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Lorenzi, V.

Publications and source records attributed to Lorenzi, V..

11 recordsLinked to original sources

Multi-scale modeling of human tissues from spatial transcriptomics with TERRA

Spatial transcriptomics maps gene expression at cellular resolution, revealing how cells organize into multicellular niches. Yet computational analyses remain dataset-specific, without a transferable representation of tissue organization that generalizes across datasets, tasks and tissues or predicts how tissues behave under perturbation. We present TERRA, a foundation model pretrained on 112 million human cells profiled by spatial transcriptomics. From a single pretrained backbone, TERRA yields embeddings at the scale of cells, the genes they express and the neighborhoods in which they reside, and supports spatial in silico perturbation, all applied zero-shot to unseen tissues. At the cell level, in newly generated spatial data for developing pancreas, TERRA identified an islet-associated capillary state which we posit represents a developmental precursor of the mature islet microvasculature. At the gene level, in untreated kidney sections, in silico knockout of immune-checkpoint targets predicted a gene program of immune-checkpoint-blockade-associated nephrotoxicity, which we validated in treatment-exposed tissue and recovered in blood. At the neighborhood level, TERRA mapped macrophages across tissues to identify recurring cross-organ niches, which we term archetypes, including a tumor-boundary niche associated with poor prognosis in kidney cancer. Together, TERRA captures the spatial and multicellular logic of human tissue and predicts, in silico, its response to perturbation, providing a multi-scale framework for tissue biology, therapeutic development and clinical application.

genomics↗

An integrated multimodal pan-organ atlas of the female reproductive system across the lifespan contextualises gynaecological pathologies

Single cell transcriptomics has transformed our knowledge of reproductive tissues, yet studies remain largely organ-specific and temporally limited, leaving an incomplete picture of how cell types are distributed across the reproductive system over a lifetime. Gynaecological conditions affect more than one in four females and frequently span multiple organs and life stages. To advance our understanding and treatment of these conditions, an integrated cellular reference is essential. Here we present the Human Female Reproductive System Cell Atlas v1: a single-cell transcriptomic resource integrating more than 2M cells across the ovary, fallopian tube, uterus, cervix and vagina over the lifespan and menstrual cycle, further integrated with spatial transcriptomics and chromatin accessibility profiling to define 210 cell types through community-based annotation. Cross-organ integration resolves shared and organ-specific cellular states, identifying uterine-specific perivascular populations lining uterine spiral arteries, hypoxia-sensing type 3 innate lymphoid cells (ILC3s) enriched in the uterus, and lipid-associated macrophages with distinct subsets in each reproductive organ, including a previously undescribed population shared between the uterus and fallopian tube. Cross-organ integration enables detection of ectopic epithelial populations in otherwise healthy donors, including endometrial-like cells within a paediatric ovary consistent with early endometriosis. Integration with genome-wide association studies (GWAS) reveals that risk variants for major gynecological conditions act in mesenchymal cell states defined by specific transcriptional programmes and spatial or temporal context - for instance, heavy menstrual bleeding risk is enriched in basal fibroblasts (SFRP5) of the regenerative endometrial compartment. An integrated chromatin accessibility atlas provides peak-to-gene maps across reproductive cell types, enabling nomination of disease effector genes and providing the first regulatory evidence linking a Polyendocrine Metabolic Ovarian Syndrome (PMOS) risk locus to INHBB in granulosa cells. Together, this resource establishes a cellular and molecular framework for reproductive biology and the pathogenesis of neglected gynaecological conditions.

