The Role of Redox Dysregulation in the Effects of Prenatal Stress on Embryonic Interneuron Migration

Bittle, Jada; Menezes, Edênia da Cunha; McCormick, Michael L.; Spitz, Douglas R.; Dailey, Michael E.; Stevens, Hanna E.

doi:10.1093/cercor/bhz052

Cited by 14 publications

(6 citation statements)

References 84 publications

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“…Finally, adult rats that have received the mitotoxin Methylazoxymethanol Acetate (MAM) during late gestation show deficits in hippocampal and prefrontal PV neurons, weakened PNN, and impaired neuronal synchronization alongside with OxS and decreased brain GSH levels [15,[96][97][98]. Moreover, OxS induced by a prenatal stress slows down the migration of inhibitory interneuron progenitors, a migration that can be accelerated by antioxidants [99]. Altogether, these indicate that OxS during development disrupts maturation and function of PV neuron-associated networks.…”

Section: Developmental Perspectivementioning

confidence: 99%

Caught in vicious circles: a perspective on dynamic feed-forward loops driving oxidative stress in schizophrenia

Cuénod¹,

Steullet²,

Cabungcal³

et al. 2021

Mol Psychiatry

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A growing body of evidence has emerged demonstrating a pathological link between oxidative stress and schizophrenia. This evidence identifies oxidative stress as a convergence point or “central hub” for schizophrenia genetic and environmental risk factors. Here we review the existing experimental and translational research pinpointing the complex dynamics of oxidative stress mechanisms and their modulation in relation to schizophrenia pathophysiology. We focus on evidence supporting the crucial role of either redox dysregulation, N-methyl-D-aspartate receptor hypofunction, neuroinflammation or mitochondria bioenergetics dysfunction, initiating “vicious circles” centered on oxidative stress during neurodevelopment. These processes would amplify one another in positive feed-forward loops, leading to persistent impairments of the maturation and function of local parvalbumin-GABAergic neurons microcircuits and myelinated fibers of long-range macrocircuitry. This is at the basis of neural circuit synchronization impairments and cognitive, emotional, social and sensory deficits characteristic of schizophrenia. Potential therapeutic approaches that aim at breaking these different vicious circles represent promising strategies for timely and safe interventions. In order to improve early detection and increase the signal-to-noise ratio for adjunctive trials of antioxidant, anti-inflammatory and NMDAR modulator drugs, a reverse translation of validated circuitry approach is needed. The above presented processes allow to identify mechanism based biomarkers guiding stratification of homogenous patients groups and target engagement required for successful clinical trials, paving the way towards precision medicine in psychiatry.

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Section: Developmental Perspectivementioning

confidence: 99%

Caught in vicious circles: a perspective on dynamic feed-forward loops driving oxidative stress in schizophrenia

Cuénod¹,

Steullet²,

Cabungcal³

et al. 2021

Mol Psychiatry

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“…Sulfur-containing amino acids are not only important sources of sulfur nutrients in humans and mammals but also play an important role in various biochemical processes such as transformation and synthesis of proteins, immunity, , as well as oxidative stress resistance. − It is generally considered that redox reaction balance of many sulfur-containing amino acids is closely associated with cardiovascular disease, neuropsychiatric disorder, neurogenic diseases, renalischemia, liver failure, diabetes, cancer, and aging. ,,− The sulfur-containing amino acids supplementation may readily scavenge biological reactive oxidants in vivo through their redox reactions to protect the stability and activity of other essential amino acids in proteins reducing the damage to cell membrane and DNA caused by oxidative stress and, in turn, incidence of these diseases.…”

Section: Introductionmentioning

confidence: 99%

Autoinhibition by Iodide Ion in the Methionine–Iodine Reaction

Csekõ

Horváth

2020

J. Phys. Chem. A

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The methionine–iodine reaction was reinvestigated spectrophotometrically in detail monitoring the absorbance belonging to the isosbestic point of iodine at 468 nm, at T = 25.0 ± 0.1 °C, and at 0.5 M ionic strength in buffered acidic medium. The stoichiometric ratio of the reactants was determined to be 1:1 producing methionine sulfoxide as the lone sulfur-containing product. The direct reaction between methionine and iodine was found to be relatively rapid in the absence of initially added iodide ion, and it can conveniently be followed by the stopped-flow technique. Reduction of iodine eventually leads to the formation of iodide ion that inhibits the reaction making the whole system autoinhibitory with respect to the halide ion. We have also shown that this inhibitory effect appears quite prominently, and addition of iodide ion in the millimole concentration range may result in a rate law where the formal kinetic order of this species becomes −2. In contrast to this, hydrogen ion has just a mildly inhibitory effect giving rise to the fact that iodine is the kinetically active species in the system but not hypoiodous acid. The surprisingly complex kinetics of this simple reaction may readily be interpreted via the initiating rapidly established iodonium-transfer process between the reactants followed by the subsequent hydrolytic decomposition of the short-lived iodinated methionine. A seven-step kinetic model to be able to describe the most important characteristics of the measured kinetic curves is established and discussed in detail.

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“…However, the role for "basic science" studies of pre-natal maternal stress and mental health has remained surprisingly descriptive, with little attention dedicated to the study of biological mechanisms. Despite novel insight from several studies in non-human species (e.g., Gapp et al, 2014;Jašarević et al, 2018;Nugent et al, 2018;Bittle et al, 2019;Jašarević and Bale, 2019), our understanding of candidate mechanisms involved in prenatal stress remains poor. Furthermore, studies of pre-natal maternal stress in non-human species have largely failed to integrate major advances in the biological sciences, such as single-cell sequencing methods, CRISPR-Cas9 based genetic manipulation and brain organoids.…”

Section: Summary and Perspectivementioning

confidence: 99%

Maternal Distress and Offspring Neurodevelopment: Challenges and Opportunities for Pre-clinical Research Models

Fitzgerald

Parent

Kee

et al. 2021

Front. Hum. Neurosci.

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Pre-natal exposure to acute maternal trauma or chronic maternal distress can confer increased risk for psychiatric disorders in later life. Acute maternal trauma is the result of unforeseen environmental or personal catastrophes, while chronic maternal distress is associated with anxiety or depression. Animal studies investigating the effects of pre-natal stress have largely used brief stress exposures during pregnancy to identify critical periods of fetal vulnerability, a paradigm which holds face validity to acute maternal trauma in humans. While understanding these effects is undoubtably important, the literature suggests maternal stress in humans is typically chronic and persistent from pre-conception through gestation. In this review, we provide evidence to this effect and suggest a realignment of current animal models to recapitulate this chronicity. We also consider candidate mediators, moderators and mechanisms of maternal distress, and suggest a wider breadth of research is needed, along with the incorporation of advanced -omics technologies, in order to understand the neurodevelopmental etiology of psychiatric risk.

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The Role of Redox Dysregulation in the Effects of Prenatal Stress on Embryonic Interneuron Migration

Cited by 14 publications

References 84 publications

Caught in vicious circles: a perspective on dynamic feed-forward loops driving oxidative stress in schizophrenia

Caught in vicious circles: a perspective on dynamic feed-forward loops driving oxidative stress in schizophrenia

Autoinhibition by Iodide Ion in the Methionine–Iodine Reaction

Maternal Distress and Offspring Neurodevelopment: Challenges and Opportunities for Pre-clinical Research Models

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