Lipoprotein-based nanoparticles rescue the memory loss of mice with alzheimer's disease by accelerating the clearance of amyloid-beta

ACS Nano

Volumn 8, Issue 3, 2014, Pages 2345-2359

  Song, Qingxiang ^a   Huang, Meng ^a   Yao, Lei ^a   Wang, Xiaolin ^a   Gu, Xiao ^a   Chen, Juan ^b   Chen, Jun ^c   Huang, Jialin ^a   Hu, Quanyin ^c   Kang, Ting ^c   Rong, Zhengxing ^a   Qi, Hong ^a   Zheng, Gang ^b   Chen, Hongzhuan ^a   Gao, Xiaoling ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF TORONTO   (Canada)

^c FUDAN UNIVERSITY   (China)

Author keywords

Alzheimer's disease; amyloid beta; apoliporpotein E; clearance; nanomedicine; reconstituted high density lipoprotein

Indexed keywords

BINDING ENERGY; BIOMIMETICS; DISEASE CONTROL; GLYCOPROTEINS; MEDICAL NANOTECHNOLOGY; NANOSTRUCTURES; NEURODEGENERATIVE DISEASES; TRANSMISSION ELECTRON MICROSCOPY;

ALZHEIMER'S DISEASE; AMYLOID BETAS; APOLIPORPOTEIN E; CLEARANCE; HIGH DENSITY LIPOPROTEIN;

LIPOPROTEINS;

AMYLOID BETA PROTEIN; APOLIPOPROTEIN E3; HIGH DENSITY LIPOPROTEIN; NANOPARTICLE;

ALZHEIMER DISEASE; ANIMAL; ARTICLE; ASTROCYTE; BRAIN; CHEMISTRY; DRUG EFFECT; KINETICS; MEMORY DISORDER; METABOLISM; MICROGLIA; MOUSE; NANOMEDICINE; PATHOLOGY; PATHOPHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; APOLIPOPROTEIN E3; ASTROCYTES; BRAIN; KINETICS; LIPOPROTEINS, HDL; MEMORY DISORDERS; MICE; MICROGLIA; NANOMEDICINE; NANOPARTICLES; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84896948757     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn4058215     Document Type: Article

References (60)

