Jump to ContentJump to Main Navigation
Show Summary Details
In This Section

Polish Journal of Veterinary Sciences

The Journal of Committee of Veterinary Sciences of Polish Academy of Sciences and University of Warmia and Mazury in Olsztyn

4 Issues per year

IMPACT FACTOR 2016: 0.697
5-year IMPACT FACTOR: 0.773

CiteScore 2016: 0.73

SCImago Journal Rank (SJR) 2016: 0.315
Source Normalized Impact per Paper (SNIP) 2016: 0.486

Open Access
See all formats and pricing
In This Section

MicroRNA expression profiles in liver and colon of sexually immature gilts after exposure to Fusarium mycotoxins

P. Brzuzan
  • Corresponding author
  • Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, Słoneczna 45G, 10-709 Olsztyn, Poland
  • Email:
/ M. Woźny
  • Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, Słoneczna 45G, 10-709 Olsztyn, Poland
/ L. Wolińska-Nizioł
  • Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, Słoneczna 45G, 10-709 Olsztyn, Poland
/ A. Piasecka
  • Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, Słoneczna 45G, 10-709 Olsztyn, Poland
/ M. Florczyk
  • Department of Environmental Biotechnology, Faculty of Environmental Sciences, University of Warmia and Mazury in Olsztyn, Słoneczna 45G, 10-709 Olsztyn, Poland
/ E. Jakimiuk
  • Department of Veterinary Prevention and Feed Hygiene, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Oczapowskiego 13, 10-950 Olsztyn, Poland
/ M. Góra
  • Department of Organic Chemistry, Faculty of Chemistry, Jagiellonian University, Ingardena 3, 30-060 Cracow, Poland
/ M.K. Łuczyński
  • Department of Chemistry, Faculty of Environmental Management and Agriculture, University of Warmia and Mazury in Olsztyn, Pl. Łódzki 4, 10-957 Olsztyn, Poland
/ M. Gajęcki
  • Department of Veterinary Prevention and Feed Hygiene, Faculty of Veterinary Medicine, University of Warmia and Mazury in Olsztyn, Oczapowskiego 13, 10-950 Olsztyn, Poland
Published Online: 2015-04-04 | DOI: https://doi.org/10.1515/pjvs-2015-0004


To improve our knowledge of the role of microRNAs (miRs) in responses of the porcine digestive system to two Fusarium mycotoxins, zearalenone (ZEN) and deoxynivalenol (DON), we examined the expression of 7 miRs (miR-9, miR-15a, miR-21, miR-34a, miR-122, miR-125b, and miR-192), previously found to be deregulated in diseased liver and colon cells. In this study, immature gilts were exposed to NOEL doses of ZEN (40 μg/kg/d), DON (12 μg/kg/d), ZEN+DON (40+12 μg/kg/d), and placebo (negative control group) for 7, 14, 21, 28, 35, and 42 days. Before the treatment, expression levels of the selected miRs were measured in the liver, the duodenum, the jejunum, and the ascending and the descending colon of the gilts. Hierarchical clustering of the tissues by their miR expression profiles was consistent with what would be expected based on the anatomical locations and the physiological functions of the organs, suggesting that functions of the miRs are related to the specificities of the tissues in which they are expressed. A subset of 2 pairs of miRs (miR-21+miR-192 and miR-15a+miR-34a), which were assigned to two distinct clusters based on their tissue abundance, was then evaluated in the liver and the ascending and the descending colon during the treatment. The most meaningful results were obtained from the ascending colon, where a significant effect of the treatment was observed, suggesting that during the exposure to mycotoxins, the pathways involved in cell proliferation and survival were disordered. Changes in miR expression in the liver and the descending colon of the treated gilts were smaller, and were associated more with treatment duration than the exposure to ZEN, DON, or ZEN+DON. Further research should focus on identification of genes whose expression is regulated by these aberrantly expressed miRs. This should facilitate understanding of the miRNA-regulated biological effects of mycotoxins.

Key words: deoxynivalenol; domestic pig; miRNA expression; zearalenone


  • Ahamed S, Foster JS, Bukovsky A, Wimalasena J (2001) Signal transduction through the Ras/Erk pathway is essential for the mycoestrogen zearalenone-induced cell-cycle progression in MCF-7 cells. Mol Carcinog 30: 88-98.Google Scholar

  • Ambros V (2004) The functions of animal microRNAs. Nature 431: 350-355.Google Scholar

  • Ason B, Darnell DK, Wittbrodt B, Berezikov E, Kloosterman WP, Wittbrodt J, Antin PB, Plasterk RH (2006) Differences in vertebrate microRNA expression. Proc Natl Acad Sci USA 103: 14385-14389.Google Scholar

  • Asslaber D, Piñón JD, Seyfried I, Desch P, Stöcher M, Tinhofer I, Egle A, Merkel O, Greil R (2010) micro-RNA-34a expression correlates with MDM2 SNP309 polymorphism and treatment-free survival in chronic lymphocytic leukemia. Blood 115: 4191-4197.Google Scholar

