Serum MicroRNAs as potential biomarkers for early diagnosis of hepatitis C virus-related hepatocellular carcinoma in egyptian patients

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Motawi, Tarek K ^a   Shaker, Olfat G ^b   El Maraghy, Shohda A ^a   Senousy, Mahmoud A ^a  

^a CAIRO UNIVERSITY   (Egypt)

^b CAIRO UNIVERSITY   (Egypt)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 130A; MICRORNA 146A; MICRORNA 192; MICRORNA 195; MICRORNA 19A; MICRORNA 296; MICRORNA 34A; TUMOR MARKER; UNCLASSIFIED DRUG; MIRN146 MICRORNA, HUMAN; MIRN19 MICRORNA, HUMAN; MIRN192 MICRORNA, HUMAN; MIRN195 MICRORNA, HUMAN;

ADULT; ARTICLE; BLOOD LEVEL; CANCER DIAGNOSIS; CANCER STAGING; CHRONIC LIVER DISEASE; CONTROLLED STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE COURSE; DISEASE SEVERITY; DOWN REGULATION; EARLY DIAGNOSIS; EGYPTIAN; FEMALE; GENE EXPRESSION; HEPATITIS C VIRUS; HEPATITIS C VIRUS RELATED HEPATOCELLULAR CARCINOMA; HUMAN; LIVER CELL CARCINOMA; LIVER FIBROSIS; MAJOR CLINICAL STUDY; MALE; PORTAL VEIN THROMBOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BLOOD; EARLY CANCER DIAGNOSIS; HEPACIVIRUS; LIVER CIRRHOSIS; LIVER TUMOR; MIDDLE AGED; PATHOGENICITY; PATHOLOGY; PROGNOSIS; VIROLOGY;

BIOMARKERS, TUMOR; CARCINOMA, HEPATOCELLULAR; EARLY DETECTION OF CANCER; FEMALE; HEPACIVIRUS; HUMANS; LIVER CIRRHOSIS; LIVER NEOPLASMS; MALE; MICRORNAS; MIDDLE AGED; PROGNOSIS;

EID: 84944809993     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137706     Document Type: Article

References (60)

