MMP-9 responsive PEG cleavable nanovesicles for efficient delivery of chemotherapeutics to pancreatic cancer

Molecular Pharmaceutics

Volumn 11, Issue 7, 2014, Pages 2390-2399

  Kulkarni, Prajakta S ^a   Haldar, Manas K ^a   Nahire, Rahul R ^a   Katti, Preeya ^b   Ambre, Avinash H ^c   Muhonen, Wallace W ^d   Shabb, John B ^d   Padi, Sathish K R ^a   Singh, Raushan K ^a   Borowicz, Pawel P ^a   Shrivastava, D K ^a   Katti, Kalpana S ^c   Reindl, Katie ^a   Guo, Bin ^a   Mallik, Sanku ^a  

^a NORTH DAKOTA STATE UNIVERSITY   (United States)

^b Davies High School   (United States)

^c North Dakota State University   (United States)

^d UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

drug delivery; drug release; matrix metalloproteinase 9; nanoparticle; pancreatic cancer cell spheroids; peptide

Indexed keywords

2 OLEOYL 1 PALMITOYLPHOSPHATIDYLCHOLINE; CHOLESTEROL HYDROGEN SUCCINATE; COLLAGEN; GELATINASE B; GEMCITABINE; GLUTATHIONE; GLYCEROPHOSPHOETHANOLAMINE; LIPOPEPTIDE; LIPOSOME; MACROGOL; NANOPARTICLE; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; ANTINEOPLASTIC AGENT; DEOXYCYTIDINE; DRUG CARRIER; LIPID BILAYER; MACROGOL DERIVATIVE; PHOSPHATIDYLCHOLINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CHEMOTHERAPY; CARCINOMA CELL LINE; CELL VIABILITY; CONTROLLED STUDY; COVALENT BOND; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG RELEASE; FEMALE; HUMAN; HUMAN CELL; HYDROLYSIS; IN VITRO STUDY; IN VIVO STUDY; LIPID BILAYER; LIPID VESICLE; MOUSE; NANOENCAPSULATION; NONHUMAN; PANCREAS CANCER; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; QUANTITATIVE ANALYSIS; SPHEROID CELL; TREATMENT DURATION; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ANALOGS AND DERIVATIVES; ANIMAL; CARCINOMA, PANCREATIC DUCTAL; CHEMISTRY; EXTRACELLULAR MATRIX; METABOLISM; NUDE MOUSE; PANCREATIC NEOPLASMS; PROCEDURES; TRANSPORT VESICLE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; CARCINOMA, PANCREATIC DUCTAL; CELL LINE, TUMOR; DEOXYCYTIDINE; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; EXTRACELLULAR MATRIX; FEMALE; GLUTATHIONE; HUMANS; HYDROLYSIS; LIPID BILAYERS; LIPOPEPTIDES; MATRIX METALLOPROTEINASE 9; MICE; MICE, NUDE; NANOPARTICLES; PANCREATIC NEOPLASMS; PHOSPHATIDYLCHOLINES; POLYETHYLENE GLYCOLS; TRANSPORT VESICLES;

EID: 84903977849     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp500108p     Document Type: Article

References (36)

