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Endoplasmic reticulum stress-induced NLRP3 inflammasome activation as a novel mechanism of polystyrene microplastics (PS-MPs)-induced pulmonary inflammation in chickens

内质网应激诱导的NLRP3炎性体激活是聚苯乙烯微塑料(PS-MPs)诱导的鸡肺部炎症的新机制

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Abstract

Microplastics (MPs) have attracted growing attention worldwide as an increasingly prevalent environmental pollutant. In addition, chicken meat is currently the most widely consumed kind of poultry in the global market. Consumer demand for chicken is on the rise both at home and abroad. As a result, the safety of chicken raising has also received significant attention. The lungs play an essential role in the physiological activities of chickens, and they are also the most vulnerable organs. Lung injury is difficult to repair after the accumulation of contaminants, and the mortality rate is high, which brings huge economic losses to farmers. The research on the toxicity of MPs has mainly focused on the marine ecosystem, while the mechanisms of toxicity and lung damage in chickens have been poorly studied. Thus, this study explored the effects of exposure to polystyrene microplastics (PS-MPs) at various concentrations for 42 d on chicken lungs. PS-MPs could cause lung pathologies and ultrastructural abnormalities, such as endoplasmic reticulum (ER) swelling, inflammatory cell infiltration, chromatin agglutination, and plasma membrane rupture. Simultaneously, PS-MPs increased the expression of genes related to the heat shock protein family (Hsp60, Hsp70, and Hsp90), ER stress signaling (activating transcription factor 6 (ATF6),ATF4, protein kinase RNA-like ER kinase (PERK), and eukaryotic translation initiation factor 2 subunit a (eIF2α)), pyroptosis-related genes (NOD-, LRR- and pyrin domain-containing protein 3 (NLRP3), apoptosis-associated speck-like protein containing a caspase recruitment domain (ASC), interleukin-1β (IL-1β), cysteinyl aspartate-specific proteinase 1 (Caspase1), and gasdermin-D (GSDMD)), and the inflammatory signaling pathway (nuclear factor-κB (NF-κB), inducible nitric oxide synthase (iNOS), and cyclooxygenase-2 (COX-2)). The above results showed that PS-MP exposure could result in lung stress, ER stress, pyroptosis, and inflammation in broilers. Our findings provide new scientific clues for further research on the mechanisms of physical health and toxicology regarding MPs.

摘要

作为一种普遍的环境污染物,微塑料(MPs)已引起全球关注。鸡作为目前全球消费最广泛的家禽,随着消费者的需求不断上升,其饲养的安全性受到极大关注。肺是鸡生理活动中的重要器官,也是最脆弱 的器官。因污染物积累导致的鸡的肺损伤难以修复,死亡率较高,给饲养者带来巨大经济损失。目前,对MPs毒性研究主要集中在海洋生态系统,而对鸡的毒性和肺损伤机制的研究相对较少。本研究主要探讨了 不同浓度的聚苯乙烯微塑料(PS-MPs)暴露42天对鸡肺的影响。结果显示,PS-MPs可引起鸡肺病理和超微结构的异常,具体包括内质网肿胀、炎症细胞浸润、染色质凝集和质膜破裂。同时,PS-MPs可增加以下 相关基因的表达:热休克蛋白(Hsp60、Hsp70、Hsp90)、内质网应激信号通路(ATF6、ATF4、PERK、eIF2α)、焦亡相关基因(NLRP3、ASC、IL-1β、Caspase1、GSDMD)和炎症通路(NF-κB、iNOS、COX-2)。 综上所述,PS-MPs暴露可导致肉鸡肺应激、内质网应激、焦亡和炎症反应,为进一步研究MPs的生理健康和毒理学机制提供了新的科学线索。

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Data will be made available on request.

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Acknowledgments

This work was supported by the Key Projects of Natural Science Foundation of Heilongjiang Province of China (No. ZD2020C005).

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Hongmin LU performed the conceptualization, data curation, software, formal analysis, writing–original draft, and writing–review & editing. Tiantian GUO performed the conceptualization and software. Yue ZHANG contributed to the formal analysis and investigation. Dewang LIU performed the visualization. Lulu HOU contributed to the data curation, writing–review & editing, and software. Chengxue MA performed the validation, visualization, and writing–review & editing. Mingwei XING contributed to the data curation, validation, resources, funding acquisition, and project administration. All authors have read and agreed the final version of the manuscript. The authors have full access to all the data in the study and take responsibility for the integrity and security of the data.

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Correspondence to Chengxue Ma  (马成学) or Mingwei Xing  (邢明伟).

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Hongmin LU, Tiantian GUO, Yue ZHANG, Dewang LIU, Lulu HOU, Chengxue MA, and Mingwei XING declare that they have no conflict of interest.

All institutional and national guidelines for the care and use of laboratory animals were followed. The Experimental Animal Committee of Northeastern Forestry University approved the study (Approval No. UT-31; June 20, 2014).

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Lu, H., Guo, T., Zhang, Y. et al. Endoplasmic reticulum stress-induced NLRP3 inflammasome activation as a novel mechanism of polystyrene microplastics (PS-MPs)-induced pulmonary inflammation in chickens. J. Zhejiang Univ. Sci. B 25, 233–243 (2024). https://doi.org/10.1631/jzus.B2300409

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