Degradation of tau protein by puromycin-sensitive aminopeptidase in vitro

Biochemistry

Volumn 45, Issue 50, 2006, Pages 15111-15119

  Sengupta, Soma ^a   Horowitz, Peleg M ^a   Karsten, Stanislav L ^b   Jackson, George R ^b   Geschwind, Daniel H ^b   Fu, Yifan ^a   Berry, Robert W ^a   Binder, Lester I ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO TERMINAL DEGRADATION; MICROTUBULES; PAIRED HELICAL FILAMENTS (PHF); PUROMYCIN-SENSITIVE AMINOPEPTIDASE (PSA);

AGGLOMERATION; AMINO ACIDS; ANTIBODIES; BIODEGRADATION; ENZYME KINETICS; METABOLISM;

PROTEINS;

AMINOPEPTIDASE; ANTIBODY; BRAIN PROTEIN; CHROMOGENIC SUBSTRATE; METAL ION; MICROTUBULE ASSOCIATED PROTEIN; PROTEINASE; PROTEINASE INHIBITOR; PUROMYCIN; PUROMYCIN SENSITIVE AMINOPEPTIDASE; RECOMBINANT ENZYME; TAU ANTIBODY; TAU PROTEIN;

ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME MECHANISM; ENZYME PURIFICATION; ESCHERICHIA COLI; FEMALE; GENETIC SCREENING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL; NONHUMAN; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN POLYMERIZATION; PROTEIN PROCESSING; TAUOPATHY;

ALZHEIMER DISEASE; AMINOPEPTIDASES; BRAIN; ENZYME ACTIVATION; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PUROMYCIN; RECOMBINANT PROTEINS; TAU PROTEINS;

ESCHERICHIA COLI;

EID: 33845591342     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi061830d     Document Type: Article

References (61)

