In vivo uptake of β-amyloid by non-plaque associated microglia

Current Alzheimer Research

Volumn 9, Issue 8, 2012, Pages 890-901

  Hawkes, Cheryl A ^a   Deng, LeHua ^b   Fenili, Daniela ^a,c   Nitz, Mark ^b   McLaurin, JoAnne ^a,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alzheimer's disease; Anti aggregant; Transgenic mouse model

Indexed keywords

1 DEOXY 1 FLUORO SCYLLO INOSITOL; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; INOSITOL DERIVATIVE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; DOSE RESPONSE; DRUG TRANSPORT; FEMALE; GENE MUTATION; HIPPOCAMPUS; MALE; MEMORY DISORDER; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL MEMORY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INOSITOL; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; MICROGLIA; NEUROPROTECTIVE AGENTS;

EID: 84864318278     PISSN: 15672050     EISSN: 18755828     Source Type: Journal    
DOI: 10.2174/156720512803251084     Document Type: Article

References (59)

1. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-6 (2002).
2. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8:79-84 (2005).
3. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416:535-9 (2002).
4. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-7 (2006).
5. D'Andrea MR, Cole GM, Ard MD. The microglial phagocytic role with specific plaque types in the Alzheimer disease brain. Neurobiol Aging 25:675-83 (2004).
6. Nagele RG, Wegiel J, Venkataraman V, Imaki H, Wang KC. Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol Aging 25:663-74 (2004).
7. Bolmont T, Haiss F, Eicke D, Radde R, Mathis CA, Klunk WE, et al. Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci 28:4283-92 (2008).
8. Chung H, Brazil MI, Soe TT, Maxfield FR. Uptake, degradation, and release of fibrillar and soluble forms of Alzheimer's amyloid beta-peptide by microglial cells. J Biol Chem 274:32301-8 (1999).
9. Mandrekar S, Jiang Q, Lee CY, Koenigsknecht-Talboo J, Holtzman DM, Landreth GE. Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J Neurosci 29:4252-62 (2009).
10. Stalder M, Deller T, Staufenbiel M, Jucker M. 3D-Reconstruction of microglia and amyloid in APP23 transgenic mice: no evidence of intracellular amyloid. Neurobiol Aging 22:427-34 (2001).
11. Stalder M, Phinney A, Probst A, Sommer B, Staufenbiel M, Jucker M. Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am J Pathol 154:1673-84 (1999).
12. Wegiel J, Wisniewski HM. The complex of microglial cells and amyloid star in three-dimensional reconstruction. Acta Neuropathol 81:116-24 (1990).
13. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, et al. Peripherally administered antibodies against amyloid betapeptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat Med 6:916-9 (2000).
14. Wilcock DM, Rojiani A, Rosenthal A, Levkowitz G, Subbarao S, Alamed J, et al. Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J Neurosci 24:6144-51 (2004).
15. Koenigsknecht-Talboo J, Meyer-Luehmann M, Parsadanian M, Garcia-Alloza M, Finn MB, Hyman BT, et al. Rapid microglial response around amyloid pathology after systemic anti-Abeta antibody administration in PDAPP mice. J Neurosci 28:14156-64 (2008).
16. Okura Y, Kohyama K, Park IK, Matsumoto Y. Nonviral DNA vaccination augments microglial phagocytosis of beta-amyloid deposits as a major clearance pathway in an Alzheimer disease mouse model. J Neuropathol Exp Neurol 67:1063-71 (2008).
