Skip to main content
Top
Published in: Journal of Neuro-Oncology 3/2013

01-05-2013 | Laboratory Investigation

Comparison of microRNA expression levels between initial and recurrent glioblastoma specimens

Authors: Aysegül Ilhan-Mutlu, Adelheid Wöhrer, Anna Sophie Berghoff, Georg Widhalm, Christine Marosi, Ludwig Wagner, Matthias Preusser

Published in: Journal of Neuro-Oncology | Issue 3/2013

Login to get access

Abstract

Glioblastoma is the most frequent primary brain tumour in adults. Recent therapeutic advances increased patient's survival, but tumour recurrence inevitably occurs. The pathobiological mechanisms involved in glioblastoma recurrence are still unclear. MicroRNAs are small RNAs proposed o have important roles for cancer including proliferation, aggressiveness and metastases development. There exist only few data on the involvement of microRNAs in glioblastoma recurrence. We selected the following 7 microRNAs with potential relevance for glioblastoma pathobiology by means of a comprehensive literature search: microRNA-10b, microRNA-21, microRNA-181b, microRNA-181c, microRNA-195, microRNA-221 and microRNA-222. We further selected 15 primary glioblastoma patients, of whom formalin fixed and paraffin embedded tissue (FFPE) of the initial and recurrence surgery were available. All patients had received first line treatment consisting of postoperative combined radiochemotherapy with temozolomide (n = 15). Non-neoplastic brain tissue samples from 3 patients with temporal lobe epilepsy served as control. The expression of the microRNAs were analysed by RT-qPCR. These were correlated with each other and with clinical parameters. All microRNAs showed detectable levels of expressions in glioblastoma group, whereas microRNA-10b was not detectable in epilepsy patients. MicroRNAs except microRNA-21 showed significantly higher levels in epilepsy patients when compared to the levels of first resection of glioblastoma. Comparison of microRNA levels between first and second resections revealed no significant change. Cox regression analyses showed no significant association of microRNA expression levels in the tumor tissue with progression free survival times. Expression levels of microRNA-10b, microRNA-21, microRNA-181b, microRNA-181c, microRNA-195, microRNA-221 and microRNA-222 do not differ significantly between initial and recurrent glioblastoma.
Literature
1.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef
2.
go back to reference Stupp R, Roila F (2009) Malignant glioma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 20(Suppl 4):126–128PubMed Stupp R, Roila F (2009) Malignant glioma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 20(Suppl 4):126–128PubMed
3.
go back to reference Preusser M, de Ribaupierre S, Wohrer A, Erridge SC, Hegi M, Weller M, Stupp R (2011) Current concepts and management of glioblastoma. Ann Neurol 70:9–21PubMedCrossRef Preusser M, de Ribaupierre S, Wohrer A, Erridge SC, Hegi M, Weller M, Stupp R (2011) Current concepts and management of glioblastoma. Ann Neurol 70:9–21PubMedCrossRef
4.
5.
go back to reference Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28:5369–5380PubMedCrossRef Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28:5369–5380PubMedCrossRef
6.
go back to reference Conti A, Aguennouz M, La Torre D, Tomasello C, Cardali S, Angileri FF, Maio F, Cama A, Germano A, Vita G, Tomasello F (2009) MiR-21 and 221 upregulation and miR-181b downregulation in human grade II-IV astrocytic tumors. J Neurooncol 93:325–332PubMedCrossRef Conti A, Aguennouz M, La Torre D, Tomasello C, Cardali S, Angileri FF, Maio F, Cama A, Germano A, Vita G, Tomasello F (2009) MiR-21 and 221 upregulation and miR-181b downregulation in human grade II-IV astrocytic tumors. J Neurooncol 93:325–332PubMedCrossRef
7.
go back to reference Shi L, Chen J, Yang J, Pan T, Zhang S, Wang Z (2010) MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity. Brain Res 1352:255–264PubMedCrossRef Shi L, Chen J, Yang J, Pan T, Zhang S, Wang Z (2010) MiR-21 protected human glioblastoma U87MG cells from chemotherapeutic drug temozolomide induced apoptosis by decreasing Bax/Bcl-2 ratio and caspase-3 activity. Brain Res 1352:255–264PubMedCrossRef
8.
