In vitro and in vivo characterization of several functionalized ultrasmall particles of iron oxide, vectorized against amyloid plaques and potentially able to cross the blood-brain barrier: Toward earlier diagnosis of Alzheimer's disease by molecular imaging

Contrast Media and Molecular Imaging

Volumn 10, Issue 3, 2015, Pages 211-224

  Ansciaux, Emilie ^a   Burtea, Carmen ^a   Laurent, Sophie ^a   Crombez, Deborah ^a   Nonclercq, Denis ^a   Vander Elst, Luce ^a   Muller, Robert N ^a,b  

^a UNIVERSITY OF MONS   (Belgium)

^b Center for Microscopy and Molecular Imaging   (Belgium)

Author keywords

Alzheimer's disease; Amyloid peptide; Blood brain barrier; Contrast agents; Functionalized iron oxide nanoparticles; MRI

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; CONTRAST MEDIUM; CREATININE; CYSTEINE ISOLEUCYLPROLYLLEUCYLPROLYLPHENYLALANYLTRYPTOPHANYLASPARAGINYL CYSTEINE; MACROGOL; PEPTIDE; ULTRASMALL PARTICLE OF IRON OXIDE; UNCLASSIFIED DRUG; FERRIC ION; FERRIC OXIDE; METAL NANOPARTICLE;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BIOACCUMULATION; BLOOD BRAIN BARRIER; CHEMICAL LABELING; CONTROLLED STUDY; CREATININE URINE LEVEL; DISSOCIATION CONSTANT; DRUG CLEARANCE; DRUG DISTRIBUTION; DRUG HALF LIFE; DRUG PENETRATION; DRUG SYNTHESIS; EARLY DIAGNOSIS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR IMAGING; MOUSE; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; SENSITIVITY AND SPECIFICITY; TOXICITY TESTING; ANIMAL; BRAIN; DISEASE MODEL; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PHYSIOLOGY; PLAQUE, AMYLOID; PROCEDURES; TRANSGENIC MOUSE; TUMOR CELL LINE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE, TUMOR; CONTRAST MEDIA; DISEASE MODELS, ANIMAL; FERRIC COMPOUNDS; METAL NANOPARTICLES; MICE; MICE, TRANSGENIC; MOLECULAR IMAGING; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PLAQUE, AMYLOID; SENSITIVITY AND SPECIFICITY;

EID: 84930908986     PISSN: 15554309     EISSN: 15554317     Source Type: Journal    
DOI: 10.1002/cmmi.1626     Document Type: Article

References (54)

