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Triggered Drug Release and Enhanced Drug Transport from Ultrasound-Responsive Nanoparticles

  • James J. Kwan
  • Constantin C. CoussiosEmail author
Chapter

Abstract

Conventional systemic drug therapy across all drug classes does not adequately provide safe and efficacious treatment for a broad range of fatal diseases. To address this challenge, there have been major advances in stimulus-responsive technologies for active drug delivery. Ultrasound-mediated drug therapy in particular has garnered much attention because it is highly accessible, cost effective, drug agnostic, and noninvasive. Broadly speaking, ultrasound is capable of providing thermal and mechanical effects. As a result, ultrasound-responsive nanoparticles have been developed to react to specific ultrasound stimuli. In this chapter, we discuss the current challenges that face drug delivery to cancer, cardiovascular, and neurological disorders. We then explore the different means by which ultrasound enables drug release, drug transport, and sonoporation of cell membranes from ultrasound-responsive nanoparticles.

Keywords

Active drug delivery Ultrasound Nanoparticles Acoustic cavitation 

References

  1. 1.
    Krall N, Pretto F, Decurtins W, Bernardes GJL, Supuran CT, Neri D. A small-molecule drug conjugate for the treatment of carbonic anhydrase IX expressing tumors. Angew Chem Int Ed. 2014;53(16):4231–5.CrossRefGoogle Scholar
  2. 2.
    Hay M, Thomas DW, Craighead JL, Economides C, Rosenthal J. Clinical development success rates for investigational drugs. Nat Biotechnol. 2014;32(1):40–51.PubMedCrossRefGoogle Scholar
  3. 3.
    O'Reilly LP, Luke CJ, Perlmutter DH, Silverman GA, Pak SC. C. elegans in high-throughput drug discovery. Adv Drug Deliver Rev. 2014;69:247–53.CrossRefGoogle Scholar
  4. 4.
    Lipshultz. Long-term cardiovascular toxicity in children, adolescents, and young adults who receive cancer therapy: pathophysiology, course, monitoring, management, prevention, and research directions: a scientific statement from the American Heart Association (vol 128, p. 1927, 2013). Circulation. 2013;128(19):E394–E.Google Scholar
  5. 5.
    Kramer AH, Jenne CN, Zygun DA, Roberts DJ, Hill MD, Holodinsky JK, et al. Intraventricular fibrinolysis with tissue plasminogen activator is associated with transient cerebrospinal fluid inflammation: a randomized controlled trial. J Cerebr Blood F Met. 2015;35(8):1241–8.CrossRefGoogle Scholar
  6. 6.
    Brott T, Broderick J, Kothari R, ODonoghue M, Barsan W, Tomsick T, et al. Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke. Stroke. 1997;28(11):2109–18.CrossRefGoogle Scholar
  7. 7.
    Goldstein LB. Acute ischemic stroke treatment in 2007. Circulation. 2007;116(13):1504–14.PubMedCrossRefGoogle Scholar
  8. 8.
    Mitragotri S, Burke PA, Langer R. Overcoming the challenges in administering biopharmaceuticals: formulation and delivery strategies. Nat Rev Drug Discov. 2014;13(9):655–72.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Minchinton AI, Tannock IF. Drug penetration in solid tumours. Nat Rev Cancer. 2006;6(8):583–92.PubMedCrossRefGoogle Scholar
  10. 10.
    Primeau AJ, Rendon A, Hedley D, Lilge L, Tannock IF. The distribution of the anticancer drug doxorubicin in relation to blood vessels in solid tumors. Clin Cancer Res. 2005;11(24):8782–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Baker JHE, Lindquist KE, Huxham L, Kyle AH, Sy JT, Minchinton AI. Direct visualization of heterogeneous extravascular distribution of trastuzumab in human epidermal growth factor receptor type 2 overexpressing xenografts. Clin Cancer Res. 2008;14(7):2171–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Tailor TD, Hanna G, Yarmolenko PS, Dreher MR, Betof AS, Nixon AB, et al. Effect of pazopanib on tumor microenvironment and liposome delivery. Mol Cancer Ther. 2010;9(6):1798–808.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7(1):41–53.PubMedCrossRefGoogle Scholar
  14. 14.
    Carlisle R, Coussios CC. Mechanical approaches to oncological drug delivery. Ther Deliv. 2013;4(10):1213–5. Epub 2013/10/15.PubMedCrossRefGoogle Scholar
  15. 15.
    Crown J, O'Leary M. The taxanes: an update. Lancet. 2000;355(9210):1176–8.PubMedCrossRefGoogle Scholar
  16. 16.
