Sequential application of a cytotoxic nanoparticle and a PI3K inhibitor enhances antitumor efficacy

Cancer Research

Volumn 74, Issue 3, 2014, Pages 675-685

  Pandey, Ambarish ^a   Kulkarni, Ashish ^a   Roy, Bhaskar ^a   Goldman, Aaron ^a   Sarangi, Sasmit ^a   Sengupta, Poulomi ^a   Phipps, Colin ^b,c   Kopparam, Jawahar ^a   Oh, Michael ^a   Basu, Sudipta ^a   Kohandel, Mohammad ^b   Sengupta, Shiladitya ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b FIELDS INSTITUTE   (Canada)

^c UNIVERSITY OF WATERLOO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; FEMALE; HUMANS; MICE; MODELS, BIOLOGICAL; NANOPARTICLES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION;

EID: 84893838492     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-3783     Document Type: Article

References (51)

1. Ravandi F, Cortes JE, Jones D, Faderl S, Garcia-Manero G, Konopleva MY, et al. Phase I/II study of combination therapy with sorafenib, idarubicin, and cytarabine in younger patients with acute myeloid leukemia. J Clin Oncol 2010;28:1856-62.
2. Takabatake D, Fujita T, Shien T, Kawasaki K, Taira N, Yoshitomi S, et al. Tumor inhibitory effect of gefitinib (ZD1839, Iressa) and taxane combination therapy in EGFR-overexpressing breast cancer cell lines (MCF7/ADR, MDA-MB-231). Int J Cancer 2007;120:181-8.
3. Wu S, Singh RK. Resistance to chemotherapy and molecularly targeted therapies: rationale for combination therapy in malignant melanoma. Curr Mol Med 2011;11:553-63.
4. Sandler A, Gray R, Perry MC, Brahmer J, Schiller JH, Dowlati A, et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N Engl J Med 2006;355:2542-50.
5. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, Cohen KS, 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.
6. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62.
7. Van der Veldt AA, Lubberink M, Bahce I, Walraven M, de Boer MP, Greuter HN, et al. Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of antiangiogenic drugs. Cancer Cell 2012;21:82-91.
8. Fang J, Nakamura H, Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv Drug Deliv Rev 2011; 63:136-51.
9. Sengupta S, Eavarone D, Capila I, Zhao G, Watson N, Kiziltepe T, et al. Temporal targeting of tumour cells and neovasculature with a nanoscale delivery system. Nature 2005;436:568-72.
10. Conlin AK, Seidman AD, Bach A, Lake D, Dickler M, D'Andrea G, et al. Phase II trial of weekly nanoparticle albumin-bound paclitaxel with carboplatin and trastuzumab as first-line therapy for women with HER2-overexpressing metastatic breast cancer. Clin Breast Cancer 2010;10:281-7.
11. Orlowski RZ, Nagler A, Sonneveld P, Blade J, Hajek R, Spencer A, et al. Randomized phase III study of pegylated liposomal doxorubicin plus bortezomib compared with bortezomib alone in relapsed or refractory multiple myeloma: combination therapy improves time to progression. J Clin Oncol 2007;25:3892-901.
12. Rossi A, Di Maio M, Chiodini P, Rudd RM, Okamoto H, Skarlos DV, et al. Carboplatin-or cisplatin-based chemotherapy in first-line treatment of small-cell lung cancer: the COCIS meta-analysis of individual patient data. J Clin Oncol 2012;30:1692-8.
13. Lorch A, Kleinhans A, Kramar A, Kollmannsberger CK, Hartmann JT, Bokemeyer C, et al. Sequential versus single high-dose chemotherapy in patients with relapsed or refractory germ cell tumors: long-term results of a prospective randomized trial. J Clin Oncol 2012;30:800-5.
14. Staudacher L, Cottu PH, Dieras V, Vincent-Salomon A, GuilhaumeMN, Escalup L, et al. Platinum-based chemotherapy in metastatic triplenegative breast cancer: the Institut Curie experience. Ann Oncol 2011;22:848-56.
15. Sanchez-Gonzalez PD, Lopez-Hernandez FJ, Lopez-Novoa JM, Morales AI. An integrative view of the pathophysiological events leading to cisplatin nephrotoxicity. Crit Rev Toxicol 2011;41:803-21.
16. Sengupta P, Basu S, Soni S, Pandey A, Roy B, Oh M, et al. A cholesterol-tethered platinum II-based supramolecular nanoparticle increases antitumor efficacy and reduces nephrotoxicity. Proc Natl Acad Sci 2012;109:11294-9.
17. Belyanskaya LL, Hopkins-Donaldson S, Kurtz S, Simoes-Wust AP, Yousefi S, Simon HU, et al. Cisplatin activates Akt in small cell lung cancer cells and attenuates apoptosis by survivin upregulation. Int J Cancer 2005;117:755-63.
18. Eissing T, Conzelmann H, Gilles ED, Allgower F, Bullinger E, Scheurich P. Bistability analyses of a caspase activation model for receptorinduced apoptosis. J Biol Chem 2004;279:36892-7.
19. Choi HS, Han S, Yokota H, Cho KH. Coupled positive feedbacks provoke slow induction plus fast switching in apoptosis. FEBS Lett 2007;581:2684-90.
20. Albeck JG, Burke JM, Spencer SL, Lauffenburger DA, Sorger PK. Modeling a snap-action, variable-delay switch controlling extrinsic cell death. PLoS Biol 2008;6:2831-52.
21. Spencer SL, Sorger PK. Measuring and modeling apoptosis in single cells. Cell 2011;144:926-39.
22. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998;282:1318-21.
