CuO-NPs-triggered heterophil extracellular traps exacerbate liver injury in chicks by promoting oxidative stress and inflammatory responses.
Animals
Caspases
Chickens
Copper
/ toxicity
Cyclooxygenase 2
Deoxyribonuclease I
/ pharmacology
Extracellular Traps
Interleukin-6
Liver
Metal Nanoparticles
/ toxicity
NADPH Oxidases
/ pharmacology
NLR Family, Pyrin Domain-Containing 3 Protein
Oxidative Stress
Oxides
Protein Kinases
RNA, Messenger
Superoxide Dismutase
Tumor Necrosis Factor-alpha
Chicken
CuO-NPs
Heterophile extracellular traps
Liver damage
Oxidative stress
Journal
Archives of toxicology
ISSN: 1432-0738
Titre abrégé: Arch Toxicol
Pays: Germany
ID NLM: 0417615
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
received:
13
05
2022
accepted:
03
08
2022
pubmed:
14
8
2022
medline:
5
10
2022
entrez:
13
8
2022
Statut:
ppublish
Résumé
With the widespread use of copper oxide nanoparticles (CuO-NPs), their potential toxicity to the environment and biological health has attracted close attention. Heterophil extracellular traps (HETs) are an innate immune mechanism of chicken heterophils against adverse stimuli, but excessive HETs cause damage. Here, we explored the effect and mechanism of CuO-NPs on HETs formation in vitro and further evaluated the potential role of HETs in chicken liver and kidney injury. Heterophils were exposed to 5, 10, and 20 µg/mL of CuO-NPs for 2 h. The results showed that CuO-NPs induced typical HETs formation, which was dependent on NADPH oxidase, P38 and extracellular regulated protein kinases (ERK
Identifiants
pubmed: 35962800
doi: 10.1007/s00204-022-03357-4
pii: 10.1007/s00204-022-03357-4
doi:
Substances chimiques
Interleukin-6
0
NLR Family, Pyrin Domain-Containing 3 Protein
0
Oxides
0
RNA, Messenger
0
Tumor Necrosis Factor-alpha
0
Copper
789U1901C5
Cyclooxygenase 2
EC 1.14.99.1
Superoxide Dismutase
EC 1.15.1.1
NADPH Oxidases
EC 1.6.3.-
Protein Kinases
EC 2.7.-
Deoxyribonuclease I
EC 3.1.21.1
Caspases
EC 3.4.22.-
cupric oxide
V1XJQ704R4
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2913-2926Subventions
Organisme : Guangdong Basic and Applied Basic Research Foundation
ID : 2019A1515110524
Organisme : National Natural Science Foundation of China
ID : 32002309
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Aldabbous L, Abdul-Salam V, McKinnon T et al (2016) Neutrophil extracellular traps promote angiogenesis: evidence from vascular pathology in pulmonary hypertension. Arterioscler Thromb Vasc Biol 36(10):2078–2087. https://doi.org/10.1161/atvbaha.116.307634
doi: 10.1161/atvbaha.116.307634
pubmed: 27470511
Atha DH, Wang H, Petersen EJ et al (2012) Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environ Sci Technol 46(3):1819–1827. https://doi.org/10.1021/es202660k
doi: 10.1021/es202660k
pubmed: 22201446
Bajpai R, Matulis SM, Wei C et al (2016) Targeting glutamine metabolism in multiple myeloma enhances BIM binding to BCL-2 eliciting synthetic lethality to venetoclax. Oncogene 35(30):3955–3964. https://doi.org/10.1038/onc.2015.464
doi: 10.1038/onc.2015.464
pubmed: 26640142
Borregaard N, Herlin T (1982) Energy metabolism of human neutrophils during phagocytosis. J Clin Investig 70(3):550–557. https://doi.org/10.1172/jci110647
doi: 10.1172/jci110647
pubmed: 7107894
pmcid: 370256
Brinkmann V, Reichard U, Goosmann C et al (2004) Neutrophil extracellular traps kill bacteria. Science (new York, NY) 303(5663):1532–1535. https://doi.org/10.1126/science.1092385
