Quantitative proteomic analysis reveals effects of Epidermal Growth Factor Receptor (EGFR) on invasion-promoting proteins secreted by glioblastoma cells

Molecular and Cellular Proteomics

Volumn 13, Issue 10, 2014, Pages 2618-2631

  Sangar, Vineet ^a   Funk, Cory C ^a   Kusebauch, Ulrike ^a   Campbell, David S ^a   Moritz, Robert L ^a   Price, Nathan D ^a  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; STABLE ISOTOPE; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR VIII; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PTEN PROTEIN, HUMAN; SIGNAL PEPTIDE;

ARTICLE; CANCER CELL; CANCER PROGNOSIS; CELL CULTURE; CELL MUTANT; CELL PROLIFERATION; CELL VIABILITY; COLLISIONALLY ACTIVATED DISSOCIATION; COMPARATIVE STUDY; ELECTROSPRAY; EXTRACELLULAR MATRIX; GLIOBLASTOMA; HUMAN; INTRACELLULAR SIGNALING; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; OXIDATIVE STRESS; PROTEIN ANALYSIS; PROTEOMICS; TANDEM MASS SPECTROMETRY; TUMOR CELL; TUMOR INVASION; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; PROCEDURES; SECRETION (PROCESS); SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASM INVASIVENESS; PROTEOMICS; PTEN PHOSPHOHYDROLASE; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84907948608     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.040428     Document Type: Article

References (112)

1. Ohgaki, H., and Kleihues, P. (2005) Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas. J. Neuropathol. Exp. Neurol. 64, 479-489
2. Ohgaki, H., and Kleihues, P. (2005) Epidemiology and etiology of gliomas. Acta Neuropathol. 109, 93-108
3. Furnari, F. B., Fenton, T., Bachoo, R. M., Mukasa, A., Stommel, J. M., Stegh, A., Hahn, W. C., Ligon, K. L., Louis, D. N., Brennan, C., Chin, L., DePinho, R. A., and Cavenee, W. K. (2007) Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 21, 2683-2710
4. Stupp, R., Mason, W. P., van den Bent, M. J., Weller, M., Fisher, B., Taphoorn, M. J., Belanger, K., Brandes, A. A., Marosi, C., Bogdahn, U., Curschmann, J., Janzer, R. C., Ludwin, S. K., Gorlia, T., Allgeier, A., Lacombe, D., Cairncross, J. G., Eisenhauer, E., and Mirimanoff, R. O. (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987-996
5. Parsons, D. W., Jones, S., Zhang, X., Lin, J. C., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I. M., Gallia, G. L., Olivi, A., McLendon, R., Rasheed, B. A., Keir, S., Nikolskaya, T., Nikolsky, Y., Busam, D. A., Tekleab, H., Diaz, L. A., Jr., Hartigan, J., Smith, D. R., Strausberg, R. L., Marie, S. K., Shinjo, S. M., Yan, H., Riggins, G. J., Bigner, D. D., Karchin, R., Papadopoulos, N., Parmigiani, G., Vogelstein, B., Velculescu, V. E., and Kinzler, K. W. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321, 1807-1812
6. Cancer Genome Atlas Research, N. (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455, 1061-1068
7. Brennan, C. W., Verhaak, R. G., McKenna, A., Campos, B., Noushmehr, H., Salama, S. R., Zheng, S., Chakravarty, D., Sanborn, J. Z., Berman, S. H., Beroukhim, R., Bernard, B., Wu, C. J., Genovese, G., Shmulevich, I., Barnholtz-Sloan, J., Zou, L., Vegesna, R., Shukla, S. A., Ciriello, G., Yung, W. K., Zhang, W., Sougnez, C., Mikkelsen, T., Aldape, K., Bigner, D. D., Van Meir, E. G., Prados, M., Sloan, A., Black, K. L., Eschbacher, J., Finocchiaro, G., Friedman, W., Andrews, D. W., Guha, A., Iacocca, M., O'Neill, B. P., Foltz, G., Myers, J., Weisenberger, D. J., Penny, R., Kucherlapati, R., Perou, C. M., Hayes, D. N., Gibbs, R., Marra, M., Mills, G. B., Lander, E., Spellman, P., Wilson, R., Sander, C., Weinstein, J., Meyerson, M., Gabriel, S., Laird, P. W., Haussler, D., Getz, G., Chin, L., and Network, T. R. (2013) The somatic genomic landscape of glioblastoma. Cell 155, 462-477
