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Function of maternal mRNA during zebrafishembryogenesis

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NIGMS - National Institute of General Medical Sciences

Project Summary Our research focuses on unraveling the fundamental processes of early vertebrate embryogenesis, particularly the dynamic molecular mechanisms that regulate maternal and zygotic RNAs during the maternal-to-zygotic transition (MZT). This crucial period involves the degradation of maternal RNAs and activation of the zygotic genome, processes essential for proper embryonic development. Our goal is to dissect the spatial and temporal regulation of maternal and zygotic transcripts, identify the functions of individual maternal RNAs, and understand their roles in gene expression, including mRNA stability and translational regulation. Our recent work has established transformative tools and frameworks for investigating embryogenesis, including the development of the CRISPR-Cas13d system for efficient maternal RNA knockdown in zebrafish embryos. This system has overcome limitations in traditional genetic approaches, including lethal and/or masked phenotypes due to maternal contribution, enabling us to systematically target maternal RNAs and investigate their functions with unprecedented precision. Through integrative multi-omics approaches—such as RNA-seq, SLAM-seq, ribosome profiling, and quantitative proteomics—we have made significant progress in understanding codon-dependent mRNA stability, maternal-zygotic gene expression, and the interplay of transcription, translation, and protein accumulation during early embryogenesis. Over the next five years, we aim to expand these efforts by addressing key questions surrounding the spatial and temporal regulation of maternal RNAs and their influence on early development. Our studies will focus on: Maternal RNA Decay, Localization and function during MZT: Investigating how maternal RNAs, such as cth1, are regulated by spatial and cell-specific decay mechanisms. This will include identifying cis-regulatory elements in their untranslated regions and characterizing the molecular factors that mediate their localization and stability. Leveraging CRISPR-Cas13d and multi-omics techniques to uncover the roles of maternal RNAs in zygotic genome activation and early cellular processes. Broader Exploration of Maternal RNAs: Systematically investigating additional maternal genes, including genes encoding small translated open reading frames, genes with specific temporal expression and spatially localized transcripts with critical developmental roles. The overarching vision of our research is to establish a comprehensive understanding of how gene regulation is orchestrated at multiple levels—spatial, temporal, and molecular—during the earliest stages of vertebrate development. Our work has broad implications for advancing knowledge in developmental biology, reproductive health, and gene regulation, with potential applications in areas such as fertility, regenerative medicine, and mRNA-based therapeutics. By integrating cutting-edge technologies with innovative approaches, our research program is poised to uncover fundamental principles of gene regulation and mRNA stability, contributing to a deeper understanding of the molecular processes that drive the transformation of a single cell into a multicellular organism.

Up to $429K

Deadline: 2031-01-31

Health

Functional and biochemical analysis of RNA exosome variants linked to neurological disorders

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NINDS - National Institute of Neurological Disorders and Stroke

