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Biology subjects

Kang, S. W.

Publications and source records attributed to Kang, S. W..

16 recordsLinked to original sources

Multimodal Imaging of the Cellular and Extracellular Microenvironment on the Same Formalin-Fixed Paraffin-Embedded Tissue Section

Same-tissue section multimodal imaging is a powerful strategy that spatially profiles tissue histology, cell populations and molecular composition while maximizing tissue economy, preserving spatial molecular relationships, and increasing co-registration capacity. However, performing multiple modalities on the same tissue section can destroy or chemically alter the tissue, compromising downstream data. Here, we systematically assess integration of picrosirius red staining, hematoxylin and eosin staining, and multiplexed immunofluorescence into N-glycan and extracellular matrix peptide matrix-assisted laser/desorption ionization imaging mass spectrometry (IMS) workflows. We evaluate alterations in tissue morphology, stain efficiency, IMS feature intensity as well as IMS feature localization after upstream modality integration. We propose an optimized multimodal sequence that maximizes data quality and follows a very specific order of: autofluorescence microscopy, multiplexed immunofluorescence, picrosirius red staining, N-glycan IMS, hematoxylin and eosin staining, and extracellular matrix peptide IMS. Overall, this work develops an optimized multimodal workflow that comprehensively images tissue morphology, collagen fibers, and cell populations at single-cell resolution as well as multiplexed N-glycan composition and multiplexed extracellular matrix peptides with post-translational modification status from a single tissue section.

biochemistry↗

Fructose utilization by GM-CSF-differentiated macrophages aggravates autoimmune inflammation via MG-derived AGE-RAGE signaling

Excessive fructose intake is increasingly associated with metabolic and inflammatory pathologies; however, the direct impact of fructose metabolism on immune cell function remains insufficiently understood. Here, we demonstrate that GM-CSF-differentiated macrophages markedly upregulate the fructose-specific transporter GLUT5, enabling efficient fructose utilization through two complementary metabolic pathways. Using 13C-fructose tracing, we identified distinct carbon fluxes via a hexokinase (HK)-dependent glycolytic route and a ketohexokinase (KHK)-ALDOB-mediated fructolytic route. The HK-dependent pathway sustains glycolytic activity under glucose-limiting conditions, stabilizing HIF-1 and preserving pro-inflammatory gene expression. Conversely, the KHK-ALDOB axis increases dihydroxyacetone phosphate (DHAP) production, leading to methylglyoxal-derived advanced glycation end-products (MG-AGEs) that engage receptor for AGE (RAGE) signaling. This activation enhances MMP9 expression in macrophages and drives Th17 differentiation in CD4 T cells, amplifying inflammatory and tissue-remodeling processes. In vivo, fructose intake exacerbates autoimmune arthritis in SKG mice, and elevated fructose-driven glycolysis and MG-AGE accumulation are observed in monocytes from patients with rheumatoid arthritis. These results link fructose-driven carbonyl stress to macrophage effector programs and downstream T cell polarization. Collectively, these findings uncover a dual fructose metabolic program that integrates nutrient stress with persistent inflammation via the MG-AGE-RAGE axis and underscore the immunometabolic risks of excessive fructose exposure.

immunology↗

Tumor-infiltrating natural killer cell profiling for therapeutic stratification in patients with resectable non-small cell lung cancer

