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Biology subjects

Morrisey, E. E.

Publications and source records attributed to Morrisey, E. E..

18 recordsLinked to original sources

A multipotent mouse distal airway secretory cell population that contributes to both airway and alveolar regeneration

The distal airway is a spatially distinct compartment whose contribution to lung repair remains poorly defined. We have identified an epithelial cell population enriched in the most distal airways of the mouse lung, that is not present in the alveolar epithelium. Using lineage tracing tools based on Cldn10 expression which marks these cells, we show that the Cldn10+ lineage in homeostatic conditions marks distal airway secretory cells in a highly specific manner, with only a small contribution to multi-ciliated cells and no contribution towards the basal stem cell lineage. Remarkably, these Cldn10+ distal secretory cells proliferate and display a high degree of multi-potency across the lung epithelial axis after injury, generating basal cells, multi-ciliated cells, and alveolar epithelium. In severely remodeled regions after injury, we show that Cldn10 lineage-labeled cells migrate from the airways and differentiate into alveolar epithelial cells. These findings establish the Cldn10 lineage that defines a distal airway secretory facultative progenitor with both intrapulmonary airway and alveolar potential, providing a genetic system for studying distal lung repair.

cell biology↗

A Single-Cell Atlas of PVOD Across the Lifespan Reveals Cellular and Molecular Therapeutic Targets

Rationale Pulmonary veno-occlusive disease (PVOD) is a progressive and lethal disease cured only lung transplant. While genetic mutations in EIF2AK4 have been identified in some cases, 70% of PVOD patients have no known etiology. Objectives To construct a single-cell atlas to define the cellular and molecular constituents driving pathophysiology in PVOD. Methods Lung samples were collected from four idiopathic non-EIF2AK4 mutation pediatric and adult PVOD patients and age-matched controls. Analyses of single-cell RNA sequencing, Xenium spatial transcriptomics, and immunohistochemistry were performed to identify cell state changes and differential gene expression between controls and PVOD and subsequent transcriptome comparison between our PVOD and published pulmonary arterial hypertension (PAH) datasets. Measurement and Main Results The single-cell atlas reveals marked changes in the PVOD endothelium compared to controls. EndMT and ectopic COL15A1+ systemic venous shunts and pulmonary vein endothelium are hallmarks of PVOD. Molecular analyses reveal activation of the integrated stress response (ISR)/ATF4, TGF{beta} signaling, MAPK signaling, and BRD4 are potential key players in the pathophysiology of PVOD. While PVOD and PAH share both pathological and some molecular mechanisms, ISR and TGF{beta} signaling are more prominent in PVOD than PAH. Conclusions These data indicate that endothelial dysfunction is a primary etiology in the development of PVOD with activation of multiple pathways with druggable targets.

molecular biology↗

Cytoskeletal-nuclear control of alveolar fibroblast identity directs lung regeneration

Respiratory mechanics direct cell fate in the lung, but the mechanisms by which these mechanical signals are sensed and transmitted to the nucleus to control cell state remain unclear. We paired in vivo perturbations of respiratory mechanics with single-cell genomics and found that alveolar fibroblasts are highly sensitive to physical changes in their microenvironment, exhibiting persistent shifts in their transcriptional identity after injury. Surprisingly, transmission of these signals through the nuclear envelope was not essential for maintaining transcriptional or epigenetic stability during homeostasis. However, severing mechanical-nuclear signaling promoted the normalization of alveolar fibroblast identity after acute injury, resulting in improved epithelial regeneration and reduced dysplastic remodeling. These studies reveal the importance of mechanical-nuclear signaling in the regulation of alveolar cell identity and function and reveal that targeting this complex can enhance tissue regeneration.

cell biology↗

Mechanical force-mediated cellular crosstalk maintains the integrity of the lung gas exchange niche

Respiratory motion imposes a constant mechanical strain that has important but poorly defined impact on tissue niches in the lung. We developed a reversible bronchial ligation model to induce and reverse unilateral blockade of lung mechanical motion in vivo and show that this leads to transcriptomic changes in multiple cell lineages that are not normalized upon reinitiation of respiratory motion. Perturbation of mechanosignaling specifically in alveolar epithelial type I (AT1) cells alters the transcriptomic state and fate of their niche neighbors, demonstrating that AT1 cells act as a node that propagates a mechanical cascade throughout the lung alveolus. Mechanically perturbed AT1 cells induce a distinct capillary endothelial cell state that persists after reactivation of respiratory motion, which is mediated by an integrin/TGF-{beta} network within the alveolus that is vulnerable to pharmacological intervention. Importantly, AT1 mechanosignaling and intercellular communication are altered in chronic human lung diseases, highlighting the critical role of an AT1-driven mechanosensing network in lung disease biology. Thus, mechanosensing cells propagate biophysical signals that regulate tissue function and program tissue responses in disease.

