shaped them are largely unknown. Here, we combine insights from metabolic modelling, the organization of protein structure space, and protein folding mechanisms to probe the emergence of two ubiquitous cofactor- binding folds: Rossmanns and P-loop NTPases. While both folds are essential for contemporary life, we show that Rossmanns catalyze reactions deeper within the metabolic core and are more central in structure space than P-loop NTPases. Folding mechanism analysis further reveals that, whereas P-loop NTPases may require non-local interactions to fold, Rossmann folding can be nucleated by a structural module at the heart of the fold that contains a nucleotide-binding motif. Because this motif also directly mediates biochemical activity, this result suggests how early proteins may have compactly satisfied both folding and biochemical activity. Our results imply that folding constraints favored early enzymatic forms with compact binding motifs and modest catalytic roles. We conclude that the early emergence of the Rossmann fold reflects the chemical and physical constraints of protein folding, explaining both its profound antiquity and sustained longevity.

biochemistry↗

Full-Atom MPNN Based Redesign of Plant Dehydrogenase Enables Thermostability Enhancement Without Loss of Stereoselectivity

Protein stabilization is a "Holy Grail" of biocatalysis, and stability design is an area of intense research interest. While it is increasingly feasible to effectively increase enzyme thermostability, optimization without compromising activity or selectivity remains a significant challenge. Here, we use full-atom protein sequence design with sidechain conditioning (FAMPNN) to engineer thermostable variants of the borneol dehydrogenase from Salvia rosmarinus (SrBDH1), an enzyme from a family where unselective enzymes dominate, and selectivity is determined by dynamical considerations. By combining FAMPNN design with residue conservation analysis and avoiding active site residues, we were able to computationally design SrBDH1 variants with up to 10 {degrees}C enhanced thermostability and strongly increased half-life time at elevated temperature, while retaining selectivity towards (+)-borneol. This design framework, integrating de novo and physics-based protein design tools, demonstrates that stability can be enhanced without disrupting functionally relevant dynamics, providing a route to engineer robust and selective biocatalysts. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=198 SRC="FIGDIR/small/719482v1_ufig1.gif" ALT="Figure 1"> View larger version (97K): org.highwire.dtl.DTLVardef@1a35073org.highwire.dtl.DTLVardef@f6c56dorg.highwire.dtl.DTLVardef@11b965forg.highwire.dtl.DTLVardef@2d6eef_HPS_FORMAT_FIGEXP M_FIG Graphical Abstract C_FIG

biochemistry↗

Cancer-Causing Mutations Alter the Interplay Between Loop Dynamics and Catalysis in the Protein Tyrosine Phosphatases SHP-1 and SHP-2

The protein tyrosine phosphatases (PTPs) SHP-1 and SHP-2 play complex roles in a variety of signaling pathways, including those involved in cancers and other diseases, making them important drug targets. These two PTPs have superimposable active sites, but different biological functions in vivo, including opposing roles in cancer development. Unique to these PTPs is the presence of two tandem Src homology 2 (SH2) domains, which regulate access to the phosphate binding site in the catalytic domain, through an autoinhibition mechanism. Studies of the allosteric regulation and dynamics of these PTPs, as well as associated drug discovery efforts, typically focus on autoinhibition rather than the dynamics of a catalytic loop in the phosphatase domain, the WPD-loop, which is essential for PTPase activity. However, recent deep mutational scanning data has demonstrated that oncogenic mutations also regulate WPD-loop motion in SHP-2. We provide here a detailed computational study of WPD-loop dynamics and catalysis in wild-type and mutant full-length and truncated (catalytic domain only) SHP-1 and SHP-2, demonstrating that many oncogenic residues lie on the allosteric pathways regulating WPD-loop dynamics. Mutations at these positions alter WPD-loop dynamics, disrupting the active site and negatively impacting catalysis. Further, our simulations provide molecular insight into the link between the presence of the SH2 domains and loop motion in the catalytic domain, and, importantly, how it differs between the two PTPs. Taken together, our work showcases the impact of altered WPD-loop motion in oncogenic SHP-1 and SHP-2 variants, opening new strategies for selectively targeting these important therapeutic enzymes.

