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Journal of Zhejiang University SCIENCE B 2024 Vol.25 No.3 P.233-243

http://doi.org/10.1631/jzus.B2300409


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


Author(s):  Hongmin LU, Tiantian GUO, Yue ZHANG, Dewang LIU, Lulu HOU, Chengxue MA, Mingwei XING

Affiliation(s):  College of Wildlife and Protected Area, Northeast Forestry University, Harbin 150040, China

Corresponding email(s):   mch007@vip.163.com, xingmingwei@nefu.edu.cn

Key Words:  Polystyrene microplastics, Endoplasmic reticulum stress, Lung, NLRP3 inflammasome, Inflammation


Hongmin LU, Tiantian GUO, Yue ZHANG, Dewang LIU, Lulu HOU, Chengxue MA, Mingwei XING. Endoplasmic reticulum stress-induced NLRP3 inflammasome activation as a novel mechanism of polystyrene microplastics (PS-MPs)-induced pulmonary inflammation in chickens[J]. Journal of Zhejiang University Science B, 2024, 25(3): 233-243.

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author="Hongmin LU, Tiantian GUO, Yue ZHANG, Dewang LIU, Lulu HOU, Chengxue MA, Mingwei XING",
journal="Journal of Zhejiang University Science B",
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pages="233-243",
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%T Endoplasmic reticulum stress-induced NLRP3 inflammasome activation as a novel mechanism of polystyrene microplastics (PS-MPs)-induced pulmonary inflammation in chickens
%A Hongmin LU
%A Tiantian GUO
%A Yue ZHANG
%A Dewang LIU
%A Lulu HOU
%A Chengxue MA
%A Mingwei XING
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T1 - Endoplasmic reticulum stress-induced NLRP3 inflammasome activation as a novel mechanism of polystyrene microplastics (PS-MPs)-induced pulmonary inflammation in chickens
A1 - Hongmin LU
A1 - Tiantian GUO
A1 - Yue ZHANG
A1 - Dewang LIU
A1 - Lulu HOU
A1 - Chengxue MA
A1 - Mingwei XING
J0 - Journal of Zhejiang University Science B
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DOI - 10.1631/jzus.B2300409


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 α (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.

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

陆洪敏,郭甜甜,张悦,刘德旺,侯露露,马成学,邢明伟
东北林业大学野生动物与自然保护地学院,中国哈尔滨市,150040
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(Hsp60Hsp70Hsp90)、内质网应激信号通路(ATF6ATF4PERKeIF2α)、焦亡相关基因(NLRP3ASCIL-1βCaspase1GSDMD)和炎症通路(NF-κBiNOSCOX-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。

关键词:聚苯乙烯微塑料;内质网应激;肺;NLRP3炎症小体;炎症

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]AkdoganZ, GuvenB, 2019. Microplastics in the environment: a critical review of current understanding and identification of future research needs. Environ Pollut, 254:113011.

[2]AutaHS, EmenikeCU, FauziahSH, 2017. Distribution and importance of microplastics in the marine environment: a review of the sources, fate, effects, and potential solutions. Environ Int, 102:165-176.

[3]Abd-ElmawlaMA, GHAIADHR, GAD ES, et al., 2023. Suppression of NLRP3 inflammasome by ivermectin ameliorates bleomycin-induced pulmonary fibrosis. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 24(8):723-733.

[4]ChiQR, HuXY, LiuZY, et al., 2021. H2S exposure induces cell death in the broiler thymus via the ROS-initiated JNK/MST1/FOXO1 pathway. Ecotoxicol Environ Saf, 222:112488.

[5]DudejaV, VickersSM, SalujaAK, 2009. The role of heat shock proteins in gastrointestinal diseases. Gut, 58(7):1000-1009.

[6]GongZG, ZhaoY, WangZY, et al., 2022. Epigenetic regulator BRD4 is involved in cadmium-induced acute kidney injury via contributing to lysosomal dysfunction, autophagy blockade and oxidative stress. J Hazard Mater, 423:127110.

[7]GongJ, WangXZ, WangT, et al., 2017. Molecular signal networks and regulating mechanisms of the unfolded protein response. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 18(1):1-14.

