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Research Articles

Ultrasound-induced cell permeabilisation and hyperthermia: Strategies for local delivery of compounds with intracellular mode of action

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Pages 311-319 | Received 20 Dec 2011, Accepted 01 Feb 2012, Published online: 23 May 2012

References

  • Deckers R, Moonen CT. Ultrasound triggered, image guided, local drug delivery. J Control Release 2010; 148: 25–33
  • Kong G, Anyarambhatla G, Petros WP, Braun RD, Colvin OM, Needham D, et al. Efficacy of liposomes and hyperthermia in a human tumor xenograft model: Importance of triggered drug release. Cancer Res 2000; 60: 6950–6957
  • Viglianti BL, Abraham SA, Michelich CR, Yarmolenko PS, MacFall JR, Bally MB, et al. In vivo monitoring of tissue pharmacokinetics of liposome/drug using MRI: Illustration of targeted delivery. Magn Reson Med 2004; 51: 1153–1162
  • Bos C, Lepetit-Coiffe M, Quesson B, Moonen CT. Simultaneous monitoring of temperature and T1: Methods and preliminary results of application to drug delivery using thermosensitive liposomes. Magn Reson Med 2005; 54: 1020–1024
  • Khoobehi B, Peyman GA, Niesman MR, Oncel M. Hyperthermia and temperature-sensitive liposomes: Selective delivery of drugs into the eye. Jpn J Ophthalmol 1989; 33: 405–412
  • Dromi S, Frenkel V, Luk A, Traughber B, Angstadt M, Bur M, et al. Pulsed high intensity focused ultrasound and low temperature-sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin Cancer Res 2007; 13: 2722–2727
  • McDannold N, Fossheim SL, Rasmussen H, Martin H, Vykhodtseva N, Hynynen K. Heat-activated liposomal MR contrast agent: Initial in vivo results in rabbit liver and kidney. Radiology 2004; 230: 743–752
  • Negussie AH, Yarmolenko PS, Partanen A, Ranjan A, Jacobs G, Woods D, et al. Formulation and characterisation of magnetic resonance imageable thermally sensitive liposomes for use with magnetic resonance-guided high intensity focused ultrasound. Int J Hyperthermia 2011; 27: 140–155
  • Yatvin MB, Weinstein JN, Dennis WH, Blumenthal R. Design of liposomes for enhanced local release of drugs by hyperthermia. Science 1978; 202: 1290–1293
  • Needham D, Anyarambhatla G, Kong G, Dewhirst MW. A new temperature-sensitive liposome for use with mild hyperthermia: Characterization and testing in a human tumor xenograft model. Cancer Res 2000; 60: 1197–1201
  • Sandstrom MC, Ickenstein LM, Mayer LD, Edwards K. Effects of lipid segregation and lysolipid dissociation on drug release from thermosensitive liposomes. J Control Release 2005; 107: 131–142
  • Bikram M, West JL. Thermo-responsive systems for controlled drug delivery. Expert Opin Drug Deliv 2008; 5: 1077–1091
  • Tagami T, Ernsting MJ, Li SD. Efficient tumor regression by a single and low dose treatment with a novel and enhanced formulation of thermosensitive liposomal doxorubicin. J Control Release 2011; 152: 303–309
  • Sharma D, Chelvi TP, Kaur J, Ralhan R. Thermosensitive liposomal taxol formulation: Heat-mediated targeted drug delivery in murine melanoma. Melanoma Res 1998; 8: 240–244
  • Nie S, Hsiao WL, Pan W, Yang Z. Thermoreversible Pluronic F127-based hydrogel containing liposomes for the controlled delivery of paclitaxel: In vitro drug release, cell cytotoxicity, and uptake studies. Int J Nanomedicine 2011; 6: 151–166
  • Kakinuma K, Tanaka R, Takahashi H, Sekihara Y, Watanabe M, Kuroki M. Drug delivery to the brain using thermosensitive liposome and local hyperthermia. Int J Hyperthermia 1996; 12: 157–165
  • Aoki H, Kakinuma K, Morita K, Kato M, Uzuka T, Igor G, et al. Therapeutic efficacy of targeting chemotherapy using local hyperthermia and thermosensitive liposome: Evaluation of drug distribution in a rat glioma model. Int J Hyperthermia 2004; 20: 595–605
  • Poon RT, Borys N. Lyso-thermosensitive liposomal doxorubicin: A novel approach to enhance efficacy of thermal ablation of liver cancer. Expert Opin Pharmacother 2009; 10: 333–343
