Drug release kinetics, cell uptake, and tumor toxicity of hybrid VVVVVVKK peptide-assembled polylactide nanoparticles

European Journal of Pharmaceutics and Biopharmaceutics

Volumn 84, Issue 1, 2013, Pages 49-62

  Jabbari, Esmaiel ^a   Yang, Xiaoming ^a,b   Moeinzadeh, Seyedsina ^a   He, Xuezhong ^a  

^a University of South Carolina   (United States)

^b Dorn Research Institute   (United States)

Author keywords

Cell uptake; Drug pharmacokinetics; Hybrid nanoparticle; Polymer conjugation; Self assembling peptide; Tumor toxicity

Indexed keywords

ASPARAGINASE MACROGOL; DNA; DOXORUBICIN; LOW MOLECULAR WEIGHT POLYLACTIDE; NANOPARTICLE; PACLITAXEL; PEPTIDE DERIVATIVE; POLYLACTIDE; SELF ASSEMBLED MONOLAYER; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AREA UNDER THE CURVE; ARTICLE; BREAST CARCINOMA; CELL MEMBRANE; CONTROLLED STUDY; DNA DAMAGE; DRUG DISTRIBUTION; DRUG RELEASE; DRUG STABILITY; EMBRYO; ENCAPSULATION; FEMALE; HUMAN; HUMAN CELL; HYDROPHOBICITY; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN INTERACTION; SIMULATION; STATIC ELECTRICITY; TUMOR CELL; TUMOR INVASION;

ANIMALS; BONE MARROW CELLS; CELL LINE, TUMOR; CELL SURVIVAL; MICE; MICE, INBRED C3H; NANOPARTICLES; OLIGOPEPTIDES; POLYESTERS; RATS; RATS, WISTAR;

EID: 84876911492     PISSN: 09396411     EISSN: 18733441     Source Type: Journal    
DOI: 10.1016/j.ejpb.2012.12.012     Document Type: Article

References (91)

