Uptake mechanism of ApoE-modified nanoparticles on brain capillary endothelial cells as a blood-brain barrier model

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Wagner, Sylvia ^a   Zensi, Anja ^b   Wien, Sascha L ^a   Tschickardt, Sabrina E ^c   Maier, Wladislaw ^c   Vogel, Tikva ^d   Worek, Franz ^e   Pietrzik, Claus U ^c   Kreuter, Jörg ^b   von Briesen, Hagen ^a  

^a FRAUNHOFER INSTITUTE FOR BIOMEDICAL ENGINEERING   (Germany)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^d NATIONAL CANCER INSTITUTE   (United States)

^e Bundeswehr Institute of Pharmacology und Toxicology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; NANOPARTICLE; SERUM ALBUMIN;

ACTIVE TRANSPORT; ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CAPILLARY ENDOTHELIUM; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; ENDOTHELIUM CELL; FLOW CYTOMETRY; IN VITRO STUDY; MOUSE; NONHUMAN; PASSIVE TRANSPORT; TRANSPORT KINETICS; ANIMAL; BRAIN; BRAIN DISEASE; CHEMISTRY; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG DELIVERY SYSTEM; HUMAN; METABOLISM; METHODOLOGY; NANOTECHNOLOGY; PROTEIN BINDING; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE; VASCULARIZATION;

ANIMALS; APOLIPOPROTEINS E; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; BRAIN DISEASES; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; ENDOTHELIAL CELLS; FLOW CYTOMETRY; HUMANS; MICE; MICROSCOPY, CONFOCAL; NANOPARTICLES; NANOTECHNOLOGY; PROTEIN BINDING; SERUM ALBUMIN;

EID: 84857747571     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032568     Document Type: Article

References (53)

