The impact of polystyrene microplastics on cardiomyocytes pyroptosis through NLRP3/Caspase-1 signaling pathway and oxidative stress in Wistar rats.
cardiotoxicity
inflammatory stimuli
microplastics
oxidative stress
pyroptosis
Journal
Environmental toxicology
ISSN: 1522-7278
Titre abrégé: Environ Toxicol
Pays: United States
ID NLM: 100885357
Informations de publication
Date de publication:
May 2021
May 2021
Historique:
received:
24
11
2020
accepted:
27
12
2020
pubmed:
7
1
2021
medline:
28
4
2021
entrez:
6
1
2021
Statut:
ppublish
Résumé
The extensive existing of microplastics (MPs) in the ecosystem have increased considerable attention concerning their potential adverse effects, the toxicities and the underlying mechanism of MPs are still scarce. To explore the effect of MPs on cardiac tissue in Wistar rats and unravel the mechanism of pyroptosis and oxidative stress in the process of cardiomyocytes injury, 32 male Wister rats were divided into control group and three model groups, which were exposed to 0.5 mm PS MPs at 0.5, 5 and 50 mg/L for 90 days. Results revealed that MPs could damage cardiac structure and function with impaired mitochondria integrity, as well as increased levels of creatine kinase-MB and cardiac troponinI (cTnI). Moreover, MPs administration triggered oxidative stress as indicated by increased levels of malondialdehyde and decreased activity of superoxide dismutase, glutathione peroxidase and catalase. Treatment with MPs resulted in apoptosis and pyroptosis as evidenced by increasing expressions of interleukin (IL)-1β, IL-18. Additionally, MPs were shown to induce the NOD-like receptor protein 3 inflammasomes activation in cardiac tissue, enabling activation of Caspase-1-dependent signaling pathway induced by inflammatory stimuli resulting from oxidative stress. In summary, these results illustrated that pyroptosis played a vital role in polystyrene MPs-induced cardiotoxicity, which might be helpful to understand the mechanism of cardiac dysfunction and induced by MPs.
Substances chimiques
Microplastics
0
NLR Family, Pyrin Domain-Containing 3 Protein
0
Nlrp3 protein, rat
0
Plastics
0
Polystyrenes
0
Caspase 1
EC 3.4.22.36
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
935-944Subventions
Organisme : National Natural Science Foundation of China
Informations de copyright
© 2021 Wiley Periodicals LLC.
Références
Phillips MB, Bonner TH. Occurrence and amount of microplastic ingested by fishes in watersheds of the Gulf of Mexico. Mar Pollut Bull. 2015;100(1):264-269.
Bouwmeester H, Hollman PC, Peters RJ. Potential health impact of environmentally released micro- and Nanoplastics in the human food production chain: experiences from Nanotoxicology. Environ Sci Technol. 2015;49(15):8932-8947.
Gigault J, Halle AT, Baudrimont M, et al. Current opinion: what is a nanoplastic? Environ Pollut. 2018;235:1030-1034.
Andrady AL. Microplastics in the marine environment. Mar Pollut Bull. 2011;62(8):1596-1605.
Chang X, Xue Y, Li J, Zou L, Tang M. Potential health impact of environmental micro- and nanoplastics pollution. J Appl Toxicol. 2020;40(1):4-15.
Brennecke D, Ferreira EC, Costa TM, et al. Ingested microplastics (>100 mum) are translocated to organs of the tropical fiddler crab Uca rapax. Mar Pollut Bull. 2015;96(1-2):491-495.
Ivar do Sul JA, Costa MF. The present and future of microplastic pollution in the marine environment. Environmental Pollution. 2014;185:352-364.
Li B, Ding Y, Cheng X, et al. Polyethylene microplastics affect the distribution of gut microbiota and inflammation development in mice. Chemosphere. 2020;244:125492.
Fackelmann G, Sommer S. Microplastics and the gut microbiome: how chronically exposed species may suffer from gut dysbiosis. Mar Pollut Bull. 2019;143:193-203.
