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01-09-2009 | ORIGINAL PAPER

microRNAs in Gliomas: Small Regulators of a Big Problem

Authors: Joachim Silber, C. David James, J. Graeme Hodgson

Published in: NeuroMolecular Medicine | Issue 3/2009

Abstract

Gliomas are the most common form of primary brain tumors and are associated with a poor clinical outcome. The molecular mechanisms that contribute to gliomagenesis have become increasingly clear in recent years, yet much remains to be learned. This is particularly true for the role of microRNAs in gliomagenesis, as an appreciation for the significance of aberrant miRNA expression in human cancer has only emerged in the last 5 years. It is now evident that microRNAs regulate a wide variety of tumorigenic processes including cellular proliferation, differentiation, angiogenesis, invasion, and apoptosis. Here we review the current state of knowledge related to the role of microRNAs in glial tumor development. This is a rapidly evolving field and it is likely that we have only begun to appreciate the involvement of microRNAs in relation to glioma formation, and the therapeutic potential of microRNAs to improve outcome for glioma patients.

Alcantara Llaguno, S., Chen, J., Kwon, C. H., Jackson, E. L., Li, Y., Burns, D. K., et al. (2009). Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell, 15, 45–56.PubMedCrossRef

Aoki, H., Yokoyama, T., Fujiwara, K., Tari, A. M., Sawaya, R., Suki, D., et al. (2007). Phosphorylated Pak1 level in the cytoplasm correlates with shorter survival time in patients with glioblastoma. Clinical Cancer Research, 13, 6603–6609.PubMedCrossRef

Argyriou, A. A., Giannopoulou, E., & Kalofonos, H. P. (2009). Angiogenesis and anti-angiogenic molecularly targeted therapies in malignant gliomas. Oncology, 77, 1–11.PubMedCrossRef

Bao, S., Wu, Q., McLendon, R. E., Hao, Y., Shi, Q., Hjelmeland, A. B., et al. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature, 444, 756–760.PubMedCrossRef

Birner, P., Gatterbauer, B., Oberhuber, G., Schindl, M., Rossler, K., Prodinger, A., et al. (2001). Expression of hypoxia-inducible factor-1 alpha in oligodendrogliomas: its impact on prognosis and on neoangiogenesis. Cancer, 92, 165–171.PubMedCrossRef

Camps, C., Buffa, F. M., Colella, S., Moore, J., Sotiriou, C., Sheldon, H., et al. (2008). hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clinical Cancer Research, 14, 1340–1348.PubMedCrossRef

Carmeliet, P., Dor, Y., Herbert, J. M., Fukumura, D., Brusselmans, K., Dewerchin, M., et al. (1998). Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature, 394, 485–490.PubMedCrossRef

Cavalla, P., Piva, R., Bortolotto, S., Grosso, R., Cancelli, I., Chio, A., et al. (1999). P27/kip1 expression in oligodendrogliomas and its possible prognostic role. Acta Neuropathologica, 98, 629–634.PubMedCrossRef

Chalhoub, N., & Baker, S. J. (2009). PTEN and the PI3-kinase pathway in cancer. Annual Review of Pathology, 4, 127–150.PubMedCrossRef

Chan, J. A., Krichevsky, A. M., & Kosik, K. S. (2005). MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Research, 65, 6029–6033.PubMedCrossRef

Chen, X., Guo, X., Zhang, H., Xiang, Y., Chen, J., Yin, Y., et al. (2009). Role of miR-143 targeting KRAS in colorectal tumorigenesis. Oncogene, 28, 1385–1392.PubMedCrossRef

Chen, Y., Liu, W., Chao, T., Zhang, Y., Yan, X., Gong, Y., et al. (2008). MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Letters, 272, 197–205.PubMedCrossRef

Cheng, A. M., Byrom, M. W., Shelton, J., & Ford, L. P. (2005). Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Research, 33, 1290–1297.PubMedCrossRef

