Combined targeting of interleukin-6 and vascular endothelial growth factor potently inhibits glioma growth and invasiveness

International Journal of Cancer

Volumn 125, Issue 5, 2009, Pages 1054-1064

  Saidi, Ahlame ^a   Hagedorn, Martin ^a   Allain, Nathalie ^a   Verpelli, Chiara ^b,c   Sala, Carlo ^b   Bello, Lorenzo ^b,c   Bikfalvi, Andreas ^a   Javerzat, Sophie ^a  

^a INSERM   (France)

^b UNIVERSITY OF MILAN   (Italy)

^c FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

Author keywords

Anti angiogenesis; Combinatory therapy; Glioblastoma; Interleukin 6; Invasion; Microarray; Vascular endothelial growth factor

Indexed keywords

BEVACIZUMAB; INTERLEUKIN 6; KI 67 ANTIGEN; VASCULOTROPIN; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIANGIOGENIC THERAPY; ARTICLE; BIOMICROSCOPY; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CHORIOALLANTOIS; CONTROLLED STUDY; DRUG POTENTIATION; GLIOMA; HUMAN; HUMAN CELL; IMMUNOHISTOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PRIORITY JOURNAL; RNA INTERFERENCE; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL; BRAIN NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; GENE EXPRESSION PROFILING; GLIOMA; HUMANS; IMMUNOENZYME TECHNIQUES; INTERLEUKIN-6; MICE; MICE, NUDE; NEOVASCULARIZATION, PATHOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 67650087998     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24380     Document Type: Article

References (61)

1. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA. Malignant glioma: genetics and biology of a grave matter. Genes Dev 2001;15:1311-33.
2. Vredenburgh JJ, Desjardins A, Herndon JE, II, Dowell JM, Reardon DA, Quinn JA, Rich JN, Sathornsumetee S, Gururangan S, Wagner M, Bigner DD, Friedman AH, et al. Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res 2007;13:1253-9.
3. Willett CG, Boucher Y, di Tomaso E, Duda DG, Munn LL, Tong RT, Chung DC, Sahani DV, Kalva SP, Kozin SV, Mino M, Cohen KS, et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 2004;10:145-7.
4. Bello L, Lucini V, Costa F, Pluderi M, Giussani C, Acerbi F, Carrabba G, Pannacci M, Caronzolo D, Grosso S, Shinkaruk S, Colleoni F, et al. Combinatorial administration of molecules that simultaneously inhibit angiogenesis and invasion leads to increased therapeutic efficacy in mouse models of malignant glioma. Clin Cancer Res 2004;10:4527-37.
5. Hagedorn M, Javerzat S, Gilges D, Meyre A, de Lafarge B, Eichmann A, Bikfalvi A. Accessing key steps of human tumor progression in vivo by using an avian embryo model. Proc Natl Acad Sci USA 2005;102:1643-8.
6. Saidi A, Javerzat S, Bellahcene A, De Vos J, Bello L, Castronovo V, Deprez M, Loiseau H, Bikfalvi A, Hagedorn M. Experimental antiangiogenesis causes upregulation of genes associated with poor survival in glioblastoma. Int J Cancer 2008;122:2187-98.
7. Van Meir E, Sawamura Y, Diserens AC, Hamou MF, de Tribolet N. Human glioblastoma cells release interleukin 6 in vivo and in vitro. Cancer Res 1990;50:6683-8.
8. Rolhion C, Penault-Llorca F, Kemeny JL, Lemaire JJ, Jullien C, Labit-Bouvier C, Finat-Duclos F, Verrelle P. Interleukin-6 overexpression as a marker of malignancy in human gliomas. J Neurosurg 2001;94:97-101.
9. Weissenberger J, Loeffler S, Kappeler A, Kopf M, Lukes A, Afanasieva TA, Aguzzi A, Weis J. IL-6 is required for glioma development in a mouse model. Oncogene 2004;23:3308-16.
10. Trikha M, Corringham R, Klein B, Rossi JF. Targeted anti-interleukin-6 monoclonal antibody therapy for cancer: a review of the rationale and clinical evidence. Clin Cancer Res 2003;9:4653-65.
11. Sebba A. Tocilizumab: the first interleukin-6-receptor inhibitor. Am J Health Syst Pharm 2008;65:1413-8.
12. Hong DS, Angelo LS, Kurzrock R. Interleukin-6 and its receptor in cancer: implications for translational therapeutics. Cancer 2007;110:1911-28.
13. Hagedorn M, Balke M, Schmidt A, Bloch W, Kurz H, Javerzat S, Rousseau B, Wilting J, Bikfalvi A. VEGF coordinates interaction of pericytes and endothelial cells during vasculogenesis and experimental angiogenesis. Dev Dyn 2004;230:23-33.
14. Geronimi F, Richard E, Lamrissi-Garcia I, Lalanne M, Ged C, Redonnet-Vernhet I, Moreau-Gaudry F, de Verneuil H. Lentivirus-mediated gene transfer of uroporphyrinogen III synthase fully corrects the porphyric phenotype in human cells. J Mol Med 2003;81:310-20.
15. Schmidt NO, Ziu M, Carrabba G, Giussani C, Bello L, Sun Y, Schmidt K, Albert M, Black PM, Carroll RS. Antiangiogenic therapy by local intracerebral microinfusion improves treatment efficiency and survival in an orthotopic human glioblastoma model. Clin Cancer Res 2004;10:1255-62.
16. Bello L, Giussani C, Carrabba G, Pluderi M, Lucini V, Pannacci M, Caronzolo D, Tomei G, Villani R, Scaglione F, Carroll RS, Bikfalvi A. Suppression of malignant glioma recurrence in a newly developed animal model by endogenous inhibitors. Clin Cancer Res 2002;8:3539-48.
17. Squire JA, Arab S, Marrano P, Bayani J, Karaskova J, Taylor M, Becker L, Rutka J, Zielenska M. Molecular cytogenetic analysis of glial tumors using spectral karyotyping and comparative genomic hybridization. Mol Diagn 2001;6:93-108.
18. Mulholland PJ, Fiegler H, Mazzanti C, Gorman P, Sasieni P, Adams J, Jones TA, Babbage JW, Vatcheva R, Ichimura K, East P, Poullikas C, et al. Genomic profiling identifies discrete deletions associated with translocations in glioblastoma multiforme. Cell Cycle 2006;5:783-91.
19. Goswami S, Gupta A, Sharma SK. Interleukin-6-mediated autocrine growth promotion in human glioblastoma multiforme cell line U87MG. J Neurochem 1998;71:1837-45.
20. Tchirkov A, Rolhion C, Bertrand S, Dore JF, Dubost JJ, Verrelle P. IL-6 gene amplification and expression in human glioblastomas. Br J Cancer 2001;85:518-22.
