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Zearalenone and the Immune Response: Comparison
Please note this is a comparison between Version 2 by Conner Chen and Version 1 by Daniela Eliza Marin.

Zearalenone (ZEA) is an estrogenic fusariotoxin, being classified as a phytoestrogen, or as a mycoestrogen. ZEA and its metabolites are able to bind to estrogen receptors, 17β-estradiol specific receptors, leading to reproductive disorders which include low fertility, abnormal fetal development, reduced litter size and modification at the level of reproductive hormones especially in female pigs. ZEA has also significant effects on immune response with immunostimulatory or immunosuppressive results. This review presents the effects of ZEA and its derivatives on all levels of the immune response such as innate immunity with its principal component inflammatory response as well as the acquired immunity with two components, humoral and cellular immune response. The mechanisms involved by ZEA in triggering its effects are addressed. 

  • zearalenone
  • cell immunity
  • humoral immunity
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References

  1. Bakker, M.G.; Brown, D.W.; Kelly, A.C.; Kim, H.-S.; Kurtzman, C.P.; Mccormick, S.P.; O’Donnell, K.L.; Proctor, R.H.; Vaughan, M.M.; Ward, T.J. Fusarium mycotoxins: A trans-disciplinary overview. Can. J. Plant Pathol. 2018, 40, 161–171.
  2. Rai, A.; Das, M.; Tripathi, A. Occurrence and toxicity of a fusarium mycotoxin, zearalenone. Crit. Rev. Food Sci. Nutr. 2020, 60, 2710–2729.
  3. Cavret, S.; Lecoeur, S. Fusariotoxin transfer in animal. Food Chem. Toxicol. 2006, 44, 444–453.
  4. Ünüsan, N. Systematic review of mycotoxins in food and feeds in Turkey. Food Control 2019, 97, 1–14.
  5. Aiko, V.; Mehta, A. Occurrence, detection and detoxification of mycotoxins. J. Biosci. 2015, 40, 943–954.
  6. Eriksen, G.S.; Pettersson, H.; Lindberg, J.E. Absorption, metabolism and excretion of 3-acetyl DON in pigs. Arch. Tierernahr. 2003, 57, 335–345.
  7. Kamle, M.; Mahato, D.K.; Devi, S.; Lee, K.E.; Kang, S.G.; Kumar, P. Fumonisins: Impact on Agriculture, Food, and Human Health and their Management Strategies. Toxins 2019, 11, 328.
  8. Rodríguez-Blanco, M.; Ramos, A.J.; Sanchis, V.; Marín, S. Mycotoxins occurrence and fungal populations in different types of silages for dairy cows in Spain. Fungal Biol. 2019.
  9. Rogowska, A.; Pomastowski, P.; Sagandykova, G.; Buszewski, B. Zearalenone and its metabolites: Effect on human health, metabolism and neutralisation methods. Toxicon 2019, 162, 46–56.
  10. Maragos, C. Zearalenone occurrence and human exposure. World Mycotoxin J. 2010, 3.
  11. Złoch, M.; Rogowska, A.; Pomastowski, P.; Railean-Plugaru, V.; Walczak-Skierska, J.; Rudnicka, J.; Buszewski, B. Use of Lactobacillus paracasei strain for zearalenone binding and metabolization. Toxicon 2020, 181, 9–18.
  12. Jia, R.; Liu, W.; Zhao, L.; Cao, L.; Shen, Z. Low doses of individual and combined deoxynivalenol and zearalenone in naturally moldy diets impair intestinal functions via inducing inflammation and disrupting epithelial barrier in the intestine of piglets. Toxicol. Lett. 2020, 333, 159–169.
  13. Zhou, J.; Zhu, L.; Chen, J.; Wang, W.; Zhang, R.; Li, Y.; Zhang, Q.; Wang, W. Degradation mechanism for Zearalenone ring-cleavage by Zearalenone hydrolase RmZHD: A QM/MM study. Sci. Total Environ. 2020, 709, 135897.
  14. Kowalska, K.; Habrowska-Górczyńska, D.E.; Piastowska-Ciesielska, A.W. Zearalenone as an endocrine disruptor in humans. Environ. Toxicol. Pharmacol. 2016, 48, 141–149.
  15. Busk, Ø.L.; Ndossi, D.; Verhaegen, S.; Connolly, L.; Eriksen, G.; Ropstad, E.; Sørlie, M. Relative quantification of the proteomic changes associated with the mycotoxin zearalenone in the H295R steroidogenesis model. Toxicon 2011, 58, 533–542.