1. Pardridge WM, (2005) The blood-brain barrier: bottleneck in brain drug development. NeuroRx 2: 3-14.
2. Crone C, Olesen SP, (1982) Electrical resistance of brain microvascular endothelium. Brain Res 241: 49-55.
3. Butt AM, Jones HC, Abbott NJ, (1990) Electrical resistance across the blood-brain barrier in anaesthetized rats: a developmental study. J Physiol 429: 47-62.
4. Rubin LL, Staddon JM, (1999) The cell biology of the blood-brain barrier. Annu Rev Neurosci 22: 11-28.
5. Begley DJ, (2003) Understanding and circumventing the blood-brain barrier. Acta Paediatr Suppl 92: 83-91.
6. Begley DJ, (2004) Delivery of therapeutic agents to the central nervous system: the problems and the possibilities. Pharmacol Ther 104: 29-45.
7. Pardridge WM, (1997) Drug delivery to the brain. J Cereb Blood Flow Metab 17: 713-731.
8. Pardridge WM, (1988) Recent advances in blood-brain barrier transport. Annu Rev Pharmacol Toxicol 28: 25-39.
9. Neuwelt EA, Barnett PA, (1989) Implications of the Blood-Brain Barrier and its Manipulation New York Springer.
10. Calvo P, Gouritin B, Chacun H, Desmaele D, D'Angelo J, et al. (2001) Long-circulating PEGylated polycyanoacrylate nanoparticles as new drug carrier for brain delivery. Pharm Res 18: 1157-1166.
11. Kreuter J, Alyautdin RN, Kharkevich DA, Ivanov AA, (1995) Passage of peptides through the blood-brain barrier with colloidal polymer particles (nanoparticles). Brain Res 674: 171-174.
12. Calvo P, Gouritin B, Brigger I, Lasmezas C, Deslys J, et al. (2001) PEGylated polycyanoacrylate nanoparticles as vector for drug delivery in prion diseases. J Neurosci Methods 111: 151-155.
13. Gulyaev AE, Gelperina SE, Skidan IN, Antropov AS, Kivman GY, et al. (1999) Significant transport of doxorubicin into the brain with polysorbate 80-coated nanoparticles. Pharm Res 16: 1564-1569.
14. Hekmatara T, Bernreuther C, Khalansky AS, Theisen A, Weissenberger J, et al. (2009) Efficient systemic therapy of rat glioblastoma by nanoparticle-bound doxorubicin is due to antiangiogenic effects. Clin Neuropathol 28: 153-164.
15. Steiniger SC, Kreuter J, Khalansky AS, Skidan IN, Bobruskin AI, et al. (2004) Chemotherapy of glioblastoma in rats using doxorubicin-loaded nanoparticles. Int J Cancer 109: 759-767.
16. Alyautdin R, Gothier D, Petrov V, Kharkevich D, Kreuter J, (1995) Analgesic activity of the hexapeptide dalargin adsorbed on the surface of polysorbate 80-coated poly(butyl cyanoacrylate) nanoparticles. Eur J Pharm Biopharm 41: 44-48.
17. Schroeder U, Sommerfeld P, Ulrich S, Sabel BA, (1998) Nanoparticle technology for delivery of drugs across the blood-brain barrier. J Pharm Sci 87: 1305-1307.
18. Alyautdin RN, Petrov VE, Langer K, Berthold A, Kharkevich DA, et al. (1997) Delivery of loperamide across the blood-brain barrier with polysorbate 80-coated polybutylcyanoacrylate nanoparticles. Pharm Res 14: 325-328.
19. Kreuter J, Hekmatara T, Dreis S, Vogel T, Gelperina S, et al. (2007) Covalent attachment of apolipoprotein A-I and apolipoprotein B-100 to albumin nanoparticles enables drug transport into the brain. J Control Release 118: 54-58.
20. Ulbrich K, Hekmatara T, Herbert E, Kreuter J, (2009) Transferrin- and transferrin-receptor-antibody-modified nanoparticles enable drug delivery across the blood-brain barrier (BBB). Eur J Pharm Biopharm 71: 251-256.
21. Alyautdin RN, Tezikov EB, Ramge P, Kharkevich DA, Begley DJ, et al. (1998) Significant entry of tubocurarine into the brain of rats by adsorption to polysorbate 80-coated polybutylcyanoacrylate nanoparticles: an in situ brain perfusion study. J Microencapsul 15: 67-74.
22. Friese A, Seiller E, Quack G, Lorenz B, Kreuter J, (2000) Increase of the duration of the anticonvulsive activity of a novel NMDA receptor antagonist using poly(butylcyanoacrylate) nanoparticles as a parenteral controlled release system. Eur J Pharm Biopharm 49: 103-109.
23. Rhaese S, von Briesen H, Rubsamen-Waigmann H, Kreuter J, Langer K, (2003) Human serum albumin-polyethylenimine nanoparticles for gene delivery. J Control Release 92: 199-208.
24. Petri B, Bootz A, Khalansky A, Hekmatara T, Muller R, et al. (2007) Chemotherapy of brain tumour using doxorubicin bound to surfactant-coated poly(butyl cyanoacrylate) nanoparticles: revisiting the role of surfactants. J Control Release 117: 51-58.
25. Kreuter J, (2001) Nanoparticulate systems for brain delivery of drugs. Adv Drug Deliv Rev 47: 65-81.
26. Lück M, (1997) Plasmaproteinadsorption als möglicher Schlüsselfaktor für eine kontrollierte Arzneistoffapplikation mit partikulären Trägern Berlin Freie Universität Berlin.
27. Kreuter J, Shamenkov D, Petrov V, Ramge P, Cychutek K, et al. (2002) Apolipoprotein-mediated transport of nanoparticle-bound drugs across the blood-brain barrier. J Drug Target 10: 317-325.
