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Goldman, G.

Publications and source records attributed to Goldman, G..

At least 19 recordsLinked to original sources

Efficient exploration of sequence space enables rapid generation of functional genome editors

The problem of how protein sequences translate into defined functions remains largely unsolved despite decades of progress. New methods to efficiently explore protein sequence space will help to shed light on these sequence-function relationships, particularly for complex protein function. Here, we describe an approach to create novel, functional proteins through the integration of deep mutational scanning, structural analysis, and evolutionary mining within prompts for a generative protein language model (PLM). We demonstrate the utility of this approach with the generation of novel compact RNA-guided nucleases. This approach is highly efficient, resulting in active nucleases with [~]40% sequence divergence relative to natural proteins and activity equivalent to or exceeding by up to [~]3X that of other compact nucleases at multiple endogenous loci in human cells. The approach described here is rapidly deployable and produces new sequences that will serve as scaffolds for further exploration of complex protein functionality, as well as substrates for novel genome engineering applications.

synthetic biology↗

Opportunistic pathogenicity in fungi can transcend species boundaries

Multiple fungal lineages have independently evolved the ability to opportunistically infect humans, imposing a major burden on public health. Opportunistic pathogenicity requires the confluence of pre-existing fungal traits that facilitate host colonization (e.g., the ability to grow at 37{degrees}C) and host immune filters that permit the survival of some colonizers (e.g., inborn errors of immunity). Numerous studies have shown that fungal pathogens can exhibit extensive strain-to-strain variation in the ability to cause disease. Moreover, it is also well established that non-pathogenic fungi can occasionally cause severe infections. Together, these observations raise the question: What differentiates opportunistic fungal pathogens from non-pathogens? To address this empirically, we compared phenotypic, metabolomic, and genomic variation between Aspergillus fumigatus, an organism responsible for more than 300,000 infections per year, and Aspergillus fischeri, a close relative that is not considered clinically relevant. By examining 26 phenotypic traits across 16 representative strains of A. fumigatus and 16 of A. fischeri, we found that infection-relevant traits measured under in vitro monoculture conditions showed species-specific distributions, whereas traits measured under in vitro coculture with murine macrophages overlapped. Strikingly, strains of the two species also overlapped in their virulence profiles in an immunocompromised murine model of pulmonary aspergillosis; three strains of A. fischeri exhibited lethality rates of >50% while two A. fumigatus strains were among the least virulent of all 32 strains tested. Consistent with this overlap, we could not associate virulence variation with the presence of specific genomic elements, phenotypic traits, or secondary metabolites. Our results raise the hypothesis that opportunistic pathogenicity can extend beyond the boundaries of individual species. We propose a conceptual model in which the opportunistic pathogenic potential of any fungal strain is the product of complex interactions among numerous genomic, ecological, and host immunity factors.

evolutionary biology↗

An integrative genomic and chemical similarity approach linking fungal secondary metabolites and biosynthetic gene clusters

Fungi are well known to biosynthesize structurally complex secondary metabolites (SMs) with diverse bioactivities. These fungal SMs are frequently produced by biosynthetic gene clusters (BGCs). Linking SMs to their BGCs is key to understanding their chemical and biological functions. Reasoning that structural similarity of SMs arises from similarities in the genes involved in their biosynthesis, we developed an integrative approach that leverages known BGC-SM pairs to predict global links across SMs and BGCs in fungi. As proof of concept, we systematically interrogated metabolomes and genomes of 16 strains of the filamentous fungus Aspergillus fischeri, detecting a total of 60 metabolites. Of those, we were able to assign 22 to known BGC-SM pairs and propose specific hypotheses for the remaining 38 metabolites. These results suggest that coupling genomic similarity and chemical structure-based similarity is a straightforward and high-throughput approach for linking fungal SMs to their BGCs.

microbiology↗

RAB5c controls the assembly of non-canonical autophagy machinery to promote phagosome maturation and microbicidal function of macrophages

