M1 muscarinic receptor activation protects neurons from β-amyloid toxicity. A role for Wnt signaling pathway

Neurobiology of Disease

Volumn 17, Issue 2, 2004, Pages 337-348

  Farías, Ginny G ^a   Godoy, Juan A ^a   Hernández, Félix ^b   Avila, Jesús ^b   Fisher, Abraham ^c   Inestrosa, Nibaldo C ^a  

^a Fac Cie Biol Pont Univ C   (Chile)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c ISRAEL INSTITUTE FOR BIOLOGICAL RESEARCH   (Israel)

Author keywords

A neurotoxicity; Alzheimer's disease; GSK 3 transgenic mice; M1 mAChR; Wnt Signaling

Indexed keywords

AMYLOID BETA PROTEIN; CYCLIN D1; MUSCARINIC M1 RECEPTOR; MUSCARINIC M1 RECEPTOR AGONIST; WNT PROTEIN;

ANIMAL CELL; ARTICLE; EMBRYO; GENE TARGETING; INHIBITION KINETICS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

AMYLOID BETA-PROTEIN; ANIMALS; BETA CATENIN; CELLS, CULTURED; CYTOPROTECTION; CYTOSKELETAL PROTEINS; EMBRYO; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; MICE; MICE, TRANSGENIC; NEURONS; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M1; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; WNT PROTEINS;

EID: 5144234244     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.07.016     Document Type: Article

References (64)

