Exposure to Benzo[a]pyrene impairs the corpus luteum vascular network in rats during early pregnancy

Liu, Min; Deng, Ting; He, Junlin; Ding, Yubin; Liu, Xueqing; Xu, Hang; Gao, Rufei; Mu, Xinyi; Geng, Yanqing; Liu, Tai-Hang; Wang, Yingxiong

doi:10.1016/j.envpol.2020.113915

Cited by 15 publications

(8 citation statements)

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“…1c and d). Since embryo implantation and decidualization, are related to estrogen and progesterone levels, which are produced by the corpus luteum of the ovary [14]. We determined the effects of HFD-induced obesity on the ovary during early pregnancy.…”

Section: Resultsmentioning

confidence: 99%

High-Fat Diet-Induced Obesity Primes Impaired Fatty Acid β-Oxidation and Consequent Ovarian Dysfunction During Early Pregnancy

Qingying¹,

Guo²,

Yang³

et al. 2021

Preprint

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Background: Obesity is associated with many adverse effects on female fertility. Obese women are more likely to have ovulatory dysfunction due to dysregulation of the hypothalamic-pituitary-ovarian axis. However, ovarian function in obese women during early pregnancy still needs further assessment. Methods: Obesity was induced in C57BL6/J mice using high-fat diets (HFD) for 12 weeks; In vitro high-fat model was established with KGN cells treated with Oleate acid and Palmitic acid. Ovarian morphology of obese mice in early pregnancy was assessed by Hematoxylin and Eosin staining and its function was assessed using ELISA, Western blotting and Immunohistochemistry. The Oil Red O staining and Transmission electron microscopy were used to detect fatty acid accumulation and specific markers relating to ovarian functional mechanism were assessed by Real time PCR, Western blotting, Lactate detection, ATP detection, Biochemical analyses and ELISA.Results: The results of this study showed that during early pregnancy, the number of corpus luteum, serum estradiol and progesterone levels, and the expression of genes CYP19A1, CYP11A1 and StAR, which are related to steroid biosynthesis, were significantly increased in HFD female mice. HFD-fed mice also showed a significant increase in ovarian lipid accumulation on day 7 of pregnancy. Genes involved in fatty acid synthesis (Acsl4 and Elovl5) and fatty acid uptake and transport (Slc27a4), together with the β-oxidation rate-limiting enzyme (Cpt1a) were significantly upregulated in HFD-fed mice. Specifically, there was abnormal elevation of ATP level and aberrant expression of tricarboxylic acid cycle (TCA) and electron transport chain related genes in the ovary of HFD pregnant mice. Treatment of KGN cells with etomoxir targeting β-oxidation of fatty acid, showed decrease tricarboxylic acid cycle and electron transport chain. The elevated ATP level and the increased estradiol and progesterone levels were reversed. Conclusions: This study indicated that during early pregnancy, high-fat diet and induced-obesity increased fatty acid β-oxidation, which in turn increase the tricarboxylic acid cycle and the electron transport chain, and consequently increases ATP production and ovarian dysfunction.

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Section: Resultsmentioning

confidence: 99%

High-Fat Diet-Induced Obesity Primes Impaired Fatty Acid β-Oxidation and Consequent Ovarian Dysfunction During Early Pregnancy

Qingying¹,

Guo²,

Yang³

et al. 2021

Preprint

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“…Moreover, constituents of petroleum products such as PAHs have been shown to adversely affect placental development and function (Drwal, Rak, & Gregoraszczuk, 2019). For instance, BaP exposure during pregnancy has been reported to disrupt vascular networks in the decidua (Li et al, 2017) and corpus luteum (Liu et al, 2020). However, petroleum products, fracturing fluids, or wastewaters produced as a consequence of oil and gas extraction contain a number of other constituents including sulfur‐containing heterocyclic aromatic compounds whose toxicity is largely unknown.…”

Section: Discussionmentioning

confidence: 99%

“…PAHs are a broad group of organic compounds that contain two or more benzene rings, which can be substituted with alkyl groups or nitrogen, sulfur, or oxygen atoms to form heterocyclic aromatic compounds (Alegbeleye, Opeolu, & Jackson, 2017). PAHs have been reported to cause endocrine disruption and reproductive impairment (Alegbeleye, Opeolu, & Jackson, 2017) in part due to their ability to interfere with estrogen and progesterone synthesis and signaling (Gozgit, Nestor, Fasco, Pentecost, & Arcaro, 2004; Kummer et al, 2008; X. Li et al, 2017; M. Liu et al, 2020; Sadeu & Foster, 2011; Y. Zhang, Dong, Wang, Tao, & Kiyama, 2016; Zhao et al, 2014). For example, exposure to a commonly studied PAH, benzo[a]pyrene (BaP), has been shown to decrease estradiol production in isolated mouse ovarian follicle culture (Sadeu & Foster, 2011) and alter estradiol and progesterone production following in vivo administration (Li et al, 2017; Liu et al, 2020; Zhao et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…PAHs have been reported to cause endocrine disruption and reproductive impairment (Alegbeleye, Opeolu, & Jackson, 2017) in part due to their ability to interfere with estrogen and progesterone synthesis and signaling (Gozgit, Nestor, Fasco, Pentecost, & Arcaro, 2004; Kummer et al, 2008; X. Li et al, 2017; M. Liu et al, 2020; Sadeu & Foster, 2011; Y. Zhang, Dong, Wang, Tao, & Kiyama, 2016; Zhao et al, 2014). For example, exposure to a commonly studied PAH, benzo[a]pyrene (BaP), has been shown to decrease estradiol production in isolated mouse ovarian follicle culture (Sadeu & Foster, 2011) and alter estradiol and progesterone production following in vivo administration (Li et al, 2017; Liu et al, 2020; Zhao et al, 2014). Importantly, estrogen and progesterone are required for successful placentation, including the establishment of the feto‐maternal vasculature (Chatuphonprasert, Jarukamjorn, & Ellinger, 2018; Costa, 2016; Maliqueo, Echiburú, & Crisosto, 2016; Mandalà, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Effects of dibenzothiophene, a sulfur‐containing heterocyclic aromatic hydrocarbon, and its alkylated congener, 2,4,7‐trimethyldibenzothiophene, on placental trophoblast cell function

