Intelligent design of multifunctional lipid-coated nanoparticle platforms for cancer therapy

Therapeutic Delivery

Volumn 3, Issue 12, 2012, Pages 1429-1445

  Ramishetti, Srinivas ^a   Huang, Leaf ^a  

^a University of North Carolina   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; LIPID CALCIUM PHOSPHATE NANOPARTICLE; LIPID DNA PROTAMINE NANOPARTICLE; LIPID NANOCAPSULE; LIPOSOME; MACROGOL; MAGNETOLIPOSOME; MESOPOROUS SILICA NANOPARTICLE; MICRORNA; NANOCAPSULE; NANOCRYSTAL; NANOPARTICLE; PACLITAXEL; POLYCATION; PROTOCELL; SMALL INTERFERING RNA; STAT5B PROTEIN; SUPERPARAMAGNETIC IRON OXIDE NANOCRYSTAL; UNCLASSIFIED DRUG;

BIOACCUMULATION; BIODISTRIBUTION; BREAST CANCER; CANCER RESEARCH; CANCER THERAPY; CHEMICAL PARAMETERS; CHEMICAL PROCEDURES; CLEARANCE; DRUG DELIVERY SYSTEM; DRUG STABILITY; DRUG TARGETING; ENHANCED PERMEABILITY AND RETENTION EFFECT; HALF LIFE TIME; HUMAN; HYDROPHILICITY; HYDROPHOBICITY; HYPERTHERMIC THERAPY; INTRACELLULAR SIGNALING; LIPID BILAYER; MONONUCLEAR PHAGOCYTE SYSTEM CLEARANCE; NANOENCAPSULATION; NONHUMAN; OPSONIZATION; OVARY CANCER; PARTICLE SIZE; PEGYLATION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; SURFACE CHARGE; SURFACE PROPERTY;

EID: 84870663655     PISSN: 20415990     EISSN: 20416008     Source Type: Journal    
DOI: 10.4155/tde.12.127     Document Type: Review

References (181)

1. Sinha R, Kim GJ, Nie S, Shin DM. Nanotechnology in cancer therapeutics: bioconjugated nanoparticles for drug delivery. Mol. Cancer Ther. 5(8), 1909-1917 (2006).
2. Jabr-Milane LS, Van Vlerken LE, Yadav S, Amiji MM. Multi-functional nanocarriers to overcome tumor drug resistance. Cancer Treat. Rev. 34(7), 592-602 (2008).
3. Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science 331(6024), 1559-1564 (2011).
4. Marshall E. Cancer research and the $90 billion metaphor. Science 331(6024), 1540-1541 (2011).
5. Zhang L, Gu FX, Chan JM, Wang AZ, Langer RS, Farokhzad OC. Nanoparticles in medicine: therapeutic applications and developments. Clin. Pharmacol. Ther. 83(5), 761-769 (2008).
6. Kim BY, Rutka JT, Chan WC. Nanomedicine. N. Engl. J. Med. 363(25), 2434-2443 (2010).
7. Buse J, El-Aneed A. Properties, engineering and applications of lipid-based nanoparticle drug-delivery systems: current research and advances. Nanomedicine (Lond.) 5(8), 1237-1260 (2010).
8. Yu MK, Park J, Jon S. Targeting strategies for multifunctional nanoparticles in cancer imaging and therapy. Theranostics 2(1), 3-44 (2012).
9. Farrell D, Ptak K, Panaro NJ, Grodzinski P. Nanotechnology-based cancer therapeutics - promise and challenge - lessons learned through the NCI alliance for nanotechnology in cancer. Pharm. Res. 28(2), 273-278 (2011).
10. Riehemann K, Schneider SW, Luger TA, Godin B, Ferrari M, Fuchs H. Nanomedicine - challenge and perspectives. Angew. Chem. Int. Ed. Engl. 48(5), 872-897 (2009).
11. Sokolova V, Epple M. Inorganic nanoparticles as carriers of nucleic acids into cells. Angew. Chem. Int. Ed. Engl. 47(8), 1382-1395 (2008).
12. Gratton SE, Ropp PA, Pohlhaus PD et al. The effect of particle design on cellular internalization pathways. Proc. Natl Acad. Sci. USA 105(33), 11613-11618 (2008).
13. Decuzzi P, Pasqualini R, Arap W, Ferrari M. Intravascular delivery of particulate systems: does geometry really matter? Pharm. Res. 26(1), 235-243 (2009).
14. Champion JA, Mitragotri S. Shape induced inhibition of phagocytosis of polymer particles. Pharm. Res. 26(1), 244-249 (2009).
15. Smith BR, Kempen P, Bouley D et al. Shape matters: intravital microscopy reveals surprising geometrical dependence for nanoparticles in tumor models of extravasation. Nano Letts 12(7), 3369-3377 (2012)
16. Davis ME, Chen ZG, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat. Rev. Drug. Discov. 7(9), 771-782 (2008).
17. Alexis F, Pridgen E, Molnar LK, Farokhzad OC. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol. Pharm. 5(4), 505-515 (2008).
