Small-molecule inhibitors of FGFR, integrins and FAK selectively decrease L1CAM-stimulated glioblastoma cell motility and proliferation

Cellular Oncology

Volumn 39, Issue 3, 2016, Pages 229-242

  Anderson, Hannah J ^a   Galileo, Deni S ^a,b  

^a UNIVERSITY OF DELAWARE   (United States)

^b HELEN F GRAHAM CANCER CENTER   (United States)

Author keywords

Fibroblast growth factor receptor; Focal adhesion kinase; Glioblastoma; L1; L1CAM

Indexed keywords

1 TERT BUTYL 3 [6 (3,5 DIMETHOXYPHENYL) 2 (4 DIETHYLAMINOBUTYLAMINO)PYRIDO[2,3 D]PYRIMIDIN 7 YL]UREA; CILENGITIDE; DNA; ENZYME INHIBITOR; FIBROBLAST GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE; INTEGRIN; NERVE CELL ADHESION MOLECULE L1; PF 431396; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; Y 15; 1,2,4,5-BENZENETETRAAMINE; ALPHAVBETA5 INTEGRIN; ANILINE DERIVATIVE; ANTINEOPLASTIC AGENT; FOCAL ADHESION KINASE 1; PTK2 PROTEIN, HUMAN; PYRIMIDINE DERIVATIVE; SNAKE VENOM; VITRONECTIN RECEPTOR;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DNA CONTENT; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; MICROSCOPY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TIME-LAPSE MICROSCOPY; ANTAGONISTS AND INHIBITORS; BRAIN TUMOR; CELL MOTION; DRUG EFFECTS; GLIOBLASTOMA; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANILINE COMPOUNDS; ANTINEOPLASTIC AGENTS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; FOCAL ADHESION KINASE 1; GLIOBLASTOMA; HUMANS; INTEGRIN ALPHAVBETA3; NEURAL CELL ADHESION MOLECULE L1; PYRIMIDINES; RECEPTORS, FIBROBLAST GROWTH FACTOR; RECEPTORS, VITRONECTIN; SNAKE VENOMS;

EID: 84958779238     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-016-0267-7     Document Type: Article

References (64)