8. Frattini, V., Trifonov, V., Chan, J. M., Castano, A., Lia, M., Abate, F., Keir, S. T., Ji, A. X., Zoppoli, P., Niola, F., Danussi, C., Dolgalev, I., Porrati, P., Pellegatta, S., Heguy, A., Gupta, G., Pisapia, D. J., Canoll, P., Bruce, J. N., McLendon, R. E., Yan, H., Aldape, K., Finocchiaro, G., Mikkelsen, T., Prive, G. G., Bigner, D. D., Lasorella, A., Rabadan, R., and Iavarone, A. (2013) The integrated landscape of driver genomic alterations in glioblastoma. Nat. Genet. 45, 1141-1149
9. Huang, P. H., Xu, A. M., and White, F. M. (2009) Oncogenic EGFR signaling networks in glioma. Sci. Signal. 2, re6
10. Ferguson, K. M., Berger, M. B., Mendrola, J. M., Cho, H. S., Leahy, D. J., and Lemmon, M. A. (2003) EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol. Cell 11, 507-517
11. Citri, A., and Yarden, Y. (2006) EGF-ERBB signalling: towards the systems level. Nat. Rev.. Mol. Cell Biol. 7, 505-516
12. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev.. Mol. Cell Biol. 2, 127-137
13. Wells, A. (1999) EGF receptor. Int. J. Biochem. Cell Biol 31, 637-643
14. Dikic, I. (2003) Mechanisms controlling EGF receptor endocytosis and degradation. Biochem. Soc. Trans. 31, 1178-1181
15. Verbeek, B. S., Adriaansen-Slot, S. S., Vroom, T. M., Beckers, T., and Rijksen, G. (1998) Overexpression of EGFR and c-erbB2 causes enhanced cell migration in human breast cancer cells and NIH3T3 fibroblasts. FEBS Lett. 425, 145-150
16. Ekstrand, A. J., James, C. D., Cavenee, W. K., Seliger, B., Pettersson, R. F., and Collins, V. P. (1991) Genes for epidermal growth factor receptor, transforming growth factor alpha, and epidermal growth factor and their expression in human gliomas in vivo. Cancer Res. 51, 2164-2172
17. Ohgaki, H., and Kleihues, P. (2007) Genetic pathways to primary and secondary glioblastoma. Am. J. Pathol. 170, 1445-1453
18. Brat, D. J., Shehata, B. M., Castellano-Sanchez, A. A., Hawkins, C., Yost, R. B., Greco, C., Mazewski, C., Janss, A., Ohgaki, H., and Perry, A. (2007) Congenital glioblastoma: a clinicopathologic and genetic analysis. Brain Pathol. 17, 276-281
19. Kim, H. G., Kassis, J., Souto, J. C., Turner, T., and Wells, A. (1999) EGF receptor signaling in prostate morphogenesis and tumorigenesis. Histol. Histopathol. 14, 1175-1182
20. Chaffanet, M., Chauvin, C., Laine, M., Berger, F., Chedin, M., Rost, N., Nissou, M. F., and Benabid, A. L. (1992) EGF receptor amplification and expression in human brain tumours. Eur. J. Cancer 28, 11-17
21. Sharma, S. V., Bell, D. W., Settleman, J., and Haber, D. A. (2007) Epidermal growth factor receptor mutations in lung cancer. Nat. Rev. Cancer 7, 169-181
22. Ohgaki, H., Dessen, P., Jourde, B., Horstmann, S., Nishikawa, T., Di Patre, P. L., Burkhard, C., Schuler, D., Probst-Hensch, N. M., Maiorka, P. C., Baeza, N., Pisani, P., Yonekawa, Y., Yasargil, M. G., Lutolf, U. M., and Kleihues, P. (2004) Genetic pathways to glioblastoma: a population-based study. Cancer Res. 64, 6892-6899
23. Singh, A. B., and Harris, R. C. (2005) Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell. Signal. 17, 1183-1193
24. Humphrey, P. A., Gangarosa, L. M., Wong, A. J., Archer, G. E., Lund-Johansen, M., Bjerkvig, R., Laerum, O. D., Friedman, H. S., and Bigner, D. D. (1991) Deletion-mutant epidermal growth factor receptor in human gliomas: effects of type II mutation on receptor function. Biochem. Biophys. Res. Commun. 178, 1413-1420
