Open Access Open Access  Restricted Access Subscription Access

Alternative RNA Splicing in the Pathogenesis of GBM

Amy Haseley Thorne, Webster K Cavenee, Frank B. Furnari


Alternative splicing enables the generation of different proteins from a single gene, greatly increasing the use of genetic information. The resultant protein isoforms often have different biological properties effecting the phenotype of the cell in which it is expressed. Dysregulation of alternative splicing is a common occurrence in cancer and may lead to the formation of truncated or degraded proteins through the introduction of immature stop codons or nonsense mediated decay.  Increasing evidence indicates that cancer-associated splicing variants play an important role in tumor initiation and progression. In this review, we summarize the evidence supporting the relevance of alternative splicing in glioblastoma multiforme (GBM). Specifically, we focus on the role of alternative splicing in GBM pathogenesis with an emphasis on the effect of aberrant alternative splicing of FGFR, GLI-1, and EGFR. The significance of exploiting alternatively spliced isoforms as potential biomarkers which may contribute to the development of diagnostic and prognostic methods, in addition to serving as molecular targets in GBM, will be discussed.


Glioblastoma, Alternative Splicing

Full Text:


Arteaga, M. F., T. Coric, C. Straub, and C. M. Canessa. 2008. "A brain-specific SGK1 splice isoform regulates expression of ASIC1 in neurons." Proc Natl Acad Sci U S A 105 (11):4459-64. doi: 10.1073/pnas.0800958105.

Babic, I., E. S. Anderson, K. Tanaka, D. Guo, K. Masui, B. Li, S. Zhu, Y. Gu, G. R. Villa, D. Akhavan, D. Nathanson, B. Gini, S. Mareninov, R. Li, C. E. Camacho, S. K. Kurdistani, A. Eskin, S. F. Nelson, W. H. Yong, W. K. Cavenee, T. F. Cloughesy, H. R. Christofk, D. L. Black, and P. S. Mischel. 2013. "EGFR mutation-induced alternative splicing of Max contributes to growth of glycolytic tumors in brain cancer." Cell Metab 17 (6):1000-8. doi: 10.1016/j.cmet.2013.04.013.

Badie, B., J. Schartner, J. Klaver, and J. Vorpahl. 1999. "In vitro modulation of microglia motility by glioma cells is mediated by hepatocyte growth factor/scatter factor." Neurosurgery 44 (5):1077-82; discussion 1082-3.

Baron, A. T., J. A. Wilken, D. E. Haggstrom, S. T. Goodrich, and N. J. Maihle. 2009. "Clinical implementation of soluble EGFR (sEGFR) as a theragnostic serum biomarker of breast, lung and ovarian cancer." IDrugs 12 (5):302-8.

Bertolesi, G. E., R. Walia Da Silva, C. A. Jollimore, C. Shi, S. Barnes, and M. E. Kelly. 2006. "Ca(v)3.1 splice variant expression during neuronal differentiation of Y-79 retinoblastoma cells." Neuroscience 141 (1):259-68. doi: 10.1016/j.neuroscience.2006.03.067.

Borsi, L., E. Balza, P. Castellani, B. Carnemolla, M. Ponassi, G. Querze, and L. Zardi. 1994. "Cell-cycle dependent alternative splicing of the tenascin primary transcript." Cell Adhes Commun 1 (4):307-17.

Boutz, P. L., P. Stoilov, Q. Li, C. H. Lin, G. Chawla, K. Ostrow, L. Shiue, M. Ares, Jr., and D. L. Black. 2007. "A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons." Genes Dev 21 (13):1636-52. doi: 10.1101/gad.1558107.

Brack, S. S., M. Silacci, M. Birchler, and D. Neri. 2006. "Tumor-targeting properties of novel antibodies specific to the large isoform of tenascin-C." Clin Cancer Res 12 (10):3200-8. doi: 10.1158/1078-0432.CCR-05-2804.

Brennan, C. W., R. G. Verhaak, A. McKenna, B. Campos, H. Noushmehr, S. R. Salama, S. Zheng, D. Chakravarty, J. Z. Sanborn, S. H. Berman, R. Beroukhim, B. Bernard, C. J. Wu, G. Genovese, I. Shmulevich, J.

Barnholtz-Sloan, L. Zou, R. Vegesna, S. A. Shukla, G. Ciriello, W. K. Yung, W. Zhang, C. Sougnez, T. Mikkelsen, K. Aldape, D. D. Bigner, E. G. Van Meir, M. Prados, A. Sloan, K. L. Black, J. Eschbacher, G. Finocchiaro, W. Friedman, D. W. Andrews, A. Guha, M. Iacocca, B. P. O'Neill, G. Foltz, J. Myers, D. J. Weisenberger, R. Penny, R. Kucherlapati, C. M. Perou, D. N. Hayes, R. Gibbs, M. Marra, G. B. Mills, E. Lander, P. Spellman, R. Wilson, C. Sander, J. Weinstein, M. Meyerson, S. Gabriel, P. W. Laird, D. Haussler, G. Getz, L. Chin, and Tcga Research Network. 2013. "The somatic genomic landscape of glioblastoma." Cell 155 (2):462-77. doi: 10.1016/j.cell.2013.09.034.

Bruno, I. G., W. Jin, and G. J. Cote. 2004. "Correction of aberrant FGFR1 alternative RNA splicing through targeting of intronic regulatory elements." Hum Mol Genet 13 (20):2409-20. doi: 10.1093/hmg/ddh272.

Caldas, H., Y. Jiang, M. P. Holloway, J. Fangusaro, C. Mahotka, E. M. Conway, and R. A. Altura. 2005. "Survivin splice variants regulate the balance between proliferation and cell death." Oncogene 24 (12):1994-2007. doi: 10.1038/sj.onc.1208350.

Camacho-Vanegas, O., G. Narla, M. S. Teixeira, A. DiFeo, A. Misra, G. Singh, A. M. Chan, S. L. Friedman, B. G. Feuerstein, and J. A. Martignetti. 2007. "Functional inactivation of the KLF6 tumor suppressor gene by loss of heterozygosity and increased alternative splicing in glioblastoma." Int J Cancer 121 (6):1390-5. doi: 10.1002/ijc.22809.

Campos, B., F. Wan, M. Farhadi, A. Ernst, F. Zeppernick, K. E. Tagscherer, R. Ahmadi, J. Lohr, C. Dictus, G. Gdynia, S. E. Combs, V. Goidts, B. M. Helmke, V. Eckstein, W. Roth, P. Beckhove, P. Lichter, A. Unterberg, B. Radlwimmer, and C. Herold-Mende. 2010. "Differentiation therapy exerts antitumor effects on stem-like glioma cells." Clin Cancer Res 16 (10):2715-28. doi: 10.1158/1078-0432.CCR-09-1800.

