In vivo modification of Abeta plaque toxicity as a novel neuroprotective lithium-mediated therapy for Alzheimer's disease pathology

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Trujillo Estrada, Laura ^a,c   Jimenez, Sebastian ^b,c,d   De Castro, Vanessa ^a,c   Torres, Manuel ^b,c,d,e   Baglietto Vargas, David ^a,c,f   Moreno Gonzalez, Ines ^a,c,g   Navarro, Victoria ^b,c,d   Sanchez Varo, Raquel ^a,c   Sanchez Mejias, Elisabeth ^a,c   Davila, Jose Carlos ^a,c   Vizuete, Marisa ^b,c,d   Gutierrez, Antonia ^a,c   Vitorica, Javier ^b,c,d  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^d HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^e UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Abeta plaques; Alzheimer; Axonal dystrophies; Lithium treatment; Neuronal degeneration; Toxicity; Transgenic mice

Indexed keywords

AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; LITHIUM DERIVATIVE; NEUROPROTECTIVE AGENT; PRESENILIN 1; PSEN1 PROTEIN, HUMAN;

ALZHEIMER DISEASE; ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; CELL DEATH; DISEASE MODEL; DRUG EFFECTS; GENETICS; HUMAN; MALE; MEMORY DISORDERS; METABOLISM; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PLAQUE, AMYLOID; RANDOMIZATION; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ASTROCYTES; BRAIN; CELL DEATH; DISEASE MODELS, ANIMAL; HUMANS; LITHIUM COMPOUNDS; MALE; MEMORY DISORDERS; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; NEUROPROTECTIVE AGENTS; PLAQUE, AMYLOID; PRESENILIN-1; RANDOM ALLOCATION;

EID: 85005781364     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/20515960173     Document Type: Article

References (53)