    Hurley LH. DNA and its associated processes as targets for cancer therapy. Nat Rev Cancer. 2002;2(3):188–200.PubMedCrossRefGoogle Scholar
  17. 17.
    Lee K, Qian DZ, Rey S, Wei H, Liu JO, Semenza GL. Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells. Proc Natl Acad Sci U S A. 2009;106(7):2353–8.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Karahoca M, Momparler RL. Pharmacokinetic and pharmacodynamic analysis of 5-aza-2'-deoxycytidine (decitabine) in the design of its dose-schedule for cancer therapy. Clin Epigenetics. 2013;5.Google Scholar
  19. 19.
    Chu MY, Fischer GA. A proposed mechanism of action of 1-beta-D-arabinofuranosyl-cytosine as an inhibitor of growth of leukemic cells. Biochem Pharmacol. 1962;11:423.PubMedCrossRefGoogle Scholar
  20. 20.
    Hans R, Andtbacka I, Collichio FA, Amatruda T, Senzer NN, Chesney J, et al. OPTiM: a randomized phase III trial of talimogene laherparepvec (T-VEC) versus subcutaneous (SC) granulocyte-macrophage colony-stimulating factor (GM-CSF) for the treatment (tx) of unresected stage IIIB/C and IV melanoma. J Clin Oncol. 2013;31(18).Google Scholar
  21. 21.
    Folkman J. Antiangiogenesis in cancer therapy—endostatin and its mechanisms of action. Exp Cell Res. 2006;312(5):594–607.PubMedCrossRefGoogle Scholar
  22. 22.
    Salama AKS, Hodi FS. Cytotoxic T-lymphocyte-associated antigen-4. Clin Cancer Res. 2011;17(14):4622–8.PubMedCrossRefGoogle Scholar
  23. 23.
    Brahmer JR, Tykodi SS, Chow LQM, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 2012;366(26):2455–65.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Topalian SL, Drake CG, Pardoll DM. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr Opin Immunol. 2012;24(2):207–12.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Wardlaw JM, Murray V, Berge E, del Zoppo G, Sandercock P, Lindley RL, et al. Recombinant tissue plasminogen activator for acute ischaemic stroke: an updated systematic review and meta-analysis. Lancet. 2012;379(9834):2364–72.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Williams JM, Navin TJ, Levi CR, Jude M. Recombinant tissue plasminogen activator (rt-PA) utilisation by rural clinicians in acute ischaemic stroke: an audit of current practice and clinical outcomes. Int J Stroke. 2012;7:42–3.Google Scholar
  27. 27.
    Lapchak PA, Chapman DF, Zivin JA. Metalloproteinase inhibition reduces thrombolytic (tissue plasminogen activator)-induced hemorrhage after thromboembolic stroke. Stroke. 2000;31(12):3034–9.PubMedCrossRefGoogle Scholar
  28. 28.
    Mangialasche F, Solomon A, Winblad B, Mecocci P, Kivipelto M. Alzheimer’s disease: clinical trials and drug development. Lancet Neurol. 2010;9(7):702–16.PubMedCrossRefGoogle Scholar
  29. 29.
    Olanow CW, Rascol O, Hauser R, Feigin PD, Jankovic J, Lang A, et al. A double-blind, delayed-start trial of rasagiline in Parkinson’s disease. N Engl J Med. 2009;361(13):1268–78.PubMedCrossRefGoogle Scholar
  30. 30.
    Schapira AHV, Bezard E, Brotchie J, Calon F, Collingridge GL, Ferger B, et al. Novel pharmacological targets for the treatment of Parkinson’s disease. Nat Rev Drug Discov. 2006;5(10):845–54.PubMedCrossRefGoogle Scholar
  31. 31.
    Goetz CG, Poewe W, Rascol O, Sampaio C. Evidence-based medical review update: pharmacological and surgical treatments of Parkinson’s disease: 2001 to 2004. Mov Disord. 2005;20(5):523–39.PubMedCrossRefGoogle Scholar
  32. 32.
    Kaplitt MG, Feigin A, Tang C, Fitzsimons HL, Mattis P, Lawlor PA, et al. Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson’s disease: an open label, phase I trial. Lancet. 2007;369(9579):2097–105.PubMedCrossRefGoogle Scholar
  33. 33.
    Landreth G, Jiang QG, Mandrekar S, Heneka M. PPAR gamma agonists as therapeutics for the treatment of Alzheimer’s disease. Neurotherapeutics. 2008;5(3):481–9.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Cobbold RS. Foundations of biomedical ultrasound. Oxford University Press on Demand; 2007.Google Scholar
  35. 35.
    Ter Haar G, Coussios C. High intensity focused ultrasound: physical principles and devices. Int J Hyperther. 2007;23(2):89–104.CrossRefGoogle Scholar
  36. 36.
