Novel anti-glioblastoma agents and therapeutic combinations identified from a collection of FDA approved drugs

Journal of Translational Medicine

Volumn 12, Issue 1, 2014, Pages

  Jiang, Pengfei ^a   Mukthavavam, Rajesh ^a   Chao, Ying ^a   Bharati, Ila S ^a   Fogal, Valentina ^a   Pastorino, Sandra ^a   Cong, Xiuli ^a   Nomura, Natsuko ^a   Gallagher, Matt ^a   Abbasi, Taher ^c   Vali, Shireen ^c   Pingle, Sandeep C ^a   Makale, Milan ^a   Kesari, Santosh ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CellWorks Inc   (United States)

Author keywords

Drug screening; Glioblastoma; Patient derived glioblastoma cell lines; Rational combination

Indexed keywords

2(1H) PYRIMIDINONE; 5 NONYLOXYTRYPTAMINE; CERIVASTATIN; CHLORO 2' DEOXYADENOSINE; CLOFAZIMINE; DACTINOMYCIN; DEOXYADENOSINE DERIVATIVE; DOCETAXEL; DOXORUBICIN; EPIRUBICIN; FLUBENDAZOLE; HOMOHARRINGTONINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IDARUBICIN; IRINOTECAN; ITRACONAZOLE; MULTIDRUG RESISTANCE PROTEIN 1; NAVELBINE; NISOLDIPINE; PITAVASTATIN; PYRIMIDINONE DERIVATIVE; SEROTONIN UPTAKE INHIBITOR; SERTRALINE; TOPOTECAN; TRIPTOLIDE; UNCLASSIFIED DRUG; VINCRISTINE; VINDESINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL CULTURE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER STEM CELL; CONTROLLED STUDY; DOSE RESPONSE; DRUG MEGADOSE; DRUG POTENCY; DRUG POTENTIATION; DRUG SCREENING; FOOD AND DRUG ADMINISTRATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LOW DRUG DOSE; MOUSE; NONHUMAN; PROTEIN GLYCOSYLATION;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; AUTOPHAGY; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CAMPTOTHECIN; CELL LINE, TUMOR; CELL SURVIVAL; DISEASE-FREE SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; DRUG APPROVAL; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MICE; MICE, NUDE; NEOPLASTIC STEM CELLS; P-GLYCOPROTEIN; QUINOLINES; SPHEROIDS, CELLULAR; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84892455642     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-12-13     Document Type: Article

References (53)