1. Serrano-Pozo, A.; Frosch, M. P.; Masliah, E.; Hyman, B. T. Neuropathological Alterations in Alzheimer Disease Cold Spring Harbor Perspect. Med. 2011, 1, a6189
2. Haass, C.; Kaether, C.; Thinakaran, G.; Sisodia, S. Trafficking and Proteolytic Processing of APP Cold Spring Harbor Perspect. Med. 2012, 2, a6270
3. Gilbert, B. J. The Role of Amyloid Beta in the Pathogenesis of Alzheimer's Disease J. Clin. Pathol. 2013, 66, 362-366
4. Brambilla, D.; Verpillot, R.; Le Droumaguet, B.; Nicolas, J.; Taverna, M.; Kona, J.; Lettiero, B.; Hashemi, S. H.; De Kimpe, L.; Canovi, M. PEGylated Nanoparticles Bind to and Alter Amyloid-Beta Peptide Conformation: Toward Engineering of Functional Nanomedicines for Alzheimer's Disease ACS Nano 2012, 6, 5897-5908
5. Liao, Y. H.; Chang, Y. J.; Yoshiike, Y.; Chang, Y. C.; Chen, Y. R. Negatively Charged Gold Nanoparticles Inhibit Alzheimer's Amyloid-Beta Fibrillization, Induce Fibril Dissociation, and Mitigate Neurotoxicity Small 2012, 8, 3631-3639
6. Le Droumaguet, B.; Nicolas, J.; Brambilla, D.; Mura, S.; Maksimenko, A.; De Kimpe, L.; Salvati, E.; Zona, C.; Airoldi, C.; Canovi, M. Versatile and Efficient Targeting Using a Single Nanoparticulate Platform: Application to Cancer and Alzheimer's Disease ACS Nano 2012, 6, 5866-5879
7. Taylor, M.; Moore, S.; Mourtas, S.; Niarakis, A.; Re, F.; Zona, C.; La Ferla, B.; Nicotra, F.; Masserini, M.; Antimisiaris, S. G. Effect of Curcumin-Associated and Lipid Ligand-Functionalized Nanoliposomes on Aggregation of the Alzheimer's Abeta Peptide Nanomedicine 2011, 7, 541-550
8. Mawuenyega, K. G.; Sigurdson, W.; Ovod, V.; Munsell, L.; Kasten, T.; Morris, J. C.; Yarasheski, K. E.; Bateman, R. J. Decreased Clearance of CNS Beta-Amyloid in Alzheimer's Disease Science 2010, 330, 1774
9. Castellano, J. M.; Kim, J.; Stewart, F. R.; Jiang, H.; DeMattos, R. B.; Patterson, B. W.; Fagan, A. M.; Morris, J. C.; Mawuenyega, K. G.; Cruchaga, C. Human apoE Isoforms Differentially Regulate Brain Amyloid-Beta Peptide Clearance Sci. Transl. Med. 2011, 3, 57r-89r
10. Sagare, A.; Deane, R.; Bell, R. D.; Johnson, B.; Hamm, K.; Pendu, R.; Marky, A.; Lenting, P. J.; Wu, Z.; Zarcone, T. Clearance of Amyloid-Beta by Circulating Lipoprotein Receptors Nat. Med. 2007, 13, 1029-1031
11. Prada, C. M.; Garcia-Alloza, M.; Betensky, R. A.; Zhang-Nunes, S. X.; Greenberg, S. M.; Bacskai, B. J.; Frosch, M. P. Antibody-Mediated Clearance of Amyloid-Beta Peptide From Cerebral Amyloid Angiopathy Revealed by Quantitative in Vivo Imaging J. Neurosci. 2007, 27, 1973-1980
12. Cramer, P. E.; Cirrito, J. R.; Wesson, D. W.; Lee, C. Y.; Karlo, J. C.; Zinn, A. E.; Casali, B. T.; Restivo, J. L.; Goebel, W. D.; James, M. J. ApoE-directed Therapeutics Rapidly Clear Beta-Amyloid and Reverse Deficits in AD Mouse Models Science 2012, 335, 1503-1506
13. Liu, Y. H.; Giunta, B.; Zhou, H. D.; Tan, J.; Wang, Y. J. Immunotherapy for Alzheimer Disease: The Challenge of Adverse Effects Nat. Rev. Neurol. 2012, 8, 465-469
14. Patil, S. P.; Ballard, R.; Sanchez, S.; Osborn, J.; Santangelo, D. J. ApoE: The Link Between Alzheimer's-related Glucose Hypometabolism and Abeta Deposition? Med. Hypotheses 2012, 78, 494-496