23. Asselin E, Mills GB, Tsang BK. XIAP regulates Akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res 2001; 61:1862-8.
24. Dan HC, Sun M, Kaneko S, Feldman RI, Nicosia SV, WangHG, et al. Akt phosphorylation and stabilization of X-linked inhibitor of apoptosis protein (XIAP). J Biol Chem 2004;279:5405-12.
25. Deveraux QL, Leo E, Stennicke HR, Welsh K, Salvesen GS, Reed JC. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J 1999;18: 5242-51.
26. Hornle M, Peters N, Thayaparasingham B, Vorsmann H, Kashkar H, Kulms D. Caspase-3 cleaves XIAP in a positive feedback loop to sensitize melanoma cells to TRAIL-induced apoptosis. Oncogene 2011;30:575-87.
27. Winograd-Katz SE, Levitzki A. Cisplatin induces PKB/Akt activation and p38(MAPK) phosphorylation of the EGF receptor. Oncogene 2006;25:7381-90.
28. Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM. An induced proximity model for caspase-8 activation. J Biol Chem 1998;273:2926-30.
29. Gonzalez VM, Fuertes MA, Alonso C, Perez JM. Is cisplatin-induced cell death always produced by apoptosis? Mol Pharmacol 2001;59: 657-63.
30. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997;91:479-89.
31. Pal SK, Childs BH, Pegram M. Triple negative breast cancer: unmet medical needs. Breast Cancer Res Treat 2011;125:627-36.
32. Rastelli F, Biancanelli S, Falzetta A, Martignetti A, Casi C, Bascioni R, et al. Triple-negative breast cancer: current state of the art. Tumori 2010;96:875-88.
33. Eckstein N. Platinum resistance in breast and ovarian cancer cell lines. J Exp Clin Cancer Res 2011;30:91.
34. Paraskar AS, Soni S, Chin KT, Chaudhuri P, Muto KW, Berkowitz J, et al. Harnessing structure-activity relationship to engineer a cisplatin nanoparticle for enhanced antitumor efficacy. Proc Natl Acad SciUS A 2010;107:12435-40.
35. Perez-Tenorio G, Stal O. Activation of AKT/PKB in breast cancer predicts a worse outcome among endocrine treated patients. Br J Cancer 2002;86:540-5.
36. Yang X, Fraser M, Moll UM, Basak A, Tsang BK. Akt-mediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspasedependent mitochondrial death pathway. Cancer Res 2006;66: 3126-36.
37. Moulder SL. Does the PI3K pathway play a role in basal breast cancer? Clin Breast Cancer 2010;10 Suppl 3:S66-71.
38. Miller TW, Balko JM, Arteaga CL. Phosphatidylinositol 3-kinase and antiestrogen resistance in breast cancer. J Clin Oncol 2011;29: 4452-61.
39. Bunney TD, Katan M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer 2010;10:342-52.
40. Goldman AJ, Shunmugam I, Kulkarni A, Rivera F, Sengupta S. Chemotherapy-induced Akt survival signaling is regulated by CD44-Ezrin/ Radaxin Moesin (ERM) scaffolding, dependent on EGFR activity. Cancer Res 15, 2012;72(8 Supplement):
41. Saito T, Okada S, Ohshima K, Yamada E, Sato M, Uehara Y, et al. Differential activation of epidermal growth factor (EGF) receptor downstream signaling pathways by betacellulin and EGF. Endocrinology 2004;145:4232-43.
42. Humtsoe JO, Kramer RH. Differential epidermal growth factor receptor signaling regulates anchorage-independent growth bymodulation of the PI3K/AKT pathway. Oncogene 2010;29:1214-26.
43. Benhar M, Engelberg D, Levitzki A. Cisplatin-induced activation of the EGF receptor. Oncogene 2002;21:8723-31.
44. Bender A, Opel D, Naumann I, Kappler R, Friedman L, von Schweinitz D, et al. PI3K inhibitors prime neuroblastomacells for chemotherapy by shifting the balance towards pro-apoptotic Bcl-2 proteins and enhanced mitochondrial apoptosis. Oncogene 2011;30:494-503.
45. Kim SH, Song YC, Jo H, Song YS. Effect of epidermal growth factor receptor inhibitor alone and in combination with cisplatin on growth of vulvar cancer cells. Ann N Y Acad Sci 2009; 1171:642-8.
46. Tsai CM, Chen JT, Stewart DJ, Chiu CH, Lai CL, Hsiao SY, et al. Antagonism between gefitinib and cisplatin in non-small cell lung cancer cells: why randomized trials failed? J Thorac Oncol 2011;6: 559-68.
47. Davies AM, Ho C, Lara PN Jr, Mack P, Gumerlock PH, Gandara DR. Pharmacodynamic separation of epidermal growth factor receptor tyrosine kinase inhibitors and chemotherapy in non-small-cell lung cancer. Clin Lung Cancer 2006;7:385-8.
48. Mahaffey CM, Davies AM, Lara PN Jr, Pryde B, Holland W, Mack PC, et al. Schedule-dependent apoptosis in K-ras mutant non-small-cell lung cancer cell lines treated with docetaxel and erlotinib: rationale for pharmacodynamic separation. Clin Lung Cancer 2007;8:548-53.
49. Lee MJ, Ye AS, Gardino AK, Heijink AM, Sorger PK, Macbeath G, et al. Sequential application of anticancer drugs enhances cell death by rewiring apoptotic signaling networks. Cell 2012;149:780-94.
50. Gharbi SI, Zvelebil MJ, Shuttleworth SJ, Hancox T, Saghir N, Timms JF, et al. Exploring the specificity of the PI3K family inhibitor LY294002. Biochem J 2007;404:15-21.
51. Tao K, Fang M, Alroy J, Sahagian GG. Imagable 4T1 model for the study of late stage breast cancer. BMC Cancer 2008;8:228.