Functionalization of liposomes with ApoE-derived peptides at different density affects cellular uptake and drug transport across a blood-brain barrier model

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 7, Issue 5, 2011, Pages 551-559

  Re, Francesca ^a   Cambianica, Ilaria ^a   Zona, Cristiano ^a   Sesana, Silvia ^a   Gregori, Maria ^a   Rigolio, Roberta ^a   La Ferla, Barbara ^a   Nicotra, Francesco ^a   Forloni, Gianluigi ^b   Cagnotto, Alfredo ^b   Salmona, Mario ^b   Masserini, Massimo ^a   Sancini, Giulio ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

ApoE peptide; Blood brain barrier; Brain endothelial cells; Nanoliposomes

Indexed keywords

APOE PEPTIDE; APOLIPOPROTEIN E (APOE); BLOOD-BRAIN BARRIER; BLOOD-BRAIN BARRIER MODELS; BRAIN CAPILLARY ENDOTHELIAL CELLS; CELL MONOLAYERS; CELLULAR UPTAKE; CURCUMIN DERIVATIVES; DRUG TRANSPORT; FLUORESCENCE ACTIVATED CELL SORTING; FUNCTIONALIZATIONS; FUNCTIONALIZED; NANOCARRIERS; NANOLIPOSOMES; NEURODEGENERATIVE; PEPTIDE FRAGMENTS; VARIOUS DENSITIES;

CONFOCAL MICROSCOPY; DIMERS; DRUG DELIVERY; ENDOTHELIAL CELLS; LIPOSOMES; MONOLAYERS; MONOMERS; NEURODEGENERATIVE DISEASES; PEPTIDES; PHOSPHOLIPIDS;

BLOOD;

APOLIPOPROTEIN E; CURCUMIN; CURCUMIN DERIVATIVE; LIPOSOME; NANOLIPOSOME; TRITIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BLOOD BRAIN BARRIER; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG TRANSPORT; DRUG UPTAKE; FLUORESCENCE ACTIVATED CELL SORTER; ISOTOPE LABELING; NANOPHARMACEUTICS; NONHUMAN; RAT;

ANIMALS; APOLIPOPROTEINS E; BIOLOGICAL TRANSPORT; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE; CURCUMIN; DRUG DELIVERY SYSTEMS; ENDOTHELIAL CELLS; FLOW CYTOMETRY; HUMANS; LIPOSOMES; MICROSCOPY, CONFOCAL; NANOPARTICLES; PERMEABILITY; RATS;

EID: 80053209371     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2011.05.004     Document Type: Article

References (46)

