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Chandrasekaran, R.

Publications and source records attributed to Chandrasekaran, R..

13 recordsLinked to original sources

Macrocyclic Peptide Tools for Huntingtin-bound HAP40

Huntingtons disease is a fatal neurodegenerative disorder caused by expansion of a cytosine-adenosine-guanine repeat in exon 1 of the Huntingtin (HTT) gene, resulting in a polyglutamine-expanded HTT protein. Although the genetic cause of Huntingtons is well defined, the molecular functions of HTT and the mechanisms linking polyglutamine expansion to neurodegeneration remain incompletely understood. Huntingtin Associated Protein 40 kDa (HAP40) is a key HTT interaction partner that forms a stable complex with HTT and is increasingly recognized as an important player in the HTT structure-function paradigm. However, investigation of HAP40 biology has been limited by a lack of tools capable of directly targeting endogenous protein. Here, we report the discovery and characterization of a panel of nanomolar-affinity macrocyclic peptides targeting HAP40 identified using Random nonstandard Peptide Integrated discovery platform. We characterized macrocycle binding in vitro using surface plasmon resonance, fluorescence polarization, and hydrogen-deuterium exchange mass spectrometry, revealing selective, high-affinity engagement of distinct epitopes on HAP40. We further demonstrate that these macrocycles engage endogenous HAP40 in cellular lysates, enable selective isolation of HAP40-containing protein complexes using macrocycle precipitations and insights into interaction partners of distinct HTT and HAP40 proteoforms. Together, these macrocycles establish a new toolkit for investigating HTT-HAP40 biology and provide a framework for dissecting HAP40-specific functions relevant to Huntingtons disease pathogenesis.

molecular biology↗

Identification and Characterization of a Small Molecule Ligand for the Huntingtin-HAP40 Complex

Huntingtons disease (HD) is caused by a CAG repeat expansion mutation, giving rise to a polyglutamine expansion in the huntingtin (HTT). However, the explicit molecular functions of HTT and opportunities for direct pharmacological modulation remain incompletely understood. Here, we report the discovery of a small molecule ligand for the full-length HTT protein in complex with its partner, HAP40. Using affinity selection mass spectrometry (AS-MS), we identified a stereoselective binder, whose binding was characterized by surface plasmon resonance, hydrogen-deuterium exchange mass spectrometry, and cryo-electron microscopy at 2.3 [A] resolution. The ligand binds HTT-HAP40 in vitro with single-digit micromolar affinity and one-to-one stoichiometry at a druggable interface previously predicted computationally. In silico studies predicted and experimental analyses confirmed the (R)-enantiomer as the eutomer and initial structure activity relationship was established experimentally. This work details a structurally-validated chemical scaffold and highlights a ligandable pocket which could enable development of chemical probes for probing HTT biology, as well as therapeutics such as degraders and imaging agents for HD.

pharmacology and toxicology↗

Development of a dual chemical probe for the USP16 and HDAC6 zinc-finger ubiquitin-binding domain

Ubiquitin-specific peptidase 16 (USP16) is a deubiquitinase that specifically cleaves ubiquitin from histone H2A, and modulates gene expression, cell cycle regulation, and various other cellular processes. The USP16 zinc-finger ubiquitin-binding domain (UBD) binds the free C-terminal end of both ubiquitin and ISG15, two major signaling proteins that mediate many biological pathways. Because the precise function of USP16-UBD and its interactions remains unclear, a small molecule antagonist targeting the USP16-UBD could enable cellular studies to elucidate its biological role. Here we report SGC-UBD1031 (15), a chemical probe targeting USP16-UBD with similar in vitro binding profiles to HDAC6-UBD and selectivity over nine other UBDs. In cellular assays, 15 disrupts the interaction between the C-terminus of ISG15 and USP1-UBD, as well as the interaction between ISG15 and HDAC6 UBD, at a concentration of 1 M. The corresponding enantiomer SGC-UBD1031N (16), does not interfere with these interactions, even at concentrations as high as 30 M, and thus serves as a negative control. Table of Contents graphic O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=117 SRC="FIGDIR/small/684218v2_ufig1.gif" ALT="Figure 1"> View larger version (23K): org.highwire.dtl.DTLVardef@50def6org.highwire.dtl.DTLVardef@15dedc4org.highwire.dtl.DTLVardef@1a50169org.highwire.dtl.DTLVardef@1ffbb4b_HPS_FORMAT_FIGEXP M_FIG C_FIG

molecular biology↗

Candida albicans activates Staphylococcus aureus virulence regulatory systems to drive toxin-mediated human cell death

