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  1. Article ; Online: Spatiotemporally resolved protein synthesis as a molecular framework for memory consolidation.

    Shrestha, Prerana / Klann, Eric

    Trends in neurosciences

    2022  Volume 45, Issue 4, Page(s) 297–311

    Abstract: De novo protein synthesis is required for long-term memory consolidation. Dynamic regulation of protein synthesis occurs via a complex interplay of translation factors and modulators. Many components of the protein synthesis machinery have been targeted ... ...

    Abstract De novo protein synthesis is required for long-term memory consolidation. Dynamic regulation of protein synthesis occurs via a complex interplay of translation factors and modulators. Many components of the protein synthesis machinery have been targeted either pharmacologically or genetically to establish its requirement for memory. The combination of ligand/light-gating and genetic strategies, that is, chemogenetics and optogenetics, has begun to reveal the spatiotemporal resolution of protein synthesis in specific cell types during memory consolidation. This review summarizes current knowledge of the macroscopic and microscopic neural substrates for protein synthesis in memory consolidation. In addition, we highlight future directions for determining the localization and timing of de novo protein synthesis for memory consolidation with tools that permit unprecedented spatiotemporal precision.
    MeSH term(s) Humans ; Memory Consolidation/physiology ; Memory, Long-Term ; Protein Biosynthesis
    Language English
    Publishing date 2022-02-17
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
    ZDB-ID 282488-7
    ISSN 1878-108X ; 0378-5912 ; 0166-2236
    ISSN (online) 1878-108X
    ISSN 0378-5912 ; 0166-2236
    DOI 10.1016/j.tins.2022.01.004
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  2. Article ; Online: Mutational Analysis of

    Shrestha, Prerana / Razvi, Ali / Fung, Brittany L / Eichinger, Steven J / Visick, Karen L

    Journal of bacteriology

    2022  Volume 204, Issue 7, Page(s) e0010922

    Abstract: The symbiont Vibrio fischeri uses motility to colonize its host. In numerous bacterial species, motility is negatively controlled by cyclic-di-GMP (c-di-GMP), which is produced by diguanylate cyclases (DGCs) with GGDEF domains and degraded by ... ...

    Abstract The symbiont Vibrio fischeri uses motility to colonize its host. In numerous bacterial species, motility is negatively controlled by cyclic-di-GMP (c-di-GMP), which is produced by diguanylate cyclases (DGCs) with GGDEF domains and degraded by phosphodiesterases with either EAL or HD-GYP domains. To begin to decode the functions of the 50 Vibrio fischeri genes with GGDEF, EAL, and/or HD-GYP domains, we deleted each gene and assessed each mutant's migration through tryptone broth salt (TBS) soft agar medium containing or lacking magnesium (Mg) and calcium (Ca), which are known to influence V. fischeri motility. We identified 6, 13, and 16 mutants with altered migration in TBS-Mg, TBS, and TBS-Ca soft agar, respectively, a result that underscores the importance of medium conditions in assessing gene function. A biosensor-based assay revealed that Mg and Ca affected c-di-GMP levels negatively and positively, respectively; the severe decrease in c-di-GMP caused by Mg addition correlates with its strong positive impact on bacterial migration. A mutant defective for
    MeSH term(s) Agar ; Aliivibrio fischeri/genetics ; Aliivibrio fischeri/metabolism ; Bacterial Proteins/genetics ; Bacterial Proteins/metabolism ; Biofilms ; Calcium/metabolism ; Cyclic GMP/analogs & derivatives ; Cyclic GMP/metabolism ; Escherichia coli Proteins/metabolism ; Gene Expression Regulation, Bacterial ; Magnesium/metabolism ; Vibrio cholerae/metabolism
    Chemical Substances Bacterial Proteins ; Escherichia coli Proteins ; bis(3',5')-cyclic diguanylic acid (61093-23-0) ; Agar (9002-18-0) ; Cyclic GMP (H2D2X058MU) ; Magnesium (I38ZP9992A) ; Calcium (SY7Q814VUP)
    Language English
    Publishing date 2022-06-27
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 2968-3
    ISSN 1098-5530 ; 0021-9193
    ISSN (online) 1098-5530
    ISSN 0021-9193
    DOI 10.1128/jb.00109-22
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  3. Article: Opto4E-BP, an optogenetic tool for inducible, reversible, and cell type-specific inhibition of translation initiation.

    Alapin, Jessica M / Mohamed, Muhaned S / Shrestha, Prerana / Khaled, Houda G / Vorabyeva, Anna G / Bowling, Heather L / Oliveira, Mauricio M / Klann, Eric

    bioRxiv : the preprint server for biology

    2023  

    Abstract: The protein kinase mechanistic target of rapamycin complex 1 (mTORC1) is one of the primary triggers for initiating cap-dependent translation. Amongst its functions, mTORC1 phosphorylates eIF4E-binding proteins (4E-BPs), which prevents them from binding ... ...

