Temperature-sensitive paramagnetic liposomes for image-guided drug delivery: Mn2 + versus [Gd(HPDO3A)(H2O)]

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 11, 2014, Pages 2807-2816

  Yeo, Sin Yuin ^a,c   De Smet, Mariska ^a,c   Langereis, Sander ^b,c   Vander Elst, Luce ^d   Muller, Robert N ^d,e   Grüll, Holger ^a,b,c  

^a EINDHOVEN UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b PHILIPS RESEARCH LABORATORIES   (Netherlands)

^c Center for Imaging Research and Education (CIRE)   (Netherlands)

^d UNIVERSITY OF MONS   (Belgium)

^e Center for Microscopy and Molecular Imaging   (Belgium)

Author keywords

Doxorubicin; Hyperthemia; Image guided drug delivery; Manganese; Temperature sensitive liposomes; Gd(HPDO3A)(H2O)

Indexed keywords

DOXORUBICIN; GADOTERIDOL; LIPOSOME; MANGANESE; TEMPERATURE SENSITIVE LIPOSOME; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG RELEASE; DRUG RETENTION; DRUG STABILITY; ENCAPSULATION; HEATING; HIGH TEMPERATURE; LOW TEMPERATURE; MEMBRANE TRANSPORT; PHOSPHOLIPID BILAYER; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; TITRIMETRY; TRANSMEMBRANE WATER EXCHANGE;

EID: 84940288833     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.07.019     Document Type: Article

References (54)

