Non-invasive delivery of stealth, brain-penetrating nanoparticles across the blood - Brain barrier using MRI-guided focused ultrasound

Journal of Controlled Release

Volumn 189, Issue , 2014, Pages 123-132

  Nance, Elizabeth ^a,b   Timbie, Kelsie ^c   Miller, G Wilson ^d   Song, Ji ^c   Louttit, Cameron ^c   Klibanov, Alexander L ^d   Shih, Ting Yu ^b   Swaminathan, Ganesh ^b   Tamargo, Rafael J ^a   Woodworth, Graeme F ^e   Hanes, Justin ^a,b   Price, Richard J ^c  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b Johns Hopkins University   (United States)

^c University of Virginia   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

^e UNIVERSITY OF MARYLAND   (United States)

Author keywords

Central nervous system; Focused ultrasound; Nanoparticles

Indexed keywords

BLOOD; DRUG DELIVERY; ETHYLENE; FUNCTIONAL POLYMERS; NEUROPHYSIOLOGY; ULTRASONICS;

BLOOD-BRAIN BARRIER; CENTRAL NERVOUS SYSTEMS; FOCUSED ULTRASOUND; INTRAVENOUS ADMINISTRATION; MICROENVIRONMENTS; POLYMERIC NANOPARTICLES; RAT BRAIN TISSUE; SPATIAL ACCURACY;

NANOPARTICLES;

BRAIN PENETRATING NANOPARTICLE; CENTRAL NERVOUS SYSTEM AGENTS; FLUORESCENT DYE; GADOLINIUM PENTETATE MEGLUMINE; NANOPARTICLE; UNCLASSIFIED DRUG; ALEXA FLUOR 647; CARBOCYANINE; POLYMER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN SLICE; BRAIN TISSUE; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; ECHOGRAPHY; EX VIVO STUDY; FOCUSED ULTRASOUND; HISTOPATHOLOGY; IN VIVO STUDY; MICROBUBBLE; NON INVASIVE PROCEDURE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PARENCHYMA; POLYMERIZATION; PRIORITY JOURNAL; RAT; ULTRASOUND SCANNER; ANIMAL; CHEMISTRY; METABOLISM; PROCEDURES; SPRAGUE DAWLEY RAT; ULTRASOUND;

ANIMALS; BLOOD-BRAIN BARRIER; CARBOCYANINES; DRUG DELIVERY SYSTEMS; FLUORESCENT DYES; MAGNETIC RESONANCE IMAGING; MICROBUBBLES; NANOPARTICLES; POLYMERS; RATS, SPRAGUE-DAWLEY; ULTRASONICS;

EID: 84904282240     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2014.06.031     Document Type: Article

References (59)