18. Longmire M, Choyke PL, Kobayashi H. Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. Nanomedicine (Lond.) 3(5), 703-717 (2008).
19. Klibanov AL, Maruyama K, Torchilin VP, Huang L. Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes. FEBS Lett. 268(1), 235-237 (1990).
20. Barreto JA, O'Malley W, Kubeil M, Graham B, Stephan H, Spiccia L. Nanomaterials: applications in cancer imaging and therapy. Adv. Mater. 23(12), 18-40 (2011).
21. Geng Y, Dalhaimer P, Cai S et al. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nanotechnol. 2(4), 249-255 (2007).
22. Champion JA, Mitragotri S. Role of target geometry in phagocytosis. Proc. Natl Acad. Sci. USA 103(13), 4930-4934 (2006).
23. Decuzzi P, Godin B, Tanaka T et al. Size and shape effects in the biodistribution of intravascularly injected particles. J. Control. Release 141(3), 320-327 (2010).
24. Schipper ML, Iyer G, Koh AL et al. Particle size, surface coating, and PEGylation influence the biodistribution of quantum dots in living mice. Small 5(1), 126-134 (2009).
25. Bartlett DW, Davis ME. Physicochemical and biological characterization of targeted, nucleic acid-containing nanoparticles. Bioconjug. Chem. 18(2), 456-468 (2007).
26. Lee H, Lee K, Park TG. Hyaluronic acid-paclitaxel conjugate micelles: synthesis, characterization, and antitumor activity. Bioconjug. Chem. 19(6), 1319-1325 (2008).
27. Bartneck M, Keul HA, Wambach M et al. Effects of nanoparticle surface-coupled peptides, functional endgroups, and charge on intracellular distribution and functionality of human primary reticuloendothelial cells. Nanomedicine doi: 10.1016/j. nano.2012.02.012 (2012) (Epub ahead of print).
28. Xiao K, Li Y, Luo J et al. The effect of surface charge on in vivo biodistribution of PEG-oligocholic acid based micellar nanoparticles. Biomaterials 32(13), 3435-3446 (2011).
29. Juliano RL, Stamp D. The effect of particle size and charge on the clearance rates of liposomes and liposome encapsulated drugs. Biochem. Biophys. Res. Commun. 63(3), 651-658 (1975).
30. Aggarwal P, Hall JB, Mcleland CB, Dobrovolskaia MA, Mcneil SE. Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv. Drug Deliv. Rev. 61(6), 428-437 (2009).
31. Allen TM, Hansen C. Pharmacokinetics of stealth versus conventional liposomes: effect of dose. Biochim. Biophys. Acta. 1068(2), 133-141 (1991).
32. Malam Y, Loizidou M, Seifalian AM. Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. Trends Pharmacol. Sci. 30(11), 592-599 (2009).
33. Owens DE 3rd, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int. J. Cancer 307(1), 93-102 (2006).
34. Choi HS, Ipe BI, Misra P, Lee JH, Bawendi MG, Frangioni JV. Tissue- and organ-selective biodistribution of NIR fluorescent quantum dots. Nano Letts 9(6), 2354-2359 (2009).
35. Kaminskas LM, Boyd BJ, Karellas P et al. The impact of molecular weight and PEG chain length on the systemic pharmacokinetics of PEGylated poly l-lysine dendrimers. Mol. Pharm. 5(3), 449-463 (2008).
36. Peracchia MT, Fattal E, Desmaele D et al. Stealth PEGylated polycyanoacrylate nanoparticles for intravenous administration and splenic targeting. J. Control. Release 60(1), 121-128 (1999).
37. Zamboni WC. Liposomal, nanoparticle, and conjugated formulations of anticancer agents. Clin. Cancer Res. 11(23), 8230-8234 (2005).
38. Petros RA, Desimone JM. Strategies in the design of nanoparticles for therapeutic applications. Nat. Rev. Drug. Discov. 9(8), 615-627 (2010).
39. Nakamura T, Akita H, Yamada Y, Hatakeyama H, Harashima H. A multifunctional envelope-type nanodevice for use in nanomedicine: concept and applications. Acc. Chem. Res. 45(7), 1113-1121 (2012).
40. Wang T, Upponi JR, Torchilin VP. Design of multifunctional non-viral gene vectors to overcome physiological barriers: dilemmas and strategies. Int. J. Cancer 427(1), 3-20 (2012).
41. Hatakeyama H, Akita H, Kogure K et al. Development of a novel systemic gene delivery system for cancer therapy with a tumor-specific cleavable PEG-lipid. Gene Ther. 14(1), 68-77 (2007).
42. Romberg B, Hennink WE, Storm G. Sheddable coatings for long-circulating nanoparticles. Pharm. Res. 25(1), 55-71 (2008).
