Effect and Mechanism of Reactive Oxygen Species-mediated NOD-like Receptor Family Pyrin Domain-containing 3 Inflammasome Activation in Hepatic Alveolar Echinococcosis

Overview

Journal World J Gastroenterol

Publisher Baishideng Publishing Group

Specialty Gastroenterology

Date 2023 May 1

PMID 37122606

Authors

Cai-Song Chen

Yao-Gang Zhang

Hai-Jiu Wang

Hai-Ning Fan

Affiliations

Soon will be listed here.

Abstract

Background: The NOD-like receptor family pyrin domain-containing 3 (NLRP3) inflammasome is a significant component of the innate immune system that plays a vital role in the development of various parasitic diseases. However, its role in hepatic alveolar echinococcosis (HAE) remains unclear.

Aim: To investigate the NLRP3 inflammasome and its mechanism of activation in HAE.

Methods: We assessed the expression of NLRP3, caspase-1, interleukin (IL)-1β, and IL-18 in the marginal zone and corresponding normal liver of 60 patients with HAE. A rat model of HAE was employed to investigate the role of the NLRP3 inflammasome in the marginal zone of HAE. Transwell experiments were conducted to investigate the effect of () in stimulating Kupffer cells and hepatocytes. Furthermore, immunohistochemistry, Western blotting, and enzyme-linked immunosorbent assay were used to evaluate NLRP3, caspase-1, IL-1β, and IL-18 expression; flow cytometry was used to detect apoptosis and reactive oxygen species (ROS).

Results: NLRP3 inflammasome activation was significantly associated with ROS. Inhibition of ROS production decreased NLRP3-caspase-1-IL-1β pathway activation and mitigated hepatocyte damage and inflammation.

Conclusion: induces hepatocyte damage and inflammation by activating the ROS-mediated NLRP3-caspase-1-IL-1β pathway in Kupffer cells, indicating that ROS may serve as a potential target for the treatment of HAE.

References

Xu X, Gao C, Ye H, Wang Z, Wang Z, Zhou Y . Diagnosis and treatment of a case of hepatic mixed echinococcosis infection combined with distant organ metastasis. J Int Med Res. 2019; 48(2):300060519851651. PMC: 7574518. DOI: 10.1177/0300060519851651. View

Dey N, Sinha M, Gupta S, Gonzalez M, Fang R, Endsley J . Caspase-1/ASC inflammasome-mediated activation of IL-1β-ROS-NF-κB pathway for control of Trypanosoma cruzi replication and survival is dispensable in NLRP3-/- macrophages. PLoS One. 2014; 9(11):e111539. PMC: 4221042. DOI: 10.1371/journal.pone.0111539. View

Martinon F, Burns K, Tschopp J . The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell. 2002; 10(2):417-26. DOI: 10.1016/s1097-2765(02)00599-3. View

Xie W, Ding J, Xie X, Yang X, Wu X, Chen Z . Hepatitis B virus X protein promotes liver cell pyroptosis under oxidative stress through NLRP3 inflammasome activation. Inflamm Res. 2020; 69(7):683-696. PMC: 7261280. DOI: 10.1007/s00011-020-01351-z. View

Kellner M, Noonepalle S, Lu Q, Srivastava A, Zemskov E, Black S . ROS Signaling in the Pathogenesis of Acute Lung Injury (ALI) and Acute Respiratory Distress Syndrome (ARDS). Adv Exp Med Biol. 2017; 967:105-137. PMC: 7120947. DOI: 10.1007/978-3-319-63245-2_8. View

Mortimer L, Moreau F, Cornick S, Chadee K . The NLRP3 Inflammasome Is a Pathogen Sensor for Invasive Entamoeba histolytica via Activation of α5β1 Integrin at the Macrophage-Amebae Intercellular Junction. PLoS Pathog. 2015; 11(5):e1004887. PMC: 4425650. DOI: 10.1371/journal.ppat.1004887. View

Ataide M, Andrade W, Zamboni D, Wang D, Souza M, Franklin B . Malaria-induced NLRP12/NLRP3-dependent caspase-1 activation mediates inflammation and hypersensitivity to bacterial superinfection. PLoS Pathog. 2014; 10(1):e1003885. PMC: 3894209. DOI: 10.1371/journal.ppat.1003885. View

