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Lara-Astiaso, D.

Publications and source records attributed to Lara-Astiaso, D..

11 recordsLinked to original sources

Spatially resolved, multimodal in vivo Perturb-seq using antibody-based cell hashing

Large-scale perturbation screens have begun to map cell intrinsic gene-function relationships, yet how genes shape tissue architecture remains largely unexplored. To address this gap, we developed PerturbSpace, a novel approach that integrates CRISPR perturbations with spatially hashed single-cell multiomics. This approach enables the first high-throughput, spatially resolved Perturb-seq analysis across complex tissue architecture in vivo. Notably, PerturbSpace enables spatial transcriptome-wide perturbation readouts at organ scale and can be seamlessly integrated with orthogonal modalities. We combine PerturbSpace with surface proteomics and expressed lineage tracing barcodes to demonstrate multimodal compatibility. We use PerturbSpace to study the genetic determinants of tissue architecture. First, we map how 40 transcriptional regulators determine the size and lineage composition of colonies in the spleen during regenerative hematopoiesis. Second, we characterize immune-niche interactions in the liver by dissecting the extrinsic effects mediated by cytokine-secreting immune cells on their neighboring cells. Collectively, our work establishes PerturbSpace as a scalable and cost-effective approach for transcriptome-wide spatial profiling of whole cells while remaining compatible with the single-cell multiomics workflows that the field has already adopted at scale.

genomics↗

Differences between in vivo and ex vivo hematopoietic model systems modulate the outcomes of genetic perturbations.

Ex vivo experimental models are extensively used as reductionist models, yet the impact of model choice on molecular states and perturbation responses has not been systematically evaluated. Here, we compared the outcomes of genetic perturbations in hematopoietic stem cells between in vivo and ex vivo model systems. This revealed strong baseline differences characterized by a reduced interferon response and elevated growth and metabolism signatures in ex vivo models, a pattern recapitulated in various orthogonal human and mouse systems. We further found substantial differences between perturbation effects between in vivo and ex vivo models, with some perturbations showing opposite effects. Finally, we evaluated whether AI-based perturbation prediction models can predict in vivo perturbation effects from ex vivo perturbation effects, which proved challenging. Together, our findings reveal systematic biases in ex vivo models, demonstrate how these biases influence perturbation outcomes, suggest approaches to enhance ex vivo systems, and provide a test case for computational prediction of perturbation effects.

systems biology↗

Identification of epigenetic regulators of fibrotic transformation in cardiac fibroblasts through bulk and single-cell CRISPR screens

Cardiac fibrosis is mediated by the persistent activity of myofibroblasts, which differentiate from resident cardiac fibroblasts in response to tissue damage and stress signals. The signaling pathways and transcription factors regulating fibrotic transformation have been thoroughly studied. In contrast, the roles of chromatin factors in myofibroblast differentiation and their contribution to pathogenic cardiac fibrosis remain poorly understood. Here, we combined bulk and single-cell CRISPR screens to characterize the roles of chromatin factors in the fibrotic transformation of primary cardiac fibroblasts. We uncover strong regulators of fibrotic states including Srcap and Kat5 chromatin remodelers. We confirm that these factors are required for functional processes underlying fibrosis including collagen synthesis and cell contractility. Using chromatin profiling in perturbed cardiac fibroblasts, we demonstrate that pro-fibrotic chromatin complexes facilitate the activity of well-characterized pro-fibrotic transcription factors. Finally, we show that KAT5 inhibition alleviates fibrotic responses in patient-derived human fibroblasts.

cell biology↗

Diversity and evolution of chromatin regulatory states across eukaryotes

Histone post-translational modifications (hPTMs) are key regulators of chromatin states1,2, influencing gene expression, epigenetic memory, and transposable element repression across eukaryotic genomes. While many hPTMs are evolutionarily conserved3, the extent to which the chromatin states they define are similarly preserved remains unclear. Here, we developed a combinatorial indexing ChIP-seq method to simultaneously profile specific hPTMs across diverse eukaryotic lineages4, including amoebozoans, rhizarians, discobans, and cryptomonads. Our analyses revealed highly conserved euchromatin states at active gene promoters and gene bodies. In contrast, we observed diverse configurations of repressive heterochromatin states associated with silenced genes and transposable elements, characterized by various combinations of hPTMs such as H3K9me3, H3K27me3 and/or different H3K79 methylations. These findings suggest that while core hPTMs are ancient and broadly conserved, their functional readout has diversified throughout eukaryotic evolution, shaping lineage-specific chromatin landscapes.

evolutionary biology↗

Delayed Trp53 activation protects Dnmt3a-mutant hematopoietic stem cells from inflammatory attrition.

