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Biology subjects

Zhou, F. Y.

Publications and source records attributed to Zhou, F. Y..

At least 19 recordsLinked to original sources

Deciphering the Multiscale Morphology of Somatic Oncogenic Alterations in Hepatocellular Carcinoma

Somatic oncogenic mutations are typically defined by their molecular alterations, yet how they reorganize cellular architecture within intact tissues remain largely unknown. Here, we demonstrate that distinct oncogenic drivers produce unique multiscale architectural phenotypes that can be quantitatively resolved in intact liver tissue. Using iterative expansion microscopy, multiscale light-sheet imaging, and three-dimensional morphometric analysis, we systematically mapped structural remodeling from single-cell morphology to mitochondrial architecture in mosaic mouse models of hepatocellular oncogene activation. NRAS and CTNNB1 induced fundamentally different morphological programs. NRAS activation drove extensive remodeling of cell morphology, membrane curvature, and surface irregularity, whereas CTNNB1 activation largely preserved global cell morphology while selectively altering mitochondrial organization and shape. We first established a zonation-aware reference state for interpreting oncogene-associated organelle remodeling by resolving mitochondrial differences between periportal and pericentral hepatocytes. Within this framework, CTNNB1 activation shifted mitochondrial features toward a pericentral-like state, consistent with the role of Wnt/{beta}-catenin signaling in hepatic zonation and metabolic identity. Furthermore, integrating cellular morphology, membrane geometry, and mitochondrial architecture improved discrimination of oncogenic states beyond any individual structural feature, demonstrating that mutation-specific phenotypes arise through coordinated remodeling across multiple biological scales. Together, these findings establish multiscale structural phenotyping as a framework for linking oncogenic genotype to three-dimensional cellular organization and reveal that distinct oncogenic drivers remodel different architectural compartments during liver oncogene activation.

cancer biology↗

Quantitative multi-scale morphodynamic analysis reveals ratchet-like collective DVE migration and epiblast retrograde cell flow during anterior patterning in the mouse embryo

The collective unidirectional migration of distal visceral endoderm (DVE) cells in the early mouse embryo is required to pattern the anterior-posterior (A-P) axis in the epiblast. It is unknown to what extent A-P axial asymmetries exist prior to DVE migration, how migration becomes channeled towards one side of the embryo, and whether the epiblast cells they migrate over have coordinated movements. We developed a quantitative embryo-wide, tissue-tracking approach to analyse visceral endoderm and epiblast tissue morphodynamics in a longitudinal light-sheet imaged, multi-embryo data-set. Here we show that asymmetric morphology of the ectoplacental cone already present prior to DVE migration correlates with the alignment of the A-P axis but not its polarity. DVE cell movements are initiated with a relatively low cell coordination and small net migration, then get channelled in an abrupt transition to a highly coordinated, uni-directional anterior motion. This anteriorwards migration is characterised by a ratchet-like, intermittent motion. Vertex modelling demonstrates that tissue rheology can account for DVE start-stop motion, and suggests that T1-mediated stress relaxation in the surrounding tissue can facilitate intermittent DVE motion without requiring intrinsic fluctuations in DVE velocity. Finally, comparing cell movement of the DVE with the underlying epiblast reveals a previously unknown coordinated motion in the anterior epiblast, opposite to the direction of DVE migration. Together these data provide insights into the origin of embryonic axial asymmetry and a previously unappreciated coordination between VE and epiblast tissue-motion during anterior-posterior patterning. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=102 SRC="FIGDIR/small/720339v1_ufig1.gif" ALT="Figure 1"> View larger version (33K): org.highwire.dtl.DTLVardef@1cfe4fdorg.highwire.dtl.DTLVardef@1c2c3e6org.highwire.dtl.DTLVardef@1cb6a5corg.highwire.dtl.DTLVardef@1b3ed19_HPS_FORMAT_FIGEXP M_FIG C_FIG See supplemental movie: animated abstract

developmental biology↗

Modulation of Oncogenic KRAS Signaling by Branched Actin-driven Cell Membrane Protrusions

