Glioma cell migration and invasion as potential target for novel treatment strategies

Translational Neuroscience

Volumn 4, Issue 3, 2013, Pages 314-329

  Naumann, Ulrike ^a   Harter, Patrick N ^b   Rubel, Jennifer ^a   Ilina, Elena ^b   Blank, Anna Eva ^b   Esteban, Hugo Bastida ^a   Mittelbronn, Michel ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

Glioblastoma; Glioma; Invasion; Migration

Indexed keywords

ANTINEOPLASTIC AGENT; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; EPHRIN B2; GUANOSINE TRIPHOSPHATASE; INTEGRIN; LIGAND; MATRIX METALLOPROTEINASE; MICRORNA; MICRORNA 451; NETRIN 1; ROUNDABOUT RECEPTOR; SEMAPHORIN 3A; SLIT PROTEIN; STROMAL CELL DERIVED FACTOR 1; THROMBOPLASTIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ASYMPTOMATIC DISEASE; CANCER CHEMOTHERAPY; CANCER CONTROL; CANCER GRADING; CANCER INFILTRATION; CANCER MODEL; CANCER RADIOTHERAPY; CANCER STEM CELL; CANCER SURGERY; CANCER SURVIVAL; CELL ASSAY; CELL INVASION; CELL MIGRATION; CELL MOTILITY; CLINICAL FEATURE; CYTOSKELETON; EX VIVO STUDY; EXTRACELLULAR MATRIX; GLIOMA; GLIOMA CELL; HISTOPATHOLOGY; HUMAN; IN VITRO STUDY; MOLECULAR BIOLOGY; NEUROLOGIC DISEASE; NEUROSURGERY; NONHUMAN; OVERALL SURVIVAL; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; REVIEW; SURVIVAL TIME; TARGET CELL DESTRUCTION; TRANSGENIC ANIMAL; WOUND HEALING;

EID: 84892976541     PISSN: 20813856     EISSN: 20816936     Source Type: Journal    
DOI: 10.2478/s13380-013-0126-1     Document Type: Review

References (177)

1. Youland R.S., Schomas D.A., Brown P.D., Nwachukwu C., Buckner J. C., Giannini C., et al., Changes in presentation, treatment, and outcomes of adult low-grade gliomas over the past fifty years, Neuro Oncol., 2013, 15, 1102-1110
2. Chang S.M., Parney I.F., Huang W., Anderson F.A. Jr., Asher A.L., Bernstein M., et al., Patterns of care for adults with newly diagnosed malignant glioma, JAMA, 2005, 293: 557-564
3. Fisher J.L., Schwartzbaum J.A., Wrensch M., Berger M.S., Evaluation of epidemiologic evidence for primary adult brain tumor risk factors using evidence-based medicine, Prog. Neurol. Surg., 2006, 19, 54-79
4. Wrensch M., Minn Y., Chew T., Bondy M., Berger M.S., Epidemiology of primary brain tumors: current concepts and review of the literature, Neuro Oncol., 2002, 4, 278-299
5. Ohgaki H., Kim Y.H., Steinbach J.P., Nervous system tumors associated with familial tumor syndromes, Curr. Opin. Neurol., 2010, 23, 583-591
6. Ohgaki H., Kleihues P., Epidemiology and etiology of gliomas, Acta Neuropathol., 2005, 109, 93-108
7. Johnson D.R., O'Neill B.P., Glioblastoma survival in the United States before and during the temozolomide era, J. Neurooncol., 2012, 107, 359-364
8. Ohgaki H., Kleihues P., Population-based studies on incidence, survival rates, and genetic alterations in astrocytic and oligodendroglial gliomas, J. Neuropathol. Exp. Neurol., 2005, 64, 479-489
9. Laperriere N., Zuraw L., Cairncross G., Radiotherapy for newly diagnosed malignant glioma in adults: a systematic review, Radiother. Oncol., 2002, 64, 259-273
10. Claes A., Idema A.J., Wesseling P., Diffuse glioma growth: a guerilla war, Acta Neuropathol., 2007, 114, 443-458
11. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., et al., The 2007 WHO classification of tumours of the central nervous system, Acta Neuropathol., 2007, 114, 97-109
12. Scherer H.J., The forms of growth in gliomas and their practical significance, Brain, 1940, 63, 1-35
13. Giese A., Loo M.A., Tran N., Haskett D., Coons S.W., Berens M.E., Dichotomy of astrocytoma migration and proliferation, Int. J. Cancer, 1996, 67, 275-282
14. Godlewski J., Bronisz A., Nowicki M.O., Chiocca E.A., Lawler S., microRNA-451: a conditional switch controlling glioma cell proliferation and migration, Cell Cycle, 2010, 9, 2742-2748
15. Tan X., Wang S., Yang B., Zhu L., Yin B., Chao T., et al., The CREB-miR-9 negative feedback minicircuitry coordinates the migration and proliferation of glioma cells, PLoS One, 2012, 7, e49570
16. Höring E., Harter P.N., Seznec J., Schittenhelm J., Bühring H.J., Bhattacharyya S., et al., The "go or grow" potential of gliomas is linked to the neuropeptide processing enzyme carboxypeptidase E and mediated by metabolic stress, Acta Neuropathol., 2012, 124, 83-97
17. Farin A., Suzuki S.O., Weiker M., Goldman J.E., Bruce J.N., Canoll P., Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis, Glia, 2006, 53, 799-808