Carnemolla, B., P. Castellani, M. Ponassi, L. Borsi, S. Urbini, G. Nicolo, A. Dorcaratto, G. Viale, G. Winter, D. Neri, and L. Zardi. 1999. "Identification of a glioblastoma-associated tenascin-C isoform by a high affinity recombinant antibody." Am J Pathol 154 (5):1345-52. doi: 10.1016/S0002-9440(10)65388-6.

Carpenter, R. L., and H. W. Lo. 2012. "Hedgehog pathway and GLI1 isoforms in human cancer." Discov Med 13 (69):105-13.

Chan, A. M., J. S. Rubin, D. P. Bottaro, D. W. Hirschfield, M. Chedid, and S. A. Aaronson. 1991. "Identification of a competitive HGF antagonist encoded by an alternative transcript." Science 254 (5036):1382-5.

Chaneton, B., and E. Gottlieb. 2012. "Rocking cell metabolism: revised functions of the key glycolytic regulator PKM2 in cancer." Trends Biochem Sci 37 (8):309-16. doi: 10.1016/j.tibs.2012.04.003.

Chen, C. H., S. L. Howng, T. S. Cheng, M. H. Chou, C. Y. Huang, and Y. R. Hong. 2003. "Molecular characterization of human ninein protein: two distinct subdomains required for centrosomal targeting and regulating signals in cell cycle." Biochem Biophys Res Commun 308 (4):975-83.

Chen, C. H., S. L. Howng, S. L. Hwang, C. K. Chou, C. H. Liao, and Y. R. Hong. 2000. "Differential expression of four human dynamin-like protein variants in brain tumors." DNA Cell Biol 19 (3):189-94. doi: 10.1089/104454900314573.

Chen, W. S., C. S. Lazar, K. A. Lund, J. B. Welsh, C. P. Chang, G. M. Walton, C. J. Der, H. S. Wiley, G. N. Gill, and M. G. Rosenfeld. 1989. "Functional independence of the epidermal growth factor receptor from a domain required for ligand-induced internalization and calcium regulation." Cell 59 (1):33-43.

Chen, X., L. Zhang, I. Y. Zhang, J. Liang, H. Wang, M. Ouyang, S. Wu, A. Carvalho da Fonseca, L. Weng, Y. Yamamoto, H. Yamamoto, R. Natarajan, and B. Badie. 2014. "RAGE Expression in Tumor-associated Macrophages Promotes Angiogenesis in Glioma." Cancer Res. doi: 10.1158/0008-5472.CAN-14-1240.

Cheng, S. Y., M. Nagane, H. S. Huang, and W. K. Cavenee. 1997. "Intracerebral tumor-associated hemorrhage caused by overexpression of the vascular endothelial growth factor isoforms VEGF121 and VEGF165 but not VEGF189." Proc Natl Acad Sci U S A 94 (22):12081-7.

Cheung, H. C., L. J. Corley, G. N. Fuller, I. E. McCutcheon, and G. J. Cote. 2006. "Polypyrimidine tract binding protein and Notch1 are independently re-expressed in glioma." Mod Pathol 19 (8):1034-41. doi: 10.1038/modpathol.3800635.

Cheung, H. C., T. Hai, W. Zhu, K. A. Baggerly, S. Tsavachidis, R. Krahe, and G. J. Cote. 2009. "Splicing factors PTBP1 and PTBP2 promote proliferation and migration of glioma cell lines." Brain 132 (Pt 8):2277-88. doi: 10.1093/brain/awp153.

Cho, J., S. Pastorino, Q. Zeng, X. Xu, W. Johnson, S. Vandenberg, R. Verhaak, A. D. Cherniack, H. Watanabe, A. Dutt, J. Kwon, Y. S. Chao, R. C. Onofrio, D. Chiang, Y. Yuza, S. Kesari, and M. Meyerson. 2011.

"Glioblastoma-derived epidermal growth factor receptor carboxyl-terminal deletion mutants are transforming and are sensitive to EGFR-directed therapies." Cancer Res 71 (24):7587-96. doi: 10.1158/0008-5472.CAN-11-0821.

Christofk, H. R., M. G. Vander Heiden, M. H. Harris, A. Ramanathan, R. E. Gerszten, R. Wei, M. D. Fleming, S. L. Schreiber, and L. C. Cantley. 2008. "The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth." Nature 452 (7184):230-3. doi: 10.1038/nature06734.

Chunduru, S., H. Kawami, R. Gullick, W. J. Monacci, G. Dougherty, and M. L. Cutler. 2002. "Identification of an alternatively spliced RNA for the Ras suppressor RSU-1 in human gliomas." J Neurooncol 60 (3):201-11.

Clower, C. V., D. Chatterjee, Z. Wang, L. C. Cantley, M. G. Vander Heiden, and A. R. Krainer. 2010. "The alternative splicing repressors hnRNP A1/A2 and PTB influence pyruvate kinase isoform expression and cell metabolism." Proc Natl Acad Sci U S A 107 (5):1894-9. doi: 10.1073/pnas.0914845107.

Cui, D., Q. Xu, K. Wang, and X. Che. 2010. "Gli1 is a potential target for alleviating multidrug resistance of gliomas." J Neurol Sci 288 (1-2):156-66. doi: 10.1016/j.jns.2009.09.006.

David, C. J., and J. L. Manley. 2010. "Alternative pre-mRNA splicing regulation in cancer: pathways and programs unhinged." Genes Dev 24 (21):2343-64. doi: 10.1101/gad.1973010.

Decker, S. J., C. Alexander, and T. Habib. 1992. "Epidermal growth factor (EGF)-stimulated tyrosine phosphorylation and EGF receptor degradation in cells expressing EGF receptors truncated at residue 973." J Biol Chem 267 (2):1104-8.

Dours-Zimmermann, M. T., and D. R. Zimmermann. 1994. "A novel glycosaminoglycan attachment domain identified in two alternative splice variants of human versican." J Biol Chem 269 (52):32992-8.

Faustino, N. A., and T. A. Cooper. 2003. "Pre-mRNA splicing and human disease." Genes Dev 17 (4):419-37. doi: 10.1101/gad.1048803.

Feller, S. M., G. Posern, J. Voss, C. Kardinal, D. Sakkab, J. Zheng, and B. S. Knudsen. 1998. "Physiological signals and oncogenesis mediated through Crk family adapter proteins." J Cell Physiol 177 (4):535-52. doi: 10.1002/(SICI)1097-4652(199812)177:4<535::AID-JCP5>3.0.CO;2-E.

