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Lund, J. M.

Publications and source records attributed to Lund, J. M..

13 recordsLinked to original sources

TCRdenoise - an unsupervised similarity-based approach for denoising of TCR-pMHC specificity data

Public repositories of T cell receptor (TCR)-peptide-MHC (pMHC) interactions constitute a critical resource for studying adaptive immunity and developing predictive models of TCR specificity. However, recent evidence suggests that a substantial fraction of reported TCR-pMHC interactions may be incorrectly annotated, limiting the quality of downstream analyses and machine learning applications. Here, we present an unsupervised sequence similarity-based framework for denoising peptide-specific TCR repertoires. The method combines pairwise TCR similarity metrics derived from TCRbase and TCRdist3 with hierarchical clustering and a novel adaptation of the silhouette score designed to address the prevalence of singleton clusters and highly imbalanced cluster structures. By incorporating a pseudo-cluster containing singleton and background TCRs, and by optimising both clustering distance thresholds and minimum cluster-size criteria, the proposed approach identifies TCRs likely to represent true antigen-specific binders while filtering putative noise. Using experimentally validated repertoires from TCRvdb, we demonstrate that the modified silhouette score closely tracks clustering solutions that maximise separation between binding and non-binding TCRs, achieving strong agreement with independent validation based on the Matthews correlation coefficient. Extension to a large collection of peptide-specific TCR data revealed a strong negative correlation between the percentage of TCRs classified as noise and the predictive performance of peptide-specific binding models. Further, the denoising classification labels on this data set were corroborated using structural modeling confidence scores of the peptide-TCR interface extracted from a refined AlphaFold 3 modeling pipeline. Additionally, retraining NetTCR on denoised data improved internal cross-validated performance compared with models trained on the full data set, whereas models trained exclusively on TCRs classified as noise performed close to random. Together, these results demonstrate that sequence similarity-based denoising can effectively enrich for biologically meaningful TCR-pMHC interactions and improve the quality of training data for predictive immunological models. The proposed framework provides a scalable strategy for improving the reliability of public TCR databases and facilitating the development of more accurate TCR specificity prediction methods.

bioinformatics↗

Menstruation is associated with cyclical granulysin peaks in vaginal secretions despite stable expression by cervicovaginal immune cells

ProblemThe anti-microbial protein granulysin is present in vaginal secretions during the follicular phase of the menstrual cycle but nearly disappears during the luteal phase. The reason for this change is unknown. Method of studyParticipants (n = 23) with regular menstrual cycles collected daily vaginal swabs for granulysin ELISAs. Endocervical cytobrushes, ectocervical biopsies, vaginal biopsies, and PBMC were collected across the cycle to enumerate granulysin-expressing cells by flow cytometry. Cycle phase was determined by daily urinary luteinizing hormone testing and confirmed by serum progesterone levels. ResultsGranulysin levels in secretions were up to 10,000 times higher during menstruation than during the luteal phase (menstruation, median 3,924 pg/mL [IQR 400-17,280]; luteal, median and IQR undetectable [<7.81 pg/mL]). In the endocervical canal, granulysin-expressing cells were much more abundant during menstruation than during the mid-follicular or mid-luteal phases. In contrast, the number of granulysin-expressing cells in the ectocervix and vagina remained stable during the cycle. The most abundant granulysin-expressing cell types in the mucosa were CD8 T cells and NK cells. In a minority of participants, granulysin was consistently detected in luteal-phase swabs; this phenomenon was associated with parity. ConclusionsGranulysin in vaginal secretions is associated with menstruation and concomitant with a spike in granulysin-expressing cells in the endocervical canal. This result explains the much higher granulysin levels in secretions during the follicular than the luteal phase. In contrast, immune cells from ectocervical and vaginal biopsies express granulysin independently of the menstrual cycle, indicating their continuous ability to respond to microbial infection.

immunology↗

Regulatory T cells restrain IL-15-mediated cytotoxic and bystander T cell activity in mucosal tissue without compromising antigen-driven memory

ABSTRACT/SUMMARYMany pathogenic human infections enter the host via a mucosal surface. These nonlymphoid tissues are abundantly populated by polyclonal memory CD8 T cells that persist following infections for protection upon repeat exposure. Memory T cells can be triggered via T cell receptor recognition of their cognate antigen upon re-infection to exert effector functions, including cytotoxicity and cytokine production, and assist in pathogen elimination. Alternatively, some T cells are bystander activated by cytokines without an antigenic signal. This layered approach boosts efacient pathogen clearance but also poses a threat to host tissues if this response is not properly controlled. Here, we investigate the regulatory mechanisms modulating the tissue memory CD8 T cell response upon recall, leveraging viral rechallenge mouse models to distinguish antigen-driven versus cytokine-activated memory tissue CD8 T cell immunity. We and that regulatory T cells (Treg) participate in restricting cytotoxic and bystander activity without compromising the antigen-driven protective memory CD8 T cell response in mucosal T cells. Critically, Treg provide extrinsic regulation of tissue CD8 T cell cytotoxicity in part through restriction of available IL-2 and IL-15 trans-presentation. Our andings help deane the extrinsic environmental and cellular cues in mucosal tissues that direct tissue-memory CD8 T cells.

