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Published in: Virchows Archiv 4/2014

01-04-2014 | Original Article

microRNA expression might predict prognosis of epithelial hepatoblastoma

Authors: Mónika Gyugos, Gábor Lendvai, István Kenessey, Krisztina Schlachter, Judit Halász, Péter Nagy, Miklós Garami, Zsuzsa Jakab, Zsuzsa Schaff, András Kiss

Published in: Virchows Archiv | Issue 4/2014

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Abstract

Hepatoblastoma (HB) is the most common primary liver cancer in childhood. The fetal and mixed embryonal/fetal epithelial subtypes of HB differ not only in grade of differentiation but probably also in prognosis. We aimed to determine microRNA (miRNA) expression patterns of the main subtypes of epithelial HBs to reveal differences and relate them to survival. We studied 20 cases of epithelial HB, subtyped as pure fetal (n = 12) or embryonal/fetal (n = 8). Tissues were sampled according to subtype to arrive at 15 purely fetal and eight purely embryonal samples (n = 8) and 15 samples of non-tumorous surrounding liver (SL). Relative expression of miR-17-5p, miR-18a, miR-21, miR-34a, miR-96, miR-122, miR-181a, miR-195, miR-210, miR-214, miR-221, miR-222, miR-223, and miR-224 was determined by TaqMan MicroRNA Assays applying miR-140 as reference. A higher level of miR-18a (p < 0.01) was found in embryonal samples than in fetal samples. Lower miR-17-5p, miR-195, miR-210, miR-214, and higher miR-221 levels were detected in fetal samples (p < 0.02) in comparison with SL samples, whereas a lower miR-122 level was observed in embryonal samples (p < 0.003). Histological subtype did not correlate with survival; however, high miR-21, low miR-222, and low miR-224 levels proved to be independently prognostic for HB with significantly increased overall survival (p < 0.03). The fetal and embryonal components of epithelial HB, as well as SL, revealed different miRNA expression patterns. Furthermore, miR-21, miR-222, and miR-224 levels predict overall survival of HB patients regardless of epithelial subtype.
Literature
1.
2.
go back to reference Lopez-Terrada D, Zimmermann A (2012) Current issues and controversies in the classification of pediatric hepatocellular tumors. Pediatr Blood Cancer 59:780–784PubMedCrossRef Lopez-Terrada D, Zimmermann A (2012) Current issues and controversies in the classification of pediatric hepatocellular tumors. Pediatr Blood Cancer 59:780–784PubMedCrossRef
3.
go back to reference Allan BJ, Parikh PP, Diaz S, Perez EA, Neville HL, Sola JE (2013) Predictors of survival and incidence of hepatoblastoma in the paediatric population. HPB (Oxford) 15:741–746CrossRef Allan BJ, Parikh PP, Diaz S, Perez EA, Neville HL, Sola JE (2013) Predictors of survival and incidence of hepatoblastoma in the paediatric population. HPB (Oxford) 15:741–746CrossRef
4.
go back to reference Purcell R, Childs M, Maibach R, Miles C, Turner C, Zimmermann A, Sullivan M (2011) HGF/c-Met related activation of beta-catenin in hepatoblastoma. J Exp Clin Cancer Res 30:96PubMedCentralPubMedCrossRef Purcell R, Childs M, Maibach R, Miles C, Turner C, Zimmermann A, Sullivan M (2011) HGF/c-Met related activation of beta-catenin in hepatoblastoma. J Exp Clin Cancer Res 30:96PubMedCentralPubMedCrossRef
5.
go back to reference Dezso K, Halasz J, Bisgaard HC, Paku S, Turanyi E, Schaff Z, Nagy P (2008) Delta-like protein (DLK) is a novel immunohistochemical marker for human hepatoblastomas. Virchows Arch 452:443–448PubMedCrossRef Dezso K, Halasz J, Bisgaard HC, Paku S, Turanyi E, Schaff Z, Nagy P (2008) Delta-like protein (DLK) is a novel immunohistochemical marker for human hepatoblastomas. Virchows Arch 452:443–448PubMedCrossRef
6.
go back to reference Halasz J, Holczbauer A, Paska C, Kovacs M, Benyo G, Verebely T, Schaff Z, Kiss A (2006) Claudin-1 and claudin-2 differentiate fetal and embryonal components in human hepatoblastoma. Hum Pathol 37:555–561PubMedCrossRef Halasz J, Holczbauer A, Paska C, Kovacs M, Benyo G, Verebely T, Schaff Z, Kiss A (2006) Claudin-1 and claudin-2 differentiate fetal and embryonal components in human hepatoblastoma. Hum Pathol 37:555–561PubMedCrossRef
7.
