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Dandekar, R.

Publications and source records attributed to Dandekar, R..

11 recordsLinked to original sources

Innate Immune Dysregulation Precedes Clinical Onset in Neuromyelitis Optica

Neuromyelitis optica spectrum disorder (NMOSD) is a disabling inflammatory central nervous system (CNS) disease characterized by pathogenic aquaporin 4 (AQP4) autoantibodies. The biological events that precede clinical onset remain unknown. In a unique longitudinal NMOSD cohort from the U.S. Department of Defense Serum Repository, with samples collected up to 24 years before onset, we applied discovery proteomics (~5,400 proteins), pan-viral antibody profiling (VirScan), and in silico analyses to characterize preclinical NMOSD versus matched healthy controls. Innate immune activation, particularly CXCL1 elevation, was the dominant immunological feature of preclinical NMOSD, preceding onset by ~12.7 years. AQP4-IgG was detectable more than 3 years before onset, while CNS injury markers increased only after disease manifestation. VirScan identified enhanced CMV-specific antibody reactivity following AQP4- IgG seroconversion, and network analyses revealed interactions between NMOSD-associated and CMV-derived proteins. Together, these findings establish a novel multi-hit model of NMOSD, with implications for understanding antibody-mediated autoimmunity more broadly.

immunology↗

Humoral Immune Dysregulation Defines High-Risk Cirrhotic Ascites

Fluid accumulates within serosal cavities in diverse disease states, where it creates biologically active and potentially pathologic niches. How these expanded microenvironments reflect and shape disease biology remains incompletely resolved. Here, we investigated human ascites fluid (n = 118), a hallmark of decompensated cirrhosis, to determine whether signatures of microbial exposure and local host response distinguish outcomes. Cirrhotic ascites was characterized by barrier remodeling, depletion of plasma cell-associated programs, and enrichment of oropharyngeal microbes. Surprisingly, detection of oropharyngeal microbes in ascites was not associated with adverse outcomes. Instead, the ascites of cirrhotic patients with poor outcomes was marked by profound plasma cell depletion and significantly reduced dimeric IgA, despite the presence of antigen-experienced B cells. Together, these findings identify local B cell dysregulation as a previously underappreciated component of cirrhosis-associated immune dysfunction. Impaired local humoral immunity, rather than microbial translocation alone, emerges as a feature of high-risk decompensated cirrhosis.

immunology↗

AEGIS reveals epitope- and clone-resolved convergence of CNS B and T cell autoreactivity in ROHHAD

Autoimmune diseases arise when B and T lymphocytes lose tolerance to self. Yet in most disorders, the underlying molecular determinants, including autoantibodies, epitopes and lymphocyte clones that drive tissue injury remain undefined. Rapid-onset obesity with hypothalamic dysfunction, hypoventilation and autonomic dysregulation (ROHHAD) is a rare and often fatal pediatric neuroendocrine syndrome with strong evidence of antigen-driven paraneoplastic autoimmunity, including association with the intracellular autoantigen ZSCAN1. However, the effector immune circuit and the epitope-level determinants operating within the hypothalamus and brainstem have remained unknown. To address this challenge in ROHHAD and more broadly in autoimmune disease, we developed the Autoimmune Epitope and immunoGlobulin/Immune-receptor identification System (AEGIS), an integrated framework that links immune repertoires to their cognate self-epitopes. AEGIS combines B cell and T cell receptor profiling from sites of tissue injury with high-resolution epitope mapping, direct sequencing of antigen-specific autoantibodies, in silico antibody-antigen folding, selection, and T cell antigen discovery. Applied to a deeply phenotyped child with ROHHAD, AEGIS revealed a compartmentalized, clonally restricted immune response in which brain-deposited IgG and expanded cerebrospinal fluid B cell and CD4 T cell clonotypes converged on shared ZSCAN1 epitopes, resolved to minimal determinants and peptide-MHC ligands. These findings provide a clone- and epitope-linked mechanistic map of ROHHAD autoimmunity and establish a generalizable framework for identifying candidate pathogenic clones and antigens across diverse autoimmune diseases.

