Circulating microRNAs reveal time course of organ injury in a porcine model of acetaminophen-induced acute liver failure

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Baker, Luisa A ^a   Lee, Karla C L ^a   Jimenez, Carolina Palacios ^a   Alibhai, Hatim ^a   Chang, Yumei ^a   Leckie, Pamela J ^b   Mookerjee, Rajeshwar P ^b   Davies, Nathan A ^b   Andreola, Fausto ^b   Jalan, Rajiv ^b  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CREATININE; GENOMIC DNA; MICRORNA; MICRORNA 122; MICRORNA 124 1; MICRORNA 191; MICRORNA 192; MICRORNA 26A; PARACETAMOL; UNCLASSIFIED DRUG;

ACUTE LIVER FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; BRAIN PERFUSION; CONTROLLED STUDY; DISEASE COURSE; DISEASE MARKER; EXOSOME; GENE FUNCTION; GENE IDENTIFICATION; GENETIC ANALYSIS; INTERNATIONAL NORMALIZED RATIO; INTRACRANIAL PRESSURE; NONHUMAN; PIG; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; TISSUE LEVEL; WESTERN BLOTTING; ANIMAL; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; TOXIC HEPATITIS;

ACETAMINOPHEN; ANIMALS; CHEMICAL AND DRUG INDUCED LIVER INJURY; DISEASE MODELS, ANIMAL; INTRACRANIAL PRESSURE; LIVER FAILURE, ACUTE; MICRORNAS; SWINE;

EID: 84958267410     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128076     Document Type: Article

References (50)