Co-infection with Staphylococcus aureus and Candida albicans leads to worsened disease severity compared to mono-microbial infection. Because our understanding of the mechanisms driving enhanced disease severity during co-infection is limited, we sought to evaluate how interactions with C. albicans regulate S. aureus virulence towards host cells. We determined that C. albicans enhances S. aureus cytotoxicity towards murine monocytes via a mechanism requiring the Agr system. Agr is a major regulator of S. aureus virulence factors and was previously shown to be activated by C. albicans, but the Agr-regulated virulence factors driving immune cell death are unknown. We identified that enhanced murine monocyte cell death requires the -type phenol soluble modulins and {psi}-hemolysin. Because several S. aureus toxins have species-specific effects, we also tested how co-culture impacts cytotoxicity towards human monocytes. Unexpectedly, we discovered that C. albicans induces robust cytotoxicity of an S. aureus agr mutant ({Delta}agr), which is completely non-toxic towards murine monocytes. Using reporter strains and combinatorial mutants, we identified that co-culture activates the SaeRS regulatory system in S. aureus, and SaeRS is required for human-specific cytotoxicity. We further discovered that the SaeRS-regulated toxin Panton-Valentine Leukocidin (PVL) drives S. aureus {Delta}agr cytotoxicity following co-culture. Finally, we observed similar cytotoxicity phenotypes using both S. aureus and C. albicans clinical isolates, demonstrating broad conservation of this interaction. Interestingly, the magnitude by which C. albicans isolates induce cytotoxicity of S. aureus {Delta}agr varies among strains tested. Overall, this study identifies that C. albicans activates a major S. aureus virulence regulatory system in a typically non-toxic strain, triggering S. aureus to induce potent human-selective cell death.

microbiology↗

Novel monoclonal antibodies against the C-terminal HEAT domain of Huntingtin

BACKGROUNDReliable detection of huntingtin (HTT) is essential for understanding Huntingtons disease (HD) biology and evaluating therapeutic strategies. However, high-quality monoclonal antibodies (mAbs) against the HTT C-terminal domain remain limited. OBJECTIVEWe sought to generate and validate novel monoclonal antibodies targeting the HTT C-terminal HEAT-containing domain to better detect HTT independently of potential effects of polyglutamine length that can impact some N-terminally targeted antibodies. METHODSWe immunized mice with a highly purified, well-characterized recombinant protein corresponding to the HTT C-terminal domain. We generated monoclonal antibody-producing hybridoma cell lines and characterized the antibodies using parental and HTT-knockout cell lines in common immuno-applications. RESULTSThree novel, independent hybridoma lines producing anti-HTT monoclonal antibodies were derived. Using CRISPR-edited HTT knockout cell lines we identified one clone, anti-HTT [2F8], that was specific and effective across Western blot, immunofluorescence, and ELISA assays. All antibodies bound full-length HTT irrespective of HAP40 interaction or polyQ length and showed no cross-reactivity to the N-terminal HEAT domain. CONCLUSIONSThese C-terminal HTT mAbs are thus valuable additional tools for studying endogenous HTT function in both normal and disease contexts.

neuroscience↗

High-Affinity, Structure-Validated and Selective Macrocyclic Peptide Tools for Chemical Biology Studies of Huntingtin

