15 years of ATTEMPTS: A macromolecular drug delivery system based on the CPP-mediated intracellular drug delivery and antibody targeting

Journal of Controlled Release

Volumn 205, Issue , 2015, Pages 58-69

  Ye, Junxiao ^a,b   Shin, Meong Cheol ^c   Liang, Qiuling ^b   He, Huining ^b   Yang, Victor C ^c,d  

^a TIANJIN UNIVERSITY   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF MICHIGAN   (United States)

^d Seoul National University   (South Korea)

Author keywords

Antibody targeting; ATTEMPTS; CPP mediated intracellular drug delivery; Prodrug

Indexed keywords

DRUG DELIVERY; DRUG INTERACTIONS; HISTOLOGY; POLYSACCHARIDES; TUMORS;

ATTEMPTS; CELL-PENETRATING PEPTIDE; CHARGE INTERACTIONS; INTRACELLULAR DRUG DELIVERY; MACROMOLECULAR DRUGS; PRODRUGS; SYSTEMIC TOXICITIES; THERAPEUTIC EFFECTS;

ANTIBODIES;

ANTIBODY; ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; CELL PENETRATING PEPTIDE; DRUG CARRIER; GEL PROTEIN, GELONIUM MULTIFLORUM; HEPARIN; PEPTIDE FRAGMENT; PRODRUG; RIBOSOME INACTIVATING PROTEIN 1; TRANSACTIVATOR PROTEIN;

ANIMAL; CHEMISTRY; DRUG DELIVERY SYSTEM; DRUG SCREENING; HISTORY; HUMAN; MEDICINAL CHEMISTRY; METABOLISM; PHARMACEUTICS; PROCEDURES; TRENDS;

ANIMALS; ANTIBODIES; ANTINEOPLASTIC AGENTS; CELL-PENETRATING PEPTIDES; CHEMISTRY, PHARMACEUTICAL; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HEPARIN; HISTORY, 21ST CENTURY; HUMANS; IMMUNOCONJUGATES; PEPTIDE FRAGMENTS; PRODRUGS; RIBOSOME INACTIVATING PROTEINS, TYPE 1; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TECHNOLOGY, PHARMACEUTICAL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84938398102     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.12.002     Document Type: Article

References (102)

