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Beechem, J. M.

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

At least 19 recordsLinked to original sources

Breast cancer through the lens of whole transcriptome spatial imaging

Using the worlds first transcriptome-scale spatial imaging of a breast tumor, we assessed what could be learned about one patients disease. We cataloged heterogeneity across 3 morphological regions, 9 spatial domains, 37 cell types, and 1692 pathways. Then, employing a new algorithm for spatially stratified differential expression, we tested >2 million hypotheses about cell types behavior across space. We measured how CD8+ T cells change upon entering the tumor, how cancer cells adapt to nutrient-poor microenvironments, how tumor glycolysis impacts nearby healthy cells, and how low-proliferation zones of the tumor are distinct. We found several instances of druggable biology: the tumors heterogeneity and invasion programs suggested aggressiveness independent of traditional grading; PDCD1 expression and exhaustion limited T-cell activity; cancer cells engaged angiogenic signaling but struggled to proliferate in hypoxic regions; and a tumor subcluster up-regulated lipid metabolism. These findings demonstrate the insights obtainable through spatial profiling of individual tumors.

cancer biology↗

Single-cell Spatial Transcriptional Profiling Uncovers Heterogeneous Cellular Responses to Pathogenic Tau in a Mouse Model of Neurodegeneration

Intracellular tau accumulation contributes to neurodegeneration and systemic dysfunction. Although tau primarily aggregates in neurons as neurofibrillary tangles (NFTs), it also affects other cell types through poorly understood mechanisms. To define the molecular characteristics of tangle-bearing neurons and their influence on surrounding cells, we used CosMx SMI to evaluate the expression of 950 genes in more than 265,000 cells from rTg(tauP301L)4510 tauopathy and control mouse brains. In the cerebral cortex, tau pathology disrupted the excitatory-inhibitory neuron balance and altered pathways critical for myelination, similar myelin changes were observed in postmortem brain tissue from patients with progressive supranuclear palsy. In the hypothalamus, tau accumulation was associated with transcriptional changes linked to pathways involved in body weight and metabolic regulation. These findings reveal molecular mechanisms underlying both cell-autonomous and non-autonomous effects of tauopathy and identify targets for further investigation into tau pathogenesis and its systemic impact.

neuroscience↗

Spatial Multi-Omics Workflow and Analytical Guidelines for Alzheimer's Neuropathology

Spatial biology technologies enable high-dimensional profiling within intact tissues, revealing how molecular and cellular organization drives function and disease. As these platforms gain broader adoption, standardized analytical frameworks are needed to ensure data quality and reproducibility. Here, we present an end-to-end pipeline for the GeoMx Digital Spatial Profiler that simultaneously generates whole-transcriptome and 637-protein measurements from user-defined regions within the same tissue sections. The workflow integrates morphology-guided region selection, quality control, normalization, and multi-modal data interpretation. Applied to formalin-fixed cortical tissues from Alzheimers disease, dementia with Lewy bodies, amyotrophic lateral sclerosis, and controls, the framework resolves spatially distinct molecular domains. Transcript and protein signals diverge across amyloid plaque cores and surrounding glial-rich regions, with RNA-protein concordance varying by disease condition, while single-neuron profiling with and without pathogenic tau deposition illustrates protein assay sensitivity. This dataset provides a rigorously validated resource for spatial multi-omic analyses and establishes broadly applicable guidelines for reliable, reproducible profiling of complex tissues.

