Stealth CD44-targeted hyaluronic acid supramolecular nanoassemblies for doxorubicin delivery: Probing the effect of uncovalent pegylation degree on cellular uptake and blood long circulation

Journal of Controlled Release

Volumn 197, Issue , 2015, Pages 29-40

  Han, Xiaopeng ^a   Li, Zhenbao ^a   Sun, Jin ^a   Luo, Cong ^a   Li, Lin ^a   Liu, Yuhai ^a   Du, Yuqian ^a   Qiu, Shuhong ^a   Ai, Xiaoyu ^a   Wu, Chunnuan ^a   Lian, He ^a   He, Zhonggui ^a  

^a SHENYANG PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Cellular uptake; Host guest interaction; Hyaluronic acid; Long circulation times; Pegylation

Indexed keywords

BLOOD; CARDIOVASCULAR SYSTEM; COATINGS; LIGANDS; ORGANIC ACIDS; PHYSIOLOGY; POLYETHYLENE GLYCOLS; POLYETHYLENE OXIDES; SUPRAMOLECULAR CHEMISTRY;

ANTI-TUMOR EFFICACY; ANTICANCER ACTIVITIES; CELLULAR UPTAKE; DOUBLE-HYDROPHILIC COPOLYMER; HOST GUEST INTERACTIONS; LONG CIRCULATIONS; PEGYLATION; POLAR INTERACTIONS;

HYALURONIC ACID;

2 HYDROXYPROPYL BETA CYCLODEXTRIN; ADAMANTANE DERIVATIVE; ALPHA TOCOPHEROL SUCCINATE; CD44V ANTIGEN; COPOLYMER; DOXORUBICIN; HYALURONIC ACID; MACROGOL; NANOCARRIER; 2-HYDROXYPROPYL-BETA-CYCLODEXTRIN; ANTINEOPLASTIC ANTIBIOTIC; BETA CYCLODEXTRIN DERIVATIVE; DRUG CARRIER; GYRASE INHIBITOR; HERMES ANTIGEN; MACROGOL DERIVATIVE; NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL VIABILITY; CHEMICAL MODIFICATION; CIRCULATION TIME; CONTROLLED DRUG RELEASE; CONTROLLED STUDY; CYTOTOXICITY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG TARGETING; DRUG UPTAKE; IN VITRO STUDY; IN VIVO STUDY; MALE; MICELLE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PARTICLE SIZE; PEGYLATION; RAT; SUPRAMOLECULAR CHEMISTRY; ZETA POTENTIAL; ANIMAL; BAGG ALBINO MOUSE; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM; NEOPLASMS; PATHOLOGY; SPRAGUE DAWLEY RAT; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; ANTIGENS, CD44; BETA-CYCLODEXTRINS; CELL LINE, TUMOR; CELL SURVIVAL; DOXORUBICIN; DRUG CARRIERS; HUMANS; HYALURONIC ACID; MALE; MICE; MICE, INBRED BALB C; NANOPARTICLES; NEOPLASMS; POLYETHYLENE GLYCOLS; RATS, SPRAGUE-DAWLEY; TOPOISOMERASE II INHIBITORS; TUMOR BURDEN;

EID: 84910606013     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.10.024     Document Type: Article

References (62)