1. Y.J. Park, J.F. Liang, H. Song, Y.T. Li, S. Naik, and V.C. Yang ATTEMPTS: a heparin/protamine-based triggered release system for the delivery of enzyme drugs without associated side-effects Adv. Drug Deliv. Rev. 55 2003 251 265
2. Y. Huang, Y.S. Park, J. Wang, C. Moon, Y.M. Kwon, H.S. Chung, Y.J. Park, and V.C. Yang ATTEMPTS system: a macromolecular prodrug strategy for cancer drug delivery Curr. Pharm. Des. 16 2010 2369 2376
3. V. Ling Multidrug resistance: molecular mechanisms and clinical relevance Cancer Chemother. Pharmacol. 40 1997 S3 S8 (Suppl.)
4. R. Perez-Tomas Multidrug resistance: retrospect and prospects in anti-cancer drug treatment Curr. Med. Chem. 13 2006 1859 1876
5. Q. Wu, Z. Yang, Y. Nie, Y. Shi, and D. Fan Multi-drug resistance in cancer chemotherapeutics: mechanisms and lab approaches Cancer Lett. 347 2014 159 166
6. D.A. Kessler, R.H. Austin, and H. Levine Resistance to chemotherapy: patient variability and cellular heterogeneity Cancer Res. 74 2014 4663 4670
7. J.F. Liang, Y.T. Li, H. Song, Y.J. Park, S.S. Naik, and V.C. Yang ATTEMPTS: a heparin/protamine-based delivery system for enzyme drugs J. Control. Release 78 2002 67 79
8. S.S. Naik, J.F. Liang, Y.J. Park, W.K. Lee, and V.C. Yang Application of "ATTEMPTS" for drug delivery J. Control. Release 101 2005 35 45
9. H. He, A. David, B. Chertok, A. Cole, K. Lee, J. Zhang, J. Wang, Y. Huang, and V.C. Yang Magnetic nanoparticles for tumor imaging and therapy: a so-called theranostic system Pharm. Res. 30 2013 2445 2458
10. H. He, J. Ye, J. Sheng, J. Wang, Y. Huang, G. Chen, J. Wang, and V.C. Yang Overcoming oral insulin delivery barriers: application of cell penetrating peptide and silica-based nanoporous composites Front. Chem. Sci. Eng. 7 2013 9 19
11. H. He, Q. Liang, M. Shin, K. Lee, J. Gong, J. Ye, Q. Liu, J. Wang, and V.C. Yang Significance and strategies in developing delivery systems for bio-macromolecular drugs Front. Chem. Sci. Eng. 7 2013 496 507
12. J. Ye, H. He, J. Gong, W. Dong, Y. Huang, J. Wang, G. Chen, and V.C. Yang Ultrasound-mediated targeted microbubbles: a new vehicle for cancer therapy Front. Chem. Sci. Eng. 7 2013 20 28
13. H. He, W. Dong, J. Gong, J. Wang, and V.C. Yang Developing macromolecular therapeutics: the future drug-of-choice Front. Chem. Eng. China 4 2010 10 17
14. X. Ren, H. Chen, V.C. Yang, and D. Sun Iron oxide nanoparticle-based theranostics for cancer imaging and therapy Front. Chem. Sci. Eng. 2014 1 12
15. H. Maeda Macromolecular therapeutics in cancer treatment: the EPR effect and beyond J. Control. Release 164 2012 138 144
16. L. Bildstein, C. Dubernet, and P. Couvreur Prodrug-based intracellular delivery of anticancer agents Adv. Drug Deliv. Rev. 63 2011 3 23
17. C. Du, D. Deng, L. Shan, S. Wan, J. Cao, J. Tian, S. Achilefu, and Y. Gu A pH-sensitive doxorubicin prodrug based on folate-conjugated BSA for tumor-targeted drug delivery Biomaterials 34 2013 3087 3097
18. C.P. Guise, A.M. Mowday, A. Ashoorzadeh, R. Yuan, W.H. Lin, D.H. Wu, J.B. Smaill, A.V. Patterson, and K. Ding Bioreductive prodrugs as cancer therapeutics: targeting tumor hypoxia Chin. J. Cancer 33 2014 80 86
19. Y. Jounaidi, C.S. Chen, G.J. Veal, and D.J. Waxman Enhanced antitumor activity of P450 prodrug-based gene therapy using the low Km cyclophosphamide 4-hydroxylase P450 2B11 Mol. Cancer Ther. 5 2006 541 555
20. H. Wang, H. Song, and V.C. Yang A recombinant prodrug type approach for triggered delivery of streptokinase J. Control. Release 59 1999 119 122
21. L. Yuan, W. Chen, J. Hu, J.Z. Zhang, and D. Yang Mechanistic study of the covalent loading of paclitaxel via disulfide linkers for controlled drug release Langmuir 29 2013 734 743
22. M.C. Shin, J. Zhang, K.A. Min, K. Lee, C. Moon, J.P. Balthasar, and V.C. Yang Combination of antibody targeting and PTD-mediated intracellular toxin delivery for colorectal cancer therapy J. Control. Release 194 2014 197 210