go back to reference Purcell R, Childs M, Maibach R, Miles C, Turner C, Zimmermann A, Czauderna P, Sullivan M (2012) Potential biomarkers for hepatoblastoma: results from the SIOPEL-3 study. Eur J Cancer 48:1853–1859PubMedCrossRef Purcell R, Childs M, Maibach R, Miles C, Turner C, Zimmermann A, Czauderna P, Sullivan M (2012) Potential biomarkers for hepatoblastoma: results from the SIOPEL-3 study. Eur J Cancer 48:1853–1859PubMedCrossRef
8.
go back to reference Kiss A, Szepesi A, Lotz G, Nagy P, Schaff Z (1998) Expression of transforming growth factor-alpha in hepatoblastoma. Cancer 83:690–697PubMedCrossRef Kiss A, Szepesi A, Lotz G, Nagy P, Schaff Z (1998) Expression of transforming growth factor-alpha in hepatoblastoma. Cancer 83:690–697PubMedCrossRef
9.
go back to reference Adesina AM, Lopez-Terrada D, Wong KK, Gunaratne P, Nguyen Y, Pulliam J, Margolin J, Finegold MJ (2009) Gene expression profiling reveals signatures characterizing histologic subtypes of hepatoblastoma and global deregulation in cell growth and survival pathways. Hum Pathol 40:843–853PubMedCentralPubMedCrossRef Adesina AM, Lopez-Terrada D, Wong KK, Gunaratne P, Nguyen Y, Pulliam J, Margolin J, Finegold MJ (2009) Gene expression profiling reveals signatures characterizing histologic subtypes of hepatoblastoma and global deregulation in cell growth and survival pathways. Hum Pathol 40:843–853PubMedCentralPubMedCrossRef
10.
go back to reference Cairo S, Armengol C, Buendia MA (2012) Activation of Wnt and Myc signaling in hepatoblastoma. Front Biosci (Elite Ed) 4:480–486CrossRef Cairo S, Armengol C, Buendia MA (2012) Activation of Wnt and Myc signaling in hepatoblastoma. Front Biosci (Elite Ed) 4:480–486CrossRef
11.
go back to reference Ciesla M, Skrzypek K, Kozakowska M, Loboda A, Jozkowicz A, Dulak J (2011) MicroRNAs as biomarkers of disease onset. Anal Bioanal Chem 401:2051–2061PubMedCrossRef Ciesla M, Skrzypek K, Kozakowska M, Loboda A, Jozkowicz A, Dulak J (2011) MicroRNAs as biomarkers of disease onset. Anal Bioanal Chem 401:2051–2061PubMedCrossRef
14.
go back to reference Cairo S, Wang Y, de Reynies A, Duroure K, Dahan J, Redon MJ, Fabre M, McClelland M, Wang XW, Croce CM, Buendia MA (2010) Stem cell-like micro-RNA signature driven by Myc in aggressive liver cancer. Proc Natl Acad Sci U S A 107:20471–20476PubMedCentralPubMedCrossRef Cairo S, Wang Y, de Reynies A, Duroure K, Dahan J, Redon MJ, Fabre M, McClelland M, Wang XW, Croce CM, Buendia MA (2010) Stem cell-like micro-RNA signature driven by Myc in aggressive liver cancer. Proc Natl Acad Sci U S A 107:20471–20476PubMedCentralPubMedCrossRef
17.
go back to reference Rong M, Chen G, Dang Y (2013) Increased miR-221 expression in hepatocellular carcinoma tissues and its role in enhancing cell growth and inhibiting apoptosis in vitro. BMC Cancer 13:21PubMedCentralPubMedCrossRef Rong M, Chen G, Dang Y (2013) Increased miR-221 expression in hepatocellular carcinoma tissues and its role in enhancing cell growth and inhibiting apoptosis in vitro. BMC Cancer 13:21PubMedCentralPubMedCrossRef
18.
