Multifunctional polymersomes for cytosolic delivery of gemcitabine and doxorubicin to cancer cells

Biomaterials

Volumn 35, Issue 24, 2014, Pages 6482-6497

  Nahire, Rahul ^a   Haldar, Manas K ^a   Paul, Shirshendu ^c   Ambre, Avinash H ^b   Meghnani, Varsha ^a   Layek, Buddhadev ^a   Katti, Kalpana S ^b   Gange, Kara N ^a   Singh, Jagdish ^a   Sarkar, Kausik ^c,d   Mallik, Sanku ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b North Dakota State University   (United States)

^c UNIVERSITY OF DELAWARE   (United States)

^d George Washington University   (United States)

Author keywords

Drug delivery; Gemcitabine; Liposome; Pancreatic cancer; Polymersome

Indexed keywords

CELLS; DRUG DELIVERY; DRUG PRODUCTS; LIPOSOMES; ULTRASONIC IMAGING;

AMPHIPHILIC POLYMERS; DIAGNOSTIC ULTRASOUND; ENCAPSULATED DRUGS; GEMCITABINE; MULTI-FUNCTIONAL NANOCARRIERS; PANCREATIC CANCERS; POLYMERSOMES; TRIGGERED RELEASE;

POLYMERS;

CALCEIN; DEOXYCYTIDINE; DOXORUBICIN; FLUORESCEIN DERIVATIVE; GEMCITABINE; LIPOSOME; POLYMER; REDUCING AGENT;

ACOUSTICS; ANALOGS AND DERIVATIVES; ATOMIC FORCE MICROSCOPY; CELL SURVIVAL; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOSOL; DIFFERENTIAL SCANNING CALORIMETRY; DRUG DELIVERY SYSTEM; DRUG EFFECTS; FLUORESCENCE; GEL CHROMATOGRAPHY; HUMAN; METABOLISM; MULTICELLULAR SPHEROID; NEOPLASMS; OXIDATION REDUCTION REACTION; PARTICLE SIZE; PATHOLOGY; PH; SYNTHESIS; TUMOR CELL LINE; ULTRASOUND; ULTRASTRUCTURE; ULTRAVIOLET SPECTROPHOTOMETRY;

ACOUSTICS; CALORIMETRY, DIFFERENTIAL SCANNING; CELL LINE, TUMOR; CELL SURVIVAL; CHROMATOGRAPHY, GEL; CYTOSOL; DEOXYCYTIDINE; DOXORUBICIN; DRUG DELIVERY SYSTEMS; FLUORESCEINS; FLUORESCENCE; HUMANS; HYDROGEN-ION CONCENTRATION; LIPOSOMES; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, CONFOCAL; NEOPLASMS; OXIDATION-REDUCTION; PARTICLE SIZE; POLYMERS; REDUCING AGENTS; SPECTROPHOTOMETRY, ULTRAVIOLET; SPHEROIDS, CELLULAR; ULTRASONICS;

EID: 84901448814     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.04.026     Document Type: Article

References (69)

