Prenatal exposure to PM2.5 led to impaired respiratory function in adult mice

Jushan Zhang; Haoxiang Cheng; Kateryna Yevdokimova; Yujie Zhu; Shuanshuan Xie; Rui Liu; Pengbo Zhao; Guohao Li; Lu Jiang; Xiaowen Shao; Zhongyang Zhang; Jia Chen; Linda Rogers; Ke Hao

Ecotoxicology and Environmental Safety (Oct 2024)

Prenatal exposure to PM2.5 led to impaired respiratory function in adult mice

Jushan Zhang,
Haoxiang Cheng,
Kateryna Yevdokimova,
Yujie Zhu,
Shuanshuan Xie,
Rui Liu,
Pengbo Zhao,
Guohao Li,
Lu Jiang,
Xiaowen Shao,
Zhongyang Zhang,
Jia Chen,
Linda Rogers,
Ke Hao

Affiliations

Jushan Zhang: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China; College of Environmental Science and Engineering, Tongji University, Shanghai, China; State Key Laboratory of Pollution Control and Resource Reuse (Tongji University), China
Haoxiang Cheng: Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, New York, USA
Kateryna Yevdokimova: Division of Pulmonary, Critical Care and Sleep Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA
Yujie Zhu: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China
Shuanshuan Xie: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China
Rui Liu: College of Environmental Science and Engineering, Tongji University, Shanghai, China
Pengbo Zhao: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China; College of Environmental Science and Engineering, Tongji University, Shanghai, China
Guohao Li: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China; College of Environmental Science and Engineering, Tongji University, Shanghai, China
Lu Jiang: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China; College of Environmental Science and Engineering, Tongji University, Shanghai, China
Xiaowen Shao: Department of Obstetrics and Gynecology, Shanghai Tenth People's Hospital, Tongji University, Shanghai, China
Zhongyang Zhang: Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, New York, USA
Jia Chen: Environmental Medicine and Public Health, Icahn School of Medicine at Mount Sinai, New York, New York, USA
Linda Rogers: Division of Pulmonary, Critical Care and Sleep Medicine, Icahn School of Medicine at Mount Sinai, New York, New York, USA
Ke Hao: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China; College of Environmental Science and Engineering, Tongji University, Shanghai, China; State Key Laboratory of Pollution Control and Resource Reuse (Tongji University), China; Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, New York, USA; Corresponding auther at: Department of Respiratory Medicine, Shanghai Tenth People’s Hospital, Tongji University, Shanghai, China.

Journal volume & issue: Vol. 285
p. 117052

Abstract

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Background: PM2.5 is a complex mixture, with water-soluble inorganic ions (WSII), mainly NH4+, SO42−, and NO3−, constituting major components. Early-life PM2.5 exposure has been shown to induce adverse health consequence but it is difficult to determine whether such an effect occurs prenatally (preconception, gestational) or postnatally in human studies. Methods: Four groups of C57BL/6 J mice were assigned to four exposure conditions: PM2.5 NO3−, PM2.5 SO42−, PM2.5 NH4+ and clean air, and exposure started at 4 weeks old. At 8 weeks old, mice bred within group. The exposure continued during gestation. After delivery, both the maternal and F1 mice (offspring) were kept in clean air without exposure to PM2.5. Respiratory function and pulmonary pathology were assessed in offspring mice at 8 weeks of age. In parallel, placenta tissue was collected for transcriptome profiling and mechanistic investigation. Results: F1 mice in PM2.5 NH4+, SO42- and NO3− groups had 32.2 % (p=6.0e-10), 30.3 % (p=3.8e-10) and 16.9 % (p=5.7e-8) lower peak expiratory flow (PEF) than the clean air group. Importantly, the exposure-induced lung function decline was greater in male than female offspring. Moreover, exposure to PM2.5 WSII before conception and during gestation was linked to increased airway wall thickness and elevated pulmonary neutrophil and macrophage counts in the offspring mice. At the molecular level, the exposure significantly disrupted gene expression in the placenta, affecting crucial functional pathways related to sex hormone response and inflammation. Conclusions: PM2.5 WSII exposure during preconception and gestational period alone without post-natal exposure substantially impacted offspring’s respiratory function as measured at adolescent age. Our results support the paradigm of fetal origin of environmentally associated chronic lung disease and highlight sex differences in susceptibility to air pollution exposure.

Published in Ecotoxicology and Environmental Safety

ISSN: 0147-6513 (Print); 1090-2414 (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Technology: Environmental technology. Sanitary engineering: Environmental pollution; Geography. Anthropology. Recreation: Environmental sciences
Website: https://www.journals.elsevier.com/ecotoxicology-and-environmental-safety

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