Combining bevacizumab with temozolomide increases the antitumor efficacy of temozolomide in a human glioblastoma orthotopic xenograft model

Neoplasia

Volumn 10, Issue 12, 2008, Pages 1383-1392

  Mathieu, Véronique ^a   De Nève, Nancy ^b   Le Mercier, Marie ^a   Dewelle, Janique ^b   Gaussin, Jean François ^b   Dehoux, Mischael ^b   Kiss, Robert ^a   Lefranc, Florence ^a,c  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b Unibioscreen SA   (Belgium)

^c ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BEVACIZUMAB; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 2; MYC PROTEIN; TEMOZOLOMIDE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIANGIOGENIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CELL MIGRATION; CELL PROLIFERATION; CHRONIC DRUG ADMINISTRATION; COMBINATION CHEMOTHERAPY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSAGE SCHEDULE COMPARISON; DOWN REGULATION; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; ENDOTHELIUM CELL; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; HYPOXIA; IC 50; IN VITRO STUDY; IN VIVO STUDY; MONOTHERAPY; MOUSE; NONHUMAN; ORTHOTOPIC TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SUPERNATANT; TREATMENT DURATION; TUMOR VASCULARIZATION; TUMOR XENOGRAFT; WESTERN BLOTTING;

EID: 57349110570     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.08928     Document Type: Article

References (58)

