Synergistic targeting/prodrug strategies for intravesical drug delivery - Lectin-modified PLGA microparticles enhance cytotoxicity of stearoyl gemcitabine by contact-dependent transfer

Journal of Controlled Release

Volumn 169, Issue 1-2, 2013, Pages 62-72

  Neutsch, L ^a   Wirth, E M ^a   Spijker, S ^a   Pichl, C ^a   Kahlig H ^a   Gabor, F ^a   Wirth, M ^a  

^a UNIVERSITY OF VIENNA   (Austria)

Author keywords

Bioadhesion; Bladder cancer; Intravesical therapy; Poly(lactide co glycolide); Urothelium; Wheat germ agglutinin

Indexed keywords

BIO-ADHESION; BLADDER CANCERS; INTRAVESICAL THERAPY; POLY LACTIDE-CO-GLYCOLIDE; UROTHELIUM; WHEAT GERM AGGLUTININ;

COPOLYMERS; DISEASES; DRUG DELIVERY; TISSUE;

DRUG PRODUCTS;

GEMCITABINE; GLYCAN; HUMAN SERUM ALBUMIN; LECTIN; POLYGLACTIN; STEAROYL GEMCITABINE; UNCLASSIFIED DRUG; WHEAT GERM AGGLUTININ;

ARTICLE; CYTOTOXICITY; DRUG ACTIVATION; DRUG DELIVERY SYSTEM; FLUORESCENCE; INTRAVESICAL DRUG ADMINISTRATION; PRIORITY JOURNAL;

ANTIMETABOLITES, ANTINEOPLASTIC; CELL LINE, TUMOR; CELL SURVIVAL; DEOXYCYTIDINE; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; LACTIC ACID; LECTINS; POLYGLYCOLIC ACID; PRODRUGS; URINARY BLADDER; URINARY BLADDER NEOPLASMS; UROTHELIUM;

EID: 84877082375     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.04.004     Document Type: Article

References (50)