Cell Biology↗

Full-thickness spatial transcriptomics of the human uterus reveals basalis niche architecture and regeneration gradients during menstrual breakdown

The human endometrium (uterine lining) undergoes cyclical breakdown and scarless regeneration during each menstrual cycle, representing an exceptional model of adult tissue renewal. Regeneration is driven primarily by progenitor cells retained within the deep, basalis compartment during menstruation, yet the full-depth spatiotemporal dynamics of this process have remained understudied due to anatomical and technical limitations. Here, we map spatial gene-expression gradients across the full thickness of the human endometrium, from the myometrial-endometrial boundary to the luminal surface, using high-resolution spatial transcriptomics integrated with single-cell transcriptomics. We profile more than ten million cells from biopsies, hysterectomy samples and menstrual fluid, enriching for the menstrual and proliferative phases, which are underrepresented in previous studies. We show that endometrial breakdown, regeneration and rapid luminal re-epithelialisation are concurrent rather than temporally separated, organised across distinct tissue compartments, revealing a mode of tissue renewal in which shedding and repair operate simultaneously. Continuous basalis-to-luminal transcriptional gradients link progenitor identity, niche signalling, and tissue remodelling, defining a coordinated regenerative axis spanning the full tissue depth. We resolve the basalis epithelial niche at unprecedented molecular resolution, identifying for the first time a discrete, predominantly quiescent progenitor-like epithelial subset and specialised supporting SFRP5+ fibroblasts, both characterised by WNT inhibition, alongside lymphoid aggregates, forming a multi-component architecture that persists after menopause, consistent with a long-lived regenerative reservoir. Together, these findings establish spatial transcriptional gradients as a central organising principle of endometrial renewal, providing a molecular framework for understanding disorders of menstruation, implantation failure, and impaired tissue repair.

cell biology↗

A transient epithelial plasticity state defines the developmental window for uterine gland specification

Uterine gland development and function is essential for reproduction and womens health, yet the epithelial cell states and signaling interactions that govern gland fate specification are not well understood. Here, integration of single cell and spatial transcriptomics with organoid culture, lineage tracing, and genetic and hormonal perturbation models were used to define mechanisms regulating postnatal uterine epithelial differentiation. A developmentally restricted epithelial plasticity state was identified that precedes luminal and glandular cell lineage segregation and is accompanied by dynamic reorganization of stromal-epithelial communication during uterine differentiation. Pseudotime analysis revealed progressive acquisition of gland-associated programs, including forkhead box A2 (Foxa2), retinoic acid metabolic genes, and epithelial estrogen receptor alpha (Esr1) expression. Functional studies revealed that ESR1 acquisition and retinoic acid signaling suppress the multilayered organoid phenotype associated with epithelial plasticity, thereby promoting epithelial specification and lineage commitment. Moreover, neonatal hormonal perturbation of adenogenesis and conditional deletion of Foxa2 abolished this organoid phenotype. Together, these findings demonstrate that ESR1 acquisition, retinoic acid signaling and FOXA2-dependent glandular differentiation each restrict a transient epithelial plasticity state, coupling the loss of developmental plasticity to the emergence of the glandular lineage.

developmental biology↗

An integrated single cell and spatial omics atlas of human prenatal development

Single cell genomics has enabled analysis of human prenatal development at unprecedented resolution. However, most studies have relied on dissociated tissues during restricted windows of development, limiting insights into how spatially distributed networks of cells, and multicellular niches emerge and adapt to distinct organ microenvironments in situ. Moreover, existing human developmental atlases have not yet been harmonised, and we thus lack a comprehensive catalogue of known cell types in the developing human body. Here, we introduce the Human Developmental Cell Atlas (HDCA), a unified structural, cellular and molecular resource for prenatal human development. The HDCA integrates published and unpublished single cell/nucleus RNAseq atlases across prenatal organs, and includes a newly generated, spatially resolved, multimodal cell atlas of intact human embryos. Spanning 4-22 post conceptional weeks, capturing embryonic and early to mid fetal stages, the HDCA contains [~]4.6 million cells/nuclei which resolve into [~]450 cell types, explorable with a bespoke web portal. For a global overview of the human embryos multicellular communities, we applied unsupervised deep learning to our intact human embryo spatial data, charting 114 tissue niches that are structural and signalling hubs for the cellular interactions of the embryo. Guided by these niches, we profiled cellular networks over space and time, not examinable using single-organ atlases. In so doing, we revealed tissue-specific fibroblast patterning from previously undescribed mesenchyme progenitors, early diversification of organ-specific blood capillaries and lymphatic vasculature, emergence of neural crest cell fates, the formation of placode-and neural crest-derived peripheral sensory neurons, and how tissue niches guide peripheral neuron maturation and axonal migration. The HDCA thus serves as a comprehensive step towards a comprehensive understanding of human prenatal development, and a template towards unravelling the biology of congenital disorders.