[8]HouBL, WangFY, LiuT, et al., 2021. Reproductive toxicity of polystyrene microplastics: in vivo experimental study on testicular toxicity in mice. J Hazard Mater, 405:124028.

[9]HouLL, WangDX, YinK, et al., 2022. Polystyrene microplastics induce apoptosis in chicken testis via crosstalk between NF-κB and Nrf2 pathways. Comp Biochem Physiol Part C Toxicol Pharmacol, 262:109444.

[10]HuangRX, HouLY, RuanZZ, et al., 2020. NLRP3 inflammasome mediates 2,‍5-hexanedione-induced neurotoxicity through regulation of macrophage infiltration in rats. Chem Biol Interact, 330:109232.

[11]ImranM, DasKR, NaikMM, 2019. Co-selection of multi-antibiotic resistance in bacterial pathogens in metal and microplastic contaminated environments: an emerging health threat. Chemosphere, 215:846-857.

[12]JeremiasI, KupattC, Martin-VillalbaA, et al., 2000. Involvement of CD95/Apo1/Fas in cell death after myocardial ischemia. Circulation, 102(8):915-920.

[13]JinYX, XiaJZ, PanZH, et al., 2018. Polystyrene microplastics induce microbiota dysbiosis and inflammation in the gut of adult zebrafish. Environ Pollut, 235:322-329.

[14]LernerAG, UptonJP, PraveenPVK, 2012. IRE1α induces thioredoxin-interacting protein to activate the NLRP3 inflammasome and promote programmed cell death under irremediable ER stress. Cell Metab, 16(2):250-264.

[15]LiJH, ZhangWY, ZhouP, et al., 2022. Selenium deficiency induced apoptosis via mitochondrial pathway caused by Oxidative Stress in porcine gastric tissues. Res Vet Sci, 144:142-148.

[16]LiL, 2003. The biochemistry and physiology of metallic fluoride: action, mechanism, and implications. Crit Rev Oral Biol Med, 14(2):100-114.

[17]LiN, WangW, JiangWY, et al., 2020. Cytosolic DNA-STING-NLRP3 axis is involved in murine acute lung injury induced by lipopolysaccharide. Clin Transl Med, 10(7):e228.

[18]LianCY, ChuBX, XiaWH, et al., 2023. Persistent activation of Nrf2 in a p62-dependent non-canonical manner aggravates lead-induced kidney injury by promoting apoptosis and inhibiting autophagy. J Adv Res, 46:87-100.

[19]LiuQ, DuPY, ZhuY, et al., 2022. Thioredoxin reductase 3 suppression promotes colitis and carcinogenesis via activating pyroptosis and necrosis. Cell Mol Life Sci,79(2):106.

[20]LuHM, SuH, LiuYC, et al., 2022. NLRP3 inflammasome is involved in the mechanism of the mitigative effect of lycopene on sulfamethoxazole-induced inflammatory damage in grass carp kidneys. Fish Shellfish Immunol, 123:348-357.

[21]MoJH, RuanSY, YangBC, et al., 2023. A novel defined risk signature of endoplasmic reticulum stress-related genes for predicting the prognosis and immune infiltration status of ovarian cancer. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 24(1):64-77.

[22]MooreCJ, 2008. Synthetic polymers in the marine environment: a rapidly increasing, long-term threat. Environ Res, 108(2):131-139.

[23]OslowskiCM, HaraT, O'Sullivan-MurphyB, et al., 2012. Thioredoxin-interacting protein mediates ER stress-induced β cell death through initiation of the inflammasome. Cell Metab, 16(2):265-273.

[24]Overley-AdamsonB, ArtlettCM, StephensC, et al., 2014. Targeting the unfolded protein response, XBP1, and the NLRP3 inflammasome in fibrosis and cancer. Cancer Biol Ther, 15(4):452-462.

[25]OyagbemiAA, AdejumobiOA, JarikreTA, et al., 2022. Clofibrate, a peroxisome proliferator-activated receptor-alpha (PPARα) agonist, and its molecular mechanisms of action against sodium fluoride-induced toxicity. Biol Trace Elem Res, 200(3):1220-1236.