go back to reference Sasayama T, Nishihara M, Kondoh T, Hosoda K, Kohmura E (2009) MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int J Cancer 125:1407–1413PubMedCrossRef Sasayama T, Nishihara M, Kondoh T, Hosoda K, Kohmura E (2009) MicroRNA-10b is overexpressed in malignant glioma and associated with tumor invasive factors, uPAR and RhoC. Int J Cancer 125:1407–1413PubMedCrossRef
9.
go back to reference Slaby O, Lakomy R, Fadrus P, Hrstka R, Kren L, Lzicarova E, Smrcka M, Svoboda M, Dolezalova H, Novakova J, Valik D, Vyzula R, Michalek J (2010) MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma 57:264–269PubMedCrossRef Slaby O, Lakomy R, Fadrus P, Hrstka R, Kren L, Lzicarova E, Smrcka M, Svoboda M, Dolezalova H, Novakova J, Valik D, Vyzula R, Michalek J (2010) MicroRNA-181 family predicts response to concomitant chemoradiotherapy with temozolomide in glioblastoma patients. Neoplasma 57:264–269PubMedCrossRef
10.
go back to reference Ujifuku K, Mitsutake N, Takakura S, Matsuse M, Saenko V, Suzuki K, Hayashi K, Matsuo T, Kamada K, Nagata I, Yamashita S (2010) MiR-195, miR-455-3p and miR-10a(*) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett 296:241–248PubMedCrossRef Ujifuku K, Mitsutake N, Takakura S, Matsuse M, Saenko V, Suzuki K, Hayashi K, Matsuo T, Kamada K, Nagata I, Yamashita S (2010) MiR-195, miR-455-3p and miR-10a(*) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett 296:241–248PubMedCrossRef
11.
go back to reference Preusser M, Wohrer A, Stary S, Hoftberger R, Streubel B, Hainfellner JA (2011) Value and limitations of immunohistochemistry and gene sequencing for detection of the IDH1-R132H mutation in diffuse glioma biopsy specimens. J Neuropathol Exp Neurol 70:715–723PubMedCrossRef Preusser M, Wohrer A, Stary S, Hoftberger R, Streubel B, Hainfellner JA (2011) Value and limitations of immunohistochemistry and gene sequencing for detection of the IDH1-R132H mutation in diffuse glioma biopsy specimens. J Neuropathol Exp Neurol 70:715–723PubMedCrossRef
12.
go back to reference Preusser M, Hoeftberger R, Woehrer A, Gelpi E, Kouwenhoven M, Kros JM, Sanson M, Idbaih A, Brandes AA, Heinzl H, Gorlia T, Hainfellner JA, van den Bent M (2012) Prognostic value of Ki67 index in anaplastic oligodendroglial tumours–a translational study of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Histopathology 60:885–894PubMedCrossRef Preusser M, Hoeftberger R, Woehrer A, Gelpi E, Kouwenhoven M, Kros JM, Sanson M, Idbaih A, Brandes AA, Heinzl H, Gorlia T, Hainfellner JA, van den Bent M (2012) Prognostic value of Ki67 index in anaplastic oligodendroglial tumours–a translational study of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Histopathology 60:885–894PubMedCrossRef
13.
go back to reference Capper D, Weissert S, Balss J, Habel A, Meyer J, Jager D, Ackermann U, Tessmer C, Korshunov A, Zentgraf H, Hartmann C, von Deimling A (2010) Characterization of R132H mutation-specific IDH1 antibody binding in brain tumors. Brain Pathol 20:245–254PubMedCrossRef Capper D, Weissert S, Balss J, Habel A, Meyer J, Jager D, Ackermann U, Tessmer C, Korshunov A, Zentgraf H, Hartmann C, von Deimling A (2010) Characterization of R132H mutation-specific IDH1 antibody binding in brain tumors. Brain Pathol 20:245–254PubMedCrossRef
14.
