Induction of astrocytic Slc22a3 regulates sensory processing through histone serotonylation

Sardar, Debosmita; Cheng, Yi-Ting; Woo, Junsung; Choi, Dong‐Joo; Lee, Zhung-Fu; Kwon, Wookbong; Chen, Hsiao‐Chi; Lozzi, Brittney; Cervantes, Alexis; Rajendran, Kavitha; Huang, Teng-Wei; Jain, Antrix; Arenkiel, Benjamin R.; Maze, Ian; Deneen, Benjamin

doi:10.1126/science.ade0027

Cited by 15 publications

(6 citation statements)

References 67 publications

(110 reference statements)

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“…111 Recently, a newly identified epigenetic role for serotonin uptake has been described. 112 In particular, neuronal activity, through the increase of OCT3 expression and histone serotonylation in olfactory bulb astrocytes, has been demonstrated to enhance the levels of astrocytic GABA biosynthesis and release, with effects on olfactory processing and behavior.…”

Section: Transmissionmentioning

confidence: 99%

“…In addition, 5-HT modulation of astrocytes has been correlated also to other effects, for example, in sleep and depression. − Furthermore, besides being responsive to serotonergic signaling thanks to the expression of 5-HT receptors, astrocytes are also capable of uptaking extracellular serotonin , thanks to the expression of the transporter SERT , and other monoamine transporters, such as the organic cation transporter 3 (OCT3) . Recently, a newly identified epigenetic role for serotonin uptake has been described . In particular, neuronal activity, through the increase of OCT3 expression and histone serotonylation in olfactory bulb astrocytes, has been demonstrated to enhance the levels of astrocytic GABA biosynthesis and release, with effects on olfactory processing and behavior.…”

Section: Serotonin–glia Interplay Via Volume Transmissionmentioning

confidence: 99%

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Wiring and Volume Transmission: An Overview of the Dual Modality for Serotonin Neurotransmission

Gianni,

Pasqualetti

2023

ACS Chem. Neurosci.

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Serotonin is a neurotransmitter involved in the modulation of a multitude of physiological and behavioral processes. In spite of the relatively reduced number of serotoninproducing neurons present in the mammalian CNS, a complex long-range projection system provides profuse innervation to the whole brain. Heterogeneity of serotonin receptors, grouped in seven families, and their spatiotemporal expression pattern account for its widespread impact. Although neuronal communication occurs primarily at tiny gaps called synapses, wiring transmission, another mechanism based on extrasynaptic diffusion of neuroactive molecules and referred to as volume transmission, has been described. While wiring transmission is a rapid and specific one-toone modality of communication, volume transmission is a broader and slower mode in which a single element can simultaneously act on several different targets in a one-to-many mode. Some experimental evidence regarding ultrastructural features, extrasynaptic localization of receptors and transporters, and serotonin−glia interactions collected over the past four decades supports the existence of a serotonergic system of a dual modality of neurotransmission, in which wiring and volume transmission coexist. To date, in spite of the radical difference in the two modalities, limited information is available on the way they are coordinated to mediate the specific activities in which serotonin participates. Understanding how wiring and volume transmission modalities contribute to serotonergic neurotransmission is of utmost relevance for the comprehension of serotonin functions in both physiological and pathological conditions.

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Section: Transmissionmentioning

confidence: 99%

Section: Serotonin–glia Interplay Via Volume Transmissionmentioning

confidence: 99%

Wiring and Volume Transmission: An Overview of the Dual Modality for Serotonin Neurotransmission

Gianni,

Pasqualetti

2023

ACS Chem. Neurosci.

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“…The findings of unique transcriptomic profiles of astrocytes highlight several intriguing possibilities, including functional specializations within known astrocyte function 75,80,81 . Furthermore, the number of unique genes between ASTs outnumbered the shared ones, which indicates potentially uniquely specialized astrocyte cell types 76,82,83 . For example, AST4 possesses a unique transcriptome with a small overlap with other ASTs, and GO terms suggest that this subtype could be linked to functions in the neuro-vascular unit 80 .…”

Section: Discussionmentioning

confidence: 99%

Functional diversities within neurons and astrocytes in the adult rat auditory cortex revealed by single-nucleus RNA sequencing

Aydin,

Lemenze,

Bieszczad

2024

Preprint

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The mammalian cerebral cortex is composed of a rich diversity of cell types. Cortical cells are organized into networks that rely on their functional diversity to ultimately carry out a variety of sophisticated cognitive functions. To investigate the breadth of transcriptionally diverse cell types in the cortex, we used single-nucleus RNA sequencing (snRNA-seq) in the auditory cortex of the adult rat. A variety of unique excitatory and inhibitory neuron types were identified. In addition, we report for the first time a diversity of astrocytes in the auditory cortex that may represent functionally unique subtypes. Together, these results pave the way for building models of how neurons in the sensory cortex work in concert with astrocytes at synapses to fulfill high-cognitive functions like learning and memory.

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“…Glutamate elicits Ca 2+ signaling 55,56 that promotes the release of gliotransmitters, including glutamate, ATP and D-serine 57 . Neural activity also regulates expression of astrocyte genes, including those that regulate synapse formation and function 58 . Yet the molecular mechanisms by which astrocytes translate neural activity into changes in gene expression have not been identified.…”

Section: Discussionmentioning

confidence: 99%

Astrocyte modulation of synaptic plasticity mediated by activity-dependent Sonic hedgehog signaling

Le,

Fu,

Kumar

et al. 2024

Preprint

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The influence of neural activity on astrocytes and their reciprocal interactions with neurons has emerged as an important modulator of synapse function. Activity regulates gene expression in astrocytes, yet the molecular mechanisms by which such activity is translated into functional changes in gene expression have remained largely unknown. The molecular signaling pathway, Sonic hedgehog (Shh), mediates neuron-astrocyte communication and regulates the organization of cortical synapses. Here, we demonstrate that sensory experience stimulates SHH signaling in cortical astrocytes. Whisker stimulation and chemogenetic activation both increase SHH activity in deep layers of the somatosensory cortex, where neuron-astrocyte SHH signaling is predominantly found. Selective loss of SHH signaling in astrocytes occludes experience-dependent structural plasticity of synapses. We further demonstrate that sensory experience promotes expression of the synapse modifying molecules, Hevin and SPARC, in a SHH-dependent manner. Taken together, these data identify SHH signaling as an activity-dependent, neuronal derived cue that stimulates astrocyte interactions with synapses and promotes synaptic plasticity.

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Induction of astrocytic Slc22a3 regulates sensory processing through histone serotonylation

Cited by 15 publications

References 67 publications

Wiring and Volume Transmission: An Overview of the Dual Modality for Serotonin Neurotransmission

Wiring and Volume Transmission: An Overview of the Dual Modality for Serotonin Neurotransmission

Functional diversities within neurons and astrocytes in the adult rat auditory cortex revealed by single-nucleus RNA sequencing

Astrocyte modulation of synaptic plasticity mediated by activity-dependent Sonic hedgehog signaling

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