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Article ; Online: Tripartite synaptomics: Cell-surface proximity labeling in vivo.

Takano, Tetsuya / Soderling, Scott H

2021 Volume 173, Page(s) 14–21

Abstract: The astrocyte is a central glial cell and plays a critical role in the architecture and activity of neuronal circuits and brain functions through forming a tripartite synapse with neurons. Emerging evidence suggests that dysfunction of tripartite ... ...

Abstract	The astrocyte is a central glial cell and plays a critical role in the architecture and activity of neuronal circuits and brain functions through forming a tripartite synapse with neurons. Emerging evidence suggests that dysfunction of tripartite synaptic connections contributes to a variety of psychiatric and neurodevelopmental disorders. Furthermore, recent advancements with transcriptome profiling, cell biological and physiological approaches have provided new insights into the molecular mechanisms into how astrocytes control synaptogenesis in the brain. In addition to these findings, we have recently developed in vivo cell-surface proximity-dependent biotinylation (BioID) approaches, TurboID-surface and Split-TurboID, to comprehensively understand the molecular composition between astrocytes and neuronal synapses. These proteomic approaches have discovered a novel molecular framework for understanding the tripartite synaptic cleft that arbitrates neuronal circuit formation and function. Here, this short review highlights novel in vivo cell-surface BioID approaches and recent advances in this rapidly evolving field, emphasizing how astrocytes regulate excitatory and inhibitory synapse formation in vitro and in vivo.
MeSH term(s)	Astrocytes ; Neurogenesis ; Neurons ; Proteomics ; Synapses
Language	English
Publishing date	2021-05-19
Publishing country	Ireland
Document type	Journal Article ; Review
ZDB-ID	605842-5
ISSN	1872-8111 ; 0168-0102 ; 0921-8696
ISSN (online)	1872-8111
ISSN	0168-0102 ; 0921-8696
DOI	10.1016/j.neures.2021.05.002
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Article: Identification of new ciliary signaling pathways in the brain and insights into neurological disorders.

Loukil, Abdelhalim / Ebright, Emma / Uezu, Akiyoshi / Gao, Yudong / Soderling, Scott H / Goetz, Sarah C

bioRxiv : the preprint server for biology

2023

Abstract: Primary cilia are conserved sensory hubs essential for signaling transduction and embryonic development. Ciliary dysfunction causes a variety of developmental syndromes with neurological features and cognitive impairment, whose basis mostly remains ... ...

Abstract	Primary cilia are conserved sensory hubs essential for signaling transduction and embryonic development. Ciliary dysfunction causes a variety of developmental syndromes with neurological features and cognitive impairment, whose basis mostly remains unknown. Despite connections to neural function, the primary cilium remains an overlooked organelle in the brain. Most neurons have a primary cilium; however, it is still unclear how this organelle modulates brain architecture and function, given the lack of any systemic dissection of neuronal ciliary signaling. Here, we present the first in vivo glance at the molecular composition of cilia in the mouse brain. We have adapted
Language	English
Publishing date	2023-12-21
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.12.20.572700
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Article ; Online: A Ventromedial Prefrontal-to-Lateral Entorhinal Cortex Pathway Modulates the Gain of Behavioral Responding During Threat.

Hisey, Erin / Purkey, Alicia / Gao, Yudong / Hossain, Kazi / Soderling, Scott H / Ressler, Kerry J

Biological psychiatry

2023 Volume 94, Issue 3, Page(s) 239–248

Abstract: Background: The ability to correctly associate cues and contexts with threat is critical for survival, and the inability to do so can result in threat-related disorders such as posttraumatic stress disorder. The prefrontal cortex (PFC) and hippocampus ... ...