1. Fleige, E.; Quadir, M. A.; Haag, R. Stimuli-responsive polymeric nanocarriers for the controlled transport of active compounds: Concepts and applications Adv. Drug Delivery Rev. 2012, 64 (9) 866-884
2. Ganta, S.; Devalapally, H.; Shahiwala, A.; Amiji, M. A review of stimuli-responsive nanocarriers for drug and gene delivery J. Controlled Release 2008, 126 (3) 187-204
3. Radhakrishnan, K.; Tripathy, J.; Raichur, A. M. Dual enzyme responsive microcapsules simulating an "OR" logic gate for biologically triggered drug delivery applications Chem. Commun. 2013, 49 (47) 5390-2
4. de la Rica, R.; Aili, D.; Stevens, M. M. Enzyme-responsive nanoparticles for drug release and diagnostics Adv. Drug Delivery Rev. 2012, 64 (11) 967-978
5. Coleman, J. D.; Thompson, J. T.; Smith, R. W., 3rd; Prokopczyk, B.; Vanden, H. J. P. Role of Peroxisome Proliferator-Activated Receptor β/δ and B-Cell Lymphoma-6 in Regulation of Genes Involved in Metastasis and Migration in Pancreatic Cancer Cells PPAR Res. 2013, 2013, 121956
6. Tauro, J. R.; Gemeinhart, R. A. Matrix metalloprotease triggered delivery of cancer chemotherapeutics from hydrogel matrixes Bioconjugate Chem. 2005, 16 (5) 1133-9
7. Molineux, G. PEGylation: engineering improved pharmaceuticals for enhanced therapy Cancer Treat Rev. 2002, 28 (Suppl. A) 13-16
8. Moribe, K.; Maruyama, K. Reviews on PEG coated liposomal drug carriers Drug Delivery Syst. 2001, 16 (3) 165-171
9. Liu, D.-L.; Chang, X.; Dong, C.-M. Reduction- and thermo-sensitive star polypeptide micelles and hydrogels for on-demand drug delivery Chem. Commun. 2013, 49 (12) 1229-1231
10. Li, J.; Ge, Z.; Liu, S. PEG-sheddable polyplex micelles as smart gene carriers based on MMP-cleavable peptide-linked block copolymers Chem. Commun. 2013, 49, 6974-6976
11. Määttä, M.; Soini, Y.; Liakka, A.; Autio-Harmainen, H. Differential expression of matrix metalloproteinase (MMP)-2, MMP-9, and membrane type 1-MMP in hepatocellular and pancreatic adenocarcinoma: implications for tumor progression and clinical prognosis Clin. Cancer Res. 2000, 6 (7) 2726-2734
12. Yingyuad, P.; Mevel, M.; Prata, C.; Furegati, S.; Kontogiorgis, C.; Thanou, M.; Miller, A. D. Enzyme-Triggered PEGylated pDNA-Nanoparticles for Controlled Release of pDNA in Tumors Bioconjugate Chem. 2013, 24 (3) 343-362
13. Koo, A. N.; Lee, H. J.; Kim, S. E.; Chang, J. H.; Park, C.; Kim, C.; Park, J. H.; Lee, S. C. Disulfide-cross-linked PEG-poly(amino acid)s copolymer micelles for glutathione-mediated intracellular drug delivery Chem. Commun. 2008, 48) 6570-6572
14. Ren, T.-B.; Xia, W.-J.; Dong, H.-Q.; Li, Y.-Y. Sheddable micelles based on disulfide-linked hybrid PEG-polypeptide copolymer for intracellular drug delivery Polymer 2011, 52 (16) 3580-3586
15. Zhang, A.; Zhang, Z.; Shi, F.; Ding, J.; Xiao, C.; Zhuang, X.; He, C.; Chen, L.; Chen, X. Disulfide crosslinked PEGylated starch micelles as efficient intracellular drug delivery platforms Soft Matter 2013, 9 (7) 2224-2233
16. Abbott, A. Cell culture: biologys new dimension Nature 2003, 424 (6951) 870-872
17. Phung, Y. T.; Barbone, D.; Broaddus, V. C.; Ho, M. Rapid generation of in vitro multicellular spheroids for the study of monoclonal antibody therapy J. Cancer 2011, 2, 507
18. Longati, P.; Jia, X.; Eimer, J.; Wagman, A.; Witt, M.-R.; Rehnmark, S.; Verbeke, C.; Toftgård, R.; Löhr, M.; Heuchel, R. L. 3D pancreatic carcinoma spheroids induce a matrix-rich, chemoresistant phenotype offering a better model for drug testing BMC Cancer 2013, 13 (1) 1-13
19. Celano, M.; Calvagno, M. G.; Bulotta, S.; Paolino, D.; Arturi, F.; Rotiroti, D.; Filetti, S.; Fresta, M.; Russo, D. Cytotoxic effects of gemcitabine-loaded liposomes in human anaplastic thyroid carcinoma cells BMC Cancer 2004, 4 (1) 63
