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Johnson, J. D.

Publications and source records attributed to Johnson, J. D..

At least 19 recordsLinked to original sources

Endogenous insulin mediates dynamic coordination between pancreatic cancer and systemic metabolism

Pancreatic ductal adenocarcinoma (PDAC) is commonly associated with obesity, diabetes, and cachexia. The pancreatic anabolic hormone, insulin, is implicated in each of these metabolic diseases, but how insulin levels affect tumor growth and relevant host physiological factors, was unclear. To address this, we transplanted orthotopic PDAC patient-derived organoids into mice consuming a hyperinsulinemia-inducing high-fat diet (HFD). We found that insulin concentrations were higher in tumors compared to circulation. Genetically reducing insulin levels reduced PDAC growth, particularly in HFD-fed mature male mice. In turn, we found the presence of pancreatic tumors increased glucose clearance and limited the expected dietary-induced gains in insulin, weight and fat mass. Interestingly, tumor growth in normal-chow-fed mice, but not HFD-fed mice, was associated with declining circulating insulin levels, as well as declines in fat and muscle mass. Together, these data provide new insights into the complex, insulin-centred interplay between PDAC and the hosts systemic metabolism that underlie cancer-associated metabolic dysfunction.

cancer biology↗

Functional, transcriptomic, and proteomic profiles of human primary and stem cell-derived beta cells in a state of high insulin production and increased fragility

Insulin production is a cardinal feature of pancreatic {beta} cells. Studies in rodents show that {beta} cells can switch between low and high insulin gene activity states and that elevated insulin production makes {beta} cells more vulnerable to stresses associated with diabetes. In people, genetically elevated insulin production increases the risk of type 1 diabetes. Via effects on obesity, hyperinsulinemia contributes to the pathogenesis of type 2 diabetes. Here, we characterize {beta} cells in low and high INS gene activity states sorted from primary human islets transduced with INS-GFP adenovirus and differentiated INS-EGFP knock-in embryonic stem cells (SC{beta} cells). We profile {beta} cell function, protein synthesis, resilience to diabetes associated stress, single {beta} cell transcriptomes and their co-activity networks, and purified {beta} cell proteomes. We show that human {beta} cells transition between distinct states. High INS cells have elevated maturity marker mRNAs and proteins, increased protein translation, are larger, but also more susceptible to cell death when exposed to diabetes-relevant stresses. We also catalogue thousands of differences in proteins in high INS stem cell-derived {beta} cells compared directly with high INS primary {beta} cells. Our study improves our understanding of the delicate balance between insulin production and {beta} cell resilience and guides the engineering of better {beta} cells. Blurbtranscriptional, proteomic, and functional analyses of insulin gene expression states in human {beta} cells from donor islets and stem cells Key findingsO_LIWe identify high and low INS gene activity states in human insulin-producing cells from donor islets and embryonic stem cell differentiations. C_LIO_LIWe characterize the relationship between insulin production and fragility, demonstrating that increased insulin production comes at a cost of reduced resilience to multiple stresses. C_LIO_LIFunctional, transcriptomic, and proteomic analyses identify similarities and differences between how primary and stem cell-derived {beta} cells manage stress and insulin production. C_LIO_LIWe report a comprehensive side-by-side proteomic analysis of purified primary and stem cell- derived {beta} cells in the high INS state and identify differences in protein production and secretion machinery, providing a roadmap for making better {beta} cells. C_LI

physiology↗

Cardiomyocyte pyruvate dehydrogenase kinase 1 knockout activates Rho-mediated remodeling and decreases fatty acyl availability in female mice

Pyruvate dehydrogenase kinase 1 (PDK1) inhibits pyruvate dehydrogenase (PDH) and therefore may regulate the balance between glucose and fatty acid oxidation in cardiomyocytes. We assessed metabolism and function in tamoxifen-inducible, cardiomyocyte-specific Pdk1 knockout (Pdk1cKO) mice, including both males and females fed a high fat diet, to resolve the role of PDK1 in the heart. Female, but not male, Pdk1cKO hearts showed the expected increase in cardiac PDH activity. Though cardiac function was largely preserved, female Pdk1cKO hearts had smaller left ventricles. Proteomics and phosphoproteomics revealed no change in classical hypertrophic markers but downregulated aerobic respiration alongside upregulated Ca2+ handling and Rho signalling, suggesting metabolic remodeling with altered cardiomyocyte contractility and cytoarchitecture in Pdk1cKO hearts. Concordantly, lipidomics revealed membrane remodeling marked by elevated saturated phosphatidylcholine in female Pdk1cKO hearts and decreased triacylglycerols, free fatty acids and fatty acid uptake proteins (CD36, FABP3). These findings reveal novel, female-predominant cardiometabolic roles for PDK1.

