Plasmonic nanobubble-enhanced endosomal escape processes for selective and guided intracellular delivery of chemotherapy to drug-resistant cancer cells

Biomaterials

Volumn 33, Issue 6, 2012, Pages 1821-1826

  Lukianova Hleb, Ekaterina Y ^a   Belyanin, Andrey ^a   Kashinath, Shruti ^a   Wu, Xiangwei ^b   Lapotko, Dmitri O ^a  

^a RICE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Drug delivery; Drug release; Gold; Laser; Liposome; Nanoparticle

Indexed keywords

CANCER CELLS; CANCER CHEMOTHERAPY; DRUG RELEASE; ENCAPSULATED DRUGS; ESCAPE PROCESS; GOLD NANOPARTICLES; HETEROGENEOUS ENVIRONMENTS; INTRACELLULAR DELIVERY; INTRACELLULAR DRUG DELIVERY; MULTIDRUG RESISTANCE; NANOBUBBLES; PLASMONIC; THERAPEUTIC EFFICACY; TREATMENT TIME;

CELLS; CHEMOTHERAPY; CYTOLOGY; DISEASES; DRUG DELIVERY; GOLD; LASERS; LIPOSOMES; NANOPARTICLES; PLASMONS; TOXICITY;

DRUG DOSAGE;

DOXORUBICIN; GOLD NANOPARTICLE; NANOBUBBLE;

ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOPLASM; DRUG DELIVERY SYSTEM; DRUG EFFICACY; ENDOSOME; HUMAN; HUMAN CELL; NANOENCAPSULATION; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CYTOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; DOXORUBICIN; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; GOLD; HUMANS; LASERS; LIPOSOMES; METAL NANOPARTICLES; NANOPARTICLES; NANOTECHNOLOGY; NEOPLASMS;

EID: 83555178368     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2011.11.015     Document Type: Article

References (43)