Ciafre, S. A., Galardi, S., Mangiola, A., Ferracin, M., Liu, C. G., Sabatino, G., et al. (2005). Extensive modulation of a set of microRNAs in primary glioblastoma. Biochemical and Biophysical Research Communications, 334, 1351–1358.PubMedCrossRef

Conaco, C., Otto, S., Han, J. J., & Mandel, G. (2006). Reciprocal actions of REST and a microRNA promote neuronal identity. Proceedings of the National Academy of Sciences, USA, 103, 2422–2427.CrossRef

Conti, A., Aguennouz, M., La Torre, D., Tomasello, C., Cardali, S., Angileri, F. F., et al. (2009). miR-21 and 221 upregulation and miR-181b downregulation in human grade II–IV astrocytic tumors. Journal of Neurooncology, 93, 325–332.CrossRef

Corsten, M. F., Miranda, R., Kasmieh, R., Krichevsky, A. M., 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 Research, 67, 8994–9000.PubMedCrossRef

De Pietri Tonelli, D., Pulvers, J. N., Haffner, C., Murchison, E. P., Hannon, G. J., & Huttner, W. B. (2008). miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development, 135, 3911–3921.PubMedCrossRef

DeGregori, J. (2002). The genetics of the E2F family of transcription factors: shared functions and unique roles. Biochimica et Biophysica Acta, 1602, 131–150.PubMed

Dews, M., Homayouni, A., Yu, D., Murphy, D., Sevignani, C., Wentzel, E., et al. (2006). Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nature Genetics, 38, 1060–1065.PubMedCrossRef

Du, R., Petritsch, C., Lu, K., Liu, P., Haller, A., Ganss, R., et al. (2008). Matrix metalloproteinase-2 regulates vascular patterning and growth affecting tumor cell survival and invasion in GBM. Neuro-Oncology, 10, 254–264.PubMedCrossRef

Ekholm, S. V., & Reed, S. I. (2000). Regulation of G(1) cyclin-dependent kinases in the mammalian cell cycle. Current Opinion in Cell Biology, 12, 676–684.PubMedCrossRef

Elias, M. C., Tozer, K. R., Silber, J. R., Mikheeva, S., Deng, M., Morrison, R. S., et al. (2005). TWIST is expressed in human gliomas and promotes invasion. Neoplasia, 7, 824–837.PubMedCrossRef

Ewan, L. C., Jopling, H. M., Jia, H., Mittar, S., Bagherzadeh, A., Howell, G. J., et al. (2006). Intrinsic tyrosine kinase activity is required for vascular endothelial growth factor receptor 2 ubiquitination, sorting and degradation in endothelial cells. Traffic, 7, 1270–1282.PubMedCrossRef

Fasanaro, P., D’Alessandra, Y., Di Stefano, V., Melchionna, R., Romani, S., Pompilio, G., et al. (2008). MicroRNA-210 modulates endothelial cell response to hypoxia and inhibits the receptor tyrosine kinase ligand Ephrin-A3. Journal of Biological Chemistry, 283, 15878–15883.PubMedCrossRef

Fasano, C. A., Dimos, J. T., Ivanova, N. B., Lowry, N., Lemischka, I. R., & Temple, S. (2007). shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell, 1, 87–99.PubMedCrossRef

Fischer, I., Gagner, J. P., Law, M., Newcomb, E. W., & Zagzag, D. (2005). Angiogenesis in gliomas: biology and molecular pathophysiology. Brain Pathology, 15, 297–310.PubMedCrossRef

Foshay, K. M., & Gallicano, G. I. (2007). Small RNAs, big potential: The role of MicroRNAs in stem cell function. Current Stem Cell Research & Therapy, 2, 264–271.CrossRef

Furnari, F. B., Fenton, T., Bachoo, R. M., Mukasa, A., Stommel, J. M., Stegh, A., et al. (2007). Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes and Development, 21, 2683–2710.PubMedCrossRef