1. M. Yatvin, J. Weinstein, W. Dennis, and R. Blumenthal Design of liposomes for enhanced local release of drugs by hyperthermia Science 202 1978 1290 1293 (Pubitemid 9154441)
2. M. de Smet, E. Heijman, S. Langereis, N.M. Hijnen, and H. Grüll 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 2011 102 110
3. D. Needham, G. Anyarambhatla, G. Kong, and M.W. Dewhirst A new temperature-sensitive liposome for use with mild hyperthermia: characterization and testing in a human tumor xenograft model Cancer Res. 60 2000 1197 1201 (Pubitemid 30151982)
4. P.S. Yarmolenko, Y. Zhao, C. Landon, I. Spasojevic, F. Yuan, D. Needham, B.L. Viglianti, and M.W. Dewhirst Comparative effects of thermosensitive doxorubicin-containing liposomes and hyperthermia in human and murine tumours Int. J. Hyperth. 26 2010 485 498
5. G.R. Anyarambhatla, and D. Needham 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. 9 1999 491 506
6. J.K. Mills, and D. Needham Lysolipid incorporation in dipalmitoylphosphatidylcholine bilayer membranes enhances the ion permeability and drug release rates at the membrane phase transition Biochim. Biophys. Acta Biomembr. 1716 2005 77 96 (Pubitemid 41532286)
7. C.D. Landon, J.Y. Park, D. Needham, and M.W. Dewhirst Nanoscale drug delivery and hyperthermia: the materials design and preclinical and clinical testing of low temperature-sensitive liposomes used in combination with mild hyperthermia in the treatment of local cancer Open Nanomedicine J. 3 2011 38 64
8. A.M. Ponce, B.L. Viglianti, D. Yu, P.S. Yarmolenko, C.R. Michelich, J. Woo, M.B. Bally, and M.W. Dewhirst Magnetic resonance imaging of temperature-sensitive liposome release: drug dose painting and antitumor effects J. Natl. Cancer Inst. 99 2007 53 63
9. B.L. Viglianti, S.A. Abraham, C.R. Michelich, P.S. Yarmolenko, J.R. MacFall, M.B. Bally, and M.W. Dewhirst In vivo monitoring of tissue pharmacokinetics of liposome/drug using MRI: illustration of targeted delivery Magn. Reson. Med. 51 2004 1153 1162 (Pubitemid 38797000)
10. B.L. Viglianti, A.M. Ponce, C.R. Michelich, D. Yu, S.A. Abraham, L. Sanders, P.S. Yarmolenko, T. Schroeder, J.R. MacFall, D.P. Barboriak, O.M. Colvin, M.B. Bally, and M.W. Dewhirst Chemodosimetry of in vivo tumor liposomal drug concentration using MRI Magn. Reson. Med. 56 2006 1011 1018 (Pubitemid 44691343)
11. 2 + Release World Congress on Medical Physics and Biomedical Engineering, September 7-12, 2009 vol. 25/13 2010 Springer Berlin Heidelberg Munich, Germany 21 22
12. M. de Smet, N.M. Hijnen, S. Langereis, A. Elevelt, E. Heijman, L. Dubois, P. Lambin, and H. Grüll Magnetic resonance guided high-intensity focused ultrasound mediated hyperthermia improves the intratumoral distribution of temperature-sensitive liposomal Doxorubicin Invest. Radiol. 48 2013 395 405
13. M. de Smet, S. Langereis, S.v. den Bosch, and H. Grüll Temperature-sensitive liposomes for doxorubicin delivery under MRI guidance J. Control. Release 143 2010 120 127
14. M. de Smet, S. Langereis, S. van den Bosch, K. Bitter, N. Hijnen, E. Heijman, and H. Grüll SPECT/CT imaging of temperature-sensitive liposomes for MR-image guided drug delivery with high intensity focused ultrasound J. Control. Release 169 2013 82 90
15. G. Bacić, M.R. Niesman, H.F. Bennett, R.L. Magin, and H.M. Swartz Modulation of Water Proton Relaxation Rates by Liposomes Containing Paramagnetic Materials 1988
16. V.J. Caride, H.D. Sostman, R.J. Winchell, and J.C. Gore Relaxation enhancement using liposomes carrying paramagnetic species Magn. Reson. Imaging 2 1984 107 112 (Pubitemid 14050413)
17. L. Frich, A. Bjørnerud, S. Fossheim, T. Tillung, and I. Gladhaug Experimental application of thermosensitive paramagnetic liposomes for monitoring magnetic resonance imaging guided thermal ablation Magn. Reson. Med. 52 2004 1302 1309 (Pubitemid 39612818)
18. A.H. Negussie, P.S. Yarmolenko, A. Partanen, A. Ranjan, G. Jacobs, D. Woods, H. Bryant, D. Thomasson, M.W. Dewhirst, B.J. Wood, and M.R. Dreher Formulation and characterisation of magnetic resonance imageable thermally sensitive liposomes for use with magnetic resonance-guided high intensity focused ultrasound Int. J. Hyperth. 27 2011 140 155
