Alzheimer's disease: Correlation of the suppression of β-amyloid peptide secretion from cultured cells with inhibition of the chymotrypsin- like activity of the proteasome

Journal of Neurochemistry

Volumn 73, Issue 1, 1999, Pages 195-204

  Christie, G ^a   Markwell, R E ^a   Gray, C W ^a   Smith, L ^a   Godfrey, F ^a   Mansfield, F ^a   Wadsworth, H ^a   King, R ^a   McLaughlin, M ^a   Cooper, D G ^a   Ward, R V ^a   Howlett, D R ^a   Hartmann, T ^c   Lichtenthaler, S F ^c   Beyreuther, K ^c   Underwood, J ^d   Gribble, S K ^d   Cappai, R ^d   Masters, C L ^d   Tamaoka, A ^e   Gardner, R L ^b   Rivett, A J ^b   Karran, E H ^a   Allsop, D ^a,f   more..

^a GLAXOSMITHKLINE   (United Kingdom)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF TSUKUBA   (Japan)

^f LANCASTER UNIVERSITY   (United Kingdom)

Author keywords

Amyloid peptide; Alzheimer's disease; Amyloid; Inhibitor; Proteasome

Indexed keywords

2 PYRAZINYLCARBONYLPHENYLALANINE BOROLEUCINE; AMYLOID BETA PROTEIN; BORONIC ACID DERIVATIVE; BORONIC ACID INHIBITOR; CHYMOTRYPSIN; PROTEASOME; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL VIABILITY; DRUG MECHANISM; DRUG POTENCY; DRUG PROTEIN BINDING; HUMAN; HUMAN CELL; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN SECRETION; STRUCTURE ANALYSIS;

ALDEHYDES; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; BORONIC ACIDS; CELL LINE; CHYMOTRYPSIN; CYSTEINE ENDOPEPTIDASES; MULTIENZYME COMPLEXES; PEPTIDE FRAGMENTS; PROTEASOME ENDOPEPTIDASE COMPLEX; TRANSFECTION;

EID: 0032999202     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0730195.x     Document Type: Article

References (47)

