SPION-enhanced magnetic resonance imaging of Alzheimer's disease plaques in AβPP/PS-1 transgenic mouse brain

Journal of Alzheimer's Disease

Volumn 34, Issue 2, 2013, Pages 349-365

  Sillerud, Laurel O ^a   Solberg, Nathan O ^a   Chamberlain, Ryan ^c   Orlando, Robert A ^a   Heidrich, John E ^b   Brown, David C ^a   Brady, Christina I ^a   Vander Jagt, Thomas A ^a,b   Garwood, Michael ^c   Vander Jagt, David L ^a,b  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b Quatros   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Magnetic resonance imaging; superparamagnetic iron oxide nanoparticles; transgenic mice

Indexed keywords

AMYLOID PRECURSOR PROTEIN; PRESENILIN 1; SUPERPARAMAGNETIC IRON OXIDE NANOPARTICLE;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN; CONTRAST TO NOISE RATIO; CONTROLLED STUDY; DRUG CONJUGATION; DRUG PENETRATION; HISTOPATHOLOGY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; TRANSGENICS;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; FERRIC COMPOUNDS; HUMANS; MAGNETIC RESONANCE IMAGING; METAL NANOPARTICLES; MICE; MICE, TRANSGENIC; PLAQUE, AMYLOID; PRESENILIN-1;

EID: 84874340063     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-121171     Document Type: Article

References (95)

1. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer's disease in the U.S. population: Prevalence estimates using the 2000 census. Arch Neurol 60, 1119-1122 (Pubitemid 36975801)
2. Fodero-Tavoletti AT, Villemagne VL, Rowe CC, Masters CL, Barnham KJ, Cappai R (2011) Amyloid-2277;: The seeds of darkness. Int J Biochem Cell Biol 43, 1247-1251
3. Iqbal K, Liu F, Gong C, Grundke-Iqbal I (2010) Tau in Alzheimer disease and related tauopathies. Curr Alzheimer Res 7, 656-664
4. Masters CL, Cappai R, Barnham KJ, Villemagne VL (2006) Molecular mechanisms for Alzheimer's disease: Implications for neuroimaging and therapeutics. J Neurochem 106, 1700-1725 (Pubitemid 43873662)
5. Karran E, Mercken M, De Strooper B (2011) The amyloid cascade hypothesis for Alzheimer's disease: An appraisal for the development of therapeutics. Nat Med 10, 698-712
6. Mattson MP (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631-639 (Pubitemid 39061671)
7. Selkoe DJ, Schenk D (2003) Alzheimer's disease: Molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43, 545-584 (Pubitemid 37372653)
8. Lùhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, D?obeli H, Schubert D, Riek R (2005) 3D structure of Alzheimer's amyloid-2277; (1-42) fibrils. Proc Natl Acad Sci U S A 102, 17342-17347 (Pubitemid 41740868)
9. Gaspar RC, Villarreal SA, Bowles N, Hepler RW, Joyce JG, Shughrue PJ (2010) Oligomers of 2277;-amyloid are sequestered into and seed newplaques in the brains of anADmouse model. Exp Neurol 223, 394-400
10. Urbanc B, Betnel M, Cruz L, Bitan G, TeplowDB (2010) Elucidation of amyloid-2277; protein oligomerization mechanisms: Discrete molecular dynamics study. J Am Chem Soc 132, 4266-4280
11. Schnabel J (2011) Amyloid: Little proteins, big clues. Nature 475, S12-S14
12. Hardy J, Allsop D (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12, 383-388
13. Hardy J (1997) Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci 20, 154-159 (Pubitemid 27116286)
14. Hsaio K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, A 2277; elevation, and amyloid plaques in transgenic mice. Science 274, 99-102 (Pubitemid 26332733)
15. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Mueller R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C,Younkin S, Hsiao K, Duff K (1998) Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 4, 97-100 (Pubitemid 28133087)