1. Louis DN (2006). Molecular pathology of malignant gliomas. Annu Rev Pathol Mech Dis 1, 97-117.
2. Ohgaki H and Kleihues P (2007). Genetic pathways to primary and secondary glioblastoma. Am J Pathol 170, 1445-1453.
3. Lefranc F, Brotchi J, and Kiss R (2005). Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 23, 2411-2422.
4. Lefranc F and Kiss R (2008). The sodium pump alpha1 subunit as a potential target to combat apoptosis-resistant glioblastomas. Neoplasia 10, 198-206.
5. Lefranc F, Sadeghi N, Camby I, Metens T, Dewitte O, and Kiss R (2006). Present and potential future issues in glioblastoma treatment. Expert Rev Anticancer Ther 6, 719-732.
6. Lefranc F, Facchini V, and Kiss R (2007). Proautophagic drugs: a novel means to combat apoptosis-resistant cancers, with a special emphasis on glioblastomas. Oncologist 12, 1395-1403.
7. Wemmert S, Ketter R, Rahnenführer J, Beerenwinkel N, Strowitzki M, Feiden W, Hartmann C, Lengauer T, Stockhammer F, Zang KD, et al. (2005). Patients with high-grade gliomas harboring deletions of chromosomes 9p and 10q benefit from temozolomide treatment. Neoplasia 7, 883-893.
8. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, et al. (2005). Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352, 987-996.
9. Chakravarti A, Erkkinen MG, Nestler U, Stupp R, Mehta M, Aldape K, Gilbert MR, Black PM, and Loeffler JS (2006). Temozolomide-mediated radiation enhancement in glioblastoma: a report on underlying mechanisms. Clin Cancer Res 12, 4738-4746.
10. Kanzawa T, Germano IM, Komata T, Itoh H, Konco Y, and Kondo S (2004). Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ 11, 448-457.
11. Roos WP, Batista LF, Naumann SC, Wick W, Weller M, Menck CF, and Kaina B (2007). Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine. Oncogene 26, 186-197.
12. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, et al. (2005). MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352, 997-1003.
13. 6-methylguanine DNA methyltransferase and p53 status predict temozolomide sensitivity in human malignant glioma cells. J Neurochem 96, 766-776.
14. 6-methylguanine induced inhibition of p65 DNA binding. Cancer Res 67, 6889-6898.
15. Hu X, Pandolfi PP, Li Y, Koutcher JA, Rosenblum M, and Holland EC (2005). mTOR promotes survival and astrocytic characteristics induced by Pten/AKT signaling in glioblastoma. Neoplasia 7, 356-368.
16. Hirose Y, Katayama M, Mirzoeva OK, Berger MS, and Pieper RO (2005). Akt activation suppresses Chk2-mediated, methylating agent-induced G2 arrest and protects from temozolomide-induced mitotic catastrophe and cellular senescence. Cancer Res 65, 4861-4869.
17. Kurzen H, Schmitt S, Näher H, and Möhler T (2003). Inhibition of angiogenesis by non-toxic doses of temozolomide. Anticancer Drugs 14, 515-522.
18. Son MJ, Kim JS, Kim MH, Song HS, Kim JT, Kim H, Shin T, Jeon HJ, Lee DS, Park SY, et al. (2006). Combination treatment with temozolomide and thalidomide inhibits tumor growth and angiogenesis in an orthotopic glioma model. Int J Oncol 28, 39-53.
19. Kim JT, Kim JS, Ko KW, Kong DS, Kang CM, Kim MH, Son MJ, Song HS, Shin HJ, Lee DS, et al. (2006). Metronomic treatment of temozolomide inhibits tumor cell growth through reduction of angiogenesis and augmentation of apoptosis in orthotopic models of gliomas. Oncol Rep 16, 33-39.
20. Zhou Q, Guo P, Wang X, Nuthalapati S, and Gallo JM (2007). Preclinical pharmacokinetic and pharmacodynamic evaluation of metronomic and conventional temozolomide dosing regimens. J Pharmacol Exp Ther 321, 265-275.
21. Katayama M, Kawaguchi T, Berger MS, and Pieper RO (2007). DNA damaging agent-induced autophagy produces a cytoprotective adenosine triphosphate surge in malignant glioma cells. Cell Death Differ 14, 548-558.
22. Fisher T, Galanti G, Lavie G, Jacob-Hirsch J, Kventsel I, Zeligson S, Winkler R, Simon AJ, Amariglio N, Rechavi G, et al. (2007). Mechanisms operative in the antitumor activity of temozolomide in glioblastoma multiforme. Cancer J 13, 335-349.