neuroscience↗

Tracing colorectal malignancy transformation from cell to tissue scale

The transformation of normal intestinal epithelium into colorectal cancer (CRC) involves coordinated changes across molecular, cellular, and architectural scales; yet, how these layers integrate remains poorly resolved. Here, we survey colorectal tumorigenesis by combining whole-transcriptome spatial molecular imaging (WTx CosMx SMI) with single-nucleus RNA-sequencing (snPATHO-seq) and digital histopathology on colon samples containing reference mucosa, adenomas and carcinomas, as well as a metastatic lymph node. Leveraging (discrete) histological annotations and (continuous) data-driven trajectories, we quantify the dynamics of cellular density, heterogeneity, function and signaling along the reference-adenoma-carcinoma axis, which is concordant in its spatial and molecular definition. This combination of analytical approaches across different data views let us chart tissue transformation across dimensions (physical/transcriptional) and scales (cell/tissue). We resolve [~]3.5 million cells into 43 epithelial, immune, and stromal subpopulations that exhibit a bi-furcating tumor evolution: On the one hand, LGR5+ stem-like epithelial cells are enriched in highly homogeneous proliferative tumor cores. On the other hand, MMP7+ fetal-like states are restricted to immunosuppressive invasive fronts, rich in cancer-associated fibroblasts (CAFs) and tumor-associated macrophages. These subpopulations form concentric spatial layers that organize transformed regions, and their compound aligns with histological malignancy. We further define transition crypts - single colonic crypts with divided histological and transcriptional makeup - that arise from rare crypt fusion or abrupt transformation events. Finally, we trace MMP7+ fetal-like tumor cell states and concomitant myofibroblast-like FAP+ CAFs to lymphovascular invasion sites and matched lymph node metastases, thereby recapitulating invasive programs at single-cell resolution and across sites. In all, we present single cell- and WTx-resolved spatial data that are among the first of their kind. These open up spatial-centric, out-of-the-box analytical avenues to resolve the molecular, cellular and architectural dynamics that attend tissue transformation during CRC onset, progression and dissemination.

cancer biology↗

FastReseg: using transcript locations to refine image-based cell segmentation results in spatial transcriptomics

Spatial transcriptomics (ST) is a rapidly advancing field, yet it is challenged by persistent issues with cell segmentation accuracy, which can bias biological interpretations by making cells appear more similar to their neighbors than they truly are. FastReseg introduces a novel class of algorithm that employs transcriptomic data not to redefine cell boundaries but to rectify inaccuracies within existing image-based segmentation outputs. By combining the rich information from image-based methods with the 3D precision of transcriptomic analysis, FastReseg enhances cell segmentation accuracy. A key innovation of FastReseg approach is its transcript scoring system, which scores each transcript for its goodness-of-fit within host cell using log-likelihood ratio. This scoring system facilitates the quick identification and correction of spatial doublets, i.e. cells erroneously segmented due to close proximity or spatial overlap in 2D. FastReseg approach offers several advantages: it reduces the risks of circularity in deriving cell boundaries from expression data and minimizes spatial-dependent biases arising from erroneous segmentation. It also addresses computational challenges often associated with existing transcript-based methods by introducing a heuristic, modular workflow that efficiently processes large datasets, a critical feature given the increasing size of spatial transcriptomics datasets. Its modular workflow allows for individual components to be optimized and seamlessly integrated back into the overall pipeline, accommodating ongoing advancements in segmentation technology. By enabling efficient management of large datasets and providing a scalable solution for refining cell segmentation, FastReseg is poised to enhance the quality and interpretability of spatial transcriptomics data even as underlying image-based cell segmentation techniques evolve.

bioinformatics↗

Sub-cellular Imaging of the Entire Protein-Coding Human Transcriptome (18933-plex) on FFPE Tissue Using Spatial Molecular Imaging