1. Hardy J, Selkoe DJ: The Amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297: 353-356. 10.1126/science.1072994
2. Wyss-Coray T, Rogers J: Inflammation in Alzheimer Disease's. A Brief Review of the Basic Science and Clinical Literature. Cold Spring Harb Perspect Med 2012, 2: a006346. 10.1101/cshperspect.a006346
3. Diniz B, Machado-Vieira R, Forlenza O: Lithium and neuroprotection: translational evidence and implications for the treatment of neuropsychiatric disorders. Neuropsychiatr Dis Treat 2013, 9: 493-500.
4. Forlenza O, Paula V, Machado-Vieira R, Diniz B, Gattaz W: Does Lithium Prevent Alzheimer's disease? Drugs Aging 2012, 29: 335-342. 10.2165/11599180-000000000-00000
5. Nunes PV, Forlenza OV, Gattaz WF: Lithium and risk for Alzheimer's disease in elderly patients with bipolar disorder. B J Psychiatry 2007, 190: 359-360. 10.1192/bjp.bp.106.029868
6. Young AH: More good news about the magic ion: lithium may prevent dementia. B J Psychiatry 2011, 198: 336-337. 10.1192/bjp.bp.110.082875
7. Bhat RV, Budd Haeberlein SL, Avila J: Glycogen synthase kinase 3: a drug target for CNS therapies. J Neurochem 2004, 89: 1313-1317. 10.1111/j.1471-4159.2004.02422.x
8. Hernandez F, Lucas JJ, Avila J: GSK3 and Tau: two convergence points in Alzheimer's disease. J Alzheime Dis 2013, 33: S141-S144.
9. Jin M, Shepardson N, Yang T, Chen G, Walsh D, Selkoe DJ: Soluble amyloid beta protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc Natl Acad Sci USA 2011, 108: 5819-5824. 10.1073/pnas.1017033108
10. Leroy K, Ando K, Laporte V, Dedecker R, Suain V, Authelet M, et al.: Lack of Tau proteins rescues neuronal cell death and decreases Amyloidogenic Processing of APP in APP/PS1 Mice. Am J Pathol 2012, 181: 1928-1940. 10.1016/j.ajpath.2012.08.012
11. Caccamo A, Oddo S, Tran LX, LaFerla FM: Lithium reduces Tau Phosphorylation but not Abeta or working memory deficits in a transgenic model with both plaques and tangles. Am J Pathol 2007, 170: 1669-1678. 10.2353/ajpath.2007.061178
12. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, et al.: Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 2005, 170: 1101-1111. 10.1083/jcb.200504035
13. Sarkar S, Rubinsztein DC: Inositol and IP3 Levels Regulate Autophagy: Biology and Therapeutic Speculations. Autophagy 2006, 2: 132-134.
14. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, et al.: Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 2005, 64: 113-122.
15. Sanchez-Varo R, Trujillo-Estrada L, Sanchez-Mejias E, Torres M, Baglietto-Vargas D, Moreno-Gonzalez I, et al.: Abnormal accumulation of autophagic vesicles correlates with axonal and synaptic pathology in young Alzheimer's mice hippocampus. Acta Neuropathol 2012, 123: 53-70. 10.1007/s00401-011-0896-x
16. Torres M, Jimenez S, Sanchez-Varo R, Navarro V, Trujillo-Estrada L, Sanchez-Mejias E, et al.: Defective lysosomal proteolysis and axonal transport are early pathogenic events that worsen with age leading to increased APP metabolism and synaptic Abeta in transgenic APP/PS1 hippocampus. Mol Neurodegener 2012, 7: 59. 10.1186/1750-1326-7-59
17. Yu WH, Cuervo AM, Kumar A, Peterhoff CM, Schmidt SD, Lee JH, et al.: Macroautophagy-a novel beta-amyloid peptide-generating pathway activated in Alzheimer's disease. J Cell Biol 2005, 171: 87-98. 10.1083/jcb.200505082
18. Phiel CJ, Wilson CA, Lee VMY, Klein PS: GSK-3[alpha] regulates production of Alzheimer's disease amyloid-[beta] peptides. Nature 2003, 423: 435-439. 10.1038/nature01640
19. Su Y, Ryder J, Li B, Wu X, Solenberg P, Brune K, et al.: Lithium, a common drug for bipolar disorder treatment, regulates amyloid-beta precursor protein processing. Biochemistry 2004, 43: 6899-6908. 10.1021/bi035627j
20. Toledo EM, Inestrosa NC: Activation of Wnt signaling by lithium and rosiglitazone reduced spatial memory impairment and neurodegeneration in brains of an APPswe/PSEN1DeltaE9 mouse model of Alzheimer's disease. Mol Psychiatry 2009, 15: 272-285.