go back to reference Magrelli A, Azzalin G, Salvatore M, Viganotti M, Tosto F, Colombo T, Devito R, Di Masi A, Antoccia A, Lorenzetti S, Maranghi F, Mantovani A, Tanzarella C, Macino G, Taruscio D (2009) Altered microRNA expression patterns in hepatoblastoma patients. Transl Oncol 2:157–163PubMedCentralPubMedCrossRef Magrelli A, Azzalin G, Salvatore M, Viganotti M, Tosto F, Colombo T, Devito R, Di Masi A, Antoccia A, Lorenzetti S, Maranghi F, Mantovani A, Tanzarella C, Macino G, Taruscio D (2009) Altered microRNA expression patterns in hepatoblastoma patients. Transl Oncol 2:157–163PubMedCentralPubMedCrossRef
19.
go back to reference Haas JE, Feusner JH, Finegold MJ (2001) Small cell undifferentiated histology in hepatoblastoma may be unfavorable. Cancer 92:3130–3134PubMedCrossRef Haas JE, Feusner JH, Finegold MJ (2001) Small cell undifferentiated histology in hepatoblastoma may be unfavorable. Cancer 92:3130–3134PubMedCrossRef
20.
go back to reference Perilongo G, Malogolowkin M, Feusner J (2012) Hepatoblastoma clinical research: lessons learned and future challenges. Pediatr Blood Cancer 59:818–821PubMedCrossRef Perilongo G, Malogolowkin M, Feusner J (2012) Hepatoblastoma clinical research: lessons learned and future challenges. Pediatr Blood Cancer 59:818–821PubMedCrossRef
21.
go back to reference Perilongo G, Shafford E, Maibach R, Aronson D, Brugieres L, Brock P, Childs M, Czauderna P, MacKinlay G, Otte JB, Pritchard J, Rondelli R, Scopinaro M, Staalman C, Plaschkes J (2004) Risk-adapted treatment for childhood hepatoblastoma. Final report of the second study of the international society of paediatric oncology—SIOPEL 2. Eur J Cancer 40:411–421PubMedCrossRef Perilongo G, Shafford E, Maibach R, Aronson D, Brugieres L, Brock P, Childs M, Czauderna P, MacKinlay G, Otte JB, Pritchard J, Rondelli R, Scopinaro M, Staalman C, Plaschkes J (2004) Risk-adapted treatment for childhood hepatoblastoma. Final report of the second study of the international society of paediatric oncology—SIOPEL 2. Eur J Cancer 40:411–421PubMedCrossRef
22.
go back to reference Doleshal M, Magotra AA, Choudhury B, Cannon BD, Labourier E, Szafranska AE (2008) Evaluation and validation of total RNA extraction methods for microRNA expression analyses in formalin-fixed, paraffin-embedded tissues. J Mol Diagn 10:203–211PubMedCentralPubMedCrossRef Doleshal M, Magotra AA, Choudhury B, Cannon BD, Labourier E, Szafranska AE (2008) Evaluation and validation of total RNA extraction methods for microRNA expression analyses in formalin-fixed, paraffin-embedded tissues. J Mol Diagn 10:203–211PubMedCentralPubMedCrossRef
23.
go back to reference Karakatsanis A, Papaconstantinou I, Gazouli M, Lyberopoulou A, Polymeneas G, Voros D (2013) 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 52:297–303PubMedCrossRef Karakatsanis A, Papaconstantinou I, Gazouli M, Lyberopoulou A, Polymeneas G, Voros D (2013) 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 52:297–303PubMedCrossRef
24.
go back to reference Varnholt H, Drebber U, Schulze F, Wedemeyer I, Schirmacher P, Dienes HP, Odenthal M (2008) MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology 47:1223–1232PubMedCrossRef Varnholt H, Drebber U, Schulze F, Wedemeyer I, Schirmacher P, Dienes HP, Odenthal M (2008) MicroRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology 47:1223–1232PubMedCrossRef
25.
go back to reference Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, Mazzaferro V, Lowe SW, Croce CM, Dejean A (2010) miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci U S A 107:264–269PubMedCentralPubMedCrossRef Pineau P, Volinia S, McJunkin K, Marchio A, Battiston C, Terris B, Mazzaferro V, Lowe SW, Croce CM, Dejean A (2010) miR-221 overexpression contributes to liver tumorigenesis. Proc Natl Acad Sci U S A 107:264–269PubMedCentralPubMedCrossRef
26.
go back to reference Andersen CL, Jensen JL, Orntoft TF (2004) 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 64:5245–5250PubMedCrossRef Andersen CL, Jensen JL, Orntoft TF (2004) 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 64:5245–5250PubMedCrossRef
27.