For over three decades, we have known that oncogenic RAS alters the actin cytoskeleton organization and cell surface morphology1,2. RAS activates the GTPase RAC1, which triggers the growth of branched actin networks to promote cell membrane protrusions3,4. In melanoma, the hyperactive RAC1 mutant, Rac1P29S, was recently shown to drive extended lamellipodia, which then empower cell proliferation through sequestration and localized inhibition of the merlin tumor suppressor5. This discovery illustrates cell morphological programs not only as outputs but also as regulators of human oncogenic signals. Hence, we wondered whether the pronounced branched actin-driven membrane protrusions (BAMPs) downstream of oncogenic RAS are not mere outputs of RAS signaling but rather an active component in mediating the oncogenic penetrance of RAS mutants. We used volumetric light sheet microscopy and biochemical approaches to investigate the role of BAMPs in regulating the molecular signaling of oncogenic KRAS in pancreatic and lung cancer models. We found that elevated BAMP formation regulated the interaction of oncogenic KRAS with downstream effectors, specifically with the RAC1 GEF TIAM1. This implies that BAMPs amplify their own upstream regulators in a positive feedback. This meritorious cycle upregulates cyclin D1 expression by inactivating the merlin tumor suppressor, independently of the mitogen activated protein kinase pathway (MAPK). In the absence of BAMPs, cells carrying oncogenic KRAS mutations are unable to attain their full penetrance in proliferation. Overall, this work unveils the long-overlooked role of branched actin-driven cell morphology in the functionalization of KRAS mutants as potent oncogenes.

cancer biology↗

Unraveling Subcellular Ultrastructure with Cyclically Multiplexed Expansion Microscopy

Despite advances in fluorescence microscopy, spectral overlap and limited resolution hinder the dense mapping of the cellular ultrastructure. To overcome these challenges, we developed Cy-ExM, a high-plex imaging strategy that integrates optimized cryo-fixation for antigen preservation, expansion microscopy, and iterative immunofluorescence labeling. Using oblique plane microscopy, we perform three-dimensional super-resolution imaging of 20 biological targets encompassing the full cellular volume of individual mammalian cells.

cell biology↗

Development of a universal imaging "phenome" using Shape, Appearance and Motion (SAM) features and the SAM Observation Tool (SPOT)

Cells are plastic, highly heterogeneous and change over time. High-content timelapse imaging promises to reveal dynamic cell behaviors, enabling more accurate identification of cell state and cell fate prediction for biological hypothesis generation and perturbation screens. To empower live-cell imaging based screen, we report the development of 1) a Shape, Appearance, Motion (SAM) "phenome"; a universal set of 2185 image-derived features that act as a image-"transcriptome" to comprehensively quantify an objects instantaneous phenotype; 2) the SAM-Phenotype-Observation-Tool (SPOT), for image-"sequencing" analysis of phenomes. We validated the effectiveness of unbiased SAM-SPOT workflow on publicly available computer vision and 2D single cell imaging datasets. Importantly, we demonstrated that SAM-phenome outperformed features generated by deep learning AI models trained on >1 million fixed single cell and >5000 single cell video frames, respectively. SAM-phenome and SPOT delivers high-throughput, object-treatment-agnostic, comprehensive screening readouts of dynamics, promising to advance novel molecular target discovery and new medicine development.

bioinformatics↗

Identifying phenotype-genotype-function coupling in 3D organoid imaging using Shape, Appearance and Motion Phenotype Observation Tool (SPOT)

Live cells in tissue are plastic, phenotypically dynamic, and modify their function in response to genetic and environmental perturbations. To unleash the power of live-cell imaging to identify phenotype-genotype-function coupling over time, we report the development of a standardized Shape-Appearance-Motion (SAM) "phenome" and SAM-Phenotype-Observation-Tool (SPOT), that act as an image-"transcriptome" and image-"transcriptome analyzer" respectively, and provide unbiased and comprehensive description of morpho-dynamic phenotypes without prior knowledge. We developed and applied SAM-SPOT to our simulated organoids database with known ground-truth and >1.6 million mouse and human organoid instances with defined genetic and chemical perturbations. SAM-SPOT can effectively and robustly characterize 3D morpho-dynamics from 2D projection videos. Combined with single-cell RNA sequencing, SAM-SPOT revealed that altered WNT signaling, but not mutant RAS or p53, predisposes intestinal organoids to irregular morphogenesis. SAM-SPOT advances biomedical discovery by empowering live-cell imaging to identify phenotype-genotype-function relationships through large-scale and cost-effective label-free live-cell imaging.

cancer biology↗

Multi-immersion Oblique Plane Microscope (miOPM): A reconfigurable platform for high-resolution Light-Sheet Fluorescence Microscopy.