1. P.Y. Wen, S. Kesari, Malignant gliomas in adults. N. Engl. J. Med. 359, 492–507 (2008)
2. F.B. Furnari, T. Fenton, R.M. Bachoo, A. Mukasa, J.M. Stommel, A. Stegh, W.C. Hahn, K.L. Ligon, D.N. Louis, C. Brennan, L. Chin, R.A. DePinho, W.K. Cavenee, Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 21, 2683–2710 (2007)
3. S. Lee, S.R. Piccolo, K. Allen-Brady, Robust meta-analysis shows that glioma transcriptional subtyping complements traditional approaches. Cell. Oncol. 37, 317–329 (2014)
4. P. De Bonis, C. Anile, A. Pompucci, A. Fiorentino, M. Balducci, S. Chiesa, L. Lauriola, G. Maira, A. Mangiola, The influence of surgery on recurrence pattern of glioblastoma. Clin. Neurol. Neurosurg. 115, 37–43 (2013)
5. R. Stupp, W.P. Mason, M.J. van den Bent, M. Weller, B. Fisher, M.J.B. Taphoorn, K. Belanger, A.A. Brandes, C. Marosi, U. Bogdahn, J. Curschmann, R.C. Janzer, S.K. Ludwin, T. Gorlia, A. Allgeier, D. Lacombe, J.G. Cairncross, E. Eisenhauer, R.O. Mirimanoff, for the European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups and the National Cancer Institute of Canada Clinical Trials Group, Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 352, 987–996 (2005)
6. N.R. Smoll, K. Schaller, O.P. Gautschi, Long-term survival of patients with glioblastoma multiforme (GBM). J. Clin. Neurosci. Off. J. Neurosurg. Soc. Aust. 20, 670–675 (2013)
7. A. Faissner, D.B. Teplow, D. Kübler, G. Keilhauer, V. Kinzel, M. Schachner, Biosynthesis and membrane topography of the neural cell adhesion molecule L1. EMBO J. 4, 3105–3113 (1985)
8. M. Moos, R. Tacke, H. Scherer, D. Teplow, K. Früh, M. Schachner, Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature 334, 701–703 (1988)
9. S. Chang, F.G. Rathjen, J.A. Raper, Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J. Cell Biol. 104, 355–362 (1987)
10. G. Fischer, V. Künemund, M. Schachner, Neurite outgrowth patterns in cerebellar microexplant cultures are affected by antibodies to the cell surface glycoprotein L1. J. Neurosci. 6, 605–612 (1986)
11. G. Keilhauer, A. Faissner, M. Schachner, Differential inhibition of neurone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature 316, 728–730 (1985)
12. J. Lindner, F.G. Rathjen, M. Schachner, L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305, 427–430 (1983)
13. M. Conacci-Sorrell, A. Kaplan, S. Raveh, N. Gavert, T. Sakurai, A. Ben-Ze’ev, The shed ectodomain of Nr-CAM stimulates cell proliferation and motility, and confers cell transformation. Cancer Res. 65, 11605–11612 (2005)
14. P.M. Wood, M. Schachner, R.P. Bunge, Inhibition of Schwann cell myelination in vitro by antibody to the L1 adhesion molecule. J. Neurosci. 10, 3635–3645 (1990)
15. P. Liljelund, P. Ghosh, A.N. van den Pol, Expression of the neural axon adhesion molecule L1 in the developing and adult rat brain. J. Biol. Chem. 269, 32886–32895 (1994)
16. T. Maretzky, M. Schulte, A. Ludwig, S. Rose-John, C. Blobel, D. Hartmann, P. Altevogt, P. Saftig, K. Reiss, L1 is sequentially processed by two differently activated metalloproteases and presenilin/γ-secretase and regulates neural cell adhesion, cell migration, and neurite outgrowth. Mol. Cell. Biol. 25, 9040–9053 (2005)
17. M. Fogel, S. Mechtersheimer, M. Huszar, A. Smirnov, A. Abu-Dahi, W. Tilgen, J. Reichrath, T. Georg, P. Altevogt, P. Gutwein, L1 adhesion molecule (CD 171) in development and progression of human malignant melanoma. Cancer Lett. 189, 237–247 (2003)