21. Feyt C, Kienlen-Campard P, Leroy K, N'Kuli F, Courtoy PJ, Brion JP, et al.: Lithium Chloride increases the production of Amyloid-beta Peptide independently from its inhibition of Glycogen Synthase Kinase 3. J Biol Chem 2005, 280: 33220-33227. 10.1074/jbc.M501610200
22. Sudduth TL, Wilson JG, Everhart A, Colton CA, Wilcock DM: Lithium treatment of APPSwDI/NOS2 (-/-) Mice Leads to Reduced Hyperphosphorylated Tau. Increased amyloid deposition and altered inflammatory phenotype. PLoS ONE 2012, 7: e31993. 10.1371/journal.pone.0031993
23. Moreno-Gonzalez I, Baglietto-Vargas D, Sanchez-Varo R, Jimenez S, trujillo-estrada L, Sanchez-mejias E, et al.: Extracellular Amyloid-beta and Cytotoxic Glial Activation induce significant entorhinal neuron loss in young PS1M146L/APP751SLMice. J Alzheimers Dis 2009, 18: 755-776.
24. Ramos B, Baglietto-Vargas D, Rio JC, Moreno-Gonzalez I, Santa-Maria C, Jimenez S, et al.: Early neuropathology of Somatostatin/NPY GABAergic cells in the hippocampus of a PS1 x APP transgenic model of Alzheimer's disease. Neurobiol Aging 2006, 27: 1658-1672. 10.1016/j.neurobiolaging.2005.09.022
25. Chan-Palay V, Lang W, Allen YS, Haesler U, Polak JM: Cortical neurons immunoreactive with antisera against neuropeptide Y are altered in Alzheimer's-type dementia. J Comp Neurol 1985, 238: 390-400. 10.1002/cne.902380404
26. Davies P, Katzman R, Terry RD: Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementa. Nature 1980, 288: 279-280. 10.1038/288279a0
27. Blanchard V, Moussaoui S, Czech C, Touchet N, Bonici B, Planche M, et al.: Time sequence of maturation of dystrophic neurites associated with A[beta] deposits in APP/PS1 transgenic mice. ExpNeurol 2003, 184: 247-263.
28. Filali M, Lalonde R, Theriault P, Julien C, Calon F, Planel E: Cognitive and non-cognitive behaviors in the triple transgenic mouse model of Alzheimer's disease expressing mutated APP, PS1, and Mapt (3xTg-AD). Behav Brain Res 2012, 234: 334-342. 10.1016/j.bbr.2012.07.004
29. Davis KE, Easton A, Eacott MJ, Gigg J: Episodic-like memory for What-Where-Which occasion is selectively impaired in the 3xTgAD mouse model of Alzheimer's disease. J Alzheimer Dis 2013, 33: 681-698.
30. Jimenez S, Baglietto-Vargas D, Caballero C, Moreno-Gonzalez I, Torres M, Sanchez-Varo R, et al.: Inflammatory response in the Hippocampus of PS1M146L/APP751SL mouse model of Alzheimer's disease: age-dependent switch in the microglial phenotype from alternative to classic. J Neurosci 2008, 28: 11650-11661. 10.1523/JNEUROSCI.3024-08.2008
31. Jimenez S, Torres M, Vizuete M, Sanchez-Varo R, Sanchez-Mejias E, Trujillo-Estrada L, et al.: Age-dependent Accumulation of Soluble Amyloid beta (Abeta) Oligomers reverses the Neuroprotective Effect of Soluble Amyloid Precursor Protein alpha (sAPPalpha) by Modulating Phosphatidylinositol 3-Kinase (PI3K)/Akt-GSK-3beta Pathway in Alzheimer mouse model. J Biol Chem 2011, 286: 18414-18425. 10.1074/jbc.M110.209718
32. Araujo F, Tan S, Ruano D, Schoemaker H, Benavides J, Vitorica J: Molecular and pharmacological characterization of native cortical gamma-aminobutyric acid(A) receptors containing both alpha(1) and alpha(3) subunits. J Biol Chem 1996, 271: 27902-27911. 10.1074/jbc.271.44.27902
33. Cohen E, Paulsson JF, Blinder P, Burstyn-Cohen T, Du D, Estepa G, et al.: Reduced IGF-1 Signaling delays age-associated proteotoxicity in mice. Cell 2009, 139: 1157-1169. 10.1016/j.cell.2009.11.014
34. Koffie RM, Meyer-Luehmann M, Hashimoto T, Adams KW, Mielke ML, Garcia-Alloza M, et al.: Oligomeric amyloid-beta| associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc Natl Acad Sci USA 2009, 106: 4012-4017. 10.1073/pnas.0811698106
35. Kraft AW, Hu X, Yoon H, Yan P, Xiao Q, Wang Y, et al.: Attenuating astrocyte activation accelerates plaque pathogenesis in APP/PS1 mice. FASEB J 2013, 27: 187-198. 10.1096/fj.12-208660
