Developmental control of Presenilin1 expression, endoproteolysis, and interaction in zebrafish embryos

Experimental Cell Research

Volumn 289, Issue 1, 2003, Pages 124-132

  Nornes, Svanhild ^a   Groth, Casper ^a   Camp, Esther ^a   Ey, Peter ^a   Lardelli, Michael ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Alzheimer's disease; Embryo development; Notch; Presenilin; Somitogenesis; Zebrafish

Indexed keywords

PRESENILIN 1; PRESENILIN 2;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE OVEREXPRESSION; KNOCKOUT MOUSE; MOLECULAR GENETICS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; ZEBRA FISH;

DANIO RERIO;

EID: 0042162816     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00257-X     Document Type: Article

References (66)

1. Selkoe D.J., Wolfe M.S. In search of gamma-secretase presenilin at the cutting edge . Proc. Natl. Acad. Sci. USA. 97:2000;5690-5692.
2. Wolfe M.S. Presenilin and gamma-secretase structure meets function . J. Neurochem. 76:2001;1615-1620.
3. Vassar R., Citron M. Abeta-generating enzymes recent advances in beta- and gamma-secretase research . Neuron. 27:2000;419-422.
4. De-Strooper B. Alzheimer's disease closing in on gamma-secretase . Nature. 405:2000;629.
5. Kaether C., Lammich S., Edbauer D., Ertl M., Rietdorf J., Capell A., Steiner H., Haass C. Presenilin-1 affects trafficking and processing of betaAPP and is targeted in a complex with nicastrin to the plasma membrane. J. Cell Biol. 158:2002;551-561.
6. Doan A., Thinakaran G., Borchelt D.R., Slunt H.H., Ratovitsky T., Podlisny M., Selkoe D.J., Seeger M., Gandy S.E., Price D.L., Sisodia S.S. Protein topology of presenilin 1. Neuron. 17:1996;1023-1030.
7. Li X., Greenwald I. Additional evidence for an eight-transmembrane-domain topology for Caenorhabditis elegans and human presenilins. Proc. Natl. Acad. Sci. USA. 95:1998;7109-7114.
8. Kovacs D.-M., Fausett H.-J., Page K.-J., Kim T.-W., Moir R.-D., Merriam D.-E., Hollister R.-D., Hallmark O.-G., Mancini R., Felsenstein K.-M., Hyman B.-T., Tanzi R.-E., Wasco W. Alzheimer-associated presenilins 1 and 2 neuronal expression in brain and localization to intracellular membranes in mammalian cells . Nat. Med. 2:1996;224-229.
9. De-Strooper B., Beullens M., Contreras B., Levesque L., Craessaerts K., Cordell B., Moechars D., Bollen M., Fraser P., George-Hyslop P.-S., Van-Leuven F. Phosphorylation, subcellular localization, and membrane orientation of the Alzheimer's disease-associated presenilins. J. Biol. Chem. 272:1997;3590-3598.
10. Ratovitski T., Slunt H.-H., Thinakaran G., Price D.-L., Sisodia S.-S., Borchelt D.-R. Endoproteolytic processing and stabilization of wild-type and mutant presenilin. J. Biol. Chem. 272:1997;24536-24541.
11. Li J., Xu M., Zhou H., Ma J., Potter H. Alzheimer presenilins in the nuclear membrane, interphase kinetochores, and centrosomes suggest a role in chromosome segregation. Cell. 90:1997;917-927.
12. Ray W.-J., Yao M., Mumm J., Schroeter E.-H., Saftig P., Wolfe M., Selkoe D.-J., Kopan R., Goate A.-M. Cell surface presenilin-1 participates in the gamma-secretase-like proteolysis of Notch. J. Biol. Chem. 274:1999;36801-36807.
13. Schwarzman A.-L., Singh N., Tsiper M., Gregori L., Dranovsky A., Vitek M.-P., Glabe C.-G., St. George-Hyslop P.-H., Goldgaber D. Endogenous presenilin 1 redistributes to the surface of lamellipodia upon adhesion of Jurkat cells to a collagen matrix. Proc. Natl. Acad. Sci. USA. 96:1999;7932-7937.
14. Petanceska S.-S., Seeger M., Checler F., Gandy S. Mutant presenilin 1 increases the levels of Alzheimer amyloid beta-peptide Abeta42 in late compartments of the constitutive secretory pathway. J. Neurochem. 74:2000;1878-1884.
