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Article ; Online: eIF4E phosphorylation recruits β-catenin to mRNA cap and promotes Wnt pathway translation in dentate gyrus LTP maintenance.

Patil, Sudarshan / Chalkiadaki, Kleanthi / Mergiya, Tadiwos F / Krimbacher, Konstanze / Amorim, Inês S / Akerkar, Shreeram / Gkogkas, Christos G / Bramham, Clive R

iScience

2023 Volume 26, Issue 5, Page(s) 106649

Abstract: The mRNA cap-binding protein, eukaryotic initiation factor 4E (eIF4E), is crucial for translation and regulated by Ser209 phosphorylation. However, the biochemical and physiological role of eIF4E phosphorylation in translational control of long-term ... ...

Abstract	The mRNA cap-binding protein, eukaryotic initiation factor 4E (eIF4E), is crucial for translation and regulated by Ser209 phosphorylation. However, the biochemical and physiological role of eIF4E phosphorylation in translational control of long-term synaptic plasticity is unknown. We demonstrate that phospho-ablated
Language	English
Publishing date	2023-04-15
Publishing country	United States
Document type	Journal Article
ISSN	2589-0042
ISSN (online)	2589-0042
DOI	10.1016/j.isci.2023.106649
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Article: The Role of the Eukaryotic Translation Initiation Factor 4E (eIF4E) in Neuropsychiatric Disorders.

Amorim, Inês S / Lach, Gilliard / Gkogkas, Christos G

Frontiers in genetics

2018 Volume 9, Page(s) 561

Abstract: Protein synthesis in eukaryotic cells is a complex, multi-step and tightly regulated process. Translation initiation, the rate limiting step in protein synthesis, is dependent on the activity of eukaryotic translation Initiation Factor 4E (eIF4E). eIF4E ... ...

Abstract	Protein synthesis in eukaryotic cells is a complex, multi-step and tightly regulated process. Translation initiation, the rate limiting step in protein synthesis, is dependent on the activity of eukaryotic translation Initiation Factor 4E (eIF4E). eIF4E is the cap-binding protein which, in synergy with proteins such as the helicase eIF4A and the scaffolding protein eIF4G, binds to mRNA, allowing the recruitment of ribosomes and translation initiation. The function of eIF4E is tightly regulated in cells under normal physiological conditions and can be controlled by post-translational modifications, such as phosphorylation, and by the binding of inhibitory proteins, including eIF4E binding proteins (4E-BPs) and CYFIP1. Recent studies have highlighted the importance of eIF4E in normal or aberrant function of the nervous system. In this mini-review, we will highlight the role of eIF4E function and regulation in the pathophysiology of neurodevelopmental and neuropsychiatric disorders.
Language	English
Publishing date	2018-11-23
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2606823-0
ISSN	1664-8021
ISSN	1664-8021
DOI	10.3389/fgene.2018.00561
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Article ; Online: A seeding-based neuronal model of tau aggregation for use in drug discovery.

Amorim, Ines S / Challal, Sylvie / Cistarelli, Laetitia / Dorval, Thierry / Abjean, Laurene / Touzard, Manuelle / Arbez, Nicolas / François, Arnaud / Panayi, Fany / Jeggo, Ross / Cecon, Erika / Oishi, Atsuro / Dam, Julie / Jockers, Ralf / Machado, Patricia

PloS one

2023 Volume 18, Issue 4, Page(s) e0283941

Abstract: Intracellular accumulation of tau protein is a hallmark of Alzheimer's Disease and Progressive Supranuclear Palsy, as well as other neurodegenerative disorders collectively known as tauopathies. Despite our increasing understanding of the mechanisms ... ...