1. H. Aberle, A. Bauer, J. Stappert, A. Kispert, and R. Kemler β-catenin is a target for the ubiquitin-proteasome pathway EMBO J. 16 1997 3797 3804
2. A. Alvarez, R. Alarcon, C. Opazo, E.O. Campos, F.J. Munoz, and F.H. Calderon Stable complexes involving acetylcholinesterase and amyloid-β peptide change the biochemical properties of the enzyme and increase the neurotoxicity of Alzheimer's fibrils J. Neurosci. 18 1998 3213 3223
3. A. Alvarez, J.A. Godoy, K. Mullendorff, G.H. Olivares, M. Bronfman, and N.C. Inestrosa Wnt-3a overcomes β-amyloid toxicity in rat hippocampal neurons Exp. Cell Res. 297 2004 186 196
4. A. Alvarez, C. Opazo, R. Alarcon, J. Garrido, and N.C. Inestrosa Acetylcholinesterase promotes the aggregation of amyloid-β-peptide fragments by forming a complex with the growing fibrils J. Mol. Biol. 272 1997 348 361
5. G. Alvarez, J.R. Munoz-Montano, J. Satrustegui, J. Avila, E. Bogonez, and J. Diaz-Nido Lithium protects cultured neurons against β-amyloid-induced neurodegeneration J. FEBS Lett. 453 1999 260 264
6. S.G. Anagnostaras, G.G. Murphy, S.E. Hamilton, S.L. Mitchell, N.P. Rahnama, and N.M. Nathanson Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice Nat. Neurosci. 6 2003 51 58
7. V. Asghari, J.F. Wang, J.S. Reiach, and L.T. Young Differential effects of mood stabilizers on Fos/Jun proteins and AP-1 DNA binding activity in human neuroblastoma SH-SY5Y cells Brain Res. Mol. Brain Res. 58 1998 95 102
8. G.N. Bijur, and R.S. Jope Proapoptotic stimuli induce nuclear accumulation of glycogen synthase kinase-3β J. Biol. Chem. 276 2001 37436 37442
9. G.N. Bijur, P. De Sarno, and R.S. Jope Glycogen synthase kinase-3β facilitates staurosporine- and heat shock-induced apoptosis. Protection by lithium J. Biol. Chem. 275 2000 7583 7590
10. A.N. Billin, H. Thirlwell, and D.E. Ayer β-catenin-histone deacetylase interactions regulate the transition of LEF1 from a transcriptional repressor to an activator Mol. Cell. Biol. 20 2000 6882 6890
11. J.D. Buxbaum, M. Oishi, H.I. Chen, R. Pinkas-Kramarski, E.A. Jaffe, and S.E. Gandy Cholinergic agonists and interleukin 1 regulate processing and secretion of the Alzheimer β/A4 amyloid protein precursor Proc. Natl. Acad. Sci. U. S. A. 89 1992 10075 10078
12. A. Cáceres, G. Banker, O. Steward, L. Binder, and M. Payne MAP2 is localized to the dendrites of hippocampal neurons which develop in culture Brain Res. 315 1984 314 318
13. A. Caricasole, A. Copani, A. Caruso, F. Caraci, L. Iacovelli, and M.A. Sortino The Wnt pathway, cell-cycle activation and β-amyloid: novel therapeutic strategies in Alzheimer's disease? Trends Pharmacol. Sci. 24 2003 233 238
14. D. Cook, M.J. Fry, K. Hughes, R. Sumathipala, J.R. Woodgett, and T.C. Dale Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C EMBO J. 15 1996 4526 4536
15. J.T. Coyle, D.L. Price, and M.R. DeLong Alzheimer's disease: a disorder of cortical cholinergic innervation Science 219 1983 1184 1190
16. G.V. De Ferrari, and N.C. Inestrosa Wnt signaling function in Alzheimer's disease Brain Res. Brain Res. Rev. 33 2000 1 12
17. G.V. De Ferrari, M.A. Chacon, M.I. Barria, J.L. Garrido, J.A. Godoy, and G. Olivares Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by β-amyloid fibrils Mol. Psychiatry 8 2003 195 208
18. P. De Sarno, S.A. Shestopal, T.D. King, A. Zmijewska, L. Song, and R.S. Jope Muscarinic receptor activation protects cells from apoptotic effects of DNA damage, oxidative stress, and mitochondrial inhibition J. Biol. Chem. 278 2003 11086 11093
19. R.M. Eglen, A. Choppin, and N. Watson Therapeutic opportunities from muscarinic receptor research Trends Pharmacol. Sci. 22 2001 409 414
20. A. Fisher Therapeutic strategies in Alzheimer's disease: M1 muscarinic agonists Jpn. J. Pharmacol. 84 2000 101 112
21. A. Fisher, R. Brandeis, N. Bar-Ner, M. Kliger-Spatz, N. Natan, and H. Sonego AF150(S) and AF267B: M1 muscarinic agonists as innovative therapies for Alzheimer's disease J. Mol. Neurosci. 19 2002 145 153
