Experience-dependent myelination following stress is mediated by the neuropeptide dynorphin

Osso, Lindsay A.; Rankin, Kelsey A; Chan, Jonah R.

doi:10.1016/j.neuron.2021.08.015

Cited by 37 publications

(25 citation statements)

References 69 publications

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“…One possibility is that neurons and axons release inducible signals and initiate OPC differentiation. For example, dynorphin-expressing neurons regulate the myelination of neighboring axons by releasing dynorphin, which binds to the kappa opioid receptor on OPCs to initiate differentiation and myelination (Mei, Mayoral, et al, 2016;Osso et al, 2021).…”

Section: 11mentioning

confidence: 99%

“…Since myelin changes alter the speed and frequency of the propagation of action potentials, the addition or elimination of myelin sheaths can reshape neuronal circuitries and modulate neuronal functions (Hughes & Orthmann-Murphy, 2018;McKenzie et al, 2014;Pan et al, 2020;Steadman et al, 2020;Xiao et al, 2016). Moreover, myelin formation can substantially change synaptogenesis in the developing CNS and alter neuronal activity and expression in adult brains (Osso et al, 2021;Pan et al, 2020;. These findings indicate that myelin changes represent a type of neuroplasticity that modulates fundamental brain functions, such as learning and memory (McKenzie et al, 2014;Pan et al, 2020;Wang et al, 2020;Xiao et al, 2016).…”

Section: Myelin Changes and Neuronal Functionsmentioning

confidence: 99%

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Oligodendrocytes and myelin: Active players in neurodegenerative brains?

Chen

Wang

Huang

et al. 2022

Developmental Neurobiology

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Oligodendrocytes (OLs) are a major type of glial cells in the central nervous system that generate multiple myelin sheaths to wrap axons. Myelin ensures fast and efficient propagation of action potentials along axons and supports neurons with nourishment. The decay of OLs and myelin has been implicated in age-related neurodegenerative diseases and these changes are generally considered as an inevitable result of neuron loss and axon degeneration. Noticeably, OLs and myelin undergo dynamic changes in healthy adult brains, that is, newly formed OLs are continuously added throughout life from the differentiation of oligodendrocyte precursor cells (OPCs) and the pre-existing myelin sheaths may undergo degeneration or remodeling. Increasing evidence has shown that changes in OLs and myelin are present in the early stages of neurodegenerative diseases, and even prior to significant neuronal loss and functional deficits. More importantly, oligodendroglia-specific manipulation, by either deletion of the disease gene or enhancement of myelin renewal, can alleviate functional impairments in neurodegenerative animal models. These findings underscore the possibility that OLs and myelin are not passively but actively involved in neurodegenerative diseases and may play an important role in modulating neuronal function and survival. In this review, we summarize recent work characterizing by OLs and myelin changes in both healthy and neurodegenerative brains and discuss the potential of targeting oligodendroglial cells in treating neurodegenerative diseases.

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Section: 11mentioning

confidence: 99%

Section: Myelin Changes and Neuronal Functionsmentioning

confidence: 99%

Oligodendrocytes and myelin: Active players in neurodegenerative brains?

Chen

Wang

Huang

et al. 2022

Developmental Neurobiology

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“…pain perception, dysphoria, neuroendocrine regulation, extrapyramidal motor control, cardiovascular function, respiration, water balance system (diuresis), temperature regulation and feeding behaviour ( Fallon and Leslie, 1986 ). Recently, it has also been shown that KOR activation could decrease the differentiation process during neurogenesis ( Xu et al, 2021 ), and that dynorphin promotes both developmental and stress-induced oligodendrocyte precursor cell differentiation and myelination in the striatum ( Osso et al, 2021 ). As other opioid receptors, KOR mediate peripheral analgesia, by acting on the pain pathway at primary sensory neurons, the spinal cord and the brainstem ( Figure 1 ).…”

Section: The Dynorphin/kappa-opioid Receptor Systemmentioning

confidence: 99%

Traumatic Stress-Induced Vulnerability to Addiction: Critical Role of the Dynorphin/Kappa Opioid Receptor System

