Inhibition of the JAK-2/STAT3 signaling pathway impedes the migratory and invasive potential of human glioblastoma cells

Journal of Neuro-Oncology

Volumn 101, Issue 3, 2011, Pages 393-403

  Senft, Christian ^a   Priester, Maike ^a   Polacin, Margareth ^a   Schröder, Katrin ^a   Seifert, Volker ^a   Kögel, Donat ^a   Weissenberger, Jakob ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

Glioblastoma; Invasion; Migration; STAT3

Indexed keywords

GELATINASE A; GELATINASE B; JANUS KINASE 2; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; STAT3 PROTEIN;

ANGIOGENESIS; ARTICLE; CANCER CELL CULTURE; CELL GROWTH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ZYMOGRAPHY;

APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; GLIOBLASTOMA; HUMANS; JANUS KINASE 2; MATRIX METALLOPROTEINASE 2; NEOPLASM INVASIVENESS; PHOSPHORYLATION; PTEN PHOSPHOHYDROLASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYRPHOSTINS; UMBILICAL VEINS; WOUND HEALING;

EID: 79952189765     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-010-0273-y     Document Type: Article

References (34)

1. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996 (Pubitemid 40349501)
2. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, Chin L, DePinho RA, Cavenee WK (2007) Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 21:2683-2710 (Pubitemid 350070717)
3. Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624-1636 (Pubitemid 46594118)
4. Claes A, Idema AJ, Wesseling P (2007) Diffuse glioma growth: a guerilla war. Acta Neuropathol 114:443-458 (Pubitemid 47521501)
5. Dauer DJ, Ferraro B, Song L, Yu B, Mora L, Buettner R, Enkemann S, Jove R, Haura EB (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24:3397-3408 (Pubitemid 40756241)
6. Brantley EC, Benveniste EN (2008) Signal transducer and activator of transcription-3: a molecular hub for signaling pathways in gliomas. Mol Cancer Res 6:675-684
7. Weissenberger J, Loeffler S, Kappeler A, Kopf M, Lukes A, Afanasieva TA, Aguzzi A, Weis J (2004) IL-6 is required for glioma development in a mouse model. Oncogene 23:3308-3316 (Pubitemid 38669820)
8. Lo HW, Cao X, Zhu H, Ali-Osman F (2008) Constitutively activated STAT3 frequently coexpresses with epidermal growth factor receptor in high-grade gliomas and targeting STAT3 sensitizes them to Iressa and alkylators. Clin Cancer Res 14:6042-6054
9. Loeffler S, Fayard B, Weis J, Weissenberger J (2005) Interleukin-6 induces transcriptional activation of vascular endothelial growth factor (VEGF) in astrocytes in vivo and regulates VEGF promoter activity in glioblastoma cells via direct interaction between STAT3 and Sp1. Int J Cancer 115:202-213 (Pubitemid 40586728)
10. Yu H, Pardoll D, Jove R (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev 9:798-809
11. Schlessinger K, Levy DE (2005) Malignant transformation but not normal cell growth depends on signal transducer and activator of transcription 3. Cancer Res 65:5828-5834 (Pubitemid 40911187)
12. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif) 25:402-408
13. Ponce ML (2001) In vitro matrigel angiogenesis assays. In: Murray JC (ed) Angiogenesis protocols. Humana Press, Totowa, NJ, pp 205-208
14. Shingu T, Yamada K, Hara N, Moritake K, Osago H, Terashima M, Uemura T, Yamasaki T, Tsuchiya M (2003) Growth inhibition of human malignant glioma cells induced by the PI3-K-specific inhibitor. J Neurosurg 98:154-161 (Pubitemid 36050459)
15. Meydan N, Grunberger T, Dadi H, Shahar M, Arpaia E, Lapidot Z, Leeder JS, Freedman M, Cohen A, Gazit A, Levitzki A, Roifman CM (1996) Inhibition of acute lymphoblastic leukaemia by a Jak-2 inhibitor. Nature 379:645-648 (Pubitemid 26053453)
16. Bollrath J, Greten FR (2009) IKK/NF-kappaB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis. EMBO Rep 10:1314-1319
17. Judge A, MacLachlan I (2008) Overcoming the innate immune response to small interfering RNA. Hum Gene Ther 19:111-124 (Pubitemid 351271512)