Abstract	Background: The ability to correctly associate cues and contexts with threat is critical for survival, and the inability to do so can result in threat-related disorders such as posttraumatic stress disorder. The prefrontal cortex (PFC) and hippocampus are well known to play critical roles in cued and contextual threat memory processing. However, the circuits that mediate prefrontal-hippocampal modulation of context discrimination during cued threat processing are less understood. Here, we demonstrate the role of a previously unexplored projection from the ventromedial region of PFC (vmPFC) to the lateral entorhinal cortex (LEC) in modulating the gain of behavior in response to contextual information during threat retrieval and encoding. Methods: We used optogenetics followed by in vivo calcium imaging in male C57/B6J mice to manipulate and monitor vmPFC-LEC activity in response to threat-associated cues in different contexts. We then investigated the inputs to, and outputs from, vmPFC-LEC cells using Rabies tracing and channelrhodopsin-assisted electrophysiology. Results: vmPFC-LEC cells flexibly and bidirectionally shaped behavior during threat expression, shaping sensitivity to contextual information to increase or decrease the gain of behavioral output in response to a threatening or neutral context, respectively. Conclusions: Glutamatergic vmPFC-LEC cells are key players in behavioral gain control in response to contextual information during threat processing and may provide a future target for intervention in threat-based disorders.
MeSH term(s)	Animals ; Male ; Mice ; Behavior/physiology ; Calcium Signaling ; Channelrhodopsins/metabolism ; Cues ; Fear ; Glutamic Acid/metabolism ; Mice, Inbred C57BL ; Neural Pathways ; Olfactory Cortex/cytology ; Olfactory Cortex/physiology ; Optogenetics ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology ; Stress Disorders, Post-Traumatic/physiopathology ; Patch-Clamp Techniques
Chemical Substances	Channelrhodopsins ; Glutamic Acid (3KX376GY7L)
Language	English
Publishing date	2023-01-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209434-4
ISSN	1873-2402 ; 0006-3223
ISSN (online)	1873-2402
ISSN	0006-3223
DOI	10.1016/j.biopsych.2023.01.009
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Article: Presynaptic Rac1 in the hippocampus selectively regulates working memory.

Kim, Jaebin / Bustamante, Edwin / Sotonyi, Peter / Maxwell, Nicholas D / Parameswaran, Pooja / Kent, Julie K / Wetsel, William C / Soderblom, Erik J / Rácz, Bence / Soderling, Scott H

bioRxiv : the preprint server for biology

2024

Abstract: One of the most extensively studied members of the Ras superfamily of small GTPases, Rac1 is an intracellular signal transducer that remodels actin and phosphorylation signaling networks. Previous studies have shown that Rac1-mediated signaling is ... ...

Abstract	One of the most extensively studied members of the Ras superfamily of small GTPases, Rac1 is an intracellular signal transducer that remodels actin and phosphorylation signaling networks. Previous studies have shown that Rac1-mediated signaling is associated with hippocampal-dependent working memory and longer-term forms of learning and memory and that Rac1 can modulate forms of both pre- and postsynaptic plasticity. How these different cognitive functions and forms of plasticity mediated by Rac1 are linked, however, is unclear. Here, we show that spatial working memory is selectively impaired following the expression of a genetically encoded Rac1-inhibitor at presynaptic terminals, while longer-term cognitive processes are affected by Rac1 inhibition at postsynaptic sites. To investigate the regulatory mechanisms of this presynaptic process, we leveraged new advances in mass spectrometry to identify the proteomic and post-translational landscape of presynaptic Rac1 signaling. We identified serine/threonine kinases and phosphorylated cytoskeletal signaling and synaptic vesicle proteins enriched with active Rac1. The phosphorylated sites in these proteins are at positions likely to have regulatory effects on synaptic vesicles. Consistent with this, we also report changes in the distribution and morphology of synaptic vesicles and in postsynaptic ultrastructure following presynaptic Rac1 inhibition. Overall, this study reveals a previously unrecognized presynaptic role of Rac1 signaling in cognitive processes and provides insights into its potential regulatory mechanisms.
Language	English
Publishing date	2024-03-18
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.03.18.585488
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Article ; Online: Actin Out: Regulation of the Synaptic Cytoskeleton.

Spence, Erin F / Soderling, Scott H

The Journal of biological chemistry

2015 Volume 290, Issue 48, Page(s) 28613–28622

Abstract: The small size of dendritic spines belies the elaborate role they play in excitatory synaptic transmission and ultimately complex behaviors. The cytoskeletal architecture of the spine is predominately composed of actin filaments. These filaments, which ... ...

Abstract	The small size of dendritic spines belies the elaborate role they play in excitatory synaptic transmission and ultimately complex behaviors. The cytoskeletal architecture of the spine is predominately composed of actin filaments. These filaments, which at first glance might appear simple, are also surprisingly complex. They dynamically assemble into different structures and serve as a platform for orchestrating the elaborate responses of the spine during spinogenesis and experience-dependent plasticity. Multiple mutations associated with human neurodevelopmental and psychiatric disorders involve genes that encode regulators of the synaptic cytoskeleton. A major, unresolved question is how the disruption of specific actin filament structures leads to the onset and progression of complex synaptic and behavioral phenotypes. This review will cover established and emerging mechanisms of actin cytoskeletal remodeling and how this influences specific aspects of spine biology that are implicated in disease.
MeSH term(s)	Actins/metabolism ; Animals ; Humans ; Spinal Diseases/metabolism ; Spinal Diseases/pathology ; Spine/metabolism ; Spine/pathology ; Stress Fibers/metabolism ; Stress Fibers/pathology ; Synapses/metabolism ; Synapses/pathology
Chemical Substances	Actins
Language	English
Publishing date	2015-10-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2997-x
ISSN	1083-351X ; 0021-9258
ISSN (online)	1083-351X
ISSN	0021-9258
DOI	10.1074/jbc.R115.655118
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Article ; Online: Grab your partner with both hands: cytoskeletal remodeling by Arp2/3 signaling.