25. Wong, A. J., Ruppert, J. M., Bigner, S. H., Grzeschik, C. H., Humphrey, P. A., Bigner, D. S., and Vogelstein, B. (1992) Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc. Natl. Acad. Sci. U. S. A. 89, 2965-2969
26. Peschard, P., and Park, M. (2007) From Tpr-Met to Met, tumorigenesis and tubes. Oncogene 26, 1276-1285
27. Huang, H. S., Nagane, M., Klingbeil, C. K., Lin, H., Nishikawa, R., Ji, X. D., Huang, C. M., Gill, G. N., Wiley, H. S., and Cavenee, W. K. (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, 2927-2935
28. Schmidt, M. H., Furnari, F. B., Cavenee, W. K., and Bogler, O. (2003) Epidermal growth factor receptor signaling intensity determines intracellular protein interactions, ubiquitination, and internalization. Proc. Natl. Acad. Sci. U. S. A. 100, 6505-6510
29. Helin, K., Velu, T., Martin, P., Vass, W. C., Allevato, G., Lowy, D. R., and Beguinot, L. (1991) The biological activity of the human epidermal growth factor receptor is positively regulated by its C-terminal tyrosines. Oncogene 6, 825-832
30. Shao, H., Cheng, H. Y., Cook, R. G., and Tweardy, D. J. (2003) Identification and characterization of signal transducer and activator of transcription 3 recruitment sites within the epidermal growth factor receptor. Cancer Res. 63, 3923-3930
31. Huang, P. H., Mukasa, A., Bonavia, R., Flynn, R. A., Brewer, Z. E., Cavenee, W. K., Furnari, F. B., and White, F. M. (2007) Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc. Natl. Acad. Sci. U. S. A. 104, 12867-12872
32. Mosesson, Y., Mills, G. B., and Yarden, Y. (2008) Derailed endocytosis: an emerging feature of cancer. Nat. Rev. Cancer 8, 835-850
33. Feldkamp, M. M., Lala, P., Lau, N., Roncari, L., and Guha, A. (1999) Expression of activated epidermal growth factor receptors, Rasguanosine triphosphate, and mitogen-activated protein kinase in human glioblastoma multiforme specimens. Neurosurgery 45, 1442-1453
34. Nishikawa, R., Ji, X. D., Harmon, R. C., Lazar, C. S., Gill, G. N., Cavenee, W. K., and Huang, H. J. (1994) A mutant epidermal growth factor receptor common in human glioma confers enhanced tumorigenicity. Proc. Natl. Acad. Sci. U. S. A. 91, 7727-7731
35. Nagane, M., Coufal, F., Lin, H., Bogler, O., Cavenee, W. K., and Huang, H. J. (1996) A common mutant epidermal growth factor receptor confers enhanced tumorigenicity on human glioblastoma cells by increasing proliferation and reducing apoptosis. Cancer Res. 56, 5079-5086
36. Ding, H., Shannon, P., Lau, N., Wu, X., Roncari, L., Baldwin, R. L., Takebayashi, H., Nagy, A., Gutmann, D. H., and Guha, A. (2003) Oligodendrogliomas result from the expression of an activated mutant epidermal growth factor receptor in a RAS transgenic mouse astrocytoma model. Cancer Res. 63, 1106-1113
37. Holland, E. C., Hively, W. P., DePinho, R. A., and Varmus, H. E. (1998) A constitutively active epidermal growth factor receptor cooperates with disruption of G1 cell-cycle arrest pathways to induce glioma-like lesions in mice. Genes Dev. 12, 3675-3685
38. Zhu, H., Acquaviva, J., Ramachandran, P., Boskovitz, A., Woolfenden, S., Pfannl, R., Bronson, R. T., Chen, J. W., Weissleder, R., Housman, D. E., and Charest, A. (2009) Oncogenic EGFR signaling cooperates with loss of tumor suppressor gene functions in gliomagenesis. Proc. Natl. Acad. Sci. U. S. A. 106, 2712-2716
39. Frederick, L., Eley, G., Wang, X. Y., and James, C. D. (2000) Analysis of genomic rearrangements associated with EGRFvIII expression suggests involvement of Alu repeat elements. Neuro Oncol. 2, 159-163
40. Sugawa, N., Ekstrand, A. J., James, C. D., and Collins, V. P. (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, 8602-8606