43. Ishida T, Maeda R, Ichihara M, Irimura K, Kiwada H. Accelerated clearance of PEGylated liposomes in rats after repeated injections. J. Control. Release 88(1), 35-42 (2003).
44. Ishida T, Kiwada H. Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes. Int. J. Cancer 354(1-2), 56-62 (2008).
45. Ishihara T, Takeda M, Sakamoto H et al. Accelerated blood clearance phenomenon upon repeated injection of PEG-modified PLA-nanoparticles. Pharm. Res. 26(10), 2270-2279 (2009).
46. Xu H, Wang KQ, Deng YH, Chen Da W. Effects of cleavable PEG-cholesterol derivatives on the accelerated blood clearance of PEGylated liposomes. Biomaterials 31(17), 4757-4763 (2010).
47. Takeuchi H, Kojima H, Yamamoto H, Kawashima Y. Evaluation of circulation profiles of liposomes coated with hydrophilic polymers having different molecular weights in rats. J. Control. Release 75(1-2), 83-91 (2001).
48. Torchilin VP, Levchenko TS, Whiteman KR et al. Amphiphilic poly-N-vinylpyrrolidones. synthesis, properties and liposome surface modification. Biomaterials 22(22), 3035-3044 (2001).
49. Whiteman KR, Subr V, Ulbrich K, Torchilin VP. Poly(Hpma)-coated liposomes demonstrate prolonged circulation in mice. J. Liposome Res. 11(2-3), 153-164 (2001).
50. Metselaar JM, Bruin P, De Boer LW et al. A novel family of l-amino acid-based biodegradable polymer-lipid conjugates for the development of long-circulating liposomes with effective drug-targeting capacity. Bioconjug. Chem. 14(6), 1156-1164 (2003).
51. Fang J, Nakamura H, Maeda H. The EPR effect: unique features of tumor blood vessels for drug delivery, factors involved, and limitations and augmentation of the effect. Adv. Drug Deliv. Rev. 63(3), 136-151 (2011).
52. Yuan F, Leunig M, Huang SK, Berk DA, Papahadjopoulos D, Jain RK. Microvascular permeability and interstitial penetration of sterically stabilized (stealth) liposomes in a human tumor xenograft. Cancer Res. 54(13), 3352-3356 (1994).
53. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2(12), 751-760 (2007).
54. Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science 303(5665), 1818-1822 (2004).
55. Hobbs SK, Monsky WL, Yuan F et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl Acad. Sci. USA 95(8), 4607-4612 (1998).
56. Heldin CH, Rubin K, Pietras K, Ostman A. High interstitial fluid pressure - an obstacle in cancer therapy. Nat. Rev. Cancer 4(10), 806-813 (2004).
57. Farokhzad OC, Langer R. Impact of nanotechnology on drug delivery. ACS Nano. 3(1), 16-20 (2009).
58. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat. Rev. Cancer 2(1), 48-58 (2002).
59. Kirpotin DB, Drummond DC, Shao Y et al. Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models. Cancer Res. 66(13), 6732-6740 (2006).
60. Van Rooy I, Mastrobattista E, Storm G, Hennink WE, Schiffelers RM. Comparison of five different targeting ligands to enhance accumulation of liposomes into the brain. J. Control. Release 150(1), 30-36 (2011).
61. Kwon IK, Lee SC, Han B, Park K. Analysis on the current status of targeted drug delivery to tumors. J. Control. Release doi: 10.1016/j. jconrel.2012.07.010 (2012) (Epub ahead of print).
62. Shi J, Xiao Z, Kamaly N, Farokhzad OC. Self-assembled targeted nanoparticles: evolution of technologies and bench to bedside translation. Acc. Chem. Res. 44(10), 1123-1134 (2011).
63. Kirpotin D, Park JW, Hong K et al. Sterically stabilized anti-HER2 immunoliposomes: design and targeting to human breast cancer cells in vitro. Biochemistry 36(1), 66-75 (1997).
64. Bangham AD, Horne RW. Negative staining of phospholipids and their structural modification by surface-active agents as observed in the electron microscope. J. Mol. Biol. 8, 660-668 (1964).
65. Srinivas R, Samanta S, Chaudhuri A. Cationic amphiphiles: promising carriers of genetic materials in gene therapy. Chem. Soc. Rev. 38(12), 3326-3338 (2009).
66. Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 4(2), 145-160 (2005).
67. Puri A, Loomis K, Smith B et al. Lipid-based nanoparticles as pharmaceutical drug carriers: from concepts to clinic. Crit. Rev. Ther. Drug Carrier Syst. 26(6), 523-580 (2009).
68. Ramishetti S, Arup G, Gopikrishna M, Sachin BA, Chaudhuri A. A long-lasting dendritic cell DNA vaccination system using lysinylated amphiphiles with mannose-mimicking head-groups. Biomaterials 33(26) 6220-6229 (2012).