23. E. Kondo, K. Saito, Y. Tashiro, K. Kamide, S. Uno, and T. Furuya Tumour lineage-homing cell-penetrating peptides as anticancer molecular delivery systems Nat. Commun. 3 2012 951
24. T. Teesalu, K.N. Sugahara, and E. Ruoslahti Tumor-penetrating peptides Front. Oncol. 3 2013 216
25. Q. Hu, X. Gao, G. Gu, T. Kang, Y. Tu, and Z. Liu Glioma therapy using tumor homing and penetrating peptide-functionalized PEG-PLA nanoparticles loaded with paclitaxel Biomaterials 34 2013 5640 5650
26. J. Zhang, M.C. Shin, and V.C. Yang Magnetic targeting of novel heparinized iron oxide nanoparticles evaluated in a 9L-glioma mouse model Pharm. Res. 31 2014 579 592
27. B. Chertok, A.E. David, and V.C. Yang Brain tumor targeting of magnetic nanoparticles for potential drug delivery: effect of administration route and magnetic field topography J. Control. Release 155 2011 393 399
28. B. Chertok, A.E. David, and V.C. Yang Magnetically-enabled and MR-monitored selective brain tumor protein delivery in rats via magnetic nanocarriers Biomaterials 32 2011 6245 6253
29. B. Chertok, A.E. David, and V.C. Yang Polyethyleneimine-modified iron oxide nanoparticles for brain tumor drug delivery using magnetic targeting and intra-carotid administration Biomaterials 31 2010 6317 6324
30. J. Zhang, M.C. Shin, A.E. David, J. Zhou, K. Lee, H. He, and V.C. Yang Long-circulating heparin-functionalized magnetic nanoparticles for potential application as a protein drug delivery platform Mol. Pharm. 10 2013 3892 3902
31. Y. Huang, F. Yu, Y.S. Park, J. Wang, M.C. Shin, H.S. Chung, and V.C. Yang Co-administration of protein drugs with gold nanoparticles to enable percutaneous delivery Biomaterials 31 2010 9086 9091
32. H. He, J. Ye, Y. Wang, Q. Liu, H.S. Chung, Y.M. Kwon, M.C. Shin, K. Lee, and V.C. Yang Cell-penetrating peptides meditated encapsulation of protein therapeutics into intact red blood cells and its application J. Control. Release 176 2014 123 132
33. Y.M. Kwon, H.S. Chung, C. Moon, J. Yockman, Y.J. Park, S.D. Gitlin, A.E. David, and V.C. Yang L-Asparaginase encapsulated intact erythrocytes for treatment of acute lymphoblastic leukemia ALL J. Control. Release 139 2009 182 189
34. R. Li, F. Feng, Y. Wang, X. Yang, X. Yang, and V.C. Yang Folic acid-conjugated pH/temperature/redox multi-stimuli responsive polymer microspheres for delivery of anti-cancer drug J. Colloid Interface Sci. 429 2014 34 44
35. J. Zhang, D. Deng, H. Zhu, Y. Byun, V.C. Yang, and Y. Gu Folate-conjugated thermo-responsive micelles for tumor targeting J. Biomed. Mater. Res. A 100 2012 3134 3142
36. M.C. Shin, J. Zhang, K.A. Min, K. Lee, Y. Byun, A.E. David, H. He, and V.C. Yang Cell-penetrating peptides: achievements and challenges in application for cancer treatment J. Biomed. Mater. Res. A 102 2014 575 587
37. Y. Huang, Y. Jiang, H. Wang, J. Wang, M.C. Shin, Y. Byun, H. He, Y. Liang, and V.C. Yang Curb challenges of the "Trojan Horse" approach: smart strategies in achieving effective yet safe cell-penetrating peptide-based drug delivery Adv. Drug Deliv. Rev. 65 2013 1299 1315
38. Y. Park, J. Liang, Z. Yang, and V.C. Yang Controlled release of clot-dissolving tissue-type plasminogen activator from a poly(L-glutamic acid) semi-interpenetrating polymer network hydrogel J. Control. Release 75 2001 37 44
39. J.F. Liang, Y.J. Park, H. Song, Y.T. Li, and V.C. Yang ATTEMPTS: a heparin/protamine-based prodrug approach for delivery of thrombolytic drugs J. Control. Release 72 2001 145 156
40. J.F. Liang, Y.T. Li, and V.C. Yang A novel approach for delivery of enzyme drugs: preliminary demonstration of feasibility and utility in vitro Int. J. Pharm. 202 2000 11 20
41. Y.M. Kwon, Y.T. Li, J.F. Liang, Y.J. Park, L.C. Chang, and V.C. Yang PTD-modified ATTEMPTS system for enhanced asparaginase therapy: a proof-of-concept investigation J. Control. Release 130 2008 252 258
