Growth factor receptors signaling in glioblastoma cells: Therapeutic implications

Journal of Neuro-Oncology

Volumn 92, Issue 2, 2009, Pages 137-147

  Carapancea, Mia ^a   Alexandru, Oana ^a   Fetea, Ani S ^b   Dragutescu, Laura ^b   Castro, Juan ^a   Georgescu, Ada ^c   Popa Wagner, A ^d   Bäcklund, Magnus L ^a   Lewensohn, Rolf ^a   Dricu, Anica ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF MEDICINE AND PHARMACY OF CRAIOVA   (Romania)

^c Medico Science SRL   (Romania)

^d UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Glioma; IGF 1R; PDGFR

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; AG 1433; ANTINEOPLASTIC AGENT; LY 29004; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; GLIOBLASTOMA; HUMAN; HUMAN CELL; IONIZING RADIATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; FLOW CYTOMETRY; GLIOBLASTOMA; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; RECEPTOR, IGF TYPE 1; RECEPTORS, GROWTH FACTOR; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 61349202875     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-008-9753-8     Document Type: Article

References (73)

1. Allalunis-Turner MJ, Zia PK, Barron GM, Mirzayans R, Day RSIII (1995) Radiation-induced DNA damage and repair in cells of a radiosensitive human malignant glioma cell line. Radiat Res 144:288-293. doi: 10.2307/ 3578948
2. Anderson CW, Dunn JJ, Freimuth PI, Galloway AM, Allalunis-Turner MJ (2001) Frameshift mutation in PRKDC, the gene for DNA-PKcs, in the DNA repair-defective, human, glioma-derived cell line M059J. Radiat Res 156:2-9. doi: 10.1667/0033-7587(2001)156[0002:FMIPTG]2.0.CO;2
3. Andrews DW, Resnicoff M, Flanders AE, Kenyon L, Curtis M, Merli G, Baserga R, Iliakis G, Aiken RD (2001) Results of a pilot study involving the use of an antisense oligodeoxynucleotide directed against the insulin-like growth factor type I receptor in malignant astrocytomas. J Clin Oncol 19:2189-2200
4. Antoniades HN, Galanopoulos T, Neville-Golden J, Maxwell M (1992) Expression of insulin-like growth factors I and II and their receptor mRNAs in primary human astrocytomas and meningiomas; in vivo studies using in situ hybridization and immunocytochemistry. Int J Cancer 50:215-222. doi: 10.1002/ijc.2910500210
5. Backlund LM, Nilsson BR, Goike HM, Schmidt EE, Liu L, Ichimura K, Collins VP (2003) Short postoperative survival for glioblastoma patients with a dysfunctional Rb1 pathway in combination with no wild-type PTEN. Clin Cancer Res 9:4151-4158
6. Backlund LM, Nilsson BR, Liu L, Ichimura K, Collins VP (2005) Mutations in Rb1 pathway-related genes are associated with poor prognosis in anaplastic astrocytomas. Br J Cancer 93:124-130. doi: 10.1038/ sj.bjc.6602661
7. Baserga R, Sell C, Porcu P, Rubini M (1994) The role of the IGF-I receptor in the growth and transformation of mammalian cells. Cell Prolif 27:63-71. doi: 10.1111/j.1365-2184.1994.tb01406.x
8. Bridle KR, Li L, O'Neill R, Britton RS, Bacon BR (2006) Coordinate activation of intracellular signaling pathways by insulin-like growth factor-1 and platelet-derived growth factor in rat hepatic stellate cells. J Lab Clin Med 147:234-241. doi: 10.1016/j.lab.2005.12.009
9. Brodt P, Samani A, Navab R (2000) Inhibition of the type I insulin-like growth factor receptor expression and signaling: Novel strategies for antimetastatic therapy. Biochem Pharmacol 60:1101-1107. doi: 10.1016/ S0006-2952(00)00422-6
10. Cantley LC (2002) The phosphoinositide 3-kinase pathway. Science 296:1655-1657. doi: 10.1126/science.296.5573.1655