Feng, H., B. Hu, K. Vuori, J. N. Sarkaria, F. B. Furnari, W. K. Cavenee, and S. Y. Cheng. 2014. "EGFRvIII stimulates glioma growth and invasion through PKA-dependent serine phosphorylation of Dock180." Oncogene 33 (19):2504-12. doi: 10.1038/onc.2013.198.

Ferrarese, R., G. R. th Harsh, A. K. Yadav, E. Bug, D. Maticzka, W. Reichardt, S. M. Dombrowski, T. E. Miller, A. P. Masilamani, F. Dai, H. Kim, M. Hadler, D. M. Scholtens, I. L. Yu, J. Beck, V. Srinivasasainagendra, F. Costa, N. Baxan, D. Pfeifer, D. von Elverfeldt, R. Backofen, A. Weyerbrock, C. W. Duarte, X. He, M. Prinz, J. P. Chandler, H. Vogel, A. Chakravarti, J. N. Rich, M. S. Carro, and M. Bredel. 2014. "Lineage-specific splicing of a brain-enriched alternative exon promotes glioblastoma progression." J Clin Invest 124 (7):2861-76. doi: 10.1172/JCI68836.

Floor, S. L., J. E. Dumont, C. Maenhaut, and E. Raspe. 2012. "Hallmarks of cancer: of all cancer cells, all the time?" Trends Mol Med 18 (9):509-15. doi: 10.1016/j.molmed.2012.06.005.

Francis, J. M., C. Z. Zhang, C. L. Maire, J. Jung, V. E. Manzo, V. A. Adalsteinsson, H. Homer, S. Haidar, B. Blumenstiel, C. S. Pedamallu, A. H. Ligon, J. C. Love, M. Meyerson, and K. L. Ligon. 2014. "EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing." Cancer Discov 4 (8):956-71. doi: 10.1158/2159-8290.CD-13-0879.

Frederick, L., X. Y. Wang, G. Eley, and C. D. James. 2000. "Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas." Cancer Res 60 (5):1383-7.

Fu, R. H., S. P. Liu, S. J. Huang, H. J. Chen, P. R. Chen, Y. H. Lin, Y. C. Ho, W. L. Chang, C. H. Tsai, W. C. Shyu, and S. Z. Lin. 2013. "Aberrant alternative splicing events in Parkinson's disease." Cell Transplant 22 (4):653-61. doi: 10.3727/096368912X655154.

Glatz, D. C., D. Rujescu, Y. Tang, F. J. Berendt, A. M. Hartmann, F. Faltraco, C. Rosenberg, C. Hulette, K. Jellinger, H. Hampel, P. Riederer, H. J. Moller, A. Andreadis, K. Henkel, and S. Stamm. 2006. "The alternative splicing of tau exon 10 and its regulatory proteins CLK2 and TRA2-BETA1 changes in sporadic Alzheimer's disease." J Neurochem 96 (3):635-44. doi: 10.1111/j.1471-4159.2005.03552.x.

Golan-Gerstl, R., M. Cohen, A. Shilo, S. S. Suh, A. Bakacs, L. Coppola, and R. Karni. 2011. "Splicing factor hnRNP A2/B1 regulates tumor suppressor gene splicing and is an oncogenic driver in glioblastoma." Cancer Res 71 (13):4464-72. doi: 10.1158/0008-5472.CAN-10-4410.

Guerin, C., C. Luddy, R. Abounader, B. Lal, and J. Laterra. 2000. "Glioma inhibition by HGF/NK2, an antagonist of scatter factor/hepatocyte growth factor." Biochem Biophys Res Commun 273 (1):287-93. doi: 10.1006/bbrc.2000.2935.

Guillaudeau, A., K. Durand, B. Bessette, A. Chaunavel, I. Pommepuy, F. Projetti, S. Robert, F. Caire, H. Rabinovitch-Chable, and F. Labrousse. 2012. "EGFR soluble isoforms and their transcripts are expressed in meningiomas." PLoS One 7 (5):e37204. doi: 10.1371/journal.pone.0037204.

Guillaudeau, A., K. Durand, H. Rabinovitch-Chable, I. Pommepuy, L. Mesturoux, S. Robert, A. Chaunavel, J. J. Moreau, and F. Labrousse. 2012. "Adult diffuse gliomas produce mRNA transcripts encoding EGFR isoforms lacking a tyrosine kinase domain." Int J Oncol 40 (4):1142-52. doi: 10.3892/ijo.2011.1287.

Hamasuna, R., H. Kataoka, T. Moriyama, H. Itoh, M. Seiki, and M. Koono. 1999. "Regulation of matrix metalloproteinase-2 (MMP-2) by hepatocyte growth factor/scatter factor (HGF/SF) in human glioma cells: HGF/SF enhances MMP-2 expression and activation accompanying up-regulation of membrane type-1 MMP." Int J Cancer 82 (2):274-81.

Hamid, F. M., and E. V. Makeyev. 2014. "Regulation of mRNA abundance by polypyrimidine tract-binding protein-controlled alternate 5' splice site choice." PLoS Genet 10 (11):e1004771. doi: 10.1371/journal.pgen.1004771.

Han, A., P. Stoilov, A. J. Linares, Y. Zhou, X. D. Fu, and D. L. Black. 2014. "De novo prediction of PTBP1 binding and splicing targets reveals unexpected features of its RNA recognition and function." PLoS Comput Biol 10 (1):e1003442. doi: 10.1371/journal.pcbi.1003442.

Hanahan, D., and R. A. Weinberg. 2000. "The hallmarks of cancer." Cell 100 (1):57-70.

Hanahan, D., and R. A. Weinberg. 2011. "Hallmarks of cancer: the next generation." Cell 144 (5):646-74. doi: 10.1016/j.cell.2011.02.013.

Hannon, G. J., D. Casso, and D. Beach. 1994. "KAP: a dual specificity phosphatase that interacts with cyclin-dependent kinases." Proc Natl Acad Sci U S A 91 (5):1731-5.

Hong, X., F. Jiang, S. N. Kalkanis, Z. G. Zhang, X. Zhang, X. Zheng, H. Jiang, T. Mikkelsen, and M. Chopp. 2008. "Increased chemotactic migration and growth in heparanase-overexpressing human U251n glioma cells." J Exp Clin Cancer Res 27:23. doi: 10.1186/1756-9966-27-23.

Hong, X., K. K. Nelson, A. C. deCarvalho, and S. N. Kalkanis. 2010. "Heparanase expression of glioma in human and animal models." J Neurosurg 113 (2):261-9. doi: 10.3171/2009.9.JNS09682.