Single-cell RNA-seq revolutionized single-cell biology, by providing a complete whole transcriptome view of individual cells. Regrettably, this was accomplished only for individual, tissue-dissociated cells. High-plex spatial biology has begun to recover the x, y, and z-coordinates of single-cells, but typically at the expense of far less than whole transcriptome coverage. To solve this problem, Bruker Spatial Biology has accomplished a commercial-grade panel (CosMx(R) Spatial Molecular Imager Whole Transcriptome Panel (WTx)), using 37,872 imaging barcodes, capable of sub-cellular imaging of the entire human protein-coding transcriptome. The imaging barcodes are encoded with 156 bits of information (4 on-cycles and 35 dark-cycles per code), at a Hamming Distance of 4 from each other to achieve a very low false-code detection. Key to achieving this high-plex capability was the ability to manufacture imaging barcodes that require no in-tissue amplification (every barcode is manufactured under GMP to contain exactly 30 fluorescent dyes) and uniform, size-exclusion purified, extremely small imaging barcodes ([~] 20 nm). A detailed study of six different human FFPE tissue types was performed (Colon, Pancreas, Hippocampus, Skin, Breast, Kidney), yielding over 5.4 billion transcripts from 2.7 million cells. We counted over 1,550 transcripts-per-cell on average and observed 900 unique genes per cell (measured as the median). Single fixed-cells containing well over 10,000 subcellularly imaged transcripts were accomplished. Advancing single-cell imaging to the whole transcriptome level opens a single unified approach to accomplish essentially all single-cell experiments, both imaging and non-imaging. Depending upon the sample type (e.g. fixed-cells, organoids, tissue sections, etc.), the transcripts per cell and genes per cell measured using the whole transcriptome panel often exceeds that obtained by the highest-resolution single-cell RNA-seq, can be performed on a single 5 {micro}m FFPE tissue section, with no dissociation bias (every cell is counted). Pathway analysis within the tumor bed of a colon adenocarcinoma sample found evidence of enrichment in pathways suggestive of an aggressive tumor type, and localized ligand-receptor analysis showed spatially restricted patterns related to adhesion, migration, and proliferation. The high-dimensional whole transcriptome data is streamed directly to a cloud-based Spatial Informatics Platform, allowing for the scalable processing of millions-of-single-cells and billions-of-transcripts per operation. The WTx data are combined with high-resolution antibody-based cell-morphology imaging and data-driven machine-learning cell segmentation algorithms, to generate the most complete view of single cell and sub-cellular spatial biology that has ever been obtained.

genomics↗

InSituCor: a toolkit for discovering non-trivial spatial correlations in spatial transcriptomics

Spatial transcriptomics presents the best kind of problem: how to find the many biological insights hidden within complex datasets. Spatially correlated genes can reveal high-interest phenomena like cell-cell interactions and latent variables. We introduce InSituCor, a toolkit for discovering modules of spatially correlated genes. A major contribution is that InSituCor returns only correlations not explainable by obvious factors like the cell type landscape; this spares precious analyst effort for non-trivial findings. InSituCor supports both unbiased discovery of whole-dataset correlations and knowledge-driven exploration of genes of interest. As a special case, it evaluates ligand-receptor pairs for spatial co-regulation.

bioinformatics↗

Therapy-associated remodeling of pancreatic cancer revealed by single-cell spatial transcriptomics and optimal transport analysis

In combination with cell intrinsic properties, interactions in the tumor microenvironment modulate therapeutic response. We leveraged high-plex single-cell spatial transcriptomics to dissect the remodeling of multicellular neighborhoods and cell-cell interactions in human pancreatic cancer associated with specific malignant subtypes and neoadjuvant chemotherapy/radiotherapy. We developed Spatially Constrained Optimal Transport Interaction Analysis (SCOTIA), an optimal transport model with a cost function that includes both spatial distance and ligand-receptor gene expression. Our results uncovered a marked change in ligand-receptor interactions between cancer-associated fibroblasts and malignant cells in response to treatment, which was supported by orthogonal datasets, including an ex vivo tumoroid co-culture system. Overall, this study demonstrates that characterization of the tumor microenvironment using high-plex single-cell spatial transcriptomics allows for identification of molecular interactions that may play a role in the emergence of chemoresistance and establishes a translational spatial biology paradigm that can be broadly applied to other malignancies, diseases, and treatments.

cancer biology↗

An information theoretic approach to detecting spatially varying genes

Identifying genes with spatially coherent expression patterns is a key task in spatial transcriptomics. We adopt an information theoretic perspective on this problem by equating the degree of spatial coherence with the mutual information between nearby expression measurements. To avoid the notoriously difficult problem of computing mutual information, we use modern methods of approximation, in a method we call maximization of spatial information (Maxspin). As well as being highly scalable, we demonstrate improved accuracy across several spatial transcriptomics platforms and a variety of simulations when compared to both existing specialized methods and traditional spatial statistics methods. We use the method to analyze a renal cell carcinoma sample profiled using CosMx Spatial Molecular Imaging, revealing previously undescribed gene expression patterns.