11. Chakravarti A, Loeffler JS, Dyson NJ (2002) Insulin-like growth factor receptor I mediates resistance to anti-epidermal growth factor receptor therapy in primary human glioblastoma cells through continued activation of phosphoinositide 3-kinase signaling. Cancer Res 62:200-207
12. Chou TC, Talalay P (1984) Quantitative analysis of dose-effect relationships: The combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22:27-55. doi: 10.1016/0065-2571(84)90007-4
13. Cosaceanu D, Budiu RA, Carapancea M, Castro J, Lewensohn R, Dricu A (2007) Ionizing radiation activates IGF-1R triggering a cytoprotective signaling by interfering with Ku-DNA binding and by modulating Ku86 expression via a p38 kinase-dependent mechanism. Oncogene 26:2423-2434. doi: 10.1038/sj.onc.1210037
14. Del Valle L, Enam S, Lassak A, Wang JY, Croul S, Khalili K, Reiss K (2002) Insulin-like growth factor I receptor activity in human medulloblastomas. Clin Cancer Res 8:1822-1830
15. DiBiase SJ, Zeng ZC, Chen R, Hyslop T, Curran WJ Jr, Iliakis G (2000) DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res 60:1245-1253
16. Dimova EY, Moller U, Herzig S, Fink T, Zachar V, Ebbesen P, Kietzmann T (2005) Transcriptional regulation of plasminogen activator inhibitor-1 expression by insulin-like growth factor-1 via MAP kinases and hypoxia-inducible factor-1 in HepG2 cells. Thromb Haemost 93:1176-1184
17. Dricu A, Carlberg M, Wang M, Larsson O (1997) Inhibition of N-linked glycosylation using tunicamycin causes cell death in malignant cells: role of down-regulation of the insulin-like growth factor 1 receptor in induction of apoptosis. Cancer Res 57:543-548
18. Fleming TP, Saxena A, Clark WC, Robertson JT, Oldfield EH, Aaronson SA, Ali IU (1992) Amplification and/or overexpression of platelet-derived growth factor receptors and epidermal growth factor receptor in human glial tumors. Cancer Res 52:4550-4553
19. Fomchenko EI, Holland EC (2007) Platelet-derived growth factor-mediated gliomagenesis and brain tumor recruitment. Neurosurg Clin N Am 18:39-58, viii. doi: 10.1016/j.nec.2006.10.006
20. Foulstone E, Prince S, Zaccheo O, Burns JL, Harper J, Jacobs C, Church D, Hassan AB (2005) Insulin-like growth factor ligands, receptors, and binding proteins in cancer. J Pathol 205:145-153. doi: 10.1002/path.1712
21. Fresno Vara JA, Casado E, de Castro J, Cejas P, Belda-Iniesta C, Gonzalez-Baron M (2004) PI3K/Akt signalling pathway and cancer. Cancer Treat Rev 30:193-204. doi: 10.1016/j.ctrv.2003.07.007
22. Froesch ER, Schmid C, Schwander J, Zapf J (1985) Actions of insulin-like growth factors. Annu Rev Physiol 47:443-467. doi: 10.1146/ annurev.ph.47.030185.002303
23. Germano IM, Ito M, Cho KG, Hoshino T, Davis RL, Wilson CB (1989) Correlation of histopathological features and proliferative potential of gliomas. J Neurosurg 70:701-706
24. Grossman SA, Batara JF (2004) Current management of glioblastoma multiforme. Semin Oncol 31:635-644. doi: 10.1053/j.seminoncol.2004.07.005
25. Hagerstrand D, Hesselager G, Achterberg S, Wickenberg Bolin U, Kowanetz M, Kastemar M, Heldin CH, Isaksson A, Nister M, Ostman A (2006) Characterization of an imatinib-sensitive subset of high-grade human glioma cultures. Oncogene 25:4913-4922. doi: 10.1038/sj.onc.1209497
26. Halatsch ME, Schmidt U, Behnke-Mursch J, Unterberg A, Wirtz CR (2006) Epidermal growth factor receptor inhibition for the treatment of glioblastoma multiforme and other malignant brain tumours. Cancer Treat Rev 32:74-89. doi: 10.1016/j.ctrv.2006.01.003