Hu, J., A. L. Ho, L. Yuan, B. Hu, S. Hua, S. S. Hwang, J. Zhang, T. Hu, H. Zheng, B. Gan, G. Wu, Y. A. Wang, L. Chin, and R. A. DePinho. 2013. "From the Cover: Neutralization of terminal differentiation in gliomagenesis." Proc Natl Acad Sci U S A 110 (36):14520-7. doi: 10.1073/pnas.1308610110.

Huang, H., J. Held-Feindt, R. Buhl, H. M. Mehdorn, and R. Mentlein. 2005. "Expression of VEGF and its receptors in different brain tumors." Neurol Res 27 (4):371-7. doi: 10.1179/016164105X39833.

Huang, H. S., M. Nagane, C. K. Klingbeil, H. Lin, R. Nishikawa, X. D. Ji, C. M. Huang, G. N. Gill, H. S. Wiley, and W. K. Cavenee. 1997. "The enhanced tumorigenic activity of a mutant epidermal growth factor receptor common in human cancers is mediated by threshold levels of constitutive tyrosine phosphorylation and unattenuated signaling." J Biol Chem 272 (5):2927-35.

Huang, Y., X. Chen, N. Chen, L. Nie, M. Xu, and Q. Zhou. 2011. "Expression and prognostic significance of survivin splice variants in diffusely infiltrating astrocytoma." J Clin Pathol 64 (11):953-9. doi: 10.1136/jclinpath-2011-200066.

Hudson, B. I., A. M. Carter, E. Harja, A. Z. Kalea, M. Arriero, H. Yang, P. J. Grant, and A. M. Schmidt. 2008. "Identification, classification, and expression of RAGE gene splice variants." FASEB J 22 (5):1572-80. doi: 10.1096/fj.07-9909com.

Humphrey, P. A., L. M. Gangarosa, A. J. Wong, G. E. Archer, M. Lund-Johansen, R. Bjerkvig, O. D. Laerum, H. S. Friedman, and D. D. Bigner. 1991. "Deletion-mutant epidermal growth factor receptor in human gliomas: effects of type II mutation on receptor function." Biochem Biophys Res Commun 178 (3):1413-20.

Humphrey, P. A., A. J. Wong, B. Vogelstein, H. S. Friedman, M. H. Werner, D. D. Bigner, and S. H. Bigner. 1988. "Amplification and expression of the epidermal growth factor receptor gene in human glioma xenografts." Cancer Res 48 (8):2231-8.

Inda, M. M., R. Bonavia, A. Mukasa, Y. Narita, D. W. Sah, S. Vandenberg, C. Brennan, T. G. Johns, R. Bachoo, P. Hadwiger, P. Tan, R. A. Depinho, W. Cavenee, and F. Furnari. 2010. "Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma." Genes Dev 24 (16):1731-45. doi: 10.1101/gad.1890510.

Izaguirre, D. I., W. Zhu, T. Hai, H. C. Cheung, R. Krahe, and G. J. Cote. 2012. "PTBP1-dependent regulation of USP5 alternative RNA splicing plays a role in glioblastoma tumorigenesis." Mol Carcinog 51 (11):895-906. doi: 10.1002/mc.20859.

Jin, W., I. G. Bruno, T. X. Xie, L. J. Sanger, and G. J. Cote. 2003. "Polypyrimidine tract-binding protein down-regulates fibroblast growth factor receptor 1 alpha-exon inclusion." Cancer Res 63 (19):6154-7.

Jin, W., E. S. Huang, W. Bi, and G. J. Cote. 1998. "Exon sequence is required for regulated RNA splicing of the human fibroblast growth factor receptor-1 alpha-exon." J Biol Chem 273 (26):16170-6.

Jin, W., E. S. Huang, W. Bi, and G. J. Cote. 1999. "Redundant intronic repressors function to inhibit fibroblast growth factor receptor-1 alpha-exon recognition in glioblastoma cells." J Biol Chem 274 (39):28035-41.

Jin, W., I. E. McCutcheon, G. N. Fuller, E. S. Huang, and G. J. Cote. 2000. "Fibroblast growth factor receptor-1 alpha-exon exclusion and polypyrimidine tract-binding protein in glioblastoma multiforme tumors." Cancer Res 60 (5):1221-4.

Jules, J., D. Maiguel, and B. I. Hudson. 2013. "Alternative splicing of the RAGE cytoplasmic domain regulates cell signaling and function." PLoS One 8 (11):e78267. doi: 10.1371/journal.pone.0078267.

Jurica, M. S., A. Mesecar, P. J. Heath, W. Shi, T. Nowak, and B. L. Stoddard. 1998. "The allosteric regulation of pyruvate kinase by fructose-1,6-bisphosphate." Structure 6 (2):195-210.

Karni, R., E. de Stanchina, S. W. Lowe, R. Sinha, D. Mu, and A. R. Krainer. 2007. "The gene encoding the splicing factor SF2/ASF is a proto-oncogene." Nat Struct Mol Biol 14 (3):185-93. doi: 10.1038/nsmb1209.

Kastenhuber, E. R., J. T. Huse, S. H. Berman, A. Pedraza, J. Zhang, Y. Suehara, A. Viale, M. Cavatore, A. Heguy, N. Szerlip, M. Ladanyi, and C. W. Brennan. 2014. "Quantitative assessment of intragenic receptor tyrosine kinase deletions in primary glioblastomas: their prevalence and molecular correlates." Acta Neuropathol 127 (5):747-59. doi: 10.1007/s00401-013-1217-3.

Kikuchi, Y., T. Kakeya, O. Nakajima, A. Sakai, K. Ikeda, N. Yamaguchi, T. Yamazaki, K. Tanamoto, H. Matsuda, J. Sawada, and K. Takatori. 2008. "Hypoxia induces expression of a GPI-anchorless splice variant of the prion protein." FEBS J 275 (11):2965-76. doi: 10.1111/j.1742-4658.2008.06452.x.

Kim, E., A. Goren, and G. Ast. 2008. "Alternative splicing: current perspectives." Bioessays 30 (1):38-47. doi: 10.1002/bies.20692.

Kinzler, K. W., S. H. Bigner, D. D. Bigner, J. M. Trent, M. L. Law, S. J. O'Brien, A. J. Wong, and B. Vogelstein. 1987. "Identification of an amplified, highly expressed gene in a human glioma." Science 236 (4797):70-3.

Kraus, A., F. Neff, M. Behn, M. Schuermann, K. Muenkel, and J. Schlegel. 1999. "Expression of alternatively spliced mdm2 transcripts correlates with stabilized wild-type p53 protein in human glioblastoma cells." Int J Cancer 80 (6):930-4.