  16. Zinedine, A.; Soriano, J.M.; Moltó, J.C.; Mañes, J. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: An oestrogenic mycotoxin. Food Chem. Toxicol. 2007, 45, 1–18.
  17. Rogowska, A.; Pomastowski, P.; Rafińska, K.; Railean-Plugaru, V.; Złoch, M.; Walczak, J.; Buszewski, B. A study of zearalenone biosorption and metabolisation by prokaryotic and eukaryotic cells. Toxicon 2019, 169, 81–90.
  18. Bennett, J.W.; Klich, M. Mycotoxins. Clin. Microbiol. Rev. 2003, 16, 497 LP–516.
  19. Marin, D.E.; Taranu, I.; Burlacu, R.; Manda, G.; Motiu, M.; Neagoe, I.; Dragomir, C.; Stancu, M.; Calin, L. Effects of zearalenone and its derivatives on porcine immune response. Toxicol. Vitr. 2011, 25, 1981–1988.
  20. Chang, S.; Su, Y.; Sun, Y.; Meng, X.; Shi, B.; Shan, A. Response of the nuclear receptors PXR and CAR and their target gene mRNA expression in female piglets exposed to zearalenone. Toxicon 2018, 151, 111–118.
  21. Pierron, A.; Alassane-Kpembi, I.; Oswald, I.P. Impact of mycotoxin on immune response and consequences for pig health. Anim. Nutr. 2016, 2, 63–68.
  22. Groschwitz, K.R.; Hogan, S.P. Intestinal barrier function: Molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 2009, 124, 3–20.
  23. Vancamelbeke, M.; Vermeire, S. The intestinal barrier: A fundamental role in health and disease. Expert Rev. Gastroenterol. Hepatol. 2017, 11, 821–834.
  24. Lahjouji, T.; Bertaccini, A.; Neves, M.; Puel, S.; Oswald, I.P.; Soler, L. Acute Exposure to Zearalenone Disturbs Intestinal Homeostasis by Modulating the Wnt/β-Catenin Signaling Pathway. Toxins 2020, 12, 113.
  25. Lewczuk, B.; Przybylska-Gornowicz, B.; Gajęcka, M.; Targońska, K.; Ziółkowska, N.; Prusik, M.; Gajęcki, M. Histological structure of duodenum in gilts receiving low doses of zearalenone and deoxynivalenol in feed. Exp. Toxicol. Pathol. 2016, 68, 157–166.
  26. Gajęcka, M.; Tarasiuk, M.; Zielonka, Ł.; Dąbrowski, M.; Gajęcki, M. Risk assessment for changes in the metabolic profile and body weights of pre-pubertal gilts during long-term monotonic exposure to low doses of zearalenone (ZEN). Res. Vet. Sci. 2016, 109, 169–180.
  27. Liu, M.; Gao, R.; Meng, Q.; Zhang, Y.; Bi, C.; Shan, A. Toxic Effects of Maternal Zearalenone Exposure on Intestinal Oxidative Stress, Barrier Function, Immunological and Morphological Changes in Rats. PLoS One 2014, 9, 1–14.
  28. Zheng, W.-L.; Wang, B.-J.; Wang, L.; Shan, Y.-P.; Zou, H.; Song, R.-L.; Wang, T.; Gu, J.-H.; Yuan, Y.; Liu, X.-Z.; et al. ROS-Mediated Cell Cycle Arrest and Apoptosis Induced by Zearalenone in Mouse Sertoli Cells via ER Stress and the ATP/AMPK Pathway. Toxins 2018, 10, 24.
  29. Johansson, M.E.V.; Hansson, G.C. Mucus and the Goblet Cell. Dig. Dis. 2013, 31, 305–309.
  30. Wang, X.; Yu, H.; Fang, H.; Zhao, Y.; Jin, Y.; Shen, J.; Zhou, C.; Zhou, Y.; Fu, Y.; Wang, J.; et al. Transcriptional profiling of zearalenone-induced inhibition of IPEC-J2 cell proliferation. Toxicon 2019, 172, 8–14.
  31. Marin, D.; Motiu, M.; Taranu, I. Food Contaminant Zearalenone and Its Metabolites Affect Cytokine Synthesis and Intestinal Epithelial Integrity of Porcine Cells. Toxins 2015, 7, 1979–1988.
