Molecular Mechanisms of Glioma Cell Migration and Invasion (original) (raw)
References
Graham CH, Connelly I, MacDougall JR, Kerbel RS, Stetler-Stevenson WG, Lala PK: Resistance of malignant trophoblast cells to both the anti-proliferative and antiinvasive effects of transforming growth factor-beta. Exp Cell Res 214: 93–99, 1994 Google Scholar
Hynes RO, Lander, AD: Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68: 303–322, 1992 Google Scholar
Gumbiner BM: Epithelial morphogenesis. Cell 69: 385–387, 1992 Google Scholar
Alattia JR, Tong KI, Takeichi M, Ikura M: Cadherins. Methods Mol Biol 172: 199–210, 2002 Google Scholar
Stanley JR: Autoantibodies against adhesion molecules and structures in blistering skin diseases. J Exp Med 181: 1–4, 1995 Google Scholar
Anderson DC, Springer TA: Leukocyte adhesion defi-ciency: an inherited defect in the Mac-1, LFA-1, and p 150,95 glycoproteins. Annu Rev Med 38: 175–194, 1987 Google Scholar
Etzioni A, Frydma M, Pollack S, Avidor I, Phillips ML, Paulson JC, Gershoni-Baruch R: Brief report: recurrent severe infections caused by a novel leukocyte adhesion deficiency. N Engl J Med 327: 1789–1792, 1992 Google Scholar
Clezardin P: Recent insights into the role of integrins in cancer metastasis. Cell Mol Life Sci 54: 541–548, 1998 Google Scholar
Rutka JT, Apodaca G, Stern R, Rosenblum M: The extracellular matrix of the central and peripheral nervous systems: structure and function. J Neurosurg 69: 155–170, 1988 Google Scholar
Giese A, Rief MD, Loo MA, Berens ME: Determinants of human astrocytoma migration. Cancer Res 54: 3897–3904, 1994 Google Scholar
Ohnishi T, Arita N, Hiraga. S, Taki T, Izumoto S, Fukushima Y, Hayakawa T: Fibronectin-medirated cell migration promotes glioma cell invasion through chemokinetic activity. Clin Exp Metastasis 15: 538–546, 1997 Google Scholar
Berens ME, Rief MD, Loo MA, Giese A: The role of extracellular matrix in human astrocytoma migration and proliferation studied in a microliter scale assay. Clin Exp Metastasis 12: 405–415, 1994 Google Scholar
Tysnes BB, Larser LF, Ness GO, Mahesparan R, Edvardsen K, Garcia-Cabrera I, Bjerkvig R: Stimulation of glioma-cell migration by laminin and inhibition by antialpha3 and anti-betal integrin antibodies. Int J Cancer 67: 777–784, 1996 Google Scholar
Giese A, Loo MA, Norman SA, Treasurywala S, Berens ME: Contrasting migratory response of astrocytoma cells to tenascin mediated by different integrins. J Cell Sci 109(Pt 8): 2161–2168, 1996 Google Scholar
Kaczarek E, Zapf S, Bouterfa H, Tonn JC, Westphal M, Giese A: Dissecting glioma invasion: interrelation of adhesion, migration and intercellular contacts determine the invasive phenotype. Int J Dev Neurosci 17: 625–641, 1999 Google Scholar
Mahesparan R, Tysnes BB, Read TA, Enger PO, Bjerkvig R, Lund-Johansen M: Extracellular matrix-induced cell migration from glioblastoma biopsy specimens in vitro. Acta Neuropathol (Berl) 97: 231–239, 1999 Google Scholar
Leins A, Riva P, Lindstedt R, Davidoff MS, Mehraei P, Weis S: Expression of tenascin-C in various human brain tumors and its relevance for survival in patients with astrocytoma. Cancer 98: 2430–2439, 2003 Google Scholar
Zagzag D, Friedlander DR, Miller DC, Dosik J, Cangiarella J, Kostianovsky M, Cohen H, Grumet M, Greco MA: Tenascin expression in astrocytomas correlates with angiogenesis. Cancer Res 55: 907–914, 1995 Google Scholar
