Ambient BTEX exposure and mid-pregnancy inflammatory biomarkers in pregnant African American women

Cassidy‐Bushrow, Andrea E.; Burmeister, Charlotte; Birbeck, Johnna A.; Chen, Yalei; Lamerato, Lois; Lemke, Lawrence D.; Li, Jia; Mor, Gil; O'Leary, B. F.; Peters, Rosalind M.; Reiners, John J.; Sperone, F. Gianluca; Westrick, Judy A.; Wiewiora, Evan; Straughen, Jennifer K.

doi:10.1016/j.jri.2021.103305

Cited by 25 publications

(11 citation statements)

References 45 publications

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“…Transcriptomic changes of 1 ppm benzene exposure were also related to the perturbation of the immune system during embryogenesis. Previous studies found benzene can dysregulate the cytokine network in vitro and in vivo, potentially through alteration of gene expression, or direct damage of hematopoietic progenitor cells [ 65 , 66 , 67 ]. In our study, one of the top networks is the crosstalk between PI3k/Akt signaling and PLTP modulation, which is implicated with the alteration of immune cell trafficking and inflammatory activation.…”

Section: Discussionmentioning

confidence: 99%

Evaluating Phenotypic and Transcriptomic Responses Induced by Low-Level VOCs in Zebrafish: Benzene as an Example

Blount

Haimbaugh

et al. 2022

Toxics

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Urban environments are plagued by complex mixtures of anthropogenic volatile organic compounds (VOCs), such as mixtures of benzene, toluene, ethylene, and xylene (BTEX). Sources of BTEX that drive human exposure include vehicle exhaust, industrial emissions, off-gassing of building material, as well as oil spillage and leakage. Among the BTEX mixture, benzene is the most volatile compound and has been linked to numerous adverse health outcomes. However, few studies have focused on the effects of low-level benzene on exposure during early development, which is a susceptible window when hematological, immune, metabolic, and detoxification systems are immature. In this study, we used zebrafish to conduct a VOC exposure model and evaluated phenotypic and transcriptomic responses following 0.1 and 1 ppm benzene exposure during the first five days of embryogenesis (n = 740 per treatment). The benzene body burden was 2 mg/kg in 1 ppm-exposed larval zebrafish pools and under the detection limit in 0.1 ppm-exposed fish. No observable phenotypic changes were found in both larvae except for significant skeletal deformities in 0.1 ppm-exposed fish (p = 0.01) compared with unexposed fish. Based on transcriptomic responses, 1 ppm benzene dysregulated genes that were implicated with the development of hematological system, and the regulation of oxidative stress response, fatty acid metabolism, immune system, and inflammatory response, including apob, nfkbiaa, serpinf1, foxa1, cyp2k6, and cyp2n13 from the cytochrome P450 gene family. Key genes including pik3c2b, pltp, and chia.2 were differentially expressed in both 1 and 0.1 ppm exposures. However, fewer transcriptomic changes were induced by 0.1 ppm compared with 1 ppm. Future studies are needed to determine if these transcriptomic responses during embryogenesis have long-term consequences at levels equal to or lower than 1 ppm.

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Section: Discussionmentioning

confidence: 99%

Evaluating Phenotypic and Transcriptomic Responses Induced by Low-Level VOCs in Zebrafish: Benzene as an Example

Blount

Haimbaugh

et al. 2022

Toxics

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“…This study focused on ambient exposure to BTEX (benzene, toluene, ethylbenzene, and xylene) and measured maternal inflammatory markers during the second trimester. A positive association was found between the levels of BTEX exposure and inflammatory cytokines IL-1β and TNF-α ( 97 ). Maternal exposure to benzene during pregnancy was found to be associated with low birth weight and head circumference ( 98 – 100 ).…”

Section: Mechanisms Linking Hypothalamic Metabolic Programming and Po...mentioning

confidence: 99%

“…Maternal inflammation and maternal immune activation (MIA) are known to be harmful to a developing fetus (44,(92)(93)(94)(95)(96). A recent study indicates that exposure of pregnant African American women to air pollution was associated with inflammation in the mothers by mid-pregnancy (97). This study focused on ambient exposure to BTEX (benzene, toluene, ethylbenzene, and xylene) and measured maternal inflammatory markers during the second trimester.…”