biochemistry↗

Minimal Perturbation of Activation Loop Dynamics Rewires KinaseSignaling

Enzymes are central to life, with their catalytic activity often shaped by the dynamic conformations of regulatory loops. In hub enzymes such as tyrosine kinases, the activation loop critically controls substrate specificity, catalytic efficiency, and downstream signaling, shaping cellular fate. Yet, the molecular mechanisms by which loop dynamics encode these functions remain incompletely understood. Here, we used SRC kinase as a model to dissect how minimal perturbations of the activation loop reprogram kinase behavior. By generating and characterizing multiple variants, we identified a triple-deletion mutant with altered loop dynamics. Structural and biochemical analyses revealed that this variant explores distinct loop conformations and exhibits a subtle shift in substrate preference toward more acidic motifs. These fine-tuned conformational changes translated into specific cellular signaling outcomes, as demonstrated by phosphoproteomic profiling. Comparative analysis across species further showed that nature exploits similar loop remodeling strategies to modulate kinase function. Together, our findings provide a blueprint for rationally tuning kinase activity and offer a generalizable framework for rewiring signaling pathways in diverse cellular contexts.

biochemistry↗

Conformational Dynamics and Catalytic Backups in a Hyper-Thermostable Engineered Archaeal Protein Tyrosine Phosphatase

Protein tyrosine phosphatases (PTPs) are a family of enzymes that play important roles in regulating cellular signaling pathways. The activity of these enzymes is regulated by the motion of a catalytic loop that places a critical conserved aspartic acid side chain into the active site for acid-base catalysis upon loop closure. These enzymes also have a conserved phosphate binding loop that is typically highly rigid and forms a well-defined anion binding nest. The intimate links between loop dynamics and chemistry in these enzymes make PTPs an excellent model system for understanding the role of loop dynamics in protein function and evolution. In this context, archaeal PTPs, which have evolved in extremophilic organisms, are highly understudied, despite their unusual biophysical properties. We present here an engineered chimeric PTP (ShufPTP) generated by shuffling the amino acid sequence of five extant hyperthermophilic archaeal PTPs. Despite ShufPTPs high sequence similarity to its natural counterparts, ShufPTP presents a suite of unique properties, including high flexibility of the phosphate binding P-loop, facile oxidation of the active site cysteine, mechanistic promiscuity, and most notably, hyperthermostability, with a denaturation temperature likely >130 {degrees}C (>8 {degrees}C higher than the highest recorded growth temperature of any archaeal strain). Our combined structural, biochemical, biophysical and computational analysis provides insight both into how small steps in evolutionary space can radically modulate the biophysical properties of an enzyme, and showcase the tremendous potential of archaeal enzymes for biotechnology, to generate novel enzymes capable of operating under extreme conditions. Table of Contents Graphic O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=68 SRC="FIGDIR/small/645524v3_ufig1.gif" ALT="Figure 1"> View larger version (22K): org.highwire.dtl.DTLVardef@186bfccorg.highwire.dtl.DTLVardef@19a265borg.highwire.dtl.DTLVardef@14c526corg.highwire.dtl.DTLVardef@1b75920_HPS_FORMAT_FIGEXP M_FIG C_FIG

biochemistry↗

High-efficiency Kemp eliminases by complete computational design

We present a fully computational workflow for de novo design of efficient enzymes using backbone fragments from natural proteins and without recourse to iterative experimental optimization. The best designed Kemp eliminase exhibits >140 mutations from any natural protein, high stability (>85 {degrees}C) and unprecedented catalytic efficiency (12,700 M-1s-1), surpassing previous computational designs by two orders of magnitude. We find that mutations both inside and outside the active site contribute synergistically to the high observed activity and stability. Mutation of an aromatic residue used in all prior Kemp eliminase designs increases efficiency to >105 M-1s-1. Our approach addresses critical limitations in design methodology, generating stable, high-efficiency, new-to-nature enzymes in complex folds and enables testing hypotheses on the fundamentals of biocatalysis through a limited experimental effort.