Project Summary Over 300 million individuals worldwide are affected by developmental disorders. Many such disorders arise from dysfunction of RNA-binding proteins and regulatory factors that play general roles in gene expression but often cause pathology within specific organ systems. An example of a critical RNA processing factor linked to disease is the RNA exosome, an essential and conserved 3’ to 5’ ribonuclease complex, which processes and/or degrades most types of cellular RNAs. Notably, dysfunction of the RNA exosome is associated with human diseases, termed “RNA exosomopathies”, which manifest during development and can result in neurological disorders such as microcephaly, pontocerebellar hypoplasia and motor neuron deficiencies as well as cardiac conduction and rhythm abnormalities which can cause sudden cardiac death. Patients with RNA exosomopathies rarely live beyond childhood, and the diseases currently have no treatments. RNA exosomopathies are typically caused by single amino acid changes in conserved regions of the structural subunits of the RNA exosome complex. The list of RNA exosomopathies continues to expand, highlighting the need to characterize these diseases and uncover disease mechanisms. My proposal will be the first to analyze a series of missense mutations that occur in the EXOSC5 subunit of the RNA exosome to understand how each of these changes similarly or distinctly alters RNA exosome function and leads to disease. I hypothesize that different mutations within EXOSC5 cause distinct functional changes in RNA exosome activity. Because individuals with pathogenic mutations in the EXOSC5 gene show both neurological and cardiac symptoms, I will focus on defining how a series of missense mutations in this gene impact RNA exosome activity and function using a rapid and facile system by modeling these changes in budding yeast. Thus, my studies will test this hypothesis by exploiting the Saccharomyces cerevisiae ortholog of EXOSC5, Rrp46. Due to the evolutionary, functional and structural conservation of the RNA exosome, budding yeast provides a versatile system to characterize functional consequences of changes linked to RNA exosome disease. For these aims, we have generated five rrp46 missense mutations that cause RNA exosomopathies associated with both neurodevelopmental and cardiac pathologies: rrp46-Q86I, rrp46-L127T, and rrp46-L191H (linked to different severities of cerebellar hypoplasia and risk of sudden cardiac death), a new mutant obtained from our clinical collaborators, rrp46-C202L (linked to congenital ataxia), and rrp46-V73K (linked to cardiac abnormalities). Using these models, I will: Aim 1) examine the impact of each mutation on RNA exosome function through a combination of functional assays and unbiased comparative transcriptomics; and Aim 2) examine the impact of each mutation on RNA exosome structural integrity and interactions through subunit co-migration assays and extragenic suppressor screens. Through these aims, my studies will uncover how different RNA exosome mutations impact the complex to cause distinct molecular outcomes and provide me with critical training.

Up to $50K

Deadline: 2029-01-31

Health

Functional characterization of adipocyte-derived lipocalin 2-containing extracellular vesicles in senescence

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NIA - National Institute on Aging

PROJECT SUMMARY Maintaining healthy adipose tissue function is essential for metabolic homeostasis and the prevention of metabolic diseases. As potent endocrine cells, adipocytes secret various bioactive molecules and extracellular vesicles that influence the function of tissues and organs throughout the body. Besides adipocytes, multipotent stem and progenitor cells in adipose tissue are crucial for tissue maintenance and repair throughout life. With aging, adipose tissue undergoes species-conserved changes, including decreased subcutaneous adiposity, increased visceral adiposity, and a decline in the thermogenic capacity of brown and beige adipose tissue. In contrast to the detrimental effects of adipocyte hypertrophy, hyperplasia, a process known as adipogenesis, supports tissue development, repair, and metabolic health. However, adipogenesis is impaired during aging, which has been linked to adipose progenitor cell senescence, potentially contributing to the development of metabolic diseases. Recent studies indicate that extracellular vehicles (EVs), particularly adipocyte-derived EVs (Ad-EVs) play a role in intercellular communication within adipose tissue, regulating its function. Ad-EVs exhibit heterogeneity, with large and small Ad-EVs differing in protein and lipid composition, suggesting functional diversity. However, the specific subtypes of Ad-EVs secreted by adipocytes and their distinct roles in local and systemic metabolic regulation remain unexplored. Our preliminary studies indicate that Lipocalin 2 (LCN2), a novel phosphatidic acid (PA) binding protein, plays a potential role in senescence and adipogenesis of adipose stem and progenitor cells (ASPCs) through EV-mediated intercellular communication. Lcn2 deficiency impairs adipogenesis and results in hypertrophic obesity. Stromal- vascular (SV) cells from the brown and white adipose tissue of Lcn2 knockout mice exhibit increased senescence and decreased adipogenesis. Importantly, we have identified LCN2 in a distinct subpopulation of Ad-EVs that is separate from adiponectin-containing Ad-EVs. In this proposal, we aim to characterize the cargo composition and function of LCN2-containing EVs (LCN2+EVs) released from adipocytes, examining their role in ASPC senescence and adipogenesis during aging. We hypothesize that adipocyte-derived LCN2+EVs possess anti-senescence properties that maintain ASPC health and adipogenic capacity through adipocyte-to-ASPC communication within adipose tissue, and this effect is context-dependent. We propose two aims to characterize the cargo composition of LCN2+EVs released from adipocytes upon metabolic and inflammatory stress, and 2) determine the role of adipocyte-derived LCN2+EVs in ASPC senescence and adipogenesis during aging. The project outcomes are expect to provide new perspectives on the pathogenesis of aging-related metabolic disorders and pave the way for developing new therapeutic strategies targeting adipose tissue function.