Gabriely, G., Wurdinger, T., Kesari, S., Esau, C. C., Burchard, J., Linsley, P. S., et al. (2008). MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Molecular and Cellular Biology, 28, 5369–5380.PubMedCrossRef

Galardi, S., Mercatelli, N., Giorda, E., Massalini, S., Frajese, G. V., Ciafre, S. A., et al. (2007). miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. Journal of Biological Chemistry, 282, 23716–23724.PubMedCrossRef

Gaur, A., Jewell, D. A., Liang, Y., Ridzon, D., Moore, J. H., Chen, C., et al. (2007). Characterization of microRNA expression levels and their biological correlates in human cancer cell lines. Cancer Research, 67, 2456–2468.PubMedCrossRef

Giaccia, A., Siim, B. G., & Johnson, R. S. (2003). HIF-1 as a target for drug development. Nature Reviews Drug Discovery, 2, 803–811.PubMedCrossRef

Gillies, J. K., & Lorimer, I. A. (2007). Regulation of p27Kip1 by miRNA 221/222 in glioblastoma. Cell Cycle, 6, 2005–2009.PubMed

Godlewski, J., Nowicki, M. O., Bronisz, A., Williams, S., Otsuki, A., Nuovo, G., et al. (2008). Targeting of the Bmi-1 oncogene/stem cell renewal factor by microRNA-128 inhibits glioma proliferation and self-renewal. Cancer Research, 68, 9125–9130.PubMedCrossRef

Guo, C., Sah, J. F., Beard, L., Willson, J. K., Markowitz, S. D., & Guda, K. (2008). The noncoding RNA, miR-126, suppresses the growth of neoplastic cells by targeting phosphatidylinositol 3-kinase signaling and is frequently lost in colon cancers. Genes Chromosomes Cancer, 47, 939–946.PubMedCrossRef

Guo, W. J., Zeng, M. S., Yadav, A., Song, L. B., Guo, B. H., Band, V., et al. (2007). Mel-18 acts as a tumor suppressor by repressing Bmi-1 expression and down-regulating Akt activity in breast cancer cells. Cancer Research, 67, 5083–5089.PubMedCrossRef

Hashizume, R., Ozawa, T., Gryaznov, S. M., Bollen, A. W., Lamborn, K. R., Frey II, W. H., et al. (2008). New therapeutic approach for brain tumors: Intranasal delivery of telomerase inhibitor GRN163. Neuro-Oncology, 10, 112–120.PubMedCrossRef

Hayes, M. E., Drummond, D. C., Hong, K., Zheng, W. W., Khorosheva, V. A., Khorosheva, V. A., et al. (2006a). Increased target specificity of anti-HER2 genospheres by modification of surface charge and degree of PEGylation. Molecular Pharmacology, 3, 726–736.CrossRef

Hayes, M. E., Drummond, D. C., Kirpotin, D. B., Zheng, W. W., Noble, C. O., Park, J. W., et al. (2006b). Genospheres: Self-assembling nucleic acid-lipid nanoparticles suitable for targeted gene delivery. Gene Therapy, 13, 646–651.PubMedCrossRef

Hebert, C., Norris, K., Scheper, M. A., Nikitakis, N., & Sauk, J. J. (2007). High mobility group A2 is a target for miRNA-98 in head and neck squamous cell carcinoma. Molecular Cancer, 6, 5.PubMedCrossRef

Holland, E. C., Celestino, J., Dai, C., Schaefer, L., Sawaya, R. E., & Fuller, G. N. (2000). Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nature Genetics, 25, 55–57.PubMedCrossRef

Huang, Q., Gumireddy, K., Schrier, M., le Sage, C., Nagel, R., Nair, S., et al. (2008). The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nature Cell Biology, 10, 202–210.PubMedCrossRef