Zagzag D, Friedlander DR, Dosik J, Chikramane S, Chan W, Greco MA, Allen JC, Dorovini-Zis K, Grumet M: Tenascin-C expression by angiogenic vessels in human astrocytomas and by human brain endothelial cells in vitro. Cancer Res, 56: 182–189, 1996 Google Scholar
Kostianovsky M, Greco MA, Cangiarella J, Zagzag D: Tenascin-C expression in ultrastructurally defined angiogenic and vasculogenic lesions. Ultrastruct Pathol 21: 537–544, 1997 Google Scholar
Zagzag D, Capo V: Angiogenesis in the central nervous system: a role for vascular endothelial growth factor/ vascular permeability factor and tenascin-C. Common molecular effectors in cerebral neoplastic, and non-neoplastic ‘angiogenic diseases’. Histol Histopathol 17: 301–321, 2002 Google Scholar
Plopper GE, McNamee HP, Dike LE, Bojanowski K, Ingber DE: Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol Biol Cell 6: 1349–1365, 1995 Google Scholar
Guan JL, Shalloway D: Regulation of focal adhesionassociated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 358: 690–692, 1992 Google Scholar
Mariani L, Beaudry C, McDonough WS, Hoelzinger DB, Demuth T, Ross KR, Berens T, Coons SW, Watts G, Trent JM, Wei JS, Giese A, Berens ME: Glioma cell motility is associated with reduced transcription of proapoptotic and proliferation genes: a cDNA microarray analysis. J Neurooncol 53: 161–176, 2001 Google Scholar
Mahesparan R, Read TA, Lund-Johansen M, Skaftnesmo, KO, Bjerkvig R, Engebraaten O: Expression of extracellular matrix components in a highly infiltrative in vivo glioma model. Acta Neuropathol (Berl) 105: 49–57, 2003 Google Scholar
Bigner DD, Brown M, Coleman RE, Friedman, AH, Friedman HS, McLendo RE, Bigner SH, Zhao XG, Wikstrand CJ, Pegram, CN, et al.: Phase I studies of treatment of malignant gliomas and neoplastic meningitis with 131I-radiolabeled monoclonal antibodies anti-tenascin 81C6 and anti-chondroitin proteoglycan sulfate Mel-14 F (ab')2– a preliminary report. J Neurooncol 24: 109–122, 1995 Google Scholar
Kurpad SN, Zhao XG, Wikstrand CJ, Batra SK, McLendon RE, Bigner DD. Tumor antigens in astrocyti: gliomas. Glia 15: 244–256, 1995 Google Scholar
Reardon DA, Akabani G, Coleman RE, Friedman AH, Friedman HS, Herndon JE, 2nd, Cokgor I, McLendon RE, Pegram CN, Provenzale JM, Quinn JA, Rich JN, Regalado LV, Sampson JH, Shafman TD, Wikstrand CJ, Wong TZ, Zhao XG, Zalutsky MR, Bigner DD: 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: 1389–1397, 2002 Google Scholar
Goetz C, Riva P, Poepperl G, Gildehaus FJ, Hischa A, Tatsch K, Reulen HJ: Locoregional radioimmunotherapy in selected patients with malignant glioma: experiences, side effects and survival times. J Neurooncol 62: 321–328, 2003 Google Scholar
Lamszus K, Kunkel P, Westkphal M: Invasion as limitation to anti-angiogenic glioma therapy. Acta Neurochir Suppl 88: 169–177, 2003 Google Scholar
Rempel SA, Golembieski WA, Ge S, Lemke N, Elisevich K, Mikkelsen T Gutierrez JA: SPARC: a signal of astrocytic neoplastic transformation and reactive response, in human primary and xenograft gliomas. J Neuropathol Exp Neurol 57: 1112–1121, 1998 Google Scholar
Golembieski WA, Ge S, Nelson K, Mikkelsen T, Rempel SA: Increased SPARC expression promotes U87 glioblastoma invasion in vitro. Int J Dev Neurosci 17: 463–472, 1999 Google Scholar
Vadlamuri SV, Media J, Sankey SS, Nakeff A, Divine G, Rempel SA: SPARC affects glioma cell growth differently when grown on brain ECM proteins in vitro under standard versus reduced-serum stress conditions. Neurooncol 5: 244–254, 2003 Google Scholar
Golembieski WA, Rempel SA: cDNA array analysis of SPARC–modulated changes in glioma gene expression. J Neurooncol 60: 213–226, 2002 Google Scholar