bioinformatics↗

Insitutype: likelihood-based cell typing for single cell spatial transcriptomics

Accurate cell typing is fundamental to analysis of spatial single-cell transcriptomics, but legacy scRNA-seq algorithms can underperform in this new type of data. We have developed a cell typing algorithm, Insitutype, designed for statistical and computational efficiency in spatial transcriptomics data. Insitutype is based on a likelihood model that weighs the evidence from every expression value, extracting all the information available in each cells expression profile. This likelihood model underlies a Bayes classifier for supervised cell typing, and an Expectation-Maximization algorithm for unsupervised and semi-supervised clustering. Insitutype also leverages alternative data types collected in spatial studies, such as cell images and spatial context, by using them to inform prior probabilities of cell type calls. We demonstrate rapid clustering of millions of cells and accurate fine-grained cell typing of kidney and non-small cell lung cancer samples.

bioinformatics↗

Ultra High-Plex Spatial Proteogenomic Investigation of Giant Cell Glioblastoma Multiforme Immune Infiltrates Reveals Distinct Protein and RNA Expression Profiles

A deeper understanding of complex biological processes, including tumor development and immune response, requires ultra high-plex, spatial interrogation of multiple "omes". Here we present the development and implementation of a novel spatial proteogenomic (SPG) assay on the GeoMx(R) Digital Spatial Profiler platform with NGS readout that enables ultra high-plex digital quantitation of proteins (> 100-plex) and RNA (whole transcriptome, > 18,000-plex) from a single FFPE sample. This study highlighted the high concordance, R > 0.85, and <11% change in sensitivity between SPG assay and the single analyte -assays on various cell lines and tissues from human and mouse. Furthermore, we demonstrate that the SPG assay was reproducible across multiple users. When used in conjunction with advanced cellular neighborhood segmentation, distinct immune or tumor RNA and protein targets were spatially resolved within individual cell subpopulations in human colorectal cancer and non-small cell lung cancer. We used the SPG assay to interrogate 23 different glioblastoma multiforme samples across 4 pathologies. The study revealed distinct clustering of both RNA and protein based on pathology and anatomic location. The in-depth investigation of giant cell glioblastoma multiforme revealed distinct protein and RNA expression profiles compared to that of the more common glioblastoma multiforme. More importantly, the use of spatial proteogenomics allowed simultaneous interrogation of critical protein post-translational modifications alongside whole transcriptomic profiles within the same distinct cellular neighborhoods.

cancer biology↗

Background modeling, Quality Control and Normalization for GeoMx RNA data with GeoDiff

BackgroundNanoStrings GeoMx Digital Spatial Profiler (DSP) RNA assay can measure mRNA from hundreds of regions of customizable shape and size, yet it gives unique challenge in Quality Control(QC) and normalizating due to the omnipresent background noise incurred by the non-specific probe binding, which could not be addressed by conventional methods. Results and discussionUsing Poisson Background model, Background Score Test, Negative Binomial threshold model and Poisson threshold model for normalization from the R package GeoDiff, we perform tasks including size factor estimation, QC and normalization on GoeMx RNA assay data. They are shown to outperform conventional methods like Limit of Quantification for QC as to consistency/false positive rate and 75% quantile normalization as to eliminating technical variability and recovering true signal. ConclusionsWe present a statistical model based workflow for QC and normalizing GeoMx RNA data using GeoDiff, justified by statistical theory and validated by real/simulated data.

bioinformatics↗

High-Plex Multiomic Analysis in FFPE Tissue at Single-Cellular and Subcellular Resolution by Spatial Molecular Imaging

The Spatial Molecular Imaging platform (CosMxTM SMI, NanoString Technologies, Seattle, WA) utilizes high-plex in-situ imaging chemistry for both RNA and protein detection. This automated instrument provides 1000s of plex, at high sensitivity (1 to 2 copies/cell), very low error rate (0.0092 false calls/cell) and background ([~]0.04 counts/cell). The imaging system generates three-dimensional super-resolution localization of analytes at [~]2 million cells per sample, four samples per run. Cell segmentation is morphology-based using antibodies, compatible with FFPE samples. Multiomic data (980 RNAs, 108 proteins) were measured at subcellular resolution using FFPE tissues (non-small cell lung (NSCLC) and breast cancer) and allowed identification of over 18 distinct cell types, 10 unique tumor microenvironments, and 100 pairwise ligand-receptor interactions. Over 800,000 single cells and [~]260 million transcripts data are released into the public domain allowing extended data analysis by the entire spatial biology research community.