1. 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
2. Y. Lu, and P.S. Low Folate-mediated delivery of macromolecular anticancer therapeutic agents Adv. Drug Deliv. Rev. 64 2012 342 352
3. W. Scarano, H.T. Duong, H. Lu, P.L. De Souza, and M.H. Stenzel Folate conjugation to polymeric micelles via boronic acid ester to deliver platinum drugs to ovarian cancer cell lines Biomacromolecules 14 2013 962 975
4. H. Yuan, K. Luo, Y. Lai, Y. Pu, B. He, G. Wang, Y. Wu, and Z. Gu A novel poly (l-glutamic acid) dendrimer based drug delivery system with both pH-sensitive and targeting functions Mol. Pharm. 7 2010 953 962
5. T.L. Kaneshiro, and Z.-R. Lu Targeted intracellular codelivery of chemotherapeutics and nucleic acid with a well-defined dendrimer-based nanoglobular carrier Biomaterials 30 2009 5660 5666
6. Y. Gao, Z. Wang, J. Zhang, Y. Zhang, H. Huo, T. Wang, T. Jiang, and S. Wang RVG peptide-linked trimethylated chitosan for delivery of siRNA to the brain Biomacromolecules 15 2014 1010 1018
7. C. Surace, S. Arpicco, A.l. Dufaÿ-Wojcicki, V.r. Marsaud, C.l. Bouclier, D. Clay, L. Cattel, J.-M. Renoir, and E. Fattal Lipoplexes targeting the CD44 hyaluronic acid receptor for efficient transfection of breast cancer cells Mol. Pharm. 6 2009 1062 1073
8. J.-H. Park, H.-J. Cho, H.Y. Yoon, I.-S. Yoon, S.-H. Ko, J.-S. Shim, J.-H. Cho, J.H. Park, K. Kim, and I.C. Kwon Hyaluronic acid derivative-coated nanohybrid liposomes for cancer imaging and drug delivery J. Control. Release 174 2014 98 108
9. X. Wang, H. Sun, F. Meng, R. Cheng, C. Deng, and Z. Zhong Galactose-decorated reduction-sensitive degradable chimaeric polymersomes as a multifunctional nanocarrier to efficiently chaperone apoptotic proteins into hepatoma cells Biomacromolecules 14 2013 2873 2882
10. D.A. Ossipov Nanostructured hyaluronic acid-based materials for active delivery to cancer Expert. Opin. Drug. Deliv. 7 2010 681 703
11. K.Y. Choi, K.H. Min, J.H. Na, K. Choi, K. Kim, J.H. Park, I.C. Kwon, and S.Y. Jeong Self-assembled hyaluronic acid nanoparticles as a potential drug carrier for cancer therapy: synthesis, characterization, and in vivo biodistribution J. Mater. Chem. 19 2009 4102 4107
12. V.J. Wielenga, K.-H. Heider, G. Johan, A. Offerhaus, G.R. Adolf, F.M. van den Berg, H. Ponta, P. Herrlich, and S.T. Pals Expression of CD44 variant proteins in human colorectal cancer is related to tumor progression Cancer Res. 53 1993 4754 4756
13. R.E. Eliaz, and F.C. Szoka Liposome-encapsulated doxorubicin targeted to CD44 a strategy to kill CD44-overexpressing tumor cells Cancer Res. 61 2001 2592 2601
14. K.N. Sugahara, T. Murai, H. Nishinakamura, H. Kawashima, H. Saya, and M. Miyasaka Hyaluronan oligosaccharides induce CD44 cleavage and promote cell migration in CD44-expressing tumor cells J. Biol. Chem. 278 2003 32259 32265
15. H. Lee, K. Lee, and T.G. Park Hyaluronic acid - paclitaxel conjugate micelles: synthesis, characterization, and antitumor activity Bioconjug. Chem. 19 2008 1319 1325
16. S. Taetz, A. Bochot, C. Surace, S. Arpicco, J.-M. Renoir, U.F. Schaefer, V. Marsaud, S. Kerdine-Roemer, C.-M. Lehr, and E. Fattal Hyaluronic acid-modified DOTAP/DOPE liposomes for the targeted delivery of anti-telomerase siRNA to CD44-expressing lung cancer cells Oligonucleotides 19 2009 103 116
17. Y. He, G. Cheng, L. Xie, Y. Nie, B. He, and Z. Gu Polyethyleneimine/DNA polyplexes with reduction-sensitive hyaluronic acid derivatives shielding for targeted gene delivery Biomaterials 34 2013 1235 1245
18. E.N. Harris, J.A. Weigel, and P.H. Weigel Endocytic function, glycosaminoglycan specificity, and antibody sensitivity of the recombinant human 190-kDa hyaluronan receptor for endocytosis (HARE) J. Biol. Chem. 279 2004 36201 36209
19. Z. Amoozgar, J. Park, Q. Lin, and Y. Yeo Low molecular-weight chitosan as a pH-sensitive stealth coating for tumor-specific drug delivery Mol. Pharm. 9 2012 1262 1270
20. C.-M.J. Hu, L. Zhang, S. Aryal, C. Cheung, R.H. Fang, and L. Zhang Erythrocyte membrane-camouflaged polymeric nanoparticles as a biomimetic delivery platform Proc. Natl. Acad. Sci. U. S. A. 108 2011 10980 10985