1. Larson AM, Polson J, Fontana RJ, Davern TJ, Lalani E, Hynan LS, et al. Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study. Hepatology. 2005;42:1364-1372. PMID: 16317692
2. O'Grady JG, Schalm SW, Williams R. Acute liver failure: redefining the syndromes. Lancet. 1993;342:273-275. PMID: 8101303
3. O'Riordan A, Brummell Z, Sizer E, Auzinger G, Heaton N, O'Grady JG, et al. Acute kidney injury in patients admitted to a liver intensive therapy unit with paracetamol-induced hepatotoxicity. Nephrol Dial Transplant. 2011;26:3501-3508. doi: 10.1093/ndt/gfr050 PMID: 21652548
4. Moore JK, Love E, Craig DG, Hayes PC, Simpson KJ. Acute kidney injury in acute liver failure: a review. Expert Rev Gastroenterol Hepatol. 2013;7:701-712. doi: 10.1586/17474124.2013.837264 PMID: 24134153
5. Stravitz RT, Larsen FS. Therapeutic hypothermia for acute liverfailure. CritCare Med. 2009;37:S258-264. doi: 10.1097/CCM.0b013e3181aa5fb8 PMID: 19535956
6. Bernal W, Auzinger G, Dhawan A, Wendon J. Acute liverfailure. Lancet. 2000;376:190-201. doi: 10. 1016/S0140-6736 (10) 60274-7 PMID: 20638564
7. Cholongitas E, Theocharidou E, Vasianopoulou P, Betrosian A, Shaw S, Patch D, et al. Comparison of the sequential organ failure assessment score with the King's College Hospital criteria and the model for end-stage liver disease score for the prognosis of acetaminophen-induced acute liverfailure. Liver Transpl. 2012;18:405-412. doi: 10.1002/lt.23370 PMID: 22213443
8. Lee WM. Liver: determining prognosis in acute liverfailure. Nat Rev Gastroenterol Hepatol. 2012;9:192-194. doi: 10.1038/nrgastro.2012.34 PMID: 22392292
9. Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11:373-384. doi: 10.1038/ni.1863 PMID: 20404851
10. Weiland M, Gao XH, Zhou L, Mi QS. Small RNAs have a large impact: circulating microRNAs as biomarkers for human diseases. RNABiol. 2012;9:850-859. doi: 10.4161/rna.20378 PMID: 22699556
11. Williams CD, Antoine DJ, Shaw PJ, Benson C, Farhood A, Williams DP, et al. Role of the Nalp3 inflammasome in acetaminophen-induced sterile inflammation and liver injury. Toxicol Appl Pharmacol. 2011;252:289-297. doi: 10.1016/j.taap. 2011.03.001 PMID: 21396389
12. Wang K, Zhang S, Marzolf B, Troisch P, Brightman A, Hu Z, et al. Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc Natl Acad Sci USA. 2009;106:4402-4407. doi: 10.1073/pnas.0813371106 PMID: 19246379
13. Imaeda AB, Watanabe A, Sohail MA, Mahmood S, Mohamadnejad M, Sutterwala FS, et al. Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J Clin Invest. 2009;119:305-314. doi: 10.1172/JCI35958 PMID: 19164858
14. Kong YW, Ferland-McCollough D, Jackson TJ, Bushell M. microRNAs in cancer management. Lancet Oncol. 2012;13:e249-258. doi: 10.1016/S1470-2045 (12) 70073-6 PMID: 22652233
15. Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18:997-1006. doi: 10. 1038/cr.2008.282 PMID: 18766170
16. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513-10518. doi: 10.1073/pnas.0804549105 PMID: 18663219
17. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39:7223-7233. doi: 10.1093/nar/gkr254 PMID: 21609964
18. Starkey Lewis PJ, Dear J, Platt V, Simpson KJ, Craig DG, Antoine DJ, et al. Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology. 2001;54:1767-1776. doi: 10.1002/hep. 24538 PMID: 22045675
19. Antoine DJ, Dear JW, Lewis PS, Platt V, Coyle J, Masson M, et al. Mechanistic biomarkers provide early and sensitive detection of acetaminophen-induced acute liver injury at first presentation to hospital. Hepatology. 2013;58:777-787. doi: 10.1002/hep. 26294 PMID: 23390034
20. John K, Hadem J, Krech T, Wahl K, Manns MP, Dooley S, et al. MicroRNAs play a role for spontaneous recoveryfrom acute liver failure. Hepatology. 2004;60:1346-1355. doi: 10.1002/hep. 27250 PMID: 24913549
21. Sun Y, Koo S, White N, Peralta E, Esau C, Dean NM, et al. Development of a micro-array to detect human and mouse microRNAs and characterization of expression in human organs. Nucleic Acids Res. 2004;32:e188. PMID: 15616155
22. Mladinov D, Liu Y, Mattson DL, Liang M. MicroRNAs contribute to the maintenance of cell-type-specific physiological characteristics: miR-192 targets Na+/K+-ATPase beta1. Nucleic Acids Res. 2013;41:1273-1283. doi: 10.1093/nar/gks1228 PMID: 23221637
23. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129:1401-1414. PMID: 17604727
24. Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T. Identification of tissue-specific microRNAs from mouse. Curr Biol. 2002;12:735-739. PMID: 12007417
25. Laterza OF, Lim L, Garrett-Engele PW, Vlasakova K, Muniappa N, Tanaka WK, et al. Plasma MicroRNAs as sensitive and specific biomarkers of tissue injury. Clin Chem. 2009;55:1977-1983. doi: 10. 1373/clinchem.2009.131797 PMID: 19745058
26. Gilje P, Gidlof O, Rundgren M, Cronberg T, Al-Mashat M, Olde B, et al. The brain-enriched microRNA miR-124 in plasma predicts neurological outcome after cardiac arrest. CritCare. 2014;18:R40. doi: 10.1186/cc13753 PMID: 24588965