doi: 10.1126/science.1092385
Chuammitri P, Ostojić J, Andreasen CB, Redmond SB, Lamont SJ, Palić D (2009) Chicken heterophil extracellular traps (HETs): novel defense mechanism of chicken heterophils. Vet Immunol Immunopathol 129(1–2):126–131. https://doi.org/10.1016/j.vetimm.2008.12.013
doi: 10.1016/j.vetimm.2008.12.013
pubmed: 19178950
Clem B, Telang S, Clem A et al (2008) Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth. Mol Cancer Ther 7(1):110–120. https://doi.org/10.1158/1535-7163.Mct-07-0482
doi: 10.1158/1535-7163.Mct-07-0482
pubmed: 18202014
Ehrke E, Arend C, Dringen R (2015) 3-bromopyruvate inhibits glycolysis, depletes cellular glutathione, and compromises the viability of cultured primary rat astrocytes. J Neurosci Res 93(7):1138–1146. https://doi.org/10.1002/jnr.23474
doi: 10.1002/jnr.23474
pubmed: 25196479
Fadini GP, Menegazzo L, Rigato M et al (2016) NETosis delays diabetic wound healing in mice and humans. Diabetes 65(4):1061–1071. https://doi.org/10.2337/db15-0863
doi: 10.2337/db15-0863
pubmed: 26740598
Genovese KJ, He H, Swaggerty CL, Kogut MH (2013) The avian heterophil. Dev Comp Immunol 41(3):334–340. https://doi.org/10.1016/j.dci.2013.03.021
doi: 10.1016/j.dci.2013.03.021
pubmed: 23583524
Gonzales-Eguia A, Fu C-M, Lu F-Y, Lien T-F (2009) Effects of nanocopper on copper availability and nutrients digestibility, growth performance and serum traits of piglets. Livestock Sci 126(1–3):122–129
doi: 10.1016/j.livsci.2009.06.009
Hakkim A, Fuchs TA, Martinez NE et al (2011) Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat Chem Biol 7(2):75–77. https://doi.org/10.1038/nchembio.496
doi: 10.1038/nchembio.496
pubmed: 21170021
Han Z, Zhang Y, Wang C et al (2019) Ochratoxin a-triggered chicken heterophil extracellular traps release through reactive oxygen species production dependent on activation of NADPH oxidase, ERK, and p38 MAPK signaling pathways. J Agric Food Chem 67(40):11230–11235. https://doi.org/10.1021/acs.jafc.9b03155
doi: 10.1021/acs.jafc.9b03155
pubmed: 31523955
Hassanen EI, Tohamy AF, Issa MY, Ibrahim MA, Farroh KY, Hassan AM (2019) Pomegranate juice diminishes the mitochondria-dependent cell death and NF-kB signaling pathway induced by copper oxide nanoparticles on liver and kidneys of rats. Int J Nanomed 14:8905–8922. https://doi.org/10.2147/ijn.S229461
doi: 10.2147/ijn.S229461
He H, Farnell MB, Kogut MH (2003) Inflammatory agonist stimulation and signal pathway of oxidative burst in neonatal chicken heterophils. Comp Biochem Physiol A Mol Integr Physiol 135(1):177–184. https://doi.org/10.1016/s1095-6433(03)00049-7
doi: 10.1016/s1095-6433(03)00049-7
pubmed: 12727554
He H, Zou Z, Wang B et al (2020) Copper oxide nanoparticles induce oxidative DNA damage and cell death via copper ion-mediated P38 MAPK activation in vascular endothelial cells. Int J Nanomed 15:3291–3302. https://doi.org/10.2147/ijn.S241157
doi: 10.2147/ijn.S241157
Healy DA, Watson RW, Newsholme P (2002) Glucose, but not glutamine, protects against spontaneous and anti-Fas antibody-induced apoptosis in human neutrophils. Clin Sci (london, England: 1979) 103(2):179–189. https://doi.org/10.1042/cs1030179
doi: 10.1042/cs1030179
Holan V, Javorkova E, Vrbova K et al (2019) A murine model of the effects of inhaled CuO nanoparticles on cells of innate and adaptive immunity—a kinetic study of a continuous three-month exposure. Nanotoxicology 13(7):952–963. https://doi.org/10.1080/17435390.2019.1602679
