Co-delivery of peptide-modified cisplatin and doxorubicin via mucoadhesive nanocapsules for potential synergistic intravesical chemotherapy of non-muscle-invasive bladder cancer

European Journal of Pharmaceutical Sciences

Volumn 84, Issue , 2016, Pages 103-115

  Lu, Shengjie ^a   Xu, Liqun ^a   Kang, En Tang ^a   Mahendran, Ratha ^a   Chiong, Edmund ^a   Neoh, Koon Gee ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Bladder cancer; Cisplatin; Doxorubicin; Intravesical co delivery; Mucoadhesive nanocapsules; Synergistic effect

Indexed keywords

ACETYLCYSTEINE; CISPLATIN; DOXORUBICIN; NANOCAPSULE; NANOCARRIER; PEPTIDE; ANTINEOPLASTIC AGENT; CHITOSAN; LYSINE; MUCIN; N(ALPHA)-ACETYLLYSINE; POLYMETHACRYLIC ACID; POLYMETHACRYLIC ACID DERIVATIVE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BLADDER; CANCER CELL LINE; CANCER CHEMOTHERAPY; CELL KILLING; CELL SURFACE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG POTENTIATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; MASS SPECTROMETRY; MUCOADHESION; NON MUSCLE INVASIVE BLADDER CANCER; PRIORITY JOURNAL; SUSTAINED DRUG RELEASE; UROTHELIUM; ADHESION; ANALOGS AND DERIVATIVES; ANIMAL; CHEMISTRY; DRUG EFFECTS; INTRAVESICAL DRUG ADMINISTRATION; PIG; TUMOR CELL LINE; URINARY BLADDER NEOPLASMS;

ADHESIVENESS; ADMINISTRATION, INTRAVESICAL; ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; CHITOSAN; CISPLATIN; DOXORUBICIN; DRUG SYNERGISM; HUMANS; LYSINE; MUCINS; NANOCAPSULES; PEPTIDES; POLYMETHACRYLIC ACIDS; SWINE; URINARY BLADDER; URINARY BLADDER NEOPLASMS;

EID: 84955597711     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2016.01.013     Document Type: Article

References (74)