Huntingtons disease (HD) is a fatal neurodegenerative disorder caused by a CAG repeat expansion in the Huntingtin (HTT) gene, with no disease-modifying therapies currently available. The precise molecular function of the HTT protein is unclear, and the lack of selective chemical tools has limited functional studies. We have identified and characterized macrocyclic peptide binders targeting HTT. These binders exhibit low-nanomolar affinity in vitro and engage distinct HTT and HTT-HAP40 interfaces, as revealed by hydrogen-deuterium exchange mass spectrometry and cryo-electron microscopy. Chemoproteomics confirmed selective binding in cell extracts from wildtype but not HTT-null cell lines. HAP40 consistently and stoichiometrically co-purified with HTT across cell lines, including with HTT variants containing different CAG repeat lengths, highlighting the broad presence of the HTT-HAP40 complex. Significance StatementHuntingtin (HTT) is a large, essential protein with conserved roles in development, intracellular trafficking, and protein homeostasis, yet its precise molecular functions remain incompletely defined. Here, we report the first high-affinity, selective, and structurally validated macrocyclic peptide ligands for HTT. These chemical tools bind HTT and its complex with HAP40 across polyglutamine repeat lengths, enabling direct interrogation of HTT structure and function in health and disease contexts. By overcoming longstanding barriers to studying HTT at the molecular level, these ligands open new avenues for discovery in neurobiology, cell biology, and offer opportunities for therapeutic development. This study delivers urgently needed tools to both the Huntingtons disease field and the broader scientific community seeking to understand this elusive and biologically fundamental protein.

biochemistry↗

Challenges and advances for huntingtin detection in cerebrospinal fluid: in support of relative quantification

Huntington disease (HD) is a progressive and devastating neurodegenerative disease caused by expansion of a glutamine-coding CAG tract in the huntingtin (HTT) gene above a critical threshold of [~]35 repeats resulting in expression of mutant HTT (mHTT). A promising treatment approach being tested in clinical trials is HTT lowering, which aims to reduce levels of the mHTT protein. Target engagement of these therapies in the brain are inferred using antibody-based assays to measure mHTT levels in the cerebrospinal fluid (CSF), which is frequently reported as absolute mHTT concentration based on a monomeric protein standard used to generate a standard curve. However, patient biofluids are a complex milieu of different mHTT protein species, suggesting that absolute quantitation is challenging, and a single, recombinant protein standard may not be sufficient to interpret assay signal as molar mHTT concentration. In this study, we used immunoprecipitation and flow cytometry (IP-FCM) to investigate different factors that influence mHTT detection assay signal. Our results show that HTT protein fragmentation, protein-protein interactions, affinity tag positioning, oligomerization and polyglutamine tract length affect assay signal intensity, indicating that absolute HTT quantitation in heterogeneous biological samples is not possible with current technologies using a single standard protein. We also explore the binding specificity of the MW1 anti-polyglutamine antibody, commonly used in these assays as a mHTT-selective reagent and demonstrate that mHTT binding is preferred but not specific. Furthermore, we find that MW1 depletion is not only incomplete, leaving residual mHTT, but also non-specific, resulting in pull down of some wildtype HTT protein. Based on these observations, we recommend that mHTT detection assays report only relative mHTT quantitation using normalized arbitrary units of assay signal intensity, rather than molar concentrations, in the assessment of central nervous system HTT lowering in ongoing clinical and preclinical studies, and that MW1-depletion not be used a method for quantifying wildtype HTT protein.

neuroscience↗

Huntingtin is an RNA-binding protein and participates in NEAT1-mediated paraspeckles

AbstractHuntingtin protein, mutated in Huntington disease, is implicated in nucleic acid- mediated processes, yet evidence for direct huntingtin-nucleic acid interaction is limited. Here we show wildtype and mutant huntingtin co-purify with nucleic acids, primarily RNA, and interact directly with G-rich RNAs in in vitro assays. Huntingtin RNA immunoprecipitation sequencing from patient-derived fibroblasts and neuronal progenitor cells expressing wildtype and mutant huntingtin revealed NEAT1 as a significantly enriched transcript. Altered NEAT1 levels were evident in Huntingtons disease cells and postmortem brain tissues, and huntingtin knockdown decreased NEAT1 levels. Huntingtin co-localized with NEAT1 in paraspeckles, and we identified a high-affinity RNA motif preferred by huntingtin. This study highlights NEAT1 as a novel huntingtin interactor, demonstrating huntingtins involvement in RNA-mediated functions and paraspeckle regulation. One-Sentence SummaryHTT is an RNA-binding protein that interacts with G-rich sequences, including those in the paraspeckle lncRNA NEAT1.