Burridge K, Chrzanowska-Wodnicka M: Focal adhesions, contractility and signaling. Annu Rev Cell Dev Biol 12: 463–518, 1996 Google Scholar
Zamir E, Katz M, Posen Y, Erez N, Yamada KM, Katz BZ, Lin S, Lin DC, Bershadsky A, Kam Z, Geiger B: Dynamics and segregation of cell-matrix adhesions in cultures fibroblasts. Nat Cell Biol 2: 191–196, 2000 Google Scholar
Friedl P, Wolf K: Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3: 362–374, 2003 Google Scholar
Kinbara K, Goldfinger LE, Hansen M, Chou FL, Ginsberg MH: Ras GTPases: integrins' friends or foes? Nat Rev Mol Cell Biol 4: 767–776, 2003 Google Scholar
Cukierman E, Pankov R, Stevens DR, Yamada KM: Taking cell-matrix adhesions to the third dimension. Science 294: 1708–1712, 2001 Google Scholar
Rabinovitz I, Mercurio AM: The integrin alpha6beta4 functions in carcinoma cell migration on laminin-1 by mediating the formation and stabilization of actin-containing motility structures. J Cell Biol 139: 1873–1884, 1997 Google Scholar
Leavesley DI, Ferguson GD, Wayner EA, Cheresh DA: Requirement of the integrin beta 3 subunit for carcinoma cell spreading or migration on vitronectin and fibrinogen. J Cell Bio 117: 1101–1107, 1992 Google Scholar
Maaser K, Wolf K, Klein CE, Niggemann B, Zanker KS, Brocker EB, Friedl P: Functional hierarchy of simultaneously expressed adhesion receptors integrin alpha2beta but not CD44 mediates MV3 melanoma cell migration and matrix reorganization within three-dimensional hyaluronan containing collagen matrices. Mol Biol Cell 10: 3067–3079, 1999 Google Scholar
Paulus W, Baur I, Beutler AS, Reeves SA: Diffuse brain invasion of glioma cells requires beta 1 integrins. Lab Invest 75: 819–826, 1996 Google Scholar
Tonn JC, Wunderlich S, Kerkau S, Klein CE, Roosen K: Invasive behaviour of human gliomas is mediated by interindividually different integrin patterns. Anticancer Res 18: 2599–2605, 1998 Google Scholar
Rooprai HK, Vanmeter T, Panou C, Schnull S, Trillo-Pazos G, Davies D, Pilkinton GJ: The role of integrin receptors in aspects of glioma invasion in vitro. Int J Dev Neurosci 17: 613–623, 1999 Google Scholar
Deryugina EI, Bourdon MA: Tenascin mediates human glioma cell migration and modulates cell migration on fibronectin. J Cell Sci 109 ( Pt 3): 643–652, 1996 Google Scholar
Platten M, Wick W, Wild-Bode C, Aulwurm S, Dichgans J, Wellr M: Transforming growth factors beta(1) (TGFbeta( 1)) and TGF-beta(2) promote glioma cell migration via Up-regulation of alpha(V)beta(3) integrin expression. Biochem Biophys Res Commun 268: 607–611, 2000 Google Scholar
Belot N, Rorive S, Doye I Lefranc F, Bruyneel E, Dedecker R, Micik S, Brotchi J, Decaestecker C, Salmon I, Kiss R, Camby I: Molecular characterization of cell substratum attachments in human glial tumors relates to prognostic features. Glia 36: 375–390, 2001 Google Scholar
Taga T, Suzuki A, Gonzalez-Gomez I, Gilles FH, Stins M, Shimada H, Barsky L, Weinberg KI, Laug WE: alpha v-Integrin antagonist EMD 121974 induces apoptosis in brain tumor cells growing on vitronectin and tenascin. Int J Cancer 98: 690–697, 2002 Google Scholar
MacDonald TJ, Taga T, Shimada H, Tabrizi, P, Zlokovic BV, Cheresh DA, Laug WE: Preferential susceptibility of brain tumors to the antiangiogenic effects of an alpha(v) integrin antagonist. Neurosurgery 48: 151–157 2001 Google Scholar
Phase I Study of Cilengitide (EMD 121974) in Children With Refractory Primary Brain Tumors. Pediatric Brain Tumor Consortium, 2003.