41. Wang, M. Y., Lu, K. V., Zhu, S., Dia, E. Q., Vivanco, I., Shackleford, G. M., Cavenee, W. K., Mellinghoff, I. K., Cloughesy, T. F., Sawyers, C. L., and Mischel, P. S. (2006) Mammalian target of rapamycin inhibition promotes response to epidermal growth factor receptor kinase inhibitors in PTEN-deficient and PTEN-intact glioblastoma cells. Cancer Res. 66, 7864-7869
42. Kolibaba, K. S., and Druker, B. J. (1997) Protein tyrosine kinases and cancer. Biochim. Biophys. Acta 1333, F217-248
43. Holland, E. C., Celestino, J., Dai, C., Schaefer, L., Sawaya, R. E., and Fuller, G. N. (2000) Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nat. Genet. 25, 55-57
44. Sonoda, Y., Ozawa, T., Aldape, K. D., Deen, D. F., Berger, M. S., and Pieper, R. O. (2001) Akt pathway activation converts anaplastic astrocytoma to glioblastoma multiforme in a human astrocyte model of glioma. Cancer Res. 61, 6674-6678
45. Talasila, K. M., Soentgerath, A., Euskirchen, P., Rosland, G. V., Wang, J., Huszthy, P. C., Prestegarden, L., Skaftnesmo, K. O., Sakariassen, P. O., Eskilsson, E., Stieber, D., Keunen, O., Brekka, N., Moen, I., Nigro, J. M., Vintermyr, O. K., Lund-Johansen, M., Niclou, S., Mork, S. J., Enger, P. O., Bjerkvig, R., and Miletic, H. (2013) EGFR wild-type amplification and activation promote invasion and development of glioblastoma independent of angiogenesis. Acta Neuropathol. 125, 683-698
46. Burger, P. C., and Bigner, S. H. (1988) Practical approaches to the diagnosis of central nervous system tumors. Mod. Pathol. 1, 493-511
47. Scheithauer, B. W., and Bruner, J. M. (1987) Central nervous system tumors. Clin. Lab. Med. 7, 157-179
48. Hunter, S. B., Brat, D. J., Olson, J. J., Von Deimling, A., Zhou, W., and Van Meir, E. G. (2003) Alterations in molecular pathways of diffusely infiltrating glial neoplasms: application to tumor classification and anti-tumor therapy (Review). Int. J. Oncol. 23, 857-869
49. Teodorczyk, M., and Martin-Villalba, A. (2010) Sensing invasion: cell surface receptors driving spreading of glioblastoma. J. Cell. Physiol. 222, 1-10
50. Tysnes, B. B., and Mahesparan, R. (2001) Biological mechanisms of glioma invasion and potential therapeutic targets. J. Neurooncol. 53, 129-147
51. Chambers, M. C., Maclean, B., Burke, R., Amodei, D., Ruderman, D. L., Neumann, S., Gatto, L., Fischer, B., Pratt, B., Egertson, J., Hoff, K., Kessner, D., Tasman, N., Shulman, N., Frewen, B., Baker, T. A., Brusniak, M. Y., Paulse, C., Creasy, D., Flashner, L., Kani, K., Moulding, C., Seymour, S. L., Nuwaysir, L. M., Lefebvre, B., Kuhlmann, F., Roark, J., Rainer, P., Detlev, S., Hemenway, T., Huhmer, A., Langridge, J., Connolly, B., Chadick, T., Holly, K., Eckels, J., Deutsch, E. W., Moritz, R. L., Katz, J. E., Agus, D. B., MacCoss, M., Tabb, D. L., and Mallick, P. (2012) A cross-platform toolkit for mass spectrometry and proteomics. Nat, Biotechnol. 30, 918-920
52. Craig, R., and Beavis, R. C. (2004) TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20, 1466-1467
53. Keller, A., Eng, J., Zhang, N., Li, X. J., and Aebersold, R. (2005) A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol. Syst. Biol. 1, 2005 0017
54. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658
55. Farrah, T., Deutsch, E. W., Kreisberg, R., Sun, Z., Campbell, D. S., Mendoza, L., Kusebauch, U., Brusniak, M. Y., Huttenhain, R., Schiess, R., Selevsek, N., Aebersold, R., and Moritz, R. L. (2012) PASSEL: the PeptideAtlas SRMexperiment library. Proteomics 12, 1170-1175