22. A. Fisher, Z. Pittel, R. Haring, N. Bar-Ner, M. Kliger-Spatz, and N. Natan M1 muscarinic agonists can modulate major hallmarks in Alzheimer's disease: implications in future therapy J. Mol. Neurosci. 20 2003 139 145
23. J.L. Garrido, J.A. Godoy, A. Alvarez, M. Bronfman, and N.C. Inestrosa Protein kinase C inhibits amyloid β peptide neurotoxicity by acting on members of the Wnt pathway FASEB J. 16 2002 1982 1984
24. I. Genis, A. Fisher, and D.M. Michaelson Site-specific dephosphorylation of tau of apolipoprotein E-deficient and control mice by M1 muscarinic agonist treatment J. Neurochem. 72 1999 206 213
25. C. Geula, and M.M. Mesulam Cholinergic systems and related neuropathological predilection patterns in Alzheimer disease R.D. Terry R. Katzman K.L. Bick Alzheimer Disease 1994 Raven Press New York 263 291
26. N. Goode, K. Hughes, J.R. Woodgett, and P.J. Parker Differential regulation of glycogen synthase kinase-3β by protein kinase C isotypes J. Biol. Chem. 267 1992 16878 16882
27. Z. Gu, P. Zhong, and Z. Yan Activation of muscarinic receptors inhibits β-amyloid peptide-induced signaling in cortical slices J. Biol. Chem. 278 2003 17546 17556
28. R. Haring, A. Fisher, D. Marciano, Z. Pittel, Y. Kloog, and A. Zuckerman Mitogen-activated protein kinase-dependent and protein kinase C-dependent pathways link the m1 muscarinic receptor to β-amyloid precursor protein secretion J. Neurochem. 71 1998 2094 2103
29. F. Hernandez, J. Borrell, C. Guaza, J. Avila, and J.J. Lucas Spatial learning deficit in transgenic mice that conditionally over-express GSK-3β in the brain but do not form tau filaments J. Neurochem. 83 2002 1529 1533
30. O. Huber, R. Korn, J. McLaughlin, M. Ohsugi, B.G. Herrmann, and R. Kemler Nuclear localization of β-catenin by interaction with transcription factor LEF-1 Mech. Dev. 59 1996 3 10
31. N.C. Inestrosa, A. Alvarez, C.A. Perez, R.D. Moreno, M. Vicente, and C. Linker Acetylcholinesterase accelerates assembly of amyloid-β-peptides into Alzheimer's fibrils: possible role of the peripheral site of the enzyme Neuron 16 1996 881 891
32. N.C. Inestrosa, A. Alvarez, J. Godoy, A. Reyes, and G.V. De Ferrari Acetylcholinesterase-amyloid-β-peptide interaction and Wnt signaling involvement in Abeta neurotoxicity Acta Neurol. Scand., Suppl. 176 2000 53 59
33. N.C. Inestrosa, S. Urra, and M. Colombres Acetylcholinesterase (AChE)-amyloid-β-peptide complexes in Alzheimer's Disease. The Wnt signaling pathway Curr. Alzheimer's Res. 2004 (in press)
34. J.N. Joyce, R.B. Gibbs, C.W. Cotman, and J.F. Marshall Regulation of muscarinic receptor in hippocampus following cholinergic denervation and reinnervation by septal and striatal transplants J. Neurosci. 9 1989 2776 2791
35. D. Kaufer, A. Friedman, S. Seidman, and H. Soreq Acute stress facilitates long-lasting changes in cholinergic gene expression Nature 393 1998 373 377
36. D. Kim, K.S. Jun, S.B. Lee, N.G. Kang, D.S. Min, and Y.H. Kim Phospholipase C isozymes selectively couple to specific neurotransmitter receptors Nature 389 1997 290 293
37. C. Leloup, D.M. Michaelson, A. Fisher, T. Hartmann, K. Beyreuther, and R. Stein M1 muscarinic receptors block caspase activation by phosphoinositide 3-kinase- and MAPK/ERK-independent pathways Cell Death Differ. 7 2000 825 833
38. A.I. Levey Muscarinic acetylcholine receptor expression in memory circuits: implications for treatment of Alzheimer disease Proc. Natl. Acad. Sci. U. S. A. 93 1996 13541 13546
39. A.I. Levey, S.M. Edmunds, V. Koliatsos, R.G. Wiley, and C.J. Heilman Expression of m1-m4 muscarinic acetylcholine receptor proteins in rat hippocampus and regulation by cholinergic innervation J. Neurosci. 15 1995 4077 4092
40. L. Lin, B. Georgievska, A. Mattsson, and O. Isacson Cognitive changes and modified processing of amyloid precursor protein in the cortical and hippocampal system after cholinergic synapse loss and muscarinic receptor activation Proc. Natl. Acad. Sci. U. S. A. 96 1999 12108 12113
41. J.J. Lucas, F. Hernandez, P. Gomez-Ramos, M.A. Moran, R. Hen, and J. Avila Decreased nuclear β-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3β conditional transgenic mice EMBO J. 20 2001 27 39