Up to $424K

Deadline: 2028-01-31

Health

Gating properties of specific voltage-gated sodium channel complexes involved in rare disease

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NCATS - National Center for Advancing Translational Sciences

ABSTRACT This proposal addresses the need to investigate understudied proteins associated with rare diseases, such as Brugada Syndrome (PAR-25-122). One class of proteins highlighted in this RFA—Scn2b, Scn3b, and Scn4b— belongs to a family of β subunits that associate with the large pore-forming α subunits of voltage-gated sodium channels (NaV), which regulate electrical excitability throughout the body. In total, there are four distinct β subunits that can mix and match with nine different α subunits. Beta subunits are widely recognized for their ability to regulate the gating properties, trafficking, and pharmacology of Nav channel complexes. Dysfunction of these subunits has been linked to several human diseases, including epilepsy and cardiac arrhythmias such as long QT syndrome, atrial fibrillation, and Brugada syndrome. Additionally, mutations in NaV α subunits have been implicated in rare diseases, including SCN8A encephalopathy (SCN8A/ NaV 1.6), hereditary sensory and autonomic neuropathy type 7 (SCN11A/ NaV1.9), and dilated cardiomyopathy-1E (SCN5A/ NaV1.5). A critical step in understanding how beta subunits contribute to disease is elucidating their precise modulatory effects on NaV function. Electrophysiological studies in heterologous cells have demonstrated the ability of beta subunits to influence channel gating, pharmacology, and trafficking. However, results across multiple studies have been inconsistent, often due to variability in the cell lines used. A major confounding factor is that many cell lines endogenously express beta subunits, which can interfere with exogenously introduced β subunits under investigation. To overcome this limitation, we developed a specialized cell line lacking all β subunits, including Scn2b, Scn3b, and Scn4b, as well as Scn1b, MPZ, MPZL1, MPZL2, and MPZL3. These cells, termed beHAPe cells (beta- eliminated haploid cells for expression), provide a controlled system to study NaV channel regulation. Our initial electrophysiological studies using beHAPe cells reveal novel properties of beta subunits in modulating NaV1.5, the primary α subunit in cardiac tissue. Building on these findings, we propose to produce stably-expressing human (HEK) cell lines to systematically define the roles of Scn2b, Scn3b, and Scn4b in modulating additional α subunits, including NaV1.6 (a key subunit in the central nervous system) and NaV1.7, NaV 1.8, and NaV 1.9 (which are predominant in the peripheral nervous system). This work will provide deeper insights into their function in these tissues and their associated diseases. Additionally, our new data suggest that Nav1.8 plays a previously unrecognized role in cardiac function alongside NaV1.5. Understanding how β subunits modulate pore-forming subunits could provide new insights into their involvement in cardiac arrhythmias, expanding their known roles beyond the nervous system. Taken together, in addition to providing new information on the understudied Scn2b, Scn3b, and Scn4b proteins, our newly generated stable cell lines will enable studies for the development of novel therapeutics for isoform specific modulation of specific α- and β-subunit pairs.