Huang, T. H., Wu, F., Loeb, G. B., Hsu, R., Heidersbach, A., Brincat, A., et al. (2009). Upregulation of miR-21 by HER2/neu signaling promotes cell invasion. Journal of Biological Chemistry, 284, 18515–18524.PubMedCrossRef

Huse, J. T., Brennan, C., Hambardzumyan, D., Wee, B., Pena, J., Rouhanifard, S. H., et al. (2009). The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes and Development, 23, 1327–1337.PubMedCrossRef

Jackson, E. L., & Alvarez-Buylla, A. (2008). Characterization of adult neural stem cells and their relation to brain tumors. Cells Tissues Organs, 188, 212–224.PubMedCrossRef

Jackson, E. L., Garcia-Verdugo, J. M., Gil-Perotin, S., Roy, M., Quinones-Hinojosa, A., VandenBerg, S., et al. (2006). PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron, 51, 187–199.PubMedCrossRef

James, C. D., & Cavenee, W. K. (2009). Stem cells for treating glioblastoma: how close to reality? Neuro-Oncology, 11, 101.PubMedCrossRef

Johnson, S. M., Grosshans, H., Shingara, J., Byrom, M., Jarvis, R., Cheng, A., et al. (2005). RAS is regulated by the let-7 microRNA family. Cell, 120, 635–647.PubMedCrossRef

Kanellopoulou, C., Muljo, S. A., Kung, A. L., Ganesan, S., Drapkin, R., Jenuwein, T., et al. (2005). Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes and Development, 19, 489–501.PubMedCrossRef

Kanu, O. O., Mehta, A., Di, C., Lin, N., Bortoff, K., Bigner, D. D., et al. (2009). Glioblastoma multiforme: A review of therapeutic targets. Expert Opinion on Therapeutic Targets, 13, 701–718.PubMedCrossRef

Kefas, B., Godlewski, J., Comeau, L., Li, Y., Abounader, R., Hawkinson, M., et al. (2008). microRNA-7 inhibits the epidermal growth factor receptor and the Akt pathway and is down-regulated in glioblastoma. Cancer Research, 68, 3566–3572.PubMedCrossRef

Kuehbacher, A., Urbich, C., Zeiher, A. M., & Dimmeler, S. (2007). Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circulation Research, 101, 59–68.PubMedCrossRef

Kuhnert, F., Mancuso, M. R., Hampton, J., Stankunas, K., Asano, T., Chen, C. Z., et al. (2008). Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development, 135, 3989–3993.PubMedCrossRef

Kulshreshtha, R., Ferracin, M., Wojcik, S. E., Garzon, R., Alder, H., Agosto-Perez, F. J., et al. (2007). A microRNA signature of hypoxia. Molecular and Cellular Biology, 27, 1859–1867.PubMedCrossRef

Kumar, M. S., Erkeland, S. J., Pester, R. E., Chen, C. Y., Ebert, M. S., Sharp, P. A., et al. (2008). Suppression of non-small cell lung tumor development by the let-7 microRNA family. Proceedings of the National Academy of Sciences, USA, 105, 3903–3908.CrossRef

Kumar, R., Gururaj, A. E., & Barnes, C. J. (2006). P21-activated kinases in cancer. Nature Reviews Cancer, 6, 459–471.PubMedCrossRef

Kumar, M. S., Lu, J., Mercer, K. L., Golub, T. R., & Jacks, T. (2007). Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nature Genetics, 39, 673–677.PubMedCrossRef

Laws, E. R., Parney, I. F., Huang, W., Anderson, F., Morris, A. M., Asher, A., et al. (2003). Survival following surgery and prognostic factors for recently diagnosed malignant glioma: Data from the Glioma Outcomes Project. Journal of Neurosurgery, 99, 467–473.PubMedCrossRef

le Sage, C., Nagel, R., Egan, D. A., Schrier, M., Mesman, E., Mangiola, A., et al. (2007). Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO Journal, 26, 3699–3708.PubMedCrossRef