Phase I Study of EMD 121974 in Patients With Advanced Solid Tumors. University of Colorado Cancer Center at University of Colorado Health Sciences Center, 2003
Frisch SM, Francis H: Disruption epithelial cell-matrix interactions induces apoptosis. J Cell Biol 124: 619–626, 1994 Google Scholar
Zhang Z, Vuori K, Reed JC, Ruoslahti E: The alpha 5 beta 1 integrin supports survival of cells on fibronectin and up-regulates Bcl-2 expression. Proc Natl Acad Sci USA 92: 6161–6165, 1995 Google Scholar
Nollet F, Kools P, van Roy F: Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 299: 551–572, 2000 Google Scholar
Gumbiner BM: Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84: 345–357, 1996 Google Scholar
Perez-Moreno M, Jamora, C, Fuchs E: Sticky business: orchestrating cellular signals at adherens junctions. Cell 112: 535–548, 2003 Google Scholar
Vasioukhin V, Bauer C, Yin M, Fuchs E: Directed actin polymerization is the driving force for epithelial cell–cell adhesion. Cell 100: 209–219, 2000 Google Scholar
Bremnes RM, Veve R, Hirsch FR, Franklin WA: The Ecadherin cell-cell adhesion complex and lung cancer invasion, metastasis, and prognosis. Lung Cancer 36: 115–124, 2002 Google Scholar
Chen WC, Obrink B: Cell–cell contacts mediated by Ecadherin (uvomorulin) restrict invasive behavior of L-cells. J Cell Biol 114: 319–327, 1991 Google Scholar
Vleminckx K, Vakaet L Jr, Mareel M, Fiers W, van Roy F: Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66: 107–119, 1991 Google Scholar
Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronsor SA: Exogenous expression of N-cadherin in breast-gander cells induces cell migration, invasion, and metastasis. J Cell Biol 148: 779–790, 2000 Google Scholar
Shinoura N, Paradies NE, Warnick RE, Chen H, Larson JJ, Tew JJ, Simon M, Lynch RA, Kanai Y, Hirohashi S, et al: Expression of N-cadhri and alpha-catenin in astrocytomas and glioblastomas. Br J Cancer 72: 627–633, 1995 Google Scholar
Kotelevets L, van Hengel J, Bruyneel E, Mareel M, van Roy, F, Chastre E: The lipid phosphatase activity of PTEN is critical for stabilizing intercellular junctions and reverting invasiveness. J Cell Biol 155: 1129–1135, 2001 Google Scholar
Utsuki S, Sato Y, Oka H, Tsuchiya B, Suzuki S, Fujii K: Relationship between the expression of E-, N-cadherins and beta-catenin and tumor grade in astrocytomas. J Neurooncol 57: 187–192, 2002 Google Scholar
Perego C, Vanoni C, Massari S, Longhi R, Pietrini G: Mammalian LIN-7. PDZ proteins associate with betacatenin at the cell–cell junctions of epithelia and neurons. Embo J 19: 3978–3989, 2000 Google Scholar
Gumbiner BM: Signal transduction of beta-catenin. Curr Opin Cell Biol 7: 634–640, 1995 Google Scholar
Hsueh YP, Wang TF, Yang FC, Sheng M: Nuclear translocation and transcription regulation by the membrane-associated guanylate kinase CASK/LIN-2. Nature 404: 298–302, 2000 Google Scholar
Merzak A, Koocheckpour S, Pilkington GJ: CD44 mediates human glioma cell adhesion and invasion in vitro. Cancer Res 54: 3988–3992, 1994 Google Scholar