    Szabo TL. Diagnostic ultrasound imaging: inside out. Boston: Academic Press; 2004.Google Scholar
  37. 37.
    McDannold N, Clement G, Black P, Jolesz F, Hynynen K. Transcranial MRI-guided focused ultrasound surgery of brain tumors: initial findings in three patients. Neurosurgery. 2010;66(2):323.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Salomir R, Vimeux FC, de Zwart JA, Grenier N, Moonen CTW. Hyperthermia by MR-guided focused ultrasound: accurate temperature control based on fast MRI and a physical model of local energy deposition and heat conduction. Magnet Reson Med. 2000;43(3):342–7.CrossRefGoogle Scholar
  39. 39.
    Rieke V, Pauly KB. MR thermometry. J Magn Reson Imaging. 2008;27(2):376–90.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Bradley Jr WG. MR-guided focused ultrasound: a potentially disruptive technology. J Am Coll Radiol. 2009;6(7):510–3. Epub 2009/06/30.PubMedCrossRefGoogle Scholar
  41. 41.
    Sarvazyan AP, Rudenko OV, Nyborg WL. Biomedical applications of radiation force of ultrasound: historical roots and physical basis. Ultrasound Med Biol. 2010;36(9):1379–94. Epub 2010/08/31.PubMedCrossRefGoogle Scholar
  42. 42.
    Leighton T. The acoustic bubble. London: Academic Press; 2012.Google Scholar
  43. 43.
    Maxwell AD, Cain CA, Hall TL, Fowlkes JB, Xu Z. Probability of cavitation for single ultrasound pulses applied to tissues and tissue-mimicking materials. Ultrasound Med Biol. 2013;39(3):449–65. Epub 2013/02/06.PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Stride EP, Coussios CC. Cavitation and contrast: the use of bubbles in ultrasound imaging and therapy. Proc Inst Mech Eng H. 2010;224(H2):171–91.PubMedCrossRefGoogle Scholar
  45. 45.
    Kwan JJ, Myers R, Coviello CM, Graham SM, Shah AR, Stride E, et al. Ultrasound-propelled nanocups for drug delivery. Small. 2015. Epub 2015/08/25.Google Scholar
  46. 46.
    Arvanitis CD, Bazan-Peregrino M, Rifai B, Seymour LW, Coussios CC. Cavitation-enhanced extravasation for drug delivery. Ultrasound Med Biol. 2011;37(11):1838–52. Epub 2011/10/04.PubMedCrossRefGoogle Scholar
  47. 47.
    Ammi AY, Cleveland RO, Mamou J, Wang GI, Bridal SL, O'Brien Jr WD. Ultrasonic contrast agent shell rupture detected by inertial cavitation and rebound signals. IEEE Trans Ultrason Ferroelectr Freq Control. 2006;53(1):126–36. Epub 2006/02/14.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Roberts WW, Hall TL, Ives K, Wolf Jr JS, Fowlkes JB, Cain CA. Pulsed cavitational ultrasound: a noninvasive technology for controlled tissue ablation (histotripsy) in the rabbit kidney. J Urol. 2006;175(2):734–8. Epub 2006/01/13.PubMedCrossRefGoogle Scholar
  49. 49.
    Wang YN, Khokhlova T, Bailey M, Hwang JH, Khokhlova V. Histological and biochemical analysis of mechanical and thermal bioeffects in boiling histotripsy lesions induced by high intensity focused ultrasound. Ultrasound Med Biol. 2013;39(3):424–38. Epub 2013/01/15.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Schade GR, Keller J, Ives K, Cheng X, Rosol TJ, Keller E, et al. Histotripsy focal ablation of implanted prostate tumor in an ACE-1 canine cancer model. J Urol. 2012;188(5):1957–64. Epub 2012/09/25.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Bloch SH, Short RE, Ferrara KW, Wisner ER. The effect of size on the acoustic response of polymer-shelled contrast agents. Ultrasound Med Biol. 2005;31(3):439–44. Epub 2005/03/08.PubMedCrossRefGoogle Scholar
  52. 52.
    Dicker S, Mleczko M, Siepmann M, Wallace N, Sunny Y, Bawiec CR, et al. Influence of shell composition on the resonance frequency of microbubble contrast agents. Ultrasound Med Biol. 2013;39(7):1292–302. Epub 2013/05/21.PubMedCrossRefGoogle Scholar
  53. 53.
    Collis J, Manasseh R, Liovic P, Tho P, Ooi A, Petkovic-Duran K, et al. Cavitation microstreaming and stress fields created by microbubbles. Ultrasonics. 2010;50(2):273–9. Epub 2009/11/10.PubMedCrossRefGoogle Scholar
  54. 54.