biochemistry↗

Redefining the Limits of Functional Continuity in the Early Evolution of P-Loop NTPases

At the heart of many nucleoside triphosphatases is a conserved sequence motif that binds phosphate. A current model of early enzyme evolution proposes that this 6-8 residue motif could have sparked the emergence of the very first nucleoside triphosphatases - a striking example of evolutionary continuity from simple beginnings, if true. To test whether this provocative evolutionary model holds for the ancient and ubiquitous P-Loop NTPases, the properties of seven disembodied Walker A-derived peptides were extensively characterized by Hamiltonian replica exchange molecular dynamics simulations. Although dynamic flickers of nest-like conformations were observed, significant structural similarity between the situated peptide and its disembodied counterpart was not detected - even in the presence of orthophosphate or a nucleotide. Simulations suggest that phosphate binding is non-specific, with a slight preference for GTP over orthophosphate. Control peptides with the same amino acid composition but different sequences and situated conformations behaved similarly to the Walker A peptides with respect to conformational dynamics and phosphate binding, revealing no indication that the Walker A sequence is privileged as a disembodied peptide. We conclude that the evolutionary history of the P-Loop NTPase family is unlikely to have started with a disembodied Walker A peptide in an aqueous environment. The limits of evolutionary continuity for this protein family, and the environmental context within which it emerged, must be reconsidered. Finally, we argue that motifs such as the Walker A motif may represent incomplete or fragmentary molecular fossils - the true nature of which have been eroded by time. Significance StatementThe first proteins were undoubtedly small, but when did those seeds emerge, and what did they look like? It is widely believed that the Walker A P-loop motif is a seed for the emergence of phosphate binding proteins, snugly binding phosphate in a structurally conserved nest. We probe this hypothesis through detailed computational characterization of disembodied Walker A and control peptides, showing that any nest formation is transient, and phosphate binding is weak and non-specific. Thus, we do not find structural continuity represented in the conserved Walker A motif, and current models of early P-loop evolution require revision. Further, care is required when interpreting highly conserved sequence fragments more broadly, as these may merely represent eroded molecular fossils.

biophysics↗

Conformational modulation of a mobile loop controls catalysis in the (βα)8-barrel enzyme of histidine biosynthesis HisF

The overall significance of loop motions for enzymatic activity is generally accepted. However, it has largely remained unclear whether and how such motions can control different steps of catalysis. We have studied this problem on the example of the mobile active site {beta}11-loop (loop1) of the ({beta})8-barrel enzyme HisF, which is the cyclase subunit of imidazole glycerol phosphate synthase. Loop1 variants containing single mutations of conserved amino acids showed drastically reduced rates for the turnover of the substrates N-[(5-phosphoribulosyl) formimino]-5-aminoimidazole-4-carboxamide ribonucleotide (PrFAR) and ammonia to the products imidazole glycerol phosphate (ImGP) and 5-aminoimidazole-4-carboxamide-ribotide (AICAR). A comprehensive mechanistic analysis including stopped-flow kinetics, X-ray crystallography, NMR spectroscopy, and molecular dynamics simulations detected three conformations of loop1 (open, detached, closed) whose populations differed between wild-type HisF and functionally affected loop1 variants. Transient stopped-flow kinetic experiments demonstrated that wt-HisF binds PrFAR by an induced-fit mechanism whereas catalytically impaired loop1 variants bind PrFAR by a simple two-state mechanism. Our findings suggest that PrFAR-induced formation of the closed conformation of loop1 brings active site residues in a productive orientation for chemical turnover, which we show to be the rate-limiting step of HisF catalysis. After the cyclase reaction, the closed loop conformation is destabilized, which favors the formation of detached and open conformations and hence facilitates the release of the products ImGP and AICAR. Our data demonstrate how different conformations of active site loops contribute to different catalytic steps, a finding that is presumably of broad relevance for the reaction mechanisms of ({beta})8-barrel enzymes and beyond. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=127 SRC="FIGDIR/small/600150v1_ufig1.gif" ALT="Figure 1"> View larger version (24K): org.highwire.dtl.DTLVardef@9c5db4org.highwire.dtl.DTLVardef@1cc090dorg.highwire.dtl.DTLVardef@6646d7org.highwire.dtl.DTLVardef@b4e1f9_HPS_FORMAT_FIGEXP M_FIG C_FIG

