Nanomedicines Eradicating Cancer Stem-like Cells in Vivo by pH-Triggered Intracellular Cooperative Action of Loaded Drugs

ACS Nano

Volumn 10, Issue 6, 2016, Pages 5643-5655

  Kinoh, Hiroaki ^a   Miura, Yutaka ^b   Chida, Tsukasa ^b   Liu, Xueying ^b   Mizuno, Kazue ^b   Fukushima, Shigeto ^c   Morodomi, Yosuke ^d   Nishiyama, Nobuhiro ^e   Cabral, Horacio ^c   Kataoka, Kazunori ^a,b,c  

^a Innovation Center of NanoMedicine   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

cancer stem like cells; chemotherapy; epirubicin; mesothelioma; polymeric micelles; staurosporine

Indexed keywords

CHEMOTHERAPY; CYTOLOGY; DISEASES; DRUG INTERACTIONS; DRUG THERAPY; ENZYME ACTIVITY; ENZYME INHIBITION; MICELLES; POLYMERS; STEM CELLS; TUMORS;

EFFLUX TRANSPORTER; EPIRUBICIN; INTRACELLULAR DELIVERY; MESOTHELIOMA; POLYMERIC MICELLE; RESISTANCE MECHANISMS; SIGNALING PATHWAYS; STAUROSPORINES;

CELLS;

ANTINEOPLASTIC AGENT; EPIRUBICIN;

CANCER STEM CELL; HUMAN; MICELLE; NANOMEDICINE; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; EPIRUBICIN; HUMANS; MICELLES; NANOMEDICINE; NEOPLASTIC STEM CELLS;

EID: 84976639275     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/acsnano.6b00900     Document Type: Article

References (56)