Abstract	Intracellular accumulation of tau protein is a hallmark of Alzheimer's Disease and Progressive Supranuclear Palsy, as well as other neurodegenerative disorders collectively known as tauopathies. Despite our increasing understanding of the mechanisms leading to the initiation and progression of tau pathology, the field still lacks appropriate disease models to facilitate drug discovery. Here, we established a novel and modulatable seeding-based neuronal model of full-length 4R tau accumulation using humanized mouse cortical neurons and seeds from P301S human tau transgenic animals. The model shows specific and consistent formation of intraneuronal insoluble full-length 4R tau inclusions, which are positive for known markers of tau pathology (AT8, PHF-1, MC-1), and creates seeding competent tau. The formation of new inclusions can be prevented by treatment with tau siRNA, providing a robust internal control for use in qualifying the assessment of potential therapeutic candidates aimed at reducing the intracellular pool of tau. In addition, the experimental set up and data analysis techniques used provide consistent results in larger-scale designs that required multiple rounds of independent experiments, making this is a versatile and valuable cellular model for fundamental and early pre-clinical research of tau-targeted therapies.
MeSH term(s)	Mice ; Animals ; Humans ; tau Proteins/genetics ; tau Proteins/metabolism ; Mice, Transgenic ; Brain/metabolism ; Tauopathies/metabolism ; Alzheimer Disease/pathology ; Neurons/metabolism ; Drug Discovery
Chemical Substances	tau Proteins
Language	English
Publishing date	2023-04-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0283941
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Article ; Online: Uncovering memory-related gene expression in contextual fear conditioning using ribosome profiling.

Simbriger, Konstanze / Amorim, Inês S / Lach, Gilliard / Chalkiadaki, Kleanthi / Kouloulia, Stella / Jafarnejad, Seyed Mehdi / Khoutorsky, Arkady / Gkogkas, Christos G

Progress in neurobiology

2020 Volume 197, Page(s) 101903

Abstract: Contextual fear conditioning (CFC) in rodents is the most widely used behavioural paradigm in neuroscience research to elucidate the neurobiological mechanisms underlying learning and memory. It is based on the pairing of an aversive unconditioned ... ...

Abstract	Contextual fear conditioning (CFC) in rodents is the most widely used behavioural paradigm in neuroscience research to elucidate the neurobiological mechanisms underlying learning and memory. It is based on the pairing of an aversive unconditioned stimulus (US; e.g. mild footshock) with a neutral conditioned stimulus (CS; e.g. context of the test chamber) in order to acquire associative long-term memory (LTM), which persists for days and even months. Using genome-wide analysis, several studies have generated lists of genes modulated in response to CFC in an attempt to identify the "memory genes", which orchestrate memory formation. Yet, most studies use naïve animals as a baseline for assessing gene-expression changes, while only few studies have examined the effect of the US alone, without pairing to context, using genome-wide analysis of gene-expression. Herein, using the ribosome profiling methodology, we show that in male mice an immediate shock, which does not lead to LTM formation, elicits pervasive translational and transcriptional changes in the expression of Immediate Early Genes (IEGs) in dorsal hippocampus (such as Fos and Arc), a fact which has been disregarded by the majority of CFC studies. By removing the effect of the immediate shock, we identify and validate a new set of genes, which are translationally and transcriptionally responsive to the association of context-to-footshock in CFC, and thus constitute salient "memory genes".
MeSH term(s)	Animals ; Conditioning, Classical ; Fear ; Gene Expression ; Hippocampus ; Male ; Mice ; Ribosomes
Language	English
Publishing date	2020-08-26
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	185535-9
ISSN	1873-5118 ; 0301-0082
ISSN (online)	1873-5118
ISSN	0301-0082
DOI	10.1016/j.pneurobio.2020.101903
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Article ; Online: Monitoring translation in synaptic fractions using a ribosome profiling strategy.

Simbriger, Konstanze / Amorim, Inês S / Chalkiadaki, Kleanthi / Lach, Gilliard / Jafarnejad, Seyed Mehdi / Khoutorsky, Arkady / Gkogkas, Christos G

Journal of neuroscience methods

2019 Volume 329, Page(s) 108456

Abstract: Background: The aim of this study was to develop a method to study genome-wide local translation in biochemically isolated synaptic fractions (synaptoneurosomes). This methodology is of particular interest for neurons, due to the cardinal role of local ... ...