go back to reference Ismail H, Broniszczak D, Kalicinski P, Dembowska-Baginska B, Perek D, Teisseyre J, Kluge P, Kosciesza A, Lembas A, Markiewicz M (2012) Changing treatment and outcome of children with hepatoblastoma: analysis of a single center experience over the last 20 years. J Pediatr Surg 47:1331–1339PubMedCrossRef Ismail H, Broniszczak D, Kalicinski P, Dembowska-Baginska B, Perek D, Teisseyre J, Kluge P, Kosciesza A, Lembas A, Markiewicz M (2012) Changing treatment and outcome of children with hepatoblastoma: analysis of a single center experience over the last 20 years. J Pediatr Surg 47:1331–1339PubMedCrossRef
28.
go back to reference Shenouda SK, Alahari SK (2009) MicroRNA function in cancer: oncogene or a tumor suppressor? Cancer Metastasis Rev 28:369–378PubMedCrossRef Shenouda SK, Alahari SK (2009) MicroRNA function in cancer: oncogene or a tumor suppressor? Cancer Metastasis Rev 28:369–378PubMedCrossRef
29.
go back to reference Lopez-Terrada D, Gunaratne PH, Adesina AM, Pulliam J, Hoang DM, Nguyen Y, Mistretta TA, Margolin J, Finegold MJ (2009) Histologic subtypes of hepatoblastoma are characterized by differential canonical Wnt and Notch pathway activation in DLK + precursors. Hum Pathol 40:783–794PubMedCrossRef Lopez-Terrada D, Gunaratne PH, Adesina AM, Pulliam J, Hoang DM, Nguyen Y, Mistretta TA, Margolin J, Finegold MJ (2009) Histologic subtypes of hepatoblastoma are characterized by differential canonical Wnt and Notch pathway activation in DLK + precursors. Hum Pathol 40:783–794PubMedCrossRef
30.
go back to reference Chopra A, Iyer VK, Agarwala S, Mathur SR, Aron M, Gupta SD, Verma K (2010) Apoptotic protein expression, glycogen content, DNA ploidy and cell proliferation in hepatoblastoma subtyping and their role in prognostication. Pediatr Surg Int 26:1173–1178PubMedCrossRef Chopra A, Iyer VK, Agarwala S, Mathur SR, Aron M, Gupta SD, Verma K (2010) Apoptotic protein expression, glycogen content, DNA ploidy and cell proliferation in hepatoblastoma subtyping and their role in prognostication. Pediatr Surg Int 26:1173–1178PubMedCrossRef
31.
go back to reference von Frowein J, Pagel P, Kappler R, von Schweinitz D, Roscher A, Schmid I (2011) MicroRNA-492 is processed from the keratin 19 gene and up-regulated in metastatic hepatoblastoma. Hepatology 53:833–842CrossRef von Frowein J, Pagel P, Kappler R, von Schweinitz D, Roscher A, Schmid I (2011) MicroRNA-492 is processed from the keratin 19 gene and up-regulated in metastatic hepatoblastoma. Hepatology 53:833–842CrossRef
32.
go back to reference Scisciani C, Vossio S, Guerrieri F, Schinzari V, De Iaco R, D’Onorio de Meo P, Cervello M, Montalto G, Pollicino T, Raimondo G, Levrero M, Pediconi N (2012) Transcriptional regulation of miR-224 upregulated in human HCCs by NFkappaB inflammatory pathways. J Hepatol 56:855–861PubMedCrossRef Scisciani C, Vossio S, Guerrieri F, Schinzari V, De Iaco R, D’Onorio de Meo P, Cervello M, Montalto G, Pollicino T, Raimondo G, Levrero M, Pediconi N (2012) Transcriptional regulation of miR-224 upregulated in human HCCs by NFkappaB inflammatory pathways. J Hepatol 56:855–861PubMedCrossRef
33.
go back to reference Boutz DR, Collins PJ, Suresh U, Lu M, Ramirez CM, Fernandez-Hernando C, Huang Y, Abreu Rde S, Le SY, Shapiro BA, Liu AM, Luk JM, Aldred SF, Trinklein ND, Marcotte EM, Penalva LO (2011) Two-tiered approach identifies a network of cancer and liver disease-related genes regulated by miR-122. J Biol Chem 286:18066–18078PubMedCentralPubMedCrossRef Boutz DR, Collins PJ, Suresh U, Lu M, Ramirez CM, Fernandez-Hernando C, Huang Y, Abreu Rde S, Le SY, Shapiro BA, Liu AM, Luk JM, Aldred SF, Trinklein ND, Marcotte EM, Penalva LO (2011) Two-tiered approach identifies a network of cancer and liver disease-related genes regulated by miR-122. J Biol Chem 286:18066–18078PubMedCentralPubMedCrossRef
34.