Hikawa T, Mori T, Abe T, Hori S: The ability in adhesion and invasion of drug-resistant human glioma cells. J Exp Clin Cancer Res 19: 357–362, 2000 Google Scholar
Teicher BA, Herman TS, Holden SA, Wang YY, Pfeffer MR, Crawford JW, Frei E 3rd: Tumor'resistance to alkylating agents conferred by mechanisms operative only in vivo. Science 247: 1457–1461, 1990 Google Scholar
Frankel A, Buckman R, Kerbel RS: Abrogation of taxolinduced G2-M arrest apoptosis in human ovarian cancer cells grown as multicellular tumor spheroids. Cancer Res 57: 2388–2393, 1997 Google Scholar
Damiano JS, Cress AE, Hazlehurst LA, Shtil AA, and Dalton WS: Cell adhesion mediated drug resistance (CAM-DR): role of integrins and resistance to apoptosis in human myeloma cell lines. Blood 93: 1658–1667, 1999 Google Scholar
de la Fuente MT, Casanova B, Garcia-Gila M, Silva A Garcia-Parda A: Fibronectin interaction with atpha4beta1 integrin prevents apoptosis in B cell chronic lymphocytic leukemia: correlation with Bcl-2 and Bax. Leukemia 13 266–274, 1999 Google Scholar
Hazlehurst LA, Valkov N, Wisner L, Storey JA, Boulware D, Sullivan DM, Dalton WS: Reduction in drug-induce DNA double-strand breaks associated with beta1 integrinmediated adhesion correlates with drug resistance in U937 cells. Blood 98: 1897–1903, 2001 Google Scholar
Bruzzone R, White TW, Paul DL: Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238: 1–27, 1996 Google Scholar
Goodenough DA, Goliger JA, Paul DL: Connexins, connexons, and intercellular communication. Annu Rev Biochem 65: 475–502, 1996 Google Scholar
Ruch RJ: The role of gap junctional intercellular communication in neoplasia. Ann Clin Lab Sci 24: 216–231, 1994 Google Scholar
Dermietzel R, Spray DC: Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 16: 186–192, 1993 Google Scholar
McDonough WS, Johansson A, Jorfee H, Giese A, Berens ME: Gap junction intercellular communication in gliomas is inversely related to cell motility. Int J Dev Neurosci 17: 601–611, 1999 Google Scholar
Soroceanu L, Manning TJ Jr, Sontheimer H: Reduced expression of connexin-43 and functional gap junction coupling in human gliomas. Glia 33: 107–117, 2001 Google Scholar
Lin JH, Takano T, Cotrina ML, Arcuino G, Kang J, Liu S, Gao Q, Jiang L, Li F, Lichtenberg-Frate H, Haubrich S Willecke K, Goldman SA, Nedergaard M: Connexin 43 enhances the adhesivity and mediates the invasion of malignant glioma cells. J Neurosci 22: 4302–4311, 2002 Google Scholar
Huang RP, Fan Y, Hossain MZ, Peng A, Zeng ZL, Boynton AL: Reversion of the neoplastic phenotype of human glioblastoma cells by connexin 43 (cx43). Cancer Res 58: 5089–5096, 1998 Google Scholar
Huang RP, Hossain MZ, Sehgal A, Boynton AL: Reduced connexin43 expression in high-grade human brain glioma cells. J Surg Oncol 70: 21–74, 1999 Google Scholar
Huang R, Lin Y, Wang CC, Gano J, Lin B, Shi Q, Boynton A, Burke J, Huang RP: Connexin 43 suppresses human glioblastoma cell growth by down-regulation of monocyte chemotactic protein 1, as discovered using protein array technology. Cancer Res 62: 2806–2812, 2002 Google Scholar
Huang RP, Hossain MZ, Huang R, Gano J, Fan Y, Boynton AL: Connexin 43(cx43) enhances chemotherapyinduced apoptosis in human glioblastoma cells. Int J Cancer 92: 130–138, 2001 Google Scholar
