Sonosensitive theranostic liposomes for preclinical in vivo MRI-guided visualization of doxorubicin release stimulated by pulsed low intensity non-focused ultrasound

Journal of Controlled Release

Volumn 202, Issue , 2015, Pages 21-30

  Rizzitelli, S ^a   Giustetto, P ^a   Cutrin, J C ^a   Delli Castelli, D ^a   Boffa, C ^a   Ruzza, M ^a   Menchise, V ^a   Molinari, F ^b   Aime, S ^a   Terreno, E ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b POLITECNICO DI TORINO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOTHERAPY; DRUG PRODUCTS; FLUORESCENCE MICROSCOPY; MEDICAL NANOTECHNOLOGY; TUMORS; ULTRASONIC APPLICATIONS;

ANTITUMOR DRUGS; FOCUSED ULTRASOUND; IMAGING AGENT; MRI CONTRASTS; THERANOSTIC AGENTS; THERAPEUTIC BENEFITS; THERAPEUTIC OUTCOMES; TRANSLATABILITY;

LIPOSOMES;

DOXORUBICIN; GADOTERIDOL; LIPOSOME; ANTINEOPLASTIC ANTIBIOTIC; CONTRAST MEDIUM; GADOLINIUM; HETEROCYCLIC COMPOUND; ORGANOMETALLIC COMPOUND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CELL; CONFOCAL MICROSCOPY; CONTRAST ENHANCEMENT; CONTRAST TO NOISE RATIO; CONTROLLED STUDY; DRUG RELEASE; EX VIVO STUDY; FEMALE; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; IN VIVO STUDY; LIPOSOMAL DELIVERY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PULSED LOW INTENSITY NON FOCUSED ULTRASOUND; ULTRASOUND; ANIMAL; BAGG ALBINO MOUSE; CHEMISTRY; DRUG EFFECTS; ECHOGRAPHY; MAMMARY NEOPLASMS, EXPERIMENTAL; METABOLISM; PATHOLOGY; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; CELL LINE, TUMOR; CONTRAST MEDIA; DOXORUBICIN; FEMALE; GADOLINIUM; HETEROCYCLIC COMPOUNDS; LIPOSOMES; MAGNETIC RESONANCE IMAGING; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE, INBRED BALB C; ORGANOMETALLIC COMPOUNDS; TUMOR BURDEN;

EID: 84921957698     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.01.028     Document Type: Article

References (66)

