Translocation of LRP1 targeted carbon nanotubes of different diameters across the blood-brain barrier in vitro and in vivo

Journal of Controlled Release

Volumn 225, Issue , 2016, Pages 217-229

  Kafa, Houmam ^a   Wang, Julie Tzu Wen ^a   Rubio, Noelia ^a   Klippstein, Rebecca ^a   Costa, Pedro M ^a   Hassan, Hatem A F M ^a   Sosabowski, Jane K ^b   Bansal, Sukhvinder S ^a   Preston, Jane E ^a   Abbott, N Joan ^a   Al Jamal, Khuloud T ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Angiopep 2; Brain delivery; Carbon nanotube; Nanomedicine; Targeting; Transcytosis

Indexed keywords

BLOOD; CARBON NANOTUBES; ENDOTHELIAL CELLS; LIGANDS; MEDICAL NANOTECHNOLOGY; NANOPARTICLES; NANOTUBES; NEURODEGENERATIVE DISEASES; NUCLEAR MEDICINE; TUMORS; YARN;

ANGIOPEP-2; BRAIN DELIVERY; DRUG DELIVERY APPLICATIONS; FUNCTIONALISED MULTI-WALLED CARBON NANOTUBES; INTRAVENOUS ADMINISTRATION; LOW DENSITY LIPOPROTEIN RECEPTORS; TARGETING; TRANSCYTOSIS;

MULTIWALLED CARBON NANOTUBES (MWCN);

ANGIOPEP 2; LIGAND; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MULTI WALLED NANOTUBE; UNCLASSIFIED DRUG; ANGIOPEP-2; CARBON NANOTUBE; DRUG CARRIER; LOW DENSITY LIPOPROTEIN RECEPTOR; LRP1 PROTEIN, MOUSE; PEPTIDE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; DRUG CONJUGATION; DRUG DELIVERY SYSTEM; FEMALE; GAMMA SCINTIGRAPHY; GLIOMA; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; MOUSE; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; SPECT SCANNER; ANIMAL; BRAIN; BRAIN TUMOR; C57BL MOUSE; CELL CULTURE; CHEMISTRY; COCULTURE; ENDOTHELIUM CELL; METABOLISM; PIG; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE; WISTAR RAT;

ANIMALS; ASTROCYTES; BIOLOGICAL TRANSPORT; BRAIN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; DRUG CARRIERS; ENDOTHELIAL CELLS; FEMALE; GLIOMA; MICE, INBRED C57BL; NANOTUBES, CARBON; PEPTIDES; RATS, WISTAR; RECEPTORS, LDL; SWINE; TUMOR SUPPRESSOR PROTEINS;

EID: 84957559339     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2016.01.031     Document Type: Article

References (40)

