Increased expression of the oligopeptidase THOP1 is a neuroprotective response to Aβ toxicity

Neurobiology of Disease

Volumn 31, Issue 1, 2008, Pages 145-158

  Pollio, Giuseppe ^a   Hoozemans, Jeroen J M ^b   Andersen, Claus A ^a   Roncarati, Renza ^a   Rosi, Maria Cristina ^c   van Haastert, Elise S ^b   Seredenina, Tamara ^a   Diamanti, Daniela ^a   Gotta, Stefano ^a   Fiorentini, Anna ^c   Magnoni, Letizia ^a   Raggiaschi, Roberto ^a   Rozemuller, Annemieke J M ^b   Casamenti, Fiorella ^c   Caricasole, Andrea ^a   Terstappen, Georg C ^a  

^a Siena Biotech SpA   (Italy)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF FLORENCE   (Italy)

Author keywords

AD post mortem brain tissue; Alzheimer's disease; Neuroprotection; Phosphoproteomics; RNAi; TgCRND8 mouse; Thimet oligopeptidase; THOP1

Indexed keywords

AMYLOID BETA PROTEIN; THIMET OLIGOPEPTIDASE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEMENTIA; FEMALE; HUMAN; HUMAN TISSUE; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEOMICS; RAT; RNA INTERFERENCE; TRANSGENIC MOUSE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; METALLOENDOPEPTIDASES; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MIDDLE AGED; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SENILE PLAQUES; TRANSFECTION;

EID: 44949174006     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2008.04.004     Document Type: Article

References (53)