Up to $156K

Deadline: 2027-01-31

Health

Generating Critical Knowledge on the NMP Peptide Signaling in the Peripheral Nervous System

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NINDS - National Institute of Neurological Disorders and Stroke

PROJECT SUMMARY This new R21 application focuses on extending our work on the neuronal membrane proteasome derived peptides (NMP-peptides)1-7 and their link to peripheral neuron crosstalk and regulation. In this proposal, we present new data describing NMP-peptides presence and function on DRG neuron signaling in the PNS. In our previous studies using central nervous system (CNS) neurons, we developed new tools and protocols to purify, identify, and test specific NMP-derived peptides.2,4,5 In the peripheral nervous system (PNS), we made the important discovery that NMPs are expressed only on a subset (Mgpra3+ and Cystlr2+) of somatosensory DRG neurons.7 Using approaches developed for our CNS studies, we have found a preliminary set of NMP-peptide sequences that can lead to modulation of neuronal signaling in diverse populations of naïve DRG neuronal subtypes, including those that do not express NMPs. Taken together, we now hypothesize that specific NMP- peptides mediate ‘crosstalk’ between sensory DRG neuron subtypes (NMP(+) and NMP(-)) to induce downstream changes in neuronal signaling. Consistent with our hypothesis, we demonstrated that inhibition of NMPs modulate cell autonomous and cell non-autonomous responses to stimulation between DRG subtypes.7 In this proposal we aim to test our hypothesis in the PNS, using proteomics, calcium imaging, and single cell RNA sequencing studies with the following expected outcomes: 1) Identify sequences of PNS NMP-peptides following distinct stimuli; 2) Determine which NMP-peptides actively stimulate specific DRG subtypes; And 3) Show the NMP-peptide induced sensory neuron-specific transcriptional changes. Our goal with this application will be to reveal the actions of NMP-peptides in the PNS and provide a foundation for further studying this novel mechanism of crosstalk between sensory neurons that we have shown is critical for sensory behaviors such as touch and pain.7 NMP peptides offer a new opportunity in this area of DRG crosstalk and this R21 is foundational as a first of its kind investigation in NMP peptides and PNS function. To attain our goal, we will focus on the mouse DRG sensory neurons which has a variety of tools for evaluating the details of cell type specific biochemical, cellular, and calcium signaling changes. Specifically: Aim 1. To define and classify the stimulus induced NMP-derived peptides from DRG neurons, to test our working hypothesis that NMP expressing DRG neurons produce NMP-peptides following specific stimuli (depolarization or pruritogen stimulation). Aim 2. To study and identify the NMP-peptides that activate DRG neurons, to test our working hypothesis that active NMP-peptides have unique signature sequence and stimulate distinct subsets of DRG neurons. Aim 3. To determine the DRG-specific transcriptional programs stimulated by active NMP- peptides, to test our working hypothesis that NMP-peptides work to drive new downstream transcriptional changes in diverse populations of DRGs. This will begin to define a mechanistic link between specific NMP- peptides and the downstream autonomous and non-autonomous regulation of DRG subtypes.

Up to $233K

Deadline: 2028-01-31

Health

Genetic determinants of AAV liver transduction and toxicity

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NIDDK - National Institute of Diabetes and Digestive and Kidney Diseases