Lee, E. J., Gusev, Y., Jiang, J., Nuovo, G. J., Lerner, M. R., Frankel, W. L., et al. (2007). Expression profiling identifies microRNA signature in pancreatic cancer. International Journal of Cancer, 120, 1046–1054.CrossRef

Li, N., Fu, H., Tie, Y., Hu, Z., Kong, W., Wu, Y., et al. (2009a). miR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Letters, 275, 44–53.PubMedCrossRef

Li, T., Li, D., Sha, J., Sun, P., & Huang, Y. (2009b). MicroRNA-21 directly targets MARCKS and promotes apoptosis resistance and invasion in prostate cancer cells. Biochemical and Biophysical Research Communications, 383, 280–285.PubMedCrossRef

Li, W., & Szoka, F. C., Jr. (2007). Lipid-based nanoparticles for nucleic acid delivery. Pharmaceutical Research, 24, 438–449.PubMedCrossRef

Louis, D. N., Ohgaki, H., Wiestler, O. D., Cavenee, W. K., Burger, P. C., Jouvet, A., et al. (2007). The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathologica, 114, 97–109.PubMedCrossRef

Lu, J., Getz, G., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., et al. (2005). MicroRNA expression profiles classify human cancers. Nature, 435, 834–838.PubMedCrossRef

Lujambio, A., Ropero, S., Ballestar, E., Fraga, M. F., Cerrato, C., Setien, F., et al. (2007). Genetic unmasking of an epigenetically silenced microRNA in human cancer cells. Cancer Research, 67, 1424–1429.PubMedCrossRef

Ma, L., Teruya-Feldstein, J., & Weinberg, R. A. (2007). Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature, 449, 682–688.PubMedCrossRef

Makeyev, E. V., Zhang, J., Carrasco, M. A., & Maniatis, T. (2007). The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Molecular Cell, 27, 435–448.PubMedCrossRef

Medina, R., Zaidi, S. K., Liu, C. G., Stein, J. L., van Wijnen, A. J., Croce, C. M., et al. (2008). MicroRNAs 221 and 222 bypass quiescence and compromise cell survival. Cancer Research, 68, 2773–2780.PubMedCrossRef

Melo, S. A., Ropero, S., Moutinho, C., Aaltonen, L. A., Yamamoto, H., Calin, G. A., et al. (2009). A TARBP2 mutation in human cancer impairs microRNA processing and DICER1 function. Nature Genetics, 41, 365–370.PubMedCrossRef

Meng, F., Henson, R., Lang, M., Wehbe, H., Maheshwari, S., Mendell, J. T., et al. (2006). Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology, 130, 2113–2129.PubMedCrossRef

Merritt, W. M., Lin, Y. G., Han, L. Y., Kamat, A. A., Spannuth, W. A., Schmandt, R., et al. (2008). Dicer, Drosha, and outcomes in patients with ovarian cancer. New England Journal of Medicine, 359, 2641–2650.PubMedCrossRef

Miletic, H., Niclou, S. P., Johansson, M., & Bjerkvig, R. (2009). Anti-VEGF therapies for malignant glioma: treatment effects and escape mechanisms. Expert Opinion on Therapeutic Targets, 13, 455–468.PubMedCrossRef

Mischel, P. S., Cloughesy, T. F., & Nelson, S. F. (2004). DNA-microarray analysis of brain cancer: molecular classification for therapy. Nature Reviews Neuroscience, 5, 782–792.PubMedCrossRef

Mizumatsu, S., Tamiya, T., Ono, Y., Abe, T., Matsumoto, K., Furuta, T., et al. (1999). Expression of cell cycle regulator p27Kip1 is correlated with survival of patients with astrocytoma. Clinical Cancer Research, 5, 551–557.PubMed