69. Vasievich EA, Ramishetti S, Zhang Y, Huang L. Trp2 peptide vaccine adjuvanted with (R)-DOTAP inhibits tumor growth in an advanced melanoma model. Mol. Pharm. 9(2), 261-268 (2012).
70. Un K, Kawakami S, Suzuki R, Maruyama K, Yamashita F, Hashida M. Development of an ultrasound-responsive and mannose-modified gene carrier for DNA vaccine therapy. Biomaterials 31(30), 7813-7826 (2010).
71. Stover TC, Sharma A, Robertson GP, Kester M. Systemic delivery of liposomal short-chain ceramide limits solid tumor growth in murine models of breast adenocarcinoma. Clin. Cancer Res.11(9), 3465-3474 (2005).
72. Goncalves A, Braud AC, Viret F et al. Phase I study of pegylated liposomal doxorubicin (Caelyx) in combination with carboplatin in patients with advanced solid tumors. Anticancer Res. 23(4), 3543-3548 (2003).
73. Schwonzen M, Kurbacher CM, Mallmann P. Liposomal doxorubicin and weekly paclitaxel in the treatment of metastatic breast cancer. Anticancer Drugs 11(9), 681-685 (2000).
74. Shapiro EM, Skrtic S, Sharer K, Hill JM, Dunbar CE, Koretsky AP. MRI detection of single particles for cellular imaging. Proc. Natl Acad. Sci. USA 101(30), 10901-10906 (2004).
75. Bulte JW, Zhang S, Van Gelderen P et al. Neurotransplantation of magnetically labeled oligodendrocyte progenitors: magnetic resonance tracking of cell migration and myelination. Proc. Natl Acad. Sci. USA 96(26), 15256-15261 (1999).
76. Wilhelm C, Fortin JP, Gazeau F. Tumour cell toxicity of intracellular hyperthermia mediated by magnetic nanoparticles. J. Nanosci. Nanotechnol. 7(8), 2933-2937 (2007).
77. Lin BL, Shen XD, Cui S. Application of nanosized Fe3O4 in anticancer drug carriers with target-orientation and sustained-release properties. Biomed. Mater. 2(2), 132-134 (2007).
78. Sun C, Lee JS, Zhang M. Magnetic nanoparticles in MR imaging and drug delivery. Adv. Drug Deliv. Rev. 60(11), 1252-1265 (2008).
79. Bhattarai SR, Kim SY, Jang KY et al. N-hexanoyl chitosan-stabilized magnetic nanoparticles: enhancement of adenoviral-mediated gene expression both in vitro and in vivo. Nanomedicine 4(2), 146-154 (2008).
80. Plank C, Schillinger U, Scherer F et al. The magnetofection method: using magnetic force to enhance gene delivery. Biol. Chem. 384(5), 737-747 (2003).
81. De Cuyper M, Joniau M. Magnetoliposomes. Formation and structural characterization. Eur. Biophys. J. 15(5), 311-319 (1988).
82. Cesur H, Rubinstein I, Pai A, Onyuksel H. Self-associated indisulam in phospholipid-based nanomicelles: a potential nanomedicine for cancer. Nanomedicine 5(2), 178-183 (2009).
83. Sabate R, Barnadas-Rodriguez R, Callejas- Fernandez J, Hidalgo-Alvarez R, Estelrich J. Preparation and characterization of extruded magnetoliposomes. Int. J. Cancer 347(1-2), 156-162 (2008).
84. Martina MS, Fortin JP, Menager C et al. Generation of superparamagnetic liposomes revealed as highly efficient MRI contrast agents for in vivo imaging. J. Am. Chem. Soc. 127(30), 10676-10685 (2005).
85. Janib SM, Moses AS, Mackay JA. Imaging and drug delivery using theranostic nanoparticles. Adv. Drug Deliv. Rev. 62(11), 1052-1063 (2010).
86. Zhang Y, Kohler N, Zhang M. Surface modification of superparamagnetic magnetite nanoparticles and their intracellular uptake. Biomaterials 23(7), 1553-1561 (2002).
87. Tai LA, Tsai PJ, Wang YC, Wang YJ, Lo LW, Yang CS. Thermosensitive liposomes entrapping iron oxide nanoparticles for controllable drug release. Nanotechnology 20(13), 135101 (2009).
88. Chen Y, Bose A, Bothun GD. Controlled release from bilayer-decorated magnetoliposomes via electromagnetic heating. ACS nano. 4(6), 3215-3221 (2010).
89. Pradhan P, Giri J, Rieken F et al. Targeted temperature sensitive magnetic liposomes for thermo-chemotherapy. J. Control. Release 142(1), 108-121 (2010).
90. Yang X, Grailer JJ, Rowland IJ et al. Multifunctional SPIO/DOX-loaded wormlike polymer vesicles for cancer therapy and MR imaging. Biomaterials 31(34), 9065-9073 (2010).
91. Wang H, Wang S, Liao Z et al. Folate-targeting magnetic core-shell nanocarriers for selective drug release and imaging. Int. J. Cancer 430(1-2), 342-349 (2012).
