Modulation of gene expression and cytoskeletal dynamics by the amyloid precursor protein intracellular domain (AICD)

Molecular Biology of the Cell

Volumn 18, Issue 1, 2007, Pages 201-210

  Müller, Thorsten ^a,d   Concannon, Caoimhin G ^b   Ward, Manus W ^b   Walsh, Ciara M ^b   Tirniceriu, Anca L ^a,e   Tribl, Florian ^d   Kögel, Donat ^c   Prehn, Jochen H M ^b   Egensperger, Rupert ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^c UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

^e UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ALPHA ACTIN; ALPHA2 ACTIN; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CYTOSKELETON PROTEIN; PROTEIN; TRANSGELIN; UNCLASSIFIED DRUG;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOID PRECURSOR PROTEIN INTRACELLULAR DOMAIN; ANIMAL CELL; ARTICLE; BRAIN CELL; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; FRONTAL CORTEX; FUNCTIONAL PROTEOMICS; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NERVE CELL CULTURE; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN PROCESSING; UPREGULATION;

ACTINS; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL LINE; CEREBRAL CORTEX; CYTOSKELETON; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; MICE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; PROTEIN STRUCTURE, TERTIARY; TRANSFECTION;

MURINAE;

EID: 33846092979     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-04-0283     Document Type: Article

References (52)