Nelson, P. T., Baldwin, D. A., Kloosterman, W. P., Kauppinen, S., Plasterk, R. H., & Mourelatos, Z. (2006). RAKE and LNA-ISH reveal microRNA expression and localization in archival human brain. RNA, 12, 187–191.PubMedCrossRef

Nieder, C., Adam, M., Molls, M., & Grosu, A. L. (2006). Therapeutic options for recurrent high-grade glioma in adult patients: recent advances. Critical Reviews in Oncology/Hematology, 60, 181–193.PubMedCrossRef

Okamoto, T., Sanda, T., & Asamitsu, K. (2007). NF-kappa B signaling and carcinogenesis. Current Pharmaceutical Design, 13, 447–462.PubMedCrossRef

Otsuka, M., Zheng, M., Hayashi, M., Lee, J. D., Yoshino, O., Lin, S., et al. (2008). Impaired microRNA processing causes corpus luteum insufficiency and infertility in mice. Journal of Clinical Investigation, 118, 1944–1954.PubMedCrossRef

Pallante, P., Visone, R., Ferracin, M., Ferraro, A., Berlingieri, M. T., Troncone, G., et al. (2006). MicroRNA deregulation in human thyroid papillary carcinomas. Endocrine-Related Cancer, 13, 497–508.PubMedCrossRef

Panner, A., James, C. D., Berger, M. S., & Pieper, R. O. (2005). mTOR controls FLIPS translation and TRAIL sensitivity in glioblastoma multiforme cells. Molecular and Cellular Biology, 25, 8809–8823.PubMedCrossRef

Papagiannakopoulos, T., Shapiro, A., & Kosik, K. S. (2008). MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Research, 68, 8164–8172.PubMedCrossRef

Piccirillo, S. G., Reynolds, B. A., Zanetti, N., Lamorte, G., Binda, E., Broggi, G., et al. (2006). Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature, 444, 761–765.PubMedCrossRef

Piva, R., Cavalla, P., Bortolotto, S., Cordera, S., Richiardi, P., & Schiffer, D. (1997). P27/kip1 expression in human astrocytic gliomas. Neuroscience Letters, 234, 127–130.PubMedCrossRef

Powis, G., & Kirkpatrick, L. (2004). Hypoxia inducible factor-1alpha as a cancer drug target. Molecular Cancer Therapeutics, 3, 647–654.PubMed

Pulkkinen, K., Malm, T., Turunen, M., Koistinaho, J., & Yla-Herttuala, S. (2008). Hypoxia induces microRNA miR-210 in vitro and in vivo ephrin-A3 and neuronal pentraxin 1 are potentially regulated by miR-210. FEBS Letters, 582, 2397–2401.PubMedCrossRef

Rane, S., He, M., Sayed, D., Vashistha, H., Malhotra, A., Sadoshima, J., et al. (2009). Downregulation of miR-199a derepresses hypoxia-inducible factor-1alpha and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circulation Research, 104, 879–886.PubMedCrossRef

Reddy, S. D., Ohshiro, K., Rayala, S. K., & Kumar, R. (2008). MicroRNA-7, a homeobox D10 target, inhibits p21-activated kinase 1 and regulates its functions. Cancer Research, 68, 8195–8200.PubMedCrossRef

Rich, J. N., & Bao, S. (2007). Chemotherapy and cancer stem cells. Cell Stem Cell, 1, 353–355.PubMedCrossRef

Rieger, J., Naumann, U., Glaser, T., Ashkenazi, A., & Weller, M. (1998). APO2 ligand: A novel lethal weapon against malignant glioma? FEBS Letters, 427, 124–128.PubMedCrossRef

Saito, R., Krauze, M. T., Noble, C. O., Drummond, D. C., Kirpotin, D. B., Berger, M. S., et al. (2006). Convection-enhanced delivery of Ls-TPT enables an effective, continuous, low-dose chemotherapy against malignant glioma xenograft model. Neuro-Oncology, 8, 205–214.PubMedCrossRef