1. E. Jabbari Targeted delivery with peptidomimetic conjugated self-assembled nanoparticles Pharm. Res. 26 3 2009 612 630
2. D.E. Owens, and N.A. Peppas Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles Int. J. Pharm. 307 1 2006 93 102
3. K.K. Upadhyay, H.G. Agrawal, C. Upadhyay, C. Schatz, J.F. Le Meins, A. Misra, and S. Lecommandoux Role of block copolymer nanoconstructs in cancer therapy Crit. Rev. Ther. Drug 26 2 2009 157 205
4. E.A. Rossi, R.M. Sharkey, W. McBride, H. Karacay, L. Zeng, H.J. Hansen, D.M. Goldenberg, and C.H. Chang Development of new multivalent-bispecific agents for pretargeting tumor localization and therapy Clin. Cancer Res. 9 10 2003 3886S 3896S
5. K.F. Pirollo, and E.H. Chang Does a targeting ligand influence nanoparticle tumor localization or uptake? Trends Biotechnol. 26 10 2008 552 558
6. K. Buyens, S.C. De Smedt, K. Braeckmans, J. Demeester, L. Peeters, L.A. van Grunsven, X.D. du Jeu, R. Sawant, V. Torchilin, K. Farkasova, M. Ogris, and N.N. Sanders Liposome based systems for systemic siRNA delivery: stability in blood sets the requirements for optimal carrier design J. Control. Release 158 3 2012 362 370
7. L. Battaglia, and M. Gallarate Lipid nanoparticles: state of the art, new preparation methods and challenges in drug delivery Exp. Opin. Drug Deliv. 9 5 2012 497 508
8. Z.H. Liu, Y.T. Wang, and N. Zhang Micelle-like nanoassemblies based on polymer-drug conjugates as an emerging platform for drug delivery Exp. Opin. Drug Deliv. 9 7 2012 805 822
9. W.X. Ma, M.S. Chen, S. Kaushal, M. McElroy, Y. Zhang, C. Ozkan, M. Bouvet, C. Kruse, D. Grotjahn, T. Ichim, and B. Minev PLGA nanoparticle-mediated delivery of tumor antigenic peptides elicits effective immune responses Int. J. Nanomed. 7 2012 1475 1487
10. S. Parveen, and S.K. Sahoo Long circulating chitosan/PEG blended PLGA nanoparticle for tumor drug delivery Eur. J. Pharmacol. 670 2-3 2011 372 383
11. M. Gupta, G.P. Agrawal, S.P. Vyas, Polymeric nanomedicines as promising vehicle for solid tumor therapy and targeting, Curr. Mol. Med. (2012) PMID: 22834834.
12. G. Deepa, N.A. Kumar, J.J. Pillai, and G.S. Kumar Polymer nanoparticles-a novel strategy for administration of paclitaxel in cancer chemotherapy Curr. Med. Chem. 19 36 2012 6207 6213
13. N. Nishiyama, and K. Kataoka Current state, achievements, and future prospects of polymeric micelles as nanocarriers for drug and gene delivery Pharmacol. Ther. 112 3 2006 630 648
14. K. Avgoustakis, A. Beletsi, Z. Panagi, P. Klepetsanis, A.G. Karydas, and D.S. Ithakissios PLGA-mPEG nanoparticles of cisplatin: in vitro nanoparticle degradation, in vitro drug release and in vivo drug residence in blood properties J. Control. Release 79 1-3 2002 123 135
15. R. Manchanda, A. Fernandez-Fernandez, A. Nagesetti, and A.J. McGoron Preparation and characterization of a polymeric (PLGA) nanoparticulate drug delivery system with simultaneous incorporation of chemotherapeutic and thermo-optical agents Colloids Surf. B: Biointerf. 75 1 2010 260 267
16. Z. Zhang, and S.-S. Feng Nanoparticles of poly(lactide)/vitamin E TPGS copolymer for cancer chemotherapy: synthesis, formulation, characterization and in vitro drug release Biomaterials 27 2 2006 262 270
17. A. Musyanovych, J. Dausend, M. Dass, P. Walther, V. Mailander, and K. Landfester Criteria impacting the cellular uptake of nanoparticles: a study emphasizing polymer type and surfactant effects Acta Biomater. 7 12 2011 4160 4168
18. M. Li, Z. Panagi, K. Avgoustakis, and J. Reineke Physiologically based pharmacokinetic modeling of PLGA nanoparticles with varied mPEG content Int. J. Nanomed. 7 2012 1345 1356