1. M.H. Kamel, P.C. Moore, N.K. Bissada, and S.M. Heshmat Potential years of life lost due to urogenital cancer in the United States: trends from 1972 to 2006 based on data from the SEER database J. Urol. 187 2012 868 871
2. P. Khandelwal, S.N. Abraham, and G. Apodaca Cell biology and physiology of the uroepithelium Am. J. Physiol. Renal Physiol. 297 2009 F1477 F1501
3. S. GuhaSarkar, and R. Banerjee Intravesical drug delivery: challenges, current status, opportunities and novel strategies J. Control. Release 148 2010 147 159
4. J.P.B. Gasion, and J.F.J. Cruz Improving efficacy of intravesical chemotherapy Eur. Urol. 50 2006 225 234 (Pubitemid 44041091)
5. P. Gontero, L. Marini, and B. Frea Intravesical gemcitabine for superficial bladder cancer: rationale for a new treatment option BJU Int. 96 2005 970 976 (Pubitemid 41531397)
6. J.J. Tomaszewski, and M.C. Smaldone Emerging intravesical therapies for management of nonmuscle invasive bladder cancer Open Access J. Urol. 2 2010 67 84
7. A. Bohle, H. Leyh, C. Frei, M. Kuhn, R. Tschada, T. Pottek, W. Wagner, H.H. Knispel, W. von Pokrzywnitzki, F. Zorlu, K. Helsberg, B. Lubben, V. Soldatenkova, C. Stoffregen, and H. Buttner Single postoperative instillation of gemcitabine in patients with non-muscle-invasive transitional cell carcinoma of the bladder: a randomised, double-blind, placebo-controlled phase III multicentre study Eur. Urol. 56 2009 495 503
8. E. Mini, S. Nobili, B. Caciagli, I. Landini, and T. Mazzei Cellular pharmacology of gemcitabine Ann. Oncol. 17 Suppl. 5 2006 v7 v12
9. L.P. Jordheim, and C. Dumontet Review of recent studies on resistance to cytotoxic deoxynucleoside analogues Biochim. Biophys. Acta 1776 2007 138 159 (Pubitemid 350061069)
10. L. Bildstein, C. Dubernet, and P. Couvreur Prodrug-based intracellular delivery of anticancer agents Adv. Drug Deliv. Rev. 63 2011 3 23
11. X. Song, P.L. Lorenzi, C.P. Landowski, B.S. Vig, J.M. Hilfinger, and G.L. Amidon Amino acid ester prodrugs of the anticancer agent gemcitabine: synthesis, bioconversion, metabolic bioevasion, and hPEPT1-mediated transport Mol. Pharm. 2 2005 157 167 (Pubitemid 41295363)
12. D.M. Bender, J. Bao, A.H. Dantzig, W.D. Diseroad, K.L. Law, N.A. Magnus, J.A. Peterson, E.J. Perkins, Y.J. Pu, S.M. Reutzel-Edens, D.M. Remick, J.J. Starling, G.A. Stephenson, R.K. Vaid, D. Zhang, and J.R. McCarthy Synthesis, crystallization, and biological evaluation of an orally active prodrug of gemcitabine J. Med. Chem. 52 2009 6958 6961
13. M.L. Immordino, P. Brusa, F. Rocco, S. Arpicco, M. Ceruti, and L. Cattel Preparation, characterization, cytotoxicity and pharmacokinetics of liposomes containing lipophilic gemcitabine prodrugs J. Control. Release 100 2004 331 346 (Pubitemid 39572916)
14. F. Castelli, M.G. Sarpietro, M. Ceruti, F. Rocco, and L. Cattel Characterization of lipophilic gemcitabine prodrug-liposomal membrane interaction by differential scanning calorimetry Mol. Pharm. 3 2006 737 744 (Pubitemid 46087489)
15. B.R. Sloat, M.A. Sandoval, D. Li, W.G. Chung, P.D. Lansakara, P.J. Proteau, K. Kiguchi, J. DiGiovanni, and Z. Cui In vitro and in vivo anti-tumor activities of a gemcitabine derivative carried by nanoparticles Int. J. Pharm. 409 2011 278 288
16. A.M. Bergman, A.D. Adema, J. Balzarini, S. Bruheim, I. Fichtner, P. Noordhuis, O. Fodstad, F. Myhren, M.L. Sandvold, H.R. Hendriks, and G.J. Peters Antiproliferative activity, mechanism of action and oral antitumor activity of CP-4126, a fatty acid derivative of gemcitabine, in in vitro and in vivo tumor models Invest. New Drugs 29 2011 456 466