Non-canonical conjugation of ATG8 proteins, including LC3, to single membranes implicates the autophagy machinery in cell functions unrelated to metabolic stress. One such pathway is LC3-associated phagocytosis (LAP), which aids in phagosome maturation and subsequent signaling upon cargo uptake mediated by certain innate immunity-associated receptors. Here, we show that a specific isoform of RAB5 GTPases, the molecular switches controlling early endosome traffic, is necessary for LAP. We demonstrate that RAB5c regulates phagosome recruitment and function of complexes required for phosphatidylinositol-3-phosphate [PI(3)P] and reactive oxygen species (ROS) generation by macrophages. RAB5c facilitates phagosome translocation of the V-ATPase transmembrane core, which is needed for ATG16L1 binding and consequent LC3 conjugation. RAB5c depletion impaired macrophage elimination of the fungal pathogen Aspergillus fumigatus and disruption of the V-ATPase-ATG16L1 axis increased susceptibility in vivo. Therefore, early endosome-to-phagosome traffic is differentially regulated to promote LAP and ROS contributes to resistance against A. fumigatus by effecting LAP. HIGHLIGHTSO_LIRAB5c is required for LC3-associated phagocytosis C_LIO_LIRAB5c finetunes NAPDH oxidase assembly and ROS generation in the phagosome C_LIO_LIRAB5c regulates V-ATPase assembly on the phagosome C_LIO_LIRAB5c and V-ATPase-ATG16L1 axis are required for the killing of A. fumigatus C_LI

immunology↗

A Blueprint of Sex-Specific Neuronal Regulation in the C. elegans Nervous System at Single-Cell Resolution

Sex-specific behaviors are often attributed to differences in neuronal wiring and molecular composition, yet how genetic sex shapes the molecular architecture of the nervous system at the individual neuron level remains unclear. Here, we use single-cell RNA sequencing to profile the transcriptome of sex-shared neurons in adult Caenorhabditis elegans males and hermaphrodites. We uncover widespread molecular dimorphism across the nervous system, including in previously unrecognized neuron-types such as the touch receptors. Neuropeptides and signaling-related genes exhibit strong sex-biased expression, particularly in males, reinforcing the notion that neuropeptides are crucial for diversifying connectome outputs. Despite these differences, neurotransmitter identities remain largely conserved, indicating that functional dimorphism arises through modulatory, not identity-defining, changes. We show that sex-biased expression of neurotransmitter-related genes correlates with bias in outgoing synaptic connectivity and identify regulatory candidates for synaptic wiring, including both shared and sex-specific genes. This dataset provides a molecular framework for understanding how subtle regulatory differences tune conserved circuits to drive sex-specific behaviors.

neuroscience↗

A novel Mannan-specific chimeric antigen receptor M-CAR redirects T cells to interact with Candida spp. hyphae and Rhizopus oryzae spores

Invasive fungal infections (IFIs) are responsible for elevated rates of morbidity and mortality, causing around of 1.5 million deaths annually worldwide. One of the main causative agents of IFIs is Candida albicans, and non-albicans Candida species have emerged as a spreading global public health concernment. Furthermore, COVID-19 has contributed to a boost in the incidence of IFIs, such as mucormycosis, in which Rhizopus oryzae is the most prevalent causative agent. The effector host immune response against IFIs depends on the activity of T cells, which are susceptible to the regulatory effects triggered by fungal virulence factors. The fungal cell wall plays a crucial role as a virulence factor, and its remodeling compromises the development of a specific T-cell response. The redirection of Jurkat T cells to target Candida spp. by recognizing targets expressed on the fungal cell wall can be facilitated using chimeric antigen receptor (CAR) technology. This study generated an M-CAR that contains an scFv with specificity to -1,6 mannose backbone of fungal mannan, and the expression of M-CAR on the surface of modified Jurkat cells triggered a strong activation against Candida albicans (hyphae form), Candida tropicalis (hyphae form), Candida parapsilosis (pseudohyphal form), and Candida glabrata (yeast form). Moreover, M-CAR Jurkat cells recognized Rhizopus oryzae spores, which induced high expression of cell activation markers. Thus, a novel Mannan-specific CAR enabled strong signal transduction in modified Jurkat cells in the presence of Candida spp. or R. oryzae.

bioengineering↗

Enhanced antifungal activity of NK-92 cells against Candida albicans mediated by a mannan-specific chimeric antigen receptor

