Serum interferon-related microRNAs as biomarkers to predict the response to interferon therapy in chronic hepatitis C genotype

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Motawi, Tarek Kamal ^a   Shaker, Olfat Gamil ^b   El Maraghy, Shohda Assem ^a   Senousy, Mahmoud Ahmed ^a  

^a CAIRO UNIVERSITY   (Egypt)

^b CAIRO UNIVERSITY   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; INTERFERON; MICRORNA; MICRORNA 130A; MICRORNA 146A; MICRORNA 192; MICRORNA 195; MICRORNA 19A; MICRORNA 296; MICRORNA 34A; PEGINTERFERON ALPHA; PEGINTERFERON ALPHA2B; RIBAVIRIN; RNA; UNCLASSIFIED DRUG; ALPHA INTERFERON; ANTIVIRUS AGENT; MACROGOL DERIVATIVE; RECOMBINANT PROTEIN;

ADULT; ARTICLE; BLOOD LEVEL; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DISEASE ASSOCIATION; DOWN REGULATION; DRUG EFFICACY; DRUG RESPONSE; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; GENOTYPE; HEPATITIS C; HUMAN; MAJOR CLINICAL STUDY; MALE; MOLECULAR DYNAMICS; OUTCOME ASSESSMENT; PHARMACOGENETICS; PREDICTION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNDROME DELINEATION; UPREGULATION; BLOOD; CASE CONTROL STUDY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEPATITIS C, CHRONIC; PERSONALIZED MEDICINE; PROGNOSIS; RECEIVER OPERATING CHARACTERISTIC; STATISTICAL MODEL; TREATMENT OUTCOME;

HEPATITIS C VIRUS;

ADULT; ANTIVIRAL AGENTS; BIOMARKERS; CASE-CONTROL STUDIES; FEMALE; GENE EXPRESSION REGULATION; GENOTYPE; HEPATITIS C, CHRONIC; HUMANS; INTERFERON-ALPHA; INTERFERONS; LOGISTIC MODELS; MALE; MICRORNAS; POLYETHYLENE GLYCOLS; PRECISION MEDICINE; PROGNOSIS; RECOMBINANT PROTEINS; RIBAVIRIN; ROC CURVE; TREATMENT OUTCOME;

EID: 84961288243     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120794     Document Type: Article

References (54)