42. Y. Zhang, V.K. Singh, and V.C. Yang Novel approach for optimizing the capacity and efficacy of a protamine filter for clinical extracorporeal heparin removal ASAIO J. 44 1998 M368 M373
43. J.F. Liang, L. Zhen, L.C. Chang, and V.C. Yang A less toxic heparin antagonist-low molecular weight protamine Biochemistry 68 2003 116 120
44. J.S. Kim, A.J. Yang, and V.C. Yang Protamine immobilization and heparin adsorption on the protamine-bound cellulose fiber membrane Biotechnol. Bioeng. 39 1992 450 456
45. Y.S. Choi, J.Y. Lee, J.S. Suh, S.J. Lee, V.C. Yang, C.P. Chung, and Y.J. Park Cell penetrating peptides for tumor targeting Curr. Pharm. Biotechnol. 12 2011 1166 1182
46. H. Song, J.F. Liang, and V.C. Yang A prodrug approach for delivery of t-PA: construction of the cationic t-PA prodrug by a recombinant method and preliminary in vitro evaluation of the construct ASAIO J. 46 2000 663 668
47. Y.M. Kwon, Y. Li, S. Naik, J.F. Liang, Y. Huang, Y.J. Park, and V.C. Yang The ATTEMPTS delivery systems for macromolecular drugs Expert Opin. Drug Deliv. 5 2008 1255 1266
48. H. He, J. Ye, E. Liu, Q. Liang, Q. Liu, and V.C. Yang Low molecular weight protamine (LMWP): a nontoxic protamine substitute and an effective cell-penetrating peptide J. Control. Release 193C 2014 63 73
49. Y. Byun, and V.C. Yang Delivery system for targeted thrombolysis without the risk of hemorrhage ASAIO J. 44 1998 M638 M641
50. J.F. Liang, H. Song, Y.T. Li, and V.C. Yang A novel heparin/protamine-based pro-drug type delivery system for protease drugs J. Pharm. Sci. 89 2000 664 673
51. J.F. Liang, Y.T. Li, M.E. Connell, and V.C. Yang Synthesis and characterization of positively charged tPA as a prodrug using heparin/protamine-based drug delivery system AAPS PharmSci. 2 2000 E7
52. J.F. Liang, Y. Li, and V.C. Yang The potential mechanism for the effect of heparin on tissue plasminogen activator-mediated plasminogen activation Thromb. Res. 97 2000 349 358
53. V.C. Yang, S.S. Naik, H. Song, A.A. Dombkowski, G. Crippen, and J.F. Liang Construction and characterization of a t-PA mutant for use in ATTEMPTS: a drug delivery system for achieving targeted thrombolysis J. Control. Release 110 2005 164 176
54. Y.S. Choi, J.Y. Lee, J.S. Suh, Y.M. Kwon, S.J. Lee, J.K. Chung, D.S. Lee, V.C. Yang, C.P. Chung, and Y.J. Park The systemic delivery of siRNAs by a cell penetrating peptide, low molecular weight protamine Biomaterials 31 2010 1429 1443
55. Y.J. Park, J.F. Liang, K.S. Ko, S.W. Kim, and V.C. Yang Low molecular weight protamine as an efficient and nontoxic gene carrier: in vitro study J. Gene Med. 5 2003 700 711
56. Y. Byun, V.K. Singh, and V.C. Yang Low molecular weight protamine: a potential nontoxic heparin antagonist Thromb. Res. 94 1999 53 61
57. L.C. Chang, H.F. Lee, Z. Yang, and V.C. Yang Low molecular weight protamine (LMWP) as nontoxic heparin/low molecular weight heparin antidote (I): preparation and characterization AAPS PharmSci 3 2001 E17
58. L.C. Chang, J.F. Liang, H.F. Lee, L.M. Lee, and V.C. Yang Low molecular weight protamine (LMWP) as nontoxic heparin/low molecular weight heparin antidote (II): in vitro evaluation of efficacy and toxicity AAPS PharmSci 3 2001 E18
59. H. Wang, Y. Zhao, H. Wang, J. Gong, H. He, M.C. Shin, V.C. Yang, and Y. Huang Low-molecular-weight protamine-modified PLGA nanoparticles for overcoming drug-resistant breast cancer J. Control. Release 192 2014 47 56
60. T.Y. Lee, Y.S. Park, G.A. Garcia, R.K. Sunahara, J.H. Woods, and V.C. Yang Cell permeable cocaine esterases constructed by chemical conjugation and genetic recombination Mol. Pharm. 9 2012 1361 1373
61. H. He, J. Sheng, A.E. David, Y.M. Kwon, J. Zhang, Y. Huang, J. Wang, and V.C. Yang The use of low molecular weight protamine chemical chimera to enhance monomeric insulin intestinal absorption Biomaterials 34 2013 7733 7743