1. I. Brasnjevic, H.W. Steinbusch, C. Schmitz, and P. Martinez-Martinez European NanoBioPharmaceutics research I. Delivery of peptide and protein drugs over the blood-brain barrier Prog. Neurobiol. 87 2009 212 251
2. S. Wohlfart, S. Gelperina, and J. Kreuter Transport of drugs across the blood-brain barrier by nanoparticles J. Control. Release 161 2012 264 273
3. N. Saito, Y. Usui, K. Aoki, N. Narita, M. Shimizu, K. Hara, and et al. Carbon nanotubes: biomaterial applications Chem. Soc. Rev. 38 2009 1897 1903
4. H.J. Lee, J. Park, O.J. Yoon, H.W. Kim, Y. Lee do, H. Kim do, and et al. Amine-modified single-walled carbon nanotubes protect neurons from injury in a rat stroke model Nat. Nanotechnol. 6 2011 121 125
5. K.T. Al-Jamal, L. Gherardini, G. Bardi, A. Nunes, C. Guo, C. Bussy, and et al. Functional motor recovery from brain ischemic insult by carbon nanotube-mediated siRNA silencing Proc. Natl. Acad. Sci. U. S. A. 108 2011 10952 10957
6. D. Zhao, D. Alizadeh, L. Zhang, W. Liu, O. Farrukh, E. Manuel, and et al. Carbon nanotubes enhance CpG uptake and potentiate antiglioma immunity Clin. Cancer Res. 17 2011 771 782
7. H. Kafa, J.T.-W. Wang, N. Rubio, K. Venner, G. Anderson, E. Pach, and et al. The interaction of carbon nanotubes with an in vitro blood-brain barrier model and mouse brain in vivo Biomaterials 53 2015 437 452
8. M. Demeule, A. Regina, C. Che, J. Poirier, T. Nguyen, R. Gabathuler, and et al. Identification and design of peptides as a new drug delivery system for the brain J. Pharmacol. Exp. Ther. 324 2008 1064 1072
9. A.P. Lillis, I. Mikhailenko, and D.K. Strickland Beyond endocytosis: LRP function in cell migration, proliferation and vascular permeability J. Thromb. Haemost. 3 2005 1884 1893
10. Y. Bertrand, J.C. Currie, J. Poirier, M. Demeule, A. Abulrob, D. Fatehi, and et al. Influence of glioma tumour microenvironment on the transport of ANG1005 via low-density lipoprotein receptor-related protein 1 Br. J. Cancer 105 2011 1697 1707
11. M. Demeule, J.C. Currie, Y. Bertrand, C. Che, T. Nguyen, A. Regina, and et al. Involvement of the low-density lipoprotein receptor-related protein in the transcytosis of the brain delivery vector angiopep-2 J. Neurochem. 106 2008 1534 1544
12. M. Demeule, N. Beaudet, A. Regina, E. Besserer-Offroy, A. Murza, P. Tetreault, and et al. Conjugation of a brain-penetrant peptide with neurotensin provides antinociceptive properties J. Clin. Invest. 124 2014 1199 1213
13. K. Shao, R. Huang, J. Li, L. Han, L. Ye, J. Lou, and et al. Angiopep-2 modified PE-PEG based polymeric micelles for amphotericin B delivery targeted to the brain J. Control. Release 147 2010 118 126
14. W.L. Ke, K. Shao, R.Q. Huang, L. Han, Y. Liu, J.F. Li, and et al. Gene delivery targeted to the brain using an angiopep-conjugated polyethyleneglycol-modified polyamidoamine dendrimer Biomaterials 30 2009 6976 6985
15. S. Ruan, M. Yuan, L. Zhang, G. Hu, J. Chen, X. Cun, and et al. Tumor microenvironment sensitive doxorubicin delivery and release to glioma using angiopep-2 decorated gold nanoparticles Biomaterials 37 2015 425 435
16. K.-C. Mei, N. Rubio, Costa PM, H. Kafa, V. Abbate, F. Festy, and et al. Synthesis of double-clickable functionalised graphene oxide for biological applications Chem. Commun. 2015
17. J.T.W. Wang, C. Fabbro, E. Venturelli, C. Menard-Moyon, O. Chaloin, T. Da Ros, and et al. The relationship between the diameter of chemically-functionalized multi-walled carbon nanotubes and their organ biodistribution, profiles in vivo Biomaterials 35 2014 9517 9528
18. G. Pastorin, W. Wu, S. Wieckowski, J.P. Briand, K. Kostarelos, M. Prato, and et al. Double functionalisation of carbon nanotubes for multimodal drug delivery Chem. Commun. 1182-4 2006
19. K.T. Al-Jamal, A. Nunes, L. Methven, H. Ali-Boucetta, S. Li, F.M. Toma, and et al. Degree of chemical functionalization of carbon nanotubes determines tissue distribution and excretion profile Angew. Chem. Int. Ed. Engl. 51 2012 6389 6393
20. L.L. Rubin, D.E. Hall, S. Porter, K. Barbu, C. Cannon, H.C. Horner, and et al. A cell culture model of the blood-brain barrier J. Cell Biol. 115 1991 1725 1735