17. McLaurin J, Kierstead ME, Brown ME, Hawkes CA, Lambermon MH, Phinney AL, et al. Cyclohexanehexol inhibitors of Abeta aggregation prevent and reverse Alzheimer phenotype in a mouse model. Nat Med 12:801-8 (2006).
18. Sun S, Adejare A. Fluorinated molecules as drugs and imaging agents in the CNS. Curr Top Med Chem 6:1457-64 (2006).
19. Purser S, Moore PR, Swallow S, Gouverneur V. Fluorine in medicinal chemistry. Chem Soc Rev 37:320-30 (2008).
20. Muller K, Faeh C, Diederich F. Fluorine in pharmaceuticals: looking beyond intuition. Science 317:1881-6 (2007).
21. Kirk KL. Selective fluorination in drug design and development: an overview of biochemical rationales. Curr Top Med Chem 6:1447-56 (2006).
22. Sun Y, Zhang G, Hawkes CA, Shaw JE, McLaurin J, Nitz M. Synthesis of scyllo-inositol derivatives and their effects on amyloid beta peptide aggregation. Bioorg Med Chem 16:7177-84 (2008).
23. Frank S, Burbach GJ, Bonin M, Walter M, Streit W, Bechmann I, et al. TREM2 is upregulated in amyloid plaque-associated microglia in aged APP23 transgenic mice. Glia 56:1438-47 (2008).
24. McLaurin J, Golomb R, Jurewicz A, Antel JP, Fraser PE. Inositol stereoisomers stabilize an oligomeric aggregate of Alzheimer amyloid beta peptide and inhibit abeta-induced toxicity. J Biol Chem 275:18495-502 (2000).
25. Spector R. Myo-inositol transport through the blood-brain barrier. Neurochem Res 13:785-7 (1988).
26. Uldry M, Ibberson M, Horisberger JD, Chatton JY, Riederer BM, Thorens B. Identification of a mammalian H(+)-myo-inositol symporter expressed predominantly in the brain. EMBO J 20:4467-77 (2001).
27. Kwon HM, Yamauchi A, Uchida S, Preston AS, Garcia-Perez A, Burg MB, et al. Cloning of the cDNa for a Na+/myo-inositol cotransporter, a hypertonicity stress protein. J Biol Chem 267:6297-301 (1992).
28. Janus C, Pearson J, McLaurin J, Mathews PM, Jiang Y, Schmidt SD, et al. A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408:979-82 (2000).
29. Dodart JC, Bales KR, Gannon KS, Greene SJ, DeMattos RB, Mathis C, et al. Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat Neurosci 5:452-7 (2002).
30. Tambuyzer BR, Ponsaerts P, Nouwen EJ. Microglia: gatekeepers of central nervous system immunology. J Leukoc Biol 85:352-70 (2009).
31. Luhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, Dobeli H, et al. 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc Natl Acad Sci U S A 102:17342-7 (2005).
32. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71-82 (2003).
33. Kim WK, Alvarez X, Fisher J, Bronfin B, Westmoreland S, McLaurin J, et al. CD163 identifies perivascular macrophages in normal and viral encephalitic brains and potential precursors to perivascular macrophages in blood. Am J Pathol 168:822-34 (2006).
34. Hawkes CA, McLaurin J. Selective targeting of perivascular macrophages for clearance of beta-amyloid in cerebral amyloid angiopathy. Proc Natl Acad Sci U S A 106:1261-6 (2009).
35. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49:489-502 (2006).
36. Boissonneault V, Filali M, Lessard M, Relton J, Wong G, Rivest S. Powerful beneficial effects of macrophage colony-stimulating factor on beta-amyloid deposition and cognitive impairment in Alzheimer's disease. Brain 132:1078-92 (2009).
37. Nicoll JA, Barton E, Boche D, Neal JW, Ferrer I, Thompson P, et al. Abeta species removal after abeta42 immunization. J Neuropathol Exp Neurol 65:1040-8 (2006).
38. Mak SK, McCormack AL, Manning-Bog AB, Cuervo AM, Di Monte DA. Lysosomal degradation of {alpha}-synuclein in vivo. J Biol Chem 285:13621-9 (2010).
