Inverse and distinct modulation of tau-dependent neurodegeneration by presenilin 1 and amyloid-β in cultured cortical neurons: Evidence that tau phosphorylation is the limiting factor in amyloid-β-induced cell death

Journal of Neurochemistry

Volumn 101, Issue 5, 2007, Pages 1303-1315

  Leschik, Julia ^a   Welzel, Alfred ^a   Weissmann, Carina ^a   Eckert, Anne ^b   Brandt, Roland ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Alzheimer's disease; Amyloid precursor protein A ; Herpes simplex virus; Presenilin; Tau; Transgenic cortical cultures

Indexed keywords

AMYLOID BETA PROTEIN; PRESENILIN 1; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DEATH; CONTROLLED STUDY; CYTOCHEMISTRY; EMBRYO; FLUORESCENCE; GENE TRANSFER; HERPES SIMPLEX VIRUS 1; MOUSE; NERVE CELL; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PERIKARYON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSGENICS;

AMYLOID BETA-PROTEIN; ANIMALS; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; EMBRYO; GREEN FLUORESCENT PROTEINS; HUMANS; INDOLES; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NERVE DEGENERATION; NEURONS; PHOSPHORYLATION; PRESENILIN-1; SIMPLEXVIRUS; TAU PROTEINS; TRANSFECTION;

HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 34248222732     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04435.x     Document Type: Article

References (56)

