Liposomes bi-functionalized with phosphatidic acid and an ApoE-derived peptide affect Aβ aggregation features and cross the blood-brain-barrier: Implications for therapy of Alzheimer disease

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 10, Issue 7, 2014, Pages 1583-1590

  Bana, Laura ^a   Minniti, Stefania ^a   Salvati, Elisa ^a   Sesana, Silvia ^a   Zambelli, Vanessa ^a   Cagnotto, Alfredo ^c   Orlando, Antonina ^a   Cazzaniga, Emanuela ^a   Zwart, Rob ^b   Scheper, Wiep ^b   Masserini, Massimo ^a   Re, Francesca ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Abeta peptide; Alzheimer disease; ApoE peptide; Blood brain barrier; Liposomes

Indexed keywords

BLOOD; DISEASE CONTROL; MAMMALS; NANOSTRUCTURED MATERIALS; NEURODEGENERATIVE DISEASES; PEPTIDES; PLASMONS; SURFACE PLASMON RESONANCE;

AGGREGATION/DISAGGREGATION; ALZHEIMER DISEASE; ALZHEIMER'S DISEASE; AMYLOID-BETA PEPTIDES; BLOOD-BRAIN BARRIER; FUNCTIONALIZATIONS; PEPTIDE AGGREGATION; PHOSPHATIDIC ACIDS;

LIPOSOMES;

AMYLOID BETA PROTEIN; LIPOSOME; MODIFIED APOLIPOPROTEIN E DERIVED PEPTIDE PHOSPHATIDIC ACID LIPOSOME; NANOCARRIER; PENETRATION ENHANCING AGENT; PHOSPHATIDIC ACID; THIOFLAVINE; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; PEPTIDE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BIOCOMPATIBILITY; BLOOD BRAIN BARRIER; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MEMBRANE TRANSPORT; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN AGGREGATION; PROTEIN DEGRADATION; RADIOACTIVITY; SURFACE PLASMON RESONANCE; WESTERN BLOTTING; CHEMISTRY; HUMAN;

ALZHEIMER DISEASE; APOLIPOPROTEINS E; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; LIPOSOMES; PEPTIDES; PHOSPHATIDIC ACIDS; SURFACE PLASMON RESONANCE;

EID: 84912150441     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2013.12.001     Document Type: Article

References (40)