21. A. Patabendige, R.A. Skinner, L. Morgan, and N.J. Abbott A detailed method for preparation of a functional and flexible blood-brain barrier model using porcine brain endothelial cells Brain Res. 1521 2013 16 30
22. N.J. Abbott, D.E. Dolman, S. Drndarski, and S.M. Fredriksson An improved in vitro blood-brain barrier model: rat brain endothelial cells co-cultured with astrocytes Methods Mol. Biol. 814 2012 415 430
23. L.Z. Shi, and W. Zheng Early lead exposure increases the leakage of the blood-cerebrospinal fluid barrier, in vitro Hum. Exp. Toxicol. 26 2007 159 167
24. I. van Rooy, E. Mastrobattista, G. Storm, W.E. Hennink, and R.M. Schiffelers Comparison of five different targeting ligands to enhance accumulation of liposomes into the brain J. Control. Release 150 2011 30 36
25. K.S. Chu, W. Hasan, S. Rawal, M.D. Walsh, E.M. Enlow, J.C. Luft, and et al. Plasma, tumor and tissue pharmacokinetics of docetaxel delivered via nanoparticles of different sizes and shapes in mice bearing SKOV-3 human ovarian carcinoma xenograft Nanomedicine 9 2013 686 693
26. P. Poulin, and F.P. Theil A priori prediction of tissue: plasma partition coefficients of drugs to facilitate the use of physiologically-based pharmacokinetic models in drug discovery J. Pharm. Sci. 89 2000 16 35
27. R.Q. Huang, Y.H. Qu, W.L. Ke, J.H. Zhu, Y.Y. Pei, and C. Jiang Efficient gene delivery targeted to the brain using a transferrin-conjugated polyethyleneglycol-modified polyamidoamine dendrimer FASEB J. 21 2007 1117 1125
28. K. Ulbrich, T. Knobloch, and J. Kreuter Targeting the insulin receptor: nanoparticles for drug delivery across the blood-brain barrier (BBB) J. Drug Target. 19 2011 125 132
29. F.Y.J. Huang, W.J. Chen, W.Y. Lee, S.T. Lo, T.W. Lee, and J.M. Lo In vitro and in vivo evaluation of lactoferrin-conjugated liposomes as a novel carrier to improve the brain delivery Int. J. Mol. Sci. 14 2013 2862 2874
30. K. Ulbrich, T. Hekmatara, E. Herbert, and J. Kreuter Transferrin- and transferrin-receptor-antibody-modified nanoparticles enable drug delivery across the blood-brain barrier (BBB) Eur. J. Pharm. Biopharm. 71 2009 251 256
31. S. Wagner, A. Zensi, S.L. Wien, S.E. Tschickardt, W. Maier, T. Vogel, and et al. Uptake mechanism of ApoE-modified nanoparticles on brain capillary endothelial cells as a blood-brain barrier model PLoS One 7 2012
32. J. Herz, and D.K. Strickland LRP: a multifunctional scavenger and signaling receptor J. Clin. Investig. 108 2001 779 784
33. M.M.M. Wilhelmus, I. Otte-Höller, J.J.J. van Triel, R. Veerhuis, M.L.C. Maat-Schieman, G. Bu, and et al. Lipoprotein receptor-related protein-1 mediates amyloid-β-mediated cell death of cerebrovascular cells Am. J. Pathol. 171 2007 1989 1999
34. G. William Rebeck, J.S. Reiter, D.K. Strickland, and B.T. Hyman Apolipoprotein E in sporadic Alzheimer's disease: allelic variation and receptor interactions Neuron 11 1993 575 580
35. S.E. Gratton, P.A. Ropp, P.D. Pohlhaus, J.C. Luft, V.J. Madden, M.E. Napier, and et al. The effect of particle design on cellular internalization pathways Proc. Natl. Acad. Sci. U. S. A. 105 2008 11613 11618
36. H. Meng, S. Yang, Z. Li, T. Xia, J. Chen, Z. Ji, and et al. Aspect ratio determines the quantity of mesoporous silica nanoparticle uptake by a small GTPase-dependent macropinocytosis mechanism ACS Nano 5 2011 4434 4447
37. E. Afergan, H. Epstein, R. Dahan, N. Koroukhov, K. Rohekar, H.D. Danenberg, and et al. Delivery of serotonin to the brain by monocytes following phagocytosis of liposomes J. Control. Release 132 2008 84 90
38. Y. Yu, Z.Q. Pang, W. Lu, Q. Yin, H.L. Gao, and X.G. Jiang Self-assembled polymersomes conjugated with lactoferrin as novel drug carrier for brain delivery Pharm. Res. 29 2012 83 96
39. J. Ren, S. Shen, D. Wang, Z. Xi, L. Guo, Z. Pang, and et al. The targeted delivery of anticancer drugs to brain glioma by PEGylated oxidized multi-walled carbon nanotubes modified with angiopep-2 Biomaterials 33 2012 3324 3333
40. D. Palmieri, Q.R. Smith, P.R. Lockman, J. Bronder, B. Gril, A.F. Chambers, and et al. Brain metastases of breast cancer Breast Dis. 26 2006-2007 139 147