Hematopoietic stem cells (HSCs) accumulate somatic mutations over time, some conferring a fitness advantage that can lead to clonal hematopoiesis (CH). Mutations in DNMT3A, particularly at hotspot R882, are the most prevalent in CH and carry an increased risk of acute myeloid leukemia (AML). Although DNMT3A R882 mutations are linked to global DNA hypomethylation, the mechanisms underlying their selective advantage remain unclear. Here, we show that Dnmt3a-R882H mutant HSCs exhibit resilience under inflammatory and genotoxic stress. During IL-1{beta}-induced emergency granulopoiesis, Dnmt3a R882H/+ HSCs uncouple increased proliferation from stem cell exhaustion. In contrast, wild-type HSCs rapidly progress to terminal differentiation. We link this phenotype to a delayed activation of the p53-p21-DREAM axis, that allows mutant HSCs to avoid attrition, despite increased replication stress. Similarly, mutant HSCs exhibit delayed Trp53 activation following irradiation, but eventually recover a physiological Trp53 response. Analysis of patient data reveals shared phenotypic features between DNMT3A and monoallelic TP53 mutations in CH and myeloid neoplasms, highlighting potential functional similarities. Collectively, these findings suggest that the expansion of DNMT3A-mutant clones is affected by impaired TP53 signaling, which confers resilience against stressors. Therapeutic strategies targeting inflammatory pathways or the p53-p21-DREAM axis may reduce DNMT3A-CH expansion and/or progression and its associated risks.

molecular biology↗

Adenine DNA methylation associated to transcription is widespread across eukaryotes

DNA methylation in the form of 5-methylcytosine (5mC) is widespread in eukaryotes, while the presence of N6-methyladenine (6mA) has sparked considerable debate. Methodological disparities in quantifying and mapping 6mA in genomic DNA have fueled this controversy. Yet, the distantly related early branching fungi, ciliates and the algae Chlamydomonas reinhardtii exhibit robust 6mA methylation patterns, but the origin and evolution of 6mA remain unknown. Here we use Oxford Nanopore modified base calling to profile 6mA at base pair resolution in 18 unicellular eukaryotes spanning all major eukaryotic supergroups. Our results reveal that only species encoding the adenine methyltransferase AMT1 display robust genomic 6mA patterns. Notably, 6mA consistently accumulates downstream of transcriptional start sites, aligning with H3K4me3-enriched nucleosomes, suggesting a conserved role in placing transcriptionally permissive nucleosomes. Intriguingly, the recurrent loss of the 6mA pathway across eukaryotes, particularly in major multicellular lineages, implies a convergent alteration in the dual methylation system of the Last Eukaryotic Common Ancestor, which featured transcription-associated 6mA and repression-associated 5mC.

genomics↗

Uncovering the cis-regulatory program of early human B-cell commitment and its implications in the pathogenesis of B-cell acute lymphoblastic leukemia

Dysregulation of the early stages of B-cell lymphopoiesis, orchestrating the development of cellular immunity, may induce malignant transformations. Therefore, it is essential to characterize the gene regulatory network (GRN) driving B-cell lymphopoiesis in healthy individuals to uncover malignancy mechanisms. To this end, we generated a dataset that included paired human data for chromatin accessibility and gene expression in eight B-cell precursor stages, providing the first deep characterization of early B-cell lymphopoiesis, including the identification of regulatory elements and the reconstruction of the GRN. Using this data, we recapitulated well-known regulatory elements and revealed new regulons, such as ELK3, enriched in pro-B cells with a putative role in cell cycle progression. Moreover, a single-cell multi-omics analysis validated and enhanced the resolution of the regulatory landscape recovered by bulk data, revealing MYBL2 and ZNF367 as specific regulons of cycling cell states, and CEBPA associated with lymphoid multipotent progenitors (LMPPs). Importantly, this dataset enabled us to uncover B-cell acute lymphoblastic leukemia (B-ALL) triggers. We identified different cellular origins of malignant transformation depending on the B-ALL subtype, including the association of the ETV6-RUNX1 with pro-B cells and the increased expression of ELK3 in this ALL subtype. Overall, our dataset provides the most comprehensive atlas to date of early human B-cell regulation (B-rex; https://translationalbio.shinyapps.io/brex/), facilitating further understanding of B-cell differentiation in health and disease.

immunology↗

Systematic functional screening of chromatin factors identifies strong lineage and disease dependencies in normal and malignant haematopoiesis

