Evidence for a new mechanism behind HIFU-triggered release from liposomes

Journal of Controlled Release

Volumn 168, Issue 3, 2013, Pages 327-333

  Oerlemans, Chris ^a,b   Deckers, Roel ^b   Storm, Gert ^c   Hennink, Wim E ^c   Nijsen, J Frank W ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Controlled release; Drug delivery systems (DDS); High intensity focused ultrasound (HIFU); Nanoparticles; Thermosensitive liposomes; Triggered release

Indexed keywords

CONTROLLED RELEASE; DRUG DELIVERY SYSTEM; HIGH INTENSITY FOCUSED ULTRASOUND; THERMOSENSITIVE LIPOSOMES; TRIGGERED RELEASE;

CAVITATION; DRUG DELIVERY; DRUG PRODUCTS; HYDROPHILICITY; NANOPARTICLES; PHOSPHOLIPIDS; POLYDISPERSITY; ULTRASONICS;

LIPOSOMES;

FLUORESCEIN; LIPOSOME;

ARTICLE; DRUG FORMULATION; DRUG RELEASE; HIGH INTENSITY FOCUSED ULTRASOUND; HYDROPHOBICITY; LIGHT SCATTERING; LIPOPHILICITY; MICROBUBBLE; PRIORITY JOURNAL; PULSE WAVE; QUANTITATIVE ANALYSIS; RADIATION; THERMOREGULATION; THERMOSENSITIVE GENIC MALE STERILITY;

ACOUSTICS; DRUG DELIVERY SYSTEMS; FLUORESCEIN; FLUORESCENT DYES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPOSOMES; OXAZINES; TEMPERATURE;

EID: 84878585041     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2013.03.019     Document Type: Article

References (58)