Section: Mechanisms Linking Hypothalamic Metabolic Programming and Po...mentioning

confidence: 99%

Prenatal Pollutant Exposures and Hypothalamic Development: Early Life Disruption of Metabolic Programming

et al. 2022

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Environmental contaminants in ambient air pollution pose a serious risk to long-term metabolic health. Strong evidence shows that prenatal exposure to pollutants can significantly increase the risk of Type II Diabetes (T2DM) in children and all ethnicities, even without the prevalence of obesity. The central nervous system (CNS) is critical in regulating whole-body metabolism. Within the CNS, the hypothalamus lies at the intersection of the neuroendocrine and autonomic systems and is primarily responsible for the regulation of energy homeostasis and satiety signals. The hypothalamus is particularly sensitive to insults during early neurodevelopmental periods and may be susceptible to alterations in the formation of neural metabolic circuitry. Although the precise molecular mechanism is not yet defined, alterations in hypothalamic developmental circuits may represent a leading cause of impaired metabolic programming. In this review, we present the current knowledge on the links between prenatal pollutant exposure and the hypothalamic programming of metabolism.

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“…Recent epidemiological studies have highlighted the association of VOC exposure and particularly benzene, one of the main volatile organic compounds (VOCs) in ambient air, with increased risk for gestational diabetes mellitus (GDM) (4). Indeed, increased offspring risk for cardiovascular and metabolic disease later in life has also been described in the context of the altered maternal environment, such as GDM, obesity, and exposure to environmental toxic compounds during pregnancy (5)(6)(7). In support, we have recently shown that gestational exposure to benzene at the levels relevant to cigarette smoking, induces deleterious effects on energy homeostasis, hyperglycemia, and insulin resistance in adult offspring (8).…”

Section: Introductionmentioning

confidence: 99%

Prenatal benzene exposure alters offspring hypothalamic development predisposing to metabolic disease in later life

Koshko

Scofield

Debarba

et al. 2023

Preprint

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The hypothalamus is essential in the regulation of metabolism, notably during critical windows of development. An abnormal hormonal and inflammatory milieu during development can trigger persistent changes in the function of hypothalamic circuits, leading to long-lasting effects on the body’s energy homeostasis and metabolism. We recently demonstrated that gestational exposure to benzene at smoking levels induces severe metabolic dysregulation in the offspring. Given the central role of the hypothalamus in metabolic control, we hypothesized that prenatal exposure to benzene impacts hypothalamic development, contributing to the adverse metabolic effects in the offspring. C57BL/6JB dams were exposed to benzene in the inhalation chambers exclusively during pregnancy (from E0.5 to E19). The transcriptome analysis of the offspring hypothalamus at postnatal day 21 (P21) revealed changes in genes related to metabolic regulation, inflammation, and neurodevelopment exclusively in benzene-exposed male offspring. Moreover, the hypothalamus of prenatally benzene-exposed male offspring displayed alterations in orexigenic and anorexigenic projections, impairments in leptin signaling, and increased microgliosis. Additional exposure to benzene during lactation did not promote further microgliosis or astrogliosis in the offspring, while the high-fat diet (HFD) challenge in adulthood exacerbated glucose metabolism and hypothalamic inflammation in benzene-exposed offspring of both sexes. These findings reveal the persistent impact of prenatal benzene exposure on hypothalamic circuits and neuroinflammation, predisposing the offspring to long-lasting metabolic health conditions.

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Ambient BTEX exposure and mid-pregnancy inflammatory biomarkers in pregnant African American women

Cited by 25 publications

References 45 publications

Evaluating Phenotypic and Transcriptomic Responses Induced by Low-Level VOCs in Zebrafish: Benzene as an Example

Evaluating Phenotypic and Transcriptomic Responses Induced by Low-Level VOCs in Zebrafish: Benzene as an Example

Prenatal Pollutant Exposures and Hypothalamic Development: Early Life Disruption of Metabolic Programming

Prenatal benzene exposure alters offspring hypothalamic development predisposing to metabolic disease in later life

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