1. Binder, L. I., Guillozet-Bongaarts, A. L., Garcia-Sierra, F., and Berry, R. W. (2005) Tau, tangles, and Alzheimer's disease, Biochim. Biophys. Acta. 1739, 216-223.
2. Johnson, G. V. W., and Jenkins, S. M. (1996) Tau protein in normal and Alzheimer's disease brain, Alzheimer's Dis. Rev. 1, 38-54.
3. Johnson, G. V. W., and Hartigan, J. A. (1998) Tau protein in normal and Alzheimer's disease brain: An update, Alzheimer's Dts. Rev. 3, 125-141.
4. Goedert, M., Spillantini, M. G., and Davies, S. W. (1998) Filamentous nerve cell inclusions in neurodegenerative diseases, Curr. Opin. Neurobiol. 8, 619-632.
5. Hutton, M. (2001) Missense and splice site mutations in tau associated with FTDP-17: multiple pathogenic mechanisms, Neurology 56, S21-S25.
6. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies, Annu. Rev. Neurosci. 24, 1121-1159.
7. Ikeda, K., Akiyama, H., Arai, T., Kondo, H., Haga, C., Iritani, S., and Tsuchiya, K. (1998) Alz-50/Gallyas-positive lysosome-like intraneuronal granules in Alzheimer's disease and control brains, Neurosci. Lett. 258, 113-116.
8. Kosik, K. S., Joachim, C. L., and Selkoe, D. J. (1986) Microtubule-associated protein tau (tau) is a major antigenic component of paired helical filaments in Alzheimer disease, Proc. Natl. Acad. Sci. U.S.A. 83, 4044-4048.
9. Bancher, C., Brunner, C., Lassmann, H., Budka, H., Jellinger, K., Wiche, G., Seitelberger, F., Grundke-Iqbal, I., Iqbal, K., and Wisniewski, H. M. (1989) Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease, Brain Res. 477, 90-99.
10. Ksiezak-Reding, H., and Yen, S. H. (1991) Structural stability of paired helical filaments requires microtubule-binding domains of tau: a model for self-association, Neuron. 6, 717-728.
11. Kenessey, A., Nacharaju, P., Ko, L. W., and Yen, S. H. (1997) Degradation of tau by lysosomal enzyme cathepsin D: implication for Alzheimer neurofibrillary degeneration, J. Neurochem. 69, 2026-2038.
12. Mercken, M., Grynspan, F., and Nixon, R. A. (1995) Differential sensitivity to proteolysis by brain calpain of adult human tau, fetal human tau and PHF-tau, FEBS Lett. 368, 10-14.
13. Gamblin, T. C., Chen, F., Zambrano, A., Abraha, A., Lagalwar, S., Guillozet, A. L., Lu, M., Fu, Y., Garcia-Sierra, F., LaPointe, N., Miller, R., Berry, R. W., Binder, L. I., and Cryns, V. L. (2003) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease, Proc. Natl. Acad. Sci. U.S.A. 100, 10032-10037.
14. Horowitz, P. M., Patterson, K. R., Guillozet-Bongaarts, A. L., Reynolds, M. R., Carroll, C. A., Weintraub, S. T., Bennett, D. A., Cryns, V. L., Berry, R. W., and Binder, L. I. (2004) Early N-terminal changes and caspase-6 cleavage of tau in Alzheimer's disease, J. Neurosci. 24, 7895-7902.
15. David, D. C., Layfield, R., Serpell, L., Narain, Y., Goedert, M., and Spillantini, M. G. (2002) Proteasomal degradation of tau protein, J. Neurochem. 83, 176-185.
16. Wang, X., An, S., and Wu, J. M. (1996) Specific processing of native and phosphorylated tau protein by proteases, Biochem. Biophys. Res. Commun. 219, 591-597.
17. Diesen, O. F. (1994) Proteolytic degradation of microtubule associated protein tau by thrombin, Biochem. Biophys. Res. Commun. 201, 716-721.
18. Rawlings, N. D., and Barrett, A. J. (1993) Evolutionary families of peptidases, Biochem. J. 290, 205-218.
19. Hooper, N. M. (1994) Families of zinc metalloproteases, FEBS Lett. 354, 1-6.
20. Karsten, S. L., Sang, T. K., Gehman, L. T., Chatterjee, S., Liu, J., Lawless, G. M., Sengupta, S., Berry, R. W., Pomakian, J., Oh, H. S., Schulz, C., Hui, K. S., Wiedau-Pazos, M., Vinters, H. V., Binder, L. I., Geschwind, D. H., and Jackson, G. R. (2006) A genomic screen for modifiers of tauopathy identifies puromycin-sensitive aminopeptidase as an inhibitor of tau-induced neurodegeneration, Neuron. 51, 549-560.
21. Hayashi, M. (1978) Monkey brain arylamidase. II. Further characterization and studies on mode of hydrolysis of physiologically active peptides, J. Biochem. 84, 1363-1372.