21. A.K. Nowinski, A.D. White, A.J. Keefe, and S. Jiang Biologically inspired stealth peptide-capped gold nanoparticles Langmuir 30 2014 1864 1870
22. D. Jain, R. Athawale, A. Bajaj, S. Shrikhande, P.N. Goel, and R.P. Gude Studies on stabilization mechanism and stealth effect of Poloxamer 188 onto PLGA nanoparticles Colloids Surf. B: Biointerfaces 109 2013 59 67
23. L.J. Cruz, P.J. Tacken, R. Fokkink, and C.G. Figdor The influence of PEG chain length and targeting moiety on antibody-mediated delivery of nanoparticle vaccines to human dendritic cells Biomaterials 32 2011 6791 6803
24. S.-D. Li, and L. Huang Stealth nanoparticles: high density but sheddable PEG is a key for tumor targeting J. Control. Release 145 2010 178 181
25. S. Hak, E. Helgesen, H.H. Hektoen, E.M. Huuse, P.A. Jarzyna, W.J. Mulder, O. Haraldseth, and C.d.L. Davies The effect of nanoparticle polyethylene glycol surface density on ligand-directed tumor targeting studied in vivo by dual modality imaging ACS Nano 6 2012 5648 5658
26. S. Svenson, M. Wolfgang, J. Hwang, J. Ryan, and S. Eliasof Preclinical to clinical development of the novel camptothecin nanopharmaceutical CRLX101 J. Control. Release 153 2011 49 55
27. H. He, S. Chen, J. Zhou, Y. Dou, L. Song, L. Che, X. Zhou, X. Chen, Y. Jia, and J. Zhang Cyclodextrin-derived pH-responsive nanoparticles for delivery of paclitaxel Biomaterials 34 2013 5344 5358
28. Y. Zhu, L. Che, H. He, Y. Jia, J. Zhang, and X. Li Highly efficient nanomedicines assembled via polymer-drug multiple interactions: tissue-selective delivery carriers J. Control. Release 152 2011 317 324
29. W.-F. Lai Cyclodextrins in non-viral gene delivery Biomaterials 35 2014 401 411
30. B.V. Schmidt, M. Hetzer, H. Ritter, and C. Barner-Kowollik Complex macromolecular architecture design via cyclodextrin host/guest complexes Prog. Polym. Sci. 39 2014 235 249
31. K.Y. Choi, H. Chung, K.H. Min, H.Y. Yoon, K. Kim, J.H. Park, I.C. Kwon, and S.Y. Jeong Self-assembled hyaluronic acid nanoparticles for active tumor targeting Biomaterials 31 2010 106 114
32. B. Yang, J. Lin, Y. Chen, and Y. Liu Artemether/hydroxypropyl-β-cyclodextrin host-guest system: characterization, phase-solubility and inclusion mode Bioorg. Med. Chem. 17 2009 6311 6317
33. C.-S. Wu, and H.-T. Liao A new biodegradable blends prepared from polylactide and hyaluronic acid Polymer 46 2005 10017 10026
34. S.S. Banerjee, and D.-H. Chen Cyclodextrin-conjugated nanocarrier for magnetically guided delivery of hydrophobic drugs J. Nanoparticle Res. 11 2009 2071 2078
35. Z. Gao, A.N. Lukyanov, A. Singhal, and V.P. Torchilin Diacyllipid-polymer micelles as nanocarriers for poorly soluble anticancer drugs Nano Lett. 2 2002 979 982
36. G. Fontana, M. Licciardi, S. Mansueto, D. Schillaci, and G. Giammona Amoxicillin-loaded polyethylcyanoacrylate nanoparticles: influence of PEG coating on the particle size, drug release rate and phagocytic uptake Biomaterials 22 2001 2857 2865
37. Z.M. Qian, H. Li, H. Sun, and K. Ho Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway Pharmacol. Rev. 54 2002 561 587
38. Z. Zhang, S. Huey Lee, and S.-S. Feng Folate-decorated poly (lactide-co-glycolide)-vitamin E TPGS nanoparticles for targeted drug delivery Biomaterials 28 2007 1889 1899
39. L. Milane, Z. Duan, and M. Amiji Development of EGFR-targeted polymer blend nanocarriers for combination paclitaxel/lonidamine delivery to treat multi-drug resistance in human breast and ovarian tumor cells Mol. Pharm. 8 2010 185 203
40. Y. Zhang, H. Zhang, X. Wang, J. Wang, X. Zhang, and Q. Zhang The eradication of breast cancer and cancer stem cells using octreotide modified paclitaxel active targeting micelles and salinomycin passive targeting micelles Biomaterials 33 2012 679 691
41. J. Ding, C. Xiao, Y. Li, Y. Cheng, N. Wang, C. He, X. Zhuang, X. Zhu, and X. Chen Efficacious hepatoma-targeted nanomedicine self-assembled from galactopeptide and doxorubicin driven by two-stage physical interactions J. Control. Release 169 2012 193 203
42. Y. Pu, S. Chang, H. Yuan, G. Wang, B. He, and Z. Gu The anti-tumor efficiency of poly (l-glutamic acid) dendrimers with polyhedral oligomeric silsesquioxane cores Biomaterials 14 2013 3658 3666