16. Bornemann KD, Wiederhold KH, Pauli C, Ermini F, Stalder M, Schnell L, Sommer B, Jucker M, Staufenbiel M (2001) Abeta-induced inflammatory processes in microglia cells of APP23 transgenic mice. Am J Pathol 158, 63-73 (Pubitemid 32096472)
17. Dickson DW (1997) Neuropathological diagnosis of Alzheimer's disease: A perspective from longitudinal clinicopathological studies. Neurobiol Aging 18, S21-S26 (Pubitemid 27454692)
18. Dubois B, Feldman HH, Jacova C, Dekosky ST, Barberger-Gateau P, Cummings J, Delacourte A, Galasko D, Gauthier S, Jicha G, Meguro K, O'brien J, Pasquier F, Robert P, Rossor M, Salloway S, Stern Y, Visser PJ, Scheltens P (2007) Research criteria for the diagnosis of Alzheimer's disease: Revising the NINCDS-ADRDA criteria. Lancet Neurol 6, 734-746 (Pubitemid 47058377)
19. Jack CR Jr, Albert MS, Knopman DS, McKhann GM, Sperling RA, Carrillo MC, Thies B, Phelps CH (2011) Introduction to the recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 7, 257-262
20. Benveniste H, Einstein G, Kim KR, Hulette C, Johnson GA (1999) Detection of neuritic plaques in Alzheimer's disease by magnetic resonance microscopy. Proc Natl Acad Sci U S A 96, 14079-14084
21. Jack CR, Garwood M, Wengenack TM, Borowski B, Curran GL, Lin J, Adriany G, Gr?ohn OH, Grimm R, Poduslo JF (2004) In vivo visualization of Alzheimer's amyloid plaques by MRI in transgenic mice without a contrast agent. Magn Reson Med 52, 1263-1271 (Pubitemid 39612814)
22. Jack CR, Wengenack TM, Reyes DA, Garwood M, Curran GL, Borowski BJ, Lin J, Preboske GM, Holasek SS, Adriany G, Poduslo JF (2005) In vivo magnetic resonance microimaging of individual amyloid plaques in Alzheimer's transgenic mice. J Neurosci 25, 10041-10048 (Pubitemid 41528043)
23. Borthakur A, Gur T, Wheaton AJ, Corbo M, Trojanowski JQ, Lee VM, Reddy R (2006) In vivo measurement of plaque burden in a mouse model of Alzheimer's disease. J Magn Reson Imag 24, 1011-1017 (Pubitemid 44658237)
24. Braakman N, Matysik J, van Duinen SG, Verbeek F, Schliebs R, de Groot HJ, Alia A (2006) Longitudinal assessment of Alzheimer's beta-amyloid plaque development in transgenic mice monitored by in vivo magnetic resonance microimaging. J Magn Reson Imag 24, 530-536 (Pubitemid 44320553)
25. Benveniste H, Ma Y, Dhawan J, Gifford A, Smith SD, Feinstein I, Du C, Grant SC, Hof PR (2007) Anatomical and functional phenotyping of mice models of Alzheimer's disease by MR microscopy. Ann N Y Acad Sci 1097, 12-29 (Pubitemid 47084883)
26. Chamberlain R, Reyes D, Curran GL, Marjanska M, Wengenack TM, Poduslo JF, Garwood M, Jack CR (2009) Comparison of amyloid plaque contrast generated by T2-weighted, T2*-weighted, and susceptibility-weighted imaging methods in transgenic mouse models of Alzheimer's disease. Magn Reson Med 61, 1158-1164
27. Dhenain M, El Tannir El Tayara N, Wu TD, Guegan M, Volk A, Quintana C, Delatour B (2009) Characterization of in vivo MRI detectable thalamic amyloid plaques from APP/PS1 mice. Neurobiol Aging 30, 41-53
28. Zhang J, Yarowsky P, Gordon MN, Di Carlo G, Munireddy S, van Zijl PC, Mori S (2004) Detection of amyloid plaques in mouse models of Alzheimer's disease by magnetic resonance imaging. Magn Reson Med 51, 452-457 (Pubitemid 38298656)
29. Faber C, Zahneisen B, Tippmann F, Schroeder A, Fahrenholz F (2007) Gradient-echo and CRAZED imaging for minute detection of Alzheimer plaques in an APPV717I x ADAM10-dn mouse model. Magn Reson Med 57, 696-703 (Pubitemid 46731795)