ObjectiveNeoadjuvant chemoimmunotherapy has improved outcomes in resectable non-small cell lung cancer (NSCLC), yet its real-world implementation is often challenged by surgical delays, immune-mediated fibrosis, and postoperative complications. Smokers with NSCLC, despite a high risk for surgical morbidity, show enhanced responses to neoadjuvant chemoimmunotherapy. This study aimed to identify smoking-associated immune cell determinants that could guide treatment strategies. MethodsSingle-cell RNA sequencing (scRNAseq) was performed on 61 lung tissues from non-smokers and smokers to identify smoking-related immune compositions. The scRNAseq data from 19 invasive lung adenocarcinomas were used to validate their presence in the tumor-immune microenvironment. Bulk RNA sequencing data from 102 resected NSCLC and 24 NSCLC patients treated with neoadjuvant chemoimmunotherapy followed by surgery were used for in silico cellular deconvolution and outcome analyses. ResultsAmong 135 lung cellular phenotypes, two natural killer (NK) cell subsets were strongly associated with smoking and chronic obstructive pulmonary disease (COPD) severity. "Stress-responsive" NK (NKSR) cells exhibited immature features and cytokine-responsive features, and "Adaptive and immunoregulatory NK" (NKAIR) cells showed mature features and elevated multiple immune checkpoint expression. High intratumoral NKSR cells correlated with improved survival after surgery, particularly in current smokers. Conversely, tumors with low NKSR and high NKAIR cells responded more favorably to neoadjuvant chemoimmunotherapy. ConclusionsIntratumoral NK cell phenotyping may aid in therapeutic stratification in patients with NSCLC. NKSR cell preservation predicts benefit from upfront surgery, while NKAIR cell enrichment indicates improved response to neoadjuvant chemoimmunotherapy. These NK cell profiles may help optimize treatment by balancing therapeutic benefit and risk. Graphic Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=112 SRC="FIGDIR/small/696292v1_ufig1.gif" ALT="Figure 1"> View larger version (50K): org.highwire.dtl.DTLVardef@168bc03org.highwire.dtl.DTLVardef@10fa947org.highwire.dtl.DTLVardef@132a92dorg.highwire.dtl.DTLVardef@100e4a4_HPS_FORMAT_FIGEXP M_FIG C_FIG Central Picture O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=81 SRC="FIGDIR/small/696292v1_ufig2.gif" ALT="Figure 2"> View larger version (21K): org.highwire.dtl.DTLVardef@1a2d3b4org.highwire.dtl.DTLVardef@f8f84borg.highwire.dtl.DTLVardef@17510bcorg.highwire.dtl.DTLVardef@9da763_HPS_FORMAT_FIGEXP M_FIG C_FIG NK cell profiling for treatment stratification in resectable NSCLC Central MessageTumor-infiltrating NK cell profiling identifies distinct immune phenotypes that can inform personalized treatment strategies in resectable NSCLC. Perspective statementAbundance of intratumoral stress-responsive NK cells predicts favorable outcomes after upfront surgery, whereas enrichment of adaptive and immunoregulatory NK cells suggests greater benefit from neoadjuvant chemoimmunotherapy. These findings support incorporating NK-cell profiling into preoperative decision-making to optimize therapy selection and balance risks in the high-risk surgical population.

immunology↗

Decrypting cellular engagement and recruitment from spatially resolved transcriptomics

The recruitment of the various types of cells into the tissue microenvironment and how these cells engage with other cells in the tissue sites play critical biological roles. However, it is difficult to study these processes on a genome-wide scale using traditional low-throughput experiments. To address this gap, we developed a fully interpretable multi-instance deep learner, coined "spacer". Spacer digests the transcriptomics and spatial modalities of spatially resolved transcriptomics (SRT) data in alignment with the biological principles of the tissue spatial architecture. We deployed spacer to a panel of 17 high definition and 20 low definition SRT datasets, for studying how stromal and immune cells were recruited into tumors and heart during myocarditis. Spacer discovered novel biological insights not affordable by prior spatial data analysis tools, which were validated by orthogonal immuno-peptidomics, spatial T cell receptor (TCR) sequencing, and single cell sequencing experiments. We discovered genes that encode more immunogenic peptides and that are involved in developmental pathways are more potent in recruiting T cells to local tumor sites, while the recruitment of B cells and macrophages is stipulated by a different molecular program. On the other hand, expression of mucins in the tumor cells was found to repel T cell localization. For the engaging cell side, we also uncovered T cell-intrinsic features that determine their localization, validated by spatial-TCR-seq data. Spacer also unexpectedly revealed that CD4+ T cells, though fewer in numbers, are more responsive than CD8+ T cells in the heart during myocarditis. Collectively, this study establishes a new spatially resolved paradigm for studying cellular localization mechanisms in situ and shifts the paradigm from descriptive mapping to mechanistic discovery.

bioinformatics↗

Drosophila Pyruvate Kinase Links Metabolic State with Circadian Output via TARANIS and PDF