19. M. Peller, A. Schwerdt, M. Hossann, H.M. Reinl, T. Wang, S. Sourbron, M. Ogris, and L.H. Lindner MR characterization of mild hyperthermia-induced gadodiamide release from thermosensitive liposomes in solid tumors Invest. Radiol. 43 2008 877 892
20. T. Tagami, W.D. Foltz, M.J. Ernsting, C.M. Lee, I.F. Tannock, J.P. May, and S.-D. Li MRI monitoring of intratumoral drug delivery and prediction of the therapeutic effect with a multifunctional thermosensitive liposome Biomaterials 32 2011 6570 6578
21. S.L. Fossheim, K.A. Il'yasov, J. Hennig, and A. Bjørnerud Thermosensitive paramagnetic liposomes for temperature control during MR imaging-guided hyperthermia: in vitro feasibility studies Acad. Radiol. 7 2000 1107 1115
22. K.A. Il'yasov, S.L. Fossheim, U.N. Wiggen, A. Rogstad, J. Hennig, and A. Bjørnerud Paramagnetic liposomes as thermosensitive probes for MRI-guided thermal treatment: in vitro feasibility studies Appl. Magn. Reson. 33 2008 469 480
23. N. McDannold, S.L. Fossheim, H. Rasmussen, H. Martin, N. Vykhodtseva, and K. Hynynen Heat-activated liposomal MR contrast agent: initial in vivo results in rabbit liver and kidney1 Radiology 230 2004 743 752 (Pubitemid 38252872)
24. C. Bos, M. Lepetit-Coiffé, B. Quesson, and C.T.W. Moonen Simultaneous monitoring of temperature and T1: methods and preliminary results of application to drug delivery using thermosensitive liposomes Magn. Reson. Med. 54 2005 1020 1024 (Pubitemid 41457075)
25. T. Wang, M. Hossann, H.M. Reinl, M. Peller, H. Eibl, M. Reiser, R.D. Issels, and L.H. Lindner In vitro characterization of phosphatidylglyceroglycerol-based thermosensitive liposomes with encapsulated 1H MR T1-shortening gadodiamide Contrast Media Mol. Imaging 3 2008 19 26 (Pubitemid 351493975)
26. S.L. Fossheim, A.K. Fahlvik, J. Klaveness, and R.N. Muller Paramagnetic liposomes as MRI contrast agents: influence of liposomal physicochemical properties on the in vitro relaxivity Magn. Reson. Imaging 17 1999 83 89 (Pubitemid 29036107)
27. S.H. Koenig, Q.F. Ahkong, R.D. Brown, M. Lafleur, M. Spiller, E. Unger, and C. Tilcock Permeability of liposomal membranes to water: results from the magnetic field dependence of T1 of solvent protons in suspensions of vesicles with entrapped paramagnetic ions Magn. Reson. Med. 23 1992 275 286
28. S.A. Abraham, K. Edwards, G. Karlsson, S. MacIntosh, L.D. Mayer, C. McKenzie, and M.B. Bally Formation of transition metal-doxorubicin complexes inside liposomes Biochim. Biophys. Acta 1565 2002 41 54 (Pubitemid 35239831)
29. G.N. Chiu, S.A. Abraham, L.M. Ickenstein, R. Ng, G. Karlsson, K. Edwards, E.K. Wasan, and M.B. Bally Encapsulation of doxorubicin into thermosensitive liposomes via complexation with the transition metal manganese J. Control. Release 104 2005 271 288 (Pubitemid 40724929)
30. S.A. Abraham, D.N. Waterhouse, L.D. Mayer, P.R. Cullis, T.D. Madden, and M.B. Bally The liposomal formulation of doxorubicin Methods Enzymol. 391 2005 71 97 (Pubitemid 40254030)
31. A.P. Koretsky, and A.C. Silva Manganese-enhanced magnetic resonance imaging (MEMRI) NMR Biomed. 17 2004 527 531 (Pubitemid 40124778)
32. A.C. Silva, J.H. Lee, I. Aoki, and A.P. Koretsky Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations NMR Biomed. 17 2004 532 543 (Pubitemid 40124779)
33. G. Wolf, and L. Baum Cardiovascular toxicity and tissue proton T1 response to manganese injection in the dog and rabbit Am. J. Roentgenol. 141 1983 193 197 (Pubitemid 13063905)
34. M.N. Eakins, S.M. Eaton, R.A. Fisco, R.J. Hunt, C.E. Ita, T. Katona, L.M. Owies, E. Schramm, J.W. Sulner, C.W. Thompson, G.W. White, and S. Murthy Yerramilli Physicochemical properties, pharmacokinetics, and biodistribution of gadoteridol injection in rats and dogs Acad. Radiol. 2 1995 584 591
35. G. Rouser, S. Fleischer, and A. Yamamoto Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots Lipids 5 1970 494 496
36. S. Langereis, H.-A.T. Kooistra, M.H.P. van Genderen, and E.W. Meijer Probing the interaction of the biotin-avidin complex with the relaxivity of biotinylated Gd-DTPA Org. Biomol. Chem. 2 2004 1271 1273