20. Sarkar, N.; Banerjee, J.; Hanson, A. J.; Elegbede, A. I.; Rosendahl, T.; Krueger, A. B.; Banerjee, A. L.; Tobwala, S.; Wang, R.; Lu, X.; Mallik, S.; Srivastava, D. K. Matrix metalloproteinase-assisted triggered release of liposomal contents Bioconjugate Chem. 2008, 19 (1) 57-64
21. Elegbede, A. I.; Banerjee, J.; Hanson, A. J.; Tobwala, S.; Ganguli, B.; Wang, R.; Lu, X.; Srivastava, D. K.; Mallik, S. Mechanistic studies of the triggered release of liposomal contents by matrix metalloproteinase-9 J. Am. Chem. Soc. 2008, 130 (32) 10633-10642
22. Li, S.-D.; Huang, L. Stealth nanoparticles: high density but sheddable PEG is a key for tumor targeting J. Controlled Release 2010, 145 (3) 178
23. Estrela, J. M.; Ortega, A.; Obrador, E. Glutathione in cancer biology and therapy Crit. Rev. Clin. Lab. Sci. 2006, 43 (2) 143-181
24. Pompella, A.; Visvikis, A.; Paolicchi, A.; Tata, V. D.; Casini, A. F. The changing faces of glutathione, a cellular protagonist Biochem. Pharmacol. 2003, 66 (8) 1499-1503
25. Banerjee, J.; Hanson, A. J.; Gadam, B.; Elegbede, A. I.; Tobwala, S.; Ganguly, B.; Wagh, A. V.; Muhonen, W. W.; Law, B.; Shabb, J. B.; Srivastava, D. K.; Mallik, S. Release of liposomal contents by cell-secreted matrix metalloproteinase-9 Bioconjugate Chem. 2009, 20 (7) 1332-1339
26. Akers, W. J.; Xu, B.; Lee, H.; Sudlow, G. P.; Fields, G. B.; Achilefu, S.; Edwards, W. B. Detection of MMP-2 and MMP-9 activity in vivo with a triple-helical peptide optical probe Bioconjugate Chem. 2012, 23 (3) 656-663
27. Knapinska, A.; Fields, G. B. Chemical biology for understanding matrix metalloproteinase function ChemBioChem 2012, 13 (14) 2002-2020
28. Nahire, R.; Paul, S.; Scott, M. D.; Singh, R. K.; Muhonen, W. W.; Shabb, J.; Gange, K. N.; Srivastava, D. K.; Sarkar, K.; Mallik, S. Ultrasound enhanced matrix metalloproteinase-9 triggered release of contents from echogenic liposomes Mol. Pharmaceutics 2012, 9 (9) 2554-2564
29. Choi, M.-R.; Stanton-Maxey, K. J.; Stanley, J. K.; Levin, C. S.; Bardhan, R.; Akin, D.; Badve, S.; Sturgis, J.; Robinson, J. P.; Bashir, R. A cellular Trojan Horse for delivery of therapeutic nanoparticles into tumors Nano Lett. 2007, 7 (12) 3759-3765
30. Han, L. F.; Chen, Q. B.; Hu, Z. T.; Piao, J. G.; Hong, C. Y.; Yan, J. J.; You, Y. Z. Stimuli-triggered growth and removal of a bioreducible nanoshell on nanoparticles Macromol. Rapid Commun. 2014, 35 (6) 649-654
31. Cai, X.; Dong, C.; Dong, H.; Wang, G.; Pauletti, G. M.; Pan, X.; Wen, H.; Mehl, I.; Li, Y.; Shi, D. Effective gene delivery using stimulus-responsive catiomer designed with redox-sensitive disulfide and acid-labile imine linkers Biomacromolecules 2012, 13 (4) 1024-1034
32. Chen, F.; Ohashi, N.; Li, W.; Eckman, C.; Nguyen, J. H. Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure Hepatology 2009, 50 (6) 1914-1923
33. Sutherland, R. M. Cell and environment interactions in tumor microregions: the multicell spheroid model Science 1988, 240 (4849) 177-184
34. Sasaki, T.; Ohno, T. Cytotoxicity tests on eye drop preparations by LDH release assay in human cultured cell lines Toxicol. In Vitro 1994, 8 (5) 1113-1119
35. Cosco, D.; Bulotta, A.; Ventura, M.; Celia, C.; Calimeri, T.; Perri, G.; Paolino, D.; Costa, N.; Neri, P.; Tagliaferri, P.; Tassone, P.; Fresta, M. In vivo activity of gemcitabine-loaded PEGylated small unilamellar liposomes against pancreatic cancer Cancer Chemother. Pharmacol. 2009, 64 (5) 1009-1020
36. Brusa, P.; Immordino, M. L.; Rocco, F.; Cattel, L. Antitumor activity and pharmacokinetics of liposomes containing lipophilic gemcitabine prodrugs Anticancer Res. 2007, 27 (1A) 195-199