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Jameson, S. C.

Publications and source records attributed to Jameson, S. C..

11 recordsLinked to original sources

STEVE: Single-cell Transcriptomics Expression Visualization and Evaluation

Single-cell RNA sequencing (scRNA-seq) has become a key technology for characterizing cell-type heterogeneity in complex tissues. However, its utility depends on accurate and reproducible cell-type annotation, which remains a major analytical challenge. Although hundreds of computational tools have been developed for automated annotation, there is currently no systematic framework to evaluate annotation robustness in a dataset-specific manner or within the context of complete analytical pipelines. Here, we present STEVE (Single-cell Transcriptomics Expression Visualization and Evaluation), a quantitative framework designed to assess the accuracy, robustness, and reproducibility of cell-type annotation in scRNA-seq studies. STEVE implements three complementary in silico evaluation modules: (i) Subsampling Evaluation to quantify annotation stability under varying reference sizes and data partitions; (ii) Novel Cell Evaluation to assess the ability to detect previously unseen cell types; and (iii) Annotation Benchmarking to compare alternative annotation tools against ground-truth labels. In addition, STEVE includes a Reference Transfer Annotation module that enables cross-dataset cell-type mapping using external reference datasets. All modules are built upon a unified probabilistic framework that provides consistent confidence estimation across evaluation scenarios. We evaluated STEVE across four independent scRNA-seq datasets with experimentally defined or expert-curated cell-type labels. Our results show that annotation robustness is strongly influenced by the annotation method, biological separability, dataset complexity, and batch effects. STEVE provides a practical framework for quantifying annotation uncertainty and improving reproducibility in single-cell transcriptomic analyses. STEVE is freely available at GitHub (https://github.com/XiaoDongLab/STEVE).

bioinformatics↗

Diverse Microbial Exposure Enhances CD8+ T Cell Effector Memory Output and Function

Mice with normalized microbial exposure (NME) harbor an immune system that more accurately reflects that of humans compared to mice maintained as specific pathogen-free (SPF). An explanation for the observed alterations in the composition of the T cell compartment in NME mice has not been reported. We compared the T cell landscape in NME versus SPF mice at baseline and after acute LCMV infection. Using the immgenT dataset, we found no unique T cell populations in NME, but the landscape shifted towards activated T cells with increased propensity for effector functions and improved pathogen clearance. CD8+ KLRG1+ cells (immgenT CD8_cl12) are significantly expanded in NME mice. Their predominance was a result of both increased formation and the conversion of other memory populations to a KLRG1+ phenotype. Thus, NME mice provide insight into a diverse T cell compartment rich with cells previously found to be limited in SPF mice.

immunology↗

Bcl-2 protein Noxa is required for metabolic reprogramming to glutamine dependence and for apoptosis in stimulated human CD8+ T cells

Naive or memory T cells reprogram their metabolism upon antigenic stimulation. They increase their glucose uptake, relying on aerobic glycolysis for generating biomass while switching to glutamine to fuel energy production. Here we have identified a requirement for human Bcl-2 family, Noxa, in the metabolic switch to glutamine dependence in activated CD8+ T cells, that is independent of its canonical role in apoptosis at the end of the immune response. Using an in vitro co-stimulation model, we demonstrate that Noxa is induced in CD8+ T cells and remains elevated during the proliferative and differentiation phases of the response and through the onset of apoptosis. Noxa protein induction requires glutamine, is mediated via mTOR, and is independent of glutaminolysis. Glutamine, in turn, requires Noxa to facilitate its conversion to glutamate. CD8+ T cells lacking Noxa showed reduced levels of intracellular glutamate but no impairment of mitochondrial or effector function, and decreased dependence on glutamine for both respiration and growth during the proliferative phase. NOXA knockout CD8 T cells also displayed significantly higher viability in the apoptotic phase of the immune response. CD8+ T cells from a human NOXA gene-replacement mouse responded normally to in vitro stimulation and in vivo acute infection. However, human Noxa-expressing murine CD8+ T cells displayed a distinctly proliferative gene signature in their transcriptome following activation, supporting an early growth-promoting role for this BH3-only protein. Our studies suggest that knocking out NOXA in human CD8+ T cells to increase their lifespan as well as their ability to survive and function in glutamine-poor microenvironments could be a promising immunotherapeutic strategy.

