Hypoxia, oxidative stress, and immune evasion: a trinity of the trichothecenes T-2 toxin and deoxynivalenol (DON)

. 2021 Jun ; 95 (6) : 1899-1915. [epub] 20210325

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid33765170
Odkazy

PubMed 33765170
DOI 10.1007/s00204-021-03030-2
PII: 10.1007/s00204-021-03030-2
Knihovny.cz E-zdroje

T-2 toxin and deoxynivalenol (DON) are type A and B trichothecenes, respectively. They widely occur as pollutants in food and crops and cause a series of toxicities, including immunotoxicity, hepatotoxicity, and neurotoxicity. Oxidative stress is the primary mechanistic basis of these toxic effects. Increasing amounts of evidence have shown that mitochondria are significant targets of apoptosis caused by T-2 toxin- and DON-induced oxidative stress via regulation of Bax/B-cell lymphoma-2 and caspase-3/caspase-9 signaling. DNA methylation and autophagy are involved in oxidative stress related to apoptosis, and hypoxia and immune evasion are related to oxidative stress in this context. Hypoxia induces oxidative stress by stimulating mitochondrial reactive oxygen species production and regulates the expression of cytokines, such as interleukin-1β and tumor necrosis factor-α. Programmed cell death-ligand 1 is upregulated by these cytokines and by hypoxia-inducible factor-1, which allows it to bind to programmed cell death-1 to enable escape of immune cell surveillance and achievement of immune evasion. This review concentrates on novel findings regarding the oxidative stress mechanisms of the trichothecenes T-2 toxin and DON. Importantly, we discuss the new evidence regarding the connection of hypoxia and immune evasion with oxidative stress in this context. Finally, the trinity of hypoxia, oxidative stress and immune evasion is highlighted. This work will be conducive to an improved understanding of the oxidative stress caused by trichothecene mycotoxins.

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Agrawal M, Bhaskar AS, Lakshmana Rao PV (2015) Involvement of mitogen-activated protein kinase pathway in T-2 toxin-induced cell cycle alteration and apoptosis in human neuroblastoma cells. Mol Neurobiol 51(3):1379–1394. https://doi.org/10.1007/s12035-014-8816-4 PubMed DOI

Arslan F, Lai RC, Smeets MB et al (2013) Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury. Stem Cell Res 10(3):301–312. https://doi.org/10.1016/j.scr.2013.01.002 PubMed DOI

Asgarova A, Asgarov K, Godet Y et al (2018) PD-L1 expression is regulated by both DNA methylation and NF-kB during EMT signaling in non-small cell lung carcinoma. Oncoimmunology 7(5):e1423170. https://doi.org/10.1080/2162402x.2017.1423170 PubMed DOI PMC

Ayers M, Lunceford J, Nebozhyn M et al (2017) IFN-gamma-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest 127(8):2930–2940. https://doi.org/10.1172/jci91190 PubMed DOI PMC

Bailly C (2020) Regulation of PD-L1 expression on cancer cells with ROS-modulating drugs. Life Sci 246:117403. https://doi.org/10.1016/j.lfs.2020.117403 PubMed DOI

Balamurugan K (2016) HIF-1 at the crossroads of hypoxia, inflammation, and cancer. Int J Cancer 138(5):1058–1066. https://doi.org/10.1002/ijc.29519 PubMed DOI

Barsoum IB, Smallwood CA, Siemens DR, Graham CH (2014) A mechanism of hypoxia-mediated escape from adaptive immunity in cancer cells. Cancer Res 74(3):665–674. https://doi.org/10.1158/0008-5472.Can-13-0992 PubMed DOI

Beccard IJ, Hofmann L, Schroeder JC et al (2020) Immune suppressive effects of plasma-derived exosome populations in head and neck cancer. Cancers (Basel) 12(7):1997. https://doi.org/10.3390/cancers12071997 DOI

Botti G, Fratangelo F, Cerrone M et al (2017) COX-2 expression positively correlates with PD-L1 expression in human melanoma cells. J Transl Med 15(1):46. https://doi.org/10.1186/s12967-017-1150-7 PubMed DOI PMC

Boussiotis VA (2016) Molecular and biochemical aspects of the PD-1 checkpoint pathway. N Engl J Med 375(18):1767–1778. https://doi.org/10.1056/NEJMra1514296 PubMed DOI PMC

Chain EPoCitF, Knutsen HK, Alexander J, et al (2017) Risks to human and animal health related to the presence of deoxynivalenol and its acetylated and modified forms in food and feed. EFSA J 15(9):e04718 https://doi.org/10.2903/j.efsa.2017.4718

Chan L-C, Li C-W, Xia W et al (2019) IL-6/JAK1 pathway drives PD-L1 Y112 phosphorylation to promote cancer immune evasion. J Clin Invest 129(8):3324–3338. https://doi.org/10.1172/jci126022 PubMed DOI PMC

Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci USA 95(20):11715–11720. https://doi.org/10.1073/pnas.95.20.11715 PubMed DOI

Chandel NS, McClintock DS, Feliciano CE et al (2000a) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J Biol Chem 275(33):25130–25138. https://doi.org/10.1074/jbc.M001914200 PubMed DOI

Chandel NS, Trzyna WC, McClintock DS, Schumacker PT (2000b) Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol (Baltim, Md: 1950) 165(2):1013–21 https://doi.org/10.4049/jimmunol.165.2.1013

Charras A, Arvaniti P, Le Dantec C et al (2019) JAK Inhibitors and oxidative stress control. Front Immunol 10:2814. https://doi.org/10.3389/fimmu.2019.02814 PubMed DOI PMC

Che F, Heng X, Zhang H et al (2017) Novel B7–H4-mediated crosstalk between human non-Hodgkin lymphoma cells and tumor-associated macrophages leads to immune evasion via secretion of IL-6 and IL-10. Cancer Immunol Immunother 66(6):717–729. https://doi.org/10.1007/s00262-017-1961-7 PubMed DOI

Chen G, Huang AC, Zhang W, et al (2018) Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature 560(7718):382. https://doi.org/10.1038/s41586-018-0392-8

Chen Y, Han S, Wang Y et al (2019) Oxidative stress and apoptotic changes in broiler chicken splenocytes exposed to T-2 toxin. Biomed Res Int 2019:5493870. https://doi.org/10.1155/2019/5493870 PubMed DOI PMC

Chen J, Zhou J, Fu H, Ni X, Shan Y (2020) Upregulation of oxidative stress-responsive 1(OXSR1) predicts poor prognosis and promotes hepatocellular carcinoma progression. Bioengineered 11(1):958–971. https://doi.org/10.1080/21655979.2020.1814659 PubMed DOI

Chettimada S, Lorenz DR, Misra V et al (2018) Exosome markers associated with immune activation and oxidative stress in HIV patients on antiretroviral therapy. Sci Rep 8(1):7227. https://doi.org/10.1038/s41598-018-25515-4 PubMed DOI PMC

Coimbra-Costa D, Alva N, Duran M, Carbonell T, Rama R (2017) Oxidative stress and apoptosis after acute respiratory hypoxia and reoxygenation in rat brain. Redox Biol 12:216–225. https://doi.org/10.1016/j.redox.2017.02.014 PubMed DOI PMC

Cui XG, Han ZT, He SH et al (2017) HIF1/2alpha mediates hypoxia-induced LDHA expression in human pancreatic cancer cells. Oncotarget 8(15):24840–24852. https://doi.org/10.18632/oncotarget.15266 PubMed DOI PMC

Cui C, Fu K, Yang L et al (2019) Hypoxia-inducible gene 2 promotes the immune escape of hepatocellular carcinoma from nature killer cells through the interleukin-10-STAT3 signaling pathway. J Exp Clin Cancer Res 38(1):229. https://doi.org/10.1186/s13046-019-1233-9 PubMed DOI PMC

da Silva EO, Gerez JR, Hohmann MSN, Verri WA Jr, Bracarense A (2019) Phytic acid decreases oxidative stress and intestinal lesions induced by fumonisin B(1) and deoxynivalenol in intestinal explants of pigs. Toxins (Basel) 11(1):18. https://doi.org/10.3390/toxins11010018 DOI

Dai C, Xiao X, Sun F et al (2019) T-2 toxin neurotoxicity: role of oxidative stress and mitochondrial dysfunction. Arch Toxicol 93(11):3041–3056. https://doi.org/10.1007/s00204-019-02577-5 PubMed DOI

Darwish WS, Chen Z, Li Y, Tan H, Chiba H, Hui SP (2020) Deoxynivalenol-induced alterations in the redox status of HepG2 cells: identification of lipid hydroperoxides, the role of Nrf2-Keap1 signaling, and protective effects of zinc. Mycotoxin Res 36(3):287–299. https://doi.org/10.1007/s12550-020-00392-x PubMed DOI

Deegan S, Saveljeva S, Logue SE et al (2014) Deficiency in the mitochondrial apoptotic pathway reveals the toxic potential of autophagy under ER stress conditions. Autophagy 10(11):1921–1936. https://doi.org/10.4161/15548627.2014.981790 PubMed DOI PMC

Deng C, Ji C, Qin W et al (2016) Deoxynivalenol inhibits proliferation and induces apoptosis in human umbilical vein endothelial cells. Environ Toxicol Pharmacol 43:232–241. https://doi.org/10.1016/j.etap.2016.02.002 PubMed DOI

Doedens AL, Stockmann C, Rubinstein MP et al (2010) Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res 70(19):7465–7475. https://doi.org/10.1158/0008-5472.Can-10-1439 PubMed DOI PMC

Eldh M, Ekström K, Valadi H et al (2010) Exosomes communicate protective messages during oxidative stress; possible role of exosomal shuttle RNA. PLoS ONE 5(12):e15353. https://doi.org/10.1371/journal.pone.0015353 PubMed DOI PMC