1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med 2008, 359:492-507. 10.1056/NEJMra0708126, 18669428.
2. Duffner PK. Risk factors for cognitive decline in children treated for brain tumors. Eur J Paediatr Neurol 2010, 14:106-115. 10.1016/j.ejpn.2009.10.005, 19931477.
3. Salacz ME, Watson KR, Schomas DA. Glioblastoma: Part I. Current state of affairs. Mo Med 2011, 108:187-194.
4. Fueyo J, Gomez-Manzano C, Yung WK. Advances in translational research in neuro-oncology. Arch Neurol 2011, 68:303-308. 3109723, 21059986.
5. Sharma A, Jacob A, Tandon M, Kumar D. Orphan drug: development trends and strategies. J Pharm Bioallied Sci 2010, 2:290-299. 10.4103/0975-7406.72128, 2996062, 21180460.
6. Omuro AM, Faivre S, Raymond E. Lessons learned in the development of targeted therapy for malignant gliomas. Mol Cancer Ther 2007, 6:1909-1919. 10.1158/1535-7163.MCT-07-0047, 17620423.
7. Jeon SH, Kim SH, Kim Y, Kim YS, Lim Y, Lee YH, Shin SY. The tricyclic antidepressant imipramine induces autophagic cell death in U-87MG glioma cells. Biochem Biophys Res Commun 2011, 413:311-317. 10.1016/j.bbrc.2011.08.093, 21889492.
8. Kast RE. Glioblastoma: synergy of growth promotion between CCL5 and NK-1R can be thwarted by blocking CCL5 with miraviroc, an FDA approved anti-HIV drug and blocking NK-1R with aprepitant, an FDA approved anti-nausea drug. J Clin Pharm Ther 2010, 35:657-663. 10.1111/j.1365-2710.2009.01148.x, 21054456.
9. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004, 64:7011-7021. 10.1158/0008-5472.CAN-04-1364, 15466194.
10. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401. 10.1038/nature03128, 15549107.
11. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, Bayani J, Head R, Lee M, Bernstein M, et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4:568-580. 10.1016/j.stem.2009.03.014, 19497285.
12. Diamandis P, Wildenhain J, Clarke ID, Sacher AG, Graham J, Bellows DS, Ling EK, Ward RJ, Jamieson LG, Tyers M, et al. Chemical genetics reveals a complex functional ground state of neural stem cells. Nat Chem Biol 2007, 3:268-273. 10.1038/nchembio873, 17417631.
13. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006, 9:391-403. 10.1016/j.ccr.2006.03.030, 16697959.
14. Reynolds BA, Rietze RL. Neural stem cells and neurospheres-re-evaluating the relationship. Nat Methods 2005, 2:333-336. 10.1038/nmeth758, 15846359.
15. Shen G, Shen F, Shi Z, Liu W, Hu W, Zheng X, Wen L, Yang X. Identification of cancer stem-like cells in the C6 glioma cell line and the limitation of current identification methods. In Vitro Cell Dev Biol Anim 2008, 44:280-289. 10.1007/s11626-008-9115-z, 18594936.
16. Chen J, McKay RM, Parada LF. Malignant glioma: lessons from genomics, mouse models, and stem cells. Cell 2012, 149:36-47. 10.1016/j.cell.2012.03.009, 3719882, 22464322.
17. Vik-Mo EO, Sandberg C, Joel M, Stangeland B, Watanabe Y, Mackay-Sim A, Moe MC, Murrell W, Langmoen IA. A comparative study of the structural organization of spheres derived from the adult human subventricular zone and glioblastoma biopsies. Exp Cell Res 2011, 317:1049-1059. 10.1016/j.yexcr.2010.12.022, 21199649.
18. Reardon DA, Friedman HS, Powell JB, Gilbert M, Yung WK. Irinotecan: promising activity in the treatment of malignant glioma. Oncology (Williston Park) 2003, 17:9-14.
19. Prados MD, Lamborn K, Yung WK, Jaeckle K, Robins HI, Mehta M, Fine HA, Wen PY, Cloughesy T, Chang S, et al. A phase 2 trial of irinotecan (CPT-11) in patients with recurrent malignant glioma: a North American Brain Tumor Consortium study. Neuro Oncol 2006, 8:189-193. 10.1215/15228517-2005-010, 1871932, 16533878.