1. Wolburg H, Noell S, Mack A, Wolburg-Buchholz K, Fallier-Becker P Brain endothelial cells and the glio-vascular complex. Cell Tissue Res 2009, 335:75-96.
2. Omidi Y, Barar J, Ahmadian S, Heidari HR, Gumbleton M Characterization and astrocytic modulation of system L transporters in brain microvasculature endothelial cells. Cell Biochem Funct 2008, 26:381-391.
3. de Boer AG, van der Sandt IC, Gaillard PJ The role of drug transporters at the blood-brain barrier. Annu Rev Pharmacol Toxicol 2003, 43:629-656.
4. Deeken JF, Löscher W The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin Cancer Res 2007, 13:1663-1674.
5. Cerletti A, Drewe J, Fricker G, Eberle AN, Huwyler J Endocytosis and transcytosis of an immunoliposome-based brain drug delivery system. J Drug Target 2000, 8:435-446.
6. Markoutsa E, Pampalakis G, Niarakis A, Romero IA, Weksler B, Couraud PO, et al. Uptake and permeability studies of BBB-targeting immunoliposomes using the hCMEC/D3 cell line. Eur J Pharm Biopharm 2011, 77:265-274.
7. Dehouck B, Dehouck MP, Fruchart JC, Cecchelli R Upregulation of the low-density lipoprotein receptor at the blood-brain barrier: intercommunications between brain capillary endothelial cells and astrocytes. J Cell Biol 1994, 126:465-473.
8. Dehouck B, Fenart L, Dehouck MP, Pierce A, Torpier G, Cecchelli R A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier. J Cell Biol 1997, 138:877-889.
9. Mims MP, Darnule AT, Tovar RW, Pownall HJ, Sparrow DA, Sparrow JT, et al. A nonexchangeable apolipoprotein E peptide that mediates binding to the low-density lipoprotein receptor. J Biol Chem 1994, 269:20539-20547.
10. Datta G, Chaddha M, Garber DW, Chung BH, Tytler EM, Dashti N, et al. The receptor binding domain of apolipoprotein E, linked to a model class A amphipathic helix, enhances internalization and degradation of LDL by fibroblasts. Biochemistry 2000, 39:213-220.
11. Dyer CA, Cistola DP, Parry GC, Curtiss LK Structural features of synthetic peptides of apolipoprotein E that bind the LDL receptor. J Lipid Res 1995, 36:80-88.
12. Wang X, Ciraolo G, Morris R, Gruenstein E Identification of a neuronal endocytic pathway activated by an apolipoprotein E (apoE) receptor binding peptide. Brain Res 1997, 778:6-15.
13. Sauer I, Dunay IR, Weisgraber K, Bienert M, Dathe M An apolipoprotein E-derived peptide mediates uptake of sterically stabilized liposomes into brain capillary endothelial cells. Biochemistry 2005, 44:2021-2029.
14. Datta G, Garber DW, Chung BH, Chaddha M, Dashti N, Bradley WA, et al. Cationic domain 141-150 of apoE covalently linked to a class A amphipathic helix enhances atherogenic lipoprotein metabolism in vitro and in vivo. J Lipid Res 2001, 42:959-966.
15. Brooks H, Lebleu B, Vivès E Tat peptide-mediated cellular delivery: back to basics. Adv Drug Deliv Rev 2005, 57:559-577.
16. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 1999, 285:1569-1572.
17. Eguchi A, Akuta T, Okuyama H, Senda T, Yokoi H, Inokuchi H, et al. Protein transduction domain of HIV-1 Tat protein promotes efficient delivery of DNA into mammalian cells. J Biol Chem 2001, 276:26204-26210.
18. Tian W, Ying X, Du J, Guo J, Men Y, Zhang Y, et al. Enhanced efficacy of functionalized epirubicin liposomes in treating brain glioma-bearing rats. Eur J Pharm Sci 2010, 41:232-243.
19. Begley DJ, Lechardeur D, Chen ZD, Rollinson C, Bardoul M, Roux F, et al. Functional expression of P-glycoprotein in an immortalised cell line of rat brain endothelial cells, RBE4. J Neurochem 1996, 67:988-995.
20. Roux F, Couraud PO Rat brain endothelial cell lines for the study of blood-brain barrier permeability and transport functions. Cell Mol Neurobiol 2005, 25:41-58.
21. Zona C, La Ferla B. Synthesis of labeled curcumin derivatives as tools for in vitro blood brain barrier trafficking studies. J Labelled Comp Radiopharm. In press.
22. Gobbi M, Re F, Canovi M, Beeg M, Gregori M, Sesana S, et al. Lipid-based nanoparticles with high binding affinity for amyloid-beta-1-42 peptide. Biomaterials 2010, 31:6519-6529.
23. Bartlett GR Phosphorus assay in column chromatography. J Biol Chem 1959, 234:466-468.