molecular biology↗

Active Neural Representation of Stimulus Categories Outside of the Focus of Attention

Previous research on the brain correlates of working memory using functional magnetic resonance imaging (fMRI) and multivariate pattern analysis (MVPA) have shown that neural activity related to information currently needed to respond on a test is considered to be in the focus of attention (FoA). An ongoing controversy pertains to the neural representation of information in working memory that is not needed for the upcoming test but possibly for a subsequent one, which is considered to reside in an activated portion of long-term memory (aLTM). The key theoretical issue regarding aLTM is whether it corresponds solely to an activity-silent neural state. Here, by using a retrospective cuing task in which two arrays of stimuli from different categories were presented in succession on the same trial, and a pattern classifier trained on the first-presented category during the presentation of the second, we provide evidence that aLTM is associated with an active neural state. Specifically, the aLTM effect was demonstrated to be dissociable in direction from that related to the FoA, there was considerable overlap between brain regions representing information in a stronger form in the FoA and a weaker form in aLTM, and the two states appeared to be differentially subject to flexible cognitive control versus natural decay.

neuroscience↗

Midkine Dependency Defines a Therapeutically Actionable Vulnerability in Medulloblastoma

Medulloblastoma (MB), the most common malignant pediatric brain tumor, remains associated with high recurrence rates and substantial treatment-related morbidity despite aggressive multimodal therapy. Here, we identify midkine (MDK), a secreted growth factor/cytokine, as a previously unrecognized central regulator of MB growth and survival. Tissue microarray analysis revealed elevated MDK protein expression in MB specimens, and single-cell RNA sequencing datasets showed tumor cell-specific MDK expression. Genetic depletion or antibody-mediated neutralization of MDK suppressed proliferation and survival and induced apoptosis across multiple MB cell lines, whereas recombinant MDK supplementation exerted the opposite effect. Mechanistically, phosphokinase profiling and immunoblot analyses showed that MDK signals through multiple receptors, including nucleolin (NCL), LRP1, and syndecan-2 (SDC2), to sustain oncogenic ERK1/2 and Akt-mTOR-S6 signaling. Transcriptomic profiling following MDK silencing or depletion revealed marked suppression of ribosome biogenesis, global protein translation, and MYC-driven programs, coupled with activation of inflammatory and apoptotic responses. Consistently, mechanistic studies utilizing RPS6 staining, ribosomal RNA quantification, puromycin SUnSET, and OPP incorporation assays confirmed that loss of MDK impairs ribosome biogenesis and protein synthesis. Notably, MDK suppression also triggered robust activation of the IFN-cGAS-STING pathway, linking translational stress to innate immune signaling. In orthotopic xenograft models, CRISPR-mediated MDK knockout significantly reduced tumor growth and prolonged survival. Together, these findings establish MDK as a key integrator of oncogenic signaling, translational control, and innate immunity in MB, highlighting MDK as a compelling therapeutic target.

cancer biology↗

Psilocybin Attenuates Cortical Representations of Aversion in the Mouse Auditory Cortex

Psilocybin can produce sustained benefits in affective and trauma-related disorders, yet if and how it reshapes sensory representations of learned valence associations remains largely unclear. To address this, we used longitudinal two-photon calcium imaging in awake C57BL/6 mice to examine how psilocybin modulates layer 2/3 auditory cortex activity at single-cell and population levels. Evoked responses were measured for tones with or without prior associations with valenced stimuli, as well as for the valenced stimuli themselves. Most responsive neurons were selective for tones alone, while distinct subsets responded exclusively to reward or aversive stimuli, and a smaller population encoded both. Psilocybin selectively reduced responses to aversive stimuli and earlier-established aversive-associated tones, without affecting aversive association, reward responses, or responses to newly aversive-associated tones. At the population level, psilocybin acutely increased coordination across tone-responsive neurons, while later reducing it selectively among neurons encoding the aversive-associated tone. These results demonstrate that psilocybin preferentially dampens well consolidated aversive sensory representations in auditory cortex, rather than fresh associations, without broadly affecting auditory processing or new aversive learning.