20. Yanae M, Tsubaki M, Satou T, Itoh T, Imano M, Yamazoe Y, Nishida S. Statin-induced apoptosis via the suppression of ERK1/2 and Akt activation by inhibition of the geranylgeranyl-pyrophosphate biosynthesis in glioblastoma. J Exp Clin Cancer Res 2011, 30:74. 10.1186/1756-9966-30-74, 3163617, 21831290.
21. Hindler K, Cleeland CS, Rivera E, Collard CD. The role of statins in cancer therapy. Oncologist 2006, 11:306-315. 10.1634/theoncologist.11-3-306, 16549815.
22. Brown JM, Giaccia AJ. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy. Cancer Res 1998, 58:1408-1416.
23. Juillerat-Jeanneret L. The targeted delivery of cancer drugs across the blood-brain barrier: chemical modifications of drugs or drug-nanoparticles?. Drug Discov Today 2008, 13:1099-1106. 10.1016/j.drudis.2008.09.005, 18848640.
24. Yu SP, Yang XJ, Zhang B, Ming HL, Chen C, Ren BC, Liu ZF, Liu B. Enhanced invasion in vitro and the distribution patterns in vivo of CD133+ glioma stem cells. Chin Med J (Engl) 2011, 124:2599-2604.
25. Claes A, Wesseling P, Jeuken J, Maass C, Heerschap A, Leenders WP. Antiangiogenic compounds interfere with chemotherapy of brain tumors due to vessel normalization. Mol Cancer Ther 2008, 7:71-78. 10.1158/1535-7163.MCT-07-0552, 18187807.
26. Nicolazzo JA, Charman SA, Charman WN. Methods to assess drug permeability across the blood-brain barrier. J Pharm Pharmacol 2006, 58:281-293. 10.1211/jpp.58.3.0001, 16536894.
27. Fan Y, Unwalla R, Denny RA, Di L, Kerns EH, Diller DJ, Humblet C. Insights for predicting blood-brain barrier penetration of CNS targeted molecules using QSPR approaches. J Chem Inf Model 2010, 50:1123-1133. 10.1021/ci900384c, 20578728.
28. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 2006, 58(3):621-681. 10.1124/pr.58.3.10, 16968952.
29. Mathieu V, De Neve N, Le Mercier M, Dewelle J, Gaussin JF, Dehoux M, Kiss R, Lefranc F. Combining bevacizumab with temozolomide increases the antitumor efficacy of temozolomide in a human glioblastoma orthotopic xenograft model. Neoplasia 2008, 10:1383-1392. 2586689, 19048117.
30. Mrugala MM, Chamberlain MC. Mechanisms of disease: temozolomide and glioblastoma-look to the future. Nat Clin Pract Oncol 2008, 5:476-486. 10.1038/ncponc1155, 18542116.
31. Yost SE, Pastorino S, Rozenzhak S, Smith EN, Chao YS, Jiang P, Kesari S, Frazer KA, Harismendy O. High-resolution mutational profiling suggests the genetic validity of glioblastoma patient-derived pre-clinical models. PLoS One 2013, 8:e56185. 10.1371/journal.pone.0056185, 3575368, 23441165.
32. Fukumura D, Jain RK. Tumor microenvironment abnormalities: causes, consequences, and strategies to normalize. J Cell Biochem 2007, 101:937-949. 10.1002/jcb.21187, 17171643.
33. Gonzalez-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquere S, Eskelinen EL, Pierron G, Saftig P, Kroemer G. The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J Cell Sci 2005, 118:3091-3102. 10.1242/jcs.02447, 15985464.
34. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005, 25:1025-1040. 10.1128/MCB.25.3.1025-1040.2005, 543994, 15657430.
35. Shi R, Weng J, Zhao L, Li XM, Gao TM, Kong J. Excessive autophagy contributes to neuron death in cerebral ischemia. CNS Neurosci Ther 2012, 18:250-260. 10.1111/j.1755-5949.2012.00295.x, 22449108.
36. Whitacre CM, Zborowska E, Willson JK, Berger NA. Detection of poly(ADP-ribose) polymerase cleavage in response to treatment with topoisomerase I inhibitors: a potential surrogate end point to assess treatment effectiveness. Clin Cancer Res 1999, 5:665-672.