19. J. Park, P.M. Fong, J. Lu, K.S. Russell, C.J. Booth, W.M. Saltzman, and T.M. Fahmy PEGylated PLGA nanoparticles for the improved delivery of doxorubicin Nanomed. Nanotechnol. Biol. Med. 5 4 2009 410 418
20. P. Liu, L. Qin, Q. Wang, Y. Sun, M. Zhu, M. Shen, and Y. Duan CRGD-functionalized mPEG-PLGA-PLL nanoparticles for imaging and therapy of breast cancer Biomaterials 33 28 2012 6739 6747
21. A.E. Mercado, X. Yang, X. He, E. Jabbari, Effect of grafting BMP2-derived peptide to nanoparticles on osteogenic and vasculogenic expression of stromal cells, J. Tissue Eng. Regen. Med. (2012), http://dx.doi.org/10.1002/term.1487, PMID: 22764116.
22. J. Ge, E. Neofytou, J. Lei, R.E. Beygui, and R.N. Zare Protein-polymer hybrid nanoparticles for drug delivery Small 8 23 2012 3573 3578
23. M.J. Clift, B. Rothen-Rutishauser, D.M. Brown, R. Duffin, K. Donaldson, L. Proudfoot, K. Guy, and V. Stone The impact of different nanoparticle surface chemistry and size on uptake and toxicity in a murine macrophage cell line Toxicol. Appl. Pharmacol. 232 3 2008 418 427
24. Y. Niu, G. Bai, H. Wu, R.E. Wang, Q. Qiao, S. Padhee, R. Buzzeo, C. Cao, and J. Cai Cellular translocation of a gamma-AApeptide mimetic of Tat peptide Mol. Pharm. 9 5 2012 1529 1534
25. S. Santoso, W. Hwang, H. Hartman, and S. Zhang Self-assembly of surfactant-like peptides with variable glycine tails to form nanotubes and nanovesicles Nano Lett. 2 7 2002 687 691
26. G. von Maltzahn, S. Vauthey, S. Santoso, and S.U. Zhang Positively charged surfactant-like peptides self-assemble into nanostructures Langmuir 19 10 2003 4332 4337
27. H. Hillaireau, and P. Couvreur Nanocarriers' entry into the cell: relevance to drug delivery Cell. Mol. Life Sci. 66 17 2009 2873 2896
28. S. Moeinzadeh, and E. Jabbari Mesoscale simulation of the effect of a lactide segment on the nanostructure of star poly(ethylene glycol-co-lactide)- acrylate macromonomers in aqueous solution J. Phys. Chem. B 116 5 2012 1536 1543
29. R.D. Groot, and P.B. Warren Dissipative particle dynamics: bridging the gap between atomistic and mesoscopic simulation J. Chem. Phys. 107 11 1997 4423 4435
30. E. Jabbari, and X. He Synthesis and characterization of bioresorbable in situ crosslinkable ultra low molecular weight poly(lactide) macromer J. Mater. Sci. Mater. Med. 19 1 2008 311 318
31. E. Jabbari, X. He, M.T. Valarmathi, A.S. Sarvestani, and W. Xu Material properties and bone marrow stromal cells response to in situ crosslinkable RGD-functionlized lactide-co-glycolide scaffolds J. Biomed. Mater. Res. A 89 1 2009 124 137
32. X. He, and E. Jabbari Material properties and cytocompatibility of injectable MMP degradable poly(lactide ethylene oxide fumarate) hydrogel as a carrier for marrow stromal cells Biomacromolecules 8 3 2007 780 792
33. X. He, J. Ma, and E. Jabbari Effect of grafting RGD and BMP-2 protein-derived peptides to a hydrogel substrate on osteogenic differentiation of marrow stromal cells Langmuir 24 21 2008 12508 12516
34. X. He, and E. Jabbari Solid-phase synthesis of reactive peptide crosslinker by selective deprotection Prot. Pept. Lett. 13 2006 515 518
35. E. Kaiser, C.D. Bossinger, R.L. Colescott, and D.B. Olsen Color test for terminal prolyl residues in the solid-phase synthesis of peptides Anal. Chim. Acta 118 1 1980 149 151
36. A.E. Mercado, X. He, W. Xu, and E. Jabbari The release characteristics of a model protein from self-assembled succinimide-terminated poly(lactide-co- glycolide ethylene oxide fumarate) nanoparticles Nanotechnology 19 2008 12 pp
37. X. He, J. Ma, A.E. Mercado, W.J. Xu, and E. Jabbari Cytotoxicity of paclitaxel in biodegradable self-assembled core-shell poly(lactide-co-glycolide ethylene oxide fumarate) nanoparticles Pharm. Res. 25 7 2008 1552 1562