21. Tchirkov A, Khalil T, Chautard E, Mokhtari K, Veronese L, Irthum B, Vago P, Kemeny JL, Verrelle P. Interleukin-6 gene amplification and shortened survival in glioblastoma patients. Br J Cancer 2007;96:474-6.
22. Loeffler S, Fayard B, Weis J, Weissenberger J. 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 2005;115:202-13.
23. Wei LH, Kuo ML, Chen CA, Chou CH, Lai KB, Lee CN, Hsieh CY. Interleukin-6 promotes cervical tumor growth by VEGF-dependent angiogenesis via a STAT3 pathway. Oncogene 2003;22:1517-27.
24. Forooghian F, Das B. Anti-angiogenic effects of ribonucleic acid interference targeting vascular endothelial growth factor and hypoxia-inducible factor-1alpha. Am J Ophthalmol 2007;144:761-8.
25. Angelo LS, Kurzrock R. Vascular endothelial growth factor and its relationship to inflammatory mediators. Clin Cancer Res 2007;13:2825-30.
26. Hong X, Jiang F, Kalkanis SN, Zhang ZG, Zhang X, Zheng X, Mikkelsen T, Jiang H, Chopp M. Decrease of endogenous vascular endothelial growth factor may not affect glioma cell proliferation and invasion. J Exp Ther Oncol 2007;6:219-29.
27. Kayaselcuk F, Zorludemir S, Gumurduhu D, Zeren H, Erman T. PCNA and Ki-67 in central nervous system tumors: correlation with the histological type and grade. J Neurooncol 2002;57:115-21.
28. Nafe R, Franz K, Schlote W, Schneider B. Morphology of tumor cell nuclei is significantly related with survival time of patients with glioblastomas. Clin Cancer Res 2005;11:2141-8.
29. Demuth T, Rennert JL, Hoelzinger DB, Reavie LB, Nakada M, Beaudry C, Nakada S, Anderson EM, Henrichs AN, McDonough WS, Holz D, Joy A, et al. Glioma cells on the run - the migratory transcriptome of 10 human glioma cell lines. BMC Genomics 2008;9:54.
30. Mentlein R, Forstreuter F, Mehdorn HM, Held-Feindt J. Functional significance of vascular endothelial growth factor receptor expression on human glioma cells. J Neurooncol 2004;67:9-18.
31. Yoo SA, Bae DG, Ryoo JW, Kim HR, Park GS, Cho CS, Chae CB, Kim WU. Arginine-rich anti-vascular endothelial growth factor (anti-VEGF) hexapeptide inhibits collagen-induced arthritis and VEGF-stimulated productions of TNF-alpha and IL-6 by human monocytes. J Immunol 2005;174:5846-55.
32. Wicki A, Lehembre F, Wick N, Hantusch B, Kerjaschki D, Christofori G. Tumor invasion in the absence of epithelial-mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 2006;9:261-72.
33. Wicki A, Christofori G. The potential role of podoplanin in tumour invasion. Br J Cancer 2007;96:1-5.
34. Yamaguchi Y, Mann DM, Ruoslahti E. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 1990;346:281-4.
35. Merle B, Durussel L, Delmas PD, Clezardin P. Decorin inhibits cell migration through a process requiring its glycosaminoglycan side chain. J Cell Biochem 1999;75:538-46.
36. Engel S, Isenmann S, Stander M, Rieger J, Bahr M, Weller M. Inhibition of experimental rat glioma growth by decorin gene transfer is associated with decreased microglial infiltration. J Neuroimmunol 1999;99:13-8.
37. Biglari A, Bataille D, Naumann U, Weller M, Zirger J, Castro MG, Lowenstein PR. Effects of ectopic decorin in modulating intracranial glioma progression in vivo, in a rat syngeneic model. Cancer Gene Ther 2004;11:721-32.
38. Jing C, El-Ghany MA, Beesley C, Foster CS, Rudland PS, Smith P, Ke Y. Tazarotene-induced gene 1 (TIG1) expression in prostate carcinomas and its relationship to tumorigenicity. J Natl Cancer Inst 2002;94:482-90.
39. Rambow F, Malek O, Geffrotin C, Leplat JJ, Bouet S, Piton G, Hugot K, Bevilacqua C, Horak V, Vincent-Naulleau S. Identification of differentially expressed genes in spontaneously regressing melanoma using the MeLiM swine model. Pigment Cell melanoma Res 2008;21:147-61.
40. Mertsch S, Schmitz N, Jeibmann A, Geng JG, Paulus W, Senner V. Slit2 involvement in glioma cell migration is mediated by Robo1 receptor. J Neurooncol 2008;87:1-7.
41. Clifford N, Smith LM, Powell J, Gattenlohner S, Marx A, O'Connor R. The EphA3 receptor is expressed in a subset of rhabdomyosarcoma cell lines and suppresses cell adhesion and migration. J Cell Biochem 2008;105:1250-9.
