Sonoporation enhances liposome accumulation and penetration in tumors with low EPR

Journal of Controlled Release

Volumn 231, Issue , 2016, Pages 77-85

  Theek, Benjamin ^a   Baues, Maike ^a   Ojha, Tarun ^a   Möckel, Diana ^a   Veettil, Seena Koyadan ^b   Steitz, Julia ^b   Van Bloois, Louis ^c   Storm, Gert ^c,d   Kiessling, Fabian ^a   Lammers, Twan ^a,c,d  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

EPR; Liposomes; Microbubbles; Sonoporation; Ultrasound

Indexed keywords

BIOLOGICAL MATERIALS; BLOOD VESSELS; COMPUTERIZED TOMOGRAPHY; HYPERTHERMIA THERAPY; LIPOSOMES; PARAMAGNETIC RESONANCE; TOMOGRAPHY; ULTRASONICS;

ENHANCED PERMEABILITY AND RETENTION EFFECTS; INDIVIDUAL VARIABILITY; MICROBUBBLES; PANCREATIC CARCINOMA; SONOPORATION; TUMOR ACCUMULATION; TWO-PHOTON LASER SCANNING MICROSCOPIES; VASCULAR NORMALIZATION;

TUMORS;

LIPOSOME; FLUORESCENT DYE; NANOPARTICLE; POLYMER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHEMICAL PARAMETERS; CHEMICAL PROCEDURES; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; ENHANCED PERMEABILITY AND RETENTION; FEMALE; FLUORESCENCE MOLECULAR TOMOGRAPHY; LASER MICROSCOPY; MICROBUBBLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SONOPORATION; TOMOGRAPHY; ULTRASOUND; ANIMAL; CHEMISTRY; DRUG DELIVERY SYSTEM; FLUORESCENCE IMAGING; HUMAN; NUDE MOUSE; PERMEABILITY; PROCEDURES; SURFACE PROPERTY; THERAPEUTIC USE; TUMOR CELL LINE; X-RAY COMPUTED TOMOGRAPHY; XENOGRAFT;

ANIMALS; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; FEMALE; FLUORESCENT DYES; HETEROGRAFTS; HUMANS; LIPOSOMES; MICE; MICE, NUDE; MICROBUBBLES; NANOPARTICLES; OPTICAL IMAGING; PERMEABILITY; POLYMERS; SURFACE PROPERTIES; TOMOGRAPHY, X-RAY COMPUTED; ULTRASONIC WAVES;

EID: 84976217379     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.02.021     Document Type: Article

References (58)

