Inhibition of amyloid-beta peptide aggregation rescues the autophagic deficits in the TgCRND8 mouse model of Alzheimer disease

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1822, Issue 10, 2012, Pages 1629-1637

  Lai, Aaron Y ^a   McLaurin, JoAnne ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alzheimer disease; Amyloid beta peptide; Autophagy; Lysosome; Scyllo Inositol; TgCRND8

Indexed keywords

AMYLOID BETA PROTEIN; INOSITOL DERIVATIVE; RAB7 PROTEIN; SCYLLO INOSITOL; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CELL FRACTIONATION; CELL FUSION; CELL VACUOLE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; FUNCTIONAL DISEASE; GLIA CELL; LYSOSOME; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; STEREOISOMERISM;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; AUTOPHAGY; BRAIN; DISEASE MODELS, ANIMAL; INOSITOL; LYSOSOMES; MICE; MICE, INBRED C3H; MICE, INBRED C57BL;

MUS;

EID: 84864471069     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2012.07.003     Document Type: Article

References (47)

1. Palmano K.P., Whiting P.H., Hawthorne J.N. Free and lipid myo-inositol in tissues from rats with acute and less severe streptozotocin-induced diabetes. Biochem. J. 1977, 167:229-235.
2. Michaelis T., Helms G., Merboldt K.D., Hänicke W., Bruhn H., Frahm J. Identification of scyllo-inositol in proton NMR spectra of human brain in vivo. NMR Biomed. 1993, 6:105-109.
3. Takenawa T., Egawa K. CDP-diglyceride:inositol transferase from rat liver. Purification and properties. J. Biol. Chem. 1977, 252:5419-5423.
4. Fenili D., Brown M., Rappaport R., McLaurin J. Properties of scyllo-inositol as a therapeutic treatment of AD-like pathology. J. Mol. Med. (Berl) 2007, 85:603-611.
5. McLaurin J., Golomb R., Jurewicz A., Antel J.P., Fraser P.E. Inositol stereoisomers stabilize an oligomeric aggregate of Alzheimer amyloid beta peptide and inhibit Abeta-induced toxicity. J. Biol. Chem. 2000, 275:18495-18502.
6. Wenk G.L. Neuropathologic changes in Alzheimer's disease. J. Clin. Psychiatry 2003, 64(Suppl. 9):7-10.
7. McLaurin J., Kierstead M.E., Brown M.E., Hawkes C.A., Lambermon M.H., Phinney A.L., Darabie A.A., Cousins J.E., French J.E., Lan M.F., Chen F., Wong S.S., Mount H.T., Fraser P.E., Westaway D., St George-Hyslop P. Cyclohexanehexol inhibitors of Abeta aggregation prevent and reverse Alzheimer phenotype in a mouse model. Nat. Med. 2006, 12:801-808.
8. Hawkes C.A., Deng L.H., Shaw J.E., Nitz M., McLaurin J. Small molecule beta-amyloid inhibitors that stabilize protofibrillar structures in vitro improve cognition and pathology in a mouse model of Alzheimer's disease. Eur. J. Neurosci. 2010, 31:203-213.
9. Salloway S., Sperling R., Keren R., Porsteinsson A.P., van Dyck C.H., Tariot P.N., Gilman S., Arnold D., Abushakra S., Hernandez C., Crans G., Liang E., Quinn G., Bairu M., Pastrak A., Cedarbaum J.M. ELND005-AD201 investigators, A phase 2 randomized trial of ELND005, scyllo-inositol, in mild to moderate Alzheimer disease. Neurology 2011, 77:1253-1262.
10. Nixon R.A., Yang D.S. Autophagy failure in Alzheimer's disease-locating the primary defect. Neurobiol. Dis. 2011, 43:38-45.
11. Cheung Z.H., Ip N.Y. Autophagy deregulation in neurodegenerative diseases - recent advances and future perspectives. J. Neurochem. 2011, 118:317-325.
