Amyloid β inhibits retinoic acid synthesis exacerbating Alzheimer disease pathology which can be attenuated by an retinoic acid receptor α agonist

European Journal of Neuroscience

Volumn 37, Issue 7, 2013, Pages 1182-1192

  Goncalves, Maria B ^a   Clarke, Earl ^a   Hobbs, Carl ^a   Malmqvist, Tony ^a   Deacon, Robert ^b   Jack, Julian ^a   Corcoran, Jonathan P T ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid clearance, insulin degrading enzyme; Neprilysin; Retinoic acid

Indexed keywords

4 [(5,6,7,8 TETRAHYDRO 5,5,8,8 TETRAMETHYL 2 NAPHTHYL)CARBOXAMIDO]BENZOIC ACID; 6 [3 (1 ADAMANTYL) 4 HYDROXYPHENYL] 2 NAPHTHOIC ACID; 6 [4 METHOXY 3 (1 METHYLCYCLOHEXYL)PHENYL] 2 NAPHTHOIC ACID; AMYLOID BETA PROTEIN; INSULINASE; MEMBRANE METALLOENDOPEPTIDASE; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; TAU PROTEIN; TUMOR NECROSIS FACTOR ALPHA;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; EMBRYO; ENZYME ACTIVITY; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BENZOATES; COGNITION; DOWN-REGULATION; INSULYSIN; MICE; MICROGLIA; NEPRILYSIN; NEURONS; RETINOID X RECEPTOR ALPHA; SIGNAL TRANSDUCTION; TETRAHYDRONAPHTHALENES; TRETINOIN;

EID: 84875639160     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12142     Document Type: Article

References (62)