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. International Journal of Cancer, 125, 1407–1413.CrossRef

Shi, L., Cheng, Z., Zhang, J., Li, R., Zhao, P., Fu, Z., et al. (2008). Hsa-Mir-181a and Hsa-Mir-181b function as tumor suppressors in human glioma cells. Brain Research, 1236, 185–193.PubMedCrossRef

Shilo, S., Roy, S., Khanna, S., & Sen, C. K. (2008). Evidence for the involvement of miRNA in redox regulated angiogenic response of human microvascular endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 28, 471–477.PubMedCrossRef

Silber, J., Lim, D. A., Petritsch, C., Persson, A. I., Maunakea, A. K., Yu, M., et al. (2008). miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med, 6, 14.PubMedCrossRef

Smirnova, L., Grafe, A., Seiler, A., Schumacher, S., Nitsch, R., & Wulczyn, F. G. (2005). Regulation of miRNA expression during neural cell specification. European Journal of Neuroscience, 21, 1469–1477.PubMedCrossRef

Sonoda, Y., Ozawa, T., Hirose, Y., Aldape, K. D., McMahon, M., Berger, M. S., et al. (2001). Formation of intracranial tumors by genetically modified human astrocytes defines four pathways critical in the development of human anaplastic astrocytoma. Cancer Research, 61, 4956–4960.PubMed

Suarez, Y., Fernandez-Hernando, C., Yu, J., Gerber, S. A., Harrison, K. D., Pober, J. S., et al. (2008). Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proceedings of the National Academy of Sciences, USA, 105, 14082–14087.CrossRef

Sulman, E. P., Guerrero, M., & Aldape, K. (2009). Beyond grade: molecular pathology of malignant gliomas. Seminars in Radiation Oncology, 19, 142–149.PubMedCrossRef

Taguchi, A., Yanagisawa, K., Tanaka, M., Cao, K., Matsuyama, Y., Goto, H., et al. (2008). Identification of hypoxia-inducible factor-1 alpha as a novel target for miR-17-92 microRNA cluster. Cancer Research, 68, 5540–5545.PubMedCrossRef

Takata, H., Kato, M., Denda, K., & Kitamura, N. (2000). A hrs binding protein having a Src homology 3 domain is involved in intracellular degradation of growth factors and their receptors. Genes Cells, 5, 57–69.PubMedCrossRef

van’t Veer, L. J., & Bernards, R. (2008). Enabling personalized cancer medicine through analysis of gene-expression patterns. Nature, 452, 564–570.PubMedCrossRef

Visvanathan, J., Lee, S., Lee, B., Lee, J. W., & Lee, S. K. (2007). The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes and Development, 21, 744–749.PubMedCrossRef

Wang, S., Aurora, A. B., Johnson, B. A., Qi, X., McAnally, J., Hill, J. A., et al. (2008a). The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Developmental Cell, 15, 261–271.PubMedCrossRef

Wang, Y., Baskerville, S., Shenoy, A., Babiarz, J. E., Baehner, L., & Blelloch, R. (2008b). Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nature Genetics, 40, 1478–1483.PubMedCrossRef

Wang, Y., Medvid, R., Melton, C., Jaenisch, R., & Blelloch, R. (2007). DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nature Genetics, 39, 380–385.PubMedCrossRef

Webster, R. J., Giles, K. M., Price, K. J., Zhang, P. M., Mattick, J. S., & Leedman, P. J. (2009). Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. Journal of Biological Chemistry, 284, 5731–5741.PubMedCrossRef

Weiss, W. A., Burns, M. J., Hackett, C., Aldape, K., Hill, J. R., Kuriyama, H., et al. (2003). Genetic determinants of malignancy in a mouse model for oligodendroglioma. Cancer Research, 63, 1589–1595.PubMed