27. Han VK, D'Ercole AJ, Lund PK (1987) Cellular localization of somatomedin (insulin-like growth factor) messenger RNA in the human fetus. Science 236:193-197. doi: 10.1126/science.3563497
28. Hanada M, Feng J, Hemmings BA (2004) Structure, regulation and function of PKB/AKT - a major therapeutic target. Biochim Biophys Acta 1697:3-16
29. Hoppe BS, Jensen RB, Kirchgessner CU (2000) Complementation of the radiosensitive M059J cell line. Radiat Res 153:125-130. doi: 10.1667/ 0033-7587(2000)153[0125:COTRMC]2.0.CO;2
30. Jiang R, Mircean C, Shmulevich I, Cogdell D, Jia Y, Tabus I, Aldape K, Sawaya R, Bruner JM, Fuller GN, Zhang W (2006) Pathway alterations during glioma progression revealed by reverse phase protein lysate arrays. Proteomics 6:2964-2971. doi: 10.1002/pmic.200500555
31. Johnson TR, Trojan J, Anthony DD, Rudin SD, Tykocinski ML, Ilan J, Ilan J (1994) Gene therapy of rat brain glioblastoma by an episome-based transcriptional cassette expressing antisense IGF-I cDNA. Indian J Biochem Biophys 31:1-13
32. Kasprzak HA, Trojan J, Bierwagen M, Kopinski P, Jarocki P, Bartczak K, Czapiewska J (2006) [Usefulness of the antisense and triplex anti-IGF-1 techniques for postoperative cellular gene therapy of malignant gliomas expressing IGF-1]. Neurol Neurochir Pol 40:509-515 (discussion 516)
33. Khandwala HM, McCutcheon IE, Flyvbjerg A, Friend KE (2000) The effects of insulin-like growth factors on tumorigenesis and neoplastic growth. Endocr Rev 21:215-244. doi: 10.1210/er.21.3.215
34. Kiess W, Lee L, Graham DE, Greenstein L, Tseng LY, Rechler MM, Nissley SP (1989) Rat C6 glial cells synthesize insulin-like growth factor I (IGF-I) and express IGF-I receptors and IGF-II/mannose 6-phosphate receptors. Endocrinology 124:1727-1736
35. Kilic T, Alberta JA, Zdunek PR, Acar M, Iannarelli P, O'Reilly T, Buchdunger E, Black PM, Stiles CD (2000) Intracranial inhibition of platelet-derived growth factor-mediated glioblastoma cell growth by an orally active kinase inhibitor of the 2-phenylaminopyrimidine class. Cancer Res 60:5143-5150
36. Kurmasheva RT, Houghton PJ (2006) IGF-I mediated survival pathways in normal and malignant cells. Biochim Biophys Acta 1766:1-22
37. Lees-Miller SP, Godbout R, Chan DW, Weinfeld M, Day RSIII, Barron GM, Allalunis-Turner J (1995) Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science 267:1183-1185. doi: 10.1126/science.7855602
38. Lokker NA, Sullivan CM, Hollenbach SJ, Israel MA, Giese NA (2002) Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: Evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res 62:3729-3735
39. Longley DB, Johnston PG (2005) Molecular mechanisms of drug resistance. J Pathol 205:275-292. doi: 10.1002/path.1706
40. Ly A, Duc HT, Kalamarides M, Trojan LA, Pan Y, Shevelev A, Francois JC, Noel T, Kane A, Henin D, Anthony DD, Trojan J (2001) Human glioma cells transformed by IGF-I triple helix technology show immune and apoptotic characteristics determining cell selection for gene therapy of glioblastoma. Mol Pathol 54:230-239. doi: 10.1136/mp.54.4.230
41. MacKeigan JP, Taxman DJ, Hunter D, Earp HSIII, Graves LM, Ting JP (2002) Inactivation of the antiapoptotic phosphatidylinositol 3-kinase-Akt pathway by the combined treatment of taxol and mitogen-activated protein kinase inhibition. Clin Cancer Res 8:2091-2099
42. Martin DM, Yee D, Carlson RO, Feldman EL (1992) Gene expression of the insulin-like growth factors and their receptors in human neuroblastoma cell lines. Brain Res Mol Brain Res 15:241-246. doi: 10.1016/ 0169-328X(92)90114-Q