1. de Oliveria Andrade LJ, D'Oliveira A, Melo RC, De Souza EC, Costa Silva CA, Parana R. Association between hepatitis C and hepatocellular carcinoma. J Glob Infect Dis. 2009; 1: 33-37. doi: 10.4103/0974-777X.52979 PMID: 20300384
2. Mohamoud YA, Mumtaz GR, Riome S, Miller D, Abu-Raddad LJ. The epidemiology of hepatitis C virus in Egypt: a systematic review and data synthesis. BMC Infect Dis. 2013; 13: 288. doi: 10.1186/1471- 2334-13-288 PMID: 23799878
3. Razavi H, Waked I, Sarrazin C, Myers RP, Idilman R, Calinas F, et al. The present and future disease burden of hepatitis C virus (HCV) infection with today's treatment paradigm. J Viral Hepat. 2014; 21 Suppl 1: 34-59. doi: 10.1111/jvh.12248 PMID: 24713005
4. Mabrouk M, El-Raziky M, Zayed N, Salama R, El-Akel W, Awad T, et al. Clinical, biochemical and pathological profiles of 5464 Egyptian chronic hepatitis C-infected patients. Hepatogastroenterology. 2013; 60: 1731-1735. PMID: 24634943
5. Shehab H, Elbaz T, Deraz D, Hafez A, Elattar I. The Efficacy of a Hansenula-Derived 20 kDa Pegylated Interferon Alpha-2a in the Treatment of Genotype 4 Chronic Hepatitis C. J Interferon Cytokine Res. 2014; 34: 727-733. doi: 10.1089/jir.2013.0127 PMID: 24730368
6. Jacobson IM, McHutchison JG, Dusheiko G, Di Bisceglie AM, Reddy KR, Bzowej NH, et al. Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med. 2011; 364: 2405-2416. doi: 10.1056/NEJMoa1012912 PMID: 21696307
7. Pol S, Roberts SK, Andreone P, Younossi Z, Diago M, Lawitz EJ, et al. Efficacy and safety of telaprevir based regimens in cirrhotic patients with hcv genotype 1 and prior peginterferon/ ribavirin treatment failure: subanalysis of the REALIZE phase III study. Hepatology. 2011; 54(Suppl.1): 374A-375A.
8. Maasoumy B, Port K, Markova AA, Serrano BC, Rogalska-Taranta M, Sollik L, et al. Eligibility and safety of triple therapy for hepatitis C: lessons learned from the first experience in a real world setting. PLoS One. 2013; 8: e55285. doi: 10.1371/journal.pone.0055285 PMID: 23383319
9. Hatzakis A, Van Damme P, Alcorn K, Gore C, Benazzouz M, Berkane S, et al. The state of hepatitis B and C in the Mediterranean and Balkan countries: report from a summit conference. J Viral Hepat. 2013; 20 Suppl 2: 1-20. doi: 10.1111/jvh.12120 PMID: 23827008
10. Kamal SM. Hepatitis C virus genotype 4 therapy: progress and challenges. Liver Int. 2011; 31 Suppl 1: 45-52. doi: 10.1111/j.1478-3231.2010.02385.x PMID: 21205137
11. Allegra A, Alonci A, Campo S, Penna G, Petrungaro A, Gerace D, et al. Circulating microRNAs: new biomarkers in diagnosis, prognosis and treatment of cancer (review). Int J Oncol. 2012; 41: 1897-1912. doi: 10.3892/ijo.2012.1647 PMID: 23026890
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 U S A. 2009; 106: 4402-4407. doi: 10.1073/ pnas.0813371106 PMID: 19246379
13. Cermelli S, Ruggieri A, Marrero JA, Ioannou GN, Beretta L. Circulating microRNAs in patients with chronic hepatitis C and non-alcoholic fatty liver disease. PLoS One. 2011; 6: e23937. doi: 10.1371/ journal.pone.0023937 PMID: 21886843
14. Sedger LM. microRNA control of interferons and interferon induced anti-viral activity. Mol Immunol. 2013; 56: 781-793. doi: 10.1016/j.molimm.2013.07.009 PMID: 23962477
15. Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, et al. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007; 449: 919-922. PMID: 17943132
16. Steuerwald NM, Parsons JC, Bennett K, Bates TC, Bonkovsky HL. Parallel microRNA and mRNA expression profiling of (genotype 1b) human hepatoma cells expressing hepatitis C virus. Liver Int. 2010; 30: 1490-1504. doi: 10.1111/j.1478-3231.2010.02321.x PMID: 20825557
17. Zhang X, Daucher M, Armistead D, Russell R, Kottilil S. MicroRNA expression profiling in HCV-infected human hepatoma cells identifies potential anti-viral targets induced by interferon-alpha. PLoS One. 2013; 8: e55733. doi: 10.1371/journal.pone.0055733 PMID: 23418453
18. Bruni R, Marcantonio C, Tritarelli E, Tataseo P, Stellacci E, Costantino A, et al. An integrated approach identifies IFN-regulated microRNAs and targeted mRNAs modulated by different HCV replicon clones. BMC Genomics. 2011; 12: 485. doi: 10.1186/1471-2164-12-485 PMID: 21970718