Shio M, Christian J, Jung J, Chang K, Olivier M . PKC/ROS-Mediated NLRP3 Inflammasome Activation Is Attenuated by Leishmania Zinc-Metalloprotease during Infection. PLoS Negl Trop Dis. 2015; 9(6):e0003868. PMC: 4482689. DOI: 10.1371/journal.pntd.0003868. View

Dey R, Joshi A, Oliveira F, Pereira L, Guimaraes-Costa A, Serafim T . Gut Microbes Egested during Bites of Infected Sand Flies Augment Severity of Leishmaniasis via Inflammasome-Derived IL-1β. Cell Host Microbe. 2018; 23(1):134-143.e6. PMC: 5832060. DOI: 10.1016/j.chom.2017.12.002. View

10.

Wei Q, Guo P, Mu K, Zhang Y, Zhao W, Huai W . Estrogen suppresses hepatocellular carcinoma cells through ERβ-mediated upregulation of the NLRP3 inflammasome. Lab Invest. 2015; 95(7):804-16. DOI: 10.1038/labinvest.2015.63. View

11.

Hashimoto D, Chow A, Noizat C, Teo P, Beasley M, Leboeuf M . Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity. 2013; 38(4):792-804. PMC: 3853406. DOI: 10.1016/j.immuni.2013.04.004. View

12.

Du Q, Zhou Y, Fan H . Treatment of hepatic alveolar echinococcosis infringing the inferior vena cava. Rev Soc Bras Med Trop. 2019; 52:e20180342. DOI: 10.1590/0037-8682-0342-2018. View

13.

Deplazes P, Rinaldi L, Alvarez Rojas C, Torgerson P, Harandi M, Romig T . Global Distribution of Alveolar and Cystic Echinococcosis. Adv Parasitol. 2017; 95:315-493. DOI: 10.1016/bs.apar.2016.11.001. View

14.

Tang S, Mao X, Chen Y, Yan L, Ye L, Li S . Reactive Oxygen Species Induce Fatty Liver and Ischemia-Reperfusion Injury by Promoting Inflammation and Cell Death. Front Immunol. 2022; 13:870239. PMC: 9098816. DOI: 10.3389/fimmu.2022.870239. View

15.

Liu X, Zhang Y, Cai C, Ni X, Zhu Q, Ren J . Taurine Alleviates Schistosoma-Induced Liver Injury by Inhibiting the TXNIP/NLRP3 Inflammasome Signal Pathway and Pyroptosis. Infect Immun. 2019; 87(12). PMC: 6867867. DOI: 10.1128/IAI.00732-19. View

16.

Baumann S, Shi R, Liu W, Bao H, Schmidberger J, Kratzer W . Worldwide literature on epidemiology of human alveolar echinococcosis: a systematic review of research published in the twenty-first century. Infection. 2019; 47(5):703-727. PMC: 8505309. DOI: 10.1007/s15010-019-01325-2. View

17.

Zhang H, Chen X, Zong B, Yuan H, Wang Z, Wei Y . Gypenosides improve diabetic cardiomyopathy by inhibiting ROS-mediated NLRP3 inflammasome activation. J Cell Mol Med. 2018; 22(9):4437-4448. PMC: 6111804. DOI: 10.1111/jcmm.13743. View

18.

de Carvalho R, Silva A, Santos L, Andrade W, de Sa K, Zamboni D . Macrophage priming is dispensable for NLRP3 inflammasome activation and restriction of Leishmania amazonensis replication. J Leukoc Biol. 2019; 106(3):631-640. DOI: 10.1002/JLB.MA1118-471R. View

19.

Minutoli L, Puzzolo D, Rinaldi M, Irrera N, Marini H, Arcoraci V . ROS-Mediated NLRP3 Inflammasome Activation in Brain, Heart, Kidney, and Testis Ischemia/Reperfusion Injury. Oxid Med Cell Longev. 2016; 2016:2183026. PMC: 4835650. DOI: 10.1155/2016/2183026. View

20.

Sharma D, Kanneganti T . The cell biology of inflammasomes: Mechanisms of inflammasome activation and regulation. J Cell Biol. 2016; 213(6):617-29. PMC: 4915194. DOI: 10.1083/jcb.201602089. View