  32. Taranu, I.; Marin, D.E.; Pistol, G.C.; Motiu, M.; Pelinescu, D. Induction of pro-inflammatory gene expression by Escherichia coli and mycotoxin zearalenone contamination and protection by a Lactobacillus mixture in porcine IPEC-1 cells. Toxicon 2015, 97, 53–63.
  33. Fan, W.; Lv, Y.; Ren, S.; Shao, M.; Shen, T.; Huang, K.; Zhou, J.; Yan, L.; Song, S. Zearalenone (ZEA)-induced intestinal inflammation is mediated by the NLRP3 inflammasome. Chemosphere 2018, 190, 272–279.
  34. Long, M.; Chen, X.; Wang, N.; Wang, M.; Pan, J.; Tong, J.; Li, P.; Yang, S.; He, J. Proanthocyanidins Protect Epithelial Cells from Zearalenone-Induced Apoptosis via Inhibition of Endoplasmic Reticulum Stress-Induced Apoptosis Pathways in Mouse Small Intestines. Molecules 2018, 23, 1508.
  35. Ben Salem, I.; Prola, A.; Boussabbeh, M.; Guilbert, A.; Bacha, H.; Abid-Essefi, S.; Lemaire, C. Crocin and Quercetin protect HCT116 and HEK293 cells from Zearalenone-induced apoptosis by reducing endoplasmic reticulum stress. Cell Stress Chaperones 2015, 20, 927–938.
  36. Obremski, K.; Gonkowski, S.; Wojtacha, P. Zearalenone-induced changes in the lymphoid tissue and mucosal nerve fibers in the porcine ileum. Pol. J. Vet. Sci. 2015, 18, 357–365.
  37. Islam, M.R.; Kim, J.W.; Roh, Y.-S.; Kim, J.-H.; Han, K.M.; Kwon, H.-J.; Lim, C.W.; Kim, B. Evaluation of immunomodulatory effects of zearalenone in mice. J. Immunotoxicol. 2017, 14, 125–136.
  38. Kato, L.M.; Kawamoto, S.; Maruya, M.; Fagarasan, S. Gut TFH and IgA: Key players for regulation of bacterial communities and immune homeostasis. Immunol. Cell Biol. 2014, 92, 49–56.
  39. Okumura, R.; Takeda, K. Maintenance of intestinal homeostasis by mucosal barriers. Inflamm. Regen. 2018, 38, 5.
  40. Wang, X.; Yu, H.; Shan, A.; Jin, Y.; Fang, H.; Zhao, Y.; Shen, J.; Zhou, C.; Zhou, Y.; Fu, Y.; et al. Toxic effects of Zearalenone on intestinal microflora and intestinal mucosal immunity in mice. Food Agric. Immunol. 2018, 29, 1002–1011.
  41. Linden, S.K.; Sutton, P.; Karlsson, N.G.; Korolik, V.; McGuckin, M.A. Mucins in the mucosal barrier to infection. Mucosal Immunol. 2008, 1, 183–197.
  42. Wan, L.-Y.M.; Allen, K.J.; Turner, P.C.; El-Nezami, H. Modulation of Mucin mRNA (MUC5AC and MUC5B) Expression and Protein Production and Secretion in Caco-2/HT29-MTX Co-cultures Following Exposure to Individual and Combined Fusarium Mycotoxins. Toxicol. Sci. 2014, 139, 83–98.
  43. Wan, M.L.-Y.; Woo, C.-S.J.; Allen, K.J.; Turner, P.C.; El-Nezami, H. Modulation of Porcine β-Defensins 1 and 2 upon Individual and Combined Fusarium Toxin Exposure in a Swine Jejunal Epithelial Cell Line. Appl. Environ. Microbiol. 2013, 79, 2225–2232.
  44. Taranu, I.; Braicu, C.; Marin, D.E.; Pistol, G.C.; Motiu, M.; Balacescu, L.; Beridan Neagoe, I.; Burlacu, R. Exposure to zearalenone mycotoxin alters in vitro porcine intestinal epithelial cells by differential gene expression. Toxicol. Lett. 2015, 232, 310–325.
  45. Braicu, C.; Selicean, S.; Cojocneanu-Petric, R.; Lajos, R.; Balacescu, O.; Taranu, I.; Marin, D.E.; Motiu, M.; Jurj, A.; Achimas-Cadariu, P.; et al. Evaluation of cellular and molecular impact of zearalenone and Escherichia coli co-exposure on IPEC-1 cells using microarray technology. BMC Genomics 2016, 17, 576.