Kuan, C. T., C. J. Wikstrand, and D. D. Bigner. 2001. "EGF mutant receptor vIII as a molecular target in cancer therapy." Endocr Relat Cancer 8 (2):83-96.

Lamszus, K., N. O. Schmidt, L. Jin, J. Laterra, D. Zagzag, D. Way, M. Witte, M. Weinand, I. D. Goldberg, M. Westphal, and E. M. Rosen. 1998. "Scatter factor promotes motility of human glioma and neuromicrovascular endothelial cells." Int J Cancer 75 (1):19-28.

Laterra, J., M. Nam, E. Rosen, J. S. Rao, K. Lamszus, I. D. Goldberg, and P. Johnston. 1997. "Scatter factor/hepatocyte growth factor gene transfer enhances glioma growth and angiogenesis in vivo." Lab Invest 76 (4):565-77.

Latour, I., D. F. Louw, A. M. Beedle, J. Hamid, G. R. Sutherland, and G. W. Zamponi. 2004. "Expression of T-type calcium channel splice variants in human glioma." Glia 48 (2):112-9. doi: 10.1002/glia.20063.

Lefave, C. V., M. Squatrito, S. Vorlova, G. L. Rocco, C. W. Brennan, E. C. Holland, Y. X. Pan, and L. Cartegni. 2011. "Splicing factor hnRNPH drives an oncogenic splicing switch in gliomas." EMBO J 30 (19):4084-97. doi: 10.1038/emboj.2011.259.

Li, Z., P. Yang, and Z. Li. 2014. "The multifaceted regulation and functions of PKM2 in tumor progression." Biochim Biophys Acta 1846 (2):285-296. doi: 10.1016/j.bbcan.2014.07.008.

Lo, H. W., H. Zhu, X. Cao, A. Aldrich, and F. Ali-Osman. 2009. "A novel splice variant of GLI1 that promotes glioblastoma cell migration and invasion." Cancer Res 69 (17):6790-8. doi: 10.1158/0008-5472.CAN-09-0886.

Loilome, W., A. D. Joshi, C. M. ap Rhys, S. Piccirillo, A. L. Vescovi, G. L. Gallia, and G. J. Riggins. 2009. "Glioblastoma cell growth is suppressed by disruption of Fibroblast Growth Factor pathway signaling." J Neurooncol 94 (3):359-66. doi: 10.1007/s11060-009-9885-5.

Lu, K. V., S. Zhu, A. Cvrljevic, T. T. Huang, S. Sarkaria, D. Ahkavan, J. Dang, E. B. Dinca, S. B. Plaisier, I. Oderberg, Y. Lee, Z. Chen, J. S. Caldwell, Y. Xie, J. A. Loo, D. Seligson, A. Chakravari, F. Y. Lee, R. Weinmann, T. F. Cloughesy, S. F. Nelson, G. Bergers, T. Graeber, F. B. Furnari, C. D. James, W. K. Cavenee, T. G. Johns, and P. S. Mischel. 2009. "Fyn and SRC are effectors of oncogenic epidermal growth factor receptor signaling in glioblastoma patients." Cancer Res 69 (17):6889-98. doi: 10.1158/0008-5472.CAN-09-0347.

Luwor, R. B., T. G. Johns, C. Murone, H. J. Huang, W. K. Cavenee, G. Ritter, L. J. Old, A. W. Burgess, and A. M. Scott. 2001. "Monoclonal antibody 806 inhibits the growth of tumor xenografts expressing either the de2-7 or amplified epidermal growth factor receptor (EGFR) but not wild-type EGFR." Cancer Res 61 (14):5355-61.

Matera, A. G., and Z. Wang. 2014. "A day in the life of the spliceosome." Nat Rev Mol Cell Biol 15 (2):108-21. doi: 10.1038/nrm3742.

Matsumoto, R., M. Tada, M. Nozaki, C. L. Zhang, Y. Sawamura, and H. Abe. 1998. "Short alternative splice transcripts of the mdm2 oncogene correlate to malignancy in human astrocytic neoplasms." Cancer Res 58 (4):609-13.

Matsushita, H., A. Uenaka, T. Ono, K. Hasegawa, S. Sato, F. Koizumi, K. Nakagawa, M. Toda, T. Shingo, T. Ichikawa, Y. Noguchi, T. Tamiya, T. Furuta, T. Kawase, I. Date, and E. Nakayama. 2005. "Identification of glioma-specific RFX4-E and -F isoforms and humoral immune response in patients." Cancer Sci 96 (11):801-9. doi: 10.1111/j.1349-7006.2005.00112.x.

Mishima, K., T. G. Johns, R. B. Luwor, A. M. Scott, E. Stockert, A. A. Jungbluth, X. D. Ji, P. Suvarna, J. R. Voland, L. J. Old, H. J. Huang, and W. K. Cavenee. 2001. "Growth suppression of intracranial xenografted glioblastomas overexpressing mutant epidermal growth factor receptors by systemic administration of monoclonal antibody (mAb) 806, a novel monoclonal antibody directed to the receptor." Cancer Res 61 (14):5349-54.

Moriyama, T., H. Kataoka, R. Hamasuna, K. Yokogami, H. Uehara, H. Kawano, T. Goya, H. Tsubouchi, M. Koono, and S. Wakisaka. 1998. "Up-regulation of vascular endothelial growth factor induced by hepatocyte growth factor/scatter factor stimulation in human glioma cells." Biochem Biophys Res Commun 249 (1):73-7. doi: 10.1006/bbrc.1998.9078.

Mulherkar, N., K. V. Prasad, and B. S. Prabhakar. 2007. "MADD/DENN splice variant of the IG20 gene is a negative regulator of caspase-8 activation. Knockdown enhances TRAIL-induced apoptosis of cancer cells." J Biol Chem 282 (16):11715-21. doi: 10.1074/jbc.M701085200.

Nagane, M., F. Coufal, H. Lin, O. Bogler, W. K. Cavenee, and H. J. Huang. 1996. "A common mutant epidermal growth factor receptor confers enhanced tumorigenicity on human glioblastoma cells by increasing proliferation and reducing apoptosis." Cancer Res 56 (21):5079-86.

Nagane, M., A. Levitzki, A. Gazit, W. K. Cavenee, and H. J. Huang. 1998. "Drug resistance of human glioblastoma cells conferred by a tumor-specific mutant epidermal growth factor receptor through modulation of Bcl-XL and caspase-3-like proteases." Proc Natl Acad Sci U S A 95 (10):5724-9.