30. Chamberlain R, Wengenack TM, Poduslo JF, Garwood M, Jack CF (2011) Magnetic resonance imaging of amyloid plaques in transgenic mouse models of Alzheimer's disease. Curr Med Imaging Rev 7, 3-7
31. Wengenack TM, Reyes DA, Curran GL, Borowski BJ, Lin J, Preboske GM, Holasek SS, Gilles EJ, Chamberlain R, Marjanska M, Jack CR, Garwood M, Poduslo JF (2011) Regional differences in MRI detection of amyloid plaques in AD transgenic mouse brain. Neuroimage 54, 113-122
32. Poduslo JF, Wengenack TM, Curran GL, Wisniewski T, Sigurdsson EM, Macura SI, Borowski BJ, Jack CR (2002) Molecular targeting of Alzheimer's amyloid plaques for contrast-enhanced magnetic resonance imaging. Neurobiol Dis 11, 315-329 (Pubitemid 36135695)
33. Poduslo JF, Curran GL, Peterson JA, McCormick DJ, Fauq AH, Khan MA, Wengenack TM (2004) Design and chemical synthesis of a magnetic resonance contrast agent with enhanced in vitro binding, high blood-brain permeability, and in vivo targeting to Alzheimer's disease amyloid plaques. Biochemistry 43, 6064-6075 (Pubitemid 38669474)
34. Petiet A, Santin M, Bertrand A, Wiggins CJ, Petit F, Houitte D, Hantraye P, Benavides J, Debeir T, Rooney T, Dhenain M (2012) Gadolinium-staining reveals amyloid plaques in the brain of Alzheimer's transgenic mice. Neurobiol Aging 33, 1533-1544
35. Dhenain M, Delatour B, Walczak C, Volk A (2006) Passive staining: A novel ex vivo MRI protocol to detect amyloid deposits in mouse models of Alzheimer's disease. Magn Reson Med 55, 687-693 (Pubitemid 43352570)
36. Wadghiri YZ, Sigurdsson EM, Sadowski M, Elliott JI, Li Y, Scholtzova H, Tang CY, Aguinaldo G, Pappolla M, Duff K, Wisniewski T, Turnbull DH (2003) Detection of Alzheimer's amyloid in transgenic mice using magnetic resonance microimaging. Magn Reson Med 50, 293-302 (Pubitemid 36950848)
37. Meadowcroft MD, Connor JR, Smith MB, Yang QX (2009) Magnetic resonance imaging and histological analysis of beta-amyloid plaques in both human Alzheimer's disease and APP/PS1 transgenic mice. J Magn Reson Imaging 29, 997-1007
38. Scholtzova H, Wadghiri YZ, Douadi M, Sigurdsson EM, Li Y-S, Quartermain D, Banerjee P, Wisniewski T (2008) Memantine leads to behavioral improvement and amyloid reduction in Alzheimer's disease model transgenic mice shown as by micromagnetic resonance imaging. J Neurosci Res 86, 2784-2791
39. Zhang J, Shu C, Reid J, Owens LS, Cai T, Gibson HW, Long GL, Corwin FD, Chen Z-J, Fatouros PP, Dorn HC (2010) High relaxivity trimetallic nitride (Gd3N) metallofullerene MRI contrast agents with optimized functionality. Bioconjug Chem 21, 610-615
40. Higuchi M, Iwata N, Matsuba Y, Sato K, Sasamoto K, Saido TC (2005) 19F and 1H MRI detection of amyloid 2277; plaques in vivo. Nat Neurosci 8, 527-533 (Pubitemid 41007572)
41. Amatsubo T, Yanagisawa D, Morikawa S, Taguchi H, Tooyama I (2010) Amyloid imaging using high-field magnetic resonance. Magn Reson Med Sci 9, 95-99
42. Yanagisawa D, Amatsubo T, Morikawa S, Taguchi H, Urushitani M, Shirai N, Hirao K, Shiino A, Inubushi T, Tooyama I (2011) In vivo detection of amyloid 2277; deposition using 19F magnetic resonance imaging with a 19F-containing curcumin derivative in a mouse model of Alzheimer's disease. Neuroscience 184, 120-127
43. Petri-Fink A, Hofman H (2007) Superparamagnetic Iron oxide Nanoparticles (SPIONs): From synthesis to in vivo studies-A summary of synthesis, characterization, in vitro and in vivo investigations of SPIONs with particular focus on surface and colloidal properties. IEEE Trans Nanobiosci 6, 1536-1541