18. Wiranowska M., Rojiani M.V., Extracellular matrix microenvironment in glioma progression, In: Ghosh A. (ed.) Glioma - exploring its biology and practical relevance, InTech, Rijeka, Croatia, 2011
19. Ram R., Lorente G., Nikolich K., Urfer R., Foehr E., Nagavarapu U., Discoidin domain receptor-1a (DDR1a) promotes glioma cell invasion and adhesion in association with matrix metalloproteinase-2, J. Neurooncol., 2006, 76, 239-248
20. Ulrich T.A., de Juan Pardo E.M., Kumar S., The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells, Cancer Res., 2009, 69, 4167-4174
21. Bellail A.C., Hunter S.B., Brat D.J., Tan C., Van Meir E.G., Microregional extracellular matrix heterogeneity in brain modulates glioma cell invasion, Int. J. Biochem. Cell. Biol., 2004, 36, 1046-1069
22. Forsyth P.A., Wong H., Laing T.D., Rewcastle N.B., Morris D.G., Muzik H., et al., Gelatinase-A (MMP-2), gelatinase-B (MMP-9) and membrane type matrix metalloproteinase-1 (MT1-MMP) are involved in different aspects of the pathophysiology of malignant gliomas, Br. J. Cancer, 1999, 79, 1828-1835
23. Wang M., Wang T., Liu S., Yoshida D., Teramoto A., The expression of matrix metalloproteinase-2 and -9 in human gliomas of different pathological grades, Brain Tumor Pathol., 2003, 20, 65-72
24. Deryugina E.I., Bourdon M.A., Luo G.X., Reisfeld R.A., Strongin A., Matrix metalloproteinase-2 activation modulates glioma cell migration, J. Cell. Sci., 1997, 110, 2473-2482
25. VanMeter T.E., Rooprai H.K., Kibble M.M., Fillmore H.L., Broaddus W.C., Pilkington G.J., The role of matrix metalloproteinase genes in glioma invasion: co-dependent and interactive proteolysis, J Neurooncol., 2001, 53, 213-235
26. Rome C., Arsaut J., Taris C., Couillaud F., Loiseau H., MMP-7 (matrilysin) expression in human brain tumors, Mol. Carcinog., 2007, 46, 446-452
27. Wild-Bode C., Weller M., Wick W., Molecular determinants of glioma cell migration and invasion, J. Neurosurg., 2001, 94, 978-984
28. Guo P., Imanishi Y., Cackowski F.C., Jarzynka M.J., Tao H.Q., Nishikawa R., et al., Up-regulation of angiopoietin-2, matrix metalloprotease-2, membrane type 1 metalloprotease, and laminin 5 gamma 2 correlates with the invasiveness of human glioma, Am. J. Pathol., 2005, 166, 877-890
29. Morrison C.J., Butler G.S., Rodriguez D., Overall C.M., Matrix metalloproteinase proteomics: substrates, targets, and therapy, Curr. Opin. Cell. Biol., 2009, 21, 645-653
30. Sato H., Takino T., Coordinate action of membrane-type matrix metalloproteinase-1 (MT1-MMP) and MMP-2 enhances pericellular proteolysis and invasion, Cancer Sci., 2010, 101, 843-847
31. Sameshima T., Nabeshima K., Toole B.P., Yokogami K., Okada Y., Goya T., et al., Expression of emmprin (CD147), a cell surface inducer of matrix metalloproteinases, in normal human brain and gliomas, Int. J. Cancer., 2000, 88, 21-27
32. Sameshima T., Nabeshima K., Toole B.P., Yokogami K., Okada Y., Goya T., et al., Glioma cell extracellular matrix metalloproteinase inducer (EMMPRIN) (CD147) stimulates production of membrane-type matrix metalloproteinases and activated gelatinase A in co-cultures with brain-derived fibroblasts, Cancer Lett., 2000, 157, 177-184
33. Platten M., Wick W., Weller M., Malignant glioma biology: role for TGFbeta in growth, motility, angiogenesis, and immune escape, Microsc. Res. Tech., 2001, 52, 401-410
34. Wick W., Platten M., Weller M., Glioma cell invasion: regulation of metalloproteinase activity by TGF-beta, J. Neurooncol., 2001, 53, 177-185
35. Lettau I., Hattermann K., Held-Feindt J., Brauer R., Sedlacek R., Mentlein R., Matrix metalloproteinase-19 is highly expressed in astroglial tumors and promotes invasion of glioma cells, J. Neuropathol. Exp. Neurol., 2010, 69, 215-223
36. Stojic J., Hagemann C., Haas S., Herbold C., Kühnel S., Gerngras S., et al. Expression of matrix metalloproteinases MMP-1, MMP-11 and MMP-19 is correlated with the WHO-grading of human malignant gliomas, Neurosci. Res., 2008, 60, 40-49
37. Deng Y., Li W., Li Y., Yang H., Xu H., Liang S., et al., Expression of Matrix Metalloproteinase-26 promotes human glioma U251 cell invasion in vitro and in vivo, Oncol. Rep., 2010, 23, 69-78
38. Brauer R., Beck I.M., Roderfeld M., Roeb E., Sedlacek R., Matrix metalloproteinase-19 inhibits growth of endothelial cells by generating angiostatin-like fragments from plasminogen, BMC Biochem., 2011, 12, 38