1. Visvader, J. E.; Lindeman, G. J. Cancer Stem Cells in Solid Tumours: Accumulating Evidence and Unresolved Questions Nat. Rev. Cancer 2008, 8, 755-768 10.1038/nrc2499
2. Magee, J. A.; Piskounova, E.; Morrison, S. J. Cancer Stem Cells: Impact, Heterogeneity, and Uncertainty Cancer Cell 2012, 21, 283-296 10.1016/j.ccr.2012.03.003
3. Medema, J. P. Cancer Stem Cells: The Challenges Ahead Nat. Cell Biol. 2013, 15, 338-344 10.1038/ncb2717
4. Diehn, M.; Majeti, R. Metastatic Cancer Stem Cells: An Opportunity for Improving Cancer Treatment? Cell Stem Cell 2010, 6, 502-503 10.1016/j.stem.2010.05.001
5. Dean, M.; Fojo, T.; Bates, S. Tumour Stem Cells and Drug Resistance Nat. Rev. Cancer 2005, 4, 275-284 10.1038/nrc1590
6. Dreesen, O.; Brivanlou, A. H. Signaling Pathways in Cancer and Embryonic Stem Cells Stem Cell Rev. 2007, 3, 7-17 10.1007/s12015-007-0004-8
7. Dubrovska, A.; Kim, S.; Salamone, R. J.; Walker, J. R.; Maira, S.-M.; García-Echeverría, C.; Schultz, P. G.; Reddy, V. A. The Role of PTEN/Akt/PI3K Signaling in the Maintenance and Viability of Prostate Cancer Stem-like Cell Populations Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 268-273 10.1073/pnas.0810956106
8. Reya, T.; Clevers, H. Wnt Signalling in Stem Cells and Cancer Nature 2005, 434, 843-850 10.1038/nature03319
9. Hoffmeyer, K.; Raggioli, A.; Rudloff, S.; Anton, R.; Hierholzer, A.; Del Valle, I.; Hein, K.; Vogt, R.; Kemler, R. Wnt/Beta-Catenin Signaling Regulates Telomerase in Stem Cells and Cancer Cells Science 2012, 336, 1549-1554 10.1126/science.1218370
10. Zhou, J.; Wulfkuhle, J.; Zhang, H.; Gu, P.; Yang, Y.; Deng, J.; Margolick, J. B.; Liotta, L. A.; Petricoin, E., 3rd; Zhang, Y. Activation of the PTEN/Mtor/STAT3 Pathway in Breast Cancer Stem-Like Cells is Required for Viability and Maintenance Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 16158-16163 10.1073/pnas.0702596104
11. Takebe, N.; Harris, P. J.; Warren, R. Q.; Ivy, S. P. Targeting Cancer Stem Cells by Inhibiting Wnt, Notch, and Hedgehog Pathways Nat. Rev. Clin. Oncol. 2011, 8, 97-106 10.1038/nrclinonc.2010.196
12. Grinshtein, N.; Datti, A.; Fujitani, M.; Uehling, D.; Prakesch, M.; Isaac, M.; Irwin, M. S.; Wrana, J. L.; Al-Awar, R.; Kaplan, D. R. Small Molecule Kinase Inhibitor Screen Identifies Polo-Like Kinase 1 as a Target for Neuroblastoma Tumor-Initiating Cells Cancer Res. 2011, 71, 1385-1395 10.1158/0008-5472.CAN-10-2484
13. Gupta, P. B.; Onder, T. T.; Jiang, G.; Tao, K.; Kuperwasser, C.; Weinberg, R. A.; Lander, E. S. Identification of Selective Inhibitors of Cancer Stem Cells by High-Throughput Screening Cell 2009, 138, 645-659 10.1016/j.cell.2009.06.034
14. Sachlos, E.; Risueno, R. M.; Laronde, S.; Shapovalova, Z.; Lee, J. H.; Russell, J.; Malig, M.; McNicol, J. D.; Fiebig-Comyn, A.; Graham, M.; Levadoux-Martin, M.; Lee, J. B.; Giacomelli, A. O.; Hassell, J. A.; Fischer-Russell, D.; Trus, M. R.; Foley, R.; Leber, B.; Xenocostas, A.; Brown, E. D. et al. Identification of Drugs Including a Dopamine Receptor Antagonist that Selectively Target Cancer Stem Cells Cell 2012, 149, 1284-1297 10.1016/j.cell.2012.03.049
15. Brechbiel, J.; Miller-Moslin, K.; Adjei, A. A. Crosstalk between Hedgehog and Other Signaling Pathways as a Basis for Combination Therapies in Cancer Cancer Treat. Rev. 2014, 40, 750-759 10.1016/j.ctrv.2014.02.003
16. Ferrari, M. (2005) Cancer Nanotechnology: Opportunities and Challenges Nat. Rev. Cancer 2005, 5, 161-171 10.1038/nrc1566
17. Kim, B. Y.; Rutka, J. T.; Chan, W. C. Nanomedicine N. Engl. J. Med. 2010, 363, 2434-2443 10.1056/NEJMra0912273