  • Poon RT, Borys N. Lyso-thermosensitive liposomal doxorubicin: An adjuvant to increase the cure rate of radiofrequency ablation in liver cancer. Future Oncol 2011; 7: 937–945
  • Ferrara KW. Driving delivery vehicles with ultrasound. Adv Drug Deliv Rev 2008; 60: 1097–1102
  • Dittmar KM, Xie J, Hunter F, Trimble C, Bur M, Frenkel V, et al. Pulsed high-intensity focused ultrasound enhances systemic administration of naked DNA in squamous cell carcinoma model: Initial experience. Radiology 2005; 235: 541–546
  • Hancock HA, Smith LH, Cuesta J, Durrani AK, Angstadt M, Palmeri ML, et al. Investigations into pulsed high-intensity focused ultrasound-enhanced delivery: Preliminary evidence for a novel mechanism. Ultrasound Med Biol 2009; 35: 1722–1736
  • Hynynen K. Focused ultrasound for blood–brain disruption and delivery of therapeutic molecules into the brain. Expert Opin Drug Deliv 2007; 4: 27–35
  • Hynynen K. Ultrasound for drug and gene delivery to the brain. Adv Drug Deliv Rev 2008; 60: 1209–1217
  • Hallow DM, Mahajan AD, Prausnitz MR. Ultrasonically targeted delivery into endothelial and smooth muscle cells in ex vivo arteries. J Control Release 2007; 118: 285–293
  • Larkin JO, Casey GD, Tangney M, Cashman J, Collins CG, Soden DM, et al. Effective tumor treatment using optimized ultrasound-mediated delivery of bleomycin. Ultrasound Med Biol 2008; 34: 406–413
  • Yudina A, Lepetit-Coiffe M, Moonen CT. Evaluation of the temporal window for drug delivery following ultrasound-mediated membrane permeability enhancement. Mol Imaging Biol 2011; 13: 239–249
  • Deckers R, Quesson B, Arsaut J, Eimer S, Couillaud F, Moonen CT. Image-guided, noninvasive, spatiotemporal control of gene expression. Proc Natl Acad Sci USA 2009; 106: 1175–1180
  • Frenkel V. Ultrasound mediated delivery of drugs and genes to solid tumors. Adv Drug Deliv Rev 2008; 60: 1193–1208
  • Tempany CM, McDannold NJ, Hynynen K, Jolesz FA. Focused ultrasound surgery in oncology: Overview and principles. Radiology 2011; 259: 39–56
  • Kennedy JE. High-intensity focused ultrasound in the treatment of solid tumours. Nat Rev Cancer 2005; 5: 321–327
  • Kim SH, Jung SE, Kim HL, Hahn ST, Park GS, Park WC. The potential role of dynamic MRI in assessing the effectiveness of high-intensity focused ultrasound ablation of breast cancer. Int J Hyperthermia 2010; 26: 594–603
  • Illing RO, Kennedy JE, Wu F, ter Haar GR, Protheroe AS, Friend PJ, et al. The safety and feasibility of extracorporeal high-intensity focused ultrasound (HIFU) for the treatment of liver and kidney tumours in a western population. Br J Cancer 2005; 93: 890–895
  • Wang Y, Wang W, Wang Y, Tang J. Ultrasound-guided high-intensity focused ultrasound treatment for needle-track seeding of hepatocellular carcinoma: Preliminary results. Int J Hyperthermia 2010; 26: 441–447
  • Wang Y, Wang W, Tang J. Ultrasound-guided high intensity focused ultrasound treatment for extra-abdominal desmoid tumours: Preliminary results. Int J Hyperthermia 2011; 27: 648–653
  • Huisman M, van den Bosch MA. MR-guided high-intensity focused ultrasound for noninvasive cancer treatment. Cancer Imaging 2011; 11: S161–166
  • Zhou YF. High intensity focused ultrasound in clinical tumor ablation. World J Clin Oncol 2011; 2: 8–27
  • Chua TC, Thornbury K, Saxena A, Liauw W, Glenn D, Zhao J, et al. Radiofrequency ablation as an adjunct to systemic chemotherapy for colorectal pulmonary metastases. Cancer 2010; 116: 2106–2114
  • Patel PR, Luk A, Durrani A, Dromi S, Cuesta J, Angstadt M, et al. In vitro and in vivo evaluations of increased effective beam width for heat deposition using a split focus high intensity ultrasound (HIFU) transducer. Int J Hyperthermia 2008; 24: 537–549
  • Frenkel V, Li KC. Potential role of pulsed high intensity focused ultrasound in gene therapy. Future Oncol 2006; 2: 111–119