    Liu X, Wu J. Acoustic microstreaming around an isolated encapsulated microbubble. J Acoust Soc Am. 2009;125(3):1319–30. Epub 2009/03/12.PubMedCrossRefGoogle Scholar
  55. 55.
    Won JM, Lee JH, Lee KH, Rhee K, Chung SK. Propulsion of water-floating objects by acoustically oscillating microbubbles. Int J Precis Eng Man. 2011;12(3):577–80.CrossRefGoogle Scholar
  56. 56.
    Samiotaki G, Vlachos F, Tung YS, Konofagou EE. A quantitative pressure and microbubble-size dependence study of focused ultrasound-induced blood-brain barrier opening reversibility in vivo using MRI. Magnet Reson Med. 2012;67(3):769–77.CrossRefGoogle Scholar
  57. 57.
    Qiu YY, Zhang CB, Tu J, Zhang D. Microbubble-induced sonoporation involved in ultrasound-mediated DNA transfection in vitro at low acoustic pressures. J Biomech. 2012;45(8):1339–45.PubMedCrossRefGoogle Scholar
  58. 58.
    Juffermans LJM, van Dijk A, Jongenelen CAM, Drukarch B, Reijerkerk A, de Vries HE, et al. Ultrasound and microbubble-induced intra- and intercellular bioeffects in primary endothelial cells. Ultrasound Med Biol. 2009;35(11):1917–27.PubMedCrossRefGoogle Scholar
  59. 59.
    VanBavel E. Effects of shear stress on endothelial cells: possible relevance for ultrasound applications. Prog Biophys Mol Bio. 2007;93(1-3):374–83.CrossRefGoogle Scholar
  60. 60.
    Zhong P, Cioanta I, Cocks FH, Preminger GM. Inertial cavitation and associated acoustic emission produced during electrohydraulic shock wave lithotripsy. J Acoust Soc Am. 1997;101(5):2940–50.PubMedCrossRefGoogle Scholar
  61. 61.
    Salgaonkar VA, Datta S, Holland CK, Mast TD. Passive cavitation imaging with ultrasound arrays. J Acoust Soc Am. 2009;126(6):3071–83.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Farny CH, Holt RG, Roy RA. Temporal and spatial detection of Hifu-induced inertial and hot-vapor cavitation with a diagnostic ultrasound system. Ultrasound Med Biol. 2009;35(4):603–15.PubMedCrossRefGoogle Scholar
  63. 63.
    Gyongy M, Coussios CC. Passive spatial mapping of inertial cavitation during HIFU exposure. IEEE Trans Biomed Eng. 2010;57(1):48–56.PubMedCrossRefGoogle Scholar
  64. 64.
    Davis ME, Chen Z, Shin DM. Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov. 2008;7(9):771–82.PubMedCrossRefGoogle Scholar
  65. 65.
    Peer D, Karp JM, Hong S, FaroKHzad OC, Margalit R, Langer R. Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol. 2007;2(12):751–60.PubMedCrossRefGoogle Scholar
  66. 66.
    Malam Y, Loizidou M, Seifalian AM. Liposomes and nanoparticles: nanosized vehicles for drug delivery in cancer. Trends Pharmacol Sci. 2009;30(11):592–9.PubMedCrossRefGoogle Scholar
  67. 67.
    Allen TM, Cullis PR. Drug delivery systems: entering the mainstream. Science. 2004;303(5665):1818–22.PubMedCrossRefGoogle Scholar
  68. 68.
    Torchilin VP. Recent advances with liposomes as pharmaceutical carriers. Nat Rev Drug Discov. 2005;4(2):145–60.PubMedCrossRefGoogle Scholar
  69. 69.
    Andresen TL, Jensen SS, Jorgensen K. Advanced strategies in liposomal cancer therapy: problems and prospects of active and tumor specific drug release. Prog Lipid Res. 2005;44(1):68–97.PubMedCrossRefGoogle Scholar
  70. 70.
    Yatvin MB, Weinstein JN, Dennis WH, Blumenthal R. Design of liposomes for enhanced local release of drugs by hyperthermia. Science. 1978;202(4374):1290–3.PubMedCrossRefGoogle Scholar
  71. 71.
    Weinstein JN, Magin RL, Yatvin MB, Zaharko DS. Liposomes and local hyperthermia—selective delivery of methotrexate to heated tumors. Science. 1979;204(4389):188–91.PubMedCrossRefGoogle Scholar
  72. 72.
    Anyarambhatla GR, Needham D. Enhancement of the phase transition permeability of DPPC liposomes by incorporation of MPPC: a new temperature-sensitive liposome for use with mild hyperthermia. J Liposome Res. 1999;9(4):491–506.CrossRefGoogle Scholar
  73. 73.
