Dictyostelium possesses highly diverged presenilin/γ-secretase that regulates growth and cell-fate specification and can accurately process human APP: A system for functional studies of the presenilin/γ-secretase complex

DMM Disease Models and Mechanisms

Volumn 3, Issue 9-10, 2010, Pages 581-594

  McMains, Vanessa C ^a,b   Myre, Michael ^c   Kreppel, Lisa ^a,d   Kimmel, Alan R ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d MEDIMMUNE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; GAMMA SECRETASE; NOTCH RECEPTOR; PRESENILIN;

ALZHEIMER DISEASE; ARTICLE; CELL FATE; CELL GROWTH; CONTROLLED STUDY; DICTYOSTELIUM; ENZYME ACTIVITY; HUMAN; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; WILD TYPE;

AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; DICTYOSTELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VARIATION; HUMANS; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTATION; PHAGOCYTOSIS; PRESENILINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; SPORES;

DICTYOSTELIUM; EUKARYOTA; MAMMALIA; METAZOA;

EID: 77956533673     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.004457     Document Type: Article

References (66)

1. Berezovska, O., Jack, C., McLean, P., Aster, J. C., Hicks, C., Xia, W., Wolfe, M. S., Kimberly, W. T., Weinmaster, G., Selkoe, D. J. et al. (2000). Aspartate mutations in presenilin and gamma-secretase inhibitors both impair notch1 proteolysis and nuclear translocation with relative preservation of notch1 signaling. J. Neurochem. 75, 583-593. (Pubitemid 30485439)
2. Borchelt, D. R., Thinakaran, G., Eckman, C. B., Lee, M. K., Davenport, F., Ratovitsky, T., Prada, C. M., Kim, G., Seekins, S., Yager, D. et al. (1996). Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo. Neuron 17, 1005-1013.
3. Brodskii, L. I., Ivanov, V. V., Kalaidzidis Ia, L., Leontovich, A. M., Nikolaev, V. K., Feranchuk, S. I. and Drachev, V. A. (1995). GeneBee-NET: An Internet based server for biopolymer structure analysis. Biokhimiia 60, 1221-1230.
4. Cao, X. and Sudhof, T. C. (2001). A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293, 115-120.
5. Carmine-Simmen, K., Proctor, T., Tschape, J., Poeck, B., Triphan, T., Strauss, R. and Kretzschmar, D. (2009). Neurotoxic effects induced by the Drosophila amyloid-beta peptide suggest a conserved toxic function. Neurobiol. Dis. 33, 274-281.
6. Chen, G., Zhuchenko, O. and Kuspa, A. (2007). Immune-like phagocyte activity in the social amoeba. Science 317, 678-681. (Pubitemid 47229969)
7. Chumakov, K. M. and Iushmanov, S. V. (1988). A principle of maximum topological similarity in molecular systematics. Mol. Gen. Mikrobiol. Virusol. 3, 3-9.
8. De Strooper, B., Saftig, P., Craessaerts, K., Vanderstichele, H., Guhde, G., Annaert, W., Von Figura, K. and Van Leuven, F. (1998). Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387-390.
9. De Strooper, B., Annaert, W., Cupers, P., Saftig, P., Craessaerts, K., Mumm, J. S., Schroeter, E. H., Schrijvers, V., Wolfe, M. S., Ray, W. J. et al. (1999). A presenilin-1- dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398, 518-522.
10. Donoviel, D. B., Hadjantonakis, A. K., Ikeda, M., Zheng, H., Hyslop, P. S. and Bernstein, A. (1999). Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes Dev. 13, 2801-2810.
11. Dries, D. R. and Yu, G. (2008). Assembly, maturation, and trafficking of the gamma-secretase complex in Alzheimer's disease. Curr. Alzheimer Res. 5, 132-146.
12. Edbauer, D., Winkler, E., Regula, J. T., Pesold, B., Steiner, H. and Haass, C. (2003). Reconstitution of gamma-secretase activity. Nat. Cell Biol. 5, 486-488.