go back to reference Quintavalle C, Garofalo M, Zanca C, Romano G, Iaboni M, del Basso De Caro M, Martinez-Montero JC, Incoronato M, Nuovo G, Croce CM, Condorelli G (2012) MiR-221/222 overexpession in human glioblastoma increases invasiveness by targeting the protein phosphate PTPmu. Oncogene 31: 858–868 Quintavalle C, Garofalo M, Zanca C, Romano G, Iaboni M, del Basso De Caro M, Martinez-Montero JC, Incoronato M, Nuovo G, Croce CM, Condorelli G (2012) MiR-221/222 overexpession in human glioblastoma increases invasiveness by targeting the protein phosphate PTPmu. Oncogene 31: 858–868
15.
go back to reference Wuchty S, Arjona D, Li A, Kotliarov Y, Walling J, Ahn S, Zhang A, Maric D, Anolik R, Zenklusen JC, Fine HA (2011) Prediction of associations between microRNAs and gene expression in glioma biology. PLoS ONE 6:e14681PubMedCrossRef Wuchty S, Arjona D, Li A, Kotliarov Y, Walling J, Ahn S, Zhang A, Maric D, Anolik R, Zenklusen JC, Fine HA (2011) Prediction of associations between microRNAs and gene expression in glioma biology. PLoS ONE 6:e14681PubMedCrossRef
16.
go back to reference Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M, Vandenberg SR, Ginzinger DG, James CD, Costello JF, Bergers G, Weiss WA, Alvarez-Buylla A, Hodgson JG (2008) MiR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC medicine 6:14PubMedCrossRef Silber J, Lim DA, Petritsch C, Persson AI, Maunakea AK, Yu M, Vandenberg SR, Ginzinger DG, James CD, Costello JF, Bergers G, Weiss WA, Alvarez-Buylla A, Hodgson JG (2008) MiR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC medicine 6:14PubMedCrossRef
17.
go back to reference Stefanits H, Czech T, Pataraia E, Baumgartner C, Derhaschnig N, Slana A, Kovacs GG (2012) Prominent oligodendroglial response in surgical specimens of patients with temporal lobe epilepsy. Clin Neuropathol 31:409–417PubMed Stefanits H, Czech T, Pataraia E, Baumgartner C, Derhaschnig N, Slana A, Kovacs GG (2012) Prominent oligodendroglial response in surgical specimens of patients with temporal lobe epilepsy. Clin Neuropathol 31:409–417PubMed
18.
go back to reference Lakomy R, Sana J, Hankeova S, Fadrus P, Kren L, Lzicarova E, Svoboda M, Dolezelova H, Smrcka M, Vyzula R, Michalek J, Hajduch M, Slaby O (2011) MiR-195, miR-196b, miR-181c, miR-21 expression levels and O-6-methylguanine-DNA methyltransferase methylation status are associated with clinical outcome in glioblastoma patients. Cancer Sci 102:2186–2190PubMedCrossRef Lakomy R, Sana J, Hankeova S, Fadrus P, Kren L, Lzicarova E, Svoboda M, Dolezelova H, Smrcka M, Vyzula R, Michalek J, Hajduch M, Slaby O (2011) MiR-195, miR-196b, miR-181c, miR-21 expression levels and O-6-methylguanine-DNA methyltransferase methylation status are associated with clinical outcome in glioblastoma patients. Cancer Sci 102:2186–2190PubMedCrossRef
19.
go back to reference Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769–773PubMedCrossRef Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433:769–773PubMedCrossRef
20.
go back to reference Litofsky NS, Mix TC, Baker SP, Recht LD, Smith TW (1998) Ki-67 (clone MIB-1) proliferation index in recurrent glial neoplasms: no prognostic significance. Surg Neurol 50:579–585PubMedCrossRef Litofsky NS, Mix TC, Baker SP, Recht LD, Smith TW (1998) Ki-67 (clone MIB-1) proliferation index in recurrent glial neoplasms: no prognostic significance. Surg Neurol 50:579–585PubMedCrossRef
21.