18. Rahaman SO, Harbor PC, Chernova O, Barnett GH, Vogelbaum MA, Haque SJ (2002) Inhibition of constitutively active Stat3 suppresses proliferation and induces apoptosis in glioblastoma multiforme cells. Oncogene 21:8404-8413 (Pubitemid 36054883)
19. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C, Darnell JE Jr (1999) Stat3 as an oncogene. Cell 98:295-303 (Pubitemid 29380565)
20. Gu J, Li G, Sun T, Su Y, Zhang X, Shen J, Tian Z, Zhang J (2008) Blockage of the STAT3 signaling pathway with a decoy oligonucleotide suppresses growth of human malignant glioma cells. J Neurooncol 89:9-17
21. Lopez-Gines C, Gil-Benso R, Benito R, Mata M, Pereda J, Sastre J, Roldan P, Gonzalez-Darder J, Cerda-Nicolas M (2008) The activation of ERK1/2 MAP kinases in glioblastoma pathobiology and its relationship with EGFR amplification. Neuropathology 28:507-515
22. Huang S (2007) Regulation of metastases by signal transducer and activator of transcription 3 signaling pathway: clinical implications. Clin Cancer Res 13:1362-1366
23. Silbergeld DL, Rostomily RC, Alvord EC Jr (1991) The cause of death in patients with glioblastoma is multifactorial: clinical factors and autopsy findings in 117 cases of supratentorial glioblastoma in adults. J Neurooncol 10:179-185
24. Wick W, Stupp R, Beule AC, Bromberg J, Wick A, Ernemann U, Platten M, Marosi C, Mason WP, van den Bent M, Weller M, Rorden C, Karnath HO (2008) A novel tool to analyze MRI recurrence patterns in glioblastoma. Neuro Oncol 10:1019-1024
25. Abdulghani J, Gu L, Dagvadorj A, Lutz J, Leiby B, Bonuccelli G, Lisanti MP, Zellweger T, Alanen K, Mirtti T, Visakorpi T, Bubendorf L, Nevalainen MT (2008) Stat3 promotes metastatic progression of prostate cancer. Am J Pathol 172:1717-1728 (Pubitemid 351793362)
26. Carro MS, Lim WK, Alvarez MJ, Bollo RJ, Zhao X, Snyder EY, Sulman EP, Anne SL, Doetsch F, Colman H, Lasorella A, Aldape K, Califano A, Iavarone A (2010) The transcriptional network for mesenchymal transformation of brain tumours. Nature 463: 318-325
27. Rao JS (2003) Molecular mechanisms of glioma invasiveness: the role of proteases. Nat Rev 3:489-501
28. Xie TX, Wei D, Liu M, Gao AC, Ali-Osman F, Sawaya R, Huang S (2004) Stat3 activation regulates the expression of matrix metalloproteinase-2 and tumor invasion and metastasis. Oncogene 23:3550-3560 (Pubitemid 38658421)
29. de la Iglesia N, Konopka G, Lim KL, Nutt CL, Bromberg JF, Frank DA, Mischel PS, Louis DN, Bonni A (2008) Deregulation of a STAT3-interleukin 8 signaling pathway promotes human glioblastoma cell proliferation and invasiveness. J Neurosci 28:5870-5878
30. Shariftabrizi A, Khorramizadeh MR, Saadat F, Alimoghadam K, Safavifar F, Ebrahimkhani MR (2005) Concomitant reduction of matrix metalloproteinase-2 secretion and intracellular reactive oxygen species following anti-sense inhibition of telomerase activity in PC-3 prostate carcinoma cells. Mol Cell Biochem 273:109-116 (Pubitemid 40766791)
31. Kargiotis O, Chetty C, Gondi CS, Tsung AJ, Dinh DH, Gujrati M, Lakka SS, Kyritsis AP, Rao JS (2008) 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 27:4830-4840
32. Munaut C, Noel A, Hougrand O, Foidart JM, Boniver J, Deprez M (2003) Vascular endothelial growth factor expression correlates with matrix metalloproteinases MT1-MMP, MMP-2 and MMP-9 in human glioblastomas. Int J Cancer 106:848-855 (Pubitemid 37071662)
33. Schaefer LK, Ren Z, Fuller GN, Schaefer TS (2002) Constitutive activation of Stat3alpha in brain tumors: localization to tumor endothelial cells and activation by the endothelial tyrosine kinase receptor (VEGFR-2). Oncogene 21:2058-2065 (Pubitemid 34270894)
34. Birner P, Toumangelova-Uzeir K, Natchev S, Guentchev M (2010) STAT3 tyrosine phosphorylation influences survival in glioblastoma. J Neuro Oncol. doi:10.1007/s11060-010-0195-8