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Repeated gestational exposure to diesel engine exhaust affects the fetal olfactory system and alters olfactory-based behavior in rabbit offspring
Particle and Fibre Toxicology ( IF 7.2 ) Pub Date : 2019-01-17 , DOI: 10.1186/s12989-018-0288-7
Estefanía Bernal-Meléndez 1, 2 , Marie-Christine Lacroix 1 , Pascaline Bouillaud 2 , Jacques Callebert 3 , Benoit Olivier 2 , Marie-Annick Persuy 1 , Didier Durieux 1 , Delphine Rousseau-Ralliard 4 , Josiane Aioun 4 , Flemming Cassee 5, 6 , Anne Couturier-Tarrade 4 , Sarah Valentino 4 , Pascale Chavatte-Palmer 4 , Henri Schroeder 2 , Christine Baly 1
Affiliation  

Airborne pollution, especially from diesel exhaust (DE), is known to have a negative effect on the central nervous system in exposed human populations. However, the consequences of gestational exposure to DE on the fetal brain remain poorly explored, with various effects depending on the conditions of exposure, as well as little information on early developmental stages. We investigated the short-term effects of indirect DE exposure throughout gestation on the developing brain using a rabbit model. We analyzed fetal olfactory tissues at the end of gestation and tested behaviors relevant to pups’ survival at birth. Pregnant dams were exposed by nose-only inhalation to either clean air or DE with a content of particles (DEP) adjusted to 1 mg/m3 by diluting engine exhaust, for 2 h/day, 5 days/week, from gestational day 3 (GD3) to day 27 (GD27). At GD28, fetal olfactory mucosa, olfactory bulbs and whole brains were collected for anatomical and neurochemical measurements. At postnatal day 2 (PND2), pups born from another group of exposed or control female were examined for their odor-guided behavior in response to the presentation of the rabbit mammary pheromone 2-methyl-3-butyn-2-ol (2MB2). At GD28, nano-sized particles were observed in cilia and cytoplasm of the olfactory sensory neurons in the olfactory mucosa and in the cytoplasm of periglomerular cells in the olfactory bulbs of exposed fetuses. Moreover, cellular and axonal hypertrophies were observed throughout olfactory tissues. Concomitantly, fetal serotoninergic and dopaminergic systems were affected in the olfactory bulbs. Moreover, the neuromodulatory homeostasis was disturbed in a sex-dependent manner in olfactory tissues. At birth, the olfactory sensitivity to 2MB2 was reduced in exposed PND2 pups. Gestational exposure to DE alters olfactory tissues and affects monoaminergic neurotransmission in fetuses’ olfactory bulbs, resulting in an alteration of olfactory-based behaviors at birth. Considering the anatomical and functional continuum between the olfactory system and other brain structures, and due to the importance of monoamine neurotransmission in the plasticity of neural circuits, such alterations could participate to disturbances in higher integrative structures, with possible long-term neurobehavioral consequences.

中文翻译:


妊娠期反复接触柴油发动机废气会影响胎儿的嗅觉系统并改变兔子后代的嗅觉行为



众所周知,空气污染,尤其是来自柴油机尾气 (DE) 的污染,会对暴露人群的中枢神经系统产生负面影响。然而,妊娠期暴露于 DE 对胎儿大脑的影响仍知之甚少,其影响取决于暴露条件,而且关于早期发育阶段的信息也很少。我们使用兔子模型研究了整个妊娠期间间接接触 DE 暴露对大脑发育的短期影响。我们分析了妊娠末期胎儿的嗅觉组织,并测试了与幼崽出生时存活相关的行为。从妊娠第 3 天开始,怀孕母鼠通过仅鼻子吸入清洁空气或 DE,通过稀释发动机废气将颗粒含量 (DEP) 调整至 1 mg/m3,每天 2 小时,每周 5 天( GD3) 至第 27 天 (GD27)。在GD28时,收集胎儿嗅粘膜、嗅球和全脑用于解剖学和神经化学测量。出生后第 2 天 (PND2),检查另一组暴露或对照雌性所生的幼崽,检查其气味引导行为,以响应兔乳腺信息素 2-甲基-3-丁炔-2-醇 (2MB2) 的出现。在 GD28 时,在暴露胎儿的嗅粘膜嗅感觉神经元的纤毛和细胞质中以及嗅球的肾小球周围细胞的细胞质中观察到纳米尺寸的颗粒。此外,在整个嗅觉组织中观察到细胞和轴突肥大。与此同时,胎儿嗅球的血清素能和多巴胺能系统受到影响。此外,嗅觉组织中的神经调节稳态以性别依赖性方式受到干扰。出生时,接触 PND2 的幼崽对 2MB2 的嗅觉敏感性降低。 妊娠期暴露于 DE 会改变嗅觉组织并影响胎儿嗅球中的单胺能神经传递,导致出生时嗅觉行为的改变。考虑到嗅觉系统和其他大脑结构之间的解剖和功能连续体,并且由于单胺神经传递在神经回路可塑性中的重要性,这种改变可能参与更高整合结构的干扰,并可能产生长期神经行为后果。
更新日期:2019-01-17
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