doi: 10.1080/17435390.2019.1602679
pubmed: 31012774
Hong CS, Graham NA, Gu W et al (2016) MCT1 modulates cancer cell pyruvate export and growth of tumors that co-express MCT1 and MCT4. Cell Rep 14(7):1590–1601. https://doi.org/10.1016/j.celrep.2016.01.057
doi: 10.1016/j.celrep.2016.01.057
pubmed: 26876179
pmcid: 4816454
Huang H, Chen HW, Evankovich J et al (2013) Histones activate the NLRP3 inflammasome in Kupffer cells during sterile inflammatory liver injury. J Immunol (baltimore, Md: 1950) 191(5):2665–2679. https://doi.org/10.4049/jimmunol.1202733
doi: 10.4049/jimmunol.1202733
Huang H, Tohme S, Al-Khafaji AB et al (2015) Damage-associated molecular pattern-activated neutrophil extracellular trap exacerbates sterile inflammatory liver injury. Hepatology (baltimore, MD) 62(2):600–614. https://doi.org/10.1002/hep.27841
doi: 10.1002/hep.27841
Javed R, Ahmed M, Haq IU, Nisa S, Zia M (2017) PVP and PEG doped CuO nanoparticles are more biologically active: antibacterial, antioxidant, antidiabetic and cytotoxic perspective. Mater Sci Eng, C Mater Biol Appl 79:108–115. https://doi.org/10.1016/j.msec.2017.05.006
doi: 10.1016/j.msec.2017.05.006
Jeong J, Kim J, Seok SH, Cho WS (2016) Indium oxide (In2O3) nanoparticles induce progressive lung injury distinct from lung injuries by copper oxide (CuO) and nickel oxide (NiO) nanoparticles. Arch Toxicol 90(4):817–828. https://doi.org/10.1007/s00204-015-1493-x
doi: 10.1007/s00204-015-1493-x
pubmed: 25731971
Jiang A, Zhang Y, Wu D et al (2021) Sodium molybdate induces heterophil extracellular traps formation in chicken. Ecotoxicol Environ Saf 210:111886. https://doi.org/10.1016/j.ecoenv.2020.111886
doi: 10.1016/j.ecoenv.2020.111886
pubmed: 33421725
Johnston HJ, Verdon R, Gillies S et al (2018) Adoption of in vitro systems and zebrafish embryos as alternative models for reducing rodent use in assessments of immunological and oxidative stress responses to nanomaterials. Crit Rev Toxicol 48(3):252–271. https://doi.org/10.1080/10408444.2017.1404965
doi: 10.1080/10408444.2017.1404965
pubmed: 29239234
Joshi MB, Baipadithaya G, Balakrishnan A et al (2016) Elevated homocysteine levels in type 2 diabetes induce constitutive neutrophil extracellular traps. Sci Rep 6:36362. https://doi.org/10.1038/srep36362
doi: 10.1038/srep36362
pubmed: 27811985
pmcid: 5095649
Kennedy AD, DeLeo FR (2009) Neutrophil apoptosis and the resolution of infection. Immunol Res 43(1–3):25–61. https://doi.org/10.1007/s12026-008-8049-6
doi: 10.1007/s12026-008-8049-6
pubmed: 19066741
Klopf J, Brostjan C, Eilenberg W, Neumayer C (2021) Neutrophil extracellular traps and their implications in cardiovascular and inflammatory disease. Int J Mol Sci. https://doi.org/10.3390/ijms22020559
doi: 10.3390/ijms22020559
pubmed: 33429925
pmcid: 7828090
Lee KH, Kronbichler A, Park DD et al (2017) Neutrophil extracellular traps (NETs) in autoimmune diseases: a comprehensive review. Autoimmun Rev 16(11):1160–1173. https://doi.org/10.1016/j.autrev.2017.09.012
doi: 10.1016/j.autrev.2017.09.012
pubmed: 28899799
Liu H, Lai W, Liu X et al (2021) Exposure to copper oxide nanoparticles triggers oxidative stress and endoplasmic reticulum (ER)-stress induced toxicology and apoptosis in male rat liver and BRL-3A cell. J Hazard Mater 401:123349. https://doi.org/10.1016/j.jhazmat.2020.123349
doi: 10.1016/j.jhazmat.2020.123349
pubmed: 32659578