1. F. Ali-Osman, M.S. Berger, S. Rajagopal, A. Spence, and R.B. Livingston Topoisomerase II inhibition and altered kinetics of formation and repair of nitrosourea and cisplatin-induced DNA interstrand cross-links and cytotoxicity in human glioblastoma cells Cancer Res. 53 1993 5663 5668
2. G.P. Andrews, T.P. Laverty, and D.S. Jones Mucoadhesive polymeric platforms for controlled drug delivery Eur. J. Pharm. Biopharm. 71 2009 505 518
3. T.G. Appleton, J.R. Hall, and P.D. Prenzler Reaction of the cis-diamminediaquaplatinum(II) cation with N-acetylglycine Inorg. Chem. 28 1989 815 819
4. R. Arantes-Rodrigues, R. Pinto-Leite, L. Fidalgo-Goncalves, C. Palmeira, L. Santos, A. Colaco, and P. Oliveira Synergistic effect between cisplatin and sunitinib malate on human urinary bladder-cancer cell lines Biomed Res. Int. 2013 10.1155/2013/791406
5. T. Bachleitner-Hofmann, M.Y. Sun, C.T. Chen, D. Liska, Z.S. Zeng, A. Viale, A.B. Olshen, M. Mittlboeck, J.G. Christensen, N. Rosen, D.B. Solit, and M.R. Weiser Antitumor activity of SNX-2112, a synthetic heat shock protein-90 inhibitor, in MET-amplified tumor cells with or without resistance to selective MET inhibition Clin. Cancer Res. 17 2011 122 133
6. J. Barthelmes, G. Perera, J. Hombach, S. Dunnhaupt, and A. Bernkop-Schnurch Development of a mucoadhesive nanoparticulate drug delivery system for a targeted drug release in the bladder Int. J. Pharm. 416 2011 339 345
7. A. Bernkop-Schnurch Chitosan and its derivatives: potential excipients for peroral peptide delivery systems Int. J. Pharm. 194 2000 1 13
8. M. Bigioni, A. Benzo, C. Irrissuto, G. Lopez, B. Curatella, C.A. Maggi, S. Manzini, A. Crea, S. Caroli, F. Cubadda, and M. Binaschi Antitumour effect of combination treatment with sabarubicin (MEN 10755) and cis-platin (DDP) in human lung tumour xenograft Cancer Chemother. Pharmacol. 62 2008 621 629
9. B.N. Breyer, J.M. Whitson, P.R. Carroll, and B.R. Konety Sequential intravesical gemcitabine and mitomycin C chemotherapy regimen in patients with non-muscle invasive bladder cancer Urol. Oncol. 28 2010 510 514
10. F.C. Carvalho, M.S. Barbi, V.H. Sarmento, L.A. Chiavacci, F.M. Netto, and M.P. Gremiao Surfactant systems for nasal zidovudine delivery: structural, rheological and mucoadhesive properties J. Pharm. Pharmacol. 62 2010 430 439
11. C.H. Chen, H.J. Yang, C.T. Shun, C.Y. Huang, K.H. Huang, H.J. Yu, and Y.S. Pu A cocktail regimen of intravesical mitomycin-C, doxorubicin, and cisplatin (MDP) for non-muscle-invasive bladder cancer Urol. Oncol. 30 2012 421 427
12. Y.W. Cho, J.D. Kim, and K. Park Polycation gene delivery systems: escape from endosomes to cytosol J. Pharm. Pharmacol. 55 2003 721 734
13. K.J. Cho, X. Wang, S.M. Nie, Z. Chen, and D.M. Shin Therapeutic nanoparticles for drug delivery in cancer Clin. Cancer Res. 14 2008 1310 1316
14. T.C. Chou Derivation and properties of Michaelis-Menten type and Hill type equations for reference ligands J. Theor. Biol. 59 1976 253 276
15. T.C. Chou Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies Pharmacol. Rev. 58 2006 621 681
16. T.C. Chou Drug combination studies and their synergy quantification using the Chou-Talalay method Cancer Res. 70 2010 440 446
17. M. Colombel, M. Soloway, H. Akaza, A. Bohle, J. Palou, R. Buckley, D. Lamm, M. Brausi, J.A. Witjes, and R. Persad Epidemiology, staging, grading, and risk stratification of bladder cancer Eur. Urol. Suppl. 7 2008 618 626
18. D. Cosco, D. Paolino, J. Maiuolo, D. Russo, and M. Fresta Liposomes as multicompartmental carriers for multidrug delivery in anticancer chemotherapy Drug Deliv. Transl. Res. 1 2011 66 75