1. Abramov, E., Dolev, I., Fogel, H., Ciccotosto, G.D., Ruff, E. & Slutsky, I. (2009) Amyloid-beta as a positive endogenous regulator of release probability at hippocampal synapses. Nat. Neurosci., 12, 1567-1576.
2. Agudo, M., Yip, P., Davies, M., Bradbury, E., Doherty, P., McMahon, S., Maden, M. & Corcoran, J.P. (2010) A retinoic acid receptor beta agonist (CD2019) overcomes inhibition of axonal outgrowth via phosphoinositide 3-kinase signalling in the injured adult spinal cord. Neurobiol. Dis., 37, 147-155.
3. Aoto, J., Nam, C.I., Poon, M.M., Ting, P. & Chen, L. (2008) Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron, 60, 308-320.
4. Camandola, S. & Mattson, M.P. (2011) Aberrant subcellular neuronal calcium regulation in aging and Alzheimer's disease. Biochim. Biophys. Acta, 1813, 965-973.
5. Cameron, B. & Landreth, G.E. (2010) Inflammation, microglia, and Alzheimer's disease. Neurobiol. Dis., 37, 503-509.
6. Carson, J.A. & Turner, A.J. (2002) Beta-amyloid catabolism: roles for neprilysin (NEP) and other metallopeptidases? J. Neurochem., 81, 1-8.
7. Chen, N., Onisko, B. & Napoli, J.L. (2008) The nuclear transcription factor RARalpha associates with neuronal RNA granules and suppresses translation. J. Biol. Chem., 283, 20841-20847.
8. Cheng, J.S., Dubal, D.B., Kim, D.H., Legleiter, J., Cheng, I.H., Yu, G.Q., Tesseur, I., Wyss-Coray, T., Bonaldo, P. & Mucke, L. (2009) Collagen VI protects neurons against Abeta toxicity. Nat. Neurosci., 12, 119-121.
9. Cirrito, J.R., Yamada, K.A., Finn, M.B., Sloviter, R.S., Bales, K.R., May, P.C., Schoepp, D.D., Paul, S.M., Mennerick, S. & Holtzman, D.M. (2005) Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron, 48, 913-922.
10. Corcoran, J.P., So, P.L. & Maden, M. (2004) Disruption of the retinoid signalling pathway causes a deposition of amyloid beta in the adult rat brain. Eur. J. Neurosci., 20, 896-902.
11. Cramer, P.E., Cirrito, J.R., Wesson, D.W., Lee, C.Y., Karlo, J.C., Zinn, A.E., Casali, B.T., Restivo, J.L., Goebel, W.D., James, M.J., Brunden, K.R., Wilson, D.A. & Landreth, G.E. (2012) ApoE-directed therapeutics rapidly clear beta-amyloid and reverse deficits in AD mouse models. Science, 335, 1503-1506.
12. Deacon, R.M. (2006) Assessing nest building in mice. Nat. Protoc., 1, 1117-1119.
13. Deacon, R.M. & Rawlins, J.N. (2006) T-maze alternation in the rodent. Nat. Protoc., 1, 7-12.
14. Delrieu, J., Ousset, P.J., Caillaud, C. & Vellas, B. (2012) 'Clinical trials in Alzheimer's disease': immunotherapy approaches. J. Neurochem., 120(Suppl 1), 186-193.
15. Ding, Y., Qiao, A., Wang, Z., Goodwin, J.S., Lee, E.S., Block, M.L., Allsbrook, M., McDonald, M.P. & Fan, G.H. (2008) Retinoic acid attenuates beta-amyloid deposition and rescues memory deficits in an Alzheimer's disease transgenic mouse model. J. Neurosci., 28, 11622-11634.
16. Donmez, G., Wang, D., Cohen, D.E. & Guarente, L. (2010) SIRT1 suppresses beta-amyloid production by activating the alpha-secretase gene ADAM10. Cell, 142, 320-332.
17. Duong, V. & Rochette-Egly, C. (2011) The molecular physiology of nuclear retinoic acid receptors. From health to disease. Biochim. Biophys. Acta, 1812, 1023-1031.
18. 2+ dysfunction in neurodegenerative disorders: Alzheimer's disease. BioFactors, 37, 189-196.
19. Goncalves, M.B., Boyle, J., Webber, D.J., Hall, S., Minger, S.L. & Corcoran, J.P. (2005) Timing of the retinoid-signalling pathway determines the expression of neuronal markers in neural progenitor cells. Dev. Biol., 278, 60-70.
20. Goodman, A.B. & Pardee, A.B. (2003) Evidence for defective retinoid transport and function in late onset Alzheimer's disease. Proc. Natl. Acad. Sci. USA, 100, 2901-2905.
21. Hardy, J. & Selkoe, D.J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science, 297, 353-356.
22. Hickman, S.E., Allison, E.K. & El Khoury, J. (2008) Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J. Neurosci., 28, 8354-8360.
