MAPK recruitment by β-amyloid in organotypic hippocampal slice cultures depends on physical state and exposure time

Journal of Neurochemistry

Volumn 91, Issue 2, 2004, Pages 349-361

  Bell, Karen A ^a,c   O'Riordan, Kenneth J ^a   Sweatt, J David ^a   Dineley, Kelly T ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

^c VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alpha7; Alzheimer; Hippocampus; Nicotinic receptor; Oligomer

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; CHOLINERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINE; NICOTINIC RECEPTOR; OLIGOMER; PHOSPHATIDYLINOSITOL 3 KINASE; S6 KINASE;

ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HIPPOCAMPUS; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; TISSUE CULTURE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMYLOID BETA-PROTEIN; ANIMALS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; ENZYME INHIBITORS; HIPPOCAMPUS; MACROMOLECULAR SUBSTANCES; MITOGEN-ACTIVATED PROTEIN KINASES; NICOTINE; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SIGNAL TRANSDUCTION; TIME FACTORS;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 5444257609     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02722.x     Document Type: Article

References (75)

1. Backman L., Andersson J. L., Nyberg L., Winblad B., Nordberg A. and Almkvist O. (1999) Brain regions associated with episodic retrieval in normal aging and Alzheimer's disease. Neurology 52, 1861-1870.
2. Backman L., Small B. J. and Fratiglioni L. (2001) Stability of the preclinical episodic memory deficit in Alzheimer's disease. Brain 124, 96-102.
3. Baudry M., Arst D., Oliver M. and Lynch G. (1981) Development of glutamate binding sites and their regulation by calcium in rat hippocampus. Brain Res. 227, 37-48.
4. Burdick D., Soreghan B., Kwon M., Kosmoski J., Knauer M., Henschen A., Yates J., Cotman C. and Glabe C. (1992) Assembly and aggregation properties of synthetic Alzheimer's A4/beta amyloid peptide analogs. J. Biol. Chem. 267, 546-554.
5. Casamayor A., Morrice N. A. and Alessi D. R. (1999) Phosphorylation of Ser-241 is essential for the activity of 3-phosphoinositide-dependent protein kinase-1: identification of five sites of phosphorylation in vivo. Biochem. J. 342, 287-292.
6. Chandler L. J., Sutton G., Dorairaj N. R. and Norwood D. (2001) N-Methyl D-aspartate receptor-mediated bidirectional control of extracellular signal-regulated kinase activity in cortical neuronal cultures. J. Biol. Chem. 276, 2627-2636.
7. Chapman P. F., White G. L., Jones M. W. et al. (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 2, 271-276.
8. Chijiwa T., Mishima A., Hagiwara M., Sano M., Hayashi K., Inoue T., Naito K., Toshioka T. and Hidaka H. (1990) Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5- isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 265, 5267-5272.
9. Cook S. J. and McCormick F. (1993) Inhibition by cAMP of Ras-dependent activation of Raf. Science 262, 1069-1072.
10. Court J. A., Lloyd S., Thomas N., Piggott M. A., Marshall E. F., Morris C. M., Lamb H., Perry R. H., Johnson M. and Perry E. K. (1998) Dopamine and nicotinic receptor binding and the levels of dopamine and homovanillic acid in human brain related to tobacco use. Neuroscience 87, 63-78.
11. Dahlgren K. N., Manelli A. M., Stine W. B. Jr, Baker L. K., Krafft G. A. and LaDu M. J. (2002) Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 277, 32046-32053.
12. Dajas-Bailador F. A., Soliakov L. and Wonnacott S. (2002) Nicotine activates the extracellular signal-regulated kinase 1/2 via the alpha7 nicotinic acetylcholine receptor and protein kinase A, in SH-SY5Y cells and hippocampal neurones. J. Neurochem. 80, 520-530.
13. Dineley K. T., Westerman M., Bui D., Bell K., Ashe K. H. and Sweatt J. D. (2001) beta-Amyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha? nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease. J. Neurosci. 21, 4125-4133.
14. Dineley K. T., Bell K. A., Bui D. and Sweatt J. D. (2002) beta-Amyloid peptide activates alpha 7 nicotinic acetylcholine receptors expressed in Xenopus oocytes. J. Biol. Chem. 277, 25056-25061.