19. D. Cosco, D. Paolino, J. Maiuolo, L. Di Marzio, M. Carafa, C.A. Ventura, and M. Fresta Ultradeformable liposomes as multidrug carrier of resveratrol and 5-fluorouracil for their topical delivery Int. J. Pharm. 489 2015 1 10
20. M.E. Davis, Z. Chen, and D.M. Shin Nanoparticle therapeutics: an emerging treatment modality for cancer Nat. Rev. Drug Discov. 7 2008 771 782
21. J.C. Delto, T. Kobayashi, M. Benson, J. McKiernan, and C. Abate-Shen Preclinical analyses of intravesical chemotherapy for prevention of bladder cancer progression Oncotarget 4 2013 269 276
22. J.P. Eder Jr., V.T. Chan, S.W. Ng, N.A. Rizvi, S. Zacharoulis, B.A. Teicher, and L.E. Schnipper DNA topoisomerase II alpha expression is associated with alkylating agent resistance Cancer Res. 55 1995 6109 6116
23. C. Fabre, N. Mimura, K. Bobb, S.Y. Kong, G. Gorgun, D. Cirstea, Y. Hu, J. Minami, H. Ohguchi, J. Zhang, J. Meshulam, R.D. Carrasco, Y.T. Tai, P.G. Richardson, T. Hideshima, and K.C. Anderson Dual inhibition of canonical and noncanonical NF-kappaB pathways demonstrates significant antitumor activities in multiple myeloma Clin. Cancer Res. 18 2012 4669 4681
24. N. Fang, V. Chan, H.-Q. Mao, and K.W. Leong Interactions of phospholipid bilayer with chitosan: effect of molecular weight and pH Biomacromolecules 2 2001 1161 1168
25. M. Ferrari Cancer nanotechnology: opportunities and challenges Nat. Rev. Cancer 5 2005 161 171
26. F. Greco, and M.J. Vicent Combination therapy: opportunities and challenges for polymer-drug conjugates as anticancer nanomedicines Adv. Drug Deliv. Rev. 61 2009 1203 1213
27. S. GuhaSarkar, and R. Banerjee Intravesical drug delivery: challenges, current status, opportunities and novel strategies J. Control. Release 148 2010 147 159
28. B.A. Hadaschik, M.G. ter Borg, J. Jackson, R.D. Sowery, A.I. So, H.M. Burt, and M.E. Gleave Paclitaxel and cisplatin as intravesical agents against non-muscle-invasive bladder cancer BJU Int. 101 2008 1347 1355
29. 2 +, with N-acetyl-l-cysteine Russ. J. Inorg. Chem. 55 2010 223 228
30. H. He, Y. Wang, H. Wen, and X.R. Jia Dendrimer-based multilayer nanocarrier for potential synergistic paclitaxel-doxorubicin combination drug delivery RSC Adv. 4 2014 3643 3652
31. C.F. Higgins Multiple molecular mechanisms for multidrug resistance transporters Nature 446 2007 749 757
32. G.N. Hortobagyi Anthracyclines in the treatment of cancer - an overview Drugs 54 1997 1 7
33. Y. Hu, X.Q. Jiang, Y. Ding, Q. Chen, and C.Z. Yang Core-template-free strategy for preparing hollow nanospheres Adv. Mater. 16 2004 933 937
34. Y. Hu, Q. Chen, Y. Ding, R.T. Li, X.Q. Jiang, and B.R. Liu Entering and lighting up nuclei using hollow chitosan-gold hybrid nanospheres Adv. Mater. 21 2009 3639 3643
35. C. Huang, K.G. Neoh, L. Xu, E.T. Kang, and E. Chiong Polymeric nanoparticles with encapsulated superparamagnetic iron oxide and conjugated cisplatin for potential bladder cancer therapy Biomacromolecules 13 2012 2513 2520
36. L. Kelland The resurgence of platinum-based cancer chemotherapy Nat. Rev. Cancer 7 2007 573 584
37. M.K. Kos, M. Bogataj, P. Veranic, and A. Mrhar Permeability of pig urinary bladder wall: time and concentration dependent effect of chitosan Biol. Pharm. Bull. 29 2006 1685 1691
38. D. Lane Designer combination therapy for cancer Nat. Biotechnol. 24 2006 163 164
39. S.M. Lee, T.V. O'Halloran, and S.T. Nguyen Polymer-caged nanobins for synergistic cisplatin-doxorubicin combination chemotherapy J. Am. Chem. Soc. 132 2010 17130 17138
40. B.D. Liboiron, and L.D. Mayer Nanoscale particulate systems for multidrug delivery: towards improved combination chemotherapy Ther. Deliv. 5 2014 149 171