Jin H, Ma T, Sha X, et al. Polystyrene microplastics induced male reproductive toxicity in mice. J Hazard Mater. 2021;401:123430.
Sistino JJ. Epidemiology of cardiovascular disease in the last decade: treatment options and implications for perfusion in the 21st century. Perfusion. 2003;18(2):73-77.
Heil B, Tang WH. Biomarkers: their potential in the diagnosis and treatment of heart failure. Cleve Clin J Med. 2015;82(2):S28-S35.
Browne MA, Dissanayake A, Galloway TS, Lowe DM, Thompson RC. Ingested microscopic plastic translocates to the circulatory system of the mussel, Mytilus edulis (L). Environ Sci Technol. 2008;42(13):5026-5031.
Mostovenko E, Young T, Muldoon PP, et al. Nanoparticle exposure driven circulating bioactive peptidome causes systemic inflammation and vascular dysfunction. Part Fibre Toxicol. 2019;16(1):20.
Yang H, Xiong H, Mi K, Xue W, Wei W, Zhang Y. Toxicity comparison of nano-sized and micron-sized microplastics to goldfish Carassius auratus larvae. J Hazard Mater. 2020;388:122058.
Fischer R, Maier O. Interrelation of oxidative stress and inflammation in neurodegenerative disease: role of TNF. Oxid Med Cell Longev. 2015;2015:1-18.
Li Y, Ren X, Lio C, et al. A chlorogenic acid-phospholipid complex ameliorates post-myocardial infarction inflammatory response mediated by mitochondrial reactive oxygen species in SAMP8 mice. Pharmacol Res. 2018;130:110-122.
Xie X, Deng T, Duan J, Xie J, Yuan J, Chen M. Exposure to polystyrene microplastics causes reproductive toxicity through oxidative stress and activation of the p38 MAPK signaling pathway. Ecotoxicol Environ Saf. 2020;190:110133.
Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun. 2005;73(4):1907-1916.
Miao EA, Rajan JV, Aderem A. Caspase-1-induced pyroptotic cell death. Immunol Rev. 2011;243(1):206-214.
Li H, Nookala S, Re F. Aluminum hydroxide adjuvants activate caspase-1 and induce IL-1beta and IL-18 release. J Immunol. 2007;178(8):5271-5276.
Xin W, Wang Q, Zhang D, Wang C. A new mechanism of inhibition of IL-1beta secretion by celastrol through the NLRP3 inflammasome pathway. Eur J Pharmacol. 2017;814:240-247.
Dowling JK, O'Neill LA. Biochemical regulation of the inflammasome. Crit Rev Biochem Mol Biol. 2012;47(5):424-443.
Teng JF, Mei QB, Zhou XG, et al. Polyphyllin VI induces Caspase-1-mediated Pyroptosis via the induction of ROS/NF-kappaB/NLRP3/GSDMD signal Axis in non-small cell lung cancer. Cancers (Basel). 2020;12(1):193.
AshaRani PV, Low Kah Mun G, Hande MP, et al. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano. 2009;3(2):279-290.
Bhabra G, Sood A, Fisher B, et al. Nanoparticles can cause DNA damage across a cellular barrier. Nat Nanotechnol. 2009;4(12):876-883.
Li Z, Zhu S, Liu Q, et al. Polystyrene microplastics cause cardiac fibrosis by activating Wnt/β-catenin signaling pathway and promoting cardiomyocyte apoptosis in rats. Environmental Pollution. 2020;265, 115025.
Mastro F, Guida P, Scrascia G, et al. Cardiac troponin I and creatine kinase-MB release after different cardiac surgeries. J Cardiovasc Med (Hagerstown). 2015;16(6):456-464.
Anbumani S, Kakkar P. Ecotoxicological effects of microplastics on biota: a review. Environ Sci Pollut Res Int. 2018;25(15):14373-14396.
Kim JA, Montagnani M, Koh KK, et al. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation. 2006;113(15):1888-1904.
Sorriento D, Iaccarino G. Inflammation and cardiovascular diseases: the Most recent findings. Int J Mol Sci. 2019;20(16):3879.
