Sequential dosing in chemosensitization: Targeting the PI3K/Akt/mTOR pathway in neuroblastoma

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Westhoff, Mike Andrew ^a   Faham, Najmeh ^a   Marx, Daniela ^a   Nonnenmacher, Lisa ^a   Jennewein, Claudia ^a   Enzenmüller, Stefanie ^a   Gonzalez, Patrick ^a   Fulda, Simone ^a,b   Debatin, Klaus Michael ^a  

^a UNIVERSITY HOSPITAL ULM   (Germany)

^b GOETHE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 (3 CHLORO 4 HYDROXYANILINO) 3 (2 NITROPHENYL)MALEIMIDE; 2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; ANTINEOPLASTIC AGENT; BAFILOMYCIN A1; BETA ACTIN; BUPARLISIB; CASPASE 3; CISPLATIN; CYTOCHROME C; DACTOLISIB; DOXORUBICIN; ETOPOFOS; ETOPOSIDE; MAMMALIAN TARGET OF RAPAMYCIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NU 7026; PHOSPHATIDYLINOSITOL 3 KINASE; PORIN; PROTEIN KINASE B; RAPAMYCIN; TOPOTECAN; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CYCLE ARREST; CHEMOSENSITIZATION; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG EFFICACY; DRUG POTENTIATION; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NEUROBLASTOMA CELL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL LINE, TUMOR; DOXORUBICIN; DRUG SYNERGISM; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMIDAZOLES; MEMBRANE POTENTIAL, MITOCHONDRIAL; NEUROBLASTOMA; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; QUINOLINES; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; VOLTAGE-DEPENDENT ANION CHANNEL 1;

EID: 84896691989     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083128     Document Type: Article

References (50)