go back to reference Ralte AM, Sharma MC, Karak AK, Mehta VS, Sarkar C (2001) Clinicopathological features, MIB-1 labeling index and apoptotic index in recurrent astrocytic tumors. Pathol Oncol Res 7:267–278PubMedCrossRef Ralte AM, Sharma MC, Karak AK, Mehta VS, Sarkar C (2001) Clinicopathological features, MIB-1 labeling index and apoptotic index in recurrent astrocytic tumors. Pathol Oncol Res 7:267–278PubMedCrossRef
22.
go back to reference Schroder R, Feisel KD, Ernestus RI (2002) Ki-67 labeling is correlated with the time to recurrence in primary glioblastomas. J Neurooncol 56:127–132PubMedCrossRef Schroder R, Feisel KD, Ernestus RI (2002) Ki-67 labeling is correlated with the time to recurrence in primary glioblastomas. J Neurooncol 56:127–132PubMedCrossRef
23.
go back to reference Lin J, Teo S, Lam DH, Jeyaseelan K, Wang S (2012) MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell Death Dis 3:e398PubMedCrossRef Lin J, Teo S, Lam DH, Jeyaseelan K, Wang S (2012) MicroRNA-10b pleiotropically regulates invasion, angiogenicity and apoptosis of tumor cells resembling mesenchymal subtype of glioblastoma multiforme. Cell Death Dis 3:e398PubMedCrossRef
24.
go back to reference Dong CG, Wu WK, Feng SY, Wang XJ, Shao JF, Qiao J (2012) Co-inhibition of microRNA-10b and microRNA-21 exerts synergistic inhibition on the proliferation and invasion of human glioma cells. Int J Oncol 41:1005–1012PubMed Dong CG, Wu WK, Feng SY, Wang XJ, Shao JF, Qiao J (2012) Co-inhibition of microRNA-10b and microRNA-21 exerts synergistic inhibition on the proliferation and invasion of human glioma cells. Int J Oncol 41:1005–1012PubMed
25.
go back to reference Gabriely G, Teplyuk NM, Krichevsky AM (2011) Context effect: microRNA-10b in cancer cell proliferation, spread and death. Autophagy 7:1384–1386PubMedCrossRef Gabriely G, Teplyuk NM, Krichevsky AM (2011) Context effect: microRNA-10b in cancer cell proliferation, spread and death. Autophagy 7:1384–1386PubMedCrossRef
26.
go back to reference Gabriely G, Yi M, Narayan RS, Niers JM, Wurdinger T, Imitola J, Ligon KL, Kesari S, Esau C, Stephens RM, Tannous BA, Krichevsky AM (2011) Human glioma growth is controlled by microRNA-10b. Cancer Res 71:3563–3572PubMedCrossRef Gabriely G, Yi M, Narayan RS, Niers JM, Wurdinger T, Imitola J, Ligon KL, Kesari S, Esau C, Stephens RM, Tannous BA, Krichevsky AM (2011) Human glioma growth is controlled by microRNA-10b. Cancer Res 71:3563–3572PubMedCrossRef
27.
go back to reference Costa PM, Cardoso AL, Nobrega C, Pereira de Almeida LF, Bruce JN, Canoll P, Pedroso de Lima MC (2013) MicroRNA-21 silencing enhances the cytotoxic effect of the antiangiogenic drug sunitinib in glioblastoma. Hum Mol Genet 22(5):904–918PubMedCrossRef Costa PM, Cardoso AL, Nobrega C, Pereira de Almeida LF, Bruce JN, Canoll P, Pedroso de Lima MC (2013) MicroRNA-21 silencing enhances the cytotoxic effect of the antiangiogenic drug sunitinib in glioblastoma. Hum Mol Genet 22(5):904–918PubMedCrossRef
28.
go back to reference Costa PM, Cardoso AL, Pereira de Almeida LF, Bruce JN, Canoll P, Pedroso de Lima MC (2012) PDGF-B-mediated downregulation of miR-21: new insights into PDGF signaling in glioblastoma. Hum Mol Genet 21:5118–5130PubMedCrossRef Costa PM, Cardoso AL, Pereira de Almeida LF, Bruce JN, Canoll P, Pedroso de Lima MC (2012) PDGF-B-mediated downregulation of miR-21: new insights into PDGF signaling in glioblastoma. Hum Mol Genet 21:5118–5130PubMedCrossRef
29.