44. Lin MM, Kim DK, El Haj AJ, Dobson J (2008) Development of Superparamagnetic Iron Oxide Nanoparticles (SPIONS) for translation to clinical applications. IEEE Trans Nanobiosci 7, 298-305
45. Brambilla D, Le Droumaguet B, Nicolas J, Hashemi SH, Wu LP, Moghimi SM, Couvreur P, Andrieux K (2011) Nanotechnologies for Alzheimer's disease: Diagnosis, therapy, and safety issues. Nanomedicine 7, 521-540
46. Skaat H, Margel S (2009) Synthesis of fluorescent-maghemite nanoparticles as multimodal imaging agents for amyloid-beta fibrils detection and removal by a magnetic field. Biochem Biophys Res Commun 386, 645-649
47. Taylor RM, Huber DL, Monson TC, Ali AS, Bisoffi M, Sillerud LO (2011) Multifunctional iron platinum stealth immunomicelles: Targeted detection of human prostate cancer cells using both fluorescence and magnetic resonance imaging. J Nanopart Res 13, 4717-4729
48. Kim YS, Joh TH (2006) Microglia, major player in the brain inflammation: Their roles in the pathogenesis of Parkinson's disease. Exp Mol Med 38, 333-347
49. Granic I, Dolga AM, Nijholt IM, van Dijk G, Eisel UL (2009) Inflammation and NF-kappaB in Alzheimer's disease and diabetes. J Alzheimers Dis 16, 809-821
50. Khandelwal PJ, Herman AM, Moussa CE (2011) Inflammation in the early stages of neurodegenerative pathology. J Neuroimmunol 238, 1-11
51. Couturier J, Paccalin M, Morel M, Terro F, Milin S, Pontcharraud R, Fauconneau B, Page G (2011) Prevention of the 2277;-amyloid peptide-induced inflammatory process by inhibition of double-stranded RNA-dependent protein kinase in primary murine mixed co-cultures. J Neuroinflammation 8, 72
52. Mrak RE, Griffin WST (2005) Glia and their cytokines in a progression of neurodegeneration. Neurobiol Aging 26, 349-354 (Pubitemid 40082718)
53. El Khoury J, Luster AD (2008) Mechanisms of microglia accumulation in Alzheimer's disease: Therapeutic implications. Trends Pharmacol Sci 29, 626-632
54. Schlachetzki JC, Hùll M (2009) Microglial activation in Alzheimer's disease. Curr Alzheimer Res 6, 554-563
55. GraeberMB(2010) Changing face of microglia. Science 330, 783-788
56. Burguillos MA, Deierborg T, Kavanagh E, Persson A, Hajji N, Garcia-Quintanilla A, Cano J, Brundin P, Englund E, Venero JL, Joseph B (2011) Caspase signalling controls microglia activation and neurotoxicity. Nature 472, 319-324
57. Alafuzoff I, Adolfsson R, Grundke-Iqbal I, Winblad B (1987) Blood-brain barrier in Alzheimer dementia and in non-demented elderly. An immunocytochemical study. Acta Neuropathol 73, 160-166 (Pubitemid 17060012)
58. Kalaria RN (2006) The blood-brain barrier and cerebrovascular pathology in Alzheimer's disease. Ann N Y Acad Sci 893, 113-125
59. Anderson VC, Lenar DP, Quinn JF, Rooney WD (2011) The blood-brain barrier and microvascular water exchange in Alzheimer's disease. Cardiovasc Psychiatry Neurol 2011, Article ID 615829
60. Dalkara T, Gursoy-Ozdemir Y, Yemisci M (2011) Brain microvascular pericytes in health and disease. Acta Neuropathol 122, 1-9
61. del Valle J, Duran-Vilaregut J, Manich G, Pallàs M, Camins A,Vilaplana J, PelegŕiC(2011) Cerebral amyloid angiopathy, blood-brain barrier disruption and amyloid accumulation in SAMP8 mice. Neurodegener Dis 8, 421-429
62. Mundt AP,Winter C, Mueller S,Wuerfel J, Tysiak E, Schnorr J, Taupitz M, Heinz A, Juckel G (2009) Targeting activated microglia in Alzheimer's pathology by intraventricular delivery of a phagocytosable MRI contrast agent in APP23 transgenic mice. Neuroimage 46, 367-372