18. M. Fogel, P. Gutwein, S. Mechtersheimer, S. Riedle, A. Stoeck, A. Smirnov, L. Edler, A. Ben-Arie, M. Huszar, P. Altevogt, L1 expression as a predictor of progression and survival in patients with uterine and ovarian carcinomas. Lancet 362, 869–875 (2003)
19. N. Gavert, M. Conacci-Sorrell, D. Gast, A. Schneider, P. Altevogt, T. Brabletz, A. Ben-Ze’ev, L1, a novel target of beta-catenin signaling, transforms cells and is expressed at the invasive front of colon cancers. J. Cell Biol. 168, 633–642 (2005)
20. M. Yang, S. Adla, M.K. Temburni, V.P. Patel, E.L. Lagow, O.A. Brady, J. Tian, M.I. Boulos, D.S. Galileo, Stimulation of glioma cell motility by expression, proteolysis, and release of the L1 neural cell recognition molecule. Cancer Cell Int. 9, 27 (2009)
21. Y. Li, D.S. Galileo, Soluble L1CAM promotes breast cancer cell adhesion and migration in vitro, but not invasion. Cancer Cell Int. 10, 34 (2010)
22. D. Chen, Z. Zeng, J. Yang, C. Ren, D. Wang, W. Wu, R. Xu, L1cam promotes tumor progression and metastasis and is an independent unfavorable prognostic factor in gastric cancer. J. Hematol. Oncol. 6, 43 (2013)
23. P. Gutwein, S. Mechtersheimer, S. Riedle, A. Stoeck, D. Gast, S. Joumaa, H. Zentgraf, M. Fogel, D.P. Altevogt, ADAM10-mediated cleavage of L1 adhesion molecule at the cell surface and in released membrane vesicles. FASEB J. 17, 292–294 (2003)
24. H. Kiefel, S. Bondong, J. Hazin, J. Ridinger, U. Schirmer, S. Riedle, P. Altevogt, L1CAM: a major driver for tumor cell invasion and motility. Cell Adhes. Migr. 6, 374–384 (2012)
25. M. Yang, Y. Li, K. Chilukuri, O.A. Brady, M.I. Boulos, J.C. Kappes, D.S. Galileo, L1 stimulation of human glioma cell motility correlates with FAK activation. J. Neurooncol. 105, 27–44 (2011)
26. V. Mohanan, M.K. Temburni, J.C. Kappes, D.S. Galileo, L1CAM stimulates glioma cell motility and proliferation through the fibroblast growth factor receptor. Clin. Exp. Metastasis 30, 507–520 (2013)
27. S. Mechtersheimer, P. Gutwein, N. Agmon-Levin, A. Stoeck, M. Oleszewski, S. Riedle, R. Postina, F. Fahrenholz, M. Fogel, V. Lemmon, P. Altevogt, Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J. Cell Biol. 155, 661–673 (2001)
28. B. Felding-Habermann, S. Silletti, F. Mei, C.H. Siu, P.M. Yip, P.C. Brooks, D.A. Cheresh, T.E. O’Toole, M.H. Ginsberg, A.M. Montgomery, A single immunoglobulin-like domain of the human neural cell adhesion molecule L1 supports adhesion by multiple vascular and platelet integrins. J. Cell Biol. 139, 1567–1581 (1997)
29. A.M. Montgomery, J.C. Becker, C.H. Siu, V.P. Lemmon, D.A. Cheresh, J.D. Pancook, X. Zhao, R.A. Reisfeld, Human neural cell adhesion molecule L1 and rat homologue NILE are ligands for integrin alpha v beta 3. J. Cell Biol. 132, 475–485 (1996)
30. M. Oleszewski, S. Beer, S. Katich, C. Geiger, Y. Zeller, U. Rauch, P. Altevogt, Integrin and neurocan binding to L1 involves distinct Ig domains. J. Biol. Chem. 274, 24602–24610 (1999)
31. O. Ebeling, A. Duczmal, S. Aigner, C. Geiger, S. Schöllhammer, J.T. Kemshead, P. Möller, R. Schwartz-Albiez, P. Altevogt, L1 adhesion molecule on human lymphocytes and monocytes: expression and involvement in binding to alpha v beta 3 integrin. Eur. J. Immunol. 26, 2508–2516 (1996)
32. S. Blaess, R.A. Kammerer, H. Hall, Structural analysis of the sixth immunoglobulin-like domain of mouse neural cell adhesion molecule L1 and its interactions with alpha(v)beta3, alpha(IIb)beta3, and alpha5beta1 integrins. J. Neurochem. 71, 2615–2625 (1998)