1. Araki W., Yuasa K., Takeda S., Takeda K., Shirotani K., Takahashi K. Tabira T. (2001) Pro-apoptotic effects of presenilin 2 (PS2) overexpression is associated with down-regulation of Bcl-2 in cultured neurons. J. Neurochem. 79, 1161 1168.
2. Baki L., Shioi J., Wen P., Shao Z., Schwarzman A., Gama-Sosa M., Neve R. Robakis N. K. (2004) PS1 activates PI3 K thus inhibiting GSK-3 activity and tau-overphosphorylation: effects of FAD mutations. EMBO J. 23, 2586 2596.
3. Blanchard V., Moussaoui S., Czech C. et al. (2003) Time sequence of maturation of dystrophic neurites associated with Abeta deposits in APP/PS1 transgenic mice. Exp. Neurol. 184, 247 263.
4. Brandt R. Leschik J. (2004) Functional interactions of tau and their relevance for Alzheimer's disease. Curr. Alzheimer Res. 1, 255 269.
5. Brandt R., Leger J. Lee G. (1995) Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J. Cell Biol. 131, 1327 1340.
6. Brandt R., Hundelt M. Shahani N. (2005) Tau alteration and neuronal degeneration in tauopathies: mechanisms and models. Biochim. Biophys. Acta 1739, 331 354.
7. Bursztajn S., De Souza R., Mc Phie D. L., Berman S. A., Shioi J., Robakis N. K. Neve R. L. (1998) Overexpression in neurons of human presenilin 1 or presenilin 1 familial Alzheimer disease mutant does not enhance apoptosis. J. Neurosci. 18, 9790 9799.
8. Busciglio J., Lorenzo A., Yeh J. Yankner B. A. (1995) Beta-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14, 879 888.
9. Calhoun M. E., Wiederhold K. H., Abramowski D., Phinney A. L., Probst A., Sturchler-Pierrat C., Staufenbiel M., Sommer B. Jucker M. (1998) Neuron loss in APP transgenic mice. Nature 395, 755 756.
10. Chui D. H., Tanahashi H., Ozawa K. et al. (1999) Transgenic mice with Alzheimer presenilin 1 mutations show accelerated neurodegeneration without amyloid plaque formation. Nat. Med. 5, 560 564.
11. Citron M., Westaway D., Xia W., Carlson G., Diehl T., Levesque G. Selkoe D. E. A. (1997) Mutant presenilins of Alzheimer's disease increase the production of 42-residue amyloid beta-protein in both transfected cells and transgenic mice. Nat. Med. 3, 67 72.
12. Czech C., Delaere P., Macq A. F. et al. (1997) Proteolytic processing of mutated human amyloid precursor protein in transgenic mice. Brain Res. Mol. Brain Res. 47, 108 116.
13. Czech C., Lesort M., Tremp G. et al. (1998) Characterization of human presenilin 1 transgenic rats: increased sensitivity to apoptosis in primary neuronal cultures. J. Neurosci. 87, 325 336.
14. Dickson D. W., Yen S. H., Suzuki K. I., Davies P., Garcia J. H. Hirano A. (1986) Ballooned neurons in select neurodegenerative diseases contain phosphorylated neurofilament epitopes. Acta Neuropathol. (Berl.) 71, 216 223.
15. Echeverria V., Ducatenzeiler A., Dowd E. et al. (2004) Altered mitogen-activated protein kinase signaling, tau hyperphosphorylation and mild spatial learning dysfunction in transgenic rats expressing the beta-amyloid peptide intracellularly in hippocampal and cortical neurons. J. Neurosci. 129, 583 592.
16. Eckmann C. B., Mehta N. D., Crook R. et al. (1997) A new pathogenic mutation in the APP gene (I716 V) increass the relative proportion of Aβ42(43). Hum. Mol. Gen. 5, 2087 2089.
17. Eidenmuller J., Fath T., Hellwig A., Reed J., Sontag E. Brandt R. (2000) Structural and functional implications of tau hyperphosphorylation: information from phosphorylation-mimicking mutated tau proteins. Biochemistry 39, 13 166 13 175.
18. Eidenmuller J., Fath T., Maas T., Pool M., Sontag E. Brandt R. (2001) Phosphorylation-mimicking glutamate clusters in the proline-rich region are sufficient to simulate the functional deficiencies of hyperphosphorylated tau protein. Biochem. J. 357, 759 767.
19. Estus S., Tucker H. M., Van Rooyen C., Wright S., Brigham E. F., Wogulis M. Rydel R. E. (1997) Aggregated amyloid-beta protein induces cortical neuronal apoptosis and concomitant 'apoptotic' pattern of gene induction. J. Neurosci. 17, 7736 7745.
20. Fath T., Eidenmuller J. Brandt R. (2002) Tau-mediated cytotoxicity in a pseudohyperphosphorylation model of Alzheimer's disease. J. Neurosci. 22, 9733 9741.
21. Fujino Y., Delucia M. W., Davies P. Dickson D. W. (2004) Ballooned neurones in the limbic lobe are associated with Alzheimer type pathology and lack diagnostic specificity. Neuropathol. Appl. Neurobiol. 30, 676 682.
22. Gervais F. G., Xu D., Robertson G. S. et al. (1999) Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell 97, 395 406.
23. Gleckman A. M., Jiang Z., Liu Y. Smith T. W. (1999) Neuronal and glial DNA fragmentation in Pick's disease. Acta Neuropathol. (Berl.) 98, 55 61.
24. Gong C. X., Singh T. J., Grundke-Iqbal I. Grundke-Iqbal K. (1993) Phosphoprotein phosphatase activities in Alzheimer disease brain. J. Neurochem. 61, 921 927.
25. Greenberg S. M., Qiu W. Q., Selkoe D. J., Ben-Itzhak A. Kosik K. S. (1995) Aminoterminal region of beta-amyloid precursor protein activates mitogen-activated protein kinase. Neurosci. Lett. 198, 52 56.
26. Hass M. R. Yankner B. (2005) A γ-secretase-independent mechanism of signal transduction by the amyloid precursor protein. J. Biol. Chem. 280, 36 895 36 904.
27. Hoshi M., Takashima A., Noguchi K., Murayama M., Sato K., Kondo S., Saitoh Y., Ishiguro K., Hoshino T. Imahori K. (1996) Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain. Proc. Natl Acad. Sci. U S A 93, 2719 2723.
28. Jicha G. A., Weaver C., Lane E., Vianna C., Kress Y., Rockwood J. Davies P. (1999) CAMP-dependent protein kinase phosphorylations on tau in Alzheimer's disease. J. Neurosci. 19, 7486 7494.