go back to reference Hu J, Xu Y, Hao J, Wang S, Li C, Meng S (2012) MiR-122 in hepatic function and liver diseases. Protein Cell 3:364–371PubMedCrossRef Hu J, Xu Y, Hao J, Wang S, Li C, Meng S (2012) MiR-122 in hepatic function and liver diseases. Protein Cell 3:364–371PubMedCrossRef
35.
go back to reference Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM (2009) MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology 50:113–121PubMedCrossRef Xu T, Zhu Y, Xiong Y, Ge YY, Yun JP, Zhuang SM (2009) MicroRNA-195 suppresses tumorigenicity and regulates G1/S transition of human hepatocellular carcinoma cells. Hepatology 50:113–121PubMedCrossRef
36.
go back to reference Chen L, Jiang M, Yuan W, Tang H (2012) miR-17-5p as a novel prognostic marker for hepatocellular carcinoma. J Invest Surg 25:156–161PubMedCrossRef Chen L, Jiang M, Yuan W, Tang H (2012) miR-17-5p as a novel prognostic marker for hepatocellular carcinoma. J Invest Surg 25:156–161PubMedCrossRef
37.
go back to reference Yang W, Sun T, Cao J, Liu F, Tian Y, Zhu W (2012) Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res 318:944–954PubMedCrossRef Yang W, Sun T, Cao J, Liu F, Tian Y, Zhu W (2012) Downregulation of miR-210 expression inhibits proliferation, induces apoptosis and enhances radiosensitivity in hypoxic human hepatoma cells in vitro. Exp Cell Res 318:944–954PubMedCrossRef
38.
go back to reference El Tayebi HM, Omar K, Hegy S, El Maghrabi M, El Brolosy M, Hosny KA, Esmat G, Abdelaziz AI (2013) Repression of miR-17-5p with elevated expression of E2F-1 and c-MYC in non-metastatic hepatocellular carcinoma and enhancement of cell growth upon reversing this expression pattern. Biochem Biophys Res Commun 434:421–427PubMedCrossRef El Tayebi HM, Omar K, Hegy S, El Maghrabi M, El Brolosy M, Hosny KA, Esmat G, Abdelaziz AI (2013) Repression of miR-17-5p with elevated expression of E2F-1 and c-MYC in non-metastatic hepatocellular carcinoma and enhancement of cell growth upon reversing this expression pattern. Biochem Biophys Res Commun 434:421–427PubMedCrossRef
39.
go back to reference Wang X, Chen J, Li F, Lin Y, Zhang X, Lv Z, Jiang J (2012) MiR-214 inhibits cell growth in hepatocellular carcinoma through suppression of beta-catenin. Biochem Biophys Res Commun 428:525–531PubMedCrossRef Wang X, Chen J, Li F, Lin Y, Zhang X, Lv Z, Jiang J (2012) MiR-214 inhibits cell growth in hepatocellular carcinoma through suppression of beta-catenin. Biochem Biophys Res Commun 428:525–531PubMedCrossRef
40.
go back to reference Wu W, Takanashi M, Borjigin N, Ohno SI, Fujita K, Hoshino S, Osaka Y, Tsuchida A, Kuroda M (2013) MicroRNA-18a modulates STAT3 activity through negative regulation of PIAS3 during gastric adenocarcinogenesis. Br J Cancer 108:653–661PubMedCentralPubMedCrossRef Wu W, Takanashi M, Borjigin N, Ohno SI, Fujita K, Hoshino S, Osaka Y, Tsuchida A, Kuroda M (2013) MicroRNA-18a modulates STAT3 activity through negative regulation of PIAS3 during gastric adenocarcinogenesis. Br J Cancer 108:653–661PubMedCentralPubMedCrossRef
41.
go back to reference Brock M, Trenkmann M, Gay RE, Gay S, Speich R, Huber LC (2011) MicroRNA-18a enhances the interleukin-6-mediated production of the acute-phase proteins fibrinogen and haptoglobin in human hepatocytes. J Biol Chem 286:40142–40150PubMedCentralPubMedCrossRef Brock M, Trenkmann M, Gay RE, Gay S, Speich R, Huber LC (2011) MicroRNA-18a enhances the interleukin-6-mediated production of the acute-phase proteins fibrinogen and haptoglobin in human hepatocytes. J Biol Chem 286:40142–40150PubMedCentralPubMedCrossRef
42.