immunology↗

Steady-state, therapeutic, and helminth-induced IL-4 compromise protective CD8 T cell bystander activation

Memory CD8 T cells (Tmem) can be activated into innate-like killers by cytokines like IL-12, IL-15, and/or IL-18; but mechanisms regulating this phenomenon (termed bystander activation) are not fully resolved. We found strain-intrinsic deficiencies in bystander activation using specific pathogen-free mice, whereby basal IL-4 signals antagonize IL-18 sensing. We show that therapeutic and helminth-induced IL-4 impairs protective bystander-mediated responses against pathogens. However, this IL-4/IL-18 axis does not completely abolish bystander activation but rather tunes the expression of direct versus indirect mediators of cytotoxicity (granzymes and interferon-{gamma}, respectively). We show that antigen-experience overrides strain-specific deficiencies in bystander activation, leading to uniform IL-18 receptor expression and enhanced capacity for bystander activation/cytotoxicity. Our data highlight that bystander activation is not a binary process but tuned/deregulated by other cytokines that are elevated by contemporaneous infections. Further, our findings underscore the importance of antigen-experienced Tmem to dissect the contributions of bystander Tmem in health and disease.

immunology↗

Collaboration between IL-7 and IL-15 enables adaptation of tissue-resident and circulating memory CD8+ T cells

Interleukin-7 (IL-7) is considered a critical regulator of memory CD8+ T cell homeostasis, but this is primarily based on analysis of circulating and not tissue-resident memory (TRM) subsets. Furthermore, the cell-intrinsic requirement for IL-7 signaling during memory homeostasis has not been directly tested. Using inducible deletion, we found that Il7ra loss had only a modest effect on persistence of circulating memory and TRM subsets and that IL-7R was primarily required for normal basal proliferation. Loss of IL-15 signaling imposed heightened IL-7R dependence on memory CD8+ T cells, including TRM populations previously described as IL-15-independent. In the absence of IL-15 signaling, IL-7R was upregulated, and loss of IL-7R signaling reduced proliferation in response to IL-15, suggesting cross-regulation in memory CD8+ T cells. Thus, across subsets and tissues, IL-7 and IL-15 act in concert to support memory CD8+ T cells, conferring resilience to altered availability of either cytokine. HighlightsTissue-resident and circulating memory CD8+ T cells modestly decline after loss of IL-7R IL-7R is required for normal self-renewal of memory CD8+ T cells Combined loss of IL-7 and IL-15 causes a profound defect across memory CD8+ T cell subsets Cross-regulation of IL-7 and IL-15 signaling occurs in memory CD8+ T cells O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=70 SRC="FIGDIR/small/596695v1_ufig1.gif" ALT="Figure 1"> View larger version (17K): org.highwire.dtl.DTLVardef@8e439corg.highwire.dtl.DTLVardef@1f8e42forg.highwire.dtl.DTLVardef@14cfceforg.highwire.dtl.DTLVardef@171e4eb_HPS_FORMAT_FIGEXP M_FIG C_FIG

immunology↗

Dysfunctional T Follicular Helper Cells Cause Intestinal and Hepatic Inflammation in NASH