Ferrari L, Cantoni AM, Borghetti P, De Angelis E, Corradi A (2009) Cellular immune response and immunotoxicity induced by DON (deoxynivalenol) in piglets. Vet Res Commun 33:S133–S135. https://doi.org/10.1007/s11259-009-9265-9 DOI

Filippova M, Filippov V, Williams VM et al (2014) Cellular levels of oxidative stress affect the response of cervical cancer cells to chemotherapeutic agents. Biomed Res Int 2014:574659. https://doi.org/10.1155/2014/574659 PubMed DOI PMC

Gillies LA, Kuwana T (2014) Apoptosis regulation at the mitochondrial outer membrane. J Cell Biochem 115(4):632–640. https://doi.org/10.1002/jcb.24709 PubMed DOI

Gordon SR, Maute RL, Dulken BW et al (2017) PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature 545(7655):495–499. https://doi.org/10.1038/nature22396 PubMed DOI PMC

Gu X, Guo W, Zhao Y, Liu G, Wu J, Chang C (2019) Deoxynivalenol-induced cytotoxicity and apoptosis in IPEC-J2 cells through the activation of autophagy by inhibiting PI3K-AKT-mTOR signaling pathway. ACS Omega 4(19):18478–18486. https://doi.org/10.1021/acsomega.9b03208 PubMed DOI PMC

Guo W, Gu X, Tong Y, Wang X, Wu J, Chang C (2019) Protective effects of mannan/β-glucans from yeast cell wall on the deoxyniyalenol-induced oxidative stress and autophagy in IPEC-J2 cells. Int J Biol Macromol 135:619–629. https://doi.org/10.1016/j.ijbiomac.2019.05.180 PubMed DOI

Guzy RD, Hoyos B, Robin E et al (2005) Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing. Cell Metab 1(6):401–408. https://doi.org/10.1016/j.cmet.2005.05.001 PubMed DOI

Habrowska-Gorczynska DE, Kowalska K, Urbanek KA, Dominska K, Sakowicz A, Piastowska-Ciesielska AW (2019) Deoxynivalenol modulates the viability, ROS production and apoptosis in prostate cancer cells. Toxins (Basel) 11(5):265. https://doi.org/10.3390/toxins11050265 DOI

Haddad JJ (2007) The role of Bax/Bcl-2 and pro-caspase peptides in hypoxia/reperfusion-dependent regulation of MAPK(ERK): discordant proteomic effect of MAPK(p38). Protein Pept Lett 14(4):361–371. https://doi.org/10.2174/092986607780363925 PubMed DOI

Han J, Wang Q-C, Zhu C-C et al (2016) Deoxynivalenol exposure induces autophagy/apoptosis and epigenetic modification changes during porcine oocyte maturation. Toxicol Appl Pharmacol 300:70–76. https://doi.org/10.1016/j.taap.2016.03.006 PubMed DOI

Hayashi Y, Yokota A, Harada H, Huang G (2019) Hypoxia/pseudohypoxia-mediated activation of hypoxia-inducible factor-1alpha in cancer. Cancer Sci 110(5):1510–1517. https://doi.org/10.1111/cas.13990 PubMed DOI PMC

Heddleston JM, Li Z, Lathia JD, Bao S, Hjelmeland AB, Rich JN (2010) Hypoxia inducible factors in cancer stem cells. Br J Cancer 102(5):789–795. https://doi.org/10.1038/sj.bjc.6605551 PubMed DOI PMC

Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L (2011) Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS ONE 6(2):e16899. https://doi.org/10.1371/journal.pone.0016899 PubMed DOI PMC

Huang D, Luqing C, Xianglian L et al (2018) Protective mechanisms involving enhanced mitochondrial functions and mitophagy against T-2 toxin-induced toxicities in GH3 cells. Toxicol Lett 295:41–53. https://doi.org/10.1016/j.toxlet.2018.05.041 DOI

Huang M-H, Zhang X-B, Wang H-L et al (2019) Intermittent hypoxia enhances the tumor programmed death ligand 1 expression in a mouse model of sleep apnea. Ann Transl Med 7(5):97. https://doi.org/10.21037/atm.2019.01.44 PubMed DOI PMC

Ibrahim HM, Mohammed-Geba K, Tawfic AA, El-Magd MA (2019) Camel milk exosomes modulate cyclophosphamide-induced oxidative stress and immuno-toxicity in rats. Food Funct 10(11):7523–7532. https://doi.org/10.1039/c9fo01914f PubMed DOI

Izawa S, Kono K, Mimura K et al (2011) H PubMed DOI

Jeong H, Kim S, Hong B-J et al (2019) Tumor-associated macrophages enhance tumor hypoxia and aerobic glycolysis. Cancer Res 79(4):795–806. https://doi.org/10.1158/0008-5472.Can-18-2545 PubMed DOI