  46. Benthem de Grave, X.; Saltzmann, J.; Laurain, J.; Rodriguez, M.A.; Molist, F.; Dänicke, S.; Santos, R.R. Transmission of Zearalenone, Deoxynivalenol, and Their Derivatives from Sows to Piglets during Lactation. Toxins 2021, 13, 37.
  47. Medzhitov, R.; Janeway, C.J. Innate immune recognition: Mechanisms and pathways. Immunol. Rev. 2000, 173, 89–97.
  48. Shaw, A.C.; Joshi, S.; Greenwood, H.; Panda, A.; Lord, J.M. Aging of the innate immune system. Curr. Opin. Immunol. 2010, 22, 507–513.
  49. Edreva, A. Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agric. Ecosyst. Environ. 2005, 106, 119–133.
  50. Chen, X.; Song, M.; Zhang, B.; Zhang, Y. Reactive Oxygen Species Regulate T Cell Immune Response in the Tumor Microenvironment. Oxid. Med. Cell. Longev. 2016, 2016, 1580967.
  51. Wang, J.; Wei, Z.; Han, Z.; Liu, Z.; Zhu, X.; Li, X.; Wang, K.; Yang, Z. Zearalenone Induces Estrogen-Receptor-Independent Neutrophil Extracellular Trap Release in Vitro. J. Agric. Food Chem. 2019, 67.
  52. Marin, D.E.; Taranu, I.; Burlacu, R.; Tudor, D.S. Effects of zearalenone and its derivatives on the innate immune response of swine. Toxicon 2010, 56, 956–963.
  53. Murata, H.; Sultana, P.; Shimada, N.; Yoshioka, M. Structure-activity relationships among zearalenone and its derivatives based on bovine neutrophil chemiluminescence. Vet. Hum. Toxicol. 2003, 45, 18—20.
  54. Borutova, R.; Faix, S.; Placha, I.; Gresakova, L.; Cobanova, K.; Leng, L. Effects of deoxynivalenol and zearalenone on oxidative stress and blood phagocytic activity in broilers. Arch. Anim. Nutr. 2008, 62, 303–312.
  55. Solhaug, A.; Karlsøen, L.M.; Holme, J.A.; Kristoffersen, A.B.; Eriksen, G.S. Immunomodulatory effects of individual and combined mycotoxins in the THP-1 cell line. Toxicol. Vitr. 2016, 36, 120–132.
  56. Chen, F.; Li, Q.; Zhang, Z.; Lin, P.; Lei, L.; Wang, A.; Jin, Y. Endoplasmic Reticulum Stress Cooperates in Zearalenone-Induced Cell Death of RAW 264.7 Macrophages. Int. J. Mol. Sci. 2015, 16, 19780–19795.
  57. Hueza, I.; Raspantini, P.; Raspantini, L.; Latorre, A.; Górniak, S. Zearalenone, an Estrogenic Mycotoxin, Is an Immunotoxic Compound. Toxins 2014, 6, 1080–1095.
  58. Skiepko, N.; Przybylska-Gornowicz, B.; Gajęcka, M.; Gajęcki, M.; Lewczuk, B. Effects of Deoxynivalenol and Zearalenone on the Histology and Ultrastructure of Pig Liver. Toxins 2020, 12, 463.
  59. Oswald, I.I.; Bouhet, S.; Marin, D.E.; Pinton, P.P.; Taranu, I. Mycotoxin effects on the pig immune system. Feed Compd. 2003, 09, 16–20.
  60. Peveri, P.; Walz, A.; Dewald, B.; Baggiolini, M. A novel neutrophil-activating factor produced by human mononuclear phagocytes. J. Exp. Med. 1988, 167, 1547–1559.
  61. Ding, J.; Yeh, C.-R.; Sun, Y.; Lin, C.; Chou, J.; Ou, Z.; Chang, C.; Qi, J.; Yeh, S. Estrogen receptor β promotes renal cell carcinoma progression via regulating LncRNA HOTAIR-miR-138/200c/204/217 associated CeRNA network. Oncogene 2018, 37, 5037–5053.
  62. Ruh, M.F.; Bi, Y.; Cox, L.; Berk, D.; Howlett, A.C.; Bellone, C.J. Effect of environmental estrogens on IL-1beta promoter activity in a macrophage cell line. Endocrine 1998, 9, 207–211.