1. Y. Matsumura, and H. Maeda A new concept for macromolecular therapeutics in cancer chemotherapy: mechanism of tumoritropic accumulation of proteins and the antitumor agent SMANCS Cancer Res. 46 1986 6387 6392
2. H. Maeda Macromolecular therapeutics in cancer treatment: the EPR effect and beyond J. Control. Release 164 2012 138 144
3. R.K. Jain, and T. Stylianopoulos Delivering nanomedicine to solid tumors Nat. Rev. Clin. Oncol. 7 2010 653 664
4. T. Lammers SMART drug delivery systems: back to the future vs. clinical reality Int. J. Pharm. 2013
5. M.I. Koukourakis, S. Koukouraki, A. Giatromanolaki, S. Kakolyris, V. Georgoulias, A. Velidaki, S. Archimandritis, and N.N. Karkavitsas High intratumoral accumulation of stealth liposomal doxorubicin in sarcomas - rationale for combination with radiotherapy Acta Oncol. 39 2000 207 211
6. K.J. Harrington, S. Mohammadtaghi, P.S. Uster, D. Glass, A.M. Peters, R.G. Vile, and J.S. Stewart Effective targeting of solid tumors in patients with locally advanced cancers by radiolabeled pegylated liposomes Clin. Cancer Res. 7 2001 243 254
7. T. Lammers, L.Y. Rizzo, G. Storm, and F. Kiessling Personalized nanomedicine Clin. Cancer Res. 18 2012 4889 4894
8. D. Simberg Opening windows into tumors ACS Nano 2015
9. 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
10. L.Y. Rizzo, B. Theek, G. Storm, F. Kiessling, and T. Lammers Recent progress in nanomedicine: therapeutic, diagnostic and theranostic applications Curr. Opin. Biotechnol. 24 2013 1159 1166
11. N. Bertrand, J. Wu, X. Xu, N. Kamaly, and O.C. Farokhzad Cancer nanotechnology: the impact of passive and active targeting in the era of modern cancer biology Adv. Drug Deliv. Rev. 66 2014 2 25
12. J. Ehling, B. Theek, F. Gremse, S. Baetke, D. Mockel, J. Maynard, S.A. Ricketts, H. Grull, M. Neeman, R. Knuechel, W. Lederle, F. Kiessling, and T. Lammers Micro-CT imaging of tumor angiogenesis: quantitative measures describing micromorphology and vascularization Am. J. Pathol. 184 2014 431 441
13. B. Theek, L.Y. Rizzo, J. Ehling, F. Kiessling, and T. Lammers The theranostic path to personalized nanomedicine Clin. Transl. Imaging 2 2014 66 76
14. T. Ojha, L. Rizzo, G. Storm, F. Kiessling, and T. Lammers Image-guided drug delivery: preclinical applications and clinical translation Expert Opin. Drug Deliv. 2015 1 5
15. S. Kunjachan, J. Ehling, G. Storm, F. Kiessling, and T. Lammers Noninvasive imaging of nanomedicines and nanotheranostics: principles, progress, and prospects Chem. Rev. 115 2015 10907 10937
16. L. Davies Cde, L.M. Lundstrom, J. Frengen, L. Eikenes, S.O. Bruland, O. Kaalhus, M.H. Hjelstuen, and C. Brekken Radiation improves the distribution and uptake of liposomal doxorubicin (caelyx) in human osteosarcoma xenografts Cancer Res. 64 2004 547 553
17. P.A. Netti, D.A. Berk, M.A. Swartz, A.J. Grodzinsky, and R.K. Jain Role of extracellular matrix assembly in interstitial transport in solid tumors Cancer Res. 60 2000 2497 2503
18. Z. Popovic, W. Liu, V.P. Chauhan, J. Lee, C. Wong, A.B. Greytak, N. Insin, D.G. Nocera, D. Fukumura, R.K. Jain, and M.G. Bawendi A nanoparticle size series for in vivo fluorescence imaging Angew. Chem. Int. Ed. Engl. 49 2010 8649 8652
19. T. Stylianopoulos, B. Diop-Frimpong, L.L. Munn, and R.K. Jain Diffusion anisotropy in collagen gels and tumors: the effect of fiber network orientation Biophys. J. 99 2010 3119 3128
20. C. Wong, T. Stylianopoulos, J. Cui, J. Martin, V.P. Chauhan, W. Jiang, Z. Popovic, R.K. Jain, M.G. Bawendi, and D. Fukumura Multistage nanoparticle delivery system for deep penetration into tumor tissue Proc. Natl. Acad. Sci. U. S. A. 108 2011 2426 2431
21. H. Cabral, Y. Matsumoto, K. Mizuno, Q. Chen, M. Murakami, M. Kimura, Y. Terada, M.R. Kano, K. Miyazono, M. Uesaka, N. Nishiyama, and K. Kataoka Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size Nat. Nanotechnol. 6 2011 815 823