18. Kataoka, K.; Harada, A.; Nagasaki, Y. Block Copolymer Micelles for Drug Delivery: Design, Characterization and Biological Significance Adv. Drug Delivery Rev. 2001, 47, 113-131 10.1016/S0169-409X(00)00124-1
19. Cabral, H.; Kataoka, K. Progress of Drug-Loaded Polymeric Micelles into Clinical Studies J. Controlled Release 2014, 190, 465-476 10.1016/j.jconrel.2014.06.042
20. Varghese, S.; Whipple, R.; Martin, S. S.; Alexander, H. R. Multipotent Cancer Stem Cells Derived from Human Malignant Peritoneal Mesothelioma Promote Tumorigenesis PLoS One 2012, 7, e52825 10.1371/journal.pone.0052825
21. Jänne, P. A.; Wozniak, A. J.; Belani, C. P.; Keohan, M. L.; Ross, H. J.; Polikoff, J. A.; Mintzer, D. M.; Ye, Z.; Monberg, M. J.; Obasaju, C. K. Pemetrexed Alone or in Combination with Cisplatin in Previously Treated Malignant Pleural Mesothelioma: Outcomes From a Phase IIIB Expanded Access Program J. Thorac. Oncol. 2006, 1, 506-512 10.1097/01243894-200607000-00002
22. Cortes-Dericks, L.; Carboni, G. L.; Schmid, R. A.; Karoubi, G. Putative Cancer Stem Cells in Malignant Pleural Mesothelioma Show Resistance to Cisplatin and Pemetrexed Int. J. Oncol. 2010, 37, 437-444 10.3892/ijo-00000692
23. Shapiro, I. M.; Kolev, V. N.; Vidal, C. M.; Kadariya, Y.; Ring, J. E.; Wright, Q.; Weaver, D. T.; Menges, C.; Padval, M.; McClatchey, A. I.; Xu, Q.; Testa, J. R.; Pachter, J. A. Merlin Deficiency Predicts FAK Inhibitor Sensitivity: A Synthetic Lethal Relationship Sci. Transl. Med. 2014, 6, 237ra68 10.1126/scitranslmed.3008639
24. Cortes-Dericks, L.; Froment, L.; Boesch, R.; Schmid, R. A.; Karoubi, G. Cisplatin-Resistant Cells in Malignant Pleural Mesothelioma Cell Lines Show ALDH(High)CD44(+) Phenotype and Sphere-Forming Capacity BMC Cancer 2014, 14, 304 10.1186/1471-2407-14-304
25. Frei, C.; Opitz, I.; Soltermann, A.; Fischer, B.; Moura, U.; Rehrauer, H.; Weder, W.; Stahel, R.; Felley-Bosco, E. Pleural Mesothelioma Side Populations Have a Precursor Phenotype Carcinogenesis 2011, 32, 1324-1332 10.1093/carcin/bgr127
26. Yamazaki, H.; Naito, M.; Ghani, F. I.; Dang, N. H.; Iwata, S.; Morimoto, C. Characterization of Cancer Stem Cell Properties of CD24 and CD26-Positive Human Malignant Mesothelioma Cells Biochem. Biophys. Res. Commun. 2012, 419, 529-536 10.1016/j.bbrc.2012.02.054
27. Kinoshita, N.; Iioka, H.; Miyakoshi, A.; Ueno, N. PKC Is Essential for Dishevelled Function in a Noncanonical Wnt Pathway that Regulates Xenopus Convergent Extension Movements Genes Dev. 2003, 17, 1663-1676 10.1101/gad.1101303
28. Felli, M. P.; Vacca, A.; Calce, A.; Bellavia, D.; Campese, A. F.; Grillo, R.; Di Giovine, M.; Checquolo, S.; Talora, C.; Palermo, R.; Di Mario, G.; Frati, L.; Gulino, A.; Screpanti, I. PKC Mediates Pre-TCR Signaling and Contributes to Notch3-Induced T-Cell Leukemia Oncogene 2005, 24, 992-1000 10.1038/sj.onc.1208302
29. Szulkin, A.; Otvos, R.; Hillerdal, C. O.; Celep, A.; Yousef-Fadhel, E.; Skribek, H.; Hjerpe, A.; Székely, L.; Dobra, K. Characterization and Drug Sensitivity Profiling of Primary Malignant Mesothelioma Cells from Pleural Effusions BMC Cancer 2014, 14, 709 10.1186/1471-2407-14-709
30. Mattson, K.; Giaccone, G.; Kirkpatrick, A.; Evrard, D.; Tammilehto, L.; van Breukelen, F. J.; Planteydt, H. T.; van Zandwijk, N. Epirubicin in Malignant Mesothelioma: A Phase II Study of the European Organization for Research and Treatment of Cancer Lung Cancer Cooperative Group J. Clin. Oncol. 1992, 10, 824-828
31. Gescher, A. Staurosporine Analogues-Pharmacological Toys or Useful Antitumour Agents? Crit. Rev. Oncol. Hematol. 2000, 34, 127-135 10.1016/S1040-8428(00)00058-5