go back to reference Quintavalle C, Donnarumma E, Iaboni M, Roscigno G, Garofalo M, Romano G, Fiore D, De Marinis P, Croce CM, Condorelli G (2012) Effect of miR-21 and miR-30b/c on TRAIL-induced apoptosis in glioma cells. Oncogene. doi:10.1038/onc.2012.410 Quintavalle C, Donnarumma E, Iaboni M, Roscigno G, Garofalo M, Romano G, Fiore D, De Marinis P, Croce CM, Condorelli G (2012) Effect of miR-21 and miR-30b/c on TRAIL-induced apoptosis in glioma cells. Oncogene. doi:10.​1038/​onc.​2012.​410
30.
go back to reference Ilhan-Mutlu A, Wagner L, Wohrer A, Furtner J, Widhalm G, Marosi C, Preusser M (2012) Plasma microRNA-21 concentration may be a useful biomarker in glioblastoma patients. Cancer Invest 30:615–621PubMedCrossRef Ilhan-Mutlu A, Wagner L, Wohrer A, Furtner J, Widhalm G, Marosi C, Preusser M (2012) Plasma microRNA-21 concentration may be a useful biomarker in glioblastoma patients. Cancer Invest 30:615–621PubMedCrossRef
31.
go back to reference Wang Q, Li P, Li A, Jiang W, Wang H, Wang J, Xie K (2012) Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. J Exp Clin Cancer Res 31:97PubMedCrossRef Wang Q, Li P, Li A, Jiang W, Wang H, Wang J, Xie K (2012) Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. J Exp Clin Cancer Res 31:97PubMedCrossRef
32.
go back to reference Wong ST, Zhang XQ, Zhuang JT, Chan HL, Li CH, Leung GK (2012) MicroRNA-21 inhibition enhances in vitro chemosensitivity of temozolomide-resistant glioblastoma cells. Anticancer Res 32:2835–2841PubMed Wong ST, Zhang XQ, Zhuang JT, Chan HL, Li CH, Leung GK (2012) MicroRNA-21 inhibition enhances in vitro chemosensitivity of temozolomide-resistant glioblastoma cells. Anticancer Res 32:2835–2841PubMed
33.
go back to reference Wang YY, Sun G, Luo H, Wang XF, Lan FM, Yue X, Fu LS, Pu PY, Kang CS, Liu N, You YP (2012) MiR-21 modulates hTERT through a STAT3-dependent manner on glioblastoma cell growth. CNS Neurosci Ther 18:722–728PubMedCrossRef Wang YY, Sun G, Luo H, Wang XF, Lan FM, Yue X, Fu LS, Pu PY, Kang CS, Liu N, You YP (2012) MiR-21 modulates hTERT through a STAT3-dependent manner on glioblastoma cell growth. CNS Neurosci Ther 18:722–728PubMedCrossRef
34.
go back to reference Zhang S, Wan Y, Pan T, Gu X, Qian C, Sun G, Sun L, Xiang Y, Wang Z, Shi L (2012) MicroRNA-21 inhibitor sensitizes human glioblastoma U251 stem cells to chemotherapeutic drug temozolomide. J Mol Neurosci 47:346–356PubMedCrossRef Zhang S, Wan Y, Pan T, Gu X, Qian C, Sun G, Sun L, Xiang Y, Wang Z, Shi L (2012) MicroRNA-21 inhibitor sensitizes human glioblastoma U251 stem cells to chemotherapeutic drug temozolomide. J Mol Neurosci 47:346–356PubMedCrossRef
35.
go back to reference Gaur AB, Holbeck SL, Colburn NH, Israel MA (2011) Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro Oncol 13:580–590PubMedCrossRef Gaur AB, Holbeck SL, Colburn NH, Israel MA (2011) Downregulation of Pdcd4 by mir-21 facilitates glioblastoma proliferation in vivo. Neuro Oncol 13:580–590PubMedCrossRef
36.