1. Povova J., Ambroz P., Bar M., Pavukova V., Sery O., Tomaskova H., et al. Epidemiological of and risk factors for Alzheimer's disease: a review. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2012, 156:108-114.
2. Serrano-Pozo A., Frosch M.P., Masliah E., Hyman B.T. Neuropathological alterations in Alzheimer disease. Cold Spring Harb Perspect Med 2011, 1:a006189.
3. Selkoe D.J. Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 2001, 3:75-80.
4. Findeis M.A. The role of amyloid beta peptide 42 in Alzheimer's disease. Pharmacol Ther 2007, 116:266-286.
5. Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., et al. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-754.
6. De Kimpe L., Scheper W. From alpha to omega with Abeta: targeting the multiple molecular appearances of the pathogenic peptide in Alzheimer's disease. Curr Med Chem 2010, 17:198-212.
7. Ono K., Hirohata M., Yamada M. Ferulic acid destabilizes preformed b-amyloid fibrils in vitro. Biochem Biophys Res Commun 2005, 336:444-449.
8. Feng Y., Wang X., Yang S., Wang Y., Zhang X., Du X.T., et al. Resveratrol inhibits beta-amyloid oligomeric cytotoxicity but does not prevent oligomer formation. Neurotoxicology 2009, 30:986-995.
9. Durairajan S.S.K., Yuan Q., Xie L., Chan W., Kum W., Koo I., et al. Salvianolic acid B inhibits Abeta fibril formation and disaggregates preformed fibrils and protects against Abeta-induced cytotoxicty. Neurochem Int 2008, 52:741-750.
10. Liu W.Y., Wang Z.B., Zhang L.C., Wei X., Li L. Tight junction in blood-brain barrier: an overview of structure, regulation, and regulator substances. CNS Neurosci Ther 2012, 18:609-615.
11. Potschka H. Targeting the brain-surmounting or bypassing the blood-brain barrier. Handb Exp Pharmacol 2010, 197:411-431.
12. Banks W.A. Developing drugs that can cross the blood-brain barrier: applications to Alzheimer's disease. BMC Neurosci 2008, 9(Suppl. 3):S2.
13. Fazil M., Shadab, Baboota S., Sahni J.K., Ali J. Nanotherapeutics for Alzheimer's disease (AD): Past, present and future. J Drug Target 2012, 20:97-113.
14. Re F., Gregori M., Masserini M. Nanotechnology for neurodegenerative disorders. Nanomedicine 2012, 8(Suppl. 1):S51-S58.
15. Gobbi M., Re F., Canovi M., Beeg M., Gregori M., Sesana S., et al. Lipid-based nanoparticles with high binding affinity for amyloid-beta1-42 peptide. Biomaterials 2010, 31:6519-6529.
16. Re F., Cambianica I., Zona C., Sesana S., Gregori M., Rigolio R., et al. Functionalization of liposomes with ApoE-derived peptides at different density affects cellular uptake and drug transport across a blood-brain barrier model. Nanomedicine 2011, 7:551-559.
17. Re F., Cambianica I., Sesana S., Salvati E., Cagnotto A., Salmona M., et al. Functionalization with ApoE-derived peptides enhances the interaction with brain capillary endothelial cells of nanoliposomes binding amyloid-beta peptide. J Biotechnol 2010, 156:341-346.
18. Le Droumaguet B., Nicolas J., Brambilla D., Mura S., Maksimenko A., De Kimpe L., et al. Versatile and efficient targeting using a single nanoparticulate platform: application to cancer and Alzheimer's disease. ACS Nano 2012, 6:5866-5879.
19. Taylor M., Moore S., Mourtas S., Niarakis A., Re F., Zona C., et al. Effect of curcumin-associated and lipid ligand-functionalized nanoliposomes on aggregation of the Alzheimer's Aβ peptide. Nanomedicine 2011, 7:541-550.
20. Dahlgren K.N., Manelli A.M., Stine W.B., Baker L.K., Krafft G.A., et al. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 2002, 277:32046-32053.
21. Yang T., Roder K.E., Abbruscato T.J. Evaluation of bEnd5 cell line as an in vitro model for the blood-brain barrier under normal and hypoxic/aglycemic conditions. J Pharm Sci 2007, 96:3196-3213.
22. Cecchelli R., Dehouck B., Descamps L., Fenart L., Buée-Scherrer V.V., Duhem C., et al. In vitro model for evaluating drug transport across the blood-brain barrier. Adv Drug Deliv Rev 1999, 36:165-178.
23. Omidi Y., Campbell L., Barar J., Connel D., Akhtar S., Gumbleton M. 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 2003, 990:95-112.
24. Markoutsa E., Pampalakis G., Niarakis A., Romero I.A., Weksler B., Couraud P.O., et al. Uptake and permeability studies of BBB-targeting immunoliposomes using the hCMEC/D3 cell line. Eur J Pharm Biopharm 2011, 77:265-274.
25. Sauer I., Dunay I.R., 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.
26. Garcia-Garcia E., Andrieux K., Gil S., Kim H.R., Le Doan T., Desmaële D., et al. A methodology to study intracellular distribution of nanoparticles in brain endothelial cells. Int J Pharm 2005, 298:310-314.
27. Wan L., Pooyan S., Hu P., Leibowitz M.J., Stein S., Sinko P.J. Peritoneal macrophage uptake, pharmacokinetics and biodistribution of macrophage-targeted PEG-fMLF (N-formyl-methionyl-leucyl-phenylalanine) nanocarriers for improving HIV drug delivery. Pharm Res 2007, 24:2110-2119.
28. Kanwar J.R., Sriramoju B., Kanwar R.K. Neurological disorders and therapeutics targeted to surmount the blood-brain barrier. Int J Nanomedicine 2012, 7:3259-3278.
29. Salvati E., Re F., Sesana S., Cambianica I., Sancini G., Masserini M., et al. Liposomes functionalized to overcome the blood-brain barrier and to target amyloid-β peptide: the chemical design affects the permeability across an in vitro model. Int J Nanomedicine 2013, 8:1749-1758.
30. Sancini G., Gregori M., Salvati E., Cambianica I., Re F., Ornaghi F., et al. Functionalization with TAT-peptide enhances blood-brain barrier crossing in vitro of nanoliposomes carrying a curcumin-derivative to bind amyloid-β peptide. Nanomed Nanotechnol 2013, 4:1-8.
31. Andersen A.J., Hashemi S.H., Galimberti G., Re F., Masserini M., et al. The interaction of complement system with abeta-binding liposomes: towards engineering of safer vesicles for the management of Alzheimer's disease. J Biotechnol 2010, 150:S97-S98.
32. Ahyayauch H., Raab M., Busto J.V., Andraka N., Arrondo J.L., et al. Binding of β-amyloid (1-42) peptide to negatively charged phospholipid membranes in the liquid-ordered state: modeling and experimental studies. Biophys J 2012, 103:453-463.
33. Datta G., Chaddha M., Garber D.W., Chung B.H., Tytler E.M., 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.
34. Martineau E., de Guzman J.M., Rodionova L., Kong X., Mayer P.M., et al. Investigation of the noncovalent interactions between anti-amyloid agents and amyloid beta peptides by ESI-MS. J Am Soc Mass Spectrom 2010, 21:1506-1514.
35. Brouillette J., Caillierez R., Zommer N., Alves-Pires C., Benilova I., et al. Neurotoxicity and memory deficits induced by soluble low-molecular-weight amyloid-β1-42 oligomers are revealed in vivo by using a novel animal model. J Neurosci 2012, 32:7852-7861.
36. Wu W.H., Liu Q., Sun X., Yu J.S., Zhao D.S., et al. Fibrillar seeds alleviate amyloid-β cytotoxicity by omitting formation of higher-molecular-weight oligomers. Biochem Biophys Res Commun 2013, 439:321-326.
37. Pinzón-Daza M., Garzón R., Couraud P., Romero I.A., Weksler B., Ghigo D., et al. The association of statins plus LDL receptor-targeted liposome-encapsulated doxorubicin increases in vitro drug delivery across blood-brain barrier cells. Br J Pharmacol 2012, 167:1431-1447.
38. Datta G., Chaddha M., Handattu S.P., Palgunachari M.N., Nayyar G., Garber D.W., et al. ApoE mimetic peptide reduces plasma lipid hydroperoxide content with a concomitant increase in HDL paraoxonase activity. Adv Exp Med Biol 2010, 660:1-4.
39. Markoutsa E., Papadia K., Clemente C., Flores O., Antimisiaris S.G. Anti-Aβ-MAb and dually decorated nanoliposomes: effect of Aβ1-42 peptides on interaction with hCMEC/D3 cells. Eur J Pharm Biopharm 2012, 81:49-56.
40. Matsuoka Y., Saito M., LaFrancois J., Saito M., Gaynor K., et al. Novel therapeutic approach for the treatment of Alzheimer's disease by peripheral administration of agents with an affinity to beta-amyloid. J Neurosci 2003, 23:29-33.