immunology↗

Autoantibody Repertoires in Healthy Individuals Vary According to HLA Class II Genotype

The link between HLA genotype and the presence of pathogenic autoantibodies has previously been established across different autoimmune disorders. However, the functional process linking specific antibodies to specific HLA remains unclear. Additionally, autoantibodies - usually associated with autoimmune disease - are also present in healthy individuals. To this end, we sought to determine the spectrum of self-antigen antibody specificity (the "autoreactome") in healthy individuals, stratified by HLA genotypes. We utilized Phage ImmunoPrecipitation Sequencing (PhIP-Seq), a programmable phage display for interrogation of antibody specificity, which encompasses over 700,000 peptides tiled across the entire human proteome. Serum from 741 donors without diagnosed autoimmune disease were grouped by their five homozygous HLA-DRB1 genotypes and analyzed for differences in autoreactivity profiles. We applied a custom filter to the PhIP-Seq normalized data and obtained a set of enriched peptides for each HLA-DRB1 genotype. We found that the autoreactome in healthy individuals with different HLA-DRB1 genotypes are generally distinct. Binary logistic regression successfully identified whether a sample belongs to a specific HLA-DRB1 genotype (HLA-DRB1*01, HLA-DRB1*03, HLA-DRB1*04, HLA-DRB1*07, and HLA-DRB1*15) with the following accuracies: 96%, 92%, 90%, 94%, and 90%, and multinomial models predicted HLA-DRB1 genotype with up to 90% accuracy. Finally, gene-level analysis suggests that individuals with specific HLA autoimmune risk alleles may harbor potentially pathogenic autoantibodies in the absence of, or prior to the establishment of, overt disease. Our analysis demonstrates that autoreactivity profiles in healthy people vary according to HLA class II genotype, and may provide insight into the pathological processes associated with development of autoimmune and other immune-mediated diseases.

immunology↗

Permissive central tolerance plus defective peripheral checkpoints licence pathogenic memory B cells in CASPR2-antibody encephalitis

Autoimmunity affects 10% of the population. Within this umbrella, autoantibody-mediated diseases targeting one autoantigen provide a unique opportunity to comprehensively understand the developmental pathway of disease-causing B cells and autoantibodies. While such autoreactivities are believed to be generated during germinal centre reactions, the roles of earlier immune checkpoints in autoantigen-specific B cell tolerance are poorly understood. We address this concept in patients with CASPR2-autoantibody encephalitis and healthy controls. In both groups, comparable and high ([~]0.5%) frequencies of unmutated CASPR2-reactive naive B cells were identified. By contrast, CASPR2-reactive memory B cells were exclusive to patients, and their B cell receptors demonstrated affinity-enhancing somatic mutations with heterogenous binding kinetics. These effector molecules possessed epitope-dependent pathogenic effects in vitro neuronal cultures and in vivo. The unmutated common ancestors of these memory B cells showed a distinctive balance between strong CASPR2 reactivity and very limited binding across the remaining human proteome. Our results are the first to propose mechanisms underlying autoantigen-specific tolerance in humans. We identify permissive central tolerance, defective peripheral tolerance and heterogenous autoantibody binding properties as sequential pathogenic steps which licence CASPR2-directed pathology. By leveraging the basic immunobiology, we rationally direct tolerance-restoring approaches in CASPR2-antibody diseases. This paradigm is applicable across autoimmune conditions.

immunology↗

Chronic Viral Reactivation and Associated Host Immune Response and Clinical Outcomes in Acute COVID-19 and Post-Acute Sequelae of COVID-19