go back to reference Li Y, Zhao S, Zhen Y, Li Q, Teng L, Asai A, Kawamoto K (2011) A miR-21 inhibitor enhances apoptosis and reduces G(2)-M accumulation induced by ionizing radiation in human glioblastoma U251 cells. Brain Tumor Pathol 28:209–214PubMedCrossRef Li Y, Zhao S, Zhen Y, Li Q, Teng L, Asai A, Kawamoto K (2011) A miR-21 inhibitor enhances apoptosis and reduces G(2)-M accumulation induced by ionizing radiation in human glioblastoma U251 cells. Brain Tumor Pathol 28:209–214PubMedCrossRef
37.
go back to reference Schramedei K, Morbt N, Pfeifer G, Lauter J, Rosolowski M, Tomm JM, von Bergen M, Horn F, Brocke-Heidrich K (2011) MicroRNA-21 targets tumor suppressor genes ANP32A and SMARCA4. Oncogene 30:2975–2985PubMedCrossRef Schramedei K, Morbt N, Pfeifer G, Lauter J, Rosolowski M, Tomm JM, von Bergen M, Horn F, Brocke-Heidrich K (2011) MicroRNA-21 targets tumor suppressor genes ANP32A and SMARCA4. Oncogene 30:2975–2985PubMedCrossRef
38.
go back to reference Ren Y, Zhou X, Mei M, Yuan XB, Han L, Wang GX, Jia ZF, Xu P, Pu PY, Kang CS (2010) MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC Cancer 10:27PubMedCrossRef Ren Y, Zhou X, Mei M, Yuan XB, Han L, Wang GX, Jia ZF, Xu P, Pu PY, Kang CS (2010) MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC Cancer 10:27PubMedCrossRef
39.
go back to reference Zhou X, Ren Y, Moore L, Mei M, You Y, Xu P, Wang B, Wang G, Jia Z, Pu P, Zhang W, Kang C (2010) Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN status. Lab Invest 90:144–155PubMedCrossRef Zhou X, Ren Y, Moore L, Mei M, You Y, Xu P, Wang B, Wang G, Jia Z, Pu P, Zhang W, Kang C (2010) Downregulation of miR-21 inhibits EGFR pathway and suppresses the growth of human glioblastoma cells independent of PTEN status. Lab Invest 90:144–155PubMedCrossRef
40.
go back to reference Chen Y, Liu W, Chao T, Zhang Y, Yan X, Gong Y, Qiang B, Yuan J, Sun M, Peng X (2008) MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Lett 272:197–205PubMedCrossRef Chen Y, Liu W, Chao T, Zhang Y, Yan X, Gong Y, Qiang B, Yuan J, Sun M, Peng X (2008) MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Lett 272:197–205PubMedCrossRef
41.
go back to reference Papagiannakopoulos T, Shapiro A, Kosik KS (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68:8164–8172PubMedCrossRef Papagiannakopoulos T, Shapiro A, Kosik KS (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68:8164–8172PubMedCrossRef
42.
go back to reference Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R, Shah K (2007) MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res 67:8994–9000PubMedCrossRef Corsten MF, Miranda R, Kasmieh R, Krichevsky AM, Weissleder R, Shah K (2007) MicroRNA-21 knockdown disrupts glioma growth in vivo and displays synergistic cytotoxicity with neural precursor cell delivered S-TRAIL in human gliomas. Cancer Res 67:8994–9000PubMedCrossRef
43.
go back to reference Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029–6033PubMedCrossRef Chan JA, Krichevsky AM, Kosik KS (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65:6029–6033PubMedCrossRef
44.
go back to reference Zhang QQ, Xu H, Huang MB, Ma LM, Huang QJ, Yao Q, Zhou H, Qu LH (2012) MicroRNA-195 plays a tumor-suppressor role in human glioblastoma cells by targeting signaling pathways involved in cellular proliferation and invasion. Neuro Oncol 14:278–287PubMedCrossRef Zhang QQ, Xu H, Huang MB, Ma LM, Huang QJ, Yao Q, Zhou H, Qu LH (2012) MicroRNA-195 plays a tumor-suppressor role in human glioblastoma cells by targeting signaling pathways involved in cellular proliferation and invasion. Neuro Oncol 14:278–287PubMedCrossRef
45.