19. Burska AN, Roget K, Blits M, Soto Gomez L, van de Loo F, Hazelwood LD, et al. Gene expression analysis in RA: towards personalized medicine. Pharmacogenomics J. 2014; 14: 93-106. doi: 10.1038/tpj. 2013.48 PMID: 24589910
20. Murakami Y, Tanaka M, Toyoda H, Hayashi K, Kuroda M, Tajima A, et al. Hepatic microRNA expression is associated with the response to interferon treatment of chronic hepatitis C. BMC Med Genomics. 2010; 3: 48. doi: 10.1186/1755-8794-3-48 PMID: 20969775
21. Su TH, Liu CH, Liu CJ, Chen CL, Ting TT, Tseng TC, et al. Serum microRNA-122 level correlates with virologic responses to pegylated interferon therapy in chronic hepatitis C. Proc Natl Acad Sci U S A. 2013; 110: 7844-7849. doi: 10.1073/pnas.1306138110 PMID: 23613588
22. Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W. Decreased levels of microRNA miR-122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med. 2009; 15: 31-33. doi: 10.1038/nm.1902 PMID: 19122656
23. Scagnolari C, Zingariello P, Vecchiet J, Selvaggi C, Racciatti D, Taliani G, et al. Differential expression of interferon-induced microRNAs in patients with chronic hepatitis C virus infection treated with pegylated interferon alpha. Virol J. 2010; 7: 311. doi: 10.1186/1743-422X-7-311 PMID: 21070682
24. Sekiya Y, Ogawa T, Iizuka M, Yoshizato K, Ikeda K, Kawada N. Down-regulation of cyclin E1 expression by microRNA-195 accounts for interferon-beta-induced inhibition of hepatic stellate cell proliferation. J Cell Physiol. 2011; 226: 2535-2542. doi: 10.1002/jcp.22598 PMID: 21792910
25. Siegrist F, Singer T, Certa U. MicroRNA Expression Profiling by Bead Array Technology in Human Tumor Cell Lines Treated with Interferon-Alpha-2a. Biol Proced Online. 2009; 11: 113-129. doi: 10. 1007/s12575-009-9012-1 PMID: 19629613
26. Reinsbach S, Nazarov PV, Philippidou D, Schmitt M, Wienecke-Baldacchino A, Muller A, et al. Dynamic regulation of microRNA expression following interferon-gamma-induced gene transcription. RNA Biol. 2012; 9: 978-989. doi: 10.4161/rna.20494 PMID: 22767256
27. Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology. 1996; 24: 289-293. PMID: 8690394
28. Ohno O, Mizokami M, Wu RR, Saleh MG, Ohba K, Orito E, et al. New hepatitis C virus (HCV) genotyping system that allows for identification of HCV genotypes 1a, 1b, 2a, 2b, 3a, 3b, 4, 5a, and 6a. J Clin Microbiol. 1997; 35: 201-207. PMID: 8968908
29. Mu Y, Zhou H, Li W, Hu L, Zhang Y. Evaluation of RNA quality in fixed and unembedded mouse embryos by different methods. Exp Mol Pathol. 2013; 95: 206-212. doi: 10.1016/j.yexmp.2013.07.005 PMID: 23895953
30. Sperveslage J, Hoffmeister M, Henopp T, Kloppel G, Sipos B. Establishment of robust controls for the normalization of miRNA expression in neuroendocrine tumors of the ileum and pancreas. Endocrine. 2014; 46: 226-230. doi: 10.1007/s12020-014-0202-5 PMID: 24535468
31. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3: 1101-1108. PMID: 18546601
32. Antaki N, Craxi A, Kamal S, Moucari R, Van der Merwe S, Haffar S, et al. The neglected hepatitis C virus genotypes 4, 5 and 6: an international consensus report. Liver Int. 2010; 30: 342-355. doi: 10. 1111/j.1478-3231.2009.02188.x PMID: 20015149
33. Chen Y, Gelfond JA, McManus LM, Shireman PK. Reproducibility of quantitative RT-PCR array in miRNA expression profiling and comparison with microarray analysis. BMC Genomics. 2009; 10: 407. doi: 10.1186/1471-2164-10-407 PMID: 19715577
34. Shwetha S, Gouthamchandra K, Chandra M, Ravishankar B, Khaja MN, Das S. Circulating miRNA profile in HCV infected serum: novel insight into pathogenesis. Scientific reports. 2013; 3: 1-7.
35. Kim Y, Hammerman PS, Kim J, Yoon JA, Lee Y, Sun JM, et al. Integrative and comparative genomic analysis of lung squamous cell carcinomas in East Asian patients. J Clin Oncol. 2014; 32: 121-128. doi: 10.1200/JCO.2013.50.8556 PMID: 24323028
36. Kurbanov F, Abdel-Hamid M, Latanich R, Astemborski J, Mohamed M, Mikhail NM, et al. Genetic polymorphism in IL28B is associated with spontaneous clearance of hepatitis C virus genotype 4 infection in an Egyptian cohort. J Infect Dis. 2011; 204: 1391-1394. doi: 10.1093/infdis/jir536 PMID: 21933876