1. V.P. Torchilin Multifunctional nanocarriers Adv. Drug Deliv. Rev. 58 2006 1532 1555
2. T.M. Allen, and P.R. Cullis Drug delivery systems: entering the mainstream Science 303 2004 1818 1822
3. G.A. Koning, and G.C. Krijger Targeted multifunctional lipid-based nanocarriers for image-guided drug delivery Anticancer Agents Med. Chem. 7 2007 425 440
4. T. Lammers, F. Kiessling, W.E. Hennink, and G. Storm Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress J. Control. Release 161 2012 175 187
5. C. Oerlemans, W. Bult, M. Bos, G. Storm, J.F. Nijsen, and W.E. Hennink Polymeric micelles in anticancer therapy: targeting, imaging and triggered release Pharm. Res. 27 2010 2569 2589
6. I.K. Kwon, S.C. Lee, B. Han, and K. Park Analysis on the current status of targeted drug delivery to tumors J. Control. Release 164 2012 108 114
7. K. Riehemann, S.W. Schneider, T.A. Luger, B. Godin, M. Ferrari, and H. Fuchs Nanomedicine-challenge and perspectives Angew. Chem. Int. Ed. Engl. 48 2009 872 897
8. B.Y. Kim, J.T. Rutka, and W.C. Chan Nanomedicine N. Engl. J. Med. 363 2010 2434 2443
9. K. Greish Enhanced permeability and retention of macromolecular drugs in solid tumors: a royal gate for targeted anticancer nanomedicines J. Drug Target. 15 2007 457 464
10. H. Maeda, J. Wu, T. Sawa, Y. Matsumura, and K. Hori Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review J. Control. Release 65 2000 271 284
11. H. Maeda Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects Bioconjug. Chem. 21 2010 797 802
12. V.P. Torchilin Recent advances with liposomes as pharmaceutical carriers Nat. Rev. Drug Discov. 4 2005 145 160
13. K. Maruyama, S. Unezaki, N. Takahashi, and M. Iwatsuru Enhanced delivery of doxorubicin to tumor by long-circulating thermosensitive liposomes and local hyperthermia Biochim. Biophys. Acta 1149 1993 209 216
14. D. Needham, and M.W. Dewhirst The development and testing of a new temperature-sensitive drug delivery system for the treatment of solid tumors Adv. Drug Deliv. Rev. 53 2001 285 305
15. D. Papahadjopoulos, K. Jacobson, S. Nir, and T. Isac Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol Biochim. Biophys. Acta 311 1973 330 348
16. M.B. Yatvin, J.N. Weinstein, W.H. Dennis, and R. Blumenthal Design of liposomes for enhanced local release of drugs by hyperthermia Science 202 1978 1290 1293
17. R.T. Poon, and N. Borys Lyso-thermosensitive liposomal doxorubicin: an adjuvant to increase the cure rate of radiofrequency ablation in liver cancer Future Oncol. 7 2011 937 945
18. J. Siepmann, and F. Siepmann Modeling of diffusion controlled drug delivery J. Control. Release 161 2012 351 362
19. L.K. Zeng, and X.Y. Wu Modeling the sustained release of lipophilic drugs from liposomes Appl. Phys. Lett. 97 2010
20. E.K. Rowinsky, and R.C. Donehower Paclitaxel (taxol) N. Engl. J. Med. 332 1995 1004 1014
21. V. Guarneri, M.V. Dieci, and P. Conte Enhancing intracellular taxane delivery: current role and perspectives of nanoparticle albumin-bound paclitaxel in the treatment of advanced breast cancer Expert. Opin. Pharmacother. 13 2012 395 406
22. T. Okusaka, S. Okada, T. Nakanishi, S. Fujiyama, and Y. Kubo Phase II trial of intra-arterial chemotherapy using a novel lipophilic platinum derivative (SM-11355) in patients with hepatocellular carcinoma Invest. New Drugs 22 2004 169 176
23. Y. Yu, L.G. Lou, W.P. Liu, H.J. Zhu, Q.S. Ye, X.Z. Chen, W.G. Gao, and S.Q. Hou Synthesis and anticancer activity of lipophilic platinum(II) complexes of 3,5-diisopropylsalicylate Eur. J. Med. Chem. 43 2008 1438 1443
24. L. Zhao, and S.S. Feng Effects of lipid chain unsaturation and headgroup type on molecular interactions between paclitaxel and phospholipid within model biomembrane J. Colloid Interface Sci. 285 2005 326 335
25. M. de Smet, S. Langereis, S. van den Bosch, and H. Grull Temperature-sensitive liposomes for doxorubicin delivery under MRI guidance J. Control. Release 143 2010 120 127
26. C. Oerlemans, F. Nijsen, M. van Amersfoort, L. van Bloois, E. Heijman, P. Luijten, W. Mali, and G. Storm A novel approach to identify non-palpable breast lesions combining fluorescent liposomes and magnetic resonance-guided high intensity focused ultrasound-triggered release Eur. J. Pharm. Biopharm. 77 2011 458 464
27. R. Staruch, R. Chopra, and K. Hynynen Localised drug release using MRI-controlled focused ultrasound hyperthermia Int. J. Hyperthermia 27 2011 156 171
28. A. Ranjan, G.C. Jacobs, D.L. Woods, A.H. Negussie, A. Partanen, P.S. Yarmolenko, C.E. Gacchina, K.V. Sharma, V. Frenkel, B.J. Wood, and M.R. Dreher Image-guided drug delivery with magnetic resonance guided high intensity focused ultrasound and temperature sensitive liposomes in a rabbit Vx2 tumor model J. Control. Release 158 2012 487 494
29. N. Rapoport Ultrasound-mediated micellar drug delivery Int. J. Hyperth. 28 2012 374 385
30. A. Marin, M. Muniruzzaman, and N. Rapoport Mechanism of the ultrasonic activation of micellar drug delivery J. Control. Release 75 2001 69 81