92. Fattahi H, Laurent S, Liu F, Arsalani N, Vander Elst L, Muller RN. Magnetoliposomes as multimodal contrast agents for molecular imaging and cancer nanotheragnostics. Nanomedicine (Lond.) 6(3), 529-544 (2011).
93. Felgner PL, Tsai YJ, Sukhu L et al. Improved cationic lipid formulations for in vivo gene therapy. Ann. N. Y. Acad. Sci. 772, 126-139 (1995).
94. Gustafsson J, Arvidson G, Karlsson G, Almgren M. Complexes between cationic liposomes and DNA visualized by cryo-TEM. Biochim. Biophys. Acta. 1235(2), 305-312 (1995).
95. Li S, Rizzo MA, Bhattacharya S, Huang L. Characterization of cationic lipid-protamine- DNA (LPD) complexes for intravenous gene delivery. Gene Ther. 5(7), 930-937 (1998).
96. Li S, Huang L. In vivo gene transfer via intravenous administration of cationic lipid-protamine-DNA (LPD) complexes. Gene Ther. 4(9), 891-900 (1997).
97. Li B, Li S, Tan Y et al. Lyophilization of cationic lipid-protamine-DNA (LPD) complexes. J. Pharm. Sci. 89(3), 355-364 (2000).
98. Gao X, Huang L. Potentiation of cationic liposome-mediated gene delivery by polycations. Biochemistry 35(3), 1027-1036 (1996).
99. Li SD, Huang L. Surface-modified LPD nanoparticles for tumor targeting. Ann. N. Y. Acad. Sci. 1082, 1-8 (2006).
100. Li SD, Huang L. Nanoparticles evading the reticuloendothelial system: role of the supported bilayer. Biochim. Biophys. Acta. 1788(10), 2259-2266 (2009).
101. Li SD, Huang L. Stealth nanoparticles: high density but sheddable PEG is a key for tumor targeting. J. Control. Release 145(3), 178-181 (2010).
102. Megalizzi V, Le Mercier M, Decaestecker C. Sigma receptors and their ligands in cancer biology: overview and new perspectives for cancer therapy. Med. Res. Rev. 32(2), 410-427 (2012).
103. Banerjee R, Tyagi P, Li S, Huang L. Anisamide-targeted stealth liposomes: a potent carrier for targeting doxorubicin to human prostate cancer cells. Int. J. Cancer 112(4), 693-700 (2004).
104. John CS, Vilner BJ, Geyer BC, Moody T, Bowen WD. Targeting sigma receptor-binding benzamides as in vivo diagnostic and therapeutic agents for human prostate tumors. Cancer Res. 59(18), 4578-4583 (1999).
105. John CS, Bowen WD, Fisher SJ et al. Synthesis, in vitro pharmacologic characterization, and preclinical evaluation of N-[2-(1́-piperidinyl) ethyl]-3-[125I]iodo-4- methoxybenzamide (P[125I]MBA) for imaging breast cancer. Nucl. Med. Biol. 26(4), 377-382 (1999).
106. Li SD, Chono S, Huang L. Efficient gene silencing in metastatic tumor by siRNA formulated in surface-modified nanoparticles. J. Control. Release 126(1), 77-84 (2008).
107. Li SD, Chen YC, Hackett MJ, Huang L. Tumor-targeted delivery of siRNA by self-assembled nanoparticles. Mol. Ther. 16(1), 163-169 (2008).
108. Chen Y, Bathula SR, Yang Q, Huang L. Targeted nanoparticles deliver siRNA to melanoma. J. Invest. Dermatol. 130(12), 2790-2798 (2010).
109. Chen Y, Bathula SR, Li J, Huang L. Multifunctional nanoparticles delivering small interfering RNA and doxorubicin overcome drug resistance in cancer. J. Biol. Chem. 285(29), 22639-22650 (2010).
110. Chen Y, Zhu X, Zhang X, Liu B, Huang L. Nanoparticles modified with tumor-targeting scFv deliver siRNA and miRNA for cancer therapy. Mol. Ther. 18(9), 1650-1656 (2010).
111. Johnson FM, Saigal B, Tran H, Donato NJ. Abrogation of signal transducer and activator of transcription 3 reactivation after Src kinase inhibition results in synergistic antitumor effects. Clin. Cancer Res. 13(14), 4233-4244 (2007).
112. Kloth MT, Laughlin KK, Biscardi JS, Boerner JL, Parsons SJ, Silva CM. STAT5b, a mediator of synergism between c-Src and the epidermal growth factor receptor. J. Biol. Chem. 278(3), 1671-1679 (2003).
113. Shelburne CP, Mccoy ME, Piekorz R et al. Stat5 expression is critical for mast cell development and survival. Blood 102(4), 1290-1297 (2003).
114. Kim SK, Huang L. Nanoparticle delivery of a peptide targeting EGFR signaling. J. Control. Release 157(2), 279-286 (2012).