Ji X, Zheng W, Yao W (2019) Protective role of hydrogen gas on oxidative damage and apoptosis in intestinal porcine epithelial cells (IPEC-J2) induced by deoxynivalenol: a preliminary study. Toxins (Basel) 12(1):5. https://doi.org/10.3390/toxins12010005 DOI

Kovesi B, Pelyhe C, Zandoki E, Mezes M, Balogh K (2020) Combined effects of aflatoxin B1 and deoxynivalenol on the expression of glutathione redox system regulatory genes in common carp. J Anim Physiol Anim Nutr (Berl) 105(5):1531–1539. https://doi.org/10.1111/jpn.13343 DOI

Kowalska K, Habrowska-Gorczynska DE, Urbanek KA, Dominska K, Sakowicz A, Piastowska-Ciesielska AW (2019) Estrogen receptor beta plays a protective role in zearalenone-induced oxidative stress in normal prostate epithelial cells. Ecotoxicol Environ Saf 172:504–513. https://doi.org/10.1016/j.ecoenv.2019.01.115 PubMed DOI

Koyasu S, Kobayashi M, Goto Y, Hiraoka M, Harada H (2018) Regulatory mechanisms of hypoxia-inducible factor 1 activity: two decades of knowledge. Cancer Sci 109(3):560–571. https://doi.org/10.1111/cas.13483 PubMed DOI PMC

Lando D, Peet DJ, Whelan DA, Gorman JJ, Whitelaw ML (2002) Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science 295(5556):858–861. https://doi.org/10.1126/science.1068592 PubMed DOI

Lässer C, Alikhani VS, Ekström K et al (2011) Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med 9:9. https://doi.org/10.1186/1479-5876-9-9 PubMed DOI PMC

Lei Y, Guanghui Z, Xi W et al (2017) Cellular responses to T-2 toxin and/or deoxynivalenol that induce cartilage damage are not specific to chondrocytes. Sci Rep 7(1):2231. https://doi.org/10.1038/s41598-017-02568-5 PubMed DOI PMC

Li M, Cuff CF, Pestka JJ (2006) T-2 toxin impairment of enteric reovirus clearance in the mouse associated with suppressed immunoglobulin and IFN-gamma responses. Toxicol Appl Pharmacol 214(3):318–325. https://doi.org/10.1016/j.taap.2006.01.007 PubMed DOI PMC

Li D, Ye Y, Lin S et al (2014) Evaluation of deoxynivalenol-induced toxic effects on DF-1 cells in vitro: cell-cycle arrest, oxidative stress, and apoptosis. Environ Toxicol Pharmacol 37(1):141–149. https://doi.org/10.1016/j.etap.2013.11.015 PubMed DOI

Li F, Liang J, Tang D (2018) Brahma-related gene 1 ameliorates the neuronal apoptosis and oxidative stress induced by oxygen-glucose deprivation/reoxygenation through activation of Nrf2/HO-1 signaling. Biomed Pharmacother 108:1216–1224. https://doi.org/10.1016/j.biopha.2018.09.144 PubMed DOI

Li Z, Zhang C, Du J-X et al (2020) Adipocytes promote tumor progression and induce PD-L1 expression via TNF-alpha/IL-6 signaling. Cancer Cell Int 20(1):179. https://doi.org/10.1186/s12935-020-01269-w PubMed DOI PMC

Liao Y, Peng Z, Chen L, Nuessler AK, Liu L, Yang W (2018) Deoxynivalenol, gut microbiota and immunotoxicity: a potential approach? Food Chem Toxicol 112:342–354. https://doi.org/10.1016/j.fct.2018.01.013 PubMed DOI

Liao S, Tang S, Tan B et al (2020) Chloroquine improves deoxynivalenol-induced inflammatory response and intestinal mucosal damage in piglets. Oxid Med Cell Longev 2020:9834813. https://doi.org/10.1155/2020/9834813 PubMed DOI PMC

Liu X, Guo P, Liu A et al (2017) Nitric oxide (NO)-mediated mitochondrial damage plays a critical role in T-2 toxin-induced apoptosis and growth hormone deficiency in rat anterior pituitary GH3 cells. Food Chem Toxicol 102:11–23. https://doi.org/10.1016/j.fct.2017.01.017 PubMed DOI

Liu A, Sun Y, Wang X et al (2019) DNA methylation is involved in pro-inflammatory cytokines expression in T-2 toxin-induced liver injury. Food Chem Toxicol 132:110661. https://doi.org/10.1016/j.fct.2019.110661 PubMed DOI

Liu A, Xu X, Hou R et al (2019) DNA methylation and RASSF4 expression are involved in T-2 toxin-induced hepatotoxicity. Toxicology 425:152246. https://doi.org/10.1016/j.tox.2019.152246 PubMed DOI

MacIntyre NR (2014) Tissue hypoxia: implications for the respiratory clinician. Respir Care 59(10):1590–1596. https://doi.org/10.4187/respcare.03357 PubMed DOI