Raez-Villanueva

Perono

Jamshed

et al. 2020

J of Applied Toxicology

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Worldwide demand for petroleum products has resulted in increased oil and gas activities in many countries. Conventional and unconventional oil and gas extraction, production, and transport lead to increased levels of petroleum‐derived polycyclic aromatic hydrocarbons (PAHs) in the environment. PAH exposure has profound effects on reproduction by affecting pathways involved in placental trophoblast cell function and impairing normal placental development and function—key contributors to reproductive success. However, other components found in petroleum and wastewaters from oil and gas extraction, including the sulfur‐containing heterocyclic aromatic compounds such as dibenzothiophene (DBT) and its alkylated derivatives, may also impact reproductive success. The goal of this study was to examine the effect of exposure to DBT, a compound commonly detected in the environment, and one of its alkylated analogues, 2,4,7‐trimethyldibenzothiophene (2,4,7‐DBT), on steroidogenic and angiogenic pathways critical for mammalian development in placental trophoblast cells (HTR‐8/SVneo cells). 2,4,7‐DBT but not DBT increased estradiol output in association with increased tube‐like formation (surrogate for angiogenesis). These changes in angiogenesis did not appear to be related to altered expression of the key placental angiogenic gene targets (ANGPTL4, VEGFA, and PGF). Neither compound showed a concentration related effect on progesterone synthesis or its receptor expression. Our results suggest that 2,4,7‐DBT can disrupt key pathways important for placental trophoblast function and highlight the importance of determining the impact of exposure to both parent and alkylated compounds. Further, these data suggest that exposure to sulfur‐containing heterocyclic aromatic compounds may lead to placental dysfunction and impact reproductive success at environmentally relevant levels.

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“…However, it is only in recent years, the cardiovascular toxicity of BaP attracted considerable attention. Currently, as an independent risk factor for CVDs, BaP has been found to be closely related to CVDs, including AS, HTN and AAA, and shows multiple kinds of vascular toxicity ( 10 , 11 , 13 , 42 ). Preclinical studies have found that BaP exposure is correlated with oxidative stress and vascular toxicity.…”

Section: Vascular Toxicity Effects and Underlying Mechanism Of Bapmentioning

confidence: 99%

Benzo(a)pyrene and cardiovascular diseases: An overview of pre-clinical studies focused on the underlying molecular mechanism

et al. 2022

Front. Nutr.

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Benzo(a)pyrene (BaP) is a highly toxic and carcinogenic polycyclic aromatic hydrocarbon (PAH) whose toxicological effects in the vessel-wall cells have been recognized. Many lines of evidence suggest that tobacco smoking and foodborne BaP exposure play a pivotal role in the dysfunctions of vessel-wall cells, such as vascular endothelial cell and vascular smooth muscle cells, which contribute to the formation and worsening of cardiovascular diseases (CVDs). To clarify the underlying molecular mechanism of BaP-evoked CVDs, the present study mainly focused on both cellular and animal reports whose keywords include BaP and atherosclerosis, abdominal aortic aneurysm, hypertension, or myocardial injury. This review demonstrated the aryl hydrocarbon receptor (AhR) and its relative signal transduction pathway exert a dominant role in the oxidative stress, inflammation response, and genetic toxicity of vessel-wall cells. Furthermore, antagonists and synergists of BaP are also discussed to better understand its mechanism of action on toxic pathways.

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Exposure to Benzo[a]pyrene impairs the corpus luteum vascular network in rats during early pregnancy

Cited by 15 publications

References 47 publications

High-Fat Diet-Induced Obesity Primes Impaired Fatty Acid β-Oxidation and Consequent Ovarian Dysfunction During Early Pregnancy

High-Fat Diet-Induced Obesity Primes Impaired Fatty Acid β-Oxidation and Consequent Ovarian Dysfunction During Early Pregnancy

Effects of dibenzothiophene, a sulfur‐containing heterocyclic aromatic hydrocarbon, and its alkylated congener, 2,4,7‐trimethyldibenzothiophene, on placental trophoblast cell function

Benzo(a)pyrene and cardiovascular diseases: An overview of pre-clinical studies focused on the underlying molecular mechanism

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