Cathepsins S, B and L with aminopeptidases display β-secretase activity associated with the pathogenesis of Alzheimer's disease

Biological Chemistry

Volumn 392, Issue 6, 2011, Pages 555-569

  Schechter, Israel ^a   Ziv, Etty ^a  

^a Yenuvun Research Laboratory   (Israel)

Author keywords

BACE1; cleavage of site sequence; cleavage points; kcat; Km; new secretases; WT site sequence

Indexed keywords

BETA SECRETASE; CATHEPSIN B; CATHEPSIN D; CATHEPSIN L; CATHEPSIN S; CYTOSOL AMINOPEPTIDASE;

ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; WILD TYPE;

ALZHEIMER DISEASE; AMINOPEPTIDASES; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; CATHEPSIN B; CATHEPSIN L; CATHEPSINS; CATTLE; HUMANS; KIDNEY; RECOMBINANT PROTEINS; SPLEEN;

ANIMALIA;

EID: 79958026120     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2011.054     Document Type: Article

References (62)

1. Abbenante, G., Kovacs, D.M., Leung, D.L., Craik, D,J., Tanzi, R.E., and Fairlie, D.P. (2000). Inhibitors of b-amyloid formation based on the b-secretase cleavage site. Biochem. Biophys. Res. Commun. 268, 133-135. (Pubitemid 30116623)
2. Aronson, N.N. and Barrett, A.J. (1978). The specificity of cathepsin B. Hydrolysis of glucagon at the C-terminus by a peptidyldipeptidase mechanism. Biochem. J. 171, 759-765. (Pubitemid 8348753)
3. Bohme, L., Hoffmann, T., Manhart, S., Wolf, R., and Demuth, H.U. (2008). Isoaspartate-containing amyloid precursor proteinderived peptides alter efficacy and specificity of potential bsecretases. Biol. Chem. 389, 1055-1066.
4. Bromme, D., Bonneau, P.R., Lachance, P., Wiederanders, B., Kirschke, H., Peters, C., Thomas, D.Y., Storer, A.C., and Vernet, T. (1993). Functional expression of human cathepsin S in Saccharomyces cerevisiae. Purification and characterization of the recombinant enzyme. J. Biol. Chem. 468, 4832-4880.
5. Cai, H., Wang, Y., McCarthy, D., Wen, H., Borchelt, D.R., Price, D.L., and Wong, P.C. (2001). BACE1 is the major b-secretase for generation of Abeta peptides by neurons. Nat. Neurosci. 4, 233-234. (Pubitemid 32194867)
6. Cataldo, A.M. and Nixon, R.A. (1990). Enzymatically active lysosomal proteases are associated with amyloid deposits in Alzheimer brain. Proc. Natl. Acad. Sci. USA 87, 3861-3865.
7. Cataldo, A.M., Paskevich, P.A., Kominami, E., and Nixon, R.A. (1991). Lysosomal hydrolases of different classes are abnormally distributed in brains of patients with Alzheimer disease. Proc. Natl. Acad. Sci. USA 88, 10998-11002. (Pubitemid 21915966)
8. Cataldo, A.M., Petanceska, S., Terio N.B., Peterhoff, C.M., Durham, R., Mercken, M., Mehta, P.D., Buxbaum, J., Haroutunian, V. and Nixon, R.A. (2004). A b localization in abnormal endosomes: association with earliest Ab elevations in AD and Down syndrome. Neurobiol. Aging 25, 1263-272. (Pubitemid 39299162)
9. Chapman, H.A., Riese, R.J., and Shi, G.P. (1997). Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59, 63-88. (Pubitemid 27142435)
10. Cole, S.L. and Vassar, R. (2008). The role of amyloid precursor protein processing by BACE1, the b-secretase, in Alzheimer disease pathophysiology. J. Biol. Chem. 283, 29621-29625.
11. Dunn, B.M. and Hung, S. (2000). The two sides of enzyme-substrate specificity: lessons from the aspartic proteinases. Biochim. Biophys. Acta 1477, 231-240. (Pubitemid 30119903)
12. Erickson, A.H. (1989). Biosynthesis of lysosomal endopeptidases. J. Cell. Biochem. 40, 31-41. (Pubitemid 19146198)