Nonalcoholic steatohepatitis (NASH), characterized by hepatic inflammation and cellular damage, is the most severe form of nonalcoholic fatty liver disease and the fastest-growing indication for a liver transplant. The intestinal immune system is a central modulator of local and systemic inflammation. In particular, Peyers patches (PPs) contain T follicular helper (Tfh) cells that support germinal center (GC) responses required for the generation of high-affinity intestinal IgA and the maintenance of intestinal homeostasis. However, our understanding of the mechanisms regulating mucosal immunity during the pathogenesis of NASH is incomplete. Here, using a preclinical mouse model that resembles the key features of human disease, we discovered an essential role for Tfh cells in the pathogenesis of NASH. We have found that mice fed a high-fat high-carbohydrate (HFHC) diet have an inflamed intestinal microenvironment, characterized by enlarged PPs with an expansion of Tfh cells. Surprisingly, the Tfh cells in the PPs of NASH mice showed evidence of dysfunction, along with defective GC responses and reduced IgA+ B cells. Tfh-deficient mice fed the HFHC diet showed compromised intestinal permeability, increased hepatic inflammation, and aggravated NASH, suggesting a fundamental role for Tfh cells in maintaining gut-liver homeostasis. Mechanistically, HFHC diet feeding leads to an aberrant increase in the expression of the transcription factor KLF2 in Tfh cells which inhibits its function. Thus, transgenic mice with reduced KLF2 expression in CD4 T cells displayed improved Tfh cell function and ameliorated NASH, including hepatic steatosis, inflammation, and fibrosis after HFHC feeding. Overall, these findings highlight Tfh cells as key intestinal immune cells involved in the regulation of inflammation in the gut-liver axis during NASH.

immunology↗

Pannexin-1 channels promote CD8+ T cell effector and memory responses through distinct intracellular pathways

Sensing of extracellular ATP (eATP) controls CD8+ T cell function. Their accumulation can occur through export by specialized molecules, such as the release channel Pannexin-1 (Panx1). Whether Panx1 controls CD8+ T cell immune responses in vivo, however, has not been previously addressed. Here, we report that T cell-specific Panx1 is needed for CD8+ T cell responses to viral infections and cancer. We found that CD8-specific Panx1 promotes both effector and memory CD8+ T cell responses. Panx1 favors initial effector CD8+ T cell activation through extracellular ATP (eATP) export and subsequent P2RX4 activation, which helps promote full effector differentiation through extracellular lactate accumulation and its subsequent recycling. In contrast, Panx1 promotes memory CD8+ T cell survival primarily through ATP export and subsequent P2RX7 engagement, leading to improved mitochondrial metabolism. In summary, Panx1-mediated eATP export regulates effector and memory CD8+ T cells through distinct purinergic receptors and different metabolic and signaling pathways.

immunology↗

The extracellular ATP receptor P2RX7 imprints a pro-memory transcriptional signature in effector CD8+ T cells

Development of central memory (Tcm) and resident memory (Trm) CD8+ T cells, which respectively promote immunity in the circulation and in barrier tissues, is not completely understood. Tcm and Trm cells may arise from common precursors, however their fate-inducing signals are elusive. We found that virus-specific effector CD8+ T cells display heterogeneous expression of the extracellular ATP sensor P2RX7. P2RX7-high expression is confined, at peak effector phase, to CD62L+ memory precursors which preferentially form Tcm cells. Among early effector CD8+ T cells, asymmetrical P2RX7 distribution correlated with distinct transcriptional signatures, with P2RX7-high cells enriched for memory and tissue-residency sets. P2RX7-high early effectors preferentially form both Tcm and Trm cells. Defective Tcm and Trm formation in P2RX7 deficiency is significantly reverted when the transcriptional repressor Zeb2 is ablated. Our study indicates that unequal P2RX7 upregulation in effector CD8+ T cells is a foundational element of the early Tcm/Trm fate.