39. Fukuda H., Mochizuki S., Abe H., Okano H.J., Hara-Miyauchi C., Okano H., et al. Host-derived MMP-13 exhibits a protective role in lung metastasis of melanoma cells by local endostatin production, Br. J. Cancer, 2011, 105, 1615-1624
40. Hamano Y., Zeisberg M., Sugimoto H., Lively J.C., Maeshima Y., Yang C., et al., Physiological levels of tumstatin, a fragment of collagen IV α3 chain, are generated by MMP-9 proteolysis and suppress angiogenesis via αVβ3 integrin, Cancer Cell, 2003, 3, 589-601
41. Nakano A., Tani E., Miyazaki K., Yamamoto Y., Furuyama J., Matrix metallo-proteinases and tissue inhibitors of metalloproteinases in human gliomas, J. Neurosurg., 1995, 83, 298-307
42. Lampert K., Machein U., Machein M.R., Conca W., Peter H.H., Volk B., Expression of matrix metalloproteinases and their tissue inhibitors in human brain tumors, Am. J. Pathol., 1998, 153, 429-437
43. Nakada M., Kita D., Futami K., Yamashita J., Fujimoto N., Sato H., et al., Roles of membrane type 1 matrix metalloproteinase and tissue inhibitor of metalloproteinases 2 in invasion and dissemination of human malignant glioma, J. Neurosurg., 2001, 94, 464-473
44. Wang Z., Juttermann R., Soloway P.D., TIMP-2 is required for efficient activation of proMMP-2 in vivo, J. Biol. Chem., 2000, 275, 26411-26415
45. Lu K.V., Jong K.A., Rajasekaran A.K., Cloughesy T.F., Mischel P.S., Upregulation of tissue inhibitor of metalloproteinases (TIMP)-2 promotes matrix metalloproteinase (MMP)-2 activation and cell invasion in a human glioblastoma cell line, Lab. Invest., 2004, 84, 8-20
46. Surawska H., Ma P.C., Salgia R., The role of ephrins and Eph receptors in cancer, Cytokine Growth Factor Rev., 2004, 15, 419-433
47. Chedotal A., Kerjan G., Moreau-Fauvarque C., The brain within the tumor: new roles for axon guidance molecules in cancers, Cell Death Differ., 2005, 12, 1044-1056
48. Hedgecock E.M., Culotti J.G., Hall D.H., The unc-5, unc-6, and unc- 40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans, Neuron, 1990, 4, 61-85
49. Ishii N., Wadsworth W.G., Stern B.D., Culotti J.G., Hedgecock E.M., UNC- 6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans, Neuron, 1992, 9, 873-881
50. Wadsworth W.G., Bhatt H., Hedgecock E.M., Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans, Neuron, 1996, 16, 35-46
51. Hedgecock E.M., Norris C.R., Netrins evoke mixed reactions in motile cells, Trends Genet., 1997, 13, 251-253
52. Serafini T., Colamarino S.A., Leonardo E.D., Wang H., Beddington R., Skarnes W.C., et al., Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system, Cell, 1996, 87, 1001-1014
53. Harter P.N., Bunz B., Dietz K., Hoffmann K., Meyermann R., Mittelbronn M., Spatio-temporal deleted in colorectal cancer (DCC) and netrin-1 expression in human foetal brain development, Neuropathol. Appl. Neurobiol., 2010, 36, 623-635
54. Meyerhardt J.A., Caca K., Eckstrand B.C., Hu G., Lengauer C., Banavali S., et al., Netrin-1: interaction with deleted in colorectal cancer (DCC) and alterations in brain tumors and neuroblastomas, Cell Growth Differ., 1999, 10, 35-42
55. Jarjour A.A., Durko M., Luk T.L., Marcal N., Shekarabi M., Kennedy T.E., Autocrine netrin function inhibits glioma cell motility and promotes focal adhesion formation, PLoS One, 2011, 6, e25408
56. Manitt C., Colicos M.A., Thompson K.M., Rousselle E., Peterson A.C., Kennedy T.E. Widespread expression of netrin-1 by neurons and oligodendrocytes in the adult mammalian spinal cord, J. Neurosci., 2001, 21, 3911-3922
57. Mehlen P., Thibert C., Dependence receptors: between life and death, Cell. Mol. Life Sci., 2004, 61, 1854-1866
58. Forcet C., Stein E., Pays L., Corset V., Llambi F., Tessier-Lavigne M., et al., Netrin-1-mediated axon outgrowth requires deleted in colorectal cancer-dependent MAPK activation, Nature, 2002, 417, 443-447
59. Shekarabi M., Kennedy T.E., The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1, Mol. Cell. Neurosci., 2002, 19, 1-17
60. Shekarabi M., Moore S.W., Tritsch N.X., Morris S.J., Bouchard J.F., Kennedy T.E., Deleted in colorectal cancer binding netrin-1 mediates cell substrate adhesion and recruits Cdc42, Rac1, Pak1, and N-WASP into an intracellular signaling complex that promotes growth cone expansion, J. Neurosci., 2005, 25, 3132-3141