cell biology↗

Identification of Meibomian gland stem cell populations and mechanisms of aging

Meibomian glands secrete lipid-rich meibum, which prevents tear evaporation. Aging-related Meibomian gland shrinkage may result in part from stem cell exhaustion and is associated with evaporative dry eye disease, a common condition lacking effective treatment. The identities and niche of Meibomian gland stem cells and the signals controlling their activity are poorly defined. Using snRNA-seq, in vivo lineage tracing, ex vivo live imaging, and genetic studies in mice, we identified markers for stem cell populations that maintain distinct regions of the gland and uncovered Hh signaling as a key regulator of stem cell proliferation. Consistent with this, human Meibomian gland carcinoma exhibited increased Hh signaling. Aged glands displayed decreased Hh and EGF signaling, deficient innervation, and loss of collagen I in niche fibroblasts, indicating that alterations in both glandular epithelial cells and their surrounding microenvironment contribute to age-related degeneration. These findings suggest new approaches to treat aging-associated Meibomian gland loss.

cell biology↗

FZD2 inhibits YAP and prevents cell cycle reentry in adult murine cardiomyocytes

RationaleFully differentiated cardiomyocytes (CMs) are post-mitotic and cannot repopulate damaged tissue after myocardial infarction (MI). Understanding the mechanisms preventing CM proliferation or promoting their survival after injury may lead to treatment strategies for MI. While the effects of canonical WNT/{beta}-catenin signaling in adult CMs have been examined, roles for non-canonical WNT signaling in cardiac homeostasis and repair remain unexplored. ObjectiveTo determine the function of the non-canonical WNT receptor frizzled 2 (FZD2) in adult cardiac homeostasis and injury. Methods and ResultsFZD2 was deleted from the CMs of adult mice to investigate its role in myocardial homeostasis. Fzd2 conditional knockout (CKO) mice had cardiomegaly but not hypertrophy. FZD2-deficient CMs expressed proliferation and cytokinesis markers, suggesting that they have increased proliferation potential. FZD2-deletion caused the accumulation of {beta}-catenin. However, {beta}-catenin localized to the membranes of FZD2-deficient CMs and did not activate target gene expression. Instead, the YES-associated protein (YAP) regulated genes v-myc avian myelocytomatosis viral oncogene 1 (Mycl), and B cell leukemia/lymphoma 2 (Bcl2l1) were upregulated in Fzd2 CKO CMs relative to controls. Knockdown of FZD2 increased YAP activity in neonatal ventricular CMs (NVCMs), while overexpressing FZD2 inhibited YAP. Neither {beta}-catenin knockdown nor mutating the large tumor suppressor 1 and 2 (LATS1/2) target site on YAP blocked the effects of FZD2 on YAP in NVCMs, suggesting that FZD2 utilizes different effectors than canonical WNT and Hippo signaling. Fzd2 CKO and control mice were subjected to MI to determine if FZD2-deletion affects cardiac repair. While ischemia and necrosis were similar 24 hours post MI, Fzd2 CKO mice had better cardiac function and less scarring than controls. ConclusionsFZD2 reduces YAP activity and prevents adult murine CMs from reentering the cell cycle. FZD2-deletion improves heart function and reduces scarring in mice after MI, implicating FZD2 as a target for pharmacological intervention.

cell biology↗

A longitudinal atlas of post-viral lung regeneration reveals persistent injury-associated cell states

Functional regeneration of the lungs gas exchange surface following injury requires the coordination of a complex series of cell behaviors within the alveolar niche. Using a multi-modal approach, we have mapped the temporal sequencing of mouse lung regeneration after acute viral injury, demonstrating that this response is asynchronously phased across different cellular compartments. This longitudinal atlas of regeneration has produced a catalogue of new cell states that reflect transient and persistent transcriptional alterations in daughter cells as they transit across axes of differentiation. These new cell states include an injury-induced capillary endothelial cell (iCAP) that arises after injury, persists indefinitely, and shares transcriptional hallmarks with both developing lung endothelium and the endothelial aberrations found in degenerative human lung diseases. This comprehensive atlas of lung regeneration provides a foundational resource to understand the complexity of the cellular and molecular responses to injury, reveals the critical importance of capillary endothelium in maintaining and rebuilding the alveolar niche after injury, and correlates these responses to those found in development and human lung diseases.

cell biology↗

An injury-induced tissue niche shaped by mesenchymal plasticity coordinates the regenerative and disease response in the lung