17. P. Couvreur, B. Stella, L.H. Reddy, H. Hillaireau, C. Dubernet, D. Desmaele, S. Lepetre-Mouelhi, F. Rocco, N. Dereuddre-Bosquet, P. Clayette, V. Rosilio, V. Marsaud, J.M. Renoir, and L. Cattel Squalenoyl nanomedicines as potential therapeutics Nano Lett. 6 2006 2544 2548 (Pubitemid 46076946)
18. J.L. Arias, L.H. Reddy, and P. Couvreur Magnetoresponsive squalenoyl gemcitabine composite nanoparticles for cancer active targeting Langmuir 24 2008 7512 7519
19. D. Desmaele, R. Gref, and P. Couvreur Squalenoylation: a generic platform for nanoparticular drug delivery J. Control. Release 161 2012 609 618
20. P. Couvreur, L.H. Reddy, S. Mangenot, J.H. Poupaert, D. Desmaele, S. Lepetre-Mouelhi, B. Pili, C. Bourgaux, H. Amenitsch, and M. Ollivon Discovery of new hexagonal supramolecular nanostructures formed by squalenoylation of an anticancer nucleoside analogue Small 4 2008 247 253 (Pubitemid 351271158)
21. Y.G. Jin, Y.J. Lian, and L.N. Du Self-assembly of N-acyl derivatives of gemcitabine at the air/water interface and the formation of nanoscale structures in water Colloids Surf. A 393 2012 60 65
22. B. Stella, S. Arpicco, F. Rocco, V. Marsaud, J.M. Renoir, L. Cattel, and P. Couvreur Encapsulation of gemcitabine lipophilic derivatives into polycyanoacrylate nanospheres and nanocapsules Int. J. Pharm. 344 2007 71 77 (Pubitemid 47464827)
23. P.D. Lansakara, B.L. Rodriguez, and Z. Cui Synthesis and in vitro evaluation of novel lipophilic monophosphorylated gemcitabine derivatives and their nanoparticles Int. J. Pharm. 429 2012 123 134
24. M.A. Sandoval, B.R. Sloat, D.S.P. Lansakara, A. Kumar, B.L. Rodriguez, K. Kiguchi, J. DiGiovanni, and Z.R. Cui EGFR-targeted stearoyl gemcitabine nanoparticles show enhanced anti-tumor activity J. Control. Release 157 2012 287 296
25. C. Fillafer, D.S. Friedl, M. Wirth, and F. Gabor Fluorescent bionanoprobes to characterize cytoadhesion and cytoinvasion Small 4 2008 627 633 (Pubitemid 351808061)
26. C. Wischke, and S.P. Schwendeman Principles of encapsulating hydrophobic drugs in PLA/PLGA microparticles Int. J. Pharm. 364 2008 298 327
27. G. Ratzinger, U. Langer, L. Neutsch, F. Pittner, M. Wirth, and F. Gabor Surface modification of PLGA particles: the interplay between stabilizer, ligand size, and hydrophobic interactions Langmuir 26 2010 1855 1859
28. W.G. Chung, M.A. Sandoval, B.R. Sloat, D.S.P. Lansakara, and Z.R. Cui Stearoyl gemcitabine nanoparticles overcome resistance related to the over-expression of ribonucleotide reductase subunit M1 J. Control. Release 157 2012 132 140
29. L. Bildstein, B. Pili, V. Marsaud, S. Wack, F. Meneau, S. Lepetre-Mouelhi, D. Desmaele, C. Bourgaux, P. Couvreur, and C. Dubernet Interaction of an amphiphilic squalenoyl prodrug of gemcitabine with cellular membranes Eur. J. Pharm. Biopharm. 79 2011 612 620
30. S. Damaraju, V.L. Damaraju, D. Mowles, M.B. Sawyer, S. Damaraju, and C.E. Cass Cytotoxic activity of gemcitabine in cultured cell lines derived from histologically different types of bladder cancer: Role of thymidine kinase 2 Biochem. Pharmacol. 79 2010 21 29
31. L. Bildstein, C. Dubernet, V. Marsaud, H. Chacun, V. Nicolas, C. Gueutin, A. Sarasin, H. Benech, S. Lepetre-Mouelhi, D. Desmaele, and P. Couvreur Transmembrane diffusion of gemcitabine by a nanoparticulate squalenoyl prodrug: an original drug delivery pathway J. Control. Release 147 2010 163 170
32. M.V. Berridge, P.M. Herst, and A.S. Tan Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction Biotechnol. Annu. Rev. 11 2005 127 152 (Pubitemid 41510276)