43. Mauro A, Di Sapio A, Mocellini C, Schiffer D (1995) Control of meningioma cell growth by platelet-derived growth factor (PDGF). J Neurol Sci 131:135-143. doi: 10.1016/0022-510X(95)00106-C
44. Mrugala MM, Kesari S, Ramakrishna N, Wen PY (2004) Therapy for recurrent malignant glioma in adults. Expert Rev Anticancer Ther 4:759-782. doi: 10.1586/14737140.4.5.759
45. Nathoo N, Goldlust S, Vogelbaum MA (2004) Epidermal growth factor receptor antagonists: Novel therapy for the treatment of high-grade gliomas. Neurosurgery 54:1480-1488. doi: 10.1227/ 01.NEU.0000125006.88478.F6 (discussion 1488-1489)
46. Nicholas MK, Lukas RV, Jafri NF, Faoro L, Salgia R (2006) Epidermal growth factor receptor - mediated signal transduction in the development and therapy of gliomas. Clin Cancer Res 12:7261-7270. doi: 10.1158/ 1078-0432.CCR-06-0874
47. Nicholson KM, Anderson NG (2002) The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 14:381-395. doi: 10.1016/ S0898-6568(01)00271-6
48. Ozaki K (2007) Targeted molecular strategies for cancer therapy based on the blockade of oncogenic pathways in human tumor cells. Yakugaku Zasshi 127:983-991. doi: 10.1248/yakushi.127.983
49. Perer ES, Madan AK, Shurin A, Zakris E, Romeguera K, Pang Y, Beech DJ (2000) Insulin-like growth factor I receptor antagonism augments response to chemoradiation therapy in colon cancer cells. J Surg Res 94:1-5. doi: 10.1006/jsre.2000.5923
50. Ponten J, Westermark B (1978) Properties of human malignant glioma cells in vitro. Med Biol 56:184-193
51. Pulkkanen KJ, Yla-Herttuala S (2005) Gene therapy for malignant glioma: current clinical status. Mol Ther 12:585-598. doi: 10.1016/ j.ymthe.2005.07.357
52. Resnicoff M, Sell C, Rubini M, Coppola D, Ambrose D, Baserga R, Rubin R (1994) Rat glioblastoma cells expressing an antisense RNA to the insulin-like growth factor-1 (IGF-1) receptor are nontumorigenic and induce regression of wild-type tumors. Cancer Res 54:2218-2222
53. Resnicoff M, Li W, Basak S, Herlyn D, Baserga R, Rubin R (1996) Inhibition of rat C6 glioblastoma tumor growth by expression of insulin-like growth factor I receptor antisense mRNA. Cancer Immunol Immunother 42:64-68. doi: 10.1007/s002620050252
54. Sandberg-Nordqvist AC, Stahlbom PA, Reinecke M, Collins VP, von Holst H, Sara V (1993) Characterization of insulin-like growth factor 1 in human primary brain tumors. Cancer Res 53:2475-2478
55. Sanson M, Laigle-Donadey F, Benouaich-Amiel A (2006) Molecular changes in brain tumors: Prognostic and therapeutic impact. Curr Opin Oncol 18:623-630. doi: 10.1097/01.cco.0000245322.11787.72
56. Schmidberger H, Rave-Frank M, Lehmann JJ, Weiss E, Gerl L, Dettmer N, Glomme S, Hess CF (2003) Lack of interferon beta-induced radiosensitization in four out of five human glioblastoma cell lines. Int J Radiat Oncol Biol Phys 55:1348-1357. doi: 10.1016/ S0360-3016(02)04575-3
57. Shamah SM, Stiles CD, Guha A (1993) Dominant-negative mutants of platelet-derived growth factor revert the transformed phenotype of human astrocytoma cells. Mol Cell Biol 13:7203-7212
58. Soroceanu L, Kharbanda S, Chen R, Soriano RH, Aldape K, Misra A, Zha J, Forrest WF, Nigro JM, Modrusan Z, Feuerstein BG, Phillips HS (2007) Identification of IGF2 signaling through phosphoinositide-3-kinase regulatory subunit 3 as a growth-promoting axis in glioblastoma. Proc Natl Acad Sci USA 104:3466-3471. doi: 10.1073/pnas.0611271104