56. Kusebauch, U., Deutsch EW., Campbell DS., Sun Z., Farrah T., Moritz RL. (2014) Using PeptideAtlas, SRMAtlas and PASSEL - Comprehensive resources for discovery and targeted proteomics. Curr. Protoc. Bioinformatics in press
57. MacLean, B., Tomazela, D. M., Shulman, N., Chambers, M., Finney, G. L., Frewen, B., Kern, R., Tabb, D. L., Liebler, D. C., and MacCoss, M. J. (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26, 966-968
58. Polisetty, R. V., Gupta, M. K., Nair, S. C., Ramamoorthy, K., Tiwary, S., Shiras, A., Chandak, G. R., and Sirdeshmukh, R. (2011) Glioblastoma cell secretome: analysis of three glioblastoma cell lines reveal 148 non-redundant proteins. J. Proteomics 74, 1918-1925
59. Formolo, C. A., Williams, R., Gordish-Dressman, H., MacDonald, T. J., Lee, N. H., and Hathout, Y. (2011) Secretome signature of invasive glioblastoma multiforme. J. Proteome Res. 10, 3149-3159
60. Micallef, J., Taccone, M., Mukherjee, J., Croul, S., Busby, J., Moran, M. F., and Guha, A. (2009) Epidermal growth factor receptor variant III-induced glioma invasion is mediated through myristoylated alanine-rich protein kinase C substrate overexpression. Cancer Res. 69, 7548-7556
61. Rangaswami, H., Bulbule, A., and Kundu, G. C. (2006) Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol. 16, 79-87
62. Ku, B. M., Lee, Y. K., Ryu, J., Jeong, J. Y., Choi, J., Eun, K. M., Shin, H. Y., Kim, D. G., Hwang, E. M., Yoo, J. C., Park, J. Y., Roh, G. S., Kim, H. J., Cho, G. J., Choi, W. S., Paek, S. H., and Kang, S. S. (2011) CHI3L1 (YKL-40) is expressed in human gliomas and regulates the invasion, growth and survival of glioma cells. Int. J. Cancer 128, 1316-1326
63. Muslimovic, A., Ismail, I. H., Gao, Y., and Hammarsten, O. (2008) An optimized method for measurement of gamma-H2AX in blood mononuclear and cultured cells. Nat. Protoc. 3, 1187-1193
64. Mebratu, Y., and Tesfaigzi, Y. (2009) How ERK1/2 activation controls cell proliferation and cell death: Is subcellular localization the answer? Cell Cycle 8, 1168-1175
65. Hoshino, D., Jourquin, J., Emmons, S. W., Miller, T., Goldgof, M., Costello, K., Tyson, D. R., Brown, B., Lu, Y., Prasad, N. K., Zhang, B., Mills, G. B., Yarbrough, W. G., Quaranta, V., Seiki, M., and Weaver, A. M. (2012) Network analysis of the focal adhesion to invadopodia transition identifies a PI3K-PKCalpha invasive signaling axis. Sci. Signal. 5, ra66
66. Kleber, S., Sancho-Martinez, I., Wiestler, B., Beisel, A., Gieffers, C., Hill, O., Thiemann, M., Mueller, W., Sykora, J., Kuhn, A., Schreglmann, N., Letellier, E., Zuliani, C., Klussmann, S., Teodorczyk, M., Grone, H. J., Ganten, T. M., Sultmann, H., Tuttenberg, J., von Deimling, A., Regnier-Vigouroux, A., Herold-Mende, C., and Martin-Villalba, A. (2008) Yes and PI3K bind CD95 to signal invasion of glioblastoma. Cancer Cell 13, 235-248
67. Kitamura, T., Asai, N., Enomoto, A., Maeda, K., Kato, T., Ishida, M., Jiang, P., Watanabe, T., Usukura, J., Kondo, T., Costantini, F., Murohara, T., and Takahashi, M. (2008) Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin. Nat. Cell Biol. 10, 329-337
68. Prasad, N., Topping, R. S., and Decker, S. J. (2002) Src family tyrosine kinases regulate adhesion-dependent tyrosine phosphorylation of 5′-inositol phosphatase SHIP2 during cell attachment and spreading on collagen I. J. Cell Sci. 115, 3807-3815
69. Luwor, R. B., Stylli, S. S., and Kaye, A. H. (2013) The role of Stat3 in glioblastoma multiforme. J. Clin. Neurosci. 20, 907-911
70. Huang, P. H., Miraldi, E. R., Xu, A. M., Kundukulam, V. A., Del Rosario, A. M., Flynn, R. A., Cavenee, W. K., Furnari, F. B., and White, F. M. (2010) Phosphotyrosine signaling analysis of site-specific mutations on EGFRvIII identifies determinants governing glioblastoma cell growth. Mol. Biosyst. 6, 1227-1237