immunology↗

Genital herpes shedding episodes associate with alterations in the spatial organization and activation of mucosal immune cells

Herpes Simplex Virus 2 (HSV-2) infection results in variable rates of local viral shedding in anogenital skin. The impact of episodic viral exposures on immune cells in adjacent mucosal tissues, including the genital tract, is unknown. However, any immune responses at this site could impact protective mucosal immunity, tissue homeostasis, and adverse health outcomes. To investigate the impact of HSV-2 on cervicovaginal tract immunity, we applied flow cytometry, immunofluorescent imaging, analysis of soluble immune factors, and spatial transcriptomics to cervicovaginal tissue and blood samples provided by a total of 232 HSV-2 seropositive and seronegative participants, with genital HSV-2 shedding evaluated at the time of biopsy. This unique dataset was used to define and spatially map immune cell subsets and localized gene expression via spatial transcriptomics. HSV-2 seropositivity alone was associated with minimal differences in cervicovaginal and circulating T cell phenotypes. However, the vaginal mucosa during active HSV-2 shedding was associated with alterations in T cell, macrophage, and dendritic cell localization and gene expression consistent with increased immune surveillance, with immune activating and suppressing signals potentially reinforcing mucosal tissue homeostasis. SummaryIn context of episodic HSV-2 shedding, immune cells mobilize and co-localize in the vaginal epithelium, expressing cytotoxic and inflammatory genes and immunoregulatory genes that collectively may promote tissue homeostasis in settings of episodic viral shedding to limit damage.

immunology↗

Mucosal tissue NK cells tune their function between optimal anti-pathogen activity and tissue protection

Preserving barrier integrity while mounting effective immunity is essential at mucosal surfaces. In examining the immune cells that mediate both inflammation and tissue homeostasis, we uncovered a dual role for natural killer (NK) cells in barrier immunity. While NK cells are known to control viral infections, here we identify a previously unrecognized reparative function for NK cells in mucosal tissues. Using single-cell RNA sequencing and high-dimensional flow cytometry, we reveal a distinct population of human mucosal NK cells marked by tissue residency, immunoregulatory profiles, and limited cytotoxic potential at homeostasis, yet highly responsive to inflammatory cues. In a mouse model of acute HSV-2 infection, NK cells are required for limiting infection-associated tissue damage. Mucosal NK cells express the epithelial growth factor amphiregulin (Areg), and their depletion leads to increased tissue barrier damage despite preserved viral clearance, suggesting a novel role in tissue protection. Mechanistically, we demonstrate that the barrier-derived cytokines IL-18 and IL-33 induce Areg expression by both human and mouse NK cells, linking local inflammatory cues to reparative NK cell programming that is able to potentiate wound healing. Together, our findings reveal a context-dependent, dual function of mucosal NK cells in immune defense and mucosal tissue protection, expanding current models of NK cell biology.

immunology↗

Promoter-centric gene regulation in drug-resistant cancer

In eukaryotic cells, gene-distal regulatory elements (REs) facilitate long-range gene regulation, ensuring cell type-specific transcriptional programs. This mechanism is frequently disrupted in cancer, often driven by transcription factors (TFs) that serve as targets for cancer therapy. However, targeting these TFs can lead to acquired resistance mechanisms that are not fully understood. We demonstrate that mesothelioma cancer cells, dependent on the oncogenic driver TF family TEAD, develop resistance to a pan-TEAD inhibitor and revert to an evolutionarily ancient, promoter-centric gene regulatory mechanism to recover gene expression following TEAD inhibition. Base-pair-resolution 3D chromatin conformation mapping reveals that RE-promoter interactions are disrupted in resistant cells, despite epigenetic and transcriptomic recovery. Mechanistically, in resistant cells, TF complexes, including resistance-specific FOSL1 and KLF4, preferentially bind and enhance promoter activity to recover gene expression, rendering distal REs dispensable. Our findings highlight promoter elements and promoter-specific TFs as potential therapeutic targets using a model of drug-resistant cancer.

cancer biology↗

Bacterial vaginosis-driven changes in vaginal T cell phenotypes and their implications for HIV susceptibility