Wu, L., & Belasco, J. G. (2005). Micro-RNA regulation of the mammalian lin-28 gene during neuronal differentiation of embryonal carcinoma cells. Molecular and Cellular Biology, 25, 9198–9208.PubMedCrossRef

Wu, H., Zhu, S., & Mo, Y. Y. (2009). Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Research, 19, 439–448.PubMedCrossRef

Wurdinger, T., Tannous, B. A., Saydam, O., Skog, J., Grau, S., Soutschek, J., et al. (2008). miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell, 14, 382–393.PubMedCrossRef

Xia, H. F., He, T. Z., Liu, C. M., Cui, Y., Song, P. P., Jin, X. H., et al. (2009a). MiR-125b expression affects the proliferation and apoptosis of human glioma cells by targeting Bmf. Cellular Physiology and Biochemistry, 23, 347–358.PubMedCrossRef

Xia, H., Qi, Y., Ng, S. S., Chen, X., Chen, S., Fang, M., et al. (2009b). MicroRNA-15b regulates cell cycle progression by targeting cyclins in glioma cells. Biochemical and Biophysical Research Communications, 380, 205–210.PubMedCrossRef

Xia, H., Qi, Y., Ng, S. S., Chen, X., Li, D., Chen, S., et al. (2009c). microRNA-146b inhibits glioma cell migration and invasion by targeting MMPs. Brain Research.

Yamashita, Y., Krauze, M. T., Kawaguchi, T., Noble, C. O., Drummond, D. C., Park, J. W., et al. (2007). Convection-enhanced delivery of a topoisomerase I inhibitor (nanoliposomal topotecan) and a topoisomerase II inhibitor (pegylated liposomal doxorubicin) in intracranial brain tumor xenografts. Neuro-Oncology, 9, 20–28.PubMedCrossRef

Yang, K., Handorean, A. M., & Iczkowski, K. A. (2009). MicroRNAs 373 and 520c are downregulated in prostate cancer, suppress CD44 translation and enhance invasion of prostate cancer cells in vitro. International Journal of Clinical and Experimental Pathology, 2, 361–369.PubMed

Yang, H., Kong, W., He, L., Zhao, J. J., O’Donnell, J. D., Wang, J., et al. (2008). MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Research, 68, 425–433.PubMedCrossRef

Yu, S. L., Chen, H. Y., Chang, G. C., Chen, C. Y., Chen, H. W., Singh, S., et al. (2008). MicroRNA signature predicts survival and relapse in lung cancer. Cancer Cell, 13, 48–57.PubMedCrossRef

Zagzag, D., Lukyanov, Y., Lan, L., Ali, M. A., Esencay, M., Mendez, O., et al. (2006). Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Laboratory Investigation, 86, 1221–1232.PubMedCrossRef

Zagzag, D., Zhong, H., Scalzitti, J. M., Laughner, E., Simons, J. W., & Semenza, G. L. (2000). Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer, 88, 2606–2618.PubMedCrossRef

Zhang, Y., Chao, T., Li, R., Liu, W., Chen, Y., Yan, X., et al. (2009). MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. Journal of Molecular Medicine, 87, 43–51.PubMedCrossRef

Zhong, H., De Marzo, A. M., Laughner, E., Lim, M., Hilton, D. A., Zagzag, D., et al. (1999). Overexpression of hypoxia-inducible factor 1alpha in common human cancers and their metastases. Cancer Research, 59, 5830–5835.PubMed

Title: microRNAs in Gliomas: Small Regulators of a Big Problem
Authors: Joachim Silber
C. David James
J. Graeme Hodgson
Publication date: 01-09-2009
Publisher: Humana Press Inc
Published in: NeuroMolecular Medicine / Issue 3/2009
Print ISSN: 1535-1084
Electronic ISSN: 1559-1174
DOI: https://doi.org/10.1007/s12017-009-8087-9

Keynote webinar | Spotlight on medication adherence

Springer Medicine

microRNAs in Gliomas: Small Regulators of a Big Problem

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

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