immunology↗

γδ-Thymocyte Maturation and Emigration

The thymus is the site of both {beta} and {gamma}{delta}-T cell development. After several unique waves of {gamma}{delta}-T cells are generated in, and exported from, the fetal/neonatal thymus, the adult thymus continues to produce a stream of {gamma}{delta}-T cells throughout life. One intriguing feature of {gamma}{delta} T cell development is the coordination of differentiation and acquisition of effector function within the fetal thymus, however, it is less clear whether this paradigm holds true in adult animals. To investigate the relationship between maturation and time since V(D)J recombination in adult-derived {gamma}{delta}-thymocytes, we used the Rag2pGFP model. Immature (CD24+) {gamma}{delta}-thymocytes expressed high levels of GFP while only a small minority of mature (CD24-) {gamma}{delta}-thymocytes were GFP+. Similarly, most GFP+ {gamma}{delta}-splenocytes were immature, while some were mature. Analysis of {gamma}{delta}-recent thymic emigrants (RTEs) indicated that most {gamma}{delta}-T cell RTEs were CD24+ and GFP+ and adoptive transfer experiments showed that immature {gamma}{delta}-thymocytes could be maintained in the periphery for at least 3 days over which time they matured. With respect to the mature {gamma}{delta}-thymocytes that were GFP-, parabiosis experiments demonstrated that mature {gamma}{delta}-T cells did not recirculate from the periphery. Instead, a population of mature {gamma}{delta}-thymocytes remained resident in the thymus for at least 60 days while mature {gamma}{delta}-thymocytes derived solely from adult hematopoiesis were mostly lost from the thymus within 60 days. Collectively, these data demonstrate two streams of actively developing {gamma}{delta}-T cells in adult mice: an immature subset that quickly leaves the thymus and matures in the periphery, and one that completes maturation within the thymus over a longer period of time. Furthermore, there is a fetal-derived and heterogeneous population of resident {gamma}{delta}-thymocytes of unknown functional importance.

immunology↗

Non-deletional CD8+ T cell self-tolerance permits responsiveness but limits tissue damage

Self-specific CD8+ T cells often escape clonal deletion, but the properties and capabilities of such cells in a physiological setting are unclear. We characterized polyclonal CD8+ T cells specific for the melanocyte antigen tyrosinase-related protein 2 (Trp2) in mice that express or lack this enzyme due to deficiency in Dct, which encodes Trp2. The size, phenotype, and gene expression profile of the pre-immune Trp2/Kb-specific pool were similar in wild-type (WT) and Dct-deficient (Dct-/-) mice. Despite comparable initial responses to Trp2 immunization, WT Trp2/Kb-specific cells showed blunted expansion, and scRNAseq revealed WT cells less readily differentiated into a CD25+ proliferative population. Functional self-tolerance clearly emerged when assessing immunopathology: adoptively transferred WT Trp2/Kb-specific cells mediated vitiligo much less efficiently. Hence, CD8+ T cell self-specificity is poorly predicted by precursor frequency, phenotype or even initial responsiveness, while deficient activation-induced CD25 expression and other gene expression characteristics may help to identify functionally tolerant cells.

immunology↗

ZipSeq : Barcoding for Real-time Mapping of Single Cell Transcriptomes

Spatial transcriptomics seeks to integrate single-cell transcriptomic data within the 3-dimensional space of multicellular biology. Current methods use glass substrates pre-seeded with matrices of barcodes or fluorescence hybridization of a limited number of probes. We developed an alternative approach, called ZipSeq, that uses patterned illumination and photocaged oligonucleotides to serially print barcodes (Zipcodes) onto live cells within intact tissues, in real-time and with on-the-fly selection of patterns. Using ZipSeq, we mapped gene expression in three settings: in-vitro wound healing, live lymph node sections and in a live tumor microenvironment (TME). In all cases, we discovered new gene expression patterns associated with histological structures. In the TME, this demonstrated a trajectory of myeloid and T cell differentiation, from periphery inward. A variation of ZipSeq efficiently scales to the level of single cells, providing a pathway for complete mapping of live tissues, subsequent to real-time imaging or perturbation.

genomics↗