1. J.Y. Li, R.J. Boado, and W.M. Pardridge Blood-brain barrier genomics J. Cereb. Blood Flow Metab. 21 1 2001 61 68 (Pubitemid 32016840)
2. W.M. Pardridge Blood-brain barrier drug targeting: the future of brain drug development Mol. Interv. 3 2 2003 90 105 (51)
3. M. Patel et al. Plasma and cerebrospinal fluid pharmacokinetics of intravenous temozolomide in non-human primates J. Neurooncol. 61 3 2003 203 207 (Pubitemid 36342297)
4. L. Rosso et al. A new model for prediction of drug distribution in tumor and normal tissues: pharmacokinetics of temozolomide in glioma patients Cancer Res. 69 1 2009 120 127
5. M.A. Rudek et al. Temozolomide in patients with advanced cancer: phase I and pharmacokinetic study Pharmacotherapy 24 1 2004 16 25 (Pubitemid 38056248)
6. P. Kleihues et al. The WHO classification of tumors of the nervous system J. Neuropathol. Exp. Neurol. 61 3 2002 215 225 (discussion 226-9) (Pubitemid 34212595)
7. K. Schoknecht, and H. Shalev Blood-brain barrier dysfunction in brain diseases: clinical experience Epilepsia 53 Suppl. 6 2012 7 13
8. A. Wunder et al. Imaging blood-brain barrier dysfunction in animal disease models Epilepsia 53 Suppl. 6 2012 14 21
9. A. Claes, A.J. Idema, and P. Wesseling Diffuse glioma growth: a guerilla war Acta Neuropathol. 114 5 2007 443 458 (Pubitemid 47521501)
10. A. Urayama The blood-brain barrier and neurodegenerative lysosomal storage diseases Brain Nerve 65 2 2013 153 163
11. W. El-Hage et al. Mechanisms of antidepressant resistance Front. Pharmacol. 4 2013 146
12. L. Edvinsson, and P. Tfelt-Hansen The blood-brain barrier in migraine treatment Cephalalgia 28 12 2008 1245 1258
13. K. Hynynen et al. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits Radiology 220 3 2001 640 646 (Pubitemid 32799969)
14. K. Hynynen et al. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications Neuroimage 24 1 2005 12 20 (Pubitemid 39611021)
15. N. McDannold et al. Temporary disruption of the blood-brain barrier by use of ultrasound and microbubbles: safety and efficacy evaluation in rhesus macaques Cancer Res. 72 14 2012 3652 3663
16. S.S. Abdelmoneim et al. Safety of contrast agent use during stress echocardiography in patients with elevated right ventricular systolic pressure: a cohort study Circ. Cardiovasc. Imaging 3 3 2010 240 248
17. F. Kiessling et al. Ultrasound microbubbles for molecular diagnosis, therapy, and theranostics J. Nucl. Med. 53 3 2012 345 348
18. S.T. Kang, and C.K. Yeh Ultrasound microbubble contrast agents for diagnostic and therapeutic applications: current status and future design Chang Gung Med. J. 35 2 2012 125 139
19. B.D. Meijering et al. Ultrasound and microbubble-targeted delivery of macromolecules is regulated by induction of endocytosis and pore formation Circ. Res. 104 5 2009 679 687
20. A. van Wamel et al. Ultrasound microbubble induced endothelial cell permeability J. Control. Release 116 2 2006 e100 e102
21. J. Wu, and W.L. Nyborg Ultrasound, cavitation bubbles and their interaction with cells Adv. Drug Deliv. Rev. 60 10 2008 1103 1116
22. S. Qin, and K.W. Ferrara Acoustic response of compliable microvessels containing ultrasound contrast agents Phys. Med. Biol. 51 20 2006 5065 5088 (Pubitemid 44540119)
23. L.J. Juffermans et al. Ultrasound and microbubble-induced intra- and intercellular bioeffects in primary endothelial cells Ultrasound Med. Biol. 35 11 2009 1917 1927
24. N. Hosseinkhah, and K. Hynynen A three-dimensional model of an ultrasound contrast agent gas bubble and its mechanical effects on microvessels Phys. Med. Biol. 57 3 2012 785 808
25. N. Sheikov et al. Effect of focused ultrasound applied with an ultrasound contrast agent on the tight junctional integrity of the brain microvascular endothelium Ultrasound Med. Biol. 34 7 2008 1093 1104 (Pubitemid 351893156)
26. N. Sheikov et al. Brain arterioles show more active vesicular transport of blood-borne tracer molecules than capillaries and venules after focused ultrasound-evoked opening of the blood-brain barrier Ultrasound Med. Biol. 32 9 2006 1399 1409 (Pubitemid 44332656)
27. X. Shang et al. Mechanism of low-frequency ultrasound in opening blood-tumor barrier by tight junction J. Mol. Neurosci. 43 3 2011 364 369
28. F.Y. Yang et al. Pulsed high-intensity focused ultrasound enhances the relative permeability of the blood-tumor barrier in a glioma-bearing rat model IEEE Trans. Ultrason. Ferroelectr. Freq. Control 58 5 2011 964 970
29. H.L. Liu et al. Blood-brain barrier disruption with focused ultrasound enhances delivery of chemotherapeutic drugs for glioblastoma treatment Radiology 255 2 2010 415 425
30. J.F. Jordao et al. Antibodies targeted to the brain with image-guided focused ultrasound reduces amyloid-beta plaque load in the TgCRND8 mouse model of Alzheimer's disease PLoS ONE 5 5 2010 e10549
31. M. Kinoshita et al. Noninvasive localized delivery of Herceptin to the mouse brain by MRI-guided focused ultrasound-induced blood-brain barrier disruption Proc. Natl. Acad. Sci. U. S. A. 103 31 2006 11719 11723 (Pubitemid 44182517)