Nagane, M., Y. Narita, K. Mishima, A. Levitzki, A. W. Burgess, W. K. Cavenee, and H. J. Huang. 2001. "Human glioblastoma xenografts overexpressing a tumor-specific mutant epidermal growth factor receptor sensitized to cisplatin by the AG1478 tyrosine kinase inhibitor." J Neurosurg 95 (3):472-9. doi: 10.3171/jns.2001.95.3.0472.

Narla, G., A. Difeo, H. L. Reeves, D. J. Schaid, J. Hirshfeld, E. Hod, A. Katz, W. B. Isaacs, S. Hebbring, A. Komiya, S. K. McDonnell, K. E. Wiley, S. J. Jacobsen, S. D. Isaacs, P. C. Walsh, S. L. Zheng, B. L. Chang, D. M. Friedrichsen, J. L. Stanford, E. A. Ostrander, A. M. Chinnaiyan, M. A. Rubin, J. Xu, S. N. Thibodeau, S. L. Friedman, and J. A. Martignetti. 2005. "A germline DNA polymorphism enhances alternative splicing of the KLF6 tumor suppressor gene and is associated with increased prostate cancer risk." Cancer Res 65 (4):1213-22. doi: 10.1158/0008-5472.CAN-04-4249.

Narla, G., A. DiFeo, S. Yao, A. Banno, E. Hod, H. L. Reeves, R. F. Qiao, O. Camacho-Vanegas, A. Levine, A. Kirschenbaum, A. M. Chan, S. L. Friedman, and J. A. Martignetti. 2005. "Targeted inhibition of the KLF6 splice variant, KLF6 SV1, suppresses prostate cancer cell growth and spread." Cancer Res 65 (13):5761-8. doi: 10.1158/0008-5472.CAN-05-0217.

Nasser, N. J., A. Avivi, I. Shafat, E. Edovitsky, E. Zcharia, N. Ilan, I. Vlodavsky, and E. Nevo. 2009. "Alternatively spliced Spalax heparanase inhibits extracellular matrix degradation, tumor growth, and metastasis." Proc Natl Acad Sci U S A 106 (7):2253-8. doi: 10.1073/pnas.0812846106.

Nathanson, D. A., B. Gini, J. Mottahedeh, K. Visnyei, T. Koga, G. Gomez, A. Eskin, K. Hwang, J. Wang, K. Masui, A. Paucar, H. Yang, M. Ohashi, S. Zhu, J. Wykosky, R. Reed, S. F. Nelson, T. F. Cloughesy, C. D. James, P. N. Rao, H. I. Kornblum, J. R. Heath, W. K. Cavenee, F. B. Furnari, and P. S. Mischel. 2014. "Targeted therapy resistance mediated by dynamic regulation of extrachromosomal mutant EGFR DNA." Science 343 (6166):72-6. doi: 10.1126/science.1241328.

Nicholas, M. K., R. V. Lukas, N. F. Jafri, L. Faoro, and R. Salgia. 2006. "Epidermal growth factor receptor - mediated signal transduction in the development and therapy of gliomas." Clin Cancer Res 12 (24):7261-70. doi: 10.1158/1078-0432.CCR-06-0874.

Nilsen, T. W. 2003. "The spliceosome: the most complex macromolecular machine in the cell?" Bioessays 25 (12):1147-9. doi: 10.1002/bies.10394.

Nishikawa, R., X. D. Ji, R. C. Harmon, C. S. Lazar, G. N. Gill, W. K. Cavenee, and H. J. Huang. 1994. "A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity." Proc Natl Acad Sci U S A 91 (16):7727-31.

Ogiso, H., R. Ishitani, O. Nureki, S. Fukai, M. Yamanaka, J. H. Kim, K. Saito, A. Sakamoto, M. Inoue, M. Shirouzu, and S. Yokoyama. 2002. "Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains." Cell 110 (6):775-87.

Okamoto, I., L. C. Kenyon, D. R. Emlet, T. Mori, J. Sasaki, S. Hirosako, Y. Ichikawa, H. Kishi, A. K. Godwin, M. Yoshioka, M. Suga, M. Matsumoto, and A. J. Wong. 2003. "Expression of constitutively activated EGFRvIII in non-small cell lung cancer." Cancer Sci 94 (1):50-6.

Oltean, S., and D. O. Bates. 2014. "Hallmarks of alternative splicing in cancer." Oncogene 33 (46):5311-5318. doi: 10.1038/onc.2013.533.

Park, I. H., S. I. Yeon, J. H. Youn, J. E. Choi, N. Sasaki, I. H. Choi, and J. S. Shin. 2004. "Expression of a novel secreted splice variant of the receptor for advanced glycation end products (RAGE) in human brain astrocytes and peripheral blood mononuclear cells." Mol Immunol 40 (16):1203-11.

Pedersen, M. W., M. Meltorn, L. Damstrup, and H. S. Poulsen. 2001. "The type III epidermal growth factor receptor mutation. Biological significance and potential target for anti-cancer therapy." Ann Oncol 12 (6):745-60.

Perez-Torres, M., B. L. Valle, N. J. Maihle, L. Negron-Vega, R. Nieves-Alicea, and E. M. Cora. 2008. "Shedding of epidermal growth factor receptor is a regulated process that occurs with overexpression in malignant cells." Exp Cell Res 314 (16):2907-18. doi: 10.1016/j.yexcr.2008.07.013.

Piccione, E. C., T. J. Lieu, C. F. Gentile, T. R. Williams, A. J. Connolly, A. K. Godwin, A. C. Koong, and A. J. Wong. 2012. "A novel epidermal growth factor receptor variant lacking multiple domains directly activates transcription and is overexpressed in tumors." Oncogene 31 (24):2953-67. doi: 10.1038/onc.2011.465.

Pines, G., P. H. Huang, Y. Zwang, F. M. White, and Y. Yarden. 2010. "EGFRvIV: a previously uncharacterized oncogenic mutant reveals a kinase autoinhibitory mechanism." Oncogene 29 (43):5850-60. doi: 10.1038/onc.2010.313.

Puthalakath, H., D. C. Huang, L. A. O'Reilly, S. M. King, and A. Strasser. 1999. "The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex." Mol Cell 3 (3):287-96.

Reardon, D. A., G. Akabani, R. E. Coleman, A. H. Friedman, H. S. Friedman, J. E. Herndon, 2nd, I. Cokgor, R. E. McLendon, C. N. Pegram, J. M. Provenzale, J. A. Quinn, J. N. Rich, L. V. Regalado, J. H. Sampson, T. D. Shafman, C. J. Wikstrand, T. Z. Wong, X. G. Zhao, M. R. Zalutsky, and D. D. Bigner. 2002. "Phase II trial of murine (131)I-labeled antitenascin monoclonal antibody 81C6 administered into surgically created resection cavities of patients with newly diagnosed malignant gliomas." J Clin Oncol 20 (5):1389-97.