1. E. Terreno, F. Uggeri, and S. Aime Image guided therapy: the advent of theranostic agents J. Control. Release 161 2 2012 328 337
2. P. Prabhu, and V. Patravale The upcoming field of theranostic nanomedicine: an overview J. Biomed. Nanotechnol. 8 6 2012 859 882
3. B. Sumer, and J.M. Gao Theranostic nanomedicine for cancer Nanomedicine 3 2 2008 137 140
4. R. Weissleder, and M.J. Pittet Imaging in the era of molecular oncology Nature 452 7187 2008 580 589
5. T.F. Massoud, and S.S. Gambhir Molecular imaging in living subjects: seeing fundamental biological processes in a new light Genes Dev. 17 5 2003 545 580
6. R. Weissleder Molecular imaging: exploring the next frontier Radiology 212 3 1999 609 614
7. R.E. Jacobs, and S.R. Cherry Complementary emerging techniques: high-resolution PET and MRI Curr. Opin. Neurobiol. 11 5 2001 621 629
8. A.A. Manzoor Overcoming limitations in nanoparticle drug delivery: triggered, intravascular release to improve drug penetration into tumors Cancer Res. 72 21 2012 5566 5575
9. T. Lammers Theranostic nanomedicine Acc. Chem. Res. 44 10 2011 1029 1038
10. V. Torchilin Liposomes in drug delivery J. Siepmann, R.A. Siegel, M.J. Rathbone, Fundamentals and Applications of Controlled Release Drug Delivery 2012 Springer New York 289 328
11. A.M. Ponce Hyperthermia mediated liposomal drug delivery Int. J. Hyperth. 22 3 2006 205 213
12. G.A. Koning Hyperthermia and thermosensitive liposomes for improved delivery of chemotherapeutic drugs to solid tumors Pharm. Res. 27 8 2010 1750 1754
13. D. Needham A new temperature-sensitive liposome for use with mild hyperthermia: characterization and testing in a human tumor xenograft model Cancer Res. 60 5 2000 1197 1201
14. E. Torres Improved paramagnetic liposomes for MRI visualization of pH triggered release J. Control. Release 154 2 2011 196 202
15. P. Kuppusamy Noninvasive imaging of tumor redox status and its modification by tissue glutathione levels Cancer Res. 62 1 2002 307 312
16. D. Mellal, and A. Zumbuehl Exit-strategies - smart ways to release phospholipid vesicle cargo J. Mater. Chem. B 2 3 2014 247 252
17. L. Zhu, and V.P. Torchilin Stimulus-responsive nanopreparations for tumor targeting Integr. Biol. 5 1 2013 96 107
18. R. Singh, and S.V. Torti Carbon nanotubes in hyperthermia therapy Adv. Drug Deliv. Rev. 65 15 2013 2045 2060
19. B. Bazrafshan Temperature imaging of laser-induced thermotherapy (LITT) by MRI: evaluation of different sequences in phantom Lasers Med. Sci. 29 1 2014 173 183
20. M. Kostrzewa Microwave ablation of osteoid osteomas using dynamic MR imaging for early treatment assessment: preliminary experience J. Vasc. Interv. Radiol. 25 1 2014 106 111
21. M. de Smet Magnetic resonance guided high-intensity focused ultrasound mediated hyperthermia improves the intratumoral distribution of temperature-sensitive liposomal doxorubicin Investig. Radiol. 48 6 2013 395 405
22. H. Grull, and S. Langereis Hyperthermia-triggered drug delivery from temperature-sensitive liposomes using MRI-guided high intensity focused ultrasound J. Control. Release 161 2 2012 317 327
23. A.H. Negussie Formulation and characterisation of magnetic resonance imageable thermally sensitive liposomes for use with magnetic resonance-guided high intensity focused ultrasound Int. J. Hyperth. 27 2 2011 140 155
24. A. Ranjan 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 3 2012 487 494
25. L. Li Mild hyperthermia triggered doxorubicin release from optimized stealth thermosensitive liposomes improves intratumoral drug delivery and efficacy J. Control. Release 168 2 2013 142 150
26. G.M. Lanza Assessing the barriers to image-guided drug delivery Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 6 1 2014 1 14
27. R. Fernando MRI-guided monitoring of thermal dose and targeted drug delivery for cancer therapy Pharm. Res. 30 11 2013 2709 2717
28. M.W. Dewhirst Novel Approaches to Treatment of Hepatocellular Carcinoma and Hepatic Metastases Using Thermal Ablation and Thermosensitive Liposomes Surgical Oncology Clinics of North America 22 3 2013 545 561
29. J.R. McDaniel, M.W. Dewhirst, and A. Chilkoti Actively targeting solid tumours with thermoresponsive drug delivery systems that respond to mild hyperthermia Int. J. Hyperth. 29 6 2013 501 510
30. D. Sharma, T.P. Chelvi, and R. Ralhan Thermosensitive liposomal taxol formulation: heat-mediated targeted drug delivery in murine melanoma Melanoma Res. 8 3 1998 240 244
31. D. Papahadjopoulos Phase transitions in phospholipid vesicles. Fluorescence polarization and permeability measurements concerning the effect of temperature and cholesterol Biochim. Biophys. Acta 311 3 1973 330 348
32. B.M. Dicheva, and G.A. Koning Targeted thermosensitive liposomes: an attractive novel approach for increased drug delivery to solid tumors Expert Opin. Drug Deliv. 11 1 2014 83 100
33. L. Li A novel two-step mild hyperthermia for advanced liposomal chemotherapy J. Control. Release 174 2014 202 208
34. M. Nakayama, J. Akimoto, and T. Okano Polymeric micelles with stimuli-triggering systems for advanced cancer drug targeting J. Drug Target. 22 7 2014 584 599