Tonn JC, Goldbrunner R: Mechanisms of glioma cell invasion. Acta Neurochir Suppl 88: 163–167, 2003 Google Scholar
Tonn JC, Kerkau S, Hanke A, Bouterfa H, Mueller JG, Wagner S, Vince GH, Roosen K: Effect of synthetic matrix-metalloproteinase inhibitors on invasive capacity and proliferation of human malignant gliomas in vitro. Int J Cancer 80: 764–772, 1999 Google Scholar
Demchik LL, Sameni M, Nelson K, Mikkelsen T, Sloane BF: Cathepsin B and glioma invasion. Int J Dev Neurosci 17: 483–494, 1999 Google Scholar
Rempel SA, Rosenblum ML, Mikkelsen T, Yan. PS, Ellis KD, Golembieski WA, Sameni M, Rozhin J, Ziegler G, Sloane BF: Cathepsin B expression and localization in glioma progression and invasion. Cancer Res 54: 6027–6031, 1994 Google Scholar
Sivaparvathi M, Sawaya R, Wang SW, Rayford A, Yamamoto M, Liotta LA, Nicolson GL, Rao JS: Overexpression and localization of cathepsin B during the progression of human gliomas. Clin Exp Metastasis 13: 49–56, 1995 Google Scholar
Mohanam S, Jasti SL, Kondraganti SR, Chandrasekar N, Lakka SS, Kin Y, Fuller GN, Yung AW, Kyritsis AP, Dinh DH; Olivero WC, Gujrati M, Ali-Osman F, Rao JS: Down-regulation of cathepsin B expression impairs the invasive and tumorigenic potential of human glioblastoma cells. Oncogene 20: 3665–3673, 2001 Google Scholar
Levicar N, Dewey RA, Daley E, Bates TE, Davies D, Kos J, Pilkington GJ, and Lah TT: Selective suppression of cathepsin L by antisense cDNA impairs human braintumor cell invasion in vitro and promotes apoptosis. Cancer Gene Then 10: 141–151, 2003 Google Scholar
Etienne-Manneville S, Hall A: Rho GTPases in cell biology. Nature 420; 629–635, 2002 Google Scholar
Ridley AJ, Hall A: The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389–399, 1992 Google Scholar
Clark EA, Golub TR, Lander ES, Hynes RO: Genomic analysis of metastasis reveals an essential role for RhoC. Nature, 406: 532–535, 2000 Google Scholar
Forget MA, Desrosiers RR, Del M, Moumdjian R, Shedid D, Berthelet F, Beliveau R: The expression of rho proteins decreases with human brain tumor progression: potential tumor markers. Clin Exp Metastasis 19: 9–15, 2002 Google Scholar
Ding Q, Stewart J Jr, Prince CW, Chang PL, Trikha M, Han X, Grammer JR, Gladson CL: Promotion of malignant astrocytoma cell migration by osteopontin expressed in the normal brain: differences in integrin signaling during cell adhesion to osteopontin versus vitronectin. Cancer Res 62: 5336–5343, 2002 Google Scholar
Senger DL, Tudan C, Guiot MC, Mazzoni IE, Molenkamp G, LeBlanc R, Antel J, Olivier A, Snipes GJ, Kaplan DR: Suppression of Rac activity induces apoptosis of human glioma cells but not normal human astrocytes. Cancer Res, 62: 2131–2140, 2002 Google Scholar
Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A: The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell, 70: 401–410, 1992 Google Scholar
Nobes CD, Lauritzen I, Mattei MG, Paris S, Hall A, Chardin P: A new mem be of the Rho family, Rnd1 promotes disassembly of actin filament structures and loss of cell adhesion. J Cell Biol 141: 187–197, 1998 Google Scholar