36. Ojha J, Masilamoni G, Dunlap D, Udoff RA, Cashikar AG: Sequestration of Toxic Oligomers by HspB1 as a Cytoprotective Mechanism. Mol Cell Biol 2011, 31: 3146-3157. 10.1128/MCB.01187-10
37. Yin KJ, Cirrito JR, Yan P, Hu X, Xiao Q, Pan X, et al.: Matrix Metalloproteinases expressed by astrocytes mediate extracellular Amyloid-beta peptide catabolism. J Neurosci 2006, 26: 10939-10948. 10.1523/JNEUROSCI.2085-06.2006
38. Cascella R, Conti S, Tatini F, Evangelisti E, Scartabelli T, Casamenti F, et al.: Extracellular chaperones prevent Abeta-induced toxicity in rat brains. Biochim Biophys Acta - Molecular Basis of Disease 1832, 2013: 1217-1226.
39. Hoshino T, Murao N, Namba T, Takehara M, Adachi H, Katsuno M, et al.: Suppression of Alzheimer's disease-related phenotypes by expression of heat shock protein 70 in mice. J Neurosci 2011, 31: 5225-5234. 10.1523/JNEUROSCI.5478-10.2011
40. Mannini B, Cascella R, Zampagni M, Waarde-Verhagen M, Meehan S, Roodveldt C, et al.: Molecular mechanisms used by chaperones to reduce the toxicity of aberrant protein oligomers. Proc Natl Acad Sci USA 2012, 109: 12479-12484. 10.1073/pnas.1117799109
41. Narayan P, Meehan S, Carver JA, Wilson MR, Dobson CM, Klenerman D: Amyloid-beta Oligomers are Sequestered by both Intracellular and Extracellular Chaperones. Biochemistry 2012, 51: 9270-9276. 10.1021/bi301277k
42. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, et al.: Lysosomal Proteolysis and Autophagy require Presenilin 1 and Are disrupted by Alzheimer-related PS1 mutations. Cell 2010, 141: 1146-1158. 10.1016/j.cell.2010.05.008
43. Yang DS, Stavrides P, Mohan PS, Kaushik S, Kumar A, Ohno M, et al.: Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 2011, 134: 258-277. 10.1093/brain/awq341
44. J A, Wandosell F, Herníndez F: Role of glycogen synthase kinase-3 in Alzheimer's disease pathogenesis and glycogen synthase kinase-3 inhibitors. Expert Rev Neurotherapeutics 2010, 10: 703-710. 10.1586/ern.10.40
45. Heiseke A, Aguib Y, Riemer C, Baier M, Schtzl HM: Lithium induces clearance of protease resistant prion protein in prion-infected cells by induction of autophagy. J Neurochem 2009, 109: 25-34. 10.1111/j.1471-4159.2009.05906.x
46. Parr C, Carzaniga R, Gentleman SM, Van Leuven F, Walter J, Sastre M: Glycogen Synthase Kinase 3 Inhibition Promotes Lysosomal Biogenesis and Autophagic Degradation of the Amyloid- + | Precursor Protein. Mol Cell Biol 2012, 32: 4410-4418. 10.1128/MCB.00930-12
47. Kandalepas P, Sadleir K, Eimer W, Zhao J, Nicholson D, Vassar R: Erratum to: The Alzheimer's beta-secretase BACE1 localizes to normal presynaptic terminals and to dystrophic presynaptic terminals surrounding amyloid plaques. Acta Neuropathol 2013, 126: 329-352. 10.1007/s00401-013-1152-3
48. Xie H, Hou S, Jiang J, Sekutowicz M, Kelly J, Bacskai BJ: Rapid cell death is preceded by amyloid plaque-mediated oxidative stress. Proc Natl Acad Sci USA 2013, 110: 7904-7909. 10.1073/pnas.1217938110
49. Perez-Nievas BG, Stein TD, Tai HC, Dols-Icardo O, Scotton TC, Barroeta-Espar I, et al.: Dissecting phenotypic traits linked to human resilience to Alzheimer's pathology. Brain 2013, 136: 2510-2526. 10.1093/brain/awt171
50. Condello C, Schain A, Grutzendler J: Multicolor time-stamp reveals the dynamics and toxicity of amyloid deposition. Sci Rep 2011, 1: 19.
51. Tomic JL, Pensalfini A, Head E, Glabe CG: Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction. Neurobiol Disease 2009, 35: 352-358. 10.1016/j.nbd.2009.05.024
52. Renkawek K, Bosman G, de Jong W: Expression of small heat-shock protein hsp 27 in reactive gliosis in Alzheimer disease and other types of dementia. Acta Neuropathol 1994, 87: 511-519. 10.1007/BF00294178
53. Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M, Milligan CE: Regulation of heat shock protein 70 release in astrocytes: Role of signaling kinases. Devel Neurobiol 2007, 67: 1815-1829. 10.1002/dneu.20559