1. Park JR, Eggert A, Caron H (2010) Neuroblastoma: biology, prognosis, and treatment. Hematol Oncol Clin North Am 24: 65-86.
2. Berthold F, Boos J, Burdach S, Erttmann R, Henze G, et al. (2005) Myeloablative megatherapy with autologous stem-cell rescue versus oral maintenance chemotherapy as consolidation treatment in patients with high-risk neuroblastoma: a randomised controlled trial. Lancet Oncol 6: 649-658. (Pubitemid 41222755)
3. Brodeur GM (2003) Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3: 203-216.
4. Opel D, Poremba C, Simon T, Debatin KM, Fulda S (2007) Activation of Akt predicts poor outcome in neuroblastoma. Cancer Res 67: 735-745. (Pubitemid 46192214)
5. Boller D, Schramm A, Doepfner KT, Shalaby T, von Bueren AO, et al. (2008) Targeting the phosphoinositide 3-kinase isoform p110delta impairs growth and survival in neuroblastoma cells. Clin Cancer Res 14: 1172-1181. (Pubitemid 351302566)
6. Li Z, Thiele CJ (2007) Targeting Akt to increase the sensitivity of neuroblastoma to chemotherapy: lessons learned from the brain-derived neurotrophic factor/ TrkB signal transduction pathway. Expert Opin Ther Targets 11: 1611-1621. (Pubitemid 350300963)
7. Chanthery YH, Gustafson WC, Itsara M, Persson A, Hackett CS, et al (2012). Paracrine signaling through MYCN enhances tumor-vascular interactions in neuroblastoma. Sci Transl Med 4: 115ra3.
8. Bender A, Opel D, Naumann I, Kappler R, Friedman L, et al. (2010) PI3K inhibitors prime neuroblastoma cells for chemotherapy by shifting the balance towards pro-apoptotic Bcl-2 proteins and enhanced mitochondrial apoptosis. Oncogene 30: 494-503.
9. Paz-Ares L, Blanco-Aparicio C, Garcia-Carbonero R, Carnero A (2009) Inhibiting PI3K as a therapeutic strategy against cancer. Clin Transl Oncol 11: 572-579.
10. Hixon ML, Paccagnella L, Millham R, Perez-Olle R, Gualberto A (2010) Development of inhibitors of the IGF-IR/PI3K/Akt/mTOR pathway. Rev Recent Clin Trials 5: 189-208.
11. Coughlin CM, Johnston DS, Strahs A, Burczynski ME, Bacus S, et al. (2010) Approaches and limitations of phosphatidylinositol-3-kinase pathway activation status as a predictive biomarker in the clinical development of targeted therapy. Breast Cancer Res Treat 124: 1-11.
12. Qayum N, Im J, Stratford MR, Bernhard EJ, McKenna WG, et al. (2012) Modulation of the tumor microvasculature by phosphoinositide-3 kinase inhibition increases doxorubicin delivery in vivo. Clin Cancer Res 18: 161-169.
13. Lee MJ, Ye AS, Gardino AK, Heijink AM, Sorger PK, et al. (2012) Sequential application of anticancer drugs enhances cell death by rewiring apoptotic signaling networks. Cell 149: 780-794.
14. Ammirante M, Luo JL, Grivennikov S, Nedospasov S, Karin M (2010) B-cell-derived lymphotoxin promotes castration-resistant prostate cancer. Nature 464: 302-305.
15. Cheung NV, Heller G (1991) Chemotherapy dose intensity correlates strongly with response, median survival, and median progression-free survival in metastatic neuroblastoma. J Clin Oncol 9: 1050-1058.
16. Opel D, Westhoff MA, Bender A, Braun V, Debatin KM, et al. (2008) Phosphatidylinositol 3-kinase inhibition broadly sensitizes glioblastoma cells to death receptor- and drug-induced apoptosis. Cancer Res 68: 6271-6280.
17. Westhoff MA, Kandenwein JA, Karl S, Vellanki SH, Braun V, et al. (2009) The pyridinylfuranopyrimidine inhibitor, PI-103, chemosensitizes glioblastoma cells for apoptosis by inhibiting DNA repair. Oncogene 28: 3586-3596.
18. Mueller S, Yang X, Sottero TL, Gragg A, Prasad G, et al. (2011) Cooperation of the HDAC inhibitor vorinostat and radiation in metastatic neuroblastoma: efficacy and underlying mechanisms. Cancer Lett 306: 223-229.
19. Caren H, Kryh H, Nethander M, Sjoberg RM, Trager C, et al. (2010) High-risk neuroblastoma tumors with 11q-deletion display a poor prognostic, chromosome instability phenotype with later onset. Proc Natl Acad Sci U S A 107: 4323-4328.
20. Ross RA, Spengler BA, Biedler JL (1983) Coordinate morphological and biochemical interconversion of human neuroblastoma cells. J Natl Cancer Inst 71: 741-747. (Pubitemid 14232388)
21. Caren H, Erichsen J, Olsson L, Enerback C, Sjoberg RM, et al. (2008) High-resolution array copy number analyses for detection of deletion, gain, amplification and copy-neutral LOH in primary neuroblastoma tumors: four cases of homozygous deletions of the CDKN2A gene. BMC Genomics 9: 353.
22. Davidoff AM (2012) Neuroblastoma. Semin Pediatr Surg 21: 2-14.
23. Enzenmuller S, Gonzalez P, Karpel-Massler G, Debatin KM, Fulda S (2013) GDC-0941 enhances the lysosomal compartment via TFEB and primes glioblastoma cells to lysosomal membrane permeabilization and cell death. Cancer Lett 329: 27-36.
24. Enzenmuller S, Gonzalez P, Debatin KM, Fulda S (2013) Chloroquine overcomes resistance of lung carcinoma cells to the dual PI3K/mTOR inhibitor PI103 by lysosome-mediated apoptosis. Anticancer Drugs 24: 14-19.
