Browse > Article
http://dx.doi.org/10.7847/jfp.2016.29.1.025

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)
Publication Information
Journal of fish pathology / v.29, no.1, 2016 , pp. 25-33 More about this Journal
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.
Keywords
Circulating microRNA-122; Acetaminophen; Olive flounder; Liver toxicity; Indicator;
Citations & Related Records
연도 인용수 순위
  • Reference
1 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.   DOI
2 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.   DOI
3 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.   DOI
4 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.   DOI
5 Margis, R., Margis, R., Rieder, C. R. M.: Identification of blood microRNAs associated to Parkinsons disease. J. Biotechnol., 152(3): 96-101, 2011.   DOI
6 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.   DOI
7 Nathwani, R. A., Pais, S., Reynolds, T. B., Kaplowitz, N.: Serum alanine aminotransferase in skeletal muscle diseases. Hepatology, 41(2): 380-382, 2005.   DOI
8 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.   DOI
9 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.   DOI
10 Ramachandran, R., Kakar, S.: Histological patterns in drug-induced liver disease. J. Clin. Pathol., 62(6): 481-492, 2009.   DOI
11 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.   DOI
12 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.
13 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.   DOI
14 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.   DOI
15 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.   DOI
16 Teleman, A. A., Cohen, S. M.: Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev., 20(4): 417-422, 2006.   DOI
17 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.   DOI
18 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.   DOI
19 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.   DOI
20 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.   DOI
21 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.   DOI
22 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.   DOI
23 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.
24 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.   DOI
25 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.   DOI
26 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
27 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.   DOI
28 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.   DOI
29 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.   DOI
30 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.   DOI
31 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.   DOI
32 Bartel, D. P.: MicroRNAs: Genomics, Biogenesis, Mechanism, and Function. Cell, 116(2): 281-297, 2004.   DOI
33 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.   DOI
34 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.   DOI
35 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.   DOI
36 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.   DOI
37 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.   DOI
38 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.   DOI
39 Carrington, J. C., Ambros, V.: Role of MicroRNAs in Plant and Animal Development. Science, 301(5631): 336-338, 2003.   DOI
40 Carthew, R. W., Sontheimer, E. J.: Origins and Mechanisms of microRNAs and siRNAs. Cell, 136(4): 642-655, 2009.   DOI
41 Ding, S., Voinnet, O.: Antiviral immunity directed by small RNAs. Cell, 130(3): 413-426, 2007.   DOI
42 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.   DOI
43 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.   DOI
44 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.   DOI
45 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.
46 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.   DOI
47 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.
48 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.   DOI
49 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.   DOI
50 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.   DOI
51 Hinton DE, S. H., Braunbeck T: Target organ toxicity in marine and freshwater teleosts, : Schlenk D, Benson WH (Taylor & Francis, London). 2001
52 Hutvagner, G., Zamore, P. D.: A microRNA in a Multiple-Turnover RNAi Enzyme Complex. Science, 297 (5589): 2056-2060, 2002.   DOI
53 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.   DOI
54 Klaassen, C. D.: Casarett and Doull's Toxicology, The Basic Science of Poisons, Toxic responses of the liver: McGraw-Hill, New York. 2008
55 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.   DOI
56 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.   DOI