The circadian clock generates [~]24-hour rhythms that anticipate daily environmental changes. Circadian clock and glucose metabolism are tightly interconnected, and both are disrupted in aging and disease. To examine how glucose hypometabolism impacts circadian rhythm, we downregulated glycolytic enzymes - Hexokinase-C (Hex-C), Phosphofructokinase (Pfk), and Pyruvate kinase (Pyk) - in Drosophila clock cells. Only Hex-C and Pyk knock-down (KD) altered period, lengthening and shortening rhythms, respectively. Notably, Pyk KD induced period shortening persisted in adult-specific KD (AKD), indicating a role independent of developmental effects. Pyk AKD reduced both PERIOD and Pigment-dispersing factor (PDF) protein levels, with PDF loss driving the short-period phenotype. Mechanistically, the transcriptional co-regulator TARANIS (TARA) was required: Pyk AKD lowered tara expression, while tara overexpression rescued PDF and circadian period. Our findings identify a novel PYK-TARA-PDF regulatory axis linking glycolytic activity to circadian neuropeptide output, providing mechanistic insight into how metabolic dysfunction contributes to circadian disruption in aging and neurodegenerative diseases.

neuroscience↗

Coordinated changes in thymic stromal and hematopoietic cells that define the perinatal to juvenile transition

T cells in the perinatal thymus have distinct phenotypes and functions that may be instructed by age-specific features of the microenvironment. We evaluated molecular and cellular profiles of thymic stromal cells, including thymic epithelial cells (TECs), mesenchyme, endothelium, and hematopoietic antigen presenting cells (hAPCs), from birth through one-month of age in mice. Single-cell transcriptional profiling, flow cytometry, and immunohistochemistry revealed coordinated stromal changes accompanied by altered thymocyte differentiation at defined transitional ages during the shift from perinatal growth to juvenile homeostasis, which was mirrored in humans. These analyses link diminished IGF2 expression by mesenchymal cells with activation of the RB pathway in TECs at the transition. Moreover, a coordinated increase in type I interferon signaling in stroma across the transition is associated with altered antigen processing and presentation signatures in TECs and hAPCs. Collectively, these datasets provide a resource to interrogate thymic stroma across the perinatal to juvenile transition.

immunology↗

Identification of QTL for reproductive success under heat stress conditions through a tomato MAGIC population

Heat stress threatens tomato productivity by reducing pollen viability, fruit set, and consequently, overall yield. While heat-tolerant traits are predominantly found in wild tomatoes, the introgression of heat tolerance into elite cultivars remains challenging due to linkage drag. To address this issue, the World Vegetable Center developed a Multi-parent Advanced Generation Inter-Cross (MAGIC) population, derived from crosses between four heat-tolerant and disease-resistant cultivars. Phenotypic evaluations revealed that fruit number accounted for approximately 57% of reproductive output, making it a critical selection index for heat tolerance. A total of 16,350 SNPs were developed for the MAGIC population, and genome-wide association studies (GWAS) identified 50 QTLs linked to the evaluated traits. Notably, three QTLs on chromosomes 1, 3 and 11 emerged as hubs influencing multiple reproductive traits, underscoring their critical role in heat tolerance. SL4.0CH11_47205149 associated with fruit number was converted into a Kompetitive Allele-Specific PCR (KASP) marker and validated for its significant association with yield. The identification of key QTLs and the prioritization of fruit number as a primary determinant of reproductive success offer valuable insights for targeted breeding strategies. HighlightNumber of fruits is crucial for selecting heat-tolerant tomatoes in open fields. A marker linked to high fruit production helps develop high-yielding tomatoes better suited to withstand climate change.

genomics↗

Pathobiont-triggered induction of epithelial IDO1 drives regional susceptibility to Inflammatory Bowel Disease

The structure and function of the mammalian gut vary by region, yet why inflammatory diseases manifest in specific regions and not others remains unclear. We use a TNF-overexpressing Crohns disease (CD) model (Tnf{Delta}ARE/+), which typically presents in the terminal ileum (TI), to investigate how environmental factors interact with the hosts immune susceptibility to drive region-specific disease. We identified Chlamydia muridarum, an intracellular bacterium and murine counterpart to the human sexually transmitted C. trachomatis, as necessary and sufficient to trigger disease manifestation in the ascending colon (AC), another common site of human CD. Disease manifestation in the AC depends on indoleamine 2,3-dioxygenase (IDO1) activity induced by hypersensitive surface secretory cells in genetically susceptible hosts. Single-cell and microbial analyses of human specimens also implicates this pathobiont-epithelial IDO1 pathway in patients with a history of CD in the AC. Our findings demonstrate that genetic and microbial factors can independently drive region-specific disease and provide a unique model to study CD specific to the AC.

cell biology↗

Acquisition of discrete immune suppressive barriers contributes to the initiation and progression of preinvasive to invasive human lung cancer.