37. Shaker OG, Sadik NA, El-Dessouki A. Single-nucleotide polymorphism in the promoter region of the osteopontin gene at nucleotide-443 as a marker predicting the efficacy of pegylated interferon/ ribavirin-therapy in Egyptians patients with chronic hepatitis C. Hum Immunol. 2012; 73: 1039-1045. doi: 10.1016/j.humimm.2012.07.329 PMID: 22836041
38. Hermeking H. p53 enters the microRNA world. Cancer Cell. 2007; 12: 414-418. PMID: 17996645
39. Abouheif MM, Nakasa T, Shibuya H, Niimoto T, KongcharoensombatW, Ochi M. Silencing microRNA- 34a inhibits chondrocyte apoptosis in a rat osteoarthritis model in vitro. Rheumatology (Oxford). 2010; 49: 2054-2060. doi: 10.1093/rheumatology/keq247 PMID: 20675358
40. Peng X, Li Y, Walters KA, Rosenzweig ER, Lederer SL, Aicher LD, et al. Computational identification of hepatitis C virus associated microRNA-mRNA regulatory modules in human livers. BMC Genomics. 2009; 10: 373. doi: 10.1186/1471-2164-10-373 PMID: 19671175
41. Wang LG, Gu J. Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis. Cancer Epidemiol. 2012; 36: e61-67. doi: 10.1016/j.canep.2011.05.002 PMID: 22018950
42. Bellecave P, Moradpour D. A fresh look at interferon-alpha signaling and treatment outcomes in chronic hepatitis C. Hepatology. 2008; 48: 1330-1333. doi: 10.1002/hep.22571 PMID: 18821612
43. 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. 2012; 56: 1946-1957. doi: 10.1002/hep.25873 PMID: 22684891
44. Ji F, Yang B, Peng X, Ding H, You H, Tien P. Circulating microRNAs in hepatitis B virus-infected patients. J Viral Hepat. 2011; 18: e242-251. doi: 10.1111/j.1365-2893.2011.01443.x PMID: 21692939
45. Tan Y, Ge G, Pan T, Wen D, Gan J. A Pilot Study of Serum MicroRNAs Panel as Potential Biomarkers for Diagnosis of Nonalcoholic Fatty Liver Disease. PLoS One. 2014; 9: e105192. doi: 10.1371/journal. pone.0105192 PMID: 25141008
46. Ishida H, Tatsumi T, Hosui A, Nawa T, Kodama T, Shimizu S, et al. Alterations in microRNA expression profile in HCV-infected hepatoma cells: involvement of miR-491 in regulation of HCV replication via the PI3 kinase/Akt pathway. Biochem Biophys Res Commun. 2011; 412: 92-97. doi: 10.1016/j.bbrc.2011. 07.049 PMID: 21802413
47. Bhanja Chowdhury J, Shrivastava S, Steele R, Di Bisceglie AM, Ray R, Ray RB. Hepatitis C virus infection modulates expression of interferon stimulatory gene IFITM1 by upregulating miR-130A. J Virol. 2012; 86: 10221-10225. doi: 10.1128/JVI.00882-12 PMID: 22787204
48. Liu X, Wang T, Wakita T, Yang W. Systematic identification of microRNA and messenger RNA profiles in hepatitis C virus-infected human hepatoma cells. Virology. 2010; 398: 57-67. doi: 10.1016/j.virol. 2009.11.036 PMID: 20006370
49. Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE, Pfeffer S, et al. Cellular cofactors affecting hepatitis C virus infection and replication. Proc Natl Acad Sci U S A. 2007; 104: 12884-12889. PMID: 17616579
50. Li S, Duan X, Li Y, Liu B, McGilvray I, Chen L. MicroRNA-130a inhibits HCV replication by restoring the innate immune response. J Viral Hepat. 2014; 21: 121-128. doi: 10.1111/jvh.12131 PMID: 24383925
51. Collins AS, McCoy CE, Lloyd AT, O'Farrelly C, Stevenson NJ. miR-19a: an effective regulator of SOCS3 and enhancer of JAK-STAT signalling. PLoS One. 2013; 8: e69090. doi: 10.1371/journal.pone. 0069090 PMID: 23894411
52. El-Ekiaby N, Hamdi N, Negm M, Ahmed R, Zekri AR, Esmat G, et al. Repressed induction of interferonrelated microRNAs miR-146a and miR-155 in peripheral blood mononuclear cells infected with HCV genotype 4. FEBS Open Bio. 2012; 2: 179-186. doi: 10.1016/j.fob.2012.07.005 PMID: 23650597
53. Bala S, Tilahun Y, Taha O, Alao H, Kodys K, Catalano D, et al. Increased microRNA-155 expression in the serum and peripheral monocytes in chronic HCV infection. J Transl Med. 2012; 10: 151. doi: 10. 1186/1479-5876-10-151 PMID: 22846613
54. Taganov KD, Boldin MP, Chang KJ, Baltimore D. NF-kappaB-dependent induction of microRNA miR- 146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci U S A. 2006; 103: 12481-12486. PMID: 16885212