biochemistry↗

Catalytic Redundancies and Conformational Plasticity Drives Selectivity and Promiscuity in Quorum Quenching Lactonases

Several enzymes from the metallo-{beta}-lactamase-like family of lactonases (MLLs) degrade N- acyl-L-homoserine lactones (AHLs). In doing so, they play a role in a microbial communication system, quorum sensing, which contributes to pathogenicity and biofilm formation. There is currently great interest in designing quorum quenching (QQ) enzymes that can interfere with this communication and be used in a range of industrial and biomedical applications. However, tailoring these enzymes for specific targets requires a thorough understanding of their mechanisms and the physicochemical properties that determine their substrate specificities. We present here a detailed biochemical, computational, and structural study of the MLL GcL, which is highly proficient, thermostable, and has broad substrate specificity. Strikingly, we show that GcL does not only accept a broad range of substrates but is also capable of utilizing different reaction mechanisms that are differentially used in function of the substrate structure or the remodeling of the active site via mutations. Comparison of GcL to other lactonases such as AiiA and AaL demonstrates similar mechanistic promiscuity, suggesting this is a shared feature across lactonases in this enzyme family. Mechanistic promiscuity has previously been observed in the lactonase/paraoxonase PON1, as well as with protein tyrosine phosphatases that operate via a dual general-acid mechanism. The apparent prevalence of this phenomenon is significant from both a biochemical and an engineering perspective: in addition to optimizing for specific substrates, it is possible to optimize for specific mechanisms, opening new doors not just for the design of novel quorum quenching enzymes, but also of other mechanistically promiscuous enzymes.

biochemistry↗

The N-terminal helix of MarA as a key element in the mechanism of DNA binding

Efflux is one of the mechanisms employed by Gram-negative bacteria to become resistant to routinely used antibiotics. The inhibition of efflux by targeting their regulators is a promising strategy to re-sensitise bacterial pathogens to antibiotics. AcrAB-TolC is the main Resistance-Nodulation-Division efflux pump in Enterobacteriaceae. MarA is an AraC/XylS family global regulator that regulates more than 40 genes related to the antimicrobial resistance phenotype, including acrAB. The aim of this work was to understand the role of the N-terminal helix of MarA in the mechanism of DNA binding. An N-terminal deletion of MarA showed that the N-terminal helix has a role in the recognition of the functional marboxes. By engineering two double cysteine variants of MarA, and combining in vitro electrophoretic mobility assays and in vivo measurements of acrAB transcription with molecular dynamic simulations, it was shown that the immobilization of the N-terminal helix of MarA prevents binding to DNA. This new mechanism of inhibition seems to be universal for the monomeric members of the AraC/XylS family, as suggested by additional molecular dynamics simulations of the two-domain protein Rob. These results point to the N-terminal helix of the AraC/XylS family monomeric regulators as a promising target for the development of inhibitors.

molecular biology↗

A sensor complements the steric gate when DNA polymerase ϵ discriminates ribonucleotides.