1. Abraham C.R., McGraw W.T., Slot F., and Yamin R. Alpha 1-antichymotrypsin inhibits A beta degradation in vitro and in vivo. Ann. N.Y. Acad. Sci. 920 (2000) 245-248
2. Akiyama H., et al. Inflammation and Alzheimer's disease. Neurobiol. Aging 21 (2000) 383-421
3. Bellucci A., Luccarini I., Scali C., Prosperi C., Giovannini M.G., Pepeu G., and Casamenti F. Cholinergic dysfunction, neuronal damage and axonal loss in TgCRND8 mice. Neurobiol. Dis. 23 (2006) 260-272
4. Bellucci A., Rosi M.C., Grossi C., Fiorentini A., Luccarini I., and Casamenti F. Abnormal processing of tau in the brain of aged TgCRND8 mice. Neurobiol. Dis. 27 (2007) 328-338
5. Benjamini Y., and Hochberg Y. Controlling the False Discovery Rate: a Practical and Powerful Approach to Multiple Testing. (1995) 289-300
6. Braak H., and Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82 (1991) 239-259
7. Carreno F.R., Goni C.N., Castro L.M., and Ferro E.S. 14-3-3 epsilon modulates the stimulated secretion of endopeptidase 24.15. J. Neurochem. 93 (2005) 10-25
8. Carson J.A., and Turner A.J. Beta-amyloid catabolism: roles for neprilysin (NEP) and other metallopeptidases?. J. Neurochem. 81 (2002) 1-8
9. Chaerkady R., and Sharma K.K. Characterization of a bradykinin-hydrolyzing protease from the bovine lens. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1214-1223
10. Citron M. Strategies for disease modification in Alzheimer's disease. Nat. Rev., Neurosci. 5 (2004) 677-685
11. Conn K.J., Pietropaolo M., Ju S.T., and Abraham C.R. Monoclonal antibodies against the human metalloprotease EC 3.4.24.15 label neurofibrillary tangles in Alzheimer's disease brain. J. Neurochem. 66 (1996) 2011-2018
12. Copani A., Condorelli F., Caruso A., Vancheri C., Sala A., Giuffrida Stella A.M., Canonico P.L., Nicoletti F., and Sortino M.A. Mitotic signaling by beta-amyloid causes neuronal death. FASEB J. 13 (1999) 2225-2234
13. Copani A., Hoozemans J.J., Caraci F., Calafiore M., Van Haastert E.S., Veerhuis R., Rozemuller A.J., Aronica E., Sortino M.A., and Nicoletti F. DNA polymerase-beta is expressed early in neurons of Alzheimer's disease brain and is loaded into DNA replication forks in neurons challenged with beta-amyloid. J. Neurosci. 26 (2006) 10949-10957
14. Dando P.M., Brown M.A., and Barrett A.J. Human thimet oligopeptidase. Biochem. J. 294 Pt 2 (1993) 451-457
15. Ekins S., Bugrim A., Nikolsky Y., and Nikolskaya T. Systems Biology: Applications in Drug Discovery (2005), Wiley 123-183
16. Ferro E.S., Carreno F.R., Goni C., Garrido P.A., Guimaraes A.O., Castro L.M., Oliveira V., Araujo M.C., Rioli V., Gomes M.D., Fontenele-Neto J.D., and Hyslop S. The intracellular distribution and secretion of endopeptidases 24.15 (EC 3.4.24.15) and 24.16 (EC 3.4.24.16). Protein Pept. Lett. 11 (2004) 415-421
17. Gong B., Cao Z., Zheng P., Vitolo O.V., Liu S., Staniszewski A., Moolman D., Zhang H., Shelanski M., and Arancio O. Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 126 (2006) 775-788
18. Hardy J., and Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol. Sci. 12 (1991) 383-388
19. Hardy J., and Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002) 353-356
20. Hoozemans J.J., Bruckner M.K., Rozemuller A.J., Veerhuis R., Eikelenboom P., and Arendt T. Cyclin D1 and cyclin E are co-localized with cyclo-oxygenase 2 (COX-2) in pyramidal neurons in Alzheimer disease temporal cortex. J. Neuropathol. Exp. Neurol. 61 (2002) 678-688
21. Ichai C., Chevallier N., Delaere P., Dournaud P., Epelbaum J., Hauw J.J., Vincent J.P., and Checler F. Influence of region-specific alterations of neuropeptidase content on the catabolic fates of neuropeptides in Alzheimer's disease. J. Neurochem. 62 (1994) 645-655
22. Janus C., and Westaway D. Transgenic mouse models of Alzheimer's disease. Physiol. Behav. 73 (2001) 873-886
23. Kim S.I., Pabon A., Swanson T.A., and Glucksman M.J. Regulation of cell-surface major histocompatibility complex class I expression by the endopeptidase EC3.4.24.15 (thimet oligopeptidase). Biochem. J. 375 (2003) 111-120
24. Kitano H., Funahashi A., Matsuoka Y., and Oda K. Using process diagrams for the graphical representation of biological networks. Nat. Biotechnol. 23 (2005) 961-966
25. Knight C.G., Dando P.M., and Barrett A.J. Thimet oligopeptidase specificity: evidence of preferential cleavage near the C-terminus and product inhibition from kinetic analysis of peptide hydrolysis. Biochem. J. 308 Pt 1 (1995) 145-150
26. Koike H., Seki H., Kouchi Z., Ito M., Kinouchi T., Tomioka S., Sorimachi H., Saido T.C., Maruyama K., Suzuki K., and Ishiura S. Thimet oligopeptidase cleaves the full-length Alzheimer amyloid precursor protein at a beta-secretase cleavage site in COS cells. J. Biochem. (Tokyo) 126 (1999) 235-242
27. Loo D.T., Copani A., Pike C.J., Whittemore E.R., Walencewicz A.J., and Cotman C.W. Apoptosis is induced by beta-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 7951-7955
28. Lovell M.A., Xiong S., Markesbery W.R., and Lynn B.C. Quantitative proteomic analysis of mitochondria from primary neuron cultures treated with amyloid beta peptide. Neurochem. Res. 30 (2005) 113-122
29. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 430 (2004) 631-639
30. Montiel M., Caro M.C., and Jimenez E. Agonist-induced internalisation of the angiotensin II-binding sites from plasma membranes of isolated rat hepatocytes. J. Endocrinol. 152 (1997) 407-412
31. Nagele R.G., D'Andrea M.R., Lee H., Venkataraman V., and Wang H.Y. Astrocytes accumulate A beta 42 and give rise to astrocytic amyloid plaques in Alzheimer disease brains. Brain Res. 971 (2003) 197-209
32. Papastoitsis G., Siman R., Scott R., and Abraham C.R. Identification of a metalloprotease from Alzheimer's disease brain able to degrade the beta-amyloid precursor protein and generate amyloidogenic fragments. Biochemistry 33 (1994) 192-199
33. Paratore S., Parenti R., Torrisi A., Copani A., Cicirata F., and Cavallaro S. Genomic profiling of cortical neurons following exposure to beta-amyloid. Genomics 88 (2006) 468-479
34. Perry G., Avila J., Espey M.G., Wink D.A., Atwood C.S., and Smith M.A. Biochemistry of neurodegeneration. Science 291 (2001) 595-597
35. Portaro F.C., Hayashi M.A., Silva C.L., and de Camargo A.C. Free ATP inhibits thimet oligopeptidase (EC 3.4.24.15) activity, induces autophosphorylation in vitro, and controls oligopeptide degradation in macrophage. Eur. J. Biochem. 268 (2001) 887-894
36. Raggiaschi R., Lorenzetto C., Diodato E., Caricasole A., Gotta S., and Terstappen G.C. Detection of phosphorylation patterns in rat cortical neurons by combining phosphatase treatment and DIGE technology. Proteomics 6 (2006) 748-756
37. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81 (2001) 741-766
38. Selkoe D.J. Deciphering the genesis and fate of amyloid beta-protein yields novel therapies for Alzheimer disease. J. Clin. Invest. 110 (2002) 1375-1381
39. Shrimpton C.N., and Smith A.I. Soluble neutral metallopeptidases: physiological regulators of peptide action. J. Pept. Sci. 6 (2000) 251-263
40. Shrimpton C.N., Smith A.I., and Lew R.A. Soluble metalloendopeptidases and neuroendocrine signaling. Endocr. Rev. 23 (2002) 647-664
41. Sigman J.A., Sharky M.L., Walsh S.T., Pabon A., Glucksman M.J., and Wolfson A.J. Involvement of surface cysteines in activity and multimer formation of thimet oligopeptidase. Protein Eng. 16 (2003) 623-628
42. Smith A.I., Shrimpton C.N., Norman U.M., Clarke I.J., Wolfson A.J., and Lew R.A. Neuropeptidases regulating gonadal function. Biochem. Soc. Trans. 28 (2000) 430-434
43. Stein T.D., and Johnson J.A. Lack of neurodegeneration in transgenic mice overexpressing mutant amyloid precursor protein is associated with increased levels of transthyretin and the activation of cell survival pathways. J. Neurosci. 22 (2002) 7380-7388
44. Sultana R., Newman S.F., Abdul H.M., Cai J., Pierce W.M., Klein J.B., Merchant M., and Butterfield D.A. Protective effect of D609 against amyloid-beta1-42-induced oxidative modification of neuronal proteins: redox proteomics study. J. Neurosci. Res. 84 (2006) 409-417
45. Thomas S.N., Soreghan B.A., Nistor M., Sarsoza F., Head E., and Yang A.J. Reduced neuronal expression of synaptic transmission modulator HNK-1/neural cell adhesion molecule as a potential consequence of amyloid beta-mediated oxidative stress: a proteomic approach. J. Neurochem. 92 (2005) 705-717
46. Tullai J.W., Cummins P.M., Pabon A., Roberts J.L., Lopingco M.C., Shrimpton C.N., Smith A.I., Martignetti J.A., Ferro E.S., and Glucksman M.J. The neuropeptide processing enzyme EC 3.4.24.15 is modulated by protein kinase A phosphorylation. J. Biol. Chem. 275 (2000) 36514-36522
47. Vassar R., et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286 (1999) 735-741
48. von Mering C., Jensen L.J., Kuhn M., Chaffron S., Doerks T., Kruger B., Snel B., and Bork P. STRING 7-recent developments in the integration and prediction of protein interactions. Nucleic Acids Res. 35 (2007) D358-D362
49. Yamin R., Malgeri E.G., Sloane J.A., McGraw W.T., and Abraham C.R. Metalloendopeptidase EC 3.4.24.15 is necessary for Alzheimer's amyloid-beta peptide degradation. J. Biol. Chem. 274 (1999) 18777-18784
50. 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., Carter D.B., Tomasselli A.G., Parodi L.A., Heinrikson R.L., and Gurney M.E. Membrane-anchored aspartyl protease with Alzheimer's disease beta-secretase activity. Nature 402 (1999) 533-537
51. Yavin Z., and Yavin E. Survival and maturation of cerebral neurons on poly(l-lysine) surfaces in the absence of serum. Dev. Biol. 75 (1980) 454-459
52. York I.A., Mo A.X., Lemerise K., Zeng W., Shen Y., Abraham C.R., Saric T., Goldberg A.L., and Rock K.L. The cytosolic endopeptidase, thimet oligopeptidase, destroys antigenic peptides and limits the extent of MHC class I antigen presentation. Immunity 18 (2003) 429-440
53. Zou K., Yamaguchi H., Akatsu H., Sakamoto T., Ko M., Mizoguchi K., Gong J.S., Yu W., Yamamoto T., Kosaka K., Yanagisawa K., and Michikawa M. Angiotensin-converting enzyme converts amyloid beta-protein 1-42 (Abeta(1-42)) to Abeta(1-40), and its inhibition enhances brain Abeta deposition. J. Neurosci. 27 (2007) 8628-8635