1. Cho K., Wang X., Nie S., Chen Z.G., Shin D.M. Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer Res 2008, 14:1310-1316.
2. Peer D., Karp J.M., Hong S., Farokhzad O.C., Margalit R., Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2007, 2:751-760.
3. Meng H., Liong M., Xia T., Li Z., Ji Z., Zink J.I., et al. Engineered design of mesoporous silica nanoparticles to deliver doxorubicin and P-glycoprotein siRNA to overcome drug resistance in a cancer cell line. ACS Nano 2010, 4:4539-4550.
4. Liang X.J., Meng H., Wang Y., He H., Meng J., Lu J., et al. Metallofullerene nanoparticles circumvent tumor resistance to cisplatin by reactivating endocytosis. Proc Natl Acad Sci USA 2010, 107:7449-7454.
5. Sajja H.K., East M.P., Mao H., Wang Y.A., Nie S., Yang L. Development of multifunctional nanoparticles for targeted drug delivery and noninvasive imaging of therapeutic effect. Curr Drug Discov Technol 2009, 6:43-51.
6. Prabaharan M., Grailer J.J., Pilla S., Steeber D.A., Gong S.Q. Gold nanoparticles with a monolayer of doxorubicin-conjugated amphiphilic block copolymer for tumor-targeted drug delivery. Biomaterials 2009, 30:6065-6075.
7. Yuk S.H., Oh K.S., Koo H., Jeon H., Kim K., Kwon I.C. Multi-core vesicle nanoparticles based on vesicle fusion for delivery of chemotherapic drugs. Biomaterials 2011, 32:7924-7931.
8. Wu G.H., Milkhailovsky A., Khant H.A., Fu C., Chiu W., Zasadzinski J.A. Remotely triggered liposome release by near-infrared light absorption via hollow gold nanoshells. J Am Chem Soc 2008, 130:8175-8177.
9. Braun G.B., Pallaoro A., Wu G., Missirlis D., Zasadzinski J.A., Tirrell M., et al. Laser-activated gene silencing via gold nanoshell-siRNA conjugates. ACS Nano 2009, 3:2007-2015.
10. Wang F., Wang Y.C., Dou S., Xiong M.H., Sun T.M., Wang J. Doxorubicin-tethered responsive gold nanoparticles facilitate intracellular drug delivery for overcoming multidrug resistance in cancer cells. ACS Nano 2011, 5:3679-3692.
11. Kim B., Han G., Toley B.J., Kim C.K., Rotello V.M., Forbes N.S. Tuning payload delivery in tumour cylindroids using gold nanoparticles. Nat Nanotechnol 2010, 5:465-472.
12. Paasonen L., Sipila T., Subrizi A., Laurinmaki P., Butcher S.J., Rappolt M., et al. Gold-embedded photosensitive liposomes for drug delivery: triggering mechanism and intracellular release. J Control Release 2010, 147:136-143.
13. Pissuwan D., Niidome T., Cortie M.B. The forthcoming applications of gold nanoparticles in drug and gene delivery systems. J Control Release 2011, 149:65-71.
14. Musacchio T., Torchilin V.P. Recent developments in lipid-based pharmaceutical nanocarriers. Front Biosci 2011, 16:1388-1412.
15. Kuykendall D.W., Zimmerman S.C. Nanoparticles - A very versatile nanocapsule. Nat Nanotechnol 2007, 2:201-202.
16. Fechheimer M., Boylan J.F., Parker S., Sisken J.E., Patel G.L., Zimmer S.G. Transfection of mammalian cells with plasmid DNA by scrape loading and sonication loading. Proc Natl Acad Sci USA 1987, 84:8463-8467.
17. Prentice P., Cuschierp A., Dholakia K., Prausnitz M., Campbell P. Membrane disruption by optically controlled microbubble cavitation. Nat Phys 2005, 1:107-110.
18. Yoshida S., Kashiwamura S.I., Hosoya Y., Luo E., Matsuoka H., Ishii A., et al. Direct immunization of malaria DNA vaccine into the liver by gene gun protects against lethal challenge of Plasmodium berghei sporozoite. Biochem Biophys Res Commun 2000, 271:107-115.
19. Lee S., McAuliffe D.J., Flotte T.J., Kollias N., Doukas A.G. Photomechanical transcutaneous delivery of macromolecules. J Invest Dermatol 1998, 111:925-929.
20. Qiu Y., Luo Y., Zhang Y., Cui W., Zhang D., Wu J., et al. The correlation between acoustic cavitation and sonoporation involved in ultrasound-mediated DNA transfection with polyethylenimine (PEI) in vitro. J Control Release 2010, 145:40-48.
21. Haas K., Sin W.C., Javaherian A., Li Z., Cline H.T. Single-cell electroporation for gene transfer in vivo. Neuron 2001, 29:583-591.