neuroscience↗

Tabular foundation model predicts alternative lengthening of telomeres (ALT) and identifies SMARCAL1 as a target in ALT-driven cancers

Alternative lengthening of telomeres (ALT) is a telomerase-independent pathway used by aggressive cancers to maintain their replicative immortality. Because ALT is absent from normal human cells, it is an appealing target for cancer therapy, but the lack of ability to determine ALT status at scale has hindered discovery. Here, we developed ALTitude, a machine learning method from a tabular foundation model that infers ALT from cell line whole genome sequencing data, without need for paired germline analysis. We deployed ALTitude across the DepMap, doubling the number of known ALT+ cancer models. Systematic integration of ALTitude with CRISPR-Cas9 screens yielded the selective dependency on SMARCAL1 in ALT+ cell lines, where we show it stabilizes the ALT phenotype. Acute depletion of SMARCAL1 leads to G2/M arrest, mitotic catastrophe, and cell death. These data provide a valuable resource for studying ALT-related genomic features and present SMARCAL1 as a therapeutic target for ALT+ malignancies.

cancer biology↗

Lowering insulin mitigates female reproductive aging and diet-induced ovarian dysfunction

Hyperinsulinemia has consequences beyond metabolic dysfunction, including reproductive system effects. We found that hyperinsulinemia at age 46-47 was predictive of earlier menopause in the Study of Womens Health Across the Nation. To test causality between insulin levels and reproductive aging, we longitudinally evaluated chow- or high-fat, high-sucrose (HFHS)-fed Ins1-null female mice with full or partial Ins2 insulin gene expression. Ins1-/-;Ins2+/-mice had lower HFHS-induced hyperinsulinemia and less weight gain than their full-Ins2 littermates, despite comparable HFHS-induced glucose intolerance up to 9 months. By 15 months, Ins1-/-;Ins2+/+ ovaries showed multinucleated giant cell accumulation with HFHS, while Ins1-/-;Ins2+/- mice were protected against this response and maintained a higher reserve of follicles. Moreover, aged Ins1-/-;Ins2+/- mice were 9-fold more likely to conceive on HFHS than hyperinsulinemic Ins1-/-;Ins2+/+ mice. Elevated insulin is therefore a critical mechanistic link between metabolic dysfunction and reproductive aging, and curtailing insulin levels protects against subfertility and HFHS-induced ovarian decline.

physiology↗

Biological sex affects human islet gene expression and mitochondrial function in type 2 diabetes

The clinical characteristics of type 2 diabetes (T2D) differ between the sexes. For example, the risk of T2D is higher in males than in premenopausal females, whereas the risk of T2D-associated cardiovascular disease is higher in females. However, the sex-dependent mechanisms of T2D pathogenesis remain incompletely understood. Publicly available human islet datasets, such as HPAP and Humanislets.com, offer a valuable tool for uncovering the impact of biological sex on islet structure, gene expression, and function at a scale that was not previously possible. We performed an integrated analysis of data from publicly available sources to identify sex differences in baseline islet characteristics in donors without diabetes and subsequently examined these features in donors who lived with T2D. Among donors without diabetes, female islets had a greater proportion of alpha-cells compared with male islets and showed enriched expression of ribosomal and mitochondrial pathways in both beta- and alpha-cells. Measurements of mitochondrial function in female islets revealed lower spare respiratory capacity compared to male islets. Male and female islets had distinct changes in gene and protein expression in the context of T2D with female islets having greater preservation of insulin content and fewer defects in islet function. Together, these data show female islets have fewer islet impairments in T2D. This highlights the need for detailed mechanistic studies in both sexes to support effective and sex-informed interventions for T2D.