22. Hersh, L. B. (1985) Characterization of membrane-bound aminopeptidases from rat brain: identification of the enkephalin-degrading aminopeptidase, J. Neurochem. 44, 1427-1435.
23. Tobler, A. R., Constam, D. B., Schmitt-Graff, A., Malipiero, U., Schlapbach, R., and Fontana, A. (1997) Cloning of the human puromycin-sensitive aminopeptidase and evidence for expression in neurons, J. Neurochem. 68, 889-897.
24. Dyer, S. H., Slaughter, C. A., Orth, K., Moomaw, C. R., and Hersh, L. B. (1990) Comparison of the soluble and membrane-bound forms of the puromycin-sensitive enkephalin-degrading aminopeptidases from rat, J. Neurochem. 54, 547-554.
25. Hersh, L. B., and McKelvy, J. F. (1981) An aminopeptidase from bovine brain which catalyzes the hydrolysis of enkephalin, J. Neurochem. 36, 171-178.
26. McLellan, S., Dyer, S. H., Rodriguez, G., and Hersh, L. B. (1988) Studies on the tissue distribution of the puromycin-sensitive enkephalin-degrading aminopeptidases, J. Neurochem. 51, 1552-1559.
27. Wagner, G. W., Tavianini, M. A., Herrmann, K. M., and Dixon, J. E. (1981) Purification and characterization of an enkephalin aminopeptidase from rat brain, Biochemistry 20, 3884-3890.
28. Huber, G., Thompson, A., Gruninger, F., Mechler, H., Hochstrasser, R., Hauri, H. P., and Malherbe, P. (1999) cDNA cloning and molecular characterization of human brain metalloprotease MP100: a beta-secretase candidate? J. Neurochem. 72, 1215-1223.
29. Constam, D. B., Tobler, A. R., Rensing-Ehl, A., Kemler, I., Hersh, L. B., and Fontana, A. (1995) Puromycin-sensitive aminopeptidase. Sequence analysis, expression, and functional characterization, Journal of Biol. Chem. 270, 26931-26939.
30. Schulz, C., Perezgasga, L., and Fuller, M. T. (2001) Genetic analysis of dPsa, the Drosophila orthologue of puromycin-sensitive aminopeptidase, suggests redundancy of aminopeptidases, Dev. Genes Evol. 211, 581-588.
31. Hui, K. S., Wang, Y. J., and Lajtha, A. (1983) Purification and characterization of an enkephalin aminopeptidase from rat brain membranes, Biochemistry 22, 1062-1067.
32. Schnebli, H. P., Phillipps, M. A., and Barclay, R. K. (1979) Isolation and characterization of an enkephalin-degrading aminopeptidase from rat brain, Biochim. Biophys. Acta 569, 89-98.
33. Botbol, V., and Scornik, O. A. (1983) Peptide intermediates in the degradation of cellular proteins. Bestatin permits their accumulation in mouse liver in vivo, J. Biol. Chem. 258, 1942-1949.
34. Goldberg, A. L., and Rock, K. AL. (1992) Proteolysis, proteasomes and antigen presentation, Nature 357, 375-379.
35. Stoltze, L., Schirle, M., Schwarz, G., Schroter, C., Thompson, M. W., Hersh, L. B., Kalbacher, H., Stevanovic, S., Rammensee, H. G., and Schild, H. (2000) Two new proteases in the MHC class I processing pathway, Nat. Immunol. 1, 413-418.
36. Osada, T., Ikegami, S., Takiguchi-Hayashi, K., Yamazaki, Y., Katoh-Fukui, Y., Higashinakagawa, T., Sakaki, Y., and Takeuchi, T. (1999) Increased anxiety and impaired pain response in puromycin-sensitive aminopeptidase gene-deficient mice obtained by a mouse gene-trap method, J. Neurosci. 19, 6068-6078.
37. Gros, C., Giros, B., and Schwartz, J. C. (1985) Identification of aminopeptidase M as an enkephalin-inactivating enzyme in rat cerebral membranes, Biochemistry 24, 2179-2185.
38. Kerr, M. A., and Kenny, A. J. (1974) The purification and specificity of a neutral endopeptidase from rabbit kidney brush border, Biochem. J. 137, 477-488.
39. Malfroy, B., Swerts, J. P., Guyon, A., Roques, B. P., and Schwartz, J. C. (1978) High-affinity enkephalin-degrading peptidase in brain is increased after morphine, Nature 276, 523-526.
40. Matsas, R., Stephenson, S. L., Hryszko, J., Kenny, A. J., and Turner, A. J. (1985) The metabolism of neuropeptides. Phase separation of synaptic membrane preparations with Triton X-114 reveals the presence of aminopeptidase N, Biochem. J. 231, 445-449.
41. Traficante, L. J., Rotrosen, J., Siekierski, J., Tracer, H., and Gershon, S. (1980) Enkephalin inactivation by N-terminal tyrosine cleavage: purification and partial characterization of a highly specific enzyme from human brain, Life Sci. 26, 1697-1706.
