13-Desmethyl spirolide-C is neuroprotective and reduces intracellular Aβ and hyperphosphorylated tau in vitro

Neurochemistry International

Volumn 59, Issue 7, 2011, Pages 1056-1065

  Alonso, Eva ^a   Vale, Carmen ^a   Vieytes, Mercedes R ^a   Laferla, Frank M ^b   Giménez Llort, Lydia ^c   Botana, Luis M ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c INSTITUT DE NEUROCIÈNCIES   (Spain)

Author keywords

Acetylcholine; Alzheimer disease; Amyloid beta; Spirolides; Tau protein

Indexed keywords

13 DESMETHYL SPIROLIDE C; ACETYLCHOLINE; AMYLOID BETA PROTEIN; BUNGAROTOXIN RECEPTOR; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3BETA; IMINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; NEUROPROTECTIVE AGENT; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MOUSE; NERVE CELL; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSGENIC ANIMAL;

AMYLOID BETA-PEPTIDES; ANIMALS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MICE; NEUROPROTECTIVE AGENTS; PHOSPHORYLATION; SPIRO COMPOUNDS; TAU PROTEINS;

MUS MUSCULUS;

EID: 80055007441     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.08.013     Document Type: Article

References (58)

1. J. Apelt, A. Kumar, and R. Schliebs Impairment of cholinergic neurotransmission in adult and aged transgenic Tg2576 mouse brain expressing the Swedish mutation of human beta-amyloid precursor protein Brain Res. 953 2002 17 30
2. K.R. Bales, E.T. Tzavara, S. Wu, M.R. Wade, F.P. Bymaster, S.M. Paul, and G.G. Nomikos Cholinergic dysfunction in a mouse model of Alzheimer disease is reversed by an anti-A beta antibody J. Clin. Invest. 116 2006 825 832
3. K.A. Bell, K.J. O'Riordan, J.D. Sweatt, and K.T. Dineley MAPK recruitment by beta-amyloid in organotypic hippocampal slice cultures depends on physical state and exposure time J. Neurochem. 91 2004 349 361
4. W. Billard, H. Binch 3rd, G. Crosby, and R.D. McQuade Identification of the primary muscarinic autoreceptor subtype in rat striatum as m2 through a correlation of in vivo microdialysis and in vitro receptor binding data J. Pharmacol. Exp. Ther. 273 1995 273 279
5. L.M. Billings, S. Oddo, K.N. Green, J.L. McGaugh, and F.M. LaFerla Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice Neuron 45 2005 675 688
6. Birks, J., 2006. Cholinesterase inhibitors for Alzheimer's disease. Cochrane Database Syst. Rev. CD005593.
7. Y. Bourne, Z. Radic, R. Araoz, T.T. Talley, E. Benoit, D. Servent, P. Taylor, J. Molgo, and P. Marchot Structural determinants in phycotoxins and AChBP conferring high affinity binding and nicotinic AChR antagonism Proc. Natl. Acad. Sci. USA 107 2010 6076 6081
8. A. Caccamo, S. Oddo, L.M. Billings, K.N. Green, H. Martinez-Coria, A. Fisher, and F.M. LaFerla M1 receptors play a central role in modulating AD-like pathology in transgenic mice Neuron 49 2006 671 682
9. S.L. Chan, K. Furukawa, and M.P. Mattson Presenilins and APP in neuritic and synaptic plasticity: implications for the pathogenesis of Alzheimer's disease Neuromol. Med. 2 2002 167 196
10. D.W. Choi, M. Maulucci-Gedde, and A.R. Kriegstein Glutamate neurotoxicity in cortical cell culture J. Neurosci. 7 1987 357 368