61. Rajasekharan S., Baker K.A., Horn K.E., Jarjour A.A., Antel J.P., Kennedy T.E., Netrin 1 and Dcc regulate oligodendrocyte process branching and membrane extension via Fyn and RhoA, Development, 2009, 136, 415-426
62. van Nimwegen M.J., van de Water B., Focal adhesion kinase: a potential target in cancer therapy, Biochem. Pharmacol., 2007, 73, 597-609
63. Shimizu A., Nakayama H., Wang P., König C., Akino T., Sandlund J., et al., Netrin-1 promotes glioblastoma cell invasiveness and angiogenesis by multiple pathways including activation of RhoA, cathepsin B, and cAMP-response element-binding protein, J. Biol. Chem., 2013, 288, 2210-2222
64. Wilson B.D., Ii M., Park K.W., Suli A., Sorensen L.K., Larrieu-Lahargue F., et al., Netrins promote developmental and therapeutic angiogenesis, Science, 2006, 313, 640-644
65. Larrivée B., Freitas C., Trombe M., Lv X, DeLafarge B., Yuan L., et al., Activation of the UNC5B receptor by Netrin-1 inhibits sprouting angiogenesis, Genes Dev., 2007, 21, 2433-2447
66. Bouvree K., Larrivée B., Lv X., Yuan L., DeLafarge B., Freitas C., et al., Netrin-1 inhibits sprouting angiogenesis in developing avian embryos, Dev. Biol., 2008, 318, 172-183
67. Hirai H., Maru Y., Hagiwara K., Nishida J., Takaku F., A novel putative tyrosine kinase receptor encoded by the eph gene, Science, 1987, 238, 1717-1720
68. Pasquale E.B., Eph receptors and ephrins in cancer: bidirectional signalling and beyond, Nat. Rev. Cancer, 2010, 10, 165-180
69. Beauchamp A., Debinski W., Ephs and ephrins in cancer: ephrin-A1 signalling, Semin. Cell. Dev. Biol., 2012, 23, 109-115
70. Chen J., Regulation of tumor initiation and metastatic progression by Eph receptor tyrosine kinases, Adv. Cancer Res., 2012, 114, 1-20
71. Fukai J., Yokote H., Yamanaka R., Arao T., Nishio K., Itakura T., EphA4 promotes cell proliferation and migration through a novel EphA4- FGFR1 signaling pathway in the human glioma U251 cell line, Mol. Cancer Ther., 2008, 7, 2768-2778
72. Nakada M., Hayashi Y., Hamada J., Role of Eph/ephrin tyrosine kinase in malignant glioma, Neuro Oncol., 2011, 13, 1163-1170
73. Ying M., Wang S., Sang Y., Sun Y., Lal B., Goodwin C.R., et al., Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition, Oncogene, 2011, 30, 3454-3467
74. Holmberg J., Armulik A., Senti K.A., Edoff K., Spalding K., Momma S., et al., Ephrin-A2 reverse signaling negatively regulates neural progenitor proliferation and neurogenesis, Genes Dev., 2005. 19, 462-471
75. Nakada M., Niska J.A., Miyamori H., McDonough W.S., Wu J., Sato H., et al., The phosphorylation of EphB2 receptor regulates migration and invasion of human glioma cells, Cancer Res., 2004, 64, 3179-3185
76. Fukushima K., Ueno Y., Inoue J., Kanno N., Shimosegawa T., Filopodia formation via a specific Eph family member and PI3K in immortalized cholangiocytes, Am. J. Physiol. Gastrointest. Liver Physiol., 2006, 291, G812-819
77. Steinle J.J., Meininger C.J., Chowdhury U., Wu G., Granger H.J., Role of ephrin B2 in human retinal endothelial cell proliferation and migration, Cell Signal., 2003, 15, 1011-1017
78. Miao H., Wei B.R., Peehl D.M., Li Q., Alexandrou T., Schelling J.R., et al., Activation of EphA receptor tyrosine kinase inhibits the Ras/MAPK pathway. Nat. Cell Biol., 2001, 3, 527-530
79. Brose K., Bland K.S., Wang K.H., Arnott D., Henzel W., Goodman C.S., et al., Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance, Cell, 1999, 96, 795-806
80. Wang K.H., Brose K., Arnott D., Kidd T., Goodman C.S., Henzel W., et al., Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching, Cell, 1999, 96, 771-784
81. Ballard M.S., Hinck L., A roundabout way to cancer, Adv. Cancer Res., 2012, 114, 187-235
82. Dickinson R.E., Dallol A., Bieche I., Krex D., Morton D., Maher E.R., et al., Epigenetic inactivation of SLIT3 and SLIT1 genes in human cancers, Br. J. Cancer., 2004, 91, 2071-2078
83. Dallol A., Krex D., Hesson L., Eng C., Maher E.R., Latif F., Frequent epigenetic inactivation of the SLIT2 gene in gliomas, Oncogene, 2003, 22, 4611-4616
84. Werbowetski-Ogilvie T.E., Seyed Sadr M., Jabado N., Angers-Loustau A., Agar N.Y., Wu J., et al., Inhibition of medulloblastoma cell invasion by Slit, Oncogene, 2006, 25, 5103-5112
85. Mertsch S., Schmitz N., Jeibmann A., Geng J.G., Paulus W., Senner V., Slit2 involvement in glioma cell migration is mediated by Robo1 receptor, J. Neurooncol., 2008, 87, 1-7