Chronic viral infections are ubiquitous in humans, with individuals harboring multiple latent viruses that can reactivate during acute illnesses. Recent studies have suggested that SARS- CoV-2 infection can lead to reactivation of latent viruses such as Epstein-Barr Virus (EBV) and cytomegalovirus (CMV), yet, the extent and impact of viral reactivation in COVID-19 and its effect on the host immune system remain incompletely understood. Here we present a comprehensive multi-omic analysis of viral reactivation of all known chronically infecting viruses in 1,154 hospitalized COVID-19 patients, from the Immunophenotyping Assessment in a COVID-19 Cohort (IMPACC) study, who were followed prospectively for twelve months. We reveal significant reactivation of Herpesviridae, Enteroviridae, and Anelloviridae families during acute stage of COVID-19 (0-40 days post- hospitalization), each exhibiting distinct temporal dynamics. We also show that viral reactivation correlated with COVID-19 severity, demographic characteristics, and clinical outcomes, including mortality. Integration of cytokine profiling, cellular immunophenotyping, metabolomics, transcriptomics, and proteomics demonstrated virus-specific host responses, including elevated pro-inflammatory cytokines (e.g. IL-6, CXCL10, and TNF), increased activated CD4+ and CD8+ T-cells, and upregulation of cellular replication genes, independent of COVID-19 severity and SARS-CoV-2 viral load. Notably, persistent Anelloviridae reactivation during convalescence ([≥]3 months post-hospitalization) was associated with Post-Acute Sequelae of COVID-19 (PASC) symptoms, particularly physical function and fatigue. Our findings highlight a remarkable prevalence and potential impact of chronic viral reactivation on host responses and clinical outcomes during acute COVID-19 and long term PASC sequelae. Our data provide novel immune, transcriptomic, and metabolomic biomarkers of viral reactivation that may inform novel approaches to prognosticate, prevent, or treat acute COVID- 19 and PASC.

immunology↗

Antigen-Specific T Cell Receptor Discovery for Treating Progressive Multifocal Leukoencephalopathy

BackgroundProgressive multifocal leukoencephalopathy (PML) is a frequently fatal disease of the central nervous system caused by JC virus (JCV). Survival is dependent on early diagnosis and ability to re-establish anti-viral T cell immunity. Adoptive transfer of polyomavirus-specific T cells has shown promise; however, there are no readily available HLA-matched anti-viral T cells to facilitate rapid treatment. ObjectiveIdentify epitopes of the JCV major capsid protein VP1 that elicit an immune response in the context of human leukocyte antigen allele A*02:01 (HLA-A2) and isolate cognate T cell receptors (TCRs) from healthy donors. Evaluate individual VP1-specific TCRs for their capacity to be expressed in T cells and clear JCV in vitro. MethodsPBMCs from HLA-A2+ healthy donors were stimulated with peptide libraries tiled across the JCV VP1 protein. Multiple rounds of stimulation were performed to identify the antigens that induced the largest expansion and CD8+ T cell response (measured as INF{gamma}, TNF, CD137, and CD69 expression). High-affinity, antigen-specific CD8+ T cells were isolated based on intensity of tetramer binding for downstream single-cell TCR sequencing. Candidate TCRs were selected based on tetramer binding affinity and activation assays. Promising TCRs were introduced into the T cell genome via viral transduction for in vitro validation including peptide-pulsed K562 cells and astrocyte cells, and JCV-infected astrocytes. ResultsFour conserved JCV VP1 epitopes (amino acids 100-108, 251-259, 253-262, and 274-283) presented by HLA-A2 were identified. VP1(100-108) consistently elicited the highest level of IFN-{gamma} production from multiple donors and this peptide is in a highly conserved region of VP1. We next identified fourteen high avidity TCRs specific for VP1(100-108). When virally transduced into primary human T cells, seven of these TCRs demonstrated specific binding to VP1(100-108):HLA-A2 tetramers, and four showed increased IFN-{gamma} response when incubated with peptide. Primary CD8+ T cells expressing two of these TCRs cleared both HLA-A2 positive K562 cells and HLA-A2 positive SVG astrocyte cell line presenting exogenously added VP1 peptide at a range of E:T ratios. In addition, both TCR-transduced T cell populations effectively lysed JCV-infected astrocytes. ConclusionsWe identified JCV VP1 epitopes that are immunogenic in the context of HLA-A2 MHC-I, including epitopes that have not been previously described. The VP1(100-108) epitope was used to isolate HLA-A2-restricted TCRs. When cloned into primary human CD8+ T cells, these TCRs recognized VP1 (100-108)-presenting targets, and the transduced T cells conferred cytotoxic activity and eliminated K562 and astrocyte cells displaying the VP1(100-108) peptide and not sham peptide, as well as JCV-infected astrocytes. Taken together, these data suggest that JCV VP1-specific TCRs could be appealing therapeutics for HLA-A2+ individuals with PML in whom intrinsic T cell immunity cannot be rescued.