39. van der Hilst JC, Kluve-Beckerman B, van der Meer JW, Simon A. Cathepsin D activity protects against development of type AA amyloid fibrils. Eur J Clin Invest 39:412-6 (2009).
40. Huang WC, Yen FC, Shiao YJ, Shie FS, Chan JL, Yang CN, et al. Enlargement of Abeta aggregates through chemokine-dependent microglial clustering. Neurosci Res 63:280-7 (2009).
41. Dal Bianco A, Bradl M, Frischer J, Kutzelnigg A, Jellinger K, Lassmann H. Multiple sclerosis and Alzheimer's disease. Ann Neurol 63:174-83 (2008).
42. Andras IE, Eum SY, Huang W, Zhong Y, Hennig B, Toborek M. HIV-1-induced amyloid beta accumulation in brain endothelial cells is attenuated by simvastatin. Mol Cell Neurosci 43:232-43 (2009).
43. Pulliam L. HIV regulation of amyloid beta production. J Neuroimmune Pharmacol 4:213-7 (2009).
44. Grathwohl SA, Kalin RE, Bolmont T, Prokop S, Winkelmann G, Kaeser SA, et al. Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat Neurosci 12:1361-3 (2009).
45. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8:752-8 (2005).
46. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308:1314-8 (2005).
47. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14:837-42 (2008).
48. Liu Z, Condello C, Schain A, Harb R, Grutzendler J. CX3CR1 in microglia regulates brain amyloid deposition through selective protofibrillar amyloid-beta phagocytosis. J Neurosci 30:17091-101 (2010).
49. Asami-Odaka A, Obayashi-Adachi Y, Matsumoto Y, Takahashi H, Fukumoto H, Horiguchi T, et al. Passive immunization of the Abeta42(43) C-terminal-specific antibody BC05 in a mouse model of Alzheimer's disease. Neurodegener Dis 2:36-43 (2005).
50. Solomon B, Koppel R, Frankel D, Hanan-Aharon E. Disaggregation of Alzheimer beta-amyloid by site-directed mAb. Proc Natl Acad Sci U S A 94:4109-12 (1997).
51. Wilcock DM, DiCarlo G, Henderson D, Jackson J, Clarke K, Ugen KE, et al. Intracranially administered anti-Abeta antibodies reduce beta-amyloid deposition by mechanisms both independent of and associated with microglial activation. J Neurosci 23:3745-51 (2003).
52. Bayer TA, Wirths O. Intracellular accumulation of amyloid-Beta-a predictor for synaptic dysfunction and neuron loss in Alzheimer's disease. Front Aging Neurosci 2:8 (2010).
53. D'Andrea MR, Reiser PA, Polkovitch DA, Gumula NA, Branchide B, Hertzog BM, et al. The use of formic acid to embellish amyloid plaque detection in Alzheimer's disease tissues misguides key observations. Neurosci Lett 342:114-8 (2003).
54. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 8:499-509 (2007).
55. Ohyagi Y, Tsuruta Y, Motomura K, Miyoshi K, Kikuchi H, Iwaki T, et al. Intraneuronal amyloid beta42 enhanced by heating but counteracted by formic acid. J Neurosci Methods 159:134-8 (2007).
56. Barrachina M, Maes T, Buesa C, Ferrer I. Lysosome-associated membrane protein 1 (LAMP-1) in Alzheimer's disease. Neuropathol Appl Neurobiol 32:505-16 (2006).
57. Ard MD, Cole GM, Wei J, Mehrle AP, Fratkin JD. Scavenging of Alzheimer's amyloid beta-protein by microglia in culture. J Neurosci Res 43:190-202 (1996).
58. Paresce DM, Chung H, Maxfield FR. Slow degradation of aggregates of the Alzheimer's disease amyloid beta-protein by microglial cells. J Biol Chem 272:29390-7 (1997).
59. Zotova E, Holmes C, Johnston D, Neal JW, Nicoll JA, Boche D. Microglial alterations in human Alzheimer's disease following Ab42 immunisation. Neuropathol Appl Neurobiol Dec 17. doi: 10.1111/j.1365-2990.2010.01156.x. 37(5): 513-24 (2011).