cell biology↗

Loss of brain insulin production impairs learning and memory in female mice

Diabetes is characterized by dysfunctional insulin release and action, and it is a risk factor for Alzheimers disease, the most common form of dementia. Alterations in brain insulin signalling and metabolism have been linked with Alzheimers disease. The ancestral insulin gene, Ins2, is transcribed locally within the brain. Here we demonstrate that hippocampal Ins2 mRNA is higher in females than males, and modulated by diet. To specifically determine how locally-produced insulin influences hippocampal function, we used mice with germline Ins2 knockout (Ins2-/-) and the normal complement of wildtype Ins1 alleles. Compensation from the Ins1 gene ensured normal glucose tolerance, normal insulin sensitivity, normal fasting insulin, and normal body weight under these conditions. Using the Morris water maze, we found that visuo-spatial learning and memory performance of female Ins2-/- mice was significantly impaired relative to wild-type mice, whereas the performance of male Ins2-/- and wild-type mice did not differ. We profiled isolated hippocampi from female Ins2-/- and littermate control mice using RNA sequencing to provide an unbiased analysis of gene expression differences that underlie these behavioural changes. Cyclin D1 (Ccnd1) was significantly reduced in Ins2-/- mice, prompting us to examine adult neurogenesis using exogenous mitotic marker EdU and the immature neuronal marker doublecortin (DCX). Our data demonstrate female-specific roles for brain-derived Ins2 on learning and memory function in mice. Research in contextO_ST_ABSWhat is already known about this subject?C_ST_ABSO_LIAlzheimers disease and type 2 diabetes share common risk factors and metabolic dysfunction. C_LIO_LIInsulin and insulin signalling are known to have positive effects on neuronal health and cognition. C_LIO_LILocal insulin production has been reported in the brain, including the hippocampus, which plays critical roles in learning and memory, as well as Alzheimers pathophysiology. C_LI What is the key question?O_LIWhat are the consequences of deleting the Ins2 gene, which selectively prevents local brain insulin production, on learning and memory in mice? C_LI What are the new findings?O_LIHippocampal insulin production via the Ins2 gene is sexually dimorphic and modulated by diet. C_LIO_LIKnocking out brain insulin production in Ins2-/- mice does not have significant effects on glucose homeostasis in these diet and housing conditions. C_LIO_LIKnocking out brain insulin production in Ins2-/- mice results in learning and memory impairments in female but not male mice. C_LI How might this impact on clinical practice in the foreseeable future?O_LIThese pre-clinical observations demonstrate a causal role for insulin in learning and memory, but will require additional human studies before they can impact clinical practice. C_LI

physiology↗

A prioritized medium-throughput screen on human stem cell derived insulin secreting beta cells identifies FGF4, FGF5, FGF8F, FGF19 and FGF21 as protective factors

AbstractStem cell-derived {beta}-like cells (SC{beta} cells) are a potential alternative to cadaveric {beta} cells for replacement therapy in type 1 diabetes. However, SC{beta} cells face a multitude of stresses that must be overcome. Both {beta} cells and SC{beta} cells reside in complex microtissues and can therefore be modulated by hundreds of autocrine/paracrine signals within these islets or spheroids. Here, we leveraged multi-omics data from late-stage SC{beta} cells and human islets to map ligand-receptor pairs and generate a prioritized list of ligands for high-content SC{beta} cell survival screening. Our medium-throughput screen tracked cell number, cell death, and INS production over several days using automated, high-content imaging. Members of the fibroblast growth factor (FGF) family significantly prevented cytokine-induced cell death, with the top validated hits being FGF4, FGF5, FGF19, FGF21, and FGF8F. With these results, there is the potential to improve SC{beta} cell survival in vitro via readily targetable pathways and to produce a more robust product for translation to the clinic.

molecular biology↗

Cell type-specific eQTL detection from single-cell RNA-seq reveals post-transcriptional regulatory mechanisms in human islets

Gene regulatory networks (GRNs) must be robust to maintain cellular identity across individuals yet flexible to accommodate population genetic variants. Comparing expression quantitative trait loci (eQTLs) in health and disease can therefore reveal hidden players in gene regulation. Here, we developed a computational pipeline to infer post-transcriptional regulatory events and their functional consequences from eQTL signals located in the 3' untranslated region of genes using single-cell RNA sequencing. As a case study, we repurposed datasets from human islets of donors with and without type 2 diabetes (T2D). We identified eQTL landscapes differing by cell type and diabetes status, with cell-type specificity associated with gene differential expression and RNA-binding proteins. Integrating eQTLs with GWAS and miRNA hits linked variants in G6PC2, QDPR, and RELL1 to insulin secretion, endoplasmic reticulum stress, and oxidative phosphorylation. Our pipeline provides a framework to unravel post-transcriptional regulatory mechanisms in health and disease at cell type resolution.