38. N. Faisant, J. Akiki, F. Siepmann, J.P. Benoit, and J. Siepmann Effects of the type of release medium on drug release from PLIGA-based microparticles: experiment and theory Int. J. Pharm. 314 2 2006 189 197
39. M. Huang, Z. Ma, E. Khor, and L.-Y. Lim Uptake of FITC-chitosan nanoparticles by a549 cells Pharm. Res. 19 10 2002 1488 1494
40. X. Yang, P.A. Wood, E.Y. Oh, J. Du-Quiton, C.M. Ansell, and W.J.M. Hrushesky Down regulation of circadian clock gene Period 2 accelerates breast cancer growth by altering its daily growth rhythm Breast Cancer Res. Treat. 117 2 2009 423 431
41. X. He, J. Ma, and E. Jabbari Migration of marrow stromal cells in response to sustained release of stromal-derived factor-1[alpha] from poly(lactide ethylene oxide fumarate) hydrogels Int. J. Pharm. 390 2 2010 107 116
42. A. Elstner, N. Holtkamp, and A.v. Deimling Involvement of Hif-1 in desferrioxamine-induced invasion of glioblastoma cells Clin. Exp. Metast. 24 2007 57 66
43. L. Shorts-Cary, M. Xu, J. Ertel, B.K. Kleinschmidt-Demasters, K. Lillehei, I. Matsuoka, S. Nielsen-Preiss, and M.E. Wierman Bone morphogenetic protein and retinoic acid-inducible neural specific protein-3 is expressed in gonadotrope cell pituitary adenomas and induces proliferation, migration, and invasion Endocrinology 148 3 2007 967 975
44. X.D. Guo, L.J. Zhang, Z.M. Wu, and Y. Qian Dissipative particle dynamics studies on microstructure of ph-sensitive micelles for sustained drug delivery Macromolecules 43 18 2010 7839 7844
45. X.D. Guo, J.P.K. Tan, S.H. Kim, L.J. Zhang, Y. Zhang, J.L. Hedrick, Y.Y. Yang, and Y. Qian Computational studies on self-assembled paclitaxel structures: templates for hierarchical block copolymer assemblies and sustained drug release Biomaterials 30 33 2009 6556 6563
46. P. Espanol, and P. Warren Statistical-mechanics of dissipative particle dynamics Europhys. Lett. 30 4 1995 191 196
47. P.J. Hoogerbrugge, and J.M.V.A. Koelman Simulating microscopic hydrodynamic phenomena with dissipative particle dynamics Europhys. Lett. 19 3 1992 155 160
48. R.D. Groot, and K.L. Rabone Mesoscopic simulation of cell membrane damage, morphology change and rupture by nonionic surfactants Biophys. J. 81 2 2001 725 736
49. Materials Studio, V 5.5. Accelrys, San Diego, 2011.
50. H. Sun COMPASS: an ab initio force-field optimized for condensed-phase applications-overview with details on alkane and benzene compounds J. Phys. Chem. B 102 38 1998 7338 7364
51. T.P. Russell The characterization of polymer interfaces Ann. Rev. Mater. Sci. 21 1991 249 268
52. S.K. Hobbs, W.L. Monsky, F. Yuan, W.G. Roberts, L. Griffith, V.P. Torchilin, and R.K. Jain Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment Proc. Natl. Acad. Sci. USA 95 1998 4607 4612
53. S. Unezaki, K. Maruyama, J. Hosoda, I. Nagae, Y. Koyanagi, M. Nakata, O. Ishida, M. Iwatsuru, and S. Tsuchiya Direct measurement of the extravasation of polyethyleneglycol-coated liposomes into solid tumor tissue by in vivo fluorescence microscopy Int. J. Pharm. 144 1996 11 17
54. F. Ahmed, R.I. Pakunlu, A. Brannan, F. Bates, T. Minko, and D.E. Discher Biodegradable polymersomes loaded with both paclitaxel and doxorubicin permeate and shrink tumors, inducing apoptosis in proportion to accumulated drug J. Control. Release 116 2006 150 158
55. R. Lin, L.S. Ng, and C.-H. Wang In vitro study of anticancer drug doxorubicin in PLGA-based microparticles Biomaterials 26 2005 4476 4485
56. X. Xu, X. Chen, Z. Wang, and X. Jing Ultrafine PEG-PLA fibers loaded with both paclitaxel and doxorubicin hydrochloride and their in vitro cytotoxicity Eur. J. Pharm. Biopharm. 72 2009 18 25
