Journal of fish pathology (한국어병학회지)

The Korean Society of Fish Pathology (한국어병학회)
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Effects of acetaminophen administration on liver histopathology, serum GOT/GPT levels and circulating microRNA-122 concentration in olive flounder (Paralichthys olivaceus)

  • Najib, Abdellaoui (Department of Aquatic Life Medicine, Pukyong National University) ;
  • Kim, Dong Soo (Department of Aquatic Life Medicine, Pukyong National University) ;
  • Kim, Ki Hong (Department of Aquatic Life Medicine, Pukyong National University)
  • Received : 2015.11.24
  • Accepted : 2016.04.22
  • Published : 2016.04.30
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Abstract

In human medicine, circulating microRNAs have been successfully utilized as early biomarkers for various abnormalities and disease states. Vertebrate miR-122 is a liver-specific microRNA which is expressed almost solely in hepatocytes and plays an important role in the regulation of hepatocyte function. In this study, to evaluate the potential utility of circulating miR-122 as a biomarker for liver injury in olive flounder (Paralichthys olivaceus), fish were orally intubated with two doses of acetaminophen (500 mg/kg or 1.000 mg/kg of body weight), and the expression of miR-122 in serum was quantified using real time-PCR. Histological change in liver, and the enzymatic activity of glutamic oxaloacetic transaminase (GOT) and glutamic pyruvic transaminase (GPT) were also analyzed. The results showed that miR-122 was higher in acetaminophen administered groups compared to control group. The histopathological effect of acetaminophen on olive flounder liver was not distinct. The serum level of GPT and GOT was increased within 2 folds compared to control group by acetaminophen administration. However, the serum miR-122 level was increased more than 3 or 4 folds compared to the control group by administration of 1000 mg/kg of acetaminophen. These results suggest the possible use of miR-122 as an indicator of liver injury in olive flounder, even when histopathological effects are not distinctive.

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References

  1. Anderson, E. T., Stoskopf, M. K., Morris, J. A., Clarke, E. O., Harms, C. A.: Hematology, Plasma Biochemistry, and Tissue Enzyme Activities of Invasive Red Lionfish Captured off North Carolina, USA. J. Aquat. Anim. Health, 22(4): 266-273, 2010. https://doi.org/10.1577/H10-029.1
  2. Antoine, D. J., Dear, J. W., Lewis, P. S., Platt, V., Coyle, J., Masson, M., Thanacoody, R. H., Gray, A. J., Webb, D. J., Moggs, J. G., Bateman, D. N., Goldring, C. E., Park, B. K.: Mechanistic biomarkers provide early and sensitive detection of acetaminopheninduced acute liver injury at first presentation to hospital. Hepatology, 58(2): 777-787, 2013. https://doi.org/10.1002/hep.26294
  3. Asha, V. V., Akhila, S., Wills, P. J., Subramoniam, A.: Further studies on the antihepatotoxic activity of Phyllanthus maderaspatensis Linn. J. Ethnopharmacol., 92(1): 67-70, 2004. https://doi.org/10.1016/j.jep.2004.02.005
  4. Bartel, D. P.: MicroRNAs: Genomics, Biogenesis, Mechanism, and Function. Cell, 116(2): 281-297, 2004. https://doi.org/10.1016/S0092-8674(04)00045-5
  5. Blair, J. B., Hinton, D. E., Miller, M. R.: Morphological changes in trout hepatocytes exposed to acetaminophen. Mar. Environ. Res., 28(1-4): 357-361, 1989. https://doi.org/10.1016/0141-1136(89)90262-6