genetics↗

FROM FEAR TO FEAST: RATTLESNAKES NAVIGATE THE LANDSCAPE OF FEAR TO OPTIMIZE FORAGING

According to optimal foraging theory, mesopredators should forage in areas where their prey is abundant while avoiding high predation risk. Here, we investigate how environmental factors influence mesopredators abilities to minimize spatiotemporal overlap with predators while increasing spatiotemporal overlap with prey. We paired thirty western diamond-backed rattlesnake (Crotalus atrox) 3D-printed replicas with game cameras in West Texas for two years to quantify several spatiotemporal factors affecting prey availability and predation risk. Concurrently, 25 Crotalus atrox were radiotracked at the same site to gather activity and microhabitat selection data regarding free-ranging individuals. Random forest algorithms were trained using data obtained from the game camera and applied to predict the probability of predation and the probability of prey encounter for each radiotracking event. Time of day, month, vegetation structure, and concealment percentage, all had a significant association with the probability of predation and the probability of prey encounter. Our results suggest that rattlesnakes choose to be active when and where the probability of prey encounter was significantly higher than the probability of detection by predators, thus following optimal foraging theory. Our results demonstrate that mesopredators increase chances of prey capture while reducing predator detection in natural setting.

ecology↗

Pyruvate dehydrogenase kinase 1 controls triacylglycerol hydrolysis in cardiomyocytes

Pyruvate dehydrogenase kinase (PDK) 1 is one of four isozymes that inhibit the oxidative decarboxylation of pyruvate to acetyl-CoA via pyruvate dehydrogenase. PDK activity is elevated in fasting or starvation conditions to conserve carbohydrate reserves. PDK has also been shown to increase mitochondrial fatty acid utilization. In cardiomyocytes, metabolic flexibility is crucial for the fulfillment of high energy requirements. The PDK1 isoform is abundant in cardiomyocytes, but its specific contribution to cardiomyocyte metabolism is unclear. Here we show that PDK1 regulates cardiomyocyte fuel preference by mediating triacylglycerol turnover in differentiated H9c2 myoblasts using lentiviral shRNA to knockdown Pdk1. Somewhat surprisingly, PDK1 loss did not affect overall PDH activity, basal glycolysis, or glucose oxidation revealed by oxygen consumption rate experiments and 13C6 glucose labelling. On the other hand, we observed decreased triacylglycerol turnover in H9c2 cells with PDK1 knockdown, which was accompanied by decreased mitochondrial fatty acid utilization following nutrient deprivation. 13C16 palmitate tracing of uniformly labelled acyl chains revealed minimal acyl chain shuffling within triacylglycerol, indicating that the triacylglycerol hydrolysis, and not re-esterification, was dysfunctional in PDK1 suppressed cells. Importantly, PDK1 loss did not significantly impact the cellular lipidome or triacylglycerol accumulation following palmitic acid treatment, suggesting that effects of PDK1 on lipid metabolism were specific to the nutrient-deprived state. We validated that PDK1 loss decreased triacylglycerol turnover in Pdk1 knockout mice. Together, these findings implicate a novel role for PDK1 in lipid metabolism in cardiomyocytes, independent of its canonical roles in glucose metabolism.

biochemistry↗

HumanIslets: An integrated platform for human islet data access and analysis

Comprehensive molecular and cellular phenotyping of human islets can enable deep mechanistic insights for diabetes research. We established the Human Islet Data Analysis and Sharing (HI-DAS) consortium to advance goals in accessibility, usability, and integration of data from human islets isolated from donors with and without diabetes at the Alberta Diabetes Institute (ADI) IsletCore. Here we introduce HumanIslets.com, an open resource for the research community. This platform, which presently includes data on 547 human islet donors, allows users to access linked datasets describing molecular profiles, islet function and donor phenotypes, and to perform various statistical and functional analyses at the donor, islet and single-cell levels. As an example of the analytic capacity of this resource we show a dissociation between cell culture effects on transcript and protein expression, and an approach to correct for exocrine contamination found in hand-picked islets. Finally, we provide an example workflow and visualization that highlights links between type 2 diabetes status, SERCA3b Ca2+-ATPase levels at the transcript and protein level, insulin secretion and islet cell phenotypes. HumanIslets.com provides a growing and adaptable set of resources and tools to support the metabolism and diabetes research community.