86. Yiin J.J., Hu B., Jarzynka M.J., Feng H., Liu K.W., Wu J.Y., et al., Slit2 inhibits glioma cell invasion in the brain by suppression of Cdc42 activity, Neuro Oncol., 2009, 11, 779-789
87. Tessier-Lavigne M., Goodman C.S., The molecular biology of axon guidance, Science, 1996, 274, 1123-1133
88. Yazdani U., Terman J.R., The semaphorins, Genome Biol., 2006, 7, 211
89. Fujisawa H., Discovery of semaphorin receptors, neuropilin and plexin, and their functions in neural development, J. Neurobiol., 2004, 59, 24-33
90. Takahashi T., Fournier A., Nakamura F., Wang L.H., Murakami Y., Kalb R.G., et al., Plexin-neuropilin-1 complexes form functional semaphorin-3A receptors, Cell, 1999, 99, 59-69
91. Derijck A.A., Van Erp S., Pasterkamp R.J., Semaphorin signaling: molecular switches at the midline, Trends Cell. Biol., 2010, 20, 568-576
92. Shimizu A., Mammoto A., Italiano J.E. Jr., et al., Pravda E., Dudley A.C., Ingber D.E., et al., ABL2/ARG tyrosine kinase mediates SEMA3Finduced RhoA inactivation and cytoskeleton collapse in human glioma cells, J. Biol. Chem., 2008, 283, 27230-27238
93. Coma S., Amin D.N., Shimizu A., Lasorella A., Iavarone A., Klagsbrun M., Id2 promotes tumor cell migration and invasion through transcriptional repression of semaphorin 3F, Cancer Res., 2010, 70, 3823-3832
94. Karayan-Tapon L., Wager M., Guilhot J., Levillain P., Marquant C., Clarhaut J., et al., Semaphorin, neuropilin and VEGF expression in glial tumours: SEMA3G, a prognostic marker?, Br. J. Cancer, 2008, 99, 1153-1160
95. Schwarz Q., Gu C., Fujisawa H., Sabelko K., Gertsenstein M., Nagy A., et al., Vascular endothelial growth factor controls neuronal migration and cooperates with Sema3A to pattern distinct compartments of the facial nerve, Genes Dev., 2004, 18, 2822-2834
96. Sabag A.D., Bode J., Fink D., Kigel B., Kugler W., Neufeld G., Semaphorin-3D and semaphorin-3E inhibit the development of tumors from glioblastoma cells implanted in the cortex of the brain, PLoS One, 2012, 7, e42912
97. Tamkun J.W., DeSimone D.W., Fonda D., Patel R.S., Buck C., Horwitz A.F., et al., Structure of integrin, a glycoprotein involved in the transmembrane linkage between fibronectin and actin, Cell, 1986, 46, 271-282
98. Hynes R.O., Cell adhesion: old and new questions, Trends Cell. Biol., 1999, 9, M33-37
99. Hynes R.O., Integrins: a family of cell surface receptors, Cell, 1987, 48, 549-554
100. Giancotti F.G., Ruoslahti E., Integrin signaling, Science, 1999, 285, 1028-1032
101. Kumar C.C., Integrin αvβ3 as a therapeutic target for blocking tumor-induced angiogenesis, Curr. Drug Targets, 2003, 4, 123-131
102. Rooprai H.K., Vanmeter T., Panou C., Schnüll S., Trillo-Pazos G., Davies D., et al., The role of integrin receptors in aspects of glioma invasion in vitro, Int. J. Dev. Neurosci., 1999, 17, 613-623
103. Tonn J.C., Wunderlich S., Kerkau S., Klein C.E., Roosen K., Invasive behaviour of human gliomas is mediated by interindividually different integrin patterns, Anticancer Res., 1998, 18, 2599-2605
104. Uhm J.H., Gladson C.L., Rao J.S., The role of integrins in the malignant phenotype of gliomas, Front. Biosci., 1999, 4, D188-199
105. Tabatabai G., Tonn J.C., Stupp R., Weller M., The role of integrins in glioma biology and anti-glioma therapies, Curr. Pharm. Des., 2011, 17, 2402-2410
106. Nikolopoulos S.N., Blaikie P., Yoshioka T., Guo W., Giancotti F.G., Integrin β4 signaling promotes tumor angiogenesis, Cancer Cell., 6, 2004, 471-483
107. Guo W., Giancotti F.G., Integrin signalling during tumour progression, Nat. Rev. Mol. Cell. Biol., 2004, 5, 816-826
108. Kwiatkowska A., Symons M., Signaling determinants of glioma cell invasion, Adv. Exp. Med. Biol., 2013, 986, 121-141
109. Mittelbronn M., Warth A., Meyermann R., Goodman S., Weller M., Expression of integrins αvβ3 and αvβ5 and their ligands in primary and secondary central nervous system neoplasms, Histol. Histopathol., 2013, 28, 749-758
110. Saitoh Y., Kuratsu J., Takeshima H., Yamamoto S., Ushio Y., Expression of osteopontin in human glioma. Its correlation with the malignancy, Lab. Invest., 1995, 72, 55-63
111. Sreekanthreddy P., Srinivasan H., Kumar D.M., Nijaguna M.B., Sridevi S., Vrinda M., et al., Identification of potential serum biomarkers of glioblastoma: serum osteopontin levels correlate with poor prognosis, Cancer Epidemiol. Biomarkers Prev., 2010, 19, 1409-1422