    Abstract The protein kinase mechanistic target of rapamycin complex 1 (mTORC1) is one of the primary triggers for initiating cap-dependent translation. Amongst its functions, mTORC1 phosphorylates eIF4E-binding proteins (4E-BPs), which prevents them from binding to eIF4E and thereby enables translation initiation. mTORC1 signaling is required for multiple forms of protein synthesis-dependent synaptic plasticity and various forms of long-term memory (LTM), including associative threat memory. However, the approaches used thus far to target mTORC1 and its effectors, such as pharmacological inhibitors or genetic knockouts, lack fine spatial and temporal control. The development of a conditional and inducible eIF4E knockdown mouse line partially solved the issue of spatial control, but still lacked optimal temporal control to study memory consolidation. Here, we have designed a novel optogenetic tool (Opto4E-BP) for cell type-specific, light-dependent regulation of eIF4E in the brain. We show that light-activation of Opto4E-BP decreases protein synthesis in HEK cells and primary mouse neurons.
    Language English
    Publishing date 2023-08-31
    Publishing country United States
    Document type Preprint
    DOI 10.1101/2023.08.30.554643
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  4. Article ; Online: Alzheimer's disease: Lost memories found.

    Shrestha, Prerana / Klann, Eric

    Nature

    2016  Volume 531, Issue 7595, Page(s) 450–451

    MeSH term(s) Alzheimer Disease/pathology ; Alzheimer Disease/physiopathology ; Animals ; Dentate Gyrus/cytology ; Dentate Gyrus/physiology ; Disease Models, Animal ; Humans ; Male ; Memory, Long-Term/physiology
    Language English
    Publishing date 2016-03-24
    Publishing country England
    Document type Comment ; Journal Article
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/nature17312
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  5. Article: The modulation of emotional and social behaviors by oxytocin signaling in limbic network.

    Triana-Del Rio, Rodrigo / Ranade, Sayali / Guardado, Jahel / LeDoux, Joseph / Klann, Eric / Shrestha, Prerana

    Frontiers in molecular neuroscience

    2022  Volume 15, Page(s) 1002846

    Abstract: Neuropeptides can exert volume modulation in neuronal networks, which account for a well-calibrated and fine-tuned regulation that depends on the sensory and behavioral contexts. For example, oxytocin (OT) and oxytocin receptor (OTR) trigger a signaling ... ...

    Abstract Neuropeptides can exert volume modulation in neuronal networks, which account for a well-calibrated and fine-tuned regulation that depends on the sensory and behavioral contexts. For example, oxytocin (OT) and oxytocin receptor (OTR) trigger a signaling pattern encompassing intracellular cascades, synaptic plasticity, gene expression, and network regulation, that together function to increase the signal-to-noise ratio for sensory-dependent stress/threat and social responses. Activation of OTRs in emotional circuits within the limbic forebrain is necessary to acquire stress/threat responses. When emotional memories are retrieved, OTR-expressing cells act as gatekeepers of the threat response choice/discrimination. OT signaling has also been implicated in modulating social-exposure elicited responses in the neural circuits within the limbic forebrain. In this review, we describe the cellular and molecular mechanisms that underlie the neuromodulation by OT, and how OT signaling in specific neural circuits and cell populations mediate stress/threat and social behaviors. OT and downstream signaling cascades are heavily implicated in neuropsychiatric disorders characterized by emotional and social dysregulation. Thus, a mechanistic understanding of downstream cellular effects of OT in relevant cell types and neural circuits can help design effective intervention techniques for a variety of neuropsychiatric disorders.
    Language English
    Publishing date 2022-11-17
    Publishing country Switzerland
    Document type Journal Article ; Review
    ZDB-ID 2452967-9
    ISSN 1662-5099
    ISSN 1662-5099
    DOI 10.3389/fnmol.2022.1002846
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  6. Article ; Online: An AAV-CRISPR/Cas9 strategy for gene editing across divergent rodent species: Targeting neural oxytocin receptors as a proof of concept.

    Boender, Arjen J / Boon, Marina / Albers, H Elliott / Eck, Samantha R / Fricker, Brandon A / Kelly, Aubrey M / LeDoux, Joseph E / Motta, Simone C / Shrestha, Prerana / Taylor, Jack H / Trainor, Brian C / Triana-Del Rio, Rodrigo / Young, Larry J

    Science advances

    2023  Volume 9, Issue 22, Page(s) eadf4950

    Abstract: A major issue in neuroscience is the poor translatability of research results from preclinical studies in animals to clinical outcomes. Comparative neuroscience can overcome this barrier by studying multiple species to differentiate between species- ... ...