genomics↗

Spatially resolved whole transcriptome profiling in human and mouse tissue using Digital Spatial Profiling

Emerging spatial profiling technology has enabled high-plex molecular profiling in biological tissues, preserving the spatial and morphological context of gene expression. Here we describe expanding the chemistry for the Digital Spatial Profiling platform to quantify whole transcriptomes in human and mouse tissues using a wide range of spatial profiling strategies and sample types. We designed multiplexed in situ hybridization probe pools targeting the protein-coding genes in the human and mouse transcriptomes, hereafter referred to as the human or mouse Whole Transcriptome Atlas (WTA). We validated the human and mouse WTA using cell lines to demonstrate concordance with orthogonal gene expression profiling methods in profiled region sizes ranging from ~10-500 cells. By benchmarking against bulk RNAseq and fluorescence in situ hybridization, we demonstrate robust transcript detection possible down to ~100 transcripts per region. To assess the performance of WTA across tissue and sample types, we applied WTA to biological questions in cancer, molecular pathology, and developmental biology. We show that spatial profiling with WTA can detect expected spatial gene expression differences between tumor and tumor microenvironment, identify spatial disease-specific heterogeneity in gene expression in histological structures of the human kidney, and comprehensively map transcriptional programs in anatomical substructures of nine organs in the developing mouse embryo. Digital Spatial Profiling technology with the WTA assays provides a flexible method for spatial whole transcriptome profiling applicable to diverse tissue types and biological contexts.

genomics↗

Transcriptome-wide spatial RNA profiling maps the cellular architecture of the developing human neocortex

Spatial genomic technologies can map gene expression in tissues, but provide limited potential for transcriptome-wide discovery approaches and application to fixed tissue samples. Here, we introduce the GeoMX Whole Transcriptome Atlas (WTA), a new technology for transcriptome-wide spatial profiling of tissues with cellular resolution. WTA significantly expands the Digital Spatial Profiling approach to enable in situ hybridisation against 18,190 genes at high-throughput using a sequencing readout. We applied WTA to generate the first spatial transcriptomic map of the fetal human neocortex, validating transcriptome-wide spatial profiling on formalin-fixed tissue material and demonstrating the spatial enrichment of autism gene expression in deep cortical layers. To demonstrate the value of WTA for cell atlasing, we integrated single-cell RNA-sequencing (scRNA-seq) and WTA data to spatially map dozens of neural cell types and showed that WTA can be used to directly measure cell type specific transcriptomes in situ. Moreover, we developed computational tools for background correction of WTA data and accurate integration with scRNA-seq. Our results present WTA as a versatile transcriptome-wide discovery tool for cell atlasing and fixed tissue spatial transcriptomics.

genomics↗

A single-cell and spatial atlas of autopsy tissues reveals pathology and cellular targets of SARS-CoV-2