  63. Seyed Toutounchi, N.; Hogenkamp, A.; Varasteh, S.; van’t Land, B.; Garssen, J.; Kraneveld, A.D.; Folkerts, G.; Braber, S. Fusarium Mycotoxins Disrupt the Barrier and Induce IL-6 Release in a Human Placental Epithelium Cell Line. Toxins 2019, 11, 665.
  64. Pistol, G.C.; Gras, M.A.; Marin, D.E.; Israel-Roming, F.; Stancu, M.; Taranu, I. Natural feed contaminant zearalenone decreases the expressions of important pro- and anti-inflammatory mediators and mitogen-activated protein kinase/NF-κB signalling molecules in pigs. Br. J. Nutr. 2014, 111, 452–464.
  65. Abbès, S.; Salah-Abbès, J.B.; Sharafi, H.; Noghabi, K.A.; Oueslati, R. Interaction of Lactobacillus plantarum MON03 with Tunisian Montmorillonite clay and ability of the composite to immobilize Zearalenone in vitro and counteract immunotoxicity in vivo. Immunopharmacol. Immunotoxicol. 2012, 34, 944–950.
  66. Salah-Abbès, J.; Abbes, S.; Houas, Z.; Abdel-Wahhab, P.M.; Oueslati, R. Zearalenone induces immunotoxicity in mice: Possible protective effects of Radish extract (Raphanus Sativus). J. Pharm. Pharmacol. 2008, 60, 761–770.
  67. Ben Salah-Abbès, J.; Belgacem, H.; Ezzdini, K.; Abdel-Wahhab, M.A.; Abbès, S. Zearalenone nephrotoxicity: DNA fragmentation, apoptotic gene expression and oxidative stress protected by Lactobacillus plantarum MON03. Toxicon 2020, 175, 28–35.
  68. Del Fabbro, L.; Jesse, C.R.; de Gomes, M.G.; Borges Filho, C.; Donato, F.; Souza, L.C.; Goes, A.R.; Furian, A.F.; Boeira, S.P. The flavonoid chrysin protects against zearalenone induced reproductive toxicity in male mice. Toxicon 2019, 165, 13–21.
  69. Virk, P.; Al-mukhaizeem, N.A.R.; Bin Morebah, S.H.; Fouad, D.; Elobeid, M. Protective effect of resveratrol against toxicity induced by the mycotoxin, zearalenone in a rat model. Food Chem. Toxicol. 2020, 146, 111840.
  70. Yin, S.; Zhang, Y.; Gao, R.; Cheng, B.; Shan, A. The immunomodulatory effects induced by dietary Zearalenone in pregnant rats. Immunopharmacol. Immunotoxicol. 2014, 36, 187–194.
  71. Abbès, S.; Salah-Abbès, J.B.; Ouanes, Z.; Houas, Z.; Othman, O.; Bacha, H.; Abdel-Wahhab, M.A.; Oueslati, R. Preventive role of phyllosilicate clay on the Immunological and Biochemical toxicity of zearalenone in Balb/c mice. Int. Immunopharmacol. 2006, 6, 1251–1258.
  72. Choi, B.-K.; Cho, J.-H.; Jeong, S.-H.; Shin, H.-S.; Son, S.-W.; Yeo, Y.-K.; Kang, H.-G. Zearalenone affects immune-related parameters in lymphoid organs and serum of rats vaccinated with porcine parvovirus vaccine. Toxicol. Res. 2012, 28, 279–288.
  73. Wu, F.; Cui, J.; Yang, X.; Liu, S.; Han, S.; Chen, B. Effects of zearalenone on genital organ development, serum immunoglobulin, antioxidant capacity, sex hormones and liver function of prepubertal gilts. Toxicon 2021, 189, 39–44.
  74. Reddy, K.; Lee, W.; Lee, S.; Jeong, J.; Kim, D.; Kim, M.; Lee, H.; Oh, Y.; Jo, H. Effects of dietary deoxynivalenol and zearalenone on the organ pro-inflammatory gene expressions and serum immunoglobulins of pigs. J. Anim. Sci. 2017, 95, 203.
  75. Ren, Z.H.; Zhou, R.; Deng, J.L.; Zuo, Z.C.; Peng, X.; Wang, Y.C.; Wang, Y.; Yu, S.M.; Shen, L.H.; Cui, H.M.; et al. Effects of the Fusarium toxin zearalenone (ZEA) and/or deoxynivalenol (DON) on the serum IgA, IgG and IgM levels in mice. Food Agric. Immunol. 2014, 25, 600–606.