  • Fotopoulou C, Cho CH, Kraetschell R, Gellermann J, Wust P, Lichtenegger W, et al. Regional abdominal hyperthermia combined with systemic chemotherapy for the treatment of patients with ovarian cancer relapse: Results of a pilot study. Int J Hyperthermia 2010; 26: 118–126
  • Issels RD, Lindner LH, Verweij J, Wust P, Reichardt P, Schem BC, et al. Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: A randomised phase 3 multicentre study. Lancet Oncol 2010; 11: 561–570
  • Craciunescu OI, Blackwell KL, Jones EL, Macfall JR, Yu D, Vujaskovic Z, et al. DCE-MRI parameters have potential to predict response of locally advanced breast cancer patients to neoadjuvant chemotherapy and hyperthermia: A pilot study. Int J Hyperthermia 2009; 25: 405–415
  • Kong G, Dewhirst MW. Hyperthermia and liposomes. Int J Hyperthermia 1999; 15: 345–370
  • Song CW. Effect of local hyperthermia on blood flow and microenvironment: A review. Cancer Res 1984; 44: 4721s–4730s
  • Horsman MR, Overgaard J. Can mild hyperthermia improve tumour oxygenation?. Int J Hyperthermia 1997; 13: 141–147
  • Jain RK. Delivery of molecular medicine to solid tumors. Science 1996; 271: 1079–1080
  • Song CW, Park HJ, Lee CK, Griffin R. Implications of increased tumor blood flow and oxygenation caused by mild temperature hyperthermia in tumor treatment. Int J Hyperthermia 2005; 21: 761–767
  • Kong G, Braun RD, Dewhirst MW. Hyperthermia enables tumor-specific nanoparticle delivery: Effect of particle size. Cancer Res 2000; 60: 4440–4445
  • Lefor AT, Makohon S, Ackerman NB. The effects of hyperthermia on vascular permeability in experimental liver metastasis. J Surg Oncol 1985; 28: 297–300
  • Song CW, Kang MS, Rhee JG, Levitt SH. Effect of hyperthermia on vascular function in normal and neoplastic tissues. Ann NY Acad Sci 1980; 335: 35–47
  • Gerlowski LE, Jain RK. Effect of hyperthermia on microvascular permeability to macromolecules in normal and tumor tissues. Int J Microcirc Clin Exp 1985; 4: 363–372
  • Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 2001; 61: 3027–3032
  • Liu P, Zhang A, Xu Y, Xu LX. Study of non-uniform nanoparticle liposome extravasation in tumour. Int J Hyperthermia 2005; 21: 259–270
  • Nishimura Y, Hiraoka M, Jo S, Akuta K, Yukawa Y, Shibamoto Y, et al. Microangiographic and histologic analysis of the effects of hyperthermia on murine tumor vasculature. Int J Radiat Oncol Biol Phys 1988; 15: 411–420
  • Fajardo LF, Schreiber AB, Kelly NI, Hahn GM. Thermal sensitivity of endothelial cells. Radiat Res 1985; 103: 276–285
  • Friedl J, Turner E, Alexander HR, Jr. Augmentation of endothelial cell monolayer permeability by hyperthermia but not tumor necrosis factor: Evidence for disruption of vascular integrity via VE-cadherin down-regulation. Int J Oncol 2003; 23: 611–616
  • Matthew CB, DuBose DA, Sils II, Tartartini KA. Hyperthermia-induced changes in the vascular permeability of rats: A model system to examine therapeutic interventions. J Therm Biol 2000; 25: 381–386
  • de Smet M, Heijman E, Langereis S, Hijnen NM, Grull H. Magnetic resonance imaging of high intensity focused ultrasound mediated drug delivery from temperature-sensitive liposomes: An in vivo proof-of-concept study. J Control Release 2011; 150: 102–110
  • Staruch R, Chopra R, Hynynen K. Localised drug release using MRI-controlled focused ultrasound hyperthermia. Int J Hyperthermia 2011; 27: 156–171
  • Apfel RE. Acoustic cavitation: A possible consequence of biomedical uses of ultrasound. Br J Cancer Suppl 1982; 5: 140–146
  • Wu J, Nyborg WL. Ultrasound, cavitation bubbles and their interaction with cells. Adv Drug Deliv Rev 2008; 60: 1103–1116
  • Krasovitski B, Frenkel V, Shoham S, Kimmel E. Intramembrane cavitation as a unifying mechanism for ultrasound-induced bioeffects. Proc Natl Acad Sci USA 2011; 108: 3258–3263
  • Kinoshita M, McDannold N, Jolesz FA, Hynynen K. Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption. Proc Natl Acad Sci USA 2006; 103: 11719–11723
  • Kinoshita M, McDannold N, Jolesz FA, Hynynen K. Targeted delivery of antibodies through the blood–brain barrier by MRI-guided focused ultrasound. Biochem Biophys Res Commun 2006; 340: 1085–1090