Six adeno-associated virus (AAV) vector based biodrugs have been approved by the FDA to treat genetic disorders. The great therapeutic success of AAV gene transfer has been tempered by the often-associated liver toxicity and, with liver-directed therapies, the concomitant fall in the transgene expression. There are marked interpatient differences in susceptibility to AAV liver toxicity and transgene expression, and we have demonstrated similar inter-donor variability in cultured human hepatocytes and in various strains of mice, strongly implicating the role of genetic background. We are proposing to study AAV liver interactions in Collaborative Cross (CC) mice, a relatively new genetic reference population engineered to maximize genetic diversity. We have successfully used CC mice to identify candidate genes which may underlie susceptibility to liver toxicity from several drugs. We have also observed marked differences between CC lines in the extent and kinetics of transgene expression after AAV liver targeting as well as liver toxicity, and this susceptibility was reproduced in hepatocyte spheroids. Our central hypothesis is that CC inter-strain susceptibility to AAV hepatotoxicity and transgene expression will be mirrored in cultured hepatocyte spheroids prepared from the strains and that combining in vivo and hepatocyte spheroid data will provide new insights that will improve the safety and efficacy of AAV gene therapy. To this end, we will pursue 3 specific aims: Aim 1. Elucidate the role of genetic factors underlying susceptibility of AAV liver toxicity and variation in transduction efficiency. After systemic administration of AAV vectors to the fully inbred CC populations (63 lines), we will identify the associations between host genetic background and protein/metabolite biomarkers and susceptibility to liver toxicity and to the long-term, stable transgene expression. Aim 2. Identify non-genetic factors influencing susceptibility to AAV liver toxicity and transduction efficiency. The effect of different parameters (AAV serotypes/variants, dose, transgene, dsAAV vs ssAAV, steroids, empty AAV virions) on AAV liver toxicity and transduction efficiency will be studied in CC strains identified in Specific Aim 1 as susceptible to liver toxicity and/or reduced transgene expression. Aim 3. Explore a novel model culture system to study AAV liver toxicity and transduction. We have demonstrated that primary hepatocytes cultured as spheroids in 386 well plates maintain a mature hepatocyte phenotype and are transduced by AAV. We propose to expand these studies to determine correlations with results from our live CC studies, and to further pursue the underlying mechanisms. Our proposed studies should provide mechanistic insight that may result in the design of safer AAV vectors, as well as identify promising biomarkers to guide safer dosing of existing AAV vectors. Moreover, our studies may support future susceptibility testing of iPSC-derived hepatocytes obtained from patients who are candidates for AAV gene therapy.

Up to $764K

Deadline: 2029-12-31

Health

Genetic dissection of the 17q21.31 MAPT locus in neurodegenerative disease

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NIA - National Institute on Aging

PROJECT SUMMARY / ABSTRACT Alzheimer’s disease and related dementias manifest with age-related progressive cognitive decline. Beyond sharing various aspects of their clinical and neuropathological presentation, these diseases are thought to also share genetic drivers, but those remain poorly characterized. One region on the long arm of chromosome 17 has been associated with risk for Alzheimer’s disease and more than 6 other neurodegenerative diseases, as well as multiple neurodevelopmental and non-brain diseases. This locus has been nicknamed the “MAPT locus” due to the presence of the microtubule-associated protein tau (MAPT) gene within this region. Abnormal deposits of the tau protein are linked to many neurodegenerative diseases. However, evidence suggests that MAPT is not the only gene that mediates disease risk in this large and gene-rich locus. Here we propose to leverage the genetic variation at the MAPT locus to pinpoint potential drivers of the diverse set of neuro- pathologies associated with this locus. The reason that these disease drivers remain unknown is that the MAPT locus is one of the most genetically complex loci in the human genome. During evolution, the locus underwent an inversion that flipped the orientation of approximately 14 genes. This inversion prevents recombination, creating two distinct alleles or “haplotypes”, named H1 and H2, within the human population. These haplotypes have diverged over time and now are distinguished by 2351 genetic variants in addition to the inversion itself. Which of these genetic variations drive disease risk and how? Why are some neurodegenerative diseases associated with the H1 haplotype while others are associated with the H2 haplotype? And to what extent does the inversion itself influence gene expression and disease susceptibility? To answer these questions, we will deploy our expertise in statistical genetics, machine learning, and functional genomics and dissect the molecular differences between the H1 and H2 haplotypes. First, we will analyze hundreds of publicly available single-nucleus multi-omic datasets to nominate genetic variants likely to impact gene expression and the brain cells in which they exert their effects (Aim 1). We will then pinpoint which of these prioritized variants are functional by engineering them into induced pluripotent stem cells and determining whether they impact gene expression once the cells are differentiated into brain cells (Aim 2). Finally, we will dissect the contribution of the inversion itself, providing, for the first time, an understanding of how the inversion has re-wired gene expression and cellular phenotypes (Aim 3). In all, our work will uncover how this enigmatic genetic locus impacts the cell types of the brain. This will provide key insights into how it is associated with such a diversity of diseases and nominate putative driver genes whose effects could be counteracted in the future with novel therapeutic interventions.

Up to $790K

Deadline: 2030-11-30

Health

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