  76. Yang, L.; Yang, W.; Feng, Q.; Huang, L.; Zhang, G.; Liu, F.; Jiang, S.; Yang, Z. Effects of purified zearalenone on selected immunological measurements of blood in post-weaning gilts. Anim. Nutr. 2016, 2, 142–148.
  77. Forsell, J.H.; Witt, M.F.; Tai, J.-H.; Jensen, R.; Pestka, J.J. Effects of 8-week exposure of the B6C3F1 mouse to dietary deoxynivalenol (vomitoxin) and zearalenone. Food Chem. Toxicol. 1986, 24, 213–219.
  78. Jakovac-Strajn, B.; Vengušt, A.; Pestevšek, U. Effects of a deoxynivalenol-contaminated diet on the reproductive performance and immunoglobulin concentrations in pigs. Vet. Rec. 2009, 165, 713–718.
  79. Pestka, J.J.; Tai, J.-H.; Witt, M.F.; Dixon, D.E.; Forsell, J.H. Suppression of immune response in the B6C3F1 mouse after dietary exposure to the fusarium mycotoxins deoxynivalenol (vomitoxin) and zearalenone. Food Chem. Toxicol. 1987, 25, 297–304.
  80. Teixeira, L.C.; Montiani-Ferreira, F.; Locatelli-Dittrich, R.; Santin, E.; Alberton, G.C. Effects of zearalenone in prepubertal gilts. Pesqui. Veterinária Bras. 2011, 31, 656–662.
  81. Antonissen, G.; Martel, A.; Pasmans, F.; Ducatelle, R.; Verbrugghe, E.; Vandenbroucke, V.; Li, S.; Haesebrouck, F.; Van Immerseel, F.; Croubels, S. The Impact of Fusarium Mycotoxins on Human and Animal Host Susceptibility to Infectious Diseases. Toxins 2014, 6.
  82. Wang, Y.C.; Deng, J.L.; Xu, S.W.; Peng, X.; Zuo, Z.C.; Cui, H.M.; Wang, Y.; Ren, Z.H. Effects of Zearalenone on IL-2, IL-6, and IFN-? mRNA Levels in the Splenic Lymphocytes of Chickens. Sci. World J. 2012, 2012, 567327.
  83. Berek, L.; Petri, I.B.; Mesterházy, Á.; Téren, J.; Molnár, J. Effects of mycotoxins on human immune functions in vitro. Toxicol. Vitr. 2001, 15, 25–30.
  84. Committee, E.S. Scientific opinion on genotoxicity testing strategies applicable to food and feed safety assessment. EFSA J. 2011, 9, 2379.
  85. Forsell, J.H.; Kateley, J.R.; Yoshizawa, T.; Pestka, J.J. Inhibition of mitogen-induced blastogenesis in human lymphocytes by T-2 toxin and its metabolites. Appl. Environ. Microbiol. 1985, 49, 1523 LP–1526.
  86. Forsell, J.H.; Pestka, J.J. Relation of 8-ketotrichothecene and zearalenone analog structure to inhibition of mitogen-induced human lymphocyte blastogenesis. Appl. Environ. Microbiol. 1985, 50, 1304 LP–1307.
  87. Vlata, Z.; Porichis, F.; Tzanakakis, G.; Tsatsakis, A.; Krambovitis, E. A study of zearalenone cytotoxicity on human peripheral blood mononuclear cells. Toxicol. Lett. 2006, 165, 274–281.
  88. Zhang, K.; Tan, X.; Li, Y.; Liang, G.; Ning, Z.; Ma, Y.; Li, Y. Transcriptional profiling analysis of Zearalenone-induced inhibition proliferation on mouse thymic epithelial cell line 1. Ecotoxicol. Environ. Saf. 2018, 153, 135–141.
  89. Zheng, W.; Fan, W.; Feng, N.; Lu, N.; Zou, H.; Gu, J.; Yuan, Y.; Liu, X.; Bai, J.; Bian, J.; et al. The Role of miRNAs in Zearalenone-Promotion of TM3 Cell Proliferation. Int. J. Environ. Res. Public Health 2019, 16, 1517.
  90. Swamy, H.V.L.N.; Smith, T.K.; Karrow, N.A.; Boermans, H.J. Effects of feeding blends of grains naturally contaminated with Fusarium mycotoxins on growth and immunological parameters of broiler chickens1. Poult. Sci. 2004, 83, 533–543.