Soderling, Scott H

Science signaling

2009 Volume 2, Issue 55, Page(s) pe5

Abstract: The seemingly simple structure of the actin filament belies the elaborate signaling pathways that regulate its assembly and disassembly in eukaryotic cells. In retrospect, this signaling complexity should not be surprising. Actin regulates many dynamic ... ...

Abstract	The seemingly simple structure of the actin filament belies the elaborate signaling pathways that regulate its assembly and disassembly in eukaryotic cells. In retrospect, this signaling complexity should not be surprising. Actin regulates many dynamic cellular processes, including protein and organelle trafficking, establishment of cell polarity, directional migration, cellular traction, and the efficiency of endocytosis. Signaling events that coordinately control actin turnover during these processes must display a high degree of sophistication. Emerging data on an important regulator of actin dynamics, the actin-related protein 2 and 3 (Arp2/3) complex, suggest a model of how this may occur.
MeSH term(s)	Actin Cytoskeleton/metabolism ; Actin-Related Protein 2-3 Complex/metabolism ; Actins/chemistry ; Animals ; Cell Movement/physiology ; Cell Polarity ; Cytoskeleton/metabolism ; Models, Biological ; Neurons/metabolism ; Protein Structure, Tertiary ; Signal Transduction
Chemical Substances	Actin-Related Protein 2-3 Complex ; Actins
Language	English
Publishing date	2009-01-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2417226-1
ISSN	1937-9145 ; 1945-0877
ISSN (online)	1937-9145
ISSN	1945-0877
DOI	10.1126/scisignal.255pe5
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Article ; Online: Training-induced circuit-specific excitatory synaptogenesis in mice is required for effort control.

Ulloa Severino, Francesco Paolo / Lawal, Oluwadamilola O / Sakers, Kristina / Wang, Shiyi / Kim, Namsoo / Friedman, Alexander David / Johnson, Sarah Anne / Sriworarat, Chaichontat / Hughes, Ryan H / Soderling, Scott H / Kim, Il Hwan / Yin, Henry H / Eroglu, Cagla

Nature communications

2023 Volume 14, Issue 1, Page(s) 5522

Abstract: Synaptogenesis is essential for circuit development; however, it is unknown whether it is critical for the establishment and performance of goal-directed voluntary behaviors. Here, we show that operant conditioning via lever-press for food reward ... ...

Abstract	Synaptogenesis is essential for circuit development; however, it is unknown whether it is critical for the establishment and performance of goal-directed voluntary behaviors. Here, we show that operant conditioning via lever-press for food reward training in mice induces excitatory synapse formation onto a subset of anterior cingulate cortex neurons projecting to the dorsomedial striatum (ACC
MeSH term(s)	Animals ; Mice ; Learning ; Conditioning, Operant ; Corpus Striatum ; Food ; Mice, Knockout
Language	English
Publishing date	2023-09-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-41078-z
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Article ; Online: Action potential-coupled Rho GTPase signaling drives presynaptic plasticity.

O'Neil, Shataakshi Dube / Rácz, Bence / Brown, Walter Evan / Gao, Yudong / Soderblom, Erik J / Yasuda, Ryohei / Soderling, Scott H

eLife

2021 Volume 10

Abstract: In contrast to their postsynaptic counterparts, the contributions of activity-dependent cytoskeletal signaling to presynaptic plasticity remain controversial and poorly understood. To identify and evaluate these signaling pathways, we conducted a ... ...