developmental biology↗

Decoding human B cell ontogeny in prenatal and adult bone marrow and in vitro models via single-cell multiomics

In humans, the bone marrow becomes the primary site for B lymphopoiesis during the second trimester of pregnancy and continues throughout life. Prenatal and adult B cell progenitors play distinct roles in the aetiology and pathology of paediatric and adult hematopoietic malignancies, though the molecular drivers of these differences remain unclear. Here, we created a comprehensive multiomics atlas of over 500k cells covering immune and stromal compartment from prenatal and adult bone marrow, enabling high-resolution analysis of the cell-intrinsic and cell-extrinsic processes that modulate prenatal and adult B lymphopoiesis. Even though B cells follow broadly similar developmental trajectories, we identify a novel postnatal lateCLP subset equivalent to prenatal preProB cells, and uncover prenatal cells carry several signatures characteristic of leukemias, including enhanced proliferation, higher RAG1/RAG2 activity, extrinsic B cell signals such as IL7, and lower retention signals in the bone marrow. We also developed and characterised, at both cellular and molecular levels, a new experimental framework for generating B cell precursors from human induced pluripotent stem cells (hiPSCs), and show that it faithfully recapitulates key stages of B cell differentiation. Together, our single-cell multiomics atlas of B lymphopoiesis in vivo and in vitro offers detailed insights into the unique molecular features of prenatal and adult B cell lymphopoiesis, and serves as a powerful resource for investigating the early events that contribute to haematological disorders.

immunology↗

Atlas-scale metabolic activities inferred from single-cell and spatial transcriptomics

Metabolism supplies energy, building blocks, and signaling molecules vital for cell function and communication, but methods to directly measure it at single-cell and/or spatial resolutions remain technically challenging and inaccessible for most researchers. Single-cell and spatial transcriptomics offer high-throughput data alternatives with a rich ecosystem of computational tools. Here, we present scCellFie, a computational framework to infer metabolic activities from human and mouse transcriptomic data at single-cell and spatial resolution. Applied to [~]30 million cell profiles, we generated a comprehensive metabolic atlas across human organs, identifying organ- and cell-type-specific activities. In the endometrium, scCellFie reveals metabolic programs contributing to healthy tissue remodeling during the menstrual cycle, with temporal patterns replicated in data from in vitro cultures. We also uncover disease-associated metabolic alterations in endometriosis and endometrial carcinoma, linked to proinflammatory macrophages, and metabolite-mediated epithelial cell communication, respectively. Ultimately, scCellFie provides a scalable toolbox for extracting interpretable metabolic functionalities from transcriptomic data.

bioinformatics↗

Spatiotemporal map of the developing human reproductive tract at single-cell resolution

The human reproductive tract plays an essential role in species perpetuation. Its development involves complex processes of sex specification, tissue patterning and morphogenesis, which, if disrupted, can cause lifelong health issues, including infertility. Here, we generated an extensive single-cell and spatial multi-omic atlas of the human reproductive tract during prenatal development, which allowed us to answer questions that smaller-scale, organ-focused experiments could not address before. We identified potential regulators of sexual dimorphism in reproductive organs, pinpointing novel genes involved in urethral canalisation of the penis, with relevance to hypospadias. By combining histological features with gene expression data, we defined the transcription factors and cell signalling events required for the regionalisation of the Mullerian and Wolffian ducts. This led to a refinement of how the HOX code is established in the distinct reproductive organs, including increased expression of thoracic HOX genes in the rostral mesenchyme of the fallopian tube and epididymis. Our study further revealed that the epithelial regionalisation of the fallopian tube and epididymis required for sperm maturation in adulthood is established early in development. In contrast, later events in gestation or postnatally are necessary for the regionalisation of the uterocervical canal epithelium. By mapping sex-specific reproductive tract regionalisation and differentiation at the cellular level, our study offers valuable insights into the causes and potential treatments of reproductive disorders.