Severe lung injury causes basal stem cells to migrate and outcompete alveolar stem cells resulting in dysplastic repair and a loss of gas exchange function. This "stem cell collision" is part of a multistep process that is now revealed to generate an injury-induced tissue niche (iTCH) containing Keratin 5+ epithelial cells and plastic Pdgfra+ mesenchymal cells. Temporal and spatial single cell analysis reveals that iTCHs are governed by mesenchymal proliferation and Notch signaling, which suppresses Wnt and Fgf signaling in iTCHs. Conversely, loss of Notch in iTCHs rewires alveolar signaling patterns to promote euplastic regeneration and gas exchange. The signaling patterns of iTCHs can differentially phenotype fibrotic from degenerative human lung diseases, through apposing flows of FGF and WNT signaling. These data reveal the emergence of an injury and disease associated iTCH in the lung and the ability of using iTCH specific signaling patterns to discriminate human lung disease phenotypes.

cell biology↗

Generation of human alveolar epithelial type I cells from pluripotent stem cells

In the distal lung, alveolar epithelial type I cells (AT1s) comprise the vast majority of alveolar surface area and are uniquely flattened to allow the diffusion of oxygen into the capillaries. This structure along with a quiescent, terminally differentiated phenotype has made AT1s particularly challenging to isolate or maintain in cell culture. As a result, there is a lack of established models for the study of human AT1 biology, and in contrast to alveolar epithelial type II cells (AT2s), little is known about the mechanisms regulating their differentiation. Here we engineer a human in vitro AT1 model system through the directed differentiation of induced pluripotent stem cells (iPSC). We first define the global transcriptomes of primary adult human AT1s, suggesting gene-set benchmarks and pathways, such as Hippo-LATS-YAP/TAZ signaling, that are enriched in these cells. Next, we generate iPSC-derived AT2s (iAT2s) and find that activating nuclear YAP signaling is sufficient to promote a broad transcriptomic shift from AT2 to AT1 gene programs. The resulting cells express a molecular, morphologic, and functional phenotype reminiscent of human AT1 cells, including the capacity to form a flat epithelial barrier which produces characteristic extracellular matrix molecules and secreted ligands. Our results indicate a role for Hippo-LATS-YAP signaling in the differentiation of human AT1s and demonstrate the generation of viable AT1-like cells from iAT2s, providing an in vitro model of human alveolar epithelial differentiation and a potential source of human AT1s that until now have been challenging to viably obtain from patients.

cell biology↗

Atf3 defines a population of pulmonary endothelial cells essential for lung regeneration

Following acute injury, the capillary vascular bed in the lung must be repaired to reestablish gas exchange with the external environment. Little is known about the transcriptional and signaling factors that drive pulmonary endothelial cell (EC) proliferation and subsequent regeneration of pulmonary capillaries, as well as their response to stress. Here, we show that the transcription factor Atf3 is essential for the regenerative response of the mouse pulmonary endothelium after influenza infection. Atf3 expression defines a subpopulation of capillary ECs enriched in genes involved in endothelial development, differentiation, and migration. During lung alveolar regeneration, this EC population expands and increases expression of genes involved in angiogenesis, blood vessel development, and cellular response to stress. Importantly, endothelial cell-specific loss of Atf3 results in defective alveolar regeneration, in part through increased apoptosis and decreased proliferation in the endothelium. This leads to the general loss of alveolar endothelium and persistent morphological changes to the alveolar niche, including an emphysema-like phenotype with enlarged alveolar airspaces lined with regions that lack vascular investment. Taken together, these data implicate Atf3 as an essential component of the vascular response to acute lung injury that is required for successful lung alveolar regeneration.

cell biology↗

Hyperactive mTOR in Lung Mesenchyme Induces Endothelial Dysfunction and Pulmonary Vascular Remodeling