37. Nabors MW, Griffin CA, Zehnbauer BA, Hruban RH, Phillips PC, Grossman SA, Brem H, Colvin OM. Multidrug resistance gene (MDR1) expression in human brain tumors. J Neurosurg 1991, 75:941-946. 10.3171/jns.1991.75.6.0941, 1682428.
38. Takeba Y, Sekine S, Kumai T, et al. Irinotecan-induced apoptosis is inhibited by increased P-glycoprotein expression and decreased p53 in human hepatocellular carcinoma cells. Biol Pharm Bull 2007, 30:1400-1406. 10.1248/bpb.30.1400, 17666793.
39. Nakai E, Park K, Yawata T, Chihara T, Kumazawa A, Nakabayashi H, Shimizu K. Enhanced MDR1 expression and chemoresistance of cancer stem cells derived from glioblastoma. Cancer Invest 2009, 27:901-908. 10.3109/07357900801946679, 19832037.
40. Shirasaka Y, Suzuki K, Shichiri M, Nakanishi T, Tamai I. Intestinal absorption of HMG-CoA reductase inhibitor pitavastatin mediated by organic anion transporting polypeptide and P-glycoprotein/multidrug resistance 1. Drug Metab Pharmacokinet 2011, 26:171-179. 10.2133/dmpk.DMPK-10-RG-073, 21206133.
41. Schinkel AH, Kemp S, Dolle M, Rudenko G, Wagenaar E. N-glycosylation and deletion mutants of the human MDR1 P-glycoprotein. J Biol Chem 1993, 268:7474-7481.
42. Nielsen SF, Nordestgaard BG, Bojesen SE. Statin use and reduced cancer- related mortality. N Engl J Med 2012, 367:1792-1802. 10.1056/NEJMoa1201735, 23134381.
43. Thurnher M, Nussbaumer O, Gruenbacher G. Novel aspects of mevalonate pathway inhibitors as antitumor agents. Clin Cancer Res 2012, 18:3524-3531. 10.1158/1078-0432.CCR-12-0489, 22529099.
44. Goldstein JL, Brown MS. Regulation of the mevalonate pathway. Nature 1990, 343:425-430. 10.1038/343425a0, 1967820.
45. McCarty MF. Suppression of dolichol synthesis with isoprenoids and statins may potentiate the cancer-retardant efficacy of IGF-I down-regulation. Med Hypotheses 2001, 56:12-16. 10.1054/mehy.2000.1073, 11133248.
46. Williams AB, Li L, Nguyen B, Brown P, Levis M, Small D. Fluvastatin inhibits FLT3 glycosylation in human and murine cells and prolongs survival of mice with FLT3/ITD leukemia. Blood 2012, 120:3069-3079. 10.1182/blood-2012-01-403493, 3471516, 22927251.
47. Guo D, Reinitz F, Youssef M, Hong C, Nathanson D, Akhavan D, Kuga D, Amzajerdi AN, Soto H, Zhu S, et al. An LXR agonist promotes GBM cell death through inhibition of an EGFR/AKT/SREBP-1/LDLR-dependent pathway. Cancer Discov 2011, 1:442-456. 10.1158/2159-8290.CD-11-0102, 3207317, 22059152.
48. Shibata Y, Matsumura A, Yoshida F, Yamamoto T, Nakai K, Nose T, Sakata I, Nakajima S. Competitive uptake of porphyrin and LDL via the LDL receptor in glioma cell lines: flow cytometric analysis. Cancer Lett 2001, 166:79-87. 10.1016/S0304-3835(00)00717-5, 11295290.
49. Tsuboi Y, Kurimoto M, Nagai S, et al. Induction of autophagic cell death and radiosensitization by the pharmacological inhibition of nuclear factor-kappa B activation in human glioma cell lines. J Neurosurg 2009, 110:594-604. 10.3171/2008.8.JNS17648, 19046042.
50. Weekes J, Lam AK-Y, Sebesan S, Ho Y-H. Irinotecan therapy and molecular targets in colorectal cancer: a systemic review. World J Gastroenterol 2009, 15:3597-3602. 10.3748/wjg.15.3597, 2721232, 19653336.
51. Vredenburgh JJ, Desjardins A, Reardon DA, Friedman HS. Experience with irinotecan for the treatment of malignant glioma. Neuro Oncol 2009, 11:80-91. 2718962, 18784279.
52. Hahn KK, Wolff JJ, Kolesar JM. Pharmacogenetics and irinotecan therapy. Am J Health Syst Pharm 2006, 63:2211-2217. 10.2146/ajhp060155, 17090741.
53. de Jong FA, de Jonge MJ, Verweij J, Mathijssen RH. Role of pharmacogenetics in irinotecan therapy. Cancer Lett 2006, 234:90-106. 10.1016/j.canlet.2005.04.040, 16343744.