41. T.Y. Lin, Y.P. Li, H. Zhang, J. Luo, N. Goodwin, T. Gao, R. de Vere White, K.S. Lam, and C.X. Pan Tumor-targeting multifunctional micelles for imaging and chemotherapy of advanced bladder cancer Nanomedicine (London) 8 2013 1239 1251
42. B. Lippert Cisplatin: chemistry and biochemistry of a leading anticancer drug Verlag Helvetica Chimica Acta 1999 Wiley-VCH Zürich Weinheim; New York
43. Y. Matsumura, and H. Maeda A new concept for macromolecular therapeutics in cancer-chemotherapy - mechanism of tumoritropic accumulation of proteins and the antitumor agent smancs Cancer Res. 46 1986 6387 6392
44. G. Minotti, P. Menna, E. Salvatorelli, G. Cairo, and L. Gianni Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity Pharmacol. Rev. 56 2004 185 229
45. N. Mishra, A.K. Goyal, S. Tiwari, R. Paliwal, S.R. Paliwal, B. Vaidya, S. Mangal, M. Gupta, D. Dube, A. Mehta, and S.P. Vyas Recent advances in mucosal delivery of vaccines: role of mucoadhesive/biodegradable polymeric carriers Expert Opin. Ther. Pat. 20 2010 661 679
46. C.E. Mora-Huertas, H. Fessi, and A. Elaissari Polymer-based nanocapsules for drug delivery Int. J. Pharm. 385 2010 113 142
47. C. Mugabe, B.A. Hadaschik, R.K. Kainthan, D.E. Brooks, A.I. So, M.E. Gleave, and H.M. Burt Paclitaxel incorporated in hydrophobically derivatized hyperbranched polyglycerols for intravesical bladder cancer therapy BJU Int. 103 2009 978 986
48. C. Mugabe, Y. Matsui, A.I. So, M.E. Gleave, J.H. Baker, A.I. Minchinton, I. Manisali, R. Liggins, D.E. Brooks, and H.M. Burt In vivo evaluation of mucoadhesive nanoparticulate docetaxel for intravesical treatment of non-muscle-invasive bladder cancer Clin. Cancer Res. 17 2011 2788 2798
49. C. Mugabe, Y. Matsui, A.I. So, M.E. Gleave, M. Heller, M. Zeisser-Labouebe, L. Heller, I. Chafeeva, D.E. Brooks, and H.M. Burt In vitro and in vivo evaluation of intravesical docetaxel loaded hydrophobically derivatized hyperbranched polyglycerols in an orthotopic model of bladder cancer Biomacromolecules 12 2011 949 960
50. C. Mugabe, P.A. Raven, L. Fazli, J.H. Baker, J.K. Jackson, R.T. Liggins, A.I. So, M.E. Gleave, A.I. Minchinton, D.E. Brooks, and H.M. Burt Tissue uptake of docetaxel loaded hydrophobically derivatized hyperbranched polyglycerols and their effects on the morphology of the bladder urothelium Biomaterials 33 2012 692 703
51. J.R. Peng, T.T. Qi, J.F. Liao, B.Y. Chu, Q. Yang, W.T. Li, Y. Qu, F. Luo, and Z.Y. Qian Controlled release of cisplatin from pH-thermal dual responsive nanogels Biomaterials 34 2013 8726 8740
52. M. Ploeg, K.K. Aben, and L.A. Kiemeney The present and future burden of urinary bladder cancer in the world World J. Urol. 27 2009 289 293 v
53. I. Richard, M. Thibault, G. De Crescenzo, M.D. Buschmann, and M. Lavertu Ionization behavior of chitosan and chitosan-DNA polyplexes indicate that chitosan has a similar capability to induce a proton-sponge effect as PEI Biomacromolecules 14 2013 1732 1740
54. I.M. Shaikh, K.B. Tan, A. Chaudhury, Y.J. Liu, B.J. Tan, B.M.J. Tan, and G.N.C. Chiu Liposome co-encapsulation of synergistic combination of irinotecan and doxorubicin for the treatment of intraperitoneally grown ovarian tumor xenograft J. Control. Release 172 2013 852 861
55. Z. Shen, T. Shen, M.G. Wientjes, M.A. O'Donnell, and J.L. Au Intravesical treatments of bladder cancer: review Pharm. Res. 25 2008 1500 1510
56. J.D. Smart The basics and underlying mechanisms of mucoadhesion Adv. Drug Deliv. Rev. 57 2005 1556 1568