Pulmonary vascular remodeling is the key structural abnormality in pulmonary hypertension (PH). Mechanistic target of rapamycin (mTOR) has long been suspected to play a role in the development of pulmonary vascular remodeling. However, underlying cellular and molecular mechanisms leading to this pathophysiological condition remain incompletely understood. To elucidate the crosstalk between lung mesenchyme with activated mTOR and endothelial cells (ECs), we focused on a monogenic lung disease, pulmonary lymphangioleiomyomatosis (LAM). LAM is a progressive cystic lung disease caused by a mutational inactivation of tuberous sclerosis complex (TSC1/TSC2), which results in constitutive mTOR activation in mesenchymal LAM cells. ECs derived from LAM lung explants showed increased proliferation, migration, and defective angiogenesis compared to age- and sex-matched ECs from control human lung. In LAM cells, we found increased WNT2 ligand expression. We also identified corresponding Frizzled 4 (FZD) receptors on ECs isolated from distal LAM lung, suggesting cellular crosstalk between LAM cells and ECs. In endothelial-fibroblast cocultures, treatment of normal ECs with WNT2 ligands recapitulated LAM EC phenotype and morphology. We observed transcriptomic upregulation in metabolic, angiogenic and growth pathways in ECs of young mice, while 1-year-old Tsc2KO mice spontaneously developed pulmonary vascular remodeling with concurrent elevation in right ventricular systolic pressure. Our study demonstrates that LAM cells are not just a pathological mesenchymal cell state but a signaling hub that contributes to dysregulated cellular response in the surrounding vasculature, eventual pulmonary vascular remodeling and PH.

molecular biology↗

FRIZZLED 2 regulates limb development by mediating both β-catenin-dependent and independent Wnt signaling pathways

Human Robinow Syndrome and omodysplasia, characterized by skeletal limb and craniofacial defects, are associated with mutations in the Wnt receptor FZD2. However, as FZD2 can activate both canonical and non-canonical Wnt pathways, its precise functions and mechanisms of action in limb development are unclear. To address these questions, we generated mice harboring a single nucleotide insertion in the Dishevelled-interacting domain of Fzd2 (Fzd2em1Smill), causing a frameshift mutation similar to the effects of human syndromic FZD2 mutations. Fzd2em1Smill mutant mice had shortened limbs resembling those of Robinow Syndrome and omodysplasia patients. Fzd2em1Smill mutant embryos displayed decreased canonical Wnt signaling in developing limb mesenchyme and disruption of digit chondrocyte elongation and orientation, which is controlled by the WNT5A/PCP pathway. In line with this, we found that tissue-specific disruption of Fzd2 function in limb mesenchyme caused formation of shortened bone elements and was associated with deficiency in both Wnt/{beta}-catenin and WNT5A/PCP signaling. These findings indicate that FZD2 controls limb development by mediating both canonical and non-canonical Wnt pathways and reveal causality of pathogenic FZD2 mutations in Robinow Syndrome and omodysplasia patients. Summary statementHuman FZD2 mutations are associated with limb defects; using genetic mouse models we revealed causality of these mutations and showed that they disrupt both canonical and non-canonical Wnt signaling.

developmental biology↗

Temporal and spatial staging of lung alveolar regeneration is determined by the grainyhead transcription factor Tfcp2l1

Alveolar epithelial type 2 (AT2) cells harbor the facultative progenitor capacity in the lung alveolus to drive regeneration after lung injury. Using single cell transcriptomics, software-guided segmentation of tissue damage, and in vivo lineage tracing, we have identified the grainyhead transcription factor Tfcp2l1 as a key regulator of this regenerative process. Tfcp2l1 expression is initiated late in lung development and restricted to the AT2 cell population in the postnatal lung. Loss of Tfcp2l1 in adult AT2 cells decreased self-renewal and enhanced AT2-AT1 differentiation during active tissue regeneration. Conversely, Tfcp2l1 blunts the proliferative response to inflammatory signaling during the early acute phase after injury. This ability of Tfcp2l1 to temporally regulate the balance of AT2 self-renewal and differentiation is spatially restricted to zones undergoing active alveolar regeneration. Single-cell transcriptomics and lineage tracing reveal that Tfcp2l1 regulates cell fate dynamics by balancing the traffic across the AT2-AT1 differentiation axis and restricting the inflammatory program in AT2 cells. Organoid modeling shows that these cell fate dynamics are controlled by Tfcp2l1 regulation of IL-1 receptor expression and activity in AT2 cells. Together, these studies reveal the critical importance of properly staging lung alveolar regeneration and the integral role of Tfcp2l1 plays in balancing epithelial cell self-renewal and differentiation in this process.

cell biology↗

Guided construction of single cell reference for human and mouse lung

Accurate cell type identification is a key and rate-limiting step in single cell data analysis. Single cell references with comprehensive cell types, reproducible and functional validated cell identities, and common nomenclatures are much needed by the research community to optimize automated cell type annotation and facilitate data integration, sharing, and collaboration. In the present study, we developed a novel computational pipeline to utilize the LungMAP CellCards as a dictionary to consolidate single-cell transcriptomic datasets of 104 human lungs and 17 mouse lung samples and constructed "LungMAP CellRef" and "LungMAP CellRef Seed" for both normal human and mouse lungs. "CellRef Seed" has an equivalent prediction power and produces consistent cell annotation as does "CellRef" but improves computational efficiency and simplifies its utilization for fast automated cell type annotation and online visualization. This atlas set incorporates 48 human and 40 mouse well-defined lung cell types catalogued from diverse anatomic locations and developmental time points. Using independent datasets, we demonstrated the utility of our CellRefs for automated cell type annotation analysis of both normal and disease lungs. User-friendly web interfaces were developed to support easy access and maximal utilization of the LungMAP CellRefs. LungMAP CellRefs are freely available to the pulmonary research community through fast interactive web interfaces to facilitate hypothesis generation, research discovery, and identification of cell type alterations in disease conditions.