42. X.H. Ma, P. Zhong, Z. Gu, J. Feng, and Z. Yan Muscarinic potentiation of GABA(A) receptor currents is gated by insulin signaling in the prefrontal cortex J. Neurosci. 23 2003 1159 1168
43. L.L. McGrew, K. Takemaru, R. Bates, and R.T. Moon Direct regulation of the Xenopus engrailed-2 promoter by the Wnt signaling pathway, and a molecular screen for Wnt-responsive genes, confirm a role for Wnt signaling during neural patterning in Xenopus Mech. Dev. 87 1999 21 32
44. J.E. Merritt, J.A. Sullivan, J. Tse, S. Wilkinson, and J.S. Nixon Different sensitivities of neutrophil responses to a selective protein kinase C inhibitor Ro 31-8425; redundancy in signal transduction Cell Signalling 9 1997 53 57
45. A. Mudher, and S. Lovestone Alzheimer's disease-do tauists and baptists finally shake hands? Trends Neurosci. 25 2002 22 26
46. R.M. Nitsch, B.E. Slack, R.J. Wurtman, and J.H. Growdon Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors Science 258 1992 304 307
47. R.M. Nitsch, S. Rossner, C. Albrecht, M. Mayhaus, J. Enderich, and R. Schliebs Muscarinic acetylcholine receptors activate the acetylcholinesterase gene promoter J. Physiol. (Paris) 92 1998 257 264
48. R. Nusse A versatile transcriptional effector of Wingless signaling Cell 89 1997 321 323
49. R. Nusse, and H.E. Varmus Wnt genes Cell 69 1992 1073 1087
50. A.M. Palmer Pharmacotherapy for Alzheimer's disease: progress and prospects Trends Pharmacol. Sci. 23 2002 426 433
51. A. Patapoutian, and L.F. Reichardt Roles of Wnt proteins in neural development and maintenance Curr. Opin. Neurobiol. 10 2000 392 399
52. A.E. Reyes, M.A. Chacon, M.C. Dinamarca, W. Cerpa, C. Morgan, and N.C. Inestrosa Acetylcholinesterase-Abeta complexes are more toxic than abeta fibrils in rat hippocampus: effect on rat beta-amyloid aggregation, laminin expression, reactive astrocytosis, and neuronal cell loss Am. J. Pathol. 164 2004 2163 2174
53. E. Sadot, D. Gurwitz, J. Barg, L. Behar, I. Ginzburg, and A. Fisher Activation of m1 muscarinic acetylcholine receptor regulates tau phosphorylation in transfected PC12 cells J. Neurochem. 66 1996 877 880
54. D.J. Selkoe Alzheimer's disease: genes, proteins, and therapy Physiol. Rev. 81 2001 741 766
55. M. Shaw, P. Cohen, and D.R. Alessi Further evidence that the inhibition of glycogen synthase kinase-3β by IGF-1 is mediated by PDK1/PKB-induced phosphorylation of Ser-9 and not by dephosphorylation of Tyr-216 FEBS Lett. 416 1997 307 311
56. L.C. Sheldahl, M. Park, C.C. Malbon, and R.T. Moon Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner Curr. Biol. 9 1999 695 698
57. R. Simantov, and R. Levy Selective regulation of different muscarinic receptors in septum and hippocampus neuronal cultures Brain Res. 505 1989 160 162
58. A. Takashima, K. Noguchi, K. Sato, T. Hoshino, and K. Imahori Tau protein kinase I is essential for amyloid β-protein-induced neurotoxicity Proc. Natl. Acad. Sci. U. S. A. 90 1993 7789 7793
59. A. Takashima, K. Noguchi, G. Michel, M. Mercken, M. Hoshi, and K. Ishiguro Exposure of rat hippocampal neurons to amyloid β-peptide (25-35) induces the inactivation of phosphatidyl inositol-3 kinase and the activation of tau protein kinase I/glycogen synthase kinase-3β Neurosci. Lett. 203 1996 33 36
60. O. Tetsu, and F. McCormick β-catenin regulates expression of cyclin D1 in colon carcinoma cells Nature 398 1999 422 426
61. J. Xie, Q. Guo, H. Zhu, M.W. Wooten, and M.P. Mattson Protein kinase C iota protects neural cells against apoptosis induced by amyloid beta-peptide Brain Res. Mol. Brain. Res. 82 2000 107 113
62. B.A. Yankner Mechanisms of neuronal degeneration in Alzheimer's disease Neuron 16 1996 921 932
63. Z. Zhang, H. Hartmann, V.M. Do, D. Abramowski, C. Sturchler-Pierrat, and M. Staufenbiel Destabilization of β-catenin by mutations in presenilin-1 potentiates neuronal apoptosis Nature 395 1998 698 702
64. F. Zhang, C.J. Phiel, L. Spece, N. Gurvich, and P.S. Klein Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3 J. Biol. Chem. 29 2003 33067 33077