Maj T, Wang W, Crespo J, et al (2017) Oxidative stress controls regulatory T cell apoptosis and suppressor activity and PD-L1-blockade resistance in tumor. Nat Immunol 18(12):1332. https://doi.org/10.1038/ni.3868

Maresca M (2013) From the gut to the brain: journey and pathophysiological effects of the food-associated trichothecene mycotoxin deoxynivalenol. Toxins (Basel) 5(4):784–820. https://doi.org/10.3390/toxins5040784 DOI

Mariño G, Niso-Santano M, Baehrecke EH, Kroemer G (2014) Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol 15(2):81–94. https://doi.org/10.1038/nrm3735 PubMed DOI PMC

Meissonnier GM, Laffitte J, Raymond I et al (2008) Subclinical doses of T-2 toxin impair acquired immune response and liver cytochrome P450 in pigs. Toxicology 247(1):46–54. https://doi.org/10.1016/j.tox.2008.02.003 PubMed DOI

Mincheva-Nilsson L, Baranov V (2014) Cancer exosomes and NKG2D receptor-ligand interactions: impairing NKG2D-mediated cytotoxicity and anti-tumour immune surveillance. Semin Cancer Biol 28:24–30. https://doi.org/10.1016/j.semcancer.2014.02.010 PubMed DOI

Minervini F, Fornelli F, Lucivero G, Romano C, Visconti A (2005) T-2 toxin immunotoxicity on human B and T lymphoid cell lines. Toxicology 210(1):81–91. https://doi.org/10.1016/j.tox.2005.01.007 PubMed DOI

Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147(4):728–741. https://doi.org/10.1016/j.cell.2011.10.026 DOI

Mohamed AA, Galal AA, Elewa YH (2015) Comparative protective effects of royal jelly and cod liver oil against neurotoxic impact of tartrazine on male rat pups brain. Acta Histochem 117(7):649–658. https://doi.org/10.1016/j.acthis.2015.07.002 PubMed DOI

Mohamed AA-R, Metwally MMM, Khalil SR, Salem GA, Ali HA (2019) Moringa oleifera extract attenuates the CoCl2 induced hypoxia of rat’s brain: Expression pattern of HIF-1 alpha, NF-kB, MAO and EPO. Biomed Pharmacother 109:1688–1697. https://doi.org/10.1016/j.biopha.2018.11.019 DOI

Moore LD, Le T, Fan G (2013) DNA methylation and its basic function. Neuropsychopharmacology 38(1):23–38. https://doi.org/10.1038/npp.2012.112 PubMed DOI

Moosavi M, Rezaei M, Kalantari H, Behfar A, Varnaseri G (2016) l-carnitine protects rat hepatocytes from oxidative stress induced by T-2 toxin. Drug Chem Toxicol 39(4):445–450. https://doi.org/10.3109/01480545.2016.1141423 PubMed DOI

Mu H, Mu P, Zhu W et al (2020) Low doses of deoxynivalenol inhibit the cell migration mediated by H3K27me3-targeted downregulation of TEM8 expression. Biochem Pharmacol 175:113897. https://doi.org/10.1016/j.bcp.2020.113897 PubMed DOI

Ning Y, Wang X, Zhang P et al (2018) Dietary exosome-miR-23b may be a novel therapeutic measure for preventing Kashin-Beck disease. Exp Ther Med 15(4):3680–3686. https://doi.org/10.3892/etm.2018.5885 PubMed DOI PMC

Noman MZ, Desantis G, Janji B, et al (2014) PD-L1 is a novel direct target of HIF-1 alpha., and its blockade under hypoxia enhanced MDSC-mediated T cell activation. J Exp Med 211(5):781–790. https://doi.org/10.1084/jem.20131916

Osselaere A, Santos R, Hautekiet V et al (2013) Deoxynivalenol impairs hepatic and intestinal gene expression of selected oxidative stress, tight junction and inflammation proteins in broiler chickens, but addition of an adsorbing agent shifts the effects to the distal parts of the small intestine. PLoS ONE 8(7):e69014. https://doi.org/10.1371/journal.pone.0069014 PubMed DOI PMC

Peng Z, Liao Y, Wang X et al (2020) Heme oxygenase-1 regulates autophagy through carbon-oxygen to alleviate deoxynivalenol-induced hepatic damage. Arch Toxicol 94(2):573–588. https://doi.org/10.1007/s00204-019-02649-6 PubMed DOI

Pestka JJ (2010) Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch Toxicol 84(9):663–679. https://doi.org/10.1007/s00204-010-0579-8 PubMed DOI

Prabhakar NR, Semenza GL (2012) Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol Rev 92(3):967–1003. https://doi.org/10.1152/physrev.00030.2011 PubMed DOI PMC

Raghubeer S, Nagiah S, Chuturgoon A (2019) Ochratoxin A upregulates biomarkers associated with hypoxia and transformation in human kidney cells. Toxicol In Vitro 57:211–216. https://doi.org/10.1016/j.tiv.2019.03.016 PubMed DOI