Light-Sheet Fluorescence Microscopy (LSFM) enables gentle, rapid, and efficient volumetric imaging of biological specimens. Despite its potential, LSFM has fragmented into multiple variants, each narrowly optimized for specific samples or imaging regimes, limiting its broad applicability. To overcome this barrier, we introduce the multi-immersion oblique plane microscope (miOPM), an adaptable LSFM platform for high-resolution imaging ranging from subcellular dynamics to whole organisms and cleared tissues. miOPM uniquely supports seamless interchangeability of oil, water, and air objectives, and maintains diffraction limited performance across a refractive index range of 1.33 - 1.51. It is compatible with standard sample mounting, current clearing protocols and high-throughput 3D imaging. We leverage miOPM to image diverse biological specimens at multiple spatial scales. By greatly expanding the adaptability and ease of use of LSFM, miOPM is poised to democratize advanced three-dimensional imaging.

bioengineering↗

CHAMP1 Complex Promotes Heterochromatin Assembly and Reduces Replication Stress

Replication stress is a major driver of genomic instability and a hallmark of cancer cells. Although dynamic heterochromatin remodeling has been implicated in replication stress response, the precise mechanisms remain unclear. Here, we identify the CHAMP1 complex, composed of CHAMP1, POGZ, HP1, and the H3K9 methyltransferase SETDB1, as a critical regulator of heterochromatin assembly at stalled replication forks. Upon replication stress, the CHAMP1 complex is recruited to stalled forks where it facilitates H3K9me3 deposition, creating a repressive chromatin environment that shields replication forks from MRE11-mediated degradation. The complex promotes the recruitment of the origin recognition complex (ORC) to sites of replication stress, such as the telomeric heterochromatin in alternative lengthening of telomeres (ALT)-positive tumor cells, thereby supporting efficient telomeric DNA replication. Loss of CHAMP1 disrupts ORC2 recruitment and impairs fork restart, leading to increased micronuclei formation and heightened sensitivity to replication stress. Notably, CHAMP1 deficiency induces synthetic lethality with FANCM inhibition in ALT-positive tumor cells, and the CHAMP1 complex is essential for the survival of CCNE1-amplified ovarian cancers. These findings uncover a chromatin-based mechanism of replication fork stabilization and suggest that CHAMP1 may represent a candidate therapeutic vulnerability in cancers with elevated replication stress.

molecular biology↗

Calcium signalling is required for anterior patterning in the mouse embryo

Anterior-Posterior axis formation in the mouse embryo requires the active migration of the DVE cell population at E5.5. While intracellular Ca2+ signalling has been shown to control cell migration in multiple cell contexts, it is unknown whether it is required for DVE migration. The pattern of Ca2+ activity in the mouse embryo at early peri-implantation stages is also unknown. Using the GCaMP6f Ca2+ reporter line we performed a detailed assessment of Ca2+ dynamics between E0.5 - E5.5 using live imaging. We find that prior to implantation, Ca2+ transients are rare, but at E5.5 widespread, periodic, Ca2+ transients in extra-embryonic tissues can be observed, including in the VE and ExE. In contrast, cells of the E5.5 epiblast remain relatively quiescent but show sporadic large-scale multi-cellular waves. Inhibition of SERCA at E5.5 abolishes Ca2+ transients and leads to DVE arrest, indicative that these transients are required for axial patterning. Together these results reveal the pattern of Ca2+ handling in the early mouse embryo and a novel requirement in anterior-posterior axis formation.

developmental biology↗

A general algorithm for consensus 3D cell segmentation from 2D segmented stacks

Cell segmentation is the foundation of a wide range of microscopy-based biological studies. Deep learning has revolutionized 2D cell segmentation, enabling generalized solutions across cell types and imaging modalities. This has been driven by the ease of scaling up image acquisition, annotation, and computation. However, 3D cell segmentation, requiring dense annotation of 2D slices still poses significant challenges. Manual labeling of 3D cells to train broadly applicable segmentation models is prohibitive. Even in high- contrast images annotation is ambiguous and time-consuming. Here we develop a theory and toolbox, u- Segment3D, for 2D-to-3D segmentation, compatible with any 2D method generating pixel-based instance cell masks. u-Segment3D translates and enhances 2D instance segmentations to a 3D consensus instance segmentation without training data, as demonstrated on 11 real-life datasets, >70,000 cells, spanning single cells, cell aggregates, and tissue. Moreover, u-Segment3D is competitive with native 3D segmentation, even exceeding when cells are crowded and have complex morphologies.

bioinformatics↗

Imaging of cellular dynamics in vitro and in situ: from a whole organism to sub-cellular imaging with self-driving, multi-scale microscopy