1. El-Serag HB, Marrero JA, Rudolph L, Reddy KR. Diagnosis and treatment of hepatocellular carcinoma. Gastroenterology. 2008; 134:1752-1763. doi: 10.1053/j.gastro.2008.02.090 PMID: 18471552
2. Freedman LS, Edwards BK, Ries LAG, Young JL, editors (2006) Cancer Incidence in Four Member Countries (Cyprus, Egypt, Israel, and Jordan) of the Middle East Cancer Consortium (MECC) Compared with US SEER. Bethesda, MD: NIH Pub: National Cancer Institute.
3. 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; 20Suppl 2:1-20. doi: 10.1111/jvh.12120 PMID: 23827008
4. Marrero JA, Feng Z, Wang Y, Nguyen MH, Befeler AS, Roberts LR, et al. Alpha-fetoprotein, desgamma carboxyprothrombin, and lectin-bound alpha-fetoprotein in early hepatocellular carcinoma. Gastroenterology. 2009; 137:110-118. doi: 10.1053/j.gastro.2009.04.005 PMID: 19362088
5. Attallah AM, Omran MM, Attallah AA, Abdallah SO, Farid K, Darwish H, et al. HCC-ART score, a simple, highly sensitive and specific test for early diagnosis of hepatocellular carcinoma: a large-scale, multicentre study. Br J Cancer. 2013; 109:1657-1665. doi: 10.1038/bjc.2013.481 PMID: 23982602
6. ElHefnawi M, Soliman B, Abu-Shahba N, Amer M. An integrative meta-analysis of microRNAs in hepatocellular carcinoma. Genomics Proteomics Bioinformatics. 2013; 11: 354-367. doi: 10.1016/j.gpb.2013.05.007 PMID: 24287119
7. Huang S, He X. The role of microRNAs in liver cancer progression. Br J Cancer. 2011; 104: 235-240. doi: 10.1038/sj.bjc.6606010 PMID: 21102580
8. Braconi C, Valeri N, Gasparini P, Huang N, Taccioli C, Nuovo G, et al. Hepatitis C virus proteins modulate microRNA expression and chemosensitivity in malignant hepatocytes. Clin Cancer Res. 2010; 16: 957-966. doi: 10.1158/1078-0432.CCR-09-2123 PMID: 20103677
9. Qi J, Wang J, Katayama H, Sen S, Liu SM. Circulating microRNAs (cmiRNAs) as novel potential biomarkers for hepatocellular carcinoma. Neoplasma. 2013; 60:135-142. PMID: 23259781
10. Matsumura H, Nirei K, Nakamura H, Higuchi T, Arakawa Y, Ogawa M, et al. Histopathology of type C liver disease for determining hepatocellular carcinoma risk factors. World J Gastroenterol. 2013; 19: 4887-4896. doi: 10.3748/wjg.v19.i30.4887 PMID: 23946593
11. Lok AS, Seeff LB, Morgan TR, di Bisceglie AM, Sterling RK, Curto TM, et al. Incidence of hepatocellular carcinoma and associated risk factors in hepatitis C-related advanced liver disease. Gastroenterology. 2009; 136:138-148. doi: 10.1053/j.gastro.2008.09.014 PMID: 18848939
12. Jeong SW, Jang JY, Chung RT. Hepatitis C virus and hepatocarcinogenesis. Clin Mol Hepatol. 2012; 18: 347-356. doi: 10.3350/cmh.2012.18.4.347 PMID: 23323249
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. Shrivastava S, Petrone J, Steele R, Lauer GM, Di Bisceglie AM, Ray RB. Up-regulation of circulating miR-20a is correlated with hepatitis C virus-mediated liver disease progression. Hepatology. 2013; 58: 863-871. doi: 10.1002/hep.26296 PMID: 23390075
15. Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet. 2003; 362:1907-1917. PMID: 14667750
16. Poynard T, Bedossa P, Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet. 1997; 349: 825-832. PMID: 9121257
17. Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM. MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology. 2009; 50:113-121. doi: 10.1002/hep.22919 PMID: 19441017
18. Braun CJ, Zhang X, Savelyeva I, Wolff S, Moll UM, Schepeler T, et al. p53-Responsive micrornas 192 and 215 are capable of inducing cell cycle arrest. Cancer Res. 2008; 68:10094-10104. doi: 10.1158/0008-5472.CAN-08-1569 PMID: 19074875
19. Ura S, Honda M, Yamashita T, Ueda T, Takatori H, Nishino R, et al. Differential microRNA expression between hepatitis B and hepatitis C leading disease progression to hepatocellular carcinoma. Hepatology. 2009; 49:1098-1112. doi: 10.1002/hep.22749 PMID: 19173277
20. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, et al. Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet. 2006; 38:1060-1065. PMID: 16878133
21. Han ZB, Zhong L, Teng MJ, Fan JW, Tang HM, Wu JY, et al. Identification of recurrence-related micro-RNAs in hepatocellular carcinoma following liver transplantation. Mol Oncol. 2012; 6: 445-457. doi: 10.1016/j.molonc.2012.04.001 PMID: 22552153
22. Henrici A, Montalbano R, Neureiter D, Krause M, Stiewe T, Slater EP, et al. The pan-deacetylase inhibitor panobinostat suppresses the expression of oncogenic miRNAs in hepatocellular carcinoma cell lines. Mol Carcinog. 2013.