33. M. Ruppert, S. Aigner, M. Hubbe, H. Yagita, P. Altevogt, The L1 adhesion molecule is a cellular ligand for VLA-5. J. Cell Biol. 131, 1881–1891 (1995)
34. A. Duczmal, S. Schöllhammer, S. Katich, O. Ebeling, R. Schwartz-Albiez, P. Altevogt, The L1 adhesion molecule supports alpha v beta 3-mediated migration of human tumor cells and activated T lymphocytes. Biochem. Biophys. Res. Commun. 232, 236–239 (1997)
35. J. Zhao, J.-L. Guan, Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev. 28, 35–49 (2009)
36. S.K. Mitra, D.A. Hanson, D.D. Schlaepfer, Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56–68 (2005)
37. L. Ding, X. Sun, Y. You, N. Liu, Z. Fu, Expression of focal adhesion kinase and phosphorylated focal adhesion kinase in human gliomas is associated with unfavorable overall survival. Transl. Res. J. Lab. Clin. Med. 156, 45–52 (2010)
38. P. Doherty, F.S. Walsh, CAM-FGF receptor interactions: a model for axonal growth. Mol. Cell. Neurosci. 8, 99–111 (1996)
39. P. Doherty, P. Smith, F.S. Walsh, Shared cell adhesion molecule (CAM) homology domains point to CAMs signalling via FGF receptors. Perspect. Dev. Neurobiol. 4, 157–168 (1996)
40. P. Auguste, D.B. Gürsel, S. Lemière, D. Reimers, P. Cuevas, F. Carceller, J.P. Di Santo, A. Bikfalvi, Inhibition of fibroblast growth factor/fibroblast growth factor receptor activity in glioma cells impedes tumor growth by both angiogenesis-dependent and -independent mechanisms. Cancer Res. 61, 1717–1726 (2001)
41. B. Rousseau, F. Larrieu-Lahargue, S. Javerzat, F. Guilhem-Ducléon, F. Beermann, A. Bikfalvi, The tyrp1-Tag/tyrp1-FGFR1-DN bigenic mouse: a model for selective inhibition of tumor development, angiogenesis, and invasion into the neural tissue by blockade of fibroblast growth factor receptor activity. Cancer Res. 64, 2490–2495 (2004)
42. W. Loilome, A.D. Joshi, C.M.J. ap Rhys, S. Piccirillo, A.L. Vescovi, V.L. Angelo, G.L. Gallia, G.J. Riggins, Glioblastoma cell growth is suppressed by disruption of Fibroblast Growth Factor pathway signaling. J. Neurooncol. 94, 359–366 (2009)
43. M. Mohammadi, S. Froum, J.M. Hamby, M.C. Schroeder, R.L. Panek, G.H. Lu, A.V. Eliseenkova, D. Green, J. Schlessinger, S.R. Hubbard, Crystal structure of an angiogenesis inhibitor bound to the FGF receptor tyrosine kinase domain. EMBO J. 17, 5896–5904 (1998)
44. R.E. Nisato, J.-C. Tille, A. Jonczyk, S.L. Goodman, M.S. Pepper, alphav beta 3 and alphav beta 5 integrin antagonists inhibit angiogenesis in vitro. Angiogenesis 6, 105–119 (2003)
45. V.M. Golubovskaya, C. Nyberg, M. Zheng, F. Kweh, A. Magis, D. Ostrov, W.G. Cance, A small molecule inhibitor, 1,2,4,5-benzenetetraamine tetrahydrochloride, targeting the y397 site of focal adhesion kinase decreases tumor growth. J. Med. Chem. 51, 7405–7416 (2008)
46. S. Han, A. Mistry, J.S. Chang, D. Cunningham, M. Griffor, P.C. Bonnette, H. Wang, B.A. Chrunyk, G.E. Aspnes, D.P. Walker, A.D. Brosius, L. Buckbinder, Structural characterization of proline-rich tyrosine kinase 2 (PYK2) reveals a unique (DFG-out) conformation and enables inhibitor design. J. Biol. Chem. 284, 13193–13201 (2009)
47. J.S. Fotos, V.P. Patel, N.J. Karin, M.K. Temburni, J.T. Koh, D.S. Galileo, Automated time-lapse microscopy and high-resolution tracking of cell migration. Cytotechnology 51, 7–19 (2006)