go back to reference Wong QW, Ching AK, Chan AW, Choy KW, To KF, Lai PB, Wong N (2010) MiR-222 overexpression confers cell migratory advantages in hepatocellular carcinoma through enhancing AKT signaling. Clin Cancer Res 16:867–875PubMedCrossRef Wong QW, Ching AK, Chan AW, Choy KW, To KF, Lai PB, Wong N (2010) MiR-222 overexpression confers cell migratory advantages in hepatocellular carcinoma through enhancing AKT signaling. Clin Cancer Res 16:867–875PubMedCrossRef
43.
go back to reference Garofalo M, Quintavalle C, Romano G, Croce CM, Condorelli G (2012) miR221/222 in cancer: their role in tumor progression and response to therapy. Curr Mol Med 12:27–33PubMedCentralPubMedCrossRef Garofalo M, Quintavalle C, Romano G, Croce CM, Condorelli G (2012) miR221/222 in cancer: their role in tumor progression and response to therapy. Curr Mol Med 12:27–33PubMedCentralPubMedCrossRef
44.
go back to reference Ma D, Tao X, Gao F, Fan C, Wu D (2012) miR-224 functions as an onco-miRNA in hepatocellular carcinoma cells by activating AKT signaling. Oncol Lett 4:483–488PubMedCentralPubMed Ma D, Tao X, Gao F, Fan C, Wu D (2012) miR-224 functions as an onco-miRNA in hepatocellular carcinoma cells by activating AKT signaling. Oncol Lett 4:483–488PubMedCentralPubMed
45.
go back to reference Shen SN, Wang LF, Jia YF, Hao YQ, Zhang L, Wang H (2013) Upregulation of microRNA-224 is associated with aggressive progression and poor prognosis in human cervical cancer. Diagn Pathol 8:69PubMedCentralPubMedCrossRef Shen SN, Wang LF, Jia YF, Hao YQ, Zhang L, Wang H (2013) Upregulation of microRNA-224 is associated with aggressive progression and poor prognosis in human cervical cancer. Diagn Pathol 8:69PubMedCentralPubMedCrossRef
46.
go back to reference Lu S, Wang S, Geng S, Ma S, Liang Z, Jiao B (2013) Upregulation of microRNA-224 confers a poor prognosis in glioma patients. Clin Transl Oncol 15:569–574PubMedCrossRef Lu S, Wang S, Geng S, Ma S, Liang Z, Jiao B (2013) Upregulation of microRNA-224 confers a poor prognosis in glioma patients. Clin Transl Oncol 15:569–574PubMedCrossRef
47.
go back to reference Zhu Q, Wang Z, Hu Y, Li J, Li X, Zhou L, Huang Y (2012) miR-21 promotes migration and invasion by the miR-21-PDCD4-AP-1 feedback loop in human hepatocellular carcinoma. Oncol Rep 27:1660–1668PubMed Zhu Q, Wang Z, Hu Y, Li J, Li X, Zhou L, Huang Y (2012) miR-21 promotes migration and invasion by the miR-21-PDCD4-AP-1 feedback loop in human hepatocellular carcinoma. Oncol Rep 27:1660–1668PubMed
48.
go back to reference Bao L, Yan Y, Xu C, Ji W, Shen S, Xu G, Zeng Y, Sun B, Qian H, Chen L, Wu M, Chen J, Su C (2013) MicroRNA-21 suppresses PTEN and hSulf-1 expression and promotes hepatocellular carcinoma progression through AKT/ERK pathways. Cancer Lett 337:226–236PubMedCrossRef Bao L, Yan Y, Xu C, Ji W, Shen S, Xu G, Zeng Y, Sun B, Qian H, Chen L, Wu M, Chen J, Su C (2013) MicroRNA-21 suppresses PTEN and hSulf-1 expression and promotes hepatocellular carcinoma progression through AKT/ERK pathways. Cancer Lett 337:226–236PubMedCrossRef
Metadata
Title
microRNA expression might predict prognosis of epithelial hepatoblastoma
Authors
Mónika Gyugos
Gábor Lendvai
István Kenessey
Krisztina Schlachter
Judit Halász
Péter Nagy
Miklós Garami
Zsuzsa Jakab
Zsuzsa Schaff
András Kiss
Publication date
01-04-2014
Publisher
Springer Berlin Heidelberg
Published in
Virchows Archiv / Issue 4/2014
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-014-1549-y

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