1. Sarazin M, Dubois B. Mild cognitive impairment or pre-demential Alzheimer's disease? Rev Neurol (Paris) 2002; 158(10 Suppl): S30-S34.
2. Soffer D. Cerebral amyloid angiopathy - a disease or age-related condition. Isr Med Assoc J 2006; 8(11): 803-806.
3. Hardy J, Selkoe DJ. Medicine - the amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297(5580): 353-356; doi: 10.1126/science.1072994.
4. Medeiros R, Baglietto-Vargas D, LaFerla FM. The role of tau in Alzheimer's disease and related disorders. CNS Neurosci Ther 2011; 17(5): 514-524; doi: 10.1111/j.1755-5949.2010.00177.x.
5. Casetta I, Govoni V, Granieri E. Oxidative stress, antioxidants and neurodegenerative diseases. Curr Pharm Des 2005; 11: 2033-2052; doi: 10.2174/1381612054065729.
6. Li S, Hong S, Shepardson DM, Shankar GM, Selkoe DJ. Soluble oligomers of amyloid β protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009; 62(6): 788-801; doi: 10.1016/j.neuron.2009.05.012.
7. Wyss-Coray T. Inflammation in Alzheimer disease: driving force, bystander or beneficial response? Nat Med 2006; 12(9): 1005-1015; doi: 10.1038/nm1474.
8. Contestabile A. The history of the cholinergic hypothesis. Behav Brain Res 2011; 221(2): 334-340; doi: 10.1016/j.bbr.2009.12.044.
9. Bozso Z, Penke B, Simon D, Laczkò I, Juhàsz G, Szegedi V, Kasza A, Soòs K, Hetényi A, Wéber E, Tohati H, Csete M, Zarandi M, Fülöp L. Controlled in situ preparation of Aβ(1-42) oligomers from the isopeptide 'iso-Aβ(1-42)', physicochemical and biological characterization. Peptide 2010; 31: 248-256; doi: 10.1016/j.peptides.2009.12.001.
10. Montalto MC, Farrar G, Hehir CT. Fibrillar and oligomeric beta-amyloid as distinct local biomarkers for Alzheimer's disease. Ann NY Acad Sci 2007; 1097: 239-258; doi: 10.1196/annals.1379.023.
11. Larbanoix L, Burtea C, Laurent S, Van Leuven F, Toubeau G, Vander Elst L, Muller RN. Potential amyloid plaque-specific peptides for the diagnosis of Alzheimer's disease. Neurobiol Aging 2010; 31: 1679-1689; doi: 10.1016/j.neurobiolaging.2008.09.021.
12. Walsh DM, Selkoe DJ. A beta oligomers - a decade of discovery. J Neurochem 2007; 101: 1172-1184; doi: 10.1111/j.1471-4159.2006.04426.x.
13. Deane R, Zlokovic BV. Role of the blood-brain barrier in the pathogenesis of Alzheimer's disease. Curr Alzheimer Res 2007; 4: 191-197; doi: 10.2174/156720507780362245.
14. Pascale CL, Miller MC, Chiu C, Boylan M, Caralopoulos IN, Gonzalez L, Johanson CE, Silverberg GD. Amyloid-beta transporter expression at the blood-CSF barrier is age-dependent. Fluids Barriers CNS 2011; 8: 21; doi: 10.1186/2045-8118-8-21.
15. Silverberg GD, Miller MC, Messier AA, Majmudar S, Machan JT, Donahue JE, Stopa EG, Johanson CE. Amyloid deposition and influx transporter expression at the blood-brain barrier increase in normal aging. J Neuropathol Exp Neurol 2010; 69: 98-108; doi: 10.1097/NEN.0b013e3181c8ad2f.
16. Donahue JE, Flaherty SL, Johanson CE, Duncan JA, Silverberg GD, Miller MC, Tavares R, Yang W, Wu Q, Sabo E, Hovanesian V, Stopa EG. RAGE, LRP-1, and amyloid-beta protein in Alzheimer's disease. Acta Neuropathol 2006; 11: 405-415; doi: 10.1007/s00401-006-0115-3.
17. Miller MC, Tavares R, Johanson CE, Hovanesian V, Donahue JE, Gonzalez L, Silverberg GD, Stopa EG. Hippocampal RAGE immunoreactivity in early and advanced Alzheimer's disease. Brain Res 2008; 1230: 273-280; doi: 10.1016/j.brainres.2008.06.124.
18. Jellinger KA, Janetzky B, Attems J, Kienzl E. Biomarkers for early diagnosis of Alzheimer disease: ALZheimer ASsociated gene - a new blood biomarker? J Cell Mol Med 2008; 12(4): 1094-1117; doi: 10.1111/j.1582-4934.2008.00313.x.
19. Freeman SH, Raju S, Hyman BT, Frosch MP, Irizarry MC. Plasma Aβ levels do not reflect brain Aβ levels. J Neuropathol Exp Neurol 2007; 66(4): 264-271; doi: 10.1097/NEN.0b013e31803d3ae4.