1. Toschi L., Finocchiaro G., Bartolini S., Gioia V., Cappuzzo F. Role of gemcitabine in cancer therapy. Future Oncol 2005, 1:7-17.
2. Dasanu C.A. Gemcitabine: vascular toxicity and prothrombotic potential. Expert Opin Drug Saf 2008, 7:703-716.
3. Moog R., Burger A.M., Brandl M., Schuler J., Schubert R., Unger C., et al. Change in pharmacokinetic and pharmacodynamic behavior of gemcitabine in human tumor xenografts upon entrapment in vesicular phospholipid gels. Cancer Chemother Pharmacol 2002, 49:356-366.
4. Farrell J.J., Elsaleh H., Garcia M., Lai R., Ammar A., Regine W.F., et al. Human equilibrative nucleoside transporter 1 levels predict response to gemcitabine in patients with pancreatic cancer. Gastroenterology 2009, 136:187-195.
5. Lee G.Y., Qian W.P., Wang L., Wang Y.A., Staley C.A., Satpathy M., et al. Theranostic nanoparticles with controlled release of gemcitabine for targeted therapy and MRI of pancreatic cancer. ACS Nano 2013, 7:2078-2089.
6. Dalla Pozza E., Lerda C., Costanzo C., Donadelli M., Dando I., Zoratti E., et al. Targeting gemcitabine containing liposomes to CD44 expressing pancreatic adenocarcinoma cells causes an increase in the antitumoral activity. Biochim Biophys Acta 2013, 1828:1396-1404.
7. Zhu S., Wonganan P., Lansakara P.D., O'Mary H.L., Li Y., Cui Z. The effect of the acid-sensitivity of 4-(N)-stearoyl gemcitabine-loaded micelles on drug resistance caused by RRM1 overexpression. Biomaterials 2013, 34:2327-2339.
8. Kotopoulis S., Dimcevski G., Gilja O.H., Hoem D., Postema M. Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study. Med Phys 2013, 40:072902.
9. Julka P.K., Chacko R.T., Nag S., Parshad R., Nair A., Koppiker C.B., et al. Aphase 2 study of sequential neoadjuvant chemotherapy with gemcitabine and doxorubicin followed by gemcitabine and cisplatin in patients with large or locally advanced operable breast cancer: results from long-term follow-up. Breast Cancer 2013, 20:357-362.
10. Crespo G., Sierra M., Losa R., Berros J.P., Villanueva N., Fra J., et al. Pegylated liposomal doxorubicin and gemcitabine in a fixed dose rate infusion for the treatment of patients with poor prognosis of recurrent ovarian cancer: a phase Ib study. Int J Gynecol Cancer 2011, 21:478-485.
11. Del Barco S., Colomer R., Calvo L., Tusquets I., Adrover E., Sanchez P., et al. Non-pegylated liposomal doxorubicin combined with gemcitabine as first-line treatment for metastatic or locally advanced breast cancer. Final results of a phase I/II trial. Breast Cancer Res Treat 2009, 116:351-358.
12. Roubaud G., Gross-Goupil M., Wallerand H., de Clermont H., Dilhuydy M.S., Ravaud A. Combination of gemcitabine and doxorubicin in rapidly progressive metastatic renal cell carcinoma and/or sarcomatoid renal cell carcinoma. Oncology 2011, 80:214-218.
13. Franchina T., Adamo B., Ricciardi G.R., Caristi N., Agostino R.M., Proto C., et al. Activity of pegylated liposomal doxorubicin in combination with gemcitabine in triple negative breast cancer with skin involvement: two case reports. Cancer Biol Ther 2012, 13:472-476.
14. Rivera E., Valero V., Arun B., Royce M., Adinin R., Hoelzer K., et al. Phase II study of pegylated liposomal doxorubicin in combination with gemcitabine in patients with metastatic breast cancer. JClin Oncol 2003, 21:3249-3254.