23. Ittner, L.M., Ke, Y.D. & Gotz, J. (2009) Phosphorylated Tau interacts with c-Jun N-terminal kinase-interacting protein 1 (JIP1) in Alzheimer disease. J. Biol. Chem., 284, 20909-20916.
24. Jarvis, C.I., Goncalves, M.B., Clarke, E., Dogruel, M., Kalindjian, S.B., Thomas, S.A., Maden, M. & Corcoran, J.P. (2010) Retinoic acid receptor-alpha signalling antagonizes both intracellular and extracellular amyloid-beta production and prevents neuronal cell death caused by amyloid-beta. Eur. J. Neurosci., 32, 1246-1255.
25. Jiang, Q., Lee, C.Y., Mandrekar, S., Wilkinson, B., Cramer, P., Zelcer, N., Mann, K., Lamb, B., Willson, T.M., Collins, J.L., Richardson, J.C., Smith, J.D., Comery, T.A., Riddell, D., Holtzman, D.M., Tontonoz, P. & Landreth, G.E. (2008) ApoE promotes the proteolytic degradation of Abeta. Neuron, 58, 681-693.
26. 3K)/Akt-GSK-3β pathway in Alzheimer mouse model. J. Biol. Chem., 286, 18414-18425.
27. Jin, M., Shepardson, N., Yang, T., Chen, G., Walsh, D. & Selkoe, D.J. (2011) Soluble amyloid β-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc. Natl. Acad. Sci. USA, 108, 5819-5824.
28. Kopeikina, K.J., Carlson, G.A., Pitstick, R., Ludvigson, A.E., Peters, A., Luebke, J.I., Koffie, R.M., Frosch, M.P., Hyman, B.T. & Spires-Jones, T.L. (2011) Tau accumulation causes mitochondrial distribution deficits in neurons in a mouse model of tauopathy and in human Alzheimer's disease brain. Am. J. Pathol., 179, 2071-2082.
29. LaFerla, F.M., Green, K.N. & Oddo, S. (2007) Intracellular amyloid-β in Alzheimer's disease. Nat. Rev. Neurosci., 8, 499-509.
30. Lane, M.A. & Bailey, S.J. (2005) Role of retinoid signalling in the adult brain. Prog. Neurobiol., 75, 275-293.
31. Larson, M.E. & Lesne, S.E. (2012) Soluble Aβ oligomer production and toxicity. J. Neurochem., 120(Suppl 1), 125-139.
32. Leissring, M.A., Farris, W., Chang, A.Y., Walsh, D.M., Wu, X., Sun, X., Frosch, M.P. & Selkoe, D.J. (2003) Enhanced proteolysis of β-amyloid in APP transgenic mice prevents plaque formation, secondary pathology, and premature death. Neuron, 40, 1087-1093.
33. Lipsky, J.J., Berti, J.J., Aquilina, J.W. & Mays, D.C. (1997) Effect of a disulfiram metabolite on retinaldehyde metabolism. Lancet, 350, 1176.
34. Luo, T., Wagner, E. & Drager, U.C. (2009) Integrating retinoic acid signaling with brain function. Dev. Psychol., 45, 139-150.
35. Maden, M. (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci., 8, 755-765.
36. Maghsoodi, B., Poon, M.M., Nam, C.I., Aoto, J., Ting, P. & Chen, L. (2008) Retinoic acid regulates RARα-mediated control of translation in dendritic RNA granules during homeostatic synaptic plasticity. Proc. Natl. Acad. Sci. USA, 105, 16015-16020.
37. Maloney, B. & Lahiri, D.K. (2011) The Alzheimer's amyloid β-peptide (Aβ) binds a specific DNA Aβ-interacting domain (AβID) in the APP, BACE1, and APOE promoters in a sequence-specific manner: characterizing a new regulatory motif. Gene, 488, 1-12.
38. Marr, R.A., Guan, H., Rockenstein, E., Kindy, M., Gage, F.H., Verma, I., Masliah, E. & Hersh, L.B. (2004) Neprilysin regulates amyloid β peptide levels. J. Mol. Neurosci., 22, 5-11.
39. Mattson, M.P., Cheng, B., Culwell, A.R., Esch, F.S., Lieberburg, I. & Rydel, R.E. (1993) Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the β-amyloid precursor protein. Neuron, 10, 243-254.
40. Mawuenyega, K.G., Sigurdson, W., Ovod, V., Munsell, L., Kasten, T., Morris, J.C., Yarasheski, K.E. & Bateman, R.J. (2010) Decreased clearance of CNS β-amyloid in Alzheimer's disease. Science, 330, 1774.
41. McCarthy, K.D. & de Vellis, J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol., 85, 890-902.
42. Meng, Q.Y., Chen, X.N., Zhao, J., Swaab, D.F. & Zhou, J.N. (2011) Distribution of retinoic acid receptor-α immunoreactivity in the human hypothalamus. Neuroscience, 174, 132-142.