42. Hui, M., Budai, E. D., Lajtha, A., Palkovits, M., and Hui, K. S. (1995) Changes in puromycin-sensitive aminopeptidases in post-mortem schizophrenic brain regions, Neurochem. Int. 27, 433-441.
43. Safavi, A., and Hersh, L. B. (1995) Degradation of dynorphin-related peptides by the puromycin-sensitive aminopeptidase and aminopeptidase M, J. Neurochem. 65, 389-395.
44. Goedert, M., Spillantini, M. G., Potier, M. C., Ulrich, J., and Crowther, R. A. (1989) Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats: differential expression of tau protein mRNAs in human brain, EMBO J. 8, 393-399.
45. Abraha, A., Ghoshal, N., Gamblin, T. C., Cryns, V., Berry, R. W., Kuret, J., and Binder, L. I. (2000) C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease, J. Cell Sci. 113, 3737-3745.
46. Carmel, G., Mager, E. M., Binder, L. I., and Kuret, J. (1996) The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology, J. Biol. Chem. 271, 32789-32795.
47. Reynolds, M. R., Reyes, J. F., Fu, Y., Bigio, E. H., Guillozet-Bongaarts, A. L., Berry, R. W., and Binder, L. I. (2006) Tau nitration occurs at tyrosine 29 in the fibrillar lesions of Alzheimer's disease and other tauopathies, J. Neurosci. 26, 10636-10645.
48. Guillozet-Bongaarts, A. L., Garcia-Sierra, F., Reynolds, M. R., Horowitz, P. M., Fu, Y., Wang, T., Cahill, M. E., Bigio, E. H., Berry, R. W., and Binder, L. I. (2005) Tau truncation during neurofîbrillary tangle evolution in Alzheimer's disease, Neurobiol. Aging 26, 1015-1022.
49. McDermott, J. R., Mantle, D., Lauffart, B., and Kidd, A. M. (1985) Purification and characterization of a neuropeptide-degrading aminopeptidase from human brain, J. Neurochem. 45, 752-759.
50. Horowitz, P. M., LaPointe, N., Guillozet-Bongaarts, A. L., Berry, R. W., and Binder, L. I. (2006) N-terminal fragments of tau inhibit full-length tau polymerization in vitro, Biochemistry 45, 12859-12866.
51. Hayashi, M., and Oshima, K. (1977) Purification and characterization of arylamidase from monkey brain, J. Biochem. 81, 631-639.
52. Billingsley, M. L., and Kincaid, R. L. (1997) Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration, Biochem. J. 323, 577-591.
53. Reynolds, M. R., Berry, R. W., and Binder, L. I. (2005) Site-specific nitration differentially influences tau assembly in vitro, Biochemistry 44, 13997-14009.
54. Ghoshal, N., Garcia-Sierra, F., Fu, Y., Beckett, L. A., Mufson, E. J., Kuret, I., Berry, R. W., and Binder, L. I. (2001) Tau-66: Evidence for a novel tau conformation in Alzheimer's disease, J. Neurochem. 77, 1372-1385.
55. Safar, J., Wille, H., Itri, V., Groth, D., Serban, H., Torchia, M., Cohen, F. E., and Prusiner, S. B. (1998) Eight prion strains have PrP(Sc) molecules with different conformations [see comments], Nat. Med. 4, 1157-1165.
56. Gamblin, T. C., Berry, R. W., and Binder, L. I. (2003) Tau polymerization: role of the amino terminus, Biochemistry 42, 2252-2257.
57. Thompson, M. W., Tobler, A., Fontana, A., and Hersh, L. B. (1999) Cloning and analysis of the gene for the human puromycin-sensitive aminopeptidase, Biochem. Biophys. Res. Commun. 258, 234-240.
58. Donlon, T., Harris, P., and Neve, R. (1987) Localization of microtubule-associated protein tau (MTBT1) to chromosome 17q21, Cytogenet. Cell Genet. 46, 607.
59. Schonlein, C., Loffler, J., and Huber, G. (1994) Purification and characterization of a novel metalloprotease from human brain with the ability to cleave substrates derived from the N-terminus of beta-amyloid protein, Biochem. Biophys. Res. Commun. 201, 45-53.
60. Minnasch, P., Yamamoto, Y., Ohkubo, I., and Nishi, K. (2003) Demonstration of puromycin-sensitive alanyl aminopeptidase in Alzheimer disease brain, Legal Med. 5, S285-S287.
61. Ghoshal, N., Garcia-Sierra, F., Wuu, J., Leurgans, S., Bennett, D. A., Berry, R. W., and Binder, L. I. (2002) Tau conformational changes correspond to impairments of episodic memory in mild cognitive impairment and Alzheimer's disease, Exp. Neurol. 177, 475-493.