15. Fabi A., Ferretti G., Papaldo P., Salesi N., Ciccarese M., Lorusso V., et al. Pegylated liposomal doxorubicin in combination with gemcitabine: a phase II study in anthracycline-naive and anthracycline pretreated metastatic breast cancer patients. Cancer Chemother Pharmacol 2006, 57:615-623.
16. Liu D., Chen Y., Feng X., Deng M., Xie G., Wang J., et al. Micellar nanoparticles loaded with gemcitabine and doxorubicin showed synergistic effect. Colloids Surf B Biointerfaces 2013, 113C:158-168.
17. Rivera E., Valero V., Syrewicz L., Rahman Z., Esteva F.J., Theriault R.L., et al. Phase I study of stealth liposomal doxorubicin in combination with gemcitabine in the treatment of patients with metastatic breast cancer. JClin Oncol 2001, 19:1716-1722.
18. D'Agostino G., Ferrandina G., Ludovisi M., Testa A., Lorusso D., Gbaguidi N., et al. Phase II study of liposomal doxorubicin and gemcitabine in the salvage treatment of ovarian cancer. Br J Cancer 2003, 89:1180-1184.
19. Jacquin J.P., Chargari C., Thorin J., Mille D., Melis A., Orfeuvre H., et al. Phase II trial of pegylated liposomal doxorubicin in combination with gemcitabine in metastatic breast cancer patients. Am J Clin Oncol 2012, 35:18-21.
20. Lammers T., Subr V., Ulbrich K., Peschke P., Huber P.E., Hennink W.E., et al. Simultaneous delivery of doxorubicin and gemcitabine to tumors invivo using prototypic polymeric drug carriers. Biomaterials 2009, 30:3466-3475.
21. Barenholz Y. Doxil(R)-the first FDA-approved nano-drug: lessons learned. JControl Release 2012, 160:117-134.
22. Maeda H., Matsumura Y. EPR effect based drug design and clinical outlook for enhanced cancer chemotherapy. Adv Drug Deliv Rev 2011, 63:129-130.
23. Discher D.E., Ortiz V., Srinivas G., Klein M.L., Kim Y., Christian D., et al. Emerging applications of polymersomes in delivery: from molecular dynamics to shrinkage of tumors. Prog Polym Sci 2007, 32:838-857.
24. Szebeni J., Baranyi L., Savay S., Bodo M., Morse D.S., Basta M., et al. Liposome-induced pulmonary hypertension: properties and mechanism of a complement-mediated pseudoallergic reaction. Am J Physiol Heart Circ Physiol 2000, 279:H1319-H1328.
25. Nahire R., Haldar M.K., Paul S., Mergoum A., Ambre A.H., Katti K.S., et al. Polymer-coated echogenic lipid nanoparticles with dual release triggers. Biomacromolecules 2013, 14:841-853.
26. Nahire R., Paul S., Scott M.D., Singh R.K., Muhonen W.W., Shabb J., et al. Ultrasound enhanced matrix metalloproteinase-9 triggered release of contents from echogenic liposomes. Mol Pharm 2012, 9:2554-2564.
27. Lee J.S., Feijen J. Polymersomes for drug delivery: design, formation and characterization. JControl Release 2012, 161:473-483.
28. Meng F., Zhong Z., Feijen J. Stimuli-responsive polymersomes for programmed drug delivery. Biomacromolecules 2009, 10:197-209.
29. Jain J.P., Ayen W.Y., Kumar N. Self assembling polymers as polymersomes for drug delivery. Curr Pharm Des 2011, 17:65-79.
30. Choucair A., Soo P.L., Eisenberg A. Active loading and tunable release of doxorubicin from block copolymer vesicles. Langmuir 2005, 21:9308-9313.
31. Ahmed F., Discher D.E. Self-porating polymersomes of PEG-PLA and PEG-PCL: hydrolysis-triggered controlled release vesicles. JControl Release 2004, 96:37-53.
32. Chiang W.H., Huang W.C., Chang C.W., Shen M.Y., Shih Z.F., Huang Y.F., et al. Functionalized polymersomes with outlayered polyelectrolyte gels for potential tumor-targeted delivery of multimodal therapies and MR imaging. JControl Release 2013, 168:280-288.
