Maternal sevoflurane exposure induces temporary defects in interkinetic nuclear migration of radial glial progenitors in the fetal cerebral cortex through the Notch signalling pathway

Jiang, Ming; Tang, Ting; Liang, Xinyue; Li, Juchen; Qiu, Yue; Liu, Shiwen; Bian, Shan; Xie, Yunyun; Fang, Fang; Cang, Jing

doi:10.1111/cpr.13042

Cited by 9 publications

(3 citation statements)

References 56 publications

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“…The concept of developmental origins of health and disease (DOHaD) theory has been widely accepted, which proposed that early life environmental factors have profound effects on vulnerability to disease in adulthood ( Haugen et al, 2015 ). Extensive range of clinical and epidemiological data suggested that gestational obesity and diabetes leave lasting impacts on the next generation, and so, the cycle of risk is perpetuated ( Godfrey et al, 2017 ; Chen et al, 2021b ; Du et al, 2021a ; Jiang et al, 2021 ; Lorenzon et al, 2021 ). Experimental research in animal models also showed that maternal high-fat diet (HF) during pregnancy and lactation predisposed offspring to metabolic disorders ( Zheng et al, 2014 ; Ribaroff et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Maternal Dietary Betaine Prevents High-Fat Diet-Induced Metabolic Disorders and Gut Microbiota Alterations in Mouse Dams and Offspring From Young to Adult

et al. 2022

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Early life is a critical window for preventing the intergenerational transmission of metabolic diseases. Betaine has been proven to play a role in improving glucose and lipid metabolism disorders in animal models. However, whether maternal betaine supplementation plays a role in regulating gut microbiota in both dams and offspring remains unclear. In this study, C57BL/6 female mice were fed with control diet (Ctr), high-fat diet (HF), and high-fat with betaine supplementation (0.3% betaine in the diet, HFB) from 3 weeks prior to mating and lasted throughout pregnancy and lactation. After weaning, the offspring got free access to normal chow diet until 20 weeks of age. We found that maternal dietary betaine supplementation significantly improved glucose and insulin resistance, as well as reduced free fatty acid (FFA) concentration in dams and offspring from young to adult. When compared to the HF group, Intestinimonas and Acetatifactor were reduced by betaine supplementation in dams; Desulfovibrio was reduced in 4-week-old offspring of the HFB group; and Lachnoclostridium was enriched in 20-week-old offspring of the HFB group. Moreover, the persistent elevated genus Romboutsia in both dams and offspring in the HFB group was reported for the first time. Overall, maternal betaine could dramatically alleviate the detrimental effects of maternal overnutrition on metabolism in both dams and offspring. The persistent alterations in gut microbiota might play critical roles in uncovering the intergenerational metabolic benefits of maternal betaine, which highlights evidence for combating generational metabolic diseases.

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Section: Introductionmentioning

confidence: 99%

Maternal Dietary Betaine Prevents High-Fat Diet-Induced Metabolic Disorders and Gut Microbiota Alterations in Mouse Dams and Offspring From Young to Adult

et al. 2022

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“…Veronica et al demonstrated that the type I interferon could reverse the nerve defects caused by the Zika virus and herpes simplex virus one in their organoid model, although type I interferon failed to reverse these defects in the monolayer neural culture models ( Krenn et al, 2021 ). Recently, cerebral organoids have been used in sevoflurane studies, and it was found that sevoflurane exposure impaired the nuclear migration in cerebral organoids ( Jiang et al, 2021 ). Thus, hMBO provides a highly relevant in vitro human model for studying the persistent effects of sevoflurane on dopaminergic neuronal development.…”

Section: Discussionmentioning

confidence: 99%

Sevoflurane promotes premature differentiation of dopaminergic neurons in hiPSC-derived midbrain organoids

Shang

Li²,

Han³

et al. 2022

Front. Cell Dev. Biol.