43. H.S.S. Qhattal, and X. Liu Characterization of CD44-mediated cancer cell uptake and intracellular distribution of hyaluronan-grafted liposomes Mol. Pharm. 8 2011 1233 1246
44. M. Stepniewski, M. Pasenkiewicz-Gierula, T. Róg, R. Danne, A. Orlowski, M. Karttunen, A. Urtti, M. Yliperttula, E. Vuorimaa, and A. Bunker Study of PEGylated lipid layers as a model for PEGylated liposome surfaces: molecular dynamics simulation and Langmuir monolayer studies Langmuir 27 2011 7788 7798
45. R. Gref, M. Lück, P. Quellec, M. Marchand, E. Dellacherie, S. Harnisch, T. Blunk, and R. Müller 'Stealth' corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption Colloids Surf. B: Biointerfaces 18 2000 301 313
46. S.-D. Li, and L. Huang Nanoparticles evading the reticuloendothelial system: role of the supported bilayer Biochim. Biophys. Acta 1788 2009 2259 2266
47. C.-L. Chan, R.N. Majzoub, R.S. Shirazi, K.K. Ewert, Y.-J. Chen, K.S. Liang, and C.R. Safinya Endosomal escape and transfection efficiency of PEGylated cationic liposome-DNA complexes prepared with an acid-labile PEG-lipid Biomaterials 33 2012 4928 4935
48. Y. Sato, H. Hatakeyama, Y. Sakurai, M. Hyodo, H. Akita, and H. Harashima A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo J. Control. Release 163 2012 267 276
49. C.E. Nelson, J.R. Kintzing, A. Hanna, J.M. Shannon, M.K. Gupta, and C.L. Duvall Balancing cationic and hydrophobic content of PEGylated siRNA polyplexes enhances endosome escape, stability, blood circulation time, and bioactivity in vivo ACS Nano 7 2013 8870 8880
50. V. Torchilin Tumor delivery of macromolecular drugs based on the EPR effect Adv. Drug Deliv. Rev. 63 2011 131 135
51. M. Sui, W. Liu, and Y. Shen Nuclear drug delivery for cancer chemotherapy J. Control. Release 155 2011 227 236
52. L. Qiu, Z. Li, M. Qiao, M. Long, M. Wang, X. Zhang, C. Tian, and D. Chen Self-assembled pH-responsive hyaluronic acid-g-poly (l-histidine) copolymer micelles for targeted intracellular delivery of doxorubicin Acta Biomater. 10 2014 2024 2035
53. U.S. Huth, R. Schubert, and R. Peschka-Süss Investigating the uptake and intracellular fate of pH-sensitive liposomes by flow cytometry and spectral bio-imaging J. Control. Release 110 2006 490 504
54. J.A. Swanson, and C. Watts Macropinocytosis Trends Cell Biol. 5 1995 424 428
55. J. Tang, Q. Fu, Y. Wang, K. Racette, D. Wang, and F. Liu Vitamin E reverses multidrug resistance in vitro and in vivo Cancer Lett. 336 2013 149 157
56. F. Fenyvesi, É. Fenyvesi, L. Szente, K. Goda, Z. Bacso, I. Bácskay, J. Váradi, T. Kiss, É. Molnár, and T. Janáky P-glycoprotein inhibition by membrane cholesterol modulation Eur. J. Pharm. Sci. 34 2008 236 242
57. J.-S. Baek, and C.-W. Cho 2-Hydroxypropyl-b-cyclodextrin-modified SLN of paclitaxel for overcoming p-glycoprotein function in multidrug-resistant breast cancer cells J. Pharm. Pharmacol. 65 2013 72 78
58. J. Wang, J. Sun, Q. Chen, Y. Gao, L. Li, H. Li, D. Leng, Y. Wang, Y. Sun, and Y. Jing Star-shape copolymer of lysine-linked di-tocopherol polyethylene glycol 2000 succinate for doxorubicin delivery with reversal of multidrug resistance Biomaterials 33 2012 6877 6888
59. M. Allmeroth, D. Moderegger, D. Gündel, H.-G. Buchholz, N. Mohr, K. Koynov, F. Rösch, O. Thews, and R. Zentel PEGylation of HPMA-based block copolymers enhances tumor accumulation in vivo: A quantitative study using radiolabeling and positron emission tomography J. Control. Release 172 2013 77 85
60. S. Zhang, C. Tang, and C. Yin Effects of poly (ethylene glycol) grafting density on the tumor targeting efficacy of nanoparticles with ligand modification Drug Deliv. 1-9 2013
61. K.Y. Choi, K.H. Min, H.Y. Yoon, K. Kim, J.H. Park, I.C. Kwon, K. Choi, and S.Y. Jeong PEGylation of hyaluronic acid nanoparticles improves tumor targetability in vivo Biomaterials 2 2011 1880 1889
62. H.S.S. Qhattal, T. Hye, A. Alali, and X. Liu Hyaluronan polymer length, grafting density, and surface poly (ethylene glycol) coating influence in vivo circulation and tumor targeting of hyaluronan-grafted liposomes ACS Nano 8 2014 5423 5440