12. Boland B., Kumar A., Lee S., Platt F.M., Wegiel J., Yu W.H., Nixon R.A. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 2008, 28:6926-6937.
13. Jaeger P.A., Wyss-Coray T. All-you-can-eat: autophagy in neurodegeneration and neuroprotection. Mol. Neurodegener. 2009, 4:16.
14. Nixon R.A., Wegiel J., Kumar A., Yu W.H., Peterhoff C., Cataldo A., Cuervo A.M. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 2005, 64:113-122.
15. Yu W.H., Cuervo A.M., Kumar A., Peterhoff C.M., Schmidt S.D., Lee J.H., Mohan P.S., Mercken M., Farmery M.R., Tjernberg L.O., Jiang Y., Duff K., Uchiyama Y., Näslund J., Mathews P.M., Cataldo A.M., Nixon R.A. Macroautophagy - a novel Beta-amyloid peptide-generating pathway activated in Alzheimer's disease. J. Cell Biol. 2005, 171:87-98.
16. Hung S.Y., Huang W.P., Liou H.C., Fu W.M. Autophagy protects neuron from Abeta-induced cytotoxicity. Autophagy 2009, 5:502-510.
17. Wang H., Ma J., Tan Y., Wang Z., Sheng C., Chen S., Ding J. Amyloid-beta1-42 induces reactive oxygen species-mediated autophagic cell death in U87 and SH-SY5Y cells. J. Alzheimers Dis. 2010, 21:597-610.
18. Yang D.S., Stavrides P., Mohan P.S., Kaushik S., Kumar A., Ohno M., Schmidt S.D., Wesson D., Bandyopadhyay U., Jiang Y., Pawlik M., Peterhoff C.M., Yang A.J., Wilson D.A., St George-Hyslop P., Westaway D., Mathews P.M., Levy E., Cuervo A.M., Nixon R.A. Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 2011, 134:258-277.
19. Chishti M.A., Yang D.S., Janus C., Phinney A.L., Horne P., Pearson J., Strome R., Zuker N., Loukides J., French J., Turner S., Lozza G., Grilli M., Kunicki S., Morissette C., Paquette J., Gervais F., Bergeron C., Fraser P.E., Carlson G.A., George-Hyslop P.S., Westaway D. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem. 2001, 276:21562-21570.
20. Ryan D.A., Narrow W.C., Federoff H.J., Bowers W.J. An improved method for generating consistent soluble amyloid-beta oligomer preparations for in vitro neurotoxicity studies. J. Neurosci. Methods 2010, 190:171-179.
21. Marzella L., Ahlberg J., Glaumann H. Isolation of autophagic vacuoles from rat liver: morphological and biochemical characterization. J. Cell Biol. 1982, 93:144-154.
22. Ford T., Rickwood D., Graham J. Buoyant densities of macromolecules, macromolecular complexes, and cell organelles in Nycodenz gradients. Anal. Biochem. 1983, 128:232-239.
23. Knight C.G. Human cathepsin B. Application of the substrate N-benzyloxycarbonyl-l-arginyl-l-arginine 2-naphthylamide to a study of the inhibition by leupeptin. Biochem. J. 1980, 189:447-453.
24. Benchoua A., Braudeau J., Reis A., Couriaud C., Onténiente B. Activation of proinflammatory caspases by cathepsin B in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 2004, 24:1272-1279.
25. Twining S.S. Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes. Anal. Biochem. 1984, 143:30-34.
26. King M.A., Goemans C.G., Hafiz F., Prehn J.H., Wyttenbach A., Tolkovsky A.M. Cytoplasmic inclusions of Htt exon1 containing an expanded polyglutamine tract suppress execution of apoptosis in sympathetic neurons. J. Neurosci. 2008, 31:14401-14415.
27. Singh R., Cuervo A.M. Autophagy in the cellular energetic balance. Cell Metab. 2011, 13:495-504.
28. Dumont F.J., Su Q. Mechanism of action of the immunosuppressant rapamycin. Life Sci. 1996, 58:373-395.
29. Tamboli I.Y., Hampel H., Tien N.T., Tolksdorf K., Breiden B., Mathews P.M., Saftig P., Sandhoff K., Walter J. Sphingolipid storage affects autophagic metabolism of the amyloid precursor protein and promotes Abeta generation. J. Neurosci. 2011, 31:1837-1849.