32. L.H. Treat et al. Improved anti-tumor effect of liposomal doxorubicin after targeted blood-brain barrier disruption by MRI-guided focused ultrasound in rat glioma Ultrasound Med. Biol. 38 10 2012 1716 1725
33. E. Sykova, and C. Nicholson Diffusion in brain extracellular space Physiol. Rev. 88 4 2008 1277 1340
34. R.G. Thorne, and C. Nicholson In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space Proc. Natl. Acad. Sci. U. S. A. 103 14 2006 5567 5572
35. E.A. Nance et al. A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue Sci. Transl. Med. 4 149 2012 149ra119
36. H.S. Yoo et al. Biodegradable nanoparticles containing doxorubicin-PLGA conjugate for sustained release Pharm. Res. 16 7 1999 1114 1118 (Pubitemid 29368162)
37. S.K. Lai et al. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus Proc. Natl. Acad. Sci. U. S. A. 104 5 2007 1482 1487 (Pubitemid 46214616)
38. B. Amsden Solute diffusion within hydrogels Mechanisms and models Macromolecules 31 23 1998 8382 8395 (Pubitemid 128563527)
39. F. Alexis et al. Factors affecting the clearance and biodistribution of polymeric nanoparticles Mol. Pharm. 5 4 2008 505 515
40. K. Avgoustakis Pegylated poly(lactide) and poly(lactide-co-glycolide) nanoparticles: preparation, properties and possible applications in drug delivery Curr. Drug Deliv. 1 4 2004 321 333
41. H. Otsuka, Y. Nagasaki, and K. Kataoka PEGylated nanoparticles for biological and pharmaceutical applications Adv. Drug Deliv. Rev. 55 3 2003 403 419 (Pubitemid 36293792)
42. A.E. Gulyaev et al. Significant transport of doxorubicin into the brain with polysorbate 80-coated nanoparticles Pharm. Res. 16 10 1999 1564 1569 (Pubitemid 29510553)
43. S.A. Kulkarni, and S.S. Feng Effects of surface modification on delivery efficiency of biodegradable nanoparticles across the blood-brain barrier Nanomedicine (Lond.) 6 2 2011 377 394
44. C.X. Wang et al. Antitumor effects of polysorbate-80 coated gemcitabine polybutylcyanoacrylate nanoparticles in vitro and its pharmacodynamics in vivo on C6 glioma cells of a brain tumor model Brain Res. 1261 2009 91 99
45. A. Ambruosi et al. Influence of surfactants, polymer and doxorubicin loading on the anti-tumour effect of poly(butyl cyanoacrylate) nanoparticles in a rat glioma model J. Microencapsul. 23 5 2006 582 592 (Pubitemid 44446597)
46. B. Petri et al. Chemotherapy of brain tumour using doxorubicin bound to surfactant-coated poly(butyl cyanoacrylate) nanoparticles: revisiting the role of surfactants J. Control. Release 117 1 2007 51 58 (Pubitemid 46164866)
47. J. Zhou et al. Highly penetrative, drug-loaded nanocarriers improve treatment of glioblastoma Proc. Natl. Acad. Sci. U. S. A. 110 29 2013 11751 11756
48. F. Alexis et al. Nanoparticle technologies for cancer therapy Handb. Exp. Pharmacol. 197 2010 55 86
49. R.J. Diaz et al. Focused ultrasound delivery of Raman nanoparticles across the blood-brain barrier: potential for targeting experimental brain tumors Nanomedicine 10 5 2014 1075 1087
50. T. Nhan et al. Drug delivery to the brain by focused ultrasound induced blood-brain barrier disruption: quantitative evaluation of enhanced permeability of cerebral vasculature using two-photon microscopy J. Control. Release 172 1 2013 274 280
51. C.W. Burke et al. Markedly enhanced skeletal muscle transfection achieved by the ultrasound-targeted delivery of non-viral gene nanocarriers with microbubbles J. Control. Release 162 2 2012 414 421
52. E.E. Konofagou Optimization of the ultrasound-induced blood-brain barrier opening Theranostics 2 12 2012 1223 1237
53. X. Guo et al. Investigation on the inertial cavitation threshold and shell properties of commercialized ultrasound contrast agent microbubbles J. Acoust. Soc. Am. 134 2 2013 1622 1631
54. Z. Fan, D. Chen, and C.X. Deng Improving ultrasound gene transfection efficiency by controlling ultrasound excitation of microbubbles J. Control. Release 170 3 2013 401 413
55. M. Gauthier, D. King, and W. O'Brien Influence of microbubble size on postexcitation collapse thresholds for single ultrasound contrast agents using double passive cavitation detection IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60 5 2013 877 879
56. J.A. Feshitan et al. Microbubble size isolation by differential centrifugation J. Colloid Interface Sci. 329 2 2009 316 324
57. J.J. Choi et al. Molecules of various pharmacologically-relevant sizes can cross the ultrasound-induced blood-brain barrier opening in vivo Ultrasound Med. Biol. 36 1 2010 58 67
58. A. Hoffmann et al. High and low molecular weight fluorescein isothiocyanate (FITC)-dextrans to assess blood-brain barrier disruption: technical considerations Transl. Stroke Res. 2 1 2011 106 111
59. N. McDannold et al. MRI investigation of the threshold for thermally induced blood-brain barrier disruption and brain tissue damage in the rabbit brain Magn. Reson. Med. 51 5 2004 913 923 (Pubitemid 38580603)