24. Palestini P, Botto L, Guzzi F, Calvi C, Ravasi D, Masserini M Developmental changes in the protein composition of sphingolipid- and cholesterol-enriched membrane domains of rat cerebellar granule cells. J Neurosci Res 2002, 67:729-738.
25. Roux F, Durieu-Trautmann O, Chaverot N, Claire M, Mailly P, Bourre JM, et al. Regulation of gamma-glutamyl transpeptidase and alkaline phosphatase activities in immortalized rat brain microvessel endothelial cells. J Cell Physiol 1994, 159:101-113.
26. Denizot F, Lang R Rapid colorimetric assay for cell growth and survival: modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 1986, 89:271-277.
27. Pardridge WM, Triguero D, Yang J, Cancilla PA Comparison of in vitro and in vivo models of drug transcytosis through the blood-brain barrier. J Pharmacol Exp Ther 1990, 253:884-891.
28. Bickel U How to measure drug transport across the blood-brain barrier. J Am Soc Exp Neurother 2005, 2:15-26.
29. Deli MA, Abraham CS, Kataoka Y, Niwa M Permeability studies on in vitro blood-brain barrier models: physiology, pathology and pharmacology. Cell Mol Neurobiol 2005, 25:59-127.
30. Cortesi R, Esposito E, Menegatti E, Gambari R, Nastruzzi CC Effect of cationic liposome composition on in vitro cytotoxicity and protective effect on carried DNA. Int J Pharm 1996, 139:69-78.
31. Smistad G, Jacobsen J, Sande SA Multivariate toxicity screening of liposomal formulations on a human buccal cell line. Int J Pharm 2007, 330:14-22.
32. Mayhev E, Ito M, Lazo R Toxicity of non-drug-containing liposomes for cultured human cells. Exp Cell Res 1987, 171:195-202.
33. Boehlke L, Winter JN Sphingomyelin/cholesterol liposomal vincristine: a new formulation for an old drug. Expert Opin Biol Ther 2006, 6:409-415.
34. Thomas DA, Sarris AH, Cortes J, Faderl S, O'Brien S, Giles FJ, et al. Phase II study of sphingosomal vincristine in patients with recurrent or refractory adult acute lymphocytic leukemia. Cancer 2006, 106:120-127.
35. Adams DH, Joyce G, Richardson VJ, Ryman BE, Wisniewski HM Liposome toxicity in the mouse central nervous system. J Neurol Sci 1977, 31:173-179.
36. Pardridge WM Drug and gene targeting to the brain with Trojan horses. Nature Rev Drug Discov 2000, 1:131-139.
37. Reichel A, Abbott NJ, Begley DJ Evaluation of the RBE4 cell line to explore carrier-mediated drug delivery to the CNS via the L-system amino acid transporter at the blood-brain barrier. J Drug Target 2002, 10:277-283.
38. Re F, Airoldi C, Zona C, Masserini M, La Ferla B, Quattrocchi N, et al. Beta amyloid aggregation inhibitors: small molecules as candidate drugs for therapy of Alzheimer's disease. Curr Med Chem 2010, 17:2990-3006.
39. Zhang C, Browne A, Child D, Tanzi RE Curcumin decreases amyloid-beta peptide levels by attenuating the maturation of amyloid-beta precursor protein. J Biol Chem 2010, 285:28472-28480.
40. Mourtas S, Canovi M, Zona C, Aurilia D, Niarakis A, La Ferla B, et al. Curcumin-decorated NL with very high affinity for amyloid-β1-42 peptide. Biomaterials 2011, 32:1635-1645.
41. Sharma RA, Gescher AJ, Steward WP Curcumin: the story so far. Eur J Cancer 2005, 41:1955-1968.
42. Narlawar R, Pickhardt M, Leuchtenberger S, Baumann K, Krause S, Dyrks T, et al. Curcumin-derived pyrazoles and isoxazoles: Swiss army knives or blunt tools for Alzheimer's disease?. Chem Med Chem 2008, 3:165-172.
43. Ono K, Hasegawa K, Naiki H, Yamada M Curcumin has potent anti-amyloidogenic effects for Alzheimer's beta-amyloid fibrils in vitro. J Neurosci Res 2004, 75:742-750.
44. Garcia-Alloza M, Borrelli LA, Rozkalne A, Hyman BT, Bacskai BJ Curcumin labels amyloid pathology in vivo, disrupts existing plaques, and partially restores distorted neurites in an Alzheimer mouse model. J Neurochem 2007, 102:1095-1104.
45. Khumsupan P, Ramirez R, Khumsupan D, Narayanaswami V Apolipoprotein E LDL receptor-binding domain-containing high-density lipoprotein: a nanovehicle to transport curcumin, an antioxidant and anti-amyloid bioflavonoid. Biochim Biophys Acta. 1808, 2011:352-359.
46. Ray B, Bisht S, Maitra A, Maitra A, Lahiri DK Neuroprotective and neurorescue effects of a novel polymeric nanoparticle formulation of curcumin (NanoCurc®) in the neuronal cell culture and animal model: implications for Alzheimer's disease. J Alzheimers Dis 2011, 23:61-77.