37. I. Tinoco, K. Sauer, and J.C. Wang Physical Chemistry: Principles and Applications in Biological Sciences 3rd ed. 1995 Chapter 11
38. S.H. Koenig, R.D. Brown 3rd, R. Kurland, and S. Ohki Relaxivity and binding of Mn2 + ions in solutions of phosphatidylserine vesicles Magn. Reson. Med. 7 1988 133 142
39. É. Tóth, L. Helm, and A. Merbach W. Krause, Relaxivity of MRI Contrast Agents Contrast Agents I vol. 221 2002 Springer Berlin/ Heidelberg 61 101
40. M.P. Federle, J.L. Chezmar, D.L. Rubin, J.C. Weinreb, P.C. Freeny, R.C. Semelka, J.J. Brown, J.A. Borrello, J.K.T. Lee, R. Mattrey, A.H. Dachman, S. Saini, B. Harmon, M. Fenstermacher, R.E. Pelsang, S.E. Harms, D.G. Mitchell, H.H. Halford Iii, M.W. Anderson, C.D. Johnson, I.R. Francis, J.G. Bova, P.J. Kenney, D.L. Klippenstein, G.S. Foster, D.A. Turner, A.E. Stillman, R.C. Nelson, S.W. Young, R.H. Patt, M. Rifkin, S.E. Seltzer, S.B. Gay, R.O. Robison, P.F. Sherwin, and R. Ballerini Safety and efficacy of mangafodipir trisodium (MnDPDP) injection for hepatic MRI in adults: results of the U.S. Multicenter Phase III Clinical Trials (Safety) J. Magn. Reson. Imaging 12 2000 186 197 (Pubitemid 30437278)
41. W. Schima, R. Függer, E. Schober, C. Oettl, P. Wamser, F. Grabenwöger, J.M. Ryan, and G. Novacek Diagnosis and staging of pancreatic cancer: comparison of mangafodipir trisodium - enhanced MR imaging and contrast-enhanced helical hydro-CT Am. J. Roentgenol. 179 2002 717 724 (Pubitemid 34919588)
42. Y. Barenholz Doxil® - the first FDA-approved nano-drug: lessons learned J. Control. Release 160 2012 117 134
43. R.M. Rifkin, S.A. Gregory, A. Mohrbacher, and M.A. Hussein Pegylated liposomal doxorubicin, vincristine, and dexamethasone provide significant reduction in toxicity compared with doxorubicin, vincristine, and dexamethasone in patients with newly diagnosed multiple myeloma Cancer 106 2006 848 858 (Pubitemid 43238452)
44. S. Stewart, H. Jablonowski, F.D. Goebel, K. Arasteh, M. Spittle, A. Rios, D. Aboulafia, J. Galleshaw, and B.J. Dezube Randomized comparative trial of pegylated liposomal doxorubicin versus bleomycin and vincristine in the treatment of AIDS-related Kaposi's sarcoma. International Pegylated Liposomal Doxorubicin Study Group J. Clin. Oncol. 16 1998 683 691 (Pubitemid 28135616)
45. L.D. Mayer, L.C.L. Tai, M.B. Bally, G.N. Mitilenes, R.S. Ginsberg, and P.R. Cullis Characterization of liposomal systems containing doxorubicin entrapped in response to pH gradients Biochim. Biophys. Acta Biomembr. 1025 1990 143 151 (Pubitemid 20199621)
46. A. Kheirolomoom, C.-Y. Lai, S.M. Tam, L.M. Mahakian, E.S. Ingham, K.D. Watson, and K.W. Ferrara Complete regression of local cancer using temperature-sensitive liposomes combined with ultrasound-mediated hyperthermia J. Control. Release 172 2013 266 273
47. A. Kheirolomoom, L.M. Mahakian, C.-Y. Lai, H.A. Lindfors, J.W. Seo, E.E. Paoli, K.D. Watson, E.M. Haynam, E.S. Ingham, L. Xing, R.H. Cheng, A.D. Borowsky, R.D. Cardiff, and K.W. Ferrara Copper-doxorubicin as a nanoparticle cargo retains efficacy with minimal toxicity Mol. Pharm. 7 2010 1948 1958
48. M.F. Tweedle The ProHance story: the making of a novel MRI contrast agent Eur. Radiol. 7 1997 S225 S230
49. A.N. Oksendal, and P.-A. Hals Biodistribution and toxicity of MR imaging contrast media J. Magn. Reson. Imaging 3 1993 157 165
50. N.a.E., and N. Karabukut Contrast agents used in MR imaging of the liver Diagn. Interv. Radiol. 12 2006 22 30
51. 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
52. H. Grüll, and S. Langereis Hyperthermia-triggered drug delivery from temperature-sensitive liposomes using MRI-guided high intensity focused ultrasound J. Control. Release 161 2012 317 327
53. N. Hijnen, S. Langereis, and H. Grüll Magnetic resonance guided high-intensity focused ultrasound for image-guided temperature-induced drug delivery Adv. Drug Deliv. Rev. 72 2014 65 81
54. S. Langereis, T. Geelen, H. Grüll, G.J. Strijkers, and K. Nicolay Paramagnetic liposomes for molecular MRI and MRI-guided drug delivery NMR Biomed. 26 2013 728 744