  • Bala S, Marcos M, Szabo G (2009) Emerging role of micro-RNAs in liver diseases. World J Gastroenterol 15: 5633-5640.Web of ScienceCrossrefGoogle Scholar

  • Betel D, Wilson M, Gabow A, Marks DS, Sander C (2008) The microRNA.org resource: targets and expression. Nucleic Acids Res 36: 149-153.Web of ScienceGoogle Scholar

  • Brzuzan P, Woźny M, Wolińska L, Piasecka A (2012) Expression profiling in vivo demonstrates rapid changes in liver microRNA levels of whitefish (Coregonus lavaretus) following microcystin-LR exposure. Aquat Toxicol 122-123: 188-196.Google Scholar

  • Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65: 6029-6033.Google Scholar

  • Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu CG, Kipps TJ, Negrini M, Croce CM (2005) miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA 102: 13944-13949.CrossrefGoogle Scholar

  • Fink-Gremmels J (1999) Mycotoxins: their implications for human and animal health. Vet Q 21: 115-120.Google Scholar

  • Fujita S, Ito T, Mizutani T, Minoguchi S, Yamamichi N, Sakurai K, Iba H (2008) miR-21 gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J Mol Biol 378: 492-504.Web of ScienceGoogle Scholar

  • Garzon R, Marcucci G, Croce CM (2010) Targeting micro-RNAs in cancer: rationale strategies and challenges. Nat Rev Drug Discov 9: 774-789.Web of ScienceGoogle Scholar

  • Georges SA, Biery MC, Kim SY, Schelter JM, Guo J, Chang AN, Jackson AL, Carleton MO, Linsley PS, Cleary MA, Chau BN (2008) Coordinated regulation of cell cycle transcripts by p53-inducible microRNAs, miR-192 and miR-215. Cancer Res 68: 10105-10112.Web of ScienceGoogle Scholar

  • Girard M, Jacquemin E, Munnich A, Lyonnet S, Henrion-Caude A (2008) miR-122, a paradigm for the role of microRNAs in the liver. J Hepatol 48: 648-656.Google Scholar

  • Glorian V, Maillot G, Poles S, Iacovoni JS, Favre G, Vagner S (2011) HuR-dependent loading of miRNA RISC to the mRNA encodnig the Ras-related small GTP-ase RhoB controls its translation during UV-induced apoptosis. Cell Death Differ 18: 1692-1701.Google Scholar

  • Hassen W, Ayed-Boussema I, Oscoz AA, Lopez AC, Bacha H (2007) The role of oxidative stress in zearalenone-mediated toxicity in Hep G2 cells: Oxidative DNA damage, gluthatione depletion and stress proteins induction. Toxicology 232: 294-302.Google Scholar

  • Hudder A, Novak RF (2008) miRNAs: Effectors of environmental influences on gene expression and disease. Toxicol Sci 103: 228-240.Web of ScienceGoogle Scholar

  • Jakimiuk E, Gajęcka M, Jana B, Brzuzan P, Zielonka Ł, Skorska-Wyszyńska E, Gajęcki M (2009) Factors determining sensitivity of prepubertal gilts to hormonal influence of zearalenone. Pol J Vet Sci 12: 149-158.PubMedGoogle Scholar

  • Kouadio JH, Mobioa TA, Baudrimont I, Moukha S, Dano SD, Creppy EE (2005) Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology 213: 56-65.Web of ScienceGoogle Scholar

  • Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, Fulci V, Chiaretti S, Foà R, Schliwka J, Fuchs U, Novosel A, Muller RU, Schermer B, Bissels U, Inman J, Phan Q, Chien M, Weir DB, Choksi R, De Vita G, Frezzetti D, Trompeter HI, Hornung V, Teng G, Hartmann G, Palkovits M, Di Lauro R, Wernet P, Macino G, Rogler CE, Nagle JW, Ju J, Papavasiliou FN, Benzing T, Lichter P, Tam W, Brownstein MJ, Bosio A, Borkhardt A, Russo JJ, Sander C, Zavolan M, Tuschl T (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129: 1401-1414.Web of ScienceGoogle Scholar

  • Liang Y, Ridzon D, Wong L, Chen C (2007) Characterization of microRNA expression profiles in normal human tissues. BMC Genomics 8: 166.CrossrefPubMedGoogle Scholar

  • Mei Y, Bian C, Li J, Du Z, Zhou H, Yang Z, Zhao RC (2013) miR-21 modulates the ERK-MAPK signaling pathway by regulating SPRY2 expression during human mesenchymal stem cell differentiation. J Cell Biochem 114: 1374-1384.Google Scholar

  • Meister G, Tuschl T (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431: 343-349.Google Scholar

  • Ofir M, Hacohen D, Ginsberg D (2011) MiR-15 and miR-16 are direct transcriptional targets of E2F1 that limit E2F-induced proliferation by targeting cyclin E. Mol Cancer Res 9: 440-447.CrossrefGoogle Scholar