57. T. Yang, F.D. Cui, M.K. Choi, J.W. Cho, S.J. Chung, C.K. Shim, and D.D. Kim Enhanced solubility and stability of PEGylated liposomal paclitaxel: in vitro and in vivo evaluation Int. J. Pharm. 338 1-2 2007 317 326
58. S.C. Lee, K.M. Huh, J. Lee, Y.W. Cho, R.E. Galinsky, and K. Park Hydrotropic polymeric micelles for enhanced paclitaxel solubility: in vitro and in vivo characterization Biomacromolecules 8 1 2007 202 208
59. X.G. Li, D.J. Hirsh, D. Cabral-Lilly, A. Zirkel, S.M. Gruner, A.S. Janoff, and W.R. Perkins Doxorubicin physical state in solution and inside liposomes loaded via a pH gradient Biochim. Biophys. Acta-Biomembr. 1415 1 1998 23 40
60. B.B. Crow, A.F. Borneman, D.L. Hawkins, G.M. Smith, and K.D. Nelson Evaluation of in vitro drug release, pH change, and molecular weight degradation of poly(L-lactic acid) and poly(D, L-lactide-co-glycolide) fibers Tissue Eng. 11 7-8 2005 1077 1084
61. A. Messaritaki, S.J. Black, C.F. van der Walle, and S.P. Rigby NMR and confocal microscopy studies of the mechanisms of burst drug release from PLGA microspheres J. Control. Release 108 2-3 2005 271 281
62. Y. Hu, L. Zhang, Y. Cao, H. Ge, X. Jiang, and C. Yang Degradation behavior of poly(e-caprolactone)-b-poly(ethylene glycol)-b-poly(e-caprolactone) micelles in aqueous solution Biomacromolecules 5 2004 1756 1762
63. G. Bulaj Formation of disulfide bonds in proteins and peptides Biotechnol. Adv. 23 1 2005 87 92
64. M.O. Oyewumi, and R.J. Mumper Influence of formulation parameters on gadolinium entrapment and tumor cell uptake using folate-coated nanoparticles Int. J. Pharm. 251 2003 85 97
65. M.O. Oyewumi, R.A. Yokel, M. Jay, T. Coakley, and R.J. Mumper Comparison of cell uptake, biodistribution and tumor retention of folate-coated and PEG-coated gadolinium nanoparticles in tumorbearing mice J. Control. Release 95 2004 613 626
66. B.D. Chithrani, A.A. Ghazani, and W.C. Chan Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells Nano Lett. 6 2006 662 668
67. M.E. O'Brien, N. Wigler, and M. Inbar Reduced cardiotoxicity and comparable efficacy in a Phase III trial of pegylated liposomal doxorubicinHCl (CAELYX/Doxil) versus conventional doxorubicin for first-line treatment of metastatic breast cancer Ann. Oncol. 15 2004 440 449
68. I. Nakase, A. Tadokoro, N. Kawabata, T. Takeuchi, H. Katoh, K. Hiramoto, M. Negishi, M. Nomizu, Y. Sugiura, and S. Futaki Interaction of arginine-rich peptides with membrane-associated proteoglycans is crucial for induction of actin organization and macropinocytosis Biochemistry 46 2007 492 501
69. H. Brooks, B. Lebleu, and E. Vives Tat peptide-mediated cellular delivery: back to basics Adv. Drug Deliv. Rev. 57 2005 559 577
70. M. Hansen, K. Kilk, and U. Langel Predicting cell-penetrating peptides Adv. Drug Deliv. Rev. 60 4-5 2008 572 579
71. J.B. Rothbard, T.C. Jessop, R.S. Lewis, B.A. Murray, and P.A. Wender Role of membrane potential and hydrogen bonding in the mechanism of translocation of guanidinium-rich peptides into cells J. Am. Chem. Soc. 126 2004 9506 9507
72. C.M. Goodman, C.D. McCusker, T. Yilmaz, and V.M. Rotello Toxicity of gold nanoparticles functionalized with cationic and anionic side chains Bioconjugate Chem. 15 4 2004 897 900
73. M.G. Bexiga, J.A. Varela, F.J. Wang, F. Fenaroli, A. Salvati, I. Lynch, J.C. Simpson, and K.A. Dawson Cationic nanoparticles induce caspase 3-, 7- and 9-mediated cytotoxicity in a human astrocytoma cell line Nanotoxicology 5 4 2011 557 567
74. A. Chompoosor, K. Saha, P.S. Ghosh, D.J. Macarthy, O.R. Miranda, Z.J. Zhu, K.F. Arcaro, and V.M. Rotello The role of surface functionality on acute cytotoxicity, ROS generation and DNA damage by cationic gold nanoparticles Small 6 20 2010 2246 2249