115. Hatakeyama H, Akita H, Harashima H. A multifunctional envelope type nano device (MEND) for gene delivery to tumours based on the EPR effect: a strategy for overcoming the PEG dilemma. Adv. Drug Deliv. Rev. 63(3), 152-160 (2011).
116. Khalil IA, Kogure K, Futaki S, Harashima H. High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression. J. Biol. Chem. 281(6), 3544-3551 (2006).
117. El-Sayed A, Khalil IA, Kogure K, Futaki S, Harashima H. Octaarginine- and octalysine-modified nanoparticles have different modes of endosomal escape. J. Biol. Chem. 283(34), 23450-23461 (2008).
118. Nakamura T, Moriguchi R, Kogure K, Shastri N, Harashima H. Efficient MHC class I presentation by controlled intracellular trafficking of antigens in octaarginine-modified liposomes. Mol. Ther. 16(8), 1507-1514 (2008).
119. Joraku A, Homhuan A, Kawai K et al. Immunoprotection against murine bladder carcinoma by octaarginine-modified liposomes incorporating cell wall of Mycobacterium bovis bacillus Calmette- Guerin. BJU Int. 103(5), 686-693 (2009).
120. Li W, Nicol F, Szoka FC Jr. GALA: a designed synthetic pH-responsive amphipathic peptide with applications in drug and gene delivery. Adv. Drug Deliv. Rev. 56(7), 967-985 (2004).
121. Hatakeyama H, Ito E, Akita H et al. A pH-sensitive fusogenic peptide facilitates endosomal escape and greatly enhances the gene silencing of siRNA-containing nanoparticles in vitro and in vivo. J. Control. Release 139(2), 127-132 (2009).
122. Sakurai Y, Hatakeyama H, Akita H et al. Efficient short interference RNA delivery to tumor cells using a combination of octaarginine, GALA and tumor-specific, cleavable polyethylene glycol system. Biol. Pharm. Bull. 32(5), 928-932 (2009).
123. Kakudo T, Chaki S, Futaki S et al. Transferrin-modified liposomes equipped with a pH-sensitive fusogenic peptide: an artificial viral-like delivery system. Biochemistry 43(19), 5618-5628 (2004).
124. Subbarao NK, Parente RA, Szoka FC Jr, Nadasdi L, Pongracz K. pH-dependent bilayer destabilization by an amphipathic peptide. Biochemistry 26(11), 2964-2972 (1987).
125. Sakurai Y, Hatakeyama H, Sato Y et al. Endosomal escape and the knockdown efficiency of liposomal-siRNA by the fusogenic peptide shGALA. Biomaterials 32(24), 5733-5742 (2011).
126. Trewyn BG, Giri S, Slowing, Ii, Lin VS. Mesoporous silica nanoparticle based controlled release, drug delivery, and biosensor systems. Chem. Commun. (Camb.) (31), 3236-3245 (2007).
127. Slowing II, Trewyn BG, Giri S, Lin VS. Mesoporous silica nanoparticles for drug delivery and biosensing applications. Adv. Funct. Mater. 17(8), 1225-1236 (2007).
128. Rosi NL, Mirkin CA. Nanostructures in biodiagnostics. Chem. Rev. 105(4), 1547-1562 (2005).
129. Jiang XM, Brinker CJ. Aerosol-assisted self-assembly of single-crystal core/nanoporous shell particles as model controlled release capsules. J. Am. Chem. Soc. 128(14), 4512-4513 (2006).
130. Cauda V, Engelke H, Sauer A et al. Colchicine-loaded lipid bilayer-coated 50 nm mesoporous nanoparticles efficiently induce microtubule depolymerization upon cell uptake. Nano Letts 10(7), 2484-2492 (2010).
131. Liu JW, Stace-Naughton A, Jiang XM, Brinker CJ. Porous nanoparticle supported lipid bilayers (protocells) as delivery vehicles. J. Am. Chem. Soc. 131(4),1354-1355 (2009).
132. Mal NK, Fujiwara M, Tanaka Y. Photocontrolled reversible release of guest molecules from coumarin-modified mesoporous silica. Nature 421(6921), 350-353 (2003).
133. Angelos S, Choi E, Vogtle F, De Cola L, Zink JI. Photo-driven expulsion of molecules from mesostructured silica nanoparticles. J. Phys. Chem. C 111(18), 6589-6592 (2007).
134. Lai CY, Trewyn BG, Jeftinija DM et al. A mesoporous silica nanosphere-based carrier system with chemically removable CdS nanoparticle caps for stimuli-responsive controlled release of neurotransmitters and drug molecules. J. Am. Chem. Soc. 125(15), 4451-4459 (2003).
135. Bally M, Bailey K, Sugihara K, Grieshaber D, Voros J, Stadler B. Liposome and lipid bilayer arrays towards biosensing applications. Small 6(22), 2481-2497 (2010).