22. Soughayer J.S., Krasieva T., Jacobson S.C., Ramsey J.M., Tromberg B.J., Allbritton N.L. Characterization of cellular optoporation with distance. Anal Chem 2000, 72:1342-1347.
23. Stevenson D., Agate B., Tsampoula X., Fischer P., Brown C.T.A., Sibbett W., et al. Femtosecond optical transfection of cells: viability and efficiency. Opt Express 2006, 14:7125-7133.
24. Lukianova-Hleb E., Hu Y., Latterini L., Tarpani L., Lee S., Drezek R.A., et al. Plasmonic nanobubbles as transient vapor nanobubbles generated around plasmonic nanoparticles. ACS Nano 2010, 4:2109-2123.
25. Lukianova-Hleb E., Lapotko D.O. Influence of transient environmental photothermal effects on optical scattering by gold nanoparticles. Nano Lett 2009, 9:2160-2166.
26. Wagner D.S., Delk N.A., Lukianova-Hleb E.Y., Hafner J.H., Farach-Carson M.C., Lapotko D.O. The in vivo performance of plasmonic nanobubbles as cell theranostic agents in zebrafish hosting prostate cancer xenografts. Biomaterials 2010, 31:7567-7574.
27. Lukianova-Hleb E., Hanna E.Y., Hafner J.H., Lapotko D.O. Tunable plasmonic nanobubbles for cell theranostics. Nanotechnology 2010, 21:82102.
28. Lukianova-Hleb E., Samaniego A., Wen J., Metelitsa L., Chang C.-C., Lapotko D. Selective gene transfection of individual cells in vitro with plasmonic nanobubbles. J Control Release 2011, 152:286-293.
29. Lapotko D.O., Lukianova-Hleb E.Y., Oraevsky A.A. Clusterization of nanoparticles during their interaction with living cells. Nanomedicine (Lond) 2007, 2:241-253.
30. Anderson L., Hansen E., Lukianova-Hleb E.Y., Hafner J.H., Lapotko D.O. Optically guided controlled release from liposomes with tunable plasmonic nanobubbles. J Control Release 2010, 144:151-158.
31. Wu G., Mikhailovsky A., Khant H.A., Zasadzinski J.A. Chapter 14-Synthesis, characterization, and optical response of gold nanoshells used to trigger release from liposomes. Methods Enzymol 2009, 464:279-307.
32. Laser Institute of America American national standard for safe use of lasers (ANSI Z136.1-2000) 2000.
33. Park J.W., Mamot C., Drummond D.C., Greiser U., Hong K., Kirpotin D.B., et al. Epidermal growth factor receptor (EGFR)-targeted immunoliposomes mediate specific and efficient drug delivery to EGFR- and EGFRvIII-overexpressing tumor cells. Cancer Res 2003, 63:3154-3161.
34. Lukyanov A.N., Elbayoumi T.A., Chakilam A.R., Torchilin V.P. Tumor-targeted liposomes: doxorubicin-loaded long-circulating liposomes modified with anti-cancer antibody. J Control Release 2004, 100:135-144.
35. Elbayoumi T.A., Torchilin V.P. Enhanced cytotoxicity of monoclonal anticancer antibody 2C5-modified doxorubicin-loaded PEGylated liposomes against various tumor cell lines. Eur J Pharm Sci 2007, 32:159-168.
36. Hleb E., Hafner J.H., Myers J.N., Hanna E.Y., Rostro B.C., Zhdanok S.A., et al. LANTCET: elimination of solid tumor cells with photothermal bubbles generated around clusters of gold nanoparticles. Nanomedicine (Lond) 2008, 3:647-667.
37. Chithrani B.D.C.W. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett 2007, 2007(7):1542-1550.
38. Salmaso S., Caliceti P., Amendola V., Meneghetti M., Magnusson J.P., Pasparakis G., et al. Cell up-take control of gold nanoparticles functionalized with a thermoresponsive polymer. J Mater Chem 2009, 19:1608-1615.
39. Neumann J., Brinkmann R. Nucleation dynamics around single microabsorbers in water heated by nanosecond laser irradiation. J Appl Phys 2007, 101:114701.
40. Vanleeuwen T.G., Jansen E.D., Motamedi M., Welch A.J., Borst C. Excimer-laser ablation of soft-tissue - a study of the content of rapidly expanding and collapsing bubbles. IEEE J Quantum Elect 1994, 30:1339-1347.
41. Vogel A., Noack J., Huttman G., Paltauf G. Mechanisms of femtosecond laser nanosurgery of cells and tissues. Appl Phys B-Lasers O 2005, 81:1015-1047.
42. Doxil Product information book 2011, vol. 3. Centocor Ortho Biotech Products, L.P. USA.
43. Qin G., Li Z., Xia R., Li F., O'Neill B.E., Goodwin J.T., et al. Partially polymerized liposomes: stable against leakage yet capable of instantaneous release for remote controlled drug delivery. Nanotechnology 2011, 22:155605.