15. Matsubara, E.; Sekijima, Y.; Tokuda, T.; Urakami, K.; Amari, M.; Shizuka-Ikeda, M.; Tomidokoro, Y.; Ikeda, M.; Kawarabayashi, T.; Harigaya, Y. Soluble Abeta Homeostasis in AD and DS: Impairment of Anti-Amyloidogenic Protection by Lipoproteins Neurobiol. Aging 2004, 25, 833-841
16. Hanson, A. J.; Bayer-Carter, J. L.; Green, P. S.; Montine, T. J.; Wilkinson, C. W.; Baker, L. D.; Watson, G. S.; Bonner, L. M.; Callaghan, M.; Leverenz, J. B. Effect of Apolipoprotein E Genotype and Diet on Apolipoprotein E Lipidation and Amyloid Peptides: Randomized Clinical Trial JAMA Neurol. 2013, 70, 972-980
17. Koffie, R. M.; Farrar, C. T.; Saidi, L. J.; William, C. M.; Hyman, B. T.; Spires-Jones, T. L. Nanoparticles Enhance Brain Delivery of Blood-Brain Barrier-Impermeable Probes for in Vivo Optical and Magnetic Resonance Imaging Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 18837-18842
18. Zensi, A.; Begley, D.; Pontikis, C.; Legros, C.; Mihoreanu, L.; Wagner, S.; Buchel, C.; von Briesen, H.; Kreuter, J. Albumin Nanoparticles Targeted with ApoE Enter the CNS by Transcytosis and are Delivered to Neurones J. Controlled Release 2009, 137, 78-86
19. Zhang, Z.; Cao, W.; Jin, H.; Lovell, J. F.; Yang, M.; Ding, L.; Chen, J.; Corbin, I.; Luo, Q.; Zheng, G. Biomimetic Nanocarrier for Direct Cytosolic Drug Delivery Angew. Chem., Int. Ed. 2009, 48, 9171-9175
20. Sabnis, N.; Lacko, A. G. Drug Delivery via Lipoprotein-Based Carriers: Answering the Challenges in Systemic Therapeutics Ther. Delivery 2012, 3, 599-608
21. Bien-Ly, N.; Andrews-Zwilling, Y.; Xu, Q.; Bernardo, A.; Wang, C.; Huang, Y. C-Terminal-Truncated Apolipoprotein (Apo) E4 Inefficiently Clears Amyloid-Beta (Abeta) and Acts in Concert with Abeta to Elicit Neuronal and Behavioral Deficits in Mice Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 4236-4241
22. Prevost, M.; Raussens, V. Apolipoprotein E-low Density Lipoprotein Receptor Binding: Study of Protein-Protein Interaction in Rationally Selected Docked Complexes Proteins 2004, 55, 874-884
23. Croy, J. E.; Brandon, T.; Komives, E. A. Two Apolipoprotein E Mimetic Peptides, ApoE(130-149) and ApoE(141-155)2, Bind to LRP1 Biochemistry 2004, 43, 7328-7335
24. Narayanaswami, V.; Maiorano, J. N.; Dhanasekaran, P.; Ryan, R. O.; Phillips, M. C.; Lund-Katz, S.; Davidson, W. S. Helix Orientation of the Functional Domains in Apolipoprotein E in Discoidal High Density Lipoprotein Particles J. Biol. Chem. 2004, 279, 14273-14279
25. 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 2011, 1808, 352-359
26. Ng, K. K.; Lovell, J. F.; Vedadi, A.; Hajian, T.; Zheng, G. Self-Assembled Porphyrin Nanodiscs with Structure-Dependent Activation for Phototherapy and Photodiagnostic Applications ACS Nano 2013, 7, 3484-3490
27. Cormode, D. P.; Briley-Saebo, K. C.; Mulder, W. J.; Aguinaldo, J. G.; Barazza, A.; Ma, Y.; Fisher, E. A.; Fayad, Z. A. An ApoA-I Mimetic Peptide High-Density-Lipoprotein-Based MRI Contrast Agent for Atherosclerotic Plaque Composition Detection Small 2008, 4, 1437-1444
28. Tokuda, T.; Calero, M.; Matsubara, E.; Vidal, R.; Kumar, A.; Permanne, B.; Zlokovic, B.; Smith, J. D.; Ladu, M. J.; Rostagno, A. Lipidation of Apolipoprotein E Influences its Isoform-Specific Interaction with Alzheimer's Amyloid Beta Peptides Biochem. J. 2000, 348 (Pt 2) 359-365
29. Blacklow, S. C. Versatility in Ligand Recognition by LDL Receptor Family Proteins: Advances and Frontiers Curr. Opin. Struct. Biol. 2007, 17, 419-426