Abstract	Background: The aim of this study was to develop a method to study genome-wide local translation in biochemically isolated synaptic fractions (synaptoneurosomes). This methodology is of particular interest for neurons, due to the cardinal role of local translational control in neuronal sub-compartments, such as dendrites, for plasticity, learning, memory, and for disorders of the nervous system. New method: We combined established methods for purifying synaptoneurosomes with translational profiling (ribosome profiling), a method that employs unbiased next generation sequencing to simultaneously assess transcription and translation in a single sample. Results: The two existing methods are compatible to use in combination and yield high quality sequencing data, which are specific to synaptic compartments. This new protocol provides an easy to implement workflow, which combines biochemical isolation of synaptoneurosomes of varying levels of purity (crude or Percoll gradient purified) with the use of a commercial kit to generate sequencing libraries. Comparison with existing methods: Compared to previous studies of the synaptic translatome, our method shows less contamination with non-neuronal cell types or non-synaptic compartments, increasing the specificity of the data obtained. Conclusions: Combining the isolation of functional synaptic units with ribosome profiling offers a powerful tool to study local translation in synaptic compartments both in health and disease.
MeSH term(s)	Animals ; Gene Expression Profiling/methods ; High-Throughput Nucleotide Sequencing ; Mice ; Mice, Inbred C57BL ; Prosencephalon ; Protein Biosynthesis/genetics ; Ribosomes/metabolism ; Synapses/metabolism ; Synaptosomes/metabolism
Language	English
Publishing date	2019-10-11
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	282721-9
ISSN	1872-678X ; 0165-0270
ISSN (online)	1872-678X
ISSN	0165-0270
DOI	10.1016/j.jneumeth.2019.108456
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Zs.A 1486: Show issues

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Article ; Online: Mnk1/2 kinases regulate memory and autism-related behaviours via Syngap1.

Brain : a journal of neurology

2022 Volume 146, Issue 5, Page(s) 2175–2190

Abstract: MAPK interacting protein kinases 1 and 2 (Mnk1/2) regulate a plethora of functions, presumably via phosphorylation of their best characterized substrate, eukaryotic translation initiation factor 4E (eIF4E) on Ser209. Here, we show that, whereas deletion ... ...

Abstract	MAPK interacting protein kinases 1 and 2 (Mnk1/2) regulate a plethora of functions, presumably via phosphorylation of their best characterized substrate, eukaryotic translation initiation factor 4E (eIF4E) on Ser209. Here, we show that, whereas deletion of Mnk1/2 (Mnk double knockout) impairs synaptic plasticity and memory in mice, ablation of phospho-eIF4E (Ser209) does not affect these processes, suggesting that Mnk1/2 possess additional downstream effectors in the brain. Translational profiling revealed only a small overlap between the Mnk1/2- and phospho-eIF4E(Ser209)-regulated translatome. We identified the synaptic Ras GTPase activating protein 1 (Syngap1), encoded by a syndromic autism gene, as a downstream target of Mnk1 because Syngap1 immunoprecipitated with Mnk1 and showed reduced phosphorylation (S788) in Mnk double knockout mice. Knockdown of Syngap1 reversed memory deficits in Mnk double knockout mice and pharmacological inhibition of Mnks rescued autism-related phenotypes in Syngap1+/- mice. Thus, Syngap1 is a downstream effector of Mnk1, and the Mnks-Syngap1 axis regulates memory formation and autism-related behaviours.
MeSH term(s)	Animals ; Mice ; Autistic Disorder ; Eukaryotic Initiation Factor-4E/genetics ; Mice, Knockout ; Phosphorylation ; ras GTPase-Activating Proteins/metabolism
Chemical Substances	Eukaryotic Initiation Factor-4E ; ras GTPase-Activating Proteins ; Syngap1 protein, mouse ; Mknk1 protein, mouse (EC 2.7.1.-) ; Mknk2 protein, mouse (EC 2.7.1.-)
Language	English
Publishing date	2022-10-31
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80072-7
ISSN	1460-2156 ; 0006-8950
ISSN (online)	1460-2156
ISSN	0006-8950
DOI	10.1093/brain/awac398
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Article: Translational profiling of dorsal root ganglia and spinal cord in a mouse model of neuropathic pain.

Uttam, Sonali / Wong, Calvin / Amorim, Inês S / Jafarnejad, Seyed Mehdi / Tansley, Shannon N / Yang, Jieyi / Prager-Khoutorsky, Masha / Mogil, Jeffrey S / Gkogkas, Christos G / Khoutorsky, Arkady

Neurobiology of pain (Cambridge, Mass.)

2018 Volume 4, Page(s) 35–44

Abstract: Acute pain serves as a protective mechanism, guiding the organism away from actual or potential tissue injury. In contrast, chronic pain is a debilitating condition without any obvious physiological function. The transition to, and the maintenance of ... ...