25. Degtyarev M, De Maziere A, Orr C, Lin J, Lee BB, et al. (2008) Akt inhibition promotes autophagy and sensitizes PTEN-null tumors to lysosomotropic agents. J Cell Biol 183: 101-116.
26. Pan T, Rawal P, Wu Y, Xie W, Jankovic J, et al. (2009) Rapamycin protects against rotenone-induced apoptosis through autophagy induction. Neuroscience 164: 541-551.
27. Gonzalez P, Mader I, Tchoghandjian A, Enzenmuller S, Cristofanon S, et al. (2012) Impairment of lysosomal integrity by B10, a glycosylated derivative of betulinic acid, leads to lysosomal cell death and converts autophagy into a detrimental process. Cell Death Differ 19: 1337-1346.
28. Zeng R, Chen Y, Zhao S, Cui GH (2012) Autophagy counteracts apoptosis in human multiple myeloma cells exposed to oridonin in vitro via regulating intracellular ROS and SIRT1. Acta Pharmacol Sin 33: 91-100.
29. Qi XJ, Wildey GM, Howe PH (2006) Evidence that Ser87 of BimEL is phosphorylated by Akt and regulates BimEL apoptotic function. J Biol Chem 281: 813-823.
30. Gardai SJ, Hildeman DA, Frankel SK, Whitlock BB, Frasch SC, et al. (2004) Phosphorylation of Bax Ser184 by Akt regulates its activity and apoptosis in neutrophils. J Biol Chem 279: 21085-21095. (Pubitemid 38656511)
31. Datta SR, Dudek H, Tao X, Masters S, Fu H, et al. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241. (Pubitemid 27456390)
32. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, et al. (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31: 227-285.
33. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, et al. (1998) The permeability transition pore complex: a target for apoptosis regulation by caspases and bcl-2-related proteins. J Exp Med 187: 1261-1271. (Pubitemid 28189115)
34. Pastorino JG, Hoek JB, Shulga N (2005) Activation of glycogen synthase kinase 3beta disrupts the binding of hexokinase II to mitochondria by phosphorylating voltage-dependent anion channel and potentiates chemotherapy-induced cytotoxicity. Cancer Res 65: 10545-10554. (Pubitemid 41743749)
35. Sims JT, Ganguly SS, Bennett H, Friend JW, Tepe J, et al. (2013). Imatinib reverses doxorubicin resistance by affecting activation of STAT3-dependent NFkappaB and HSP27/p38/AKT pathways and by inhibiting ABCB1. PLoS One 8: e55509.
36. Hui RC, Francis RE, Guest SK, Costa JR, Gomes AR, Myatt SS, et al. (2008). Doxorubicin activates FOXO3a to induce the expression of multidrug resistance gene ABCB1 (MDR1) in K562 leukemic cells. Mol Cancer Ther 7: 670-8. (Pubitemid 351482149)
37. Li X, Lu Y, Liang K, Liu B, Fan Z (2005). Differential responses to doxorubicin-induced phosphorylation and activation of Akt in human breast cancer cells. Breast Cancer Res 7: R589-97.
38. Buki A, Okonkwo DO, Wang KK, Povlishock JT (2000) Cytochrome c release and caspase activation in traumatic axonal injury. J Neurosci 20: 2825-2834. (Pubitemid 30220307)
39. Konstantinidou G, Bey EA, Rabellino A, Schuster K, Maira MS, et al. (2009) Dual phosphoinositide 3-kinase/mammalian target of rapamycin blockade is an effective radiosensitizing strategy for the treatment of non-small cell lung cancer harboring K-RAS mutations. Cancer Res 69: 7644-7652.
40. Dubrovska A, Elliott J, Salamone RJ, Kim S, Aimone LJ, et al. (2010) Combination therapy targeting both tumor-initiating and differentiated cell populations in prostate carcinoma. Clin Cancer Res 16: 5692-5702.
41. Prasad G, Sottero T, Yang X, Mueller S, James CD, et al. (2011) Inhibition of PI3K/mTOR pathways in glioblastoma and implications for combination therapy with temozolomide. Neuro Oncol 13: 384-392.
42. Hengartner MO (2000) The biochemistry of apoptosis. Nature 407: 770-776.
43. Baumann P, Mandl-Weber S, Oduncu F, Schmidmaier R (2009). The novel orally bioavailable inhibitor of phosphoinositol-3-kinase and mammalian target of rapamycin, NVP-BEZ235, inhibits growth and proliferation in multiple myeloma. Exp Cell Res 315: 485-97.
44. Magan N, Isaacs RJ, Stowell KM (2012). Treatment with the PARP-inhibitor PJ34 causes enhanced doxorubicin-mediated cell death in HeLa cells. Anticancer Drugs 23: 627-37.
45. Burden DA, Osheroff N (1998). Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim Biophys Acta 1400: 139-54. (Pubitemid 28475100)
46. Bien S, Rimmbach C, Neumann H, Niessen J, Reimer E, et al. (2010). Doxorubicin-induced cell death requires cathepsin B in HeLa cells. Biochem Pharmacol 80: 1466-77.
47. Swift LP, Rephaeli A, Nudelman A, Phillips DR, Cutts SM (2006). Doxorubicin-DNA adducts induce a non-topoisomerase II-mediated form of cell death. Cancer Res 66: 4863-71.
48. Ferraro C, Quemeneur L, Prigent AF, Taverne C, Revillard JP, et al. (2000). Anthracyclines trigger apoptosis of both G0-G1 and cycling peripheral blood lymphocytes and induce massive deletion of mature T and B cells. Cancer Res 60: 1901-7. (Pubitemid 30207650)
49. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115: 2679-2688. (Pubitemid 41434392)
50. Franke TF (2008) PI3K/Akt: getting it right matters. Oncogene 27: 6473-6488.