Nobes CD, Hall A: Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81: 53–62, 1995 Google Scholar
Michiels F, Habets GG, Stam JC, van der Kammen RA, Collard JG: A role for Rac in Tiam1-induced membrane ruffling and invasion. Nature 375: 338–340, 1995 Google Scholar
Van Aelst L, D'souza-Schorey C: Rho GTPases and signaling networks. Genes Dev 11: 2295–2322, 1997 Google Scholar
Cary LA, Guan JL: Focal adhesion kinase in integrinmediated signaling. Front: Biosci, 4: D102–113, 1999 Google Scholar
Hauck CR, Hsia DA, Schlaepfer DD: The focal adhesion kinase – a regulator of cell migration and invasion. IUBMB Life 53: 115–119, 2002 Google Scholar
Obara S, Nakata M, Takeshima H, Kuratsu J, Maruyama I, Kitajima I: Inhibition of migration of human glioblastoma cells by cerivastatin in association with focal adhesion kinase (FAK). Cancer Lett 185: 153–161, 2002 Google Scholar
Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, Kornberg L, Liu E T, Cance W G: Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res 55: 2752–2755, 1995 Google Scholar
Jones G, Machado J Jr, Merlo A: Loss of focal adhesion kinase (FAK) inhibits epidermal growth factor receptordependent migration and induces aggregation of nh(2)-terminal FAK in the nuclei of apoptotic glioblastoma cells. Cancer Res, 61: 4978–4981, 2001 Google Scholar
Zagzag D, Friedlander DR, Margolis B, Grumet M, Semenza GL, Zhong H, Simons JW, Holash. J, Wiegand, SJ, Yancopoulos GD: Molecular events implicated in brain tumor angiogenesis and invasion. Pediatr Neurosurg 33: 49–55, 2000 Google Scholar
Menegon A, Burgaya F, Baudot P, Dunlap DD, Girault JA, Valtorta F: FAK+ and PYK2/CAKbeta, two related tyrosine kinases highly expressed in the central nervous system: similarities and differences in the expression pattern. Eur J Neurosci 11: 3777–3788, 1999 Google Scholar
Lev S, Moreno H, Martinez R, Canoll P, Peles E, Musacchio JM, Plowman GD, Rudy B, Schlessinger J: Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376: 737–745, 1995 Google Scholar
Frisch SM, Vuori K, Ruoslahti E, Chan-Hui PY: Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 134: 793–799, 1996 Google Scholar
Xiong W, Parsons JT: Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally relatedto focal adhesion kinase. J Cell Biol 139: 529–539, 1997 Google Scholar
Lipinski CA, Tran NL, Bay C, Kloss J, McDonough WS, Beaudry C, Berens ME, Loftus JC: Differential role of proline-rich tyrosine kinase 2 and focal adhesion kinase in determining glioblastoma migration and proliferation. Mol Cancer Res 1: 323–332, 2003 Google Scholar
Nutt CL, Mani DR, Betensky RA, Tamayo P, Cairncross JG, Ladd C, Pohl U, Hartmann C, McLaughlin ME, Batchelor TT, Black PM, von Deimling A, Pomero SL, Goluh TR Louis DN: Gene expression-based classification of malignant gliomas correlates better with survival than histological classification. Cancer Res 63: 1602–1607, 2003 Google Scholar
Sallinen SL, Sallinen PK, Haapasalo HK, Helin HJ, Helen, PT, Schraml P, Kallioniemi OP, Kononen J: Identification of differentially expressed genes in human gliomas by DNA microarray and tissue chip techniques. Cancer Res 60: 6617–6622, 2000 Google Scholar