15. Steiner H., Capell A., Pesold B., Citron M., Kloetzel P.-M., Selkoe D.-J., Romig H., Mendla K., Haass C. Expression of Alzheimer's disease-associated presenilin-1 is controlled by proteolytic degradation and complex formation. J. Biol. Chem. 273:1998;32322-32331.
16. Thinakaran G., Harris C.-L., Ratovitski T., Davenport F., Slunt H.-H., Price D.-L., Borchelt D.-R., Sisodia S.-S. Evidence that levels of presenilins (PS1 and PS2) are coordinately regulated by competition for limiting cellular factors. J. Biol. Chem. 272:1997;28415-28422.
17. Saura C.A., Tomita T., Davenport F., Harris C.L., Iwatsubo T., Thinakaran G. Evidence that intramolecular associations between presenilin domains are obligatory for endoproteolytic processing. J. Biol. Chem. 274:1999;13818-13823.
18. Thinakaran G., Regard J.B., Bouton C.M., Harris C.L., Price D.L., Borchelt D.R., Sisodia S.S. Stable association of presenilin derivatives and absence of presenilin interactions with APP. Neurobiol. Dis. 4:1998;438-453.
19. Levitan D., Lee J., Song L., Manning R., Wong G., Parker E., Zhang L. PS1 N- and C-terminal fragments form a complex that functions in APP processing and Notch signaling. Proc. Natl. Acad. Sci. USA. 98:2001;12186-12190.
20. Capell A., Grunberg J., Pesold B., Diehlmann A., Citron M., Nixon R., Beyreuther K., Selkoe D.-J., Haass C. The proteolytic fragments of the Alzheimer's disease-associated presenilin-1 form heterodimers and occur as a 100-150-kDa molecular mass complex. J. Biol. Chem. 273:1998;3205-3211.
21. Yang D.S., Tandon A., Chen F., Yu G., Yu H., Arawaka S., Hasegawa H., Duthie M., Schmidt S.D., Ramabhadran T.V., Nixon R.A., Mathews P.M., Gandy S.E., Mount H.T.J., St. George-Hyslop P., Fraser P.E. Mature glycosylation and trafficking of nicastrin modulate its binding to presenilins. J. Biol. Chem. 277:2002;28135-28142.
22. 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., Goate A., Kopan R. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 398:1999;518-522.
23. Ray W.-J., Yao M., Nowotny P., Mumm J., Zhang W., Wu J.-Y., Kopan R., Goate A.-M. Evidence for a physical interaction between presenilin and Notch. Proc. Natl. Acad. Sci. USA. 96:1999;3263-3268.
24. Greenwald I. LIN-12/Notch signaling lessons from worms and flies . Genes Dev. 12:1998;1751-1762.
25. Baker N.-E. Master regulatory genes; telling them what to do. Bioessays. 23:2001;763-766.
26. Rawls A., Wilson R.J., Olson E.N. Genetic regulation of somite formation. Curr. Top. Dev. Biol. 47:2000;131-154.
27. Conlon R.A., Reaume A.G., Rossant J. Notch1 is required for the coordinate segmentation of somites. Development. 121:1995;1533-1545.
28. de la Pompa J.L., Wakeham A., Correia K.M., Samper E., Brown S., Aguilera R.J., Nakano T., Honjo T., Mak T.W., Rossant J., Conlon R.A. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development. 124:1997;1139-1148.
29. Handler M., Yang X., Shen J. Presenilin-1 regulates neuronal differentiation during neurogenesis. Development. 127:2000;2593-2606.
30. Shen J., Bronson R.T., Chen D.F., Xia W., Selkoe D.J., Tonegawa S. Skeletal and CNS defects in Presenilin-1-deficient mice. Cell. 89:1997;629-639.
31. Wong P.C., Zheng H., Chen H., Becher M.W., Sirinathsinghji D.J., Trumbauer M.E., Chen H.Y., Price D.L., van der Ploeg L.H., Sisodia S.S. Presenilin 1 is required for Notch1 and DII1 expression in the paraxial mesoderm. Nature. 387:1997;288-292.
32. Donoviel D.B., Hadjantonakis A.K., Ikeda M., Zheng H., Hyslop P.S., Bernstein A. Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes Dev. 13:1999;2801-2810.