cell biology↗

Expanding the Huntingtons disease research toolbox; validated huntingtin subdomain constructs for biochemical and structural investigation of the huntingtin protein

Huntingtons disease is characterised by CAG expansion in the huntingtin gene above a critical threshold of ~35 repeats, resulting in polyglutamine expansion of the huntingtin protein (HTT). The biological role of wildtype HTT and the associated mechanisms of disease pathology caused by expanded HTT remain incompletely understood, in part, due to challenges characterising interactions between HTT and putative binding partners. Here we describe a biochemical toolkit of rationally designed, high-quality recombinant HTT subdomains; one spanning the N-terminal HEAT and bridge domains (NTD) and the second spanning the C-terminal HEAT domain (CTD). Using biophysical methods and cryo-electron microscopy, we show these smaller subdomains are natively folded and can associate to reconstitute a functional full-length HTT structure capable of forming a near native-like complex with 40 kDa HTT-associated protein (HAP40). We report biotin-tagged variants of these subdomains, as well as full-length HTT, that permit immobilisation of each protein for quantitative biophysical assays without impacting protein quality. We demonstrate the CTD alone can form a stable complex when co-expressed with HAP40, which can be structurally resolved. The CTD-HAP40 complex binds the NTD, with a dissociation constant of approximately 10 nM as measured by bio-layer interferometry. We validate the interaction between the CTD and HAP40 using a luciferase two-hybrid assay and use subdomain constructs to demonstrate their respective stabilization of HAP40 in cells. These open-source biochemical tools will enable the wider HD community to study fundamental HTT biology, discover new macromolecular or small-molecule binding partners and map interaction sites across this very large protein.

biochemistry↗

Molecular engineering of a cryptic epitope in Spike RBD improves manufacturability and neutralizing breadth against SARS-CoV-2 variants

There is a continued need for sarbecovirus vaccines that can be manufactured and distributed in low- and middle-income countries (LMICs). Subunit protein vaccines are manufactured at large scales at low costs, have less stringent temperature requirements for distribution in LMICs, and several candidates have shown protection against SARS-CoV-2. We previously reported an engineered variant of the SARS-CoV-2 Spike protein receptor binding domain antigen (RBD-L452K-F490W; RBD-J) with enhanced manufacturability and immunogenicity compared to the ancestral RBD. Here, we report a second-generation engineered RBD antigen (RBD-J6) with two additional mutations to a hydrophobic cryptic epitope in the RBD core, S383D and L518D, that further improved expression titers and biophysical stability. RBD-J6 retained binding affinity to human convalescent sera and to all tested neutralizing antibodies except antibodies that target the class IV epitope on the RBD core. K18-hACE2 transgenic mice immunized with three doses of a Beta variant of RBD-J6 displayed on a virus-like particle (VLP) generated neutralizing antibodies (nAb) to nine SARS-CoV-2 variants of concern at similar levels as two doses of Comirnaty. The vaccinated mice were also protected from challenge with Alpha or Beta SARS-CoV-2. This engineered antigen could be useful for modular RBD-based subunit vaccines to enhance manufacturability and global access, or for further development of variant-specific or broadly acting booster vaccines.

bioengineering↗

Mapping the Structural Drivers of Insulin Recognition and Specificity Using Molecular Dynamics and Free Energy Calculations

A century on from the discovery of insulin, a complete understanding of insulin interactions with the insulin receptor (IR) at atomic level remains elusive. In this work, we have leveraged recent advancements in structural biology that have resulted in multiple high-resolution structures of the insulin-IR complex. As a first step, we employed molecular dynamics (MD) simulations to unravel atomic insights into the interactions between insulin-IR complexes in order to better understand ligand recognition at the receptor. The MD simulations were followed up with free energy perturbation (FEP) calculations to discriminate between and elucidate the drivers for ligand association for various natural and man-made insulin analogs. As an example, these calculations were utilized to understand the molecular mechanisms that characterized the loss-of-function seen in disease-associated insulin mutations seen in different populations. Further, multiple man-made insulin analogs spanning a range of potencies, mutations, and sequence lengths were studied using FEP and a comprehensive molecular level map of potency determinants were established. [~]85% of FEP calculations captured the direction of shift of potency, and in [~]53% of cases the predictions were within 1 kcal/mol of experiment. The impressive accuracy of FEP in recapitulating functional profiles across such a span of insulin analogs and potency profiles provided clear evidence of its utility in computational mutagenesis. In addition to the impressive accuracy, the ability of FEP to provide a dissected understanding of protein residue, solvent and solvent-mediated contributions to binding energy clearly establishes its utility in the design of novel insulins and peptides in general.