33. J.A. Witjes, and K. Hendricksen Intravesical pharmacotherapy for non-muscle-invasive bladder cancer: a critical analysis of currently available drugs, treatment schedules, and long-term results Eur. Urol. 53 2008 45 52 (Pubitemid 350167566)
34. C. Cai, S. Mao, O. Germershaus, A. Schaper, E. Rytting, D. Chen, and T. Kissel Influence of morphology and drug distribution on the release process of FITC-dextran-loaded microspheres prepared with different types of PLGA J. Microencapsul. 26 2009 334 345
35. C. Dubernet Thermoanalysis of microspheres Thermochim. Acta 248 1995 259 269
36. Y. Yeo, and K.N. Park Control of encapsulation efficiency and initial burst in polymeric microparticle systems Arch. Pharm. Res. 27 2004 1 12 (Pubitemid 43158226)
37. C.M. Lehr Lectin-mediated drug delivery: the second generation of bioadhesives J. Control. Release 65 2000 19 29
38. S.M.P. Yi, R.E. Harson, J. Zabner, and M.J. Welsh Lectin binding and endocytosis at the apical surface of human airway epithelia Gene Ther. 8 2001 1826 1832 (Pubitemid 34141488)
39. L. Neutsch, B. Eggenreich, E. Herwig, M. Marchetti-Deschmann, G. Allmaier, F. Gabor, and M. Wirth Lectin bioconjugates trigger urothelial cytoinvasion - a glycotargeted approach for improved intravesical drug delivery Eur. J. Pharm. Biopharm. 82 2012 367 375
40. E. Haltner, J.H. Easson, and C.-M. Lehr Lectins and bacterial invasion factors for controlling endo- and transcytosis of bioadhesive drug carrier systems Eur. J. Pharm. Biopharm. 44 1997 3 13 (Pubitemid 28298770)
41. C. Bies, C.M. Lehr, and J.F. Woodley Lectin-mediated drug targeting: history and applications Adv. Drug Deliv. Rev. 56 2004 425 435 (Pubitemid 38210415)
42. B.L. Bishop, M.J. Duncan, J. Song, G. Li, D. Zaas, and S.N. Abraham Cyclic AMP-regulated exocytosis of Escherichia coli from infected bladder epithelial cells Nat. Med. 13 2007 625 630 (Pubitemid 46828483)
43. M. Born, I. Pahner, G. Ahnert-Hilger, and T. Jons The maintenance of the permeability barrier of bladder facet cells requires a continuous fusion of discoid vesicles with the apical plasma membrane Eur. J. Cell Biol. 82 2003 343 350 (Pubitemid 36944163)
44. L. Neutsch, V.E. Plattner, S. Polster-Wildhofen, A. Zidar, A. Chott, G. Borchard, O. Zechner, F. Gabor, and M. Wirth Lectin mediated biorecognition as a novel strategy for targeted delivery to bladder cancer J. Urol. 186 2011 1481 1488
45. M.E. Kreft, K. Jezernik, M. Kreft, and R. Romih Apical plasma membrane traffic in superficial cells of bladder urothelium Ann. N. Y. Acad. Sci. 1152 2009 18 29
46. T. Kaasgaard, T.L. Andresen, S.S. Jensen, R.O. Holte, L.T. Jensen, and K. Jorgensen Liposomes containing alkylated methotrexate analogues for phospholipase A(2) mediated tumor targeted drug delivery Chem. Phys. Lipids 157 2009 94 103
47. P. Pietzonka, B. Rothen-Rutishauser, P. Langguth, H. Wunderli-Allenspach, E. Walter, and H.P. Merkle Transfer of lipophilic markers from PLGA and polystyrene nanoparticles to caco-2 monolayers mimics particle uptake Pharm. Res. 19 2002 595 601 (Pubitemid 34553665)
48. P. Xu, E. Gullotti, L. Tong, C.B. Highley, D.R. Errabelli, T. Hasan, J.X. Cheng, D.S. Kohane, and Y. Yeo Intracellular drug delivery by poly(lactic-co-glycolic acid) nanoparticles, revisited Mol. Pharm. 6 2009 190 201
49. S. Chutipongtanate, and V. Thongboonkerd Systematic comparisons of artificial urine formulas for in vitro cellular study Anal. Biochem. 402 2010 110 112
50. C. Ohyama Glycosylation in bladder cancer Int. J. Clin. Oncol. 13 2008 308 313.