32. Fuse, E.; Tanii, H.; Takai, K.; Asanome, K.; Kurata, N.; Kobayashi, H.; Kuwabara, T.; Kobayashi, S.; Sugiyama, Y. Altered Pharmacokinetics of a Novel Anticancer Drug, UCN-01, Caused by Specific High Affinity Binding to Alpha1-Acid Glycoprotein in Humans Cancer Res. 1999, 59, 1054-1060
33. Gillet, J.-P.; Efferth, T.; Remacle, J. Chemotherapy-Induced Resistance by ATP-Binding Cassette Transporter Genes Biochim. Biophys. Acta, Rev. Cancer 2007, 1775, 237-262 10.1016/j.bbcan.2007.05.002
34. Robey, R. W.; Shukla, S.; Steadman, K.; Obrzut, T.; Finley, E. M.; Ambudkar, S. V.; Bates, S. E. Inhibition of ABCG2-Mediated Transport by Protein Kinase Inhibitors with a Bisindolylmaleimide or Indolocarbazole Structure Mol. Cancer Ther. 2007, 6, 1877-1885 10.1158/1535-7163.MCT-06-0811
35. Castro, A. F.; Horton, J. K.; Vanoye, C. G.; Altenberg, G. A. Mechanism of Inhibition of P-Glycoprotein-Mediated Drug Transport by Protein Kinase C Blockers Biochem. Pharmacol. 1999, 58, 1723-1733 10.1016/S0006-2952(99)00288-9
36. Sakai-Kato, K.; Un, K.; Nanjo, K.; Nishiyama, N.; Kusuhara, H.; Kataoka, K.; Kawanishi, T.; Goda, Y.; Okuda, H. Elucidating the Molecular Mechanism for the Intracellular Trafficking and Fate of Block Copolymer Micelles and Their Components Biomaterials 2014, 35, 1347-1358 10.1016/j.biomaterials.2013.11.027
37. Tari, A. M.; Mehta, A.; Lopez-Berestein, G. Modulation of Akt Activity by Doxorubicin in Breast Cancer Cells J. Chemother. 2001, 13, 334-336 10.1179/joc.2001.13.3.334
38. Luo, Y.; Rockow-Magnone, S. K.; Kroeger, P. E.; Frost, L.; Chen, Z.; Han, E. K.; Ng, S. C.; Simmer, R. L.; Giranda, V. L. Blocking Chk1 Expression Induces Apoptosis and Abrogates the G2 Checkpoint Mechanism Neoplasia 2001, 3, 411-419 10.1038/sj.neo.7900175
39. Jackson, J. R.; Gilmartin, A.; Imburgia, C.; Winkler, J. D.; Marshall, L. A.; Roshak, A. An Indolocarbazole Inhibitor of Human Checkpoint Kinase (Chk1) Abrogates Cell Cycle Arrest Caused by DNA Damage Cancer Res. 2000, 60, 566-572
40. Sakaue-Sawano, A.; Kurokawa, H.; Morimura, T.; Hanyu, A.; Hama, H.; Osawa, H.; Kashiwagi, S.; Fukami, K.; Miyata, T.; Miyoshi, H.; Imamura, T.; Ogawa, M.; Masai, H.; Miyawaki, A. Visualizing Spatiotemporal Dynamics of Multicellular Cell-Cycle Progression Cell 2008, 132, 487-498 10.1016/j.cell.2007.12.033
41. Soma, C. E.; Dubernet, C.; Bentolila, D.; Benita, S.; Couvreur, P. Reversion of Multidrug Resistance by Co-Encapsulation of Doxorubicin and Cyclosporin A in Polyalkylcyanoacrylate Nanoparticles Biomaterials 2000, 21, 1-7 10.1016/S0142-9612(99)00125-8
42. Bae, Y.; Diezi, T. A.; Zhao, A.; Kwon, G. S. Mixed Polymeric Micelles for Combination Cancer Chemotherapy through the Concurrent Delivery of Multiple Chemotherapeutic Agents J. Controlled Release 2007, 122, 324-330 10.1016/j.jconrel.2007.05.038
43. Zhang, R.; Yang, J.; Sima, M.; Zhou, Y.; Kopeček, J. Sequential Combination Therapy of Ovarian Cancer with Degradable N-(2-Hydroxypropyl) Methacrylamide Copolymer Paclitaxel and Gemcitabine Conjugates Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 12181-12186 10.1073/pnas.1406233111
44. Li, Q.; Woods, K. W.; Thomas, S.; Zhu, G. D.; Packard, G.; Fisher, J.; Li, T.; Gong, J.; Dinges, J.; Song, X.; Abrams, J.; Luo, Y.; Johnson, E. F.; Shi, Y.; Liu, X.; Klinghofer, V.; Des Jong, R.; Oltersdorf, T.; Stoll, V. S.; Jakob, C. G. et al. Synthesis and Structure-Activity Relationship Of 3,4′-Bispyridinylethylenes: Discovery of a Potent 3-Isoquinolinylpyridine Inhibitor of Protein Kinase B (PKB/Akt) for the Treatment Of Cancer Bioorg. Med. Chem. Lett. 2006, 16, 2000-2007 10.1016/j.bmcl.2005.12.065