Interactions between transcription factors (TF) and chromatin factors (CF) regulate gene expression programmes to determine cellular fate. However, unlike for TF, the exact role of CF in this process is poorly understood. Using haematopoiesis as a model system and utilising novel functional CRISPR screens ex vivo and in vivo, coupled with Perturb-Seq, CF binding and genome-wide chromatin accessibility in primary murine cells, we assess the role of 550 chromatin factors in lineage choice in normal haematopoiesis and the maintenance of acute myeloid leukaemia (AML). These studies demonstrate marked specificity for a large number of CFs in lineage determination, highlighting functional diversity within specific families of chromatin regulators, including MLL-H3K4-methyltransferases and different BAF-complexes, that regulate disparate lineage decisions across haematopoiesis. Conversely, we demonstrate that unrelated Repressive complexes function similarly to restrain excessive myeloid differentiation and protect lineage diversity. We identify interactions between CF and TF that, at least in part, explain the regulatory function of CF and link Brd9-loss to a premalignant state. Utilising similar experiments in a relevant murine AML model, we demonstrate opposing effects for CF in normal haematopoiesis and AML, where MLL-H3K4-methyltransferases, c-BAF-remodelers and Repressive complexes prevent differentiation and maintain leukaemic fitness. We show that this alteration relates to differential utilisation of TF by CF complexes between normal and malignant haematopoiesis, highlighting corrupted TF-CF interactions as potential novel avenues for therapeutic intervention in AML. Together, this study provides novel insights on the functional diversity of chromatin factors in governing cell-fate.

genomics↗

Transcriptional regulation of HSCs in Aging and MDS reveals DDIT3 as a Potential Driver of Transformation

Myelodysplastic syndromes (MDS) are hematopoietic stem cell (HSC) malignancies characterized by ineffective hematopoiesis, with increased incidence in elderly individuals. In this work, we analyzed the transcriptome of human HSCs purified from young and elderly healthy donors, as well as MDS patients, identifying transcriptional alterations following eight different patterns of expression. While aging-associated lesions seemed to predispose HSCs to myeloid transformation, disease-specific alterations may trigger MDS development. Among MDS-specific lesions, we detected the upregulation of the transcription factor DDIT3. Overexpression of DDIT3 in human healthy HSCs induced an MDS-like transcriptional state, and a delay in erythropoiesis. Such effect was associated with downregulation of transcription factors required for normal erythropoiesis, and with a failure in the activation of their transcriptional programs. Moreover, DDIT3 knockdown in CD34+ cells from MDS patients with anemia was able to restore erythropoiesis. These results identify DDIT3 as a driver of dyserythropoiesis, and a potential therapeutic target to restore the inefficient erythropoiesis characterizing MDS patients. STATEMENT OF SIGNIFICANCEThis study defines how human aging and MDS development are characterized by transcriptional alterations in HSCs that follow different patterns, some of which may contribute to myeloid transformation. Among them, we demonstrate how MDS-specific upregulation of DDIT3 in HSCs induces dyserythropoiesis, while its knockdown in HSPCs from MDS patients restores proper erythroid differentiation.

cancer biology↗

Chromatin activation as a unifying principle underlying pathogenic mechanisms in multiple myeloma

Multiple myeloma (MM) is a plasma cell neoplasm associated with a broad variety of genetic lesions. In spite of this genetic heterogeneity, MMs share a characteristic malignant phenotype whose underlying molecular basis remains poorly characterized. In the present study, we examined plasma cells from MM using a multi-epigenomics approach and demonstrated that when compared to normal B cells, malignant plasma cells showed an extensive activation of regulatory elements, in part affecting co-regulated adjacent genes. Among target genes upregulated by this process, we found members of the NOTCH, NFkB, mTOR1 signaling and p53 signaling pathways. Other activated genes included sets involved in osteoblast differentiation and response to oxidative stress, all of which have been shown to be associated with the MM phenotype and clinical behavior. We functionally characterized MM specific active distant enhancers controlling the expression of thioredoxin (TXN), a major regulator of cellular redox status, and in addition identified PRDM5 as a novel essential gene for MM. Collectively our data indicates that aberrant chromatin activation is a unifying feature underlying the malignant plasma cell phenotype.

cancer biology↗

Single-cell RNA-seq analysis reveals the crucial role of Collagen Triplex Helix Repeat Containing 1 (CTHRC1) cardiac fibroblasts for ventricular remodeling after myocardial infarction

Cardiac fibroblasts have a central role during the ventricular remodeling process associated with different types of cardiac injury. Recent studies have shown that fibroblasts do not respond homogeneously to heart damage, suggesting that the adult myocardium may contain specialized fibroblast subgroups with specific functions. Due to the limited set of bona fide fibroblast markers, a proper characterization of fibroblast population dynamics in response to cardiac damage is still missing. Using single-cell RNA-seq, we identified and characterized a fibroblast subpopulation that emerges in response to myocardial infarction (MI) in a murine model. These activated fibroblasts exhibit a clear pro-fibrotic signature, express high levels of the hormone CTHRC1 and of the immunomodulatory co-receptor CD200 and localize to the injured myocardium. Combining epigenomic profiling with functional assays, we show Sox9 and the non-canonical TGF-{beta} signaling as important regulators mediating their response to cardiac damage. We show that the absence of CTHRC1, in this activated fibroblast subpopulation, results in pronounced lethality due to ventricular rupture in a mouse model of myocardial infarction. Finally, we find evidence for the existence of similar mechanisms in a pig pre-clinical model of MI and establish a correlation between CTHRC1 levels and cardiac function after MI.

cell biology↗