Computerized chest tomography (CT)-guided screening in populations at risk for lung cancer has increased the detection of preinvasive subsolid nodules, which progress to solid invasive adenocarcinoma. Despite the clinical significance, there is a lack of effective therapies for intercepting the progression of preinvasive to invasive adenocarcinoma. To uncover determinants of early disease emergence and progression, we used integrated single-cell approaches, including scRNA-seq, multiplexed imaging mass cytometry and spatial transcriptomics, to construct the first high-resolution map of the composition, lineage/functional states, developmental trajectories and multicellular crosstalk networks from microdissected non-solid (preinvasive) and solid compartments (invasive) of individual part-solid nodules. We found that early disease initiation and subsequent progression are associated with the evolution of immune-suppressive cellular phenotypes characterized by decreased cytotoxic CD8 T and NK cells, increased T cell exhaustion and accumulation of immunosuppressive regulatory T cells (Tregs) and M2-like macrophages expressing TREM2. Within Tregs, we identified a unique population of 4-1BB+ Treg subset enriched for the IL2-STAT5 suppressive pathway with transcription profiles supporting discrete metabolic alterations. Spatial analysis showed increased density of suppressive immune cells around tumor cells, increased exhaustion phenotype of both CD4 and CD8 T cells expressing chemokine CXCL13, and spatial micro-complex of endothelial and lymphocyte interactions within tertiary lymphoid structures. The single-cell architecture identifies determinants of early disease emergence and progression, which may be developed not only as diagnostic/prognostic biomarkers but also as targets for disease interception. Additionally, our dataset constitutes a valuable resource for the preinvasive lung cancer research community.

cancer biology↗

Premature thymic involution in young Foxn1lacz mutant mice causes peripheral T cell phenotypes similar to aging-induced immunosenescence

The thymus is a primary lymphoid organ generating self-restricted and self-tolerant naive T-cells. Early in life the thymus starts to involute, resulting in decreased naive T-cell output which may be more self-reactive, leading to an increased prevalence of autoimmunity. A decrease in the transcription factor FOXN1 is an early event in thymic involution. Using the Foxn1lacz model, we studied how premature thymic involution affects the thymic microenvironment, thymocytes, and peripheral T cell immunity. We found that early thymic involution led to aged-like thymic epithelial cells that resulted in aged-like thymocyte phenotypes, with a significant decrease in CD4+ single-positive T-cells. We also observed severe lymphopenia in Foxn1lacz mice caused by the premature decrease in T-cell production, resulting in a peripheral T-cell phenotype similar to de novo aged peripheral T-cells. Moreover, following T cell receptor stimulation, Foxn1lacz peripheral T cells had reduced IL-2 secretion and strong initial IFN-g responses, resembling aged wild-type peripheral T-cell responses. Lastly, influenza response in Foxn1lacz had a reduction in some aspects of T cell responses to influenza infection, similar to thymectomized mice. Our study shows an independent and direct impact of premature thymic involution on both thymopoiesis and peripheral immune niches likely contributing to immunosenescence and inflammaging as observed in the elderly population.

immunology↗

Transcriptome Profiling and Characterization of Peritoneal Metastasis Ovarian Cancer Xenografts in Humanized Mice