13. Friedrichs, B., Tepel, C., Reinheckel, T., Deussing, J., von Figura, K., Herzog, V., Peters, C, Saftig, P., and Brix, K. (2003). Thyroid functions of mouse cathepsins B, K, and L. J. Clin. Invest. 111, 1733-1745. (Pubitemid 38057754)
14. Golde, T.E., Estus, S., Younkin, L.H., Selkoe, D.J., and Younkin, S.G. (1992). Processing of the amyloid protein precursor to potentially amyloidogenic derivatives. Science 255, 728-730.
15. Haass, C., Koo, E.H., Mellon, A., Hung, A.Y., and Selkoe, D.J. (1992). Targeting of cell-surface b-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 357, 500-503.
16. Hook, V.Y., Azaryan, A.V., Hwang, S.R., and Tezapsidis, N. (1994). Proteases and the emerging role of protease inhibitors in prohormone processing. FASEB J. 8, 1269-1278.
17. Hook, V., Toneff, T., Bogyo, M., Greenbaum, D., Medzihradszky, K.F., Neveu, J., Lana, W., Hook, G., and Reisine, T. (2005). Inhibition of cathepsin B reduces b-amyloid production in regulated secretory vesicles of neuronal chromaffin cells: evidence for cathepsin B as a candidate b-secretase of Alzheimer's disease. Biol. Chem. 386, 931-940. (Pubitemid 41448149)
18. Hook, G., Hook, V.Y., and Kindy, M. (2007). Cysteine protease inhibitors reduce brain b-secretase activity in vivo and are potential Alzheimer's disease therapeutics. Biol. Chem. 388, 979-983. (Pubitemid 47258539)
19. Hook, V., Kindy, M., and Hook. G. (2008a) Inhibitors of cathepsin B improve memory and reduce b-amyloid in transgenic Alzheimer disease mice expressing the wild-type, but not the Swedish mutant, b-secretase site of the amyloid precursor protein. J. Biol. Chem. 283, 7745-7753.
20. Hook, V., Schechter, I., Demuth, H.U., and Hook, G. (2008b). Alternative pathways for production of b-amyloid peptides of Alzheimer's disease. Biol. Chem. 389, 993-1006.
21. Hook, V.Y., Kindy, M., Reinheckel, T., Peters, C., and Hook, G. (2009). Genetic cathepsin B deficiency reduces b-amyloid in transgenic mice expressing human wild-type amyloid precursor protein. Biochem. Biophys. Res. Commun. 386, 284-288.
22. Hooper, M.N. (2002). Proteases in Biology and Medicine: Essays in Biochemistry, Vol. 38 (Oxford, UK: Portland Press).
23. Hussain, I., Powell, D., Howlett, D.R., Tew, D.G., Meek, T.D., Chapman, C., Gloger, I.S., Murphy, K.E., Southan, C.D., Ryan, D.M., et al. (1999). Identification of a novel aspartic protease (Asp 2) as b-secretase. Mol. Cell Neurosci. 14, 419-427. (Pubitemid 30026585)
24. Iribar, C., Esteban, M.J., Martinez, J.M., and Peinado, J.M. (1995). Decrease in cytosolic aspartyl-aminopeptidase but not in alanylaminopeptidase activity in the frontal cortex of the aged rat. Brain Res. 687, 211-213.
25. Jacks, T. (1996). Tumor suppressor gene mutations in mice. Annu. Rev. Genet. 3, 603-636. (Pubitemid 27014480)
26. Lemere, C.A., Munger, J.S., Shi, G.P., Natkin, L., Haass, C., Chapman, H.A., and Selkoe, D.J. (1995). The lysosomal cysteine protease, cathepsin S, is increased in Alzheimer's disease and Down syndrome brain. An immunocytochemical study. Am. J. Pathol. 146, 848-860.
27. Lin, X., Koelsch, G., Wu, S., Downs, D., Dashti, A., and Tang, J. (2000). Human aspartic protease memapsin 2 cleaves the bsecretase site of b-amyloid precursor protein. Proc. Natl. Acad. Sci. USA 97, 1456-1460. (Pubitemid 30118462)