75. A. Basarkar, D. Devineni, R. Palaniappan, and J. Singh Preparation, characterization, cytotoxicity and transfection efficiency of poly(DL-lactide-co-glycolide) and poly(DL-lactic acid) cationic nanoparticles for controlled delivery of plasmid DNA Int. J. Pharm. 343 1-2 2007 247 254
76. J. Zhao, M.L. Gou, M. Dai, X.Y. Li, M. Cao, M.J. Huang, Y.J. Wen, B. Kan, Z.Y. Qian, and Y.Q. Wei Preparation, characterization, and in vitro cytotoxicity study of cationic PCL-Pluronic-PCL (PCFC) nanoparticles for gene delivery J. Biomed. Mater. Res. A 90A 2 2009 506 513
77. Y. Tomita, A. Rikimaru-Kaneko, K. Hashiguchi, and S. Shirotake Effect of anionic and cationic n-butylcyanoacrylate nanoparticles on NO and cytokine production in Raw cells Immunopharmacol. Immunotoxicol. 33 4 2011 730 737
78. M. Merhi, C.Y. Dombu, A. Brient, J. Chang, A. Platel, F. Le Curieux, D. Marzin, F. Nesslany, and D. Betbeder Study of serum interaction with a cationic nanoparticle: implications for in vitro endocytosis, cytotoxicity and genotoxicity Int. J. Pharm. 423 1 2012 37 44
79. H.Y. Zhang, T. Xia, H. Meng, M. Xue, S. George, Z.X. Ji, X. Wang, R. Liu, M.Y. Wang, B. France, R. Rallo, R. Damoiseaux, Y. Cohen, K.A. Bradley, J.I. Zink, and A.E. Nel Differential expression of syndecan-1 mediates cationic nanoparticle toxicity in undifferentiated versus differentiated normal human bronchial epithelial cells ACS Nano 5 4 2011 2756 2769
80. W. Lu, Y.Z. Tan, K.L. Hu, and X.G. Jiang Cationic albumin conjugated pegylated nanoparticle with its transcytosis ability and little toxicity against blood-brain barrier Int. J. Pharm. 295 1-2 2005 247 260
81. G.Q. Niu, C.H. Castro, N. Nguyen, S.M. Sullivan, and J.A. Hughes In vitro cytotoxic activity of cationic paclitaxel nanoparticles on MDR-3T3 cells J. Drug Target. 18 6 2010 468 476
82. E.R. Foster, and J.A. Downs Histone H2A phosphorylation in DNA double-strand break repair FEBS J. 272 13 2005 3231 3240
83. E. Perdiguero, and A.R. Nebreda Regulation of Cdc25C activity during the meiotic G(2)/M transition Cell Cycle 3 6 2004 733 737
84. S.J. Riedl, and G.S. Salvesen The apoptosome: signalling platform of cell death Nat. Rev. Mol. Cell Biol. 8 5 2007 405 413
85. C.J. Twelves, N.A. Dobbs, M. Aldhous, P.G. Harper, R.D. Rubens, and M.A. Richards Comparative pharmacokinetics of doxorubicin given by 3 different schedules with equal dose intensity in patients with breast-cancer Cancer Chemother. Pharmacol. 28 4 1991 302 307
86. D.R. Green, and J.C. Reed Mitochondria and apoptosis Science 281 1998 1309 1312
87. F. Guano, P. Pourquier, S. Tinelli, M. Binaschi, M. Bigioni, F. Animati, S. Manzini, F. Zunino, G. Kohlhagen, Y. Pommier, and G. Capranico Topoisomerase poisoning activity of novel disaccharide anthracyclines Mol. Pharmacol. 56 1999 77 84
88. W.Y. Ayen, and N. Kumar In vivo evaluation of doxorubicin-loaded (peg)(3)-pla nanopolymersomes (polydoxsome) using dmba-induced mammary carcinoma rat model and comparison with marketed LipoDox Pharm. Res. 29 9 2012 2522 2533
89. Z. Amoozgar, and Y. Yeo Recent advances in stealth coating of nanoparticle drug delivery systems Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 4 2 2012 219 233
90. C. Zhan, B. Gu, C. Xie, J. Li, Y. Liu, and W. Lu Cyclic RGD conjugated poly(ethylene glycol)-co-poly(lactic acid) micelle enhances paclitaxel anti-glioblastoma effect J. Control. Release. 143 1 2010 136 142
91. H. Xia, X. Gao, G. Gu, Z. Liu, Q. Hu, Y. Tu, Q. Song, L. Yao, Z. Pang, X. Jiang, J. Chen, and H. Chen Penetratin-functionalized PEG-PLA nanoparticles for brain drug delivery Int. J. Pharm. 436 1-2 2012 840 850