Reiter, J. L., and N. J. Maihle. 1996. "A 1.8 kb alternative transcript from the human epidermal growth factor receptor gene encodes a truncated form of the receptor." Nucleic Acids Res 24 (20):4050-6.

Reiter, J. L., D. W. Threadgill, G. D. Eley, K. E. Strunk, A. J. Danielsen, C. S. Sinclair, R. S. Pearsall, P. J. Green, D. Yee, A. L. Lampland, S. Balasubramaniam, T. D. Crossley, T. R. Magnuson, C. D. James, and N. J. Maihle. 2001. "Comparative genomic sequence analysis and isolation of human and mouse alternative EGFR transcripts encoding truncated receptor isoforms." Genomics 71 (1):1-20. doi: 10.1006/geno.2000.6341.

Sadeque, A., N. V. Serao, B. R. Southey, K. R. Delfino, and S. L. Rodriguez-Zas. 2012. "Identification and characterization of alternative exon usage linked glioblastoma multiforme survival." BMC Med Genomics 5:59. doi: 10.1186/1755-8794-5-59.

Schwechheimer, K., S. Huang, and W. K. Cavenee. 1995. "EGFR gene amplification--rearrangement in human glioblastomas." Int J Cancer 62 (2):145-8.

Scott, A. M., F. T. Lee, N. Tebbutt, R. Herbertson, S. S. Gill, Z. Liu, E. Skrinos, C. Murone, T. H. Saunder, B. Chappell, A. T. Papenfuss, A. M. Poon, W. Hopkins, F. E. Smyth, D. MacGregor, L. M. Cher, A. A. Jungbluth, G. Ritter, M. W. Brechbiel, R. Murphy, A. W. Burgess, E. W. Hoffman, T. G. Johns, and L. J. Old. 2007. "A phase I clinical trial with monoclonal antibody ch806 targeting transitional state and mutant epidermal growth factor receptors." Proc Natl Acad Sci U S A 104 (10):4071-6. doi: 10.1073/pnas.0611693104.

Shimokawa, T., U. Tostar, M. Lauth, R. Palaniswamy, M. Kasper, R. Toftgard, and P. G. Zaphiropoulos. 2008. "Novel human glioma-associated oncogene 1 (GLI1) splice variants reveal distinct mechanisms in the terminal transduction of the hedgehog signal." J Biol Chem 283 (21):14345-54. doi: 10.1074/jbc.M800299200.

Simon, P., M. Schneck, T. Hochstetter, E. Koutsouki, M. Mittelbronn, A. Merseburger, C. Weigert, A. Niess, and F. Lang. 2007. "Differential regulation of serum- and glucocorticoid-inducible kinase 1 (SGK1) splice variants based on alternative initiation of transcription." Cell Physiol Biochem 20 (6):715-28. doi: 10.1159/000110432.

Smith, D. J., C. C. Query, and M. M. Konarska. 2008. ""Nought may endure but mutability": spliceosome dynamics and the regulation of splicing." Mol Cell 30 (6):657-66. doi: 10.1016/j.molcel.2008.04.013.

Song, S. W., G. N. Fuller, H. Zheng, and W. Zhang. 2005. "Inactivation of the invasion inhibitory gene IIp45 by alternative splicing in gliomas." Cancer Res 65 (9):3562-7. doi: 10.1158/0008-5472.CAN-04-3392.

Srinivasula, S. M., M. Ahmad, Y. Guo, Y. Zhan, Y. Lazebnik, T. Fernandes-Alnemri, and E. S. Alnemri. 1999. "Identification of an endogenous dominant-negative short isoform of caspase-9 that can regulate apoptosis." Cancer Res 59 (5):999-1002.

Sugawa, N., A. J. Ekstrand, C. D. James, and V. P. Collins. 1990. "Identical splicing of aberrant epidermal growth factor receptor transcripts from amplified rearranged genes in human glioblastomas." Proc Natl Acad Sci U S A 87 (21):8602-6.

Suzuki, S. O., R. Kitai, J. Llena, S. C. Lee, J. E. Goldman, and B. Shafit-Zagardo. 2002. "MAP-2e, a novel MAP-2 isoform, is expressed in gliomas and delineates tumor architecture and patterns of infiltration." J Neuropathol Exp Neurol 61 (5):403-12.

Tafani, M., M. Di Vito, A. Frati, L. Pellegrini, E. De Santis, G. Sette, A. Eramo, P. Sale, E. Mari, A. Santoro, A. Raco, M. Salvati, R. De Maria, and M. A. Russo. 2011. "Pro-inflammatory gene expression in solid glioblastoma microenvironment and in hypoxic stem cells from human glioblastoma." J Neuroinflammation 8:32. doi: 10.1186/1742-2094-8-32.

Taguchi, A., D. C. Blood, G. del Toro, A. Canet, D. C. Lee, W. Qu, N. Tanji, Y. Lu, E. Lalla, C. Fu, M. A. Hofmann, T. Kislinger, M. Ingram, A. Lu, H. Tanaka, O. Hori, S. Ogawa, D. M. Stern, and A. M. Schmidt. 2000. "Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases." Nature 405 (6784):354-60. doi: 10.1038/35012626.

Takino, T., M. Nakada, H. Miyamori, J. Yamashita, K. M. Yamada, and H. Sato. 2003. "CrkI adapter protein modulates cell migration and invasion in glioblastoma." Cancer Res 63 (9):2335-7.

Tazi, J., N. Bakkour, and S. Stamm. 2009. "Alternative splicing and disease." Biochim Biophys Acta 1792 (1):14-26. doi: 10.1016/j.bbadis.2008.09.017.

Voldborg, B. R., L. Damstrup, M. Spang-Thomsen, and H. S. Poulsen. 1997. "Epidermal growth factor receptor (EGFR) and EGFR mutations, function and possible role in clinical trials." Ann Oncol 8 (12):1197-206.

Wahl, M. C., C. L. Will, and R. Luhrmann. 2009. "The spliceosome: design principles of a dynamic RNP machine." Cell 136 (4):701-18. doi: 10.1016/j.cell.2009.02.009.

Wang, F., M. Kan, J. Xu, G. Yan, and W. L. McKeehan. 1995. "Ligand-specific structural domains in the fibroblast growth factor receptor." J Biol Chem 270 (17):10222-30.