    Abstract A major issue in neuroscience is the poor translatability of research results from preclinical studies in animals to clinical outcomes. Comparative neuroscience can overcome this barrier by studying multiple species to differentiate between species-specific and general mechanisms of neural circuit functioning. Targeted manipulation of neural circuits often depends on genetic dissection, and use of this technique has been restricted to only a few model species, limiting its application in comparative research. However, ongoing advances in genomics make genetic dissection attainable in a growing number of species. To demonstrate the potential of comparative gene editing approaches, we developed a viral-mediated CRISPR/Cas9 strategy that is predicted to target the oxytocin receptor (
    MeSH term(s) Animals ; Gene Editing/methods ; CRISPR-Cas Systems ; Receptors, Oxytocin/genetics ; Oxytocin/genetics
    Chemical Substances Receptors, Oxytocin ; Oxytocin (50-56-6)
    Language English
    Publishing date 2023-05-31
    Publishing country United States
    Document type Journal Article
    ZDB-ID 2810933-8
    ISSN 2375-2548 ; 2375-2548
    ISSN (online) 2375-2548
    ISSN 2375-2548
    DOI 10.1126/sciadv.adf4950
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  7. Article ; Online: Layer 2/3 pyramidal cells in the medial prefrontal cortex moderate stress induced depressive behaviors.

    Shrestha, Prerana / Mousa, Awni / Heintz, Nathaniel

    eLife

    2015  Volume 4

    Abstract: Major depressive disorder (MDD) is a prevalent illness that can be precipitated by acute or chronic stress. Studies of patients with Wolfram syndrome and carriers have identified Wfs1 mutations as causative for MDD. The medial prefrontal cortex (mPFC) is ...

    Abstract Major depressive disorder (MDD) is a prevalent illness that can be precipitated by acute or chronic stress. Studies of patients with Wolfram syndrome and carriers have identified Wfs1 mutations as causative for MDD. The medial prefrontal cortex (mPFC) is known to be involved in depression and behavioral resilience, although the cell types and circuits in the mPFC that moderate depressive behaviors in response to stress have not been determined. Here, we report that deletion of Wfs1 from layer 2/3 pyramidal cells impairs the ability of the mPFC to suppress stress-induced depressive behaviors, and results in hyperactivation of the hypothalamic-pituitary-adrenal axis and altered accumulation of important growth and neurotrophic factors. Our data identify superficial layer 2/3 pyramidal cells as critical for moderation of stress in the context of depressive behaviors and suggest that dysfunction in these cells may contribute to the clinical relationship between stress and depression.
    MeSH term(s) Animals ; Depression ; Female ; Gene Knockout Techniques ; Male ; Membrane Proteins/deficiency ; Mice ; Mice, Knockout ; Prefrontal Cortex/physiology ; Pyramidal Cells/physiology ; Stress, Psychological
    Chemical Substances Membrane Proteins ; wolframin protein
    Language English
    Publishing date 2015-09-15
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 2687154-3
    ISSN 2050-084X ; 2050-084X
    ISSN (online) 2050-084X
    ISSN 2050-084X
    DOI 10.7554/eLife.08752
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  8. Article ; Online: Cell-type-specific drug-inducible protein synthesis inhibition demonstrates that memory consolidation requires rapid neuronal translation.

    Shrestha, Prerana / Ayata, Pinar / Herrero-Vidal, Pedro / Longo, Francesco / Gastone, Alexandra / LeDoux, Joseph E / Heintz, Nathaniel / Klann, Eric

    Nature neuroscience

    2020  Volume 23, Issue 2, Page(s) 281–292

    Abstract: New protein synthesis is known to be required for the consolidation of memories, yet existing methods of blocking translation lack spatiotemporal precision and cell-type specificity, preventing investigation of cell-specific contributions of protein ... ...

    Abstract New protein synthesis is known to be required for the consolidation of memories, yet existing methods of blocking translation lack spatiotemporal precision and cell-type specificity, preventing investigation of cell-specific contributions of protein synthesis. Here we developed a combined knock-in mouse and chemogenetic approach for cell-type-specific drug-inducible protein synthesis inhibition that enables rapid and reversible phosphorylation of eukaryotic initiation factor 2α, leading to inhibition of general translation by 50% in vivo. We use cell-type-specific drug-inducible protein synthesis inhibition to show that targeted protein synthesis inhibition pan-neuronally and in excitatory neurons in the lateral amygdala (LA) impaired long-term memory. This could be recovered with artificial chemogenetic activation of LA neurons, although at the cost of stimulus generalization. Conversely, genetically reducing phosphorylation of eukaryotic initiation factor 2α in excitatory neurons in the LA enhanced memory strength but reduced memory fidelity and behavioral flexibility. Our findings provide evidence for a cell-specific translation program during consolidation of threat memories.
    MeSH term(s) Amygdala/physiology ; Animals ; Eukaryotic Initiation Factor-2/metabolism ; Memory Consolidation/physiology ; Mice ; Neurons/physiology ; Protein Biosynthesis/physiology
    Chemical Substances Eukaryotic Initiation Factor-2
    Language English
    Publishing date 2020-01-20
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 1420596-8
    ISSN 1546-1726 ; 1097-6256
    ISSN (online) 1546-1726
    ISSN 1097-6256
    DOI 10.1038/s41593-019-0568-z
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  9. Article ; Online: Amygdala inhibitory neurons as loci for translation in emotional memories.