112. Wang Y., Yan W., Lu X., Qian C., Zhang J., Li P., et al., Overexpression of osteopontin induces angiogenesis of endothelial progenitor cells via the avbeta3/PI3K/AKT/eNOS/NO signaling pathway in glioma cells, Eur. J. Cell. Biol., 2011, 90, 642-648
113. Kurozumi K., Ichikawa T., Onishi M., Fujii K., Date I., Cilengitide treatment for malignant glioma: current status and future direction, Neurol. Med. Chir., 2012, 52, 539-547
114. Bar-Sagi D., Hall A., Ras and Rho GTPases: a family reunion, Cell, 2000, 103, 227-238
115. Sahai E., Olson M.F., Marshall C.J., Cross-talk between Ras and Rho signalling pathways in transformation favours proliferation and increased motility, EMBO J., 2001, 20, 755-766
116. Parri M., Chiarugi P., Rac and Rho GTPases in cancer cell motility control, Cell Commun. Signal., 2010, 8, 23
117. Yamazaki D., Kurisu S., Takenawa T., Regulation of cancer cell motility through actin reorganization, Cancer Sci., 2005, 96, 379-386
118. Yan B., Chour H.H., Peh B.K., Lim C., Salto-Tellez M., RhoA protein expression correlates positively with degree of malignancy in astrocytomas, Neurosci. Lett., 2006, 407, 124-126
119. Ye D.Z., Field J., PAK signaling in cancer, Cell Logist., 2012, 2, 105-116
120. Khalil B.D., El-Sibai M., Rho GTPases in primary brain tumor malignancy and invasion, J. Neurooncol., 2012, 108, 333-339
121. Rathinam R., Berrier A., Alahari S.K., Role of Rho GTPases and their regulators in cancer progression, Front. Biosci., 2011, 16, 2561-2571
122. Valster A., Tran N.L., Nakada M., Berens M.E., Chan A.Y., Symons M., Cell migration and invasion assays, Methods, 2005, 37, 208-215
123. Josso F., Prou-Wartelle O., Interaction of tissue factor and factor VII at the earliest phase of coagulation, Thromb. Diath. Haemorrh. Suppl., 1965, 17, 35-44
124. Contrino J., Hair G., Kreutzer D.L., Rickles F.R., In situ detection of tissue factor in vascular endothelial cells: correlation with the malignant phenotype of human breast disease, Nat. Med., 1996, 2, 209-215
125. Hamada K., Kuratsu J., Saitoh Y., Takeshima H., Nishi T., Ushio Y., Expression of tissue factor correlates with grade of malignancy in human glioma, Cancer, 1996, 77, 1877-1883
126. Magnus N., Garnier D., Rak J., Oncogenic epidermal growth factor receptor up-regulates multiple elements of the tissue factor signaling pathway in human glioma cells, Blood, 2010, 116, 815-818
127. Rong Y., Durden D.L., Van Meir E.G., Brat D.J., 'Pseudopalisading' necrosis in glioblastoma: a familiar morphologic feature that links vascular pathology, hypoxia, and angiogenesis, J. Neuropathol. Exp. Neurol., 2006, 65, 529-539
128. Gessler F., Voss V., Dutzmann S., Seifert V., Gerlach R., Kögel D., Inhibition of tissue factor/protease-activated receptor-2 signaling limits proliferation, migration and invasion of malignant glioma cells, Neuroscience, 2010, 165, 1312-1322
129. Harter P.N., Dützmann S., Drott U., Zachskorn C., Hattingen E., Capper D., et al., Anti-tissue factor (TF9-10H10) treatment reduces tumor cell invasiveness in a novel migratory glioma model, Neuropathology, 2013, Epub ahead of print, doi: 10.1111/neup.12018
130. Kaminska B., Kocyk M., Kijewska M., TGF beta signaling and its role in glioma pathogenesis, Adv. Exp. Med. Biol., 2013, 986, 171-187
131. Platten M., Wick W., Wild-Bode C., Aulwurm S., Dichgans J., Weller M., Transforming growth factors β1 (TGF-β1) and TGF-β2 promote glioma cell migration via up-regulation of αVβ3 integrin expression, Biochem. Biophys. Res. Commun., 2000, 268, 607-611
132. Wick W., Naumann U., Weller M., Transforming growth factor-beta: a molecular target for the future therapy of glioblastoma, Curr. Pharm. Des., 2006, 12, 341-349
133. Dziembowska M., Danilkiewicz M., Wesolowska A., Zupanska A., Chouaib S., Kaminska B., Cross-talk between Smad and p38 MAPK signalling in transforming growth factor beta signal transduction in human glioblastoma cells, Biochem. Biophys. Res. Commun., 2007, 354, 1101-1106
134. Hsieh H.L., Wang H.H., Wu W.B., Chu P.J., Yang C.M., Transforming growth factor-beta1 induces matrix metalloproteinase-9 and cell migration in astrocytes: roles of ROS-dependent ERK- and JNK-NFkappaB pathways, J. Neuroinflammation, 2010, 7, 88
135. Baumann F., Leukel P., Doerfelt A., Beier C.P., Dettmer K., Oefner P.J., et al., Lactate promotes glioma migration by TGF-β2-dependent regulation of matrix metalloproteinase-2, Neuro Oncol., 2009, 11, 368-380