  6. Blazka, M. E., Elwell, M. R., Holladay, S. D., Wilson, R. E., Luster, M. I.: Histopathology of Acetaminophen-Induced Liver Changes: Role of Interleukin $1{\alpha}$ and Tumor Necrosis Factor ${\alpha}$. Toxicol. Pathol., 24(2): 181-189, 1996. https://doi.org/10.1177/019262339602400206
  7. Bower, W. A., Johns, M., Margolis, H. S., Williams, I. T., Bell, B. P.: Population-Based Surveillance for Acute Liver Failure. Am. J. Gastroenterol., 102(11): 2459-2463, 2007. https://doi.org/10.1111/j.1572-0241.2007.01388.x
  8. Budhu, A., Jia, H.-L., Forgues, M., Liu, C.-G., Goldstein, D., Lam, A., Zanetti, K. A., Ye, Q.-H., Qin, L.-X., Croce, C. M., Tang, Z.-Y., Wang, X. W.: Identification of metastasis-related microRNAs in hepatocellular carcinoma. Hepatology, 47(3): 897-907, 2008. https://doi.org/10.1002/hep.22160
  9. Cai, X., Hagedorn, C. H., Cullen, B. R.: Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA, 10(12): 1957-1966, 2004. https://doi.org/10.1261/rna.7135204
  10. Campos, C., Sundaram, A., Valente, L., Conceicao, L., Engrola, S., Fernandes, J.: Thermal plasticity of the microRNA transcriptome during Senegalese sole development. BMC Genomics, 15(1): 525, 2014. https://doi.org/10.1186/1471-2164-15-525
  11. Carrington, J. C., Ambros, V.: Role of MicroRNAs in Plant and Animal Development. Science, 301(5631): 336-338, 2003. https://doi.org/10.1126/science.1085242
  12. Carthew, R. W., Sontheimer, E. J.: Origins and Mechanisms of microRNAs and siRNAs. Cell, 136(4): 642-655, 2009. https://doi.org/10.1016/j.cell.2009.01.035
  13. Chang, J., Nicolas, E., Marks, D., Sander, C., Lerro, A., Buendia, M. A., Xu, C., Mason, W. S., Moloshok, T., Bort, R., Zaret, K. S., Taylor, J. M.: miR-122, a Mammalian Liver-Specific microRNA, is Processed from hcr mRNA and MayDownregulate the High Affinity Cationic Amino Acid Transporter CAT-1. RNA Biol., 1(2): 106-113, 2004. https://doi.org/10.4161/rna.1.2.1066
  14. Chim, S. S. C., Shing, T. K. F., Hung, E. C. W., Leung, T.-y., Lau, T.-k., Chiu, R. W. K., Dennis Lo, Y. M.: Detection and Characterization of Placental MicroRNAs in Maternal Plasma. Clin. Chem., 54(3): 482-490, 2008. https://doi.org/10.1373/clinchem.2007.097972
  15. Cohen, S. D., Pumford, N. R., Khairallah, E. A., Boekelheide, K., Pohl, L. R., Amouzadeh, H. R., Hinson, J. A.: Selective Protein Covalent Binding and Target Organ Toxicity. Toxicol. Appl. Pharmacol., 143(1): 1-12, 1997. https://doi.org/10.1006/taap.1996.8074
  16. Ding, S., Voinnet, O.: Antiviral immunity directed by small RNAs. Cell, 130(3): 413-426, 2007. https://doi.org/10.1016/j.cell.2007.07.039
  17. Filipowicz, W., GroBhans, H.: The Liver-Specific Micro RNA miR-122: Biology and Therapeutic Potential. In S. M. Gasser & E. Li (Eds.), Epigenetics and Disease, Vol. 67, pp. 221-238, Springer Basel. 2011.
  18. Fu, Y., Shi, Z., Wu, M., Zhang, J., Jia, L., Chen, X.: Identification and Differential Expression of Micro RNAs during Metamorphosis of the Japanese Flounder (Paralichthys olivaceus). PLoS One, 6(7): e22957, 2011. https://doi.org/10.1371/journal.pone.0022957
  19. Gabriel, L. P., Michel, C.: Detection and Evaluation of Chemically Induced Liver Injury Principles and Methods of Toxicology, Fifth Edition, pp. 1465-1507, CRC Press. 2007.