48. C. Mas-Moruno, F. Rechenmacher, H. Kessler, Cilengitide: the first anti-angiogenic small molecule drug candidate. Design, synthesis and clinical evaluation. Anticancer Agents Med. Chem. 10, 753–768 (2010)
49. M.V. Dieci, M. Arnedos, F. Andre, J.C. Soria, Fibroblast growth factor receptor inhibitors as a cancer treatment: from a biologic rationale to medical perspectives. Cancer Discov. 3, 264–279 (2013)
50. A.N. Brooks, E. Kilgour, P.D. Smith, Molecular pathways: fibroblast growth factor signaling: a new therapeutic opportunity in cancer. Clin. Cancer Res. 18, 1855–1862 (2012)
51. F.J. Sulzmaier, C. Jean, D.D. Schlaepfer, FAK in cancer: mechanistic findings and clinical applications. Nat. Rev. Cancer 14, 598–610 (2014)
52. V.M. Golubovskaya, G. Huang, B. Ho, M. Yemma, C.D. Morrison, J. Lee, B.P. Eliceiri, W.G. Cance, Pharmacologic blockade of FAK autophosphorylation decreases human glioblastoma tumor growth and synergizes with temozolomide. Mol. Cancer Ther. 12, 162–172 (2013)
53. W.G. Roberts, E. Ung, P. Whalen, B. Cooper, C. Hulford, C. Autry, D. Richter, E. Emerson, J. Lin, J. Kath, K. Coleman, L. Yao, L. Martinez-Alsina, M. Lorenzen, M. Berliner, M. Luzzio, N. Patel, E. Schmitt, S. LaGreca, J. Jani, M. Wessel, E. Marr, M. Griffor, F. Vajdos, Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562,271. Cancer Res. 68, 1935–1944 (2008)
54. W. Zhao, Comparison of L1 expression and secretion in glioblastoma and neuroblastoma cells. Oncol. Lett. 4, 812–816 (2012)
55. V.M. Golubovskaya, Targeting FAK in human cancer: from finding to first clinical trials. Front. Biosci. Landmark Ed. 19, 687–706 (2014)
56. G. Eisele, A. Wick, A.-C. Eisele, P.M. Clément, J. Tonn, G. Tabatabai, A. Ochsenbein, U. Schlegel, B. Neyns, D. Krex, M. Simon, G. Nikkhah, M. Picard, R. Stupp, W. Wick, M. Weller, Cilengitide treatment of newly diagnosed glioblastoma patients does not alter patterns of progression. J. Neurooncol. 117, 141–145 (2014)
57. K. Färber, M. Synowitz, G. Zahn, D. Vossmeyer, R. Stragies, N. van Rooijen, H. Kettenmann, An alpha5beta1 integrin inhibitor attenuates glioma growth. Mol. Cell. Neurosci. 39, 579–585 (2008)
58. W. Wang, F. Wang, F. Lu, S. Xu, W. Hu, J. Huang, Q. Gu, X. Sun, The antiangiogenic effects of integrin alpha5beta1 inhibitor (ATN-161) in vitro and in vivo. Invest. Ophthalmol. Vis. Sci. 52, 7213–7220 (2011)
59. D.D. Schlaepfer, S.K. Mitra, D. Ilic, Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim. Biophys. Acta 1692, 77–102 (2004)
60. D.D. Schlaepfer, S.K. Mitra, Multiple connections link FAK to cell motility and invasion. Curr. Opin. Genet. Dev. 14, 92–101 (2004)
61. G.E. Plopper, H.P. McNamee, L.E. Dike, K. Bojanowski, D.E. Ingber, Convergence of integrin and growth factor receptor signaling pathways within the focal adhesion complex. Mol. Biol. Cell 6, 1349–1365 (1995)
62. H. Sarin, A.S. Kanevsky, H. Wu, A.A. Sousa, C.M. Wilson, M.A. Aronova, G.L. Griffiths, R.D. Leapman, H.Q. Vo, Physiologic upper limit of pore size in the blood-tumor barrier of malignant solid tumors. J. Transl. Med. 7, 51 (2009)
63. R.-Y. Bai, V. Staedtke, G.J. Riggins, Molecular targeting of glioblastoma: drug discovery and therapies. Trends Mol. Med. 17, 301–312 (2011)
64. Q.T. Ostrom, H. Gittleman, P. Liao, C. Rouse, Y. Chen, J. Dowling, Y. Wolinsky, C. Kruchko, J. Barnholtz-Sloan, CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2007–2011. Neuro-Oncology 16(Suppl 4), iv1–iv63 (2014)