Matsumoto T, Jimi S, Migita K, Takamatsu Y, Hara S (2016) Inhibition of glucose transporter 1 induces apoptosis and sensitizes multiple myeloma cells to conventional chemotherapeutic agents. Leuk Res 41:103–110. https://doi.org/10.1016/j.leukres.2015.12.008
doi: 10.1016/j.leukres.2015.12.008
pubmed: 26790725
Mohanty T, Fisher J, Bakochi A et al (2019) Neutrophil extracellular traps in the central nervous system hinder bacterial clearance during pneumococcal meningitis. Nat Commun 10(1):1667. https://doi.org/10.1038/s41467-019-09040-0
doi: 10.1038/s41467-019-09040-0
pubmed: 30971685
pmcid: 6458182
Nguyen TT, Ngo LQ, Promsudthi A, Surarit R (2016) Salivary lipid peroxidation in patients with generalized chronic periodontitis and acute coronary syndrome. J Periodontol 87(2):134–141. https://doi.org/10.1902/jop.2015.150353
doi: 10.1902/jop.2015.150353
pubmed: 26313018
Papayannopoulos V (2018) Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 18(2):134–147. https://doi.org/10.1038/nri.2017.105
doi: 10.1038/nri.2017.105
pubmed: 28990587
Periasamy S, Chu PY, Li YH, Hsu DZ, Liu MY (2015) Sesamol ameliorates hypotension by modulating cytokines and PPAR-gamma in systemic inflammatory response. EXCLI J 14:948–957. https://doi.org/10.17179/excli2015-367
doi: 10.17179/excli2015-367
pubmed: 26839527
pmcid: 4732502
Pisoschi AM, Pop A (2015) The role of antioxidants in the chemistry of oxidative stress: a review. Eur J Med Chem 97:55–74. https://doi.org/10.1016/j.ejmech.2015.04.040
doi: 10.1016/j.ejmech.2015.04.040
pubmed: 25942353
Rodríguez-Espinosa O, Rojas-Espinosa O, Moreno-Altamirano MM, López-Villegas EO, Sánchez-García FJ (2015) Metabolic requirements for neutrophil extracellular traps formation. Immunology 145(2):213–224. https://doi.org/10.1111/imm.12437
doi: 10.1111/imm.12437
pubmed: 25545227
pmcid: 4427386
Salehi H, Chehregani Rad A, Raza A, Chen JT (2021) Foliar application of CeO(2) nanoparticles alters generative components fitness and seed productivity in bean crop (Phaseolus vulgaris L.). Nanomaterials (basel, Switzerland). https://doi.org/10.3390/nano11040862
doi: 10.3390/nano11040862
Sarkar A, Das J, Manna P, Sil PC (2011) Nano-copper induces oxidative stress and apoptosis in kidney via both extrinsic and intrinsic pathways. Toxicology 290(2–3):208–217. https://doi.org/10.1016/j.tox.2011.09.086
doi: 10.1016/j.tox.2011.09.086
pubmed: 22000994
Satoh T (2014) Molecular mechanisms for the regulation of insulin-stimulated glucose uptake by small guanosine triphosphatases in skeletal muscle and adipocytes. Int J Mol Sci 15(10):18677–18692. https://doi.org/10.3390/ijms151018677
doi: 10.3390/ijms151018677
pubmed: 25325535
pmcid: 4227239
Sizentsov AN, Kvan OV, Miroshnikova EP, Gavrish IA, Serdaeva VA, Bykov AV (2018) Assessment of biotoxicity of Cu nanoparticles with respect to probiotic strains of microorganisms and representatives of the normal flora of the intestine of broiler chickens. Environ Sci Pollut Res Int 25(16):15765–15773. https://doi.org/10.1007/s11356-018-1761-4
doi: 10.1007/s11356-018-1761-4
pubmed: 29582323
Strauch BM, Niemand RK, Winkelbeiner NL, Hartwig A (2017) Comparison between micro- and nanosized copper oxide and water soluble copper chloride: interrelationship between intracellular copper concentrations, oxidative stress and DNA damage response in human lung cells. Part Fibre Toxicol 14(1):28. https://doi.org/10.1186/s12989-017-0209-1
doi: 10.1186/s12989-017-0209-1
pubmed: 28764715