13. Faix, J., Kreppel, L., Shaulsky, G., Schleicher, M. and Kimmel, A. R. (2004). A rapid and efficient method to generate multiple gene disruptions in Dictyostelium discoideum using a single selectable marker and the Cre-loxP system. Nucleic Acids Res. 32, e143.
14. Francis, R., McGrath, G., Zhang, J., Ruddy, D. A., Sym, M., Apfeld, J., Nicoll, M., Maxwell, M., Hai, B., Ellis, M. C. et al. (2002). aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev. Cell 3, 85-97.
15. Futai, E., Yagishita, S. and Ishiura, S. (2009). Nicastrin is dispensable for gamma-secretase protease activity in the presence of specific presenilin mutations. J. Biol. Chem. 284, 13013-13022.
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. USA 98, 14979-14984.
17. Hutton, M. and Hardy, J. (1997). The presenilins and Alzheimer's disease. Hum. Mol. Genet. 6, 1639-1646.
18. Iushmanov, S. V. and Chumakov, K. M. (1988). Algorithms for constructing phylogenetic trees of maximum topological similarity. Mol. Gen. Mikrobiol. Virusol. 3, 9-15.
19. Jutras, I., Laplante, A., Boulais, J., Brunet, S., Thinakaran, G. and Desjardins, M. (2005). Gamma-secretase is a functional component of phagosomes. J. Biol. Chem. 280, 36310-36317.
20. Kang, D. E., Soriano, S., Xia, X., Eberhart, C. G., De Strooper, B., Zheng, H. and Koo, E. H. (2002). Presenilin couples the paired phosphorylation of beta-catenin independent of axin: implications for beta-catenin activation in tumorigenesis. Cell 110, 751-762.
21. Kay, R. R. (1987). Cell differentiation in monolayers and the investigation of slime mold morphogens. Methods Cell Biol. 28, 433-448.
22. Khandelwal, A., Chandu, D., Roe, C. M., Kopan, R. and Quatrano, R. S. (2007). Moonlighting activity of presenilin in plants is independent of gamma-secretase and evolutionarily conserved. Proc. Natl. Acad. Sci. USA 104, 13337-13342. (Pubitemid 47293946)
23. Khurana, T., Brzostowski, J. A. and Kimmel, A. R. (2005). A Rab21/LIM-only/CH-LIM complex regulates phagocytosis via both activating and inhibitory mechanisms. EMBO J. 24, 2254-2264.
24. Kim, D. Y., Ingano, L. A., Carey, B. W., Pettingell, W. H. and Kovacs, D. M. (2005). Presenilin/gamma-secretase-mediated cleavage of the voltage-gated sodium channel beta2-subunit regulates cell adhesion and migration. J. Biol. Chem. 280, 23251-23261.
25. Kim, L., Liu, J. and Kimmel, A. R. (1999). The novel tyrosine kinase ZAK1 activates GSK3 to direct cell fate specification. Cell 99, 399-408.
26. Kim, L., Harwood, A. and Kimmel, A. R. (2002). Receptor-dependent and tyrosine phosphatase-mediated inhibition of GSK3 regulates cell fate choice. Dev. Cell 3, 523-532.
27. Kim, S. D. and Kim, J. (2008). Sequence analyses of presenilin mutations linked to familial Alzheimer's disease. Cell Stress Chaperones 13, 401-412.
28. Kimberly, W. T., Xia, W., Rahmati, T., Wolfe, M. S. and Selkoe, D. J. (2000). The transmembrane aspartates in presenilin 1 and 2 are obligatory for gamma-secretase activity and amyloid beta-protein generation. J. Biol. Chem. 275, 3173-3178. (Pubitemid 30083016)
29. 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.
30. Kimmel, A. R. and Firtel, R. A. (2004). Breaking symmetries: regulation of Dictyostelium development through chemoattractant and morphogen signal-response. Curr. Opin. Genet. Dev. 14, 540-549.
31. Kopan, R. and Ilagan, M. X. (2004). Gamma-secretase: proteasome of the membrane? Nat. Rev. Mol. Cell Biol. 5, 499-504.
32. Kubohara, Y., Arai, A., Gokan, N. and Hosaka, K. (2007). Pharmacological evidence that stalk cell differentiation involves increases in the intracellular Ca(2+) and H(+) concentrations in Dictyostelium discoideum. Dev. Growth Differ. 49, 253-264. (Pubitemid 46452385)