2022

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Substance use disorders (SUD) may emerge from an individual’s attempt to limit negative affective states and symptoms linked to stress. Indeed, SUD is highly comorbid with chronic stress, traumatic stress, or post-traumatic stress disorder (PTSD), and treatments approved for each pathology individually often failed to have a therapeutic efficiency in such comorbid patients. The kappa-opioid receptor (KOR) and its endogenous ligand dynorphin (DYN), seem to play a key role in the occurrence of this comorbidity. The DYN/KOR function is increased either in traumatic stress or during drug use, dependence acquisition and DYN is released during stress. The behavioural effects of stress related to the DYN/KOR system include anxiety, dissociative and depressive symptoms, as well as increased conditioned fear response. Furthermore, the DYN/KOR system is implicated in negative reinforcement after the euphoric effects of a drug of abuse ends. During chronic drug consumption DYN/KOR functions increase and facilitate tolerance and dependence. The drug-seeking behaviour induced by KOR activation can be retrieved either during the development of an addictive behaviour, or during relapse after withdrawal. DYN is known to be one of the most powerful negative modulators of dopamine signalling, notably in brain structures implicated in both reward and fear circuitries. KOR are also acting as inhibitory heteroreceptors on serotonin neurons. Moreover, the DYN/KOR system cross-regulate with corticotropin-releasing factor in the brain. The sexual dimorphism of the DYN/KOR system could be the cause of the gender differences observed in patients with SUD or/and traumatic stress-related pathologies. This review underlies experimental and clinical results emphasizing the DYN/KOR system as common mechanisms shared by SUD or/and traumatic stress-related pathologies, and suggests KOR antagonist as a new pharmacological strategy to treat this comorbidity.

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“…Over the past several decades, researchers have made great progress in elucidating the cell-intrinsic regulation of oligodendrocyte development and myelination (e.g., transcription factors, epigenetic mechanisms, and cell death pathways) (Aggarwal et al, 2013; Bergles and Richardson, 2016; Budde et al, 2010; Dugas et al, 2010; Elbaz and Popko, 2019; Elbaz et al, 2018; Emery and Lu, 2015; Emery et al, 2009; Fedder- Semmes and Appel, 2021; Foerster et al, 2020; Harrington et al, 2010; Herbert and Monk, 2017; Howng et al, 2010; Koenning et al, 2012; Mitew et al, 2018; Nawaz et al, 2015; Snaidero et al, 2017; Sun et al, 2018; Wang et al, 2017; Xu et al, 2020; Zhao et al, 2018; Zuchero et al, 2015), as well as the cell-extrinsic regulation by other cell types (e.g., neurons (Gibson et al, 2014; Hines et al, 2015; Mayoral et al, 2018; Osso et al, 2021; Redmond et al, 2016; Wake et al, 2011), microglia/macrophages (Butovsky et al, 2006; Sherafat et al, 2021), and lymphocytes (Dombrowski et al, 2017)). However, it remains unclear whether interactions among oligodendrocyte-lineage cells (OPCs and oligodendrocytes) affect oligodendrocyte development and myelination.…”

Section: Introductionmentioning

confidence: 99%

Oligodendrocyte-lineage cell exocytosis and L-type prostaglandin D synthase promote oligodendrocyte development and myelination

Pan

Trimarco

Zhang

et al. 2022

Preprint

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In the developing central nervous system, oligodendrocyte precursor cells (OPCs) differentiate into oligodendrocytes, which form myelin around axons. Oligodendrocytes and myelin are essential for the function of the central nervous system, as evidenced by the severe neurological symptoms that arise in demyelinating diseases such as multiple sclerosis and leukodystrophy. Although many cell-intrinsic mechanisms that regulate oligodendrocyte development and myelination have been reported, it remains unclear whether interactions among oligodendrocyte-lineage cells (OPCs and oligodendrocytes) affect oligodendrocyte development and myelination. Here, we show that blocking vesicle-associated membrane protein (VAMP) 1/2/3-dependent exocytosis from oligodendrocyte-lineage cells impairs oligodendrocyte development, myelination, and motor behavior in mice. Adding oligodendrocyte-lineage cell-secreted molecules to secretion-deficient OPC cultures partially restores the morphological maturation of oligodendrocytes. Moreover, we identified L-type prostaglandin D synthase as an oligodendrocyte-lineage cell-secreted protein that promotes oligodendrocyte development and myelination in vivo. These findings reveal a novel autocrine/paracrine loop model for the regulation of oligodendrocyte and myelin development.

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Experience-dependent myelination following stress is mediated by the neuropeptide dynorphin

Cited by 37 publications

References 69 publications

Oligodendrocytes and myelin: Active players in neurodegenerative brains?

Oligodendrocytes and myelin: Active players in neurodegenerative brains?

Traumatic Stress-Induced Vulnerability to Addiction: Critical Role of the Dynorphin/Kappa Opioid Receptor System

Oligodendrocyte-lineage cell exocytosis and L-type prostaglandin D synthase promote oligodendrocyte development and myelination

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