22. W. Cai, Z.J. Kerner, H. Hong, and J. Sun Targeted cancer therapy with tumor necrosis factor-alpha Biochem. Insights 2008 2008 15 21
23. S. Goel, D.G. Duda, L. Xu, L.L. Munn, Y. Boucher, D. Fukumura, and R.K. Jain Normalization of the vasculature for treatment of cancer and other diseases Physiol. Rev. 91 2011 1071 1121
24. V.P. Chauhan, T. Stylianopoulos, J.D. Martin, Z. Popovic, O. Chen, W.S. Kamoun, M.G. Bawendi, D. Fukumura, and R.K. Jain Normalization of tumour blood vessels improves the delivery of nanomedicines in a size-dependent manner Nat. Nanotechnol. 7 2012 383 388
25. U. Prabhakar, H. Maeda, R.K. Jain, E.M. Sevick-Muraca, W. Zamboni, O.C. Farokhzad, S.T. Barry, A. Gabizon, P. Grodzinski, and D.C. Blakey Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology Cancer Res. 73 2013 2412 2417
26. H. Nehoff, N.N. Parayath, L. Domanovitch, S. Taurin, and K. Greish Nanomedicine for drug targeting: strategies beyond the enhanced permeability and retention effect Int. J. Nanomedicine 9 2014 2539 2555
27. G. Kong, and M.W. Dewhirst Hyperthermia and liposomes Int. J. Hyperth. 15 1999 345 370
28. K. Kooiman, H.J. Vos, M. Versluis, and N. de Jong Acoustic behavior of microbubbles and implications for drug delivery Adv. Drug Deliv. Rev. 72 2014 28 48
29. I. Lentacker, I. De Cock, R. Deckers, S.C. De Smedt, and C.T. Moonen Understanding ultrasound induced sonoporation: definitions and underlying mechanisms Adv. Drug Deliv. Rev. 72 2014 49 64
30. R. Deckers, and C.T. Moonen Ultrasound triggered, image guided, local drug delivery J. Control. Release 148 2010 25 33
31. S. Mo, C.C. Coussios, L. Seymour, and R. Carlisle Ultrasound-enhanced drug delivery for cancer Expert Opin. Drug Deliv. 9 2012 1525 1538
32. F. Kiessling, S. Fokong, J. Bzyl, W. Lederle, M. Palmowski, and T. Lammers Recent advances in molecular, multimodal and theranostic ultrasound imaging Adv. Drug Deliv. Rev. 72 2014 15 27
33. A.K. Wood, and C.M. Sehgal A review of low-intensity ultrasound for cancer therapy Ultrasound Med. Biol. 41 2015 905 928
34. F. Kiessling, S. Fokong, P. Koczera, W. Lederle, and T. Lammers Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics J. Nucl. Med. 53 2012 345 348
35. T. Lammers, P. Koczera, S. Fokong, F. Gremse, J. Ehling, M. Vogt, A. Pich, G. Storm, M. van Zandvoort, and F. Kiessling Theranostic USPIO-loaded microbubbles for mediating and monitoring blood-brain barrier permeation Adv. Funct. Mater. 25 2015 36 43
36. M. Aryal, J. Park, N. Vykhodtseva, Y.Z. Zhang, and N. McDannold Enhancement in blood-tumor barrier permeability and delivery of liposomal doxorubicin using focused ultrasound and microbubbles: evaluation during tumor progression in a rat glioma model Phys. Med. Biol. 60 2015 2511 2527
37. J. Kang, X. Wu, Z. Wang, H. Ran, C. Xu, J. Wu, Z. Wang, and Y. Zhang Antitumor effect of docetaxel-loaded lipid microbubbles combined with ultrasound-targeted microbubble activation on VX2 rabbit liver tumors J. Ultrasound Med. 29 2010 61 70
38. S. Tinkov, C. Coester, S. Serba, N.A. Geis, H.A. Katus, G. Winter, and R. Bekeredjian New doxorubicin-loaded phospholipid microbubbles for targeted tumor therapy: in-vivo characterization J. Control. Release 148 2010 368 372
39. M.C. Cochran, J.R. Eisenbrey, M.C. Soulen, S.M. Schultz, R.O. Ouma, S.B. White, E.E. Furth, and M.A. Wheatley Disposition of ultrasound sensitive polymeric drug carrier in a rat hepatocellular carcinoma model Acad. Radiol. 18 2011 1341 1348
40. P. Li, Y. Zheng, H. Ran, J. Tan, Y. Lin, Q. Zhang, J. Ren, and Z. Wang Ultrasound triggered drug release from 10-hydroxycamptothecin-loaded phospholipid microbubbles for targeted tumor therapy in mice J. Control. Release 162 2012 349 354
41. S. Fokong, B. Theek, Z. Wu, P. Koczera, L. Appold, S. Jorge, U. Resch-Genger, M. van Zandvoort, G. Storm, F. Kiessling, and T. Lammers Image-guided, targeted and triggered drug delivery to tumors using polymer-based microbubbles J. Control. Release 163 2012 75 81