bioinformatics↗

LungMAP Portal Ecosystem: Systems-Level Exploration of the Lung

An improved understanding of the human lung necessitates advanced systems models informed by an ever-increasing repertoire of molecular omics, cellular, imaging and pathological datasets. To centralize and standardize information across broad lung research efforts we expanded the LungMAP.net website into a gateway portal. This portal connects a broad-spectrum of research networks, bulk and single-cell multi-omics data and a diverse collection of image data that span mammalian lung development and disease. The data are standardized across species and technologies using harmonized data and metadata models that leverage recent advances including those from the Human Cell Atlas, diverse ontologies, and the LungMAP CellCards initiative. To cultivate future discoveries, we have aggregated a diverse collection of single-cell atlases for multiple species (human, rhesus, mouse), to enable consistent queries across technologies, cohorts, age, disease and drug treatment. These atlases are provided as independent and integrated queriable datasets, with an emphasis on dynamic visualization, figure generation and reference-based classification of user-provided datasets (Azimuth). As this resource grows, we intend to increase the breadth of available interactive interfaces, data portals and datasets from LungMAP and external research efforts.

systems biology↗

Circadian regulation of lung repair and regeneration

Optimal lung repair and regeneration is essential for recovery from viral infections such as that induced by influenza A virus (IAV). We have previously demonstrated that lung inflammation induced by IAV is under circadian control. However, it is not known if the circadian clock exerts its influence on lung repair and regenerative processes independent of acute inflammation from IAV. Here, we demonstrate for the first time that lung organoids have a functional clock as they mature and that the absence of an intact circadian clock impairs regenerative capacity. Using several models of circadian disruption, we show that with the absence of an intact clock lung proliferation is disrupted. Further, we find that the circadian clock acts through direct control of the Wnt/{beta}-catenin pathway. We speculate, that adding the circadian dimension to the critical process of lung repair and regeneration will lead to novel therapies and improve outcomes. Finally, we use data from UK Biobank to demonstrate at the population level, the role of poor circadian rhythms in mediating negative outcomes following lung infection.

cell biology↗

Type II alveolar cells with constitutive expression of MHCII and limited antigen presentation capacity contribute to improved respiratory viral disease outcomes

Type II alveolar cells (AT2s) are critical for basic respiratory homeostasis and tissue repair after lung injury. Prior studies indicate that AT2s also express major histocompatibility complex II (MHCII) molecules, but how MHCII expression by AT2s is regulated and how it contributes to host defense remain unclear. Here we show that AT2s express high levels of MHCII independent of conventional inflammatory stimuli, and that selective loss of MHCII from AT2s in mice results in the worsening of respiratory virus disease following influenza and Sendai virus infections. We also find that AT2s exhibit MHCII presentation capacity that is substantially limited in comparison to professional antigen presenting cells. The combination of constitutive MHCII expression and restrained presentation may position AT2s to contribute to lung adaptive immune responses in a measured fashion, without over-amplifying damaging inflammation.

immunology↗

GSK3 inhibition rescues growth and telomere dysfunction in dyskeratosis congenita iPSC-derived type II alveolar epithelial cells

Dyskeratosis congenita (DC) is a rare genetic disorder characterized by deficiencies in telomere maintenance leading to very short telomeres and the premature onset of certain age-related diseases, including pulmonary fibrosis (PF). PF is thought to derive from epithelial failure, particularly that of type II alveolar epithelial (AT2) cells, which are highly dependent on Wnt signaling during development and adult regeneration. We use human iPSC-derived AT2 (iAT2) cells to model how short telomeres affect AT2 cells. Cultured DC mutant iAT2 cells accumulate shortened, uncapped telomeres and manifest defects in the growth of alveolospheres, hallmarks of senescence, and apparent defects in Wnt signaling. The GSK3 inhibitor, CHIR99021, which mimics the output of canonical Wnt signaling, enhances telomerase activity and rescues the defects. These findings support further investigation of Wnt agonists as potential therapies for DC related pathologies.

cell biology↗