28. Zensi A, Begley D, Pontikis C, Legros C, Mihoreanu L, et al. (2010) Human serum albumin nanoparticles modified with apolipoprotein A-I cross the blood-brain barrier and enter the rodent brain. J Drug Target 18: 842-848.
29. Kreuter J, (2006) Nanoparticles as drug delivery systems for the brain. In: Benita S, editors. Microencapsulation: Methods and Industrial Application New York Taylor and Francis pp. 689-706.
30. Kreuter J, (2006) Nanoparticulate carriers for drug delivery to the brain. In: Torchilin VP, editors. Nanoparticulates as Drug Carrier London Imperial College Press pp. 527-547.
31. Kreuter J, Ramge P, Petrov V, Hamm S, Gelperina SE, et al. (2003) Direct evidence that polysorbate-80-coated poly(butylcyanoacrylate) nanoparticles deliver drugs to the CNS via specific mechanisms requiring prior binding of drug to the nanoparticles. Pharm Res 20: 409-416.
32. Michaelis K, Hoffmann MM, Dreis S, Herbert E, Alyautdin RN, et al. (2006) Covalent linkage of apolipoprotein e to albumin nanoparticles strongly enhances drug transport into the brain. J Pharmacol Exp Ther 317: 1246-1253.
33. Zensi A, Begley D, Pontikis C, Legros C, Mihoreanu L, et al. (2009) Albumin nanoparticles targeted with Apo E enter the CNS by transcytosis and are delivered to neurones. J Control Release 137: 78-86.
34. Vogel T, Weisgraber KH, Zeevi MI, Ben-Artzi H, Levanon AZ, et al. (1985) Human apolipoprotein E expression in Escherichia coli: structural and functional identity of the bacterially produced protein with plasma apolipoprotein E. Proc Natl Acad Sci U S A 82: 8696-8700.
35. Langer K, Balthasar S, Vogel V, Dinauer N, von Briesen H, et al. (2003) Optimization of the preparation process for human serum albumin (HSA) nanoparticles. Int J Pharm 257: 169-180.
36. Weber C, Kreuter J, Langer K, (2000) Desolvation process and surface characteristics of HSA-nanoparticles. Int J Pharm 196: 197-200.
37. Weber C, Coester C, Kreuter J, Langer K, (2000) Desolvation process and surface characterisation of protein nanoparticles. Int J Pharm 194: 91-102.
38. Michaelis K, Hoffmann MM, Dreis S, Herbert E, Alyautdin RN, et al. (2006) Covalent linkage of apolipoprotein e to albumin nanoparticles strongly enhances drug transport into the brain. J Pharmacol Exp Ther 317: 1246-1253.
39. Pietrzik CU, Busse T, Merriam DE, Weggen S, Koo EH, (2002) The cytoplasmic domain of the LDL receptor-related protein regulates multiple steps in APP processing. EMBO J 21: 5691-5700.
40. Omidi Y, Campbell L, Barar J, Connell D, Akhtar S, et al. (2003) Evaluation of the immortalised mouse brain capillary endothelial cell line, b.End3, as an in vitro blood-brain barrier model for drug uptake and transport studies. Brain Res 990: 95-112.
41. Hertz J, Marchang P, (2003) Coaxing the LDL receptor family into the fold. Cell 112: 289-292.
42. Hatters DM, Peters-Libeu CA, Weisgraber KH, (2006) Apolipoprotein E structure: insights into function. Trends Biochem Sci 31: 445-454.
43. Innerarity TL, Pitas RE, Mahley RW, (1979) Binding of arginine-rich (E) apoprotein after recombination with phospholipid vesicles to the low density lipoprotein receptors of fibroblasts. J Biol Chem 254: 4186-4190.
44. Peters-Libeu CA, Newhouse Y, Hatters DM, Weisgraber KH, (2006) Model of biologically active apolipoprotein E bound to dipalmitoylphosphatidylcholine. J Biol Chem 281: 1073-1079.
45. Weisgraber KH, (1994) Apolipoprotein E: structure-function relationships. Adv Protein Chem 45: 249-302.
46. Bu G, Geuze HJ, Strous GJ, Schwartz AL, (1995) 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J 14: 2269-2280.
47. Bu G, Rennke S, (1996) Receptor-associated protein is a folding chaperone for low density lipoprotein receptor-related protein. J Biol Chem 271: 22218-22224.
48. Herz J, Strickland DK, (2001) LRP: a multifunctional scavenger and signaling receptor. J Clin Invest 108: 779-784.
49. Hasadsri L, Kreuter J, Hattori H, Iwasaki T, George JM, (2009) Functional protein delivery into neurons using polymeric nanoparticles. J Biol Chem 284: 6972-6981.
50. Leupold E, Nikolenko H, Beyermann M, Dathe M, (2008) Insight into the role of HSPG in the cellular uptake of apolipoprotein E-derived peptide micelles and liposomes. Biochim Biophys Acta 1778: 2781-2789.
51. Leupold E, Nikolenko H, Dathe M, (2009) Apolipoprotein E peptide-modified colloidal carriers: the design determines the mechanism of uptake in vascular endothelial cells. Biochim Biophys Acta 1788: 442-449.
52. Sauer I, Dunay IR, Weisgraber K, Bienert M, Dathe M, (2005) An apolipoprotein E-derived peptide mediates uptake of sterically stabilized liposomes into brain capillary endothelial cells. Biochemistry 44: 2021-2029.
53. Sauer I, Nikolenko H, Keller S, Abu Ajaj K, Bienert M, et al. (2006) Dipalmitoylation of a cellular uptake-mediating apolipoprotein E-derived peptide as a promising modification for stable anchorage in liposomal drug carriers. Biochim Biophys Acta 1758: 552-561.