27. Lee KC, Palacios Jimenez C, Alibhai H, Chang YM, Leckie PJ, Baker LA, et al. A reproducible, clinically relevant, intensively managed, pig model of acute liver failure for testing of therapies aimed to prolong survival. Liver Int. 2013;33:544-551. doi: 10.1111/liv. 12042 PMID: 23331547
28. Andersen CL, Jensen JL, Orntoft TF. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 2004;64:5245-5250. PMID: 15289330
29. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett. 2004;26:509-515. PMID: 15127793
30. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007;8:R19. PMID: 17291332
31. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3: RESEARCH0034.
32. Silver N, Best S, Jiang J, Thein SL. Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Mol Biol. 2006;7:33. PMID: 17026756
33. Ge Q, Zhou Y, Lu J, Bai Y, Xie X, Lu Z. miRNAin plasma exosome is stable under different storage conditions. Molecules. 2004;19:1568-1575. doi: 10.3390/molecules19021568 PMID: 24473213
34. Bala S, Petrasek J, Mundkur S, Catalano D, Levin I, Ward J, et al. Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology. 2002;56:1946-1957. doi: 10.1002/hep. 25873 PMID: 22684891
35. Martino F, Lorenzen J, Schmidt J, Schmidt M, Broll M, Gorzig Y, et al. Circulating microRNAs are not eliminated by hemodialysis. PLoSOne. 2012;7:e38269. doi: 10.1371/journal.pone.0038269 PMID: 22715378
36. McGill MR, Sharpe MR, Williams CD, Taha M, Curry SC, Jaeschke H. The mechanism underlying acetaminophen-induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNAfragmentation. J Clin Invest. 2002;122:1574-1583. doi: 10.1172/JCI59755 PMID: 22378043
37. Bajt ML, Cover C, Lemasters JJ, Jaeschke H. Nuclear translocation of endonuclease G and apoptosisinducing factor during acetaminophen-induced liver cell injury. Toxicol Sci. 2006;94:217-225. PMID: 16896059
38. Wang Y, Tang N, Hui T, Wang S, Zeng X, Li H, et al. Identification of endogenous reference genes for RT-qPCR analysis of plasma microRNAs levels in rats with acetaminophen-induced hepatotoxicity. J Appl Toxicol. 2003;33:1330-1336. doi: 10.1002/jat.2864 PMID: 23558424
39. Timoneda O, Balcells I, Cordoba S, Castello A, Sanchez A. Determination of reference microRNAs for relative quantification in porcine tissues. PLoSOne. 2012;7:e44413. doi: 10.1371/journal.pone. 0044413 PMID:22970213
40. Zhu HT, Dong QZ, Wang G, Zhou HJ, Ren N, Jia HL, et al. Identification of suitable reference genes for qRT-PCR analysis of circulating microRNAs in hepatitis B virus-infected patients. Mol Biotechnol. 2012;50:49-56. doi: 10.1007/s12033-011-9414-6 PMID: 21567136
41. Reddy AM, Zheng Y, Jagadeeswaran G, Macmil SL, Graham WB, Roe BA, et al. Cloning, characterization and expression analysis of porcine microRNAs. BMC Genomics. 2009;10:65. doi: 10.1186/1471-2164-10-65 PMID: 19196471
42. Szabo G, Bala S. MicroRNAs in liver disease. Nat Rev Gastroenterol Hepatol. 2013;10:542-552. doi: 10.1038/nrgastro.2013.87 PMID: 23689081
43. Zhang Y, Jia Y, Zheng R, Guo Y, Wang Y, Guo H, et al. PlasmamicroRNA-122asabiomarkerforviral-, alcohol-, and chemical-related hepatic diseases. Clin Chem. 2000;56:1830-1838. doi: 10.1373/clinchem.2010.147850 PMID: 20930130
44. Hoffman WE, Solter PF. Diagnostic enzymology of domestic animals. In: Kaneko JJ, Harvey JW, Bruss ML, editors. Clinical Biochemistry of Domestic Animals. 6th ed. Oxford, UK: Elsevier Inc.; 2008. pp. 351-373.
45. Ekser B, Gridelli B, Cooper DK. Porcine alanine transaminase after liver allo- and xenotransplantation. Xenotransplantation. 2012;19:52-55. doi: 10.1111/j.1399-3089.2011.00686.x PMID: 22360753
46. Timoneda O, Balcells I, Nunez JI, Egea R, Vera G, Castello A, et al. miRNA expression profile analysis in kidney of different porcine breeds. PLoS One. 2013;8:e55402. doi: 10.1371/journal.pone.0055402 PMID: 23372853
47. Bellomo R, Ronco C, Kellum JA, Mehta RL, Palevsky P, Acute Dialysis Quality Initiative w. Acute renal failure-definition, outcome measures, animal models, fluid therapy and information technology needs: the Second International Consensus Conference of the Acute Dialysis Quality Initiative (ADQI) Group. Crit Care. 2004;8:R204-212. PMID: 15312219
48. Mehta RL, Kellum JA, Shah SV, Molitoris BA, Ronco C, Warnock DG, et al. Acute Kidney Injury Network: report of an initiative to improve outcomes in acute kidney injury. Crit Care. 2007;11:R31. PMID: 17331245
49. Karali M, Manfredi A, Puppo A, Marrocco E, Gargiulo A, Allocca M, et al. MicroRNA-restrictedtransgene expression in the retina. PLoSOne. 2011;6:e22166. doi: 10.1371/journal.pone.0022166 PMID: 21818300
50. Purins K, Enblad P, Wiklund L, Lewen A. Brain tissue oxygenation and cerebral perfusion pressure thresholds of ischemia in a standardized pig brain death model. NeurocritCare. 2012;16:462-469. doi: 10.1007/s12028-012-9675-3 PMID: 22302179