136. Arslan F., Bosserhoff A.K., Nickl-Jockschat T., Doerfelt A., Bogdahn U., Hau P., The role of versican isoforms V0/V1 in glioma migration mediated by transforming growth factor-β2, Br. J. Cancer, 2007, 96, 1560-1568
137. Ehtesham M., Min E., Issar N.M., Kasl R.A., Khan I.S., Thompson R.C., The role of the CXCR4 cell surface chemokine receptor in glioma biology, J. Neurooncol., 2013, 113, 153-162
138. Hattermann K., Mentlein R., An infernal trio: the chemokine CXCL12 and its receptors CXCR4 and CXCR7 in tumor biology, Ann. Anat., 2013, 195, 103-110
139. Salmaggi A., Gelati M., Pollo B., Marras C., Silvani A., Balestrini M.R., et al., CXCL12 expression is predictive of a shorter time to tumor progression in low-grade glioma: a single-institution study in 50 patients, J. Neurooncol., 2005, 74, 287-293
140. Woerner B.M., Warrington N.M., Kung A.L., Perry A., Rubin J.B., Widespread CXCR4 activation in astrocytomas revealed by phospho-CXCR4-specific antibodies, Cancer Res., 2005, 65, 11392-11399
141. Zagzag D., Lukyanov Y., Lan L., Ali M.A., Esencay M., Mendez O., et al., Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion, Lab. Invest., 2006, 86, 1221-1232
142. Calatozzolo C., Maderna E., Pollo B., Gelati M., Marras C., Silvani A., et al., Prognostic value of CXCL12 expression in 40 low-grade oligodendrogliomas and oligoastrocytomas, Cancer Biol. Ther., 2006, 5, 827-832
143. Rubin J.B., Kung A.L., Klein R.S., Chan J.A., Sun Y., Schmidt K., et al., A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors, Proc. Natl. Acad. Sci. USA, 2003, 100, 13513-13518
144. Tseng D., Vasquez-Medrano D.A., Brown J.M., Targeting SDF-1/CXCR4 to inhibit tumour vasculature for treatment of glioblastomas, Br. J. Cancer, 2011, 104, 1805-1809
145. Tian Y., Nan Y., Han L., Zhang A., Wang G., Jia Z., et al., MicroRNA miR-451 downregulates the PI3K/AKT pathway through CAB39 in human glioma, Int. J. Oncol., 2012, 40, 1105-1112
146. Nan Y., Han L., Zhang A., Wang G., Jia Z., Yang Y., et al., MiRNA-451 plays a role as tumor suppressor in human glioma cells, Brain Res., 2010, 1359, 14-21
147. Godlewski J., Nowicki M.O., Bronisz A., Nuovo G., Palatini J., De Lay M., et al., MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells, Mol. Cell, 2010, 37, 620-632
148. Oellers P., Schallenberg M., Stupp T., Charalambous P., Senner V., Paulus W., et al., A coculture assay to visualize and monitor interactions between migrating glioma cells and nerve fibers, Nat. Protoc., 2009, 4, 923-927
149. Priester M., Copanaki E., Vafaizadeh V., Hensel S., Bernreuther C., Glatzel M., et al., STAT3 silencing inhibits glioma single cell infiltration and tumor growth, Neuro Oncol., 2013, 15, 840-852
150. Westphal M., Meissner H., Matschke J., Herrmann H.D., Tissue culture of human neurocytomas induces the expression of glial fibrilary acidic protein, J. Neurocytol., 1998, 27, 805-816
151. Ernst A., Hofmann S., Ahmadi R., Becker N., Korshunov A., Engel F., et al., Genomic and expression profiling of glioblastoma stem cell-like spheroid cultures identifies novel tumor-relevant genes associated with survival, Clin. Cancer Res., 2009, 15, 6541-6550
152. Mella O., Bjerkvig R., Schem B.C., Dahl O., Laerum O.D., A cerebral glioma model for experimental therapy and in vivo invasion studies in syngeneic BD IX rats, J. Neurooncol., 1990, 9, 93-104
153. Huszthy P.C., Immervoll H., Wang J., Goplen D., Miletic H., Eide G.E., et al., Cellular effects of oncolytic viral therapy on the glioblastoma microenvironment, Gene Ther., 2010, 17, 202-216
154. De Witt Hamer P.C., Van Tilborg A.A., Eijk P.P., Sminia P., Troost D., Van Noorden C.J., et al., The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids, Oncogene, 2008, 27, 2091-2096
155. Fomchenko E.I., Holland E.C., Mouse models of brain tumors and their applications in preclinical trials, Clin. Cancer. Res., 2006, 12, 5288-5297
156. Hambardzumyan D., Parada L.F., Holland E.C., Charest A., Genetic modeling of gliomas in mice: new tools to tackle old problems, Glia, 2011, 59, 1155-1168
157. Weissenberger J., Steinbach J.P., Malin G., Spada S., Rulicke T., Aguzzi A., Development and malignant progression of astrocytomas in GFAP-v-src transgenic mice, Oncogene, 1997, 14, 2005-2013
158. Shih A.H., Dai C., Hu X., Rosenblum M.K., Koutcher J.A., Holland E.C., Dose-dependent effects of platelet-derived growth factor-B on glial tumorigenesis, Cancer Res., 2004, 64, 4783-4789