15. Fabian-Fine R., Skehel P., Errington M. L., Davies H. A., Sher E., Stewart M. G. and Fine A. (2001) Ultrastructural distribution of the alpha? nicotinic acetylcholine receptor subunit in rat hippocampus. J. Neurosci. 21, 7993-8003.
16. Ferrer I., Blanco R., Carmona M., Ribera R., Goutan E., Puig B., Rey M. J., Cardozo A., Vinals F. and Ribalta T. (2001) Phosphorylated map kinase (ERK1, ERK2) expression is associated with early tau deposition in neurones and glial cells, but not with increased nuclear DNA vulnerability and cell death, in Alzheimer disease, Pick's disease, progressive supranuclear palsy and corticobasal degeneration. Brain Pathol. 11, 144-158.
17. Fogarty M. P., Downer E. J. and Campbell V. (2003) A role for c-Jun N-terminal kinase 1 (JNK1), but not JNK2, in the beta-amyloid-mediated stabilization of protein p53 and induction of the apoptotic cascade in cultured cortical neurons. Biochem. J. 371, 789-798.
18. Fleming Y., Armstrong C. G., Morrice N., Paterson A., Goedert M. and Cohen P. (2000) Synergistic activation of stress-activated protein kinase 1/C-Jun N-terminal kinase (SAPK1/JNK) isoforms by mitogen-activated protein kinase 4 (MKK4) and MKK7. Biochem. J. 352, 145-154.
19. Gahring L. C., Persiyanov K., Dunn D., Weiss R., Meyer E. L. and Rogers S. W. (2004) Mouse strain-specific nicotinic acetylcholine receptor expression by inhibitory interneurons and astrocytes in the dorsal hippocampus. J. Comp. Neurol. 468, 334-346.
20. Gallo K. A. and Johnson G. L. (2002) Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol Cell Biol. 3, 663-672.
21. Garrington T. P. and Johnson G. L. (1999) Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr. Opin. Cell Biol. 11, 211-218.
22. Gong Y., Chang L., Viola K. L., Lacor P. N., Lambert M. P., Finch C. E., Krafft G. A. and Klein W. L. (2003) Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl Acad. Sci. USA 100, 10417-10422.
23. Grewal S. S., York R. D. and Stork P. J. (1999) Extracellular-signal- regulated kinase signalling in neurons. Curr. Opin. Neurobiol. 9, 544-553.
24. Hajos F., Balazs R., Baker R. E., Gerics B. and Nuijtinck R. (1994) Structural maturation, cell proliferation and bioelectric activity in long-term slice-cultures of immature rat hippocampus. Int. J. Dev. Neurosci. 12, 87-97.
25. Hardy J. and Selkoe D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353-356.
26. Hartel R. and Matus A. (1997) Cytoskeletal maturation in cultured hippocampal slices. Neuroscience 78, 1-5.
27. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F. and Cole G. (1996) Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102.
28. Hyman B. T., Elvhage T. E. and Reiter J. (1994) Extracellular signal regulated kinases: localization of protein and mRNA in the human hippocampal formation in Alzheimer's disease. Am. J. Pathol. 144, 565-572.
29. Irizarry M. C., McNamara M., Fedorchak K., Hsiao K. and Hyman B. T. (1997) APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J. Neuropathol. Exp. Neurol. 56, 965-973.
30. Jang J. H. and Surh Y. J. (2002) beta-Amyloid induces oxidative DNA damage and cell death through activation of c-Jun N terminal kinase. Ann. N Y Acad. Sci. 973, 228-236.
31. Kawarabayashi T., Younkin L. H., Saido T. C., Shoji M., Ashe K. H. and Younkin S. G. (2001) Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J. Neurosci. 21, 372-381.
32. Kihara T., Shimohama S., Sawada H., Honda K., Nakamizo T., Shibasaki H., Kume T. and Akaike A. (2001) Alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloid-induced neurotoxicity. J. Biol. Chem. 276, 13541-13546.
33. Kirn S., Jee K., Kim D., Koh H. and Chung J. (2001) Cyclic AMP inhibits Akt activity by blocking the membrane localization of PDK1. J. Biol. Chem. 276, 12864-12870.
34. Lambert M. P., Barlow A. K., Chromy B. A. et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95, 6448-6453.
35. Lambert M. P., Viola K. L., Chromy B. A., Chang L., Morgan T. E., Yu J., Venton D. L., Krafft G. A., Finch C. E. and Klein W. L. (2001) Vaccination with soluble Abeta oligomers generates toxicity-neutralizing antibodies. J. Neurochem. 79, 595-605.