The cellular imbalance between high concentrations of ribonucleotides (NTPs) and low concentrations of deoxyribonucleotides (dNTPs), is challenging for DNA polymerases when building DNA from dNTPs. It is currently believed that DNA polymerases discriminate against NTPs through a steric gate model involving a clash between a tyrosine and the 2-hydroxyl of the ribonucleotide in the polymerase active site in B-family DNA polymerases. With the help of crystal structures of a B-family polymerase with a UTP or CTP in the active site, molecular dynamics simulations, biochemical assays and yeast genetics, we have identified a mechanism by which the finger domain of the polymerase sense NTPs in the polymerase active site. In contrast to the previously proposed polar filter, our experiments suggest that the amino acid residue in the finger domain senses ribonucleotides by steric hindrance. Furthermore, our results demonstrate that the steric gate in the palm domain and the sensor in the finger domain are both important when discriminating NTPs. Structural comparisons reveal that the sensor residue is conserved among B-family polymerases and we hypothesize that a sensor in the finger domain should be considered in all types of DNA polymerases.

biochemistry↗

Higher-order epistatic networks underlie the evolutionary fitness landscape of a xenobiotic- degrading enzyme

Characterizing the adaptive landscapes that encompass the emergence of novel enzyme functions can provide molecular insights into both enzymatic and evolutionary mechanisms. Here, we combine ancestral protein reconstruction with biochemical, structural, and mutational analyses to characterize the functional evolution of methyl-parathion hydrolase (MPH), a xenobiotic organophosphate-degrading enzyme. We identify five mutations that are necessary and sufficient for the evolution of MPH from an ancestral dihydrocoumarin hydrolase. In-depth analyses of the adaptive landscapes encompassing this evolutionary transition revealed that a complex interaction network, defined in part by higher-order epistasis, determined the adaptive pathways that were available. By also characterizing the adaptive landscapes in terms of their functional activity towards three other OP substrates, we reveal that subtle differences in substrate substituents drastically alter the enzymes epistatic network by changing its intramolecular interactions. Our work suggests that the mutations function collectively to enable substrate recognition via subtle structural repositioning.

biochemistry↗

Bifunctional Substrate Activation via an Arginine Residue Drives Catalysis in Chalcone Isomerases

Chalcone isomerases are plant enzymes that perform enantioselective oxa-Michael cyclizations of 2'-hydroxy-chalcones into flavanones. An X-ray crystal structure of an enzyme-product complex and molecular dynamics simulations reveal an enzyme mechanism wherein the guanidinium ion of a conserved arginine positions the nucleophilic phenoxide and activates the electrophilic enone for cyclization through Bronsted and Lewis acid interactions. The reaction terminates by asymmetric protonation of the carbanion intermediate syn to the guanidinium. Interestingly, bifunctional guanidine- and urea-based chemical reagents, increasingly used for asymmetric organocatalytic applications, are synthetic counterparts to this natural system. Comparative protein crystal structures and molecular dynamics simulations further demonstrate how two active site water molecules coordinate a hydrogen bond network that enables expanded substrate reactivity for 6'-deox-ychalcones in more recently evolved type-2 chalcone isomerases.

biochemistry↗

Evolution of chalcone isomerase from a non-catalytic ancestor

The emergence of catalysis in a non-catalytic protein scaffold is a rare, unexplored event. Chalcone isomerase (CHI), a key enzyme in plant flavonoid biosynthesis, is presumed to have evolved from a non-enzymatic ancestor related to the widely-distributed fatty-acid binding proteins (FAPs) and a plant protein family with no isomerase activity (CHILs for \"CHI-like\"). Ancestral inference confirmed that CHI evolved from a protein lacking isomerase activity. We also identified four alternative founder mutations, i.e. mutations that individually instated activity, including a mutation that is not phylogenetically traceable. Despite strong epistasis in other cases of protein evolution, CHIs laboratory reconstructed mutational trajectory shows weak epistasis. Thus, enantioselective CHI activity can readily emerge despite a catalytically inactive starting point. X-ray crystallography, NMR, and MD simulations reveal reshaping of the active site toward a productive substrate-binding mode and repositioning of the catalytic arginine that was inherited from the ancestral fatty-acid binding proteins.

biochemistry↗