biophysics↗

Germinal center activity and B cell maturation promote protective antibody responses against Plasmodium pre-erythrocytic infection

Blocking Plasmodium, the causative agent of malaria, at the asymptomatic pre-erythrocytic stage would abrogate disease pathology and prevent transmission. Rodent-infectious species of Plasmodium such as P. yoelii (Py) serve as key tools to study vaccine efficacy and disease biology in immune-competent experimental animals. Here we evaluated the differences in vaccine-elicited humoral immunity in two widely used, and vastly diverged, inbred mouse strains, BALB/cJ and C57BL/6J, and identified immunological factors associated with protection. We vaccinated with Py circumsporozoite protein (CSP), the major surface antigen on the sporozoite, and evaluated protective efficacy after mosquito bite challenge. Vaccination achieved 60% sterile protection and otherwise delayed blood stage patency in BALB/cJ mice, whereas; all C57BL/6J mice were infected similar to controls. Interestingly, protection was mediated by antibodies, and could be passively transferred from immunized BALB/cJ mice into naive C57BL/6J. Dissection of the underlying immunological features of protection revealed early deficits in antibody titers and polyclonal avidity in C57BL/6J mice. Additionally, PyCSP-vaccination in BALB/cJ induced a significantly higher proportion of antigen-specific B-cells and class-switched memory B-cell (MBCs) populations than in C57BL/6J mice. Strikingly, C57BL/6J mice also had markedly fewer germinal center experienced, CSP-specific class-switched MBCs compared to BALB/cJ mice. Analysis of the IgG {gamma} chain repertoires by next generation sequencing in PyCSP-specific memory B-cell repertoires also revealed higher somatic hypermutation rates in BALB/cJ mice than in C57BL/6J mice. These findings indicate that BALB/cJ mice achieved higher levels of B cell maturation in response to vaccination with PyCSP, which likely enabled the development of protective antibody responses. Overall, our study indicates that germinal center activity and B cell maturation are key processes in the development of vaccine-elicited protective antibodies against CSP.

immunology↗

Antibody interference by a non-neutralizing antibody abrogates humoral protection against Plasmodium liver stage

Both subunit and attenuated whole sporozoite vaccination strategies against Plasmodium infection have shown promising initial results in malaria-naive westerners but exhibited less efficacy in malaria-exposed individuals in endemic areas. It has been hypothesized that preexisting immunity to malaria represents a significant roadblock to the development of a protective vaccine. Here, we demonstrate proof-of-concept that non-neutralizing antibodies (nNAb) can directly interfere with protective anti-PyCSP humoral responses. We developed and characterized a novel monoclonal antibody, RAM1, against the P. yoelii sporozoite major surface antigen, circumsporozoite protein (CSP). Unlike the canonical PyCSP repeat domain binding and neutralizing antibody (NAb) 2F6, RAM1 does not inhibit sporozoite traversal or entry of hepatocytes in vitro. Though 2F6 and RAM1 bind non-overlapping regions of the CSP-repeat domain, pretreatment with RAM1 abrogated 2F6s capacity to block sporozoite traversal and invasion in vitro. Importantly, RAM1 reduced the efficacy of the polyclonal humoral response against CSP in vivo, paralleling the observed reduced efficacy of RTS,S in malaria-exposed populations. Taken together, our data demonstrate the interference of non-neutralizing antibodies with the efficacy of NAbs and may impact the efficacy of anti-CSP vaccines in malaria-exposed individuals.

immunology↗