neuroscience↗

Antigen-specificity of clonally-enriched CD8+ T cells in multiple sclerosis

CD8+ T cells are the dominant lymphocyte population in multiple sclerosis (MS) lesions where they are highly clonally expanded. The clonal identity, function, and antigen specificity of CD8+ T cells in MS are not well understood. Here we report a comprehensive single-cell RNA-seq and T cell receptor (TCR)-seq analysis of the cerebrospinal fluid (CSF) and blood from a cohort of treatment-naive MS patients and control participants. A small subset of highly expanded and activated CD8+ T cells were enriched in the CSF in MS that displayed high activation, cytotoxicity and tissue-homing transcriptional profiles. Using a combination of unbiased and targeted antigen discovery approaches, MS-derived CD8+ T cell clonotypes recognizing Epstein-Barr virus (EBV) antigens and multiple novel mimotopes were identified. These findings shed vital insight into the role of CD8+ T cells in MS and pave the way towards disease biomarkers and therapeutic targets. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=131 SRC="FIGDIR/small/611010v2_ufig1.gif" ALT="Figure 1"> View larger version (30K): org.highwire.dtl.DTLVardef@1a0b738org.highwire.dtl.DTLVardef@5cf5c2org.highwire.dtl.DTLVardef@10abdccorg.highwire.dtl.DTLVardef@32c7b2_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical SummaryC_FLOATNO Created in BioRender. Sabatino, J. (2024) BioRender.com/e66l598 C_FIG

immunology↗

Uncertainty quantified discovery of chemical reaction systems via Bayesian scientific machine learning

1The recently proposed Chemical Reaction Neural Network (CRNN) discovers chemical reaction pathways from time resolved species concentration data in a deterministic manner. Since the weights and biases of a CRNN are physically interpretable, the CRNN acts as a digital twin of a classical chemical reaction network. In this study, we employ a Bayesian inference analysis coupled with neural ordinary differential equations (ODEs) on this digital twin to discover chemical reaction pathways in a probabilistic manner. This allows for estimation of the uncertainty surrounding the learned reaction network. To achieve this, we propose an algorithm which combines neural ODEs with a preconditioned stochastic gradient langevin descent (pSGLD) Bayesian framework, and ultimately performs posterior sampling on the neural network weights. We demonstrate the successful implementation of this algorithm on several reaction systems by not only recovering the chemical reaction pathways but also estimating the uncertainty in our predictions. We compare the results of the pSGLD with that of the standard SGLD and show that this optimizer more efficiently and accurately estimates the posterior of the reaction network parameters. Additionally, we demonstrate how the embedding of scientific knowledge improves extrapolation accuracy by comparing results to purely data-driven machine learning methods. Together, this provides a new framework for robust, autonomous Bayesian inference on unknown or complex chemical and biological reaction systems.

systems biology↗

High-throughput Interpretation of Killer-cell Immunoglobulin-like Receptor Short-read Sequencing Data with PING