1. Artavanis-Tsakonas, S., Rand, M. D., and Lake, R. J. (1999). Notch signaling: cell fate control and signal integration in development. Science 284, 770-776.
2. Baek, S. H., Ohgi, K. A., Rose, D. W., Koo, E. H., Glass, C. K., and Rosenfeld, M. G. (2002). Exchange of N-CoR corepressor and Tip60 coactivator complexes links gene expression by NF-kappa B and beta-amyloid precursor protein. Cell 110, 55-67.
3. Banati, R. B., Gehrmann, J., Czech, C., Monning, U., Jones, L. L., Konig, G., Beyreuther, K., and Kreutzberg, G. W. (1993). Early and rapid de novo synthesis of Alzheimer beta A4-amyloid precursor protein (APP) in activated microglia. Glia 9, 199-210.
4. Bertrand, E., Brouillet, E., Caille, I., Bouillot, C., Cole, G. M., Prochiantz, A., and Allinquant, B. (2001). A short cytoplasmic domain of the amyloid precursor protein induces apoptosis in vitro and in vivo. Mol. Cell Neurosci. 18, 503-511.
5. Braak, H., and Braak, E. (1991). Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 82, 239-259.
6. Cao, X., and Sudhof, T. C. (2001). A transcriprionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293, 115-120.
7. Cao, X., and Sudhof, T. C. (2004). Dissection of amyloid-beta precursor protein-dependent transcriptional transactivation. J. Biol. Chem. 279, 24601-24611.
8. Chaudhury, A. R., Gerecke, K. M., Wyss, J. M., Morgan, D. G., Gordon, M. N., and Carroll, S. L. (2003). Neuregulin-1 and erbB4 immunoreactivity is associated with neuritic plaques in Alzheimer disease brain and in a transgenic model of Alzheimer disease. J. Neuropathol. Exp. Neurol. 62, 42-54.
9. Ciallella, J. R., Ikonomovic, M. D., Paljug, W. R., Wilbur, Y. I., Dixon, C. E., Kochanek, P. M., Marion, D. W., and DeKosky, S. T. (2002). Changes in expression of amyloid precursor protein and interleukin-1beta after experimental traumatic brain injury in rats. J. Neurotrauma 19, 1555-1567.
10. Cupers, P., Orlans, I., Craessaerts, K., Annaert, W., and De Strooper, B. (2001). The amyloid precursor protein (APP)-cytoplasmic fragment generated by gamma-secretase is rapidly degraded but distributes partially in a nuclear fraction of neurones in culture. J. Neurochem. 78, 1168-1178.
11. Edbauer, D., Willem, M., Lammich, S., and Steiner, H. (2002). Insulin-degrading enzyme rapidly removes the beta-amyloid precursor protein intracellular domain. Neurobiol. Aging 23, S559
12. EI Guendy, N., and Rangnekar, V.M. (2003). Apoptosis by Par-4 in cancer and neurodegenerative diseases. Exp. Cell Res. 283, 51-66.
13. Ermekova, K. S., Zambrano, N., Linn, H., Minopoli, G., Gertler, F., Russo, T., and Sudol, M. (1997). The WW domain of neural protein FE65 interacts with proline-rich motifs in Mena, the mammalian homolog of Drosophila enabled. J. Biol. Chem. 272, 32869-32877.
14. Farris, W., Mansourian, S., Chang, Y., Lindsley, L., Eckman, E. A., Frosch, M. P., Eckman, C. B., Tanzi, R. E., Selkoe, D. J., and Guenette, S. (2003). Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proc. Natl. Acad. Sci. 100, 4162-4167.
15. Galloway, P. G., Mulvihill, P., Siedlak, S., Mijares, M., Kawai, M., Padget, H., Kim, R., and Perry, G. (1990). Immunochemical demonstration of tropomyosin in the neurofibrillary pathology of Alzheimer's disease. Am. J. Pathol. 137, 291-300.
16. Gao, Y., and Pimplikar, S. W. (2001). The gamma-secretase-cleaved C-terminal fragment of amyloid precursor protein mediates signaling to the nucleus. Proc. Natl. Acad. Sci. 98, 14979-14984.
17. Goodman, A., Goode, B. L., Matsudaira, P., and Fink, G. R. (2003). The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton. Mol. Biol. Cell 14, 2617-2629.
18. Guenette, S., Chang, Y., Hiesberger, T., Richardson, J. A., Eckman, C. B., Eckman, E. A., Hammer, R. E., and Herz, J. (2006). Essential roles for the FE65 amyloid precursor protein-interacting proteins in brain development. EMBO J. 25, 420-431.
19. Hartley, D. M., Walsh, D. M., Ye, C. P., Diehl, T., Vasquez, S., Vassilev, P. M., Teplow, D. B., and Selkoe, D. J. (1999). Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci. 19, 8876-8884.
20. Hebert, S. S., Semeels, L., Tolia, A., Craessaerts, K., Derks, C., Filippov, M. A., Muller, U., and Strooper, B. D. (2006). Regulated intramembrane proteolysis of amyloid precursor protein and regulation of expression of putative target genes. EMBO Rep. 7, 739-745.
21. Ikura, T., Ogryzko, V. V., Grigoriev, M., Groisman, R., Wang, J., Horikoshi, M., Scully, R., Qin, J., and Nakatani, Y. (2000). Involvement of the T1P60 histone acerylase complex in DNA repair and apoptosis. Cell 102, 463-473.
22. Kim, H. S., et al. (2003). C-terminal fragments of amyloid precursor protein exert neurotoxicity by inducing glycogen synthase kinase-3beta expression. FASEB J. 17, 1951-1953.
23. Kimberly, W. T., Zheng, J. B., Guenette, S. Y., and Selkoe, D. J. (2001). The intracellular domain of the beta-amyloid precursor protein is stabilized by Fe65 and translocates to the nucleus in a notch-like manner. J. Biol. Chem. 276, 40288-40292.
24. Kinoshita, A., Whelan, C. M., Berezovska, O., and Hyman, B. T. (2002). The gamma secretase-generated carboxyl-terminal domain of the amyloid precursor protein induces apoptosis via Tip60 in H4 cells. J. Biol. Chem. 277, 28530-28536.
25. Leissring, M. A., et al. (2002). A physiologic signaling role for the gamma-secretase-derived intracellular fragment of APP. Proc. Natl. Acad. Sci. USA 99, 4697-4702.
26. Leyssen, M., Ayaz, D., Hebert, S. S., Reeve, S., De Strooper, B., and Hassan, B. A. (2005). Amyloid precursor protein promotes post-developmental neurite arborization in the Drosophila brain. EMBO J. 24, 2944-2955.
27. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
28. Maloney, M. T., Minamide, L. S., Kinley, A. W., Boyle, J. A., and Bamburg, J. R. (2005). beta-Secretase-cleaved amyloid precursor protein accumulates at actin inclusions induced in neurons by stress or amyloid beta: a feedforward mechanism for Alzheimer's disease. J. Neurosci. 25, 11313-11321.