71. Stupp, R., Hegi, M. E., Mason, W. P., van den Bent, M. J., Taphoorn, M. J., Janzer, R. C., Ludwin, S. K., Allgeier, A., Fisher, B., Belanger, K., Hau, P., Brandes, A. A., Gijtenbeek, J., Marosi, C., Vecht, C. J., Mokhtari, K., Wesseling, P., Villa, S., Eisenhauer, E., Gorlia, T., Weller, M., Lacombe, D., Cairncross, J. G., Mirimanoff, R. O., European Organisation for, R., Treatment of Cancer Brain, T., Radiation Oncology, G., and National Cancer Institute of Canada Clinical Trials, G. (2009) Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 10, 459-466
72. Berens, M. E., Rutka, J. T., and Rosenblum, M. L. (1990) Brain tumor epidemiology, growth, and invasion. Neurosurg. Clin. N. Am. 1, 1-18
73. Okamoto, I., Kawano, Y., Matsumoto, M., Suga, M., Kaibuchi, K., Ando, M., and Saya, H. (1999) Regulated CD44 cleavage under the control of protein kinase C, calcium influx, and the Rho family of small G proteins. J. Biol. Chem. 274, 25525-25534
74. Okamoto, I., Kawano, Y., Tsuiki, H., Sasaki, J., Nakao, M., Matsumoto, M., Suga, M., Ando, M., Nakajima, M., and Saya, H. (1999) CD44 cleavage induced by a membrane-associated metalloprotease plays a critical role in tumor cell migration. Oncogene 18, 1435-1446
75. Gunia, S., Hussein, S., Radu, D. L., Putz, K. M., Breyer, R., Hecker, H., Samii, M., Walter, G. F., and Stan, A. C. (1999) CD44s-targeted treatment with monoclonal antibody blocks intracerebral invasion and growth of 9L gliosarcoma. Clin. Exp. Metastasis 17, 221-230
76. Sarafian, T. A., Montes, C., Imura, T., Qi, J., Coppola, G., Geschwind, D. H., and Sofroniew, M. V. (2010) Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PloS One 5, e9532
77. Bonavia, R., Inda, M. M., Vandenberg, S., Cheng, S. Y., Nagane, M., Hadwiger, P., Tan, P., Sah, D. W., Cavenee, W. K., and Furnari, F. B. (2012) EGFRvIII promotes glioma angiogenesis and growth through the NF-kappaB, interleukin-8 pathway. Oncogene 31, 4054-4066
78. Clarke, K., Smith, K., Gullick, W. J., and Harris, A. L. (2001) Mutant epidermal growth factor receptor enhances induction of vascular endothelial growth factor by hypoxia and insulin-like growth factor-1 via a PI3 kinase dependent pathway. Br. J. Cancer 84, 1322-1329
79. Magnus, N., Garnier, D., and Rak, J. (2010) Oncogenic epidermal growth factor receptor up-regulates multiple elements of the tissue factor signaling pathway in human glioma cells. Blood 116, 815-818
80. Westermark, B., Magnusson, A., and Heldin, C. H. (1982) Effect of epidermal growth factor on membrane motility and cell locomotion in cultures of human clonal glioma cells. J. Neurosci. Res. 8, 491-507
81. Lee, S., Desai, K. K., Iczkowski, K. A., Newcomer, R. G., Wu, K. J., Zhao, Y. G., Tan, W. W., Roycik, M. D., and Sang, Q. X. (2006) Coordinated peak expression of MMP-26 and TIMP-4 in preinvasive human prostate tumor. Cell Res. 16, 750-758
82. Hernandez-Barrantes, S., Shimura, Y., Soloway, P. D., Sang, Q. A., and Fridman, R. (2001) Differential roles of TIMP-4 and TIMP-2 in pro-MMP-2 activation by MT1-MMP. Biochem. Biophys. Res. Commun. 281, 126-130
83. Niu, G., Wright, K. L., Huang, M., Song, L., Haura, E., Turkson, J., Zhang, S., Wang, T., Sinibaldi, D., Coppola, D., Heller, R., Ellis, L. M., Karras, J., Bromberg, J., Pardoll, D., Jove, R., and Yu, H. (2002) Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis. Oncogene 21, 2000-2008