35. J.P. May, and S.D. Li Hyperthermia-induced drug targeting Expert Opin. Drug Deliv. 10 4 2013 511 527
36. D. Needham Materials characterization of the low temperature sensitive liposome (LTSL): effects of the lipid composition (lysolipid and DSPE-PEG2000) on the thermal transition and release of doxorubicin Faraday Discuss. 161 2013 515 534
37. S. Langereis Paramagnetic liposomes for molecular MRI and MRI-guided drug delivery NMR Biomed. 26 7 2013 728 744
38. S. Wang Pulsed high intensity focused ultrasound increases penetration and therapeutic efficacy of monoclonal antibodies in murine xenograft tumors J. Control. Release 162 1 2012 218 224
39. X.Y. Chen, S.S. Gambhlr, and J. Cheon Theranostic nanomedicine Acc. Chem. Res. 44 10 2011 p. 841
40. C.Y. Lin Ultrasound sensitive eLiposomes containing doxorubicin for drug targeting therapy Nanomedicine 10 1 2014 67 76
41. H.Y. Lin, and J.L. Thomas Factors affecting responsivity of unilamellar liposomes to 20 kHz ultrasound Langmuir 20 15 2004 6100 6106
42. T.J. Evjen In vivo monitoring of liposomal release in tumours following ultrasound stimulation Eur. J. Pharm. Biopharm. 84 3 2013 526 531
43. P. Giustetto Release of a paramagnetic magnetic resonance imaging agent from liposomes triggered by low intensity non-focused ultrasound J. Med. Imaging Health Inform. 3 3 2013 356 366
44. S. Datta Correlation of cavitation with ultrasound enhancement of thrombolysis Ultrasound Med. Biol. 32 8 2006 1257 1267
45. A. Schroeder, J. Kost, and Y. Barenholz Ultrasound, liposomes, and drug delivery: principles for using ultrasound to control the release of drugs from liposomes Chem. Phys. Lipids 162 1-2 2009 1 16
46. A. Yudina Ultrasound-mediated intracellular drug delivery using microbubbles and temperature-sensitive liposomes J. Control. Release 155 3 2011 442 448
47. A. Schroeder Controlling liposomal drug release with low frequency ultrasound: mechanism and feasibility Langmuir 23 7 2007 4019 4025
48. M. Afadzi Mechanisms of the ultrasound-mediated intracellular delivery of liposomes and dextrans IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60 1 2013 21 33
49. B.J. Staples Role of frequency and mechanical index in ultrasonic-enhanced chemotherapy in rats Cancer Chemother. Pharmacol. 64 3 2009 593 600
50. M. Knodler An analysis of toxicity in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck (R/M SCCHN) receiving cetuximab, fluorouracil and cisplatin alone or with docetaxel in a phase II clinical trial (CeFCiD) Onkologie 35 2012 153
51. H. Fattahi Magnetoliposomes as multimodal contrast agents for molecular imaging and cancer nanotheragnostics Nanomedicine 6 3 2011 529 544
52. S. Aime Pushing the sensitivity envelope of lanthanide-based magnetic resonance imaging (MRI) contrast agents for molecular imaging applications Acc. Chem. Res. 42 7 2009 822 831
53. E. Terreno Paramagnetic liposomes as innovative contrast agents for magnetic resonance (MR) molecular imaging applications Chem. Biodivers. 5 10 2008 1901 1912
54. S.L. Fossheim Paramagnetic liposomes as MRI contrast agents: influence of liposomal physicochemical properties on the in vitro relaxivity Magn. Reson. Imaging 17 1 1999 83 89
55. D.D. Castelli Metal containing nanosized systems for MR-molecular imaging applications Coord. Chem. Rev. 252 21-22 2008 2424 2443
56. S. Rizzitelli, P. Giustetto, C. Boffa, D. Delli Castelli, J.C. Cutrin, S. Aime, and E. Terreno In vivo MRI visualization of release from liposomes triggered by local application of pulsed low intensity non focused ultrasound Nanomedicine 10 5 2014 901 904
57. A. Barge How to determine free Gd and free ligand in solution of Gd chelates. A technical note Contrast Media Mol. Imaging 1 5 2006 184 188
58. P. Nanni TS/A: a new metastasizing cell line from a BALB/c spontaneous mammary adenocarcinoma Clin. Exp. Metastasis 1 4 1983 373 380
59. M.C. Steckner, B. Liu, and L. Ying A new single acquisition, two-image difference method for determining MR image SNR Med. Phys. 36 2 2009 662 671
60. O. Dietrich Measurement of signal-to-noise ratios in MR images: influence of multichannel coils, parallel imaging, and reconstruction filters J. Magn. Reson. Imaging 26 2 2007 375 385
61. R.M. Henkelman Measurement of signal intensities in the presence of noise in mr images Med. Phys. 12 2 1985 232 233
62. G. Castellano, B.L., L.M. Li, and F. Cendes Texture analysis of medical images Clin. Radiol. 59 12 2004 1061 1069
63. R.M. Haralick, S.K., and I.H. Dinstein Textural features for image classification IEEE Trans. Syst. Man Cybern. SMC-3 6 1973 610 621
64. DA, and R.A.a.J. Quantification of histochemical staining by color deconvolution Anal. Quant. Cytol. Histol. 23 4 2001 291 299
65. D. Delli Castelli In vivo MRI multicontrast kinetic analysis of the uptake and intracellular trafficking of paramagnetically labeled liposomes J. Control. Release 144 3 2010 271 279
66. M. de Smet 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 150 1 2011 102 110