23. Le Mercier M, Lefranc F, Mijatovic T, Debeir O, Haibe-Kains B, Bontempi G, Decaestecker C, Kiss R, and Mathieu V (2008). Evidence of galectin-1 involvement in glioma chemoresistance. Toxicol Appl Pharmacol 229, 172-183.
24. LeMercier M, Mathieu V, Haibe-Kains B, Bontempi G, Mijatovic T, Decaestecker C, Kiss R, and Lefranc F (2008). Knocking down galectin-1 in human Hs683 glioblastoma cells impairs both angiogenesis through ORP150 depletion and endoplasmic reticulum stress responses. J Neuropathol Exp Neurol 67, 456-469.
25. Le QT, Shi G, Cao H, Nelson DW, Wang Y, Chen EY, Zhao S, Kong C, Richardson D, O'Byrne KJ, et al. (2005). Galectin-1: a link between tumor hypoxia and tumor immune privilege. J Clin Oncol 23, 8932-8941.
26. Thijssen VL, Postel R, Brandwijk RJ, Dings RP, Nesmelova I, Satijn S, Verhofstad N, Nakabeppu Y, Baum LG, Bakkers J, et al. (2006). Galectin-1 is essential in tumor angiogenesis and is a target for antiangiogenesis therapy. Proc Natl Acad Sci USA 103, 15975-15980.
27. Camby I, Belot N, Lefranc F, Sadeghi N, de Launoit Y, Kaltner H, Musette S, Darro F, Danguy A, Salmon I, et al. (2002). Galectin-1 modulates human glioblastoma cell migration into the brain through modifications to the actin cytoskeleton and levels of expression of small GTPases. J Neuropathol Exp Neurol 61, 585-596.
28. Norden AD, Young GS, Setayesh K, Muzikansky A, Klufas R, Ross GL, Ciampa AS, Ebbeling LG, Levy B, Drappatz J, et al. (2008). Bevacizumab for recurrent malignant gliomas: efficacy, toxicity, and patterns of recurrence. Neurology 70, 779-787.
29. Mégalizzi V, Mathieu V, Mijatovic T, Gailly P, Debeir O, De Neve N, Van Damme M, Bontempi G, Haibe-Kains B, Decaestecker C, et al. (2007). 4-IBP, a sigma1 receptor agonist, decreases the migration of human cancer cells, including glioblastoma cells, in vitro and sensitizes them in vitro and in vivo to cytotoxic insults of proapoptotic and proautophagic drugs. Neoplasia 9, 358-369.
30. Branle F, Lefranc F, Camby I, Jeuken J, Geurts-Moespot A, Sprenger S, Sweep F, Kiss R, and Salmon I (2002). Evaluation of the efficiency of chemotherapy in in vivo orthotopic models of human glioma cells with and without 1p19q deletions and in C6 rat orthotopic allografts serving for the evaluation of surgery combined with chemotherapy. Cancer 95, 641-655.
31. Lefranc F, Mijatovic T, Mathieu V, Rorive S, Decaestecker C, Debeir O, Brotchi J, Van Ham P, Salmon I, and Kiss R (2004). Characterization of gastrin-induced proangiogenic effects in vivo in orthotopic U373 experimental human glioblastomas and in vitro in human umbilical vein endothelial cells. Clin Cancer Res 10, 8250-8265.
32. Mijatovic T, Mahieu T, Bruyère C, De Nève N, Dewelle J, Simon G, Dehoux MJ, van der Aar E, Haibe-Kains B, Bontempi G, et al. (2008). UNBS5162, a novel naphthalimide that decreases CXCL chemokine expression in experimental prostate cancers. Neoplasia 10, 573-586.
33. Mathieu V, Mijatovic T, van Damme M, and Kiss R (2005). Gastrin exerts pleiotropic effects on human melanoma cell biology. Neoplasia 7, 930-943.
34. Lefranc F, Sadeghi N, Metens T, Brotchi J, Salmon I, and Kiss R (2003). Characterization of gastrin-induced cytostatic effect on cell proliferation in experimental malignant gliomas. Neurosurgery 52, 881-890discussion 890-891.
35. Benezra R, Rafii S, and Lyden D (2001). The Id proteins and angiogenesis. Oncogene 20, 8334-8341.
36. Sakurai D, Tsuchiya N, Yamaguchi A, Okaji Y, Tsuno NH, Kobata T, Takahashi K, and Tokunaga K (2004). Crucial role of inhibitor of DNA binding/differentiation in the vascular endothelial growth factor-induced activation and angiogenic processes of human endothelial cells. J Immunol 173, 5801-5809. Erratum (2005): J Immunol 174, 3818.
37. Löfstedt T, Jögi A, Sigvardsson M, Gradin K, Poellinger L, Påhlman S, and Axelson H (2004). Induction of ID2 expression by hypoxia-inducible factor-1. J Biol Chem 279, 39223-39231.
38. Lasorella A, Rothschild G, Yokota Y, Russell RG, and Iavarone A (2005). ID2 mediates tumor initiation, proliferation, and angiogenesis in Rb mutant mice. Mol Cell Biol 25, 3563-3574.