11. F. Crawford, J. Hardy, M. Mullan, A. Goate, D. Hughes, L. Fidani, P. Roques, M. Rossor, and M.C. Chartier-Harlin Sequencing of exons 16 and 17 of the beta-amyloid precursor protein gene in 14 families with early onset Alzheimer's disease fails to reveal mutations in the beta-amyloid sequence Neurosci. Lett. 133 1991 1 2
12. L. Crews, and E. Masliah Molecular mechanisms of neurodegeneration in Alzheimer's disease Hum. Mol. Genet. 19 2010 R12 R20
13. F.G. De Felice, D. Wu, M.P. Lambert, S.J. Fernandez, P.T. Velasco, P.N. Lacor, E.H. Bigio, J. Jerecic, P.J. Acton, P.J. Shughrue, E. Chen-Dodson, G.G. Kinney, and W.L. Klein Alzheimer's disease-type neuronal tau hyperphosphorylation induced by A beta oligomers Neurobiol. Aging 29 2008 1334 1347
14. K.T. Dineley, M. Westerman, D. Bui, K. Bell, K.H. Ashe, and J.D. Sweatt Beta-amyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease J. Neurosci. 21 2001 4125 4133
15. A. Fisher Cholinergic treatments with emphasis on m1 muscarinic agonists as potential disease-modifying agents for Alzheimer's disease Neurotherapeutics 5 2008 433 442
16. S. Gill, M. Murphy, J. Clausen, D. Richard, M. Quilliam, S. MacKinnon, P. LaBlanc, R. Mueller, and O. Pulido Neural injury biomarkers of novel shellfish toxins, spirolides: a pilot study using immunochemical and transcriptional analysis Neurotoxicology 24 2003 593 604
17. G.W. Gribble The diversity of naturally produced organohalogens Chemosphere 52 2003 289 297
18. 2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 1985 3440 3450
19. S.M. Gueret, and M.A. Brimble Spiroimine shellfish poisoning (SSP) and the spirolide family of shellfish toxins: isolation, structure, biological activity and synthesis Nat. Prod. Rep. 27 2010 1350 1366
20. J.P. Guo, T. Arai, J. Miklossy, and P.L. McGeer Abeta and tau form soluble complexes that may promote self aggregation of both into the insoluble forms observed in Alzheimer's disease Proc. Natl. Acad. Sci. USA 103 2006 1953 1958
21. M. Hu, J.F. Waring, M. Gopalakrishnan, and J. Li Role of GSK-3beta activation and alpha7 nAChRs in Abeta(1-42)-induced tau phosphorylation in PC12 cells J. Neurochem. 106 2008 1371 1377
22. L.S. Jefferson, J.R. Fabian, and S.R. Kimball Glycogen synthase kinase-3 is the predominant insulin-regulated eukaryotic initiation factor 2B kinase in skeletal muscle Int. J. Biochem. Cell Biol. 31 1999 191 200
23. S. Kar, and R. Quirion Amyloid beta peptides and central cholinergic neurons: functional interrelationship and relevance to Alzheimer's disease pathology Prog. Brain Res. 145 2004 261 274
24. T. Kihara, S. Shimohama, M. Urushitani, H. Sawada, J. Kimura, T. Kume, T. Maeda, and A. Akaike Stimulation of alpha4beta2 nicotinic acetylcholine receptors inhibits beta-amyloid toxicity Brain Res. 792 1998 331 334
25. F.M. LaFerla Pathways linking Abeta and tau pathologies Biochem. Soc. Trans. 38 2010 993 995
26. C.J. Langmead, J. Watson, and C. Reavill Muscarinic acetylcholine receptors as CNS drug targets Pharmacol. Ther. 117 2008 232 243
27. V. Laudenbach, F. Medja, M. Zoli, F.M. Rossi, P. Evrard, J.P. Changeux, and P. Gressens Selective activation of central subtypes of the nicotinic acetylcholine receptor has opposite effects on neonatal excitotoxic brain injuries FASEB J. 16 2002 423 425