systems biology↗

Signal transduction pathways controlling Ins2 gene activity and β cell state transitions

Pancreatic {beta} cells exist in low and high insulin gene activity states that are dynamic on a scale of hours to days. Here, we used live 3D imaging, mass spectrometry proteomics, and targeted perturbations of {beta} cell signaling to comprehensively investigate Ins2(GFP)HIGH and Ins2(GFP)LOW {beta} cell states. We identified the two Ins2 gene activity states in intact isolated islets and showed that cells in the same state were more likely to be nearer to each other. We report the proteomes of pure {beta} cells to a depth of 5555 proteins and show that {beta} cells with high Ins2 gene activity had reduced {beta} cell immaturity factors, as well as increased translation. We identified activators of cAMP signaling (GLP1, IBMX) as powerful drivers of transitions from Ins2(GFP)LOW to the Ins2(GFP)HIGH states. Okadaic acid and cyclosporine A had the opposite effects. This study provides new insight into the proteomic profiles and regulation of {beta} cell states.

cell biology↗

β-Hydroxybutyrate promotes basal insulin secretion while decreasing glucagon secretion in mouse and human islets.

Dietary carbohydrates raise blood glucose and limiting carbohydrate intake improves glycemia in patients with type 2 diabetes. Low carbohydrate intake (< 25 g) allows the body to utilize fat as its primary fuel. As a consequence of increased fatty acid oxidation, the liver produces ketones to serve as an alternative energy source. {beta}-Hydroxybutyrate ({beta}HB) is the most abundant ketone. While {beta}HB has a wide range of functions outside of the pancreas, its direct effects on islet cell function remain understudied. We examined human islet secretory response to acute racemic {beta}HB treatment and observed increased insulin secretion at low glucose concentrations (3 mM glucose). Because {beta}HB is a chiral molecule, existing as both R and S forms, we further studied insulin and glucagon secretion following acute treatment with individual {beta}HB enantiomers in human and C57BL6/J mouse islets. We found that acute treatment with R-{beta}HB increased insulin secretion and decreased glucagon secretion at physiological glucose concentrations in both human and mouse islets. Proteomic analysis of human islets treated with R-{beta}HB over 72 h showed altered abundance of proteins that may promote islet cell health and survival. Collectively, our data show that physiological concentrations of {beta}HB influence hormone secretion and signaling within pancreatic islets.

cell biology↗

Distinct expression patterns of Hedgehog signaling components in mouse gustatory system during postnatal tongue development and adult homeostasis

It is well established that the Hedgehog (HH) pathway regulates embryonic development of anterior tongue taste fungiform papilla (FP) and the posterior circumvallate (CVP) and foliate (FOP) taste papillae, and taste organ maintenance and regeneration in adults. However, there are knowledge gaps in determining HH signaling regulation in postnatal taste organ differentiation and maturation. Importantly, the HH transcription factors GLI1, GLI2 and GLI3 have not been investigated in early postnatal stages; and, the receptors PTCH1, GAS1, CDON and HHIP, required to either drive HH pathway activation or antagonism, remain unexplored. Using lacZ reporter mouse models, we mapped expression of the HH ligand SHH, receptors, and transcription factors in FP, CVP and FOP in early and late postnatal and adult stages. In adults we also studied the soft palate, and the geniculate and trigeminal ganglia which extend afferent fibers to the anterior tongue. Shh and Gas1 are the only components that were consistently expressed within taste buds of all three papillae and the soft palate. In the first postnatal week, we observed a broad expression of HH signaling components in FP and adjacent, non-taste filiform (FILIF) papillae in epithelium or stroma and tongue muscles. Remarkably, we observed elimination of Gli1 in FILIF and Gas1 in muscles, and downregulation of Ptch1 in lingual epithelium and of Cdon, Gas1 and Hhip in stroma from late postnatal stage. Further, HH receptor expression patterns in CVP and FOP epithelium differed from anterior FP. Among all the components, only known positive regulators of HH signaling, SHH, Ptch1, Gli1 and Gli2, were expressed in the ganglia. Our studies emphasize differential regulation of HH signaling in distinct postnatal developmental periods and in anterior versus posterior taste organs, and lay the foundation for functional studies to understand the roles of numerous HH signaling components in postnatal tongue development.

developmental biology↗