57. H. Takeuchi, H. Yamamoto, and Y. Kawashima Mucoadhesive nanoparticulate systems for peptide drug delivery Adv. Drug Deliv. Rev. 47 2001 39 54
58. P.G. Tardi, R.C. Gallagher, S. Johnstone, N. Harasym, M. Webb, M.B. Bally, and L.D. Mayer Coencapsulation of irinotecan and floxuridine into low cholesterol-containing liposomes that coordinate drug release in vivo Biochim. Biophys. Acta Biomembr. 1768 2007 678 687
59. J.T. Thigpen, M.F. Brady, H.D. Homesley, J. Malfetano, B. DuBeshter, R.A. Burger, and S. Liao Phase III trial of doxorubicin with or without cisplatin in advanced endometrial carcinoma: a gynecologic oncology group study J. Clin. Oncol. 22 2004 3902 3908
60. J. Thongborisute, and H. Takeuchi Evaluation of mucoadhesiveness of polymers by BIACORE method and mucin-particle method Int. J. Pharm. 354 2008 204 209
61. V.P. Torchilin Nanoparticulates as Drug Carriers 2006 Imperial College Press; World Scientific Pub. London, Hackensack, N.J
62. V.P. Torchilin Multifunctional nanocarriers Adv. Drug Deliv. Rev. 64 2012 302 315
63. P. Tyagi, P.C. Wu, M. Chancellor, N. Yoshimura, and L. Huang Recent advances in intravesical drug/gene delivery Mol. Pharm. 3 2006 369 379
64. I.M. van der Lubben, J.C. Verhoef, G. Borchard, and H.E. Junginger Chitosan and its derivatives in mucosal drug and vaccine delivery Eur. J. Pharm. Sci. 14 2001 201 207
65. P. Veranic, A. Erman, M. Kerec-Kos, M. Bogataj, A. Mrhar, and K. Jezernik Rapid differentiation of superficial urothelial cells after chitosan-induced desquamation Histochem. Cell Biol. 131 2009 129 139
66. T. Wang, S.H. Yang, L.A. Mei, C.K. Parmar, J.W. Gillespie, K.P. Praveen, V.A. Petrenko, and V.P. Torchilin Paclitaxel-loaded PEG-PE-based micellar nanopreparations targeted with tumor-specific landscape phage fusion protein enhance apoptosis and efficiently reduce tumors Mol. Cancer Ther. 13 2014 2864 2875
67. M. Wirth, V.E. Plattner, and F. Gabor Strategies to improve drug delivery in bladder cancer therapy Expert Opin. Drug Deliv. 6 2009 727 744
68. S. Wittaya-areekul, J. Kruenate, and C. Prahsarn Preparation and in vitro evaluation of mucoadhesive properties of alginate/chitosan microparticles containing prednisolone Int. J. Pharm. 312 2006 113 118
69. F.J. Xu, Z.X. Zhang, Y. Ping, J. Li, E.T. Kang, and K.G. Neoh Star-shaped cationic polymers by atom transfer radical polymerization from beta-cyclodextrin cores for nonviral gene delivery Biomacromolecules 10 2009 285 293
70. W.J. Yang, T. Cai, K.G. Neoh, E.T. Kang, S.L.M. Teo, and D. Rittschof Barnacle cement as surface anchor for "clicking" of antifouling and antimicrobial polymer brushes on stainless steel Biomacromolecules 14 2013 2041 2051
71. L. Ye, K. Letchford, M. Heller, R. Liggins, D. Guan, J.N. Kizhakkedathu, D.E. Brooks, J.K. Jackson, and H.M. Burt Synthesis and characterization of carboxylic acid conjugated, hydrophobically derivatized, hyperbranched polyglycerols as nanoparticulate drug carriers for cisplatin Biomacromolecules 12 2011 145 155
72. J. Zhang, L. Miao, S.T. Guo, Y. Zhang, L. Zhang, A. Satterlee, W.Y. Kim, and L. Huang Synergistic anti-tumor effects of combined gemcitabine and cisplatin nanoparticles in a stroma-rich bladder carcinoma model J. Control. Release 182 2014 90 96
73. L. Zhao, M.G. Wientjes, and J.L. Au Evaluation of combination chemotherapy: integration of nonlinear regression, curve shift, isobologram, and combination index analyses Clin. Cancer Res. 10 2004 7994 8004
74. Y.F. Zhu, W.J. Meng, H. Gao, and N. Hanagata Hollow mesoporous silica/poly(l-lysine) particles for codelivery of drug and gene with enzyme-triggered release property J. Phys. Chem. C 115 2011 13630 13636