63. Stoll G, Bendszus M (2009) Imaging of inflammation in the peripheral and central nervous system by magnetic resonance imaging. Neuroscience 158, 1151-1160
64. Fleige G, Nolte C, Synowitz M, Seeberger F, Kettenmann H, Zimmer C (2001) Magnetic labeling of activated microglia in experimental gliomas. Neoplasia 3, 489-499 (Pubitemid 33151015)
65. Poduslo JF, Hultman KL, Curran GL, Preboske GM, Chamberlain R, Marjanska M, Garwood M, Jack CR, Wengenack TM (2011) Targeting vascular amyloid in artierioles of Alzheimer disease transgenic mice with amyloid-2277; protein antibody-coated nanoparticles. J Neuropathol Exp Neurol 70, 653-661
66. 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 (2008) A nontoxic ligand for voxel-based MRI analysis of plaques in AD transgenic mice. Neurobiol Aging 29, 836-847 (Pubitemid 351601897)
67. Skaat H, Margel S (2009) Synthesis of fluorescent-maghemite nanoparticles as multimodal imaging agents for amyloid-beta fibrils detection and removal by a magnetic field. Biochem Biophys Res Commun 386, 645-649
68. Yang C-C, Yang S-Y, Chieh J-J, Horng H-E, Hong C-Y, Yang H-C, Chen KH, Shih BY, Ta-Chen F, Chiu M-J (2011) Biofunctionalized magnetic nanoparticles for specifically detecting biomarkers of Alzheimer's disease in vitro. ACS Chem Neurosci 2, 500-505
69. Yang J, Wadghiri YZ, Hoang DM, Tsui W, Sun Y, Chung E, Li Y, Wang A, de Leon M, Wisniewski T (2011) Detection of amyloid plaques targeted by USPIO-A 2277;1-42 in Alzheimer's disease transgenic mice using magnetic resonance microimaging. Neuroimage 55, 1600-1609
70. Stookey LL (1970) Ferrozine-a new spectrophotometric reagent for iron. Anal Chem 42, 779-781
71. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to Image J: 25 years of image analysis. Nat Methods 9, 671-675
72. Wengenack TM, Whelan S, Curran GL, Duff KE, Poduslo JF (2000) Quantitative histological analysis of amyloid deposition in Alzheimer's double transgenic mouse brain. Neuroscience 101, 939-944
73. Kelenyi G (1966) Thioflavin S fluorescent and congo red anisotropic stainings in the histologic demonstration of amyloid. Acta Neuropathol 7, 336-348
74. Falangola MF, Lee SP, Nixon RA, Duff K, Helpern JA (2005) Histological co-localization of iron in Abeta plaques of PS/APP transgenic mice. Neurochem Res 30, 201-205 (Pubitemid 40569203)
75. Beckmann N, Gerard C, Abramowski D, Cannet C, Staufenbiel M (2011) Noninvasive magnetic resonance imaging detection of cerebral amyloid angiopathy-related microvascular alterations using superparamagnetic iron oxide particles in APP transgenic mouse models of Alzheimer's disease: Application to passive A 2277; immunotherapy. J Neurosci 31, 1023-1031
76. Ramakrishnan M, Wengenack TM, Kandimalla KK, Curran GL, Gilles EJ, Ramirez-Alvarado M, Lin J, Garwood M, Jack CR Jr, Poduslo JF (2008) Selective contrast enhancement of individual Alzheimer's disease amyloid plaques using a polyamine and Gd-DOTA conjugated antibody fragment against fibrillar Abeta42 for magnetic resonance molecular imaging. Pharm Res 25, 1861-1872
77. Takeuchi A, Irizarry MC, Duff K, Saido TC, Ashe KH, Hasegawa M, Mann DMA (2000) Age-related amyloid deposition in transgenic mice overexpressing both Alzheimer mutant presenilin 1 and amyloid precursor protein Swedish mutant is not associated with global neuronal loss.AmJPathol 157, 331-339 (Pubitemid 30641749)
78. Inoue S, Kisilevsky R (2001) Beta-amyloid fibrils of Alzheimer's disease: Pathologically altered, basement membrane-associated microfibrils. Ital J Anat Embryol 106, 93-102