BackgroundAlthough immunotherapy has not yet been as successful in ovarian cancer (OC), it remains a potential therapeutic strategy. Preclinical models of OC are necessary to evaluate the efficacy of immuno-oncology (IO) drugs targeting human cancer and immune components but have been underutilized. Developing mouse models with a humanized (Hu) immune system can help understand the human immune response to IO drugs, including immune checkpoint inhibitors (ICIs), which have demonstrated limited effectiveness in OC patients. MethodsWe established OC xenograft Hu-mouse models by intraperitoneally injecting luciferase-expressing SKOV-3 Luc and OVCAR-3 Luc OC cells into CD34+ Hu-mice. Tumor growth was monitored through bioluminescence imaging (BLI). We assessed the efficacy of PD-1 blockade with pembrolizumab in the SKOV-3 Luc Hu-mouse model. The immune profiles of the tumors were characterized using colorimetric immunostaining and flow cytometry. Additionally, we analyzed RNA-seq data to investigate the gene expression signature of pembrolizumab refractory tumors. ResultsWe confirmed tumor development in both OC cell lines within CD34+ Hu-mice. In these models, human lymphocyte and myeloid cell subsets were present in the tumors, draining lymph nodes, blood, and spleens. The SKOV-3 Luc tumor-bearing Hu-mice did not respond to pembrolizumab monotherapy. These tumors exhibited a high presence of tumor-infiltrating macrophages. Tumors in Hu-mice unresponsive to pembrolizumab showed a lower abundance of CD8+ T-cells, memory B cells, plasma cells, and a higher proportion of naive M0 macrophages and mast cells compared to the PBS control. Furthermore, we identified 43 significantly enriched gene sets in these tumors. The differentially expressed genes (DEGs) were predominantly enriched in HDAC class I, RB1, KLF1/3, TCF21, MYD88, SMARCE1 target genes, and genes associated with epithelial-mesenchymal transition (EMT) and fibroblasts. ConclusionOur xenograft Hu-mouse model of OC provides a valuable tool for investigating the efficacy of IO drugs. The insights gained from this model offer potential avenues to explore mechanisms of resistance to PD-1/PD-L1 blockade in OC.

cancer biology↗

Active site mutations of F420-dependent alkene reductases reverse stereoselectivity

Ene-reductases from the Flavin/Deazaflavin Oxidoreductase (FDOR) family have potential value in biocatalysis as they typically exhibit complementary stereoselectivity to the widely utilized Old Yellow Enzyme (OYE) family, yet they are comparatively poorly understood at a mechanistic level. Here, we use a rational design approach to generate a library of 46 active site mutants of two FDORs from Mycobacterium smegmatis and examine the effects on conversion and stereoselectivity against a panel of substrates. Analysis of the effects of these mutations on stereoselectivity across all substrates revealed that the catalytic mechanism is highly sensitive to the polarity of the immediate active site. A conserved active site tyrosine in these enzymes, which does not serve as the proton donor, strongly affects stereochemical outcomes with C- (but not C{beta}-) substituted substrates. Notably, a Tyr-Met mutation at this position reversed the diastereomeric excess (de) with (R)-carvone from 85.3% to -17.3% (cis/trans). Additionally, this mutation significantly increases activity with (1S)- verbenone. Finally, we show that the altered stereoselectivity is not due to a "flipped" substrate binding mode in these mutants, but rather that the hydrogenation mode is altered to favor syn relative to anti addition. These results show that the FDORs are highly engineerable and that, despite their superficial similarity, the OYE and FDOR families differ in crucial mechanistic aspects.

synthetic biology↗

A F420-dependent single domain chemogenetic tool for protein de-dimerization

Protein-protein interactions (PPIs) mediate many fundamental cellular processes and their control through optically or chemically responsive protein domains has a profound impact on basic research and some clinical applications. Most available chemogenetic methods induce the association, i.e., dimerization or oligomerization, of target proteins, and the few available dissociation approaches either break large oligomeric protein clusters or heteromeric complexes. Here, we have exploited the controlled dissociation of a dimeric oxidoreductase from mycobacteria (MSMEG_2027) by its native cofactor, F420, which is not present in mammals, as a bioorthogonal monomerization switch. We found that in the absence of F420, MSMEG_2027 forms a unique domain-swapped dimer that occludes the cofactor binding site. Substantial remodelling of the intertwined N-terminal helix upon F420 binding results in the dissolution of the dimer. We then show that MSMEG_2027 can be expressed as fusion proteins in human cells and apply it as a tool to induce and release MAPK/ERK signalling downstream of a chimeric fibroblast growth factor receptor 1 (FGFR1) tyrosine kinase. This F420-dependent chemogenetic de-dimerization tool is stoichiometric, based on a single domain and presents a novel mechanism to investigate protein complexes in situ.