1. Allsop D., Christie G., Gray C., Holmes S., Markwell R., Owen D., Smith L., Wadsworth H., Ward R. V., Hartmann T., Lichtenthaler S. F., Evin G., Fuller S., Masters C. L., Beyreuther K., and Roberts G. W. (1997) Studies on inhibition of β-amyloid formation in APP751-transfected IMR-32 cells and SPA4CT-transfected SHSY5Y cells, in Alzheimer's Disease: Biology, Diagnostics and Therapeutics (Iqbal K., Winblad B., Nishimura T., Takeda M., and Wisniewski H. M., eds), pp. 717-727. John Wiley, New York.
2. Anderson J. P., Esch F. S., Keim P. S., Sambamurti K., Lieberberg I., and Robakis N. K. (1991) Exact cleavage site of Alzheimer amyloid precursor in neuronal PC-12 cells. Neurosci. Lett. 128, 126-128.
3. Asami-Odaka A., Ishibashi Y., Kikuchi T., Kitada C., and Suzuki N. (1995) Long amyloid β-protein secreted from wild-type human neuroblastoma IMR-32 cells. Biochemistry 34, 10272-10278.
4. Citron M., Diehl T. S., Gordon G., Biere A. L., Seubert P., and Selkoe D. J. (1996) Evidence that the 42- and 40-amino acid forms of amyloid β protein are generated from the β-amyloid precursor protein by different protease activities. Proc. Natl. Acad. Sci. USA 93, 13170-13175.
5. Coutts S. J., Kelly T. A., Snow R. J., Kennedy C. A., Barton R. W., Adams J., Krolikowski D. A., Freeman D. M., Cambell S. J., Ksiazek J. F., and Bachovchin W. W. (1996) Structure-activity relationships of boronic acid inhibitors of dipeptidyl peptidase. IV. Variation of the P2 position Pro is optimum. J. Med. Chem. 39, 2087-2094.
6. Esch F. S., Keim P. S., Beattie E. C., Blacher R. W., Culwell A. R., Olersdorf T., McClure D., and Ward P. I. (1990) Cleavage of amyloid β peptide during constitutive processing of its precursor. Science 248, 1122-1124.
7. Evin G., Cappai R., Li Q. X., Culvenor J. G., Small D. H., Beyreuther K., and Masters C. L. (1995) Candidate γ-secretases in the generation of the carboxyl terminus of the Alzheimer's disease βA4 amyloid: possible involvement of cathepsin D. Biochemistry 34, 14185-14192.
8. Fenteany G., Standaert R. F., Reichard G. A., Corey E. J., and Schreiber S. L. (1994) A β-lactone related to lactacystin induces neurite outgrowth in a neuroblastoma cell line and inhibits cell cycle progression in an osteosarcoma cell line. Proc. Natl. Acad. Sci. USA 91, 3358-3362.
9. Fenteany G., Standaert R. F., Lane W. S., Choi S., Corey E. J., and Schreiber S. L. (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268, 726-731.
10. Glenner G. G. and Wong C. W. (1984) Alzheimer's disease: initial report of the purification and characterisation of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885-890.
11. Hamazaki H. (1998) Carboxy-terminal truncation of long-tailed amyloid β-peptide is inhibited by serine protease inhibitor and peptide aldehyde. FEBS Lett. 424, 136-138.
12. Hardy J. and Allsop D. (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 12, 383-388.
13. Hartmann T., Bieger S. C., Bruhl B., Tienari P. J., Ida N., Allsop D., Roberts G. W., Masters C. L., Dotti C. G., Unsicker K., and Beyreuther K. (1997) Distinct sites of intracellular production for Alzheimer's disease Aβ 40/42 amyloid peptides. Nat. Med. 3, 1016-1020.
14. Henry A., Masters C. L., Beyreuther K., and Cappai R. (1997) Expression of human amyloid precursor protein ectodomains in Pichia pastoris: analysis of culture conditions, purification and characterisation. Protein Expr. Purif. 10, 283-291.
15. Higaki H., Quon D., Zhong Z., and Cordell B. (1995) Inhibition of β-amyloid formation identifies proteolytic precursors and subcellular site of catabolism. Neuron 14, 651-659.
16. Hilt W. and Wolf D. H. (1996) Proteasomes: destruction as a programme. Trends Biochem. Sci. 21, 96-102.
17. Ida N., Hartmann T., Pantel J., Schrode J., Zerfass R., Forstl H., Sandbrink R., Masters C. L., and Beyreuther K. (1996) Analysis of heterogeneous βA4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive western blot assay. J. Biol. Chem. 271, 22908-22914.
18. Ishiura S. (1991) Proteolytic cleavage of the Alzheimer's disease amyloid A4 precursor protein. J. Neurochem. 56, 363-369.
19. Ishiura S., Tsukahara T., Tabira T., and Sugita H. (1989) Putative N-terminal splitting enzyme of amyloid A4 peptides is the multi-catalytic proteinase, ingensin, which is widely distributed in mammalian cells. FEBS Lett. 257, 388-392.
20. Jensen T. J., Loo M. A., Pind S., Williams D. B., Goldberg A. L., and Riordan J. R. (1995) Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83, 129-135.
21. Klafki H., Paganetti P. A., Sommer B., and Staufenbiel M. (1995) Calpain inhibitor I decreases βA4 secretion from human embryonal kidney cells expressing β-amyloid precursor protein carrying the APP670/671 double mutation. Neurosci. Lett. 201, 29-32.
22. Klafki H., Abramowski D., Swoboda R.. Paganetti P. A., and Staufenbiel M. (1996) The carboxyl termini of β-amyloid peptides 1-40 and 1-42 are generated by distinct γ-secretase activities. J. Biol. Chem. 271, 28655-28659.