62. A.M. Wu, and P.D. Senter Arming antibodies: prospects and challenges for immunoconjugates Nat. Biotechnol. 23 2005 1137 1146
63. G.P. Adams, and L.M. Weiner Monoclonal antibody therapy of cancer Nat. Biotechnol. 23 2005 1147 1157
64. S.R. Urva, V.C. Yang, and J.P. Balthasar An ELISA for quantification of T84.66, a monoclonal anti-CEA antibody, in mouse plasma J. Immunoassay Immunochem. 31 2010 1 9
65. S.R. Urva, V.C. Yang, and J.P. Balthasar Physiologically based pharmacokinetic model for T84.66: a monoclonal anti-CEA antibody J. Pharm. Sci. 99 2010 1582 1600
66. P. Gold, and S.O. Freedman Specific carcinoembryonic antigens of the human digestive system J. Exp. Med. 122 1965 467 481
67. S. Hammarstrom The carcinoembryonic antigen (CEA) family: structures, suggested functions and expression in normal and malignant tissues Semin. Cancer Biol. 9 1999 67 81
68. T. Meyer, A.M. Gaya, G. Dancey, M.R. Stratford, S. Othman, S.K. Sharma, D. Wellsted, N.J. Taylor, J.J. Stirling, L. Poupard, L.K. Folkes, P.S. Chan, R.B. Pedley, K.A. Chester, K. Owen, J.A. Violet, A. Malaroda, A.J. Green, J. Buscombe, A.R. Padhani, G.J. Rustin, and R.H. Begent A phase I trial of radioimmunotherapy with 131I-A5B7 anti-CEA antibody in combination with combretastatin-A4-phosphate in advanced gastrointestinal carcinomas Clin. Cancer Res. 15 2009 4484 4492
69. S. Shibata, A. Raubitschek, L. Leong, M. Koczywas, L. Williams, J. Zhan, and J.Y. Wong A phase I study of a combination of yttrium-90-labeled anti-carcinoembryonic antigen (CEA) antibody and gemcitabine in patients with CEA-producing advanced malignancies Clin. Cancer Res. 15 2009 2935 2941
70. S.R. Urva, and J.P. Balthasar Target mediated disposition of T84.66, a monoclonal anti-CEA antibody: application in the detection of colorectal cancer xenografts MAbs 2 2010 67 72
71. Y.T. Li, Y.M. Kwon, G.J. Spangrude, J.F. Liang, H.S. Chung, Y.J. Park, and V.C. Yang Preliminary in vivo evaluation of the protein transduction domain-modified ATTEMPTS approach in enhancing asparaginase therapy J. Biomed. Mater. Res. A 91 2009 209 220
72. M.C. Shin, J. Zhao, J. Zhang, Y. Huang, H. He, M. Wang, K.A. Min, and V.C. Yang Recombinant TAT-gelonin fusion toxin: synthesis and characterization of heparin/protamine-regulated cell transduction J. Biomed. Mater. Res. A 103 2015 409 419
73. G.L. Ellman Tissue sulfhydryl groups Arch. Biochem. Biophys. 82 1959 70 77
74. L.B. Jaques, and A. Wollin A modified method for the colorimetric determination of heparin Can. J. Physiol. Pharmacol. 45 1967 787 794
75. A.J. Cole, A.E. David, J. Wang, C.J. Galban, H.L. Hill, and V.C. Yang Polyethylene glycol modified, cross-linked starch-coated iron oxide nanoparticles for enhanced magnetic tumor targeting Biomaterials 32 2011 2183 2193
76. M.C. Shin, J. Zhang, A.E. David, W.E. Trommer, Y.M. Kwon, K.A. Min, J.H. Kim, and V.C. Yang Chemically and biologically synthesized CPP-modified gelonin for enhanced anti-tumor activity J. Control. Release 172 2013 169 178
77. R. Siegel, J. Ma, Z. Zou, and A. Jemal Cancer statistics, 2014 CA Cancer J. Clin. 64 2014 9 29
78. S. Giacchetti, M. Itzhaki, G. Gruia, R. Adam, R. Zidani, F. Kunstlinger, S. Brienza, E. Alafaci, F. Bertheault-Cvitkovic, C. Jasmin, M. Reynes, H. Bismuth, J.L. Misset, and F. Levi Long-term survival of patients with unresectable colorectal cancer liver metastases following infusional chemotherapy with 5-fluorouracil, leucovorin, oxaliplatin and surgery Ann. Oncol. 10 1999 663 669
79. A. Schroeder, D.A. Heller, M.M. Winslow, J.E. Dahlman, G.W. Pratt, R. Langer, T. Jacks, and D.G. Anderson Treating metastatic cancer with nanotechnology Nat. Rev. Cancer 12 2012 39 50
80. F. Stirpe, S. Olsnes, and A. Pihl Gelonin, a new inhibitor of protein synthesis, nontoxic to intact cells. Isolation, characterization, and preparation of cytotoxic complexes with concanavalin A J. Biol. Chem. 255 1980 6947 6953