30. Corrochano S., Renna M., Carter S., Chrobot N., Kent R., Stewart M., Cooper J., Brown S.D., Rubinsztein D.C., Acevedo-Arozena A. α-Synuclein levels modulate Huntington's disease in mice. Hum. Mol. Genet. 2012, 21:485-494.
31. Congdon E.E., Wu J.W., Myeku N., Figueroa Y.H., Herman M., Marinec P.S., Gestwicki J.E., Dickey C.A., Yu W.H., Duff K. Methylthioninium chloride (methylene blue) induces autophagy and attenuates tauopathy in vitro and in vivo. Autophagy 2012, 8:1-14.
32. Eskelinen E.L. Roles of LAMP-1 and LAMP-2 in lysosome biogenesis and autophagy. Mol. Aspects Med. 2006, 27:495-502.
33. Zhang H., Ma Q., Zhang Y.W., Xu H. Proteolytic processing of Alzheimer's β-amyloid precursor protein. J. Neurochem. 2012, 120(Suppl. 1):9-12.
34. Nedelsky N.B., Todd P.K., Taylor J.P. Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection. Biochim. Biophys. Acta 2008, 1782:691-699.
35. Tseng B.P., Green K.N., Chan J.L., Blurton-Jones M., LaFerla F.M. FM, Abeta inhibits the proteasome and enhances amyloid and tau accumulation. Neurobiol. Aging 2008, 29:1607-1618.
36. Eskelinen E.L. Maturation of autophagic vacuoles in Mammalian cells. Autophagy 2005, 1:1-10.
37. Hansen T.E., Johansen T. Following autophagy step by step. BMC Biol. 2011, 9:39.
38. Zerovnik E. The emerging role of cystatins in Alzheimer's disease. Bioessays 2009, 31:597-599.
39. Wyss-Coray T., Loike J.D., Brionne T.C., Lu E., Anankov R., Yan F., Silverstein S.C., Husemann J. Adult mouse astrocytes degrade amyloid-beta in vitro and in situ. Nat. Med. 2003, 9:453-457.
40. Mohamed A., Posse de Chaves E. Aβ internalization by neurons and glia. Int. J. Alzheimers Dis. 2011, 2011:127984.
41. C.A. Hawkes, L. Deng, D. Fenili, M. Nitz, J. McLaurin, In vivo uptake of β-amyloid by non-plaque associated microglia, Curr. Alzheimer Res. (in press), http://dx.doi.org/10.2174/1567212222726212050.
42. Lee S., Sato Y., Nixon R.A. Lysosomal proteolysis inhibition selectively disrupts axonal transport of degradative organelles and causes an Alzheimer's-like axonal dystrophy. J. Neurosci. 2011, 31:7817-7830.
43. Francis B.M., Laskova V., Yang J., Song C., Bazinet R.P., Gupta S., Maj M., Robinson B.H., Mount H.T.J. Energetic Dyshomeostasis in APP-Transgenic TgCRND8 Mice, Program No. 457.7/K19 2010 Neuroscience Meeting Planner 2010, Society for Neuroscience, San Diego, CA, Online.
44. Francis B.M., Kim J., Barakat M.E., Fraenkl S., Yücel Y.H., Peng S., Michalski B., Fahnestock M., McLaurin J., Mount H.T. Object recognition memory and BDNF expression are reduced in young TgCRND8 mice. Neurobiol. Aging 2012, 33:555-563.
45. Sebastiani G., Krzywkowski P., Dudal S., Yu M., Paquette J., Malo D., Gervais F., Tremblay P. Mapping genetic modulators of amyloid plaque deposition in TgCRND8 transgenic mice. Hum. Mol. Genet. 2006, 15:2313-2323.
46. Cataldo A.M., Nixon R.A. Enzymatically active lysosomal proteases are associated with amyloid deposits in Alzheimer brain. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:3861-3865.
47. Amritraj A., Hawkes C., Phinney A.L., Mount H.T., Scott C.D., Westaway D., Kar S. Altered levels and distribution of IGF-II/M6P receptor and lysosomal enzymes in mutant APP and APP + PS1 transgenic mouse brains. Neurobiol. Aging 2009, 30:54-70.