    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(5):1197–201.PubMedGoogle Scholar
  74. 74.
    Ponce AM, Vujaskovic Z, Yuan F, Needham D, Dewhirst MW. Hyperthermia mediated liposomal drug delivery. Int J Hyperther. 2006;22(3):205–13.CrossRefGoogle Scholar
  75. 75.
    Needham D, Dewhirst MW. The development and testing of a new temperature-sensitive drug delivery system for the treatment of solid tumors. Adv Drug Deliver Rev. 2001;53(3):285–305.CrossRefGoogle Scholar
  76. 76.
    Gaber MH, Hong KL, Huang SK, Papahadjopoulos D. Thermosensitive sterically stabilized liposomes—formulation and in-vitro studies on mechanism of doxorubicin release by bovine serum and human plasma. Pharm Res. 1995;12(10):1407–16.PubMedCrossRefGoogle Scholar
  77. 77.
    Gaber MH, Wu NZ, Hong KL, Huang SK, Dewhirst MW, Papahadjopoulos D. Thermosensitive liposomes: extravasation and release of contents in tumor microvascular networks. Int J Radiat Oncol. 1996;36(5):1177–87.CrossRefGoogle Scholar
  78. 78.
    Park SM, Kim MS, Park SJ, Park ES, Choi KS, Kim YS, et al. Novel temperature-triggered liposome with high stability: formulation, in vitro evaluation, and in vivo study combined with high-intensity focused ultrasound (HIFU). J Control Release. 2013;170(3):373–9.PubMedCrossRefGoogle Scholar
  79. 79.
    Lindner LH, Eichhorn ME, Eibl H, Teichert N, Schmitt-Sody M, Issels RD, et al. Novel temperature-sensitive liposomes with prolonged circulation time. Clin Cancer Res. 2004;10(6):2168–78.PubMedCrossRefGoogle Scholar
  80. 80.
    Hossann M, Wiggenhorn M, Schwerdt A, Wachholz K, Teichert N, Eibl H, et al. In vitro stability and content release properties of phosphatidylglyceroglycerol containing thermosensitive liposomes. Biochim Biophys Acta. 2007;1768(10):2491–9.PubMedCrossRefGoogle Scholar
  81. 81.
    Mylonopoulou E, Bazan‐Peregrino M, Arvanitis CD, Coussios CC. Exploitation of cavitation‐enhanced heating for release of doxorubicin from thermosensitve liposomes by therapeutic ultrasound. J Acoust Soc Am. 2010;128(4):2418.CrossRefGoogle Scholar
  82. 82.
    Peleg-Shulman T, Gibson D, Cohen R, Abra R, Barenholz Y. Characterization of sterically stabilized cisplatin liposomes by nuclear magnetic resonance. Biochim Biophys Acta. 2001;1510(1–2):278–91.PubMedCrossRefGoogle Scholar
  83. 83.
    Torchilinl V, Papisov M. Why do polyethylene glycol-coated liposomes circulate so long?: Molecular mechanism of liposome steric protection with polyethylene glycol: Role of polymer chain flexibility. J Liposome Res. 1994;4(1):725–39.CrossRefGoogle Scholar
  84. 84.
    Schroeder A, Sigal A, Turjeman K, Barenholz Y. Using PEGylated nano-liposomes to target tissue invaded by a foreign body. J Drug Target. 2008;16(7-8):591–5.PubMedCrossRefGoogle Scholar
  85. 85.
    Dvorak HF, Nagy JA, Dvorak JT, Dvorak AM. Identification and characterization of the blood-vessels of solid tumors that are leaky to circulating macromolecules. Am J Pathol. 1988;133(1):95–109.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Schroeder A, Honen R, Turjeman K, Gabizon A, Kost J, Barenholz Y. Ultrasound triggered release of cisplatin from liposomes in murine tumors. J Control Release. 2009;137(1):63–8.PubMedCrossRefGoogle Scholar
  87. 87.
    Al Sabbagh C, Tsapis N, Novell A, Calleja-Gonzalez P, Escoffre JM, Bouakaz A, et al. Formulation and pharmacokinetics of thermosensitive stealth(A (R)) liposomes encapsulating 5-fluorouracil. Pharm Res. 2015;32(5):1585–603.PubMedCrossRefGoogle Scholar
  88. 88.
    Han HD, Shin BC, Choi HS. Doxorubicin-encapsulated thermosensitive liposomes modified with poly(N-isopropylacrylamide-co-acrylamide): drug release behavior and stability in the presence of serum. Eur J Pharm Biopharm. 2006;62(1):110–6.PubMedCrossRefGoogle Scholar
  89. 89.