synthetic biology↗

Asymmetric ene-reduction of α,β-unsaturated compounds by F420-dependent oxidoreductases A (FDOR-A) enzymes from Mycobacterium smegmatis

The stereoselective reduction of alkenes conjugated to electron-withdrawing groups by ene-reductases has been extensively applied to the commercial preparation of fine chemicals. Although several different enzyme families are known to possess ene-reductase activity, the Old Yellow Enzyme (OYE) family has been the most thoroughly investigated. Recently, it was shown that a subset of ene-reductases belonging to the flavin/deazaflavin oxidoreductase (FDOR) superfamily exhibit enantioselectivity that is generally complementary to that seen in the OYE family. These enzymes belong to one of several FDOR subgroups that use the unusual deazaflavin cofactor F420. Here, we explore several enzymes of the FDOR-A subgroup, characterizing their substrate range and enantioselectivity, including the complete conversion of both isomers of citral to (R)-citronellel with 99% ee. Protein crystallography combined with computational docking has allowed the observed stereoselectivity to be mechanistically rationalized for two enzymes. These findings add further support for the FDOR and OYE families of ene-reductases being generally stereocomplementary to each other and highlight their potential value in asymmetric ene-reduction.

biochemistry↗

Mechanisms underlying the reprogramming of mouse embryonic fibroblasts to thymic epithelial cells

Thymic epithelial cells (TECs) are a critical functional component of the thymuss ability to generate T cells for the adaptive immune system in vertebrates. However, no in vitro system for studying TEC function exists. Overexpression of the transcription factor FOXN1 initiates reprogramming of fibroblasts into TEC-like cells (iTECs) that support T cell differentiation in culture or after transplant. In this study, we characterized iTEC reprogramming at the cellular and molecular level to determine how reprogramming proceeds and identify mechanisms that can be targeted for improving this process. These data show that iTEC reprogramming consists of discrete gene expression changes that differ in early and late reprogramming, and that iTECs upregulate markers of both cortical and medullary TEC (cTEC and mTEC) lineages, although mTEC differentiation is blocked at a progenitor stage. We demonstrate that promoting proliferation enhances iTEC generation, and that Notch inhibition allows induction of mTEC differentiation. Finally, we show that a major difference between iTEC and fetal TEC is the expression of MHCII. This study supports future efforts to improve iTEC reprogramming for both research and translational uses.

developmental biology↗

Cytoplasmic zinc regulates IL-1β production by monocytes/macrophages via mTORC1-induced glycolysis in rheumatoid arthritis (RA)

The essential micronutrient zinc plays regulatory roles in immune responses through its ability to affect signaling pathways. In activated monocytes/macrophages, signaling networks mediate metabolic reprogramming in order to meet the demands of participating in immune responses. Despite its known immunoregulatory roles, the effect of zinc on metabolic reprogramming in monocytes/macrophages remains unclear. Here, we demonstrate that cytoplasmic bioavailable zinc is essential for regulating IL-1{beta} production in activated human monocytes/macrophages downstream of mTORC1-induced glycolysis. The cytoplasmic zinc level was influenced by extracellular zinc concentration through a zinc-specific importer, Zip8, which was markedly increased in monocytes of patients with rheumatoid arthritis (RA), a chronic inflammatory disease, and even in LPS-stimulated monocytes/macrophages of healthy individuals. Mechanically, phosphorylation of S6 kinase, a substrate of mTORC1, was significantly enhanced by zinc-mediated inhibition of PP2A, an S6 kinase phosphatase. As a result, IL-1{beta} production was increased due to the activation of mTORC1-induced glycolysis. The expression of Zip8 and MT2A, a zinc-inducible gene, and the phosphorylation of S6 kinase by monocytes of RA patients was significantly enhanced compared with those of HCs and Zip8 levels positively correlated with RA clinical parameters, suggesting that Zip8-mediated zinc influx is related to inflammatory conditions. These results provide insight into the role of cytoplasmic bioavailable zinc in the metabolic reprogramming of human monocytes/macrophages which is an essential process for inflammatory responses. One Sentence SummaryCytoplasmic zinc regulates IL-1{beta} production in monocytes/macrophages downstream of mTORC1-S6K-induced glycolysis via zinc-mediated inhibition of PP2A.

immunology↗