42. C.Y. Lin, J.R. Li, H.C. Tseng, M.F. Wu, and W.L. Lin Enhancement of focused ultrasound with microbubbles on the treatments of anticancer nanodrug in mouse tumors Nanomedicine (London) 8 2012 900 907
43. A. Ale, V. Ermolayev, E. Herzog, C. Cohrs, M.H. de Angelis, and V. Ntziachristos FMT-XCT: in vivo animal studies with hybrid fluorescence molecular tomography-X-ray computed tomography Nat. Methods 9 2012 615 620
44. F. Gremse, B. Theek, S. Kunjachan, W. Lederle, A. Pardo, S. Barth, T. Lammers, U. Naumann, and F. Kiessling Absorption reconstruction improves biodistribution assessment of fluorescent nanoprobes using hybrid fluorescence-mediated tomography Theranostics 4 2014 960 971
45. Y. Shi, S. Kunjachan, Z. Wu, F. Gremse, D. Moeckel, M. van Zandvoort, F. Kiessling, G. Storm, C.F. van Nostrum, W.E. Hennink, and T. Lammers Fluorophore labeling of core-crosslinked polymeric micelles for multimodal in vivo and ex vivo optical imaging Nanomedicine (London) 10 2015 1111 1125
46. S. Fokong, M. Siepmann, Z. Liu, G. Schmitz, F. Kiessling, and J. Gatjens Advanced characterization and refinement of poly N-butyl cyanoacrylate microbubbles for ultrasound imaging Ultrasound Med. Biol. 37 2011 1622 1634
47. S. Kunjachan, F. Gremse, B. Theek, P. Koczera, R. Pola, M. Pechar, T. Etrych, K. Ulbrich, G. Storm, F. Kiessling, and T. Lammers Noninvasive optical imaging of nanomedicine biodistribution ACS Nano 7 2013 252 262
48. F. Gremse, D. Doleschel, S. Zafarnia, A. Babler, W. Jahnen-Dechent, T. Lammers, W. Lederle, and F. Kiessling Hybrid μCT-FMT imaging and image analysis J. Vis. Exp. 2015
49. V. Ntziachristos, J. Ripoll, L.V. Wang, and R. Weissleder Looking and listening to light: the evolution of whole-body photonic imaging Nat. Biotechnol. 23 2005 313 320
50. V. Ntziachristos Going deeper than microscopy: the optical imaging frontier in biology Nat. Methods 7 2010 603 614
51. S. Kunjachan, R. Pola, F. Gremse, B. Theek, J. Ehling, D. Moeckel, B. Hermanns-Sachweh, M. Pechar, K. Ulbrich, W.E. Hennink, G. Storm, W. Lederle, F. Kiessling, and T. Lammers Passive versus active tumor targeting using RGD- and NGR-modified polymeric nanomedicines Nano Lett. 14 2014 972 981
52. T. Lammers, P. Peschke, R. Kuhnlein, V. Subr, K. Ulbrich, J. Debus, P. Huber, W. Hennink, and G. Storm Effect of radiotherapy and hyperthermia on the tumor accumulation of HPMA copolymer-based drug delivery systems J. Control. Release 117 2007 333 341
53. N. Rapoport, A. Payne, C. Dillon, J. Shea, C. Scaife, and R. Gupta Focused ultrasound-mediated drug delivery to pancreatic cancer in a mouse model J. Ther. Ultrasound 1 2013 11
54. P.G. Sanches, M. Muhlmeister, R. Seip, E. Kaijzel, C. Lowik, M. Bohmer, K. Tiemann, and H. Grull Ultrasound-mediated gene delivery of naked plasmid DNA in skeletal muscles: a case for bolus injections J. Control. Release 195 2014 130 137
55. B. Theek, F. Gremse, S. Kunjachan, S. Fokong, R. Pola, M. Pechar, R. Deckers, G. Storm, J. Ehling, F. Kiessling, and T. Lammers Characterizing EPR-mediated passive drug targeting using contrast-enhanced functional ultrasound imaging J. Control. Release 182 2014 83 89
56. S.N. Ekdawi, J.M. Stewart, M. Dunne, S. Stapleton, N. Mitsakakis, Y.N. Dou, D.A. Jaffray, and C. Allen Spatial and temporal mapping of heterogeneity in liposome uptake and microvascular distribution in an orthotopic tumor xenograft model J. Control. Release 207 2015 101 111
57. E. Brown, T. McKee, E. diTomaso, A. Pluen, B. Seed, Y. Boucher, and R.K. Jain Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation Nat. Med. 9 2003 796 800
58. S. Kotopoulis, G. Dimcevski, O.H. Gilja, D. Hoem, and M. Postema Treatment of human pancreatic cancer using combined ultrasound, microbubbles, and gemcitabine: a clinical case study Med. Phys. 40 2013 072902