20. Burtea C, Laurent S, Port M, Lancelot E, Ballet S, Rousseaux O, Toubeau G, Vander Elst L, Corot C, Muller RN. Magnetic resonance molecular imaging of vascular cell adhesion molecule-1 expression in inflammatory lesions using a peptide-vectorized paramagnetic imaging probe. J Med Chem 2009; 52: 4725-4742; doi: 10.1021/jm9002654.
21. Burtea C, Laurent S, Lancelot E, Ballet S, Murariu O, Rousseau O, Port M, Vander Elst L, Corot C, Muller RN. Peptidic targeting of phosphatidylserine for the MRI detection of apoptosis in atherosclerotic plaques. Mol Pharm 2009; 6: 1903-1919; doi: 10.1021/mp900106m.
22. Hammoud DA, Hoffman JM, Pomper MG. Molecular neuroimaging: from conventional to emerging techniques. Radiology 2007; 245: 21-42; doi: 10.1148/radiol.2451060731.
23. Yang L, Rieves D, Ganley C. Brain amyloid imaging - FDA approval of florbetapir F18 injection. New Engl J Med 2012; 367(10): 885-887; doi: 10.1056/NEJMp1208061.
24. 18F stilbenes and styrylpyridines for PET imaging of A beta plaques in Alzheimer's disease: a miniperspective. J Med Chem 2010; 53: 933-941; doi: 10.1021/jm901039z.
25. Sigurdsson EM, Wadghiri YZ, Mosconi L, Blind JA, Knudsen E, Asuni A, Scholtzova H, Tsui WH, Li Y, Sadowski M, Turnbull DH, de Leon MJ, Wisniewski T. A non-toxic ligand for voxel-based MRI analysis of plaques in AD transgenic mice. Neurobiol Aging 2008; 29(6): 836-847; doi: 10.1016/j.neurobiolaging.2006.12.018.
26. Poduslo JF, Curran GL, Peterson JA, McCormick DJ, Fauq AH, Khan MA, Wengenack TM. Design and chemical synthesis of a magnetic resonance contrast agent with enhanced in vitro binding, high blood-brain barrier permeability, and in vivo targeting to Alzheimer's disease amyloid plaques. Biochemistry 2004; 43(20): 6064-6075; doi: 10.1021/bi0359574.
27. Wadghiri YZ, Sigurdsson EM, Sadowski M, Elliott JI, Li Y, Scholtzova H, Tang CY, Aguinaldo G, Pappolla M, Duff K, Wisniewski T, Turnbull DH. Detection of Alzheimer's amyloid in transgenic mice using magnetic resonance microimaging. Magn Reson Med 2003; 50: 293-302; doi: 10.1002/mrm.10529.
28. Dhenain M, El Tannir El TN, Wu TD, Guegan M, Volk A, Quintana C, Delatour B. Characterization of in vivo MRI detectable thalamic amyloid plaques from APP/PS1 mice. Neurobiol Aging 2009; 30(1): 41-53; doi: 10.1016/j.neurobiolaging.2007.05.018.
29. Larbanoix L, Burtea C, Ansciaux E, Laurent S, Mahieu I, Vander Elst L, Muller RN. Design and evaluation of a 6-mer amyloid-beta protein derived phage display library for molecular targeting of amyloid plaques in Alzheimer's disease. Comparison with two cyclic heptapeptides derived from a randomized phage display library. Peptides 2011; 32(6): 1232-1243; doi: 10.1016/j.peptides.2011.04.026.
30. Soenen SJ, De Cuyper M. Assessing cytotoxicity of (iron oxide-based) nanoparticles: an overview of different methods exemplified with cationic magnetoliposomes. Contrast Media Mol Imag 2009; 4(5): 207-219; doi: 10.1002/cmmi.282.
31. Stark WJ. Nanoparticles in biological systems. Angew Chem Int Ed Engl 2011; 50(6): 1242-1258; doi: 10.1002/anie.200906684.
32. Christa Maree Stephan B, Minett T, Pagett E, Siervo M, Brayne C, McKeith IG. Diagnosing mild cognitive impairment (MCI) in clinical trials: a systematic review. BMJ Open 2013; 3(2); doi: 10.1136/bmjopen-2012-001909.
33. Kung HF. The β-amyloid hypothesis in Alzheimer's disease: seeing is believing. ACS Med Chem Lett 2012; 3: 265-267; doi: 10.1021/ml300058m.
34. Cramer PE, Cirrito JR, Wesson DW, Lee CY, Karlo JC, Zinn AE, Casali BT, Restivo JL, Goebel WD, James MJ, Brunden KR, Wilson DA, Landreth GE. ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models. Science 2012; 335(6075): 1503-1506; doi: 10.1126/science.1217697.
35. Sanchez PE, Zhu L, Verret L, Vossel KA, Orr AG, Cirrito JR, Devidze N, Ho K, Yu GQ, Palop JJ, Mucke L. Levetiracetam suppresses neuronal network dysfunction and reverses synaptic and cognitive deficits in an Alzheimer's disease model. Proc Natl Acad Sci U S A 2012; 109(42): E2895-E2903; doi: 10.1073/pnas.1121081109.