45. Tam, W. L.; Lu, H.; Buikhuisen, J.; Soh, B. S.; Lim, E.; Reinhardt, F.; Wu, Z. J.; Krall, J. A.; Bierie, B.; Guo, W.; Chen, X.; Liu, X. S.; Brown, M.; Lim, B.; Weinberg, R. A. Protein Kinase C A is a Central Signaling Node and Therapeutic Target for Breast Cancer Stem Cells Cancer Cell 2013, 24, 347-364 10.1016/j.ccr.2013.08.005
46. Kabir, J.; Lobo, M.; Zachary, I. Staurosporine Induces Endothelial Cell Apoptosis via Focal Adhesion Kinase Dephosphorylation and Focal Adhesion Disassembly Independent of Focal Adhesion Kinase Proteolysis Biochem. J. 2002, 367, 145-155 10.1042/bj20020665
47. Hosoya, T.; Arai, M. A.; Koyano, T.; Kowithayakorn, T.; Ishibashi, M. Naturally Occurring Small-Molecule Inhibitors of Hedgehog/GLI-Mediated Transcription ChemBioChem 2008, 9, 1082-1092 10.1002/cbic.200700511
48. Dlugosz, A.; Agrawal, S.; Kirkpatrick, P. Vismodegib Nat. Rev. Drug Discovery 2012, 11, 437-438 10.1038/nrd3753
49. Sekulic, A.; Migden, M. R.; Oro, A. E.; Dirix, L.; Lewis, K. D.; Hainsworth, J. D.; Solomon, J. A.; Yoo, S.; Arron, S. T.; Friedlander, P. A.; Marmur, E.; Rudin, C. M.; Chang, A. L.; Low, J. A.; Mackey, H. M.; Yauch, R. L.; Graham, R. A.; Reddy, J. C.; Hauschild, A. Efficacy and Safety of Vismodegib in Advanced Basal-Cell Carcinoma N. Engl. J. Med. 2012, 366, 2171-2179 10.1056/NEJMoa1113713
50. Gajjar, A.; Stewart, C. F.; Ellison, D. W.; Kaste, S.; Kun, L. E.; Packer, R. J.; Goldman, S.; Chintagumpala, M.; Wallace, D.; Takebe, N.; Boyett, J. M.; Gilbertson, R. J.; Curran, T. Phase I Study of Vismodegib in Children with Recurrent or Refractory Medulloblastoma: A Pediatric Brain Tumor Consortium Study Clin. Cancer Res. 2013, 19, 6305-6312 10.1158/1078-0432.CCR-13-1425
51. Kim, E. J.; Sahai, V.; Abel, E. V.; Griffith, K. A.; Greenson, J. K.; Takebe, N.; Khan, G. N.; Blau, J. L.; Craig, R.; Balis, U. G.; Zalupski, M. M.; Simeone, D. M. Pilot Clinical Trial of Hedgehog Pathway Inhibitor GDC-0449 (Vismodegib) in Combination with Gemcitabine in Patients with Metastatic Pancreatic Adenocarcinoma Clin. Cancer Res. 2014, 20, 5937-5945 10.1158/1078-0432.CCR-14-1269
52. Metcalfe, C.; de Sauvage, F. J. Hedgehog Fights Back: Mechanisms of Acquired Resistance Against Smoothened Antagonists Cancer Res. 2011, 71, 5057-5061 10.1158/0008-5472.CAN-11-0923
53. Sordet, O.; Khan, Q. A.; Plo, I.; Pourquier, P.; Urasaki, Y.; Yoshida, A.; Antony, S.; Kohlhagen, G.; Solary, E.; Saparbaev, M.; Laval, J.; Pommier, Y. Apoptotic Topoisomerase I-DNA Complexes Induced by Staurosporine-Mediated Oxygen Radicals J. Biol. Chem. 2004, 279, 50499-50504 10.1074/jbc.M410277200
54. Cabral, H.; Matsumoto, Y.; Mizuno, K.; Chen, Q.; Murakami, M.; Kimura, M.; Terada, Y.; Kano, M. R.; Miyazono, K.; Uesaka, M.; Nishiyama, N.; Kataoka, K. Accumulation of Sub-100 nm Polymeric Micelles in Poorly Permeable Tumours Depends on Size Nat. Nanotechnol. 2011, 6, 815-823 10.1038/nnano.2011.166
55. Murakami, M.; Cabral, H.; Matsumoto, Y.; Wu, S.; Kano, M. R.; Yamori, T.; Nishiyama, N.; Kataoka, K. Improving Drug Potency and Efficacy by Nanocarrier-Mediated Subcellular Targeting Sci. Transl. Med. 2011, 3, 64ra2 10.1126/scitranslmed.3001385
56. Morodomi, Y.; Yano, T.; Kinoh, H.; Harada, Y.; Saito, S.; Kyuragi, R.; Yoshida, K.; Onimaru, M.; Shoji, F.; Yoshida, T.; Ito, K.; Shikada, Y.; Maruyama, R.; Hasegawa, M.; Maehara, Y.; Yonemitsu, Y. BioKnife, a uPA Activity-Dependent Oncolytic Sendai Virus, Eliminates Pleural Spread of Malignant Mesothelioma via Simultaneous Stimulation of uPA Expression Mol. Ther. 2012, 20, 769-777 10.1038/mt.2011.305