36. Lue L. F., Kuo Y. M., Roher A. E., Brachova L., Shen Y., Sue L., Beach T., Kurth J. H., Rydel R. E. and Rogers J. (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am. J. Pathol. 155, 853-862.
37. Luth H. J., Apelt J., Ihunwo A. O., Arendt T. and Schliebs R. (2003) Degeneration of beta-amyloid-associated cholinergic structures in transgenic APP SW mice. Brain Res. 977, 16-22.
38. McLean C. A., Cherny R. A., Fraser F. W., Fuller S. J., Smith M. J., Beyreuther K., Bush A. I. and Masters C. L. (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neural. 46, 860-866.
39. Morishima Y., Gotoh Y., Zieg J., Barrett T., Takano H., Flavell R., Davis R. J., Shirasaki Y. and Greenberg M. E. (2001) beta-Amyloid induces neuronal apoptosis via a mechanism that involves the c-Jun N-terminal kinase pathway and the induction of Fas ligand. J. Neurosci. 21, 7551-7560.
40. Naslund J., Haroutunian V., Mohs R., Davis K. L., Davies P., Greengard P. and Buxbaum J. D. (2000) Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 283, 1571-1577.
41. Okano J., Gaslightwala I., Birnbaum M. J., Rustgi A. K. and Nakagawa H. (2000) Akt/protein kinase B isoforms are differentially regulated by epidermal growth factor stimulation. J. Biol. Chem. 275, 30934-30942.
42. Pearlson G. D., Harris G. J., Powers R. E., Barta P. E., Camargo E. E., Chase G. A., Noga J. T. and Tune L. E. (1992) Quantitative changes in mesial temporal volume, regional cerebral blood flow, and cognition in Alzheimer's disease. Arch. Gen. Psychiatry 49, 402-408.
43. Perry E. K., Tomlinson B. E., Blessed G., Bergmann K., Gibson P. H. and Perry R. H. (1978) Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br. Med. J. 2, 1457-1459.
44. Petersen R. C., Jack C. R. Jr, Xu Y. C., Waring S. C., O'Brien P. C., Smith G. E., Ivnik R. J., Tangalos E. G., Boeve B. F. and Kokmen E. (2000) Memory and MRI-based hippocampal volumes in aging and AD. Neurology 54, 581-587.
45. Picciotto M. R., Zoli M., Lena C., Bessis A., Lallemand Y., LeNovere N., Vincent P., Pich E. M., Brulet P. and Changeux J. P. (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374, 65-67.
46. Rameh L. E., Rhee S. G., Spokes K., Kazlauskas A., Cantley L. C. and Cantley L. G. (1998) Phosphoinositide 3-kinase regulates phospholipase Cgamma-mediated calcium signaling. J. Biol. Chem. 273, 23750-23757.
47. Ramstad C., Sundvold V., Johansen H. K. and Lea T. (2000) cAMP-dependent protein kinase (PKA) inhibits T cell activation by phosphorylating ser-43 of raf-1 in the MAPK/ERK pathway. Cell Signal. 12, 557-563.
48. Rogers S. W., Gregori N. Z., Carlson N., Gahring L. C. and Noble M. (2001) Neuronal nicotinic acetylcholine receptor expression by O2A/oligodendrocyte progenitor cells. Glia 33, 306-313.
49. Runden E., Seglen P. O., Haug F. M., Ottersen O. P., Wieloch T., Shamloo M. and Laake J. H. (1998) Regional selective neuronal degeneration after protein phosphatase inhibition in hippocampal slice cultures: evidence for a MAP kinase-dependent mechanism. J. Neurosci. 18, 7296-7305.
50. Scheid M. P., Marignani P. A. and Woodgett J. R. (2002) Multiple phosphoinositide 3-kinase-dependent steps in activation of protein kinase B. Mol. Cell Biol. 22, 6247-6260.
51. Selcher J. C., Nekrasova T., Paylor R., Landreth G. E. and Sweatt J. D. (2001) Mice lacking the ERK1 isoform of MAP kinase are unimpaired in emotional learning. Learn. Mem. 8, 11-19.
52. Selcher J. C., Weeber E. J., Christian J., Nekrasova T., Landreth G. E. and Sweatt J. D. (2003) A role for ERK MAP kinase in physiologic temporal integration in hippocampal area CA1. Learn. Mem. 10, 26-39.
53. Selkoe D. J. (2002) Alzheimer's disease is a synaptic failure. Science 298, 789-791.
54. Shaw S., Bencherif M. and Marrero M. B. (2002) Janus kinase 2, an early target of alpha 7 nicotinic acetylcholine receptor-mediated neuroprotection against Abeta-(1-42) amyloid. J. Biol. Chem. 277, 44920-44924.