Rahal A, Kumar A, Singh V et al (2014) Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int 2014:761264. https://doi.org/10.1155/2014/761264 PubMed DOI PMC

Ren Z, Wang Y, Deng H et al (2015) Deoxynivalenol induces apoptosis in chicken splenic lymphocytes via the reactive oxygen species-mediated mitochondrial pathway. Environ Toxicol Pharmacol 39(1):339–346. https://doi.org/10.1016/j.etap.2014.11.028 PubMed DOI

Ren Z, Guo C, He H et al (2020) Effects of deoxynivalenol on mitochondrial dynamics and autophagy in pig spleen lymphocytes. Food Chem Toxicol 140:111357. https://doi.org/10.1016/j.fct.2020.111357 PubMed DOI

Ricklefs FL, Alayo Q, Krenzlin H, et al (2018) Immune evasion mediated by PD-L1 on glioblastoma-derived extracellular vesicles. Sci Adv 4(3):eaar2766. https://doi.org/10.1126/sciadv.aar2766

Rushing BR, Selim MI (2019) Aflatoxin B1: a review on metabolism, toxicity, occurrence in food, occupational exposure, and detoxification methods. Food Chem Toxicol 124:81–100. https://doi.org/10.1016/j.fct.2018.11.047 PubMed DOI

Schito L, Semenza GL (2016) Hypoxia-inducible factors: master regulators of cancer progression. Trends Cancer 2(12):758–770. https://doi.org/10.1016/j.trecan.2016.10.016 PubMed DOI

Shadel GS, Horvath TL (2015) Mitochondrial ROS signaling in organismal homeostasis. Cell 163(3):560–569. https://doi.org/10.1016/j.cell.2015.10.001 PubMed DOI PMC

Song SL, Tan J, Miao YY, Li MM, Zhang Q (2017) Crosstalk of autophagy and apoptosis: involvement of the dual role of autophagy under ER stress. J Cell Physiol 232(11):2977–2984. https://doi.org/10.1002/jcp.25785 PubMed DOI

Stachurska A, Kozakowska M, Jozkowicz A, Dulak J, Loboda A (2011) Aristolochic acid I and ochratoxin A differentially regulate VEGF expression in porcine kidney epithelial cells–the involvement of SP-1 and HIFs transcription factors. Toxicol Lett 204(2–3):118–126. https://doi.org/10.1016/j.toxlet.2011.04.022 PubMed DOI PMC

Takahashi A, Hanson MG, Norell HR et al (2005) Preferential cell death of CD8+ effector memory (CCR7-CD45RA-) T cells by hydrogen peroxide-induced oxidative stress. J Immunol 174(10):6080–6087. https://doi.org/10.4049/jimmunol.174.10.6080 PubMed DOI

Tang XL, Yang XY, Jung HJ et al (2009) Asiatic acid induces colon cancer cell growth inhibition and apoptosis through mitochondrial death cascade. Biol Pharm Bull 32(8):1399–1405. https://doi.org/10.1248/bpb.32.1399 PubMed DOI

Tang Y, Li J, Li F et al (2015) Autophagy protects intestinal epithelial cells against deoxynivalenol toxicity by alleviating oxidative stress via IKK signaling pathway. Free Radic Biol Med 89:944–951. https://doi.org/10.1016/j.freeradbiomed.2015.09.012 PubMed DOI

Taylor MJ, Reddy RV, Sharma RP (1985) Immunotoxicity of repeated low level exposure to T-2 toxin, a trichothecene mycotoxin, in CD-1 mice. Mycotoxin Res 1(2):57–64. https://doi.org/10.1007/bf03192004 PubMed DOI

Tian J, Yan J, Wang W et al (2012) T-2 toxin enhances catabolic activity of hypertrophic chondrocytes through ROS-NF-kappaB-HIF-2alpha pathway. Toxicol In Vitro 26(7):1106–1113. https://doi.org/10.1016/j.tiv.2012.07.002 PubMed DOI

Upadhyay S, Vaish S, Dhiman M (2019) Hydrogen peroxide-induced oxidative stress and its impact on innate immune responses in lung carcinoma A549 cells. Mol Cell Biochem 450(1–2):135–147. https://doi.org/10.1007/s11010-018-3380-2 PubMed DOI

Vari F, Arpon D, Keane C et al (2018) Immune evasion via PD-1/PD-L1 on NK cells and monocyte/macrophages is more prominent in Hodgkin lymphoma than DLBCL. Blood 131(16):1809–1819. https://doi.org/10.1182/blood-2017-07-796342 PubMed DOI PMC

Wan MLY, Turner PC, Co VA, Wang MF, Amiri KMA, El-Nezami H (2019) Schisandrin A protects intestinal epithelial cells from deoxynivalenol-induced cytotoxicity, oxidative damage and inflammation. Sci Rep 9(1):19173. https://doi.org/10.1038/s41598-019-55821-4 PubMed DOI PMC