[26]PengS, GaoJ, LiuW, et al., 2016. Andrographolide ameliorates OVA-induced lung injury in mice by suppressing ROS-mediated NF‍-‍κB signaling and NLRP3 inflammasome activation. Oncotarget, 7(49):80262-80274.

[27]QuW, DuGL, FengB, et al., 2019. Effects of oxidative stress on blood pressure and electrocardiogram findings in workers with occupational exposure to lead. J Int Med Res, 47(6):2461-2470.

[28]RuanJW, WangSJ, WangJB, 2020. Mechanism and regulation of pyroptosis-mediated in cancer cell death. Chem Biol Interact, 323:109052.

[29]ShiJJ, GaoWQ, ShaoF, 2017. Pyroptosis: gasdermin-mediated programmed necrotic cell death. Trends Biochem Sci, 42(4):245-254.

[30]ShiX, LiXJ, SunXY, et al., 2021. Pig lung fibrosis is active in the subacute CdCl2 exposure model and exerts cumulative toxicity through the M1/M2 imbalance. Ecotoxicol Environ Saf, 225:112757.

[31]SongC, ShiDM, ChangKW, et al., 2021. Sodium fluoride activates the extrinsic apoptosis via regulating NOX4/ROS-mediated p53/DR5 signaling pathway in lung cells both in vitro and in vivo. Free Radic Biol Med, 169:137-148.

[32]SunDD, ZhuH, AiL, et al., 2021. Mitochondrial fusion protein 2 regulates endoplasmic reticulum stress in preeclampsia. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 22(2):165-170.

[33]SunT, ZhanJF, LiF, et al., 2021a. Effect of microplastics on aquatic biota: a hormetic perspective. Environ Pollut, 285:117206.

[34]SunT, ZhanJF, LiF, et al., 2021b. Environmentally relevant concentrations of microplastics influence the locomotor activity of aquatic biota. J Hazard Mater, 414:125581.

[35]WangD, DuncanB, LiXZ, et al., 2020. The role of NLRP3 inflammasome in infection-related, immune-mediated and autoimmune skin diseases. J Dermatol Sci, 98(3):146-151.

[36]WangY, ZhaoHJ, LiuYC, et al., 2021. Environmentally relevant concentration of sulfamethoxazole-induced oxidative stress-cascaded damages in the intestine of grass carp and the therapeutic application of exogenous lycopene. Environ Pollut, 274:116597.

[37]WattsAJ, UrbinaMA, CorrS, et al., 2015. Ingestion of plastic microfibers by the crab Carcinus maenas and its effect on food consumption and energy balance. Environ Sci Technol, 49(24):14597-14604.

[38]WuH, GuoJM, YaoYJ, et al., 2022. Polystyrene nanoplastics induced cardiomyocyte apoptosis and myocardial inflammation in carp by promoting ROS production. Fish Shellfish Immunol, 125:1-8.

[39]XuS, MaJ, JiR, et al., 2020. Microplastics in aquatic environments: occurrence, accumulation, and biological effects. Sci Total Environ, 703:134699.

[40]YinK, WangDX, ZhaoHJ, et al., 2021. Microplastics pollution and risk assessment in water bodies of two nature reserves in Jilin Province: correlation analysis with the degree of human activity. Sci Total Environ, 799:149390.

[41]YinLY, ChenBJ, XiaB, et al., 2018. Polystyrene microplastics alter the behavior, energy reserve and nutritional composition of marine jacopever (Sebastes schlegelii). J Hazard Mater, 360:97-105.

[42]ZhangWY, SunXY, ShiX, et al., 2023. Subacute cadmium exposure induces necroptosis in swine lung via influencing Th1/Th2 balance. Biol Trace Elem Res, 201(1):220-228.

[43]ZhangY, YinK, WangDX, et al., 2022. Polystyrene microplastics-induced cardiotoxicity in chickens via the ROS-driven NF-‍κB-NLRP3-GSDMD and AMPK-PGC-‍1α axes. Sci Total Environ, 840:156727.

[44]ZhaoHJ, WangY, LiuYC, et al., 2021. ROS-induced hepatotoxicity under cypermethrin: involvement of the crosstalk between Nrf2/Keap1 and NF-κB/iκB-α pathways regulated by proteasome. Environ Sci Technol, 55(9):6171-6183.

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