23. Wurdinger T, Tannous BA, Saydam O, Skog J, Grau S, Soutschek J, et al. miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell. 2008; 14: 382-393. doi: 10.1016/j.ccr.2008.10.005 PMID: 18977327
24. Yoon AR, Gao R, Kaul Z, Choi IK, Ryu J, Noble JR, et al. MicroRNA-296 is enriched in cancer cells and downregulates p21WAF1 mRNA expression via interaction with its 3' untranslated region. Nucleic Acids Res. 2011; 39: 8078-8091. doi: 10.1093/nar/gkr492 PMID: 21724611
25. Zhao JL, Rao DS, Boldin MP, Taganov KD, O'Connell RM, Baltimore D. NF-kappaB dysregulation in microRNA-146a-deficient mice drives the development of myeloid malignancies. Proc Natl Acad Sci U SA. 2011; 108: 9184-9189. doi: 10.1073/pnas.1105398108 PMID: 21576471
26. Katayama Y, Maeda M, Miyaguchi K, Nemoto S, Yasen M, Tanaka S, et al. Identification of pathogenesis-related microRNAs in hepatocellular carcinoma by expression profiling. Oncol Lett. 2012; 4: 817-823. PMID: 23205106
27. Gramantieri L, Ferracin M, Fornari F, Veronese A, Sabbioni S, Liu CG, et al. Cyclin G1 is a target of miR-122a, a microRNA frequently down-regulated in human hepatocellular carcinoma. Cancer Res. 2007; 67: 6092-6099. PMID: 17616664
28. Huang XH, Wang Q, Chen JS, Fu XH, Chen XL, Chen LZ, et al. Bead-based microarray analysis of microRNA expression in hepatocellular carcinoma: miR-338 is downregulated. Hepatol Res. 2009; 39: 786-794. doi: 10.1111/j.1872-034X.2009.00502.x PMID: 19473441
29. Mizuguchi Y, Mishima T, Yokomuro S, Arima Y, Kawahigashi Y, Shigehara K, et al. Sequencing and bioinformatics-based analyses of the microRNA transcriptome in hepatitis B-related hepatocellular carcinoma. PLoS One. 2011; 6: e15304. doi: 10.1371/journal.pone.0015304 PMID: 21283620
30. Pok S, Wen V, Shackel N, Alsop A, Pyakurel P, Fahrer A, et al. Cyclin E facilitates dysplastic hepatocytesto bypass G1/S checkpoint in hepatocarcinogenesis. J Gastroenterol Hepatol. 2013; 28:1545-1554. doi: 10.1111/jgh.12216 PMID: 23574010
31. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell. 2009; 137:1005-1017. doi: 10.1016/j.cell.2009.04.021 PMID: 19524505
32. Motawi TK, Shaker OG, El-Maraghy SA, Senousy MA. Serum Interferon-Related MicroRNAs as Biomarkers to Predict the Response to Interferon Therapy in Chronic Hepatitis C Genotype 4. PLoS One. 2015; 10: e0120794. doi: 10.1371/journal.pone.0120794 PMID: 25790297
33. Zhou J, Yu L, Gao X, Hu J, Wang J, Dai Z, et al. Plasma microRNA panel to diagnose hepatitis B virus-related hepatocellular carcinoma. J Clin Oncol. 2011; 29: 4781-4788. doi: 10.1200/JCO.2011.38.2697 PMID: 22105822
34. Abd-El-Fattah AA, Sadik NA, Shaker OG, Aboulftouh ML. Differential microRNAs expression in serum of patients with lung cancer, pulmonary tuberculosis, and pneumonia. Cell Biochem Biophys. 2013; 67: 875-884. doi: 10.1007/s12013-013-9575-y PMID: 23559272
35. El-Garem H, Ammer A, Shehab H, Shaker O, Anwer M, El-Akel W, et al. Circulating microRNA, miR-122 and miR-221 signature in Egyptian patients with chronic hepatitis C related hepatocellular carcinoma. World J Hepatol. 2014; 6: 818-824. doi: 10.4254/wjh.v6.i11.818 PMID: 25429320
36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25: 402-408. PMID: 11846609
37. Qu KZ, Zhang K, Li H, Afdhal NH, Albitar M. Circulating microRNAs as biomarkers for hepatocellular carcinoma. J Clin Gastroenterol. 2011; 45: 355-360. doi: 10.1097/MCG.0b013e3181f18ac2 PMID: 21278583
38. Murakami Y, Yasuda T, Saigo K, Urashima T, Toyoda H, Okanoue T, et al. Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene. 2006; 25: 2537-2545. PMID: 16331254
39. Liu M, Liu J, Wang L, Wu H, Zhou C, Zhu H, et al. Association of serum microRNA expression in hepatocellular carcinomas treated with transarterial chemoembolization and patient survival. PLoS One. 2014; 9: e109347. doi: 10.1371/journal.pone.0109347 PMID: 25275448
40. Gui J, Tian Y, Wen X, Zhang W, Zhang P, Gao J, et al. Serum microRNA characterization identifies miR-885-5p as a potential marker for detecting liver pathologies. Clin Sci (Lond). 2011; 120:183-193.
41. Hermeking H. p53 enters the microRNA world. Cancer Cell. 2007; 12: 414-418. PMID: 17996645