  • Olsen CM, Meussen-Elholm ET, Hongslo JK, Stenersen J, Tollefsen KE (2005) Estrogenic effects of environmental chemicals: an interspecies comparison. Comp Biochem Physiol C Toxicol Pharmacol 141: 267-274.Google Scholar

  • Pestka JJ, Zhou HR, Moon Y, Chung YJ (2004) Cellular and molecular mechanisms for immune modulation by deoxynivalenol and other trichothecenes: unraveling a paradox. Toxicol Lett 153: 61-73.Google Scholar

  • Pinton P, Nougayrède JP, Del Rio JC, Moreno C, Marin DE, Ferrier L, Bracarense AP, Kolf-Clauw M, Oswald IP (2009) The food contaminant deoxynivalenol decreases intestinal barrier permeability and reduces claudin expression. Toxicol Appl Pharmacol 237: 41-48.Web of ScienceGoogle Scholar

  • Pinton P, Guzylack-Piriou L, Kolf-Clauw M, Oswald IP (2012) The effect on the intestine of some fungal toxins: the trichothecenes. Curr Immunol Rev 8: 193-208.CrossrefGoogle Scholar

  • Podolska A, Anthon C, Bak M, Tommerup N, Skovgaard K, Heegaard PM, Gorodkin J, Cirera S, Fredholm M (2012) Profiling microRNAs in lung tissue from pigs infected with Actinobacillus pleuropneumoniae. BMC Genomics 13: 459.PubMedCrossrefWeb of ScienceGoogle Scholar

  • Rotkrua P, Akiyama Y, Hashimoto Y, Otsubo T, Yuasa Y (2011) MiR-9 downregulates CDX2 expression in gastric cancer cells. Int J Cancer 129: 2611-2620.Google Scholar

  • Roy S, Sen CK (2011) MiRNA in innate immune responses: novel players in wound inflammation. Physiol Genomics 43: 557-565.Web of ScienceGoogle Scholar

  • Spachmo B, Arukwe A (2012) Endocrine and developmental effects in Atlantic salmon (Salmo salar) exposed to perfluorooctane sulfonic or perfluorooctane carboxylic acids. Aquat Toxicol 108: 112-124.Web of ScienceGoogle Scholar

  • Surdziel E, Cabanski M, Dallmann I, Lyszkiewicz M, Krueger A, Ganser A, Scherr M, Eder M (2011) Enforced expression of miR-125b affects myelopoiesis by targeting multiple signaling pathways. Blood 117: 4338-4348.Google Scholar

  • Takemura H, Shim JY, Sayama K, Tsubura A, Zhu BT, Shimoi K (2007) Characterization of the estrogenic activities of zearalenone and zeranol in vivo and in vitro. J Steroid Biochem Mol Biol 103: 170-177.Web of ScienceGoogle Scholar

  • Tarasov V, Jung P, Verdoodt B, Lodygin D, Epanchintsev A, Menssen A, Meister G, Hermeking H (2007) Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6: 1586-1593.Web of ScienceCrossrefGoogle Scholar

  • Tiemann U, Tomek W, Schneider F, Vanselow J (2003) Effects of the mycotoxins alpha- and beta-zearalenol on regulation of progesterone synthesis in cultured granulosa cells from porcine ovaries. Reprod Toxicol 17: 673-681.CrossrefPubMedGoogle Scholar

  • Tsai WC, Hsu SD, Hsu CS, Lai TC, Chen SJ, Shen R, Huang Y, Chen HC, Lee CH, Tsai TF, Hsu MT, Wu JC, Huang HD, Shiao MS, Hsiao M, Tsou AP (2012) Micro-RNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest 122(8): 2884-2897.Web of ScienceGoogle Scholar

  • Wu F, Zikusoka M, Trindade A, Dassopoulos T, Harris ML, Bayless TM, Brant SR, Chakravarti S, Kwon JH (2008) MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology 135: 1624-1635.Google Scholar

  • Ye L, Su X, Wu Z, Zheng X, Wang J, Zi C, Zhu G, Wu S, Bao W (2012) Analysis of Differential miRNA Expression in the Duodenum of Escherichia coli F18-Sensitive and -Resistant Weaned Piglets. PLoS ONE 7: e43741.CrossrefGoogle Scholar

  • Zhou HR, Jia Q, Pestka JJ (2005) Ribotoxic stress response to the trichothecene deoxynivalenol in the macrophage involves the SRC family kinase Hck. Toxicol Sci 85: 916-926.Google Scholar

  • Zinedine A, Soriano JM, Moltó JC, Mañes J (2007) Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem Toxicol 45: 1-18.PubMedCrossrefWeb of ScienceGoogle Scholar

About the article

Published Online: 2015-04-04

Published in Print: 2015-03-01

Citation Information: Polish Journal of Veterinary Sciences, ISSN (Online) 2300-2557, DOI: https://doi.org/10.1515/pjvs-2015-0004.

Export Citation

© Polish Academy of Sciences, Committee of Veterinary Sciences & University of Warmia and Mazury in Olsztyn. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Comments (0)

Please log in or register to comment.
Log in