84. Hu, B., Guo, P., Bar-Joseph, I., Imanishi, Y., Jarzynka, M. J., Bogler, O., Mikkelsen, T., Hirose, T., Nishikawa, R., and Cheng, S. Y. (2007) Neuropilin-1 promotes human glioma progression through potentiating the activity of the HGF/SF autocrine pathway. Oncogene 26, 5577-5586
85. Bernhardtsen, T., Laursen, H., Bojsen-Moller, M., and Gjerris, F. (2003) Sub-classification of low-grade cerebellar astrocytoma: is it clinically meaningful? Child's Nerv. Syst. 19, 729-735
86. Tanaka, K., Hiraiwa, N., Hashimoto, H., Yamazaki, Y., and Kusakabe, M. (2004) Tenascin-C regulates angiogenesis in tumor through the regulation of vascular endothelial growth factor expression. Int. J. Cancer 108, 31-40
87. Sarkar, S., Nuttall, R. K., Liu, S., Edwards, D. R., and Yong, V. W. (2006) Tenascin-C stimulates glioma cell invasion through matrix metalloproteinase-12. Cancer Research 66, 11771-11780
88. P S Gaitonde, R. M. J., R S Dastur, S N Bhagwati, J J Nadkarni (2005) EPIDERMAL GROWTH FACTOR RECEPTOR AND TENASCIN EXPRESSION IN ASTROCYTIC GLIOMAS. Ann. Neurosci. 12
89. Berx, G., and van Roy, F. (2009) Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb. Perspect. Biol. 1, a003129
90. Philippova, M., Banfi, A., Ivanov, D., Gianni-Barrera, R., Allenspach, R., Erne, P., and Resink, T. (2006) Atypical GPI-anchored T-cadherin stimulates angiogenesis in vitro and in vivo. Arterioscler. Thromb. Vasc. Biol. 26, 2222-2230
91. Autiero, M., Waltenberger, J., Communi, D., Kranz, A., Moons, L., Lambrechts, D., Kroll, J., Plaisance, S., De Mol, M., Bono, F., Kliche, S., Fellbrich, G., Ballmer-Hofer, K., Maglione, D., Mayr-Beyrle, U., Dewerchin, M., Dombrowski, S., Stanimirovic, D., Van Hummelen, P., Dehio, C., Hicklin, D. J., Persico, G., Herbert, J. M., Communi, D., Shibuya, M., Collen, D., Conway, E. M., and Carmeliet, P. (2003) Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat. Med. 9, 936-943
92. Levicar, N., Strojnik, T., Kos, J., Dewey, R. A., Pilkington, G. J., and Lah, T. T. (2002) Lysosomal enzymes, cathepsins in brain tumour invasion. J. Neurooncol. 58, 21-32
93. Ishidoh, K., and Kominami, E. (1995) Procathepsin L degrades extracellular matrix proteins in the presence of glycosaminoglycans in vitro. Biochem. Biophys. Res. Commun. 217, 624-631
94. Somanna, A., Mundodi, V., and Gedamu, L. (2002) Functional analysis of cathepsin B-like cysteine proteases from Leishmania donovani complex. Evidence for the activation of latent transforming growth factor beta. J. Biol. Chem. 277, 25305-25312
95. Sawaya, R. E., Yamamoto, M., Gokaslan, Z. L., Wang, S. W., Mohanam, S., Fuller, G. N., McCutcheon, I. E., Stetler-Stevenson, W. G., Nicolson, G. L., and Rao, J. S. (1996) Expression and localization of 72 kDa type IV collagenase (MMP-2) in human malignant gliomas in vivo. Clin. Exp. Metastasis 14, 35-42
96. Pedron, S., Becka, E., and Harley, B. A. (2013) Regulation of glioma cell phenotype in 3D matrices by hyaluronic acid. Biomaterials
97. Merzak, A., McCrea, S., Koocheckpour, S., and Pilkington, G. J. (1994) Control of human glioma cell growth, migration and invasion in vitro by transforming growth factor beta 1. Br. J. Cancer 70, 199-203
98. Kasza, A., Kowanetz, M., Poslednik, K., Witek, B., Kordula, T., and Koj, A. (2001) Epidermal growth factor and pro-inflammatory cytokines regulate the expression of components of plasminogen activation system in U373-MG astrocytoma cells. Cytokine 16, 187-190
99. Paugh, B. S., Paugh, S. W., Bryan, L., Kapitonov, D., Wilczynska, K. M., Gopalan, S. M., Rokita, H., Milstien, S., Spiegel, S., and Kordula, T. (2008) EGF regulates plasminogen activator inhibitor-1 (PAI-1) by a pathway involving c-Src, PKCdelta, and sphingosine kinase 1 in glioblastoma cells. FASEB J.22, 455-465