    Han HD, Choi MS, Hwang T, Song CK, Seong H, Kim TW, et al. Hyperthermia-induced antitumor activity of thermosensitive polymer modified temperature-sensitive liposomes. J Pharm Sci. 2006;95(9):1909–17.PubMedCrossRefGoogle Scholar
  90. 90.
    Ta T, Convertine AJ, Reyes CR, Stayton PS, Porter TM. Thermosensitive liposomes modified with poly(N-isopropylacrylamide-co-propylacrylic acid) copolymers for triggered release of doxorubicin. Biomacromolecules. 2010;11(8):1915–20.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Chen KJ, Liang HF, Chen HL, Wang YC, Cheng PY, Liu HL, et al. A thermoresponsive bubble-generating liposomal system for triggering localized extracellular drug delivery. ACS Nano. 2013;7(1):438–46.PubMedCrossRefGoogle Scholar
  92. 92.
    Chen KJ, Chaung EY, Wey SP, Lin KJ, Cheng F, Lin CC, et al. Hyperthermia-mediated local drug delivery by a bubble-generating liposomal system for tumor-specific chemotherapy. ACS Nano. 2014;8(5):5105–15.PubMedCrossRefGoogle Scholar
  93. 93.
    Sheeran PS, Wong VP, Luois S, McFarland RJ, Ross WD, Feingold S, et al. Decafluorobutane as a phase-change contrast agent for low-energy extravascular ultrasonic imaging. Ultrasound Med Biol. 2011;37(9):1518–30.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Sheeran PS, Luois SH, Mullin LB, Matsunaga TO, Dayton PA. Design of ultrasonically-activatable nanoparticles using low boiling point perfluorocarbons. Biomaterials. 2012;33(11):3262–9.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Wang CH, Kang ST, Lee YH, Luo YL, Huang YF, Yeh CK. Aptamer-conjugated and drug-loaded acoustic droplets for ultrasound theranosis. Biomaterials. 2012;33(6):1939–47.PubMedCrossRefGoogle Scholar
  96. 96.
    Rapoport N. Phase-shift, stimuli-responsive perfluorocarbon nanodroplets for drug delivery to cancer. Wires Nanomed Nanobi. 2012;4(5):492–510.CrossRefGoogle Scholar
  97. 97.
    Rapoport N, Nam KH, Gupta R, Gao ZG, Mohan P, Payne A, et al. Ultrasound-mediated tumor imaging and nanotherapy using drug loaded, block copolymer stabilized perfluorocarbon nanoemulsions. J Control Release. 2011;153(1):4–15.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Marsh D, Seddon JM. Gel-to-inverted hexagonal (L-Beta-Hii) phase-transitions in phosphatidylethanolamines and fatty-acid phosphatidylcholine mixtures, demonstrated by P-31-Nmr spectroscopy and X-ray-diffraction. Biochim Biophys Acta. 1982;690(1):117–23.PubMedCrossRefGoogle Scholar
  99. 99.
    Evjen TJ, Nilssen EA, Rognvaldsson S, Brandl M, Fossheim SL. Distearoylphosphatidylethanolamine-based liposomes for ultrasound-mediated drug delivery. Eur J Pharm Biopharm. 2010;75(3):327–33.PubMedCrossRefGoogle Scholar
  100. 100.
    Graham SM, Carlisle R, Choi JJ, Stevenson M, Shah AR, Myers RS, et al. Inertial cavitation to non-invasively trigger and monitor intratumoral release of drug from intravenously delivered liposomes. J Control Release. 2014;178:101–7.PubMedCrossRefGoogle Scholar
  101. 101.
    Graham S. Ultrasound-triggered drug release from liposomes using nanoscale cavitation nuclei. Oxford: University of Oxford; 2014.Google Scholar
  102. 102.
    Suzaki R, Takizawa T, Negishi Y, Utoguchi N, Sawamura K, Tanaka K, et al. Tumor specific ultrasound enhanced gene transfer in vivo with novel liposomal bubbles. J Control Release. 2008;125(2):137–44.CrossRefGoogle Scholar
  103. 103.
    Suzuki R, Oda Y, Utoguchi N, Maruyama K. Progress in the development of ultrasound-mediated gene delivery systems utilizing nano- and microbubbles. J Control Release. 2011;149(1):36–41.PubMedCrossRefGoogle Scholar
  104. 104.
    Shaw GJ, Meunier JM, Huang SL, Lindsell CJ, McPherson DD, Holland CK. Ultrasound-enhanced thrombolysis with tPA-loaded echogenic liposomes. Thromb Res. 2009;124(3):306–10.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Tiukinhoy-Laing SD, Buchanan K, Parikh D, Huang SL, MacDonald RC, McPherson DD, et al. Fibrin targeting of tissue plasminogen activator-loaded echogenic liposomes. J Drug Target. 2007;15(2):109–14.PubMedCrossRefGoogle Scholar
  106. 106.