Abstract	Acute pain serves as a protective mechanism, guiding the organism away from actual or potential tissue injury. In contrast, chronic pain is a debilitating condition without any obvious physiological function. The transition to, and the maintenance of chronic pain require new gene expression to support biochemical and structural changes within the pain pathway. The regulation of gene expression at the level of mRNA translation has emerged as an important step in the control of protein expression in the cell. Recent studies show that signaling pathways upstream of mRNA translation, such as mTORC1 and ERK, are upregulated in chronic pain conditions, and their inhibition effectively alleviates pain in several animal models. Despite this progress, mRNAs whose translation is altered in chronic pain conditions remain largely unknown. Here, we performed genome-wide translational profiling of dorsal root ganglion (DRG) and spinal cord dorsal horn tissues in a mouse model of neuropathic pain, spared nerve injury (SNI), using the ribosome profiling technique. We identified distinct subsets of mRNAs that are differentially translated in response to nerve injury in both tissues. We discovered key converging upstream regulators and pathways linked to mRNA translational control and neuropathic pain. Our data are crucial for the understanding of mechanisms by which mRNA translation promotes persistent hypersensitivity after nerve injury.
Keywords	covid19
Language	English
Publishing date	2018-04-18
Publishing country	United States
Document type	Journal Article
ISSN	2452-073X
ISSN	2452-073X
DOI	10.1016/j.ynpai.2018.04.001
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Article ; Online: Loss of eIF4E Phosphorylation Engenders Depression-like Behaviors via Selective mRNA Translation.

Amorim, Inês S / Kedia, Sonal / Kouloulia, Stella / Simbriger, Konstanze / Gantois, Ilse / Jafarnejad, Seyed Mehdi / Li, Yupeng / Kampaite, Agniete / Pooters, Tine / Romanò, Nicola / Gkogkas, Christos G

The Journal of neuroscience : the official journal of the Society for Neuroscience

2018 Volume 38, Issue 8, Page(s) 2118–2133

Abstract: The MAPK/ERK (mitogen-activated protein kinases/extracellular signal-regulated kinase) pathway is a cardinal regulator of synaptic plasticity, learning, and memory in the hippocampus. One of major endpoints of this signaling cascade is the 5' mRNA cap ... ...

Abstract	The MAPK/ERK (mitogen-activated protein kinases/extracellular signal-regulated kinase) pathway is a cardinal regulator of synaptic plasticity, learning, and memory in the hippocampus. One of major endpoints of this signaling cascade is the 5' mRNA cap binding protein eIF4E (eukaryotic Initiation Factor 4E), which is phosphorylated on Ser 209 by MNK (MAPK-interacting protein kinases) and controls mRNA translation. The precise role of phospho-eIF4E in the brain is yet to be determined. Herein, we demonstrate that ablation of eIF4E phosphorylation in male mice (
MeSH term(s)	Animals ; Depression/metabolism ; Depression/physiopathology ; Eukaryotic Initiation Factor-4E/metabolism ; Inflammation/metabolism ; Inflammation/physiopathology ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Transgenic ; Phosphorylation ; Protein Biosynthesis/physiology
Chemical Substances	Eukaryotic Initiation Factor-4E ; eIF4E protein, mouse
Language	English
Publishing date	2018-01-24
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.2673-17.2018
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Article ; Online: Molecular neuropathology of the synapse in sheep with CLN5 Batten disease.

Amorim, Inês S / Mitchell, Nadia L / Palmer, David N / Sawiak, Stephen J / Mason, Roger / Wishart, Thomas M / Gillingwater, Thomas H

Brain and behavior

2015 Volume 5, Issue 11, Page(s) e00401

Abstract: Aims: Synapses represent a major pathological target across a broad range of neurodegenerative conditions. Recent studies addressing molecular mechanisms regulating synaptic vulnerability and degeneration have relied heavily on invertebrate and mouse ... ...