36. Laurent S, Burtea C, Thirifays C, Rezaee F, Mahmoudi M. Significance of cell 'observer' and protein source in nanobiosciences. J Colloid Interface Sci 2013; 392: 431-445; doi: 10.1016/j.jcis.2012.10.005.
37. Sakono M, Zako T. Amyloid oligomers: formation and toxicity of Abeta oligomers. FEBS J 2010; 277: 1348-1358; doi: 10.1111/j.1742-4658.2010.07568.x.
38. Pagani L, Eckert A. Amyloid-beta interaction with mitochondria. Int J Alzheimers Dis 2011; 2011: 925050; doi: 10.4061/2011/925050.
39. Tortora GJ, Anagnostakos NP. The cardiovascular system: vessels and routes. In Principles of Anatomy and Physiology, 6th edn. Harper & Row: New York, 1990, pp. 605-653.
40. Poduslo JF, Curran GL. Polyamine modification increases the permeability of proteins at the blood-nerve and blood-brain barriers. J Neurochem 1996; 66: 1599-1609.
41. Kandimalla KK, Curran GL, Holasek SS, Gilles EJ, Wengenack TM, Ramirez-Alvarado M, Poduslo JF. Physiological and biophysical factors that influence Alzheimer's disease amyloid plaque targeting of native and putrescine modified human amyloid beta40. J Pharmacol Exp Ther 2006; 318: 17-25.
42. Borlongan CV, Emerich DF. Facilitation of drug entry into the CNS via transient permeation of blood brain barrier: laboratory and preliminary clinical evidence from bradykinin receptor agonist, Cereport. Brain Res Bull 2003; 60: 297-306; doi: 10.1016/S0361-9230(03)00043-1.
43. Deli MA. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim Biophys Acta 2009; 1788: 892-910; doi: 10.1016/j.bbamem.2008.09.016.
44. Bartus RT. Translating the therapeutic potential of neurotrophic factors to clinical 'proof of concept': a personal saga achieving a career-long quest. Neurobiol Dis 2012; 48: 153-178; doi: 10.1016/j.nbd.2012.04.004.
45. Rubio-Aliaga I, Daniel H. Mammalian peptide transporters as targets for drug delivery. Trends Pharmacol Sci 2002; 23: 434-440.
46. Demirel Ö, Jan I, Wolters D, Blanz J, Saftig P, Tampé R, Abele R. The lysosomal polypeptide transporter TAPL is stabilized by interaction with LAMP-1 and LAMP-2. J Cell Sci 2012; 125(Pt 18): 4230-4240; doi: 10.1242/jcs.087346.
47. Strazielle N, Ghersi-Egea JF. Physiology of blood-brain interfaces in relation to brain disposition of small compounds and macromolecules. Mol Pharm 2013;10:1473-1491; doi: 10.1021/mp300518e.
48. Masserini M. Nanoparticles for brain drug delivery. ISRN Biochem 2013, article ID 238428; doi: 10.1155/2013/238428.
49. Nance EA, Woodworth GF, Sailor KA, Shih TY, Xu Q, Swaminathan G, Xiang D, Eberhart C, Hanes J. A dense poly(ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Sci Transl Med 2012; 4: 149ra119; doi: 10.1126/scitranslmed.3003594.
50. Koob AO, Colby JM, Borgens RB. Behavioral recovery from traumatic brain injury after membrane reconstruction using polyethylene glycol. J Biol Eng 2008; 2: 9; doi: 10.1186/1754-1611-2-9.
51. Burtea C, Ballet S, Laurent S, Rousseaux O, Dencausse A, Gonzalez W, Port M, Corot C, Vander Elst L, Muller RN. Development of a magnetic resonance imaging protocol for the characterization of atherosclerotic plaque by using vascular cell adhesion molecule-1 and apoptosis-targeted ultrasmall superparamagnetic iron oxide derivatives. Arterioscler Thromb Vasc Biol 2012; 32: e36-e48; doi: 10.1161/ATVBAHA.112.245415.
52. Boutry S, Burtea C, Laurent S, Toubeau G, Vander Elst L, Muller RN. Magnetic resonance imaging of inflammation with a specific selectin-targeted contrast agent. Magn Reson Med 2005; 53: 800-807.
53. Burtea C, Laurent S, Colet JM, Vander Elst L, Muller RN. Development of new glucosylated derivatives of gadolinium diethylenetriaminepentaacetic for magnetic resonance angiography. Invest Radiol 2003; 38: 320-333.
54. Moos T, Møllgård K. A sensitive post-DAB enhancement technique for demonstration of iron in the central nervous system. Histochemistry 1993; 99: 471-475.