The killer-cell immunoglobulin-like receptor (KIR) complex on chromosome 19 encodes receptors that modulate the activity of natural killer cells, and variation in these genes has been linked to infectious and autoimmune disease, as well as having bearing on pregnancy and transplant outcomes. The medical relevance and high variability of KIR genes makes short-read sequencing an attractive technology for interrogating the region, providing a high-throughput, high-fidelity sequencing method that is cost-effective. However, because this gene complex is characterized by extensive nucleotide polymorphism, structural variation including gene fusions and deletions, and a high level of homology between genes, its interrogation at high resolution has been thwarted by bioinformatic challenges, with most studies limited to examining presence or absence of specific genes. Here, we present the PING (Pushing Immunogenetics to the Next Generation) pipeline, which incorporates empirical data, novel alignment strategies and a custom alignment processing workflow to enable high-throughput KIR sequence analysis from short-read data. PING provides KIR gene copy number classification functionality for all KIR genes through use of a comprehensive alignment reference. The gene copy number determined per individual enables an innovative genotype determination workflow using genotype-matched references. Together, these methods address the challenges imposed by the structural complexity and overall homology of the KIR complex. To determine copy number and genotype determination accuracy, we applied PING to European and African validation cohorts and a synthetic dataset. PING demonstrated exceptional copy number determination performance across all datasets and robust genotype determination performance. Finally, an investigation into discordant genotypes for the synthetic dataset provides insight into misaligned reads, advancing our understanding in interpretation of short-read sequencing data in complex genomic regions. PING promises to support a new era of studies of KIR polymorphism, delivering high-resolution KIR genotypes that are highly accurate, enabling high-quality, high-throughput KIR genotyping for disease and population studies. Author summaryKiller cell immunoglobulin-like receptors (KIR) serve a critical role in regulating natural killer cell function. They are encoded by highly polymorphic genes within a complex genomic region that has proven difficult to interrogate owing to structural variation and extensive sequence homology. While methods for sequencing KIR genes have matured, there is a lack of bioinformatic support to accurately interpret KIR short-read sequencing data. The extensive structural variation of KIR, both the small-scale nucleotide insertions and deletions and the large-scale gene duplications and deletions, coupled with the extensive sequence similarity among KIR genes presents considerable challenges to bioinformatic analyses. PING addressed these issues through a highly-dynamic alignment workflow, which constructs individualized references that reflect the determined copy number and genotype makeup of a sample. This alignment workflow is enabled by a custom alignment processing pipeline, which scaffolds reads aligned to all reference sequences from the same gene into an overall gene alignment, enabling processing of these alignments as if a single reference sequence was used regardless of the number of sequences or of any insertions or deletions present in the component sequences. Together, these methods provide a novel and robust workflow for the accurate interpretation of KIR short-read sequencing data.

immunology↗

Longitudinally persistent cerebrospinal fluid B-cells resist treatment in multiple sclerosis

B-cells are key contributors to chronic autoimmune pathology in multiple sclerosis (MS). Clonally related B-cells exist in the cerebrospinal fluid (CSF), meninges, and central nervous system (CNS) parenchyma of MS patients. Longitudinally stable CSF oligoclonal band (OCB) antibody patterns suggest some local CNS B-cell persistence; however, the longitudinal B-cell dynamics within and between the CSF and blood remain unknown. We sought to address this by performing immunoglobulin heavy chain variable region repertoire sequencing on B-cells from longitudinally collected blood and CSF samples of MS patients (n=10). All patients were untreated at the time of the initial sampling; the majority (n=7) were treated with immune modulating therapies 1.2 (+/-0.3 SD) years later during the second sampling. We found clonal persistence of B-cells in the CSF of five patients; these B-cells were frequently immunoglobulin (Ig) class-switched and CD27+. We identified specific blood B-cell subsets that appear to provide input into CNS repertoires over time. We demonstrate complex patterns of clonal B-cell persistence in CSF and blood, even in patients on high-efficacy immune modulating therapy. Our findings support the concept that peripheral B-cell activation and CNS-compartmentalized immune mechanisms are in part therapy-resistant.

immunology↗