136. Ashley CE, Carnes EC, Phillips GK et al. The targeted delivery of multicomponent cargos to cancer cells by nanoporous particle-supported lipid bilayers. Nat. Mater. 10(5), 389-397 (2011).
137. Mornet S, Lambert O, Duguet E, Brisson A. The formation of supported lipid bilayers on silica nanoparticles revealed by cryoelectron microscopy. Nano Letts 5(2), 281-285 (2005).
138. Liu J, Jiang X, Ashley C, Brinker CJ. Electrostatically mediated liposome fusion and lipid exchange with a nanoparticle-supported bilayer for control of surface charge, drug containment, and delivery. J. Am. Chem. Soc. 131(22), 7567-7569 (2009).
139. Graham FL, Van Der Eb AJ. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52(2), 456-467 (1973).
140. Kataoka Y, Ka K. Block Copolymer self-assembly into monodispersive nanoparticles with hybrid core of antisense DNA and calcium phosphate. Langmuir 18(12), 4539-4543 (2002).
141. Maitra A. Calcium phosphate nanoparticles: second-generation nonviral vectors in gene therapy. Expert Rev. Mol. Diagn. 5(6), 893-905 (2005).
142. Olton D, Li J, Wilson ME et al. Nanostructured calcium phosphates (NanoCaPs) for non-viral gene delivery: influence of the synthesis parameters on transfection efficiency. Biomaterials 28(6), 1267-1279 (2007).
143. Kakizawa Y, Furukawa S, Ishii A, Kataoka K. Organic-inorganic hybrid-nanocarrier of siRNA constructing through the self-assembly of calcium phosphate and PEG-based block aniomer. J. Control. Release 111(3), 368-370 (2006).
144. Tabakovic A, Kester M, Adair JH. Calcium phosphate-based composite nanoparticles in bioimaging and therapeutic delivery applications. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 4(1), 96-112 (2012).
145. Li J, Chen YC, Tseng YC, Mozumdar S, Huang L. Biodegradable calcium phosphate nanoparticle with lipid coating for systemic siRNA delivery. J. Control. Release 142(3), 416-421 (2010).
146. Morgan TT, Muddana HS, Altinoglu EI et al. Encapsulation of organic molecules in calcium phosphate nanocomposite particles for intracellular imaging and drug delivery. Nano Letts 8(12), 4108-4115 (2008).
147. Faraji AH, Wipf P. Nanoparticles in cellular drug delivery. Bioorg. Med. Chem. 17(8), 2950-2962 (2009).
148. Li J, Yang Y, Huang L. Calcium phosphate nanoparticles with an asymmetric lipid bilayer coating for siRNA delivery to the tumor. J. Control. Release 158(1), 108-114 (2012).
149. Yang Y, Hu Y, Wang Y, Li J, Liu F, Huang L. Nanoparticle delivery of pooled siRNA for effective treatment of non-small cell lung cancer. Mol. Pharm. doi: 10.1021/mp300152v (2012) (Epub ahead of print).
150. Huang L, Liu Y. In vivo delivery of RNAi with lipid-based nanoparticles. Annu. Rev. Biomed. Eng. 13, 507-530 (2011).
151. Yang Y, Li J, Liu F, Huang L. Systemic delivery of siRNA via LCP nanoparticle efficiently inhibits lung metastasis. Mol. Ther. 20(3), 609-615 (2012).
152. Huynh NT, Passirani C, Saulnier P, Benoit JP. Lipid nanocapsules: a new platform for nanomedicine. Int. J. Cancer 379(2), 201-209 (2009).
153. Coon JS, Knudson W, Clodfelter K, Lu B, Weinstein RS. Solutol HS 15, nontoxic polyoxyethylene esters of 12-hydroxystearic acid, reverses multidrug resistance. Cancer Res. 51(3), 897-902 (1991).
154. Lamprecht A, Benoit JP. Etoposide nanocarriers suppress glioma cell growth by intracellular drug delivery and simultaneous P-glycoprotein inhibition. J. Control. Release 112(2), 208-213 (2006).
155. Garcion E, Lamprecht A, Heurtault B et al. A new generation of anticancer, drug-loaded, colloidal vectors reverses multidrug resistance in glioma and reduces tumor progression in rats. Mol. Cancer Ther. 5(7), 1710-1722 (2006).
156. Morille M, Passirani C, Dufort S et al. Tumor transfection after systemic injection of DNA lipid nanocapsules. Biomaterials 32(9), 2327-2333 (2011).
157. Vonarbourg A, Passirani C, Desigaux L et al. The encapsulation of DNA molecules within biomimetic lipid nanocapsules. Biomaterials 30(18), 3197-3204 (2009).
158. Bhaumik S. Advances in imaging gene-directed enzyme prodrug therapy. Curr. Pharm. Biotechnol. 12(4), 497-507 (2011).
159. David S, Carmoy N, Resnier P et al. In vivo imaging of DNA lipid nanocapsules after systemic administration in a melanoma mouse model. Int. J. Cancer 423(1), 108-115 (2012).