pmcid: 5540434
Tilyek A, Chai C, Hou X et al (2016) The protective effects of Ribes diacanthum Pall on cisplatin-induced nephrotoxicity in mice. J Ethnopharmacol 178:297–306. https://doi.org/10.1016/j.jep.2015.10.003
doi: 10.1016/j.jep.2015.10.003
pubmed: 26481606
Tohme S, Yazdani HO, Al-Khafaji AB et al (2016) Neutrophil extracellular traps promote the development and progression of liver metastases after surgical stress. Can Res 76(6):1367–1380. https://doi.org/10.1158/0008-5472.Can-15-1591
doi: 10.1158/0008-5472.Can-15-1591
Wang Z, von dem Bussche A, Kabadi PK, Kane AB, Hurt RH (2013) Biological and environmental transformations of copper-based nanomaterials. ACS Nano 7(10):8715–8727. https://doi.org/10.1021/nn403080y
doi: 10.1021/nn403080y
pubmed: 24032665
pmcid: 3894052
Wang JJ, Wei ZK, Han Z et al (2019) Zearalenone induces estrogen-receptor-independent neutrophil extracellular trap release in vitro. J Agric Food Chem 67(16):4588–4594. https://doi.org/10.1021/acs.jafc.8b05948
doi: 10.1021/acs.jafc.8b05948
pubmed: 30939243
Wei Z, Wang J, Wang Y et al (2019a) Effects of neutrophil extracellular traps on bovine mammary epithelial cells in vitro. Front Immunol 10:1003. https://doi.org/10.3389/fimmu.2019.01003
doi: 10.3389/fimmu.2019.01003
pubmed: 31156617
pmcid: 6533846
Wei Z, Zhao Y, Zhang N et al (2019b) Eimeria tenella induces the release of chicken heterophil extracellular traps. Vet Parasitol 275:108931. https://doi.org/10.1016/j.vetpar.2019.108931
doi: 10.1016/j.vetpar.2019.108931
pubmed: 31605936
Wei Z, Wang Z, Liu X et al (2020) Toxoplasma gondii triggers neutrophil extracellular traps release in dogs. Front Cell Infect Microbiol 10:429. https://doi.org/10.3389/fcimb.2020.00429
doi: 10.3389/fcimb.2020.00429
pubmed: 33102243
pmcid: 7546211
Wu D, Li S, Li P et al (2021) Diacetoxyscirpenol-induced heterophil extracellular traps contribute to the immune toxicity of liver injury in chickens. Food Chem Toxicol 148:111926. https://doi.org/10.1016/j.fct.2020.111926
doi: 10.1016/j.fct.2020.111926
pubmed: 33352262
Xu L, Yu Y, Sang R, Li J, Ge B, Zhang X (2018) Protective effects of taraxasterol against ethanol-induced liver injury by regulating CYP2E1/Nrf2/HO-1 and NF-κB signaling pathways in mice. Oxid Med Cell Longev 2018:8284107. https://doi.org/10.1155/2018/8284107
doi: 10.1155/2018/8284107
pubmed: 30344887
pmcid: 6174809
Zhang L, Gu FX, Chan JM, Wang AZ, Langer RS, Farokhzad OC (2008) Nanoparticles in medicine: therapeutic applications and developments. Clin Pharmacol Ther 83(5):761–769. https://doi.org/10.1038/sj.clpt.6100400
doi: 10.1038/sj.clpt.6100400
pubmed: 17957183
Zhang CH, Wang Y, Sun QQ et al (2018) Copper nanoparticles show obvious in vitro and in vivo reproductive toxicity via ERK mediated signaling pathway in female mice. Int J Biol Sci 14(13):1834–1844. https://doi.org/10.7150/ijbs.27640
doi: 10.7150/ijbs.27640
pubmed: 30443187
pmcid: 6231217
Zhang J, Dai Y, Wei C, Zhao X, Zhou Q, Xie L (2020) DNase I improves corneal epithelial and nerve regeneration in diabetic mice. J Cell Mol Med 24(8):4547–4556. https://doi.org/10.1111/jcmm.15112
doi: 10.1111/jcmm.15112
pubmed: 32168430
pmcid: 7176839
Zhuang C, Wang Y, Zhang Y, Xu N (2018) Oxidative stress in osteoarthritis and antioxidant effect of polysaccharide from angelica sinensis. Int J Biol Macromol 115:281–286. https://doi.org/10.1016/j.ijbiomac.2018.04.083
doi: 10.1016/j.ijbiomac.2018.04.083
pubmed: 29673954