  • Raymond SB, Treat LH, Dewey JD, McDannold NJ, Hynynen K, Bacskai BJ. Ultrasound enhanced delivery of molecular imaging and therapeutic agents in Alzheimer's disease mouse models. PLoS One 2008; 3: e2175
  • Yuh EL, Shulman SG, Mehta SA, Xie J, Chen L, Frenkel V, et al. Delivery of systemic chemotherapeutic agent to tumors by using focused ultrasound: Study in a murine model. Radiology 2005; 234: 431–437
  • Khaibullina A, Jang BS, Sun H, Le N, Yu S, Frenkel V, et al. Pulsed high-intensity focused ultrasound enhances uptake of radiolabeled monoclonal antibody to human epidermoid tumor in nude mice. J Nucl Med 2008; 49: 295–302
  • Huber PE, Mann MJ, Melo LG, Ehsan A, Kong D, Zhang L, et al. Focused ultrasound (HIFU) induces localized enhancement of reporter gene expression in rabbit carotid artery. Gene Ther 2003; 10: 1600–1607
  • Mehier-Humbert S, Yan F, Frinking P, Schneider M, Guy RH, Bettinger T. Ultrasound-mediated gene delivery: Influence of contrast agent on transfection. Bioconjug Chem 2007; 18: 652–662
  • van Wamel A, Kooiman K, Harteveld M, Emmer M, ten Cate FJ, Versluis M, et al. Vibrating microbubbles poking individual cells: Drug transfer into cells via sonoporation. J Control Release 2006; 112: 149–155
  • Schlicher RK, Radhakrishna H, Tolentino TP, Apkarian RP, Zarnitsyn V, Prausnitz MR. Mechanism of intracellular delivery by acoustic cavitation. Ultrasound Med Biol 2006; 32: 915–924
  • Lionetti V, Fittipaldi A, Agostini S, Giacca M, Recchia FA, Picano E. Enhanced caveolae-mediated endocytosis by diagnostic ultrasound in vitro. Ultrasound Med Biol 2009; 35: 136–143
  • Meijering BD, Juffermans LJ, van Wamel A, Henning RH, Zuhorn IS, Emmer M, et al. Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation. Circ Res 2009; 104: 679–687
  • Cruciani G, Molinari AL, Marangolo M, Morelli M, Gnani G, Mazzotti A, et al. Applicability of local hyperthermia as adjuvant to systemic chemotherapy. Tumori 1987; 73: 629–633
  • Issels RD, Lindner LH, Verweij J, Wust P, Reichardt P, Schem BC, et al. Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: A randomised phase 3 multicentre study. Lancet Oncol 2010; 11: 561–570
  • Mace TA, Zhong L, Kokolus KM, Repasky EA. Effector CD8+ T cell IFN-gamma production and cytotoxicity are enhanced by mild hyperthermia. Int J Hyperthermia 2012; 28: 9–18
  • Miller DL, Song J. Tumor growth reduction and DNA transfer by cavitation-enhanced high-intensity focused ultrasound in vivo. Ultrasound Med Biol 2003; 29: 887–893
  • Tschoep-Lechner K, Drexler I, Hammer D, Neumann D, Pohla H, Sutter G, et al. Modified vaccinia virus Ankara delivers a robust surrogate marker for immune monitoring to sarcoma cells even if cells are being exposed to chemotherapy and heat treatment. Int J Hyperthermia 2012; 28: 33–42
  • Pathak A, Patnaik S, Gupta KC. Recent trends in non-viral vector-mediated gene delivery. Biotechnol J 2009; 4: 1559–1572
  • Mir LM, Tounekti O, Orlowski S. Bleomycin: Revival of an old drug. Gen Pharmacol 1996; 27: 745–748
  • Lindenberg M, Kopp S, Dressman JB. Classification of orally administered drugs on the World Health Organization Model list of Essential Medicines according to the biopharmaceutics classification system. Eur J Pharm Biopharm 2004; 58: 265–278
  • Yudina A, de Smet M, Lepetit-Coiffe M, Langereis S, Van Ruijssevelt L, Smirnov P, et al. Ultrasound-mediated intracellular drug delivery using microbubbles and temperature-sensitive liposomes. J Control Release 2011; 155: 442–448
  • Unger EC, Hersh E, Vannan M, Matsunaga TO, McCreery T. Local drug and gene delivery through microbubbles. Prog Cardiovasc Dis 2001; 44: 45–54
  • O'Neill BE, Vo H, Angstadt M, Li KP, Quinn T, Frenkel V. Pulsed high intensity focused ultrasound mediated nanoparticle delivery: Mechanisms and efficacy in murine muscle. Ultrasound Med Biol 2009; 35: 416–424

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