  20. Gardner, C. R., Heck, D. E., Yang, C. S., Thomas, P. E., Zhang, X.-J., DeGeorge, G. L., Laskin, J. D., Laskin, D. L.: Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat. Hepatology, 27(3): 748-754, 1998. https://doi.org/10.1002/hep.510270316
  21. Gharaei, A., Ghaffari, M., Keyvanshokooh, S., Akrami, R.: Changes in metabolic enzymes, cortisol and glucose concentrations of Beluga (Huso huso) exposed to dietary methylmercury. Fish Physiol. Biochem., 37(3): 485-493, 2011. https://doi.org/10.1007/s10695-010-9450-3
  22. Gibbings, D. J., Ciaudo, C., Erhardt, M., Voinnet, O.: Multivesicular bodies associate with components of microRNA effector complexes and modulate micro RNA activity. Nat. Cell Biol., 11(9): 1143-1149, 2009. https://doi.org/10.1038/ncb1929
  23. Hinton DE, S. H., Braunbeck T: Target organ toxicity in marine and freshwater teleosts, : Schlenk D, Benson WH (Taylor & Francis, London). 2001
  24. Hutvagner, G., Zamore, P. D.: A microRNA in a Multiple-Turnover RNAi Enzyme Complex. Science, 297 (5589): 2056-2060, 2002. https://doi.org/10.1126/science.1073827
  25. Kavitha, P., Ramesh, R., Bupesh, G., Stalin, A., Subramanian, P.: Hepatoprotective activity of Tribulus terrestris extract against acetaminophen-induced toxicity in a freshwater fish (Oreochromis mossambicus). In Vitro Cellular & Developmental Biology-Animal, 47(10): 698-706, 2011. https://doi.org/10.1007/s11626-011-9457-9
  26. Klaassen, C. D.: Casarett and Doull's Toxicology, The Basic Science of Poisons, Toxic responses of the liver: McGraw-Hill, New York. 2008
  27. Knight, T. R., Jaeschke, H.: Acetaminophen-Induced Inhibition of Fas Receptor-Mediated Liver Cell Apoptosis: Mitochondrial Dysfunction versus Glutathione Depletion. Toxicol. Appl. Pharmacol., 181(2): 133-141, 2002. https://doi.org/10.1006/taap.2002.9407
  28. Laskin, D. L., Gardner, C. R., Price, V. F., Jollow, D. J.: Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen. Hepatology, 21(4): 1045-1050, 1995. https://doi.org/10.1002/hep.1840210424
  29. Laterza, O. F., Lim, L., Garrett-Engele, P. W., Vlasakova, K., Muniappa, N., Tanaka, W. K., Johnson, J. M., Sina, J. F., Fare, T. L., Sistare, F. D., Glaab, W. E.: Plasma MicroRNAs as Sensitive and Specific Biomarkers of Tissue Injury. Clin. Chem., 55(11): 1977-1983, 2009. https://doi.org/10.1373/clinchem.2009.131797
  30. Lee, K. J., You, H. J., Park, S. J., Kim, Y. S., Chung, Y. C., Jeong, T. C., Jeong, H. G.: Hepatoprotective effects of Platycodon grandiflorum on acetaminopheninduced liver damage in mice. Cancer Lett., 174(1): 73-81, 2001. https://doi.org/10.1016/S0304-3835(01)00678-4
  31. Lima, R. T., Busacca, S., Almeida, G. M., Gaudino, G., Fennell, D. A., Vasconcelos, M. H.: MicroRNA regulation of core apoptosis pathways in cancer. Eur. J. Cancer, 47(2): 163-174, 2011. https://doi.org/10.1016/j.ejca.2010.11.005
  32. Ma, H., Hostuttler, M., Wei, H., Rexroad, C. E., III, Yao, J.: Characterization of the Rainbow Trout Egg MicroRNA Transcriptome. PLoS One, 7(6): e39649, 2012. https://doi.org/10.1371/journal.pone.0039649
  33. Margis, R., Margis, R., Rieder, C. R. M.: Identification of blood microRNAs associated to Parkinsons disease. J. Biotechnol., 152(3): 96-101, 2011. https://doi.org/10.1016/j.jbiotec.2011.01.023