39. Shchors K, Shchors E, Rostker F, Lawlor ER, Brown-Swigart L, and Evan GI (2006). The Myc-dependent angiogenic switch in tumors is mediated by interleukin 1beta. Genes Dev 20, 2527-2538.
40. Watnick RS, Cheng YN, Rangarajan A, Ince TA, and Weinberg RA (2003). Ras modulates Myc activity to repress thrombospondin-1 expression and increase tumor angiogenesis. Cancer Cell 3, 219-231.
41. Kim JW, Gao P, Liu YC, Semenza GL, and Dang CV (2007). Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol Cell Biol 27, 7381-7393.
42. Huang LE (2008). Carrot and stick: HIF-alpha engages c-Myc in hypoxic adaptation. Cell Death Differ 15, 672-677.
43. Vredenburgh JJ, Desjardins A, Herndon JE II, Marcello J, Reardon DA, Quinn JA, Rich JN, Sathornsumetee S, Gururangan S, Sampson J, et al. (2007). Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 25, 4722-4729.
44. Ali MA, Choy H, Habib AA, and Saha D (2007). SNS-032 prevents tumor cell-induced angiogenesis by inhibiting vascular endothelial growth factor. Neoplasia 9, 370-381.
45. Bergers G and Benjamin LE (2003). Tumorigenesis and the angiogenic switch. Nat Rev Cancer 3, 401-410.
46. Li L, Lin X, Shoemaker AR, Albert DH, Fesik SW, and Shen Y (2006). Hypoxia-inducible factor-1 inhibition in combination with temozolomide treatment exhibits robust antitumor efficacy in vivo. Clin Cancer Res 12, 4747-4754.
47. Devineni D, Klein-Szanto A, and Gallo JM (1996). Uptake of temozolomide in a rat glioma model in the presence and absence of the angiogenesis inhibitor TNP-470. Cancer Res 56, 1983-1987.
48. Ma J, Pulfer S, Li S, Chu J, Reed K, and Gallo JM (2001). Pharmacodynamic-mediated reduction of temozolomide tumor concentrations by the angiogenesis inhibitor TNP-470. Cancer Res 61, 5491-5498.
49. Ma J, Li S, Reed K, Guo P, and Gallo JM (2003). Pharmacodynamic-mediated effects of the angiogenesis inhibitor SU5416 on the tumor disposition of temozolomide in subcutaneous and intracerebral glioma xenograft models. J Pharmacol Exp Ther 305, 833-839.
50. Claes A, Wesseling P, Jeuken J, Maass C, Heerschap A, and Leenders WP (2008). Antiangiogenic compounds interfere with chemotherapy of brain tumors due to vessel normalization. Mol Cancer Ther 7, 71-78.
51. Zhou Q, Guo P, and Gallo JM (2008). Impact of angiogenesis inhibition by sunitinib on tumor distribution of temozolomide. Clin Cancer Res 14, 1540-1549.
52. Gasparini G, Longo R, Fanelli M, and Teicher BA (2005). Combination of antiangiogenic therapy with other anticancer therapies: results, challenges, and open questions. J Clin Oncol 23, 1295-1311.
53. Bäuerle T, Hilbig H, Bartling S, Kiessling F, Kersten A, Schmitt-Gräff A, Kauczor HU, Delorme S, and Berger MR (2008). Bevacizumab inhibits breast cancer-induced osteolysis, surrounding soft tissue metastasis, and angiogenesis in rats as visualized by VCT and MRI. Neoplasia 10, 511-520.
54. Volk LD, Flister MJ, Bivens CM, Stutzman A, Desai N, Trieu V, and Ran S (2008). Nab-paclitaxel efficacy in the orthotopic model of human breast cancer is significantly enhanced by concurrent anti-vascular endothelial growth factor A therapy. Neoplasia 10, 613-623.
55. Kerbel RS (2006). Antiangiogenic therapy: a universal chemosensitization strategy for cancer? Science 312, 1171-1175.
56. Chamberlain MC (2008). Bevacizumab plus irinotecan in recurrent glioblastoma. J Clin Oncol 26, 1012-1013author reply 1013.
57. Nieder C, Wiedenmann N, Andratschke N, and Molls M (2006). Current status of angiogenesis inhibitors combined with radiation therapy. Cancer Treat Rev 32, 348-364.
58. Lai A, Filka E, McGibbon B, Nghiemphu PL, Graham C, Yong WH, Mischel P, Liau LM, Bergsneider M, Pope W, et al. (2008). Phase II pilot study of bevacizumab in combination with temozolomide and regional radiation therapy for up-front treatment of patients with newly diagnosed glioblastoma multiforme: interim analysis of safety and tolerability. Int J Radiat Oncol Biol Phys 71, 1372-1380.