Bacterial vaginosis (BV) is a dysbiosis of the vaginal microbiome that is prevalent among reproductive-age females worldwide. Adverse health outcomes associated with BV include an increased risk of sexually-acquired HIV, yet the immunological mechanisms underlying this association are not well understood. To investigate BV-driven changes to cervicovaginal tract (CVT) and circulating T cell phenotypes, participants with or without BV provided vaginal tract (VT) and ectocervical (CX) tissue biopsies and PBMC samples. High-parameter flow cytometry revealed an increased frequency of cervical conventional CD4+ T cells (Tconv) expressing CCR5. However, we found no difference in number of CD3+CD4+CCR5+ cells in the CX or VT of BV+ vs BV- individuals, suggesting that BV-driven increased HIV susceptibility may not be solely attributed to increased CVT HIV target cell abundance. Flow cytometry also revealed that individuals with BV have an increased frequency of dysfunctional CX and VT CD39+ Tconv and CX tissue-resident CD69+CD103+ Tconv, reported to be implicated in HIV acquisition risk and replication. Many soluble immune factor differences in the CVT further support that BV elicits diverse and complex CVT immune alterations. Our comprehensive analysis expands on potential immunological mechanisms that may underlie the adverse health outcomes associated with BV including increased HIV susceptibility.

immunology↗

Comparative Analysis of Commercial Single-Cell RNA Sequencing Technologies

This study evaluates ten commercially available single-cell RNA sequencing (scRNA-seq) approaches across four technology groups: Emulsion-based kits from 10x Genomics and Fluent Biosciences; Microwell-based kits from Becton Dickinson, Honeycomb Technologies and Singerlon Technologies; Combinatorial-indexing kits from Parse Biosciences and Scale Biosciences; and a Matrigel-based kit from Scipio Biosciences. Peripheral blood mononuclear cells (PBMCs) from a single donor were used to assess analytical performance. Key features such as sample compatibility, cost, and experimental duration were also compared. Notably, superior analytical performance was demonstrated by the Chromium Fixed RNA Profiling kit from 10x Genomics, which uniquely features probe hybridization for transcript detection. Additionally, the Rhapsody WTA kit from Becton Dickinson provided a cost-effective balance of performance and expense per cell. With a rich dataset of 218,154 cells, this work provides a basis for differentiating commercial scRNA-seq technologies, which is intended to facilitate the effective application and further methodological development of single cell transcriptomics.

molecular biology↗

Overloading And unpacKing (OAK) - droplet-based combinatorial indexing for ultra-high throughput single-cell multiomic profiling

Multiomic profiling of single cells by sequencing is a powerful technique for investigating cellular diversity in complex biological systems. Although the existing droplet-based microfluidic methods have advanced single-cell sequencing, they produce a plethora of cell-free droplets and underutilize barcoding capacities due to their low cell concentration prerequisites. Meanwhile, combinatorial indexing on microplates can index cells in a more effective way; however, it requires time-consuming and laborious protocols involving multiple splitting and pooling steps. Addressing these constraints, we have developed "Overloading And unpacKing" (OAK). With reduced labor intensity, OAK can provide cost-effective multiomic profiling for hundreds of thousands of cells, offering detection sensitivity on par with commercial droplet-based methods. To demonstrate OAKs versatility, we conducted single-cell RNA sequencing (scRNA-Seq) as well as joint single-nucleus RNA sequencing (snRNA-Seq) and single-nucleus Assay for Transposase Accessible Chromatin with sequencing (snATAC-Seq) using cell lines. We further showcased OAKs performance on more complex samples, including in vitro differentiated bronchial epithelial cells and primary retinal tissues. Finally, we examined transcriptomic responses of 408,000 melanoma cells across around 1,000 starting lineages over a 90-day treatment with a RAF inhibitor, belvarafenib. We discovered a rare cell population (0.12%) that underwent a sequence of transcriptomic changes, resulting in belvarafenib resistance. Ultra-high throughput, broad compatibility with diverse molecular modalities, high detection sensitivity, and simplified experimental procedures distinguish OAK from previous methods, and render OAK a powerful tool for large-scale analysis of molecular signatures, even for rare cells.

molecular biology↗

Baseline T cell immune phenotypes predict virologic and disease control upon SARS-CoV infection