Wang GL, Semenza GL (1995) Purification and characterization of hypoxia-inducible factor 1. J Biol Chem 270(3):1230–1237. https://doi.org/10.1074/jbc.270.3.1230 PubMed DOI

Wang X, Xu W, Fan M et al (2016) Deoxynivalenol induces apoptosis in PC12 cells via the mitochondrial pathway. Environ Toxicol Pharmacol 43:193–202. https://doi.org/10.1016/j.etap.2016.03.016 PubMed DOI

Wang J, Jin Y, Wu S et al (2019) Deoxynivalenol induces oxidative stress, inflammatory response and apoptosis in bovine mammary epithelial cells. J Anim Physiol Anim Nutr (Berl) 103(6):1663–1674. https://doi.org/10.1111/jpn.13180 DOI

Wang X, Jiang Y, Zhu L et al (2020) Autophagy protects PC12 cells against deoxynivalenol toxicity via the Class III PI3K/beclin 1/Bcl-2 pathway. J Cell Physiol 235(11):7803–7815. https://doi.org/10.1002/jcp.29433 PubMed DOI

Wu QH, Wang X, Yang W et al (2014) Oxidative stress-mediated cytotoxicity and metabolism of T-2 toxin and deoxynivalenol in animals and humans: an update. Arch Toxicol 88(7):1309–1326. https://doi.org/10.1007/s00204-014-1280-0 PubMed DOI

Wu Q, Wang X, Nepovimova E et al (2017) Trichothecenes: immunomodulatory effects, mechanisms, and anti-cancer potential. Arch Toxicol 91(12):3737–3785. https://doi.org/10.1007/s00204-017-2118-3 PubMed DOI

Wu J, Zhou Y, Yuan Z et al (2019) Autophagy and apoptosis interact to modulate T-2 toxin-induced toxicity in liver cells. Toxins (Basel) 11(1):45. https://doi.org/10.3390/toxins11010045 DOI

Wu J, Chen JX, He JH (2020) T-2 toxin-induced DRP-1-dependent mitophagy leads to the apoptosis of mice Leydig cells (TM3). Food Chem Toxicol 136:111082. https://doi.org/10.1016/j.fct.2019.111082 PubMed DOI

Wu Q, Wu W, Kuca K (2020) From hypoxia and hypoxia-inducible factors (HIF) to oxidative stress: a new understanding of the toxic mechanism of mycotoxins. Food Chem Toxicol 135:110968. https://doi.org/10.1016/j.fct.2019.110968 PubMed DOI

Xie MY, Chen T, Xi QY et al (2020) Porcine milk exosome miRNAs protect intestinal epithelial cells against deoxynivalenol-induced damage. Biochem Pharmacol 175:113898. https://doi.org/10.1016/j.bcp.2020.113898 PubMed DOI

Xu X, Wei Y, Shah MK et al (2020) Effects of compound active peptides on protecting liver and intestinal epithelial cells from damages and preventing hyperglycemia. Oxid Med Cell Longev 2020:3183104. https://doi.org/10.1155/2020/3183104 PubMed DOI PMC

Xu X, Yan G, Chang J et al (2020) Astilbin ameliorates deoxynivalenol-induced oxidative stress and apoptosis in intestinal porcine epithelial cells (IPEC-J2). J Appl Toxicol 40(10):1362–1372. https://doi.org/10.1002/jat.3989 PubMed DOI

Yan Y, Jiang W, Tan Y et al (2017) hucMSC exosome-derived GPX1 is required for the recovery of hepatic oxidant injury. Mol Ther 25(2):465–479. https://doi.org/10.1016/j.ymthe.2016.11.019 PubMed DOI PMC

Yang W, Yu M, Fu J et al (2014) Deoxynivalenol induced oxidative stress and genotoxicity in human peripheral blood lymphocytes. Food Chem Toxicol 64:383–396. https://doi.org/10.1016/j.fct.2013.12.012 PubMed DOI

Yang L, Yu Z, Hou J et al (2016) Toxicity and oxidative stress induced by T-2 toxin and HT-2 toxin in broilers and broiler hepatocytes. Food Chem Toxicol 87:128–137. https://doi.org/10.1016/j.fct.2015.12.003 PubMed DOI

Yang JY, Zhang YF, Li YX, Meng XP, Bao JF (2018) l-arginine protects against oxidative damage induced by T-2 toxin in mouse Leydig cells. J Biochem Mol Toxicol 32(10):e22209. https://doi.org/10.1002/jbt.22209 PubMed DOI

Yang L, Tu D, Wang N et al (2019) The protective effects of DL-Selenomethionine against T-2/HT-2 toxins-induced cytotoxicity and oxidative stress in broiler hepatocytes. Toxicol In Vitro 54:137–146. https://doi.org/10.1016/j.tiv.2018.09.016 PubMed DOI