33. Canton I., Battaglia G. Polymersomes-mediated delivery of fluorescent probes for targeted and long-term imaging in live cell microscopy. Methods Mol Biol 2013, 991:343-351.
34. Petersen M.A., Hillmyer M.A., Kokkoli E. Bioresorbable polymersomes for targeted delivery of Cisplatin. Bioconjug Chem 2013, 24:533-543.
35. Zhang Y., Zhang W., Johnston A.H., Newman T.A., Pyykko I., Zou J. Targeted delivery of Tet1 peptide functionalized polymersomes to the rat cochlear nerve. Int J Nanomedicine 2012, 7:1015-1022.
36. Zhou W., Meng F., Engbers G.H., Feijen J. Biodegradable polymersomes for targeted ultrasound imaging. JControl Release 2006, 116:e62-e64.
37. Ahmed F., Pakunlu R.I., Srinivas G., Brannan A., Bates F., Klein M.L., et al. Shrinkage of a rapidly growing tumor by drug-loaded polymersomes: pH-triggered release through copolymer degradation. Mol Pharm 2006, 3:340-350.
38. Gaitzsch J., Canton I., Appelhans D., Battaglia G., Voit B. Cellular interactions with photo-cross-linked and pH-sensitive polymersomes: biocompatibility and uptake studies. Biomacromolecules 2012, 13:4188-4195.
39. Kim H., Kang Y.J., Kang S., Kim K.T. Monosaccharide-responsive release of insulin from polymersomes of polyboroxole block copolymers at neutral pH. JAm Chem Soc 2012, 134:4030-4033.
40. Cerritelli S., Velluto D., Hubbell J.A. PEG-SS-PPS: reduction-sensitive disulfide block copolymer vesicles for intracellular drug delivery. Biomacromolecules 2007, 8:1966-1972.
41. Kamat N.P., Robbins G.P., Rawson J.S., Therien M.J., Dmochowski I.J., Hammer D.A. Ageneralized system for photo-responsive membrane rupture in polymersomes. Adv Funct Mater 2010, 20:2588-2596.
42. Amstad E., Kim S.H., Weitz D.A. Photo- and thermoresponsive polymersomes for triggered release. Angew Chem Int Ed Engl 2012, 51:12499-12503.
43. Oliveira H., Perez-Andres E., Thevenot J., Sandre O., Berra E., Lecommandoux S. Magnetic field triggered drug release from polymersomes for cancer therapeutics. JControl Release 2013, 169:165-170.
44. Saito G., Swanson J.A., Lee K.D. Drug delivery strategy utilizing conjugation via reversible disulfide linkages: role and site of cellular reducing activities. Adv Drug Deliv Rev 2003, 55:199-215.
45. West K.R., Otto S. Reversible covalent chemistry in drug delivery. Curr Drug Discov Technol 2005, 2:123-160.
46. Paul S., Russakow D., Nahire R., Nandy T., Ambre A.H., Katti K., et al. Invitro measurement of attenuation and nonlinear scattering from echogenic liposomes. Ultrasonics 2012, 52:962-969.
47. Robert J.L., Aubrecht K.B. Ring-opening polymerization of lactide to form a biodegradable polymer. JChem Educ 2008, 85:258.
48. Mayer L.D., Tai L.C., Bally M.B., Mitilenes G.N., Ginsberg R.S., Cullis P.R. Characterization of liposomal systems containing doxorubicin entrapped in response to pH gradients. Biochim Biophys Acta 1990, 1025:143-151.
49. Nahire R.R., Joshi S.S., Meghnani V., Shastri N., Surendra Nath K.V., Sathish J. Zero absorbance UV spectrophotometric assay method for simultaneous determination of amlodipine besylate and valsartan. Curr Res Bio Pharm Sci 2013, 2:1-5.
50. Kopechek J.A., Abruzzo T.M., Wang B., Chrzanowski S.M., Smith D.A., Kee P.H., et al. Ultrasound-mediated release of hydrophilic and lipophilic agents from echogenic liposomes. JUltrasound Med 2008, 27:1597-1606.
51. Kopechek J.A., Kim H., McPherson D.D., Holland C.K. Calibration of the 1-MHz Sonitron ultrasound system. Ultrasound Med Biol 2010, 36:1762-1766.