  34. Moyer, A. M., Fridley, B. L., Jenkins, G. D., Batzler, A. J., Pelleymounter, L. L., Kalari, K. R., Ji, Y., Chai, Y., Nordgren, K. K. S., Weinshilboum, R. M.: Acetaminophen-NAPQI Hepatotoxicity: A Cell Line Model System Genome-Wide Association Study. Toxicol. Sci., 120(1): 33-41, 2011. https://doi.org/10.1093/toxsci/kfq375
  35. Nathwani, R. A., Pais, S., Reynolds, T. B., Kaplowitz, N.: Serum alanine aminotransferase in skeletal muscle diseases. Hepatology, 41(2): 380-382, 2005. https://doi.org/10.1002/hep.20548
  36. Oliveira, F. A., Chaves, M. H., Almeida, F. R. C., Lima Jr, R. C. P., Silva, R. M., Maia, J. L., Brito, G. A. A. C., Santos, F. A., Rao, V. S.: Protective effect of ${\alpha}$- and ${\beta}$-amyrin, a triterpene mixture from Protium heptaphyllum (Aubl.) March. trunk wood resin, against acetaminophen-induced liver injury in mice. J. Ethnopharmacol., 98(1-2): 103-108, 2005. https://doi.org/10.1016/j.jep.2005.01.036
  37. Pineau, P., Volinia, S., McJunkin, K., Marchio, A., Battiston, C., Terris, B., Mazzaferro, V., Lowe, S. W., Croce, C. M., Dejean, A.: miR-221 overexpression contributes to liver tumorigenesis. Proc. Natl. Acad. Sci. U. S. A., 107(1): 264-269, 2010. https://doi.org/10.1073/pnas.0907904107
  38. Ramachandran, R., Kakar, S.: Histological patterns in drug-induced liver disease. J. Clin. Pathol., 62(6): 481-492, 2009. https://doi.org/10.1136/jcp.2008.058248
  39. Reitman, S., Frankel, S.: A colorimetric method for the determination of serum glutamic oxalacetic and glutamic pyruvic transaminases. Am. J. Clin. Pathol., 28(1): 56-63, 1957. https://doi.org/10.1093/ajcp/28.1.56
  40. Samanta, P., Pal, S., Mukherjee, A. K., Ghosh, A. R.: Evaluation of Metabolic Enzymes in Response to Excel Mera 71, a Glyphosate-Based Herbicide, and Recovery Pattern in Freshwater Teleostean Fishes. BioMed Research International, 2014: 6, 2014.
  41. Shivashri, C., Rajarajeshwari, T., Rajasekar, P.: Hepatoprotective action of celery (Apium graveolens) leaves in acetaminophen-fed freshwater fish (Pangasius sutchi). Fish Physiol. Biochem., 39(5): 1057-1069, 2013. https://doi.org/10.1007/s10695-012-9762-6
  42. Starkey Lewis, P. J., Dear, J., Platt, V., Simpson, K. J., Craig, D. G. N., Antoine, D. J., French, N. S., Dhaun, N., Webb, D. J., Costello, E. M., Neoptolemos, J. P., Moggs, J., Goldring, C. E., Park, B. K.: Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology, 54(5): 1767-1776, 2011. https://doi.org/10.1002/hep.24538
  43. Teleman, A. A., Cohen, S. M.: Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev., 20(4): 417-422, 2006. https://doi.org/10.1101/gad.374406
  44. Thomas, P., Wofford, H. W.: Effects of metals and organic compounds on hepatic glutathione, cysteine, and acid-soluble thiol levels in mullet (Mugil cephalus L.). Toxicol. Appl. Pharmacol., 76(1): 172-182, 1984. https://doi.org/10.1016/0041-008X(84)90040-1
  45. Thulin, P., Nordahl, G., Gry, M., Yimer, G., Aklillu, E., Makonnen, E., Aderaye, G., Lindquist, L., Mattsson, C. M., Ekblom, B., Antoine, D. J., Park, B. K., Linder, S., Harrill, A. H., Watkins, P. B., Glinghammar, B., Schuppe-Koistinen, I.: Keratin-18 and microRNA-122 complement alanine aminotransferase as novel safety biomarkers for drug-induced liver injury in two human cohorts. Liver International, 34 (3): 367-378, 2014. https://doi.org/10.1111/liv.12322