29. Kennessey A. A. Yen S. H. (1993) The extent of phosphorylation of fetal tau is comparable to that of PHF-tau from Alzheimer paired helical filaments. Brain Res. 629, 40 46.
30. Kidd M. (1963) Paired helical filaments in electron microscopy of Alzheimer's disease. Nature 197, 192 193.
31. Kim D. Y., MacKenzie L. A., Care B. W., Pettingell W. H. Kovacs D. M. (2005) Presenilin/γ-secretase-mediated cleavage of the voltage-gated sodium channel β2-subunit regulates cell adhesion and migration. J. Biol. Chem. 280, 23 251 23 261.
32. La Ferla F. M., Tinkle B. T., Bieberich C. J., Haudenschild C. C. Jay G. (1995) The Alzheimer's Aβ peptide induces neurodegeneration and apoptotic cell death in transgenic mice. Nat. Genet. 9, 21 29.
33. Lassmann H., Bancher C., Breitschopf H., Wegiel J., Bobinski M., Jellinger K. Wisniewski H. M. (1995) Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol. (Berl.) 89, 35 41.
34. Leutner S., Czech C., Schindowski K., Touchet N., Eckert A. Müller A. W. (2000) Reduced antioxidant enzyme activity in brains of mice transgenic for human presenilin-1 with single or multiple mutations. Neurosci. Lett. 292, 87 90.
35. Mattson M. P. (2004) Pathways towards and away from Alzheimer's disease. Nature 430, 631 639.
36. McPhie D. L., Golde T., Eckmann C. B., Yager D., Brant J. B. Neve R. L. (2001) Beta-secretase cleavage of the amyloid precursor protein mediates neuronal apoptosis caused by familial Alzheimer's disease mutations. Brain Res. Mol. Brain Res. 97, 103 113.
37. Neve R. L., Neve K. A., Nestler E. J. Carlezon W. A. Jr. (2005) Use of herpes virus amplicon vectors to study brain disorders. Biotechniques 39, 381 391.
38. Otth C., Concha I. I., Arendt T., Stieler J., Schliebs R., Gonzalez-Billault C. Maccioni R. B. (2002) A/betaPP induces cdk5-dependent tau hyperphosphorylation in transgenic mice Tg2576. J. Alzheimers Dis. 4, 417 430.
39. Park S. Y. Ferreira A. (2005) The generation of a 17 kDa neurotoxic fragment: an alternative mechanism by which tau mediates bera-amyloid-induced neurodegeneration. J. Neurosci. 25, 5363 5375.
40. Patrick G. N., Zukerberg L., Nicolic M., De la Monte S., Dikkes P. Tsai L. H. (1999) Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 402, 614 622.
41. Piontek J., Chen C. C., Kempf M. Brandt R. (1999) Neurotrophins differentially regulate the survival and morphological complexity of human CNS model neurons. J. Neurochem. 73, 139 146.
42. Rank K. B., Pauley A. M., Bhattacharya K., Wang Z., Evans D. B., Fleck T., Johnston J. A. Sharma S. K. (2002) Direct interaction of soluble human recombinant Abeta 1-42 results in tau aggregation und hyperphosphorylation by tau protein kinase II. FEBS Lett. 514, 263 268.
43. Rapoport M. Ferreira A. (2000) PD98059 prevents neurite degeneration induced by fibrillar beta-amyloid in mature hippocampal neurons. J. Neurochem. 74, 125 133.
44. Rapoport M., Dawson H. N., Binder L. I., Vitek M. P. Ferreira A. (2002) Tau is essentiell for beta-amyloid-induced neurotoxicity. Proc. Natl Acad. Sci. U S A 99, 6364 6369.
45. Shahani N., Subramaniam S., Wolf T., Tackenberg C. Brandt R. (2006) Tau aggregation and progressive neuronal degeneration in the absence of changes in spine density and morphology after targeted expression of Alzheimer's disease-relevant tau constructs in organotypic hippocampal slices. J. Neurosci. 26, 6103 6114.
46. Smale G., Nichols N. R., Brady D. R., Finch C. E. Horton W. E. Jr. (1995) Evidence for apoptotic cell death in Alzheimer's disease. Exp. Neurol. 133, 225 230.
47. Sturchler-Pierrat P. C., Abramowski D., Duke M. et al. (1997) Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl Acad. Sci. U S A 94, 13 287 13 292.
48. Su J. H., Anderson A. J., Cummings B. J. Cotman C. W. (1994) Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5, 2529 2533.
49. Su J. H., Zhao M., Anderson A. J., Srinivasan A. Cotman C. W. (2001) Activated caspase-3 expression in Alzheimer's and aged control brain: correlation with Alzheimer pathology. Brain Res. 898, 350 357.
50. Takashima A., Honda T., Yasutake K., Michel G., Murayama M., Murayama O., Ishiguro K. Yamaguchi H. (1998) Activation of tau protein kinase I/glycogen synthase kinase-3beta by amyloid beta peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci. Res. 31, 317 323.
51. Tanzi R. E. Bertram L. (2005) Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120, 545 555.
52. Terro F., Czech C., Esclaire F., Elyaman W., Yardin C., Baclet M.-C., Touchet N., Tremp G., Pradier L. Hugon J. (2002) Neurons overexpressing mutant presenilin-1 are more sensitive to apoptosis induced by endoplasmic reticulum-golgi stress. J. Neurosci. Res. 69, 530 539.
53. Tomidokoro Y., Ishiguro K., Harigaya Y., Matsubara E., Ikeda M., Park J. M., Yasutake K., Kawarabayashi T., Okamoto K. Shoji M. (2001) Abeta amyloidosis induces the initial stage of tau accumulation in APP(Sw) mice. Neurosci. Lett. 299, 169 172.
54. Troy C. M., Rabacchi S. A., Friedman W. J., Frappier T. F., Brown K. Shelanski M. L. (2000) Caspase-2 mediated neuronal cell death induced by β-amyloid. J. Neurosci. 20, 1386 1392.
55. Wang R., Wang B., He W. Zheng H. (2006) Wild-type presenilin 1 protects against Alzheimer disease mutation-induced amyloid pathology. J. Biol. Chem. 281, 15 330 15 336.
56. Zheng W. H., Bastianetto S., Mennicken F., Ma W. Kar S. (2002) Amyloid beta peptide induces tau phosphorylation and loss of cholinergic neurons in rat primary septal cultures. J. Neurosci. 115, 201 211.