Wang, F., M. Kan, G. Yan, J. Xu, and W. L. McKeehan. 1995. "Alternately spliced NH2-terminal immunoglobulin-like Loop I in the ectodomain of the fibroblast growth factor (FGF) receptor 1 lowers affinity for both heparin and FGF-1." J Biol Chem 270 (17):10231-5.

Wang, H., M. Zhou, B. Shi, Q. Zhang, H. Jiang, Y. Sun, J. Liu, K. Zhou, M. Yao, J. Gu, S. Yang, Y. Mao, and Z. Li. 2011. "Identification of an exon 4-deletion variant of epidermal growth factor receptor with increased metastasis-promoting capacity." Neoplasia 13 (5):461-71.

Wang, X. Q., and J. A. Rothnagel. 2001. "Post-transcriptional regulation of the gli1 oncogene by the expression of alternative 5' untranslated regions." J Biol Chem 276 (2):1311-6. doi: 10.1074/jbc.M005191200.

Wang, X., P. Sheng, X. Guo, J. Wang, L. Hou, G. Hu, C. Luo, Y. Dong, and Y. Lu. 2013. "Identification and expression of a novel MDM4 splice variant in human glioma." Brain Res 1537:260-6. doi: 10.1016/j.brainres.2013.07.054.

Wang, Z., H. Y. Jeon, F. Rigo, C. F. Bennett, and A. R. Krainer. 2012. "Manipulation of PK-M mutually exclusive alternative splicing by antisense oligonucleotides." Open Biol 2 (10):120133. doi: 10.1098/rsob.120133.

Warburg, O. 1956a. "On respiratory impairment in cancer cells." Science 124 (3215):269-70.

Warburg, O. 1956b. "On the origin of cancer cells." Science 123 (3191):309-14.

Werner, S., W. Weinberg, X. Liao, K. G. Peters, M. Blessing, S. H. Yuspa, R. L. Weiner, and L. T. Williams. 1993. "Targeted expression of a dominant-negative FGF receptor mutant in the epidermis of transgenic mice reveals a role of FGF in keratinocyte organization and differentiation." EMBO J 12 (7):2635-43.

Wong, A. J., J. M. Ruppert, S. H. Bigner, C. H. Grzeschik, P. A. Humphrey, D. S. Bigner, and B. Vogelstein. 1992. "Structural alterations of the epidermal growth factor receptor gene in human gliomas." Proc Natl Acad Sci U S A 89 (7):2965-9.

Xiang, C., R. Sarid, S. Cazacu, S. Finniss, H. K. Lee, A. Ziv-Av, T. Mikkelsen, and C. Brodie. 2007. "Cloning and characterization of human RTVP-1b, a novel splice variant of RTVP-1 in glioma cells." Biochem Biophys Res Commun 362 (3):612-8. doi: 10.1016/j.bbrc.2007.08.138.

Yadav, A. K., V. Vashishta, N. Joshi, and P. Taneja. 2014. "AR-A 014418 Used against GSK3beta Downregulates Expression of hnRNPA1 and SF2/ASF Splicing Factors." J Oncol 2014:695325. doi: 10.1155/2014/695325.

Yamada, S. M., F. Yamaguchi, R. Brown, M. S. Berger, and R. S. Morrison. 1999. "Suppression of glioblastoma cell growth following antisense oligonucleotide-mediated inhibition of fibroblast growth factor receptor expression." Glia 28 (1):66-76.

Yamada, Y., T. Kuroiwa, T. Nakagawa, Y. Kajimoto, T. Dohi, H. Azuma, M. Tsuji, K. Kami, and S. Miyatake. 2003. "Transcriptional expression of survivin and its splice variants in brain tumors in humans." J Neurosurg 99 (4):738-45. doi: 10.3171/jns.2003.99.4.0738.

Yamaguchi, F., H. Saya, J. M. Bruner, and R. S. Morrison. 1994. "Differential expression of two fibroblast growth factor-receptor genes is associated with malignant progression in human astrocytomas." Proc Natl Acad Sci U S A 91 (2):484-8.

Yamaguchi, T., T. Okada, K. Takeuchi, T. Tonda, M. Ohtaki, S. Shinoda, T. Masuzawa, K. Ozawa, and T. Inaba. 2003. "Enhancement of thymidine kinase-mediated killing of malignant glioma by BimS, a BH3-only cell death activator." Gene Ther 10 (5):375-85. doi: 10.1038/sj.gt.3301897.

Yu, F., and W. M. Fu. 2014. "Identification of differential splicing genes in gliomas using exon expression profiling." Mol Med Rep. doi: 10.3892/mmr.2014.2775.

Yu, Y., X. Jiang, B. S. Schoch, R. S. Carroll, P. M. Black, and M. D. Johnson. 2007. "Aberrant splicing of cyclin-dependent kinase-associated protein phosphatase KAP increases proliferation and migration in glioblastoma." Cancer Res 67 (1):130-8. doi: 10.1158/0008-5472.CAN-06-2478.

Zalutsky, M. R., R. P. Moseley, H. B. Coakham, R. E. Coleman, and D. D. Bigner. 1989. "Pharmacokinetics and tumor localization of 131I-labeled anti-tenascin monoclonal antibody 81C6 in patients with gliomas and other intracranial malignancies." Cancer Res 49 (10):2807-13.

Zhang, J., and J. L. Manley. 2013. "Misregulation of pre-mRNA alternative splicing in cancer." Cancer Discov 3 (11):1228-37. doi: 10.1158/2159-8290.CD-13-0253.

Zhang, Z., F. Lotti, K. Dittmar, I. Younis, L. Wan, M. Kasim, and G. Dreyfuss. 2008. "SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing." Cell 133 (4):585-600. doi: 10.1016/j.cell.2008.03.031.

Zheng, P. P., A. M. Sieuwerts, T. M. Luider, M. van der Weiden, P. A. Sillevis-Smitt, and J. M. Kros. 2004. "Differential expression of splicing variants of the human caldesmon gene (CALD1) in glioma neovascularization versus normal brain microvasculature." Am J Pathol 164 (6):2217-28. doi: 10.1016/S0002-9440(10)63778-9.

Zheng, P. P., M. van der Weiden, and J. M. Kros. 2005. "Differential expression of Hela-type caldesmon in tumour neovascularization: a new marker of angiogenic endothelial cells." J Pathol 205 (3):408-14. doi: 10.1002/path.1700.

Zhu, H., R. L. Carpenter, W. Han, and H. W. Lo. 2014. "The GLI1 splice variant TGLI1 promotes glioblastoma angiogenesis and growth." Cancer Lett 343 (1):51-61. doi: 10.1016/j.canlet.2013.09.014.

DOI: http://dx.doi.org/10.18103/mra.v0i1.11


  • There are currently no refbacks.