100. Teramoto, H., Castellone, M. D., Malek, R. L., Letwin, N., Frank, B., Gutkind, J. S., and Lee, N. H. (2005) Autocrine activation of an osteopontin-CD44-Rac pathway enhances invasion and transformation by H-RasV12. Oncogene 24, 489-501
101. Sun, B. S., Dong, Q. Z., Ye, Q. H., Sun, H. J., Jia, H. L., Zhu, X. Q., Liu, D. Y., Chen, J., Xue, Q., Zhou, H. J., Ren, N., and Qin, L. X. (2008) Lentiviral-mediated miRNA against osteopontin suppresses tumor growth and metastasis of human hepatocellular carcinoma. Hepatology 48, 1834-1842
102. Sreekanthreddy, P., Srinivasan, H., Kumar, D. M., Nijaguna, M. B., Sridevi, S., Vrinda, M., Arivazhagan, A., Balasubramaniam, A., Hegde, A. S., Chandramouli, B. A., Santosh, V., Rao, M. R., Kondaiah, P., and Somasundaram, K. (2010) Identification of potential serum biomarkers of glioblastoma: serum osteopontin levels correlate with poor prognosis. Cancer Epidemiol.Biomarkers Prev. 19, 1409-1422
103. Rappl, A., Piontek, G., and Schlegel, J. (2008) EGFR-dependent migration of glial cells is mediated by reorganisation of N-cadherin. J. Cell Sci. 121, 4089-4097
104. Kyriakakis, E., Maslova, K., Philippova, M., Pfaff, D., Joshi, M. B., Buechner, S. A., Erne, P., and Resink, T. J. (2012) T-Cadherin is an auxiliary negative regulator of EGFR pathway activity in cutaneous squamous cell carcinoma: impact on cell motility. J. Invest. Dermatol. 132, 2275-2285
105. Huang, Z. Y., Wu, Y., Hedrick, N., and Gutmann, D. H. (2003) T-cadherinmediated cell growth regulation involves G2 phase arrest and requires p21(CIP1/WAF1) expression. Mol. Cell. Biol. 23, 566-578
106. Hormigo, A., Gu, B., Karimi, S., Riedel, E., Panageas, K. S., Edgar, M. A., Tanwar, M. K., Rao, J. S., Fleisher, M., DeAngelis, L. M., and Holland, E. C. (2006) YKL-40 and matrix metalloproteinase-9 as potential serum biomarkers for patients with high-grade gliomas. Clin. Cancer Res. 12, 5698-5704
107. Brennan, C., Momota, H., Hambardzumyan, D., Ozawa, T., Tandon, A., Pedraza, A., and Holland, E. (2009) Glioblastoma subclasses can be defined by activity among signal transduction pathways and associated genomic alterations. PloS One 4, e7752
108. Khan, E. M., Heidinger, J. M., Levy, M., Lisanti, M. P., Ravid, T., and Goldkorn, T. (2006) Epidermal growth factor receptor exposed to oxidative stress undergoes Src- and caveolin-1-dependent perinuclear trafficking. J. Biol, Chem. 281, 14486-14493
109. Nitta, M., Kozono, D., Kennedy, R., Stommel, J., Ng, K., Zinn, P. O., Kushwaha, D., Kesari, S., Inda, M. D., Wykosky, J., Furnari, F., Hoadley, K. A., Chin, L., DePinho, R. A., Cavenee, W. K., D'Andrea, A., and Chen, C. C. (2010) Targeting EGFR induced oxidative stress by PARP1 inhibition in glioblastoma therapy. PloS One 5, e10767
110. Cao, J., Schulte, J., Knight, A., Leslie, N. R., Zagozdzon, A., Bronson, R., Manevich, Y., Beeson, C., and Neumann, C. A. (2009) Prdx1 inhibits tumorigenesis via regulating PTEN/AKT activity. EMBO J. 28, 1505-1517
111. Valentin, F., Bueb, J. L., Kieffer, P., Tschirhart, E., and Atkinson, J. (2005) Oxidative stress activates MMP-2 in cultured human coronary smooth muscle cells. Fundam. Clin. Pharmacol. 19, 661-667
112. DeNicola, G. M., Karreth, F. A., Humpton, T. J., Gopinathan, A., Wei, C., Frese, K., Mangal, D., Yu, K. H., Yeo, C. J., Calhoun, E. S., Scrimieri, F., Winter, J. M., Hruban, R. H., Iacobuzio-Donahue, C., Kern, S. E., Blair, I. A., and Tuveson, D. A. (2011) Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 475, 106-109