    Tiukinhoy-Laing SD, Huang SL, Klegerman M, Holland CK, McPherson DD. Ultrasound-facilitated thrombolysis using tissue-plasminogen activator-loaded echogenic liposomes. Thromb Res. 2007;119(6):777–84.PubMedCrossRefGoogle Scholar
  107. 107.
    Smith DAB, Vaidya SS, Kopechek JA, Huang SL, Klegerman ME, Mcpherson DD, et al. Ultrasound-triggered release of recombinant tissue-type plasminogen activator from echogenic liposomes. Ultrasound Med Biol. 2010;36(1):145–57.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Kopechek JA, Abruzzo TM, Wang B, Chrzanowski SM, Smith DAB, Kee PH, et al. Ultrasound-mediated release of hydrophilic and lipophilic agents from echogenic liposomes. J Ultras Med. 2008;27(11):1597–606.Google Scholar
  109. 109.
    Yin TH, Wang P, Li JG, Zheng RQ, Zheng BW, Cheng D, et al. Ultrasound-sensitive siRNA-loaded nanobubbles formed by hetero-assembly of polymeric micelles and liposomes and their therapeutic effect in gliomas. Biomaterials. 2013;34(18):4532–43.PubMedCrossRefGoogle Scholar
  110. 110.
    Ning SC, Macleod K, Abra RM, Huang AH, Hahn GM. Hyperthermia induces doxorubicin release from long-circulating liposomes and enhances their antitumor efficacy. Int J Radiat Oncol. 1994;29(4):827–34.CrossRefGoogle Scholar
  111. 111.
    Kinuya S, Yokoyama K, Hiramatsu T, Tega H, Tanaka K, Konishi S, et al. Combination radioimmunotherapy with local hyperthermia: increased delivery of radioimmunoconjugate by vascular effect and its retention by increased antigen expression in colon cancer xenografts. Cancer Lett. 1999;140(1–2):209–18.PubMedCrossRefGoogle Scholar
  112. 112.
    Cope DA, Dewhirst MW, Friedman HS, Bigner DD, Zalutsky MR. Enhanced delivery of a monoclonal-antibody F(Ab')2 fragment to subcutaneous human glioma xenografts using local hyperthermia. Cancer Res. 1990;50(6):1803–9.PubMedGoogle Scholar
  113. 113.
    Jang SH, Wientjes MG, Lu D, Au JLS. Drug delivery and transport to solid tumors. Pharm Res. 2003;20(9):1337–50.PubMedCrossRefGoogle Scholar
  114. 114.
    Vykhodtseva NI, Hynynen K, Damianou C. Histologic effects of high-intensity pulsed ultrasound exposure with subharmonic emission in rabbit brain in-vivo. Ultrasound Med Biol. 1995;21(7):969–79.PubMedCrossRefGoogle Scholar
  115. 115.
    Mesiwala AH, Farrell L, Wenzel HJ, Silbergeld DL, Crum LA, Winn HR, et al. High-intensity focused ultrasound selectively disrupts the blood-brain barrier in vivo. Ultrasound Med Biol. 2002;28(3):389–400.PubMedCrossRefGoogle Scholar
  116. 116.
    Cho CW, Liu Y, Cobb WN, Henthorn TK, Lillehei K, Christians U, et al. Ultrasound-induced mild hyperthermia as a novel approach to increase drug uptake in brain microvessel endothelial cells. Pharm Res. 2002;19(8):1123–9.PubMedCrossRefGoogle Scholar
  117. 117.
    Chen CC, Sheeran PS, Wu SY, Olumolade OO, Dayton PA, Konofagou EE. Targeted drug delivery with focused ultrasound-induced blood-brain barrier opening using acoustically-activated nanodroplets. J Control Release. 2013;172(3):795–804.PubMedCrossRefGoogle Scholar
  118. 118.
    Chen H, Kreider W, Brayman AA, Bailey MR, Matula TJ. Blood vessel deformations on microsecond time scales by ultrasonic cavitation. Phys Rev Lett. 2011;106(3):034301. Epub 2011/03/17.PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Borkent BM, Gekle S, Prosperetti A, Lohse D. Nucleation threshold and deactivation mechanisms of nanoscopic cavitation nuclei. Phys Fluids. 2009;21(10).Google Scholar
  120. 120.
    Kwan JJ, Graham S, Myers R, Carlisle R, Stride E, Coussios CC. Ultrasound-induced inertial cavitation from gas-stabilizing nanoparticles. Phys Rev E Stat Nonlin Soft Matter Phys. 2015;92(2–1):023019. Epub 2015/09/19.Google Scholar
  121. 121.