Chimeric antigen receptors (CARs) offer promising prospects for innovative cell-based therapies against invasive fungal infections such as invasive candidiasis. Here, we have developed four CARs targeting Candida albicans with distinct single-chain variable fragments (scFvs): scFv3-CAR, scFv5-CAR, scFv12-CAR, and scFv{kappa}3-1-CAR. In T cells, scFv5-CAR induced IL-2 expression in response to C. albicans hyphae, while scFv3-CAR and scFv12-CAR did not mediate cell activation against C. albicans. Notably, scFv{kappa}3-1-CAR mediated the strongest cell activation against C. albicans yeast, hyphae, and other clinically relevant Candida species. scFv{kappa}3-1-CAR-NK-92 cells exhibited elevated IFN-{gamma} and CD107a expression, reducing C. albicans viability. NOD scid gamma (NSG) mice treated with scFv{kappa}3-1-CAR-NK-92 cells had reduced C. albicans burden in the kidney 24 hours postinfection. We showed that scFv{kappa}3-1-CAR targets C. albicans mannan but no other glycans in glycan microarray screening analyses. These findings reveal the scFv{kappa}3-1-CAR potential as a therapeutic strategy for treating Candida spp. by modifying peripheral blood mononuclear cells. ImportanceRecent studies on novel immunotherapies, including chimeric antigen receptor (CAR)-T cells, have shown promising results in preclinical models against invasive fungal infections (IFIs). However, the application of CAR technology in natural killer (NK) cells for treating IFIs remains unexplored. NK cells play a key role in early fungal clearance due to their antifungal activity mediated by granzymes, perforins, and the secretion of proinflammatory cytokines. This study is the first to demonstrate the feasibility and efficacy of CAR-modified NK cells targeting Candida spp. We provided proof-of-concept data showing that CAR-expressing NK cells exhibit enhanced activation and antifungal effects against clinically relevant Candida species by targeting mannan in the fungal cell wall. These findings are significant as they open new avenues for developing CAR-NK-based therapies to treat invasive candidiasis - a severe infection with limited treatment options and high mortality rates, particularly in immunocompromised patients.

bioengineering↗

Uncovering differential tolerance to deletions versus substitutions with a protein language model

Deep mutational scanning (DMS) experiments have been successfully leveraged to understand genotype to phenotype mapping, with broad implications for protein engineering, human genetics, drug development, and beyond. To date, however, the overwhelming majority of DMS have focused on amino acid substitutions, excluding other classes of variation such as deletions or insertions. As a consequence, it remains unclear how indels differentially shape the fitness landscape relative to substitutions. In order to further our understanding of the relationship between substitutions and deletions, we leveraged a protein language model to analyze every single amino acid deletion in the human proteome. We discovered hundreds of thousands of sites that display opposing behavior for deletions versus substitutions, i.e. sites that can tolerate being substituted but not deleted, and vice versa. We identified secondary structural elements and sequence context to be important mediators of differential tolerability at these sites. Our results underscore the value of deletion-substitution comparisons at the genome-wide scale, provide novel insights into how substitutions could systematically differ from deletions, and showcase the power of protein language models to generate biological hypotheses in-silico. All deletion-substitution comparisons can be explored and downloaded at https://huggingface.co/spaces/ntranoslab/diff-tol.

bioinformatics↗

Deacetylation by sirtuins is important for Aspergillus fumigatus pathogenesis and virulence

Protein acetylation is a crucial post-translational modification that controls gene expression and a variety of biological processes. Sirtuins, a prominent class of NAD+-dependent lysine deacetylases, serve as key regulators of protein acetylation and gene expression in eukaryotes. In this study, six single knockout strains of fungal pathogen Aspergillus fumigatus were constructed, in addition to a strain lacking all predicted sirtuins (SIRTKO). Phenotypic assays suggest that sirtuins are involved in cell wall integrity, secondary metabolite production, thermotolerance, and virulence. AfsirE deletion resulted in attenuation of virulence, as demonstrated in murine and Galleria infection models. The absence of AfSirE leads to altered acetylation status of proteins, including histones and non-histones, resulting in significant changes in the expression of genes associated with secondary metabolism, cell wall biosynthesis, and virulence factors. These findings encourage testing sirtuin inhibitors as potential therapeutic strategies to combat A. fumigatus infections or in combination therapy with available antifungals.