43. Nalivaeva, N.N., Beckett, C., Belyaev, N.D. & Turner, A.J. (2012) Are amyloid-degrading enzymes viable therapeutic targets in Alzheimer's disease? J. Neurochem., 120(Suppl 1), 167-185.
44. Plant, L.D., Boyle, J.P., Smith, I.F., Peers, C. & Pearson, H.A. (2003) The production of amyloid β peptide is a critical requirement for the viability of central neurons. J. Neurosci., 23, 5531-5535.
45. + current. Neurobiol. Aging, 27, 1673-1683.
46. Puzzo, D., Privitera, L., Leznik, E., Fa, M., Staniszewski, A., Palmeri, A. & Arancio, O. (2008) Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci., 28, 14537-14545.
47. Puzzo, D., Privitera, L., Fa, M., Staniszewski, A., Hashimoto, G., Aziz, F., Sakurai, M., Ribe, E.M., Troy, C.M., Mercken, M., Jung, S.S., Palmeri, A. & Arancio, O. (2011) Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann. Neurol., 69, 819-830.
48. Qiu, W.Q., Ye, Z., Kholodenko, D., Seubert, P. & Selkoe, D.J. (1997) Degradation of amyloid β-protein by a metalloprotease secreted by microglia and other neural and non-neural cells. J. Biol. Chem., 272, 6641-6646.
49. Rogers, J., Strohmeyer, R., Kovelowski, C.J. & Li, R. (2002) Microglia and inflammatory mechanisms in the clearance of amyloid β peptide. Glia, 40, 260-269.
50. Rogers, J., Mastroeni, D., Leonard, B., Joyce, J. & Grover, A. (2007) Neuroinflammation in Alzheimer's disease and Parkinson's disease: are microglia pathogenic in either disorder? Int. Rev. Neurobiol., 82, 235-246.
51. Rossello, X.S., Igbavboa, U., Weisman, G.A., Sun, G.Y. & Wood, W.G. (2012) AP-2β regulates amyloid β-protein stimulation of apolipoprotein E transcription in astrocytes. Brain Res., 1444, 87-95.
52. Ryan, D.A., Narrow, W.C., Federoff, H.J. & Bowers, W.J. (2010) An improved method for generating consistent soluble amyloid-beta oligomer preparations for in vitro neurotoxicity studies. J. Neurosci. Methods, 190, 171-179.
53. Sarti, F., Schroeder, J., Aoto, J. & Chen, L. (2012) Conditional RARα knockout mice reveal acute requirement for retinoic acid and RARα in homeostatic plasticity. Front. Mol. Neurosci., 5, 16.
54. Serrano-Pozo, A., Frosch, M.P., Masliah, E. & Hyman, B.T. (2011) Neuropathological alterations in Alzheimer disease. Cold Spring Harb. Perspect. Med., 1, a006189.
55. Smith, J.A., Das, A., Ray, S.K. & Banik, N.L. (2012) Role of pro-inflammatory cytokines released from microglia in neurodegenerative diseases. Brain Res. Bull., 87, 10-20.
56. Sonneveld, E., van den Brink, C.E., Tertoolen, L.G., van der Burg, B. & van der Saag, P.T. (1999) Retinoic acid hydroxylase (CYP26) is a key enzyme in neuronal differentiation of embryonal carcinoma cells. Dev. Biol., 213, 390-404.
57. Tamboli, I.Y., Barth, E., Christian, L., Siepmann, M., Kumar, S., Singh, S., Tolksdorf, K., Heneka, M.T., Lutjohann, D., Wunderlich, P. & Walter, J. (2010) Statins promote the degradation of extracellular amyloid β-peptide by microglia via stimulation of exosome-associated insulin-degrading enzyme (IDE) secretion. J. Biol. Chem., 285, 37405-37414.
58. Tippmann, F., Hundt, J., Schneider, A., Endres, K. & Fahrenholz, F. (2009) Up-regulation of the α-secretase ADAM10 by retinoic acid receptors and acitretin. FASEB J., 23, 1643-1654.
59. Tuppo, E.E. & Arias, H.R. (2005) The role of inflammation in Alzheimer's disease. Int. J. Biochem. Cell Biol., 37, 289-305.
60. Vekrellis, K., Ye, Z., Qiu, W.Q., Walsh, D., Hartley, D., Chesneau, V., Rosner, M.R. & Selkoe, D.J. (2000) Neurons regulate extracellular levels of amyloid β-protein via proteolysis by insulin-degrading enzyme. J. Neurosci., 20, 1657-1665.
61. Wang, H.L., Zhang, Z., Hintze, M. & Chen, L. (2011) Decrease in calcium concentration triggers neuronal retinoic acid synthesis during homeostatic synaptic plasticity. J. Neurosci., 31, 17764-17771.
62. Wolf, G. (2006) Is 9-cis-retinoic acid the endogenous ligand for the retinoic acid-X receptor? Nutr. Rev., 64, 532-538.