81. S.F. Atkinson, T. Bettinger, L.W. Seymour, J.P. Behr, and C.M. Ward Conjugation of folate via gelonin carbohydrate residues retains ribosomal-inactivating properties of the toxin and permits targeting to folate receptor positive cells J. Biol. Chem. 276 2001 27930 27935
82. A.F. Andrade, K.S. Borges, and V.S. Silveira Update on the use of L-asparaginase in infants and adolescent patients with acute lymphoblastic leukemia Clin. Med. Insights Oncol. 8 2014 95 100
83. C.H. Fu, and K.M. Sakamoto PEG-asparaginase Expert. Opin. Pharmacother. 8 2007 1977 1984
84. R. Pieters, S.P. Hunger, J. Boos, C. Rizzari, L. Silverman, A. Baruchel, N. Goekbuget, M. Schrappe, and C.H. Pui L-asparaginase treatment in acute lymphoblastic leukemia: a focus on Erwinia asparaginase Cancer 117 2011 238 249
85. W. Salzer, N. Seibel, and M. Smith Erwinia asparaginase in pediatric acute lymphoblastic leukemia Expert. Opin. Biol. Ther. 12 2012 1407 1414
86. M.L. Graham Pegaspargase: a review of clinical studies Adv. Drug Deliv. Rev. 55 2003 1293 1302
87. B. Chertok, A.E. David, B.A. Moffat, and V.C. Yang Substantiating in vivo magnetic brain tumor targeting of cationic iron oxide nanocarriers via adsorptive surface masking Biomaterials 30 2009 6780 6787
88. B. Chertok, B.A. Moffat, A.E. David, F. Yu, C. Bergemann, and B.D. Ross Iron oxide nanoparticles as a drug delivery vehicle for MRI monitored magnetic targeting of brain tumors Biomaterials 29 2008 487 496
89. A.E. David, A.J. Cole, and V.C. Yang Magnetically targeted nanoparticles for brain tumor therapy: what does the future hold? Nanomedicine (Lond.) 6 2011 1133 1135
90. A.J. Cole, V.C. Yang, and A.E. David Cancer theranostics: the rise of targeted magnetic nanoparticles Trends Biotechnol. 29 2011 323 332
91. S. Mura, J. Nicolas, and P. Couvreur Stimuli-responsive nanocarriers for drug delivery Nat. Mater. 12 2013 991 1003
92. S.F. Buchsbaum, G. Nguyen, S. Howorka, and Z.S. Siwy DNA-modified polymer pores allow pH- and voltage-gated control of channel flux J. Am. Chem. Soc. 136 2014 9902 9905
93. J. Akimoto, M. Nakayama, and T. Okano Temperature-responsive polymeric micelles for optimizing drug targeting to solid tumors J. Control. Release 193C 2014 2 8
94. W. Chen, and J. Du Ultrasound and pH dually responsive polymer vesicles for anticancer drug delivery Sci. Rep. 3 2013 2162
95. Y. Li, Y. Qian, T. Liu, G. Zhang, and S. Liu Light-triggered concomitant enhancement of magnetic resonance imaging contrast performance and drug release rate of functionalized amphiphilic diblock copolymer micelles Biomacromolecules 13 2012 3877 3886
96. X. Xu, Y. Li, H. Li, R. Liu, M. Sheng, B. He, and Z. Gu Smart nanovehicles based on pH-triggered disassembly of supramolecular peptide-amphiphiles for efficient intracellular drug delivery Small 10 2014 1133 1140
97. M. Joglekar, and B.G. Trewyn Polymer-based stimuli-responsive nanosystems for biomedical applications Biotechnol. J. 8 2013 931 945
98. T. Garg, S. Singh, and A.K. Goyal Stimuli-sensitive hydrogels: an excellent carrier for drug and cell delivery Crit. Rev. Ther. Drug Carrier Syst. 30 2013 369 409
99. J.R. Lopes, G. Santos, P. Barata, R. Oliveira, and C.M. Lopes Physical and chemical stimuli-responsive drug delivery systems: targeted delivery and main routes of administration Curr. Pharm. Des. 19 2013 7169 7184
100. J. Zhuang, M.R. Gordon, J. Ventura, L. Li, and S. Thayumanavan Multi-stimuli responsive macromolecules and their assemblies Chem. Soc. Rev. 42 2013 7421 7435
101. S. Maya, B. Sarmento, A. Nair, N.S. Rejinold, S.V. Nair, and R. Jayakumar Smart stimuli sensitive nanogels in cancer drug delivery and imaging: a review Curr. Pharm. Des. 19 2013 7203 7218
102. Y. Li, G.H. Gao, and D.S. Lee Stimulus-sensitive polymeric nanoparticles and their applications as drug and gene carriers Adv. Healthc. Mater. 2 2013 388 417