Many biological processes span multiple time and length scales, including developmental processes and cancer metastasis. While light-sheet fluorescence microscopy (LSFM) has become a fast and efficient method for imaging of organisms, cells and sub-cellular dynamics, simultaneous observations across these scales have remained challenging. Moreover, continuous high-resolution imaging inside living organisms has mostly been limited to few hours as regions of interest quickly move out of view due to sample movement and growth. Here, we present a self-driving, multi-resolution light-sheet microscope platform controlled by a custom Python-based software, to simultaneous observe and quantify sub-cellular dynamics and entire organisms in vitro and in vivo over hours of imaging. We apply the platform to the study of developmental processes, cancer invasion and metastasis, and we provide quantitative multi-scale analysis of immune-cancer cell interactions in zebrafish xenografts.

bioengineering↗

Multiplexed 3D Analysis of Cell Plasticity and Immune Niches in Melanoma

Diseases like cancer involve alterations in in cell proportions, states, and local interactions as well as complex changes in 3D tissue architecture. However, disease diagnosis and most multiplexed spatial profiling studies rely on inspecting thin (4-5 micron) tissue specimens. Here, we use confocal microscopy and cyclic immunofluorescence (3D CyCIF) to show that few if any cells are intact in these thin sections; this reduces the accuracy of cell phenotyping and interaction analysis. In contrast, high-plex 3D CyCIF imaging of intact cells in thick tissue sections enables accurate quantification of marker proteins and detailed analysis of intracellular structures and organelles. Precise imaging of cell membranes also makes it possible to detect juxtacrine signalling among interacting tumour and immune cells and reveals the formation of spatially-restricted cytokine niches. Thus, 3D CyCIF provides insights into cell states and morphologies in preserved human tissues at a level of detail previously limited to cultured cells.

cancer biology↗

Mesoscopic Oblique Plane Microscopy via Light-sheet Mirroring

Understanding the intricate interplay and inter-connectivity of biological processes across an entire organism is important in various fields of biology, including cardiovascular research, neuroscience, and developmental biology. Here, we present a mesoscopic oblique plane microscope (OPM) that enables whole organism imaging with high speed and subcellular resolution. A microprism underneath the sample enhances the axial resolution and optical sectioning through total internal reflection of the light-sheet. Through rapid refocusing of the light-sheet, the imaging depth is extended up to threefold while keeping the axial resolution constant. Using low magnification objectives with a large field of view, we realize mesoscopic imaging over a volume of 3.7x1.5x1 mm3 with [~]2.3 microns lateral and [~]9.2 microns axial resolution. Applying the mesoscopic OPM, we demonstrate in vivo and in toto whole organism imaging of the zebrafish vasculature and its endothelial nuclei, and blood flow dynamics at 12 Hz acquisition rate, resulting in a quantitative map of blood flow across the entire organism.

biophysics↗

Prolonged DNA Damage Checkpoint Arrest Requires Constant Renewal and the Spindle Assembly Checkpoint

Cells evoke the DNA damage checkpoint (DDC) to inhibit mitosis in the presence of DNA double-strand breaks (DSBs) to allow more time for DNA repair. In budding yeast, a single irreparable DSB is sufficient to activate the DDC and induce cell cycle arrest prior to anaphase for about 12 to 15 hours, after which cells "adapt" to the damage by extinguishing the DDC and resuming the cell cycle. While activation of the DNA damage-dependent cell cycle arrest is well-understood, how it is maintained remains unclear. To address this, we conditionally depleted key DDC proteins after the DDC was fully activated and monitored changes in the maintenance of cell cycle arrest. Degradation of Ddc2ATRIP, Rad9, Rad24, or Rad53CHK2 results in premature resumption of the cell cycle, indicating that these DDC factors are required both to establish and to maintain the arrest. Dun1 is required for establishment, but not maintenance of arrest, whereas Chk1 is required for prolonged maintenance but not for initial establishment of the mitotic arrest. When the cells are challenged with 2 persistent DSBs, they remain permanently arrested. This permanent arrest is initially dependent on the continuous presence of Ddc2, Rad9, and Rad53; however, after 15 hours these proteins become dispensable. Instead, the continued mitotic arrest is sustained by spindle-assembly checkpoint (SAC) proteins Mad1, Mad2, and Bub2 but not by Bub2s binding partner Bfa1. These data suggest that prolonged cell cycle arrest in response to 2 DSBs is achieved by a handoff from the DDC to specific components of the SAC. Furthermore, the establishment and maintenance of DNA damage-induced cell cycle arrest requires overlapping but different sets of factors.

genetics↗

Surface-guided computing to analyze subcellular morphology and membrane-associated signals in 3D