28. A. Lehmann, and I. Jacobson Ion dependence and receptor mediation of glutamate toxicity in the immature rat hippocampal slice Eur. J. Neurosci. 2 1990 620 628
29. E. Levy-Lahad, E.M. Wijsman, E. Nemens, L. Anderson, K.A. Goddard, J.L. Weber, T.D. Bird, and G.D. Schellenberg A familial Alzheimer's disease locus on chromosome 1 Science 269 1995 970 973
30. G.P. Lim, F. Yang, T. Chu, E. Gahtan, O. Ubeda, W. Beech, J.B. Overmier, K. Hsiao-Ashec, S.A. Frautschy, and G.M. Cole Ibuprofen effects on Alzheimer pathology and open field activity in APPsw transgenic mice Neurobiol. Aging 22 2001 983 991
31. P.D. Livingstone, J.A. Dickinson, J. Srinivasan, J.N. Kew, and S. Wonnacott Glutamate-dopamine crosstalk in the rat prefrontal cortex is modulated by Alpha7 nicotinic receptors and potentiated by PNU-120596 J. Mol. Neurosci. 40 2010 172 176
32. S.E. Martin, N.E. de Fiebre, and C.M. de Fiebre The alpha7 nicotinic acetylcholine receptor-selective antagonist, methyllycaconitine, partially protects against beta-amyloid 1-42 toxicity in primary neuron-enriched cultures Brain Res. 1022 2004 254 256
33. H. Martinez-Coria, K.N. Green, L.M. Billings, M. Kitazawa, M. Albrecht, G. Rammes, C.G. Parsons, S. Gupta, P. Banerjee, and F.M. LaFerla Memantine improves cognition and reduces Alzheimer's-like neuropathology in transgenic mice Am. J. Pathol. 176 2010 870 880
34. M. Mercken, M. Vandermeeren, U. Lubke, J. Six, J. Boons, A. Van de Voorde, J.J. Martin, and J. Gheuens Monoclonal antibodies with selective specificity for Alzheimer tau are directed against phosphatase-sensitive epitopes Acta Neuropathol. 84 1992 265 272
35. M. Mousavi, and E. Hellstrom-Lindahl Nicotinic receptor agonists and antagonists increase sAPPalpha secretion and decrease Abeta levels in vitro Neurochem. Int. 54 2009 237 244
36. J.L. Muir Acetylcholine, aging, and Alzheimer's disease Pharmacol. Biochem. Behav. 56 1997 687 696
37. R. Munday Toxicology of cyclic imines: gymnodimine, spirolides, pinnatoxins, pteriatoxins, prorocentrolide, spiro-prorocentrimine and symbioimines L.M. Botana, Seafood and Freshwater Toxins 2008 CRC Press Boca Raton, FL 581 594
38. S. Oddo, A. Caccamo, J.D. Shepherd, M.P. Murphy, T.E. Golde, R. Kayed, R. Metherate, M.P. Mattson, Y. Akbari, and F.M. LaFerla Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction Neuron 39 2003 409 421
39. S. Oddo, A. Caccamo, B. Tseng, D. Cheng, V. Vasilevko, D.H. Cribbs, and F.M. LaFerla Blocking Abeta42 accumulation delays the onset and progression of tau pathology via the C terminus of heat shock protein70-interacting protein: a mechanistic link between Abeta and tau pathology J. Neurosci. 28 2008 12163 12175
40. M. Pakaski, and J. Kalman Interactions between the amyloid and cholinergic mechanisms in Alzheimer's disease Neurochem. Int. 53 2008 103 111
41. K.A. Roth Caspases, apoptosis, and Alzheimer disease: causation, correlation, and confusion J. Neuropathol. Exp. Neurol. 60 2001 829 838
42. G.H. Sack Jr., C.C. Talbot Jr., B.G. McCarthy, E.L. Harris, D. Kastner, L. Gruberg, and M. Pras Exclusion of linkage between familial Mediterranean fever and the human serum amyloid A (SAA) gene cluster Hum. Genet. 87 1991 506 508