31. R. Deckers, and C.T. Moonen Ultrasound triggered, image guided, local drug delivery J. Control. Release 148 2010 25 33
32. F.A. Jolesz MRI-Guided Focused Ultrasound Surgery Annu. Rev. Med. 60 2009 417 430
33. S. Dromi, V. Frenkel, A. Luk, B. Traughber, M. Angstadt, M. Bur, J. Poff, J. Xie, S.K. Libutti, K.C. Li, and B.J. Wood Pulsed-high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect Clin. Cancer Res. 13 2007 2722 2727
34. D.L. Miller, and J. Song Tumor growth reduction and DNA transfer by cavitation-enhanced high-intensity focused ultrasound in vivo Ultrasound Med. Biol. 29 2003 887 893
35. R.E. Apfel Acoustic cavitation: a possible consequence of biomedical uses of ultrasound Br. J. Cancer Suppl. 5 1982 140 146
36. G.A. Husseini, and W.G. Pitt The use of ultrasound and micelles in cancer treatment J. Nanosci. Nanotechnol. 8 2008 2205 2215
37. G.A. Husseini, D. Velluto, L. Kherbeck, W.G. Pitt, J.A. Hubbell, and D.A. Christensen Investigating the acoustic release of doxorubicin from targeted micelles Colloids Surf. B: Biointerfaces 101C 2012 153 155
38. A. Schroeder, Y. Avnir, S. Weisman, Y. Najajreh, A. Gabizon, Y. Talmon, J. Kost, and Y. Barenholz Controlling liposomal drug release with low frequency ultrasound: mechanism and feasibility Langmuir 23 2007 4019 4025
39. A. Schroeder, R. Honen, K. Turjeman, A. Gabizon, J. Kost, and Y. Barenholz Ultrasound triggered release of cisplatin from liposomes in murine tumors J. Control. Release 137 2009 63 68
40. F. Ahmadi, I.V. McLoughlin, S. Chauhan, and G. ter-Haar Bio-effects and safety of low-intensity, low-frequency ultrasonic exposure Prog. Biophys. Mol. Biol. 108 2012 119 138
41. D. Dalecki Mechanical bioeffects of ultrasound Annu. Rev. Biomed. Eng. 6 2004 229 248
42. G.A. Koning, H.W. Morselt, M.J. Velinova, J. Donga, A. Gorter, T.M. Allen, S. Zalipsky, J.A. Kamps, and G.L. Scherphof Selective transfer of a lipophilic prodrug of 5-fluorodeoxyuridine from immunoliposomes to colon cancer cells Biochim. Biophys. Acta 1420 1999 153 167
43. Y. Barenholz Doxil (R) - The first FDA-approved nano-drug: lessons learned J. Control. Release 160 2012 117 134
44. A.K. Dutta, K. Kamada, and K. Ohta Spectroscopic studies of Nile red in organic solvents and polymers J. Photochem. Photobiol. A Chem. 93 1996 57 64
45. G. Madelin, B. Hosten, C. Biateau, C. Mougenot, J.M. Franconi, and E. Thiaudiere Comparison of laser interferometry and radiation force method of measuring ultrasonic power Ultrasonics 43 2005 769 774
46. M. Bikram, and J.L. West Thermo-responsive systems for controlled drug delivery Expert. Opin. Drug Deliv. 5 2008 1077 1091
47. K. Djanashvili, T.L. ten Hagen, R. Blange, D. Schipper, J.A. Peters, and G.A. Koning Development of a liposomal delivery system for temperature-triggered release of a tumor targeting agent, Ln(III)-DOTA-phenylboronate Bioorg. Med. Chem. 19 2011 1123 1130
48. R.B. Campbell, S.V. Balasubramanian, and R.M. Straubinger Influence of cationic lipids on the stability and membrane properties of paclitaxel- containing liposomes J. Pharm. Sci. 90 2001 1091 1105
49. H.A. Hancock, L.H. Smith, J. Cuesta, A.K. Durrani, M. Angstadt, M.L. Palmeri, E. Kimmel, and V. Frenkel Investigations into pulsed high-intensity focused ultrasound-enhanced delivery: preliminary evidence for a novel mechanism Ultrasound Med. Biol. 35 2009 1722 1736
50. M.L. Palmeri, M.H. Wang, J.J. Dahl, K.D. Frinkley, and K.R. Nightingale Quantifying hepatic shear modulus in vivo using acoustic radiation force Ultrasound Med. Biol. 34 2008 546 558
51. A.P. Sarvazyan, O.V. Rudenko, and W.L. Nyborg Biomedical applications of radiation force of ultrasound: historical roots and physical basis Ultrasound Med. Biol. 36 2010 1379 1394
52. Celsion Corporation http://celsion.com/docs/pipeline-overview 2012 (accessed 10-10-2012)
53. S. Hartel, H.A. Diehl, and F. Ojeda Methyl-beta-cyclodextrins and liposomes as water-soluble carriers for cholesterol incorporation into membranes and its evaluation by a microenzymatic fluorescence assay and membrane fluidity-sensitive dyes Anal. Biochem. 258 1998 277 284
54. T. Parasassi, A.M. Giusti, M. Raimondi, and E. Gratton Abrupt modifications of phospholipid bilayer properties at critical cholesterol concentrations Biophys. J. 68 1995 1895 1902
55. C. Socaciu, R. Jessel, and H.A. Diehl Competitive carotenoid and cholesterol incorporation into liposomes: effects on membrane phase transition, fluidity, polarity and anisotropy Chem. Phys. Lipids 106 2000 79 88
56. K.W. Ferrara Driving delivery vehicles with ultrasound Adv. Drug Deliv. Rev. 60 2008 1097 1102
57. A. Yudina, M. de Smet, M. Lepetit-Coiffe, S. Langereis, L. van Ruijssevelt, P. Smirnov, V. Bouchaud, P. Voisin, H. Grull, and C.T. Moonen Ultrasound-mediated intracellular drug delivery using microbubbles and temperature-sensitive liposomes J. Control. Release 155 2011 442 448
58. S. Ibsen, M. Benchimol, D. Simberg, and S. Esener Ultrasound mediated localized drug delivery Adv. Exp. Med. Biol. 733 2012 145 153