Many signalling circuits are governed by the spatiotemporal organization of membrane-associated molecules. Growing evidence suggests that the mesoscale cell surface geometry is central in modulating this interplay. However, defining the causal hierarchy between geometric and molecular factors that control signals remains challenging. Nonlinearity and redundancy among the components prevent direct experimental perturbation, with shape being the most difficult to independently control. Towards the goal of inferring causality from observational data, we developed u-Unwrap3D as a resource to map arbitrarily complex 3D cell surfaces to diverse representations, each designed to interrogate a different aspect of the dynamic interaction between cell surface geometry and molecular cues. Using u-Unwrap3D, we discover a retrograde protrusion flow on natural killer cells associated with immunological synapse formation with cancer; establish a causal association of K14+ cells with breast tumor organoid invasion; measure the speed of ruffles; and quantify bleb-mediated assembly of septin polymers at the membrane.

bioinformatics↗

Mother centrioles generate a local pulse of Polo/PLK1 activity to initiate mitotic centrosome assembly

Mitotic centrosomes are formed when centrioles start to recruit large amounts of pericentriolar material (PCM) around themselves in preparation for mitosis. This centrosome "maturation" requires the centrioles and also Polo/PLK1 protein kinase. The PCM comprises several hundred proteins and, in Drosophila, Polo cooperates with the conserved centrosome proteins Spd-2/CEP192 and Cnn/CDK5RAP2 to assemble a PCM scaffold around the mother centriole that then recruits other PCM client proteins. We show here that in Drosophila syncytial blastoderm embryos, centrosomal Polo levels rise and fall during the assembly process--peaking, and then starting to decline, even as levels of the PCM scaffold continue to rise and plateau. Experiments and mathematical modelling indicate that a centriolar pulse of Polo activity, potentially generated by the interaction between Polo and its centriole receptor Ana1 (CEP295 in humans), could explain these unexpected scaffold assembly dynamics. We propose that centrioles generate a local pulse of Polo activity prior to mitotic entry to initiate centrosome maturation, explaining why centrioles and Polo/PLK1 are normally essential for this process.

cell biology↗

ZBP1 induces inflammatory signaling via RIPK3 and promotes SARS-CoV-2-induced cytokine expression

COVID-19 caused by the SARS-CoV-2 virus remains a threat to global health. The disease severity is mediated by cell death and inflammation, which regulate both the antiviral and the pathological innate immune responses. ZBP1, an interferon-induced cytosolic nucleic acid sensor, facilitates antiviral responses via RIPK3. Although ZBP1-mediated cell death is widely described, whether and how it promotes inflammatory signaling is unclear. Here, we report a ZBP1-induced inflammatory signaling pathway that depends on ubiquitination and RIPK3s scaffolding ability independently of cell death. In human cells, ZBP1 associates with RIPK1 and RIPK3 as well as ubiquitin ligases cIAP1 and LUBAC. RIPK1 and ZBP1 are ubiquitinated to promote TAK1- and IKK-mediated inflammatory signaling. Additionally, RIPK1 recruits the p43/41-caspase-8-p43-FLIP heterodimer to suppress RIPK3 kinase activity, which otherwise promotes inflammatory signaling in a kinase activity-dependent manner. Lastly, we show that ZBP1 contributes to SARS-CoV-2-induced cytokine production. Taken together, we describe a ZBP1-RIPK1-RIPK3-mediated inflammatory signaling pathway relayed by the scaffolding role of RIPKs and regulated by caspase-8. Our results suggest the ZBP1 pathway contributes to inflammation in response to SARS-CoV-2 infection.

immunology↗

Centriole distal-end proteins CP110 and Cep97 influence cartwheel growth at the proximal-end of centrioles

Centrioles are composed of a central cartwheel tethered to nine-fold symmetric microtubule (MT) blades. The centriole cartwheel and MTs are thought to grow from opposite ends of these organelles, so it is unclear how they coordinate their assembly. We previously showed that an oscillation of Polo-like kinase 4 (Plk4) helps to initiate and time the growth of the cartwheel at the proximal end. Here, we show that CP110 and Cep97 form a complex close to the distal-end of the centriole MTs whose levels rise and fall as the new centriole MTs grow, entrained by the core Cdk/Cyclin oscillator that drives the nuclear divisions in these embryos. These CP110/Cep97 dynamics, however, do not appear to time the period of centriole MT growth directly. Instead, we find that changing the levels of CP110/Cep97 alters the Plk4 oscillation and the growth of the cartwheel at the proximal end. These findings reveal an unexpected crosstalk between factors normally concentrated at opposite ends of the growing centrioles, which may help to coordinate centriole growth.

cell biology↗