55. Shen Y. H., Godlewski J., Zhu J., Sathyanarayana P., Leaner V., Birrer M. J., Rana A. and Tzivion G. (2003) Cross-talk between JNK/SAPK and ERK/MAPK pathways: sustained activation of JNK blocks ERK activation by mitogenic factors. J. Biol. Chem. 278, 26715-26721.
56. Shimohama S. and Kihara T. (2001) Nicotinic receptor-mediated protection against beta-amyloid neurotoxicity. Biol. Psychiatry 49, 233-239.
57. Shytle R. D., Mori T., Townsend K., Vendrame M., Sun N., Zeng J., Ehrhart J., Silver A. A., Sanberg P. R. and Tan J. (2004) Cholinergic modulation of microglial activation by alpha 7 nicotinic receptors. J. Neurochem. 89, 337-343.
58. Stanciu M. and DeFranco D. B. (2002) Prolonged nuclear retention of activated extracellular signal-regulated protein kinase promotes cell death generated by oxidative toxicity or proteasome inhibition in a neuronal cell line. J. Biol. Chem. 277, 4010-4017.
59. Stanciu M., Wang Y., Kentor R. et al. (2000) Persistent activation of ERK contributes to glutamate-induced oxidative toxicity in a neuronal cell line and primary cortical neuron cultures. J. Biol. Chem. 275, 12200-12206.
60. Stoppini L., Buchs P. A. and Muller D. (1991) A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182.
61. Sutton G. and Chandler L. J. (2002) Activity-dependent NMDA receptor-mediated activation of protein kinase B/Akt in cortical neuronal cultures. J. Neurochem. 82, 1097-1105.
62. Trojanowski J. Q., Mawal-Dewan M., Schmidt M. L., Martin J. and Lee V. M. (1993) Localization of the mitogen activated protein kinase ERK2 in Alzheimer's disease neurofibrillary tangles and senile plaque neurites. Brain Res. 618, 333-337.
63. Troy C. M., Rabacchi S. A., Xu Z., Maroney A. C., Connors T. J., Shelanski M. L. and Greene L. A. (2001) beta-Amyloid-induced neuronal apoptosis requires c-Jun N-terminal kinase activation. J. Neurochem. 77, 157-164.
64. Vlahos C. J., Matter W. F., Hui K. Y. and Brown R. F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1- benzopyran-4-one(LY294002). J. Biol. Chem. 269, 5241-5248.
65. Walsh D. M., Klyubin I., Fadeeva J. V., Cullen W. K., Anwyl R., Wolfe M. S., Rowan M. J. and Selkoe D. J. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539.
66. Wang J., Dickson D. W., Trojanowski J. Q. and Lee V. M. (1999) The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp. Neurol. 158, 328-337.
67. Wang H. Y., Lee D. H., D'Andrea M. R., Peterson P. A., Shank R. P. and Reitz A. B. (2000) beta-Amyloid (1-42) binds to alpha? nicotinic acetylcholine receptor with high affinity: implications for Alzheimer's disease pathology. J. Biol. Chem. 275, 5626-5632.
68. Wei W., Norton D. D., Wang X. and Kusiak J. W. (2002) A beta 17-42 in Alzheimer's disease activates JNK and caspase-8 leading to neuronal apoptosis. Brain 125, 2036-2043.
69. Wick M. J., Wick K. R., Chen H., He H., Dong L. Q., Quon M. J. and Liu F. (2002) Substitution of the autophosphorylation site Thr516 with a negatively charged residue confers constitutive activity to mouse 3-phosphoinositide- dependent protein kinase-1 in cells. J. Biol. Chem. 277, 16632-16638.
70. Williamson R., Scales T., Clark B. R. et al. (2002) Rapid tyrosine phosphorylation of neuronal proteins including tau and focal adhesion kinase in response to amyloid-beta peptide exposure: involvement of Src family protein kinases. J. Neurosci. 22, 10-20.
71. Xing J., Ginty D. D. and Greenberg M. E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963.
72. Zanardi A., Leo G., Biagini G. and Zoli M. (2002) Nicotine and neurodegeneration in ageing. Toxicol. Lett. 127, 207-215.
73. Zhao W. Q., Ravindranath L., Mohamed A. S., Zohar O., Chen G. H., Lyketsos C. G., Etcheberrigaray R. and Alkon D. L. (2002) MAP kinase signaling cascade dysfunction specific to Alzheimer's disease in fibroblasts. Neurobiol. Dis. 11, 166-183.
74. Zhu X., Lee H. G., Raina A. K., Perry G. and Smith M. A. (2002) The role of mitogen-activated protein kinase pathways in Alzheimer's disease. Neurosignals 11, 270-281.
75. Zoli M., Lena C., Picciotto M. R. and Changeux J. P. (1998) Identification of four classes of brain nicotinic receptors using beta2 mutant mice. J. Neurosci. 18, 4461-4472.