    Shrestha, Prerana / Shan, Zhe / Mamcarz, Maggie / Ruiz, Karen San Agustin / Zerihoun, Adam T / Juan, Chien-Yu / Herrero-Vidal, Pedro M / Pelletier, Jerry / Heintz, Nathaniel / Klann, Eric

    Nature

    2020  Volume 586, Issue 7829, Page(s) 407–411

    Abstract: To survive in a dynamic environment, animals need to identify and appropriately respond to stimuli that signal ... ...

    Abstract To survive in a dynamic environment, animals need to identify and appropriately respond to stimuli that signal danger
    MeSH term(s) Amygdala/cytology ; Amygdala/physiology ; Animals ; Conditioning, Psychological ; Cues ; Emotions ; Eukaryotic Initiation Factor-2/metabolism ; Eukaryotic Initiation Factor-4E/metabolism ; Fear/physiology ; Female ; Heterotrimeric GTP-Binding Proteins/metabolism ; Male ; Memory/physiology ; Mice ; Neural Inhibition ; Neurons/physiology ; Protein Biosynthesis ; RNA Caps/genetics ; RNA Caps/metabolism ; Signal Transduction ; Somatostatin/metabolism
    Chemical Substances Eukaryotic Initiation Factor-2 ; Eukaryotic Initiation Factor-4E ; RNA Caps ; Somatostatin (51110-01-1) ; Heterotrimeric GTP-Binding Proteins (EC 3.6.5.1)
    Language English
    Publishing date 2020-10-07
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 120714-3
    ISSN 1476-4687 ; 0028-0836
    ISSN (online) 1476-4687
    ISSN 0028-0836
    DOI 10.1038/s41586-020-2793-8
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  10. Article ; Online: Application of a translational profiling approach for the comparative analysis of CNS cell types.

    Doyle, Joseph P / Dougherty, Joseph D / Heiman, Myriam / Schmidt, Eric F / Stevens, Tanya R / Ma, Guojun / Bupp, Sujata / Shrestha, Prerana / Shah, Rajiv D / Doughty, Martin L / Gong, Shiaoching / Greengard, Paul / Heintz, Nathaniel

    Cell

    2008  Volume 135, Issue 4, Page(s) 749–762

    Abstract: Comparative analysis can provide important insights into complex biological systems. As demonstrated in the accompanying paper, translating ribosome affinity purification (TRAP) permits comprehensive studies of translated mRNAs in genetically defined ... ...

    Abstract Comparative analysis can provide important insights into complex biological systems. As demonstrated in the accompanying paper, translating ribosome affinity purification (TRAP) permits comprehensive studies of translated mRNAs in genetically defined cell populations after physiological perturbations. To establish the generality of this approach, we present translational profiles for 24 CNS cell populations and identify known cell-specific and enriched transcripts for each population. We report thousands of cell-specific mRNAs that were not detected in whole-tissue microarray studies and provide examples that demonstrate the benefits deriving from comparative analysis. To provide a foundation for further biological and in silico studies, we provide a resource of 16 transgenic mouse lines, their corresponding anatomic characterization, and translational profiles for cell types from a variety of central nervous system structures. This resource will enable a wide spectrum of molecular and mechanistic studies of both well-known and previously uncharacterized neural cell populations.
    MeSH term(s) Animals ; Brain/metabolism ; Central Nervous System/metabolism ; Chromosomes, Artificial, Bacterial/metabolism ; Genetic Techniques ; Green Fluorescent Proteins/metabolism ; Immunohistochemistry/methods ; Mice ; Mice, Transgenic ; Models, Biological ; Neurons/metabolism ; Oligonucleotide Array Sequence Analysis ; Protein Biosynthesis ; Reverse Transcriptase Polymerase Chain Reaction ; Ribosomes/metabolism
    Chemical Substances Green Fluorescent Proteins (147336-22-9)
    Language English
    Publishing date 2008-10-25
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 187009-9
    ISSN 1097-4172 ; 0092-8674
    ISSN (online) 1097-4172
    ISSN 0092-8674
    DOI 10.1016/j.cell.2008.10.029
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