  91. Delves, P.J.; Martin, S.J.; Burton, D.R.; Roitt, I.M. Roitt’s Essential Immunology, 13th ed.; Wiley-Blackwell: London, UK, 2017; ISBN 978-1-118-41577-1.
  92. Roitt, I. Roitt‘s Essential Immunology; Blackwell Publishing: London, UK, 2006.
  93. Dąbrowski, M.; Obremski, K.; Gajęcka, M.; Gajęcki, M.; Zielonka, Ł. Changes in the Subpopulations of Porcine Peripheral Blood Lymphocytes Induced by Exposure to Low Doses of Zearalenone (ZEN) and Deoxynivalenol (DON). Molecules 2016, 21, 557.
  94. Kostro, K.; Gajęcka, M.; Lisiecka, U.; Majer-Dziedzic, B.; Obremski, K.; Zielonka, Ł.; Gajęcki, M. Subpopulation of lymphocytes CD4 + and CD8 + in peripheral blood of sheep with zearalenone mycotoxicosis. Bull. Vet. Inst. Pulawy 2011, 55, 241–246.
  95. Cai, G.; Pan, S.; Feng, N.; Zou, H.; Gu, J.; Yuan, Y.; Liu, X.; Liu, Z.; Bian, J. Zearalenone inhibits T cell chemotaxis by inhibiting cell adhesion and migration related proteins. Ecotoxicol. Environ. Saf. 2019, 175, 263–271.
  96. Ren, Z.H.; Deng, H.D.; Wang, Y.C.; Deng, J.L.; Zuo, Z.C.; Wang, Y.; Peng, X.; Cui, H.M.; Fang, J.; Yu, S.M.; et al. The Fusarium toxin zearalenone and deoxynivalenol affect murine splenic antioxidant functions, interferon levels, and T-cell subsets. Environ. Toxicol. Pharmacol. 2016, 41, 195–200.
  97. Obremski, K.; Wojtacha, P.; Podlasz, P.; Żmigrodzka, M. The influence of experimental administration of low zearalenone doses on the expression of Th1 and Th2 cytokines and on selected subpopulations of lymphocytes in intestinal lymph nodes. Pol. J. Vet. Sci. 2015, 18, 489–497.
  98. Chen, P.; Liu, T.; Jiang, S.; Yang, Z.; Huang, L.; Liu, F. Effects of purified zearalenone on selected immunological and histopathologic measurements of spleen in post-weanling gilts. Anim. Nutr. 2017, 3, 212–218.
  99. Reddy, K.E.; Lee, W.; Jeong, J.Y.; Lee, Y.; Lee, H.-J.; Kim, M.S.; Kim, D.-W.; Yu, D.; Cho, A.; Oh, Y.K.; et al. Effects of deoxynivalenol- and zearalenone-contaminated feed on the gene expression profiles in the kidneys of piglets. Asian-Australas. J. Anim. Sci. 2018, 31, 138–148.
  100. Yu, J.-Y.; Zheng, Z.-H.; Son, Y.-O.; Shi, X.; Jang, Y.-O.; Lee, J.-C. Mycotoxin zearalenone induces AIF- and ROS-mediated cell death through p53- and MAPK-dependent signaling pathways in RAW264.7 macrophages. Toxicol. Vitr. 2011, 25, 1654–1663.
  101. Yang, L.-J.; Zhou, M.; Huang, L.-B.; Yang, W.-R.; Yang, Z.-B.; Jiang, S.-Z.; Ge, J.-S. Zearalenone-Promoted Follicle Growth through Modulation of Wnt-1/β-Catenin Signaling Pathway and Expression of Estrogen Receptor Genes in Ovaries of Postweaning Piglets. J. Agric. Food Chem. 2018, 66, 7899–7906.
  102. Song, T.; Yang, W.; Huang, L.; Yang, Z.; Jiang, S. Zearalenone exposure affects the Wnt/β-catenin signaling pathway and related genes of porcine endometrial epithelial cells in vitro. Asian-Australas J. Anim. Sci. 2020.
  103. Chen, F.; Wen, X.; Lin, P.; Chen, H.; Wang, A.; Jin, Y. HERP depletion inhibits zearalenone-induced apoptosis through autophagy activation in mouse ovarian granulosa cells. Toxicol. Lett. 2019, 301, 1–10.