42. Kanno A, Satoh K, Masamune A, Hirota M, Kimura K, Umino J, Hamada S, Satoh A, Egawa S, Motoi F, Unno M, Shimosegawa T. Periostin, secreted from stromal cells, has biphasic effect on cell migration and correlates with the epithelial to mesenchymal transition of human pancreatic cancer cells. Int J Cancer 2008;122:2707-18.
43. Casanovas O, Hicklin DJ, Bergers G, Hanahan D. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005;8:299-309.
44. Kunkel P, Ulbricht U, Bohlen P, Brockmann MA, Fillbrandt R, Stavrou D, Westphal M, Lamszus K. Inhibition of glioma angiogenesis and growth in vivo by systemic treatment with a monoclonal antibody against vascular endothelial growth factor receptor-2. Cancer Res 2001;61:6624-8.
45. Rubenstein JL, Kim J, Ozawa T, Zhang M, Westphal M, Deen DF, Shuman MA. Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia 2000;2:306-14.
46. Niola F, Evangelisti C, Campagnolo L, Massalini S, Bue MC, Mangiola A, Masotti A, Maira G, Farace MG, Ciafre SA. A plasmid-encoded VEGF siRNA reduces glioblastoma angiogenesis and its combination with interleukin-4 blocks tumor growth in a xenograft mouse model. Cancer Biol Ther 2006;5:174-9.
47. Du R, Lu KV, Petritsch C, Liu P, Ganss R, Passegue E, Song H, Vandenberg S, Johnson RS, Werb Z, Bergers G. HIF1alpha induces the recruitment of bone marrow-derived vascular modulatory cells to regulate tumor angiogenesis and invasion. Cancer Cell 2008;13:206-20.
48. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, Kozak KR, Cahill DP, Chen PJ, Zhu M, Ancukiewicz M, Mrugala MM, et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007;11:83-95.
49. Hagedorn M, Delugin M, Abraldes I, Allain N, Belaud-Rotureau MA, Turmo M, Prigent C, Loiseau H, Bikfalvi A, Javerzat S. FBXW7/hCDC4 controls glioma cell proliferation in vitro and is a prognostic marker for survival in glioblastoma patients. Cell Div 2007;2:9.
50. Klein A, Reichardt W, Jung V, Zang KD, Meese E, Urbschat S. Overexpression and amplification of STK15 in human gliomas. Int J Oncol 2004;25:1789-94.
51. Zeng WF, Navaratne K, Prayson RA, Weil RJ. Aurora B expression correlates with aggressive behaviour in glioblastoma multiforme. J Clin Pathol 2007;60:218-21.
52. Jung JE, Kim TK, Lee JS, Oh SY, Kwak S, Jin X, Sohn JY, Song MK, Sohn YW, Lee SY, Pian X, Lee JB, et al. Survivin inhibits antigrowth effect of p53 activated by aurora B. Biochem Biophys Res Commun 2005;336:1164-71.
53. Konnikova L, Kotecki M, Kruger MM, Cochran BH. Knockdown of STAT3 expression by RNAi induces apoptosis in astrocytoma cells. BMC Cancer 2003;3:23.
54. Zhang XH, Rao M, Loprieato JA, Hong JA, Zhao M, Chen GZ, Humphries AE, Nguyen DM, Trepel JB, Yu X, Schrump DS. Aurora A, Aurora B and survivin are novel targets of transcriptional regulation by histone deacetylase inhibitors in non-small cell lung cancer. Cancer Biol Ther 2008;7:1388-97.
55. Mottet D, Pirotte S, Lamour V, Hagedorn M, Javerzat S, Bikfalvi A, Bellahcene A, Verdin E, Castronovo V. HDAC4 represses p21(WAF1/Cip1) expression in human cancer cells through a Sp1-dependent, p53-independent mechanism. Oncogene 2009;28:243-56.
56. Yu H, Konigshoff M, Jayachandran A, Handley D, Seeger W, Kaminski N, Eickelberg O. Transgelin is a direct target of TGF-beta/Smad3-dependent epithelial cell migration in lung fibrosis. Faseb J 2008;22:1778-89.
57. Norden AD, Drappatz J, Wen PY. Antiangiogenic therapy in malignant gliomas. Curr Opin Oncol 2008;20:652-61.
58. Sansone P, Storci G, Tavolari S, Guarnieri T, Giovannini C, Taffurelli M, Ceccarelli C, Santini D, Paterini P, Marcu KB, Chieco P, Bonafe M. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J Clin Invest 2007;117:3988-4002.
59. Gao SP, Mark KG, Leslie K, Pao W, Motoi N, Gerald WL, Travis WD, Bornmann W, Veach D, Clarkson B, Bromberg JF. Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J Clin Invest 2007;117:3846-56.
60. Abou-Ghazal M, Yang DS, Qiao W, Reina-Ortiz C, Wei J, Kong LY, Fuller GN, Hiraoka N, Priebe W, Sawaya R, Heimberger AB. The incidence, correlation with tumor-infiltrating inflammation, and prognosis of phosphorylated STAT3 expression in human gliomas. Clin Cancer Res 2008;14:8228-35.
61. Szatmari T, Lumniczky K, Desaknai S, Trajcevski S, Hidvegi EJ, Hamada H, Safrany G. Detailed characterization of the mouse glioma 261 tumor model for experimental glioblastoma therapy. Cancer Sci 2006;97:546-53.