The COVID-19 pandemic has revealed that infection with SARS-CoV-2 can result in a wide range of clinical outcomes in humans, from asymptomatic or mild disease to severe disease that can require mechanical ventilation. An incomplete understanding of immune correlates of protection represents a major barrier to the design of vaccines and therapeutic approaches to prevent infection or limit disease. This deficit is largely due to the lack of prospectively collected, pre-infection samples from indiviuals that go on to become infected with SARS-CoV-2. Here, we utilized data from a screen of genetically diverse mice from the Collaborative Cross (CC) infected with SARS-CoV to determine whether circulating baseline T cell signatures are associated with a lack of viral control and severe disease upon infection. SARS-CoV infection of CC mice results in a variety of viral load trajectories and disease outcomes. Further, early control of virus in the lung correlates with an increased abundance of activated CD4 and CD8 T cells and regulatory T cells prior to infections across strains. A basal propensity of T cells to express IFNg and IL17 over TNFa also correlated with early viral control. Overall, a dysregulated, pro-inflammatory signature of circulating T cells at baseline was associated with severe disease upon infection. While future studies of human samples prior to infection with SARS-CoV-2 are required, our studies in mice with SARS-CoV serve as proof of concept that circulating T cell signatures at baseline can predict clinical and virologic outcomes upon SARS-CoV infection. Identification of basal immune predictors in humans could allow for identification of individuals at highest risk of severe clinical and virologic outcomes upon infection, who may thus most benefit from available clinical interventions to restrict infection and disease. SummaryWe used a screen of genetically diverse mice from the Collaborative Cross infected with mouse-adapted SARS-CoV in combination with comprehensive pre-infection immunophenotyping to identify baseline circulating immune correlates of severe virologic and clinical outcomes upon SARS-CoV infection.

immunology↗

Detection and treatment strategy for Tritrichomonas muris in the common laboratory mouse

Maintaining a specific pathogen-free (SPF) mouse colony is critical to avoid potentially confounding variables introduced by unknown infections. Here, we report an instance of protozoan Tritrichomonas muris (T. muris) infection of mice within an SPF facility. Although T. muris has been considered a commensal organism, we observed instances of asymmetric infection in gene-knockout mice as compared to wild-type mice. We utilized treatment with metronidazole and confirmed successful elimination of T. muris from our SPF colony using extraction of fecal DNA followed by PCR detection. We propose that T. muris testing should be considered for SPF mice, particularly in immunity studies.

microbiology↗

Progressive differentiation of memory CD8 T cells in the cervicovaginal tissue

Tissue-resident memory CD8 T cells (CD8 TRM) are critical for maintaining barrier immunity. CD8 TRM have been mainly studied in the skin and gut with recent studies suggesting that the signals that control tissue-residence and phenotype are highly tissue-dependent. We examined the T cell compartment in healthy human cervicovaginal tissue (CVT) and found that most CD8 T cells were granzyme B+ and TCF-1-. To address if this phenotype is driven by CVT tissue-residence, we used a mouse model to control for environmental factors. Using localized and systemic infection models, we found that CD8 TRM in the mouse CVT gradually acquired a granzyme B+, TCF-1- phenotype as seen in human CVT. In contrast to CD8 TRM in the gut, these CD8 TRM were not stably maintained regardless of the initial infection route, which led to reductions in local immunity. Our data show that residence in the CVT is sufficient to progressively shape the size and function of its CD8 TRM compartment. SummaryThe tissue-resident memory (TRM) CD8 T cell compartment in human and mouse cervicovaginal tissue (CVT) is remarkably similar. The CVT TRM compartment is maintained autonomously and does not reach phenoypical or numerical equilibrium. The numerical decline leads to impaired viral control in a secondary challenge.

immunology↗

Elimination of HSV-2 infected cells is mediated predominantly by paracrine effects of tissue-resident T cell derived cytokines

The mechanisms underlying rapid elimination of herpes simplex virus-2 (HSV-2) in the human genital tract despite low tissue-resident CD8+ T-cell density (TRM) are unknown. We analyzed shedding episodes during chronic HSV-2 infection: viral clearance always occurred within 24 hours of detection even if viral load exceeded 107 HSV DNA copies; surges in granzyme B and interferon-{gamma} occurred within the early hours after reactivation. We next developed a mathematical model of an HSV-2 genital ulcer to integrate mechanistic observations of TRM in situ proliferation, trafficking, cytolytic effects and cytokine alarm signaling from murine studies with viral kinetics, histopathology and lesion size data from humans. A sufficiently high density of HSV-2 specific TRM predicted rapid contact-mediated elimination of infected cells. At lower TRM densities, TRM must initiate a rapidly diffusing, polyfunctional cytokine response in order to eliminate of a majority of infected cells and eradicate briskly spreading HSV-2 infection.\n\nOne Sentence SummaryControl of herpes simplex virus-2 is primarily mediated by rapidly diffusing cytokines secreted by tissue-resident T cells.

immunology↗