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Background: Conventional animal models used in corresponding basic studies are distinct from humans in terms of the brain’s development trajectory, tissue cytoarchitecture and cell types, making it difficult to accurately evaluate the potential adverse effects of anesthetic treatments on human fetal brain development. This study investigated the effects of sevoflurane on the midbrain’s development and cytopathology using human physiologically-relevant midbrain organoids.Methods: Monolayer human induced pluripotent stem cells (hiPSC)-derived human floor plate cells and three-dimensional hiPSC-derived midbrain organoids (hMBOs) were exposed to 2% (v/v) sevoflurane for 2 or 6 h, followed by expansion or differentiation culture. Then, immunofluorescence, real-time PCR, EdU assay, Tunnel assay, and transcriptome sequencing were performed to examine the effects of sevoflurane on the midbrain’s development.Results: We found that 2% sevoflurane exposure inhibited hFPCs’ proliferation (differentiation culture: 7.2% ± 0.3% VS. 13.3% ± 0.7%, p = 0.0043; expansion culture: 48% ± 2.2% VS. 35.2% ± 1.4%, p = 0.0002) and increased their apoptosis, but did not affect their differentiation into human dopaminergic neurons After 6 h, 2% sevoflurane exposure inhibited cell proliferation (62.8% ± 5.6% VS. 100% ± 5.5%, p = 0.0065) and enhanced the premature differentiation of hMBOs (246% ± 5.2% VS. 100% ± 28%, p = 0.0065). The RNA-seq results showed long-term exposure to sevoflurane up regulates some transcription factors in the differentiation of dopaminergic neurons, while short-term exposure to sevoflurane has a weak up-regulation effect on these transcription factors.Conclusion: This study revealed that long-term exposure to sevoflurane could promote the premature differentiation of hMBOs, while short-term exposure had negligible effects, suggesting that long-term exposure to sevoflurane in pregnant women may lead to fetals’ midbrain development disorder.

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“… 25 , 81 Inhibition of neurogenesis by the Pax6 pathway has deleterious effects on fetal and offspring brains' development. 82 Maternal exposure to sevoflurane during peak neurogenesis affects fetal brains' NSCs via the Notch signaling pathways but has no long‐term effects on neurocognitive outcomes 83 (Figure 2D ).…”

Section: Effects Of Anesthetic Drugs On Nscs and Their Mechanismsmentioning

confidence: 99%

Research progress on the effects and mechanisms of anesthetics on neural stem cells

Zhang

Chang

Rizzello

et al. 2022

Ibrain

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Exposure to anesthetic drugs has been proven to seriously affect developing animals in terms of neural stem cells' (NSCs') proliferation, differentiation, and apoptosis. This can severely hamper the development of physiological learning and memory skills. Studies on the effects of anesthetics on NSCs' proliferation and differentiation are thus reviewed here, with the aim to highlight which specific drug mechanisms are the least harmful to NSCs. PubMed has been used as the preferential searching database of relevant literature to identify studies on the effects and mechanisms of NSCs' proliferation and differentiation. It was concluded that propofol and sevoflurane may be the safest options for NSCs during pregnancy and in pediatric clinical procedures, while dexmedetomidine has been found to reduce opioid-related damage in NSCs. It was also found that the growth environment may impact neurodevelopment even more than narcotic drugs. Nonetheless, the current scientific literature available further highlights how more extensive clinical trials are absolutely required for corroborating the conclusion drawn here.

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Maternal sevoflurane exposure induces temporary defects in interkinetic nuclear migration of radial glial progenitors in the fetal cerebral cortex through the Notch signalling pathway

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 9 publications

References 56 publications

Maternal Dietary Betaine Prevents High-Fat Diet-Induced Metabolic Disorders and Gut Microbiota Alterations in Mouse Dams and Offspring From Young to Adult

Maternal Dietary Betaine Prevents High-Fat Diet-Induced Metabolic Disorders and Gut Microbiota Alterations in Mouse Dams and Offspring From Young to Adult

Sevoflurane promotes premature differentiation of dopaminergic neurons in hiPSC-derived midbrain organoids

Research progress on the effects and mechanisms of anesthetics on neural stem cells

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