79. Zipser BD, Johanson CE, Gonzalez L, Berzin TM, Tavares R, Hulette CM, Vitek MP, Hovanesian V, Stopa EG (2007) Microvasculature injury and blood-brain barrier leakage in Alzheimer's disease. Neurobiol Aging 28, 977-986 (Pubitemid 46635913)
80. Sarin H, Kanevsky AS, Wu H, Sousa AA, Wilson CM, Aronova MA, Griffiths GL, Leapman RD, Vo HQ (2009) Physiologic upper limit of pore size in the blood-tumor barrier of malignant solid tumors. J Transl Med 7, 51
81. van Bree JBMM, de BoerAG, Danhof M, Ginsel LA, Breimer DD (1988) Characterization of an in vitro blood-brain barrier: Effects of molecular size and lipophilicity on cerebrovascular endothelial transport rates of drugs. J Pharmacol Exp Ther 247, 1233-1239 (Pubitemid 19022140)
82. Robinson PJ, Rapoport SI (1987) Size selectivity of bloodbrain barrier permeability at various times after osmotic opening. Am J Physiol 253, R459-R466
83. Bhaskar S, Tian F, Stoger T, Kreyling W, de la Fuente JM, Grazu V, Borm P, Estrada G, Ntziachristos V, Razansky D (2010) Multifunctional nanocarriers for diagnostics, drug delivery and targeted treatment across the blood-brain barrier: Perspectives on tracking and neuroimaging. Particle Fiber Technol 7, 1-25
84. 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
85. Kreuter J, Shamenkov D, Petrov V, Ramge P, Cychutek K, Koch-Brandt C, Alyautdin R (2002) Apolipoproteinmediated transport of nanoparticle-bound drugs across the blood-brain barrier. J Drug Target 10, 317-325 (Pubitemid 34746313)
86. Nazem A, Mansoori GA (2011) Nanotechnology for Alzheimer's disease detection and treatment. Insciences J 1, 169-193
87. Koffie RM, Farrar CT, Saidi L-J, William CM, Hyman BT, Spires-Jones TL (2011) 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 108, 18837-18842
88. Sahni JK, Doggui S, Ali J, Baboota S, Dao L, Ramassamy C (2011) Neurotherapeutic applications of nanoparticles in Alzheimer's disease. J Controlled Release 152, 208-231
89. Petiet A, Santin M, Bertrand A, Wiggins CJ, Petit F, Houitte D, Hantraye P, Benavides J, Debeir T, Rooney T, Dhenain M (2012) Gadolinium-staining reveals amyloid plaques in the brain of Alzheimer's transgenic mice. Neurobiol Aging 33, 1533-1544
90. Weiner MW, Aisen PS, Jack CR Jr, Jagust WJ, Trojanowski JQ, Shaw L, Saykin AJ, Morris JC, Cairns N, Beckett LA, Toga A, Green R, Walter S, Soares H, Snyder P, Siemers E, Potter W, Cole PE, Schmidt M (2010) The Alzheimer's disease neuroimaging inititative: Progress report and future plans. Alzheimers Dement 6, 201-211
91. Miller G (2009) Alzheimer's biomarker initiative hits its stride. Science 326, 386-389
92. Choi SR, Golding G, Zhuang Z, Zhang W, Lim N, Hefti F, Benedum TE, Kilbourn MR, Skovronsky D, Kung HF (2009) Preclinical properties of 18F-AV-45: A PET agent for Abeta plaques in the brain. J Nucl Med 50, 1887-1894
93. Yang L, Rieves D, Ganley C (2012) Brain amyloid imaging-FDA approval of florbetapir F18 injection. N Engl J Med 367, 885-887
94. Mellon EA, Pilkinton DT, Clark CM, Elliot MA, Witschley WR, Borthakur A, Reddy R (2009) Sodium MR imaging detection of mild Alzheimer disease: Preliminary study. Am J Neuroradiol 30, 978-984
95. Maeda J, Zhang M-R, Okauchi T, Ji B, Ono M, Hattori S, Kumata K, Iwata N, Saido TC, Trojanowski JQ, Lee VM, Staufenbiel M, Tomiyama T, Mori H, Fukumura T, Suhara T, Higuchi M (2011) In vivo positron emission tomographic imaging of glial responses to amyloid-and tau pathologies in mouse models of Alzheimer's disease and related disorders. J Neurosci 31, 4720-4730