33. Lammich, S., Okochi, M., Takeda, M., Kaether, C., Capell, A., Zimmer, A. K., Edbauer, D., Walter, J., Steiner, H. and Haass, C. (2002). Presenilin-dependent intramembrane proteolysis of CD44 leads to the liberation of its intracellular domain and the secretion of an Abeta-like peptide. J. Biol. Chem. 277, 44754-44759. (Pubitemid 36159067)
34. Leemans, J. C., Florquin, S., Heikens, M., Pals, S. T., van der Neut, R. and Van Der Poll, T. (2003). CD44 is a macrophage binding site for Mycobacterium tuberculosis that mediates macrophage recruitment and protective immunity against tuberculosis. J. Clin. Invest. 111, 681-689. (Pubitemid 36278586)
35. Levi, S., Polyakov, M. and Egelhoff, T. T. (2000). Green fluorescent protein and epitope tag fusion vectors for Dictyostelium discoideum. Plasmid 44, 231-238.
36. Lillis, A. P., Greenlee, M. C., Mikhailenko, I., Pizzo, S. V., Tenner, A. J., Strickland, D. K. and Bohlson, S. S. (2008). Murine low-density lipoprotein receptor-related protein 1 (LRP) is required for phagocytosis of targets bearing LRP ligands but is not required for C1q-triggered enhancement of phagocytosis. J. Immunol. 181, 364-373.
37. McLendon, C., Xin, T., Ziani-Cherif, C., Murphy, M. P., Findlay, K. A., Lewis, P. A., Pinnix, I., Sambamurti, K., Wang, R., Fauq, A. et al. (2000). Cell-free assays for gamma-secretase activity. FASEB J. 14, 2383-2386.
38. McMains, V. C., Liao, X. H. and Kimmel, A. R. (2008). Oscillatory signaling and network responses during the development of Dictyostelium discoideum. Ageing Res. Rev. 7, 234-248.
39. McPhie, D. L., Lee, R. K., Eckman, C. B., Olstein, D. H., Durham, S. P., Yager, D., Younkin, S. G., Wurtman, R. J. and Neve, R. L. (1997). Neuronal expression of beta-amyloid precursor protein Alzheimer mutations causes intracellular accumulation of a C-terminal fragment containing both the amyloid beta and cytoplasmic domains. J. Biol. Chem. 272, 24743-24746.
40. Morohashi, Y., Kan, T., Tominari, Y., Fuwa, H., Okamura, Y., Watanabe, N., Sato, C., Natsugari, H., Fukuyama, T., Iwatsubo, T. et al. (2006). C-terminal fragment of presenilin is the molecular target of a dipeptidic gamma-secretase-specific inhibitor DAPT (N-[N-(3,5-difluorophenacetyl)-L-alanyl] -S-phenylglycine t-butyl ester). J. Biol. Chem. 281, 14670-14676.
41. Oster-Granite, M. L., McPhie, D. L., Greenan, J. and Neve, R. L. (1996). Age-dependent neuronal and synaptic degeneration in mice transgenic for the C terminus of the amyloid precursor protein. J. Neurosci. 16, 6732-6741.
42. Patel, M., Morrow, J., Maxfield, F. R., Strickland, D. K., Greenberg, S. and Tabas, I. (2003). The cytoplasmic domain of the low density lipoprotein (LDL) receptor-related protein, but not that of the LDL receptor, triggers phagocytosis. J. Biol. Chem. 278, 44799-44807. (Pubitemid 37377238)
43. Plyte, S. E., O'Donovan, E., Woodgett, J. R. and Harwood, A. J. (1999). Glycogen synthase kinase-3 (GSK-3) is regulated during Dictyostelium development via the serpentine receptor cAR3. Development 126, 325-333. (Pubitemid 29083970)
44. Prager, K., Wang-Eckhardt, L., Fluhrer, R., Killick, R., Barth, E., Hampel, H., Haass, C., Walter, J., Parisiadou, L., Fassa, A. et al. (2007). A structural switch of presenilin 1 by glycogen synthase kinase 3beta-mediated phosphorylation regulates the interaction with beta-catenin and its nuclear signaling. J. Biol. Chem. 282, 14083-14093. (Pubitemid 47100423)
45. Richardson, D. L., Loomis, W. F. and Kimmel, A. R. (1994). Progression of an inductive signal activates sporulation in Dictyostelium discoideum. Development 120, 2891-2900.
46. Selkoe, D. J. (1998). The cell biology of beta-amyloid precursor protein and presenilin in Alzheimer's disease. Trends Cell. Biol. 8, 447-453.
47. Selkoe, D. J. and Wolfe, M. S. (2007). Presenilin: running with scissors in the membrane. Cell 131, 215-221.