developmental biology↗

An integrated single-cell reference atlas of the human endometrium

The human endometrium, the inner lining of the uterus, exhibits complex, dynamic changes throughout the menstrual cycle in response to ovarian hormones. Aberrant response of endometrial cells to hormones is associated with multiple disorders, including endometriosis. Previous single-cell studies of the endometrium profiled a limited number of donors and lacked consensus in defining cell types and states. Here, we introduce the Human Endometrial Cell Atlas (HECA), a high-resolution single-cell reference atlas, combining published and newly generated single-cell transcriptomics datasets of endometrial biopsies of women with and without endometriosis. The HECA assigned consensus cell types and states, and uncovered novel ones, which we mapped in situ using spatial transcriptomics. We quantified how coordinated interactions between cell states in space and time contribute to endometrial regeneration and differentiation. In the continuously changing functionalis layer, we identified an intricate coordination of TGF{beta} signalling between stromal and epithelial cells, likely crucial for cell differentiation. In the basalis layer, we defined signalling between fibroblasts and a new epithelial cell population expressing epithelial stem/progenitor markers, suggesting their role in endometrial regeneration. Additionally, integrating the HECA single-cell data with genome-wide association study data and comparing endometrial samples from women with and without endometriosis, we pinpointed subsets of decidualised stromal cells and macrophages as the most dysregulated cell states in endometriosis. Overall, the HECA is an invaluable resource for studying endometrial physiology, investigating endometrial disorders, and guiding the creation of endometrial microphysiological in vitro systems.

genomics↗

Multi-organ functions of yolk sac during human early development

The yolk sac (YS) represents an evolutionarily-conserved extraembryonic structure that ensures timely delivery of nutritional support and oxygen to the developing embryo. However, the YS remains ill-defined in humans. We therefore assemble a complete single cell 3D map of human YS from 3-8 post conception weeks by integrating multiomic protein and gene expression data. We reveal the YS as a site of primitive and definitive haematopoiesis including a YS-specific accelerated route to macrophage production, a source of nutritional/metabolic support and a regulator of oxygen-carrying capacity. We reconstruct the emergence of primitive haematopoietic stem and progenitor cells from YS hemogenic endothelium and their decline upon stromal support modulation as intraembryonic organs specialise to assume these functions. The YS therefore functions as three organs in one revealing a multifaceted relay of vital organismal functions as pregnancy proceeds. One Sentence SummaryHuman yolk sac is a key staging post in a relay of vital organismal functions during human pregnancy.

developmental biology↗

Robust temporal map of human in vitro myelopoiesis using single-cell genomics

Myeloid cells have a central role in homeostasis and tissue defence. Characterising the current in vitro protocols of myelopoiesis is imperative for their use in research and immunotherapy as well as for understanding the early stages of myeloid differentiation in humans. Here, we profiled the transcriptome of more than 400k cells and generated a robust molecular map of the differentiation of human induced pluripotent stem cells (iPSC) into macrophages. By integrating our in vitro datasets with in vivo single-cell developmental atlases, we found that in vitro macrophage differentiation recapitulates features of in vivo yolk sac hematopoiesis, which happens prior to the appearance of definitive hematopoietic stem cells (HSC). During in vitro myelopoiesis, a wide range of myeloid cells are generated, including erythrocytes, mast cells and monocytes, suggesting that, during early human development, the HSC-independent immune wave gives rise to multiple myeloid cell lineages. We leveraged this model to characterize the transition of hemogenic endothelium into myeloid cells, uncovering poorly described myeloid progenitors and regulatory programs. Taking advantage of the variety of myeloid cells produced, we developed a new protocol to produce type 2 conventional dendritic cells (cDC2) in vitro. We found that the underlying regulatory networks coding for myeloid identity are conserved in vivo and in vitro. Using genetic engineering techniques, we validated the effects of key transcription factors important for cDC2 and macrophage identity and ontogeny. This roadmap of early myeloid differentiation will serve as an important resource for investigating the initial stages of hematopoiesis, which are largely unexplored in humans, and will open up new therapeutic opportunities.

developmental biology↗