The SARS-CoV-2 pandemic has caused over 1 million deaths globally, mostly due to acute lung injury and acute respiratory distress syndrome, or direct complications resulting in multiple-organ failures. Little is known about the host tissue immune and cellular responses associated with COVID-19 infection, symptoms, and lethality. To address this, we collected tissues from 11 organs during the clinical autopsy of 17 individuals who succumbed to COVID-19, resulting in a tissue bank of approximately 420 specimens. We generated comprehensive cellular maps capturing COVID-19 biology related to patients demise through single-cell and single-nucleus RNA-Seq of lung, kidney, liver and heart tissues, and further contextualized our findings through spatial RNA profiling of distinct lung regions. We developed a computational framework that incorporates removal of ambient RNA and automated cell type annotation to facilitate comparison with other healthy and diseased tissue atlases. In the lung, we uncovered significantly altered transcriptional programs within the epithelial, immune, and stromal compartments and cell intrinsic changes in multiple cell types relative to lung tissue from healthy controls. We observed evidence of: alveolar type 2 (AT2) differentiation replacing depleted alveolar type 1 (AT1) lung epithelial cells, as previously seen in fibrosis; a concomitant increase in myofibroblasts reflective of defective tissue repair; and, putative TP63+ intrapulmonary basal-like progenitor (IPBLP) cells, similar to cells identified in H1N1 influenza, that may serve as an emergency cellular reserve for severely damaged alveoli. Together, these findings suggest the activation and failure of multiple avenues for regeneration of the epithelium in these terminal lungs. SARS-CoV-2 RNA reads were enriched in lung mononuclear phagocytic cells and endothelial cells, and these cells expressed distinct host response transcriptional programs. We corroborated the compositional and transcriptional changes in lung tissue through spatial analysis of RNA profiles in situ and distinguished unique tissue host responses between regions with and without viral RNA, and in COVID-19 donor tissues relative to healthy lung. Finally, we analyzed genetic regions implicated in COVID-19 GWAS with transcriptomic data to implicate specific cell types and genes associated with disease severity. Overall, our COVID-19 cell atlas is a foundational dataset to better understand the biological impact of SARS-CoV-2 infection across the human body and empowers the identification of new therapeutic interventions and prevention strategies.

genomics↗

Single-nucleus and spatial transcriptomics of archival pancreatic cancer reveals multi-compartment reprogramming after neoadjuvant treatment

Pancreatic ductal adenocarcinoma (PDAC) remains a treatment-refractory disease. Characterizing PDAC by mRNA profiling remains particularly challenging. Previously identified bulk expression subtypes were influenced by contaminating stroma and have not yet informed clinical management, whereas single cell RNA-seq (scRNA-seq) of fresh tumors under-represented key cell types. Here, we developed a robust single-nucleus RNA-seq (snRNA-seq) technique for frozen archival PDAC specimens and used it to study both untreated tumors and those that received neoadjuvant chemotherapy and radiotherapy (CRT). Gene expression programs learned across untreated malignant cell and fibroblast profiles uncovered a clinically relevant molecular taxonomy with improved prognostic stratification compared to prior classifications. Moreover, in the increasingly-adopted neoadjuvant treatment context, there was a depletion of classical-like phenotypes in malignant cells in favor of basal-like phenotypes associated with TNF-NFkB and interferon signaling as well as the presence of novel acinar and neuroendocrine classical-like states, which may be more resilient to cytotoxic treatment. Spatially-resolved transcriptomics revealed an association between malignant cells expressing these basal-like programs and higher immune infiltration with increased lymphocytic content, whereas those exhibiting classical-like programs were linked to sparser macrophage-predominant microniches, perhaps pointing to susceptibility to distinct therapeutic strategies. Our refined molecular taxonomy and spatial resolution can help advance precision oncology in PDAC through informative stratification in clinical trials and insights into differential therapeutic targeting leveraging the immune system.

genomics↗

Advances in mixed cell deconvolution enable quantification of cell types in spatially-resolved gene expression data

We introduce SpatialDecon, an algorithm for quantifying cell populations defined by single cell RNA sequencing within the regions of spatially-resolved gene expression studies. It obtains cell abundance estimates that are spatially-resolved, granular, and paired with highly multiplexed gene expression data. SpatialDecon incorporates several advancements in the field of gene expression deconvolution. We propose an algorithm based in log-normal regression, attaining sometimes dramatic performance improvements over classical least-squares methods. We compile cell profile matrices for 27 tissue types. We identify genes whose minimal expression by cancer cells makes them suitable for immune deconvolution in tumors. And we provide a lung tumor dataset for benchmarking immune deconvolution methods. In a lung tumor GeoMx DSP experiment, we observe a spatially heterogeneous immune response in intricate detail and identify 7 distinct phenotypes of the localized immune response. We then demonstrate how cell abundance estimates give crucial context for interpreting gene expression results.

bioinformatics↗