    Chen Y, Yin Q, Ji XF, Zhang SJ, Chen HR, Zheng YY, et al. Manganese oxide-based multifunctionalized mesoporous silica nanoparticles for pH-responsive MRI, ultrasonography and circumvention of MDR in cancer cells. Biomaterials. 2012;33(29):7126–37.PubMedCrossRefGoogle Scholar
  122. 122.
    Liang HD, Tang J, Halliwell M. Sonoporation, drug delivery, and gene therapy. Proc Inst Mech Eng H J Eng Med. 2010;224(2):343–61. Epub 2010/03/31.CrossRefGoogle Scholar
  123. 123.
    Delalande A, Kotopoulis S, Postema M, Midoux P, Pichon C. Sonoporation: mechanistic insights and ongoing challenges for gene transfer. Gene. 2013;525(2):191–9. Epub 2013/04/10.PubMedCrossRefGoogle Scholar
  124. 124.
    Nyborg WL. Ultrasonic microstreaming and related phenomena. Br J Cancer Suppl. 1982;5:156–60. Epub 1982/03/01.PubMedPubMedCentralGoogle Scholar
  125. 125.
    Brujan EA, Ikeda T, Matsumoto Y. Jet formation and shock wave emission during collapse of ultrasound-induced cavitation bubbles and their role in the therapeutic applications of high-intensity focused ultrasound. Phys Med Biol. 2005;50(20):4797–809.PubMedCrossRefGoogle Scholar
  126. 126.
    Prentice P, Cuschierp A, Dholakia K, Prausnitz M, Campbell P. Membrane disruption by optically controlled microbubble cavitation. Nat Phys. 2005;1(2):107–10.CrossRefGoogle Scholar
  127. 127.
    Hu YX, Wan JMF, Yu ACH. Membrane perforation and recovery dynamics in microbubble-mediated sonoporation. Ultrasound Med Biol. 2013;39(12):2393–405.PubMedCrossRefGoogle Scholar
  128. 128.
    Burgess MT, Porter TM. Acoustic cavitation-mediated delivery of small interfering ribonucleic acids with phase-shift nano-emulsions. Ultrasound Med Biol. 2015;41(8):2191–201. Epub 2015/05/17.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Gao D, Xu M, Cao Z, Gao J, Chen Y, Li Y, et al. Ultrasound-triggered phase-transition cationic nanodroplets for enhanced gene delivery. ACS Appl Mater Interfaces. 2015;7(24):13524–37. Epub 2015/05/29.PubMedCrossRefGoogle Scholar
  130. 130.
    Zintchenko A, Ogris M, Wagner E. Temperature dependent gene expression induced by PNIPAM-based copolymers: potential of hyperthermia in gene transfer. Bioconjug Chem. 2006;17(3):766–72. Epub 2006/05/18.PubMedCrossRefGoogle Scholar
  131. 131.
    Krupka TM, Solorio L, Wilson RE, Wu HP, Azar N, Exner AA. Formulation and characterization of echogenic lipid-pluronic nanobubbles. Mol Pharm. 2010;7(1):49–59.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Wang Y, Li X, Zhou Y, Huang PY, Xu YH. Preparation of nanobubbles for ultrasound imaging and intracellular drug delivery. Int J Pharm. 2010;384(1-2):148–53.PubMedCrossRefGoogle Scholar
  133. 133.
    Nguyen AT, Wrenn SP. Acoustically active liposome-nanobubble complexes for enhanced ultrasonic imaging and ultrasound-triggered drug delivery. Wires Nanomed Nanobi. 2014;6(3):316–25.CrossRefGoogle Scholar
  134. 134.
    Suzuki R, Takizawa T, Negishi Y, Hagisawa K, Tanaka K, Sawamura K, et al. Gene delivery by combination of novel liposomal bubbles with perfluoropropane and ultrasound. J Control Release. 2007;117(1):130–6.PubMedCrossRefGoogle Scholar
  135. 135.
    Suzuki R, Namai E, Oda Y, Nishiie N, Otake S, Koshima R, et al. Cancer gene therapy by IL-12 gene delivery using liposomal bubbles and tumoral ultrasound exposure. J Control Release. 2010;142(2):245–50.PubMedCrossRefGoogle Scholar
  136. 136.
    Negishi Y, Endo Y, Fukuyama T, Suzuki R, Takizawa T, Omata D, et al. Delivery of siRNA into the cytoplasm by liposomal bubbles and ultrasound. J Control Release. 2008;132(2):124–30.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Institute of Biomedical Engineering, Department of Engineering ScienceUniversity of OxfordOxfordUK

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