Abstract	In contrast to their postsynaptic counterparts, the contributions of activity-dependent cytoskeletal signaling to presynaptic plasticity remain controversial and poorly understood. To identify and evaluate these signaling pathways, we conducted a proteomic analysis of the presynaptic cytomatrix using in vivo biotin identification (iBioID). The resultant proteome was heavily enriched for actin cytoskeleton regulators, including Rac1, a Rho GTPase that activates the Arp2/3 complex to nucleate branched actin filaments. Strikingly, we find Rac1 and Arp2/3 are closely associated with synaptic vesicle membranes in adult mice. Using three independent approaches to alter presynaptic Rac1 activity (genetic knockout, spatially restricted inhibition, and temporal optogenetic manipulation), we discover that this pathway negatively regulates synaptic vesicle replenishment at both excitatory and inhibitory synapses, bidirectionally sculpting short-term synaptic depression. Finally, we use two-photon fluorescence lifetime imaging to show that presynaptic Rac1 activation is coupled to action potentials by voltage-gated calcium influx. Thus, this study uncovers a previously unrecognized mechanism of actin-regulated short-term presynaptic plasticity that is conserved across excitatory and inhibitory terminals. It also provides a new proteomic framework for better understanding presynaptic physiology, along with a blueprint of experimental strategies to isolate the presynaptic effects of ubiquitously expressed proteins.
MeSH term(s)	Actin Cytoskeleton/metabolism ; Actins/metabolism ; Action Potentials/physiology ; Animals ; Calcium/metabolism ; Cytoskeleton/metabolism ; Hippocampus ; Mice ; Neuronal Plasticity/physiology ; Neuropeptides/metabolism ; Proteomics ; Synapses/physiology ; Synaptic Vesicles/metabolism ; rac1 GTP-Binding Protein/genetics ; rac1 GTP-Binding Protein/metabolism ; rho GTP-Binding Proteins/genetics ; rho GTP-Binding Proteins/metabolism
Chemical Substances	Actins ; Neuropeptides ; Rac1 protein, mouse ; rac1 GTP-Binding Protein (EC 3.6.5.2) ; rho GTP-Binding Proteins (EC 3.6.5.2) ; Calcium (SY7Q814VUP)
Language	English
Publishing date	2021-07-16
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.63756
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Article ; Online: Cnksr2 Loss in Mice Leads to Increased Neural Activity and Behavioral Phenotypes of Epilepsy-Aphasia Syndrome.

Erata, Eda / Gao, Yudong / Purkey, Alicia M / Soderblom, Erik J / McNamara, James O / Soderling, Scott H

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

2021 Volume 41, Issue 46, Page(s) 9633–9649

Abstract: Epilepsy Aphasia Syndromes (EAS) are a spectrum of childhood epileptic, cognitive, and language disorders of unknown etiology. ...

Abstract	Epilepsy Aphasia Syndromes (EAS) are a spectrum of childhood epileptic, cognitive, and language disorders of unknown etiology.
MeSH term(s)	Adaptor Proteins, Signal Transducing/deficiency ; Animals ; Behavior, Animal ; Disease Models, Animal ; Landau-Kleffner Syndrome ; Mice ; Mice, Knockout ; Nerve Tissue Proteins/deficiency ; Phenotype ; Syndrome
Chemical Substances	Adaptor Proteins, Signal Transducing ; Nerve Tissue Proteins
Language	English
Publishing date	2021-09-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.0650-21.2021
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Article ; Online: Under lock and key: spatiotemporal regulation of WASP family proteins coordinates separate dynamic cellular processes.

Burianek, Lauren E / Soderling, Scott H

Seminars in cell & developmental biology

2013 Volume 24, Issue 4, Page(s) 258–266

Abstract: WASP family proteins are nucleation promoting factors that bind to and activate the Arp2/3 complex in order to stimulate nucleation of branched actin filaments. The WASP family consists of WASP, N-WASP, WAVE1-3, WASH, and the novel family members WHAMM ... ...

Abstract	WASP family proteins are nucleation promoting factors that bind to and activate the Arp2/3 complex in order to stimulate nucleation of branched actin filaments. The WASP family consists of WASP, N-WASP, WAVE1-3, WASH, and the novel family members WHAMM and JMY. Each of the family members contains a C-terminus responsible for their nucleation promoting activity and unique N-termini that allow for them to be regulated in a spatiotemporal manner. Upon activation they reorganize the cytoskeleton for different cellular functions depending on their subcellular localization and regulatory protein interactions. Emerging evidence indicates that WASH, WHAMM, and JMY have functions that require the coordination of both actin polymerization and microtubule dynamics. Here, we review the mechanisms of regulation for each family member and their associated in vivo functions including cell migration, vesicle trafficking, and neuronal development.
MeSH term(s)	Actin-Related Protein 2-3 Complex/metabolism ; Animals ; Cytoskeletal Proteins/metabolism ; Humans ; Protein Transport ; Signal Transduction ; Wiskott-Aldrich Syndrome Protein Family/metabolism ; Wiskott-Aldrich Syndrome Protein, Neuronal/metabolism
Chemical Substances	Actin-Related Protein 2-3 Complex ; Cytoskeletal Proteins ; Wiskott-Aldrich Syndrome Protein Family ; Wiskott-Aldrich Syndrome Protein, Neuronal
Language	English
Publishing date	2013-01-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2012.12.005
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