microbiology↗

Evolutionary origin, population diversity, and diagnostics for a cryptic hybrid pathogen

Cryptic fungal pathogens pose significant identification and disease management challenges due to their morphological resemblance to known pathogenic species while harboring genetic and (often) infection-relevant trait differences. The cryptic fungal pathogen Aspergillus latus, an allodiploid hybrid originating from Aspergillus spinulosporus and an unknown close relative of Aspergillus quadrilineatus within section Nidulantes, remains poorly understood. The absence of accurate diagnostics for A. latus has led to misidentifications, hindering epidemiological studies and the design of effective treatment plans. We conducted an in-depth investigation of the genomes and phenotypes of 44 globally distributed isolates (41 clinical isolates and three type strains) from Aspergillus section Nidulantes. We found that 21 clinical isolates were A. latus; notably, standard methods of pathogen identification misidentified all A. latus isolates. The remaining isolates were identified as A. spinulosporus (8), A. quadrilineatus (1), or A. nidulans (11). Phylogenomic analyses shed light on the origin of A. latus, indicating one or two hybridization events gave rise to the species during the Miocene, approximately 15.4 to 8.8 million years ago. Characterizing the A. latus pangenome uncovered substantial genetic diversity within gene families and biosynthetic gene clusters. Transcriptomic analysis revealed that both parental genomes are actively expressed in nearly equal proportions and respond to environmental stimuli. Further investigation into infection-relevant chemical and physiological traits, including drug resistance profiles, growth under oxidative stress conditions, and secondary metabolite biosynthesis, highlight distinct phenotypic profiles of the hybrid A. latus compared to its parental and closely related species. Leveraging our comprehensive genomic and phenotypic analyses, we propose five genomic and phenotypic markers as diagnostics for A. latus species identification. These findings provide valuable insights into the evolutionary origin, genomic outcome, and phenotypic implications of hybridization in a cryptic fungal pathogen, thus enhancing our understanding of the underlying processes contributing to fungal pathogenesis. Furthermore, our study underscores the effectiveness of extensive genomic and phenotypic analyses as a promising approach for developing diagnostics applicable to future investigations of cryptic and emerging pathogens.

evolutionary biology↗

Integration of spatially opposing cues by a single interneuron guides decision making in C. elegans

The capacity of animals to integrate and respond to multiple hazardous stimuli in the surroundings is crucial for their survival. In mammals, complex evaluations of the environment require large numbers and different subtypes of neurons. The nematode C. elegans avoid hazardous chemicals they encounter by reversing their direction of movement. How does the worms compact nervous system processes the spatial information and directs the change of motion? We show here that a single interneuron, AVA, receives glutamatergic excitatory signals from head sensory neurons and glutamatergic inhibitory signals from the tail sensory neurons. AVA integrates the spatially distinct and opposing cues, whose output instructs the animals behavioral decision. We further find that the differential activation of AVA from the head and tail stems from distinct anatomical localization of inhibitory and excitatory glutamate-gated receptors along the AVA process, and from different threshold sensitivities of the sensory neurons to aversive stimuli. Our results thus uncover a cellular mechanism that mediates spatial computation of nociceptive cues for efficient decision-making in C. elegans.

neuroscience↗

A host defense peptide mimetic, brilacidin, potentiates caspofungin antifungal activity against human pathogenic fungi