Mischel PS, Shai R, Shi T, Horvath S, Lu KV, Choe G, Seligson D, Kremen TJ, Palotie A, Liau LM, Cloughesy TF, Nelson SF: Identification of molecular subtypes of glioblastoma by gene expression profiling. Oncogene 22: 2361–7373, 2003 Google Scholar
Studler JM, Glowinski J, Levi-Strauss M: An abundant mRNA of the embryonic brain persists at a high level in cerebellum, hippocampus and olfactory bulb during adulthood. Eur J Neurosci 5: 614–623, 1993 Google Scholar
Mariani L, McDonough WS, Hoelzinger DB, Beaudry C, Kaczmarek E, Coons SW, Giese A, Moghaddam M, Seiler RW, Berens ME: Identification and validation of P311 as a glioblastoma invasion gene using laser capture microdissection. Cancer Res, 61: 4190–4196, 2001 Google Scholar
Kissil JL, Deiss LP, Bayewitch M, Raveh T, Khaspekov G, Kimchi A: Isolation of DAP3, a novel mediator of interferon-gamma-induced cell death. J Biol Chem 270: 27932–27936, 1995 Google Scholar
Kissil JL, Cohen O, Raveh T, Kimchi A: Structurefunction analysis of an evolutionary conserved protein, DAP3, which mediates TNF-alpha-and Fas-induced cell death. Embo J 18: 353–362, 1999 Google Scholar
Mariani L, Beaudry C, McDonough WS, Hoelzinger DB, Kaczmarek E, Ponce F, Coons SW, Giese A, Seiler RW, Berens ME: Death associated protein 3 (Dap-3) is overexpressed in invasive glioblastoma cells in vivo and in glioma cell lines with induced motility phenotype in vitro. Clin Cancer Res. 7: 2480–2489, 2001 Google Scholar
Taylor GA, Hudson E, Resau JH, Vande Woude GF: Regulation of P311 expression by Met-hepatocyte growth factor/scatter factor and the ubiquitin/proteasome system. J Biol Chern. 275: 4215–4219, 2000 Google Scholar
Tran NL, McDonough WS, Donohue PJ, Winkles JA, Berens TJ, Ross KR, Hoelzinger DB, Beaudry C, Coons SW, Berens ME: The human Fn14 receptor gene is upregulated in migrating glioma cells in vitro and overexpressed in advanced glial tumors. Am J Pathol 162: 1313–1321, 2003 Google Scholar
Wiley SR, Winkles JA: TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fnl4 receptor. Cytokine Growth Factor Rev 14: 241–249, 2003 Google Scholar
Joy AM, Beaudry CE, Tran NL Ponce FA, Holz DR, Demuth T, Berens ME: Migrating glioma cells activate the PI3-K pathway and display decreased susceptibility to apoptosis. J Cell Sci. 116: 4409–4417, 2003 Google Scholar
Cantley LC, Neel BG: New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase AKT pathway. Proc Natl Acad Sci USA 96: 4240–4245, 1999 Google Scholar
CBTRUS 2002: Statistical Report: Primary Brain Tumorsin the United States, 1995–1999: Central Brain Tumor Registry of the United States, 2002
Matsukado Y, Maccarty CS, Kernohan JW: The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. J Neurosurg 18: 636–644, 1961 Google Scholar
Dandy W: Removal of the right hemisphere for certain tumors with hemiplegia: preliminary report. J Am Med Assoc 90: 823–825, 1928 Google Scholar
Bell E, LJ K: Cerebral hemispherectomy: report of a case ten years after operation. J Neurosurg 6: 285–293, 1949 Google Scholar