  46. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., Lotvall, J. O.: Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 9(6): 654-659, 2007. https://doi.org/10.1038/ncb1596
  47. Vliegenthart, A. D. B., Lewis, P. S., Tucker, C. S., Del Pozo, J., Rider, S., Antoine, D. J., Dubost, V., Westphal, M., Moulin, P., Bailey, M. A., Moggs, J. G., Goldring, C. E., Park, B. K., Dear, J. W.: Retro-orbital blood acquisition facilitates circulating microRNA measurement in zebrafish with paracetamol hepatotoxicity. Zebrafish, 11(3): 219-226, 2014. https://doi.org/10.1089/zeb.2013.0912
  48. Wang, K., Zhang, S., Marzolf, B., Troisch, P., Brightman, A., Hu, Z., Hood, L. E., Galas, D. J.: Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc. Natl. Acad. Sci. U. S. A., 106(11): 4402-4407, 2009. https://doi.org/10.1073/pnas.0813371106
  49. Xiao, J., Zhong, H., Zhou, Y., Yu, F., Gao, Y., Luo, Y., Tang, Z., Guo, Z., Guo, E., Gan, X., Zhang, M., Zhang, Y.: Identification and Characterization of MicroRNAs in Ovary and Testis of Nile Tilapia (Oreochromis niloticus) by Using Solexa Sequencing Technology. PLoS One, 9(1): e86821, 2014. https://doi.org/10.1371/journal.pone.0086821
  50. Xie, C., Xu, S., Yang, L., Ke, Z., Xing, J., Gai, J., Gong, X., Xu, L., Bao, B.: mRNA/microRNA Profile at the Metamorphic Stage of Olive Flounder (Paralichthys olivaceus). Comparative and Functional Genomics, 2011: 12, 2011.
  51. Xu, H., He, J.-H., Xiao, Z.-D., Zhang, Q.-Q., Chen, Y.-Q., Zhou, H., Qu, L.-H.: Liver-enriched transcription factors regulate MicroRNA-122 that targets CUTL1 during liver development. Hepatology, 52(4): 1431-1442, 2010. https://doi.org/10.1002/hep.23818
  52. Yanpallewar, S. U., Sen, S., Tapas, S., Kumar, M., Raju, S. S., Acharya, S. B.: Effect of Azadirachta indica on paracetamol-induced hepatic damage in albino rats. Phytomedicine, 10(5): 391-396, 2003. https://doi.org/10.1078/0944-7113-00230
  53. Yen, F.-L., Wu, T.-H., Lin, L.-T., Lin, C.-C.: Hepatoprotective and antioxidant effects of Cuscuta chinensis against acetaminophen-induced hepatotoxicity in rats. J. Ethnopharmacol., 111(1): 123-128, 2007. https://doi.org/10.1016/j.jep.2006.11.003
  54. Zernecke, A., Bidzhekov, K., Noels, H., Shagdarsuren, E., Gan, L., Denecke, B., Hristov, M., Koppel, T., Jahantigh, M. N., Lutgens, E., Wang, S., Olson, E. N., Schober, A., Weber, C.: Delivery of Micro RNA-126 by Apoptotic Bodies Induces CXCL12-Dependent Vascular Protection (Vol. 2). 2009
  55. Zhang, C., Wang, C., Chen, X., Yang, C., Li, K., Wang, J., Dai, J., Hu, Z., Zhou, X., Chen, L., Zhang, Y., Li, Y., Qiu, H., Xing, J., Liang, Z., Ren, B., Yang, C., Zen, K., Zhang, C.-Y.: Expression Profile of MicroRNAs in Serum: A Fingerprint for Esophageal Squamous Cell Carcinoma. Clin. Chem., 56(12): 1871-1879, 2010. https://doi.org/10.1373/clinchem.2010.147553
  56. Zhang, Y., Jia, Y., Zheng, R., Guo, Y., Wang, Y., Guo, H., Fei, M., Sun, S.: Plasma MicroRNA-122 as a Biomarker for Viral-, Alcohol-, and Chemical-Related Hepatic Diseases. Clin. Chem., 56(12): 1830-1838, 2010. https://doi.org/10.1373/clinchem.2010.147850