A. fumigatus is the main etiological agent of a group of heterogeneous diseases called aspergillosis of which the most lethal form is the invasive pulmonary aspergillosis (IPA). Fungicidal azoles and amphotericin B are the first line defense against A. fumigatus, but fungistatic echinocandins, such as caspofungin (CAS), can be used as salvage therapy for IPA. Here, we screened repurposing libraries and identified several compounds that potentiate CAS activity against A. fumigatus, including the host defense peptide mimetic, brilacidin (BRI). BRI converts CAS into a fungicidal drug and potentiates voriconazole (VOR) against A. fumigatus. BRI increases the ability of both CAS and VOR to control A. fumigatus biofilm growth. BRI depolarizes the A. fumigatus cell membrane leading to disruption of membrane potential. By using a combination of protein kinase inhibitors and screening of a catalytic subunit null mutant library, we identified the mitogen activated protein kinase (MAPK) MpkA and the phosphatase calcineurin as mediators of the synergistic action of BRI. These results suggest the most likely BRI mechanism of action for CAS potentiation is the inhibition of A. fumigatus cell wall integrity (CWI) pathway. BRI potentiates CAS activity against C. albicans, C. auris, and C. neoformans. Interestingly, BRI overcomes the CAS-acquired resistance in both A. fumigatus and C. albicans and the CAS-intrinsic resistance in C. neoformans. BRI also has an additive effect on the activity of posaconazole (POSA) against several Mucorales fungi. Cell toxicity assays and fungal burden studies in an immunosuppressed murine model of IPA showed that BRI combined with CAS is not toxic to the cells and significantly clears A. fumigatus lung infection, respectively. Our results indicate that combinations of BRI and antifungal drugs in clinical use are likely to improve the treatment outcome of IPA and other fungal infections.

microbiology↗

Genome-wide prediction of disease variants with a deep protein language model

Distinguishing between damaging and neutral missense variants is an ongoing challenge in human genetics, with profound implications for clinical diagnosis, genetic studies and protein engineering. Recently, deep-learning models have achieved state-of-the-art performance in classifying variants as pathogenic or benign. However, these models are currently unable to provide predictions over all missense variants, either because of dependency on close protein homologs or due to software limitations. Here we leveraged ESM1b, a 650M-parameter protein language model, to predict the functional impact of human coding variation at scale. To overcome existing technical limitations, we developed a modified ESM1b workflow and functionalized, for the first time, all proteins in the human genome, resulting in predictions for all [~]450M possible missense variant effects. ESM1b was able to distinguish between pathogenic and benign variants across [~]150K variants annotated in ClinVar and HGMD, outperforming existing state-of-the-art methods. ESM1b also exceeded the state of the art at predicting the experimental results of deep mutational scans. We further annotated [~]2M variants across [~]9K alternatively-spliced genes as damaging in certain protein isoforms while neutral in others, demonstrating the importance of considering all isoforms when functionalizing variant effects. The complete catalog of variant effect predictions is available at: https://huggingface.co/spaces/ntranoslab/esm_variants.

bioinformatics↗

Examination of genome-wide ortholog variation in clinical and environmental isolates of the fungal pathogen Aspergillus fumigatus

Aspergillus fumigatus is both an environmental saprobe and an opportunistic human fungal pathogen. Knowledge of genomic variation across A. fumigatus isolates is essential for understanding the evolution of pathogenicity, virulence, and resistance to antifungal drugs. Here, we investigated 206 A. fumigatus isolates (133 clinical and 73 environmental isolates) aiming to identify genes with variable presence across isolates and test whether this variation was related to the clinical or environmental origin of isolates. The PanCore genome of A. fumigatus constitutes 13,085 ortholog groups, of which 7,773 (59.4%) are shared by all isolates (CORE) and 5,312 (40.6%) vary in their gene presence across isolates (ACCESSORY). Despite differences in the distribution of orthologs across all isolates, no significant differences were observed among clinical vs. environmental isolates when accounting for phylogeny. Orthologs that differ in their distribution across isolates tend to occur in low frequency and/or be restricted to specific isolates; thus, the degree of genomic conservation between orthologs of A. fumigatus is high. These results suggest that differences in the distribution of orthologs within A. fumigatus cannot be associated with the clinical or environmental origin of isolates. ImportanceAspergillus fumigatus is a cosmopolitan species of fungi responsible for thousands of cases of invasive disease. Clinical and environmental isolates of A. fumigatus exhibit extensive phenotypic differences, including differences related to virulence and antifungal drug resistance. A comprehensive survey of the genomic diversity present in A. fumigatus and its relationship to the clinical or environmental origin of isolates can contribute to the prediction of the mechanisms of evolution and infection of the species. Our results suggest that there is no significant variation in ortholog distribution between clinical and environmental isolates when accounting for evolutionary history. The work supports the hypothesis that environmental and clinical isolates of A. fumigatus do not differ in their gene contents.