33. Weinmaster G. Notch signal transduction a real rip and more . Curr. Opin. Genet. Dev. 10:2000;363-369.
34. Huppert S.S., Le A., Schroeter E.H., Mumm J.S., Saxena M.T., Milner L.A., Kopan R. Embryonic lethality in mice homozygous for a processing-deficient allele of Notch1. Nature. 405:2000;966-970.
35. Struhl G., Greenwald I. Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature. 398:1999;522-525.
36. Herreman A., Serneels L., Annaert W., Collen D., Schoonjans L., De-Strooper B. Total inactivation of gamma-secretase activity in presenilin-deficient embryonic stem cells. Nat. Cell. Biol. 2:2000;461-462.
37. Okochi M., Steiner H., Fukumori A., Tanii H., Tomita T., Tanaka T., Iwatsubo T., Kudo T., Takeda M., Haass C. Presenilins mediate a dual intramembranous gamma-secretase cleavage of Notch-1. EMBO J. 21:2002;5408-5416.
38. Capell A., Steiner H., Romig H., Keck S., Baader M., Grim M.-G., Baumeister R., Haass C. Presenilin-1 differentially facilitates endoproteolysis of the beta-amyloid precursor protein and Notch. Nat. Cell Biol. 2:2000;205-211.
39. Zhang Z., Nadeau P., Song W., Donoviel D., Yuan M., Bernstein A., Yankner B.-A. Presenilins are required for gamma-secretase cleavage of beta-APP and transmembrane cleavage of Notch-1. Nat. Cell Biol. 2:2000;463-465.
40. Berezovska O., Jack C., Deng A., Gastineau N., Rebeck G.W., Hyman B.T. Notch1 and amyloid precursor protein are competitive substrates for presenilin1-dependent gamma-secretase cleavage. J. Biol. Chem. 276:2001;30018-30023.
41. J.F. Amatruda, J.L. Shepard, H.M. Stem, L.I. Zon, Zebrafish as a cancer model system, Cancer Cell. 1 (2002) 229-231.
42. Leimer U., Lun K., Romig H., Walter J., Grunberg J., Brand M., Haass C. Zebrafish (Danio rerio) presenilin promotes aberrant amyloid beta-peptide production and requires a critical aspartate residue for its function in amyloidogenesis. Biochemistry. 38:1999;13602-13609.
43. Groth C., Nornes S., McCarty R., Tamme R., Lardelli M. Identification of a second presenilin gene in zebrafish with similarity to the human Alzheimer's disease gene presenilin2. Dev. Genes Evol. 212:2002;486-490.
44. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 203:1995;253-310.
45. Jowett T. Tissue in situ hybridisation. 1997;Wiley, New York.
46. Yamamoto A., Sahara N., Usami M., Okochi M., Kondo T., Kametani F., Tanaka K., Yahagi Y., Shirasawa T., Itoyama Y., Mori H. Abnormal gel-electrophoretic behavior of presenilin 1 and it's fragment. Biochem. Biophys. Res. Commun. 226:1996;536-541.
47. Thinakaran G., Borchelt D.-R., Lee M.-K., Slunt H.-H., Spitzer L., Kim G., Ratovitsky T., Davenport F., Nordstedt C., Seeger M., Hardy J., Levey A.-I., Gandy S.-E., Jenkins N.-A., Copeland N.-G., Price D.-L., Sisodia S.-S. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron. 17:1996;181-190.
48. Dewji N.N., Do C., Singer S.J. On the spurious endoproteolytic processing of the presenilin proteins in cultured cells and tissues. Proc. Natl. Acad. Sci. USA. 94:1997;14031-14036.
49. Mercken M., Takahashi H., Honda T., Sato K., Murayama M., Nakazato Y., Noguchi K., Imahori K., Takashima A. Characterization of human presenilin 1 using N-terminal specific monoclonal antibodies evidence that Alzheimer mutations affect proteolytic processing . FEBS Lett. 389:1996;297-303.
50. Diehlmann A., Ida N., Weggen S., Grunberg J., Haass C., Masters C.L., Bayer T.A., Beyreuther K. Analysis of presenilin 1 and presenilin 2 expression and processing by newly developed monoclonal antibodies. J. Neurosci. Res. 56:1999;405-419.