30. Fisher, C. A.; Narayanaswami, V.; Ryan, R. O. The Lipid-Associated Conformation of the Low Density Lipoprotein Receptor Binding Domain of Human Apolipoprotein E J. Biol. Chem. 2000, 275, 33601-33606
31. Re, F.; Cambianica, I.; Sesana, S.; Salvati, E.; Cagnotto, A.; Salmona, M.; Couraud, P. O.; Moghimi, S. M.; Masserini, M.; Sancini, G. 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
32. Bana, L.; Minniti, S.; Salvati, E.; Sesana, S.; Zambelli, V.; Cagnotto, A.; Orlando, A.; Cazzaniga, E.; Zwart, R.; Scheper, W. Liposomes Bi-Functionalized with Phosphatidic Acid and an ApoE-Derived Peptide Affect Abeta Aggregation Features and Cross the Blood-Brain-Barrier: Implications for Therapy of Alzheimer Disease. Nanomedicine 2013, pii: S1549-9634(13)00684-9. DOI: 10.1016/j.nano.2013.12.001.
33. Wang, Y.; Xia, Z.; Xu, J. R.; Wang, Y. X.; Hou, L. N.; Qiu, Y.; Chen, H. Z. Alpha-Mangostin, a Polyphenolic Xanthone Derivative From Mangosteen, Attenuates Beta-Amyloid Oligomers-Induced Neurotoxicity by Inhibiting Amyloid Aggregation Neuropharmacology 2012, 62, 871-881
34. Innerarity, T. L.; Pitas, R. E.; Mahley, R. W. Lipoprotein-Receptor Interactions Methods Enzymol. 1986, 129, 542-565
35. Huwyler, J.; Wu, D.; Pardridge, W. M. Brain Drug Delivery of Small Molecules Using Immunoliposomes Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 14164-14169
36. Huang, R.; Ke, W.; Liu, Y.; Jiang, C.; Pei, Y. The Use of Lactoferrin as a Ligand for Targeting the Polyamidoamine-Based Gene Delivery System to the Brain Biomaterials 2008, 29, 238-246
37. Wohlfart, S.; Khalansky, A. S.; Gelperina, S.; Begley, D.; Kreuter, J. Kinetics of Transport of Doxorubicin Bound to Nanoparticles across the Blood-Brain Barrier J. Controlled Release 2011, 154, 103-107
38. Deane, R.; Du Yan, S.; Submamaryan, R. K.; LaRue, B.; Jovanovic, S.; Hogg, E.; Welch, D.; Manness, L.; Lin, C.; Yu, J. RAGE Mediates Amyloid-Beta Peptide Transport Across the Blood-Brain Barrier and Accumulation in Brain Nat. Med. 2003, 9, 907-913
39. Triguero, D.; Buciak, J.; Pardridge, W. M. Capillary Depletion Method for Quantification of Blood-Brain Barrier Transport of Circulating Peptides and Plasma Proteins J. Neurochem. 1990, 54, 1882-1888
40. Pardridge, W. M. Blood-Brain Barrier Drug Targeting: The Future of Brain Drug Development Mol. Interventions 2003, 3, 90-105, 51.
41. Mehta, P. D.; Pirttila, T.; Mehta, S. P.; Sersen, E. A.; Aisen, P. S.; Wisniewski, H. M. Plasma and Cerebrospinal Fluid Levels of Amyloid Beta Proteins 1-40 and 1-42 in Alzheimer Disease Arch. Neurol. 2000, 57, 100-105
42. Kawarabayashi, T.; Younkin, L. H.; Saido, T. C.; Shoji, M.; Ashe, K. H.; Younkin, S. G. Age-Dependent Changes in Brain, CSF, and Plasma Amyloid (Beta) Protein in the Tg2576 Transgenic Mouse Model of Alzheimer's Disease J. Neurosci. 2001, 21, 372-381
43. Bricarello, D. A.; Smilowitz, J. T.; Zivkovic, A. M.; German, J. B.; Parikh, A. N. Reconstituted Lipoprotein: A Versatile Class of Biologically-Inspired Nanostructures ACS Nano 2011, 5, 42-57
44. Jiang, Q.; Lee, C. Y.; Mandrekar, S.; Wilkinson, B.; Cramer, P.; Zelcer, N.; Mann, K.; Lamb, B.; Willson, T. M.; Collins, J. L. ApoE Promotes the Proteolytic Degradation of Abeta Neuron 2008, 58, 681-693