48. Sherrington, R., Rogaev, E. I., Liang, Y., Rogaeva, E. A., Levesque, G., Ikeda, M., Chi, H., Lin, C., Li, G., Holman, K. et al. (1995). Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375, 754-760.
49. Steiner, H., Fluhrer, R. and Haass, C. (2008). Intramembrane proteolysis by gamma-secretase. J. Biol. Chem. 283, 29627-29631.
50. Suzuki, T. and Nakaya, T. (2008). Regulation of amyloid beta-protein precursor by phosphorylation and protein interactions. J. Biol. Chem. 283, 29633-29637.
51. Takasugi, N., Takahashi, Y., Morohashi, Y., Tomita, T. and Iwatsubo, T. (2002). The mechanism of gamma-secretase activities through high molecular weight complex formation of presenilins is conserved in Drosophila melanogaster and mammals. J. Biol. Chem. 277, 50198-50205. (Pubitemid 36014475)
52. Tesco, G. and Tanzi, R. E. (2000). GSK3 beta forms a tetrameric complex with endogenous PS1-CTF/NTF and beta-catenin. Effects of the D257/D385A and FAD-linked mutations. Ann. NY Acad. Sci. 920, 227-232.
53. Tien, A. C., Rajan, A. and Bellen, H. J. (2009). A Notch updated. J. Cell Biol. 184, 621-629.
54. Tu, H., Nelson, O., Bezprozvanny, A., Wang, Z., Lee, S. F., Hao, Y. H., Serneels, L., De Strooper, B., Yu, G. and Bezprozvanny, I. (2006). Presenilins form ER Ca2+ leak channels, a function disrupted by familial Alzheimer's disease-linked mutations. Cell 126, 981-993. (Pubitemid 44310781)
55. Vassar, R., Bennett, B. D., Babu-Khan, S., Kahn, S., Mendiaz, E. A., Denis, P., Teplow, D. B., Ross, S., Amarante, P., Loeloff, R. et al. (1999). Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741.
56. Walsh, D. M. and Selkoe, D. J. (2007). A beta oligomers-a decade of discovery. J. Neurochem. 101, 1172-1184.
57. Wang, R., Sweeney, D., Gandy, S. E. and Sisodia, S. S. (1996). The profile of soluble amyloid beta protein in cultured cell media. Detection and quantification of amyloid beta protein and variants by immunoprecipitation-mass spectrometry. J. Biol. Chem. 271, 31894-31902.
58. Williams, J. G. (2006). Transcriptional regulation of Dictyostelium pattern formation. EMBO Rep. 7, 694-698.
59. Wolfe, M. S. and Kopan, R. (2004). Intramembrane proteolysis: theme and variations. Science 305, 1119-1123.
60. Wolfe, M. S., Xia, W., Ostaszewski, B. L., Diehl, T. S., Kimberly, W. T. and Selkoe, D. J. (1999). Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 398, 513-517. (Pubitemid 129523589)
61. Xia, W. and Wolfe, M. S. (2003). Intramembrane proteolysis by presenilin and presenilin-like proteases. J. Cell Sci. 116, 2839-2844. (Pubitemid 36926973)
62. Yang, T., Arslanova, D., Gu, Y., Augelli-Szafran, C. and Xia, W. (2008). Quantification of gamma-secretase modulation differentiates inhibitor compound selectivity between two substrates Notch and amyloid precursor protein. Mol. Brain 1, 15.
63. Yoo, A. S., Cheng, I., Chung, S., Grenfell, T. Z., Lee, H., Pack-Chung, E., Handler, M., Shen, J., Xia, W., Tesco, G. et al. (2000). Presenilin-mediated modulation of capacitative calcium entry. Neuron 27, 561-572.
64. Yu, G., Nishimura, M., Arawaka, S., Levitan, D., Zhang, L., Tandon, A., Song, Y. Q., Rogaeva, E., Chen, F., Kawarai, T. et al. (2000). Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and betaAPP processing. Nature 407, 48-54.
65. Zhang, M., Haapasalo, A., Kim, D. Y., Ingano, L. A., Pettingell, W. H. and Kovacs, D. M. (2006). Presenilin/gamma-secretase activity regulates protein clearance from the endocytic recycling compartment. FASEB J. 20, 1176-1178.
66. Zhao, G., Cui, M. Z., Mao, G., Dong, Y., Tan, J., Sun, L. and Xu, X. (2005). gamma- Cleavage is dependent on zeta-cleavage during the proteolytic processing of amyloid precursor protein within its transmembrane domain. J. Biol. Chem. 280, 37689-37697. (Pubitemid 41642377)