Abstract	Aims: Synapses represent a major pathological target across a broad range of neurodegenerative conditions. Recent studies addressing molecular mechanisms regulating synaptic vulnerability and degeneration have relied heavily on invertebrate and mouse models. Whether similar molecular neuropathological changes underpin synaptic breakdown in large animal models and in human patients with neurodegenerative disease remains unclear. We therefore investigated whether molecular regulators of synaptic pathophysiology, previously identified in Drosophila and mouse models, are similarly present and modified in the brain of sheep with CLN5 Batten disease. Methods: Gross neuropathological analysis of CLN5 Batten disease sheep and controls was used alongside postmortem MRI imaging to identify affected brain regions. Synaptosome preparations were then generated and quantitative fluorescent Western blotting used to determine and compare levels of synaptic proteins. Results: The cortex was particularly affected by regional neurodegeneration and synaptic loss in CLN5 sheep, whilst the cerebellum was relatively spared. Quantitative assessment of the protein content of synaptosome preparations revealed significant changes in levels of seven out of eight synaptic neurodegeneration proteins investigated in the motor cortex, but not cerebellum, of CLN5 sheep (α-synuclein, CSP-α, neurofascin, ROCK2, calretinin, SIRT2, and UBR4). Conclusions: Synaptic pathology is a robust correlate of region-specific neurodegeneration in the brain of CLN5 sheep, driven by molecular pathways similar to those reported in Drosophila and rodent models. Thus, large animal models, such as sheep, represent ideal translational systems to develop and test therapeutics aimed at delaying or halting synaptic pathology for a range of human neurodegenerative conditions.
MeSH term(s)	Animals ; Cerebellum/pathology ; Cerebral Cortex/pathology ; Disease Models, Animal ; Female ; Male ; Neuronal Ceroid-Lipofuscinoses/pathology ; Sheep ; Sheep Diseases/pathology ; Synapses/pathology
Language	English
Publishing date	2015-10-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	2623587-0
ISSN	2162-3279 ; 2162-3279
ISSN (online)	2162-3279
ISSN	2162-3279
DOI	10.1002/brb3.401
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Article ; Online: Raptor-Mediated Proteasomal Degradation of Deamidated 4E-BP2 Regulates Postnatal Neuronal Translation and NF-κB Activity.

Kouloulia, Stella / Hallin, Erik I / Simbriger, Konstanze / Amorim, Inês S / Lach, Gilliard / Amvrosiadis, Theoklitos / Chalkiadaki, Kleanthi / Kampaite, Agniete / Truong, Vinh Tai / Hooshmandi, Mehdi / Jafarnejad, Seyed Mehdi / Skehel, Paul / Kursula, Petri / Khoutorsky, Arkady / Gkogkas, Christos G

Cell reports

2019 Volume 29, Issue 11, Page(s) 3620–3635.e7

Abstract: The translation initiation repressor 4E-BP2 is deamidated in the brain on asparagines N99/N102 during early postnatal brain development. This post-translational modification enhances 4E-BP2 association with Raptor, a central component of mTORC1 and ... ...

Abstract	The translation initiation repressor 4E-BP2 is deamidated in the brain on asparagines N99/N102 during early postnatal brain development. This post-translational modification enhances 4E-BP2 association with Raptor, a central component of mTORC1 and alters the kinetics of excitatory synaptic transmission. We show that 4E-BP2 deamidation is neuron specific, occurs in the human brain, and changes 4E-BP2 subcellular localization, but not its disordered structure state. We demonstrate that deamidated 4E-BP2 is ubiquitinated more and degrades faster than the unmodified protein. We find that enhanced deamidated 4E-BP2 degradation is dependent on Raptor binding, concomitant with increased association with a Raptor-CUL4B E3 ubiquitin ligase complex. Deamidated 4E-BP2 stability is promoted by inhibiting mTORC1 or glutamate receptors. We further demonstrate that deamidated 4E-BP2 regulates the translation of a distinct pool of mRNAs linked to cerebral development, mitochondria, and NF-κB activity, and thus may be crucial for postnatal brain development in neurodevelopmental disorders, such as ASD.
MeSH term(s)	Animals ; Brain/cytology ; Brain/metabolism ; Cells, Cultured ; Cullin Proteins/metabolism ; Eukaryotic Initiation Factors/metabolism ; Female ; HEK293 Cells ; Humans ; Male ; Mice ; Mice, Inbred C57BL ; NF-kappa B/metabolism ; Neurons/metabolism ; Proteasome Endopeptidase Complex/metabolism ; Protein Binding ; Proteolysis ; Regulatory-Associated Protein of mTOR/metabolism
Chemical Substances	Cul4B protein, mouse ; Cullin Proteins ; Eif4ebp2 protein, mouse ; Eukaryotic Initiation Factors ; NF-kappa B ; Regulatory-Associated Protein of mTOR ; Rptor protein, mouse ; Proteasome Endopeptidase Complex (EC 3.4.25.1)
Language	English
Publishing date	2019-12-10
Publishing country	United States
Document type	Journal Article
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2019.11.023
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