Yang X, Zhang X, Zhang J et al (2019) Spermatogenesis disorder caused by T-2 toxin is associated with germ cell apoptosis mediated by oxidative stress. Environ Pollut 251:372–379. https://doi.org/10.1016/j.envpol.2019.05.023 PubMed DOI

Yang J, Guo W, Wang J, Yang X, Zhang Z, Zhao Z (2020) T-2 toxin-induced oxidative stress leads to imbalance of mitochondrial fission and fusion to activate cellular apoptosis in the human liver 7702 cell line. Toxins (Basel) 12(1):43. https://doi.org/10.3390/toxins12010043 DOI

Yin H, Han S, Chen Y, Wang Y, Li D, Zhu Q (2020) T-2 toxin induces oxidative stress, apoptosis and cytoprotective autophagy in chicken hepatocytes. Toxins (Basel) 12(2):90. https://doi.org/10.3390/toxins12020090 DOI

Young MM, Takahashi Y, Khan O et al (2012) Autophagosomal membrane serves as platform for intracellular death-inducing signaling complex (iDISC)-mediated caspase-8 activation and apoptosis. J Biol Chem 287(15):12455–12468. https://doi.org/10.1074/jbc.M111.309104 PubMed DOI PMC

Yu M, Wei ZY, Xu ZH, Pan JQ, Chen JH (2018) Oxidative damage and Nrf2 translocation induced by toxicities of deoxynivalenol on the placental and embryo on gestation day 12.5 d and 18.5 d. Toxins (Basel) 10(9):370. https://doi.org/10.3390/toxins10090370

Yu LM, Zhang WH, Han XX et al (2019) Hypoxia-induced ROS contribute to myoblast pyroptosis during obstructive sleep apnea via the NF-κB/HIF-1α signaling pathway. Oxid Med Cell Longev 2019:4596368. https://doi.org/10.1155/2019/4596368 PubMed DOI PMC

Yu M, Peng Z, Liao Y et al (2019) Deoxynivalenol-induced oxidative stress and Nrf2 translocation in maternal liver on gestation day 12.5d and 18.5d. Toxicon 161:17–22. https://doi.org/10.1016/j.toxicon.2019.02.018 PubMed DOI

Yu FF, Lin XL, Wang X, Ping ZG, Guo X (2019b) Comparison of apoptosis and autophagy in human chondrocytes induced by the T-2 and HT-2 toxins. Toxins (Basel). https://doi.org/10.3390/toxins11050260

Yuan G, Nanduri J, Khan S, Semenza GL, Prabhakar NR (2008) Induction of HIF-1alpha expression by intermittent hypoxia: involvement of NADPH oxidase, Ca2+ signaling, prolyl hydroxylases, and mTOR. J Cell Physiol 217(3):674–685. https://doi.org/10.1002/jcp.21537 PubMed DOI PMC

Zhang H, Lu H, Xiang L et al (2015) HIF-1 regulates CD47 expression in breast cancer cells to promote evasion of phagocytosis and maintenance of cancer stem cells. Proc Natl Acad Sci USA 112(45):E6215–E6223. https://doi.org/10.1073/pnas.1520032112 PubMed DOI

Zhang YF, Yang JY, Li YK, Zhou W (2017) Toxicity and oxidative stress induced by T-2 toxin in cultured mouse Leydig cells. Toxicol Mech Methods 27(2):100–106. https://doi.org/10.1080/15376516.2016.1258747 PubMed DOI

Zhang W, Zhou X, Yao Q, Liu Y, Zhang H, Dong Z (2017) HIF-1-mediated production of exosomes during hypoxia is protective in renal tubular cells. Am J Physiol Renal Physiol 313(4):F906–F913. https://doi.org/10.1152/ajprenal.00178.2017 PubMed DOI PMC

Zhang YF, Su PK, Wang LJ et al (2018) T-2 toxin induces apoptosis via the Bax-dependent caspase-3 activation in mouse primary Leydig cells. Toxicol Mech Methods 28(1):23–28. https://doi.org/10.1080/15376516.2017.1354413 PubMed DOI

Zhang J-Q, Ren Q-L, Chen J-F et al (2020) Autophagy contributes to oxidative stress-induced apoptosis in porcine granulosa cells. Reprod Sci. https://doi.org/10.1007/s43032-020-00340-1 PubMed DOI PMC

Zhang J, You L, Wu W et al (2020) The neurotoxicity of trichothecenes T-2 toxin and deoxynivalenol (DON): current status and future perspectives. Food Chem Toxicol 145:111676. https://doi.org/10.1016/j.fct.2020.111676 PubMed DOI

Zou J, Fei Q, Xiao H et al (2019) VEGF-A promotes angiogenesis after acute myocardial infarction through increasing ROS production and enhancing ER stress-mediated autophagy. J Cell Physiol 234(10):17690–17703. https://doi.org/10.1002/jcp.28395 PubMed DOI

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