28. Lou, Y., Bolon, B., Kahn, S., Bennett, B.D., Babu-Khan, S., Denis, P., Fan, W., Kha, H., Zhang, J., Gong, Y., et al. (2001). Mice deficient in BACE1, the Alzheimer's b-secretase, have normal phenotype and abolished b-amyloid generation. Nat. Neurosci. 4, 231-232. (Pubitemid 32194866)
29. Maizel, J.V. (1971). Polyacrylamide gel electrophoresis of viral proteins. Methods Virol. 5, 179-216.
30. Mohamed, M.M. and Sloane, B.F. (2006). Cysteine cathepsins: multifunctional enzymes in cancer. Nat. Rev. Cancer. 6, 764-775. (Pubitemid 44450465)
31. Munger, J.S., Haass, C., Lemere, C.A., Shi, G.P., Wong., W.S., Teplow, D.B., Selkoe, D.J., and Chapman, H.A. (1995). Lysosomal processing of amyloid precursor protein to Ab peptides: a distinct role for cathepsin S. Biochem. J. 311, 299-305.
32. Neve, R.L., Finch, E.A., and Dawes, L.R. (1988). Expression of the Alzheimer amyloid precursor gene transcripts in the human brain. Neuron 1, 669-677.
33. Pasternak, S.H., Bagshaw, R.D., Guiral, M., Zhang, S., Ackerley, C.A., Pak, B.J., Callahan, J.W., Mahuran, D.J. (2003). Presenilin- 1, nicastrin, amyloid precursor protein, and gamma-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 278, 26687-26694. (Pubitemid 36876814)
34. Rawlings, N.D. and Barrett, A.J. (1993). Evolutionary families of peptidases. Biochem. J. 290, 205-218. (Pubitemid 23081221)
35. Roberds, S.L., Anderson, J., Basi, G., Bienkowski, M.J., Branstetter, D.G., Chen, K.S., Freedman, S.B., Frigon, N.L., Games, D., Hu, K., et al. (2001). BACE knockout mice are healthy despite lacking the primary b-secretase activity in brain: implications for Alzheimer's disease therapeutics. Hum. Mol. Genet. 10, 1317-1324. (Pubitemid 32600485)
36. Sahasrabudhe, 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 b-amyloid peptide. J. Biol. Chem. 268, 16699-16705. (Pubitemid 23229984)
37. Saido, T.C. (1998). Alzheimer's disease as proteolytic disorders: anabolism and catabolism of b-amyloid. Neurobiol. Aging 19, S69-S75. (Pubitemid 28178942)
38. Schechter, I. (1970). On the active sites of proteases. Cleavage of peptide bonds involving D-alanine residues by carboxypeptidase A. Eur. J. Biochem. 14, 516-520.
39. Schechter, I. (2005). Mapping the active site of proteases in the 1960s and rational design of inhibitors/drugs in the 1990s. Curr. Protein Pept. Sci. 6, 501-512. (Pubitemid 41723521)
40. Schechter, I. and Berger, A. (1966a). Peptides of L- and D-alanine. Synthesis and optical rotations. Biochemistry 5, 3362-3370.
41. Schechter, I. and Berger, A. (1966b). The hydrolysis of diastereoisomers of alanine peptides by carboxypeptidase A and leucine aminopeptidase. Biochemistry 5, 3371-3375.
42. Schechter, I. and Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
43. Schechter, I. and Berger, A. (1968). On the active site of proteases. 3. Mapping the active site of papain; specific peptide inhibitors of papain. Biochem. Biophys. Res. Commun. 32, 898-902.
44. Schechter, I. and Ziv, E. (2006). Inhibitors can activate proteases to catalyze the synthesis and hydrolysis of peptides. Biochemistry 45, 14567-14572. (Pubitemid 44906973)
45. Schechter, I. and Ziv, E. (2008). Kinetic properties of cathepsin D and BACE 1 indicate the need to search for additional b-secretase candidate(s). Biol. Chem. 389, 313-320. (Pubitemid 351329023)
46. Schilling, S., Lauber, T., Schaupp, M., Manhart, S., Scheel, E., Böhm, G., and Demuth, H.U. (2006). On the seeding and oligomerization of pGlu-amyloid peptides (in vitro). Biochemistry 45, 12393-12399. (Pubitemid 44583682)