159. Uhrbom L., Hesselager G., Nister M., Westermark B., Induction of brain tumors in mice using a recombinant platelet-derived growth factor B-chain retrovirus, Cancer Res., 1998, 58, 5275-5279
160. Sottoriva A., Spiteri I., Piccirillo S.G., Touloumis A., Collins V.P., Marioni J.C., et al., Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics, Proc. Natl. Acad. Sci. USA, 2013, 110, 4009-4014
161. Podlech O., Harter P.N., Mittelbronn M., Pöschel S., Naumann U., Fermented mistletoe extract as a multimodal antitumoral agent in gliomas, Evid. Based Complement. Alternat. Med., 2012, 501796
162. Seznec J., Silkenstedt B., Naumann U., Therapeutic effects of the Sp1 inhibitor mithramycin A in glioblastoma, J. Neurooncol., 2011, 101, 365-377
163. Kargiotis O., Chetty C., Gondi C.S., Tsung A.J., Dinh D.H., Gujrati M., et al., Adenovirus-mediated transfer of siRNA against MMP-2 mRNA results in impaired invasion and tumor-induced angiogenesis, induces apoptosis in vitro and inhibits tumor growth in vivo in glioblastoma, Oncogene, 2008, 27, 4830-4840
164. Nasarre C., Roth M., Jacob L., Roth L., Koncina E., Thien A., et al., Peptide-based interference of the transmembrane domain of neuropilin-1 inhibits glioma growth in vivo, Oncogene, 2010, 29, 2381-2392
165. Kesanakurti D., Chetty C., Bhoopathi P., Lakka S.S., Gorantla B., Tsung A.J., et al., Suppression of MMP-2 attenuates TNF-α induced NF-κB activation and leads to JNK mediated cell death in glioma, PLoS One, 2011, 6, e19341
166. Nakabayashi H., Yawata T., Shimizu K., Anti-invasive and antiangiogenic effects of MMI-166 on malignant glioma cells, BMC Cancer, 2010, 10, 339
167. Bello L., Lucini V., Carrabba G., Giussani C., Machluf M., Pluderi M., et al., Simultaneous inhibition of glioma angiogenesis, cell proliferation, and invasion by a naturally occurring fragment of human metalloproteinase-2, Cancer Res., 2001, 61, 8730-8736
168. Kim M.S., Park M.J., Kim S.J., Lee C.H., Yoo H., Shin S.H., et al., Emodin suppresses hyaluronic acid-induced MMP-9 secretion and invasion of glioma cells, Int. J. Oncol., 2005, 27, 839-846
169. Gondi C.S., Lakka S.S., Dinh D.H., Olivero W.C., Gujrati M., Rao J.S., Downregulation of uPA, uPAR and MMP-9 using small, interfering, hairpin RNA (siRNA) inhibits glioma cell invasion, angiogenesis and tumor growth, Neuron Glia Biol., 2004, 1, 165-176
170. Reardon D.A., Akabani G., Coleman R.E., Friedman A.H., Friedman H.S., Herndon J.E.2nd, et al., Salvage radioimmunotherapy with murine iodine-131-labeled antitenascin monoclonal antibody 81C6 for patients with recurrent primary and metastatic malignant brain tumors: phase II study results, J. Clin. Oncol., 2006, 24, 115-122
171. Senft C., Polacin M., Priester M., Seifert V., Kögel D., Weissenberger J., The nontoxic natural compound Curcumin exerts antiproliferative, anti-migratory, and anti-invasive properties against malignant gliomas, BMC Cancer, 2010, 10, 491
172. Yamada S., Bu X.Y., Khankaldyyan V., Gonzales-Gomez I., McComb J.G., Laug W.E., Effect of the angiogenesis inhibitor Cilengitide (EMD 121974) on
173. Reardon D.A., Fink K.L., Mikkelsen T., Cloughesy T.F., O'Neill A., Plotkin S., et al., Randomized phase II study of cilengitide, an integrin-targeting arginine-glycine-aspartic acid peptide, in recurrent glioblastoma multiforme. J. Clin. Oncol., 2008, 26, 5610-5617
174. Stupp R., Hegi M.E., Neyns B., Goldbrunner R., Schlegel U., Clement P.M., et al., Phase I/IIa study of cilengitide and temozolomide with concomitant radiotherapy followed by cilengitide and temozolomide maintenance therapy in patients with newly diagnosed glioblastoma, J. Clin. Oncol., 2010, 28, 2712-2718
175. Nabors L.B., Mikkelsen T., Hegi M.E., Ye X., Batchelor T., Lesser G., et al., A safety run-in and randomized phase 2 study of cilengitide combined with chemoradiation for newly diagnosed glioblastoma (NABTT 0306), Cancer, 2012, 118 5601-5607
176. Bello L., Lucini V., Giussani C., Carrabba G., Pluderi M., Scaglione F., et al., IS20I, a specific αvβ3 integrin inhibitor, reduces glioma growth in vivo, Neurosurgery, 2003, 52, 177-185
177. Martens T., Schmidt N.O., Eckerich C., Fillbrandt R., Merchant M., Schwall R., et al., A novel one-armed anti-c-Met antibody inhibits glioblastoma growth in vivo, Clin. Cancer Res., 2006, 12, 6144-6152