23. Kojima S. and Omori M. (1992) Two-way cleavage of β-amyloid protein precursor by multicatalytic proteinase. FEBS Lett. 304, 57-60.
24. Ladror U. S., Snyder S. W., Wang G. T., Holzman T. F., and Krafft G. A. (1994) Cleavage at the amino and carboxyl termini of Alzheimer's amyloid-β by cathepsin D. J. Biol. Chem. 269, 18422-18428.
25. Lowe J., Stock D., Jap B., Zwickl P., Baumeister W., and Huber R. (1995) Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 Å resolution. Science 268, 533-539.
26. Marambaud P., Chevallier N., Barelli H., Wilk S., and Checler F. (1997) Proteasome contributes to the α-secretase pathway of amyloid precursor protein in human cells. J. Neurochem. 68, 698-703.
27. Marambaud P., Ancolio K., Lopez-Perez L., and Checler F. (1998) Proteasome inhibitors prevent the degradation of familial Alzheimer's disease-linked presenilin 1 and potentiate Aβ42 recovery from human cells. Mol. Med. 4, 147-157.
28. Mason G. G. F., Hendil K. B., and Rivett A. J. (1996) Phosphorylation of proteasomes in mammalian cells. Identification of two phosphorylated subunits and the effect of phosphorylation on activity. Eur. J. Biochem. 238, 453-462.
29. Mason G. G. F., Murray R. Z., Pappin D., and Rivett A. J. (1998) Phosphorylation of ATPase subunits of the 26S proteasome. FEBS Lett. 430, 269-274.
30. McDermott J. R., Biggins J. A., and Gibson A. M. (1992) Human brain peptidase activity with the specificity to generate the N-terminus of the Alzheimer β-amyloid protein from its precursor. Biochem. Biophys. Res. Commun. 185, 746-752.
31. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
32. Mundy D. I. (1994) Identification of the multicatalytic enzyme as a possible γ-secretase for the amyloid precursor protein. Biochem. Biophys. Res. Commun. 204, 333-341.
33. Neill D., Hughes D., Edwardson J. A., Rima B. K., and Allsop D. (1994) Human IMR-32 neuroblastoma cells as a model cell line in Alzheimer's disease research. J. Neurosci. Res. 39, 482-493.
34. Nelson R. B., Siman R., Iqbal M. A., and Potter H. (1993) Identification of a chymotrypsin-like mast cell protease in rat brain capable of generating the N-terminus of the Alzheimer amyloid β-protein. J. Neurochem. 61, 567-577.
35. Omura S., Fujimoto T., Otoguro K., Matsuzaki K., Moriguchi R., Tanaka H., and Sasaki Y. (1991) Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J. Antibiot. (Tokyo) 44, 113-116.
36. Parvathy S., Hussain I., Karran E. H., Turner A. J., and Hooper N. M. (1998) Alzheimer's amyloid precursor protein α-secretase is inhibited by hydroxamic acid-based zinc metalloprotease inhibitors: similarities to the angiotensin converting enzyme secretase. Biochemistry 37, 1680-1685.
37. Powers J. C. and Harper J. W. (1986) Inhibitors of serine proteinases, in Proteinase Inhibitors (Barrett A. J. and Salvesen G., eds), pp. 55-152. Elsevier, New York.
38. Rich D. H. (1986) Inhibitors of cysteine proteinases, in Proteinase Inhibitors (Barrett A. J. and Salvesen G., eds), pp. 153-178. Elsevier, New York.
39. Rivett A. J. (1998) Intracellular distribution of proteasomes. Curr. Opin. Immunol. 10, 110-114.
40. Rivett A. J., Savory P. J., and Djaballah H. (1994) Multicatalytic endopeptidase complex: proteasome, in Methods in Enzymology, Vol. 244: Proteolytic Enzymes: Serine and Cysteine Peptidases (Barrett A. J., ed), pp. 331-350. Academic Press, San Diego.
41. Sanasrabudhe S. R., Brown A. M., Hulmes J. D., Jacobsen J. S., Vitek M. P., Blume A. J., and Sonnenberg J. L. (1993) Enzymatic generation of the amino terminus of the β-amyloid peptide. J. Biol. Chem. 268, 16699-16705.
42. Savage M. J., Iqbal M., Loh T., Trusko S. P., Scott R., and Siman R. (1994) Cathepsin G: localization in human cerebral cortex and generation of amyloidogenic fragments from the β-amyloid precursor protein. Neuroscience 60, 607-619.
43. Seubert P., Oltersdorf T., Lee M. G., Barbour R., Blomquist C., Davis D. L., Bryant K., Fritz L. C., Galasko D., Thal L. J., Liberberg I., and Schenk D. B. (1993) Secretion of β-amyloid precursor protein cleaved at the amino terminus of the β-amyloid peptide. Nature 361, 260-263.
44. Shinoda M., Toide K., Ohsawa I., and Kohsaka S. (1997) Specific inhibitor for prolyl endopeptidase suppresses the generation of amyloid beta protein in NG108-15 cells. Biochem. Biophys. Res. Commun. 235, 641-645.
45. Tanaka H., Katagiri M., Arima S., Matsuzaki K., Inokoshi J., and Omura S. (1995) Neuronal differentiation of Neuro 2a cells by lactacystin and its partial inhibition by the protein phosphatase inhibitors calyculin A and okadaic acid. Biochem. Biophys. Res. Commun. 216, 291-297.
46. Wolfe M. S., Citron M., Diehl T. S., Xia W., Donkor I. O., and Selkoe D. J. (1998) A substrate-based difluoroketone selectively inhibits Alzheimer's γ-secretase activity. J. Med. Chem. 41, 6-9.
47. Younkin S. G. (1995) Evidence that Aβ 42 is the real culprit in Alzheimer's disease, Ann. Neurol. 37, 287-288.