51. Honda T., Nihonmatsu N., Yasutake K., Ohtake A., Sato K., Tanaka S., Murayama O., Murayama M., Takashima A. Familial Alzheimer's disease-associated mutations block translocation of full-length presenilin 1 to the nuclear envelope. Neurosci. Res. 37:2000;101-111.
52. Takahashi H., Mercken M., Nakazato Y., Noguchi K., Murayama M., Imahori K., Takashima A. Cloning of cDNA and expression of the gene encoding rat presenilin-2. Gene. 197:1997;383-387.
53. Culvenor J.G., Evin G., Cooney M.A., Wardan H., Sharples R.A., Maher F., Reed G., Diehlmann A., Weidemann A., Beyreuther K., Masters C.L. Presenilin 2 expression in neuronal cells induction during differentiation of embryonic carcinoma cells . Exp. Cell Res. 255:2000;192-206.
54. Koizumi K., Nakajima M., Yuasa S., Saga Y., Sakai T., Kuriyama T., Shirasawa T., Koseki H. The role of presenilin 1 during somite segmentation. Development. 128:2001;1391-1402.
55. Nasevicius A., Ekker S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26:2000;216-220.
56. M. Muller, E. v Weizacker, J.A. Campos-Ortega, Expression domains of a zebrafish homologue of the Drosophila pair-rule gene hairy correspond to primordia of alternating somites, Development 122 (1996) 2071-2078.
57. Holley S.A., Julich D., Rauch G.J., Geisler R., Nusslein V.C. her1 and the notch pathway function within the oscillator mechanism that regulates zebrafish somitogenesis. Development. 129:2002;1175-1183.
58. van Eeden F.J., Granato M., Schach U., Brand M., Furutani S.M., Haffter P., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., Kelsh R.N., Mullins M.C., Odenthal J., Warga R.M., Allende M.L., Weinberg E.S., Nusslein-Volhard C. Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development. 123:1996;153-164.
59. M.S. Wolfe, W. Xia, B.L. Ostaszewski, T.S. Diehl, W.T. Kimberly, D.J. Selkoe, Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-seretase activity, Nature 398 (1999) 513-517.
60. M.B. Podlisny, M. Citron, P. Amarante, R. Sherrington, W. Xia, J. Zhang, T. Diehl, G. Levesque, P. Fraser, C. Haass, E.H. Koo, P. Seubert, P. St George-Hyslop, D.B. Teplow, D.J. Selkoe, Presenilin proteins undergo heterogeneous endoproteolysis between Thr291 and Ala299 and occur as stable N- and C-terminal fragments in normal and Alzheimer brain tissue, Neurobiol. Dis. 3 (1997) 325-337.
61. Van G.G., De J.C., Pype S., Van C.W., Julliams A., Vanderhoeven I., Woodrow S., Beyaert R., Huylebroeck D., Van B.C. Alzheimer's disease associated presenilin 1 interacts with HC5 and ZETA, subunits of the catalytic 20S proteasome. Neurobiol. Dis. 6:1999;376-391.
62. Kirschenbaum F., Hsu S.-C., Cordell B., McCarthy J.-V. Glycogen synthase kinase-3beta regulates presenilin 1 C-terminal fragment levels. J. Biol. Chem. 276:2001;30701-30707.
63. Lau K.F., Howlett D.R., Kesavapany S., Standen C.L., Dingwall C., McLoughlin D.M., Miller C.C.J. Cyclin-dependent kinase-5/p35 phosphorylates Presenilin 1 to regulate carboxy-terminal fragment stability. Mol. Cell. Neurosci. 20:2002;13-20.
64. Walter J., Grunberg J., Schindzielorz A., Haass C. Proteolytic fragments of the Alzheimer's disease associated presenilins-1 and -2 are phosphorylated in vivo by distinct cellular mechanisms. Biochemistry. 37:1998;5961-5967.
65. A. Geling, H. Steiner, M. Willem, L. Bally-Cuif, C. Haass, A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish, EMBO Rep. 3 (2002) 688-694.
66. Steiner H., Duff K., Capell A., Romig H., Grim M.G., Lincoln S., Hardy J., Yu X., Picciano M., Fechteler K., Citron M., Kopan R., Pesold B., Keck S., Baader M., Tomita T., Iwatsubo T., Baumeister R., Haass C. A loss of function mutation of presenilin-2 interferes with amyloid beta-peptide production and notch signaling. J. Biol. Chem. 274:1999;28669-28673.