29. Mattson, M. P. (2004). Pathways towards and away from Alzheimer's disease. Nature 430, 631-639.
30. McLoughlin, D. M., and Miller, C. C. (1996). The intracellular cytoplasmic domain of the Alzheimer's disease amyloid precursor protein interacts with phosphotyrosine-binding domain proteins in the yeast two-hybrid system. FEBS Lett. 397, 197-200.
31. Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M., Crain, B. J., Brownlee, L. M., Vogel, F. S., Hughes, J. P., van Belle, G., and Berg, L. (1991). The consortium to establish a registry for Alzheimer's disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486.
32. Munoz, D. G., Wang, D., and Greenberg, B. D. (1993). Hirano bodies accumulate C-terminal sequences of beta-amyloid precursor protein (beta-APP) epitopes. J. Neuropathol. Exp. Neurol. 52, 14-21.
33. Muresan, Z., and Muresan, V. (2004). A phosphorylated, carboxy-terminal fragment of beta-amyloid precursor protein localizes to the splicing factor compartment. Hum. Mol. Genet. 13, 475-488.
34. Nakano, K., Bunai, F., and Numata, O. (2005). Stg 1 is a novel SM22/ transgelin-like actin-modulating protein in fission yeast. FEBS Lett. 579, 6311-6316.
35. Nunan, J., Shearman, M. S., Checler, F., Cappai, R., Evin, G., Beyreuther, K., Masters, C. L., and Small, D. H. (2001). The C-terminal fragment of the Alzheimer's disease amyloid protein precursor is degraded by a proteasome-dependent mechanism distinct from gamma-secretase. Eur. J. Biochem. 268, 5329-5336.
36. Nunan, J., Williamson, N. A., Hill, A. F., Sernee, M. F., Masters, C. L., and Small, D. H. (2003). Proteasome-mediated degradation of the C-terminus of the Alzheimer's disease beta-amyloid protein precursor: effect of C-terminal truncation on production of beta-amyloid protein. J. Neurosci. Res. 74, 378-385.
37. Octave, J. N., Essalmani, R., Tasiaux, B., Menager, J., Czech, C., and Mercken, L. (2000). The role of presenilin-1 in the gamma-secretase cleavage of the amyloid precursor protein of Alzheimer's disease. J. Biol. Chem. 275, 1525-1528.
38. Pardossi-Piquard, R., et al. (2005). Presenilin-dependent transcriptional control of the Abeta-degrading enzyme neprilysin by intracellular domains of betaAPP and APLP. Neuron 46, 541-554.
39. Rensink, A. A., Gellekink, H., Otte-Holler, I., ten Donkelaar, H. J., de Waal, R. M., Verbeek, M. M., and Kremer, B. (2002). Expression of the cytokine leukemia inhibitory factor and pro-apoptotic insulin-like growth factor binding protein-3 in Alzheimer's disease. Acta Neuropathol. 104, 525-533.
40. Ryan, K. A., and Pimplikar, S. W. (2005). Activation of GSK-3 and phosphorylation of CRMP2 in transgenic mice expressing APP intracellular domain. J. Cell Biol. 171, 327-335.
41. Sabo, S. L., Ikin, A. F., Buxbaum, J. D., and Greengard, P. (2003). The amyloid precursor protein and its regulatory protein, FE65, in growth cones and synapses in vitro and in vivo. J. Neurosci. 23, 5407-5415.
42. Sastre, M., Steiner, H., Fuchs, K., Capell, A., Multhaup, G., Condron, M. M., Teplow, D. B., and Haass, C. (2001). Presenilin-dependent gamma-secretase processing of beta-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Rep. 2, 835-841.
43. Selkoe, D. J. (1994). Normal and abnormal biology of the beta-amyloid precursor protein. Annu. Rev. Neurosci. 17, 489-517.
44. Shi, J., Yang, S. H., Stubley, L., Day, A. L., and Simpkins, J. W. (2000). Hypoperfusion induces overexpression of beta-amyloid precursor protein mRNA in a focal ischemic rodent model. Brain Res. 853, 1-4.
45. Stokin, G. B., Lillo, C., Falzone, T. L., Brusch, R. G., Rockenstein, E., Mount, S. L., Raman, R., Davies, P., Masliah, E., Williams, D. S., and Goldstein, L. S. (2005). Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 307, 1282-1288.
46. Terman, J. R., Mao, T., Pasterkamp, R. J., Yu, H. H., and Kolodkin, A. L. (2002). MICALs, a family of conserved flavoprotein oxidoreductases, function in plexin-mediated axonal repulsion. Cell 109, 887-900.
47. Van Gool, D., Carmeliet, G., Triau, E., Cassiman, J. J., and Dom, R. (1994). Appearance of localized immunoreactivity for the alpha 4 integrin subunit and for fibronectin in brains from Alzheimer's, Lewy body dementia patients and aged controls. Neurosci. Lett. 170, 71-73.
48. von Rotz, R. C., Kohli, B. M., Bosset, J., Meier, M., Suzuki, T., Nitsch, R. M., and Konietzko, U. (2004). The APP intracellular domain forms nuclear multiprotein complexes and regulates the transcription of its own precursor. J. Cell Sci. 117, 4435-4448.
49. Walsh, D. M., Fadeeva, J. V., Lavoie, M. J., Paliga, K., Eggert, S., Kimberly, W. T., Wasco, W., and Selkoe, D. J. (2003). gamma-Secretase cleavage and binding to FE65 regulate the nuclear translocation of the intracellular C-terminal domain (ICD) of the APP family of proteins. Biochemistry 42, 6664-6673.
50. Walsh, D. M., Klyubin, I., Shankar, G. M., Townsend, M., Fadeeva, J. V., Betts, V., Podlisny, M. B., Cleary, J. P., Ashe, K. H., Rowan, M. J., and Selkoe, D. J. (2005). The role of cell-derived oligomers of Abeta in Alzheimer's disease and avenues for therapeutic intervention. Biochem. Soc. Trans. 33, 1087-1090.
51. Yu, C., Kim, S. H., Ikeuchi, T., Xu, H., Gasparini, L., Wang, R., and Sisodia, S. S. (2001). Characterization of a presenilin-mediated amyloid precursor protein carboxyl-terminal fragment gamma. Evidence for distinct mechanisms involved in gamma-secretase processing of the APP and Notch1 transmembrane domains. J. Biol. Chem. 276, 43756-43760.
52. Zambrano, N., Minopoli, G., de Candia, P., and Russo, T. (1998). The Fe65 adaptor protein interacts through its PID1 domain with the transcription factor CP2/LSF/LBP1. J. Biol. Chem. 273, 20128-20133.