go back to reference Hao J, Zhang C, Zhang A, Wang K, Jia Z, Wang G, Han L, Kang C, Pu P (2012) MiR-221/222 is the regulator of Cx43 expression in human glioblastoma cells. Oncol Rep 27:1504–1510PubMed Hao J, Zhang C, Zhang A, Wang K, Jia Z, Wang G, Han L, Kang C, Pu P (2012) MiR-221/222 is the regulator of Cx43 expression in human glioblastoma cells. Oncol Rep 27:1504–1510PubMed
46.
go back to reference Srinivasan S, Patric IR, Somasundaram K (2011) A ten-microRNA expression signature predicts survival in glioblastoma. PLoS One 6:e17438PubMedCrossRef Srinivasan S, Patric IR, Somasundaram K (2011) A ten-microRNA expression signature predicts survival in glioblastoma. PLoS One 6:e17438PubMedCrossRef
47.
go back to reference Galardi S, Mercatelli N, Farace MG, Ciafre SA (2011) NF-kB and c-Jun induce the expression of the oncogenic miR-221 and miR-222 in prostate carcinoma and glioblastoma cells. Nucleic Acids Res 39:3892–3902PubMedCrossRef Galardi S, Mercatelli N, Farace MG, Ciafre SA (2011) NF-kB and c-Jun induce the expression of the oncogenic miR-221 and miR-222 in prostate carcinoma and glioblastoma cells. Nucleic Acids Res 39:3892–3902PubMedCrossRef
48.
go back to reference Wang X, Han L, Zhang A, Wang G, Jia Z, Yang Y, Yue X, Pu P, Shen C, Kang C (2011) Adenovirus-mediated shRNAs for co-repression of miR-221 and miR-222 expression and function in glioblastoma cells. Oncol Rep 25:97–105PubMed Wang X, Han L, Zhang A, Wang G, Jia Z, Yang Y, Yue X, Pu P, Shen C, Kang C (2011) Adenovirus-mediated shRNAs for co-repression of miR-221 and miR-222 expression and function in glioblastoma cells. Oncol Rep 25:97–105PubMed
49.
go back to reference Zhang CZ, Zhang JX, Zhang AL, Shi ZD, Han L, Jia ZF, Yang WD, Wang GX, Jiang T, You YP, Pu PY, Cheng JQ, Kang CS (2010) Mir-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Mol Cancer 9:229PubMedCrossRef Zhang CZ, Zhang JX, Zhang AL, Shi ZD, Han L, Jia ZF, Yang WD, Wang GX, Jiang T, You YP, Pu PY, Cheng JQ, Kang CS (2010) Mir-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Mol Cancer 9:229PubMedCrossRef
50.
go back to reference Zhang C, Kang C, You Y, Pu P, Yang W, Zhao P, Wang G, Zhang A, Jia Z, Han L, Jiang H (2009) Co-suppression of miR-221/222 cluster suppresses human glioma cell growth by targeting p27kip1 in vitro and in vivo. Int J Oncol 34:1653–1660PubMedCrossRef Zhang C, Kang C, You Y, Pu P, Yang W, Zhao P, Wang G, Zhang A, Jia Z, Han L, Jiang H (2009) Co-suppression of miR-221/222 cluster suppresses human glioma cell growth by targeting p27kip1 in vitro and in vivo. Int J Oncol 34:1653–1660PubMedCrossRef
51.
go back to reference Gillies JK, Lorimer IA (2007) Regulation of p27Kip1 by miRNA 221/222 in glioblastoma. Cell Cycle 6:2005–2009PubMedCrossRef Gillies JK, Lorimer IA (2007) Regulation of p27Kip1 by miRNA 221/222 in glioblastoma. Cell Cycle 6:2005–2009PubMedCrossRef
Metadata
Title
Comparison of microRNA expression levels between initial and recurrent glioblastoma specimens
Authors
Aysegül Ilhan-Mutlu
Adelheid Wöhrer
Anna Sophie Berghoff
Georg Widhalm
Christine Marosi
Ludwig Wagner
Matthias Preusser
Publication date
01-05-2013
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 3/2013
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-013-1078-6

Other articles of this Issue 3/2013

Journal of Neuro-Oncology 3/2013 Go to the issue