45. Koistinaho, M.; Lin, S.; Wu, X.; Esterman, M.; Koger, D.; Hanson, J.; Higgs, R.; Liu, F.; Malkani, S.; Bales, K. R. Apolipoprotein E Promotes Astrocyte Colocalization and Degradation of Deposited Amyloid-Beta Peptides Nat. Med. 2004, 10, 719-726
46. Lee, C. Y.; Tse, W.; Smith, J. D.; Landreth, G. E. Apolipoprotein E Promotes Beta-Amyloid Trafficking and Degradation by Modulating Microglial Cholesterol Levels J. Biol. Chem. 2012, 287, 2032-2044
47. Ghosh, R. N.; Grove, L.; Lapets, O. A Quantitative Cell-Based High-Content Screening Assay for the Epidermal Growth Factor Receptor-Specific Activation of Mitogen-Activated Protein Kinase Assay Drug Dev. Technol. 2004, 2, 473-481
48. Hone, E.; Martins, I. J.; Fonte, J.; Martins, R. N. Apolipoprotein E Influences Amyloid-Beta Clearance from the Murine Periphery J. Alzheimer's Dis. 2003, 5, 1-8
49. Butterfield, D. A.; Poon, H. F. The Senescence-Accelerated Prone Mouse (SAMP8): A Model of Age-Related Cognitive Decline with Relevance to Alterations of the Gene Expression and Protein Abnormalities in Alzheimer's Disease Exp. Gerontol. 2005, 40, 774-783
50. Wyss-Coray, T. Inflammation in Alzheimer Disease: Driving Force, Bystander or Beneficial Response? Nat. Med. 2006, 12, 1005-1015
51. Sondag, C. M.; Dhawan, G.; Combs, C. K. Beta Amyloid Oligomers and Fibrils Stimulate Differential Activation of Primary Microglia J. Neuroinflammation 2009, 6, 1
52. West, M. J.; Coleman, P. D.; Flood, D. G.; Troncoso, J. C. Differences in the Pattern of Hippocampal Neuronal Loss in Normal Ageing and Alzheimer's Disease Lancet 1994, 344, 769-772
53. Takeda, T.; Matsushita, T.; Kurozumi, M.; Takemura, K.; Higuchi, K.; Hosokawa, M. Pathobiology of the Senescence-Accelerated Mouse (SAM) Exp. Gerontol. 1997, 32, 117-127
54. Floden, A. M.; Li, S.; Combs, C. K. Beta-Amyloid-Stimulated Microglia Induce Neuron Death via Synergistic Stimulation of Tumor Necrosis Factor Alpha and NMDA Receptors J. Neurosci. 2005, 25, 2566-2575
55. Saura, J.; Tusell, J. M.; Serratosa, J. High-Yield Isolation of Murine Microglia by Mild Trypsinization Glia 2003, 44, 183-189
56. Kayed, R.; Head, E.; Thompson, J. L.; McIntire, T. M.; Milton, S. C.; Cotman, C. W.; Glabe, C. G. Common Structure of Soluble Amyloid Oligomers Implies Common Mechanism of Pathogenesis Science 2003, 300, 486-489
57. Lambert, M. P.; Barlow, A. K.; Chromy, B. A.; Edwards, C.; Freed, R.; Liosatos, M.; Morgan, T. E.; Rozovsky, I.; Trommer, B.; Viola, K. L. Diffusible, Nonfibrillar Ligands Derived From Abeta1-42 are Potent Central Nervous System Neurotoxins Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 6448-6453
58. Stine, W. J.; Dahlgren, K. N.; Krafft, G. A.; LaDu, M. J. In Vitro Characterization of Conditions for Amyloid-Beta Peptide Oligomerization and Fibrillogenesis J. Biol. Chem. 2003, 278, 11612-11622
59. Chapman, M. J.; Goldstein, S.; Lagrange, D.; Laplaud, P. M. A Density Gradient Ultracentrifugal Procedure for the Isolation of the Major Lipoprotein Classes From Human Serum J. Lipid Res. 1981, 22, 339-358
60. Song, Q.; Yao, L.; Huang, M.; Hu, Q.; Lu, Q.; Wu, B.; Qi, H.; Rong, Z.; Jiang, X.; Gao, X. Mechanisms of Transcellular Transport of Wheat Germ Agglutinin-Functionalized Polymeric Nanoparticles in Caco-2 Cells Biomaterials 2012, 33, 6769-6782