52. Hensel K., Mienkina M.P., Schmitz G. Analysis of ultrasound fields in cell culture wells for invitro ultrasound therapy experiments. Ultrasound Med Biol 2011, 37:2105-2115.
53. Albrecht T., Patel N., Cosgrove D.O., Jayaram V., Blomley M.J., Eckersley R. Enhancement of power Doppler signals from breast lesions with the ultrasound contrast agent EchoGen emulsion: subjective and quantitative assessment. Acad Radiol 1998, 5(Suppl 1):S195-S198. discussion S9.
54. Ho W.Y., Yeap S.K., Ho C.L., Rahim R.A., Alitheen N.B. Development of multicellular tumor spheroid (MCTS) culture from breast cancer cell and a high throughput screening method using the MTT assay. PLoS One 2012, 7:e44640.
55. Jeong B., Bae Y.H., Lee D.S., Kim S.W. Biodegradable block copolymers as injectable drug-delivery systems. Nature 1997, 388:860-862.
56. Discher D.E., Ahmed F. Polymersomes. Annu Rev Biomed Eng 2006, 8:323-341.
57. Liu D., Mori A., Huang L. Role of liposome size and RES blockade in controlling biodistribution and tumor uptake of GM1-containing liposomes. Biochim Biophys Acta 1992, 1104:95-101.
58. Alkan-Onyuksel H., Demos S.M., Lanza G.M., Vonesh M.J., Klegerman M.E., Kane B.J., et al. Development of inherently echogenic liposomes as an ultrasonic contrast agent. JPharm Sci 1996, 85:486-490.
59. Paul S., Nahire R., Mallik S., Sarkar K. Encapsulated microbubbles and echogenic liposomes for contrast ultrasound imaging and targeted drug delivery. Comput Mech 2014, 53:413-435.
60. Jimenez-Fernandez J. Nonlinear response to ultrasound of encapsulated microbubbles. Ultrasonics 2012, 52:784-793.
61. Cleland W.W. Dithiothreitol, a new protective reagent for Sh groups. Biochemistry 1964, 3:480-482.
62. Green D.E. The reduction potentials of cysteine, glutathione and glycylcysteine. Biochem J 1933, 27:678-689.
63. Spinler K., Tian A., Christian D.A., Pantano D.A., Baumgart T., Discher D.E. Dynamic domains in polymersomes: mixtures of polyanionic and neutral diblocks respond more rapidly to changes in calcium than to pH. Langmuir 2013, 29:7499-7508.
64. Perez-Manga G., Lluch A., Alba E., Moreno-Nogueira J.A., Palomero M., Garcia-Conde J., et al. Gemcitabine in combination with doxorubicin in advanced breast cancer: final results of a phase II pharmacokinetic trial. JClin Oncol 2000, 18:2545-2552.
65. Lombardi G., Zustovich F., Farinati F., Cillo U., Vitale A., Zanus G., et al. Pegylated liposomal doxorubicin and gemcitabine in patients with advanced hepatocellular carcinoma: results of a phase 2 study. Cancer 2011, 117:125-133.
66. Nahire R.R., Joshi S.S., Meghnani V., Shastri N., Nath K.S., Sathish J. Stability indicating RP-HPLC method for simultaneous determination of amlodipine besylate and valsartan combination in bulk and commercial dosage forms. Asian J Pharm Life Sci 2012, 2:280-290.
67. Joshi S.S., Nahire R.R., Shastri N., Surendranath K.V., Satish J. Validated stability-indicating RP-HPLC UV method for simultaneous determination of metformin and repaglinide. Acta Chromatogr 2012, 24:419-432.
68. Hamid R., Rotshteyn Y., Rabadi L., Parikh R., Bullock P. Comparison of alamar blue and MTT assays for high through-put screening. Toxicol Vitro 2004, 18:703-710.
69. Goodman T.T., Ng C.P., Pun S.H. 3-D tissue culture systems for the evaluation and optimization of nanoparticle-based drug carriers. Bioconjug Chem 2008, 19:1951-1959.