  104. Zhang, G.-L.; Song, J.-L.; Zhou, Y.; Zhang, R.-Q.; Cheng, S.-F.; Sun, X.-F.; Qin, G.-Q.; Shen, W.; Li, L. Differentiation of sow and mouse ovarian granulosa cells exposed to zearalenone in vitro using RNA-seq gene expression. Toxicol. Appl. Pharmacol. 2018, 350, 78–90.
  105. Zhang, R.Q.; Sun, X.F.; Wu, R.Y.; Cheng, S.F.; Zhang, G.L.; Zhai, Q.Y.; Liu, X.L.; Zhao, Y.; Shen, W.; Li, L. Zearalenone exposure elevated the expression of tumorigenesis genes in mouse ovarian granulosa cells. Toxicol. Appl. Pharmacol. 2018, 356, 191–203.
  106. Cortinovis, C.; Caloni, F.; Schreiber, N.B.; Spicer, L.J. Effects of fumonisin B1 alone and combined with deoxynivalenol or zearalenone on porcine granulosa cell proliferation and steroid production. Theriogenology 2014, 81, 1042–1049.
  107. Pan, P.; Ma, F.; Wu, K.; Yu, Y.; Li, Y.; Li, Z.; Chen, X.; Huang, T.; Wang, Y.; Ge, R. Maternal exposure to zearalenone in masculinization window affects the fetal Leydig cell development in rat male fetus. Environ. Pollut. 2020, 263, 114357.
  108. Wang, S.; Ren, X.; Hu, X.; Zhou, L.; Zhang, C.; Zhang, M. Cadmium-induced apoptosis through reactive oxygen species-mediated mitochondrial oxidative stress and the JNK signaling pathway in TM3 cells, a model of mouse Leydig cells. Toxicol. Appl. Pharmacol. 2019, 368, 37–48.
  109. Cai, G.; Si, M.; Li, X.; Zou, H.; Gu, J.; Yuan, Y.; Liu, X.; Liu, Z.; Bian, J. Zearalenone induces apoptosis of rat Sertoli cells through Fas-Fas ligand and mitochondrial pathway. Environ. Toxicol. 2019, 34, 424–433.
  110. Márton, É.; Varga, A.; Széles, L.; Göczi, L.; Penyige, A.; Nagy, B.; Szilágyi, M. The Cell-Free Expression of MiR200 Family Members Correlates with Estrogen Sensitivity in Human Epithelial Ovarian Cells. Int. J. Mol. Sci. 2020, 21, 9725.
  111. Kowalska, K.; Habrowska-Górczyńska, D.E.; Domińska, K.; Urbanek, K.A.; Piastowska-Ciesielska, A.W. ERβ and NFκB—Modulators of Zearalenone-Induced Oxidative Stress in Human Prostate Cancer Cells. Toxins 2020, 12, 199.
  112. Minervini, F.; Dell’Aquila, M.E. Zearalenone and Reproductive Function in Farm Animals. Int. J. Mol. Sci. 2008, 9, 2570–2584.
  113. Chi, M.S.; Mirocha, C.J.; Kurtz, H.J.; Weaver, G.A.; Bates, F.; Robison, T.; Shimoda, W. Effect of Dietary Zearalenone on Growing Broiler Chicks1,2. Poult. Sci. 1980, 59, 531–536.
  114. Allen, N.K.; Mirocha, C.J.; Weaver, G.; Aakhus-Allen A, S.; Bates, F. Effects of Dietary Zearalenone on Finishing Broiler Chickens and Young Turkey Poults1,2. Poult. Sci. 1981, 60, 124–131.
  115. Kiessling, K.-H. The Effect of Zearalenone on Growth Rate, Organ Weight and Muscle Fibre Composition in Growing Rats. Acta Pharmacol. Toxicol. (Copenh). 1982, 51, 154–158.
  116. Denli, M.; Blandon, J.C.; Salado, S.; Guynot, M.E.; Pérez, J.F. Effect of dietary zearalenone on the performance, reproduction tract and serum biochemistry in young rats. J. Appl. Anim. Res. 2017, 45, 619–622.
  117. Chi, M.S.; Mirocha, C.J.; Weaver, G.A.; Kurtz, H.J. Effect of zearalenone on female White Leghorn chickens. Appl. Environ. Microbiol. 1980, 39, 1026–1030.
  118. Salah-Abbès, J.; Abbes, S.; Abdel-Wahhab, P.M.; Oueslati, R. Immunotoxicity of zearalenone in Balb/c mice in a high subchronic dosing study counteracted by Raphanus sativus extract. Immunopharmacol. Immunotoxicol. 2010, 32, 628–636.
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