Chang W, Lin J, Dong J, Li D. Pyroptosis: an inflammatory cell death implicates in atherosclerosis. Med Hypotheses. 2013;81(3):484-486.
He WT, Wan H, Hu L, et al. Gasdermin D is an executor of pyroptosis and required for interleukin-1beta secretion. Cell Res. 2015;25(12):1285-1298.
Nakajima S, Kitamura M. Bidirectional regulation of NF-kappaB by reactive oxygen species: a role of unfolded protein response. Free Radic Biol Med. 2013;65:162-174.
Mohan S, Koyoma K, Thangasamy A, Nakano H, Glickman RD, Mohan N. Low shear stress preferentially enhances IKK activity through selective sources of ROS for persistent activation of NF-kappaB in endothelial cells. Am J Physiol Cell Physiol. 2007;292(1):C362-C371.
von Moos N, Burkhardt-Holm P, Kohler A. Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Environ Sci Technol. 2012;46(20):11327-11335.
Peeters PM, Eurlings IMJ, Perkins TN, et al. Silica-induced NLRP3 inflammasome activation in vitro and in rat lungs. Part Fibre Toxicol. 2014;11:58.
Zheng R, Tao L, Jian H, et al. NLRP3 inflammasome activation and lung fibrosis caused by airborne fine particulate matter. Ecotoxicol Environ Saf. 2018;163:612-619.
Garcia JA, Volt H, Venegas C, et al. Disruption of the NF-kappaB/NLRP3 connection by melatonin requires retinoid-related orphan receptor-alpha and blocks the septic response in mice. FASEB J. 2015;29(9):3863-3875.
Ozaki E, Campbell M, Doyle SL. Targeting the NLRP3 inflammasome in chronic inflammatory diseases: current perspectives. J Inflamm Res. 2015;8:15-27.
Franchi L, Eigenbrod T, Munoz-Planillo R, et al. Cytosolic double-stranded RNA activates the NLRP3 inflammasome via MAVS-induced membrane permeabilization and K+ efflux. J Immunol. 2014;193(8):4214-4222.
Rabeony H, Pohin M, Vasseur P, et al. IMQ-induced skin inflammation in mice is dependent on IL-1R1 and MyD88 signaling but independent of the NLRP3 inflammasome. Eur J Immunol. 2015;45(10):2847-2857.
Chen H, Lu Y, Cao Z, et al. Cadmium induces NLRP3 inflammasome-dependent pyroptosis in vascular endothelial cells. Toxicol Lett. 2016;246:7-16.
Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes. Cell. 2014;157(5):1013-1022.
He Y, Hara H, Nunez G. Mechanism and regulation of NLRP3 Inflammasome activation. Trends Biochem Sci. 2016;41(12):1012-1021.
de Rivero Vaccari JP, Lotocki G, Alonso OF, et al. Therapeutic neutralization of the NLRP1 inflammasome reduces the innate immune response and improves histopathology after traumatic brain injury. J Cereb Blood Flow Metab. 2009;29(7):1251-1261.
Youm YH, Nguyen KY, Grant RW, et al. The ketone metabolite beta-hydroxybutyrate blocks NLRP3 inflammasome-mediated inflammatory disease. Nat Med. 2015;21(3):263-269.
Zhang X, Luan J, Chen W, et al. Mesoporous silica nanoparticles induced hepatotoxicity via NLRP3 inflammasome activation and caspase-1-dependent pyroptosis. Nanoscale. 2018;10(19):9141-9152.
Lei Q, Yi T, Chen C, NF-kappaB-Gasdermin D. (GSDMD) Axis couples oxidative stress and NACHT, LRR and PYD domains-containing protein 3 (NLRP3) Inflammasome-mediated Cardiomyocyte Pyroptosis following myocardial infarction. Med Sci Monit. 2018;24:6044-6052.
Shi J, Zhao Y, Wang K, et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature. 2015;526(7575):660-665.
Yang H, Lai H, Huang J, et al. Polystyrene microplastics decrease F-53B bioaccumulation but induce inflammatory stress in larval zebrafish. Chemosphere. 2020;255:127040.