bioinformatics↗

Sex-specific topology of the nociceptive circuit shapes dimorphic behavior in C. elegans

How sexually dimorphic behavior is encoded in the nervous system is poorly understood. Here, we characterize the dimorphic nociceptive behavior in C. elegans and study the underlying circuits, which are composed of the same neurons but are wired differently. We show that while sensory transduction is similar in the two sexes, the downstream network topology markedly shapes behavior. We fit a network model that replicates the observed dimorphic behavior in response to external stimuli, and use it to predict simple network rewirings that would switch the behavior between the sexes. We then show experimentally that these subtle synaptic rewirings indeed flip behavior. Strikingly, when presented with aversive cues, rewired males were compromised in finding mating partners, suggesting that network topologies that enable efficient avoidance of noxious cues have a reproductive "cost". Our results present a deconstruction of the design of a neural circuit that controls sexual behavior, and how to reprogram it.

neuroscience↗

Extensive sequence divergence of non-coding regions between Aspergillus fumigatus, a major fungal pathogen of humans, and its relatives

Invasive aspergillosis is a deadly fungal disease; more than 400,000 patients are infected worldwide each year and the mortality rate can be as high as 50-95%. Of the [~]450 species in the genus Aspergillus only a few are known to be clinically relevant, with the major pathogen Aspergillus fumigatus being responsible for [~]50% of all invasive mold infections. Genomic comparisons of A. fumigatus to other Aspergillus species have historically focused on protein-coding regions. However, most A. fumigatus genes, including those that modulate its virulence, are also present in non-pathogenic close relatives of A. fumigatus. Our hypothesis is that differential gene regulation - mediated through the non-coding regions upstream of genes transcription start sites - contributes to A. fumigatus pathogenicity. To begin testing this, we compared non-coding regions up to 500 base pairs upstream of the first codon of single-copy orthologous genes from the two A. fumigatus reference strains Af293 and A1163 and eight closely related Aspergillus section Fumigati species. We found that non-coding regions showed extensive sequence variation and lack of homology across species. By examining the evolutionary rates of both protein-coding and non-coding regions in a subset of orthologous genes with highly conserved non-coding regions across the phylogeny, we identified 418 genes, including 25 genes known to modulate A. fumigatus virulence, whose non-coding regions exhibit a different rate of evolution in A. fumigatus. Examination of sequence alignments of these non-coding regions revealed numerous instances of insertions, deletions, and other types of mutations of at least a few nucleotides in A. fumigatus compared to its close relatives. These results show that closely related Aspergillus species that vary greatly in their pathogenicity exhibit extensive non-coding sequence variation and identify numerous changes in non-coding regions of A. fumigatus genes known to contribute to virulence.

evolutionary biology↗

Resource Profile and User Guide of the Polygenic Index Repository

Polygenic indexes (PGIs) are DNA-based predictors. Their value for research in many scientific disciplines is rapidly growing. As a resource for researchers, we used a consistent methodology to construct PGIs for 47 phenotypes in 11 datasets. To maximize the PGIs prediction accuracies, we constructed them using genome-wide association studies--some of which are novel--from multiple data sources, including 23andMe and UK Biobank. We present a theoretical framework to help interpret analyses involving PGIs. A key insight is that a PGI can be understood as an unbiased but noisy measure of a latent variable we call the "additive SNP factor." Regressions in which the true regressor is the additive SNP factor but the PGI is used as its proxy therefore suffer from errors-in-variables bias. We derive an estimator that corrects for the bias, illustrate the correction, and make a Python tool for implementing it publicly available.

genomics↗

Multi-Ancestry Meta-Analysis yields novel genetic discoveries and ancestry-specific associations

We present a new method, Multi-Ancestry Meta-Analysis (MAMA), which combines genome-wide association study (GWAS) summary statistics from multiple populations to produce new summary statistics for each population, identifying novel loci that would not have been discovered in either set of GWAS summary statistics alone. In simulations, MAMA increases power with less bias and generally lower type-1 error rate than other multi-ancestry meta-analysis approaches. We apply MAMA to 23 phenotypes in East-Asian- and European-ancestry populations and find substantial gains in power. In an independent sample, novel genetic discoveries from MAMA replicate strongly.

genomics↗