59. Sourbier C, Lindner V, Lang H, Agouni A, Schordan E, Danilin S, Rothhut S, Jacqmin D, Helwig JJ, Massfelder T (2006) The phosphoinositide 3-kinase/Akt pathway: A new target in human renal cell carcinoma therapy. Cancer Res 66:5130-5142. doi: 10.1158/0008-5472.CAN-05-1469
60. Strawn LM, Mann E, Elliger SS, Chu LM, Germain LL, Niederfellner G, Ullrich A, Shawver LK (1994) Inhibition of glioma cell growth by a truncated platelet-derived growth factor-beta receptor. J Biol Chem 269:21215-21222
61. Tai YT, Fulciniti M, Hideshima T, Song W, Leiba M, Li XF, Rumizen M, Burger P, Morrison A, Podar K, Chauhan D, Tassone P, Richardson P, Munshi NC, Ghobrial I, Anderson KC (2007) Targeting MEK induces myeloma cell cytotoxicity and inhibits osteoclastogenesis. Blood 110(5):1656-1663
62. Trojan J, Blossey BK, Johnson TR, Rudin SD, Tykocinski M, Ilan J, Ilan J (1992) Loss of tumorigenicity of rat glioblastoma directed by episome-based antisense cDNA transcription of insulin-like growth factor I. Proc Natl Acad Sci USA 89:4874-4878. doi: 10.1073/pnas.89.11.4874
63. Trojan J, Johnson TR, Rudin SD, Ilan J, Tykocinski ML, Ilan J (1993) Treatment and prevention of rat glioblastoma by immunogenic C6 cells expressing antisense insulin-like growth factor I RNA. Science 259:94-97. doi: 10.1126/science.8418502
64. Trojan J, Duc HT, Upegui-Gonzalez LC, Hor F, Guo Y, Anthony D, Ilan J (1996) Presence of MHC-I and B-7 molecules in rat and human glioma cells expressing antisense IGF-I mRNA. Neurosci Lett 212:9-12. doi: 10.1016/ 0304-3940(96)12770-1
65. Trojan LA, Kopinski P, Wei MX, Ly A, Glogowska A, Czarny J, Shevelev A, Przewlocki R, Henin D, Trojan J (2002) IGF-I: From diagnostic to triple-helix gene therapy of solid tumors. Acta Biochim Pol 49:979-990
66. Trojan LA, Kopinski P, Mazurek A, Chyczewski L, Ly A, Jarocki P, Niklinski J, Shevelev A, Trzos R, Pan Y, Gitis DJ, Bierwagen M, Czapiewska JL, Wei MX, Michalkiewicz J, Henin D, Popiela T, Evrard F, Kasprzak H, Anthony D, Trojan J (2003) IGF-I triple helix gene therapy of rat and human gliomas. Rocz Akad Med Bialymst 48:18-27
67. Trojan J, Cloix JF, Ardourel MY, Chatel M, Anthony DD (2007) Insulin-like growth factor type I biology and targeting in malignant gliomas. Neuroscience 145:795-811. doi: 10.1016/ j.neuroscience.2007.01.021
68. Vassbotn FS, Andersson M, Westermark B, Heldin CH, Ostman A (1993) Reversion of autocrine transformation by a dominant negative platelet-derived growth factor mutant. Mol Cell Biol 13:4066-4076
69. von Deimling A, Louis DN, Wiestler OD (1995) Molecular pathways in the formation of gliomas. Glia 15:328-338. doi: 10.1002/glia.440150312
70. Wen B, Deutsch E, Marangoni E, Frascona V, Maggiorella L, Abdulkarim B, Chavaudra N, Bourhis J (2001) Tyrphostin AG 1024 modulates radiosensitivity in human breast cancer cells. Br J Cancer 85:2017-2021. doi: 10.1054/bjoc.2001.2171
71. Wong ML, Kaye AH, Hovens CM (2007) Targeting malignant glioma survival signalling to improve clinical outcomes. J Clin Neurosci 14:301-308. doi: 10.1016/j.jocn.2006.11.005
72. Wu CJ, Chen Z, Ullrich A, Greene MI, O'Rourke DM (2000) Inhibition of EGFR-mediated phosphoinositide-3-OH kinase (PI3-K) signaling and glioblastoma phenotype by signal-regulatory proteins (SIRPs). Oncogene 19:3999-4010. doi: 10.1038/sj.onc.1203748
73. Yin D, Tamaki N, Parent AD, Zhang JH (2005) Insulin-like growth factor-I decreased etoposide-induced apoptosis in glioma cells by increasing bcl-2 expression and decreasing CPP32 activity. Neurol Res 27:27-35. doi: 10.1179/016164105X18151