47. Schilling, S., Zeitschel, U., Hoffmann, T., Heiser, U., Francke, M., Kehlen, A., Holze, R.M., Hutter-Paier, B., Prokesch, M., Windisch, M., et al. (2008). Glutaminyl cyclase inhibition attenuates pyroglutamate Ab and Alzheimer's disease-like pathology. Nat. Med. 14, 1106-1111.
48. Selkoe, D.J. (2001). Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81, 741-766. (Pubitemid 32267077)
49. Shi, X.P., Chen, E., Yin, K.C., Na, S., Garsky, V.M., Lai, MT., Li, Y.M., Platchek, M., Register, R.B., Sardana, M.K., et al. (2001). The pro domain of b-secretase does not confer strict zymogenlike properties but does assist proper folding of the protease domain. J. Biol. Chem. 276, 10366-10373.
50. Shi, X.P., Tugusheva, K., Bruce, J.E., Lucka, A., Chen-Dodson, E., Hu, B., Wu, G.X, Price, E., Register, R.B., Lineberger, J., et al. (2005). Novel mutations introduced at the b-site of amyloid b protein precursor enhance the production of amyloid beta peptide by BACE1 in vitro and in cells. J. Alzheimer's Dis. 7, 139-148. (Pubitemid 40592188)
51. Sinha, S. and Lieberburg, I. (1999). Cellular mechanisms of b-amyloid production and secretion. Proc. Natl. Acad. Sci. USA 96, 11049-11053. (Pubitemid 29487325)
52. Sinha, S., Anderson, J.P., Barbour, R., Basi, G.S., Caccavello, R., Davis, D., Doan, M., Dovey, H.F., Frigon, N., Hong, J., et al. (1999). Purification and cloning of amyloid precursor protein bsecretase from human brain. Nature 402, 537-540.
53. Taylor, A. (1993). Aminopeptidases: structure and function. FASEB J. 7, 290-298. (Pubitemid 23067779)
54. Tedelind, S., Poliakova, K., Valeta, A., Hunegnaw, R., Yemanaberhan, E.L., Heldin, N.E., Kurebayashi, J., Weber, E., Kopitar- Jerala, N., Turk, B. et al. (2010). Nuclear cysteine cathepsin variants in thyroid carcinoma cells. Biol. Chem. 391, 923-935.
55. Tomasselli, A.G., Qahwash, I., Emmons, T.L., Lu, Y., Leone, J.W., Lull, J.M., Fok, K.F., Bannow, C.A., Smith, C.W., Bienkowski, M.J., et al. (2003). Employing a superior BACE1 cleavage sequence to probe cellular APP processing. J. Neurochem. 84, 1006-1017. (Pubitemid 36330654)
56. Turk, B., Turk, D., and Turk, V. (2000). Lysosomal cysteine proteases: more than scavengers. Biochim. Biophys. Acta 1477, 98-111. (Pubitemid 30119895)
57. Turner, R.T., Koelsch, G., Hong, L., Castanheira, P., Ermolieff, J., Ghosh, A.K., and Tang, J. (2001). Subsite specificity of memapsin 2 (b-secretase): implications for inhibitor design. Biochemistry 40, 10001-10006. (Pubitemid 32800106)
58. Vassar, R., Bennett, D., Babu-Khan, S., Kahn, S., Mendiaz, E.A., Denis, P., Teplow, D.B., Ross, S., Amarante, P., Loeloff, R., et al. (1999). b-Secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286, 735-741.
59. Wang, R., Sweeney, D., Gandy, S.E., and Sisodia, S. (1996). The profile of soluble amyloid b protein in cultured cell media. J. Biol. Chem. 271, 31894-31902.
60. Wolfe, M.S. (2006). Shutting down Alzheimer's. Sci. Am. 294, 72-79.
61. Yan, R., Bienkowski, M.J., Shuck, M.E., Miao, H., Tory, M.C., Pauley, A.M., Brashier, J.R., Stratman, N.C., Mathews, W.R., Buhl, A.E., et al. (1999). Membrane-anchored aspartyl protease with Alzheimer's disease b-secretase activity. Nature 402, 533-537.
62. Yang, L.B., Lindholm, K., Yan, R., Citron, M., Xia, W., Yang, X.L., Beach, T., Sue, L., Won, P., Price, D., et al. (2003). Elevated bsecretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat. Med. 9, 3-4. (Pubitemid 36098241)