42. Tryndyak VP, Ross SA, Beland FA, Pogribny IP. Down-regulation of the microRNAs miR-34a, miR-127, and miR-200b in rat liver during hepatocarcinogenesis induced by a methyl-deficient diet. MolCarcinog. 2009; 48: 479-487. doi: 10.1002/mc.20484 PMID: 18942116
43. Tan Y, Ge G, Pan T, Wen D, Chen L, Yu X, et al. A serum microRNA panel as potential biomarkers for hepatocellular carcinoma related with hepatitis B virus. PLoS One. 2014; 9: e107986. doi: 10.1371/journal.pone.0107986 PMID: 25238238
44. Karakatsanis A, Papaconstantinou I, Gazouli M, Lyberopoulou A, Polymeneas G, Voros D. Expression of microRNAs, miR-21, miR-31, miR-122, miR-145, miR-146a, miR-200c, miR-221, miR-222, and miR-223 in patients with hepatocellular carcinoma or intrahepatic cholangiocarcinoma and its prognostic significance. Mol Carcinog. 2013; 52: 297-303. doi: 10.1002/mc.21864 PMID: 22213236
45. Rong M, He R, Dang Y, Chen G. Expression and clinicopathological significance of miR-146a in hepatocellular carcinoma tissues. Ups J Med Sci. 2014; 119:19-24. doi: 10.3109/03009734.2013.856970 PMID: 24172202
46. Zhang Z, Zhang Y, Sun XX, Ma X, Chen ZN. microRNA-146a inhibits cancer metastasis by downregulating VEGFthrough dual pathways in hepatocellular carcinoma. Mol Cancer. 2015; 14: 5. doi: 10.1186/1476-4598-14-5 PMID: 25608619
47. Vaira V, Faversani A, Dohi T, Montorsi M, Augello C, Gatti S, et al. miR-296 regulation of a cell polarity-cell plasticity module controls tumor progression. Oncogene. 2012; 31: 27-38. doi: 10.1038/onc.2011.209 PMID: 21643016
48. Wang S, Olson EN. AngiomiRs-key regulators of angiogenesis. Curr Opin Genet Dev. 2009; 19: 205-211. doi: 10.1016/j.gde.2009.04.002 PMID: 19446450
49. Sun X, Zhang J, Hou Z, Han Q, Zhang C, Tian Z. miR-146a is directly regulated by STAT3 in human hepatocellular carcinoma cells and involved in anti-tumor immune suppression. Cell Cycle. 2015; 14: 243-252. doi: 10.4161/15384101.2014.977112 PMID: 25607648
50. Xu J, Zhu X, Wu L, Yang R, Yang Z, Wang Q, et al. MicroRNA-122 suppresses cell proliferation and induces cell apoptosis in hepatocellular carcinoma by directly targeting Wnt/beta-catenin pathway. Liver Int. 2012; 32: 752-760. doi: 10.1111/j.1478-3231.2011.02750.x PMID: 22276989
51. Xu J, Wu C, Che X, Wang L, Yu D, Zhang T, et al. Circulating microRNAs, miR-21, miR-122, and miR-223, in patients with hepatocellular carcinoma or chronic hepatitis. Mol Carcinog. 2011; 50:136-142. doi: 10.1002/mc.20712 PMID: 21229610
52. Qi P, Cheng SQ, Wang H, Li N, Chen YF, Gao CF. Serum microRNAs as biomarkers for hepatocellular carcinoma in Chinese patients with chronic hepatitis B virus infection. PLoS One. 2011; 6: e28486. doi: 10.1371/journal.pone.0028486 PMID: 22174818
53. Povero D, Eguchi A, Li H, Johnson CD, Papouchado BG, Wree A, et al. Circulating extracellular vesicles with specific proteome and liver microRNAs are potential biomarkers for liver injury in experimental fatty liver disease. PLoS One. 2014; 9: e113651. doi: 10.1371/journal.pone.0113651 PMID: 25470250
54. 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
55. Borel F, Konstantinova P, Jansen PL. Diagnostic and therapeutic potential of miRNA signatures in patients with hepatocellular carcinoma. J Hepatol. 2012; 56:1371-1383. doi: 10.1016/j.jhep.2011.11.026 PMID: 22314424
56. Trebicka J, Anadol E, Elfimova N, Strack I, Roggendorf M, Viazov S, et al. Hepatic and serum levels of miR-122 after chronic HCV-induced fibrosis. J Hepatol. 2013; 58: 234-239. doi: 10.1016/j.jhep.2012.10.015 PMID: 23085648
57. Guo CJ, Pan Q, Cheng T, Jiang B, Chen GY, Li DG. Changes in microRNAs associated with hepatic stellate cell activation status identify signaling pathways. FEBS J. 2009; 276: 5163-5176. doi: 10.1111/j.1742-4658.2009.07213.x PMID: 19674103
58. Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, et al. miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci USA. 2010; 107: 264-269. doi: 10.1073/pnas.0907904107 PMID: 20018759
59. Tomimaru Y, Eguchi H, Nagano H, Wada H, Kobayashi S, Marubashi S, et al. Circulating microRNA-21 as a novel biomarker for hepatocellular carcinoma. J Hepatol. 2012; 56:167-175. doi: 10.1016/j.jhep.2011.04.026 PMID: 21749846
60. Liu AM, Yao TJ, Wang W, Wong KF, Lee NP, Fan ST, et al. Circulating miR-15b and miR-130b in serum as potential markers for detecting hepatocellular carcinoma: a retrospective cohort study. BMJ Open. 2012; 2: e000825. doi: 10.1136/bmjopen-2012-000825 PMID: 22403344