Suppression of Hippocampal Neurogenesis and Oligodendrocyte Maturation Similar to Developmental Hypothyroidism by Maternal Exposure of Rats to Ammonium Perchlorate, a Gunpowder Raw Material and Known Environmental Contaminant

IF 4.4 3区 医学 Q2 ENVIRONMENTAL SCIENCES
Yuri Sakamaki, Momoka Shobudani, Ryota Ojiro, Shunsuke Ozawa, Qian Tang, Xinyu Zou, Yuri Ebizuka, Ayumi Karasawa, Gye-Hyeong Woo, Toshinori Yoshida, Makoto Shibutani
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Abstract

The environmental contaminant perchlorate raises concern for hypothyroidism-related brain disorders in children. This study investigated the effects of developmental perchlorate exposure on hippocampal neurogenesis and oligodendrocyte (OL) development. Pregnant Sprague–Dawley rats were administered with ammonium perchlorate (AP) in drinking water at concentrations of 0 (control), 300, and 1000 ppm from gestation day 6 until weaning [postnatal day (PND) 21]. On PND 21, offspring displayed decreased serum triiodothyronine and thyroxine concentrations at 1000 ppm and thyroid follicular epithelial cell hyperplasia at ≥300 ppm (accompanying increased proliferation activity at 1000 ppm). Hippocampal neurogenesis indicated suppressed proliferation of neurogenic cells at ≥300 ppm, causing decreases in type-1 neural stem cells (NSCs) and type-2a neural progenitor cells. In addition, an increase of SST+ GABAergic interneurons and decreasing trend for ARC+ granule cells were observed at 1000 ppm. CNPase+ mature OLs were decreased in number in the dentate gyrus hilus at ≥300 ppm. At PND 77, thyroid changes had disappeared; however, the decrease of type-1 NSCs and increase of SST+ interneurons persisted, CCK+ interneurons were increased, and white matter tissue area was decreased at 1000 ppm. Obtained results suggest an induction of hypothyroidism causing suppressed hippocampal neurogenesis (targeting early neurogenic processes and decreased synaptic plasticity of granule cells involving ameliorative interneuron responses) and suppressed OL maturation during the weaning period. In adulthood, suppression of neurogenesis continued, and white matter hypoplasia was evident. Observed brain changes were similar to those caused by developmental hypothyroidism, suggesting that AP-induced developmental neurotoxicity was due to hypothyroidism.

Abstract Image

母鼠暴露于高氯酸铵(一种火药原料和已知的环境污染物)会抑制海马神经发生和少突胶质细胞成熟,类似于发育性甲状腺机能减退。
环境污染物高氯酸盐引起了人们对儿童甲状腺机能减退相关脑部疾病的关注。本研究调查了发育期接触高氯酸盐对海马神经发生和少突胶质细胞(OL)发育的影响。从妊娠第 6 天开始至断奶[产后第 21 天],在饮用水中分别添加浓度为 0(对照组)、300 和 1000 ppm 的高氯酸铵(AP)。在断奶后第 21 天,后代的血清三碘甲状腺原氨酸和甲状腺素浓度在 1000 ppm 时下降,甲状腺滤泡上皮细胞在≥300 ppm 时增生(在 1000 ppm 时伴随着增殖活动的增加)。海马神经发生表明,当浓度≥300 ppm时,神经发生细胞的增殖受到抑制,导致1型神经干细胞(NSC)和2a型神经祖细胞减少。此外,在ppm浓度为1000时,观察到SST+ GABA能中间神经元增加,ARC+颗粒细胞呈减少趋势。ppm≥300时,齿状回脊髓中CNP酶+成熟OL数量减少。在 PND 77 时,甲状腺的变化已经消失;然而,在 1000 ppm 时,1 型 NSCs 的减少和 SST+ 中间神经元的增加仍然存在,CCK+ 中间神经元增加,白质组织面积减少。研究结果表明,甲状腺机能减退会导致海马神经发生受抑制(针对早期神经发生过程,颗粒细胞的突触可塑性降低,涉及改善性中间神经元反应),并在断奶期间抑制 OL 的成熟。成年后,神经发生继续受到抑制,白质明显发育不良。观察到的脑部变化与发育性甲状腺机能减退引起的变化相似,这表明AP诱导的发育性神经毒性是由甲状腺机能减退引起的。
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来源期刊
Environmental Toxicology
Environmental Toxicology 环境科学-毒理学
CiteScore
7.10
自引率
8.90%
发文量
261
审稿时长
4.5 months
期刊介绍: The journal publishes in the areas of toxicity and toxicology of environmental pollutants in air, dust, sediment, soil and water, and natural toxins in the environment.Of particular interest are: Toxic or biologically disruptive impacts of anthropogenic chemicals such as pharmaceuticals, industrial organics, agricultural chemicals, and by-products such as chlorinated compounds from water disinfection and waste incineration; Natural toxins and their impacts; Biotransformation and metabolism of toxigenic compounds, food chains for toxin accumulation or biodegradation; Assays of toxicity, endocrine disruption, mutagenicity, carcinogenicity, ecosystem impact and health hazard; Environmental and public health risk assessment, environmental guidelines, environmental policy for toxicants.
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