160. Trickler WJ, Munt DJ, Jain N, Joshi SS, Dash AK. Antitumor efficacy, tumor distribution and blood pharmacokinetics of chitosan/glyceryl-monooleate nanostructures containing paclitaxel. Nanomedicine (Lond.) 6(3), 437-448 (2011).
161. Hasan W, Chu K, Gullapalli A et al. Delivery of multiple siRNAs using lipid-coated PLGA nanoparticles for treatment of prostate cancer. Nano Letts. 12(1), 287-292 (2012).
162. Li W, Yang Y, Wang C et al. Carrier-free, functionalized drug nanoparticles for targeted drug delivery. Chem. Commun. (Camb.) 48(65), 8120-8122 (2012).
163. Khandare J, Calderon M, Dagia NM, Haag R. Multifunctional dendritic polymers in nanomedicine: opportunities and challenges. Chem. Soc. Rev. 41(7), 2824-2848 (2012).
164. Park JW, Hong K, Kirpotin DB et al. Anti- HER2 immunoliposomes: enhanced efficacy attributable to targeted delivery. Clin. Cancer Res. 8(4), 1172-1181 (2002).
165. Sun B, Ranganathan B, Feng SS. Multifunctional poly(d, l-lactide-co-glycolide)/montmorillonite (PLGA/MMT) nanoparticles decorated by Trastuzumab for targeted chemotherapy of breast cancer. Biomaterials 29(4), 475-486 (2008).
166. Gao J, Zhong W, He J et al. Tumor-targeted PE38KDEL delivery via PEGylated anti- HER2 immunoliposomes. Int. J. Cancer 374(1-2), 145-152 (2009).
167. Farokhzad OC, Jon S, Khademhosseini A, Tran TN, Lavan DA, Langer R. Nanoparticle-aptamer bioconjugates: a new approach for targeting prostate cancer cells. Cancer Res. 64(21), 7668-7672 (2004).
168. Farokhzad OC, Cheng J, Teply BA et al. Targeted nanoparticle-aptamer bioconjugates for cancer chemotherapy in vivo. Proc. Natl Acad. Sci. USA 103(16), 6315-6320 (2006).
169. Sahoo SK, Labhasetwar V. Enhanced antiproliferative activity of transferrin-conjugated paclitaxel-loaded nanoparticles is mediated via sustained intracellular drug retention. Mol. Pharm. 2(5), 373-383 (2005).
170. Li JL, Wang L, Liu XY et al. In vitro cancer cell imaging and therapy using transferrin-conjugated gold nanoparticles. Cancer Lett. 274(2), 319-326 (2009).
171. Thomas TP, Shukla R, Kotlyar A et al. Dendrimer-epidermal growth factor conjugate displays superagonist activity. Biomacromolecules 9(2), 603-609 (2008).
172. Karmali PP, Kotamraju VR, Kastantin M et al. Targeting of albumin-embedded paclitaxel nanoparticles to tumors. Nanomedicine 5(1), 73-82 (2009).
173. Sugahara KN, Teesalu T, Karmali PP et al. Coadministration of a tumor-penetrating peptide enhances the efficacy of cancer drugs. Science 328(5981), 1031-1035 (2010).
174. Oh S, Kim BJ, Singh NP, Lai H, Sasaki T. Synthesis and anti-cancer activity of covalent conjugates of artemisinin and a transferrin-receptor targeting peptide. Cancer Lett. 274(1), 33-39 (2009).
175. Lo A, Lin CT, Wu HC. Hepatocellular carcinoma cell-specific peptide ligand for targeted drug delivery. Mol. Cancer Ther. 7(3), 579-589 (2008).
176. Wang S, Low PS. Folate-mediated targeting of antineoplastic drugs, imaging agents, and nucleic acids to cancer cells. J. Control. Release 53(1-3), 39-48 (1998).
177. Zeng C, Vangveravong S, Xu J et al. Subcellular localization of sigma-2 receptors in breast cancer cells using two-photon and confocal microscopy. Cancer Res. 67(14), 6708-6716 (2007).
178. Hornick JR, Xu J, Vangveravong S et al. The novel sigma-2 receptor ligand SW43 stabilizes pancreas cancer progression in combination with gemcitabine. Mol. Cancer 9, 298 (2010).
179. Wang B, Rouzier R, Albarracin CT et al. Expression of sigma 1 receptor in human breast cancer. Breast Cancer Res. Treat. 87(3), 205-214 (2004).
180. Kim TH, Park IK, Nah JW, Choi YJ, Cho CS. Galactosylated chitosan/DNA nanoparticles prepared using water-soluble chitosan as a gene carrier. Biomaterials 25(17), 3783-3792 (2004).
181. Ashley CE, Carnes EC, Epler KE et al. Delivery of small interfering RNA by peptide-targeted mesoporous silica nanoparticle-supported lipid bilayers. ACS Nano 6(3), 2174-2188 (2012).