43. D.J. Selkoe Alzheimer's disease: genes, proteins, and therapy Physiol. Rev. 81 2001 741 766
44. 2+ release in the 3xTg-AD mouse model of Alzheimer's disease J. Neurochem. 94 2005 1711 1718
45. Y. Takada, A. Yonezawa, T. Kume, H. Katsuki, S. Kaneko, H. Sugimoto, and A. Akaike Nicotinic acetylcholine receptor-mediated neuroprotection by donepezil against glutamate neurotoxicity in rat cortical neurons J. Pharmacol. Exp. Ther. 306 2003 772 777
46. Y. Takada-Takatori, T. Kume, M. Sugimoto, H. Katsuki, T. Niidome, H. Sugimoto, T. Fujii, S. Okabe, and A. Akaike Neuroprotective effects of galanthamine and tacrine against glutamate neurotoxicity Eur. J. Pharmacol. 549 2006 19 26
47. Y. Takada-Takatori, T. Kume, M. Sugimoto, H. Katsuki, H. Sugimoto, and A. Akaike Acetylcholinesterase inhibitors used in treatment of Alzheimer's disease prevent glutamate neurotoxicity via nicotinic acetylcholine receptors and phosphatidylinositol 3-kinase cascade Neuropharmacology 51 2006 474 486
48. C. Vale, and D.H. Sanes Afferent regulation of inhibitory synaptic transmission in the developing auditory midbrain J. Neurosci. 20 2000 1912 1921
49. C. Vale, and D.H. Sanes The effect of bilateral deafness on excitatory and inhibitory synaptic strength in the inferior colliculus Eur. J. Neurosci. 16 2002 2394 2404
50. C. Vale, K.C. Nicolaou, M.O. Frederick, B. Gomez-Limia, A. Alfonso, M.R. Vieytes, and L.M. Botana Effects of azaspiracid-1, a potent cytotoxic agent, on primary neuronal cultures. A structure-activity relationship study J. Med. Chem. 50 2007 356 363
51. C. Vale, E. Alonso, J.A. Rubiolo, M.R. Vieytes, F.M. LaFerla, L. Gimenez-Llort, and L.M. Botana Profile for amyloid-beta and tau expression in primary cortical cultures from 3xTg-AD mice Cell. Mol. Neurobiol. 30 2010 577 590
52. T. Varming, J. Drejer, A. Frandsen, and A. Schousboe Characterization of a chemical anoxia model in cerebellar granule neurons using sodium azide: protection by nifedipine and MK-801 J. Neurosci. Res. 44 1996 40 46
53. A. Villar Gonzalez, M.L. Rodriguez-Velasco, B. Ben-Gigirey, and L.M. Botana First evidence of spirolides in Spanish shellfish Toxicon 48 2006 1068 1074
54. U. Wagner, M. Utton, J.M. Gallo, and C.C. Miller Cellular phosphorylation of tau by GSK-3 beta influences tau binding to microtubules and microtubule organisation J. Cell Sci. 109 Pt 6 1996 1537 1543
55. C.B. Wandscheer, N. Vilarino, B. Espina, M.C. Louzao, and L.M. Botana Human muscarinic acetylcholine receptors are a target of the marine toxin 13-desmethyl C spirolide Chem. Res. Toxicol. 23 2010 1753 1761
56. H.Y. Wang, W. Li, N.J. Benedetti, and D.H. Lee Alpha 7 nicotinic acetylcholine receptors mediate beta-amyloid peptide-induced tau protein phosphorylation J. Biol. Chem. 278 2003 31547 31553
57. Q. Yan, J. Zhang, H. Liu, S. Babu-Khan, R. Vassar, A.L. Biere, M. Citron, and G. Landreth Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease J. Neurosci. 23 2003 7504 7509
58. K.F. Young, S.H. Pasternak, and R.J. Rylett Oligomeric aggregates of amyloid beta peptide 1-42 activate ERK/MAPK in SH-SY5Y cells via the alpha7 nicotinic receptor Neurochem. Int. 55 2009 796 801